Malaria Di Indonesia - PDF

KOMPILASI PUBLIKASI ILMIAH
TENTANG MALARIA DI INDONESIA

Kompilasi Publikasi Ilmiah tentang Malaria di Indonesia
Kata Pengantar
Mengendalikan dan memberantas malaria di wilayah kepulauan terbesar di dunia, membentang

sepanjang 5000 km di sekitar garis khatulistiwa, merupakan hal yang sangat menantang.
Perencanaan yang dibangun dengan landasan ilmiah dan didukung fakta amatlah diperlukan
dalam mengatasi kompleksitas permasalahan malaria di negeri ini. Indonesia telah mengalami
sejarah yang panjang menghadapi malaria. Banyak kajian ilmiah yang telah dilakukan sejak
tahun 1990an. Ratusan peneliti malaria telah mencurahkan hidup dan waktunya untuk
memahami parasit ini dan mencari cara memenangkan perlawanan menghadapinya. Motivasi
ini yang mendorong kami untuk sejenak melihat ke belakang, memetakan apa yang telah dan
belum dilakukan, serta mengambil manfaat dari buah kerja mereka dalam konteks kekinian.
Harapan ini pulalah yang ingin dibagi dengan rekan-rekan pengelola malaria di seluruh
Indonesia.
Kompilasi ini terdiri atas dua kelompok artikel yaitu : kajian studi malaria (2 artikel) dan aplikasi
ilmu pemetaan dan pemodelan malaria (2 artikel). Dua artikel pertama merangkum sejarah dan
kajian malaria di bumi pertiwi sejak tahun 1900-an sampai dengan 2011. Peta distribusi 20
vektor malaria di Indonesia, deskripsi perilaku dan kerentanan nyamuk terhadap insektisida
juga diulas. Dua artikel yang terakhir fokus kepada aplikasi teknik kartografi malaria untuk
menduga besaran endemisitas Plasmodium falciparum dan P. vivax beserta perkiraan jumlah
populasi yang tinggal di wilayah beresiko malaria.
Sejauh ini, masih banyak tantangan yang menghambat perlawanan kita memberantas malaria.
Masih tingginya kasus klinis yang belum dikonfirmasi laboratorium, dosis obat primaquine yang
tidak memadai untuk menghadang infeksi relapse P. vivax, masih kurangnya data tentang
metode intervensi vektor yang sesuai untuk kondisi lokal geografis dan sosial-ekonomi,
keberagaman vektor nyamuk malaria dan perilakunya, tantangan resistensi nyamuk terhadap
insektisida dan sistem kesehatan yang belum optimal. Tantangan terbesar dihadapi oleh rekan-
rekan pengelola malaria yang menjadi ujung tombak dalam memahami kondisi epidemiologis
lokal sekaligus memikirkan pendekatan yang paling relevan.
Besar harapan kami, kumpulan tulisan ini bisa menjadi bagian untuk bersama-sama berjuang
memberantas malaria di tanah air kita. Keterbatasan waktu menyebabkan kami belum dapat
menterjemahkan artikel ini ke dalam Bahasa Indonesia, namun semoga tetap bermanfaat.
Salam Hormat
Iqbal Elyazar, MPH, DPhil

Eijkman-Oxford Clinical Research Unit (EOCRU)
Gedung Lembaga Eijkman untuk Biologi Molekuler
Jl. Diponegoro No 69, Jakarta.
1
Kompilasi Publikasi Ilmiah tentang Malaria di Indonesia
Ucapan Terima Kasih
Pertama-tama, ucapan terima kasih ditujukan kepada para rekan penulis sebagai berikut:
Prof Simon Hay, Univ. Oxford Dr Rita Kusriastuti, Depkes RI

Dr J Kevin Baird, Univ. Oxford Dr Siti Nadia Tarmizi, Depkes RI
Dr Peter Gething, Univ. Oxford Dr Desak M Wismarini, Depkes RI
Dr Anand Patil, Univ. Oxford Dr Asik Surya, Depkes RI
Dr Marianna Sinka, Univ. Oxford Dr Winarno, Depkes RI
Dr Michael Bangs, Freeport Malaria Control Dr Elvieda Sariwati, Depkes RI
Dr Niken W Palupi, Depkes RI
Hanifah Rogayah MPH, Depkes RI
Berikutnya, terimakasih atas dukungan dari University Oxford - Li Ka Shing Foundation Global
Health Program, Oxford Tropical Network dan the United States of Naval Medical Research
Unit, Jakarta (NAMRU-2). Belajar di Universitas Oxford memberikan kesempatan untuk
mendapatkan akses yang tidak terbatas kepada sumber ilmiah. Ucapan terima kasih untuk
perpustakaan Badan Litbangkes, NAMRU-2 dan Lembaga Eijkman yang telah memberikan
akses yang luar biasa kepada koleksi artikel ilmiah yang pernah diterbitkan sebelum dan
sesudah masa kemerdekaan.
Penerimaan dan dukungan dari Departemen Kesehatan Republik Indonesia, sangat dihargai
yaitu: (a) para Kasubdit Pengendalian Malaria: Dr Rita Kusriastuti, Dr Asik Surya, Dr Made
Wismarini, Dr Nadia Tarmizi, Dr Ferdinand Laihad dan Dr Arbani, (b) Kasubdit Pengendalian
Vektor: Dr Winarno, yang telah memberikan akses seluas-luasnya kepada bank data, laporan
kegiatan dan berbagi berbagai sudut pandang,
Terimakasih kepada teman-teman dan para guru selama bekerja di NAMRU-2 (1998-2010):
Departemen Parasitology, Entomology dan Quality Assurance/Good Clinical Practice. Artikel
pertama didedikasikan untuk Bapak Purnomo Projodipuro (1934-2013) dan artikel kedua untuk
Bapak Soeroto Atmosoedjono (1919-2009) atas inspirasi dan kontribusi beliau yang terus-
menerus melatih para ahli parasitologi dan entomologi di Indonesia dan belahan dunia lainnya.
Dua artikel terakhir dipersembahkan bagi para peneliti malaria dan pengelola malaria di 33
provinsi atas kesabarannya meladeni permintaan data dan kesediaannya berbagi data. Terima
kasih banyak !!
Terimakasih kepada editor, pengkaji dan penerbit untuk artikel berikut ini:
Elyazar IRF, Hay SI, Baird JK. 2011. Malaria distribution, prevalence, drug resistance and control in
Indonesia. Adv Parasitol. 74: 41-175.
Elyazar IRF, Sinka M, Gething PW, Tarmidzi SN, Surya A, Kusriastuti R, Winarno, Baird JK, Hay SI,
Bangs MJ. 2013. The distribution and bionomics of Anopheles malaria vector mosquitoes in Indonesia.
Adv Parasitol. 83: 173-266.
Elyazar IRF, Gething PW, Patil AP, Royagah H, Kusriastuti R, Wismarini DM, Tarmizi SN, Baird JK, Hay
SI. 2011. Plasmodium falciparum malaria endemicity in Indonesia in 2010. PLoS ONE. 6: 6.
Elyazar IRF, Gething PW, Patil AP, Rogayah H, Sariwati E, Palupi NW, Tarmizi SN, Kusriastuti R, Baird
JK, Hay SI. 2012. Plasmodium vivax malaria endemicity in Indonesia in 2010. PLoS ONE. 7:5.
2
CHAPTER 2
Malaria Distribution, Prevalence,
Drug Resistance and Control in
Indonesia
Iqbal R.F. Elyazar,* Simon I. Hay, and
J. Kevin Baird*,
Contents 2.1. Introduction 42

2.2. Epidemiology of Malaria 43
2.2.1. Host 43
2.2.2. Parasites 50
2.3. Malaria Control in Indonesia 77
2.3.1. Control before independence (pre-1945) 77
2.3.2. Malaria Control Program (19451958) 86
2.3.3. Malaria Eradication Program (19591968) 89
2.3.4. Malaria Control Phase (19691999) 90
2.3.5. Indonesian Roll Back Malaria campaign
(RBM; 2000present) 93
2.4. Obstacles and Opportunities in Malaria
Control in Indonesia 94
2.4.1. Malaria case detection 94
2.4.2. Malaria diagnostics 102
2.4.3. Malaria treatment 108
2.4.4. Vector control 112
2.4.5. Malaria surveillance 148
* Eijkman-Oxford Clinical Research Unit, Jakarta, Indonesia

{
Spatial Epidemiology and Ecology Group, Department of Zoology, University of Oxford, Oxford,
United Kingdom
{
Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford,
United Kingdom
Advances in Parasitology, Volume 74 # 2011 Elsevier Ltd.

ISSN 0065-308X, DOI: 10.1016/B978-0-12-385897-9.00002-1 All rights reserved.
41
42 Iqbal R.F. Elyazar et al.
2.5. Outlook for Malaria Research in Indonesia 149

Acknowledgements 151
References 151
Abstract Approximately 230 million people live in Indonesia. The country is

also home to over 20 anopheline vectors of malaria which transmit
all four of the species of Plasmodium that routinely infect humans.
A complex mosaic of risk of infection across this 5000-km-long
archipelago of thousands of islands and distinctive habitats seri-
ously challenges efforts to control malaria. Social, economic
and political dimensions contribute to these complexities.
This chapter examines malaria and its control in Indonesia, from
the earliest efforts by malariologists of the colonial Netherlands
East Indies, through the Global Malaria Eradication Campaign of the
1950s, the tumult following the coup detat of 1965, the global
resurgence of malaria through the 1980s and 1990s and finally
through to the decentralization of government authority following
the fall of the authoritarian Soeharto regime in 1998. We detail
important methods of control and their impact in the context of
the political systems that supported them. We examine prospects
for malaria control in contemporary decentralized and democra-
tized Indonesia with multidrug-resistant malaria and greatly dimin-
ished capacities for integrated malaria control management
programs.
2.1. INTRODUCTION
Each year Indonesias 230 million people collectively suffer at least sev-
eral million cases of malaria caused by all four known species of human
Plasmodium. Despite a long history of pioneering work in malaria preven-
tion, treatment and control reaching back to the early 1900s, no systematic
review of malaria in Indonesia has yet been undertaken. This chapter
attempts to remedy this with a detailed examination of the genesis, nature
and outcome of control strategies, along with a comprehensive review of
peer-reviewed and published work on malaria. We also examine contem-
porary malaria in the context of government systems arrayed against it.
This article does not include the body of knowledge on the complex array
of anopheline vectors of malaria found in Indonesia. That topic is
reserved for a separate review.
Malaria Distribution, Prevalence, Drug Resistance and Control in Indonesia 43
2.2. EPIDEMIOLOGY OF MALARIA
2.2.1. Host
2.2.1.1. Human population
The Republic of Indonesia in Southeast Asia makes up most of the Indo-
nesian archipelago that straddles the equator and stretches 5200 km from
west Malaysia to Papua New Guinea (Fig. 2.1). The country consists of
17,504 islands (only 6000 of which are inhabited), covering a land area of
1.9 million km2 (Departemen Dalam Negeri, 2004, 2008). The archipelago
comprises seven main islands: Sumatra, Java, Kalimantan, Sulawesi,
Maluku, the Lesser Sundas and Papua. Since decentralization of govern-
ment power in 2000, Indonesia has been considered to consist of 33
provinces, 465 districts/municipalities, 6093 sub-districts and 73,067 vil-
lages (Departemen Kesehatan, 2008). Census authorities in 2007 estimated
a population of 227 million people, with an average density of 118 peo-
ple/km2 (Departemen Kesehatan, 2008). The annual population growth
rate was 1.3% (Badan Pusat Statistik, 2007a). The population density on
Java and Bali (977 people/km2) was much higher than on other islands
(50 people/km2). Sixty percent of Indonesians live on Java and Bali,
representing only 7% of the land area of Indonesia. More people live in
rural (57%) than in urban areas (43%). The ratio of male to female was 1:1.
The age distribution of the population was 30% young (014 years old),
65% productive age (1564 years old) and 5% old age ( 65 years old). Life
expectancy at birth for Indonesians increased from 52 years in 1980 to 69
years in 2007 (Departemen Kesehatan, 2008). The governments
Thailand
Cambodia
Pacific Ocean
N
Malaysia
Singapore Sulawesi
Equator Line
Papua
Sumatra Kalimantan
Maluku
Java
Indian Ocean
Wallace Line Australia
Lesser Sundas
FIGURE 2.1 The map of Indonesian archipelago.

Household Health Survey estimated an illiteracy rate of 7%, with more

females (10%) than males being illiterate (4%) and with higher rates in
rural (10%) than in urban areas (4%; Badan Pusat Statistik, 2007b). The
highest illiteracy rates occurred in Papua (23%; rural 32% and urban 2%)
and West Nusa Tenggara provinces (18%; rural 20% and urban 13%;
Departemen Kesehatan, 2008). As shall be seen, these are also two of the
most malarious provinces in Indonesia.
2.2.1.2. Economics
The East Asian Economic Crisis of 1997 caused the Indonesian Rupiah to
lose 85% of its value against the US Dollar within months. This crisis
significantly diminished private savings and forced the closure of almost
every significant business activity. The crisis also precipitated the fall of
the Soeharto regime, and several years of political instability followed.
The number of poor increased from 23 million (11%) prior to the crisis to
39 million (18%) in 2006, with a monthly income of less than US$ 17
serving as the measure for the poverty line (Badan Pusat Statistik,
2007a). However, according to a global poverty map, based on night
light brightness from satellite imagery, and the criterium of a US$ 2 per
day poverty line, Elvidge et al. estimated that 73 million of Indonesias
population (32%) lived in poverty in year 2006 (Elvidge et al., 2009).
In 2008, the World Bank reported that 54% of the Indonesian population
was living below the poverty line (US$ 2 a day serving as the World
Banks poverty line measure; The World Bank, 2008). The International
Monetary Fund estimated that the annual Indonesian gross domestic
product (GDP) per capita in 2008 was US$ 2239, a significant increase
from US$ 516 in 1998 (International Monetary Fund, 2009). About 88%
of the population spent less than US$ 50 per month (rural 96%; urban 76%;
Badan Pusat Statistik, 2007a). In 2007, 199 of 465 (43%) districts/munici-
palities in Indonesia were classified as underdeveloped, with 55% of these
situated in the eastern part of Indonesia. In West Sulawesi, Central
Sulawesi, Bengkulu and Papua 100%, 90%, 89% and 87%, respectively,
of the districts/municipalities were underdeveloped (Departemen
Kesehatan, 2008).
The economic crisis also affected government expenditure on health,
causing it to fall from US$ 6 (1997) to US$ 13 (19971998) per person per
year (Departemen Keuangan, 1997, 1998, 1999). However, government
expenditures on health recovered and even surpassed precrisis figures at
US$ 8 per capita per year by 2007 (Departemen Keuangan, 2007). In 2007,
the health budget reached Rp. 18.5 trillion ( US$ 19 billion; Departemen
Kesehatan, 2008), of which 8.3% was allocated to the Directorate General of
Disease Control and Environmental Health and 1.2% was allocated to the
National Institute of Health Research and Development (NIHRD). In other
words, Indonesia spent US$ 1.8 billion on disease control and research.
The health budget in 2007 had increased threefold from that of 1999.
2.2.1.3. Healthcare delivery systems

Healthcare services are made up of primary health centres, public
hospitals, private and semi-private pharmaceutical industries and private
sector healthcare facilities and personnel. Primary health centres are
mainly located in sub-districts and provide maternal and infant care,
family planning and in-patient and out-patient services to the commu-
nity, as well as communicable disease control services. In 2007, there were
8234 primary health centres, with a centre serving, on average, about
27,400 people (Departemen Kesehatan, 2008). The number of primary
health centres increases at a rate of about 2.7% per year. The service
coverage by province ranged from 8000 to 52,000 people per health centre.
Seven provinces failed to meet the standard target of a maximum of
30,000 people per health centre. These were Riau, Banten, West Java,
Central Java, East Java, Bali and West Nusa Tenggara. The area coverage
per centre was 192 km2 on average; however, in sparsely populated
Papua, Central Kalimantan and East Kalimantan area, coverage was
greater than 1000 km2.
The number of hospitals was 1319 in 2007, which provided a total of
142,707 hospital beds (Departemen Kesehatan, 2008). Ownership of these
hospitals was 49% private and 51% public and government operated. The
overall ratio of population to each hospital bed was 1581:1. The Indone-
sian Ministry of Health (MoH) declared the ideal ratio to be 1000 people
per bed. The annual increase in hospital beds is typically 1.1%. The total
number of people seeking hospital treatment was about 30 million in
2005, with 7.8% of them being referred from lower levels of healthcare
delivery, including primary health centres (Badan Pusat Statistik, 2007b).
In order to increase the coverage of community services, Indonesia
implemented community-based health effort programs, such as health
posts, with integrated village maternity huts and village drug posts. By
2006, there were 269,202 health posts, called Pos Pelayanan Terpadu or
Posyandu, which provided maternity and child health services, family
planning, nutritional development, immunization and diarrhoea control
(Departemen Kesehatan, 2008). There are four of these Posyandu in each
village. In total, there were 25,754 maternity huts, known as Pondok
Bersalin Desa or Polindes, which provide midwives with delivery units,
as well as providing improved maternity and child health services and
family planning services. In addition, there are 9598 village drug posts,
known as Pos Obat Desa, which assist in the distribution of some essential
drugs directly to the community.
The activities of the pharmaceutical industry ensure the availability,
accessibility and distribution of drugs to the community. By 2005,
according to the Drug and Food Control Agency, there were 465 standard
pharmaceutical companies and 1634 small, traditional drug companies in
the production sector (Departemen Kesehatan, 2008). The traditional
drug companies typically produce herbal elixirs ranging from vitamin
supplements and skin ointments, to solutions purported to boost the
intellect, energy or sexual stamina. The distribution of pharmaceutical
products is managed by 2493 wholesalers, 10,275 dispensaries, and 7056
drugstores (Departemen Kesehatan, 2008). Although many statutes
restrict the distribution of prescription drugs, it is generally the case that
many anti-infective therapies, including antimalarials, which are offi-
cially prescription only drugs, can be purchased over the counter.
According to the Indonesian MoH in 2007 there was about half a
million health personnel employed in Indonesia (Departemen
Kesehatan, 2008). Nurses and midwives made up 54% and 14%, respec-
tively, of that number. Typically, for every 100,000 people, there were 138
nurses and 35 midwives. Eight percent of these half a million health
personnel were licensed physicians, yielding a service ratio of about 19
physicians per 100,000 people. Health personnel specializing in public
health made up two percent of this half a million, with a service ratio of
approximately four per 100,000 people. The distribution of health person-
nel was 257,555 (45%) at hospitals and 184,445 (32%) at healthcare centres
(Departemen Kesehatan, 2008).
The healthcare situation in Indonesia is relatively poor compared to
the situation in neighbouring countries. Table 2.1 shows several indica-
tors of health service quality in Indonesia and in four neighbouring
countries, including Cambodia, Thailand, Malaysia and Singapore
(International Monetary Fund, 2009; The World Bank, 2008; World
Health Organization, 2008b, 2009a). Cambodia has a GDP which is three
times lower than that of Indonesia, and a greater proportion of its popu-
lation live in poverty (68% vs. 54%). Thailand and Malaysia are develop-
ing countries with a higher GDP and a poverty rate which is two to four
times lower than that of Indonesia. Singapore, meanwhile, is an example
of the developed countries of Southeast Asia, with a GDP that is 17 times
higher than Indonesias and with reportedly no proportion of the popu-
lation living below the poverty line. In terms of healthcare delivery
services, the availability ratio of hospital beds in Indonesia is six times
higher than the ratio in Cambodia. This ratio is three to five times lower
than the ratio in Thailand, Malaysia and Singapore. The ratio of physi-
cians to population in Indonesia is lower (two to 15 times lower) than the
ratio in other countries. Similarly, the ratio of nurses and midwives to
population in Indonesia is about two to five times lower than the ratio in
neighbouring countries. This situation is exacerbated by the sheer size of
Indonesias population; a population 345 times the size of the popula-
tions in neighbouring countries.
TABLE 2.1 Human population, economics and healthcare delivery system indicators for Indonesia and neighbouring countries
Indicators Year Cambodia Indonesia Thailand Malaysia Singapore
Human population
Population (millions) 2008 14 227 66 27 5
Annual growth rate (%) 19972007 1.9 1.3 0.8 2 1.8
Life expectancy at birth (years) 2007 61 69 70 72 81
Economics
GDP per capita, current prices (US$) 2008 823 2239 4116 8118 38,972
Population below poverty line (%) 2005 68 54 12 8 0
Health expenditure per capita (US$) 2006 30 39 113 259 1017
Healthcare delivery systems
Hospital beds (per 10,000 population) 20002008 1 6 22 18 32
Physician (per 10,000 population) 20002007 2 1 4 7 15
Nurses and midwives (per 10,000 20002007 9 8 28 18 44
population)
Other health service providers 20002007 <1 2 12 1 3
(per 10,000 population)
The population data and the estimates of GDP per capita were derived from World Economic Outlook DatabaseOctober 2009 (International Monetary Fund, 2009). The number
of population below poverty line was acquired from World Bank Development Indicators in 2008 (The World Bank, 2008). Annual growth rate, life expectancy at birth, health
expenditure per capita and all indicators in healthcare delivery systems were regained from World Health Statistics Report 2008 and 2009 (World Health Organization, 2008b,
2009a).
2.2.1.4. Infections research and surveillance systems operated by

the government
Most government-affiliated infections research and surveillance systems
in Indonesia are managed by three separate government agencies: (1) the
NIHRD, (2) the Directorate General of Disease Control and Health Envi-
ronment and (3) the Directorate General of Medical Care. All of these are
under MoH authority. The Ministry of Research and Technology also
sponsors infections research, primarily through the research conducted
at the Eijkman Institute for Molecular Biology. Moreover, many academic
institutions operating under the authority of the Ministry of Education
have long histories of vibrant and productive research on infections,
especially in schools of medicine and of public health.
The NIHRD commenced operations in 1975. Its main functions were
(1) to develop policies, programs and implementation strategies for health
systems, health policy, biomedicine, pharmaceutics, ecology, health sta-
tus, nutrition and food, (2) to evaluate and screen health technologies and
(3) to disseminate research results. Most malaria research conducted at
the NIHRD is carried out by three main branches: (a) the Research Centre
of Biomedicine and Pharmacy, (b) the Research Centre of Ecology and
Health Status and (c) the Research and Development Centre of Vectors
and Diseases. In 2006, these three NIHRD centres had 88, 50 and 15
researchers, respectively. That year, NIHRD received Rp. 174 billion
( US$ 2 million) and spent 25% on research and development, 72% on
human resources and facilities development and 3% on research results
dissemination (Departemen Kesehatan, 2006d).
The NIHRD organizes health surveys. The Basic Health Research,
called Riskesdas or Riset Kesehatan Dasar project, initiated in 2007, is an
example of this. A total of 258,366 households and 987,205 individual
household members were sampled, with sampling reaching every prov-
ince. The survey collected information about household and individual
demographics, mortality, access to health facilities, sanitation, food and
drug consumption, history of diseases, perceived responsiveness of
health facilities, health behaviour, disabilities, mental health, immuniza-
tion, growth monitoring and infant health. Riskesdas also collected 36,357
blood samples in order to measure biomedical variables. In the specific
instance of malaria, respondents were asked about any history of con-
firmed malaria, symptoms of malaria and malaria medication usage
(National Institute of Health Research and Development, 2008).
As part of the National Health Survey System, the Central Bureau of
Statistics (with NIHRD) has conducted a Household Health Survey
(SKRT; Survey Kesehatan Rumah Tangga) every five years since 1975.
In this survey 10,000 households are selected by stratified multistage
random sampling. The survey collects information on household and
individual characteristics, environment, morbidity, mortality, pregnancy
and delivery (Soemantri et al., 2005). In addition, the National Family

Planning Bureau also conducts Indonesian Demography and Health
Surveys (SDKI, Survey Demografi dan Kesehatan Indonesia) every
3 years (this began in 1981). The surveys are designed to collect data on
fertility, family planning, and maternal and child health. A total of 35,000
households are sampled across all provinces. In order to participate,
respondents must be married and aged 1549 years (females) or 1554
years (males) (Soemantri et al., 2005).
The Directorate General of Disease Control consists of five directo-
rates: (a) the Directorate of Epidemiology Surveillance (144 personnel), (b)
the Directorate of Communicable Diseases (98 personnel), (c) the Direc-
torate of Vector-borne Diseases (104 personnel), (d) the Directorate of
Non-Communicable Diseases (80 personnel) and (e) the Directorate of
Health Environment (99 personnel). The Directorate of Vector-Borne Dis-
eases is responsible for malaria and vector control activities (Departemen
Kesehatan, 2006c).
Malaria surveillance in Indonesia begins with patient registration and
data collection at the primary health centres (commonly called by their
Indonesian acronym Puskesmas; Pusat Kesehatan Masyarakat or
Peoples Health Centre; Departemen Kesehatan, 1997). Primary health
centres generate monthly malaria reports from out-patient services and
malaria case detection activities. Primary health centres are responsible
for analysing data and producing a local area monitoring report on the
distribution and trends of the disease. In the specific case of malaria, a
puskesmas sends a report to the district malaria control officer who in
turn compiles all reports into a district health profile on malaria. The
health profile describes monthly and annual malaria cases reported at
village level. The district health office then sends aggregated malaria
reports three times a year to the provincial health office, as well as to
the Sub-Directorate of Malaria Control at the Directorate of Vector-borne
Diseases in Jakarta (Departemen Kesehatan, 2006b,f, 2007a). Malaria data
also comes from laboratory examination in hospitals. The malaria data
is collected through the Hospital Reporting System (known by the
Indonesian acronym SPRS, Sistem Pelaporan Rumah Sakit) which cov-
ers all private and government hospitals in Indonesia. The SPRS malaria
figures go to the Directorate General of Medical Care (Departemen
Kesehatan, 2003a), and they are then passed on to the Sub-Directorate of
Malaria.
Finally, primary health centres and the district malaria control office
are responsible for the management of vector control activities and for
reporting on their progress. The indoor residual spraying (IRS) report, for
instance, contains the number of houses sprayed, how many people live
in sprayed homes, the insecticide type, the amount of insecticide used and
the date of spraying. The number of insecticide-treated mosquito nets
(ITN) distributed, the number of people protected, the dates of bed net
distribution as well as larviciding activity which includes the coverage
area, the amount of larvicide used and the date of the activities are also
reported. Primary health centres and the district malaria control office
also document biological control activities such as the introduction of
larvivorous fish into areas where mosquito breeding sites have been
found. They keep a record of the number of fish introduced and the
dates of these activities (Departemen Kesehatan, 2003b).
2.2.2. Parasites
2.2.2.1. The distribution of the Plasmodium
The Malaria Atlas Project and its partners in the Sub-Directorate for
Malaria Control in the Directorate of Vector-borne Diseases aim to assem-
ble malaria parasite rate surveys across the Indonesian archipelago
(Guerra et al., 2007; Hay and Snow, 2006). Table 2.2 summarizes the
distribution of human Plasmodium throughout the Indonesian archipelago.
At the time of writing, we have recorded parasite rate surveys for 2366
locations conducted between 1900 and 2008. The surveys are not equally
distributed, with 63% of them conducted in eastern Indonesia (Moluccas,
the Lesser Sundas and Papua). From this assembly of data, we were able to
report that four species of malaria parasite routinely infect humans in
Indonesia: Plasmodium falciparum, P. vivax, P. malariae and P. ovale.
Plasmodium falciparum appears to be the most common Plasmodium
species in Indonesia. One of the earliest published documents concerning
the presence of P. falciparum in Indonesia was a report by Robert Koch in
1900 revealing its presence in Ambarawa and Ungaran (both in Central
Java) and Tanjung Priok (Jakarta; Koch, 1900). Since then, the presence of
this parasite has been recorded at 1915 (81%) locations. Most of these
locations are located in Papua (33%), the Lesser Sundas (29%) and Suma-
tra (21%). The median prevalence of P. falciparum, from 1900 to 2008, was
5% (ranging from 0.03% to 82%). However, this prevalence was not
distributed uniformly across the island groups. Prevalence was higher
in eastern Indonesia (median: 6%, range: 0.0382%) than in the rest of the
country (median: 3%, range: 0.172%).
After P. falciparum, P. vivax is the most common of the Plasmodium in
Indonesia. To the present day, it has been reported at 1786 locations (75%
of all surveys). Of these, 32% were located in Papua, 29% in the Lesser
Sundas and 23% in Sumatra. The median prevalence of P. vivax, between
1900 and 2008, was 3% (range: 0.0370%). This prevalence was not
distributed uniformly across the islands. The prevalence of P. vivax
in the eastern part of Indonesia (median: 3%, range: 0.0470%) was
higher than the prevalence in the rest of the country (median: 2.5%,
range: 0.0760%).
TABLE 2.2 The distribution of human Plasmodium throughout the Indonesian archipelago
Islands Year of sample No. sites No. exam No. Pf (%) No. P.v. (%) No. P.m. (%) No. P.o. (%)
Sumatra 19192009 676 239,109 8487 (3.5%) 7057 (2.9%) 494 (0.2%)
Java/Bali 19002006 114 105,734 3387 (3.2%) 2773 (2.6%) 221 (0.2%)
Kalimantan 19752005 17 7367 398 (5.4%) 248 (3.4%) 21 (0.3%)
Sulawesi 19722006 55 11,530 482 (4.2%) 316 (2.7%) 8 (0.1%)
Maluku 19972009 201 121,526 5311 (4.4%) 13,198 (10.9%) 3 (0.002%)
Lesser Sundas 19752009 609 383,950 23,502 (6.1%) 19,401 (5.1%) 157 (0.04%) 11 (0.003%)
Papua 19292009 694 193,043 19,848 (10.3%) 9343 (4.8%) 1395 (0.7%) 40 (0.02%)
Indonesia 19002009 2366 1,062,259 61,415 (5.8%) 52,336 (4.9%) 2299 (0.2%) 51 (0.005%)
The database of distribution of human Plasmodium was regained from 86% of unpublished data and 14% published sources. The malaria parasite rate data which acquired from
published sources listed these following references:
Sumatra: (Bosh, 1925; Carney et al., 1974a, 1975a; Clarke et al., 1973; Cross et al., 1976; Dewi et al., 1996; Doi et al., 1989; Dondero et al., 1974; Doorenbos, 1931a, b; Fryauff et al.,
2002; Gandahusada et al., 1981; Gerlach, 1935; Kaneko et al., 1987, 1989; Kirnowardoyo et al., 1993; Maguire et al., 2002b; Matsuoka et al., 1986; Mulder, 1936; Pribadi et al., 1985,
1994, 1997; Renny et al., 1989; Schuffner, 1919; Sekartuti et al., 2004a; Sieburgh, 1936; Soesilo, 1929; Stafford et al., 1977; Sudomo et al., 1997; Syafruddin et al., 2007; Tjitra et al.,
1991).
Java/Bali: (Baird et al., 1996c; Clarke et al., 1973; Koch, 1900; Maguire et al., 2005; Ompusunggu et al., 1994, 2002, 2005; Pribadi et al., 1988, 1992; Ristiyanto et al., 2002; Schuurman
and Huinink, 1929; Simanjuntak et al., 1981; Stafford et al., 1980b; Sudini and Soetanto, 2005; Tjitra et al., 1993b; Tjokrosonto et al., 1980; Utami et al., 2002; Verdrager and Arwati,
1975b).
Kalimantan: (Cross et al., 1975; Fryauff et al., 1998a; Ompusunggu et al., 1989b; Verdrager et al., 1975a).
Sulawesi: (Carney et al., 1974b,c, 1977; Chadijah et al., 2006; Clarke et al., 1974; Cross et al., 1972; Fryauff et al., 1998b; Joseph et al., 1978; Partono et al., 1973; Purnomo et al., 1987;
Stafford et al., 1980a; Syafruddin et al., 1992; Tantular et al., 1999; Tjitra et al., 1995; Widjaya et al., 2006).
Maluku: (Fryauff et al., 1999; Roosihermiatie et al., 2000; Soekirno et al., 1997).
Lesser Sundas: (Baird et al., 1990; Barodji et al., 1994, 1996; Carney et al., 1975b; Dachlan et al., 2005; Fryauff et al., 1997b; Gundelfinger et al., 1975; Hoffman et al., 1984; Jalloh et al.,
2004; Jodjana and Eblen, 1997; Joesoef and Dennis, 1980; Jones et al., 1993; Marwoto and Martono, 1991; Marwoto and Purnomo, 1992; Mucide et al., 1998; Nalim et al., 1997;
Ompusunggu et al., 2006; Smrkovski et al., 1983; Susanto et al., 2005; Syafruddin et al., 2006, 2009; Tjitra, 2001).
Papua: (Andersen et al., 1997; Anthony et al., 1992; Baird, 1998; Baird et al., 1993, 1997b; Bangs et al., 1992; Barcus et al., 2003; Cross et al., 1977; De Rook, 1929; Dimpudus et al.,
1981; Fryauff et al., 1997d, 2000; Hutapea, 1979; Kariadi, 1936; Karyana et al., 2008; Lee et al., 1980; Ling et al., 2002; Metselaar, 1956a, 1959; Meuwissen, 1961; Mooij, 1932; Pribadi
et al., 1998; Purnomo et al., 1999; Sunaryo, 2006; Tjitra, 2001; Van der Kaay et al., 1973; Verdrager et al., 1976b; Voors, 1955).
The assembled data reveal that P. falciparum and P. vivax infections

often occur together (sympatrically) in Indonesia. Of 2366 survey loca-
tions, the presence of these two species was confirmed at 1606 locations
(68%). P. falciparum dominated in more locations than P. vivax (62% vs.
33%). The median ratio of P. falciparum to P. vivax at those areas domi-
nated by P. falciparum was 3:1. The median ratio of P. vivax to P. falciparum
at P. vivax dominated areas was 2:1. In terms of geographical distribution,
64% of those areas, where the two parasites coexisted, were located in the
Lesser Sundas and Papua.
Plasmodium malariae is a relatively uncommon species in Indonesia. The
presence of P. malariae in Indonesia was first confirmed by Robert Koch in
Central Java and Jakarta in 1900 (Koch, 1900). To date, this parasite has
been confirmed at 120 survey locations (5%). The parasite was found on all
the main islands, however it was mostly recorded in eastern Indonesia, in
the Lesser Sundas (38%) and in Papua (29%). The median prevalence of
P. malariae, from 1900 to 2008, is 2% (range: 0.05% to 53%).
Reports of P. ovale come almost entirely from eastern Indonesia. This
species has not been reliably documented anywhere else in Indonesia.
The first report of P. ovale in Indonesia was from Belu (East Nusa
Tenggara) in 1975 (Gundelfinger et al., 1975). Malaria parasite rate
surveys carried out since then have recorded P. ovale at 16 survey loca-
tions (0.6%). Its presence was only recorded in the Lesser Sundas (38%)
and Papua (62%) with a median prevalence of 0.2% (range: 0.074.9%).
Plasmodium knowlesi, a Plasmodium species naturally occurring in
macaques in Southeast Asia, appears in no peer-reviewed report describ-
ing infections of humans in Indonesia. However, Berens-Riha et al. pre-
sented information showing that four of 22 human blood samples taken
from Kalimantan were positive for P. knowlesi (Berens-Riha et al., 2009).
The samples were taken from patients with severe and uncomplicated
malaria. Initially, the blood samples were morphologically diagnosed by
microscopy as P. falciparum. P. knowlesi was then determined using a
nested polymerase chain reaction (PCR) for all five human-specific pri-
mers. Two patients had a mixed infection of P. knowlesi and P. vivax, one
had a mixed infection of P. knowlesi and P. falciparum, and one showed a
very weak band of P. vivax, but a strong band of P. knowlesi. The natural
hosts of P. knowlesi are long-tailed macaques (Macaca fascicularis), pig-
tailed macaques (Macaca nemestrina) and banded leaf monkeys (Presbytis
melalophos; Eyles et al., 1962a,b). The Anopheles leucosphyrus group of
mosquitoes (about 20 distinct species) transmits P. knowlesi very effi-
ciently (Sallum et al., 2005). In Malaysian Borneo, P. knowlesi has been
found to affect in particular those humans inhabiting the natural habitat
of the simian hosts (Cox-Singh and Singh, 2008). P. knowlesi has been
reported in humans from the Philippines (Luchavez et al., 2008), Thailand
( Jongwutiwes et al., 2004), China (Zhu et al., 2006) and Singapore
(Ng et al., 2008). The natural simian and anopheline hosts of P. knowlesi
occur in abundance throughout Indonesia west of the Wallace Line
(which runs between Kalimantan and Sulawesi, and between Bali and
Lombok; Fooden, 1982). It seems very likely that the absence of reports of
P. knowlesi in humans represents a failure to conduct sufficiently sensitive
surveys (Cox-Singh et al., 2008). An understanding of P. knowlesi malaria
and preventive measures may be a useful priority for those providing
healthcare to communities living in the forest fringe habitats of western
and central Indonesia (Cox-Singh and Singh, 2008).
2.2.2.2. Reported versus actual malaria morbidity and mortality

Morbidity and mortality statistics for malaria in Indonesia are routinely
under-reported. According to the Household Health Survey conducted
by the Central Bureau of Statistics in both 1995 and 2001, an estimated
1530 million people suffered from at least one attack of malaria in their
lifetime, and an estimated 30,00038,000 deaths occurred in each of those
years (Departemen Kesehatan, 1995, 2001). In contrast, the MoH reported
only 191 deaths in 1995 and 1774 deaths in 2001 (WHO SEARO, 2008). The
World Health Organization South-East Asia Regional Office accepted that
there were no reliable records of mortality. The same agency reported
that, on average, 451774 deaths occurred in Indonesia per year between
1994 and 2003 (WHO SEARO, 2008).
Lederman et al. reported that malaria in Jakarta, the capital city, is not
rare and significantly underestimated (Lederman et al., 2006b). Between
2004 and 2005, they recorded 240 imported malaria cases at 28 hospitals,
with P. falciparum accounting for 67% of cases (mixed infections
included). The Jakarta Health Province Office reported 552 malaria
cases in 2006 (Dinas Kesehatan DKI Jakarta, 2007). However, in the
same period, the MoH reported no malaria data in Jakarta province
(Departemen Kesehatan, 2007d). Such discrepancies illustrate the failure
to implement reliable and regular case reporting between the provinces
and the MoH.
In 2008, the World Health Organization (WHO) released the estimates
of malaria cases and malaria deaths for each country (World Health
Organization, 2008e). The WHO estimated that there were 2.5 million
cases of malaria in Indonesia in 2006 (World Health Organization,
2008e). This figure was much higher than the 0.3 million cases reported
by the MoH. In other words, the figure given by the MoH was only 13.8%
of that given by the WHO. One might therefore say that the MoH was
under-reporting by as much as 86.2%. In terms of malaria deaths, the
WHO estimated that over 3000 deaths had occurred in the year 2006,
while the MoH only reported 494 deaths. The number of malaria deaths
was therefore also under-reported (85.8%).
The discrepancies in these numbers were also reflected in the World

Malaria Report published in 2008 and 2009. Table 2.3 shows the differ-
ences of malaria cases and mortality between 2001 and 2006. According to
these reports, both reports define reported malaria cases as a combination
of probable and confirmed cases. A probable case of malaria is defined as
suspected but not laboratory tested, and nonetheless reported as malaria.
Such discrepancies illustrate the difficulties in describing the burden of
malaria disease in Indonesia.
The contemporary estimates of clinical burden of P. falciparum malaria
and the number of pregnancies at risk of P. falciparum malaria in Indonesia
have been published in 2010. Hay et al. presented a new cartographic
technique and its application for deriving global clinical burden estimates
of P. falciparum malaria in 2007 (Hay et al., 2010). The 87 malaria endemic
countries were divided into countries with a low risk of transmission
(unstable transmission: Pf annual parasite incidence (API) < 0.1 cases
per 1000 people) and countries with a moderate or high risk of transmission
(stable transmission: PfAPI 0.1 cases per 1000 people). In countries
with unstable transmission, the researchers assumed a uniform annual
clinical incidence rate of 0.1 cases per 1000 people and multiplied this
by population sizes to get disease burden estimates. In countries with
TABLE 2.3 Discrepancies of reported malaria cases and reported malaria deaths in
Indonesia between the World Malaria Report 2008 (WMR2008) and the World Malaria
Report 2009 (WMR2009)
Reported malaria cases Reported malaria deaths

WMR2009- WMR2009-
Year WMR2008 Profiles Annex 3A WMR2008 WMR2009
1994 145,920 145,920 No data No data

1995 123,226 123,226 No data No data
1996 179,878 179,878 148 148
1997 161,285 161,285 199 199
1998 160,282 160,282 45 45
1999 No data No data No data No data
2000 101,185 No data No data No data
2001 1,400,596 2,776,477 267,592 68 No data
2002 1,494,165 2,416,039 273,793 197 No data
2003 1,481,748 2,554,223 223,074 No data No data
2004 1,494,636 3,016,262 268,852 No data No data
2005 1,792,992 1,445,831 437,323 No data No data
2006 1,327,431 1,320,581 347,597 494 494
stable transmission, they used a modelled relationship between clinical

incidence (number of new cases in a population per year) and prevalence
(the proportion of a population infected with malaria parasites) and
a global malaria endemicity map (a map that indicates the risk of malaria
infection in different countries) to estimate malaria incidences. Combining
these estimates for Indonesia resulted in 12.3 million (95% credible inter-
val 6.220.9 million) clinical cases of P. falciparum malaria in 2007.
Almost all this morbidity burden (99%) occurred in areas of stable
transmission.
Dellicour et al. derived the first contemporary estimates of the global
distribution of the number of pregnancies at risk of P. falciparum and
P. vivax malaria in 2007 in areas with P. falciparum and P. vivax transmis-
sion (Dellicour et al., 2010). The researchers used data from various
sources to calculate the annual number of pregnancies (the sum of live
births, induced abortions, miscarriages and still births) in each country.
Finally, they calculated the annual number of pregnancies at risk of
malaria in each country by multiplying the number of pregnancies in
the entire country by the fraction of the population living within the
spatial limits of malaria transmission in that country. In 2007, they calcu-
lated 6.4 million pregnancies occurred in areas with P. falciparum and/or
P. vivax transmission in Indonesia. These pregnancies resulted in 3.8
million live births. Of 4.4 million pregnancies in areas with P. falciparum
transmission, 2 million occurred in areas with stable transmission and 2.4
million in areas with unstable transmission. A total of 6.3 million occurred
in areas with P. vivax transmission and 4.3 million of which occurred in
areas in which P. falciparum and P. vivax coexist. The estimates are an
important step towards a spatial map of the burden of malaria in preg-
nancy and should help policy makers allocate resources for research into
and control of this important public-health problem.
2.2.2.3. Occurrence of epidemic malaria

Malaria outbreaks occur in Indonesia every year. For example, in 1998
and 1999 there were outbreaks in eight provinces, covering 10 districts
with 19,483 cases and 66 deaths (case fatality rate, CFR 0.3%; Marwoto
and Sekartuti, 2003). Between 2000 and 2005, there were outbreaks in 19
provinces, covering 65 districts/municipalities, with 58,152 malaria cases
and 536 reported deaths (CFR 0.9%; Departemen Kesehatan, 2006c). In
2006, outbreaks occurred in eight provinces with 3705 cases and 30
reported deaths (CFR 0.8%; Departemen Kesehatan, 2007c). Later,
between 2007 and 2008, outbreaks were reported in 11 provinces, cover-
ing 20 districts, with 1864 cases and 93 reported deaths (CFR 5%;
Departemen Kesehatan, 2009a).
Many factors have contributed to outbreaks of malaria in Indonesia.
Some of these outbreaks occur under unique conditions of human
migration. For instance, both in 1988 and 1992, the movement of non-
immune transmigrants from Java and Bali (hypoendemic areas) to Arso in
Papua (hyperendemic area) created local epidemics as early as 2 months
after their arrival (Baird et al., 1995d). A strong correlation has also been
shown between El Nino Southern Oscillation (ENSO)-related climatic
anomalies and the increased risk of malaria exposure and severe disease
in highly susceptible highland populations in the Jayawijaya (Papua;
Bangs and Subianto, 1999). In 1997, increased malaria coincided with a
period of dramatic deficit in precipitation, increased air temperatures and
barometric readings, with a 75% overall reduction in normal rainfall.
Drought forced people to move to lower elevations because of the grave
water and food shortages, thereby increasing exposure to intense malaria
transmission.
More typical outbreaks, resurgences in areas where case numbers
have been low for a long time, also routinely occur. The relative difficulty
of removing the breeding sites of Anopheles maculatus and A. balabacensis
has played an important role in the persistence of hypoendemic malaria
on Java (Barcus et al., 2002). Rocky streams that can be found everywhere
on steep, forested slopes are ideal breeding sites for these vectors. In
addition, hillside residents live in traditional Javanese houses made of
wooden planks and bamboo, which do little to deter mosquito access,
whilst poor or non-existent roads limit access to health care.
Marwoto et al. found that in Banyumas and Pacitan (East Java) and
Pulau Seribu (a group of islands off the shore of Jakarta) in 2000 and 2001,
immigrant workers who worked as transmigrant or seasonal workers in
endemic malarious areas outside Java Island returned to their home
villages which were receptive to malaria due to the presence of malaria
vector mosquitoes (Marwoto and Sekartuti, 2003). Marwoto et al.
recorded that in Cilacap (Central Java) and Lampung (South Sumatra)
in 1998, high mobility was a contributing factor, together with the disused
shrimp ponds or fishponds that provided ideal breeding sites for the
highly efficient malaria vector A. sundaicus (Marwoto and Sekartuti,
2003). In Kulonprogo (Yogyakarta) late case detection, a lack of vector
control such as indoor residual insecticide spraying and a lack of knowl-
edge regarding malaria all contributed to an epidemic in the late 1990s
and early 2000s (Sudini and Soetanto, 2005). All those who contracted
malaria slept without a bed net in homes lacking screening and were thus
freely accessible to feeding mosquitoes. Patients lived with cattle in or
near their homes, exacerbating rather than mitigating the risk of exposure
to those anophelines of the area that readily feed on both cattle and
humans. Weak surveillance systems contributed to the worsening of out-
breaks, thereby consolidating the epidemic (Dewi, 2002). Microscopic
diagnostic services in the epidemic zone were found to be unreliable
(Dewi, 2002).
2.2.2.4. Malaria treatment policy and practice

2.2.2.4.1. Treatment of uncomplicated P. falciparum The evolution of
Indonesias malaria treatment policy is shown in Table 2.4 (Departemen
Kesehatan, 2006e, 2007b). The first-line of treatment for uncomplicated
P. falciparum currently consists of two options. The first option is a combi-
nation of artesunate (AS) and amodiaquine(AQ) taken orally for 3 days,
with a single dose of primaquine (PQ, as a gametocytocide) given on the
first day (AS AQ PQ). The dosages of AS, AQ and PQ are 4 mg/
kg weight/day, 10 mg/kg weight/day and 0.75 mg/kg weight, respec-
tively. The alternative first line of treatment is a combination of dihy-
droartemisinin (DHA) and piperaquine (PP) taken orally for 3 days, with
a single dose of PQ (gametocytocidal) given on the first day (DHA PP
PQ). The dosages of DHA, PP and PQ are 24 mg/kg weight/day,
1632 mg/kg weight/day and 0.75 mg/kg weight, respectively. How-
ever, primaquine is contraindicated in pregnant women, infants less than
1 year old and in people with a glucose-6-phosphate dehydrogenase
(G6PD) deficiency. Routine screening for G6PD deficiency very rarely
occurs in Indonesia. The laboratory test for this deficiency is available at
very few hospitals in Indonesia, and even less so at the periphery of
healthcare delivery where most antimalarials are distributed.
The second line of treatment is a combination of quinine(QN),
doxycycline(DX) or tetracycline(TC) and primaquine (QN DX PQ
or QN TC PQ). Quinine is given orally three times a day for 7 days
at 10 mg/kg weight/medication. Doxycycline is given orally two times a
day for 7 days with adults receiving a dosage of 4 mg/kg weight/day and
children of 814 years receiving a dosage of 2 mg/kg weight/day. If DX is
not available, then TC is given orally four times a day for 7 days at
45 mg/kg weight/medication. However, doxycycline and tetracycline
are not recommended for the treatment of malaria in pregnant women or
in children under 8 years of age.
Malaria treatment for P. falciparum, where diagnostic facilities are
available but AS and AQ are not, is a single dose of sulfadoxine and
pyrimethamine at 25 and 1.25 mg/kg weight, respectively. Primaquine
is also given once on the first day at 0.75 mg/kg weight. If the treatment
fails, the patient is treated following a similar procedure to second line
treatment. For malaria endemic areas lacking diagnostic facilities, clinical
malaria is treated presumptively with standard chloroquine (CQ) and a
single dose of PQ as gametocytocide. Chloroquine is given once daily for
3 days: at 10 mg base/kg weight on the first 2 days and at 5 mg base/kg
weight on the third day, whilst the single 0.75 mg/kg weight dose of PQ
can be given on any of those days.
The treatment policy for clinical diagnoses of malaria presents a spe-
cial challenge to Indonesia. In 2006, only 13% (1,246,324/9,319,382) of
estimated clinical malaria cases came with a microscopic or rapid
TABLE 2.4 Malaria treatment policy and practice in Indonesia
P. falciparum Prevention
Clinical during
Year malaria Uncomplicated Complicated P. vivax P.m. P. ovale pregnancy Chemoprophylaxis
1991 CQ First line: CQ (IV or IM) CQ PQ CQPQ CQPQ CQ CQ

CQ PQ CQ SP (IM)
CQ PQ QN (IV or IM)
Second line:
SP PQ
Third line:
QN PQ
2004 CQ PQ First line: First line: First line: CQ CQPQ No DX
ASAQPQ AS (IV or IM) CQ PQ CQ
Second line: AM (IM) Second line:
QNDXPQ Second line: QN PQ
QNTCPQ QN (IV)
2007 CQ PQ First line: First line: First line: CQ CQPQ No DX
AS AQ PQ AM (IM) AS AQ
DHA PP PQ AS (IM) or (IV) DHA PP
Second line: Second line: CQ PQ (if
QN DX PQ QN (IV) ACT is
QN TC PQ absent)
Second line:
QN PQ
ACT, Artemisinin combination therapy; AM, Artemether; AQ, Amodiaquine; AS, Artesunate; CQ, Chloroquine; DHA, Dihydroartemisinin; DX, Doxycycline; PQ, Primaquine; IM, Intra-
muscular; IV, Intravenous; SP, Sulfadoxine-pyrimethamine; QN, Quinine; TC, Tetracycline.
diagnostic test (RDT) confirmation (World Health Organization, 2008e).

This means that 87% of known malaria cases receive treatments known to
be widely ineffective and to actually increase the odds of malaria trans-
mission. To make matters worse, the proportion of cases receiving the
appropriate treatment with artemisinin combination therapy (ACT) may
be even lower when taking into account the cases not reported to the
MoH, which probably represent the vast majority of actual malaria cases
in Indonesia. The lack of diagnostic capacity and the policy aimed at
conserving relatively costly ACT therapies almost certainly result in
most Indonesians being treated with drugs known to be ineffective.
Hasugian et al. conducted a randomized trial that compared the
efficacy and safety of treatment by AS AQ with that of DHA PP
(Hasugian et al., 2007). The study was performed at Timika (Papua) in
2005. Each treatment group enrolled 170 study subjects who were
observed over a period of 42 days. A combination of AS and AQ was
administered on the basis of weight, with a total artesunate dose of
12 mg/kg weight and a total amodiaquine dose of 30 mg/kg weight.
A combination of DHA and PP was administered at a dosage of 6.75 mg/
kg weight of dihydroartemisinin and 54 mg/kg weight of piperaquine.
The study showed that the cumulative risk of parasitological failure with
true recrudescence of P. falciparum infection on day 42 was 16% (95% CI
8.523%) with AS AQ treatment and 5% (95% CI 0.79.4%) with DHA
PP treatment. Patients treated with AS AQ showed a higher risk of
failure than those treated with DHA PP (hazard ratio 3.4; 95% CI
1.29.4). There was no difference in gametocyte carriage between treat-
ments (overall rate, 12.1 cases per 1000-patient weeks). There were signif-
icant differences between treatments in terms of tolerability. Patients
treated with AS AQ, as opposed to DHA PP, were two to three
times more likely to report nausea, vomiting and anorexia. However,
there were no reported differences between the treatments in symptoms
elicited on day 7 and thereafter. In addition, serious adverse events were
noted in three patients in the AS AQ group. Two adults developed
recurrent vomiting on day 3 after completion of a course of AS AQ,
requiring hospital admission but followed by a full recovery within a day.
An adult with P. falciparum infection developed truncal ataxia and inten-
tion tremor on day 7 and his symptoms resolved over the subsequent
8 days. He had a recurrence of P. falciparum infection on day 21 and was
retreated with DHP PP, without further recurrence of infection, symp-
toms or cerebellar signs over the subsequent 42 days. Hasugian et al.
concluded that, in Papua, DHA PP was a more effective and better
tolerated treatment for the multidrug-resistant P. falciparum.
Price et al. assessed the therapeutic efficacy of DHA PP for uncom-
plicated P. falciparum malaria in children and adults (Price et al., 2007).
The study was conducted in Timika (Papua) between 2004 and 2005.
A combination of DHA and PP was administered at a dosage of 2.25 and

18 mg/kg weight/day, respectively, in 515 patients with P. falciparum
infection or mixed infection. All doses were supervised and patients were
examined daily for 42 days. At each visit, a blood smear was taken and a
symptom questionnaire was completed. The study showed that, by day
42, cumulative risk of recurrence for P. falciparum was 7% (95% CI 4.7
9.4%). After PCR correction, the risks were 1.1% (95% CI 0.12.1%). The
median time to recurrence with P. falciparum was 36 days (range: 2245
days). The authors concluded that DHA PP was a highly effective
treatment of uncomplicated P. falciparum malaria in Papua.
Asih et al. evaluated AS AQ as a treatment for P. falciparum malaria
in West Sumba in 2006 (Asih et al., 2009). They reported that, of 103
malaria patients treated, 101 had recovered completely by day 7, one
had retained parasitemia up to day 14 and the remaining two participants
showed the reappearance of parasites on days 21 and 28. The analysis of
genotypes indicated that both participants carried different genotypes
and were thus classified as reinfections rather than treatment failures.
Gametocytes were present in six patients on day 7. In contrast to the
findings of Hasugian et al. in Papua, these authors concluded that AS
AQ was a highly effective treatment against P. falciparum in the Lesser
Sundas.
Syahril et al. evaluated the efficacy of AS AQ as a treatment for
uncomplicated P. falciparum malaria in children at Mandailing Natal
(North Sumatra) in 2006 (Syahril et al., 2008). One hundred and thirty-
five patients were given AS at a dosage of 4 mg/kg weight and AQ at a
dosage of 10 mg/kg weight for 3 days. The study resulted in a 100% cure
rate on day 28. Syahril et al. reported adverse reactions including head-
aches (n 20), vomiting (n 10) and tinnitus (n 1). They concluded
that AS AQ was a well-tolerated, safe and highly effective treatment for
uncomplicated P. falciparum malaria in children in North Sumatra.
The efficacy of QN DX and QN TC against uncomplicated
P. falciparum infections was evaluated in Indonesia. Lubis evaluated the
efficacy of QN DX in children against uncomplicated P. falciparum
infection in Natal (North Sumatra) in 2006 (Lubis, 2008). The study
involved 111 volunteers who were given quinine orally three times a
day at 10 mg/kg weight/medication for 4 days and continued at
5 mg/kg weight/medication for 3 days. Doxycycline was given orally at
dosage of 2 mg/kg weight/day for 7 days. Malaria smears were taken on
days 0, 2, 7 and 28. The study showed that only 2 of 111 volunteers had
malaria on day 2 and a recrudescent on day 28. Common complaints
reported were tinnitus (37%), headache (17%) and vomit (14%). The
study concluded that QN DX provided high efficacy against P. falci-
parum in North Sumatra for children. Similar results were also reported
by Lubis in Natal (North Sumatra) in 2007 (Lubis, 2009). The study
showed that only two of 123 volunteers had malaria on day 2, but they
found no parasitemia after day 7 to day 28. The common complaints
reported were tinnitus (33%), headache (17%) and vomit (15%). The
study also concluded that QN DX provided high efficacy against
P. falciparum in North Sumatra for children.
Tarigan investigated the efficacy of QN TC against uncomplicated
P. falciparum infection in Natal (North Sumatra) in 2002 (Tarigan, 2003).
After randomization, 100 people received QN three times a day for 5 days
(Q5) and 93 people received QN three times a day for 7 days (Q7). Quinine
was taken orally at dosage of 10 mg/kg weight/medication. Tetracycline
was given four times a day at dosage of 250 mg/day to both groups for
7 days. The study showed that 23% (15/64) of Q5 and 2% (1/67) of Q7 were
classified as malaria resistant. One individual in Q7 was RI (resistance
level 1, asexual parasites disappeared within 7 days but had recurrent
parasites between day 8 and 28). Giving QN in 7 days resulted in high
efficacy than those of Q5 (p < 0.001). The most commonly reported com-
plaints were tinnitus (78%) and balance disorder (62%), but the difference
between groups was not significant. The study concluded that giving QN
TC for 7 days was more effective against uncomplicated P. falciparum
infections in North Sumatra, than giving QN only for 5 days.
2.2.2.4.2. Treatment of complicated P. falciparum The first line of treat-

ment for complicated P. falciparum malaria is the administration of artesunate
by intramuscular (IM) or intravenous (IV) route and artemether intramuscu-
lar (IM; Departemen Kesehatan, 2007b). Artesunate with a dosage of 2.4 mg/
kg weight is given on admission, then at 12 and 24 h, and thereafter once daily
until oral medication could be taken reliably. Every 60 mg vial contains
anhydrous artesunic acid, which is dissolved in 0.6 ml 5% natrium bicarbon-
ate and then mixed with 35 ml of 5% dextrose before injection as a bolus into
an indwelling intravenous cannula. When IM artesunate is given, the same
dosage is applied. When the patient has recovered sufficiently to take tablets,
a combination of AS AQ PQ treatment is given as similar dosage at the
first-line treatment of uncomplicated P. falciparum malaria. Alternatively, IM
artemether is given at a dosage of 3.2 mg/kg weight/day, followed by
1.6 mg/kg weight/day until oral medication could be taken reliably. A
combination of AS AQ PQ treatment is then given at similar dosage
for first-line treatment of uncomplicated P. falciparum malaria.
The second line of treatment is a quinine IV drip which consists of
quinine HCl at a dosage of 20 mg base/kg weight, dissolved in 500 ml
dextrose 5% or NaCl 0.9% (Departemen Kesehatan, 2007b). The quinine
drip is administered over 8 h and then followed by 10 mg/kg weight
injected every 4 h until the patient is able to accept oral medication. When
the patient has recovered sufficiently to take tablets, oral quinine at
10 mg/kg weight is administered every 8 h to provide a total quinine
course of 7 days (as per guidelines detailed above). If the IV administra-

tion of quinine is impossible, then the patient is given quinine antipyrine
in IM single doses of 10 mg/kg weight.
The treatment for children is the IV administration of quinine
(Departemen Kesehatan, 2007b). Quinine HCl at a dosage of 10 mg/kg
weight is dissolved in the amount of 5% dextrose or NaCl 0.9% normally
used for a dosage of 75100 ml/kg weight/24 h. This dosage is adminis-
tered for every 8 h. This treatment is repeated each day until the patient is
conscious and able to accept oral medication. If the child is younger than
2 months, then the dose is reduced from 10 to 68 mg/kg weight.
South East Asian Quinine Artesunate Malaria Trial group did an
open-label randomized controlled trial in patients admitted to hospital
with severe P. falciparum malaria in Bangladesh, India, Indonesia and
Myanmar between 2003 and 2005 (SEAQUAMAT, 2005). They randomly
assigned 730 volunteers with IV artesunate and 731 subjects given IV
quinine. The treatment procedure in former group was artesunate
2.4 mg/kg weight given on admission, then at 12, 24 h, and thereafter
once daily until oral medication could be taken reliably. Every 60 mg vial
contained anhydrous artesunic acid, which was dissolved in 1 ml of 5%
sodium bicarbonate and then mixed with 5 ml of 5% dextrose before being
injected as a bolus into an indwelling IV cannula. When the patient had
recovered sufficiently to take tablets, oral artesunate 2 mg salt/kg
weight/day was administered to complete a total course of 7 days
(a total cumulative dose of 1718 mg/kg weight). Alternatively, quinine
dihydrochloride was given in a 20 mg/kg loading dose infused over 4 h
(in 500 ml 5% dextrose water or 0.9% saline), followed by 10 mg/kg
weight infused over 28 h three times a day until starting oral therapy.
When the patient had recovered sufficiently to take tablets, oral quinine at
dosage of 10 mg/kg weight was administered every 8 h to provide a total
quinine course of 7 days. The primary endpoint of this study was death
from severe malaria (in-hospital mortality). The result showed that mor-
tality was less in artesunate recipients than in quinine recipients (15% vs.
22%; p < 0.001). However, no difference in mortality was found in 289
severe P. falciparum Indonesian patients in artesunate and quinine (6% vs.
12%; p 0.078). The study suggested that IV artesunate treatment was
well tolerated, whereas IV quinine was associated with hypoglycaemia
(Risk ratio 3.2, 95% CI 1.37.8; p 0.009).
Tjitra et al. evaluated the efficacy of IM artemether and IV quinine in
complicated P. falciparum malaria adult patients in Balikpapan (East
Kalimantan) in 19931995 (Tjitra et al., 1996a). Two groups of 30 patients
received either artemether or quinine. Artemether was given at 1.6 mg/
kg weight/day on day 0 and followed by a daily dose from the second to
fifth day. Quinine dihydrochloride was given intravenously at 20 mg/kg
weight/day, dissolved in 10 ml/kg weight 5% dextrose, for first 4 h,
then followed by 10 mg/kg weight three times a day until the patient was
able to accept oral medication. Oral quinine at dosage of 10 mg/kg weight
was administered every 8 h to provide a total quinine course of 7 days. The
study showed that mortality rate in the artemether group was less than in
the quinine recipients, but not significantly difference (13% vs. 23%;
p 0.32). The most common complications were hyperbilirubinaemia
(50%), hyperparasitaemia (28%) and cerebral malaria (25%) in both
groups. The authors suggested that IM artemether was as effective as IV
quinine for the treatment of complicated P. falciparum malaria in East
Kalimantan.
2.2.2.4.3. Treatment of P. vivax The current first line of treatment for

P. vivax is AS AQ or DHA PP (Departemen Kesehatan, 2007b). A
combination of AS AQ or DHA PP is taken orally for 3 days at same
dosage as treatment for uncomplicated P. falciparum malaria. In areas
where there is resistant to CQ, the MoH proposed that P. vivax malaria
may be treated additionally with a single dose of PQ given on the first
day. However, the dosage of PQ for P. vivax was less than the treatment of
uncomplicated P. falciparum malaria (0.25 vs. 0.75 mg/kg weight). In areas
in which ACT is absent, the MoH proposed that P. vivax malaria may be
treated with CQ PQ. The CQ was taken orally with a total dosage of
25 mg base/kg weight over 3 days and PQ at dosage of 0.25 mg/kg
weight for 14 days.
The second line of treatment is a combination of quinine and prima-
quine (QN PQ; Departemen Kesehatan, 2007b). Quinine is given orally
three times a day for 7 days at 10 mg/kg weight/medication and PQ at
dosage of 0.25 mg/kg weight for 14 days.
Only one study on combined AS AQ treatment for P. vivax malaria
has been done in Indonesia. Hasugian et al. reported that the cumulative
risk of parasitological failure with P. vivax infection on day 42 was 33%
(95% CI 2542%) with AS AQ treatment and 9% (95% CI 414%) with
DHA PP treatment (Hasugian et al., 2007). Patients treated with AS
AQ showed a higher risk of failure than those treated with DHA PP
(hazard ratio 4.3; 95% CI 2.28.2). In terms of gametocyte carriage,
P. vivax gametocytemia was significantly less likely to occur with DHA
PP treatment (2.5 cases per 1000-patient weeks) than with AS AQ
treatment (36.5 cases per 1000-patient weeks). The authors concluded that
DHA PP was a more efficient and better tolerated treatment for the
multidrug-resistant P. vivax in Papua. They also concluded that the pro-
longed therapeutic effects of PP decreased the rate of recurrence of
P. vivax infection and reduced the risk of P. vivax gametocytemia. How-
ever, these assessments did not apply PQ therapy against relapse and
much of what the authors called parasitologic failure may not be accu-
rately described as such. It is more likely that these therapies were 100%
effective against asexual blood stages and that the recurrences observed
out to day 42 were relapses.
Price et al. assessed the therapeutic efficacy of DHA PP for P. vivax
infections in children and adults in Timika (Papua) between 2004 and
2005 (Price et al., 2007). A combination of DHA and PP was administered
at a dosage of 2.25 and 18 mg/kg weight/day, respectively, for 256
patients with P. vivax or mixed infection. All doses were supervised and
patients were examined daily for 42 days. At each visit, a blood smear was
taken and a symptom questionnaire was completed. The study showed
that by day 42, cumulative risk of recurrence for P. vivax was 9% (95% CI
612%). In those patients failing with pure P. vivax, the median time to
recurrence was 43 days (range: 2245 days). The authors concluded that
DHA PP was an effective treatment of P. vivax malaria in Papua.
To date, there are four studies documenting the efficacy of CQ PQ as
a treatment for P. vivax malaria in Indonesia. Firstly, in 1994, Ompusunggu
et al. reported a low cure rate of 37% (33/90) in Banjarnegara, Wonosobo
and Purworejo (Central Java; Ompusunggu et al., 1994). Secondly, in 1995,
Baird et al. documented the therapeutic failure of CQ PQ in Arso
(Papua) in 5% and 15% of cases, on days 14 and 28, respectively (Baird
et al., 1995a). Then, in 1997, Fryauff et al. evaluated the efficacy of CQ PQ
as a treatment for P. vivax in Arso X/XI (Papua; Fryauff et al., 1997a). They
reported that out of 27 P. vivax malaria patients treated with CQ PQ,
three had recurrent parasitemia by day 28. Finally, in 2005, Tjitra reported
that the cumulative incidence failure of treatment with CQ PQ was 4.7%
in Bangka (South Sumatra) and 15.4% in Lampung (Tjitra, 2005). It is
important to point out that the standard test for resistance to CQ in
P. vivax malaria prohibits the application of PQ until day 28. This is because
primaquine interferes with the assessment by killing chloroquine-resistant
blood and liver stages. At the Arso field site, for example, when PQ was
excluded from the in vivo assessment, virtually all treatments failed within
28 days (Sumawinata et al., 2003).
2.2.2.4.4. Treatment of P. malariae and P. ovale The treatment for

P. malariae is CQ once daily for 3 days at a total dosage of 25 mg base/
kg weight (Departemen Kesehatan, 2007b). The current first line of treat-
ment for P. ovale is CQ PQ. Chloroquine is given as per P. malariae and
PQ is given for 14 days at a dosage of 0.25 mg/kg weight/day. The second
line of treatment is QN PQ. Quinine is taken orally three times a day for
7 days at 10 mg/kg weight/medication. Primaquine is taken for 14 days
at a dosage of 0.25 mg/kg weight/day. A relapse of P. ovale in the next
1428 days is treated essentially as before, except that the dosage of
primaquine is increased to 0.5 mg/kg weight/day. The Indonesian
MoH as yet has no guidelines for the treatment of P. knowlesi infection.
2.2.2.4.5. Chemoprophylaxis As a chemoprophylaxis against P. falciparum

infection, the MoH recommend that non-pregnant adults and older
children receive DX at a daily dose of 2 mg/kg weight for 2 days before
travelling to endemic areas, and throughout the duration of stay in an
endemic area. Such dose can be taken for periods up to 46 weeks
(Departemen Kesehatan, 2007b). As a chemoprophylaxis against P. vivax
infection, the MoH guidelines recommend a weekly dose of 5 mg/
kg weight of CQ to be administered a week prior to entering an endemic
area, and to take whilst remaining in the area (Departemen Kesehatan,
2006e). Since P. falciparum occurs wherever P. vivax is found, the rationale
for recommending CQ prophylaxis against P. vivax malaria only is unclear.
In 1994, Ohrt et al. measured the efficacy and tolerability of DX as
malaria prophylaxis in areas in Papua with resistance to CQ and SP (Ohrt
et al., 1997). After radical cure, 67 Indonesian soldiers were randomly
assigned to receive 100 mg of DX per day and 69 soldiers received a
placebo for 13 weeks. A health worker visited each post every morning
and supervised the medication. Both the health worker and the partici-
pants signed the daily drug record form. Malaria smears were obtained
weekly and when a patient had symptoms suggesting malaria. The study
showed that only one of 67 soldiers in the DX group developed malaria,
but 53 of 69 in the placebo group. Doxycycline yielded protective effica-
cies of 99% against malaria (95% CI 94100%), 98% for P. falciparum (95%
CI 88100%) and 100% for P. vivax (95% CI 90100%). They noted that DX
was significantly better tolerated than the placebo (RR 0.64; p < 0.001).
RR < 1.0 indicated lesser risk in the DX group. They concluded that DX is
highly effective and well tolerated in preventing malaria when taken as
directed.
Several compelling evidences of PQ as prophylactic regimen were also
evaluated in Indonesia. In 19921993, Baird et al. investigated the safety
and efficacy of PQ relative to CQ for prophylaxis in non-immune people
arriving in a hyperendemic area of Arso (Papua; Baird et al., 1995b).
Forty-five subjects received PQ at 0.5 mg/kg weight every other day
and 54 people in the same village received 5 mg of CQ base/kg weight
for 1619 weeks. A blood film was taken from each subject once a week.
The study showed that the risk of malaria among people taking CQ
relative to that of subjects taking PQ was 3.9 (p 0.014) for P. falciparum
and 10.6 (p 0.012) for P. vivax. The minimal protective efficacy for PQ
prophylaxis was 74% against P. falciparum and 90% against P. vivax.
Primaquine was better tolerated than CQ. Physical complaints in the PQ
group were less than the CQ group (Incidence Density Ratio 5.7, 95%
CI 3.68.9). This study suggested that PQ may offer safe and effective
prophylaxis against hyperendemic malaria among non-immune people.
Soon after, Fryauff et al. evaluated the tolerability and safety of CQ
and PQ as prophylactic drugs in Papua in 19931994 (Fryauff et al., 1995).
After giving informed consent and being curatively treated, 126 adult
male Javanese volunteers with normal G6PD activity were randomized
to receive PQ daily at 0.5 mg/kg weight (n 43), CQ weekly at 300 mg
CQ base (n 41) and placebo (n 42) for 52 weeks. Drug consumption
was supervised and each volunteer was visited every day. Malaria smears
were made weekly or on any occasion of symptoms compatible with
malaria. Physical complaints were recorded weekly. The study showed
that prophylactic PQ provided a better protection than the placebo. The
protective efficacies of PQ relative to placebo were 95% (95% CI 5799%)
for P. falciparum and 90% (95% CI 5898%) for P. vivax. Relative to placebo,
chloroquine efficacy against P. falciparum was only 33% (95% CI 58% to
72%) and 16.5% (95% CI 77% to 61%) for P. vivax. More complaints were
recorded in volunteers receiving PQ (Incidence Density 4.7/100 per-
son-week) and CQ (ID 6.2/100 person-week) than in those taking the
placebo (ID 3.6/100 person-week; p < 0.01). Only the incidence of
cough differed significantly in PQ compared to the placebo (IDR 1.7/
100 person-week, 95% CI 1.11.3). Six of 22 men who took PQ on an empty
stomach reported gastrointestinal discomfort. In respect to complete
blood count, renal or hepatic function, there was no difference between
PQ and the placebo. Only the mean value of urea in the PQ group was
significantly higher than the placebo group (p 0.03), but all values were
in the normal range. Therefore, the authors concluded that there was no
indication that the use of daily PQ for 1 year had any negative impact on
the safety of volunteers. The study provided an evidence that PQ is
effective and well tolerated for prevention of malaria.
Fryauff et al. evaluated the response to post-prophylaxis parasitemias
after 4 and 28-weeks of daily PQ and weekly CQ prophylaxis (Fryauff
et al., 1997c). They found that only one of P. falciparum and no P. vivax
infections occurred during the first month after ending PQ prophylaxis.
In contrast, six P. falciparum and three P. vivax infections occurred within
1 month after ending CQ prophylaxis. After 28 weeks of post-prophy-
laxis, in the PQ group, nine of the 30 participants (ID 0.7 infections/
person-year) were infected by P. falciparum and 13 of 30 people
(ID 1.2 infections/person-year) infected by P. vivax. In the CQ group,
10 of 20 participants (ID 1.5 infections/person-year) were infected by
P. falciparum and 10 (ID 1.6 infections/person-year) infected by
P. vivax. Relative to the placebo, there was no significant difference of
attack rates of either infections in PQ and CQ. The geometric mean time to
infection of P. falciparum parasitemia was longer for PQ (77 days) than for
CQ (30 days) or the placebo (45 days), but not significantly (p 0.14). This
also applied for P. vivax (PQ 72 days; CQ 35 days; placebo 44
days), but not significantly (p 0.09). The parasitemias of P. falciparum
and P. vivax infections were not different between groups (p > 0.28). The
mean number of physical complaints registered by subjects receiving PQ,
CQ and placebo was uniform. The authors concluded that there was no
indication that a daily use of PQ or weekly dose of CQ for 1 year placed
subjects at greater risk of malaria infection or to more severe clinical
symptoms of malaria than subjects who had taken a placebo. The results
suggested that PQ had effectively prevented the establishment of liver-
stage parasites.
In 1999, Baird et al. investigated the chemoprophylactic efficacy of PQ
for the prevention of malaria in G6PD-normal individuals lacking clinical
immunity who were living in Armopa (Papua; Baird et al., 2001). A daily
adult regimen of 30 mg PQ for 20 weeks was given to 97 subjects and a
placebo was given to 149 subjects. Each health worker was assigned eight
to 12 subjects and tasked with visiting their homes each morning to
administer the drug with the morning meal. Compliance was verified
by signatures of the health worker and subject on a dosing card. At the
end of each day, supervisors cross-checked the signatures of dosing cards
and affirmed agreement by signing a record sheet. Prophylaxis continued
for 20 weeks or until a subject had a blood film positive for Plasmodium.
The study showed that PQ prevented malaria caused by P. falciparum and
P. vivax for 20 weeks in 95 of 97 subjects. On the contrary, 37 of 149
subjects taking placebo became parasitemic. The protective efficacy of
PQ against malaria was 93% (95% CI 7198%), 88% (95% CI 4897%)
against P. falciparum and > 92% (95% CI > 3799%) for P. vivax. No
adverse event prompted withdrawal from the study, and no serious
adverse events occurred. The only adverse events with a statistically
significant risk ratio (RR) were headache (RR 0.62), cough
(RR 0.50) and sore throat (RR 0.34). RR < 1.0 indicated lesser risk
in the PQ group. The authors concluded that a 30-mg daily adult regimen
of PQ provided well-tolerated, safe, and efficacious prophylaxis against
P. falciparum and P. vivax for 20 weeks among non-immune people living
in endemic Papua.
Primaquine offers healthcare providers an excellent option to standard
suppressive prophylactics for travellers exposed to malaria. Studies sup-
port the view that it is safe, well tolerated and effective in people who are
considered good candidates to receive it (Baird et al., 2003b). Many
evidences reported the efficacy and safety of PQ in Indonesia; however,
PQ is not approved for prophylactic use in Indonesia. The unavailability
of G6PD tests across the country suppresses the usage of PQ as a prophy-
lactic measure.
2.2.2.5. Resistance to antimalarials

Effective treatment is an essential element of malaria control (Roll Back
Malaria Partnership, 2008). The primary objective of an antimalarial treat-
ment policy is to ensure the rapid and complete cure of infections. In
doing so, one reduces morbidity, prevents the progression of
uncomplicated malaria into a severe and potentially fatal disease, reduces

the impact of malaria infection on the foetus during pregnancy, reduces
the reservoir of infection and helps prevent the emergence and spread of
drug resistance (World Health Organization, 2008e). Tests for treatment
efficacy can be used to help establish whether an antimalarial drug is still
effective (World Health Organization, 2005b). Such tests in Indonesia
reveal that drug resistance poses a major threat to malaria control efforts
(World Health Organization, 2003a). As resistance to one or more antima-
larial drugs becomes more prevalent, the malaria control program (MCP)
and other concerned institutions need to respond with new therapies.
This requires evaluating antimalarial drug efficacy in a timely, relevant
and reliable manner. A database for drug monitoring and evaluation that
collects baseline drug sensitivity data may serve as the foundation for an
appropriate monitoring system for drug efficacy (Tjitra et al., 1997). Such
systems have not been assembled in Indonesia. Instead, the characteriza-
tion of patterns of drug resistance depends upon a patchwork of discreet
clinical studies done over the past four decades. The following assembly
of these studies provides the highest possible resolution image of drug
resistance patterns in Indonesia.
To date, we have assembled records of the antimalarial susceptibility
tests carried out in 452 locations across the Indonesian archipelago since
1935. The two antimalarial treatments most often evaluated were CQ and
SP. Resistance to antimalarial treatment was found in P. falciparum,
P. vivax and P. malariae, but no report of resistance in P. ovale.
The distribution of P. falciparum resistance to CQ throughout the main
islands is shown in Table 2.5. Our analysis of the data, extracted from
in vivo and in vitro tests, shows that 52% (1539/2967) and 59% (1022/1743)
of the tests, respectively, revealed resistance to CQ. Table 2.9 shows that
P. falciparum resistance to CQ in eastern Indonesia was significantly
higher than in western Indonesia when only the data from in vivo tests
was taken into account (56%, 1122/2006 vs. 43%, 417/961; Z-test,
p < 0.001). The data from in vitro tests revealed significant difference in
resistance between the two areas (64%, 528/820 vs. 54%, 494/923; Z-test,
p < 0.001).
The distribution of P. falciparum resistance to SP throughout the main
islands is shown in Table 2.6. Eighteen percent (184/998) of the in vivo
tests and 64% (310/487) of the in vitro tests revealed resistance to SP.
Table 2.9 exhibited that P. falciparum resistance to SP in eastern Indonesia
was not significantly different from that in western Indonesia when only
the data from in vivo tests was taken into account (20%, 115/561 vs. 16%,
69/437; Z-test, p 0.057). However, the data from in vitro tests revealed
significantly lower resistance of P. falciparum to SP in eastern than in
western Indonesia (43%, 60/141 vs. 72%, 250/346; Z-test, p < 0.001).
TABLE 2.5 Plasmodium falciparum resistance to chloroquine in Indonesia throughout the Indonesian archipelago
In vivo test In vitro test
Year of No. No. No. Resistance No. No. No. Resistance

Islands sample sites examined resistance (%) Sites examined resistance (%)
Sumatra 19732002 29 439 176 40 19 226 149 66

Java/Bali 19812002 18 365 179 49 12 378 163 43
Kalimantan 19732000 20 157 62 39 11 319 182 57
Sulawesi 19852003 12 405 172 42 9 149 64 43
Maluku 19851995 2 25 8 32 1 11 8 73
Lesser Sundas 19732002 9 270 80 30 6 174 98 56
Papua 19742005 26 1306 862 66 15 486 358 74
Total 19732005 116 2967 1539 52 73 1743 1022 59
The database of P. vivax resistance to CQ was retrieved from these following references:
Sumatra: (Azlin, 2003; Azlin et al., 2004; Dondero et al., 1974; Marwoto et al., 1985b; Maryatul et al., 2005; Ompusunggu et al., 1987, 1989a; Pribadi et al., 1981, 1997; Sutanto et al.,
2010; Tjitra et al., 1997).
Java/Bali: (Baird et al., 1996b; Lederman et al., 2006a; Maguire et al., 2002a; Ompusunggu et al., 1987; Sekartuti et al., 1994, 2007; Simanjuntak et al., 1981; Tjitra et al., 1990, 1991,
1993b, 1997).
Kalimantan: (Ebisawa and Fukuyama, 1975; Fryauff et al., 1998a; Hananto et al., 2001; Ompusunggu et al., 1989b; Pribadi, 1992; Tjitra, 1991; Tjitra et al., 1992, 1993a, 1997;
Verdrager and Arwati, 1974, 1975a; Verdrager et al., 1975a, 1976a).
Sulawesi: (Departemen Kesehatan, 1996; Fryauff et al., 1998b; Kaseke et al., 2004; Ompusunggu et al., 1987; Tjitra et al., 1997).
Maluku: (Tjitra et al., 1997)
Lesser Sundas: (Fryauff et al., 1997b; Gundelfinger et al., 1975; Hoffman et al., 1984; Smrkovski et al., 1983; Sutanto et al., 2004; Tjitra et al., 1997, 2001b).
Papua: (Baird et al., 1991b, 1995c, 1997b; Cylde et al., 1976; Dimpudus et al., 1981; Ebisawa and Fukuyama, 1975; Ebisawa et al., 1976; Fryauff et al., 1999; Gomez-Saladin et al.,
1999; Maguire et al., 2001, 2006a; Nagesha et al., 2001; Pribadi et al., 1998; Ratcliff et al., 2007; Sumawinata et al., 2003; Taylor et al., 2001; Tjitra et al., 1996b, 1997, 2002; Verdrager
et al., 1975b, 1976b).
TABLE 2.6 Plasmodium falciparum resistance to sulphadoxinepyrimethamine throughout the Indonesian archipelago

Year of
Islands sample No. sites No. examined No. resistance Resistance (%) No. sites No. examined No. resistance Resistance (%)
Sumatra 19842001 6 302 43 14 10 121 79 65

Java/Bali 19842001 4 135 26 19 7 89 62 70
Kalimantan 19871991 4 136 109 80
Sulawesi 19841995 3 106 2 2 4 60 33 55
Maluku
Lesser Sundas 19842002 2 52 4 8 1 1 1 100
Papua 19792005 13 403 109 27 8 80 26 33
Total 19792005 28 998 184 18 34 487 310 64
The database of P. falciparum resistance to SP was retrieved from these following references:
Sumatra: (Azlin et al., 2004; Fryauff et al., 2002; Kaneko et al., 1989; Marwoto et al., 1984, 1987; Ompusunggu et al., 1987, 1989a; Pribadi et al., 1997; Tjitra et al., 1997).
Java/Bali: (Maguire et al., 2002a; Marwoto et al., 1984, 1985b, 1987; Ompusunggu et al., 1987; Sekartuti et al., 1994; Tjitra et al., 1990, 1991, 1993b).
Kalimantan: (Ompusunggu et al., 1989b; Pribadi, 1992; Tjitra, 1991; Tjitra et al., 1992).
Sulawesi: (Marwoto et al., 1984, 1985a; Ompusunggu et al., 1987; Tjitra et al., 1997).
Lesser Sundas: (Marwoto et al., 1984; Sutanto et al., 2004)
Papua: (Baird et al., 1991b; Fryauff et al., 1999; Hoffman et al., 1985, 1987; Nagesha et al., 2001; Pribadi et al., 1998; Rumans et al., 1979; Tjitra et al., 2001b, 2002).
Table 2.7 summarizes the distribution of P. falciparum resistance to QN

throughout the main islands. According to our data analysis, one in three
of the in vivo tests and 7% (15/229) of the in vitro tests revealed resistance
to QN. Table 2.9 presents that only a small number of in vivo tests were
carried out. One case of P. falciparum resistance to QN was revealed in
Papua through the use of in vivo test. The in vitro tests showed that
resistance was present on most of the main islands.
Table 2.8 shows the distribution of P. vivax resistance to CQ through-
out the main islands. Forty-eight percent (331/687) of the in vivo tests
revealed resistance to CQ. Table 2.9 shows that the resistance of P. vivax in
eastern Indonesia was significantly higher than in western Indonesia
(57%, 288/502 vs. 23%, 43/185; Z-test, p < 0.001).
2.2.2.5.1. Evaluations prior to 1985

2.2.2.5.1.1. Plasmodium falciparum Plasmodium falciparum resistance to
antimalarial treatments has been documented throughout Indonesia
prior to 1985. Table 2.10 shows the pre-1985 prevalence of P. falciparum
resistance to CQ, SP and QN. According to data analysis, 25% (64/252) of
the in vivo tests and 49% (62/126) of the in vitro tests revealed P. falciparum
resistance to CQ. P. falciparum resistance to SP was revealed in 8% (21/272)
of the in vivo tests and 67% (16/24) of the in vitro tests. P. falciparum
resistance to QN was reported in one of three individuals of the in vivo
test and all of three isolates of the in vitro tests during this period.
The susceptibility of P. falciparum to CQ treatment has undergone
evaluation since 1973 (Dondero et al., 1974). Dondero et al. carried out
two in vivo tests in the Seruwai Plantation, Labuan Deli (North Sumatra)
in 1973 and 1974. However, they found no resistance to CQ during their
7-day follow-up. The limitation of their study was the low P. falciparum
prevalence found (< 8%), which prevented the detection of late recrudes-
cing resistance in a 28-day study.
Verdrager and Arwati first reported 100% (3/3) P. falciparum resis-
tance to CQ in East Kalimantan in 1974 (Verdrager and Arwati, 1974).
A year later, Ebisawa and Fukuyama reported two cases of resistance in
Manokwari (Papua; Ebisawa and Fukuyama, 1975). In 1980, Simanjuntak
et al. carried out in vivo and in vitro tests and reported 100% resistance
(10/10 and 14/14, respectively) in Jepara (Central Java; Simanjuntak et al.,
1981). In 1981, Pribadi et al. documented P. falciparum resistance to CQ in
Southern Sumatra (Pribadi et al., 1981). Treatment with 1500 mg doses of
CQ base failed to cure the patients, as did increased doses up to 2250 mg.
In vitro tests for three patients showed that P. falciparum was resistant to
CQ at the RI level. In vivo observations revealed that the parasite was
resistant with a delayed recrudescence. In 1983, Smrkovski et al.
conducted in vitro tests in Flores (Lesser Sundas) and reported that
P. falciparum was resistant to CQ in 16% (7/45) of the tests (Smrkovski
TABLE 2.7 Plasmodium falciparum resistance to quinine throughout the Indonesian archipelago

Year of
Islands sample No. sites No. examined No. resistance Resistance (%) No. sites No. examined No. resistance Resistance (%)
Sumatra 1997 1 1 0 0
Java/Bali 19831993 4 6 2 33
Kalimantan 19901995 3 142 5 4
Sulawesi 19911995 1 4 1 25
Maluku
Lesser Sundas 1983 1 1 1 100
Papua 19741992 1 3 1 33 8 75 6 8
Total 19741997 1 3 1 33 18 229 15 7
The database of P. falciparum resistance to Q was retrieved from these following references:
Sumatra: (Pribadi et al., 1997).
Java/Bali: (Hoffman et al., 1983; Kirnowardoyo et al., 1993; Tjitra et al., 1993b).
Kalimantan: (Pribadi, 1992; Tjitra, 1991; Tjitra et al., 1992).
Sulawesi: (Tjitra et al., 1997).
Lesser Sundas: (Hoffman et al., 1983).
Papua: (Baird et al., 1991b; Cylde et al., 1976; Pribadi et al., 1998).
TABLE 2.8 Plasmodium vivax resistance to chloroquine throughout the Indonesian

archipelago
In vivo test
Year of No. No. No. Resistance
Islands sample sites examined resistance (%)
Sumatra 19742010 5 67 20 30
Java/Bali 19962002 2 91 11 12
Kalimantan 1998 1 27 12 44
Sulawesi 1998 1 11 1 9
Maluku
Lesser Sundas 19752009 6 87 37 43
Papua 19912008 12 404 250 62
Total 19742010 27 687 331 48
The database of P. vivax resistance to CQ was retrieved from these following references:
Sumatra: (Baird et al., 1996a; Dondero et al., 1974; Fryauff et al., 2002; Schwartz et al., 1991; Sutanto et al.,
2010).
Java/Bali: (Baird et al., 1996b; Maguire et al., 2002a).
Kalimantan: (Fryauff et al., 1998a).
Sulawesi: (Fryauff et al., 1998b).
Lesser Sundas: (Fryauff et al., 1997b; Gundelfinger et al., 1975; Hanna, 1993; McCullough et al., 1993;
Nurhayati, 2003; Sutanto et al., 2009).
Papua: (Asih, 2010; Baird et al., 1991a, 1995a, 1997a, 1997b; Fryauff et al., 1999; Murphy et al., 1993; Siswantoro
et al., 2006; Sumawinata et al., 2003; Taylor et al., 2001).
et al., 1983). Tjitra et al. reported that P. falciparum was resistant to CQ in

73% (8/11) of the in vitro tests conducted in Maluku between 1981 and
1985 (Tjitra et al., 1997).
Rumans et al. first reported P. falciparum resistance to SP in 1979 in
Jayapura (Papua; Rumans et al., 1979). Since then, Hoffman et al. have con-
ducted tests in Jayapura (Papua), revealing resistance in 5% (2/41) and 11%
(2/18) of cases, in 1983 and 1984, respectively (Hoffman et al., 1985, 1987).
2.2.2.5.1.2. P. vivax Dondero et al. carried out two in vivo tests in the
Seruwai Plantation, Labuan Deli (North Sumatra) in 1973 and 1974
(Dondero et al., 1974). However, in a total of 16 individuals with
P. vivax infections, they found no resistance to CQ during their 7-day
follow-up. Guldelfinger et al. also reported similar results on 12 indivi-
duals in Belu (Lesser Sundas) in 1973 (Gundelfinger et al., 1975).
2.2.2.5.2. Evaluations since 1985

2.2.2.5.2.1. P. falciparum Table 2.10 shows the distribution of P. falci-
parum resistance to CQ, SP and QN prior to and since the year 1985.
Our analysis shows that P. falciparum resistance to CQ increased signifi-
cantly from 25% (64/252) prior to 1985 to 54% (1475/2715) after 1985
(Z-test, p 0.001). When only in vitro test results are taken into account,
TABLE 2.9 Plasmodium falciparum and P. vivax resistance to chloroquine, sulphadoxinepyrimethamine and quinine by region.
Western Indonesia Eastern Indonesia

No. No. Resistance p-value
Parasite Drug Test No. examined No. resistance Resistance (%) examined resistance (%) (Z-test)
P. falciparum CQ In vivo 961 417 43 2006 1122 56 < 0.001

In vitro 923 494 54 820 528 64 < 0.001
P. falciparum SP In vivo 437 69 16 561 115 20 0.057
In vitro 346 250 72 141 60 43 < 0.001
P. falciparum QN In vivo 3 1 33 Not done
In vitro 149 7 5 83 8 10 0.142
P. vivax CQ In vivo 185 43 23 502 288 57 < 0.001
p-value < 0.05, significant.

TABLE 2.10 Plasmodium falciparum and P. vivax resistance to chloroquine, sulphadoxinepyrimethamine and quinine throughout the
Indonesian archipelago
Prior 1985 Since 1985

Resistance No. No. Resistance p-value
Parasite Drug Test No. examined No. resistance (%) examined resistance (%) (Z-test)
P. falciparum CQ In vivo 252 64 25 2715 1475 54 <0.001

In vitro 126 62 49 1617 960 59 0.026
P. falciparum SP In vivo 272 21 8 726 163 22 <0.001
In vitro 24 16 67 463 294 63 0.753
P. falciparum QN In vivo 3 1 33 Not done
In vitro 3 3 100 226 13 6 Not done
P. vivax CQ In vivo 28 0 0 659 331 50 <0.001
p-value < 0.05, significant.

the increase in resistance from 49% (62/126) prior to 1985 to 59% (960/
1617) since 1985 is significant (Z-test, p 0.026). The analysis of data
concerning P. falciparum resistance to SP showed different results.
According to in vivo test results, the SP resistance increased significantly
from 8% (21/272) prior to 1985, to 22% (163/726) after 1985 (Z-test,
p < 0.001). However, evidence from in vitro tests shows that resistance
was no different prior to 1985 and after 1985 (67%, 16/24 vs. 63%, 294/
463; Z-test, p 0.753). Several studies reported a resistance of P. falci-
parum to quinine; however, we were unable to calculate the difference
between levels of resistance over different periods as the sample size was
too small. Baird et al. documented the presence of P. falciparum resistance
to QN in Arso PIR (Papua) in 1991 (Baird et al., 1991b). They reported that
60% (6/10) of isolates required higher doses of QN to achieve 50% inhibi-
tion of schizont development.
2.2.2.5.2.2. P. vivax Table 2.10 shows the prevalence of P. vivax resis-
tance to CQ prior to and, since 1985. The resistance of P. vivax to CQ
increased significantly from 0% (0/28) prior to 1985 to 50% (331/659)
since 1985 (Z-test, p < 0.001). We also documented high levels of P.
vivax resistance to CQ after 1985. Baird et al. documented the existence
of CQ-resistant P. vivax in Papua in 1991 (Baird et al., 1991a). Sixteen of 24
residents in Arso PIR II, taking weekly doses of CQ prophylaxis under
supervision, developed P. vivax asexual parasitemia at least once during
8 weeks of surveillance. In June 1990, six local residents and one American
had serum levels of CQ in excess of the ordinarily suppressive 15 ng/ml
at the time of their asexual parasitemias (1670 ng/ml).
2.2.2.5.2.3. P. malariae The susceptibility of P. malariae to antimalarial
drugs in Indonesia has rarely been evaluated. P. malariae resistance to CQ
in Indonesia was first reported on the island of Legundi (Southern Suma-
tra) in 2000 (Maguire et al., 2002b). Maguire et al., using active surveil-
lance, found a 17% (127/752) prevalence of parasitemia by Plasmodium
(31.5% P. falciparum, 30% P. vivax, 37% P. malariae, 1.5% P. falciparum and
P. vivax combined). P. malariae was the most common parasite, accounting
for a majority of malaria cases (41% in Selesung village and 39% in
Keramat village). In a 28-day in vivo assessment, Maguire et al. further
revealed that among 28 study subjects from Selesung and Keramat vil-
lages, one had recurrent parasitemia on day 28 and two had persistent
parasitemia up to day 8. The 28-day cumulative incidence of therapeutic
failure was 12% by life-table analysis. Whole-blood chloroquine and
desethylchloroquine concentrations were at an effective level (larger
than 100mg/l) on day 8 in both cases of persistent parasitemia. However,
no standard definition of resistance supported that diagnosis, and it
remains at least possible (although perhaps unlikely) that CQ-sensitive
asexual blood stages may persist to the eighth day post-therapy, by virtue
of the longer asexual cycle of development in this parasite, that is, the 36-
h cycle of P. vivax versus the 48-h cycle of P. falciparum malaria. However,
Siswantoro et al. made different findings during research conducted in
Timika (Papua) in 2005 (Siswantoro et al., 2006). They evaluated the
efficacy of CQ in treating 50 patients infected by P. malariae and followed
their progress over 28 days. The results showed that there was no reap-
pearance of P. malariae between day 7 (0/42) and day 28 (0/27).
2.2.2.5.2.4. P. ovale Siswantoro et al. evaluated the efficacy of CQ as a
treatment in 14 subjects with P. ovale malaria in Timika (Papua;
Siswantoro et al., 2006). They found that there were no recurrences within
28 days following treatment. This single study constitutes the entire body
of investigation regarding the therapeutic responsiveness of P. ovale in
Indonesia.
As shown by the evidence presented thus far, the resistance to antima-
larial drugs in Indonesia varies a great deal depending on the drug, the
species of parasites, and the geographic location. MoH guidelines remain
essentially the same as they were during the Soeharto years where strong
central authority created monolithic health policies. A policy to treat
clinically diagnosed cases with CQ and SP may often prove inappropri-
ate. Moreover, 87% of clinical malaria cases appear to receive treatments
known to be widely ineffective, as shown by the evidence provided here.
2.3. MALARIA CONTROL IN INDONESIA
2.3.1. Control before independence (pre-1945)

The Dutch made their first voyages to the Indonesian archipelago between
1595 and 1600 (Snapper, 1945). In 1602, the several small navigation compa-
nies that had been competing with each other were merged to form the East
Indies Company, the Vereenigde Oost-Indische Company (VOC). By the
late eighteenth century, the company continually employed 300 surgeons to
treat the sick and to take care of the military garrisons. About 200 surgeons
were working on the ships sailing between Holland and the Indonesian
archipelago or those going between the different islands of the archipelago.
Between 1795 and 1800, no ships from Holland reached the Indonesian
archipelago because of the strict blockade imposed by England. In 1795,
the British took the offices of the Company at the Cape, Near India, Ceylon,
Malacca, the east Coast of Sumatra, Ambon and Banda into custody. In 1811,
the English conquered Java and the rest of the archipelago. Afterwards, in
1816, the Dutch were solemnly reinstated as rulers of the Indonesian archi-
pelago. Gradually, a new administration was built up.
Malaria has almost certainly been presented throughout the Indone-
sian archipelago for as long as humans have inhabited it. History
recorded by European colonists indicates that malaria was a serious

public-health burden during the colonial period, which started around
1600. According to Bontius, in 1630, malaria was prevalent in Batavia
(now Jakarta) in the form of tertian or continual fevers (Van der Brug,
1997). Van der Brug claims that malaria explains, to a large extent, the
high incidence of morbidity and mortality in 1733 in Batavia (Van der
Brug, 1997). Up until 1733, 500700 Dutch employees of the Dutch
colonial trading company (VOC) died each year as a consequence of
typhus, dysentry, malaria and a variety of other causes (accident, injury,
murder, etc.). Such losses accounted for 10% of the new Dutch arrivals
in Batavia. After 1733, the already high-mortality rate of 10% jumped to
5070% of the new arrivals (20003000 died per year). Batavia became
known as a Dutch graveyard and it seems likely that malaria was the main
cause of death. In about 1800, the Dutch began to abandon the old city near
the coast and move further inland to the Weltvreeden area (now the area
surrounding Merdeka Square). Although high malaria mortality continued
to plague the Javanese and Chinese residents of old Batavia, Dutch mortality
fell sharply in their new and healthier surroundings. It is most likely that
they distanced themselves from the dense populations of A. sundaicus, a
species which is an efficient and notorious vector of coastal malaria.
Doolan et al. reviewed naturally acquired immunity to malaria
(Doolan et al., 2009). In the review, they summarized the findings of
Robert Koch who, in 1900, first reported a scientific basis for naturally
acquired protection against malaria. Using cross-sectional studies, Koch
examined the prevalence and density of parasitemia in areas of low
endemicity in Sukabumi (West Java) and areas of high endemicity in
Ambarawa (Central Java; Koch, 1900). Koch deduced that protection
against malaria was acquired only after heavy and uninterrupted expo-
sure to malaria. He found that, in low-endemicity areas, parasites were
uniformly distributed across all ages. In high-endemicity areas, however,
the distribution of parasites was age-dependent. A number of malaria
studies, conducted in Java since the publication of Kochs work, have
largely confirmed his findings. In 1919, Schuffner published his study
carried out in Sundatar (West Sumatra; Schuffner, 1919). He found that
the prevalence of parasitemia was higher among children than adults.
Schuffner was aware of Kochs hypothesis that acquired immunity could
only occur as a result of life-long uninterrupted exposure (Baird, 1998).
Schuffner was therefore puzzled by the age-dependent protection from
parasitemia that he observed, despite the lack of the high degree of
exposure apparently necessary (Baird, 1998).
The Civil Medical Service (CMS) was founded in 1826 (Snapper, 1945),
and then reorganized in 1911 (Overbeek and Stoker, 1937). It provided
medical services to the community for a wide variety of infections,
including malaria. The Public Health Service within the CMS focused
on disease prevention, studying, amongst other things, the development

of plasmodia in local anophelines and seeking to develop best practices in
combating malaria. In 1876, a medical school for Indonesian physicians
was opened in Jakarta. In 1913, a similar school was started in Surabaya
(East Java). Medical science in Indonesia at the time also greatly profited
from the publication of several periodicals, such as Het Natuur en
Geneeskundig Archief (18441847), Het Geneeskundig Tijdschrift voor
Nederlandsch Indie (l8511942) and Medeelingen van den Dienst der
Volksgezondheid van Nederlandsch Indie (19101930). In 1924, the Cen-
tral Malaria Bureau was established as a subdivision of the Public Health
Service. This marked the beginning of programmatic malaria control in
Indonesia. The Central Malaria Bureau worked with the Division of
Sanitary Works and Housing, ensuring that they too concerned them-
selves with malaria sanitation, that is, building out or away from anophe-
line breeding sites. The Central Malaria Bureau offered training to over a
100 malaria assistants; the first cadres, or government employees, dedi-
cated to the technical tasks which form part of malaria control operations.
In this pre-1945 period, these tasks almost exclusively involved carrying
out antilarval measures.
These antilarval measures consisted mainly of environmental modifi-
cations. Following the example of Watson in British Malaysia, Swellen-
grebel pioneered the technique of species sanitation in Indonesia in 1919
(Swellengrebel, 1950). Watson had visited Swellengrebel in Sumatra in
1913 and introduced him to the working concepts of species sanitation
(Takken et al., 1990). The technique involved identifying the breeding and
feeding sites of the most important vectors, in order to then make a
systematic attack on those sites using standard civil engineering techni-
ques. Watson had beaten down a malaria epidemic at Port Swettenham in
Malaysia (the newly opened maritime port of the rubber-growing dis-
tricts) in this manner. He had simply lined the drainage ditches over an
area of 24,000 acres with cement and had thus denied the A. maculatus
species, its much preferred breeding site in rocky pools along streams.
As a result, the vector perished and malaria vanished from over 500
square miles. The measures Watson prescribed amount to the essential
basis of malaria control today: (1) determine the geographic distribution
of malaria; (2) collect, identify and list the species of anophelines present;
(3) examine the association of malaria and anopheline distribution and
thereby identify the anopheline species involved in transmission;
(4) determine the natural rate of infection with each species of malaria
parasite and (5) identify the principal breeding places of the incriminated
anopheline vector species. This approach concentrates resources for con-
trol at the crucial point for their effectiveness: the active breeding sites of
the important vectors in those areas where malaria is occurring in
humans. In other words, species sanitation was, and is, a useful approach
to combating malaria by specifically targeting only the breeding places of

those anophelines known to actively transmit malaria (Takken et al.,
1990). Swellengrebel embraced this approach (Swellengrebel, 1950),
saying in 1931, Malaria is a local disease to be dealt with by local efforts.
Takken et al. reviewed the Dutch literature describing the implemen-
tation of sanitation before 1945 (Takken et al., 1990). They described 46
sites, located in Sumatra (13 sites), Java (28 sites), Sulawesi (three sites),
the Lesser Sundas (one site) and Papua (one site), at which extensive
sanitation measures were implemented. The first systematic antimalarial
measures were undertaken in 1919 at Sibolga (North Sumatra; Takken
et al., 1990). Out of all the sites across Indonesia, 41 dealt with a total
of eight malaria vectors: A. sundaicus (26 sites), A. aconitus (nine sites),
A. maculatus (six sites), A. sinensis (three sites), A. hyrcanus (two sites),
A. minimus (one site), A. bancrofti (one site) and A. punctulatus (one site).
Only 15 of the 46 sites documented the effects of sanitation on mortality
and spleen index. For these 15 sites, the distribution of sites by species
was A. sundaicus (13 sites), A. aconitus (three sites), A. maculatus,
A. sinensis, A. bancrofti and A. punctulatus (one site each). Spleen index
refers to the percentage of people sampled who have a palpable and
therefore enlarged spleen, presumably as a consequence of relatively
heavy exposure to malaria. This was widely used as a crude measure of
transmission intensity before the advent of microscopic blood film exam-
inations. According to this criterium, the sanitation measures against
A. sundaicus proved extremely successful, with records showing a reduc-
tion of the spleen index from more than 80% to less than 20%, and a fall in
the mortality rate from 80 deaths to less than 18 deaths per 1000 of
the population per year after implementation in Sibolga (North Sumatra).
The sanitation measures implemented in Sibolga are exemplary
of antimalaria sanitation measures. In 1912, Sibolga, on the west coast of
Sumatra, was an administrative and trade centre. It was situated beside a
bay at the mouth of a river and was surrounded by steep foothills.
A European residential and administrative area was located on a nearby
coastal plain. The community based there suffered epidemic malaria,
with a mortality rate of 8% and a spleen index of 1598%. Investigation
showed that the highest larval densities occurred in a nearby swamp area.
This area was used to dump waste products from coconut plantations,
along with refuse from the town market. The waste blocked the flow of
sea water and created breeding sites for A. sundaicus. De Vogel recom-
mended eliminating breeding sites by improving drainage. He was
unsuccessful in opposing a plan to fill the tidal swamp areas; a plan
which was thus implemented by the harbour authorities in 1919
(Takken et al., 1990). This solution cost five times the amount that
De Vogel had in mind. Nonetheless, the project roughly halved the
spleen index.
Schuffner introduced a new form of species sanitation in 19161917

(Swellengrebel, 1950; Takken et al., 1990). In Mandailing (North Sumatra),
malaria was endemic, with a spleen index rate exceeding 90% in both
children and adults. Rice was grown only in the wet season, as there was
no irrigation system. When it was harvested, the rice fields remained
fallow. Scattered between these were fishponds harbouring breeding
sites for A. sundaicus and seven other anophelines. Schuffner taught the
people of Mandailing, including school children to recognize the adult
mosquitoes of this species. Village leaders from selected villages delivered
captured anophelines to the local malaria laboratory, where these were
identified and registered by location captured. This represents a superb
early example of community participation in malaria control. The detailed
and accurate knowledge of local vectors led to successful control. Unfor-
tunately, after only 1 year of such success, the central government declared
the practice an illegal forced labour. Schuffner made another contribution
when he pointed out that the fish raised in the aforementioned ponds did
not contribute to the communitys diet. In other words, the elimination of
these ponds would not directly affect nutrition in the community.
Although they made some contribution to economic activity, on the
whole they seemed disposable and they were successfully removed.
At the behest of Swellengrebel, the government purchased all fishponds
and prohibited the laying out of new ones. After just a few years, the spleen
index was down to 10%. The fact that no other species of anopheline
besides A. sundaicus had been affected by this measure offered a compel-
ling demonstration of the efficacy of properly applied species sanitation.
Another example of successful species sanitation is Mangkuwinotos
work in the plain of Cihea, Cianjur (West Java) in 1917 (Overbeek and
Stoker, 1937; Swellengrebel, 1950). Cihea plain was a rice-growing region
dependent on rain cycles for cultivation. Rice fields were cultivated once a
year during the wet season. Planting and harvesting occurred at about the
same time as the cultivation and fields lay fallow in the dry season. An
irrigation project, begun in 1854 and continuing until 1904, eventually
covered over 5000 ha of rice fields. This meant that rice could be grown all
year round. Each farmer planted and harvested at the time he thought
best. This new practice led to severe malaria epidemics. In 1911, Van
Gorkom surveyed the affected villages and found a spleen index of 42%
among native workers and their families living on the rice estate, and a
spleen index exceeding 50% in the surrounding villages (Takken et al.,
1990). In 1913, Van Gorkom showed that malaria led to a reduction in the
number of labourers who were able to cultivate water-covered rice fields.
More uncultivated rice fields in turn led to the creation of more breeding
sites for anophelines. He recommended regulating the water supply by
diverting irrigation from uncultivated rice fields, and by improving the
drainage system from all fields. These recommendations failed owing to
objections from farmers. There were insufficient labourers available to

prepare the rice fields in the short time frame imposed by his plan.
Farmers kept their fields submerged because the dry soil needed inunda-
tion before the next cycle of cultivation. In 1917, Van Lonkhuysen and
Darling incriminated A. aconitus as the vector in Cihea (Darling, 1926).
Later in the same year, Mangkuwinoto, as health officer for the region,
confirmed A. aconitus as the dominant local vector of malaria. He
described uncultivated and weed-covered rice fields as the preferred
breeding site for this mosquito. The largest quantities of larvae occurred
in fields where rice had been harvested and the remaining stalks simply
trampled down (Swellengrebel, 1950). These rice fields were still being
deliberately flooded in preparation for the next planting. Mangkuwino-
tos recommendations resembled those of Van Gorkom (Takken et al.,
1990). This time, however, the scheme proved exceptionally successful in
Cihea. He collaborated with agricultural experts and set up a revised
planting schedule. The regulation of the water supply was introduced
by dividing the agricultural area into two separate irrigation schemes. The
irrigation supply to the area covered by the first scheme was conducted
on 15 September 1919 and to the second on 1 December. At the end of
December, 70% of the fields had been prepared or planted. On February 1,
and every 2 weeks thereafter, the irrigation supply to the area of the first
scheme was reduced by one-sixth before being completely stopped on
April 15 (Takken et al., 1990). The gradual reduction of the irrigation
supply to the area of the second scheme was staggered in the same way
from the beginning of April. Following the end date for irrigation, water
was supplied only for bathing, drinking, washing and the watering of
non-rice crops. Fish cultivation was prohibited. Swellengrebel noted that
enforcing this planting schedule stopped the exhaustion of the soil and
thus improved its growing qualities (Swellengrebel, 1950). There was no
need to keep a harvested field flooded in order to provide a neighbouring
field with water. Although this measure did not completely remove all
breeding sites of A. aconitus, the number of malaria cases sunk to a very
low level. Overbeek and Stoker documented that the spleen index for the
entire Cihea plain, which had been 88% in 1919, fell to 72% in 1922, 20% in
1931 and 13% in 1935 (Overbeek and Stoker, 1937). The annual all-cause
death rate fell significantly from 34 per 1000 population (1919) to 15 per
1000 population (1935). The collaboration with local farmers was neces-
sary to keep the regulation functional. The solution, of course, had
to allow for effective agriculture. Mangkuwinoto, local administration
officials and irrigation superintendents delivered malaria education to
village leaders and landowners (Takken et al., 1990). They showed them
anopheline larvae, anopheline adults and dissected mosquito stomachs,
and also taught the preparation and reading of blood slides, described
anopheline-borne malaria transmission and explained the importance of
measures against the mosquitoes. Today, one can visit this district and see
a stone landmark praising the historic effort that so improved the health
of the residents. Unfortunately, the landmark makes no mention of the
malariologist responsible for this effort. Instead, it is dedicated to
Wiranata Koesoma, who served as Regent of Cianjur between 1912 and 1920.
Swellengrebel documented the situation in the plain of Cihea from
1942 to 1945, during the Japanese occupation of Java (Swellengrebel,
1950). The Japanese occupiers identified A. maculatus as the main vector
and discouraged the maintaining of the planting schedule. Remarkably,
residents defied this and continued to follow the schedule. In 1946,
malaria nonetheless remained a problem in Cihea with a spleen index of
30%. At some later date, probably during the Global Eradication cam-
paign of the 1950s and 1960s, malaria finally vanished from the region.
Bowolaksono concluded in 2000 that the old irrigation system implemen-
ted by Dutch colonial authorities was still being used, albeit without
irrigation scheduling (Bowolaksono, 2000). Between 1989 and 1999, not
a single case of malaria was reported by the two primary health centres
(Bojongpicung and Ciranjang). A. aconitus mosquitoes are still present,
but the parasite seems to be entirely absent.
Species sanitation measures were also implemented to combat coastal
malaria at Batavia (Jakarta) and Pasuruan (in East Java). In 1908, De Jonge
found a higher mortality rate and a higher spleen index in coastal areas of
Batavia than in other parts of the city (Takken et al., 1990). His investiga-
tions led him to identify rice fields and marine fishponds as the main
breeding sites of malaria vectors. He concluded that environmental man-
agement was not feasible and suggested instead that quinine be
distributed to malaria patients for free. Van Breemen and Sunier investi-
gated the association between malaria and the presence of marine fish-
ponds in the coastal areas of Jakarta in 1917 and 1918 (Van Breemen and
Sunier, 1919). They noted that the mortality rates and spleen indices
among communities surrounding marine fishponds were higher than in
other communities. A. sundaicus were found breeding in vast numbers in
these ponds. They recommended that all fishponds be filled in, and that
the land be reclaimed for agriculture across a broad swath of what is now
north Jakarta. However, the authorities considered these recommenda-
tions to be impractical and expensive. Moreover, the community would lose
a vital source of both food and income. The difficulty was that water plants
floating near the surface of the fishponds, whilst on the one hand providing
food for the fish, were on the other hand providing shelter for anopheles
larvae (the thick mats of algae or vegetation protect the larvae from preda-
tion by fish). Van Breemen tried to make use of tidal movements and free
access between fishponds and sea water as Mangkuwinoto had done in
Probolinggo (East Java) in 1921 (Takken et al., 1990). It was hoped that this
would make the fishponds unsuitable breeding places. However, this
approach failed because the height of the tide in Probolinggo (over 2.5 m)
had been much greater than it was here (1 m).
In Pasuruan (East Java), in 1922, Reijntjes disproved the notion that
cultivated fish depended on the water plants at the surface of the fishpond
for food (Takken et al., 1990). He showed that the blue-green algae at the
bottom of the pond were their primary food source. He drained experi-
mental ponds for a few days each month to expose the bottom of the ponds
to sunlight. A shallow layer of water was maintained for several days to
stimulate the growth of these algae. During this time, the fish were kept in
a narrow ring channel. Once the algae had thrived, the ponds were refilled
with seawater. The floating water plants were killed off by this process.
The cultivation of fish thrived and the anophelines vanished. In 1928,
fishpond management, as outlined by Reijntjes, was adopted in Jakarta.
Between 1928 and 1932, 291 ha of fishponds were sanitized against
A. sundaicus using this method. In 1931, the Central Malaria Bureau eval-
uated the efficacy of this sanitation measure and found that the number of
malaria cases (calculated according to the spleen index) had fallen from 39
per 1000 population (19251929) to 27 per 1000 population (1931).
As far as the use of quinine as a malaria treatment and a method of
control were concerned, Indonesia was well known as being the most
productive producer of cinchona in the world before 1945. In 1987,
Gramiccia reviewed the historical endeavour of smuggling cinchona seed-
lings from South America to Europe and Asia (Java and India; Gramiccia,
1987). Sydenham in 1666 and Torti in 1712 recorded how the cinchona
barks effectiveness against malaria fever increased the demand of the
plant. By 1820, Pelletier and Caventou had established how to isolate
quinine from the bark, thus creating a huge demand for bark that yielded
the highest quantities of quinine. In 18521854, the Dutch Government
sent Hasskarl, an employee at the botanical gardens in Bogor (West Java),
to South America. He soon requested that Schukraft, the Dutch Consul in
La Paz, bought good Cinchona seeds from the South American Indians
and have them sent to Java. About 75 of the 500 seedlings sent were still
alive on arrival in Bogor. In 1857, Junghuhn was appointed, after Hasskarl,
as the inspector of the cinchona-cultivation in Java and he instructed to
plan the cinchona at higher altitude (de Knecht-van Eekelen, 2000). The
cultivation of these seeds was a success on the plateau of Pangalengan
(West Java). At this early stage, however, none of the four varieties
of Cinchona calisaya yielded more than very low quantities of quinine
(0.31.5%). Commercial success was not yet within grasp. In 1865, Charles
Ledger, a British trader, sent cinchona seeds of high-yield varieties to
London. He had only managed to find these among a pure population of
cinchona trees in Eastern Bolivia in 1851, with the help of his local com-
panion, Manuel Incra Mamani. Charles Ledger asked his brother George
Ledger to sell the seeds to the British Government. The British
Government refused and George then sold 1 pound of these seeds to the
Dutch Consul in London. The seeds were sent to Java and received in
December 1865 by the Dutch Cinchona Plantation headed by Van Gorkom
(Kerbosch, 1931). Of 20,000 germinated seeds, 12,000 were planted alive.
In 1872, Moens first analysed the bark of Ledgers cinchonas and found an
astonishingly high yield of quinine in the bark (13.25% weight to weight).
Such a yield effectively gave the Dutch on Java a monopoly on the trade in
quinine. In Java, there were 127 cinchona estates and 85 of them were
located in Preanger (West Java). These plantations constituted 75% of total
production in Java. Extremely fertile volcanic soils and suitable elevation
contributed to the huge success of cinchona cultivation. In 1875, Indonesia
was responsible for 97% of the worlds production of cinchona bark.
Indonesia maintained this monopoly right up to the invasion of Java by
the Imperial Japanese Army in early 1942. Dutch merchants at seaports in
Cilacap, Batavia and Surabaya refused the requests of Allied naval com-
manders to load the many tons of quinine stored in maritime warehouses
onto their warships evacuating to Australia as the Japanese advanced. The
loss of Java and its cinchona plantations, along with this huge stock of
quinine, helped to spark the urgent wartime effort by the American gov-
ernment to develop new therapies for malaria. This effort would ulti-
mately result in chloroquine and primaquine, the former rendering
quinine no longer valuable as a trading commodity.
Leimena noted that there was no possibility of controlling malaria dur-
ing the Japanese invasion of 19421945 (Leimena, 1956). All activities were
directed at supporting Japans war machine. Many malaria sanitation mea-
sures were neglected. Although the training of malaria assistants was
continued by the Japanese, it was a superficial effort without yield (Azir,
1957). Many health personnel were captured and died in internment camps.
The medical school in Surabaya (East Java) was closed down and the newly
graduated physicians were forced into military service. Indonesian scien-
tists at the famous medical research institute of Nobel laureate Christiaan
Eijkman in Jakarta were accused by the Japanese of creating biological
weapons. They were all imprisoned and only a forced confession by the
director (Achmad Mochtar) led to their release. He was beheaded by his
captors on 3 July 1945. The long war brought starvation, deprivation, slave
labour and a surge in endemic malaria where it had existed previously, and
epidemic malaria where it had previously been brought under control. The
period between 1942 and 1945 is therefore an anomaly and by no means
representative of the progress made between 1915 and 1941.
During the period before 1945, 98 cross-sectional malaria surveys were
conducted across the archipelago. The distribution of these surveys was
as follows: 60% in Sumatra, 23% in Papua and 16% in Java. The prevalence
of P. falciparum in Papua (12%; 926/7677) was higher than it was in either
Sumatra (8.9%; 3142/35,115) or Java (5.1%; 87/1696). The prevalence of
P. vivax was also higher in Papua (6.1%; 469/7677) than it was in Sumatra
(3.4%; 1196/35,115) or Java (3.3%; 56/1696). However, the prevalence of
P. malariae was much higher in Java (13%; 221/1696) than in either
Sumatra (1.2%; 421/35,115) or Papua (0.5%; 38/7677).
Nonetheless, malaria control measures available in Indonesia in the
period before independence were, in retrospect, extremely limited. Not
only were tools such as routine microscopic diagnosis, chloroquine, prima-
quine and DDT not yet available, the few tools that were available tended
to be found only where the Dutch had a commercial interest. Vast swathes
of the archipelago lived with malaria much as they had done in the millenia
before. There was no healthcare delivery system. There was no government
to take responsibility for the health of all residents rather than only those in
areas near Dutch interests. Indonesian nationalists would fight and win a
bloody war of independence from the Dutch from 1945 to 1949.
2.3.2. Malaria Control Program (19451958)

During the early period of independence, Indonesia faced multidimen-
sional problems. After the declaration of independence on 17 August 1945,
important military clashes occurred against the British forces. They were
present primarily to disarm and repatriate Japanese forces, but they had
been forced into the position of supporting the reintroduction of Dutch
military rule and authority. In 1947 and 1948, the nationalists fought
against the reintroduced Netherlands Indies Civil Administration
(NICA). Nevertheless, as the war for independence raged, the MoH of
the Republic of Indonesia was established between 1945 and 1947. The
ministry oversaw the successful manufacture of quinine at Leles, Lawang
and Madiun (Leimena, 1956). At this time, there were only 830 physicians
in Indonesia for about 60 million people. Essential drugs were obtained
from Red Cross organizations in countries such as India, Australia, Egypt
and Malaya. After an initial peace agreement in 1948, the territory of
Indonesia was reduced and the MoH now served only 30 million people.
In Magelang (Central Java), the MoH established a malaria research centre
and a centre for rural hygiene. At this time, 472 physicians and 167 nurses
specially trained to treat malaria. After the transfer of sovereignty was
formally signed on the 27 December 1949, a period of health reconstruction
was established under the United States of Indonesia. The national MoH
was established as a collaboration of the health ministries of seven member
states. The number of physicians increased to about 1200 for 75 million
people. On 17 August 1950, the United States of Indonesia changed its
name to the Republic of Indonesia and the national body of health services
was reorganized once again. Leimena, who was Health Minister at the
time, identified malaria as public enemy number one, owing to its role in
the huge loss of manpower and economic activity. It has been estimated
that malaria affected 30 million of the 77 million people who populated the
Indonesian archipelago in the late 1940s and early 1950s (Azir, 1957;
Ketterer, 1953).
By 1945, the discovery of DDT (in 1939) and its wartime exploitation
by the Allied Forces had led to it being used for IRS for public-health
purposes. Many studies examined its effectiveness against anopheline
mosquitoes. In 1949, Swellengrebel and Lodens found that a single appli-
cation of 5% DDT solution in kerosene reduced the density of A. aconitus
and A. subpictus for 6 months in Cianjur (West Java; Swellengrebel and
Lodens, 1949). In 1950 Bonne-Wepster and Swellengrebel reported that
the residual effect of DDT on A. sundaicus lasted for 5 months in Tanjung
Priok (north Jakarta; Bonne-Wepster and Swellengrebel, 1950). In 1951,
van Thiel and Winoto reported that with two cycles of DDT spraying, the
infant parasite rate was reduced from 36% to 0% in Marunda (north
Jakarta; Van Thiel and Winoto, 1951). The results of these studies showed
the way towards an era of attacking endemic malaria.
The MCP of the fledgling Republic of Indonesia received generous
support from their counterparts abroad. Suparmo detailed the difficulty
in acquiring DDT and sprayers (Soeparmo, 1958). Mainly, the MCP was
operated by the MoH with assistance from the Technical Cooperation
Administration Mission (formerly the Economic Cooperation Administra-
tion Special Technical and Economic Mission, currently the United States
Agency for International Development, USAID). USAID assistance began
in October 1950, providing US$ 1,449,000 for DDT, technical assistance,
educational activities, sprayers and other commodities. The population
goal of the spraying program was about 5 million people by the end of
1953. In 1950, the WHO provided US$ 74,000 for a malaria control demon-
stration area on the south coast of Java. In 1951, the Malaria Institute,
USAID and the WHO launched an MCP focusing on routine DDT spray-
ing in Java, South Sumatra, Northern Central Sulawesi and Maluku in
areas with spleen indices of 50% or higher. The acceleration of the MCP
(19521959) was launched by routine implementation of DDT house
spraying and mass chloroquine treatment (Soeparmo and Laird, 1954).
In 1954, however, DDT resistance in mosquitoes was reported. Cren-
dell discovered DDT-resistant A. sundaicus at Cirebon (West Java;
Crendell, 1954). In 1956, Chow and Soeparno reported that, in Semarang
(Central Java) and Surabaya (East Java), A. sundaicus had become 2327
times more resistant to DDT than when the insecticide had first been
implemented (Chow and Soeparmo, 1956). Dieldrin was introduced to
combat this DDT resistance. A. sundaicus gradually disappeared from the
northern coastal area of Java (Soemarlan and Gandahusada, 1990).
Despite the decrease in malaria on the northern coast of Java, it persisted
(and still does) on the southern coast. This may have been a consequence
of the presence of another important vector, A. maculatus, a dominant
species found along the copious hillsides along the southern coast (the
northern coast is a plain almost completely without hills).
The success of DDT spraying was reported from what continued to
be (until 1963) the Dutch colonial possession of western New Guinea
(currently Indonesian Papua). In 1954, Metselaar carried out spraying in
houses along Lake Sentani with a 2 g/m2 dosage of 5% DDT wettable
powder (WP; Metselaar, 1956b). The parasite rate fell from 47% (736/
1566) to 20% (260/1301) in hyperendemic areas and from 16% (346/2162)
to 6% (81/1350) in mesoendemic areas. Meanwhile, in control areas (in
Nimboran), the parasite rate dropped from 87% (871/1001) to 64% (495/
773). In experiment areas, the sporozoite rate fell from 1.2% (9/744) to
0.2% (4/1657) in the punctulatus group of mosquitoes. Metselaar found
that the spraying did not completely prevent transmission as a few
sporozoite-positive mosquitoes and new infections in infants were
found. He concluded that the eradication of local vectors and malaria
parasites in New Guinea could not be achieved through residual spray-
ing, but that it was reasonable to expect a much lower degree of endemic-
ity as a result of spraying.
Spraying alone did not interrupt malaria transmission in Papua. Van
Dijk performed mass chloroquine treatment in Demta where DDT spray-
ing had been going on twice a year since 1954 (Van Dijk, 1958). He
achieved almost complete population coverage and distributed chloro-
quine once a week for 8 successive weeks. A year later, the parasite
prevalence had dropped from 41% to 2%. The use of chloroquine in
table salt distributed to the population in these highly endemic areas
may have been the starting point of the resistance to chloroquine devel-
oped by the Plasmodium on the island of New Guinea.
Malaria control produced beneficial economic effects in Indonesia.
Ketterer and Suparmo provided evidence of economic benefits to rice
production, export products and transmigration projects (Ketterer, 1953;
Soeparmo and Stoker, 1952). In September 1951, DDT spraying was con-
ducted along the bay of Banten (Northwest Java) with the total cost of
initial spraying reaching US$ 12,000. This was an area of more than 10,000
acres of highly productive land, which had been abandoned after the
Japanese occupation had destroyed the pre-war drainage system.
A malaria epidemic in 1944 affected 80% of the people living there and
had forced them to abandon the land. As soon as the DDT spraying was
successful, all idle land was cultivated and produced rice again. As a
result, the total value of rice production was US$ 740,000. In other words,
with an investment of just US$12,000 in malaria control, the direct yield in
rice production alone paid for the intervention more than 500-fold. In
palm oil estates, DDT spraying in 1950 reduced the rate of malaria admis-
sions to hospitals from 30% (700/2363) to 7% (90/1346). This resulted in a
dramatic decrease in absenteeism and an increase of working days and
productivity. DDT spraying was conducted in the transmigrant areas of

Metro (Lampung) and Dumoga (North Sulawesi) in 1951 and 1952. In
Metro, the prevalence of malaria in infants (012 months) fell from 21%
(392/1849) before spraying to 2% (27/1506) after spraying (Soeparmo and
Stoker, 1955).
In conclusion, in the period between 1945 and 1958, malaria control
activities relied heavily upon DDT spraying. The success of DDT in
various places in reducing malaria transmission motivated a broader
application. Healthcare systems were just beginning to be established at
the district level at a time of growth for the government and for military
hospitals. Passive case detection (PCD) started and clinical examination
became a dominant instrument for malaria diagnosis. In urban areas,
malaria examination was by microscopy. Whatever the method of identi-
fication, malaria was treated using chloroquine and quinine.
2.3.3. Malaria Eradication Program (19591968)

Successful malaria elimination campaigns in Greece, Italy, Japan, Taiwan,
Australia and almost all the Caribbean islands, to name a few, gave hope
that malaria could be eradicated. The Global Malaria Eradication
Program (GMEP) was launched at the 8th World Health Assembly in
1955. This strategy relied heavily on DDT spraying to interrupt malaria
transmission. In response, the Indonesian Government altered its policy
from an MCP to a Malaria Eradication Program. In January 1959, the
Indonesian Government together with the WHO and USAID established
The National Malaria Eradication Services (NMES) or KOPEM (Komando
Operasi Pembasmian Malaria) which aimed to eradicate malaria by 1970.
The program was launched by President Soekarno in Yogyakarta on 12
November 1959. This date is still celebrated in Indonesia today as
National Health Day.
The NMES divided the nation into 66 zones, each with an average
population of 1.4 million people. Each zone was further divided into
2040 sectors. The program consisted of three phases: (1) 1 year of pre-
eradication, (2) 3 years of attack and (3) 3 years of surveillance prior to
maintenance. After the first year of spraying, the transmission index or
infant parasite rate was expected to be zero, indicating that malaria
transmission had been stopped (Soemarlan and Gandahusada, 1990).
With reinfection no longer an issue, all remaining malaria cases were to
be treated and cured. Only a few cases would then remain after 3 years.
Any relapses or imported cases were to be detected and cured. DDT
spraying operations were conducted twice a year. Over 9000 tons of
DDT were used to protect about 65 million people in 42 zones of Java
and Bali during the period 19591963.
However, insecticide resistance developed among mosquitoes. A. sun-

daicus and A. aconitus were found to be resistant to the DDT replacement,
dieldrin. The first record of dieldrin resistance in A. sundaicus was on the
coast near Yogyakarta in 1959. A. aconitus was found to be resistant to
dieldrin in Subah (Central Java) in the same year (Soerono et al., 1965).
Reports of dieldrin-resistance came from South Sumatra and all of Java.
It became apparent that dieldrin resistance was spreading in A. sundaicus
and A. aconitus. This hampered the eradication plan.
Moreover, the criterium which had to be met in order to switch from
attack phase to consolidation phase was not fulfilled. An API below 0.1
per 1000 of the population was designed as the cut-off between the attack
and the consolidation phase. Data cited by Atmosoedjono in Takken et al.
showed that the API in Java and Bali was still higher than 0.1 per 1000 of
the population between 1963 and 1968 (Takken et al., 1990). Unfortu-
nately, no malaria data was reported between 1959 and 1962. PCD never
reached the minimal 10% of annual blood examination rate (ABER) as
recommended by the WHO (Ray and Beljaev, 1991). In 1966, the number
of malaria cases increased and within 2 years the number was four times
as high. The resurgence of malaria cast doubts upon the feasibility of
malaria eradication. Technical problems, government policy and financial
constraints all imposed limits on the plan for eradication (Soemarlan and
Gandahusada, 1990). In the period of violence that followed the
attempted coup detat in 1965, the NMES discontinued all its activities
(Takken et al., 1990) and, in 1968, it was integrated into the Directorate
General of Communicable Disease Control in Jakarta. This situation
weakened the eradication program and, by 1969, the national program
switched back to malaria control.
2.3.4. Malaria Control Phase (19691999)

The Indonesian MCP followed the guidelines of the global malaria control
strategy set forth by the WHO. The strategy included early diagnosis and
prompt treatment, selective and sustainable preventive measures, early
epidemic detection, containment or prevention of epidemics and the
strengthening of local capacities for basic and applied research. For the
purposes of applying distinct malaria control strategies, Indonesia was
stratified into two broad areas: (1) Java and Bali and (2) the outside
islands, representing all those islands which were not Java or Bali. The
strategy for case detection in Java and Bali differed from the strategy
in the outside islands. In Java and Bali, malaria case detection was carried
out by active and PCD, mass fever surveys, contact surveys and
migration surveillance. In contrast, in the outside islands, only PCD and
malariometric surveys were undertaken.
Malaria control activities in Java and Bali differed from those of the
outside islands. In Java and Bali, all provinces were prioritized for malaria
control, while in the outer islands, emphasis was placed on provinces in
which transmigration projects and economic development projects were
taking place, as well as on areas bordering neighbouring countries. Che-
moprophylaxis was only recommended for use among visitors or, tempo-
rarily, among migrants to the outside islands. Presumptive treatment,
radical treatment, mass drug administration and treatment for transmi-
grants differed between the two areas. For example, during this era of
control, primaquine for use as a hypnozoitocide against relapse in P. vivax
malaria, or as a gametocytocide against transmission was only recom-
mended for Java and Bali and not for the outer islands. In both areas, an
outbreak investigation was called for, owing to suspicions that an outbreak
was in progress. IRS with DDT continued as the main strategy for vector
control. Other interventions such as bed nets, larviciding, biological con-
trol and source reduction were applied only in limited areas.
Java and Bali continued DDT spraying but on a much smaller scale. By
the mid- to late 1980s, less than 2.3% of houses were covered. From 1986 to
1988, less than 6% of the houses on those islands other than Java and Bali
were covered by IRS. The government stopped using DDT in 1989 and, in
1994, it was banned altogether, largely as a consequence of the US refusing
shrimp imports from Indonesia as a result of DDT contamination. From
1979, several alternative insecticides were used for either fogging against
adult mosquitoes or for IRS activities. These insecticides included feni-
trothion, deltamethrin, bendiocarb, lambda-cyhalothrin and malathion.
Another vector control tool used in Indonesia was larviciding. Larvicid-
ing was first conducted in Bali in 1974 using kerosene (Smalt, 1937). It was
estimated that, as a result of these operations, 0.7 million people were
protected and 70 ha of larval habitat across Bali were treated. During this
period, larviciding was conducted in areas where A. sundaicus was found;
fenitrothion was used at a dosage of 1 cc/50 m2. Recommended larvicides
during this period were Paris green, kerosene, diflubenzuron and temephos.
In terms of source reduction by environmental management, several
recommendations were made during this period. In 1981, Kirnowardoyo
recommended a number of ways in which affected communities could
control A. aconitus (Kirnowardoyo, 1981). He suggested that farmers
should maintain a flow of water in irrigation ditches, rotate planting
cycles in order to prevent large areas from being flooded at the same
time, flood paddies every 10 days, alternate between using paddies for
rice in the wet season and for other crops in the dry season, release
larvivorous fish in flooded rice fields and place domesticated animals
near human dwellings in order to discourage mosquitoes from entering
dwellings (zooprophylaxis). He made similar recommendations
for the protection of communities against exposure to A. sundaicus.
His suggestions were that the community should always clean fishponds
and remove floating vegetation; the community should cover ponds with
soil; the cutting away of mangrove forests should be discouraged; if a
mangrove forest had been removed, fishponds should be created; the
public should release larvivorous fish into ponds; and zooprophylaxis
should be deployed (as described above).
Mangrove forests play an important role in Indonesias malaria control.
The Indonesia Ministry of Environment estimated that mangrove forests
in Indonesia covered an area of 9.2 million ha in 2000 (Kementerian
Lingkungan Hidup, 2007). Only 2.6 million ha of mangrove forest are
currently in good condition. These areas are of economic value. Badly
managed fishponds in coastal areas provide ideal breeding sites for
A. sundaicus. This is not merely conjecture; in the past, the loss of mangrove
forests has brought on malaria epidemics at Teluk Betung Port (1915;
Sudomo, 1994), Batavia (1919; Van Breemen, 1919), Pariaman (1921;
Sudomo, 1994), Belawan Port (1922; Schuffner and Hylkema, 1922), Nias
(1929; Soesilo, 1929), Tanjung Priok (1939; Sudomo, 1994), Cilacap (1984;
Sudomo, 1994) and South Lampung (1992; Sudomo, 1994). Sudomo found
that the recultivation of mangrove forests in Flores (East Lesser Sundas)
reduced the malaria prevalence from 16% to 4% over a period of 5 years, as
well as reducing the density of the vector population (Sudomo, 1987).
The migration of people into heavily endemic areas presents particular
challenges for malaria control. Important lessons were learnt and passed
on by Baird et al., following several years of work in transmigration
villages in northeastern Papua (Baird et al., 1995d). They suggested 10
measures to reduce the risk of epidemic malaria among transmigrants in
Papua who originated from non-endemic areas, namely (1) screening all
candidate transmigrants for G6PD deficiency and providing supervised
primaquine prophylaxis for 3 months; (2) increasing financial and admin-
istrative support for public-health officers, in order to allow them access
to the resources needed to prevent epidemic malaria, specifically among
newcomers; (3) establishing on-site microscopic diagnosis; (4) before the
arrival of the newcomers, screening and treating construction teams and
indigenous people who will live with them, providing them with G6PD
testing and primaquine prophylaxis if needed; (5) providing effective
treatment for slide-proven malaria with careful microscopic follow-up
and alternative treatment in resistant cases; (6) providing ITN, curtains
and shams; (7) conducting on-site education programs to inform people
about mosquito vector bionomics (allowing them to identify breeding
sites and feeding behaviour) and to alert them to the importance of
early diagnosis and treatment; (8) appointing a local voluntary cadre
trained to carry out a number of tasks including encouraging neighbours
to seek treatment if they recognize symptoms, spotting and eliminating
mosquito breeding sites, understanding mosquito feeding activities and
personal protective measures, collecting blood films, and reimpregnating

netting and curtains as appropriate; (9) providing reliable motorized
transport to evacuate severely sick or injured patients to hospital; and
(10) offering an incentive to motivate community participation in malaria
control efforts.
Malaria control in Indonesia during the period 19691999 faced many
constraints. In the highly endemic area of Papua, Gunawan described that
the constraints included the lack of coordination between control activ-
ities and development projects (especially transmigration and resettle-
ments projects), the difficulties of attracting and retaining experienced
and qualified personnel, the lack of supervision, the spontaneous move-
ments of transmigrants from elsewhere in Indonesia and the increase in
drug resistance brought on by negative treatment seeking and treatment
adherence behaviour (Gunawan and Marwoto, 1991).
In summary, control activities during the period 19691999 were
centred mainly on Java and Bali, where 60% of Indonesians lived and
most economic activity occurred. The burden of malaria on these islands
had been substantially reduced since 1945. Malaria control strategies were
therefore managed differently for Java and Bali than for all other islands.
Eastern Indonesia, in this period, as it still does today, faced many chal-
lenges to do with malaria and its control; challenges linked to the sparse
population, underdeveloped social and economic systems, fewer educa-
tional opportunities and the difficulties that vast distances and poor
transportation impose. The aim of malaria control in the next period
was to close the gap between western and eastern Indonesia.
2.3.5. Indonesian Roll Back Malaria campaign

(RBM; 2000present)
During this period, two global events affected malaria control policy in
Indonesia. The first was the RBM initiative launched by the WHO in 1998.
This initiative aimed to spark efforts that would lead to halving the
number of malaria deaths by 2010. In Indonesia, on 8 April 2000, the
MoH, following the WHOs global RBM campaign, launched an Indone-
sian version called Gebrak Malaria or, in English, Crush Malaria. This
program consists largely of seven steps recommended for control in
malaria endemic districts. These steps are (1) producing a map of
endemicity and identifying foci of malaria, (2) identifying the feasibility
of collaboration between communities and related government sectors,
(3) developing strategic plans for malaria control, (4) obtaining support
from the District Health Office and Legislative Council, (5) developing an
integrated working plan for malaria control, (6) implementing the work-
ing plan and (7) monitoring and evaluating the strategy and the progress
made. The Crush Malaria program is supported by the following
activities: (1) active and passive case finding coupled with periodic mass
surveys, including a mass fever survey, a mass blood survey (MBS) and a
malariometric survey (all of which require community participation at the
designated village malaria post), (2) case management with effective
drugs, (3) vector control and (4) surveillance. However, the new era of
widespread drug resistance, the broad decline of vector control activities,
the severe economic and political upheavals and the fledgling democratic
government now seeking to decentralize its authority have all been a
serious challenge to malaria control.
The second event which took place was that Indonesias MoH
launched a malaria elimination call on the 28 April 2009 (Departemen
Kesehatan, 2009b). Malaria elimination activities are to be conducted in
four stages. These stages include: (Stage 1) The thousand Islands (Jakarta)
and Bali and Batam Islands in 2010; (Stage 2) Java, Aceh and Riau Islands
in 2015; (Stage 3) Sumatra, West Nusa Tenggara, Kalimantan and Sula-
wesi in 2020 and (Stage 4) Papua, West Papua, East Nusa Tenggara and
Maluku Islands in 2030. To achieve the goal of elimination, the MoH has
set targets. The first target is that in 2010 all health service facilities must
have the capacity for malaria examination. In other words, all people
diagnosed with clinical malaria must be confirmed as malaria cases by
microscopy or reliable RDT. The second target is for Indonesia to enter the
pre-elimination stage in the year 2020. The third target is for the whole of
Indonesia to be free of malaria transmission in 2030.
Following this call for elimination, Indonesia must now start to
improve the surveillance system, the malaria outbreak management sys-
tem and the tools for communication, information and education. The
improvement of the capacity for early detection and outbreak manage-
ment is essential. A robust malaria information system must be estab-
lished to store, analyse and present information as needed. Indonesia has
to establish reliable migration and surveillance systems. The improve-
ment of malaria mapping skills is very important as risk maps can be used
to inform operations, to identify ongoing transmission foci or hot spots
and to focus elimination efforts (Feachem and Sabot, 2008; Feachem and
The Malaria Elimination Group, 2009; Feachem et al., 2009).
2.4. OBSTACLES AND OPPORTUNITIES IN MALARIA

CONTROL IN INDONESIA
2.4.1. Malaria case detection

Malaria case detection is a special challenge for an archipelago nation like
Indonesia. According to Indonesias National Malaria Control guidelines
(Departemen Kesehatan, 2007a), case detection activities cover active case
detection (ACD) and PCD, mass fever surveys, MBSs, malariometric

surveys, migration surveillance and contact surveys. ACD is conducted
by village malaria workers, health personnel or village malaria cadres.
Such teams take blood slides from symptomatic patients visited at home.
They give presumptive treatment and send the slide for microscopic
examination at a primary health centre. If proven positive, they return
to the home and deliver radical treatment. The frequency of such visits
depends on endemicity class. In regions with a high (API > five cases per
1000 per annum) or medium case incidence (API one case per 1000 per
annum), biweekly and monthly home visits, respectively, are prescribed
by the MoH. In contrast, PCD consists entirely of patients seeking treat-
ment (at hospitals, primary health centres or sub-primary health centres).
In some cases, teams may enter communities and aim to collect a blood
film from every resident with a fever or complaint of fever: this is called a
mass fever survey (MFS). The MoH prescribes MFS in areas where a
monthly parasite incidence exceeding three per 1000 people (or an annual
rate of 36/1000) has doubled from one month to the next, or in low risk
areas following a case in an infant (indicating high likelihood of local
transmission). An MBS aims to collect blood films from all residents
regardless of symptoms. This provides the most accurate estimate of
true prevalence of active malaria in a community. The MoH prescribes
MBS in areas of high endemicity or in areas where a malaria outbreak may
be in progress. The MoH classifies an MBS aimed at children below 10
years of age as a malariometric survey. The MoH also prescribes migra-
tion surveillance for residents of non- or low-endemic areas returning
from highly malarious areas of Indonesia. Finally, the MoH prescribes
contact surveys in which blood films are taken from at least five house-
holds neighbouring a confirmed malaria case. Below, we examine the
available literature on these case detection practices in Indonesia.
2.4.1.1. Active case detection

Utarini et al. studied the role and performance of ACD by village malaria
workers and PCD by health facilities in Jepara (Central Java) during the
years 19941998 (Utarini et al., 2007). They found that ACD detected more
cases than PCD (ratio 1.4:1), covered a broader geographical area (4.7 vs.
4.1 km; p < 0.05) and detected more malaria cases among children (33%
vs. 22%; p < 0.001). However, they also documented a major problem
with ACD: a significant delay between the taking of blood films and
diagnosis compared to PCD (2.3 vs. 1.1 days; p < 0.001). Village malaria
workers typically only transport slides to the health centre twice a week.
Moreover, microscopic examination services are usually not available at
health centres 7 days a week. Patients with positive slide results were
almost always given treatment the next day (mean 1.2 days). In view of
these findings, and the diminishing number of village workers available
owing to budget difficulties, Utarini et al. recommended that ACD be

continued only in highly endemic settings. In other words, PCD worked
reasonably well in areas of low to moderate risk, but an investment in
village malaria workers would be likely to pay health dividends in areas
of high endemicity. Ompusunggu et al. noted that a failure to provide
compensation to village malaria workers diminished case detection
coverage (Ompusunggu et al., 2005). During their study in Purworejo
(Central Java), village malaria workers were given Rp. 150,000/month
(US$ 16/month) from the government as well as additional incentives for
each malaria survey. This incentive scheme significantly increased the
amount of slide taken from 37% (47/128) in the previous year to 84%
(212/254) in the study period (p < 0.001). In other words, the ratio of
malaria slides collected by ACD and PCD increased from 1:2 to 5:1.
However, the proportion of slides collected by ACD dropped signifi-
cantly to 54% (37/68) in the second year (p < 0.001). The reason for this
reduction was that neither were malaria surveys conducted during this
period nor was any additional fee provided.
In an attempt to cope with a chronic shortage of village malaria work-
ers, community participation schemes have been explored in Indonesia.
Ompusunggu et al. evaluated a scheme called Ten Houses Grouping
(Dasa Wisma) in Purworejo (Central Java; Ompusunggu et al., 2005).
Each group of 10 houses elected a leader to report suspected malaria
cases to the community malaria cadre (who each represented four groups
of 10 households). The community malaria cadres were elected by group
leaders. The malaria cadre was usually a local housewife who received
video training from investigators aimed at increasing their knowledge of
malaria. Topics of training included the clinical diagnosis of malaria,
malaria blood slide creation, slide transfer, presumptive treatment and
reporting flow. Cadres in the Purworejo study usually dispatched blood
films within 24 h of collection. They got paid Rp. 1000 (US$ 0.1) per
malaria positive slide submitted by malaria patients. The government
paid the transportation cost. After 1 year, it was found that the Dasa
Wisma scheme resulted in the collection of significantly more slides
(24%; 538/2225) than the village malaria worker scheme (19%; 212/
1124; p < 0.001). They also found that more cases were detected using
Dasa Wisma (33%; 177/538) than the number of cases detected by village
workers (9%; 19/212; p < 0.001). Assessment after 2 years showed that
Dasa Wisma continued to perform better (13%; 297/2225) than the village
malaria worker scheme (3%; 37/1124; p < 0.001). However, the number
of cases detected by each scheme did not differ to a great extent (23%; 67/
297 vs. 16%; 6/37, respectively, p 0.379). Moreover, a significant reduc-
tion in slide collection in both schemes after 2 years (p < 0.001) was
observed. The number of slides collected by village malaria workers
was substantially lower than the number collected as part of Dasa
Wisma once the incentives were stopped. Ompusunggu et al. suggested

that health personnel should provide continuous support to malaria
cadres.
Some studies emphasize the importance of community participation
in bringing about successful malaria case detection. A scheme involving
such community participation was evaluated by Pribadi et al. in the
hyperendemic province of Riau in Sumatra (Pribadi et al., 1986). A pro-
gram of weekly chemoprophylaxis was instigated, with chloroquine
being administered to about 700 residents by nine cadres. Assessment
after 1 year showed that almost every household member (94%) had taken
the drug regularly. A small percentage (6%) refused the drug or agreed on
an irregular basis. The parasite rate dropped from 54% to 13% and spleen
index reduced from 22% to 5%. Also at Riau (Sumatra), Santoso et al.
evaluated a malaria task force scheme established to help with malaria
case detection and control (Santoso et al., 1991). The malaria task force
consisted of volunteer school teachers and community leaders. They
received training in the use of malaria medications and were, at least
ostensibly, supervised by the physician at the nearest primary health
centre. Each member of the task force monitored 20 households.
Some studies point to the importance of promoting such schemes for
case detection. Sekartuti studied the work of and the attitude towards 22
village malaria workers (Petugas Penemu Penderita Malaria) selected
from their local community in South Lampung in 2003 (Sekartuti, 2003).
Before training, their understanding of malaria was evaluated and found
to be poor. For example, most of them did not realize that malaria para-
sites occur in human blood. Practically none of them (1/22) had door or
window screens at home and most (15/22) did not use mosquito netting.
Among those patients who had heard of village malaria workers, most
(86/103) consented to the worker taking a blood film. Those who refused
often cited a lack of confidence in the skill and knowledge of the worker as
the reason. Nonetheless, 96% (202/210) of respondents supported the
idea of using these village workers and most (193/210) hoped the pro-
gram would continue. In East Kalimantan, the acceptance of cadres also
seemed to hinge upon the perception of their skill by the community
(Sukowati et al., 2000).
2.4.1.2. Passive case detection

Primary health centres outside Java and Bali rely almost entirely upon
PCD as the primary means of case finding (Departemen Kesehatan,
2007a). Therefore, improving PCD represents an important goal in
supporting malaria control in those relatively high endemic settings.
Sekartuti et al. reported the efforts aimed at improving PCD, that is,
improving treatment seeking behaviour among residents, in Banjarnegara
(Central Java). They used slide shows for school children and patients
(Sekartuti et al., 2004b). Shinta et al., in turn, noted the important role
played by community leaders in Purworejo (Central Java; Shinta and
Sukowati, 2005). Improving the effectiveness of PCD provides additional
benefits such as improving microscopy, competency, and community
awareness (Sekartuti, 2000).
Hunt et al. evaluated the use of 24 school health units (Usaha Kesehatan
Sekolah, UKS) for malaria case detection in three districts (Banjarnegara,
Purworejo and Jepara) in Central Java in 1991 (Hunt et al., 1991). All UKS
teachers received training from the Ministry of Education and Culture in
collaboration with the local primary health centre at the district level. The
training materials included malaria knowledge, detection, treatment and
prevention. UKS teachers had the responsibility to make malaria slides
and give presumptive treatment among students with malaria symptoms,
to send slides to primary health centre, and if positive, the health centre
staff would give radical treatment. Hunt et al. noted the advantages and
constraints involving UKS in PCD. The advantages were (1) an intensive
detection of high-risk fever cases among the school students and (2) the
teachers as malaria health educators. In contrast, the constraints were the
availability of logistic, limited time to send slides to primary health centre,
slide taking supervision and teacher turnover. However, Hunt et al.
observed that less than 10% of UKS were taking malaria slide smears.
Schools had no more supply of blood slides and the lancets. They referred
students with malaria symptoms to primary health centre or inform
malaria cadre to take malaria smear at schools. In order to intensify the
role of schools, training, supplies and supervision are encouraged.
Accurate clinical diagnoses are necessary to determine the local spe-
cific malaria symptoms. Health officers may then design a health message
for the community that stresses how clinical malaria typically occurs in
that community. Resource limitations, as in most human endeavours,
may restrict the practicality of applied research activities like these
(Sekartuti et al., 2004c). Health officers must convince funding agencies
of the practical importance of such work in the face of their continuing
reliance upon the clinical diagnosis of malaria as a consequence of the
shortages in both competent malaria microscopists and supplies of RDTs.
2.4.1.3. Migration surveillance

The mobility of people among Indonesias thousands of islands seriously
challenges malaria control. This may become particularly important as
Indonesia strives to eliminate endemic malaria from Java and Bali by
2015. Transmigration in Indonesia, that is, the movement of people within
Indonesias borders, typically sees people move from densely populated
Java and Bali to the sparsely populated and usually highly endemic outer
Islands. These migrants routinely return to Java and Bali, either perma-
nently or, more often, for family reunions and holidays. In addition, the
armed forces of Indonesia (Tentara Negara Indonesia, or TNI) and the

national police force (Polisi Republic of Indonesia, or POLRI) must sup-
plement local forces with those from Java and Bali when conducting
routine security operations in the islands outside of Java and Bali. These
civilian and military migrations, reaching tens of thousands each year,
represent a significant threat of renewed or scaled up malaria transmis-
sion on Java and Bali.
Transmigration as a government-operated enterprise in Indonesia was
launched under Dutch administration in 1905 (Hardjono, 1982). The
Republic of Indonesia continued the practice after gaining independence
in 1945. However, the practice was abruptly halted after the fall of the
Suharto regime in 1998 (Hardjono, 1982). Officially, transmigration poli-
cies and practices pursued economic development in remote areas, and
strove to offer economic opportunities to a landless peasant class. A more
cynical view, however, classified the program as a forced migration that
expanded and cemented Javas social and political sphere of influence
across a highly diverse and sometime divisive republic. In either case,
transmigration helped shape the malaria problem in Indonesia in impor-
tant ways. Moreover, these migrations continue in earnest up to the current
day, only now without formal government ownership of the movement.
People elect to migrate to the outside islands, either to set up their own
enterprises or to go directly to a large development project. Regardless of
the reasons for the movement, the impact of transmigration on malaria and
vice versa is an important consideration in the context of control.
Simanjuntak, in 1999, stated that all transmigrant locations in 21 pro-
vinces had malaria and that the average number of clinical malaria cases
per year ranged from 33 to 69 per 1000 of the population (Simanjuntak,
1999). In 1998, the highest numbers were reported from Papua (274/1000),
East Nusa Tenggara (120/1000) and West Nusa Tenggara (95/1000).
Simanjuntak claimed that two outbreaks of malaria typically occurred
each year in such locations, with usual CFR of 6%. He documented the
delay in insecticide spraying in the homes of newly arrived migrants, the
lack of antimalarial drugs and the delayed arrival of medical personnel.
Simanjuntak also implicated apparently poor site selection criteria for the
establishment of such settlements, and the apparent ease with which
mosquitoes gained access to people, owing to poor construction. Abisud-
jak et al. criticized the responsible government institutions, citing essen-
tially similar problems (Abisudjak and Kotanegara, 1989). These authors
described land usually occupied by transmigrants as having been pri-
mary forests (52%), secondary forests (13%), bushes (21%), swampy for-
ests (5%) and plantations (7%).
Baird et al. evaluated records of emergency evacuation (19972000) to
hospital with a diagnosis of severe malaria from a transmigration village
in northeastern Papua (Arso XIV; Baird et al., 2003a). Residents of Arso
XIV came predominantly from Java (83% of residents), where the risk of
malaria has been less than 1 infection/10,000 person-years for most areas
since the mid-1960s. Exposure to biting anophelines occurred in and
around homes between dusk and dawn. Attack rates for malaria in the
Arso region have typically ranged between 0.5 and 4 infections/person-
year. They found that the overall incidence of evacuation was 7.5/100
person-years. In all, 142 adults and 53 children were evacuated over the
30-month period. The 30-month risk of evacuation in adults relative to
children was 2.8 (95% CI 2.03.9; p < 0.001). RR for adults was greatest
during the first 6 months (RR > 16; 95% CI 2.0129; p < 0.001), and
diminished during the second 6 months (RR 9.4; 95% CI 2.732.8;
p < 0.001) and the third 6 months (RR 3.7; 95% CI 1.77.9; p < 0.001).
During the next two 6-month intervals, the RR for adults was 1.6 and 1.5
(95% CI range: 0.82.6; p < 0.18). The authors considered that age-related
differences in the immune systems of children and adults are the most
likely explanation for the apparent susceptibility of adults to onset of
severe disease caused by primary exposure to P. falciparum.
At a former primary forest site which had become a palm oil planta-
tion at Arso (Papua), Baird et al. documented what amounted to epi-
demics of malaria within 3 months of arrival of new migrants (Baird
et al., 1995d). Malaria blood survey of those sites showed 3070% preva-
lence of parasitemia with virtually universal symptomatic malaria. Even
several years after settlement, the incidence of malaria at Arso ranged
from two to five infections per person per year ( Jones et al., 1994), but
symptomatic malaria had sharply waned, especially among adults. Ento-
mological surveys at Arso showed that, on average, 15 anophelines would
feed on each person every night, and that 1% of these mosquitoes carried
sporozoites (Baird et al., 1995d). The average migrant at Arso in the late
1980s was exposed to sporozoites once a week, which developed into full-
blown malaria five times a year, assuming a 10% efficiency of infection
with sporozoite inoculation (Pull and Grab, 1974). This estimate agreed
with the measurements of force of infection ( Jones et al., 1994).
Baird et al. observed that nurses in transmigration villages at that time
relied almost entirely upon a clinical diagnosis of malaria (Baird et al.,
1995d). Therefore, asymptomatic carriers went undetected and fuelled the
conditions for an epidemic. Baird et al. concluded that new transmigrants
brought to highly malarious areas merited additional resources not usu-
ally prescribed for all new settlements. Such targeting, they reasoned,
would improve the likelihood of social and economic success of settle-
ment. In terms of case detection, the authors suggested that on-site micro-
scopic diagnostic capabilities (RDTs did not exist at that time) should be
established to permit monthly MBS among residents, as should the
aggressive elimination of asymptomatic gametocytemia for a period of
at least 6 months following the arrival of newcomers.
Krisin et al. documented the patterns of disease experienced by groups

of Javanese transmigrants at Armopa (Papua) from the time of first
settlement in September 1996 until 1999 (Krisin et al., 2002). During the
34 months of their continuous observation, the health clinic they had
established received over 22,000 visits (an average of 700 visits per
month) from both indigenous Papuan people and the Javanese transmi-
grants. They found 3631 new cases of malaria in the Javanese transmi-
grants. In other words, 20% of visits included a microscopically
confirmed diagnosis of malaria. In the same area, Barcus et al. documen-
ted an incidence of malaria ranging from 1.1 to 1.5 infections/person-year
(Barcus et al., 2003). The mean time to first parasitemia was 185 days
(range: 11856 days) for P. falciparum and 190 days (range: 14901 days)
for P. vivax. Unlike other new transmigration villages in that region,
however, the presence of the research team and the clinic and services it
offered resulted in the almost complete lack of attacks of severe and life-
threatening malaria (Krisin et al., 2003).
Migrations within Indonesia certainly bring cases of malaria from high
to low endemic areas. Several studies have reported high rates of those
malaria cases classified as imported. Baird et al. reported that 372% of
malaria cases were imported into West Java, Central Java and East Java
between 1985 and 1987 (Baird et al., 1993). Dakung et al. evaluated 3506
fever patients in Jakarta who were seen between 1964 and 1980, and found
that 357 (10%) had malaria (Dakung and Pribadi, 1980). The ratio of
P. vivax to P. falciparum to mixed infection was 2:1:0.1. Most cases (82%)
were known to be imported into Jakarta from Sumatra, West Java, East
Timor and Papua. More recently, Lederman et al. evaluated 240 civilian
and military patients diagnosed with malaria in Jakarta hospitals
(Lederman et al., 2006b). The majority of civilians contracted malaria
during recent travel to Papua and South Sumatra (Bangka Island and
Lampung), whereas military patients contracted malaria in Aceh (north
Sumatra). Less than 1 week of travel is much more common in civilian
travellers (5/26) than in military travellers (1/58), who almost always stay
for longer periods of duty. The number of people coming from sites in the
outer islands to Java or Bali, whatever the reason or duration, reaches
millions annually and the risk of malaria associated with these human
migrations (or travel) must be considered an obstacle to control.
The economic importance of tourist destinations in endemic settings
merits special attention as far as control is concerned. Ompusunggu et al.
evaluated the magnitude of malaria endemicity at 11 tourism beaches in
three districts in West Java (Ompusunggu et al., 2002). They found a slide
positivity rate (SPR) of 0.4% (11/3106). They considered this to be evi-
dence of local transmission and believed it was necessary to call for
stepped-up control measures. Kurniawan interviewed 22 tourists who
were diagnosed with malaria after returning from work or vacation visits
to Ujung Kulon (West Java), Purworejo (Central Java) or Papua

(Kurniawan, 2003). Although the majority of respondents (61%) knew of
the risk of malaria, none had used malaria prophylaxis. Approximately
25% used mosquito repellent as a precaution against malaria. Those
patients suggested that communications media such as brochures and
posters displayed in tourist areas would help elevate awareness of the
risk. Such measures, however, rarely prove practical or acceptable in the
tourism industry. Travellers in Indonesia, or the health professionals
advising them, should be aware of the high-risk areas and prescribe
appropriate awareness, personal protection measures or chemoprophyl-
axis to those venturing to such sites.
2.4.2. Malaria diagnostics

A reliable diagnosis of malaria lies at the core of successful control. This
is true whether the patient is resident in an endemic setting, or has
returned to a non-endemic area as a tourist, businessman or soldier. The
National MCP of Indonesia lists three diagnostic tools for routine use:
clinical diagnosis, microscopic diagnosis and RDTs (Departemen
Kesehatan, 2007a).
2.4.2.1. Clinical diagnostic

The clinical diagnosis of malaria depends almost entirely upon the
instincts of the provider. Tjitra et al. studied 560 symptomatic adults
and children attending the primary health centre in West Sumba (Lesser
Sundas) in 1998 (Tjitra et al., 1999). A diagnosis of clinical malaria was
based on fever or history of fever in the last 48 h and no other evident
cause of fever. It was revealed that 294 (53%) of the patients had para-
sitemia (with or without sexual forms) when diagnosed by microscopy.
The typical symptoms of malaria (fever, chills, headache, nausea, vomit-
ing, muscle aches, malaise, etc.) are notoriously non-specific, and may
easily be confused with a number of endemic viral or bacterial infections
in Indonesia. Even if the provider happens to be extraordinarily good at
identifying malaria, the clinical diagnosis comes with a very important
pitfall: guidelines call for treating clinically diagnosed patients with chlo-
roquine or sulfadoxine/pyrimethamine rather than artemisinin com-
bined therapy (ACT). The MoH apparently wishes to conserve ACTs for
patients confirmed to actually have malaria. The problem for the patient
who actually does have malaria is a high probability of failed therapy.
The problem linked to clinical diagnosis has been acknowledged and
in their plans for malaria elimination, Indonesian health authorities call
for all primary health centres to confirm malaria using microscopy
(Departemen Kesehatan, 2009b). The Indonesian NIHRD (Sekartuti
et al., 2004c), funded by the Global Fund, investigated the malaria
baseline data at six highly malarious districts in Eastern Indonesia,

namely Biak Numfor (Papua), Sorong (Papua), Ambon (Maluku), Ternate
(Maluku Utara), Kupang (East Lesser Sundas) and West Sumba (East
Lesser Sundas) in 2004. They revealed that primary health centres rarely
recorded the many clinical diagnoses of malaria that were made. Diag-
noses supported by microscopy or RDT were infrequently available. The
studies showed that only 16% (43,054/267,747) of malaria patients were
examined by microscopy between 2001 and 2003 (Sekartuti et al., 2004c).
In other words, 84% of malaria patients were diagnosed clinically.
Another estimate shows similar results. In 2006, the WHO estimated
that there were 9.3 million fever cases in Indonesia (World Health
Organization, 2008e). The World Malaria Report of 2008 reported that
1,246,324 microscopic or RDT diagnoses had been made in Indonesia
throughout 2006 (World Health Organization, 2008e). In other words,
only 13% of fever cases were diagnosed with a microscopic or RDT
confirmation, and 87% of malaria patients were diagnosed clinically and
presumably treated with CQ or SP. Until the availability of diagnostic
services is substantially expanded, the standard treatment for malaria in
Indonesia will continue to be CQ or SP.
2.4.2.2. Microscopic diagnostic

Many workers consider the microscopic examination of Giemsa-stained
thick and thin blood films (Wongsrichanalai et al., 2007) to be the most
suitable diagnostic instrument for malaria control. Not only can it differ-
entiate between species (as many RDTs can do), but it can also provide
detailed information about stages present and their counts per unit vol-
ume of blood (which no RDT can do). However, malaria microscopy
requires highly specialized equipment and persistently applied technical
training and certification of competency. Poor malaria microscopy is
probably more harmful to the patient and malaria control than are good
clinical diagnoses. In Indonesia, no peer-reviewed publication has yet
revealed the number of health centres that have the diagnostic capacity
for malaria microscopy, or the required level of proficiency among the
microscopists performing the tests. A research report from the NHIRD
showed that 65% of the health centres in six districts in eastern Indonesia
had microscopes (Sekartuti et al., 2004c).
Other studies have evaluated the performance of malaria diagnostic
services at primary health centres and at district level hospitals and
clinics. In Donggala (Central Sulawesi), Chadijah et al. evaluated the
performance of microscopic diagnosis in 2005 (Chadijah et al., 2006).
They used 566 malaria test slides. They found that the mean sensitivity
in primary health centres was lower than it was in district level hospitals
(42% vs. 86%). In other words, false negatives were more frequent in
primary health centres than they were in district level hospitals (58% vs.
14%). Moreover, the mean specificity in primary health centres was lower
than it was in district level hospitals (84% vs. 96%). Conversely, false
positives were more frequent in primary health centres than in district
level hospitals (16% vs. 4%). Tjokrosonto et al. evaluated the accuracy of
malaria diagnoses in Banjarnegara (Central Java) in 1990 (Tjokrosonto,
1994). They reported the lack of agreement between diagnoses made at
primary health centre level, district level and national level. Using 335 test
slides, the proportion of false positives was 37% at primary health centres
and 29% at district level hospitals. The proportion of false negatives was
14% and 9% at primary health centres and at district level hospitals,
respectively. For P. falciparum identification, the mean false positive and
false negative rates at primary level and district level were about 37% and
20%, respectively. For P. vivax identification, the mean false positive and
false negative rates at those levels were about 54% and 9%, respectively.
The high rates of error both at the health centres and district health offices
should be investigated and remedied.
Multiple factors contribute to the poor performance of microscopy
diagnosis in Indonesia. Foremost among the many likely factors will be
the low compliance to minimal laboratory standards, poor quality of slide
preparation, inadequate or obsolete microscopes, lack of supply stocks,
heavy workload and inadequate quality assurance. At Lampung (south-
ern Sumatra), Sekartuti put the low quality of microscopic diagnosis at
primary health centres down to the multiple use of slides, the low volume
of blood taken for examination and the inability to count parasite density
(Sekartuti, 2003). Ompusunggu et al. reported similar problems in West
Sumba (Lesser Sundas; Ompusunggu et al., 2006). They also observed the
repeated use of glass slides (due to the scarcity of this resource) and the
poor quality of slide preparation. Kismed conducted a qualitative study
in 10 healthcare centres in Sambas (West Kalimantan) involving 41 labo-
ratory workers, paramedics and heads of clinics (Kismed, 2001). They
concluded that a lack of human resources resulted in the poor preparation
of blood slides by the health officers. Reporting also suffered. The absence
of a system for cross-checking, together with minimal or even no feedback
from supervisors, also contributed to the poor performance of micro-
scopic examination as a diagnostic tool (World Health Organization,
2009b).
2.4.2.3. Rapid diagnostic test

The past decade has seen the emergence of immunochromatographic
technology which allows for a simple, one-step device for the diagnosis
of malaria. Several dozen commercial brands are now available, collec-
tively referred to as RDTs (Wongsrichanalai et al., 2007; World Health
Organization, 2006d), and all employing antigen capture by monoclonal
antibodies. Like the extremely simple take-home pregnancy test kits, the
malaria RDT produces a coloured line within 520 min. Some, but not all,
RDT products offer great promise in extending reliable diagnosis to areas
where traditional microscopy may be difficult to establish or maintain
(World Health Organization, 2003e). The WHO has recently published a
systematic evaluation of the performance of 41 commercially available
RDTs from 21 manufacturers (World Health Organization, 2008c). Of the
41 products, 16 detect P. falciparum alone, 22 detect and differentiate
P. falciparum from non-P. falciparum malaria, and three detect both non-
falciparum and P. falciparum malaria without distinguishing between
them. RDTs were evaluated against (1) a panel of parasite-positive, para-
site-negative cryo-preserved blood samples and a panel of parasite-nega-
tive samples, (2) thermal stability and (3) ease-of-use descriptions. This
evaluation provided a standardized laboratory-based evaluation of RDT
performance. The study showed that several RDTs are available which
consistently detect malaria at low parasite densities (200 parasites/ml),
have low false positive rates, are stable at tropical temperatures, are
relatively easy to use and can detect P. falciparum or P. vivax infections,
or both. Performance between products varied widely at low parasite
densities (200 parasites/ml), however, most products showed a high
level of detection at 2000 or 5000 parasites/ml.
In Indonesia, in 1995, several studies were carried out evaluating the
performance of RDTs. Fryauff et al. tested the sensitivity of the ParaSight
F test (F test) in detecting P. falciparum infections among malaria-immune
(410 native Papuan) and non-immune (369 new transmigrants) popula-
tions in Arso PIR V, Armopa SP-1, Oksibil and Tarontha, all hyperendemic
areas in Papua (Fryauff et al., 1997d). They found highly significant differ-
ences between populations in terms of the sensitivity of the test (Papuan,
60% vs. transmigrants, 84%; p < 0.001), and in terms of its specificity
(Papuan, 97% vs. transmigrants, 84%; p < 0.001). For the Papuan, levels
of sensitivity of the test were higher in the 10 year age group than in the
> 10 year age group (70% vs. 40%). For transmigrants, the test had high
levels of sensitivity in both age groups (8185%). The test had high levels of
specificity for both age groups in the Papuan population (9698%). For the
transmigrants, the specificity levels of the test were higher in the 10 year
age group than in the > 10 year age group (94% vs. 79%). Fryauff et al.
suggested that the significant difference in the sensitivity and specificity of
the F test was related to the age-dependent immune status of the popula-
tions being tested. Sensitivity was lower in the older generations of the
Papuan population who had had life-long exposure to P. falciparum
malaria and had therefore developed clinical immunity.
Fryauff et al. evaluated the performance of OptiMAL in Armopa
(Papua) in 1997 (Fryauff et al., 2000). Measures of sensitivity were derived
by applying the OptiMAL test for the detection and differentiation of
light, asymptomatic P. falciparum and P. vivax infections. They found
that concordance between OptiMAL and microscopy was 81% and 78%
by two independent readings. The sensitivity of the tests to any malaria
species was 60% and 70% in two separate readings and its specificity was
97% and 89% in two readings. Most cases identified by microscopy as
P. falciparum were graded as negative or non-falciparum by both OptiMAL
readings. OptiMAL false negatives and misidentifications were seen to be
related to low parasitemias (< 500/ml). The OptiMAL assay demonstrated
8892% sensitivity to infections of 5001000 parasites/ml. Fryauff et al.
concluded that this device should not be approved for diagnostic use but
could be made commercially available for research purposes only. It was
markedly less sensitive than expert microscopy in terms of discriminating
between different malaria species.
Tjitra et al. evaluated the new, combined P. falciparum and P. vivax
immunochromatographic test (ICT Malaria P.f/P.v.) in Sumba (Lesser
Sundas) in 1998 (Tjitra et al., 1999). With 560 symptomatic adults and
children, they found that the ICT Malaria P.f./P.v. was sensitive (96%)
and specific (89%) in the diagnosis of P. falciparum malaria. The specificity
for the diagnosis of P. vivax malaria was 95%. However, the sensitivity
levels (75%) were relatively low. The sensitivity to P. vivax malaria was
96% with parasitemias of > 500/microlitre but only 29% with parasite-
mias of < 500/microlitre. Nevertheless, compared with the test using
HRP2 alone, use of the combined antigen detection test would reduce
the rate of undertreatment from 15% to 4% for microscopy-positive
patients. This would be at the expense of only a modest increase in the
rate of overtreatment of microscopy-negative patients from 7% to 15%.
Tjitra et al. concluded, however, that the cost remained a major obstacle to
the widespread use of ICT Malaria P.f./P.v. in areas of endemicity.
Arum et al. compared the performance of the ICT method with that of
microscopic diagnoses in East Lombok (Lesser Sundas) in 2005 (Arum
et al., 2006). From 604 samples, they showed that the ICT revealed 100%
sensitivity, 97% specificity, 83.2% positive predictive value and 100%
negative predictive value. Therefore, Arum et al. concluded that the
malaria ICT was reliable enough to be used as a malaria test.
Ginting et al. conducted the performance of the Parascreen Pan/Pf test
with that of microscopic diagnoses in Mandailing Natal (North Sumatra)
in 2006 (Ginting et al., 2008). The Parascreen test was considered positive
P. falciparum malaria when the specific histidine-rich protein-2 (HRP-2)
line was visible. Testing 104 symptomatic adults and children, they found
that the Parascreen was moderately sensitive (76%) and highly specific
(100%) in diagnosing P. falciparum malaria. The sensitivity increased in
higher parasitemia. The sensitivity test was 81% for parasitemia of 100
200/ml, 87% for 200400 parasites/ml and 100% for more than 400 para-
sites/ml). However, the test had a very low sensitivity for parasitemia less
than 100/ml (0%).
Several studies have evaluated RDTs in the context of malaria control

strategies. Utami et al. investigated the application of RDT by village
malaria cadres in Purworejo (Central Java) in 20052006 (Utami, 2004;
Utami et al., 2008). The cadres involved, each one responsible for 40
households, had been trained to identify clinical malaria signs and symp-
toms and make blood films. The cadres were then also trained to use
RDTs. Case finding was reported to the primary health centre where
parasitological confirmation of a positive test outcome would be per-
formed. Over 12 months, the cadres identified 119 RDT-positive cases of
malaria. High specificity levels were found for P. falciparum (98%) and
P. vivax (100%). However, they found that the sensitivity of immunochro-
matographic tests (60% for P. falciparum and 57% for P. vivax) was low
when compared to microscopic diagnosis.
2.4.2.4. Improving malaria diagnostic accuracy

Improving diagnostic accuracy is a technical, financial and human invest-
ment. Chadijah et al. suggested several technical solutions, such as
repeated microscopy diagnostic training, standardized examinations,
the introduction of a microscopist certification, regular supervision and
cross-checking and the updating of equipment (Chadijah et al., 2006).
Sekartuti suggested further ways of improving the quality of microscopic
examinations: the glass slides must be clean, with proper staining, and
sufficient time must be allocated for slide reading (Sekartuti, 2003). Cor-
rect microscopy requires persistence, experience and dedication by the
microscopists and the systems supporting them (Chadijah et al., 2006).
The establishment of a quality assurance system requires standardized
operating procedures, along with materials and training modules for
improving or demonstrating the competence of microscopists. Maguire
et al. developed a standardized method for producing large numbers of
consistently high-quality malaria slides (Maguire et al., 2006b). They built
up a repository of stained blood films to use as support for training and
competency assessments. Whole blood was collected by venipuncture
from Plasmodium-positive donors in Indonesia and Cambodia, and,
importantly, individuals with no history of risk of exposure to malaria
(newly arrived expatriates in those countries). Technicians systematically
prepared hundreds of Giemsa-stained thick and thin smears from each
donor. After obtaining a provisional microscopic diagnosis, one slide
from each of the first 35 donors was distributed to 28 individuals
acknowledged by reputation as experts in the microscopic diagnosis
of malaria. These reference readers recorded the presence or absence of
Plasmodium species, the life-cycle stages and the parasite density.
The results given by the reference readers were compiled, in order to
(1) identify unqualified microscopists with consistently incompatible
results relative to other readers and (2) derive a composite diagnosis
based on the combined analyses of all the reference readers and on the
PCR analysis. The composite diagnosis was then accepted as the true
diagnosis. Three tiers of diagnostic proficiency were established and
the level of proficiency of each microscopist was established by assigning
demerit points based on the types of errors made. A false positive was
considered a more serious error (10 demerits) than a false negative (five
demerits). The accuracy of diagnosis by species was taken into account
(mixed infections, three demerits). The accuracy of the parasite count was
also considered, individual accuracy being ascertained by accepting the
median count among qualified readers as the best estimate of the true
count (one demerit given when parasite density was outside the 99%
confidence interval). When all results had been analysed, Maguire et al.
excluded four readers with demerit points greater than one standard
deviation above the mean. A composite diagnosis and parasite density
were then derived based on the remaining 24 readers. In comparison to the
composite diagnoses, reference readers correctly identified the presence of
parasites 85% of the time when parasite densities were < 100 parasites/ml.
The percentage of correct primary diagnoses improved at higher densities:
99% for densities between 100 and 350/ml and 100% for densities > 350/ml.
Reference readers correctly identified 96% of true negative slides. They
correctly identified P. falciparum, P. vivax and P. malariae mono-infections
99%, 86% and 50% of the time, respectively.
2.4.3. Malaria treatment

2.4.3.1. Access to treatment centres
Most Indonesians have difficulty accessing adequate health services and
this problem comes to bear directly upon the treatment of malaria. The
Basic Health Survey (BHS) in 2007 involved 258,366 households sampled
from over 90% of all districts/cities in the archipelago (National Institute
of Health Research and Development, 2008). This survey evaluated access
to health service facilities and community-based health efforts (Upaya
Kesehatan Berbasis Masyarakat, UKBM). Health service facilities con-
sisted of hospitals, primary health centres, practiced physicians and
nurses. UKBMs consisted of integrated service facilities (Pos Pelayanan
Terpadu), village health services (Pos Kesehatan Desa), village medicine
shops (Pos Obat Desa) and village midwifery services (Pos Bersalin Desa).
Accessibility to health facilities was measured by the BHS in terms of
distance from the facility (National Institute of Health Research and
Development, 2008). Table 2.11 shows the accessibility to health facilities
by region throughout the Indonesian archipelago. Forty-eight percent of
those households sampled were located within 1 km of health services
(western: 49% vs. eastern: 46%). Another 46% were located between 1 and
5 km from the services (western: 47% vs. eastern: 46%). Accessibility varied
TABLE 2.11 Accessibility to treatment centres by region throughout the Indonesian

archipelago
Western Eastern
Characteristics Indonesia Indonesia Total
Number of households interviewed 167,141 91,225 258,366

Number of people interviewed 624,086 362,446 986,532
Accessibility
Health service facilities
Households located within 1 km of 49% 46% 48%
health services facilities
Households located within 15 min of 71% 56% 66%
health service facilities
Community-based health efforts (UKBM)
Households located within 1 km of 80% 76% 79%
UKBM
Households located within 15 min of 88% 81% 85%
UKBM
widely among provinces, for example, the percentage of households within

1 km from a health facility ranged from 27% to 73% (National Institute of
Health Research and Development, 2008). About two-thirds of households
were within 15 min of a health facility (western: 71% vs. eastern: 56%) and
most of the remainder were between 15 and 30 min (western: 22% vs.
eastern: 27%). Only 9% of households reported needing over 30 min to
reach the closest health facility (western: 7% vs. eastern: 13%).
UKBM, as would be expected of community-based health efforts,
showed patterns of easier access when compared to health facilities.
Table 2.11 shows the accessibility to community-based health efforts by
region throughout the Indonesian archipelago. Seventy-nine percent of
those households sampled were located within a kilometre of UKBM
(western: 80% vs. eastern: 76%). Eighty-five percent of households were
within 15 min of a UKBM (western: 88% vs. eastern: 81%). Seventy-nine
percent of households were within a kilometre of a UKBM, compared to
just 48% which were within a kilometre of a health centre. This is an
important distinction with respect to the access to antimalarials and
information about malaria. Focusing malaria education and treatment
resources through UKBMs may thus be appropriate.
The village drug post, a source of common anti-infectives including
those used to treat malaria, is manned by a volunteer with limited train-
ing. About 90% of respondents in the BHS reported not using this service,
overwhelmingly (95%) as a consequence of there being no such post in
their village (National Institute of Health Research and Development,

2008). The effectiveness of the village drug post in providing easier access
to antimalarials cannot be adequately assessed until more such posts are
established.
2.4.3.2. Treatment seeking behaviours

People exhibit distinct behaviour in seeking treatment for malaria or a
malaria-like illness. Such behaviour is certainly influenced by the accessi-
bility to care, but many other factors such as risk, experience, economics
and culture also come into play. Actions taken by the community were
classified as follows: no action, self-treatment (using both modern and
traditional medicines) and consultation (going to a traditional healer,
malaria worker, midwife, paramedic, doctor, health centre or hospital;
Utarini et al., 2003).
Sanjana et al. assessed malaria knowledge, attitudes and practices in
communities experiencing epidemic malaria in Purworejo (Central Java)
in 2001 (Sanjana et al., 2006). They surveyed 1000 randomly selected
households in 50 villages. The sample was restricted to the nine sub-
districts in Purworejo which presented the greatest transmission risk
according to the malaria surveillance statistics of the reporting year
2000. All were in the Menoreh Hills or the foothills of the Dieng Plateau.
Four local residents received training on how to collect answers using the
survey consisting of 93 questions. Training focussed on interview conduct
and highlighted the necessity of strict adherence to the sampling protocol
and of obtaining informed consent. They requested an interview with the
head of the household, but any resident over the age of 15 could serve as
an interview subject. A specific protocol provided the interviewers with a
guide to the random sampling of households within villages. Trained
interviewers began by visiting the household of the head of the village.
They then walked 100 m from that house in opposite directions along
set compass headings. The house closest to that point was then sampled.
They repeated this sampling protocol, moving along their respective
assigned compass headings until completing 10 households each per
village. Of the 409 households reporting malaria illness in the year prior
to the survey, 211 (52%) respondents had treated the last malaria illness in
the family with medicine without going to a health facility. These patients
obtained medication primarily from local drug vendors (64%) and com-
munity health workers (25%). Three hundred and fifty-eight (88%) of the
409 households also sought advice or treatment outside the home (multi-
ple responses possible). The main sources consulted were health centres
(28%) and private healthcare providers (22%). The median time required
to reach the place of consultation was 15 min (range: 0240 min). The
modes of transport employed to reach the source of treatment were as
follows: on foot (51%), by motorcycle (23%), by local village transport van
(16%) and by bicycle (7%). The median cost of treatment reported by those
who self-treated and by those who sought treatment outside the home
was Rp. 6000 (US$ 0.6) and Rp. 7250 (US$ 0.7), respectively.
Karyana et al. also conducted a cluster randomized survey of malaria
treatment seeking practices in Timika in 2007 (Karyana et al., 2007). They
reported that 26% (302/1177) of the people surveyed did not seek treat-
ment when they had febrile illness as they did not feel unwell enough
(62%, 198/302). Of those people with febrile illness who did seek treat-
ment, 10% treated themselves at home. Forty percent went to a public or
malaria control clinic, 27% went to a pharmacy or drug store and 23%
went to a private clinic. As far as seeking treatment outside the home is
concerned, there was a significant difference between Papuans and non-
Papuans (57% vs. 78%; p < 0.05). In other words, indigenous Papuans
were less likely than immigrants to use health facilities as their source of
malaria treatment.
The Indonesian Health Household Survey (HHS) was implemented in
2004, by the Indonesian NIHRD and the Indonesian Centre of Statistics
(Soemantri et al., 2005). The survey selected 9082 households and 41,764
respondents were interviewed across all provinces (Pradono et al., 2005a).
Of these, 3947 respondents were under 5 years of age. Mothers were
questioned about treatment seeking behaviour when their children had
malaria. The study revealed that 4% of respondents had experienced
malaria fever in the last year. Among them, 21% took no action, 31%
self-treated and 48% obtained medication from health facilities. The
main reasons for not seeking treatment at health facilities were that
respondents did not consider malaria to be a threatening illness (67%),
did not have sufficient funds for care (37%), did not have sufficient funds
for transportation (23%) or had no transportation available at all (16%;
Pradono et al., 2005b).
In contrast, Kasnodihardjo et al. found a high rate of consultation of
health professionals among respondents with malaria in Sumatra
(Kasnodihardjo and Manalu, 2008). They surveyed 495 people from two
districts in South Tapanuli (North Sumatra) in 2008. They found that 16%
of respondents self-treated whilst 84% sought out malaria medication
from health personnel. Tana employed longitudinal surveys of 429 sub-
jects in Kulonprogo (Yogyakarta, Java) both in 2001 and in 2003
(Tana, 2003). Three percent of the subjects self-treated and 97% sought a
consultation. Similar findings were also reported among 156 respondents
surveyed by Yoda et al. in Lombok and Sumbawa (both in the Lesser
Sundas archipelago) in 2004 (Yoda et al., 2007). About 1% of respondents
either self-treated or took no action. A clear majority (81%) sought out
malaria treatment at health facilities.
A delay in receiving medication is well known to create the risk of a poor
treatment outcome with malaria. Indonesians often tend to put off visiting
health facilities until pressed to do so by worsening symptoms. Hunt et al.

reported that among 525 respondents seeking treatment in health primary
centres in three districts in Central Jawa in 1991, the mean number of days
between onset and seeking treatment was 34 days (Hunt et al., 1991). Most
of them (77%) did not go to school or work when they had malaria-like
symptoms. As a result, on average, they missed 5 days of work or school.
Mardiana et al. reported that, in Jepara (Central Java), in 2000, 24% of 100
people interviewed waited 1 or 2 days after they had fever before visiting a
health facility (Mardiana and Santoso, 2004). However, most of them visited
health facilities after the third day of fever (66%). Shinta et al. found a similar
pattern in Purworejo (Central Java) in 2003 (Shinta et al., 2005). About 25% of
the 100 respondents would visit a health facility within the first 3 days of
being ill. Three percent of respondents waited for 10 days before seeking
malaria medication at a health facility.
Health education improves peoples understanding of malaria treat-
ments and, in turn, improves adherence to prescribed therapy. Saikhu
and Gilarsi reported that of 6484 respondents in four districts in Central
Java in 2001, 75% could not describe treatments for malaria (Saikhu and
Gilarsi, 2003). However, of those respondents who had already had
malaria, only 2% did not know what malaria treatments were available.
A study was conducted in six districts in Eastern Indonesia between 2001
and 2003 revealing that only 14% of 1577 health personnel in pregnancy
clinics had received training on malaria treatment and prevention
(Sekartuti et al., 2004c). This proportion was even lower in hospitals
(0.4%, 6/1245) and primary health centres (6%, 13/233).
2.4.4. Vector control

Vector control involves strategies that reduce larval vector density, human-
vector contact or the duration of vector survival (Najera and Zaim, 2003).
The reduction of larval vector density may be achieved through either
larviciding, the use of larvivorous fish or source reduction by environmental
management. Reducing human-vector contact may be achieved by using
mosquito bed nets, screening windows and doors of homes or by employing
measures of personal protection (e.g. behavioural avoidance, appropriate
clothing, repellents and fumigant insecticides) or zooprophylaxis. The sur-
vival of adult vectors may be reduced by indoor spraying with residual
insecticides (IRS) and by the community wide use of ITN.
2.4.4.1. Control of larvae

2.4.4.1.1. Larviciding The earliest efforts to systematically control malaria
in Indonesia involved larviciding (Najera and Zaim, 2003). The effective-
ness of larviciding depends upon the permanence of breeding sites and
on their location in terms of the access provided to humans. A variety of
larvicides have been used for malaria control, including oils, chemical
insecticides, insect growth regulators and microbial insecticides.
Indonesias MCP recommends insect growth regulators (methoprene,
pyriproxyfen) and microbial insecticides (the bacterium Bacillus thurin-
gensis israelensis or BTI) as the preferred larvacidal measures. Methoprene
(World Health Organization, 2006h) and pyriproxyfen (World Health
Organization, 2005a) prevent larvae from maturing. The effectiveness of
these agents is measured in terms of the emergence of adult mosquitoes
from treated water within laboratory cages. Another larvicide, BTI (World
Health Organization, 2006f), produces toxins that effectively kill mosquito
larvae. The microbe poses no threat to humans, animals or other aquatic
organisms. The effectiveness of BTI is determined in a field setting by
counting the density of larvae in treated bodies of water.
Larviciding presents operational challenges that limit its utility to
specific settings. For example, unless breeding sites have been identified
and mapped to permit sufficient coverage, little impact upon malaria
transmission would be achieved. Also, effective dosing may vary widely
according to specific habitats. Success may hinge upon the tedious and
exacting task of determining that dose.
Many studies have evaluated BTI efficacy in Indonesia, specifically
against A. aconitus (Blondine, 2000, 2004; Blondine and Boewono, 2004;
Blondine et al., 2000a,b), A. barbirostris (Blondine et al., 1994; Widyastuti
et al., 1995, 1997.), A. maculatus (Blondine and Widiarti, 2008; Munif and
Pranoto, 1994) and A. sundaicus (Blondine et al., 2004, 2005; Hakim et al.,
2005; Kirnowardoyo et al., 1989; Schaeffer and Kirnowardoyo, 1983). How-
ever, BTI application is a challenge to apply for large-scale malaria control.
Geographical reconnaissance of the breeding places of local vectors needs
to be carried out first, along with the more detailed definition of vector
bionomics and human habitat mapping (Najera and Zaim, 2003). Once this
has been done, the task would be to determine the sufficient dosage of
larvacidal component (Kirnowardoyo et al., 1989). The susceptibility of
each vector species should be monitored after the application of BTI.
Blondine et al. reported the efficacy of the liquid formulation of BTI
cultured in coconut water against A. aconitus larvae in Semarang (Central
Java) in 2000 (Blondine, 2000). They administered dosages of 0.15 ml/
100 ml water and 0.2 ml/100 ml water. Their experiment used 15 treat-
ment pools and five control pools. Treatment pools were filled with the
locally cultured BTI from coconuts and the control pool was not treated.
The evaluation of this formulation was done by collecting larvae for
3 days before application, then conducting daily observations until day
6 after application. The study showed, at the formulation of 0.15 ml/
100 ml water, the reduction of larvae relative to control was 9499% on
the first 3 days. The reduction of larvae density decreased from 76% on
day 4 to 25% on day 6. At the formulation of 0.2 ml/100 ml water, the
reduction of larvae relative to control was 81% on day 1. The reduction of

larvae decreased from 73% on day 2 to 34% on day 6. Blondine et al.
concluded that the liquid formulation of a locally cultured strain of BTI
from coconuts, administered at a dosage of 0.15 ml/100 ml water or
0.2 ml/100 ml water was effective against A. aconitus larvae until 3 days.
In 1994, Blondine et al. executed a trial of BTI against A. barbirostris in
East Flores (Lesser Sundas archipelago; Blondine et al., 1994). A dosage of
0.06 ml of BTI per m2 in three types of pond (clear, grassy and mossy) was
evaluated. Intervention and control ponds were assigned to each pond
type. Spraying was done on a weekly basis for 4 weeks. It was revealed
that, within 24 h, the mean reduction in larval densities during four
applications in intervention ponds relative to control ponds was 98% in
clear ponds, 90% in grassy ponds and 54% in mossy ponds. They con-
cluded that BTI may be effective in clear and grassy ponds but less so in
mossy ponds. Widyastuti et al. also evaluated BTI at field-scale in East
Flores (Lesser Sundas) in 1992 (Widyastuti et al., 1995). The study used
three intervention ponds and one control pond. The tested dosages were
0.06, 0.075, 0.1 and 0.12 ml/m2. They found that mean larval densities
within 24 h in intervention ponds fell from 55 to 7 larvae per 20 dips at
dosages ranging from 0.06 to 0.12 ml/m2. No village-scale study of BTI
against A. barbirostris has been reported from Indonesia.
Munif and Pranoto conducted a trial of BTI against A. maculatus at
Kulonprogo (Jogyakarta, Java) in 1994 (Munif and Pranoto, 1994). They
evaluated three distinct means of application: sprayers, plastic bags and
direct pouring into streams. The sprayer application used a dosage of
1.5 l/ha. Spraying was done evenly on river pool surfaces. The plastic bag
application was done by placing a 1.5 l/ha dosage of larvicide in 40 plastic
bags at 40 mosquito breeding sites. The plastic bags were filled with
pebbles to hold them in place underwater. The direct pouring application
was done by dissolving larvicide at a dosage of 1.5 ml/ha in 20 l of water.
The water was then allowed to flow into the river at an upstream location.
Each method was repeated four times over 21 days, with a weekly
interval between each run. Larvae were collected at 1 h prior to treatment,
24 h post treatment and then again after weeks 1, 2 and 3. They found that
the spraying application reduced larval density from 95 to 3 larvae on day
1, a figure which increased to eight larvae (week 1), dropped again to one
larvae (week 2) and finally increased to 21 larvae (week 3). In other words,
the mean reduction of larval density relative to pre-treatment was above
96% up until week 2, but only 34% in week 3. The plastic bag application
reduced larval density from 95 larvae to none on day 1, but this increased
to 7 larvae (week 1), 23 larvae (week 2) and finally 61 larvae (week 3). The
plastic bag application therefore reduced larval density relative to pre-
treatment by about 90% up until week 2, but only by 36% in week 3. The
direct pouring technique prompted larval density to fall from 79 to 1 larva
(day 1), which dropped further to none (week 1) and then increased to
four (week 2) and seven (week 3). This technique took longer to take
effect, that is, the reduction of larvae was only 7% on day 1 and 58%
after week 1. However, a reduction rate of 98% was reached after weeks
2 and 3. It was therefore concluded that spraying and plastic bag applica-
tion reduced larvae at a faster rate than direct pouring. However, direct
pouring was effective until the third week.
Blondine et al. reported the efficacy of the liquid formulation of
BTI cultured in coconuts against A. maculatus larvae in Kulonprogo
(Yogyakarta) in 2008 (Blondine and Widiarti, 2008). BTI was cultured in
soybean infusion medium. In laboratorium scale, it was revealed that the
liquid local strain of BTI recovered from soybean medium and adminis-
tered at dosages of 0.59 ml/100 ml water killed 90% of larvae within 24 h
(lethal concentration 90% or LC90). They tested three liquid formulation
of locally strain BTI at dosages of 0.59 ml/100 ml water (LC90), 2.95 ml/
100 ml water (5 LC90) and 5.9 ml/100 ml water (10 LC90). Their
experiment used nine treatment pools for each formulation and nine
control pools. Treatment pools were filled with locally cultured BTI
from soybean and the control pool was not treated. The density of larvae
was observed a day before application, then on days 1, 2, 4 and weeks 1, 2,
3 after application. They showed that, at formulation of 0.59 ml/100 ml
water, the reduction of larvae density relative to control was 9599% on
first 2 days, then decreased from 78% on day 4 to 37% on week 3 after
application. At dosage of 2.95 ml/100 ml water, the reduction of larvae
density relative to control was 99100% on first 2 days, then decreased
from 87% on day 4 to 41% on week 3 after application. At a dosage of
5.9 ml/100 ml water, the reduction of larvae density relative to control
was 100% on first 2 days, then decreased from 87% on day 4 to 61% on
week 3 after application. Blondine et al. concluded that the liquid for-
mulations of the locally cultured strain of BTI from soybean infusion
medium, administered at a dosage of equal or higher than 0.59 ml/
100 ml water, were effective against A. maculatus larvae.
Various studies consistently show that BTI effectively reduces densi-
ties of A. sundaicus larvae in Indonesia. Kirnowardoyo et al. evaluated
the efficacy of three distinct BTI H-14 formulations (liquid, granule
and briquette) against A. sundaicus larvae in Banyuwangi (East Java)
and Jembrana (Bali) in 1984 (Kirnowardoyo et al., 1989). Active BTI
100 ml was diluted into 8 l of water, then sprayed on a 200 m2 water
surface. The liquid formulation was applied on a weekly basis for 12
months. The evaluation of this formulation was done by collecting larvae
every week, 6 h prior to treatment and then again 24 h after treatment.
They found that the larval density had fallen from 27.3 to 3.5 larvae/10
dips (reduction 87%) 24 h after the first application. The mean reduc-
tion of larval density for each application ranged from 76% to 100%.
The second (granule) formulation containing 500 g of BTI was dispersed

over a 10,000 m2 water surface. The evaluation of this formulation was
done by collecting larvae every 3 days for a month. The granule formu-
lation of BTI H-14 effected a reduction from 38 to 0.2 larva/10 dips
(reduction 99%) on the first day after treatment. After 3 days, however,
the larval density increased to 54 larva/10 dips. Between day 6 and day
25, larval density ranged from 29 to 59 larvae/10 dips. The final (bri-
quette) formulation was applied by using bamboo sticks to bind bri-
quettes to an improvised floating device. The distance between the
bamboo sticks was 3 m. It was shown that BTI H-14 briquettes could
reduce larval densities from 9.9 larvae to 2.1 larva/10 dips (reduction:
79%) within 24 h after the treatment. The effect of the briquettes
remained satisfactory ( 90% reduction in larval density) for at least 24
days. Kirnowardoyo et al. concluded that the liquid and briquette for-
mulations provided good larval control for A. sundaicus, whilst the
granule formulation was less successful.
Blondine et al. examined the efficacy of the liquid formulation of BTI
cultured in coconuts against A. sundaicus larvae in Cilacap (Central Java)
in 2003 (Blondine et al., 2004). BTI was cultured in coconuts because these
contain the amino acids and carbohydrates capable of supporting the
expansion of BTI numbers. Old coconuts (weight 400700 g) were used
as culture media. A hole with a 1.5-cm diameter was made in each
coconut. The BTI dosage used was 5 ml in 100 ml of water. BTI was
injected into 12 coconuts and the hole was then covered and coated with
candle wax. Coconuts were stored at room temperature for 47 days.
It was found that the liquid local strain of BTI recovered from coconuts
and administered at dosages of 0.1 ml/100 ml water and 0.0751 ml/
100 ml water killed 90% of larvae within 24 and 48 h. Their experiment
used 12 treatment pools and four control pools. Each pool had sentinel
traps containing 15 larvae. All larvae (dead and alive) were replaced with
15 new larvae on each observation day. Treatment pools were filled with
locally cultured BTI from coconuts and the control pool was treated with
uninfected coconut water. The mortality and density of larvae were
observed a day before application, then on days 1, 2 and 4, and weeks 1
and 2 after application. The reduction of larvae relative to control was
100% on day 1, 91% after week 1, and 84% after week 2. Blondine et al.
concluded that the liquid formulation of a locally cultured strain of BTI
from coconuts, administered at a dosage of 5 ml/100 ml water was
effective against A. sundaicus larvae.
Hakim et al. studied the residual effect of granule and liquid BTI
formulations in Ciamis (West Java) in 2005 (Hakim et al., 2005). Fifteen
A. sundaicus larvae were caught in shrimp ponds and put into the plastic
containers. The larval mortality was observed after 24 h. Probit analysis
showed LD90 at dosage of 0.869 kg/ha for granule and 1795 ml/ha for
liquid formulation. Then authors tested the LD90 and two other doses:
0.5 g/ha (granule) and 1000 ml/ha (liquid). For granule formulation,
they found 100% mortality at dosage of LD90 and the recommended
dosage on day 1 and after 2 weeks, 41% mortality rate at LD90 and 50%
at recommended dosage (p 0.229). For liquid formulation, they also
found 100% mortality at dosage of LD90 and 99% at the recommended
dosage on day 1. After 2 weeks, 45% of larvae were killed at dosage of
LD90 and 37% of larvae at recommended dosage (p 0.565). These
authors thus recommended that lower dosages than those recommended
could be applied for field purposes. They found that granule formulation
could kill more than 90% of larvae for up to a week, whilst liquid
formulation could last only 4 days. They concluded that granule formu-
lation was more effective than liquid formulation at recommended
dosages.
The effectiveness of other larvicidal measures has been examined in
Indonesia. Barodi et al. conducted a small-scale field study at Kulonprogo
(Yogyakarta) in 1993 (Barodji et al., 1995). The study focussed on nine
temporary shallow ponds located near three rivers. They assessed the
emergence of adult mosquitoes before and after the application of pyr-
iproxyfen. One to two months before application, they collected larvae
from puddles and reared them in the laboratory until adults emerged.
They found that the proportion of adult mosquitoes emerging without
larvicide was 83% (795/953). Pyriproxyfen was applied at dosages of 0.01
and 0.05 ppm against A. maculatus, A. flavirostris and A. balabacensis.
Larvae and water samples were collected for each puddle on days 1, 3,
5, 7, 35 and 49 post-application. Larvae obtained from each puddle were
reared using water samples from each. The first week collection showed a
significant reduction of adult mosquitoes emerging at a dosage of
0.01 ppm (intervention: 2.8%, 35/1257 vs. control: 86%, 472/552,
p < 0.001) and 0.05 ppm (intervention: 1.3%, 13/1033 vs. control: 86%,
472/552, p < 0.001). On day 35, a dosage of 0.01 ppm still achieved
significant reductions (intervention: 17%, 17/103 vs. control: 73%, 63/86,
p < 0.001), as did 0.05 ppm (intervention: 20%, 31/158 vs. control: 73%,
63/86, p < 0.001). However, by day 49, the reduction of emergent adult
mosquitoes was no longer significant at a dose of 0.01 ppm (intervention:
60%, 36/60 vs. control: 63%, 38/60, p 0.707). This was also true at the
higher dosage of 0.05 ppm (intervention: 58%, 35/60 vs. control: 63%, 38/
60, p 0.575). The investigators concluded that 0.01 ppm remained effec-
tive for 35 days and that increasing this dose fivefold presented no appar-
ent advantage.
Mardiana reported the efficacy of methoprene against A. farauti larvae
at laboratory-scale in 1996 (Mardiana, 1996). Briquette formulation was
used to retain four concentrations (i.e., 0.0029 g/50 l water, 0.0058 g/50
litre water, 0.0116 g/50 l water, and 0,0232 g/50 lwater). A total of 400
larvae (100 larvae per each concentration) and 100 larvae were exposed to
treatments and control, respectively. The study showed that the higher
concentration was associated with higher mosquito mortality. The mos-
quito mortality rate was 73% at concentration of 0.0029 g/50 l water, 92%
at 0.0058 g/50 l water, 97% at 0.0116 g/50 l water and 99% at 0.0232 g/50 l
water. The effective dose of methoprene was then estimated using probit
analysis for 50% lethal or 95% lethal. The analysis resulted 0.0014 g/50 l
water (50% lethal) and 0.0085 g/50 l water (95% lethal). The author
concluded that briquette methoprene was effective to control A. farauti
larvae at least in laboratory-scale.
Waris evaluated the efficacy of pyriproxyfen as larvicidal control of
Anopheles subpictus in South Kalimantan in 2003 (Waris, 2003). A total of
1,200 A. subpictus larvae were kept in groups of 150 in 25 20 3.5 cm
containers for each concentration plus a control group. A dosage of
2 grams pyriproxygen per 1 liter water was dissolved into seven concen-
trations: < 0.001 ppm, 0.0010.005 ppm, 0.01 ppm, 0.02 ppm, 0.04 ppm,
0.08 ppm, 0.16 ppm. After the larvae were treated with the various con-
centrations of pyriproxyfen, the number of dead larvae and number of
pupae were recorded for ten days. The surviving pupae were then
observed for a further ten days and the number of dead pupae and
adult mosquitoes were recorded. The study showed that in the treatment
groups, 88% (927/1,050) of the larvae were prevented from becoming
pupae in ten days. The larvae mortality rates varied among the concen-
trations from 66% and 100%. Of the 123 pupae to survive, 100% died
before maturing into adults. In comparison, the control group showed 168
out of 350 (48%) larvae failed to become pupae and of the remaining 182
pupae, 52% (95/182) died before maturing to the adult stage. In other
words, 48% of the surviving pupae emerged as adult An. subpictus mos-
quitoes. The authors concluded that pyriproxyfen was effective as a
larvicide against A. subpictus larvae in South Kalimantan.
The use of the entomopathogenic fungus Metarhizium anisopliae for
vector control has been evaluated in Indonesia. Munif et al. carried
out a study of this fungus when used in the control of A. aconitus in
Banjarnegara (Central Java) in 1994 (Munif et al., 1994). They evaluated
a 900 m paddy treated with a dosage of 300 mg conidiospora/m2. They
found a 90% reduction in larval density. More importantly, there was a
10-fold reduction in the measured biting rate of anophelines. This rela-
tively small experiment suggests that M. anisopliae is an effective control
agent. However, the further documentation of the entomopathogenic
fungus in community-based larvaciding studies is still lacking.
In terms of community support for the application of larvicides,
Blondine et al. interviewed 60 people in Cilacap (Central Java) in 2003
(Blondine et al., 2004). They assessed the communitys knowledge about,
attitude towards and practice of BTI larvicide application. Before the
community received malaria education, none of them had known that

BTI could kill mosquito larvae. Once they had received this education,
47% (14/30) understood that substances like BTI could be used to
kill mosquito larvae. Despite half the community not having a full
understanding of the use of this larvicide, 83% (25/30) agreed to apply
BTI to their fishponds in support of this control activity. They found that
fish farmers at Cilacap (Central Java), once they had been made aware
of the intent and nature of BTI application, were much more likely to
accept it.
Taken together, the studies of larvicides in Indonesia demonstrate
good results against the major anopheline vectors. The use of larvicides
with slow-release technologies appears to represent the most effective
approach. However, as with any larvicide, the strategy may only work
well when an effective coverage of breeding sites is achieved, and when
the area in which it is implemented is well mapped and characterized.
However, no studies in Indonesia have yet evaluated the impact of
larvicides on the actual risk of malaria transmission and disease burdens.
The presumption of effective control with diminished densities of larvae
may not be borne out by more careful study. Efficacy against malaria
transmission will almost certainly hinge upon the percentage of breeding
sites actually covered, much in the same way that ITN impact hinges
upon the percentage of people actually using the nets. Achieving high
levels of coverage with larvicides requires entomological and mapping
expertise that is generally not available at the district level where the
responsibility for such interventions lies. Moreover, even when such
expertise is available, larviciding may not be suitable because the breed-
ing sites of the vectors may be simply too widespread and temporary to
accomplish any significant coverage. For example, the Punctulatus group
of mosquitoes in New Guinea breeds in temporary pools such as those in
tire ruts and even footprintslarviciding such sites would be futile. The
utility of larvicides against some of the most important anophelines of
Indonesia has been proven in concept, but no demonstration of utility in
practice has been made and the settings in which this could be realized
are probably quite limited.
2.4.4.1.2. Larvivorous fish Another means of biological control of malaria

vectors is the introduction of larvivorous fish to breeding sites
(Fletcher et al., 1992; Howard et al., 2007; Kusumawathie et al., 2008; Roll
Back Malaria, 2005; Sabatinelli et al., 1991; World Health Organization,
2006c). This approach has been most effectively applied in man-made
mosquito breeding sites. It has a long history and constituted the core of
MCP strategies before the introduction of DDT (Roll Back Malaria, 2005;
Roll Back Malaria Partnership, 2008). In 1946, Gerberich reviewed the
available literature dealing with larvivorous fish and counted 216 species
of fish, used in the control of 35 species of mosquitoes, in 41 countries

(Gerberich, 1946). In 1984, Sharma identified 315 species of larvivorous
fish (Sharma, 1984). The most suitable species of fish all meet the follow-
ing criteria: carnivorous, surface feeder, rapid breeding in confined
spaces, quick swimmer, tolerant of thick vegetation and broad fluctua-
tions in temperature and acidity (WHO Study Group on Vector Control
for Malaria and other Mosquito-Borne Diseases, 1995; Wickramasinghe
and Costa, 1986). Many authors suggest the same steps in fielding fish
aimed at reducing the risk of malaria (Dua et al., 2007; Ghosh and Dash,
2007; Kusumawathie et al., 2006; Mohamed, 2003; Rasool and Suleman,
1999; Wickramasinghe and Costa, 1986). The first steps are mapping the
fish breeding sites and collecting species of fish with larvivorous potential
from those sites. The most suitable species should be identified by testing
and evaluating its feeding behaviour and then the optimum manner of
rearing the species must be found. Making the fish strategy popular
amongst the people who own or manage the sites is equally vital. The
evaluation of the impact of these fish upon larval densities should be
followed by an assessment of malaria risk in those communities covered.
The MCP in Indonesia provides guidelines for the introduction of
larvivorous fishes (Departemen Kesehatan, 2006a). The recommended
larvivorous fish in Indonesia are Poecilia reticulata (Indonesians call
these ikan guppy), Aplocheilus panchax (ikan kepala timah) and Gambusia
affinis (Departemen Kesehatan, 2006a). In Central Java, Nalim et al. inves-
tigated the potential of P. reticulata, first introduced into Indonesia in 1961,
as a method of control against the A. aconitus mosquito, which is found in
rice fields (Nalim and Boewono, 1987; Nalim et al., 1985, 1988). The study
involved 92 farmers cultivating 24 ha of rice fields. The farmers were
given training about health and agricultural practices twice a month
along with regular farmer union meetings. The first distribution of
60,000 1-month-old fish fry was a failure as a consequence of improper
handling by the farmers. Later, 478,000 fish were successfully distributed
with the assistance of local fishery personnel. The scheme initially aimed
for a density of 2 fish fry/m2. The daily consumption of larvae averaged
119 per fish. To determine the direct impact of these fish, an emergence
trap was designed to trap mosquitoes emerging from ricefields. The study
showed that P. reticulata reduced A. aconitus emergence from over 3 to
0.01 mosquitoes/m2/day. More importantly, the SPR for malaria among
residents dropped from 17% to 0.2% in the 5 years of implementation. The
study noted that proper training in fish handling is the key element in
larvivorous fish introduction.
In North Sumatra, Sudomo et al. evaluated the larva-eating activity of
Oreochromis niloticus, first introduced into Indonesia in 1969 (Nurisa,
1994), to control the fishpond mosquito A. Sundaicus (Sudomo et al.,
1998). Fishponds were found in many locations in the study area. Each
of three ponds (6 7 m) was allocated as treatment and control ponds.

The ponds were filled with water to a height of 3050 cm. After 4 weeks,
all ponds had grown water plants and A. sundaicus larvae were found in
all the ponds. O. niloticus fish were distributed at 3 fish/m2 or 126 fish/
pond. The size of these fish ranged from 6 to 8 cm in length and their
weight ranged from 10 to 12 g. The number of anopheline larvae found in
ponds with larvivorous fish after 11 weeks was 50% less than the number
found in ponds without larvivorous fish (5.5 vs. 10.1 larva/pond), but not
significantly different (p 0.128). It is somewhat doubtful whether such
modest reductions would translate into a reduced risk of malaria among
inhabitants. It may also be that the initial density of fish per pond was not
adequate.
Effectiveness may also hinge upon community awareness. Hunt
et al. reported that only 1% of 636 respondents interviewed in three sub-
districts in Central Java recognized the role of fish in paddy field for the
control of mosquito larvae (Hunt et al., 1991). Sekartuti et al. reported that
none of the 420 respondents living along a coastline in South Sumatra
knew of the existence of fish that eat mosquito larvae (Sekartuti, 2003).
Similar findings were reported from Eastern Indonesia (Sekartuti et al.,
2004c). The effective application of larvivorous fish requires studies
demonstrating coverage requirements, community acceptance and the
real impact such a strategy could have upon malaria risk in those
communities.
2.4.4.1.3. Source reduction by environmental management Environmental

management aims to create habitats not suitable for breeding by anophe-
line vector species. The history of this approach, also called species
sanitation, is detailed in Section 2.3.1. This approach is particularly impor-
tant in Indonesia due to the abundance of vectors that, if permitted, may
thrive in agricultural settings. Agricultural practices, like irrigation, crop
selection and rotation, impact on the risk of malaria transmission.
Nalim carried out a study using agricultural practice against malaria
vectors in Salatiga (Central Java) in 1980 (Nalim, 1980). She evaluated the
impact of draining two rice paddies; one selected as an intervention plot
and the other as a control plot (3 km2 each). The two sites were 6 km apart
but both had a similar ecological setting. Larval densities were measured
twice a week from the beginning of planting until the harvest 5 months
later. The measurements were taken at 30 randomly selected sites in each
of the two plots. Adult mosquito densities were also measured using six
emergence traps (42 cm in diameter) at each study plot. Flooded paddy
fields were drained for 3 days after 2 months of rice growth, and were
then flooded again for 10 days. A month after the paddy had been
flooded, all species (A. aconitus, A. annularis, A. vagus, A. indefinitus),
except A. barbirostris (larvae density: 0.04 larvae/dip; adult density:
0.61 mosquitoes/day/m2) were absent. The author concluded that 3 days

of paddy drainage could reduce the density of larvae and the emergence
of adult mosquitoes. The basic requirements for good results, as
expressed by the author, were sloped paddy for good drainage, irrigation
mechanics for ease of draining and filling and the cooperation of local
authorities and farmers.
Takagi et al. monitored larval densities of A. sundaicus in shaded and
unshaded fish farming ponds in North Sumatra in 1986 (Takagi et al.,
1995). Four fishponds were shaded for the experiment. The size of these
ponds was 2.5 m in width and 710.5 m in length. They removed all fish
from the ponds to exclude the effects of predation. Ponds were shaded
using the fresh leaves of the locally abundant Nipa palm. The density of
larvae in shaded ponds fell from 38 to 1.2 larvae/10 dips after 17 days of
shading (p < 0.001). In contrast, this difference in larva density was not
detected in the unshaded ponds (before: 11.5 vs. 11.7 larvae/10 dips;
p > 0.05). The authors argued that this shading for larval control would
be relatively easy and inexpensive. However, shading would not be
practical for the larger fishponds, as nipa palm fronds are typically
about 2 m in length. This measure also requires the monthly replacement
of the Nipa leaves.
In Bintan (Riau), in 1993, Pribadi et al. studied the communitys
knowledge about, and attitude towards malaria, as well as the malaria
prevention practices employed (Pribadi et al., 1997). Of 204 residents
interviewed, half understood that mosquitoes breed in ditches. The
other half had no concept of where mosquitoes may breed. Sampling
only 55 people, the question of eliminating breeding sites was posed.
Most identified the filling in and drying out of ditches as possible meth-
ods. Few respondents were aware that oiling water, applying insecticides
or planting mangrove trees were related to malaria control.
Historically at least, species sanitation in Indonesia has a very good
record of positive results against malaria. Moreover, a very limited num-
ber of more recent studies show data suggesting that such measures may
be superbly effective in limiting the risk of transmission. The effective
interventions carried out under Dutch colonial administration focused on
economically important zones and broader practicality was not assessed.
Contemporary studies assess this broader applicability but with a limited
scope of findings. No work in contemporary Indonesia has demonstrated
the impact of a village- or district-wide implementation of specific species
sanitation measures upon the risk of malaria.
2.4.4.2. Control of man-vector contact

2.4.4.2.1. Mosquito nets and insecticide-treated mosquito nets Sleeping
under bed nets treated with insecticides has been proven to have a
positive impact on all-cause mortality in communities with hyper- to
holoendemic malaria. As shall be seen, however, similar studies in the

hypo- to mesoendemic setting, which is typical of most endemic zones in
Indonesia, are lacking. It remains unclear what benefits, if any, are gained
by distributing ITNs. Nonetheless, Indonesia aggressively distributes
ITNs, aiming for 80% coverage in high-risk areas, in particular, amongst
young children and pregnant women. However, several problems have
arisen in regards to this prevention method in Indonesia.
In 2007, the Indonesian Demographic and Health Survey (IDHS) was
implemented by the Indonesian Centre of Statistics, supported by the
United Nations Population Fund (UNFPA), Macro International Inc., the
US Agency for International Development (USAID) and the Ford Foun-
dation and UNICEF (BPS and Macro International, 2008). Using a strati-
fied two-stage design, the survey selected 40,701 households and
interviewed 41,653 respondents in all provinces. The IDHS collected
information on the impact of malaria interventions at the community
level and included questions on the ownership of bed nets and the use
of bed nets by pregnant women and young children. The survey revealed
that the ownership of ITN in Indonesia is still low (2.8%). Fewer house-
holds in eastern Indonesia own ITNs than in western Indonesia (9% vs.
3%). Protection against malaria for children under 5 years by ITN was
low (3.3%). Fewer children under 5 years slept under ITNs in eastern
Indonesia than in western Indonesia (9.7% vs. 2.7%). The proportion of
pregnant women aged 1549 who protected themselves against malaria by
sleeping under an ITN was also low (2.3%). Fewer pregnant women slept
under ITNs in eastern Indonesia than in western Indonesia (6.1% vs. 1.9%).
Another study confirmed low rates of ITN usage in Indonesia. In 2004,
the Indonesian HHS was implemented by the Indonesian National Insti-
tute for Health Research and Development and the Indonesian Centre of
Statistics (Soemantri et al., 2005). A stratified two-stage design was used
to select 9012 households. A total of 38,276 respondents were interviewed
across all provinces (Pradono et al., 2005a). The HHS collected informa-
tion on health household status, health systems, medical check ups,
healthcare facility responsiveness, treatment costs, mortality and blood
examination and included questions on the use of ITNs. Similarly to the
IDHS, this survey found low ITN usage rates in Indonesia (2.5%). The low
rates of coverage may be related to the lack of data demonstrating the
efficacy of this intervention.
An exhaustive review of the available sociological studies involving
mosquito netting since 1990 revealed none describing malariometric or
broader all-cause morbidity and mortality effects linked to ITN interven-
tions. In 2001, Sanjana et al. conducted a cross-sectional KAP study in 50
villages in nine sub-districts of Purworejo, Central Java, in the midst of a
malaria epidemic (Sanjana et al., 2006). Of 1000 randomly surveyed
households, 36% owned at least one bed net. Of the households with
bed nets, 92% had made the purchase themselves, 51% reported that all
household members slept under the nets, 9% claimed no bed net usage,
and 40% reported that only some household members slept under the
nets. An average of three people per household had slept under a bed net
the previous night. Fifty-three percent of the households had paid less
than Rp. 20,000 (US$ 2) for their bednets, 33% had paid between
Rp. 20,000 (US$ 2) and Rp. 50,000 (US$ 5) and 0.6% had paid more than
Rp. 50,000 (> US$ 5). There was no correlation between the households
which owned bed nets and the households in which a member had
suffered from malaria in the past year (OR 1.0, p 0.89). This was
not the type of randomized, longitudinal study required to draw real
conclusions about the protective effects of ITNs. Nonetheless, these may
be the best available data on this question and they certainly point in the
direction of there being no discernable benefits, even in the epidemic
setting of this study.
Saikhu and Gilarsi used secondary data from the Benefit Evaluation
Study (BES) conducted by the Indonesian National Health Institute for
Research and Development and the Indonesian Centre of Statistics in 2001
(Saikhu and Gilarsi, 2003). The study was conducted in four districts in
Central Java: Banjarnegara, Pekalongan, Kebumen and Jepara. There
were 15,901 respondents of all ages from 4032 households. The authors
aimed to show the association between knowledge about malaria and the
number of malaria cases. Remarkably, only 6485 respondents had heard
of malaria and, perhaps more remarkable still, these were the respondents
who then went on to constitute the evaluated population. The analysis
showed that most respondents (68%) understood that malaria was trans-
mitted by biting mosquitoes. Only a quarter (26%) knew that bed nets
were a way to prevent malaria. The study found that there was no
significant correlation between the knowledge that bed nets can be used
as a prevention method and the number of malaria cases in a household
(p 0.884). Like the KAP study in Purworejo (Sanjana et al., 2006), this
survey does not serve as a demonstration of the efficacy of ITNs against
malaria. However, the results at least suggest that bed nets may have
some limited impact upon the risk of malaria in some areas of Indonesia.
In the instance of this particular survey, not knowing about bed nets as a
means of malaria prevention had no bearing upon the reported risk of
malaria (OR 0.97, 95% CI 0.71.4).
Yoda et al. evaluated the effect of a cooperative malaria control project
carried out between 2001 and 2004 by the Indonesian MoH and Nagasaki
University, Japan in Lombok and the Sumbawa Islands (Lesser Sundas;
Yoda et al., 2007). The three control activities conducted as part of this
project were malaria case detection and treatment, the systematic distri-
bution of ITNs and health education for health workers and villagers.
Eighteen months after termination of the project, its effectiveness was
evaluated by interviewing the heads of the 600 families who had been
involved. Before the project began, only 14% of households surveyed
were in possession of ITNs. During the project, 98% of the participating
households used bed nets every night. Once the project ended, 88% of the
participants continued to use the bed nets. Of those who received bed
nets, 91% did not treat them with insecticide owing to a lack of insecticide,
because they disliked insecticide, or because they felt no need to treat the
nets. People who did not use nets tended to sleep outside the house, lack
the necessary funds to purchase a net, or simply not understand that nets
protected against malaria (presuming they actually do). Unfortunately,
this study did not report the impact of the intervention upon malaria risk
or upon the burden of the disease in communities.
High levels of awareness somehow failed to translate into presumably
effective measures of self-protection, that is, obtaining and using mos-
quito netting. Sekartuti et al. conducted a health education intervention
study at high-risk sub-districts in epidemic Purworejo in 2000 (Sekartuti
et al., 2004b). Using a structured questionnaire, they surveyed the heads
of 219 randomly selected households. The percentage of respondents
sleeping under bed nets was 14%. Respondents not using nets cited
inconveniences such as comfort, cost and lack of mosquitoes. Suharjo
et al. conducted a KAP study in Banjarnegara involving 100 households
in 2002 (Suharjo et al., 2004). The study showed that the proportion of bed
net usage was 11%, even though 86% of households were easily accessible
to mosquitoes. A majority of respondents agreed with the statement that
malaria was a serious problem (64%), that it could have a serious impact
on their life (89%), and that it was a threat to health (63%). It remains
unclear just where the gap in understanding occurred that permitted
people who were perfectly aware of the risks of malaria not to take this
simple precaution against it. In Jepara, Mardiana et al. revealed that 19%
of the 100 families surveyed slept under bed nets in 2000 (Mardiana and
Santoso, 2004). The low income respondents prioritized spending money
on food as opposed to buying a net. Ompusunggu et al. observed the
behaviour of 46 patients with a P. falciparum infection in Mbilur Pangadu,
West Sumba (Lesser Sundas) in 2002 (Ompusunggu et al., 2006). The
study found that no patient had used a bed net or any other form of
protection against mosquito bites. Most of the respondents treated the
traditional houses shared between as many as four families as their
permanent residence. The wooden slat structures offered few barriers to
access by mosquitoes. This study did not compare the behaviour of these
malaria patients with that of people in the same region without malaria.
It is therefore difficult to draw conclusions on the absence of net use
among patients with malaria.
Arsunan et al. conducted a KAP study in Kapoposang Island,
Pangkajene (South Sulawesi) in 2003 (Arsunan et al., 2003). The study
involved 264 respondents selected using a random sampling procedure.

The authors found that more than half the respondents (58%)
slept under bed nets. About 81% of respondents agreed that the use of
bed nets was a good idea. Those who lacked nets cited cost as the primary
reason. There was a significant correlation between the lack of knowledge
of methods of protection against malaria and risk of being
infected (p < 0.001; OR 5.2, 95% CI 1.718.4). There was also a signifi-
cant correlation between lack of willingness to protect oneself against
malaria and risk of malaria (p < 0.001; OR 6.3, 95% CI 1.926.1).
A very significant association appeared between the extent to which
people practiced malaria protection and the risk of contracting the disease
(p < 0.001; OR 11, 95% CI 3.547). The authors also explored
the relationship between knowledge, attitude and practice. It was
found that a lack of knowledge about malaria could significantly increase
negative practice in respect to malaria prevention (OR 2.4; 95% CI
1.44.1; p < 0.001).
Roosihermiatie et al. implemented a casecontrol study to examine the
correlation between bed net usage and malaria risk in Bacan Island,
Maluku in 1998 (Roosihermiatie et al., 2000). Most subjects tended to
burn mosquito coils at night, starting at 8 p.m. Only 15% of the 112
respondents surveyed owned mosquito nets and none were ITNs. Just
10% of those who owned nets said that they slept under them. The
malaria risk for those above the age of 15 who never used mosquito nets
was insufficiently assessed to draw any conclusions.
Between 1993 and 1994, Suharjo et al. conducted a study examining
insecticide-impregnated bed net usage in malarial endemic areas in East
Mimika (Papua; Suhardjo et al., 2003). The study took place in three
villages with 1790 residents and involved the distribution of 766 ITNs
(one ITN for two to three people). In two of the three villages people were
given ITNs. The households were observed by investigators two nights
per week (1921) for 2 years. Three months and six months after distribu-
tion, all residents from the three villages received health education on
malaria. In the two villages supplied with ITNs, residents were taught
how to use and maintain the nets. The average use of ITNs increased from
41% at the time of the first health education lesson, to 63% at the time of
the second. Average ITN usage also increased from 21 days per month to
24 days per month. This study showed that health education by local
cadres slightly improved community practice in using ITNs. This study
did not evaluate the relationship between ITN use and the risk of malaria.
Another study in Eastern Indonesia (Sekartuti et al., 2004c) reported that a
very low rate of health personnel ever received training in the use of
impregnated nets (0.7%; 14/2104) and that none of the villages had the
minimal one cadre who was supposed to have received training on ITN
maintenance.
Sutanto et al. evaluated the efficacy of ITN intervention against

malaria in hypo-to holoendemic areas in Mimika (Papua) between 1993
and 1995 (Sutanto et al., 1999). Two comparable-endemicity villages were
chosen as a treatment site and a control site. The distance between the two
villages was about 2 kilometres. 158 households were located in the
treatment site and 201 households in the control site. Most of inhabitants
(90%) were indigenous population and worked as fishermen and hunters.
Before intervention, villagers usually slept on the floor or mattress with-
out bed nets. Adults normally sat outside of the houses in the early
evening until 10pm. Nylon-net was impregnated with permethrin at
dosage of 0.5 gr/m2, while control nest were impregnated with milk
solution. 277 ITNs were distributed to the treatment village (1.7 nets/
household) and 261 non-ITNs to the control village (1.3 nets/household).
Malaria surveys were conducted once before and 8 times during inter-
vention. The study showed that before intervention, the risk of malaria in
the treated village was higher than that of the control village (RR = 2.5,
95% CI 1.6-3.6). Since then, the risk of malaria in the treated village was
gradually declined. The intervention of ITN protected inhabitants in the
treated village against malaria compared to those in the control village
(RR = 0.24, 95% CI 0.1-0.4) over a year of intervention and (RR = 0.25, 95%
CI 0.2-0.4) after two years. They concluded that the ITN application was
effective to reduce the level of malaria endemicity from high endemicity
to low endemicty in the treated village in Papua.
Sutanto et al. evaluated the influence of permethrin ITNs on natural
immunity in a hyperendemic area in East Mimika (Papua) between 1993
and 1995 (Sutanto et al., 2003). One hundred and thirty-eight Papuan
inhabitants were recruited from an ITN-treated village for serological
investigation. Their sera were analysed for total IgG before intervention
and 2 years after intervention using synthetic peptides, that is, NANP5
and EENV4-BSA. Analysis was then carried out only on individuals who
were IgG positive before and after 2 years of intervention to investigate
the change of antibody. Twenty-five and 68 individuals were positive IgG
for NANP5 and EENV4-BSA, respectively. Their results showed a signifi-
cant decrease in the levels of geometric mean of antibody level IgG to
NANP5 (before 279 vs. after 132, p < 0.01) and to EENV4-BSA (before 745
vs. after 543, p 0.046). Additionally, the P. falciparum infection rates
tested with CS reduced from 18% (14/77) to 12% (9/77), but not signifi-
cant (p 0.258). However, the P. falciparum infection rates tested with
RESA reduced significantly (before: 17%, 18/108 vs. after: 1%, 1/108;
p < 0.001). In other words, the application of ITNs reduced the risk of
malaria infection, leading to a lower parasite burden and reducing the
host immune suppression. The result showed in hyperendemic malaria
peoples immune response diminished during ITN intervention.
Barodji et al. evaluated the efficacy of ITN in East Flores (Lesser

Sundas) in 19931994 (Barodji et al., 2004a). Twenty-four houses in three
villages were recruited as treatment sites and eight houses in Ebak village,
10 km away, as control sites. Nylon bed nets of 2 2 2 m were
treated with a dosage of etofenprox at 0.2 g/m2. Treatment was con-
ducted by trained health workers every 6 months for 18 months. Nets
were returned to participants after each treatment. The residual mortality
against 90 A. barbirostris was evaluated for 24 h after a 30-min exposure to
the nets. The tests were repeated on weeks 1 and 2, and each month for
5 months. Night mosquito landing density was evaluated every night
(1824 p.m.) and morning resting densities at 67 a.m. A malaria survey
was conducted 3 months before intervention began and 1 month after
each treatment cycle only at one treatment village and control village. It is
unclear why the authors only measured in one of three treatment villages
or how they selected the survey village. A direct contact test showed that
5 months after treated the mosquito mortality rate was 100%. In the
treated village, the indoor mosquito landing densities reduced from 0.29
(before intervention) to 0.22 mosquitoes/man-hour (after 6 months) and
below 0.04 mosquitoes/man-hour in the next 12 months. Relative to
control, there was a 76% of reduction in indoor mosquito landing density.
The morning resting density decreased from 0.38 mosquitoes/man-hour
(before intervention) to less than 0.08 mosquitoes/man-hour (reduction
93%) after the first 6 months, but have since increased. In terms of malaria
morbidity, the authors noted that P. falciparum prevalence in one treated
village decreased from 10% (13/128) before the intervention to 6%
(15/244) and 4% (6/142) at the second and the third cycle, respectively.
However, after 6 months, the prevalence was 13% (10/78). In the control
village, the prevalence of P. falciparum was relatively high at 8.6%
(14/163) at before intervention and, on average, 18.2% (52/286) after
first cycle. The authors noted no reported side effects by inhabitants and
health workers to the insecticide. The small sample sizes used in this
study limit what conclusion can be drawn.
Barodji et al. evaluated the efficacy of the insecticide permethrin at a
dosage of 0.5 g/m2 on nylon and cotton nets against A. maculatus and
A. barbirostris (Barodji et al., 1999). Three treatments were applied. For the
first treatment, the nets were impregnated with insecticide suspension,
and left to dry naturally. For the second treatment, the nets were inserted
into plastic bags filled with the insecticide suspension where they were
crumpled, removed and left to dry naturally for 1 day. Finally, the nets
were sprayed using IRS sprayer and also dried naturally for 1 day.
A direct contact test against A. maculatus and A. barbirostris was conducted
by exposing 30 mosquitoes of each species for 3 min to each of the treated
nets. The mosquitoes were then transferred into clean cups (no insecti-
cide). The mosquito mortality rate was observed for 24 h. Against
A. maculatus, mosquito mortality rate on nylon nets was higher compared

to the cotton nets for all three of treatments: impregnating (99% vs. 60%),
crumpling (48% vs. 16%) and spraying (87% vs. 34%). A. maculatus mor-
tality rate in impregnated nylon nets (99%) was higher than sprayed
nylon nets (87%) or crumpled nylon nets (48%). Against A. barbirostris, a
direct contact test showed that the mosquito mortality rate on nylon nets
was higher than the cotton nets for all treatment types: impregnating (97%
vs. 46%), crumpling (31% vs. 14%) and spraying (76% vs. 29%). A. barbir-
ostris mortality rate on impregnated nylon nets (97%) was higher than on
sprayed nylon nets (76%) or crumpled nylon nets (31%). Therefore, the
authors concluded that nylon was superior than cotton as net material.
They also summarized that the practice of spraying mosquito nets during
IRS was also possible method against A. maculatus and A. barbirostris.
Barodji et al. evaluated the efficacy of ITN against A. barbirostris,
A. subpictus and A. sundaicus in East Flores, Lesser Sundas in 1996
(Barodji et al., 2004b). Eight houses in Waiwadan village were recruited
as treatment sites. They had no houses for control. Nylon bed nets were
exposed to a dosage of cyfluthrin at 0.05 g/m2. The sets were treated by
trained health workers. Night mosquito landing density was evaluated
every night (1824 p.m.). A malaria survey was conducted 3 months
before the intervention and every 3 months after the ITN application.
The study showed that the cyfluthrin treated nets provided impact in
A. sundaicus and A. subpictus, but not A. barbirostris. Against A. barbirostris,
indoor mosquito landing densities only reduced from 0.74 (before inter-
vention) to 0.68 mosquitoes/man-hour (after 3 and 6 months). However,
its landing densities increased from 0.4 (before) to 0.8 mosquitoes/man-
hour (after 3 and 6 months) outdoors. Against A. subpictus, indoor mos-
quito landing densities reduced from 7.7 (before) to 2.5 mosquitoes/man-
hour (after 3 and 6 months). Outdoor mosquito landing densities
decreased from 10.1 (before) to 4 mosquitoes/man-hour (after 3 and 6
months). Indoor and outdoor landing densities of A. sundaicus before
intervention were 2.4 and 1.3 mosquitoes/man-hour. Less than
0.03 indoor or outdoor mosquitoes/man-hour landing both 3 or 6 months
after intervention. In terms of malaria prevalence, the authors reported
that SPR reduced from 17% (48/275) before the ITN intervention to 13%
(17/128) 3 months after application and 4% (11/250) 6 months after.
However, the malaria prevalence increased to 7.5% (39/518) 912 months
after intervention. The authors noted no reported side effects by inhabi-
tants and health workers to this insecticide. They concluded that ITN
application by cyfluthrin could reduce mosquito landing density of
A. sundaicus and A. subpictus in East Flores, and decreased malaria preva-
lence for 36 months after application.
Hakim et al. compared the mosquito mortality rate among permethrin,
deltamethrin and lambda-cyhalothrin ITNs at dosage of 0.5 g/m2 against
A. sundaicus in Ciamis (West Java) in 2006 (Hakim et al., 2008). Each 4-m2
net was treated by those insecticides and mixed with adhesive glue
contained 86% acrylic and 14% arthathrin. This acrylic bonded the insec-
ticide to the fibre net allowing it to remain effective after multiple washes
and arthathrin helps the acrylic particles dissolve into insecticides. As
control, they used permethrin ITN without the additional glue. Each net
was exposed to 50 A. sundaicus. At 5-min intervals, the number of dead
mosquitoes was recorded and after 40 min all remaining mosquitoes were
moved to clean cup and observed for 24 h. After the observations were
completed, nets were washed with water and detergent for 5 min, dried
and re-tested. Nets were washed 30 times. The study showed that mos-
quito mortality rate with adhesive permethrin and deltamethrin ITNs was
100% up to 20 washes, then decreased to 80% on 30 washes. Mosquito
mortality rate with lambda-cyhalothrin ITNs was 100% after 30 washes
and with the non-adhesive permethrin ITNs reduced from 100% before
washing to 92% after one wash and diminished gradually to 2% after 30
washes. The study concluded that in the laboratory at least, the presence
of acrylic and arthathrin was effective to maintain ITNs efficacy against
A. sundaicus.
Despite the distribution of 2.4 million ITNs from 2004 to 2007 (World
Health Organization, 2008e, 2009c), no study has yet demonstrated that
this intervention actually reduces the risk of malaria or the burden of
morbidity and mortality in Indonesia. No studies reveal the coverage
rates required to achieve such effects, nor is there evidence that small
children and pregnant women represent high-risk groups for malaria
morbidity or mortality. Among Javanese transmigrants in Papua, for
example, adults had a fourfold higher risk of developing severe malaria
than their children (Baird et al., 1995d). Risk of a poor outcome probably
varies among ethnic groups and among the very many endemic settings
in Indonesia. A critical examination of ITN efficacy using a prospective,
randomized and well-controlled study design of sufficient size to
measure all-cause morbidity and mortality should be carried out in a
setting typical of most malarious areas in Indonesia, that is, in a hypo-
to mesoendemic area.
2.4.4.2.2. House screening Ease of mosquito access to human dwellings

profoundly impacts on the risk of malaria. The screening of windows,
doors and open eaves represents an effective barrier to entry by feeding
anophelines. Evidence shows that even simple modifications to the
design of indigenous houses can protect people from mosquitoes and
malaria (Kirby et al., 2009; Lindsay et al., 2002).
According to the National Economic and Social Survey (Badan Pusat
Statistik, 2008) which was conducted by the Indonesian Centre of Statis-
tics in 2008 and which surveyed over 270,000 households, 65% of houses
were made of brick/cement (urban: 81% vs. rural: 51%), 23% of wood
(urban: 13% vs. rural: 33%), 10% of bamboo (urban: 5% vs. rural: 15%) and
2% of other materials. Wooden and bamboo-walled houses were common
in rural settings. In western Indonesia, more houses were made of brick/
cement than in eastern Indonesia (western Indonesia: 65% vs. eastern
Indonesia: 42%; p 0.002). Wooden-walled houses were more common
in eastern Indonesia (46% vs. 28%; p 0.044). Bamboo walls were simi-
larly rare in eastern and western Indonesia (6% vs. and 8%; p 0.719).
In West Sumba (Lesser Sundas archipelago), where stable transmission of
malaria occurs, the most common type of housing consisted of wooden
plank walls and dried palm leaf roofing (Ompusunggu et al., 2006).
Mosquitoes enjoy free access into these traditional homes through gaps
in the walls, open doors and windows or eaves.
Sanjana et al. conducted a survey of KAP towards and against malaria in
and around the Menoreh Hills (Purworejo, Central Java) in 2001 (Sanjana
et al., 2006). One thousand respondents were interviewed and it was reported
that the walls of their houses were constructed of a variety of materials,
including brick (25%), cement (20%), wooden planks (12%), bamboo (10%)
or a combination of these materials (31%). Only 2% of the 1000 houses
surveyed had screens over the window openings, but 72% had some or all
window areas covered with glass or plastic. It also became apparent that the
physical make-up of the homes was different according to whether the
respondents were residents of hills/forested areas or were living in rice
paddies or urban areas. Paddy/urban homes were more often made with
mixed materials than forest/hill homes (37% vs. 29%; p 0.007), whilst
forest/hill homes were more likely to be made from wood (15% vs. 9%;
p < 0.001). Those living in paddy/urban homes used more glass window
coverings than those in forest/hill homes (32% vs. 23%; p 0.003). Cement or
brick constructions were shown to afford greater protection against malaria
illness than all other building materials (OR 0.6, p < 0.0001). Partial glass
or no glass over windows increased malaria risk (OR 1.8, p < 0.0001).
These findings strongly suggest that house construction and barriers to
mosquito access should be targeted in malaria prevention strategies.
Roosihermiatie et al. conducted an unmatched case control study in
Bacan Island, North Maluku in 1998 (Roosihermiatie et al., 2000). The
residents of 11 villages made up the sample population. One hundred
individuals from each village confirmed as malaria positive were selected
as cases and those confirmed as malaria negative were selected as con-
trols. A positive association between house quality and malaria was
described but was extremely age-dependent. Children under 15 years of
age living in temporary houses were at a higher risk of contracting
malaria than children of the same age living in more permanent housing
(OR 8.7, 95% CI 1.2386). Among adults, no such difference existed
(OR 0.7; 95% CI 0.13.0).
Several studies have evaluated house construction in malaria endemic

areas. Sekartuti et al. conducted a cross-sectional KAP survey in two
malaria endemic villages in South Lampung in 2003 (Sekartuti, 2003).
Malaria prevalence in both sites combined was 17% (95/549), with a
dominance of P. falciparum (64%). Of the 420 households interviewed,
over 90% of houses lacked screens and the owners did not associate
these with the prevention of malaria. Arsunan et al. conducted a KAP
survey in Pangkajene Island (South Sulawesi) in 2003 (Arsunan et al.,
2003). It is unclear why, but the investigators sampled only one person per
household, not only for the interview, but also for the blood film exami-
nation. Among 264 households randomly selected, 8% of households
were malaria positive. The authors also made a note of the characteristics
of the surveyed homes and found that only 3% (8/264) used window or
door screens. Suharjo et al. also conducted a KAP survey in two sub-
districts in Banjarnegara (Central Java) in 2003 (Suharjo et al., 2004). One
hundred households were randomly selected. Only three of these used
screening. However, none of these studies analysed the possible associa-
tion between house screening and the risk of malaria.
The screening of homes, where practical, may represent an effective
means of avoiding the risk of malaria. This principle also extends to other
effective barriers applied to floors, walls and roofing in more traditional
Indonesian homes. For example, the simple act of placing inexpensive
plastic floor sheeting over wood plank flooring would largely close off an
otherwise easy means of entry. The availability of insecticide-treated eave
covers and curtains may also dramatically reduce ease of access to
humans by night-feeding anophelines. One rarely encounters these mate-
rials in rural Indonesia and awareness of their effectiveness in preventing
malaria appears to be very low, as documented in the studies discussed
above. More evidence from a range of ecoepidemiological settings will be
needed to convince policy makers that this intervention is broadly appli-
cable throughout malarious areas in Indonesia.
2.4.4.2.3. Personal protection Personal protection against biting mosqui-

toes represents a potentially important means of diminishing the risk of
malaria. Individuals may take any number of a wide range of steps to do
so. The primary means of avoidance is behavioural, that is, avoiding
being at locations where and when malaria transmission is likely to
occur. Although of limited value to residents of endemic areas, this is an
important means of risk reduction for travellers. For example, the person
aware of seasonal malaria risk at any given location avoids scheduling
travel during that season and avoids being in the countryside after dusk.
These measures alone may almost completely eliminate risk. The use of
repellents, long sleeve shirts, pants and shoes with socks also diminish
risk, and tend to be more practical for travellers than for residents.
Fumigant insecticides, like burning mosquito coils, may be effective

and practical for both travellers and residents. Indeed, these represent the
most common form of personal protection used in Indonesia. Several
studies have documented that coil usage rates in endemic areas range
from 50% to 83% (Arsunan et al., 2003; Pribadi et al., 1997; Santoso et al.,
1991, 1992). Mosquito coils are inexpensive and widely available in
endemic settings (Santoso, 1988). Saikhu and Gilarsi used secondary
data from the BES conducted in four districts in Central Java; Banjarnegara,
Pekalongan, Kebumen and Jepara (Saikhu and Gilarsi, 2003). The survey
had 15,901 respondents of all ages from 4032 households. Among the 6485
expressing awareness of malaria, the most popular method of malaria
prevention was the use of mosquito coils (72%). There was a small
correlation between the knowledge of mosquito coils as a means of
malaria prevention and a protective effect against malaria (p 0.035;
OR 1.5, 95% CI 1.032.2). Like the KAP study in Purworejo (Sanjana
et al., 2006), this survey does not serve as a demonstration of the efficacy
of coils against malaria. However, the results at least suggest that mos-
quito coils may have some impact upon the risk of malaria.
People in Indonesia also burn rubbish, clove tree foliage or coconut
leaves in a deliberate effort to repel night-feeding mosquitoes, but accord-
ing to a number of studies, only between 1% and 28% of people do so
(Mardiana and Santoso, 2004; Pribadi et al., 1985, 1997; Santoso, 1988;
Santoso et al., 1991, 1992). People in Indonesias rural endemic zones also
use insecticide spray dispensers at rates varying between 4% and 37%
(Mardiana and Santoso, 2004; Santoso and Kasnodihardjo, 1991; Santoso
et al., 1991; Sukowati et al., 2003). They also tend to wear long-sleeved
clothing when they go outdoors at night (Santoso and Friskarini, 2003).
One study in Eastern Indonesia (Sekartuti et al., 2004c) reported that
1942% of respondents did so. Ompusunggu et al. supposed that rela-
tively low prevalence among infants was attributable to clothing worn
during the night (Ompusunggu et al., 2006). Yahya et al. described the
willingness of mothers to use mosquito coils and wear appropriate cloth-
ing to protect their children (Yahya et al., 2006). Nonetheless, few children
actually wore the most effective protective clothing. For example, they
would wear a jacket or sarong, but would have no shoes or socks.
As with household screening, personal protection appears to hinge
upon awareness of malaria and the means of its transmission. In contrast
to household screening, however, personal protection measures among
residents of endemic Indonesia seem varied and quite common, which is
likely to be driven by the nuisance factor of night-feeding mosquitoes. The
rates of mosquito coil usage, for example, seem unusually high in light of
the correspondingly low rates of both bed net usage and screening. Coils
are not provided through government programs (in contrast to ITNs), and
are relatively inconvenient (igniting the coil and enduring its smoky
product). Leveraging this positive behaviour to improving barriers to

entry into homes and beds seems an obvious means of ramping up the
effectiveness of malaria control.
2.4.4.2.4. Zooprophylaxis Zooprophylaxis is defined by the WHO as the

use of wild or domestic animals, which are not the reservoir hosts of a
given disease, to divert the blood-seeking mosquito vectors from the
human hosts of that disease (Bouma and Rowland, 1955). It may be active
or passive. Active zooprophylaxis is a reduction in malaria or human
biting resulting from the deliberate deployment of domestic animals as a
barrier between mosquito breeding sites and human settlements (Bouma
and Rowland, 1955; Seyoum et al., 2002). Passive zooprophylaxis is the
serendipitous reduction in malaria purported to occur when cattle den-
sity increases within a community (Bulterys et al., 2009; Giglioli, 1963).
Several studies in Indonesia have explored the possibility of zooprophy-
laxis as a malaria control tool.
Kirnowardoyo and Supalin evaluated the association between cattle
shelter location and A. aconitus contact with humans (Kirnowardoyo and
Supalin, 1982). At three villages in Wonosobo and four villages in
Purworejo (both in Central Java) in 19811982, it was found that those people
who had cattle shelters in or attached to their homes had man-landing rates
which were 4.6 times higher than the rates for people who had their cattle
shelters separated from the house (3.2 vs. 0.7 mosquito/man-hour;
p 0.076). The proportion of captured anophelines found to have taken a
human blood meal was higher among homes with cattle shelters attached
(5.9% vs. 0.5%; p 0.076). Kirnowardoyo and Supalin concluded that the
placement of cattle away from human dwellings appeared to divert
A. aconitus and reduce man-mosquito contact (Kirnowardoyo and Supalin,
1986). This species of mosquito is known to prefer feeding on animals rather
than humans, which will certainly have had an impact on the outcome of
this evaluation. When mosquito preferences lean toward human biting,
outcomes may be radically different and the strategies concerning cattle
placement would thus also be completely different.
Boewono et al. investigated the effect of cattle shelter placement on
indoor densities of A. aconitus in Kendal (Central Java) in 1986 (Boewono
et al., 1991). In the study area, the ratio of people to cattle was 12:1. They
studied four groups: houses with cattle shelter inside (4), houses with
cattle shelter attached (4), houses with cattle shelter 20 m from dwelling
(4) and houses with no cattle shelter (2). They found a sixfold higher
mosquito density in homes with an indoor cattle shelter than in the
homes with a distant cattle shelter, as well as the two homes with no
cattle shelter. This value was fourfold when compared to homes with a
cattle shelter attached. This accords with the zoophilic feeding behaviour
of A. aconitus.
2.4.4.3. Control of adult mosquito

2.4.4.3.1. Indoor residual spraying IRS is the application of long-acting
chemical insecticides on the walls, doors and ceilings of all houses and
domestic animal shelters in a given area in order to kill the adult vector
mosquitoes that land and rest on these surfaces (World Health
Organization, 2006a). The indoor spraying of chemicals that have a
relatively long residual effect, typically 26 months, remains a vitally
important means of reducing the risk of malaria (World Health
Organization, 2008e). In addition to possible protection arising from the
excito-repellancy of some insecticides (i.e. the scent of the insecticide forces
mosquitoes to fly away from the house), insecticide kills mosquitoes that
rest on interior surfaces before or, more often, after feeding on humans. The
efficacy of IRS thus hinges upon the feeding behaviour of the local anophe-
line species responsible for malaria transmission. Some species do not
prefer feeding indoors (exophagic), or they may tend to fly directly out-
doors without resting on interior walls. Efficacy also depends upon the
dose and degree of coverage of the interior surfaces of the home. Moreover,
as with ITNs, protection improves if more homes in any given area are
covered by this form of control. One of the greatest pitfalls of IRS is the
infrastructure required to deliver it safely and effectively. The selection of
insecticide and its safe application requires relatively large numbers of
people with highly specialized training and equipment (Oemijati, 1980).
Table 2.12 shows the evolution of recommended insecticides for malaria
control in Indonesia. According to the WHO expert committee on pesti-
cides (often referred to as WHOPES) in 2009, 12 insecticides belonging to
four chemical classes are recommended for IRS (World Health
Organization, 2007a). These insecticides included the pyrethroid class
(alpha-cypermethrin, bifentrin, cyfluthrin, deltamethrin, etofenprox and
lambda-cyhalothrin), carbamate class (bendiocarb, propoxur), organopho-
sphates (fenitrothion, malathion, pirimiphos-methyl) and organochloride
(DDT). According to the Indonesian MoH released in 2003 and 2010
(Departemen Kesehatan, 2003c, 2010), six insecticides belonging to two of
these classes may be applied for IRS: pyrethroids (alpha-cypermethrin,
bifentrin, deltamethrin, etofenprox and lambda-cyhalothrin) and carba-
mates (bendiocarb). Earlier, the Indonesian MoH had recommended orga-
nophosphates for IRS (fenitrothion, malathion, pirimiphos-methyl).
According to the Indonesian MCP guidelines, IRS is targeted at endemic
areas with an API > five cases per 1000 population, areas with malaria
positive infants or areas with a high potential of malaria outbreak
(Departemen Kesehatan, 2006a). The guidelines suggest that IRS be con-
ducted 2 months prior to the median peak of malaria case numbers. The
median value is derived from the last 35 years of monthly malaria cases.
Alternatively, spraying should be done 1 month before the peak density of
TABLE 2.12 The World Health Organization (WHO) and the Indonesian Malaria Control Program (IMCP) recommended insecticides for indoor
residual spraying against malaria vectors
WHO (2009) IMCP (1993) IMCP (2003, 2010)

Dosage Dosage Dosage
Insecticide Class Recommended (g/m2) Recommended (g/m2) Recommended (g/m2)
Alpha-cypermethrin Pyrethroid Yes 0.020.03 No Yes 0.02

Bifentrin Pyrethroid Yes 0.0250.05 No Yes 0.025
Cyfluthrin Pyrethroid Yes 0.020.05 No No
Deltamethrin Pyrethroid Yes 0.020.025 No Yes 0.2
Etofenprox Pyrethroid Yes 0.10.3 No Yes 0.1
Lambda-cyhalothrin Pyrethroid Yes 0.020.03 Yes 0.025 Yes 0.025
Bendiocarb Carbamate Yes 0.10.4 Yes 0.4 Yes 0.2
Propoxur Carbamate Yes 12 No No
Fenitrothion Organophosphate Yes 2 Yes 1 No
Malathion Organophosphate Yes 2 Yes 12 No
Pirimiphos-methyl Organophosphate Yes 12 Yes 1 No
DDT Organochloride Yes 12 Yes 12 No
the local malaria vector (Departemen Kesehatan, 2006a). IRS is aimed at

houses, dangau/saung (small wooden or bamboo shelters in ricefields
where farmers wait for the rice harvest), animal shelters and public places
where evening activities are common. The guidelines recommend full cov-
erage with IRS to a height of 3 m. Several studies in Indonesia have explored
the effects of this application of insecticides against malaria vectors.
The following sections (Sections 2.4.4.3.1.12.4.4.3.1.12) include insecti-
cide-specific summaries of the available published evidence for efficacy and
tolerability of these chemicals in Indonesia. Some useful information may be
gleaned from these many studies with respect to guidance on dosage and
manner of application. However, we have found no published reports of
village-randomized trials of these interventions. Although many of the
available data do suggest good levels of efficacy and tolerability, one may
argue that convincing evidence of this has yet to be generated in Indonesia.
2.4.4.3.1.1. Alpha-cypermethrin Alpha-cypermethrin is a synthetic pyre-

throid. It has a high-knockdown effect and a strong excito-repellent effect
on anophelines (Najera and Zaim, 2001). It acts by blocking nerve
impulses by stopping the passage of sodium ions through channels in
the nerve membranes. This insecticide is classified by the WHO as a
moderately hazardous chemical (World Health Organization, 2006b).
Typically, intoxication of the mosquito results in a rapid knockdown
effect and high-mortality rate (World Health Organization, 2007b). The
dosage recommended by the WHO is 0.020.03 g/m2, giving a residual
effect of 46 months (World Health Organization, 2007a). The Indonesian
MoH recommended alpha-cypermethrin wettable powder (WP) at a dos-
age of 0.02 g/m2 for IRS (Departemen Kesehatan, 2003c, 2010). Several
studies in Indonesia have explored the application of this insecticide
against malaria vectors.
Barodji et al. conducted a village-scale trial of cypermethrin 20% WDP
applied as a residual spray at a dosage of 0.5 g/m2 against DDT-resistant
A. aconitus in Semarang (Central Java) in 1981 (Barodji, 1982; Barodji et al.,
1983). IRS was carried out for 479 households with insecticide usage
averaging 0.58 kg/house. A. aconitus mosquitoes were collected indoors
and outdoors 1 week before application and then every week after the
application for 21 weeks. A direct contact test at dosage 0.5 g/m2 of
cypermethrin on wooden and bamboo surfaces was conducted every
3 weeks for 24 weeks. It was found that cypermethrin did not reduce
indoor mosquito landing (before application: 0.5 vs. after: 0.7 mosquito/
man-hour) or outdoor landing (before: 1.4 vs. after: 1.3 mosquito/man-
hour). There was an increase of 35% in morning resting density (before:
3.4 vs. after: 4.6 mosquito/man-hour). Only a 9% reduction of the natural
outdoor resting density was achieved (before: 95 vs. after: 86 mosquito/
man-hour). A direct contact test showed that the insecticide residue could
last for 15 weeks on wooden and bamboo surfaces (mosquito mortality

rate 91% on both surfaces). Barodji et al. concluded that cypermethrin was
ineffective against A. aconitus in Central Java.
Barodji et al. experimented with the IRS application of alphamethrin
5% water dispersible powder (WDP) at a dosage of 0.1 g/m2 against DDT-
resistant A. aconitus at Kendal (Central Java) in 1985 (Barodji et al., 1989).
The IRS program involved the spraying of 1254 houses with an average of
0.02 kg insecticide/house. A. aconitus mosquitoes were collected indoors
and outdoors 2 weeks before application and every 2 weeks after applica-
tion for 12 weeks. A direct contact test at a dosage of 0.02 g/m2 alphame-
thrin on wooden and bamboo surfaces was conducted 2 weeks after
application and measured monthly afterwards. It was revealed that the
insecticide reduced the indoor mosquito landing density by only 16%
(before: 0.45 vs. after: 0.38 mosquito/man-hour) and did not reduce
outdoor mosquito landing rate, but rather seemed to cause an increase
of 57% (before: 0.37 vs. after: 0.95 mosquito/man-hour). A reduction of
46% in morning resting density was found (before: 2.8 vs. after: 1.5 mos-
quito/man-hour), while at natural outdoor resting sites a more modest
decrease of 15% occurred (before: 57.5 vs. after: 49.1 mosquito/man-
hour). A direct contact test showed that on day 16 the mosquito mortality
rate had reduced from 100% to less than 60% on wood and less than 20%
on bamboo surfaces. Alphamethrin therefore appears to be ineffective
when applied on wooden or bamboo surfaces. As in the previous study,
this insecticide was ineffective in reducing A. aconitus mosquito landing
density in Kendal (Central Java). The low efficacy of alphamethrin may
have been caused by the relatively low dosage compared to the trial at
Semarang, Central Java (Barodji, 1982; Barodji et al., 1983). However, the
authors did not explain the rationale of using a lower dosage in this trial.
Boewono et al. conducted excito-repellency tests of alpha-cypermethrin
at dosages of 0.0125, 0.025 and 0.05 g/m2 against A. sundaicus at Purwor-
ejo (Central Java) in 2000 (Boewono et al., 2002) The box interior was
coated with insecticide. The test ran for 60 min with eight replications.
Each replication used 25 mosquitoes, giving a total of 200 mosquitoes
evaluated at each dose. The number of mosquitoes able to exit the test
box was recorded. Slightly more mosquitoes exited the test box at a dosage
of 0.05 g/m2 (17%) compared to the dosage of 0.025 g/m2 (12%; p 0.16),
the dosage of 0.0125 g/m2 (9%; p 0.02) and the control (9.5%; p 0.027).
In other words, at higher doses, mosquitoes tend to avoid the insecticide
sprayed surfaces. By considering the dosage recommended by the WHO
(0.03 g/m2; World Health Organization, 2007a) and the closest dosage
evaluated, that is, 0.025 g/m2, about 88% of the mosquitoes would be
expected to die after exposure. The authors concluded that an IRS program
with alpha-cypermethrin would be likely to be effective against A. sundai-
cus in coastal areas of Purworejo (Central Java).
2.4.4.3.1.2. Bifentrin This insecticide is classified by the WHO as moder-

ately hazardous (World Health Organization, 2006b). The dosage recom-
mended by the WHO is 0.0250.05 g/m2 and should remain effective up
to 6 months (World Health Organization, 2007a). The Indonesian MoH
recommends bifentrin 10% WP at a dosage of 0.025 g/m2 for IRS
(Departemen Kesehatan, 2003c, 2010). Several studies in Indonesia have
explored the application of bifentrin against malaria vectors.
Barodji et al. measured the efficacy of bifentrin 10% WP at doses of
0.025, 0.05, 0.1 and 0.15 g/m2 against A. maculatus at Salatiga (Central
Java) in 2000 (Barodji et al., 2000). Mosquito mortality was observed
weekly for 6 months. At 6 months post-application, the dosage of
0.15 g/m2 was effectively killing A. maculatus on wood (98%), bamboo
and cement surfaces (100%). Also at 6 months post-application, the dos-
age of 0.1 g/m2 bifentrin was killing 84% of mosquitoes on wood, 100% on
bamboo, but was less effective on cement (48%). The dosage of 0.05 g/m2
was ineffective on wood (40%) and cement (46%), but remained effective
on bamboo surfaces (96%). At the lowest dose (0.025 g/m2), bifentrin was
ineffective on all types of surfaces (mortality < 14%). Barodji et al. recom-
mended the use of a dosage of 0.1 or 0.15 g/m2 against A. maculatus in
Central Java.
In 2006, Sunaryo et al. evaluated the effect of bifentrin spraying (with a
dosage of 0.025 g/m2) in Kebumen (Central Java) 35 days after application
in response to a malaria outbreak driven by A. maculatus, A. aconitus and
A. balabacensis (Sunaryo et al., 2007). Wood, bamboo and cement surfaces
from six houses were sprayed. Mortality was observed for 24 h. They
found 94% mortality on wood, 83% on bamboo and 64% on cement
surfaces. It appears that cement surfaces absorbed more insecticide than
other surface types and the insecticide remaining on the surface was
insufficient to effect a kill.
2.4.4.3.1.3. Cyfluthrin Cyfluthrin is a synthetic pyrethroid insecticide

which is effective against a wide variety of agricultural and public-health
pests (World Health Organization, 2003c). Its mode of action is character-
ized by interference with nerve signalling by inhibition of the membrane
sodium channel systems in the target organism. Cyfluthrin is mainly
a contact insecticide classified as moderately hazardous (World
Health Organization, 2006b). It has a very high-knockdown and low
excito-repellent effect (Najera and Zaim, 2001). It is also known by the
name baythroid (World Health Organization, 2003c). The WHO recom-
mends a dosage of 0.020.05 g/m2, giving a residual effect lasting three up
to 6 months (World Health Organization, 2007a). The Indonesian MoH
does not recommend this insecticide for IRS as part of its insecticide
rotation cycle policy (Departemen Kesehatan, 2003c). Several studies have
explored the application of cyfluthrin against malaria vectors in Indonesia.
Barodji et al. investigated the impact of cyfluthrin IRS against

A. barbirostris, A. subpictus and A. sundaicus in East Flores (Lesser Sundas)
in 1996 (Barodji et al., 2004b). They applied a dosage of 0.05 g/m2 with a
single application. Indoor and outdoor human-landing collections were
measured before application, and then again 3 and 6 months after appli-
cation. No physical complaints were reported from villagers or sprayers.
For A. barbirostris, they found that the indoor man-landing rate declined
from 6.4 mosquito/man-hour before application to 4.6 mosquito/man-
hour at 3 months (reduction: 28%) and 4.8 mosquito/man-hour at
6 months (reduction: 25%). The outdoor man-landing rate reduced from
5.2 mosquito/man-hour before application to 4.4 mosquito/man-hour at
3 months (reduction: 16%), but increased again by 33% to 5.4 mosquito/
man-hour at 6 months. For A. subpictus, the indoor man-landing rate
reduced from 14.3 mosquito/man-hour before application to 7.9 mos-
quito/man-hour at 3 months (reduction: 45%) and 2.6 mosquito/man-
hour at 6 months (reduction: 86%). The outdoor man-landing rate
decreased from 20.5 mosquito/man-hour before application to 16.7
mosquito/man-hour at 3 months (reduction: 19%) and to 1.5 mosquito/
man-hour at 6 months (reduction: 93%). For A. subpictus, the indoor
man-landing rate declined from 14.3 mosquito/man-hour before applica-
tion to 7.9 mosquito/man-hour at 3 months (reduction: 45%) and 2.6
mosquito/man-hour at 6 months (reduction: 86%). The outdoor man-
landing rate decreased from 20.5 mosquito/man-hour before application
to 16.7 mosquito/man-hour at 3 months (reduction: 19%) and to 1.5 mos-
quito/man-hour at 6 months (reduction: 93%). For A. sundaicus, the
indoor man-landing rate declined from 4.2 mosquito/man-hour before
application to zero at 3 and 6 months after application (reduction: 100%).
The outdoor man-landing rate reduced from 4.5 mosquito/man-hour
before application to 0.04 mosquito/man-hour at 3 months (reduction:
99%) and to zero at 6 months (reduction: 100%). They concluded that
cyfluthrin at a dosage of 0.05 g/m2 was effective in reducing man-vector
contact in the case of A. sundaicus, but not in the case of A. barbirostris
and A. subpictus. The SPR among residents in the area sprayed was 39%
(63/162) before spraying. This fell to 11% (16/145) at 3 months
post-application and to 3% (4/158) at 6 months.
2.4.4.3.1.4. Delthamethrin Deltamethrin is a synthetic pyrethroid which

has been used in malaria control in Indonesia since the late 1970s (Najera
and Zaim, 2001; World Health Organization, 2008d). Its mode of action is
primarily upon the basal ganglia causing repetitive nerve action (Najera
and Zaim, 2001). This insecticide is classified by the WHO as a moderately
hazardous insecticide. It is used at dosages of 0.020.025 g/m2, giving a
residual effect of three up to 6 months (World Health Organization,
2007a). The Indonesian MoH recommends deltamethrin 5% WP at a
dosage of 0.2 g/m2 for IRS (Departemen Kesehatan, 2003c, 2010). We

found no published IRS study of deltamethrin against malaria vectors in
Indonesia.
2.4.4.3.1.5. Etofenprox Etofenprox is a synthetic non-ester pyrethroid
which has high vapour pressure and low water solubility (World Health
Organization, 2006g). It is classified by the WHO as unlikely to pose an acute
hazard in normal use as a residual insecticide (World Health Organization,
2006b). It disturbs nerve impulses in insect nerve axons (Najera and Zaim,
2001). The WHO recommends a dosage of 0.10.3 g/m2, giving a residual
effect of three up to 6 months (World Health Organization, 2007a). The
Indonesian MoH recommends etofenprox 20% WP at a dosage of 0.1 g/m2
for IRS (Departemen Kesehatan, 2003c, 2010). An operational study has
affirmed good results for etofenprox in Indonesia.
Nalim et al. conducted a trial of etofenprox in East Flores (Lesser
Sundas) in 1994 (Nalim et al., 1997). They applied 0.2 g/m2 three times
at 6-month intervals. The suspected vectors were A. sundaicus, A. barbir-
ostris, A. flavirostris and A. maculatus. Human-landing rates and resting
densities were measured every 2 weeks for 16 months. A direct contact
test was conducted on wooden and bamboo surfaces. Mosquito mortality
was observed for 24 h in the 240 sprayed homes. The direct contact test
showed that the insecticide remained efficient for up to 4 months on
wooden surfaces and for 5 months on bamboo. The human-landing rate
decreased from 0.91 mosquito/man-hour before application to 0.23 mos-
quito/man-hour at 6 months, 0.004 mosquito/man-hour at 12 months
and zero at 18 months. Likewise, the indoor resting density dropped
from 0.9 mosquito/man-hour before application to 0.1 mosquito/man-
hour at 6 months, dropping further to zero and remaining there at 12 and
18 months of IRS. Despite this apparently superb activity, they found no
significant reduction in SPR among residents in the earlier stages of
implementation: 30.6% before spraying; 30% at first cycle; and 21%
(p 0.054) at second cycle. However, a significant reduction of SPR was
observed at 18 months after application (8%; p < 0.001). No physical
complaints were reported from villagers or sprayers. Nalim et al. con-
cluded that their study was a good demonstration of the efficacy and
tolerability of this insecticide.
2.4.4.3.1.6. Lambda-cyhalothrin Lambda-cyhalothrin is a synthetic
pyrethroid (World Health Organization, 2006e). It has a low vapour
pressure, is essentially insoluble in water, and has low volatility (Najera
and Zaim, 2001). The WHO classifies this insecticide as moderately
hazardous (World Health Organization, 2006b). It is used at a dosage of
0.020.03 g/m2, giving a residual effect of 36 months (World Health
Organization, 2007a). The Indonesian MoH recommends lambda-
cyhalothrin 10% WP at a dosage of 0.025 g/m2 for IRS (Departemen
Kesehatan, 2003c, 2010). We found no publications about the use of

lambda-cyhalothrin against malaria vectors in Indonesia.
2.4.4.3.1.7. Bendiocarb Bendiocarb is a carbamate insecticide (World
Health Organization, 2008a). It has a low vapour pressure and low
odour (Najera and Zaim, 2001). The WHO classifies it as moderately
hazardous (World Health Organization, 2006b). The WHO recommends
a dosage of 0.10.4 g/m2, giving a residual effect of two up to 6 months
(World Health Organization, 2007a). The Indonesian MoH recommends
bendiocarb 80% WP at a dosage of 0.2 g/m2 for IRS (Departemen
Kesehatan, 2003c, 2010). Three studies have been performed, document-
ing the efficacy of bendiocarb in Indonesia.
Fleming et al. conducted a village-scale trial of bendiocarb against
A. aconitus in Central Java in 1981 (Fleming et al., 1983). Bendiocarb 80%
WP at a dosage of 0.4 g/m2 was only effective in reducing human-vector
contact with A. aconitus within the first 2 months. Residual efficacy by
direct contact test lasted less than 2 weeks when sprayed on wooden or
bamboo surfaces. However, in natural resting catches, bendiocarb was
effective for 8 weeks.
Barodji et al. evaluated the efficacy of bendiocarb at a dosage of
0.4 g/m2 against A. maculatus and A. sinensis between 1996 and 1997
(Barodji et al., 1997). A. maculatus mosquitoes used for the test were
obtained from Kulonprogo (Yogyakarta) and A. sinensis from Nias (North
Sumatra). Mosquito mortality rates were observed 2 weeks post-applica-
tion, and then monthly for 6 months. The mortality rates for A. maculatus
and A. sinensis were 100% on wooden, bamboo and cement surfaces for up
to 4 months. However, at 5 months mortality rates for A. maculatus
decreased to 37% on wood, 33% on bamboo and 83% on cement. Mortality
rates for A. sinensis were reduced by 53% on wood, 70% on bamboo and
83% on cement. Wooden and bamboo surfaces failed to retain residual
activity. The authors concluded that bendiocarb spraying at 0.4 g/m2 on
cement surfaces was effective against A. maculatus and A. sinensis.
Bonsall et al. conducted safety studies of bendiocarb in a field trial in
1981 (Bonsall et al., 1981). Two of 16 sprayers experienced mild toxic
effects of short duration. Although no complaints were received from
the villagers after the spraying of over 800 homes, 39 ducklings died
and this was attributed to spraying.
2.4.4.3.1.8. Propoxur Propoxur is a carbamate insecticide which has been
used for IRS since the early 1970s (Najera and Zaim, 2001). The WHO
classifies it as a moderately hazardous chemical (World Health
Organization, 2006b). Propoxur inhibits acetylcholinesterase activity
(World Health Organization, 2003b). Acetylcholinesterase is an enzyme
which is responsible for hydrolysis of the neurotransmitter acetylcholine
(Carlier et al., 2008). Acetylcholine is a nerve system which sends
messages between nerves. The recommended dosage is 12 g/m2, giving

a residual effect of 36 months (World Health Organization, 2007a). The
Indonesian MoH does not recommend this insecticide for IRS as part of its
insecticide rotation cycle policy (Departemen Kesehatan, 2003c). We
found no publications describing the use of propoxur in Indonesia.
2.4.4.3.1.9. Fenitrothion Fenitrotion is an organophosphate insecticide

used extensively in IRS since the 1970s (Najera and Zaim, 2001). The
WHO classifies it as a moderately hazardous chemical (World Health
Organization, 2006b). The recommended dosage is 2 g/m2, giving
a residual effect of three up to 6 months (World Health Organization,
2007a). The Indonesian MoH does not recommend this insecticide for IRS
on the basis of the perception of a low margin of safety (Departemen
Kesehatan, 2003c). Nonetheless, several studies have examined the appli-
cation of fenitrotion against malaria vectors in Indonesia.
Joshi et al. conducted a village-scale fenitrotion trial against A. aconitus
in Semarang (Central Java) in 1976 ( Joshi et al., 1977). A dosage of 2 g/m2
retained residual lethal activity for 23 and 25 weeks on bamboo and
wooden surfaces, respectively. Other studies in the 1980s reported that
insecticide activity would only last 1418 weeks on similar surfaces (Bang
et al., 1981; Sukowati et al., 1979).
Suwarto et al. measured the efficacy of fenitrothion 40% WDP at a
dosage of 2 g/m2 against A. aconitus between full (0300 cm above floor)
versus selective (1085 cm above floor) coverage in Banjarnegara (Central
Java) in 1981 (Suwarto et al., 1987). Spraying was conducted in two cycles
at 6-month intervals. The number of houses sprayed in each cycle was
12,763 (full coverage) and 10,699 (selective coverage). The amount of
insecticide used for selective coverage was of course much less than full
coverage (0.48 vs. 1.4 kg/house; p < 0.001). In other words, there was a
potential saving of 65%. The average number of houses sprayed each day
using selective coverage was two times the number sprayed using full
coverage (12 vs. 6 house/day; p < 0.001). A further 50% of cost savings
could therefore be made. Indoor mosquito landing rates declined from
0.49 mosquito/man-hour before application to zero at 12 months post-
application using full coverage (reduction 100%) and from 1.29 to
0.16 mosquito/man-hour using selective coverage (reduction 88%).
Outdoor mosquito landing rates declined from 3.79 mosquito/man-
hour before application to 0.03 at 12 months post-application using full
coverage (reduction 99%), and from 0.37 to 0.04 mosquito/man-hour
using selective coverage (reduction 89%). Natural outdoor mosquito
landing rates decreased from 14.4 mosquito/man-hour before application
to 0.04 at 12 months post-application using full coverage (reduction 99%)
and from 7.3 mosquito/man-hour to 0.04 mosquito/man-hour using
selective coverage (reduction 99%). Selective coverage provided a
substantial impact on man-vector contact. The authors recommended that

full coverage should be applied only during the first cycle, with selective
coverage applied during the subsequent cycles. Gandahusada et al.
reported that there were no serious cases of intoxication among the
sprayers (Gandahusada et al., 1984). However, of 203 sprayers, a small
number were hospitalized for observation because of minor complaints,
which might possibly have been associated with exposure.
Barodji et al. measured the efficacy of fenitrotion at 1 g/m2 against
A. maculatus and A. sinensis between 1996 and 1997 (Barodji et al., 1997).
A. maculatus mosquitoes were obtained from Kulonprogo (Yogyakarta)
and A. sinensis from Nias (North Sumatra). The mosquito mortality rate
was recorded at 2 weeks post-application, and then monthly for 6 months.
Against A. maculatus, they found 100% mortality up to 3 months on wood,
2 months on bamboo and 1 month on cement. At 6 months after applica-
tion, mortality of A. maculatus was 63% on wood, 67% on bamboo and 60%
on cement. Against A. sinensis, they found 100% mortality up to 2 months
post-application on wood, and a month on either bamboo or cement.
At month 3, mortality of A. sinensis reached only 7% on all types of
surfaces. Fenitrotion IRS at 1 g/m2 was only really effective against A.
maculatus and A. sinensis on wood surfaces (on bamboo and cement the
duration of lethal activity was unacceptably brief).
Barodji et al. conducted an operational-scale trial of fenitrotion in East
Flores (Lesser Sundas) in 1995 (Barodji et al., 2004c). The local vectors
were A. sundaicus, A. barbirostris, A. flavirostris and A. maculatus. In three
sub-villages in Lewo Bunga, they applied full coverage at 1 g/m2 for one
single cycle in a year, and in three sub-villages in Ebak, they applied
0.5 g/m2 for two cycles with a 6-month interval. Indoor and outdoor
human-landing collection and indoor resting density were measured
every 3 months for 12 months. Direct contact tests were conducted on
wooden and bamboo surfaces. At the 1 g/m2 dosage, at 12-months post-
application, the indoor human-landing rate fell from 15.8 to 0.2 mos-
quito/man-hour (reduction: 99%). Likewise, the outdoor human-landing
rate fell from 19.9 to 0.1 mosquito/man-hour (reduction: 99%). Resting
density decreased from 0.05 mosquito/man-hour to zero (reduction:
100%). At the 0.5 g/m2 dosage, 12 months post-application, the indoor
human-landing rate decreased from 0.92 to 0.25 mosquito/man-hour
(reduction: 73%). The outdoor man-landing rate fell from 1.97 to 0.02 mos-
quito/man-hour (reduction: 99%). The indoor resting density decreased
from 1.7 mosquito/man-hour to zero (reduction: 100%). The 1 g/m2
dosage effectively reduced mosquito density. Direct contact tests showed
that 1 g/m2, at 2 months post-application, achieved 100% mortality on
wooden, but only 70% on bamboo surfaces. Mortality fell to 90% on wood
and 40% on bamboo at 3 months. Effective mortality lasted only 1 month
on bamboo. At 9 months post-first application, the apparent effects upon
SPR in the treated villages were very similar for 1 g/m2 (before applica-
tion: 26%, 35/134 vs. at 9 months post-first application: 9%, 11/123;
p < 0.001) and for 0.5 g/m2 (30%, 38/127 vs. 8%, 10/124; p < 0.001). No
complaints from residents or sprayers were noted.
2.4.4.3.1.10. Malathion Malathion is an organophosphorus insecticide

widely used in malaria control since the 1960s (Najera and Zaim, 2001). It
has low vapour pressure, moderate water solubility and low toxicity
(World Health Organization, 2003d). It has quite a strong and generally
unpleasant odour. The WHO classifies it as a slightly hazardous insecticide
(World Health Organization, 2006b) and recommends a dosage of 2 g/m2,
giving a residual effect of 23 months (World Health Organization, 2007a).
The Indonesian MoH does not recommend this insecticide for IRS against
malaria vectors, but it does recommend it for Aedes control (Departemen
Kesehatan, 2003c, 2010). In general, this insecticide is applied as a quick
knockdown of adult mosquitoes in outbreak settings.
A study in the 1980s explored the application of malathion as IRS in
Jombang (East Java; Martono, 1988). The investigators applied full cover-
age, at 2 g/m2 for one cycle, lasting a year, to 1100 houses. Human landing
and indoor resting densities were measured before application and at
3 months post-application. The indoor human-landing rate fell from 0.6
mosquito/man-hour to 0.06 mosquito/man-hour (reduction: 90%). Like-
wise, the outdoor human-landing rate fell from 4.5 to 0.5 mosquito/man-
hour (reduction: 89%). The morning resting density decreased from 1.3 to
0.4 mosquito/man-hour (reduction: 69%). The SPR dropped significantly
at 3 months post-application (before application: 2.3%, 22/951 vs. after:
0.2%, 2/1015; p < 0.001). Although the authors declared this insecticide to
be very effective, the powerful and unpleasant odour of this chemical
probably explains why the MoH does not recommend it for IRS.
2.4.4.3.1.11. Pirimiphos-methyl Pirimiphos-methyl is an organophospho-

rus insecticide (World Health Organization, 2006i). It is classified by the
WHO as a moderately hazardous chemical (World Health Organization,
2006b). Application of 12 g/m2 gives a residual effect for 23 months
(World Health Organization, 2007a). The Indonesian MoH does not recom-
mended this insecticide for IRS as part of its insecticide rotation cycle
policy, but it does recommend it for Aedes control (Departemen
Kesehatan, 2003c, 2010). Trials were carried out with a 25% WDP formula-
tion at a dosage of 2 g/m2 (Shaw et al., 1979) and with a 50% EC formula-
tion at dosage of 1 g/m2 (Supalin et al., 1979). Shaw et al. reported that the
pirimiphos-methyl maintained better than 70% mortality for about 12
weeks. Supalin et al. reported essentially similar findings.
2.4.4.3.1.12. DDT DDT is the only organochlorine still recommended for

IRS. Other organochlorines, for example, dieldrin, were abandoned due
to relatively high toxicity to humans (Najera and Zaim, 2001). The WHO
classifies it as a moderately hazardous chemical (World Health
Organization, 2006b). A 12 g/m2 application gives a residual effect of
more than 6 months (World Health Organization, 2007a). DDT resistance
has been reported from Indonesia (Bangs et al., 1993; Soerono et al., 1965).
The Indonesian MoH does not recommend this insecticide for any pur-
pose (Departemen Kesehatan, 2003c, 2010). The environmental contami-
nation from DDT, caused by the illegal diversion of the insecticide to
agricultural use (Najera and Zaim, 2001), underpins the governments
prohibition of DDT. The last application of DDT in Indonesia was in 1992
(World Health Organization, 1998). A study in the 1980s (Martono, 1988)
documented modest effects on SPR (3.7% vs. 1.4%; p 0.006), a relatively
modest decrease in indoor human-landing rates (0.4 to 0.1 mosquito/
man-hour) and a sharp increase in outdoor human-landing rates (2.9 to
6.8 mosquito/man-hour), the latter observation being consistent with the
well-known powerfully repellent properties of DDT. In 1982, Gandahu-
sada et al. also reported that the application of DDT had no impact on the
malaria tranmission between treated sites and non-treated sites (5%, 91/
1,807 vs. 6%, 77/1,254; Z-test, p = 0.187) during three years of study (1979-
1981) in South Kalimantan (Gandahusada et al., 1982).
2.4.4.3.2. Cattle shelter indoor residual spraying During the 1980s, inves-
tigators in Indonesia investigated the impact of cattle shelter spraying as a
supplement to IRS of human dwellings. Today, the MoH recommends
cattle shelter IRS (Departemen Kesehatan, 2006a). According to the BHS
(National Institute of Health Research and Development, 2008) in 2007,
9% of Indonesian households raised livestock such as cattle and horses.
One percent of households kept the cattle shelters inside the house and
about 8% kept them outside the house.
Barodji evaluated the impact of cattle shelter spraying on A. aconitus at
Jepara (Central Java) in 1983 and 1984 (Barodji, 1985). Two villages in
Mlonggo sub-district were selected as intervention sites. DDT-resistant
A. aconitus has been reported at those sites. SPR at the intervention sites
was 12% (1516/9509). In the first year, fenitrotion IRS was applied
monthly at 2 g/m2, and in the second year of the study, it was applied
every 2 months. A census was carried out on population homes, cattle and
their shelters. The ratio of people to cattle was 14:1 and the ratio of homes
to shelters was 7:1. Cattle shelters were typically either attached to the
owners home or standing nearby. A. aconitus is characteristically zoo-
philic and occurs in greatest abundance in and around cattle shelters.
Approximately 3000 cattle shelters were sprayed monthly. Barodji found
that within a year, reductions of human-vector contact occurred at human
dwellings; five times lower indoors (from 0.15 to 0.03 mosquito/man-

hour), nine times lower outdoors (from 0.77 to 0.09 mosquito/man-hour)
and eight times lower in cattle shelters (from 9.5 to 1.2 mosquito/man-
hour). However, when the frequency application was reduced from
monthly applications to bimonthly applications, human-vector contact
increased once again among human dwellings becoming four times
higher indoors (from 0.03 to 0.13 mosquito/man-hour), three times higher
outdoors (from 0.09 to 0.29 mosquito/man-hour) and three times higher
in cattle shelters (from 1.2 to 3.5 mosquito/man-hour). They also found
that, following monthly application, SPR fell significantly from baseline
levels (baseline: 15.9%, 1516/9509 vs. monthly: 5.8%, 797/13,724;
p < 0.001). During the bimonthly cycles, SPR increased slightly (monthly:
5.8%, 797/13,724 vs. bimonthly: 7.5%, 869/11,524 vs; p < 0.001). Cattle
shed IRS did not seem to cause A. aconitus to become less zoophilic or
more anthropophilic, that is, to switch its feeding preferences from the
protected cattle to unprotected humans. The proportion of mosquitoes
with animal blood in their gut was not significantly different before
versus after application (92%, 92/100 vs. 87%, 215/248; p 0.165). Con-
tact susceptibility tests of fenitrothion against A. aconitus after 15 applica-
tions showed 100% mortality. Repetitive applications did not decrease
susceptibility of A. aconitus to fenitrothion. Monthly cattle shelter IRS for
12 months brought a saving of 78% of insecticide compared to two cycles
IRS applied in a year (Barodji, 2003). The authors concluded that cattle
shelter IRS could diminish the risk of malaria in areas where A. aconitus
represents an important vector of malaria. Nalim reported similar find-
ings at Banjarnegara (Central Java) in 1985 (Nalim, 1986).
2.4.4.4. Community knowledge

IRS is by its nature invasive upon private citizens, and community support
represents an essential and sometimes hard-won element of success. Sev-
eral studies in Indonesia have explored this dimension of IRS. Saikhu et al.
used secondary data from the BES by the Indonesian National Institute for
Health Research and Development and the Centre of Statistics in 2001
(Saikhu and Gilarsi, 2003). The study surveyed 15,902 people from 4032
households in four districts (Banjarnegara, Kebumen, Jepara and Pekalon-
gan) in Central Java. Only 11% understood that IRS was a tool for malaria
control. No association was found between ignorance of the utility of IRS
and the risk of malaria (OR 0.06; 95% CI 0.95), nor was there any
association between the latter and attitude regarding IRS (OR 1.3, 95%
CI 0.63.0). Four percent of respondents did not want IRS due to its effects
on the home, that is, foul smell, fouling the furniture and fear of toxicity.
The KAP study by Sanjana et al. at Purworejo (Central Java) involved
1000 randomly selected households (Sanjana et al., 2006). Among the 50
villages sampled, 15100% of households had been sprayed in the past
year. Paddy/urban residents reported less spraying activity in the past

year compared to hill/forest residents (10% vs. 30%). Most malaria trans-
mission during the malaria epidemic occurred in the hills and forested
areas. The odds of malaria illness in the past year for houses sprayed with
insecticide within that year were significantly higher than among houses
sprayed more than 1 year ago (OR 1.6, p 0.03). This is not evidence of
the poor efficacy of IRS, but it points instead to a selection bias imposed by
the health authorities who direct their limited resources to the areas at
highest risk. Spray operations were often sporadic in response to ongoing
malaria outbreaks. There was no universal coverage. When asked if
respondents would be willing to pay Rp. 30,000 ( US$ 3) to have their
house sprayed, only 45 respondents (5%) said yes; however, 989 respon-
dents (99%) would agree to have their house sprayed if the service was
offered at no charge. The acceptability of IRS during a period of epidemic
malaria may be at its zenith.
Sekartuti et al. conducted a cross-sectional KAP survey in two malaria
endemic villages in South Lampung in 2003 (Sekartuti, 2003). They sur-
veyed 420 people and only 10 (2%) knew of IRS being used as a malaria
prevention tool. About 95% of participants responded favourably to IRS.
In 2003, Arsunan et al. also documented that 71% of 264 respondents in
Kapoposang Island (Pangkajene, Sulawesi) agreed to re-spraying 2 years
after the last application (Arsunan et al., 2003). Sekartuti et al. also
reported a KAP survey carried out in Banjarnegara (Central Java) in
2004 involving 219 respondents (Sekartuti et al., 2004b). They found that
75% of respondents were aware of the purpose of IRS as a malaria
prevention tool. Over 95% reported that their house had been sprayed.
Sixty-two percent of respondents agreed to place their cattle shelter at
more than 20 m from their dwelling. In 1999, Sukowati et al. documented
that 95% of 99 respondents in Lombok (Lesser Sundas) supported IRS as a
malaria intervention tool (Sukowati et al., 2003). Santoso et al. evaluated a
community participation program in Bintan (Riau Island, Sumatra) in
1991 and described complaints registered after a round of IRS (Santoso
et al., 1992). They documented that 91% of 127 respondents had had their
houses sprayed. Of 127 respondents, 31% complained of headaches and
38% reported negative effects of the insecticide on their furniture.
2.4.5. Malaria surveillance

According to the Indonesian MCP guidelines (Departemen Kesehatan,
2006b), malaria surveillance is needed to support three activities: early
warning, outbreak management and post-outbreak management. Data
collection is started from sub-primary health centres and aggregated by
the upper levels. The monthly transfer of data from the primary health
centres to the district health office is done by hand delivery, fax or email.
The district health offices then use this data to create graphs showing
trends, distribution and minimummaximum case loads. The processing
and analysing of data is conducted at primary health centre level. An
increase in the number of malaria cases, which is more than twofold the
number of cases during the normal period, was designated as the thresh-
old of a malaria warning. Another important aim of such data collection is
the informing of maps of malaria risk. The maps, in turn, inform the
placement of the limited control resources precisely where and when
they are needed. However, in 2007, Elyazar et al. showed that primary
health centres did not have the sufficient capacity to analyse these data
(Elyazar and Rachmat, 2004; Elyazar et al., 2007).
Effective surveillance of malaria in Indonesia requires important chal-
lenges to be overcome. As already described, only 1316% of estimated
clinical malaria cases come with a microscopic or RDT confirmation. In
other words, 8487% of clinical malaria cases are undetected by health
facilities. This leads to the under-reporting of malaria case figures given
by the MoH. The situation is also hampered by the existence of people
with malaria who do not seek malaria treatment (2126%) or people who
treat themselves (1031%). Therefore, the API data reported by district
health offices is unreliable. There is no correction factor of API in their
reports as high proportion of clinically diagnose malaria.
Another problem is the limited coverage of malaria cases treated by
private clinics, physicians and hospitals. The ongoing malaria surveil-
lance used by Indonesias MCP has not accommodated data generated at
those sources. The Indonesian Hospital Reporting System aggregates
malaria data from all hospitals in Indonesia. The system reports the
number of malaria cases without detailing the Plasmodium. The details
are kept by each hospital. To assemble, these data would therefore mean
to connect with over 1300 hospitals across the archipelago. There is no
adjustment of API in the MCP reports to take into account the low
contribution of data from clinics, physicians and hospitals.
2.5. OUTLOOK FOR MALARIA RESEARCH IN INDONESIA
This review summarizes the evidence demonstrating that malaria repre-

sents an important public-health challenge for Indonesia. After China and
India, no other country has more people living at risk of malaria (150220
million; Guerra et al., 2010; Hay et al., 2009). As can be seen by the work of
many presented in this review, the risk and mechanics of infection
sharply vary across the 5000-km archipelago and its many habitats. The
social complexity of Indonesias many distinct cultures, and their high
mobility, imposes further difficulty. The daunting task faced by the orga-
nizations engaging the malaria problem is to place their limited resources
precisely where and when needed, using proven tools, in this fantastically
complex mosaic of risk.
Most malariologists emphasize the locality-specific character of malaria.
In few places is this truer than among the islands of Indonesia. Control
strategy must be tailored to localities, and this largely defines the difficulty
of achieving gains against malaria at a national level. Experts in Jakarta
may be in a poor position to prescribe effective control in, for example, Alor
at the far eastern reaches of the Lesser Sundas archipelago; and health
officers at Alor may lack the technical expertise to develop control strate-
gies effectively suited to their unique transmission dynamics.
The instinct to consider as essential to progress the dissection and
grasp of every nuance of malaria transmission across the many thousands
of settings across Indonesia should be resisted by malaria experts work-
ing the problem. This would perhaps trend towards hopelessness and
abandonment of effort. Research effort is desperately needed to better
inform malaria control and elimination strategies, regardless of who
carries it out: the MoH, Ministry of Science & Technology, local govern-
ments, universities, NGOs, and, ideally, informed and determined local
citizens. The effort at gathering, digesting and summarizing the vast body
of evidence in this chapter produced an appreciation of some conspicuous
gaps in evidence. Most of these tend to reach across the daunting diversity
of transmission dynamics and thus represent likely research aims that
would inform control and elimination strategy, in almost any setting,
with useful evidence. Working to fill in such gaps represents achievable
steps forward for the malaria agenda in Indonesia.
We do not presume to list all such gaps. It is hoped that readers
will identify further gaps in evidence perhaps more relevant to their
individual areas of expertise. Nonetheless, we list here what we consider
to be seven conspicuously useful and practical areas of research endeavour
aimed at better equipping malaria control and elimination in Indonesia.
1. Characterization of antimalarial consumption by both survey instru-

ments and objective observation, especially evaluating the extent of
persisting therapeutic practice engaging chloroquine and sulfadoxine/
pyrimethamine against both P. falciparum and P. vivax malaria in both
the public and private sectors.
2. Assessing the extent of primaquine therapy being applied against both P.
falciparum malaria (gametocytocide) and P. vivax malaria (hypnozoito-
cide), including objective measurements of rates of adherence to the latter.
3. Objective epidemiological measurement of the relative contribution of
the hypnozoite reservoir to the burden of parasitemia in given com-
munities with endemic P. vivax malaria.
4. Randomized, controlled trials assessing the efficacy of primaquine as a

gametocytocide and hypnozoitocide, including the characterization of
G6PD deficiency variant diversity, distribution and relative sensitivity
to primaquine.
5. Randomized, controlled trials assessing the efficacy of ITN or IRS as an
intervention against malaria in hypo- and mesoendemic settings.
6. Prospective hospital-based studies in various endemic settings aimed
at identifying demographic groups at highest risk of severe and com-
plicated malaria.
7. Development and evaluation of surveillance systems linked to geos-
patial mapping systems aimed at focusing control resources and effort
where most needed or most likely to succeed.
Malaria in Indonesia will remain a problem for a span of time that will
extend beyond the active careers of even the youngest physician or scientist
in 2011. Achieving elimination will require advancements that fill the many
gaps in understanding of this menace to the public. The malariologists
responsible for more than 100 years of malaria research in Indonesia sum-
marized in this review provided us a framework of understanding, imper-
fect and incomplete. It falls upon contemporary malariologists to leverage
all of that effort in order to improve this understanding and thereby
achieve greater impacts with smarter interventions against malaria.
ACKNOWLEDGEMENTS
We thank Anja Bibby for proofreading the chapter. We also thank Dr Fred Piel and
Dr Marianne Sinka for inputs and comments on the chapter. The authors also acknowledge
the support of the Eijkman Institute for Molecular Biology, Jakarta, Indonesia.
Author contributions: I. R. F. E. compiled malaria parasite rate data and antimalarial drug
susceptibility test data. I. R. F. E. wrote the first draft of the chapter. J. K. B. and S. I. H.
commented on the final draft of chapter.
Funding: I. R. F. E. is funded by grants from the University of OxfordLi Ka Shing
Foundation Global Health Program and the Oxford Tropical Network. S. I. H. is funded by a
Senior Research Fellowship from the Wellcome Trust (number 079091). J. K. B. is funded by a
grant from the Wellcome Trust (number B9RJIXO). This work forms part of the output of the
Malaria Atlas Project (MAP, http://www.map.ox.ac.uk), principally funded by the
Wellcome Trust, U.K. The funders had no role in study design, data collection and analysis,
decision to publish or preparation of the chapter.
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CHAPTER THREE
The Distribution and Bionomics

of Anopheles Malaria Vector
Mosquitoes in Indonesia
Iqbal R.F. Elyazar*,1, Marianne E. Sinka, Peter W. Gething,
Siti N. Tarmidzi{, Asik Surya{, Rita Kusriastuti{, Winarno{,
J. Kevin Baird*,}, Simon I. Hay, Michael J. Bangs}
*Eijkman-Oxford Clinical Research Unit, Jakarta, Indonesia
Spatial Ecology and Epidemiology Group, Department of Zoology, University of Oxford, Oxford,
United Kingdom
{
Directorate of Vector-Borne Diseases, Indonesian Ministry of Health, Jakarta, Indonesia
}
Centre for Tropical Medicine, Nuffield Department of Medicine, University of Oxford, Oxford,
United Kingdom
}
Public Health and Malaria Control Department, International SOS, PT Freeport Indonesia, Kuala Kencana,
Indonesia
1
Corresponding author: Iqbal RF Elyazar
Contents
1. Introduction 175
2. Assembling a National Database of Anopheles Mosquitoes Susceptible
to Plasmodium spp. Infections, Host Preference, Bionomics and Insecticide
Susceptibility in Indonesia 176
3. Infectivity of Anopheles Mosquitoes to Plasmodium in Indonesia 177
4. The Distribution of Anopheles Malaria Vectors in Indonesia 178
5. Malaria Vectors in Indonesia: Plasmodium spp. Infections, Host Preferences, Larval
and Adult Bionomics and Insecticide Susceptibility 178
5.1 Anopheles (Cellia) aconitus Dnitz 178
5.2 Anopheles (Cellia) balabacensis Baisas 182
5.3 Anopheles (Anopheles) bancroftii Giles 184
5.4 Anopheles (Anopheles) barbirostris van der Wulp 186
5.5 Anopheles (Anopheles) barbumbrosus Strickland & Chowdhury 189
5.6 Anopheles (Cellia) farauti Laveran species complex 191
5.7 Anopheles (Cellia) flavirostris (Ludlow) 193
5.8 Anopheles (Cellia) karwari James 195
5.9 Anopheles (Cellia) kochi Dnitz 197
5.10 Anopheles (Cellia) koliensis Owen 199
5.11 Anopheles (Cellia) leucosphyrus Dnitz 201
5.12 Anopheles (Cellia) maculatus Theobald species subgroup 203
5.13 Anopheles (Anopheles) nigerrimus Giles 206
5.14 Anopheles (Cellia) parangensis (Ludlow) 208
5.15 Anopheles (Cellia) punctulatus Dnitz 209
Advances in Parasitology, Volume 83 # 2013 Elsevier Ltd 173

ISSN 0065-308X All rights reserved.
http://dx.doi.org/10.1016/B978-0-12-407705-8.00003-3
5.16 Anopheles (Anopheles) sinensis Wiedemann 211

5.17 Anopheles (Cellia) subpictus Grassi species complex 213
5.18 Anopheles (Cellia) sundaicus Rodenwaldt species complex 216
5.19 Anopheles (Cellia) tessellatus Theobald 219
5.20 Anopheles (Cellia) vagus Dnitz 221
6. Anopheles Susceptibility to Insecticides 238
6.1 Anopheles aconitus 239
6.2 Anopheles barbirostris 240
6.3 Anopheles farauti s.l. 240
6.4 Anopheles kochi 240
6.5 Anopheles koliensis 240
6.6 Anopheles maculatus 241
6.7 Anopheles subpictus s.l. 241
6.8 Anopheles sundaicus s.l. 241
6.9 Anopheles vagus 242
7. Outlook for Indonesian Challenges to Malaria Vector Control 242
8. Conclusions 244
Acknowledgements 244
References 245
Abstract
Malaria remains one of the greatest human health burdens in Indonesia. Although
Indonesia has a long and renowned history in the early research and discoveries of
malaria and subsequently in the successful use of environmental control methods to
combat the vector, much remains unknown about many of these mosquito species.
There are also significant gaps in the existing knowledge on the transmission epidemi-
ology of malaria, most notably in the highly malarious eastern half of the archipelago.
These compound the difficulty of developing targeted and effective control measures.
The sheer complexity and number of malaria vectors in the country are daunting. The
difficult task of summarizing the available information for each species and/or species
complex is compounded by the patchiness of the data: while relatively plentiful in one
area or region, it can also be completely lacking in others. Compared to many other
countries in the Oriental and Australasian biogeographical regions, only scant informa-
tion on vector bionomics and response to chemical measures is available in Indonesia.
That information is often either decades old, geographically patchy or completely lac-
king. Additionally, a large number of information sources are published in Dutch or
Indonesian language and therefore less accessible. This review aims to present an
updated overview of the known distribution and bionomics of the 20 confirmed malaria
vector species or species complexes regarded as either primary or secondary (inciden-
tal) malaria vectors within Indonesia. This chapter is not an exhaustive review of each of
these species. No attempt is made to specifically discuss or resolve the taxonomic
record of listed species in this document, while recognizing the ever evolving revisions
in the systematics of species groups and complexes. A review of past and current status
of insecticide susceptibility of eight vector species of malaria is also provided.
Anopheles Malaria Vector Mosquitoes in Indonesia 175
1. INTRODUCTION
An integrated approach to interventions against mosquito vectors of
malaria has become increasingly important for those nations aiming for elim-
ination of malaria transmission or a significant reduction of infection risk
(World Health Organization, 2007b). Such evidence-based strategies for
vector control require detailed knowledge of the identity, distribution
and bionomics of the primary malaria vectors within the target area
(Zahar, 1994). Recent work by the Malaria Atlas Project (www.map.ox.
ac.uk), defining the spatial distributions of the dominant vector species of
human malaria worldwide (Hay et al., 2010), has begun to address the need
for geographical species-specific information, including a detailed review
of the bionomics of these primary vectors in the Asia-Pacific region (Hay
et al., 2010; Sinka et al., 2011). On a national scale, however, and despite
a long history of study of the important Anopheles, no contemporary
systematic review of this mosquito genus has been undertaken in Indonesia.
This chapter, therefore, closely examines both the past and current state
of knowledge of many of the anopheline malaria vectors present in this
environmentally diverse archipelago.
The main arsenal for adult mosquito control consists of applying long-
lasting, residual insecticides, either on bednets or applied/sprayed directly
onto the walls within human dwellings (World Health Organization,
2010). Unfortunately, the continuous exposure of mosquitoes to these
chemicals has resulted in measurable physiological resistance, and in some
instances significant behavioural avoidance amongst a number of studied
malaria vectors species (Najera and Zaim, 2003). Physiological resistance
refers to the ability of a mosquito to tolerate doses of insecticide which
would normally prove lethal to the majority (>98%) of individuals in a
local population of the same species, whilst behavioural avoidance relates
to the tendency of mosquitoes to avoid contact with the insecticide-
treated surface, either as a result of contact irritancy, spatially active
repellency, or as a combination of both (World Health Organization,
1963). Monitoring the insecticide-resistance profile of a population
of medically important Anopheles species is essential for better design
and implementation of an evidence-based vector control policy (World
Health Organization, 1992). Until now, no contemporary review of the
insecticide-resistance patterns amongst Indonesian anophelines vectors
has been published.
2. ASSEMBLING A NATIONAL DATABASE OF ANOPHELES

MOSQUITOES SUSCEPTIBLE TO PLASMODIUM SPP.
INFECTIONS, HOST PREFERENCE, BIONOMICS AND
INSECTICIDE SUSCEPTIBILITY IN INDONESIA
A systematic search and review of published and unpublished entomo-
logical literature from online and library sources was used to assemble a data-
base of the distribution of Indonesian Anopheles, their natural infection with
human malaria parasites, bionomics and frequency of insecticide resistance.
Visits were made to university and Ministry of Health library resources to
search for more obscure or offline/unpublished information. Searches were
completed on 31 December 2011. Once a relevant data source was identi-
fied, information was extracted into an Excel worksheet including an unique
identification record of each source, year of source, location (region, island,
province, district, sub-district and specific locality such as village), species
and species identification method used (morphological and molecular
based), physiological measures (mating status, parity, age-grading, blood-
feeding preference, etc.), the sporozoite and oocyst rate (using midgut
and salivary gland dissections, circumsporozoite immunological assays and
molecular-based tests). Based on the presence of oocysts and/or sporozoites,
each record was classified into two susceptibility categories: infected (mid-
gut oocysts) or infective (presence of salivary gland sporozoites). When
a mosquito was found to be infected but not necessarily infectious, it was
classified as a suspect vector, whereas those identified as infectious were
classified as an incriminated or confirmed malaria vector (Swellengrebel
et al., 1919; Warrell and Gilles, 2002). Additional data recorded for the
number found positive for the presence of human blood (i.e. human blood
index, HBI) were also searched. Larval and adult bionomic data were
included focusing on blood-feeding behaviour and activity patterns, pre-
dominant resting sites of adults and aquatic habitats for immature stages.
These data were stratified into western and eastern sectors of the Indonesian
archipelago for descriptive purposes. Western and eastern sectors of Indone-
sia are biogeographically distinct regions of the archipelago, demarked by a
series of different transecting lines including Wallaces and Webers Lines
near the centre of the nation (surrounding the island of Sulawesi; shown
in Figs. 3.13.21; Wallace, 1863; Weber, 1890).
Finally, a database of the vector insecticide susceptibility status was
assembled identifying those sources that reported an insecticide susceptibility
test, including the method (bioassay, biochemical, molecular), the insecti-

cide (active ingredient) tested, doses (percent concentrations) used, number
of mosquitoes assayed and the mosquito mortality following exposure. The
insecticides in the database included the six currently recommended for
indoor residual spraying by the Indonesian Vector Control Program
(VCP), primarily pyrethroid and carbamate class chemicals (Departemen
Kesehatan, 2010), plus other insecticide classes used historically such as
organophosphates and organochlorine compounds.
3. INFECTIVITY OF ANOPHELES MOSQUITOES

TO PLASMODIUM IN INDONESIA
From the reviewed and compiled literature, a total of 74 sources were
used to extract 1266 records reporting Plasmodium spp. infections (sporozo-
ites or oocyst stages) for 29 Anopheles species found in Indonesia between
1919 and 2010 (Table 3.1). These data indicate the presence of 20 Anopheles
species confirmed as primary or secondary (incidental) malaria vectors in the
country. No records of naturally occurring infectious stages (sporozoites)
were found for the remaining nine species, despite four species, including
Anopheles annularis, Anopheles hyrcanus, Anopheles indefinitus and Anopheles
umbrosus being reported as suspected vectors in Indonesia (Table 3.2).
The confirmed malaria vectors are not uniformly distributed across the
archipelago. Twelve species are located in the western portion of the country
and 13 species in the eastern region of Indonesia with some overlap across
both areas: Anopheles balabacensis, Anopheles flavirostris, Anopheles nigerrimus,
Anopheles subpictus and Anopheles sundaicus were reported as natural vectors
in both regions. The distribution of malaria vectors amongst the main islands
is also not uniform (Fig. 3.1), with Java and Sulawesi appearing to contain
the greatest number of reported malaria vectors (eight species), followed by
Sumatra (six species), Papua (at least five species) and the Lesser Sundas archi-
pelago (five species). Only two species were confirmed as malaria vectors in
Kalimantan. No data on the infectivity of Anopheles species on Maluku were
identified but at least two species present in the island chain (Anopheles farauti
and Anopheles punctulatus) are known to be efficient vectors elsewhere (Papua).
A map of the distribution of the Anopheles malaria vectors in Indonesia is
provided (Fig. 3.1) which illustrates species by principal islands or island
groups from Sumatra in the west to Papua in the east. Sulawesi and the Lesser
Sundas archipelago lie in the centre of Indonesia and are between two major
zoogeographical lines (Wallaces and Webers Lines drawn to demark the
Oriental and Australasia Regions) based on unique and overlapping fauna

distributions in the region.
4. THE DISTRIBUTION OF ANOPHELES MALARIA

VECTORS IN INDONESIA
A total of 259 sources, published from 1917 to 2011, have docu-
mented the presence of 20 Anopheles malaria vector species in Indonesia rep-
resenting 755 independent sites. A greater number of sites in western
Indonesia reported vectors present than in eastern Indonesia (66% vs.
34%), no doubt reflecting the relatively higher number of investigations
in the far more densely populated western sector. Over the seven main
islands in Indonesia, the greatest number of sites where vectors have been
found were on Java (41%; 311 sites) with the least found on Papua (4%;
32 sites). Anopheles vagus was reported from the greatest number of indepen-
dent sites (46%; 349 sites) across Indonesia, while Anopheles bancroftii was the
most restricted (1%; 7 sites in Papua, 1 in Maluku).
For each species, an individual map has also been generated indicating
geo-referenced locations of occurrence and where malaria infectious mos-
quitoes have been recorded (Figs. 3.23.21). These records were then over-
laid to the Plasmodium falciparum malaria endemicity map in Indonesia that
was produced in an earlier publication (Elyazar et al., 2011a). The endemic-
ity maps defined five land categories with areas colour shaded accordingly:
no malaria risk area (light grey, where PfAPI 0 per 1000 pa), unstable
transmission risk area (medium grey, where PfAPI < 0.1 per 1000 pa),
low risk area (light red, PfPR210 < 5%), intermediate risk area (medium
red, 5% < PfPR210 < 40%) and high risk area (dark red, PfPR210 > 40%).
Using these geo-referenced records and endemicity map, distribution maps
were produced for each species or species complex. The presentation of spe-
cies is alphabetical rather than geographical or by taxonomic affinities.
5. MALARIA VECTORS IN INDONESIA: PLASMODIUM

SPP. INFECTIONS, HOST PREFERENCES, LARVAL
AND ADULT BIONOMICS AND INSECTICIDE
SUSCEPTIBILITY
5.1. Anopheles (Cellia) aconitus Dnitz
An. aconitus is a member of the Funestus Group (Garros et al., 2005). This
species is broadly distributed throughout the Indonesian archipelago,
Figure 3.1 A map of the distribution of primary Anopheles malaria vectors in Indonesia.
although relative densities and frequency vary dramatically. A total of 132

sources reported the presence of An. aconitus at 325 independent sites
(Fig. 3.2). The species has been most commonly reported from Java (197
sites) and extends across the archipelago as far east as Timor-Leste and the
Maluku Islands, but it seems absent from Papua (the Indonesian half of
New Guinea Island). Using an enzyme-linked immunosorbent assay
(ELISA) to detect the parasite circumsporozoite protein, Barodji et al.
(2007) found only one specimen amongst 1432 tested in Central Java having
malaria (P. falciparum) sporozoites. Over a 20-year period, the U.S. Naval
Medical Research Unit No. 2 (NAMRU-2) in Jakarta detected sporozoite
(P. falciparum and Plasmodium vivax) positive An. aconitus only from Central
Java Province (Bangs and Rusmiarto, 2007). No other infective specimens
have been reported from the other main islands. This species is reputed to be
a major vector on Java, but generally only when present in high human-
biting densities (Kirnowardoyo, 1988).
The adult females are predominantly zoophilic, with a greater presence
in cattle and other outdoor animal shelters than human habitations (Barodji,
1983a; Barodji et al., 1992; Chow et al., 1959; Joshi et al., 1977; Mardiana
et al., 2005; Yunianto et al., 2004). The combined proportion of mosquitoes
that contained human blood resting in cattle shelters was 2.9% (94/3185)
(Chow et al., 1959; Joshi et al., 1977; Noerhadi, 1960; World Health
Organization and Vector Biology and Control Research Unit 2 Subunit
Figure 3.2 Anopheles aconitus distribution in Indonesia. The blue stars indicate the
records of infectious An. aconitus mosquitoes found. The yellow dots show 325 records
of occurrence for this species between 1917 and 2011. Areas were defined as no risk
(light grey, where PfAPI 0 per 1000 pa), unstable transmission (medium grey, where
PfAPI < 0.1 per 1000 pa), low risk (light red, PfPR210 5%), intermediate risk (medium
red, 5% < PfPR210 < 40%) and high risk (dark red, PfPR210 40%) (Elyazar et al.,
2011a). The database of distribution of An. aconitus in Indonesia was acquired from
the references: Adrial (2003), Adrial and Harminarti (2005), Adrial et al. (2000), Alfiah
et al. (2008), Atmosoedjono et al. (1993), Atmosoedjono et al. (1975), Bang et al. (1982),
Barbara et al. (2011), Barodji (1983b,c), Barodji (1986), Barodji (2003), Barodji et al.
(2003), Barodji et al. (1984a), Barodji et al. (2007), Barodji et al. (1986a), Barodji et al.
(1992), Barodji et al. (1989a), Barodji et al. (1984b), Barodji et al. (1986b), Barodji et al.
(1998/1999), Barodji and Supratman (1983), Barodji et al. (1989b), Blondine et al. (2000),
Boesri et al. (1996a), Boesri et al. (2004), Boesri and Boewono (2006), Boewono and Nalim
(1989, 1991), Boewono et al. (1991), Boewono and Ristiyanto (2004, 2005), Boewono
et al. (2005), Brug and Bonne-Wepster (1947), Buono (1987), Citroen (1917), Dasuki and
Supratman (2005), Garjito et al. (2004b), Hadi et al. (2006), Hafni (2005), Handayani
and Darwin (2006), Hasan (2006), Hoedojo (1992, 1995), Idris-Idram et al. (1998/1999),
Ikawati et al. (2006), Ikawati et al. (2004), Isfarain and Santiyo (1981), Jastal et al.
(2002), Jastal et al. (2001), Kaneko et al (1987), Kazwaini and Martini. (2006),
Kirnowardoyo (1977), Kirnowardoyo and Supalin (1982), Kirnowardoyo and Supalin
(1986), Kirnowardoyo and Yoga (1987), Kurihara (1978), Lee et al. (1984), Lestari et al.
(2000), Lien et al. (1975), Mangkoewinoto (1919), Mardiana et al. (2002), Mardiana and
Sukana (2005), Mardiana et al. (2005), Mardihusodo et al. (1988), Marjiyo (1996),
Martono (1988a,b), Marwoto et al. (1992a), Munif (1990, 1994, 2004), Munif et al.
(2007), Munif et al. (2003), Munif et al. (1994), Nalim (1980), Nalim (1980/1981), 1985,
1986, Nalim and Boewono (1987), Nalim et al. (2000), Nalim and Tribuwono (1983),
Ndoen et al. (2010), Noor (2002), Ompusunggu et al. (2006), Ompusunggu et al.
(1994a), Pranoto and Munif (1993), Pranoto (1989), Pribadi et al. (1985), Raharjo et al.
(2007), Raharjo et al. (2006), Ramadhani et al. (2005), Saleh (2002), Schuurman and
Huinink (1929), Self et al. (1976), Sigit and Kesumawati (1988), Soekirno et al. (2006a),
Semarang, 1978), while those captured in human settlements was only

slightly higher at 6.7% (1004/14,811) (Chow et al., 1959; Garret-Jones,
1964; Joshi et al., 1977; Sundararaman et al., 1957; Walch and Sardjito,
1928; World Health Organization and Vector Biology and Control
Research Unit 2 Subunit Semarang, 1978) (Table 3.3). A stronger
exophagic (outdoor biting/blood feeding) habit is commonly reported in
Java (Barodji et al., 1992; Boesri and Boewono, 2006; Chow et al., 1959;
Ikawati et al., 2004; Joshi et al., 1977; Kirnowardoyo, 1977; Munif,
2004; Munif et al., 2007; Yunianto et al., 2002, 2004), whereas a stronger
endophagic (indoor biting) behaviour has been shown along the southern
coastal zone of western Java (Stoops et al., 2009b) and West Sumatra Prov-
ince (Adrial, 2003). Females typically reach their peak blood-feeding activity
in the second quarter of the night (Barodji et al., 2007; Boesri and Boewono,
2006; Joshi et al., 1977; Stoops et al., 2009b), after which blood-fed females
are generally found resting outdoors (Alfiah et al., 2008; Barodji et al., 1992,
2007; Boesri and Boewono, 2006; Boewono and Ristiyanto, 2005;
Boewono et al., 1991; Chow et al., 1959; Joshi et al., 1977;
Kirnowardoyo, 1977; Munif et al., 2007; Yunianto et al., 2004) in shaded
animal shelters (Boewono et al., 1991; Chow et al., 1959; Joshi et al., 1977;
Kirnowardoyo, 1977; Munif et al., 2007), rock crevices (Alfiah et al., 2008),
earthen pits (Alfiah et al., 2008) and river banks (Boesri and Boewono, 2006)
to complete their gonotrophic cycle.
The characteristic larval habitats of An. aconitus have been comprehen-
sively described in Indonesia. Larvae are most commonly found in sunlit,
exclusively fresh water, often clear in appearance, stagnant or slow flowing
(Takken et al., 1990) and either natural- or man-made habitats (Table 3.4). Nat-
ural water collections include marshes (Sudomo et al., 2010; Swellengrebel and
Swellengrebel-de Graaf, 1919a), streams (Mangkoewinoto, 1919; Stoops et al.,
Soekirno et al. (2006b), Stoops et al. (2009a), Stoops et al. (2008), Stoops et al. (2009b),
Sudomo et al. (2010), Sukowati et al. (2001), Sundararaman et al. (1957), Suparno
(1983), Susana (2005), Suwarto et al. (1987), Suwasono et al. (1993), Swellengrebel
(1921), Swellengrebel and Rodenwaldt (1932), Swellengrebel and Swellengrebel-de Graaf
(1920), Syafruddin et al. (2010), Tarore (2010), Tativ and Udin (2006), Trenggono (1985),
Van Hell (1952), Vector Biology and Control Research Unit (1979b), Verdrager and
Arwati (1975), Widiarti (2005), Widiarti et al. (2005a), Widiarti et al. (2005b), Widiarti
et al. (2001), Widiastuti et al. (2006), Widjaya et al. (2006), Widyastuti et al. (2003),
World Health Organization and Vector Biology and Control Research Unit 2 Semarang
(1977), Yoga (1991), Yudhastuti (2009), Yunianto (2002), Yunianto et al. (2002) and
Yunianto et al. (2004).
2007; Swellengrebel and Swellengrebel-de Graaf, 1919a) and river beds (Boesri
and Boewono, 2006; Boewono and Ristiyanto, 2005; Mangkoewinoto, 1919;
Swellengrebel, 1916) and man-made sources most commonly include rice
fields (Adrial, 2003, 2008; Boesri and Boewono, 2006; Boesri et al., 1996b;
Joshi et al., 1977; Mangkoewinoto, 1919; Munif et al., 2007; Ndoen et al.,
2010; Stoops et al., 2007, 2008; Sundararaman et al., 1957; Swellengrebel
and Swellengrebel-de Graaf, 1919a), fish ponds (Adrial, 2008; Swellengrebel
and Swellengrebel-de Graaf, 1919a) and irrigation ditches (Boesri and
Boewono, 2006; Joshi et al., 1977; Mangkoewinoto, 1919; Munif et al.,
2007). A positive correlation between An. aconitus larval densities and
phase of rice production has been observed with larval peak abundance occur-
ring early in the growing season, around six weeks after rice planting
(Kirnowardoyo, 1988; Munif et al., 2007). This species is widely dispersed
in the environment and can be found from the coastal plain (Ndoen et al.,
2010; Stoops et al., 2007) to hilly areas (Joshi et al., 1977; Mangkoewinoto,
1919; Ndoen et al., 2010; Soemarlan and Gandahusada, 1990; Stoops et al.,
2007; Sundararaman et al., 1957) up to altitudes of 1000 m above sea level
(asl) wherever suitable larval habitats exist (Sundararaman et al., 1957).
5.2. Anopheles (Cellia) balabacensis Baisas

An. balabacensis is a member of the Leucosphyrus Subgroup, within the
Leucosphyrus Complex (Sallum et al., 2005), a subgroup which includes
several very important vectors of human malaria in forest fringe areas of
Southeast Asia, including the Southeast Asian mainland, Philippine Islands,
Brunei, Malaysian Borneo and Indonesia (Sinka et al., 2011). Thirty-four
sources reported the presence of An. balabacensis from 43 independent sites
on Java, Kalimantan, Sulawesi and Lesser Sundas with this species was most
commonly reported from Java (30 sites) (Fig. 3.3). An. balabacensis has been
found infected with P. falciparum sporozoites in Kalimantan (Harbach et al.,
1987). Both P. falciparum and P. vivax infections were also detected in East
(Kenangan) and South Kalimantan (Salaman) and Central Java (Magelang
and Purworejo [Menoreh Hills]) (Bangs and Rusmiarto, 2007). The pres-
ence of P. vivax sporozoites has also been reported from Central Java
(Adrial et al., 2000).
The degree of anthropophily amongst female An. balabacensis appears to
depend on location. Low levels of anthropophilic behaviour have been
observed in hilly areas of Central Java (Alfiah et al., 2008), while in the
mountainous areas of Lombok Island in the Lesser Sundas a high degree
Figure 3.3 Anopheles balabacensis distribution in Indonesia. The blue stars indicate
the records of infectious An. balabacensis mosquitoes found. The yellow dots
show 43 records of occurrence for this species between 1987 and 2010. Areas were
defined as no risk (light grey, where PfAPI 0 per 1000 pa), unstable transmission
(medium grey, where PfAPI < 0.1 per 1000 pa), low risk (light red, PfPR210 5%),
intermediate risk (medium red, 5% < Pf PR210 < 40%) and high risk (dark red,
PfPR210 40%) (Elyazar et al., 2011a). The database of distribution of An. balabacensis
in Indonesia was acquired from the references: Adrial et al. (2000), Alfiah et al. (2008),
Aprianto (2002), Ariati (2004), Barodji et al. (2003), Barodji and Sularto (1993), Boesri et al.
(2004), Boewono and Ristiyanto (2005), Buono (1987), Effendi (2002), Handayani and
Darwin (2006), Harbach et al. (1987), Ikawati et al. (2006), Ikawati et al. (2004), Lestari
et al. (2000), Maekawa et al. (2009a), Maekawa et al. (2009b), Marjiyo (1996), Noor
(2002), Pranoto and Munif (1993), Raharjo et al. (2007), Santoso (2002), Sukmono
(2002), Sukowati et al. (1987), Susana (2005), Suwasono et al. (1997), Suwasono et al.
(1993), Syafruddin et al. (2010), Tarore (2010), Ustiawan and Hariastuti (2007),
Wardana (2010), Widiastuti et al. (2006) and Yunianto et al. (2002).
of anthropophily was noted (Maekawa et al., 2009b) (Table 3.3). Females

have been reported to mostly bite outdoors in Central Java (Boewono
and Ristiyanto, 2005; Ikawati et al., 2006; Suwasono et al., 1993, 1997;
Yunianto et al., 2002) and Lesser Sundas (Maekawa et al., 2009b), and
mostly feeding indoors in eastern Kalimantan (White, 1983). The feeding
activity also varies by location with peak biting normally occurring during
the second quarter of the night in Java and Lesser Sundas (Adrial, 2000;
Adrial et al., 2000; Barodji et al., 2003; Harbach et al., 1987; Ikawati
et al., 2006; Kirnowardoyo, 1988; Lestari et al., 2007; Maekawa et al.,
2009b; Raharjo et al., 2007; Sukowati et al., 1987; Suwasono et al.,
1993, 1997; Ustiawan and Hariastuti, 2007; Yunianto et al., 2002) and in the
third quarter of the night in Kalimantan (Boewono and Ristiyanto, 2005;
Kirnowardoyo, 1988; White, 1983). After blood feeding, An. balabacensis
generally exits houses soon afterwards to rest outdoors (Alfiah et al., 2008;
Barodji et al., 2003; Lestari et al., 2007) in shaded locations such as cattle shel-
ters (Boesri and Boewono, 2006; Boewono and Ristiyanto, 2005; Ikawati
et al., 2006; Lestari et al., 2007; Widiastuti et al., 2006), under trees
(Alfiah et al., 2008; Boewono and Ristiyanto, 2005; Harbach et al., 1987;
Kirnowardoyo, 1991; Sukowati et al., 1987; Suwasono et al., 1993;
Widiastuti et al., 2006; Yunianto et al., 2002), on embankments at heights
up to 1 m above ground level (Alfiah et al., 2008; Boewono and Ristiyanto,
2005; Lestari et al., 2007) and inside ground pits (Alfiah et al., 2008).
An. balabacensis larvae are found almost exclusively in shaded habitats
containing fresh, often clear water (Takken et al., 1990) in both natural- and
man-made habitats (Table 3.4) including stream-side rock pools
(Kirnowardoyo, 1988; Maekawa et al., 2009a; Pranoto and Munif, 1993;
White, 1983), pools found under shrubs or low trees (Boewono and
Ristiyanto, 2005; Kirnowardoyo, 1988; Lestari et al., 2007; Pranoto and
Munif, 1993; Raharjo et al., 2007; White, 1983; Yunianto et al., 2002), river
banks (Lestari et al., 2007; Suwasono et al., 1993), puddles, muddy (turbid) ani-
mal wallows, hoof prints and tyre tracks. This species is usually found associated
with hilly, forested terrain (Lestari et al., 2007; Pranoto and Munif, 1993;
Suwasono et al., 1993, 1997; White, 1983) up to 700 m asl (Suwasono
et al., 1997).
5.3. Anopheles (Anopheles) bancroftii Giles

An. bancroftii was reported from only seven sources and at only eight inde-
pendent sites from eastern Indonesia (Fig. 3.4): one site in Seram Island,
Maluku and seven sites in Papua (New Guinea Island). Five of the six ref-
erences were published before the 1960s. The single contemporary source
documented its presence in Jayapura, Papua in 2008 (Yamtama et al., 2008)
and An. bancroftii has also been encountered, but infrequently, in human-
landing collections in Timika, southern Papua (Bangs, Personal
communication, 2012). An. bancroftii was found in unusually high abun-
dance during a 1-year study in the late 1920s in Tanah Merah, in a remote
jungle environment in southern Papua. Seventy percent of approximately
10,100 collected Anopheles mosquitoes were morphologically identified as
An. bancroftii. In this high vector density area, this species was found infected
Figure 3.4 Anopheles bancroftii distribution in Indonesia. The blue stars indicate the
records of infectious An. bancroftii mosquitoes found. The yellow dots show eight
records of occurrence for this species between 1929 and 2008. Areas were defined
as no risk (light grey, where PfAPI 0 per 1000 pa), unstable transmission (medium grey,
where PfAPI < 0.1 per 1000 pa), low risk (light red, PfPR210 5%), intermediate risk
(medium red, 5% < PfPR210 < 40%) and high risk (dark red, PfPR210 40%) (Elyazar
et al., 2011a). The database of distribution of An. bancroftii in Indonesia was acquired
from the references: Brug and Bonne-Wepster (1947), De Rook (1929), Elsbach (1938),
Swellengrebel and Rodenwaldt (1932), Van den Assem (1959) and Yamtama et al. (2008).
with malaria oocysts (3%, 29/1199) (De Rook, 1929). The role of
An. bancroftii in malaria transmission has been confirmed in Papua with
the identification of two mosquitoes harbouring malaria sporozoites
amongst 982 dissected in Merauke in 1957 (Van den Assem and Bonne-
Wepster, 1964). Likewise, it has been confirmed a malaria vector in the
neighbouring country of Papua New Guinea (PNG) that shares a border
with Papua, Indonesia (Cooper et al., 2009). No infective An. bancroftii have
been reported from Maluku (Table 3.2). This species has not been consid-
ered a very important malaria vector (Swellengrebel and Rodenwaldt, 1932)
despite reports of high human blood indices from specimens captured on a
bednet (Walch and Sardjito, 1928) (Table 3.3). It also appears to be partially
endophilic, with Van den Assem reporting the presence of many blood-fed
females resting inside huts in southern Papua yet none having advanced
ovarian development (Van den Assem, 1959), suggesting that females
likely leave their daytime indoor resting site the following evening post
blood meal.
Table 3.4 shows gravid females and immature stages of An. bancroftii
prefer shaded habitats with fresh, clear and still to slow running water
(Russell et al., 1946). Larvae are typically found in natural habitats, such
as marshes (Koesoemowinangoen, 1953), pools associated with creeks and
rivers (Taylor, 1943), ground pools (Taylor, 1943) or man-made habitats
including heavily shaded irrigation ditches (Koesoemowinangoen, 1953).
5.4. Anopheles (Anopheles) barbirostris van der Wulp

An. barbirostris is a member of the Barbirostris Group (Sinka et al., 2011),
made up of at least 12 species. It is a taxonomically complex assemblage that
is broadly distributed throughout the Indonesian archipelago and much of
south and Southeast Asia. An. barbirostris is currently regarded as a complex
of three to five sibling species with unclear distributions and vector status in
Southeast Asia (Paredes-Esquivel et al., 2009). In Indonesia, 119 sources have
reported the presence of An. barbirostris at 330 independent sites and it was
commonly reported from Java (140 sites), Sumatra (74 sites) and Sulawesi
(55 sites) (Fig. 3.5). The species complex has a wide distribution, extending
from Sumatra, Java, Bali, Kalimantan, Sulawesi and throughout the Lesser
Sunda Island chain to Timor (OConnor and Sopa, 1981). An. barbirostris
has been documented in Maluku (Buru Island) but no reliable/confirmed
records of its presence in Papua (New Guinea) have been found.
An. barbirostris is medically important (malaria and filariasis) in the eastern
part of Indonesia and Sulawesi. The role of An. barbirostris as a malaria vector
was first reported in 1939 by Machsoes who examined 1041 mosquitoes in
South Sulawesi and found 30 (2.9%) with sporozoites (Machsoes, 1939). In
the early 1990s, Marwoto et al. (2002), Marwoto et al. (1992a) and Sukowati
et al. (2001) confirmed the infection of An. barbirostris with both P. falciparum
and P. vivax from specimens collected in the Lesser Sunda Island group
(Lombok and Flores) and northern Sulawesi. Both P. falciparum and
P. vivax infections were also detected in northern Sulawesi (Meras and
Tomohon), Flores (Korowuru and Tilang) and Adonara Island in the eastern
Lesser Sundas (Bangs and Rusmiarto, 2007). Cooper et al. (2010) also
detected sporozoite infective mosquitoes in neighbouring Timor-Leste
(Timor Island). This species complex has not been incriminated as a malaria
vector outside of Sulawesi and Lesser Sunda Island chain. In addition, this
species is an important vector of lymphatic filariasis in Sulawesi (Brugia
malayi) and eastern Lesser Sundas (Brugia timori) (Lim et al., 1985). Although
An. barbirostis is commonly found in Sumatra and Java, the most plausible
Figure 3.5 Anopheles barbirostris distribution in Indonesia. The blue stars indicate the
records of infectious An. barbirostris mosquitoes found. The yellow dots show 330 records
of occurrence for this species between 1918 and 2011. Areas were defined as no risk (light
grey, where PfAPI 0 per 1000 pa), unstable transmission (medium grey, where PfAPI < 0.1
per 1000 pa), low risk (light red, PfPR210 5%), intermediate risk (medium red, 5% <
PfPR210 < 40%) and high risk (dark red, PfPR210 > 40%) (Elyazar et al., 2011a). The database
of distribution of An. barbirostris in Indonesia was acquired from the references: Adrial
(2003, 2008), Adrial and Harminarti (2005), Adrial et al. (2000), Alfiah et al. (2008),
Atmosoedjono et al. (1993), Atmosoedjono et al. (1975), Bahang et al. (1981), Barbara et al.
(2011), Barodji et al. (2003), Barodji et al. (2007), Barodji et al. (1992), Barodji et al. (2004a),
Barodji et al. (2004b), Barodji et al. (1994), Barodji et al. (1998/1999), Barodji et al. (1996),
Blondine et al. (1994), Boesri (1994b), Boesri et al. (2004), Boewono et al. (1997b), Boewono
and Ristiyanto (2004, 2005), Brug (1931), Brug and Bonne-Wepster (1947), Buono, 1987,
Collins et al. (1979), Dasuki and Supratman (2005), Dharma et al. (2004), Djenal et al.
(1987), Fryauff et al. (1997), Gandahusada (1979), Garjito et al. (2004a), Garjito et al.
(2004b), Gundelfinger et al. (1975), Handayani and Darwin (2006), Hasan (2006), Idris-
Idram et al. (2002), Idris-Idram et al. (1998/1999), Idris et al. (2002), Ikawati et al. (2006),
Ikawati et al. (2004), Isfarain and Santiyo (1981), Iyana (1992), Jastal et al. (2002), Jastal
et al. (2003), Kaneko et al. (1987), Kazwaini and Martini (2006), Kurihara (1978), Lee et al.
(1983), Lee et al. (1984), Lestari et al. (2000), Lien et al. (1975), Maekawa et al. (2009a),
Maekawa et al. (2009b), Mangkoewinoto (1919), Mardiana et al. (2002), Mardiana and
Sukana (2005), Mardiana et al. (2005), Marjiyo (1996), Marwoto (1995), Marwoto et al.
(2002), Marwoto et al. (1992a), Munif (1990, 1994, 2004), Munif et al. (2007), Munif et al.
(2003), Nalim (1980a,b), Nalim (1982), Nalim (1985), Nalim and Boewono (1987), Nalim
et al. (2000), Nalim and Tribuwono (1983), Ndoen et al. (2010), Noor (2002), Nurdin et al.
(2003), Ompusunggu et al. (2006), Ompusunggu et al. (1994a), Partono et al. (1973), Priadi
et al. (1991), Raharjo et al. (2007), Raharjo et al. (2006), Ramadhani et al. (2005),
Schuurman and Huinink (1929), Self et al. (1976), Shinta et al. (2003), Sigit and
Kesumawati (1988), Soekirno et al. (2006a), Stoops et al. (2009a), Stoops et al. (2008),
Stoops et al. (2009b), Sudomo et al. (2010), Sukowati et al. (2005b), Sukowati et al. (2001),
(Continued)
reason it is not important as a malaria vector is due to its strong zoophilic

behaviour.
The first evidence that An. barbirostris in Indonesia is a complex of species
was based on analysis of mtDNA Cytochrome Oxidease I gene (COI) in
which three putative species were formally designated W, X and Z (form
Y was identified from Thailand) (Satoto, 2001). More recently, the molec-
ular phylogeny of An. barbirostris in Indonesia (COI and ITS2 data) has rev-
ealed several sympatric but distinct species clades exist in Java and Sumatra,
the precise distribution, biology and vector status of each and control impli-
cations have yet to be determined (Paredes-Esquivel et al., 2009).
Zoophilic and anthropophilic from of An. barbirostris have been reported
in Indonesia (Lien et al., 1977), behavioural traits which can greatly influ-
ence their capacity to transmit pathogens (Table 3.3). An. barbirostris females
are often found resting outdoors (Adrial, 2008; Barodji et al., 1992; Idris-
Idram et al., 1998/1999; Munif et al., 2007; Ompusunggu et al., 2006)
and are more common amongst cattle shelters than human settlements, espe-
cially in Java (Barodji et al., 1992, 2007; Ikawati et al., 2006; Maekawa et al.,
2009b; Mardiana and Sukana, 2005; Mardiana et al., 2002, 2005; Munif
et al., 2007; Takken et al., 1990; Walch and Sardjito, 1928). The HBI varies
depending on the source location of the mosquitoes with 12.6% (42/332)
from animal shelter resting collections containing human blood (Chow
et al., 1959; Noerhadi, 1960) and 20% (2/10) from indoor collections
(Walch and Sardjito, 1928). When biting humans, An. barbirostris typically
feeds outdoors (Adrial, 2008; Garjito et al., 2004b; Ikawati et al., 2006;
Jastal et al., 2001; Maekawa et al., 2009b; Mardiana and Sukana, 2005;
Munif et al., 2007; Ompusunggu et al., 1994a, 1996; Stoops et al.,
2009b; Widjaya et al., 2006) but the biting behaviour and activity of this
species will vary depending on geographic location. For example, in western
Java and central Sulawesi, females are more frequently found biting during
the first half of the night (Garjito et al., 2004b; Jastal et al., 2003; Stoops et al.,
Figure 3.5contd Sukowati et al. (2002), Sulaeman (2004), Sundararaman et al.

(1957), Suparno (1983), Susana (2005), Suwasono et al. (1993), Swellengrebel (1921),
Swellengrebel and Rodenwaldt (1932), Swellengrebel and Swellengrebel-de Graaf
(1920), Syafruddin et al. (2010), Tarore (2010), Tativ and Udin (2006), Trenggono
(1985), Ustiawan and Hariastuti (2007), Widiarti et al. (1993), Widiastuti et al. (2006),
Widjaya et al. (2006), Widyastuti and Widiarti (1996), Widyastuti et al. (1995), World
Health Organization and Vector Biology and Control Research Unit 2 Semarang
(1977), Yunianto et al. (2002) and Yunianto et al. (2004).
2009b), but elsewhere these mosquitoes will typically reach biting peaks
during the third quarter of the night (24:0003:00) (Garjito et al., 2004b;
Munif et al., 2007; Ompusunggu et al., 1994a, 1996; Widjaya et al., 2006).
The preferred larval habitat of An. barbirostris is sunlit water bodies con-
taining exclusively fresh, often clear water, with varying amounts of emer-
gent aquatic vegetation to (Table 3.4) (Takken et al., 1990) include lagoons
(Marwoto et al., 1992b; Ompusunggu et al., 1994b; Shinta et al., 2003),
marshes (Adrial, 2008; Boesri, 1994b; Church et al., 1995; Garjito et al.,
2004b; Sudomo et al., 2010; Widjaya et al., 2006), pools (Boewono and
Ristiyanto, 2005; Garjito et al., 2004a; Jastal et al., 2003; Nurdin et al.,
2003; Ompusunggu et al., 1994b, 1996, 2006; Shinta et al., 2003), slow run-
ning streams (Adrial, 2008; Church et al., 1995; Maekawa et al., 2009a;
Mardiana and Sukana, 2005; Miyagi et al., 1994; Ompusunggu et al.,
1994a,b), along river banks (Boewono and Ristiyanto, 2005; Marwoto
et al., 1992b; Nurdin et al., 2003), springs (Munif et al., 2007) and various
man-made habitats, such as rice fields (Adrial, 2008; Boewono and
Ristiyanto, 2005; Church et al., 1995; Garjito et al., 2004a,b; Idris-Idram
et al., 1998/1999; Jastal et al., 2003; Mardiana and Sukana, 2005;
Mardiana et al., 2002; Marwoto et al., 1992b; Miyagi et al., 1994; Munif
et al., 2007; Ndoen et al., 2010; Ompusunggu et al., 1994a, 1996;
Sekartuti et al., 1995a; Widjaya et al., 2006), fish ponds (Garjito et al.,
2004a; Sekartuti et al., 1995a), drainage ditches (Barodji et al., 2007;
Church et al., 1995; Garjito et al., 2004a; Idris-Idram et al., 1998/1999;
Mardiana and Sukana, 2005; Munif et al., 2007) and wells (Church et al.,
1995). An. barbirostris is broadly dispersed from the coastal plain (Jastal
et al., 2003; Marwoto et al., 1992a; Ndoen et al., 2010; Ompusunggu
et al., 1994a) to hilly terrain (Jastal et al., 2003; Ndoen et al., 2010;
Ompusunggu et al., 1994a) at altitudes up to 2000 m asl (Hoedojo, 1989).
5.5. Anopheles (Anopheles) barbumbrosus Strickland &

Chowdhury
An. barbumbrosus was documented by 13 sources at 63 independent sites in
Indonesia (Fig. 3.6). This species has been reported from almost all of the main
islands, excluding Papua, and most commonly from Sulawesi (45 sites). This
species can often be mistaken for An. barbirostris. Reid (1968) considers its dis-
tribution to be limited to western part of Indonesia (Sumatra and Java) and pen-
insular Malaysia, Thailand, India and Sri Lanka. It has been suggested that this
species is replaced by a very similar and closely related species, An. vanus, in Kali-
mantan, Sulawesi, Maluku and possibly the western tip of Papua. Nevertheless,
Figure 3.6 Anopheles barbumbrosus distribution in Indonesia. The blue stars indicate the
records of infectious An. barbumbrosus mosquitoes found. The yellow dots show 63 records
PfPR210 < 40%) and high risk (dark red, PfPR210 40%) (Elyazar et al., 2011a). The data-
base of distribution of An. barbumbrosus in Indonesia was acquired from the references:
Bahang et al. (1981), Brug and Bonne-Wepster (1947), Buono (1987), Garjito et al. (2004a),
Idris-Idram et al. (1998/1999), Kurihara (1978), Marwoto et al. (2002), Nurdin et al. (2003),
Sulaeman (2004), Swellengrebel and Rodenwaldt (1932), Syafruddin et al. (2010), Tarore
(2010) and Van Hell (1952).
Van Hell reported a single An. barbumbrosus female containing sporozoites

amongst 21 specimens collected from South Sulawesi in 1952 (unknown if
the infection was a human malaria parasite or other primate plasmodia) (Van
Hell, 1952). No other reports are known describing the presence of sporozoites
in this species (Nurdin et al., 2003; Sekartuti et al., 1995b). To date, this species
is only regarded as a secondary malaria vector in Sulawesi (Table 3.2) and is typ-
ically found in low abundance regard human blood feeding (Bahang et al.,
1981; Garjito et al., 2004a; Marwoto et al., 2002; Sulaeman, 2004).
Like the majority of species in the subgenera Anopheles, An. barbumbrosus
shows a marked zoophilic tendency. Sulaeman reported greater numbers of
females resting in cattle shelters than human settlements (54% vs. 46%;
n 83) and a ratio of indoor to outdoor human biting of 1:6 (Sulaeman,
2004), indicating much greater exophagy. There are no known reports
on the HBI or any evidence of preferential resting habits in Sulawesi or
elsewhere.
The immature stages of An. barbumbrosus prefer a variety of habitats

including both partially shaded and sunlit fresh and slowly running water,
grass-fringed streams to stagnant water pools (Table 3.4; Takken et al.,
1990). These include natural water collections along river banks
(Nurdin et al., 2003), clear streams emerging from jungle areas
(Koesoemowinangoen, 1953; Russel et al., 1943) open grassy ravines
(Bonne-Wepster and Swellengrebel, 1953; Koesoemowinangoen, 1953)
and man-made water collections, such as rice fields (Bonne-Wepster and
Swellengrebel, 1953; Koesoemowinangoen, 1953).
5.6. Anopheles (Cellia) farauti Laveran species complex

The An. farauti complex comprises the largest complex of sibling species
(8 members) within the Punctulatus Group (Cooper et al., 2009; Sinka
et al., 2011), seven of which have been identified on the island of New
Guinea (Cooper et al., 2009). An. farauti s.s. has the widest geographic dis-
tribution of any member in the group but is restricted to the coastal areas.
Papua has been shown to contain at least five of the sibling species based on
molecular analysis (Bangs, Personal communication, 2012), including An.
hinesorum (An. farauti 2), a confirmed malaria vector in PNG (Cooper
et al., 2009). Unfortunately, the vast majority of studies on An. farauti s.l.
occurred before the advent of molecular (DNA) analysis techniques that
provide the ability to differentiate isomorphic (morphological identical) spe-
cies in the complex (Cooper et al., 2002). Fifteen sources were found
reporting the presence of An. farauti s.l. at 31 independent sites in Indonesia
(Fig. 3.7). Of these, 19 sites were located in Papua, where the role of this
complex in malaria transmission has been well known since the mid-
1950s when Metselaar reported a sporozoite rate of 0.8% (8/1023) near Jaya-
pura (Metselaar, 1956). This species sporozoite positive (P. falciparum and
two P. vivax variants) was found in both southern (Mapurujaya, Tipuka,
Timika, Atuka) and northern (Arso, Armopa) areas of mainland Papua from
1987 through 1999 (Bangs and Rusmiarto, 2007). Evidence of sporozoite
infection in An. farauti s.s. (P. falciparum and P. vivax) has also been reported
from Gag Island, the western-most locality in Papua (east of Halmahera
Island, northern Maluku Island chain where it is also present and regarded
a malaria vector). The complex appears to exist at relative low densities in
southern Papua (<5% of collections) compared to other members in the
Punctulatus Group (Lee et al., 1980; Van den Assem, 1959), but it can be
found in high abundance in northern Papua (>50% of collections) (Sari
et al., 2004; Slooff, 1964).
Figure 3.7 Anopheles farauti s.l. distribution in Indonesia. The blue stars indicate the
records of infectious An. farauti s.l. mosquitoes found. The yellow dots show 31 records
Pf PR210 < 40%) and high risk (dark red, Pf PR210 40%) (Elyazar et al., 2011a). The data-
base of distribution of An. farauti s.l. in Indonesia was acquired from the references: Bangs
et al. (1993b), Brug and Bonne-Wepster (1947), Knight (1945), Kurihara (1978), Lee et al. (1980),
Metselaar (1956), Mulyadi (2010), Pranoto and Munif (1994), Rozeboom and Knight (1946), Sari
et al. (2004), Slooff (1964), Soekirno et al. (1997), Sutanto et al. (2003), Syafruddin et al. (2010)
and Van den Assem (1959).
The behaviour of An. farauti s.l. appears to vary by geographical location

and presumably by sibling species (note that most work on this species was con-
ducted before it was known to be a complex of sibling species). For example, a
study conducted in the coastal areas of northwestern Papua (Sorong) (Pranoto
and Munif, 1994) found the human biting ratio between indoor and outdoor
collections was 1:8, suggesting a strong exophagic tendency in that location;
whereas a longitudinal study in northeastern Papua (near Jayapura) reported
an indoor:outdoor human biting ratio of 1:3 and hence moderate or little pref-
erence in biting location (Slooff, 1964). On the coast of northwest Papua
(Pranoto and Munif, 1994) and on the northeast side of the island (Entrop near
Jayapura), biting activity peaked early in the evening hours whereas at a site
35 km away (Arso), biting was more commonly observed between the second
or third quarter of the night (Slooff, 1964). Resting behaviour may also vary by
both location and sibling species, with females from the coastal northwest of
Papua showing a preference to rest indoors immediately after feeding but
leaving the house before dawn (Pranoto and Munif, 1994). Conversely, those
in the northeast, showed a strong exophilic behaviour, with high numbers of
newly blood fed females collected in exit traps during the evening compared to
those remaining indoors (Slooff, 1964).
An. farauti s.l. larvae prefer sunlit habitats with fresh or brackish water
(Takken et al., 1990), depending on the sibling species (Table 3.4). The pri-
mary vector species in the complex, An. farauti sensu stricto, is restricted to the
coastal zones and generally prefers brackish habitats, often tolerating high
salinity levels. The larval stages of this species complex have been found in
a variety of natural habitats, including marshes, ponds and lagoons with emer-
gent vegetation (Hoedojo, 1989; Koesoemowinangoen, 1953; Lee et al.,
1980; Pranoto and Munif, 1994; Slooff, 1964; Van den Assem, 1961), large
and small streams with grassy margins and floating wood and other natural
debris (Church et al., 1995), along river banks (Hoedojo, 1989) or temporary
man- and animal-made habitats, such as borrow pits, pig-gardens, garden
pools and pools along river and stream margins (Knight, 1945; Lee et al.,
1987; Pranoto and Munif, 1994; Van den Assem, 1961), fishponds
(Pranoto and Munif, 1994) and ditches (Church et al., 1995; Pranoto and
Munif, 1994). An. farauti has also been observed in container habitats such
as discarded cans, drums, coconut shells and open canoes, as well as holes
in coral pits, wells and carb holes (Lee et al., 1987). This species complex is
found from the coastal plain (Church et al., 1995; Lee et al., 1980; Van
den Assem, 1961) to hilly and mountainous terrain (Metselaar, 1959;
Van den Assem, 1961) to altitudes up to 2250 m asl (Cooper et al., 2009;
Metselaar, 1959; Takken et al., 1990).
5.7. Anopheles (Cellia) flavirostris (Ludlow)

An. flavirostris is a member of the Minimus Subgroup (Chen et al., 2003)
and was previously considered a subspecies of the Minimus Complex;
however, molecular investigations have confirmed An. flavirostris as a valid
species. Moreover, Sinka et al. (2011) now regard all previous records of
An. minimus reported from Indonesia, the Philippines and Sabah, Malaysia
as invalid and misidentifications of An. flavirostris; therefore, data presented
here include An. minimus records. An. flavirostris was reported from
46 sources at 119 independent sites across Indonesia, most commonly from
central and southern Sulawesi (39 sites) and Java (30 sites) (Fig. 3.8),
followed but also Sumatra, Kalimantan and the Lesser Sunda Islands exten-
ding to Timor-Leste (Cooper et al., 2010). An. flavirostris has been found
infected with P. falciparum sporozoites on Sulawesi (Van Hell, 1952) and

Java (Wigati et al., 2006). In many locations in Java (Handayani and
Darwin, 2006; Lestari et al., 2000; Mardiana et al., 2002; Ndoen et al.,
2010; Stoops et al., 2009a), Lesser Sundas (Barbara et al., 2011;
Maekawa et al., 2009a; Marwoto et al., 1992a) and Sulawesi (Marwoto
et al., 2002), it has generally been reported in low abundance (<5% of
all Anopheles species collected).
Figure 3.8 Anopheles flavirostris distribution in Indonesia. The blue stars indicate the
records of infectious An. flavirostris mosquitoes found. The yellow dots show 119 records
2011a). The database of distribution of An. flavirostris in Indonesia was acquired from
the references: Alfiah et al. (2008), Arianti (2004), Atmosoedjono et al. (1993), Barbara
et al. (2011), Barodji et al. (2003), Barodji et al. (1992), Barodji et al. (2004b), Barodji
et al. (1998/1999), Barodji et al. (1996), Boesri et al. (2004), Boesri and Boewono (2006),
Boewono and Ristiyanto (2004, 2005), Brug and Bonne-Wepster (1947), Dasuki and
Supratman (2005), Gandahusada (1979), Handayani and Darwin (2006), Harbach et al.
(1987), Isfarain and Santiyo (1981), Jastal et al. (2003), Kaneko et al. (1987), Kazwaini
and Martini (2006), Lestari et al. (2000), Lien et al. (1975), Maekawa et al. (2009a),
Maekawa et al. (2009b), Mardiana et al. (2002), Marwoto et al. (2002), Marwoto et al.
(1992a), Mulyadi (2010), Ndoen et al. (2010), Noor (2002), Stoops et al. (2009a), Stoops
et al. (2008), Stoops et al. (2009b), Sudomo et al. (2010), Sukowati et al. (1987),
Sukowati et al. (2001), Suwasono et al. (1993), Swellengrebel and Rodenwaldt (1932),
Syafruddin et al. (2010), Trenggono (1985), Van Hell (1952), Wigati et al. (2006) and
An. flavirostris is typically zoophilic (Sinka et al., 2011). Greater relative

numbers of An. flavirostris mosquitoes were captured at cattle shelters than
human settlements (inside homes) in Central Java (Barodji et al., 2003;
Soekirno et al., 1983). Another study in Java reported 9% of mosquitoes
contained human blood and suggested low anthropophily (Alfiah et al.,
2008), but as only a small number of mosquitoes (n 33) were examined
and the data presented did not differentiate between indoor and outdoor
collections such a conclusion is potentially questionable (Table 3.3).
There are some apparent, albeit minor, variations in the biting habits
of An. flavirostris depending on location. For example, Barbara et al.
(2011) reported a ratio of indoor/outdoor human biting in western
Sumba Island of 1:1.2, indicating no clear preference for feeding location,
whereas an indoor/outdoor ratio of between 1:1.5 and 2.9 was reported
from Flores Island (Barodji et al., 1998/1999). In all cases, the general
tendency appears to be towards exophagy, although this preference
appears weak indicating a more opportunistic biting habit. In coastal
Flores, biting activity has been shown to peak in the second quarter of
the night, yet in the interior of the island activity can peak during the third
quarter of the night (Barodji et al., 1998/1999). In Flores, An. flavirostris
appears endophilic, preferring to rest indoors after feeding (Barodji et al.,
1998/1999).
The immature stages of An. flavirostris are often found in shaded habitats
containing fresh and clear water (Table 3.4; Takken et al., 1990) that can
include springs (Barodji et al., 1999/2000; Jastal et al., 2003; Lestari et al.,
2007), shaded grassy edges of clear, slow-flowing small streams (Barodji
et al., 1998/1999; Barodji et al., 2007; Hoedojo, 1989; Jastal et al., 2003;
Koesoemowinangoen, 1953; Lestari et al., 2007; Maekawa et al., 2009a;
Ompusunggu et al., 1994b), pools (Barodji et al., 1999/2000; Jastal et al.,
2003; Lestari et al., 2007; Ompusunggu et al., 1994b), rice fields (Ndoen
et al., 2010; Stoops et al., 2008) and irrigation ditches (Van Hell, 1952). This
species can be found from the coastal plains (Stoops et al., 2007) to the hill
areas (Barbara et al., 2011; Maekawa et al., 2009a; Ndoen et al., 2010) up to
600 m asl (Bonne-Wepster and Swellengrebel, 1953; Swellengrebel and
Swellengrebel-de Graaf, 1919b).
5.8. Anopheles (Cellia) karwari James

Anopheles karwari is a member of the Maculatus Group and the second scarc-
est species reported here from Indonesia, present at only 36 independent sites
and identified by only seven sources (Fig. 3.9), four of which were published
prior to 1985. Sumatra had the highest number of sites, with others reported
from Java, Kalimantan, Sulawesi and Papua. An. karwari is apparently absent
from the Lesser Sundas and Maluku Island chains and infective females
have only been reported from Papua (near Jayapura) (Metselaar, 1956). Very
little is known about the bionomics of this species in Indonesia because
of its infrequent and patchy occurrence in collections. It is presumed to
be primarily zoophilic.
An. karwari larvae are found in natural- and man-made shaded habitats
containing fresh water (Table 3.4), such as marshes (Koesoemowinangoen,
1953; Taylor, 1943), small, slow-moving streams (Church et al., 1995;
Koesoemowinangoen, 1953; Swellengrebel, 1921), seepages (Church et al.,
1995; Taylor, 1943), ground and rock pools (Taylor, 1943; Van den
Assem, 1961), springs (Church et al., 1995; Koesoemowinangoen, 1953)
and irrigation canals associated with rice cultivation (Church et al., 1995;
Koesoemowinangoen, 1953; Swellengrebel, 1921; Taylor, 1943).
Figure 3.9 Anopheles karwari distribution in Indonesia. The blue stars indicate the
records of infectious An. karwari mosquitoes found. The yellow dots show 36 records
2011a). The database of distribution of An. karwari in Indonesia was acquired from
the references: Brug and Bonne-Wepster (1947), De Rook (1929), Kaneko et al. (1987),
Metselaar (1957), Self et al. (1976), Susana (2005) and Swellengrebel and Rodenwaldt
(1932).
5.9. Anopheles (Cellia) kochi Dnitz

An. kochi is widely dispersed across Indonesia and is found on nearly all of the
main islands except for New Guinea (Papua). Foley et al., 2000 reported the
apparent introduction (likely by aircraft) to southern Papua but there have
been no evidence this species has established itself on the island. It has been
documented from 88 sources and 253 independent sites (Fig. 3.10). Publi-
shed accounts of its role in malaria transmission has only been confirmed in
Nias Island off the western coast of northern Sumatra (Boewono et al.,
1997a). Studies in Java (Barodji et al., 2007; Boewono and Ristiyanto,
2005; Lestari et al., 2007; Stoops et al., 2009b) and Sulawesi (Sekartuti
et al., 1995b) have been unable to detect the presence of sporozoites in
An. kochi. However, this species positive CSP-ELISA for P. falciparum
and P. vivax was found in northern Sulawesi and for P. vivax in Central Java
(Bangs and Rusmiarto, 2007).
An. kochi generally appears in low densities in human-landing collections
(Adrial, 2003; Alfiah et al., 2008; Arianti, 2004; Barbara et al., 2011; Barodji
et al., 2007; Garjito et al., 2004b; Harbach et al., 1987; Hasan, 2006;
Hoedojo, 1992, 1995; Idris-Idram et al., 1998/1999; Lee et al., 1983,
1984; Marwoto et al., 2002; Ndoen et al., 2010; Raharjo et al., 2006;
Ramadhani et al., 2005; Stoops et al., 2009b; Yunianto et al., 2004), possibly
reflecting a zoophilic feeding behaviour throughout much of its range
(Table 3.3). Indeed, females appear more common in cattle shelters than
human habitation (Adrial, 2003; Barodji et al., 1992, 2007; Garjito et al.,
2004b; Munif et al., 2007; Sulaeman, 2004). In western and eastern Java
from 554 females captured resting in cattles shelters, 15% contained human
blood (Chow et al., 1959; Noerhadi, 1960) and only 2.8% of 287 mosqui-
toes contained human blood from indoor collections in homes (Alfiah et al.,
2008; Walch, 1932). Human-landing catches in northern Sumatra recorded
an indoor/outdoor ratio of 1:6 (Idris et al., 2002), whereas a near equal dis-
tribution (1:1.2) was reported in Java (Stoops et al., 2009b) and 1:8 ratio in
central Sulawesi (Sulaeman, 2004), indicating a general tendency for
exophagy. An. kochi reach their peak blood-feeding activity during the first
half (second quarter) of the night (Chow et al., 1959). Their resting habits
depend on location for example, they appear more exophilic in Central Java
(Barodji et al., 1992) and endophilic in southern Java (Chow et al., 1959;
Soekirno et al., 1983).
An. kochi larvae prefer sunlit habitats with either fresh or brackish running
or stagnant, often muddy (turbid) water (Table 3.4; Takken et al., 1990).
Figure 3.10 Anopheles kochi distribution in Indonesia. The blue stars indicate the
records of infectious An. kochi mosquitoes found. The yellow dots show 253 records
2011a). The database of distribution of An. kochi in Indonesia was acquired from the
references: Adrial (2003), Adrial et al. (2000), Alfiah et al. (2008), Arianti (2004),
Atmosoedjono et al. (1993), Barbara et al. (2011), Barodji et al. (2003), Barodji et al.
(2007), Barodji et al. (1992), Boesri et al. (2004), Boesri and Boewono (2006), Boewono
et al. (1997b), Boewono and Ristiyanto (2004, 2005), Brug (1931), Brug and Bonne-
Wepster (1947), Buono (1987), Dasuki and Supratman (2005), Dharma et al. (2004),
Fryauff et al. (2002), Gandahusada (1979), Garjito et al. (2004a), Garjito et al. (2004b),
Harbach et al. (1987), Hasan (2006), Hoedojo (1992, 1995), Idris-Idram et al. (2002), Idris
et al. (2002), Ikawati et al. (2006), Ikawati et al. (2004), Jastal et al. (2002), Jastal et al.
(2001), Kaneko et al. (1987), Knight (1945), Kurihara (1978), Lee et al. (1983), Lee et al.
(1984), Lestari et al. (2000), Lien et al. (1975), Maekawa et al. (2009b), Mangkoewinoto
(1919), Mardiana et al. (2002), Marjiyo (1996), Marsaulina (2002, 2008), Marwoto et al.
(2002), Marwoto et al. (1992a), Mulyadi (2010), Munif (1990, 1994), Munif et al. (2007),
Munif et al. (2003), Nalim et al. (2000), Ndoen et al. (2010), Noor (2002), Priadi et al.
(1991), Raharjo et al. (2007), Raharjo et al. (2006), Ramadhani et al. (2005), Schuurman
and Huinink (1929), Self et al. (1976), Sigit and Kesumawati (1988), Stoops et al.
(2009a), Stoops et al. (2008), Stoops et al. (2009b), Sudomo et al. (2010), Sukowati et al.
(1987), Sukowati et al. (2001), Sulaeman (2004), Suparno (1983), Susana (2005),
Suwasono et al. (1993), Swellengrebel (1921), Swellengrebel and Rodenwaldt (1932),
Swellengrebel and Swellengrebel-de Graaf (1920), Syafruddin et al. (2010), Tativ and
Udin (2006), Ustiawan and Hariastuti (2007), Van Hell (1952), Van Peenen et al. (1975),
Widiastuti et al. (2006), Widyastuti et al. (1997), World Health Organization and Vector
Biology and Control Research Unit 2 Semarang (1977), Yunianto et al. (2002) and
Swellengrebel and Swellengrebel-de Graaf specifically noted this species as [a]

true dirty water breeder because of its apparent preference for muddy habitats
(Swellengrebel and Swellengrebel-de Graaf, 1919a). Larval habitats also
include natural- and man-made sites such as marshes (Adrial, 2003;
Swellengrebel and Swellengrebel-de Graaf, 1919a; Taylor, 1943), springs
(Bonne-Wepster and Swellengrebel, 1953; Koesoemowinangoen, 1953;
Lestari et al., 2007; Noerhadi, 1960; Swellengrebel and Swellengrebel-de
Graaf, 1920), rice fields (Boewono and Ristiyanto, 2005; Bonne-Wepster
and Swellengrebel, 1953; Idris et al., 2002; Koesoemowinangoen, 1953;
Marsaulina, 2008; Noerhadi, 1960; Stekhoven and Stekhoven-Mayer,
1922; Swellengrebel and Swellengrebel-de Graaf, 1919a), ponds (Adrial,
2003; Bonne-Wepster and Swellengrebel, 1953; Idris et al., 2002;
Koesoemowinangoen, 1953; Mangkoewinoto, 1919; Sudomo et al., 2010;
Swellengrebel and Swellengrebel-de Graaf, 1919a), pools (Swellengrebel
and Swellengrebel-de Graaf, 1920), buffalo wallows (Bonne-Wepster and
Swellengrebel, 1953; Swellengrebel and Swellengrebel-de Graaf, 1919a),
wells (Taylor, 1943) and ditches (Bosh, 1925; Idris-Idram et al., 1998/
1999; Koesoemowinangoen, 1953; Mangkoewinoto, 1919; Swellengrebel
and Swellengrebel-de Graaf, 1919a). This species can be found from the
coastal plain (Mangkoewinoto, 1919; Stoops et al., 2007, 2009b) to hilly loca-
tions (Mangkoewinoto, 1919; Ndoen et al., 2010; Stoops et al., 2007) at alti-
tudes up to 1100 m asl (Brug, 1931). In western Java, more An. kochi
mosquitoes were found nearer coastal locations than upland areas (99% vs.
1%; n 88) (Stoops et al., 2009b).
5.10. Anopheles (Cellia) koliensis Owen

An. koliensis is a member of the diverse Punctulatus Group (Sinka et al.,
2011) which also includes the primary malaria vectors, An. punctulatus
and An. farauti complexes (Cooper et al., 2009; Rozeboom and Knight,
1946). An. koliensis occurrence has been reported from 12 sources covering
15 independent sites which were all located in Papua (Fig. 3.11). Unfor-
tunately, the vast majority of these studies took place before the advent of
molecular (DNA) analysis techniques provide the ability to differentiate
species accurately within the group because of the occurrence of over-
lapping and variable (polymorphic) morphological characters between
species (Cooper et al., 2002). Metselaar dissected 1748 mosquitoes col-
lected in Jayapura, and found 11 containing malaria sporozoites (0.63%)
(Metselaar, 1956). Pribadi et al. (1998) reported a P. vivax sporozoite rate
Figure 3.11 Anopheles koliensis distribution in Indonesia. The blue stars indicate the
records of infectious An. koliensis mosquitoes found. The yellow dots show 15 records
red, 5% < PfPR210 < 40%) and high risk (dark red, PfPR210 > 40%) (Elyazar et al.,
2011a). The database of distribution of An. koliensis in Indonesia was acquired from
the references: Anthony et al. (1992), Bangs et al. (1993a), Bangs et al. (1996), Brug and
Bonne-Wepster (1947), Lee et al. (1980), Metselaar (1956), Pribadi et al. (1998),
Rozeboom and Knight (1946), Sari et al. (2004), Slooff (1964), Sutanto et al. (2003)
and Yamtama et al. (2008).
of 0.3% by CSP-ELISA in the Mimika area, southern Papua and an ento-

mological inoculation rate (EIR) of 0.17 infective bites/person/night. An.
koliensis appears particularly abundant in settlement areas near sago palm
and swamp forests (Lee et al., 1980; Slooff, 1964). This species has been
found infected in many locations in northern and southern Papua
(Bangs and Rusmiarto, 2007).
Lee et al. (1980) observed that due to a lack of abundance of large animals
such as cattle, buffaloes or horses in Papua, the human population is the pri-
mary host for this vector. Indeed, a high proportion of mosquitoes con-
taining human blood (74%; 126/170) have been reported from outdoor
collections (Slooff, 1964). However, before this species can be designated
as anthropophilic a well-designed host-choice experiment should be under-
taken. The feeding behaviour of An. koliensis varies depending on location.
A human indoor/outdoor biting ratio of 1:1.1 was reported from Arso,
Papua, whereas a ratio of 1:4 was found in Entrop, Papua, suggesting a
exophagic habit in some areas. In Arso, An. koliensis was the most common
vector species found biting indoors between the second and third quarters of
the night with biting occurring mainly in the first quarter of the night out-
doors. In contrast, early-biting was seen both indoors and outdoors in
Entrop. After indoor blood feeding, this species usually leaves the house very
soon afterwards to rest outdoors (Slooff, 1964).
The larval stages of An. koliensis can be found in mostly sunlit temporary
and semi-permanent sunlit habitats such as ground pools in grassland and
along the edge of jungles (Church et al., 1995; Lee et al., 1980; Van den
Assem, 1961), ditches (Anthony et al., 1992; Lee et al., 1980; Slooff,
1964), riverside ponds (Lee et al., 1980) and occasionally in pig ruts and
wallows (Anthony et al., 1992; Bangs et al., 1996) (Table 3.4). In some loca-
tions, it is often closely associated with An. farauti (Lee et al., 1987; Slooff,
1964). This species can also be found in temporary pools such as shallow
earth drains, footprints and wheel ruts, the typical habitat of An. punctulatus.
This species can be found from lowland areas (Church et al., 1995; Van
den Assem and Van Dijk, 1958) to the highlands, up to 1700 m asl
(Metselaar, 1959).
5.11. Anopheles (Cellia) leucosphyrus Dnitz

An. leucosphyrus is a member of the Leucosphyrus Subgroup (Rattanarithikul
et al., 2006). It is considered to be of epidemiological importance for malaria
transmission in forested areas of Sumatra (McArthur, 1951), reflecting its
preferred habitat. Within the Leucosphyrus complex, An. leucosphyrus is a
sister species to An. balabacensis and more recently Anopheles latens (Sallum
et al., 2007), the primary vector of zoonotic Plasmodium knowlesi between
monkeys and humans in Sarawak, Malaysia (northern Borneo) and possibly
elsewhere in Kalimantan (Indonesian Borneo). The separation of these
two species was derived from earlier cytogenetic evidence (Baimai
et al., 1988) and eventually DNA analysis (Sallum et al., 2005). An. latens
appears to be restricted to the island of Borneo. Due to confusion and
potential misidentification, Sinka et al. (2011) suggested that much of
the published literature on An. leucosphyrus should be treated with cau-
tion, specifically where referring to An. leucosphyrus in locations other
than Sumatra.
In this current study, An. leucosphyrus was reported from eight sources at
47 independent sites including Sumatra (25 sites) and Kalimantan (16 sites)
(Fig. 3.12). However, in light of the issues raised by Sinka et al. (2011) and
the clear genetic differentiation between An. latens and An. leucosphyrus,
occupying very similar environmental conditions and the existence of
An. latens in Malaysian Borneo, these latter data cannot be confirmed. How-
ever, we suggest molecular identification should be conducted on An.
leucosphyrus specimens collected from Indonesian Kalimantan to confirm
the presence of absence of these species beyond the State of Sarawak,
Malaysia.
The bionomic information for An. leucosphyrus remains limited. Walch
(1932) found that in areas where cattle are scarce, 101 of 102 An. leucosphyrus
mosquitoes collected indoors contained human blood. However, this find-
ing may be bias sampling as the same experimental design was not repeated
in areas where cattle or other alternative blood sources were abundant.
Therefore, the conclusion of human host preference may not be valid
for all localities. Limited information exists on the vector status of
Figure 3.12 Anopheles leucosphyrus distribution in Indonesia. The blue stars indicate
the records of infectious An. leucosphyrus mosquitoes found. The yellow dots show
47 records of occurrence for this species between 1932 and 2004. Areas were defined
as no risk (light grey, where PfAPI 0 per 1000 pa), unstable transmission (medium
grey, where PfAPI < 0.1 per 1000 pa), low risk (light red, PfPR210 5%), intermediate
risk (medium red, 5% < PfPR210 < 40%) and high risk (dark red, PfPR210 > 40%)
(Elyazar et al., 2011a). The database of distribution of An. leucosphyrus in Indonesia
was acquired from the references: Brug and Bonne-Wepster (1947), Harbach et al.
(1987), Idris-Idram et al. (1998/1999), Isfarain and Santiyo (1981), Kaneko et al. (1987),
McArthur (1951), Suparno (1983) and Swellengrebel and Rodenwaldt (1932).
An. leucosphyrus (via detection of natural malaria sporozoite infections). Har-

bach et al. in the 1980s did report a single sporozoite positive An. leucosphyrus
(tested by NAMRU-2) collected from southern Kalimantan (Harbach et al.,
1987) but the species identification is now in question and would need to be
confirmed.
Similar to all members of the complex, An. leucosphyrus prefers shaded
larval habitats within or very near forested environments and containing
fresh water (Table 3.4; Bonne-Wepster and Swellengrebel, 1953; White,
1983). Larval sites include marshes (Swellengrebel and Swellengrebel-de
Graaf, 1920), small streams (Swellengrebel and Swellengrebel-de Graaf,
1920; Taylor, 1943), seepage springs (Swellengrebel and Swellengrebel-
de Graaf, 1920), jungle pools (Mangkoewinoto, 1919; Swellengrebel
and Swellengrebel-de Graaf, 1920; Taylor, 1943), ground depressions
(Swellengrebel and Swellengrebel-de Graaf, 1920), fishponds
(Swellengrebel and Swellengrebel-de Graaf, 1920; Taylor, 1943), wheel
ruts (Swellengrebel and Swellengrebel-de Graaf, 1920) and hoof prints
(Swellengrebel and Swellengrebel-de Graaf, 1920).
5.12. Anopheles (Cellia) maculatus Theobald species

subgroup
An. maculatus s.l. belongs to the larger Maculatus Group comprised of several
subgroups in the Southeast Asian region (Harbach, 2004). The precise
relationship of the Indonesian populations remains to be clarified and
may represent as an yet undescribed species in the subgroup. Occurrence
data have been reported by 93 sources from 188 independent sites
(Fig. 3.13) throughout much of western and central Indonesia. The most
common sites were located on Java (86 sites) where this species group is
encountered relatively often in collections; elsewhere in Indonesia its biting
densities are typically very low. There is no evidence of this species being
present in Maluku or Papua. Plasmodium spp. infections of An. maculatus
have been reported in Indonesia, particularly from eastern (Venhuis,
1941) and Central Java (Wigati et al., 2006). Likewise, CSP-ELISA positive
P. falciparum and P. vivax specimens were also observed in three localities
near Jogyakarta (Kokap, Purworejo and Banjarmangu), in Central Java
and one locality in southern Sumatra (Tenang) (Bangs and Rusmiarto,
2007). This species is considered a major malaria vector in the Menoreh
Hills of Central Java (Barcus et al., 2002; Lestari et al., 2000; Wigati
et al., 2006).
Figure 3.13 Anopheles maculatus s.l. distribution in Indonesia. The blue stars indicate
the records of infectious An. maculatus s.l. mosquitoes found. The yellow dots show
et al., 2011a). The database of distribution of An. maculatus s.l. in Indonesia was acquired
from the references: Adrial (2003, 2008), Adrial et al. (2000), Alfiah et al. (2008), Aprianto
(2002), Ariati (2004), Atmosoedjono et al. (1993), Barbara et al. (2011), Barodji et al. (2003),
Barodji et al. (2007), Barodji et al. (1992), Barodji et al. (2004b), Barodji and Sularto (1993),
Barodji et al. (1998/1999), Blondine (2004), Blondine (2005), Blondine et al. (2003), Blondine
and Widiarti (2008), Boesri et al. (2004), Boesri and Boewono (2006), Boewono and
Ristiyanto (2004, 2005), Boewono et al. (2005), Boewono et al. (2004), Brug and Bonne-
Wepster (1947), Dasuki and Supratman (2005), Effendi (2002), Gandahusada (1979),
Garjito et al. (2004b), Handayani and Darwin (2006), Idris-Idram et al. (2002), Idris et al.
(2002), Ikawati et al. (2006), Ikawati et al. (2004), Iyana (1992), Jastal et al. (2002), Jastal
et al. (2001), Kaneko et al. (1987), Kirnowardoyo et al. (1991, 1992), Lee et al. (1984),
Lestari et al. (2000), Lien et al. (1975), Maekawa et al. (2009a), Maekawa et al. (2009b),
Mangkoewinoto (1919), Mardiana et al. (2002), Mardiana and Sukana (2005), Mardiana
et al. (2005), Marjiyo (1996), Marwoto et al. (2002), Marwoto et al. (1992a), Munif and
Pranoto (1994, 1996), Munif et al. (2007), Munif et al. (2003), Ndoen et al. (2010), Noor
(2002), Ompusunggu et al. (1994a), Pranoto and Munif (1993), Priadi et al. (1991),
Raharjo et al. (2007), Raharjo et al. (2006), Ramadhani et al. (2005), Santoso (2002), Self
et al. (1976), Setyawati (2004), Stoops et al. (2008), Stoops et al. (2009b), Sukmono
(2002), Sukowati et al. (2001), Sulaeman (2004), Suparno (1983), Susana (2005),
Suwasono et al. (1997), Suwasono et al. (1993), Swellengrebel (1921), Swellengrebel and
Rodenwaldt (1932), Swellengrebel and Swellengrebel-de Graaf (1920), Syafruddin et al.
(2010), Ustiawan and Hariastuti (2007), Van Hell (1952), Waris et al. (2004), Widiarti
et al. (2005a), Widiarti et al. (2005b), Widiastuti et al. (2006), Widyastuti et al. (2004),
Wigati et al. (2006), World Health Organization and Vector Biology and Control
Research Unit 2 Semarang (1977), Yudhastuti (2009), Yunianto et al. (2002) and
Female An. maculatus are considered primarily zoophilic throughout

most of their range and are regularly reported as more prevalent in cattle
shelters than in human habitation (Adrial, 2008; Barodji et al., 2003,
2007; Boesri and Boewono, 2006; Boewono and Ristiyanto, 2005; Jastal
et al., 2001; Lestari et al., 2000; Mardiana et al., 2002; Noerhadi, 1960;
Noor, 2002; Ompusunggu et al., 1996; Pranoto and Munif, 1993;
Raharjo et al., 2007; Ramadhani et al., 2005; Venhuis, 1941). It has been
found biting humans both indoors (Adrial, 2008) and outdoors (Adrial,
2008; Barodji et al., 2003, 2007; Boewono and Ristiyanto, 2005; Ikawati
et al., 2006; Lestari et al., 2000; Munif et al., 2007; Pranoto and Munif,
1993; Ramadhani et al., 2005; Stoops et al., 2009b; Suwasono et al.,
1997). Blood-feeding activity varies by location but in most areas
An. maculatus generally tends to bite during the first half of night (Adrial,
2008; Barodji et al., 2003; Boesri and Boewono, 2006; Boewono and
Ristiyanto, 2005; Ikawati et al., 2006; Lestari et al., 2000; Raharjo et al.,
2007; Stoops et al., 2009b; Suwasono et al., 1997); however, an increased
biting density has been observed to occur near the early morning (dawn)
hours in Central Java (Boesri and Boewono, 2006; Suwasono et al.,
1997; Yunianto et al., 2002). After feeding indoors, An. maculatus typically
leaves the house to rest outdoors (Chow et al., 1959; Munif et al., 2007) in or
near cattle shelters (Barodji et al., 2003; Boesri and Boewono, 2006;
Handayani and Darwin, 2006; Lestari et al., 2000; Pranoto and Munif,
1993; Raharjo et al., 2007), natural ground pits and amongst bushes/low
vegetation (Handayani and Darwin, 2006), under shaded plants
(Boewono and Ristiyanto, 2005; Chow et al., 1959; Lestari et al., 2000),
under moist banks of small streams (Sundararaman et al., 1957) and in
earthen overhangs in cliff sides (Lestari et al., 2000).
The larvae of An. maculatus prefer habitats that are sunlit, containing fresh
and clear water (Table 3.4; Takken et al., 1990). Larval habitats include
stream-side rock pools (Adrial, 2008; Bonne-Wepster and Swellengrebel,
1953; Lestari et al., 2000; Pranoto and Munif, 1993), along margins of small,
slow-moving streams (Boesri and Boewono, 2006; Boewono and
Ristiyanto, 2005; Maekawa et al., 2009a; Mardiana and Sukana, 2005;
Ompusunggu et al., 1994b; Takken et al., 1990; Venhuis, 1941;
Yunianto et al., 2002), drying river beds (Russel et al., 1943), ground seep-
ages (Bonne-Wepster and Swellengrebel, 1953; Sundararaman et al., 1957;
Taylor, 1943), small pools and puddles containing turbid water
(Swellengrebel and Swellengrebel-de Graaf, 1920), natural springs (Boesri
and Boewono, 2006; Bonne-Wepster and Swellengrebel, 1953; Lestari
et al., 2000; Munif et al., 2007; Noerhadi, 1960; Raharjo et al., 2007;
Sundararaman et al., 1957; Swellengrebel and Swellengrebel-de Graaf,
1920; Yunianto et al., 2002), rice fields (Adrial, 2008; Mangkoewinoto,
1919; Mardiana and Sukana, 2005; Noerhadi, 1960; Ompusunggu et al.,
1994b; Sundararaman et al., 1957; Swellengrebel and Swellengrebel-de
Graaf, 1919c, 1920), ponds (Lestari et al., 2000; Swellengrebel and
Swellengrebel-de Graaf, 1920; Taylor, 1943) and ditches (Mardiana and
Sukana, 2005; Pranoto and Munif, 1993; Swellengrebel and
Swellengrebel-de Graaf, 1920; Takken et al., 1990). This species can be
found from the coastal plain (Jastal et al., 2001; Mardiana et al., 2002;
Ndoen et al., 2010; Swellengrebel and Swellengrebel-de Graaf, 1920) to
hilly areas (Chow et al., 1959; Lestari et al., 2000; Mangkoewinoto,
1919; Ndoen et al., 2010; Sundararaman et al., 1957; Swellengrebel and
Swellengrebel-de Graaf, 1919a, 1920) at altitudes up to 1100 m asl
(Brug, 1931).
5.13. Anopheles (Anopheles) nigerrimus Giles

An. nigerrimus is a member of the Hyrcanus Group. The presence of this spe-
cies has been reported in Indonesia by 32 sources at 91 independent sites
(Fig. 3.14). It appears more common on Sulawesi (43 sites) followed by
Sumatra, Java and Kalimantan. No evidence was found of An. nigerrimus
occurrence on the eastern islands of the Lesser Sundas or Papua and only
one report from Maluku that is likely a misidentification (OConnor and
Sopa, 1981). An. nigerrimus is a confirmed malaria vector in Indonesia
with the first evidence of Plasmodium infection reported by Overbeek
from Palembang, South Sumatra in 1940 (Overbeek, 1940). This species
has been found infected in Sihepeng, northern Sumatra (Bangs and
Rusmiarto, 2007).
The host preference for this species is unclear. Only one study was found
to report HBI and they found only a low proportion of females (7%) con-
tained human blood amongst 236 examined from animal shelter collections
in eastern Java (Chow et al., 1959), however this could be the result of sam-
pling bias. An. nigerrimus appears to rest in cattle shelters in preference to
human habitations (Gandahusada, 1979; Garjito et al., 2004a). Where
human biting occurs, it tends to be exophagic (Boesri, 1994b; Boewono
et al., 1997b; Gandahusada, 1979; Garjito et al., 2004a; Idris et al., 2002;
Idris-Idram et al., 1998/1999). An. nigerrimus has been found to bite unusu-
ally early in the evening compared to most other malaria vectors, peaking
Figure 3.14 Anopheles nigerrimus distribution in Indonesia. The blue stars indicate the
records of infectious An. nigerrimus mosquitoes found. The yellow dots show 91 records
red, 5% < PfPR210 < 40%) and high risk (dark red, PfPR210 > 40%) (Elyazar et al.,
2011a). The database of distribution of An. nigerrimus in Indonesia was acquired from
the references: Atmosoedjono et al. (1993), Bahang et al. (1981), Boesri (1994b), Boewono
et al. (2002b), Boewono et al. (1997b), Brug and Bonne-Wepster (1947), Buono (1987),
Gandahusada (1979), Gandahusada et al. (1983), Garjito et al. (2004a), Hasan (2006),
Idris-Idram et al. (2002), Idris-Idram et al. (1998/1999), Idris et al. (2002), Isfarain and
Santiyo (1981), Kaneko et al. (1987), Kirnowardoyo et al. (1991, 1992), Lien et al. (1975),
Marsaulina (2008), Nalim et al. (2000), Saleh (2002), Sigit and Kesumawati (1988),
Stoops et al. (2008), Supalin (1981), Suparno (1983), Swellengrebel and Rodenwaldt
(1932), Tativ and Udin (2006), Trenggono (1985), Van Hell (1952), Van Peenen et al.
(1975) and Widjaya et al. (2006).
during first quarter of the night in Sulawesi (Garjito et al., 2004a). When it is
found biting indoors (northern Sumatra), An. nigerrimus usually exits imme-
diately after feeding to rest outdoors (Idris et al., 2002).
An. nigerrimus larvae prefer sunlit habitats containing fresh and clear still
or slow running water (Table 3.4; Takken et al., 1990). Their larval sites
include lake margins (Chow et al., 1959), marshes (Koesoemowinangoen,
1953), pools (Idris-Idram et al., 1998/1999), rice fields (Idris et al., 2002;
Koesoemowinangoen, 1953; Sekartuti et al., 1995a), irrigation channels
(Koesoemowinangoen, 1953) and fishponds (Idris et al., 2002). This species
has been found along the coastal plain to hilly environments at altitudes up to
700 m asl (Stoops et al., 2007).
5.14. Anopheles (Cellia) parangensis (Ludlow)

Anopheles parangensis is a member of the Pyretophorus Series, an assemblage
of mosquitoes that represent important vectors in both Asia and Africa.
The presence of this species was reported by 12 sources at 42 independent
sites (Fig. 3.15), most commonly from Sulawesi (40 sites). One record,
published in the early 1930s, indicated its presence on Ternate, Maluku
(Swellengrebel and Rodenwaldt, 1932). The first record of An. parangensis
from Sumatra was reported by OConnor and Sopa (1981) but with no
details on location. In 2005, this species was found in concrete pools on
Simeulue Island, Aceh, northern Sumatra (Sudomo et al., 2010). Where
present, the density of this species was lower than other biting Anopheles
species in central and southeast Sulawesi (<1%) (Bahang et al., 1981;
Garjito et al., 2004b; Widjaya et al., 2006) but higher in northern Sulawesi
(60%) (Marwoto et al., 2002). P. falciparum sporozoites have been
Figure 3.15 Anopheles parangensis distribution in Indonesia. The blue stars indicate the
records of infectious An. parangensis mosquitoes found. The yellow dots show
(medium red, 5% < PfPR210 < 40%) and high risk (dark red, PfPR210 > 40%) (Elyazar
et al., 2011a). The database of distribution of An. parangensis in Indonesia was acquired
from the references: Bahang et al. (1981), Brug and Bonne-Wepster (1947), De Rook (1929),
Garjito et al. (2004a), Garjito et al. (2004b), Jastal et al. (2003), Marwoto (1995), Marwoto
et al. (2002), Nurdin et al. (2003), Sudomo et al. (2010), Swellengrebel and Rodenwaldt
detected by NAMRU-2 in An. parangensis from Sulawesi, near Manado

(Marwoto et al., 1996) and an EIR of 0.1 infective bites/person/night
was reported from the same locality during the epidemiological investiga-
tion (Marwoto et al., 2002).
The host preference of this species is poorly known in Indonesia and
there is no known study examining the presence of human blood in this
species. Widjaya et al. (2006) observed greater numbers of An. parangensis
females resting in cattle shelters than in houses (95% vs. 5%; n 78) in central
Sulawesi. However, in northern Sulawesi, only 41% (n 7594) of resting
An. parangensis were collected from cattle shelters, together with ratio
of 1:1.6 indoor to outdoor human-landing captures (Marwoto et al.,
2002), indicating a stronger tendency for exophagic behaviour. The larval
stages are found in sunlit habitats containing either fresh or coastal
brackish water (Table 3.4; Koesoemowinangoen, 1953) including marshes
(Koesoemowinangoen, 1953; Nurdin et al., 2003), pools (Bonne-Wepster
and Swellengrebel, 1953; Rodenwaldt, 1925) or man-made habitats, such
as fish ponds (Jastal et al., 2003; Nurdin et al., 2003; Rodenwaldt, 1925)
and ground puddles (Bonne-Wepster and Swellengrebel, 1953).
5.15. Anopheles (Cellia) punctulatus Dnitz

An. punctulatus is one of 12 members of the Punctulatus Group (Sinka et al.,
2011) which also includes the malaria vectors An. farauti s.l. and An. koliensis
(Rozeboom and Knight, 1946). An. punctulatus occurrence data were
extracted from 18 sources and 46 independent sites in Indonesia
(Fig. 3.16). The two reported locations were Papua (23 sites) and Maluku
(21 sites). In Papua, this species is a proven malaria vector of P. falciparum,
P. vivax and P. malariae (Anthony et al., 1992; Bangs et al., 1996;
Metselaar, 1956) and is an important vector in neighbouring PNG
(Cooper et al., 2009). This species has been found infected with
P. falciparum and P. vivax in both southern and northern Papua, from coastal
and lowland inland areas (Armopa, Timika, Arso, Mapurujaya and Tipuka)
and highland (Obio, near Wamena and Oksibil Valley) locations (Bangs and
Rusmiarto, 2007).
An. punctulatus was reported responsible for a malaria outbreak in the high-
lands of Papua in 1989 at an elevation of 1260 m asl (Bangs et al., 1996) where
it was the predominant species (98%; n 2577) biting humans. This species
has also been implicated in transmission in the central highlands of Papua
during a period of extreme drought period (Bangs and Subianto, 1999).
Figure 3.16 Anopheles punctulatus distribution in Indonesia. The blue stars indicate the
records of infectious An. punctulatus mosquitoes found. The yellow dots show 46 records
2011a). The database of distribution of An. punctulatus in Indonesia was acquired from
the references: Anthony et al. (1992), Bangs et al. (1993b), Bangs et al. (1996), Brug and
Bonne-Wepster (1947), De Rook (1929), Kurihara (1978), Lee et al. (1980), Metselaar
(1956), Mulyadi (2010), Pribadi et al. (1998), Rozeboom and Knight (1946), Sari et al.
(2004), Slooff (1964), Suprapto (2010), Sutanto et al. (1999), Swellengrebel and
Rodenwaldt (1932), Syafruddin et al. (2010) and Yamtama et al. (2008).
An. punctulatus usually bites humans outdoors (Van den Assem and Van Dijk,
1958) but when indoor feeding does occur, peak activity is normally before
midnight (second quarter) (Bangs et al., 1996; Lee et al., 1980). After feeding,
this species will typically rest outdoors, including the exterior surfaces of house
walls and amongst surrounding vegetation (Lee et al., 1980; Slooff, 1964).
An. punctulatus larval sites are routinely sunlit containing fresh, clear or tur-
bid water (Table 3.4; Takken et al., 1990). Larvae have been sampled from
freshwater coastal marshes (Takken et al., 1990), low-lying riverine areas
(Takken et al., 1990), riverside pools (Lee et al., 1980), grasslands (Takken
et al., 1990), along jungle edges (Takken et al., 1990), pools (Lee et al.,
1980; Russel et al., 1943; Takken et al., 1990; Van den Assem, 1961; Van
den Assem and Bonne-Wepster, 1964; Van den Assem and Van Dijk,
1958), ground depressions and shallow drainage around houses (Anthony
et al., 1992), rock pools in drying stream beds (Bonne-Wepster and

Swellengrebel, 1953; Church et al., 1995), earthen drains (De Rook,
1929), footprints (Slooff, 1964; Takken et al., 1990), ditches (Anthony
et al., 1992; Lee et al., 1980), pig ruts (Anthony et al., 1992), pits with grey
turbid water (De Rook, 1929; Swellengrebel and Swellengrebel-de Graaf,
1919a) and wheel prints (Slooff, 1964; Takken et al., 1990). Lee et al.
(1987) found the most commonly recorded habitats are man-made depres-
sions (wheel ruts, road site ditches, footprints) holding water temporarily
and exposed to direct sunlight. The water is commonly without vegetation
and may be clear to muddy. Larvae have been found in water of nearly
42 C, indicating a tolerance to high temperatures (Van den Assem, 1961;
Van den Assem and Van Dijk, 1958). This species is found in the lowlands
(Lee et al., 1980; Van den Assem and Van Dijk, 1958) and in hilly and moun-
tainous terrain (Anthony et al., 1992; Slooff, 1964; Van den Assem and
Bonne-Wepster, 1964) at 1500 asl or higher (Anthony et al., 1992).
5.16. Anopheles (Anopheles) sinensis Wiedemann

Anopheles sinensis is a member of the Hyrcanus group of mosquitoes
(Harbach, 2004) and is the second member (An. nigerrimus) of the group that
is a confirmed malaria vector in Indonesia. A total of 13 sources reported the
presence of this species from 32 independent sites across Sumatra, Kaliman-
tan and Sulawesi (Fig. 3.17). An. sinensis was most commonly reported from
Sumatra (30 sites). Boewono et al. (1997a) first documented the mosquito,
including specimens with Plasmodium sporozoites, amongst 1614 examined
by headthorax dissections in Nias, northern Sumatra. An. sinensis normally
appears in low densities compared to other Anopheles mosquito populations
(<1%) in both northern Sumatra (Idris et al., 2002; Lien et al., 1975) and
eastern Kalimantan (Buono, 1987). Although this species appears to play
a relatively minor role in malaria transmission in Indonesia, it is still recog-
nized as a primary vector in Korea and central/northern China
(Harrison, 1973).
The host preferences of An. sinensis in Indonesia is poorly known but is
assumed to be mostly zoophilic. However, studies examining the impact of
cattle presence on human feeding found that in areas with cattle, 83% of
females (n 381) contained human blood, whereas 90% (n 102) contained
human blood in areas where cattle were scarce (Walch, 1932). The author
concluded that this species remained anthropophilic even in the presence of
abundant alternative hosts. However, those mosquitoes examined were
Figure 3.17 Anopheles sinensis distribution in Indonesia. The blue stars indicate the
records of infectious An. sinensis mosquitoes found. The yellow dots show 32 records
2011a). The database of distribution of An. sinensis in Indonesia was acquired from
the references: Boewono et al. (1997b), Brug (1931), Buono (1987), Fryauff et al. (2002),
Idris et al. (2002), Iyana (1992), Kaneko et al. (1987), Kirnowardoyo et al. (1991), Lien
et al. (1975), Nalim (1982), Supalin et al. (1979), Suparno (1983) and Susana (2005).
collected from indoor collections only therefore likely providing a bias sam-
pling. An. sinensis shows exophagic human biting behaviour in northern
Sumatra (Nias Island) where a 1:1.33.5 indoor to outdoor ratio was
reported (Boewono et al., 1997b). The feeding activity has been shown
to peak in the first quarter of night (Ave Lallemant et al., 1932) and with
a flight range of up to 1500 m (Ave Lallemant et al., 1932). We found no
information reporting the specific resting habits of An. sinensis in Indonesia;
however, elsewhere this species appears to mostly rest outdoors in animal
shelters after feeding (Beasles, 1984).
The larval stages of An. sinensis are typically found in sunlit habitats con-
taining fresh clear or stagnant water (Table 3.4; Takken et al., 1990). There is
some evidence of larvae being found in saline or brackish water
(Swellengrebel and Swellengrebel-de Graaf, 1919a, 1920) and it has also been
reported from rice fields where the water temperature exceeded 41 C, indi-
cating a tolerance to high temperatures (Beasles, 1984). Larvae have been
found along lake margins (Bonne-Wepster and Swellengrebel, 1953;

Mangkoewinoto, 1919; Takken et al., 1990), marshes (Bonne-Wepster and
Swellengrebel, 1953; Koesoemowinangoen, 1953; Mangkoewinoto, 1919;
Swellengrebel and Swellengrebel-de Graaf, 1919a, 1920; Takken et al.,
1990; Taylor, 1943), pools (Mangkoewinoto, 1919; Schuurman and
Huinink, 1929; Swellengrebel and Swellengrebel-de Graaf, 1920; Taylor,
1943), small streams (Bonne-Wepster and Swellengrebel, 1953; Schuurman
and Huinink, 1929; Swellengrebel and Swellengrebel-de Graaf, 1919a,
1920; Takken et al., 1990; Taylor, 1943), borrow pits (Bonne-Wepster
and Swellengrebel, 1953; Takken et al., 1990), fish ponds (Swellengrebel
and Swellengrebel-de Graaf, 1920; Taylor, 1943), rice fields (Brug, 1931;
Koesoemowinangoen, 1953; OConnor, 1980; Stekhoven and Stekhoven-
Mayer, 1922; Swellengrebel, 1916; Swellengrebel and Swellengrebel-de
Graaf, 1919a,c, 1920; Takken et al., 1990; Walch, 1924), wells (Taylor,
1943) and irrigation ditches (Bonne-Wepster and Swellengrebel, 1953;
Koesoemowinangoen, 1953; Mangkoewinoto, 1919; Swellengrebel and
Swellengrebel-de Graaf, 1919a, 1920; Takken et al., 1990). An. sinensis has
been recorded in the lowlands (Swellengrebel and Swellengrebel-de Graaf,
1920) and in hilly terrain (Stekhoven and Stekhoven-Mayer, 1924) at altitudes
up to 1100 m asl (Brug, 1931).
5.17. Anopheles (Cellia) subpictus Grassi species complex

Subpictus Complex is a member of Pyretophorus Series (Harbach, 2004)
and is by far the most widely distributed species in Indonesia, being found
from Sumatra to Papua. The Subpictus Complex has been described as con-
sisting of at least four sibling species in India: A, B, C and D (Suguna et al.,
1994). Species A, B and D are generally found in fresh water habitats, while
species B appears restricted to coastal brackish water (Sinka et al., 2011). The
presence of this species complex in Indonesia was documented by 72 sources
at 204 independent sites and was more commonly reported from Java
(74 sites) than any other island (Fig. 3.18). The role of An. subpictus as a
malaria vector in Indonesia (Vector Biology and Control Research Unit)
was first confirmed in the late 1920s when Soesilo found 32 mosquitoes with
sporozoite infections amongst 164 collected (Soesilo, 1928). Sporozoite pos-
itive females have also been reported from the Sikka area (Flores Island) in
the eastern Lesser Sundas (Marwoto et al., 1992a), Sulawesi (Marwoto et al.,
1996, 2002; Van Hell, 1952) and western Lombok (Dasuki and Supratman,
2005). Results from sporozoite CSP-ELISA have found this species infected
Figure 3.18 Anopheles subpictus s.l. distribution in Indonesia. The blue stars indicate the
records of infectious An. subpictus s.l. mosquitoes found. The yellow dots show 204
records of occurrence for this species between 1932 and 2011. Areas were defined
et al., 2011a). The database of distribution of An. subpictus s.l. in Indonesia was acquired
from the following references: Adrial (2003, 2008), Adrial and Harminarti (2005), Ariati
et al. (2007), Arwati et al. (2007), Atmosoedjono et al. (1993), Barbara et al. (2011),
Barodji et al. (1992), Barodji et al. (2004a), Barodji et al. (2004b), Barodji et al. (1998/
1999), Barodji et al. (1999/2000), Barodji et al. (1996), Boesri et al. (2004), Boesri and
Boewono (2006), Brug and Bonne-Wepster (1947), Collins et al. (1979), Dasuki and
Supratman (2005), Dharma et al. (2004), Garjito et al. (2004b), Gundelfinger et al.
(1975), Hoedojo (1992, 19950), Idris-Idram et al. (2002), Idris et al. (2002), Isfarain and
Santiyo (1981), Jastal et al. (2003), Jastal et al. (2001), Kazwaini and Martini (2006),
Kurihara (1978), Lee et al. (1983), Lee et al. (1984), Maekawa et al. (2009a), Maekawa
et al. (2009b), Mardiana et al. (2002), Marjiyo (1996), Marwoto (1995), Marwoto et al.
(2002), Marwoto et al. (1992a), Mogi et al. (1995), Nalim et al. (2000), Ndoen et al.
(2010), Noor (2002), Nurdin et al. (2003), Ompusunggu et al. (1994a), Sari et al. (2004),
Self et al. (1976), Shinta et al. (2003), Sigit and Kesumawati (1988), Soekirno et al.
(2006a), Soekirno et al. (1997), Soekirno et al. (2006b), Stoops et al. (2009a), Stoops
et al. (2008), Stoops et al. (2009b), Sudomo et al. (2010), Sukowati et al. (2001),
Sukowati et al. (2002), Sulistio (2010), Sundararaman et al. (1957), Susana (2005),
Swellengrebel and Rodenwaldt (1932), Syafruddin et al. (2010), Tjitra et al. (1987),
Ustiawan and Hariastuti (2007), Utari et al. (2002), Van Hell (1952), Van Peenen et al.
(1975), Widiarti et al. (2005b) and Yudhastuti (2009).
in northern (Briet et al., 2003) and southern Sulawesi (Selayar Island) and the
Lesser Sundas (Lombok, Flores and Adonara) (Bangs and Rusmiarto, 2007).
An. subpictus s.l. are generally zoophilic throughout most of their range
(Sinka et al., 2011). The proportion of mosquitoes collected from indoor
and outdoor sampling on Java and Sulawesi revealed only 15% (of 2093)
containing human blood (Chow et al., 1959; Collins et al., 1979; Issaris
and Sundararaman, 1954; Noerhadi, 1960; Sundararaman et al., 1957;
Walch, 1932; Walch and Sardjito, 1928). Overall, females tend to be cap-
tured more often from cattle shelters than human houses (Adrial, 2003,
2008; Adrial and Harminarti, 2005; Dasuki and Supratman, 2005; Garjito
et al., 2004b; Mardiana et al., 2002; Noor, 2002) also suggesting stronger
zoophilic tendencies. Where An. subpictus are recorded feeding on humans,
they are generally found feeding outdoors but this can vary depending on
geographic location (Adrial, 2008; Adrial and Harminarti, 2005; Barodji
et al., 1999/2000; Garjito et al., 2004b; Noor, 2002; Ompusunggu et al.,
1994a, 1996; Sukowati et al., 2000; Sundararaman et al., 1957), for example,
in western Java and northern Sulawesi where indoor biting has been
recorded (Issaris and Sundararaman, 1954; Marwoto et al., 2002; Stoops
et al., 2009b). An. subpictus has been shown to bite primarily during the
second half of the night (Adrial, 2008; Adrial and Harminarti, 2005;
Garjito et al., 2004b; Hoedojo, 1992), although in the Lesser Sundas and
Sulawesi, this species is reported to be active during the first half of the night
(Barodji et al., 1999/2000; Collins et al., 1979; Ompusunggu et al., 1994a,
1996; Sukowati et al., 2000).
A number of studies have reported An. subpictus females as endophilic
(Adrial, 2003; Adrial and Harminarti, 2005; Barodji et al., 1999/2000;
Collins et al., 1979; Dasuki and Supratman, 2005). Resting sites include
bed nets (Adrial, 2003; Adrial and Harminarti, 2005), hanging clothes
(Adrial, 2003; Adrial and Harminarti, 2005), interior wall surfaces (Adrial,
2003; Adrial and Harminarti, 2005; Issaris and Sundararaman, 1954) and
ceiling (Issaris and Sundararaman, 1954). However, in western Sumatra, this
species has been found resting outdoors (Adrial, 2008), in bushes and under
shaded trees.
An. subpictus larvae are common in sunlit aquatic habitats containing
either fresh or brackish water (Table 3.4; Takken et al., 1990), including
tidal lagoons and coastal blocked freshwater rivers and streams (Adrial,
2003; Adrial and Harminarti, 2005; Barodji et al., 1999/2000; Garjito
et al., 2004b; Hoedojo, 1992; Marwoto et al., 1992b; Ompusunggu et al.,
1994a,b, 1996; Sekartuti et al., 1995a; Soekirno et al., 1983; Sundararaman
et al., 1957; Takken et al., 1990), marshes (Adrial, 2003; Adrial and
Harminarti, 2005; Jastal et al., 2003; Takken et al., 1990), pools (Bonne-
Wepster and Swellengrebel, 1953; Church et al., 1995; Idris-Idram et al.,
1998/1999; Sekartuti et al., 1995a; Soekirno et al., 1997; Sudomo et al.,
2010), rocky streams (Adrial, 2008; Ompusunggu et al., 1994b), mangrove
forests (Takken et al., 1990), springs (Barodji et al., 1998/1999; Shinta et al.,
2003), rice fields (Darling, 1926; Dharma et al., 2004; Idris-Idram et al.,
1998/1999; Soekirno et al., 1983; Sundararaman et al., 1957; Takken
et al., 1990), fish ponds (Adrial, 2003; Ariati et al., 2007; Idris-Idram
et al., 1998/1999; Jastal et al., 2003; Maekawa et al., 2009a; Sukowati
et al., 2000; Takken et al., 1990), borrow pits (Church et al., 1995), drains
(Church et al., 1995), furrows in gardens (Church et al., 1995), water tanks
(Adrial, 2008; Adrial and Harminarti, 2005; Barodji et al., 1998/1999;
Church et al., 1995; Mardiana et al., 2002), buffalo wallows (Adrial,
2003; Adrial and Harminarti, 2005), brackish ponds (Van den Assem and
Van Dijk, 1958), seaweed ponds (Ariati et al., 2007; Maguire et al., 2005;
Takken et al., 1990) and irrigation ditches (Idris-Idram et al., 1998/1999;
Miyagi et al., 1994; Stoops et al., 2008; Takken et al., 1990). This species
can be found primarily across coastal plains (Ariati et al., 2007; Collins
et al., 1979; Jastal et al., 2003; Marwoto et al., 2002; Miyagi et al., 1994;
Ndoen et al., 2010; Ompusunggu et al., 1994b; Soekirno et al., 1983;
Stoops et al., 2009b; Utari et al., 2002) and much less so in hilly terrain
(Ndoen et al., 2010; Stoops et al., 2007; Utari et al., 2002) up to 700 m asl
(Utari et al., 2002).
5.18. Anopheles (Cellia) sundaicus Rodenwaldt species

complex
The Sundaicus Complex belongs to the Pyretophorus Series (Sinka et al.,
2011) and represents one of the most important malaria vectors in Indonesia.
Sukowati et al. (1996, 1999) first described the cytotypes (forms) A, B and
C of the An. sundaicus complex using both cytogenetics and enzymatic anal-
ysis. Form A was collected from coastal areas in Sumatra and Java, while form
B was mainly collected in the freshwater habitats at South Tapanuli in north-
ern Sumatra (>87% of samples) with fewer found in the brackish water hab-
itats near Purworejo in Central Java (only 10% of samples). Form C was only
found at a coastal location in Asahan, northeastern Sumatra, where all three
forms were sympatric (A 48%, B 15%, C 37%) (Dusfour et al., 2004a).
An. sundaicus form D has been identified only from the Nicobar Islands
in the Indian Ocean (Nanda et al., 2004). Dusfour et al. (2007b) reported
no genetic distinction between the brackish and fresh water forms using
mitochondrial DNA markers (cytochrome oxidase I and cytochrome

b genes), suggesting they were the same species. Their ecological differences
were regarded as adaptations to the prevailing ecology of the area ranging
from strongly brackish to fresh water (Dusfour et al., 2004b). Using the same
markers validated by PCR, Dusfour et al. (2007a) and Dusfour et al. (2007b)
analysed specimens collected from Sumatra and Java and found no similarity
to sympatric forms A, B and C of Sukowati (Sukowati et al., 1999) and
proposed the presence of a new sibling species of the Sundaicus Complex
in Indonesia, designated An. sundaicus E.
The distribution of An. sundaicus s.l. has been reported throughout the
main islands of the archipelago, except Papua, from 79 sources representing
205 independent sites (Fig. 3.19). More sites reported the presence of An.
sundaicus in western Indonesia than the eastern part of the country (73%
vs. 27%). Based on these reports, the complex appears most common in
Sumatra (81 sites), followed by Java (67 sites) although this is likely
influenced by sampling frequency. It has been primarily reported from
coastal lowlands but can extend inland to slightly higher elevations, up to
altitudes of 300 m asl in western Java (Stoops et al., 2007).
The An. sundaicus complex is mainly responsible for malaria transmission
in coastal areas of Indonesia. Mangkoewinoto first identified sporozoites
amongst 31 dissected An. sundaicus s.l. in western Java in 1918
(Mangkoewinoto, 1919). Nalim et al. (2000) identified both P. falciparum
and P. vivax sporozoites in specimens collected from Lampung, southern
Sumatra. Other authors have also confirmed this species as an important
malaria vector in Java (Issaris and Sundararaman, 1954; Mangkoewinoto,
1919; Soesilo, 1928; Sundararaman et al., 1957), Sulawesi (Collins et al.,
1979; Van Hell, 1952) and the Lesser Sundas (Marwoto et al., 1992a)
(Table 3.2), and most recently in western Sumba (An. sundaicus E)
(Bangs, Personal communication, 2012). Results from CSP-ELISA have
found this species infected more often than any other species tested over
a 30-year period across Sumatra (Nias, Sihepeng, Riau/Bintan Island,
Lampung), Java (Pari Island, near Jakarta) and the Lesser Sunda Islands
(Sumbawa, Flores and Adonara Islands) (Bangs and Rusmiarto, 2007).
The females of An. sundaicus have a slightly greater tendency to bite
humans compared to domesticated animals. The compiled human blood
tests for this species revealed 54% of 5928 mosquitoes collected indoors
and outdoors from Sumatra and Java contained human blood (Collins
et al., 1979; Issaris and Sundararaman, 1954; Sundararaman et al., 1957;
Walch, 1932; Walch and Sardjito, 1928) (Table 3.3). The Sundaicus Com-
plex appears to have no clear preferential biting location, exhibiting both
Figure 3.19 Anopheles sundaicus s.l. distribution in Indonesia. The blue stars indicate
the records of infectious An. sundaicus s.l. mosquitoes found. The yellow dots show
et al., 2011a). The database of distribution of An. sundaicus s.l. in Indonesia was acquired
from the references: Adrial (2003, 2008), Adrial and Harminarti (2005), Barbara et al.
(2011), Barodji et al. (2004a), Barodji et al. (2004b), Barodji et al. (1998/1999), Barodji
et al. (1996), Blondine et al. (2004), Blondine et al. (2005), Boesri (1994a), Boewono et al.
(2002a), Boewono et al. (1997b), Brug and Bonne-Wepster (1947), Budasih (1993),
Citroen (1917), Collins et al. (1979), Dharma et al. (2004), Dusfour et al. (2007a), Dusfour
et al. (2007b), Fryauff et al. (2002), Idris-Idram et al. (2002), Idris-Idram et al. (1998/
1999), Idris et al. (2002), Isfarain and Santiyo (1981), Kaneko et al. (1987), Kazwaini and
Martini (2006), Kikuchi et al. (1997), Kirnowardoyo et al. (1993), Kirnowardoyo et al.
(1989), Kirnowardoyo et al. (1991, 1992), Kurihara (1978), Lien et al. (1975), Maekawa
et al. (2009a), Maekawa et al. (2009b), Mardiana et al. (2002), Mardiana et al. (2003),
Marjiyo (1996), Marsaulina (2002, 2008), Martono (1987), Marwoto et al. (1992a), Nalim
et al. (2000), Ndoen et al. (2010), Ompusunggu et al. (1994a), Schuurman and Huinink
(1929), Setyaningrum (2006), Shinta et al. (2003), Soekirno (1990), Soekirno et al.
(2006a), Soekirno et al. (2006b), Soemarto et al. (1980), Stoops et al. (2009a), Stoops
et al. (2008), Stoops et al. (2009b), Subagyo (2006), Sudomo et al. (2010), Sudomo et al.
(1998), Sudomo and Sukirno (1982), Sukowati et al. (2005a), Sukowati et al. (2005b),
Sulistio (2010), Sundararaman et al. (1957), Susana (2005), Swellengrebel (1921),
Swellengrebel and Rodenwaldt (1932), Swellengrebel and Swellengrebel-de Graaf (1920),
Syafruddin et al. (2010), Takagi et al. (1995), Van Hell (1952), Widiarti et al. (2005b),
Widyastuti et al. (1997), Widyastuti et al. (2004), Widyastuti and Widiarti (1992) and
Yudhastuti (2009).
endophagic and exophagic behaviours. However, a stronger exophagic

habit (>60%) has been reported from Sumatra (Adrial and Harminarti,
2005; Isfarain and Santiyo, 1981), Java (Stoops et al., 2009b;
Sundararaman et al., 1957) and western Lesser Sundas (Lombok)
(Budasih, 1993), with a slightly more endophagic habit (54%) seen in the
eastern Lesser Sundas (Barbara et al., 2011). In western Java, biting activity
has been seen to be high during both the first and last quarters of the night
(Stoops et al., 2009b), while in Central Java, feeding activity begins more
slowly, peaking during the second and third quarters of the evening
(Collins et al., 1979; Sundararaman et al., 1957). After feeding, females
may be found resting indoors on clothes, curtains and walls or outdoors,
under shaded tress, rock crevices and bushes (Adrial and Harminarti,
2005; Boesri, 1994a; Sundararaman et al., 1957). Age grading of nearly
1130 An. sundaicus s.l. mosquitoes captured in early morning resting collec-
tions indoors in Sulawesi, identified 96% as fed or gravid, suggesting most
had remained indoors after blood feeding (Collins et al., 1979).
Larvae of the Sundaicus Complex are primarily found in sunlit sites con-
taining either brackish or fresh water (Table 3.4; Dusfour et al., 2004a;
Soemarlan and Gandahusada, 1990). Sites are also generally of low acidity,
varying water depth and with the presence of vegetation (Kirnowardoyo
et al., 1991; Stoops et al., 2007), in particular floating filamentous algae. Exam-
ples include: lagoons (Adrial and Harminarti, 2005; Shinta et al., 2003;
Sudomo et al., 2010), marshes (Isfarain and Santiyo, 1981; Marsaulina,
2008; Sudomo et al., 2010), pools (Adrial and Harminarti, 2005;
Marsaulina, 2008), seasonally blocked streams (Bangs and Atmosoedjono,
1990) and man-made water collections, especially abandoned fish ponds
(Adrial and Harminarti, 2005; Isfarain and Santiyo, 1981; Marsaulina, 2008;
Sudomo et al., 2010), rice fields (Idris et al., 2002; Marsaulina, 2008;
Stoops et al., 2008) and irrigation ditches (Stoops et al., 2008).
5.19. Anopheles (Cellia) tessellatus Theobald

Anopheles tessellatus is within its own group within the Neomyzomyia Series
(Rattanarithikul et al., 2006). The presence of An. tessellatus were docu-
mented by 56 sources at 121 independent sites (Fig. 3.20). The most com-
mon sites were located on Java (39 sites). This species is found throughout
the archipelago, including isolated reports from western Papua (Sorong,
Manokwari) (OConnor and Sopa, 1981). An. tessellatus has been confirmed
as a malaria vector in Sumatra with P. falciparum infected females identified in
Figure 3.20 Anopheles tessellatus distribution in Indonesia. The blue stars indicate the
records of infectious An. tessellatus mosquitoes found. The yellow dots show 121 records
red, 5%< PfPR210 < 40%) and high risk (dark red, PfPR210 40%) (Elyazar et al., 2011a).
The database of distribution of An. tessellatus in Indonesia was acquired from the refer-
ences: Adrial et al. (2000), Atmosoedjono et al. (1993), Bahang et al. (1981), Barbara et al.
(2011), Barodji et al. (1992), Boesri et al. (2004), Boesri and Boewono (2006), Boewono
et al. (1997b), Brug and Bonne-Wepster (1947), Buono (1987), Dasuki and Supratman
(2005), Dharma et al. (2004), Djenal et al. (1987), Fryauff et al. (2002), Gandahusada
(1979), Garjito et al. (2004a), Garjito et al. (2004b), Hasan (2006), Idris-Idram et al. (2002),
Idris-Idram et al. (1998/1999), Idris et al. (2002), Isfarain and Santiyo (1981), Jastal et al.
(2002), Jastal et al. (2001), Kaneko et al. (1987), Lee et al. (1983), Lee et al. (1984),
Maekawa et al. (2009a), Mardiana et al. (2002), Mardiana and Sukana (2005), Mardiana
et al. (2005), Marjiyo (1996), Marwoto et al. (2002), Munif (1994), Munif et al. (2007), Munif
et al. (2003), Nalim (1982), Ndoen et al. (2010), Nurdin et al. (2003), Priadi et al. (1991), Self
et al. (1976), Sigit and Kesumawati (1988), Soekirno et al. (2006a), Soekirno et al. (1997),
Stoops et al. (2009a), Stoops et al. (2009b), Sudomo et al. (2010), Sukowati et al. (2001),
Sulaeman (2004), Suparno (1983), Syafruddin et al. (2010), Trenggono (1985), Van Hell
(1952), Widjaya et al. (2006) and World Health Organization and Vector Biology and
Control Research Unit 2 Semarang (1977).
Nias, northern Sumatra (Boewono et al., 1997a). No other reports were

found incriminating An. tessellatus as a malaria vector on any other of
Indonesias main islands.
An. tessellatus is primarily zoophilic, with the assembled records showing
that only 10% of 182 mosquitoes examined from Sumatra and Java contained
human blood (Chow et al., 1959; Noerhadi, 1960; Walch, 1932; Walch and
Sardjito, 1928). In western Lesser Sundas, where cattle are prevalent, higher
numbers of An. tessellatus were collected from cattle shelters compared to
inside houses (>90%), also suggesting stronger zoophilic tendencies. Feed-
ing behaviour varies by location with more female An. tessellatus found bit-
ing indoors (>60%) in western Java (Stoops et al., 2009b), whereas
exophagic biting appears more common in eastern Indonesia (Sulawesi
and Lombok) (Garjito et al., 2004b; Jastal et al., 2001; Maekawa et al.,
2009b; Sulaeman, 2004; Widjaya et al., 2006). Blood-feeding activity was
also seen to peak during the second quarter of the evening in Sukabumi,
western Java (Stoops et al., 2009b). In Java, females also prefer to rest out-
doors after feeding (Barodji et al., 1992; Munif et al., 2007). An. tessellatus has
been reported in greater densities in coastal compared to upland areas
(Maekawa et al., 2009b; Stoops et al., 2009b).
The larval stages of An. tessellatus can be found in shaded habitats, typ-
ically associated with slow-moving water (Table 3.4; Takken et al., 1990).
This species is usually found in fresh water, but can also tolerate relatively
high salinity (Boyd, 1949). They are also found in ground pools (Sudomo
et al., 2010), rice fields and fish ponds (Mardiana and Sukana, 2005).
5.20. Anopheles (Cellia) vagus Dnitz

An. vagus is the third species in the Indonesia list of important malaria vectors
belonging to the Pyretophorus Series. Similar to An. subpictus, it is broadly dis-
tributed throughout the main islands of the Indonesian archipelago, excluding
Papua (OConnor and Sopa, 1981). The species is also broadly distributed
across much of Asia and it would come as no surprise if it was also a species com-
plex. The presence of this species was reported by 107 sources from 349 inde-
pendent sites (Fig. 3.21), 138 of which were found on Java, followed by 83 sites
on Sumatra. This species has been confirmed as a malaria vector (P. falciparum) in
Central Java (Purworejo, Kokap) (Wigati et al., 2006) and western Timor Island
(Kupang) (Bangs and Rusmiarto, 2007). A morphologically similar but genet-
ically different (putative) species (An. vagus genotype B) has been found infected
in neighbouring Timor-Leste on Timor Island (Cooper et al., 2010). The tax-
onomic status of this genotype remains unclear. Numerous attempts to find
Plasmodium infected An. vagus from Sumatra, Sulawesi, Maluku and other
Lesser Sunda locations has as yet failed to detect the presence of malaria parasites
(Bangs and Rusmiarto, 2007; Boesri, 1994b; Boewono and Nalim, 1996;
Cooper et al., 2010; Hoedojo, 1992, 1995; Lien et al., 1975; Marwoto
et al., 1992a; Nurdin et al., 2003; Soekirno et al., 1997).
Figure 3.21 Anopheles vagus distribution in Indonesia. The blue stars show the records of
infectious An. vagus mosquitoes found. The yellow dots show 349 records of occurrence for
this species between 1931 and 2011. Areas were defined as no risk (light grey, where
PfAPI 0 per 1000 pa), unstable transmission (medium grey, where PfAPI< 0.1 per 1000
pa), low risk (light red, PfPR210 5%), intermediate risk (medium red, 5% < PfPR210 < 40%)
and high risk (dark red, PfPR210 40%) (Elyazar et al., 2011a). The database of distribution of
An. vagus in Indonesia was acquired from the references: Adrial et al. (2000), Alfiah et al. (2008),
Aprianto (2002), Arianti (2004), Atmosoedjono et al. (1993), Atmosoedjono et al. (1975), Bahang
et al. (1981), Barodji et al. (2003), Barodji et al. (2007), Barodji et al. (1992), Barodji et al. (1998/
1999), Blondine et al. (1992), Blondine et al. (1996), Boesri (1994b), Boesri et al. (2004), Boesri and
Boewono (2006), Boewono and Ristiyanto (2004, 2005), Brug (1931), Brug and Bonne-Wepster
(1947), Buono (1987), Dasuki and Supratman (2005), Dharma et al. (2004), Effendi (2002),
Gandahusada (1979), Garjito et al. (2004a), Garjito et al. (2004b), Handayani and Darwin
(2006), Haryanto et al. (2002), Hasan (2006), Hoedojo (1992, 1995), Idris-Idram et al. (1998/
1999), Ikawati et al. (2006), Ikawati et al. (2004), Isfarain and Santiyo (1981), Iyana (1992),
Jastal et al. (2002), Jastal et al. (2001), Kaneko et al. (1987), Kazwaini and Martini (2006),
Kurihara (1978), Lee et al. (1983), Lee et al. (1984), Lestari et al. (2000), Lien et al. (1975),
Maekawa et al. (2009a), Mardiana et al. (2002), Mardiana and Sukana (2005), Mardiana
et al. (2005), Marjiyo (1996), Marwoto et al. (2002), Marwoto et al. (1992a), Mulyadi (2010),
Munif (1990, 1994), Munif et al. (2007), Munif et al. (2003), Nalim, 1980a,b, Nalim (1982),
Ndoen et al. (2010), Noerhadi (1960), Noor (2002), Nurdin et al. (2003), Ompusunggu et al.
(2006), Ompusunggu et al. (1994a), Partono et al. (1973), Priadi et al. (1991), Raharjo et al.
(2007), Raharjo et al. (2006), Santoso (2002), Self et al. (1976), Shinta et al. (2003), Sigit and
Kesumawati (1988), Soekirno et al. (2006a), Soekirno et al. (1997), Stoops et al. (2009a),
Stoops et al. (2008), Stoops et al. (2009b), Sudomo et al. (2010), Sukmono (2002), Sukowati
et al. (2001), Sulaeman (2004), Sundararaman et al. (1957), Suparno (1983), Susana (2005),
Suwasono et al. (1993), Swellengrebel and Rodenwaldt (1932), Syafruddin et al. (2010), Tativ
and Udin (2006), Trenggono (1985), Ustiawan and Hariastuti (2007), Van Hell (1952), Waris
et al. (2004), Widiarti et al. (1993), Widiastuti et al. (2006), Widjaya et al. (2006), Wiganti et al.
(2010), Wigati et al. (2006), Windarso et al. (2008), World Health Organization and Vector
Biology and Control Research Unit 2 Semarang (1977), Yunianto et al. (2002) and Yunianto
et al. (2004).
An. vagus is predominately a zoophilic, exophagic and exophilic species. It

is often found in very high densities compared to other local anophelines. The
combined proportion of mosquitoes having human blood was reported at
45% (820/1806) from studies in Sumatra and Java (Alfiah et al., 2008;
Chow et al., 1959; Noerhadi, 1960; Walch, 1932). In areas where cattle
are readily available hosts, An. vagus is typically found in much higher propor-
tions resting in cattle shelters rather than human structures; for example, in
Central Java (95%) (Barodji et al., 1992), Central Sulawesi (87%) (Garjito
et al., 2004b; Jastal et al., 2001) and Lesser Sundas (99%) (Maekawa et al.,
2009b). More An. vagus were captured at outdoor than indoor locations in
Java (85% of 5212 mosquitoes), Sulawesi (71% of 477) (Barodji et al.,
1992; Hasan, 2006; Stoops et al., 2009b) and Lesser Sundas (78% of 419)
(Maekawa et al., 2009b). In western Java (Stoops et al., 2009b), An. vagus
females blood fed throughout the night, whereas in eastern Java (Chow
et al., 1959), a clear peak was seen in the second quarter of night. Significantly,
more mosquitoes were found resting outdoors than indoors in Central Java
(64% vs. 36%; n 6982) (Barodji et al., 1992), in ground pits and tree poles
in salak (Salacca zallaca) plantations (Alfiah et al., 2008), low bushes
(Handayani and Darwin, 2006), cattle shelters (Handayani and Darwin,
2006) and grassy ditches (Idris-Idram et al., 1998/1999).
An. vagus larval habitats are typically sunlit, containing fresh, stagnant, shal-
low water (Table 3.4). Natural habitats include still margins of streams (Taylor,
1943), river edges (Maekawa et al., 2009a; Schuurman and Huinink, 1929),
small pools near beaches (Lestari et al., 2007; Sudomo et al., 2010) and springs
(Noerhadi, 1960; Raharjo et al., 2007; Shinta et al., 2003). Larvae also can be
found in many man-made habitats, such as rice fields (Boewono and
Ristiyanto, 2005; Brug, 1931; Darling, 1926; Idris-Idram et al., 1998/
1999; Mardiana and Sukana, 2005; Marwoto et al., 1992b; Miyagi et al.,
1994; Sekartuti et al., 1995a), irrigation ditches (Barodji et al., 2007; Idris-
Idram et al., 1998/1999; Mardiana and Sukana, 2005) wheel ruts (Idris-
Idram et al., 1998/1999; Russel et al., 1943) and a variety of artificial con-
tainers such as tyres, drums and upturned small boats. A 12-month longitudi-
nal survey in Sukabumi, West Java recorded the presence of larvae in 464
aquatic habitats, mostly in the lowlands, close to human habitation, and con-
taining water of low salinity and warm temperatures (Stoops et al., 2007). This
species can often be found in great abundance from the coastal plain to low
hilly areas, but predominantly associated with hillside rice fields (<140 m ele-
vation) than coastal areas (95% vs. 5%) (Ndoen et al., 2010). An. vagus had
been found at altitudes up to 1100 m asl in eastern Java (Brug, 1931).
Table 3.1 Natural Plasmodium species infections of Anopheles mosquitoes in Indonesia
Oocyst detection Sporozoite detection Plasmodium infection
Number of Number of Number of Number of
Year of mosquitoes mosquitoes Oocyst mosquitoes mosquitoes with Sporozoite P. P. P. P.
Species samples examined with oocysts rate (%) examined sporozoites rate (%) falciparum vivax malariae ovale
An. aconitus 19172007 8827 115 1.30 17,554 15 0.09 Yes Yes ? ?
An. aitkenii 1919 2 0 0.00
An. 19181931 48 0 0.00 6 0 0.00
albotaeniatus
An. 19172007 1229 2 0.16 489 0 0.00
annularis
An. 19822005 2348 111 4.73 Yes Yes ? ?
balabacensis
An. 19282002 1119 29 2.59 983 2 0.20 ? ? ? ?
bancroftii
An. 19172007 6750 314 4.65 9568 91 0.95 Yes Yes ? ?
barbirostris
An. 19402002 19 1 5.26 22 1 4.55 ? ? ? ?
barbumbrosus
An. crawfordi 19942002 773 0 0.00
An. farauti 19221979 1093 57 5.22 1199 12 1.00 Yes Yes ? ?
An. 19382007 53 5 9.43 2175 2 0.09 Yes ? ? ?
flavirostris
An. hyrcanus 19181929 30,055 682 2.27
An. 19172007 2413 1 0.04 173 0 0.00
indefinitus
An. karwari 19191955 65 0 0.00 685 6 0.88 ? ? ? ?
An. kochi 19172007 7223 89 1.23 2967 1 0.03 Yes Yes ? ?
An. koliensis 19471994 2616 24 0.92 ? Yes ? ?
An. 19181986 3757 324 8.62 89 1 1.12 Yes ? ? ?
leucosphyrus
An. 19531964 7 0 0.00
longirostris
An. 19182007 1289 26 2.02 3504 6 0.17 Yes Yes ? ?
maculatus
An. 19321995 5074 483 9.52 3443 11 0.32 ? ? ? ?
nigerrimus
An. 19392002 2 0 0.00 688 6 0.87 Yes ? ? ?
parangensis
An. 19342007 594 0 0.00
peditaeniatus
Continued
Table 3.1 Natural Plasmodium species infections of Anopheles mosquitoes in Indonesiacont'd
Oocyst detection Sporozoite detection Plasmodium infection
Number of Number of Number of Number of
Year of mosquitoes mosquitoes Oocyst mosquitoes mosquitoes with Sporozoite P. P. P. P.
Species samples examined with oocysts rate (%) examined sporozoites rate (%) falciparum vivax malariae ovale
An. 19171992 1614 1 0.06 10,501 117 1.11 Yes Yes Yes ?
punctulatus
An. sinensis 19171998 29,489 612 2.08 2733 1 0.04 ? ? ? ?
An. 19182007 32,698 130 0.40 88,784 160 0.18 Yes Yes ? ?
subpictus
An. 19172007 49,649 1469 2.96 56,624 169 0.30 Yes Yes ? ?
sundaicus
An. 19192007 2266 4 0.18 838 10 1.18 Yes ? ? ?
tessellatus
An. 19181921 257 16 6.23 25 0 0.00
umbrosus
An. vagus 19192007 10,303 2 0.02 6844 7 0.10 Yes ? ? ?
The ? mark denotes where the Plasmodium species infecting the mosquitoes is unknown. In some instances, the observed oocysts and sporozoites upon dissection might have been derived
from non-human primate or rodent hosts. Yes indicate parasite species was identified using CSP-ELISA.
The database of susceptibility of Anopheles mosquitoes to Plasmodium spp. infections in Indonesia was acquired from the following references:
An. aconitus: Bangs and Rusmiarto (2007), Barodji et al. (2007), Boesri et al. (2004), Boesri and Boewono (2006), Boewono and Ristiyanto (2005), Bosh (1925), Doorenbos (1927, 1931),
Hoedojo (1995), Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Mangkoewinoto (1919), Marwoto et al. (1992a), Nalim et al. (2000), Schuurman and Huinink (1929),
Soesilo (1935), Stoops et al. (2009b), Sundararaman et al. (1957), Swellengrebel and Rodenwaldt (1932), Swellengrebel et al. (1919) and Walch and Walch-Sordrager (1922).
An. aitkenii: Swellengrebel and Swellengrebel-de Graaf (1920).
An. albotaeniatus: Doorenbos (1927, 1931), Mangkoewinoto (1919), Swellengrebel and Rodenwaldt (1932) and Walch and Walch-Sordrager (1922).
An. annularis: Barodji et al. (2007), Boesri (1994b), Boesri and Boewono (2006), Hoedojo (1992, 1995), Kirnowardoyo et al. (1985), Lien et al. (1975), Maekawa et al. (2009b),
Schuurman and Huinink (1929), Soesilo (1935), Stoops et al. (2009b), Swellengrebel and Rodenwaldt (1932), Swellengrebel and Swellengrebel-de Graaf (1920) and Venhuis (1941).
An. balabacensis: Adrial et al. (2000), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono and Ristiyanto (2005), Harbach et al. (1987), Lestari et al. (2007), Maekawa et al.
(2009b), Pranoto and Prasetyo (1990), White (1983) and Wigati et al. (2006).
An. bancroftii: De Rook (1929), Metselaar (1956), Nurdin et al. (2003) and Van den Assem and Bonne-Wepster (1964).
An. barbirostris: Barodji et al. (2007), Boesri (1994b), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono et al. (1997a), Boewono and Ristiyanto (2005), Collins et al.
(1979), Doorenbos (1927, 1931), Gundelfinger et al. (1975), Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Machsoes (1939), Maekawa et al. (2009b),
Mangkoewinoto (1919), Marwoto et al. (2002), Marwoto et al. (1992a), Marwoto et al. (1996), Nalim et al. (2000), Nurdin et al. (2003), Soesilo (1935), Stoops et al. (2009b),
Sukowati et al. (2001), Sukowati et al. (2002), Swellengrebel and Rodenwaldt (1932), Swellengrebel et al. (1919), Swellengrebel and Swellengrebel-de Graaf (1920), Van Hell
(1952), Venhuis (1941), Walch and Walch-Sordrager (1922) and Widjaya et al. (2006).
An. barbumbrosus: Nurdin et al. (2003), Sekartuti et al. (1995b) and Van Hell (1952).
An. crawfordi: Boewono and Nalim (1996), Boewono et al. (1997a), Fryauff et al. (2002) and Nurdin et al. (2003).
An. farauti: Bangs and Rusmiarto (2007), Boyd (1949), De Rook (1929), Lee et al. (1980), Metselaar (1956), Swellengrebel and Rodenwaldt (1932) and Van den Assem and Bonne-
Wepster (1964).
An. flavirostris: Barodji et al. (1998/1999), Boewono and Ristiyanto (2005), Lestari et al. (2007), Maekawa et al. (2009b), Overbeek and Stoker (1938), Stoops et al. (2009b), Sundararaman
et al. (1957), Van Hell (1952), Venhuis (1941) and Wigati et al. (2006).
An. hyrcanus: Swellengrebel and Rodenwaldt (1932).
An. indefinitus: Boewono and Nalim (1996), Kirnowardoyo et al. (1985), Maekawa et al. (2009b), Stoops et al. (2009b), Swellengrebel et al. (1919) and Walch and Walch-Sordrager
(1922).
An. karwari: Metselaar (1956), Swellengrebel and Swellengrebel-de Graaf (1920) and Van den Assem and Bonne-Wepster (1964).
An. kochi: Bangs and Rusmiarto (2007), Barodji et al. (2007), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono et al. (1997a), Boewono and Ristiyanto (2005), Bosh
(1925), Doorenbos (1927, 1931), Fryauff et al. (2002), Hoedojo (1992, 1995), Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Nalim et al. (2000), Sekartuti et al.
(1995b), Soekirno et al. (1997), Soesilo (1935), Stoops et al. (2009b), Sundararaman et al. (1957), Swellengrebel and Rodenwaldt (1932), Swellengrebel et al. (1919), Swellengrebel and
Swellengrebel-de Graaf (1920), Venhuis (1941) and Walch and Walch-Sordrager (1922).
An. koliensis: Bangs et al. (1996), Church et al. (1995), Lee et al. (1980), Metselaar (1956), Pribadi et al. (1998) and Van den Assem and Bonne-Wepster (1964).
An. leucosphyrus: Bosh (1925), Doorenbos (1927), Harbach et al. (1987), Machsoes (1939), McArthur (1951), Swellengrebel and Rodenwaldt (1932), Swellengrebel and Swellengrebel-de
Graaf (1920) and Van Hell (1952).
An. longirostris: Metselaar (1956) and Van den Assem and Bonne-Wepster (1964).
An. maculatus: Barodji et al. (2007), Boesri and Boewono (2006), Boewono and Ristiyanto (2005), Doorenbos (1927, 1931), Kirnowardoyo et al. (1985), Kirnowardoyo et al. (1991),
Lestari et al. (2007), Lien et al. (1975), Maekawa et al. (2009b), Marwoto et al. (1992a), Stoops et al. (2009b), Sundararaman et al. (1957), Swellengrebel and Rodenwaldt (1932),
Swellengrebel and Swellengrebel-de Graaf (1920), Venhuis (1941) and Wigati et al. (2006).
An. nigerrimus: Bangs and Rusmiarto (2007), Boesri (1994b), Boewono and Nalim (1996), Boewono et al. (1997a), Kirnowardoyo et al. (1991), Nalim et al. (2000), Overbeek (1940),
Sundararaman et al. (1957), Swellengrebel and Rodenwaldt (1932), Van Hell (1952) and Venhuis (1941).
An. parangensis: Machsoes (1939), Marwoto et al. (2002), Marwoto et al. (1996) and Nurdin et al. (2003).
An. peditaeniatus: Boewono and Nalim (1996), Boewono et al. (1997a), Lien et al. (1975), Soesilo (1935) and Stoops et al. (2009b).
An. punctulatus: Bangs et al. (1996), Church et al. (1995), Doorenbos (1927, 1931), Lee et al. (1980), Metselaar (1956), Pribadi et al. (1998), Swellengrebel et al. (1919), Swellengrebel and
Swellengrebel-de Graaf (1920), Van den Assem and Bonne-Wepster (1964) and Walch and Walch-Sordrager (1922).
Continued
An. sinensis: Boewono and Nalim (1996), Boewono et al. (1997a), Bosh (1925), Doorenbos (1931), Fryauff et al. (2002), Lien et al. (1975), Mangkoewinoto (1919), Schuurman and
Huinink (1929), Soesilo (1935), Sundararaman et al. (1957), Swellengrebel et al. (1919), Swellengrebel and Swellengrebel-de Graaf (1920), Walch and Walch-Sordrager (1922) and Walch
(1924).
An. subpictus: Barodji et al. (1999/2000), Boesri and Boewono (2006), Collins et al. (1979), Dasuki and Supratman (2005), Gundelfinger et al. (1975), Hoedojo (1992, 1995), Issaris and
Sundararaman (1954), Machsoes (1939), Maekawa et al. (2009b), Mangkoewinoto (1919), Marwoto et al. (2002), Marwoto et al. (1992a), Marwoto et al. (1996), Nalim et al. (2000),
Nurdin et al. (2003), Sekartuti et al. (1995b), Soekirno et al. (1997), Soesilo (1928, 1935), Sukowati et al. (2001), Sundararaman et al. (1957), Swellengrebel and Rodenwaldt (1932),
Swellengrebel et al. (1919), Swellengrebel and Swellengrebel-de Graaf (1920) and Van Hell (1952).
An. sundaicus: Boewono and Nalim (1996), Boewono et al. (1997a), Bosh (1925), Collins et al. (1979), Doorenbos (1931), Fryauff et al. (2002), Isfarain and Santiyo (1981), Isfarain and
Santyo (1981), Issaris and Sundararaman (1954), Kirnowardoyo et al. (1991), Lien et al. (1975), Maekawa et al. (2009b), Mangkoewinoto (1919), Marwoto et al. (1992a), Nalim et al.
(2000), Overbeek and Stoker (1938), Soesilo (1928), Stoops et al. (2009b), Sundararaman et al. (1957), Swellengrebel and Rodenwaldt (1932), Swellengrebel et al. (1919), Swellengrebel
and Swellengrebel-de Graaf (1920), Takken et al. (1990), Van Breemen and Sunier (1919), Van Hell (1952) and Walch (1924).
An. tessellatus: Bangs and Rusmiarto (2007), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono et al. (1997a), Fryauff et al. (2002), Kirnowardoyo et al. (1985),
Machsoes (1939), Maekawa et al. (2009b), Nurdin et al. (2003), Schuurman and Huinink (1929), Soekirno et al. (1997), Soesilo (1935), Stoops et al. (2009b), Sundararaman et al.
(1957), Swellengrebel and Rodenwaldt (1932) and Venhuis (1941).
An. umbrosus: Bosh (1925), Doorenbos (1927, 1931), Kirnowardoyo et al. (1991), Mangkoewinoto (1919), Overbeek and Stoker (1938), Swellengrebel and Rodenwaldt (1932) and
Takken et al. (1990).
An. vagus: Barodji et al. (2007), Boesri (1994b), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono and Ristiyanto (2005), Doorenbos (1927, 1931), Hoedojo (1992,
1995), Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Maekawa et al. (2009b), Marwoto et al. (1992a), Nurdin et al. (2003), Soekirno et al. (1997), Soesilo (1935),
Stoops et al. (2009b), Swellengrebel and Rodenwaldt (1932), Venhuis (1941), Wiganti et al. (2010) and Wigati et al. (2006).
Table 3.2 Natural sporozoite infections of Anopheles mosquitoes from the main islands in Indonesiaa
Year of
Species samples Sumatra Java/Bali Kalimantan Sulawesi Maluku Lesser Sundas Papua
An. aconitus 19182007 0/15 15/17,463 0/76
(0.08)
An. 1918 0/6
albotaeniatus
An. annularis 19342007 0/107 0/283 0/99
An. balabacensis 19822005 4/138 (2.9) 60/1449 47/761 (6.18)
(4.14)
An. bancroftii 19542002 2/983 (0.2)
An. barbirostris 19182007 0/119 0/3263 82/6063 (1.35) 9/123 (7.32)
An. 19402002 1/22 (4.55)
barbumbrosus
An. crawfordi 19942002 0/773
An. farauti 19531979 12/1199 (1.0)
An. flavirostris 19412007 1/1452 (0.07) 1/60 (1.67) 0/663
An. indefinitus 19822007 0/133 0/40
An. karwari 19531955 6/685 (0.88)
An. kochi 19342007 1/1025 (0.1) 0/1864 0/1 0/75 0/2
Continued
Table 3.2 Natural sporozoite infections of Anopheles mosquitoes from the main islands in Indonesiacont'd
Year of
Species samples Sumatra Java/Bali Kalimantan Sulawesi Maluku Lesser Sundas Papua
An. koliensis 19471994 24/2616 (0.92)
An. 19381986 1/85 (1.18) 0/4
leucosphyrus
An. longirostris 19531964 0/7
An. maculatus 19412007 0/13 6/3270 (0.18) 0/213
An. nigerrimus 19391995 3/555 (0.54) 0/1343 8/1545 (0.52)
An. parangensis 19392002 6/688 (0.87)
An. 19342007 0/258 0/336
peditaeniatus
An. punctulatus 19531992 117/10,501
(1.11)
An. sinensis 19191998 1/1660 0/1072 0/1
(0.06)
An. subpictus 19182007 0/678 52/69,702 19/12,996 0/219 89/5189
(0.07) (0.15) (1.72)
An. sundaicus 19182007 6/1480 128/51,701 16/1635 19/1808
(0.41) (0.25) (0.98) (1.05)
An. tessellatus 19342007 10/455 (2.2) 0/283 0/1 0/39 0/60
An. umbrosus 19181991 0/23 0/2
An. vagus 19342007 0/92 7/6562 (0.11) 0/104 0/86
a
Sporozoite infections based on dissections only are presumed to be of human origin, but in some instances (e.g. forest/forest-fringe dwelling vectors) might have been derived from
non-human primate or rodent hosts.
The bold values emphasize the finding of natural sporozoite infections in mosquitoes which confirms the role of those species as malaria vectors.
The database of natural sporozoite infections of Anopheles mosquitoes to Plasmodium spp. infections in Indonesia was acquired from the following references:
An. aconitus: Bangs and Rusmiarto (2007), Barodji et al. (2007), Boesri et al. (2004), Boesri and Boewono (2006), Boewono and Ristiyanto (2005), Doorenbos (1931), Hoedojo (1995),
Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Mangkoewinoto (1919), Marwoto et al. (1992a), Nalim et al. (2000), Soesilo (1935), Stoops et al. (2009b) and
Sundararaman et al. (1957).
An. albotaeniatus: Mangkoewinoto (1919).
An. annularis: Barodji et al. (2007), Boesri (1994b), Boesri and Boewono (2006), Hoedojo (1992, 1995), Kirnowardoyo et al. (1985), Lien et al. (1975), Maekawa et al. (2009b), Soesilo
(1935), Stoops et al. (2009b) and Venhuis (1941).
An. balabacensis: Adrial et al. (2000), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono and Ristiyanto (2005), Harbach et al. (1987), Lestari et al. (2007), Maekawa
et al. (2009b), Pranoto and Prasetyo (1990), White (1983) and Wigati et al. (2006).
An. bancroftii: Metselaar (1956), Nurdin et al. (2003) and Van den Assem and Bonne-Wepster (1964).
An. barbirostris: Barodji et al. (2007), Boesri (1994b), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono et al. (1997a), Boewono and Ristiyanto (2005), Collins et al.
(1979), Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Machsoes (1939), Maekawa et al. (2009b), Mangkoewinoto (1919), Marwoto et al. (2002), Marwoto et al.
(1992a), Marwoto et al. (1996), Nalim et al. (2000), Nurdin et al. (2003), Soesilo (1935), Stoops et al. (2009b), Sukowati et al. (2001), Sukowati et al. (2002), Van Hell (1952), Venhuis
An. barbumbrosus: Nurdin et al. (2003), Sekartuti et al. (1995b) and Van Hell (1952).
An. crawfordi: Boewono and Nalim (1996), Boewono et al. (1997a), Fryauff et al. (2002) and Nurdin et al. (2003).
An. farauti: Bangs and Rusmiarto (2007), Lee et al. (1980), Metselaar (1956) and Van den Assem and Bonne-Wepster (1964).
An. flavirostris: Barodji et al. (1998/1999), Boewono and Ristiyanto (2005), Lestari et al. (2007), Maekawa et al. (2009b), Stoops et al. (2009b), Sundararaman et al. (1957), Van Hell
(1952), Venhuis (1941) and Wigati et al. (2006).
An. indefinitus: Boewono and Nalim (1996), Kirnowardoyo et al. (1985), Maekawa et al. (2009b) and Stoops et al. (2009b).
An. karwari: Metselaar (1956) and Van den Assem and Bonne-Wepster (1964).
An. kochi: Bangs and Rusmiarto (2007), Barodji et al. (2007), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono et al. (1997a), Boewono and Ristiyanto (2005),
Fryauff et al. (2002), Hoedojo (1992), Kirnowardoyo et al. (1985), Lestari et al. (2007), Lien et al. (1975), Nalim et al. (2000), Sekartuti et al. (1995b), Soekirno et al. (1997), Soesilo
(1935), Stoops et al. (2009b), Sundararaman et al. (1957) and Venhuis (1941).
An. koliensis: Bangs et al. (1996), Church et al. (1995), Lee et al. (1980), Metselaar (1956), Pribadi et al. (1998) and Van den Assem and Bonne-Wepster (1964).
An. leucosphyrus: Harbach et al. (1987), Machsoes (1939) and Van Hell (1952).
Continued
An. longirostris: Metselaar (1956) and Van den Assem and Bonne-Wepster (1964).
An. maculatus: Barodji et al. (2007), Boesri and Boewono (2006), Boewono and Ristiyanto (2005), Kirnowardoyo et al. (1985), Kirnowardoyo et al. (1991), Lestari et al. (2007), Lien
et al. (1975), Maekawa et al. (2009b), Marwoto et al. (1992a), Stoops et al. (2009b), Sundararaman et al. (1957), Venhuis (1941) and Wigati et al. (2006).
An. nigerrimus: Bangs and Rusmiarto (2007), Boesri (1994b), Boewono and Nalim (1996), Boewono et al. (1997a), Kirnowardoyo et al. (1991), Nalim et al. (2000), Overbeek (1940),
Sundararaman et al. (1957), Van Hell (1952) and Venhuis (1941).
An. parangensis: Machsoes (1939), Marwoto et al. (2002), Marwoto et al. (1996) and Nurdin et al. (2003).
An. peditaeniatus: Boewono and Nalim (1996), Boewono et al. (1997a), Lien et al. (1975), Soesilo (1935) and Stoops et al. (2009b).
An. punctulatus: Bangs et al. (1996), Church et al. (1995), Lee et al. (1980), Metselaar (1956), Pribadi et al. (1998) and Van den Assem and Bonne-Wepster (1964).
An. sinensis: Boewono and Nalim (1996), Boewono et al. (1997a), Fryauff et al. (2002), Lien et al. (1975), Mangkoewinoto (1919), Soesilo (1935) and Sundararaman et al. (1957).
An. subpictus: Barodji et al. (1999/2000), Boesri and Boewono (2006), Collins et al. (1979), Dasuki and Supratman (2005), Gundelfinger et al. (1975), Hoedojo (1992, 1995), Issaris and
Sundararaman (1954), Machsoes (1939), Maekawa et al. (2009b), Mangkoewinoto (1919), Marwoto et al. (2002), Marwoto et al. (1992a), Marwoto et al. (1996), Nalim et al. (2000),
Nurdin et al. (2003), Soekirno et al. (1997), Soesilo (1928, 1935), Sukowati et al. (2001), Sundararaman et al. (1957) and Van Hell (1952).
An. sundaicus: Boewono and Nalim (1996), Boewono et al. (1997a), Collins et al. (1979), Fryauff et al. (2002), Issaris and Sundararaman (1954), Kirnowardoyo et al. (1991), Lien et al.
(1975), Maekawa et al. (2009b), Mangkoewinoto (1919), Marwoto et al. (1992a), Nalim et al. (2000), Soesilo (1928), Stoops et al. (2009b), Sundararaman et al. (1957) and Van Hell
(1952).
An. tessellatus: Bangs and Rusmiarto (2007), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono et al. (1997a), Fryauff et al. (2002), Kirnowardoyo et al. (1985),
Machsoes (1939), Maekawa et al. (2009b), Nurdin et al. (2003), Soekirno et al. (1997), Soesilo (1935), Stoops et al. (2009b), Sundararaman et al. (1957) and Venhuis (1941).
An. umbrosus: Kirnowardoyo et al. (1991) and Mangkoewinoto (1919).
An. vagus: Barodji et al. (2007), Boesri (1994b), Boesri and Boewono (2006), Boewono and Nalim (1996), Boewono and Ristiyanto (2005), Hoedojo (1992, 1995), Kirnowardoyo et al.
(1985), Lestari et al. (2007), Lien et al. (1975), Maekawa et al. (2009b), Marwoto et al. (1992a), Nurdin et al. (2003), Soekirno et al. (1997), Soesilo (1935), Stoops et al. (2009b), Venhuis
(1941), Wiganti et al. (2010) and Wigati et al. (2006).
Table 3.3 Blood-feeding preference/human blood index of Anopheles malaria vectors in Indonesia
Species or species Year of Total sample giving positive reaction to Total sample contains Human blood
complexa samples blood present human blood index (%)
An. aconitus 19322003 17,762 1551 8.7
An. balabacensis 2003 82 8 9.8
An. bancroftii 1928 51 46 90.0
An. barbirostris 19322003 510 60 11.8
An. farauti s.l. 1962 20 18 90.0
An. flaviirostris 2003 33 3 9.1
An. kochi 19322003 841 89 10.6
An. koliensis 1962 170 126 74.1
An. leucosphyrus 1932 204 202 99.0
An. maculatus s.l. 19322003 425 134 31.5
An. nigerrimus 1958 236 10 7.2
An. punctulatus 19541962 84 67 79.8
An. sinensis 19321954 1157 903 78.0
An. subpictus s.l. 19321976 2093 309 14.8
Continued
Table 3.3 Blood-feeding preference/human blood index of Anopheles malaria vectors in Indonesiacont'd
Species or species Year of Total sample giving positive reaction to Total sample contains Human blood
complex samples blood present human blood index (%)
An. sundaicus 19321976 5928 3188 53.8
An. tessellatus 19321960 182 19 10.4
An. vagus 19322003 1806 820 45.4
a
No human blood index data were found for An. barbumbrosus, An. karwari and An. parangensis.
The database of blood-feeding preference/human blood index of Anopheles malaria vectors in Indonesia was acquired from the following references:
An. aconitus: Alfiah et al. (2008), Barodji et al. (1984a), Boewono et al. (1991), Chow et al. (1959), Joshi et al. (1977), Kirnowardoyo and Supalin (1982), Kirnowardoyo
and Supalin (1986), Noerhadi (1960), Sundararaman et al. (1957), Vector Biology and Control Research Unit (1979a), Walch and Sardjito (1928), Walch (1932),
Widyastuti et al. (2003), World Health Organization and Vector Biology and Control Research Unit 2 Subunit Semarang (1978) and World Health Organization
and Vector Biology and Control Research Unit Semarang (1978).
An. balabacensis: Alfiah et al. (2008).
An. bancroftii: Walch and Sardjito (1928).
An. barbirostris: Alfiah et al. (2008), Chow et al. (1959), Noerhadi (1960), Walch and Sardjito (1928) and Walch (1932).
An. farauti s.l.: Slooff (1964).
An. flavirostris: Alfiah et al. (2008).
An. kochi: Alfiah et al. (2008), Chow et al. (1959), Noerhadi (1960) and Walch (1932).
An. koliensis: Slooff (1964).
An. leucosphyrus: Walch (1932).
An. maculatus s.l.: Alfiah et al. (2008), Noerhadi (1960) and Walch (1932).
An. nigerrimus: Chow et al. (1959).
An. punctulatus: Slooff (1964) and Walch and Sardjito (1928).
An. sinensis: Walch and Sardjito (1928) and Walch (1932).
An. subpictus s.l.: Chow et al. (1959), Collins et al. (1979), Issaris and Sundararaman (1954), Noerhadi (1960), Sundararaman et al. (1957), Walch and Sardjito (1928) and
Walch (1932).
An. sundaicus s.l.: Collins et al. (1979), Issaris and Sundararaman (1954), Sundararaman et al. (1957), Walch and Sardjito (1928) and Walch (1932).
An. tessellatus: Chow et al. (1959), Noerhadi (1960), Walch and Sardjito (1928) and Walch (1932).
An. vagus: Alfiah et al. (2008), Chow et al. (1959), Noerhadi (1960) and Walch (1932).
Table 3.4 The typical larval habitats of Anopheles malaria vectors in Indonesia
Water
Light intensity Water salinity turbidity
Water movement Habitat type
Species or
species complex Sunlit Shaded Brackish Fresh Clear Turbid Stagnant Flowing Natural Man-made
An. aconitus Marshes, lakes, streams, river Rice fields, fish ponds,
beds. irrigation ditches.
An. balabacensis Ground depressions, stream- Puddles, animal wallows,
side rock pools, pools under hoof prints, tyre tracks.
shrubs or low trees, river
banks, seepage.
An. bancroftii Marshes, pools associated Heavily shaded irrigation
with slow streams, creeks and ditches.
rivers, ground pools.
An. barbirostris Lagoons, marshes, pools, Rice fields, fish ponds,
slow running streams, river drainage ditches, wells.
banks, springs.
An. barbumbrosus River banks, clear streams Rice fields.
emerging from jungle areas,
open grassy ravines.
An. farauti s.l. Marshes, lagoons, large and Pools, fish ponds, irrigation
small streams margins and ditches, pig-wallows, garden
floating wood and other pools, tins, drums, coconut
natural debris, river banks. shells, canoes.
An. flavirostris Springs, shaded grassy edges, Rice fields, irrigation
slow-flowing small streams, ditches, wells.
pools.
Continued
Table 3.4 The typical larval habitats of Anopheles malaria vectors in Indonesiacont'd
Water
Light intensity Water salinity turbidity
Water movement Habitat type
Species or
species complex Sunlit Shaded Brackish Fresh Clear Turbid Stagnant Flowing Natural Man-made
An. karwari Marshes, small slow-moving Irrigation canals associated
streams, seepages, ground with rice cultivation.
pools, rock pools, springs.
An. kochi Marshes, pools, small Rice fields, fish ponds,
streams. buffalo wallows, wells,
ditches, hoof prints.
An. koliensis Small streams, ground pools, Pig ruts and wallows, ditches.
riverside ponds, marshes.
An. leucosphyrus Marshes, small streams, Fish ponds, wheel ruts, hoof
seepage springs, jungle pools, prints.
ground depressions.
An. maculatus s.l. Stream-side rock pools, Rice fields, ponds, ditches.
margins of small slow-
moving streams, drying river
beds, ground seepages, small
pools, springs.
An. nigerrimus Lake margins, marshes, Rice fields, irrigation
pools, small streams. channels, large borrow pits.
An. parangensis Coastal marshes, pools. Fish ponds, ground
depressions.
An. punctulatus Freshwater coastal marshes, Foot prints, ditches, pig ruts,
low-lying riverine areas, pits with grey turbid water,
riverside pools, grasslands, wheel ruts.
along jungle edges, pools,
ground depressions, rock
pools in drying stream beds,
earthen drains.
An. sinensis Lake margins, marshes, small Rice fields, borrow pits, fish
streams, bogs, slow-flowing ponds, irrigation ditches.
rivers.
An. subpictus s.l. Tidal lagoons, coastal Rice fields, fish ponds,
blocked freshwater rivers and furrows in gardens, water
streams, marshes, pools, tanks, buffalo wallows,
rocky streams, mangrove brackish ponds, seaweed
forests, springs. ponds, irrigation ditches.
An. sundaicus s.l. Lagoons, marshes, pools, Fish ponds.
seasonally blocked coastal
streams.
An. tessellatus Ground pools. Rice fields, fish ponds.
An. vagus Stagnant margins of streams, Rice fields, irrigation
river edges, small and ditches, wheel ruts, hoof
swallow pools near beaches, prints, artificial containers
springs. (tyres, drums, upturned small
boats).
The mark denote the common habitat characteristics of individual Anopheles malaria vectors.
s.l. (sensu lato) indicates the existence or possibility of more than one sibling species is represented in Indonesia, therefore, collectively expanding the natural- and man-made habitats listed.
6. ANOPHELES SUSCEPTIBILITY TO INSECTICIDES

Seventy-four sources of Anopheles insecticide susceptibility data from
Indonesia were reviewed. Table 3.5 summarizes insecticide resistance
amongst Anopheles mosquitoes in Indonesia including the six insecticides
that are currently recommended by the VCP, Indonesian Ministry of
Health, for indoor residual spraying; five pyrethroids: alpha-cypermethrin,
bifenthrin, deltamethrin, etofenprox, lambda-cyhalothrin and one carba-
mate:bendiocarb (Department Kesehatan, 2003). The assembled data of
insecticide susceptibility tests reveal that resistance to four chemicals
Table 3.5 Insecticide susceptibility of Anopheles malaria vectors in Indonesia

IMCP
Insecticide Anopheles malaria
Insecticide Class 1993 2003 resistancea vector species
Alpha- Pyrethroid No Yes Yes An. barbirostris,
cypermethrin An. sundaicus
Bifentrin Pyrethroid No Yes Yes An. aconitus
Cyflutrin Pyrethroid No No No
Deltamethrin Pyrethroid No Yes Yes An. aconitus,
An. sundaicus
Etofenprox Pyrethroid No Yes No
Lambda- Pyrethroid Yes Yes No
cyhalothrin
Bendiocarb Carbamate Yes Yes Yes An. kochi
Propoxur Carbamate No No No
Fenitrothion Organophosphate Yes No Yes An. aconitus,
An. maculatus,
An. subpictus,
An. sundaicus
Malathion Organophosphate Yes No No
Pirimiphos- Organophosphate Yes No No
methyl
DDT Organochlorine Yes No Yes An. aconitus,
An. koliensis,
An. sundaicus
a
Based on physiological toxicity response tests or presence of kdr (knock-down resistance) gene mutation
in those species marked with .
(alpha-cypermethrin, bifenthrin, deltamethrin and bendiocarb) has been

detected in Indonesian anophelines, specifically An. aconitus, An. barbirostris,
An. kochi and An. sundaicus. Resistance to two other insecticides that
were used prior to 2003, fenitrothion and DDT were also found in five
Anopheles species: An. aconitus, An. koliensis, An. maculatus, An. subpictus
and An. sundaicus.
6.1. Anopheles aconitus

Insecticide resistance in An. aconitus has been known since the early 1960s. In
Indonesia, it was first noted against DDT in Central Java in 1962 (Soerono
et al., 1965). Over 275 sentinel sites were subsequently established to mon-
itor the status of DDT resistance on Java between 1960s and 1970s. These
activities confirmed that DDT resistance in An. aconitus had developed across
the island over time (Joshi et al., 1977; Martono, 1988b; OConnor and
Arwati, 1974; World Health Organization and Vector Biology and
Control Research Unit 2 Semarang, 1977). The long history of DDT use
in the rice fields of Java may have been partially (or primarily) responsible
for the swift development of resistance (OConnor and Arwati, 1974;
Syafruddin et al., 2010). Molecular analysis conducted to assess the presence
of the insecticide-resistant allele (1014F kdr mutation) (Syafruddin et al.,
2010) associated with the resistant phenotype (to organochlorine and pyre-
throid class insecticides) yet the analysis did not detect the allele, albeit only a
small sample of six An. aconitus were tested. In contrast, in southern Sumatra,
two of three An. aconitus examined indicated the existence of the kdr gene,
but again, only a small sample size was tested preventing any definitive con-
clusions being made regarding the distribution of this allele in Indonesia
and its significance in control operations.
An. aconitus has shown resistance against both fenitrothion and
deltamethrin in Indonesia. Fenitrothion resistance was first reported in Central
Java in 1976 (Joshi et al., 1977) and reconfirmed over two decades later, via
molecular analysis of specimens collected in the same region (Widiarti et al.,
2001). The proportions of An. aconitus larvae exhibiting evidence of resistance
were 23% (n 208) in high malaria endemic areas, 19% (n 210) with
medium endemicity, and only 3% (n 199) in low endemic localities, pre-
sumably a reflection of degree of previous exposure in each respective pop-
ulation. Resistance to deltamethrin was first reported in Indonesia within An.
aconitus populations from the northern coast of Central Java in 2003 (Widiarti
et al., 2005a). A mortality rate of only 66% was detected amongst 125 An.
aconitus mosquitoes following exposure with 0.05% deltamethrin for 1 h.
The Indonesian VCP routinely currently conducts insecticide suscepti-

bility tests (standard WHO contact tube tests), mostly in Java, to bifenthrin,
bendiocarb and lambda-cyhalothrin (Winarno, Unpublished data). Resis-
tance to 0.1% concentration of bifenthrin has been documented amongst less
than 50% of tested An. aconitus mosquitoes in Central Java. Exposure to
0.05% lambda-cyhalothrin also showed evidence of resistance in western
Java with a mortality rate of 80%. Resistance has not yet been detected to
0.2% bendiocarb in Java. At the time of writing, we have found no published
evidence of resistance to alpha-cypermethrin and etofenprox.
6.2. Anopheles barbirostris

WHO bioassay tests by the Indonesian VCP reported 7279% mortality
rates after 1-h exposure to 0.05% alpha-cypermethrin from An. barbirostris
collected in Central Java and southern Sumatra (Winarno, Unpublished
data). Tests exposing An. barbirostris from western Java, eastern Lesser Sundas
and northern Sulawesi to 0.2% bendiocarb, 0.05% deltamethrin and 0.05%
lambda-cyhalothrin showed no evidence of resistance (Winarno,
Unpublished data). To date, there are no published accounts of resistance
to etofenprox.
6.3. Anopheles farauti s.l.

No records were found on susceptibility status of this species complex to
residual chemicals. However, use of methoprene (an insect growth regula-
tor) for control of immature stages was found effective for the control of this
species (Maridana et al., 1997).
6.4. Anopheles kochi

The Indonesian VCP have tested of An. kochi for resistance to 0.75% alpha-
cypermethrin, 0.05% lambda-cyhalothrin and 0.1% bendiocarb (Winarno,
Unpublished data) of which only specimens from western Sumatra have
appeared to show low levels of resistance (mortality rate slightly above
70% after 1-h exposure) to 0.1% bendiocarb. No resistance was found to
alpha-cypermethrin in Maluku and lambda-cyhalothrin in eastern
Kalimantan.
6.5. Anopheles koliensis

DDT resistance has been reported in An. koliensis populations from Papua
since the late 1980s (Bangs et al., 1993b). Bioassay tests involving 404
An. koliensis resulted in a mortality rate of over 70% after 1-h exposure to
4% DDT. Further tests using 2-h 4% DDT exposure produced only a 67%
mortality rate within the 24-h holding period. Tests using 1% fenitrothion
and An. koliensis from same locality indicated no resistance to this chemical
(Bangs et al., 1993a). Very little is known about the current insecticide sus-
ceptibility profile of this species in Papua.
6.6. Anopheles maculatus

An. maculatus has been found to be resistant to fenitrothion with biochem-
ical assays indicating resistance in 6% of mosquitoes from Central Java and
27% of mosquitoes near Yogyakarta (Widiarti et al., 2005b). In contrast,
no resistance was observed after 1-h exposure with 0.05% deltamethrin
(Widiarti et al., 2005a) in six districts in Central Java Province and to
0.1% bendiocarb (Barodji et al., 1997) in Yogyakarta, central-south Java.
The VCP conducted bioassay tests for susceptibility to 0.75% alpha-
cypermethrin, 0.05% lambda-cyhalothrin, 0.2% bendiocarb and 4%
DDT (Winarno, Unpublished data) and reported no resistance amongst
specimens tested from all locations in southern Sumatra and both West
and Central Java. At the time of writing, no published resistance to
bifenthrin and etofenprox has been found.
6.7. Anopheles subpictus s.l.

Susceptibility tests to fenitrothion at nine sites in high malaria endemic areas
in Central Java and Yogyakarta revealed that approximately two percent of
An. subpictus larvae showed resistance to organophosphate and carbamate
active ingredients (Widiarti et al., 2005b). Molecular analysis of An. subpictus
from Lampung, southern Sumatra, also documented the existence of the kdr
mutation to organochlorine and pyrethroid class chemicals (Syafruddin
et al., 2010). Tests for susceptibility to 0.75% alpha-cypermethrin, 0.2%
bifenthrin, 0.05% lambda-cyhalothrin and 0.1% bendiocarb found no
evidence of resistance in northern Sumatra, southern Sulawesi, Maluku
and Lesser Sundas (Winarno, Unpublished data). No other published infor-
mation on resistance against other insecticides has been reported for this
species.
6.8. Anopheles sundaicus s.l.

An. sundaicus s.l. was the first species in Indonesia to be reported as having
developed resistance to insecticides and the first evidence of DDT resistance
in Central Java (Chow and Soeparmo, 1956; Martono, 1988b; Soerono
et al., 1965). Bioassay tests amongst 1070 An. sundaicus mosquitoes within
DDT indoor residual spray zones showed only 0.52.2% mortality rates after
exposure to 0.25% DDT (Chow and Soeparmo, 1956). The widespread
use of DDT in agriculture is believed partially responsible for the rapid
appearance of DDT resistance in this area including the broad scale use of
both aerial and ground-based spraying of DDT as a larvicide between
1945 and 1949 (Chow and Soeparmo, 1956). After the last application
of DDT in Indonesia in 1992 (World Health Organization, 1998), nearly
30% of 77 tested mosquitoes continued to demonstrate resistance after
1-h exposure with 4% DDT in southern Sumatra in 2008 (Winarno,
Unpublished data). Furthermore, molecular analysis of An. sundaicus adult
mosquitoes from South Lampung District in southern Sumatra found the
kdr mutation amongst 72.5% (29/40) mosquitoes examined (Syafruddin
et al., 2010). Resistant to alpha-cypermethrin and fenitrothion insecticides
have been detected in this species from the same area. Susceptibility
tests documented 18% resistance amongst 78 mosquitoes after exposure
of 0.005% alpha-cypermethrin (Winarno, Unpublished data) and biochem-
ical tests to fenitrothion revealed 633% of tested mosquitoes from eight
sentinel sites in Central Java were resistant in 2002 (Widiarti et al.,
2005b). To date, no published evidence of resistance bifenthrin and
etofenprox is available.
6.9. Anopheles vagus

Molecular analysis found five out of six mosquitoes of An. vagus examined
from southern Sumatra had the insecticide-resistance allele (kdr) against
pyrethroid and organochlorine class insecticides (Syafruddin et al., 2010).
The VCP conducted susceptibility tests for 0.75% alpha-cypermethrin
and 0.05% lambda-cyhalothrin (Winarno, Unpublished data) and found
no resistance amongst An. vagus specimens collected from sites in Lampung,
Kalimantan and Maluku.
7. OUTLOOK FOR INDONESIAN CHALLENGES

TO MALARIA VECTOR CONTROL
This chapter presents an updated overview of the known geographical
distribution and bionomics of 20 species or species complexes known or
suspected to transmit malaria in Indonesia. A review of the status of insec-
ticide susceptibility of eight malaria vector species also provided to illustrate
what is known in Indonesia and the general paucity of information on this

important topic.
We list here what we consider to be three challenges aimed at better
equipping vector control strategy in Indonesia:
1. Species identification: An updated keys to the anopheline fauna of
Indonesia is crucial to help in understanding the complicated nature
of malaria in Indonesia. The current keys used in much of the reviewed
literature were based on entomological/taxonomical work of decades
ago before the use of molecular species identification was available or
widely used. The variability of morphological characteristics within
and between species, the practical limitations of local keys and the
presence of cryptic species within many of the Anopheles taxa clearly
undermines the effectiveness of relying on morphological identifica-
tion techniques alone. Differences in the biological characteristics of
members of the complexes have also an important bearing on malaria
transmission dynamics. It is, therefore, imperative to determine sibling
species composition and their bionomics as well as their roles in the
transmission of malaria (World Health Organization, 2007a). The
advancement of molecular entomology tools are able to support better
understanding of anopheline species identification and the genetic
structure of anopheline populations (Collins et al., 2000). Additionally,
these molecular tools are also able to detect and distinguish the four
human Plasmodium species in individual mosquitoes or in pools of
up to one hundred mosquitoes in populations with low level parasite
infections (Benedict, 2008).
2. Vector bionomics: Knowing the local Anopheles species and adjusting the
control programme to their particular behaviour is essential if malaria
control and elimination activities in Indonesia are to be successful. In
Indonesia, relatively scant information on vector bionomics and
response to chemical measures is available, often either dated, geograph-
ically patchy or completely lacking. Understanding the feeding behav-
iour, host preference and peak feeding periods may have significant
implications for selecting the most appropriate adult vector control strat-
egies. For example, long-lasting insecticide-treated bed nets might be a
poor investment if the vectors are feeding in the early part of the night or
predominantly outdoors where most of the local human population are
unprotected during the peak transmission period. Consequently, there is
a need for implementing complementary vector control tools that can
target exophagic and early-biting vectors (Bugoro et al., 2011), such
as control of larval production and habitats, house screening and personal

protection (Elyazar et al., 2011b). Other novel methods of control
should be explored such as zooprophylaxis (host diversion) or use of spa-
tial repellents to prevent attack via a behavioural avoidance mechanism
in the vector. Integrated vector control approaches, tailor-made and site-
specific to the local ecology will therefore strengthen efforts to suppress
malaria transmitting mosquitoes (Feachem et al., 2009).
3. Insecticide susceptibility monitoring: The evolving resistance patterns of mos-
quito vectors to insecticides is one of the main challenges facing
insecticide-based malaria VCP in Asia and Indonesia (Kelly-Hope
et al., 2005; Syafruddin et al., 2010; Van Bortel et al., 2008). Resistance
to four of the six recommended insecticides has been reported in four
primary malaria vectors in the country. Therefore, comprehensive mon-
itoring of insecticide susceptibility using standardized tests against the
local main vectors species is needed to ensure the continued viability
and proper use of the chemicals currently available in the malaria control
arsenal (Kelly-Hope et al., 2005; Syafruddin et al., 2010; Van Bortel
et al., 2008).
8. CONCLUSIONS
Vector control interventions require evidence-based strategies using
accurate and current knowledge of the identity, distribution and bionomics
of the key malaria vectors in different localities in the country. This contem-
porary review of the primary anopheline malaria vectors of the Indonesian
archipelago is aimed at providing the Indonesian health authorities and other
organizations responsible for malaria control with the background and
means of better focusing their resources where vector control interventions
will be most effectively applied.
ACKNOWLEDGEMENTS
The assembly of an insecticide susceptibility test national database was possible because of the
generous assistance and collaborative spirit of the Indonesian MoH Vector Control Program.
We thank Dr. Trevor Jones for reviewing and substantially improving the manuscript. We
thank the medical entomologists at the Department of Entomology, U.S. NAMRU-2,
Jakarta, especially Saptoro Rusmiarto and the late Yoyo R. Gionar for generously sharing
their expertise. We also thank to the Library of U.S. NAMRU-2, Jakarta and the Library
of the Eijkman Institute for Molecular Biology, Jakarta for providing us free access to
their collections of scientific literature published in Dutch before 1942. This work is
dedicated to the lasting and fond memory of the late Dr. Soeroto Atmosoedjono, the
man who inspired and trained the majority of modern medical entomologists in Indonesia.
His passion finds expression in this review penned by several of his students.
Author contributions. I. E. compiled the database of Anopheles distribution, bionomics and
insecticide susceptibility status (I. E. and W.). I. E., M. E. S., P. W. G., M. J. B., J. K. B., S. I.
H. contributed to the first and subsequent drafts of the manuscript. S. N. T., A. S., R. K. and
W. provided context regarding the Indonesian vector control strategy. All authors
commented on the final submission of the manuscript.
Funding. I. E. is funded by grants from the University of OxfordLi Ka Shing
Foundation Global Health Program and the Oxford Tropical Network. M. E. S. is
funded by a project grant from the Bill and Melinda Gates Foundation via the VECNet
consortium (http://www.vecnet.org/). M. J. B. is an independent consultant funded by
various private industries. S. I. H. is funded by a Senior Research Fellowship from the
Wellcome Trust (#095066) which also supports P. W. G. S. I. H. also acknowledges
funding support from the RAPIDD program of the Science & Technology Directorate,
Department of Homeland Security, and the Fogarty International Center, National
Institutes of Health. S. N. T., A. S., R. K. and W. are funded by the Indonesian Ministry
of Health. J. K. B. is funded by a grant Vietnam Wellcome Trust Major Overseas
Programme (#B9RJIXO). This work forms part of the output of the Malaria Atlas
Project (MAP, http://www.map.ox.ac.uk), principally funded by the Wellcome Trust,
UK. The funders had no role in study design, data collection and analysis, decision to
publish or preparation of the manuscript.
Competing interests. No competing interests are declared from any of the authors.
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Plasmodium falciparum Malaria Endemicity in Indonesia
in 2010
Iqbal R. F. Elyazar1*, Peter W. Gething2, Anand P. Patil2, Hanifah Rogayah3, Rita Kusriastuti3, Desak M.
Wismarini3, Siti N. Tarmizi3, J. Kevin Baird1,4, Simon I. Hay2*
1 Eijkman-Oxford Clinical Research Unit, Jakarta, Indonesia, 2 Spatial Ecology and Epidemiology Group, Department of Zoology, University of Oxford, Oxford, United
Kingdom, 3 Directorate of Vector-borne Diseases, Indonesian Ministry of Health, Jakarta, Indonesia, 4 Nuffield Department of Clinical Medicine, Centre for Tropical
Medicine, University of Oxford, Oxford, United Kingdom
Abstract
Background: Malaria control programs require a detailed understanding of the contemporary spatial distribution of
infection risk to efficiently allocate resources. We used model based geostatistics (MBG) techniques to generate a
contemporary map of Plasmodium falciparum malaria risk in Indonesia in 2010.
Methods: Plasmodium falciparum Annual Parasite Incidence (PfAPI) data (20062008) were used to map limits of P.
falciparum transmission. A total of 2,581 community blood surveys of P. falciparum parasite rate (PfPR) were identified
(19852009). After quality control, 2,516 were included into a national database of age-standardized 210 year old PfPR data
(PfPR210) for endemicity mapping. A Bayesian MBG procedure was used to create a predicted surface of PfPR210 endemicity
with uncertainty estimates. Population at risk estimates were derived with reference to a 2010 human population count
surface.
Results: We estimate 132.8 million people in Indonesia, lived at risk of P. falciparum transmission in 2010. Of these, 70.3%
inhabited areas of unstable transmission and 29.7% in stable transmission. Among those exposed to stable risk, the vast
majority were at low risk (93.39%) with the reminder at intermediate (6.6%) and high risk (0.01%). More people in western
Indonesia lived in unstable rather than stable transmission zones. In contrast, fewer people in eastern Indonesia lived in
unstable versus stable transmission areas.
Conclusion: While further feasibility assessments will be required, the immediate prospects for sustained control are good
across much of the archipelago and medium term plans to transition to the pre-elimination phase are not unrealistic for P.
falciparum. Endemicity in areas of Papua will clearly present the greatest challenge. This P. falciparum endemicity map
allows malaria control agencies and their partners to comprehensively assess the region-specific prospects for reaching pre-
elimination, monitor and evaluate the effectiveness of future strategies against this 2010 baseline and ultimately improve
their evidence-based malaria control strategies.
Citation: Elyazar IRF, Gething PW, Patil AP, Rogayah H, Kusriastuti R, et al. (2011) Plasmodium falciparum Malaria Endemicity in Indonesia in 2010. PLoS ONE 6(6):
e21315. doi:10.1371/journal.pone.0021315
Editor: Georges Snounou, Universite Pierre et Marie Curie, France
Received April 8, 2011; Accepted May 25, 2011; Published June 29, 2011
Copyright: 2011 Elyazar et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: IE is funded by grants from the University of Oxford-Li Ka Shing Foundation Global Health Program and the Oxford Tropical Network. SIH is funded by a
Senior Research Fellowship from the Wellcome Trust (#079091), which also supports PWG. SIH also acknowledges funding support from the RAPIDD program of
the Science and Technology Directorate, Department of Homeland Security, and the Fogarty International Center, National Institutes of Health. APP is funded by a
grant from the Wellcome Trust (#091835). HR, RK, DMW, SNT are funded by the Indonesian Ministry of Health. JKB is funded by a grant from the Wellcome Trust
(#B9RJIXO). This work forms part of the output of the Malaria Atlas Project (MAP, http://www.map.ox.ac.uk), principally funded by the Wellcome Trust, U.K. The
funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected] (IRFE); [email protected] (SIH)
Introduction human malaria in Indonesia [4] with an estimated 12 million

(621 million) clinical cases of P. falciparum cases each year [5].
The Indonesian archipelago of some 17,000 islands straddles Elyazar et al. [4] detail this complex geography and mosaic of
the equator and stretches 5,200 km from western Malaysia to infection risk which seriously complicates efforts to control malaria
Papua New Guinea and covers a land area of 1.9 million km2 on the archipelago.
(Figure 1) [1]. Seven main islands or island groups comprise the On 28 April 2009, the Indonesian Ministry of Health
nation: Sumatra, Java, Kalimantan, Sulawesi, Maluku, the Lesser announced its plan [6] to reach the pre-elimination stage by
Sundas, and Papua (Figure 1). Indonesia was home to over 230 2020 and to be free of malaria transmission by 2030 [7]. The plan
million people in 2010 [2]. These islands also harbour 20 known states that these objectives would be reached in four distinct stages
anopheline vectors of malaria transmitting all four of the species of (Figure 1) [6]: (stage 1) the Thousand Islands group just north of
Plasmodium that routinely infect humans [3]. By a narrow margin Jakarta, Bali and Batam Islands in 2010; (stage 2) Java, Aceh and
over Plasmodium vivax, P. falciparum is the most common cause of Riau Islands in 2015; (stage 3) Sumatra, West Nusa Tenggara,
PLoS ONE | www.plosone.org 1 June 2011 | Volume 6 | Issue 6 | e21315

Falciparum Malaria Endemicity in Indonesia in 2010
Figure 1. The map of Indonesian provincial administrative boundaries and their elimination objectives. The Indonesian archipelago
consists of 33 provinces and comprises seven main islands: Sumatra, Java, Kalimantan, Sulawesi, Maluku, the Lesser Sundas and Papua. The dashed
lines, Wallace Line [23], separate the Western Indonesia (to left from the line) and Eastern Indonesia regions (to right from the line). The Indonesian
elimination objectives are to be implemented in four stages: (stage 1) The thousand islands (Jakarta), Bali and Batam Islands in 2010; (stage 2) Java,
Aceh and Riau Islands in 2015; (stage 3) Sumatra, West Nusa Tenggara, Kalimantan and Sulawesi in 2020 and (stage 4) Papua, West Papua, East Nusa
Tenggara and Maluku Islands in 2030.
doi:10.1371/journal.pone.0021315.g001
Kalimantan and Sulawesi in 2020 and (stage 4) Papua, West distribution maps in Vietnam for 2010 using zero-inflated Poisson
Papua, East Nusa Tenggara and Maluku Islands in 2030. These regression models in a Bayesian framework from 12 months of P.
efforts require detailed maps of malaria risk to guide the strategic falciparum and P. vivax malaria reported cases from 670 districts. In
distribution of limited fiscal resources, expertise, and, importantly, the Western Pacific, Reid et al. [19] established the baseline of
social and political capital in meeting declared objectives malaria distribution maps prior to an elimination programme on
[6,7,8,9,10,11]. Updates of the baseline map described here will the most malarious province in Vanuatu for 2010 using 220 geo-
be essential as control progresses, thus identifying the main foci of referenced villages. This work reflects increasing demand for
active transmission and bringing focus to efforts to interrupt national level malaria risk maps to help guide malaria control
sources of residual transmission and in limiting importation risk in operations, as well as growing confidence and sophistication of the
areas that have been cleared of malaria. methodologies used to derive useful and operationally relevant
There have been many recent efforts to establish national maps.
contemporary malaria distributions to help optimize malaria This report describes the use of a Bayesian model-based
intervention strategies in Africa, Asia and the Western Pacific. In geostatistics (MBG) approach [20,21] to predict the risk of P.
Africa, Kazembe et al. [12] derived malaria risk maps in Malawi falciparum malaria in Indonesia in 2010 at a spatial resolution of
using data from 73 survey sites across that country between 1977 161 km using the largest assembled contemporary empirical
and 2002. Noor et al. [13] presented P. falciparum malaria evidence for any country in Asia. This collaborative effort between
prevalence maps in Somalia in 2008 at 565 km resolution using the Ministry of Health of the Republic of Indonesia and the
452 community-based parasite prevalence surveys conducted data Malaria Atlas Project (MAP, http://www.map.ox.ac.uk) aims to
between 2005 and 2007. Noor et al. [14] also defined Kenya P. improve national planning for the implementation of malaria
falciparum risk maps at 161 km resolution in 2009 using 2,095 control and elimination strategies. This work currently addresses
malaria surveys sites between 1975 and 2009. Gosoniu et al. [15] only P. falciparum malaria as work on the important P. vivax
have produced Angolan malaria prevalence maps for 2010 at a problem is in progress.
spatial resolution of 161 km resolution using malaria data from 92
survey locations. In Asia, Brooker et al. [16] developed P. vivax Methods
maps in Afghanistan for 2006 at spatial resolution 868 km using
logistic regression models and malaria survey data from 269 Assembling a national database of Plasmodium
endemic villages. Reid et al. [17] constructed P. falciparum risk maps falciparum Annual Parasite Incidence data
for Bangladesh for 2007 at 161 km resolution using Bayesian The collation of Annual Parasite Incidence (API) at the highest
geostatistical logistic regression models and 345 malaria preva- spatial resolution available between 2006 and 2008 was routinely
lence surveys in 2007. Manh et al. [18] produced malaria conducted by the Sub-Directorate of Malaria Control at the

Directorate of Vector-borne Diseases in Jakarta. The reported malaria prevalence. This grid library has recently been described
cases of confirmed P. falciparum malaria per 1,000 population were in detail [32] and includes suites of temporal Fourier analysis
computed for each year by district level and averaged over the (TFA) [33] products deriving from time-series of remotely sensed
number of reporting years. Each PfAPI summary estimate was land-surface temperature, normalized difference vegetation index
mapped by matching it to its corresponding first and second level (NDVI), and middle infra-red (MIR) data from the Advanced
administrative unit in a geographic information system (GIS; Very High Resolution Radiometer (AVHRR) platform [34];
ArcView GIS 9.3, ESRI, 2008). equivalent TFA-processed precipitation products derived from
the WorldClim gridded climatology resource [35]; land cover
Assembling a national database of Plasmodium classifications from the GlobCover project [36]; delineations of
falciparum malariometric prevalence rural and urban areas based on the GRUMP [25] product with
The process of assembling community-based survey estimates of additional stratification of the latter into urban/peri-urban using
parasite prevalence undertaken since 1985 has been described approaches described previously [37]; and finally a bespoke
previously [22]. Searches for PfPR data are an on-going activity of temperature suitability index that captures the dynamic suitability
the Malaria Atlas Project (MAP, http://www.map.ox.ac.uk) and of local ambient temperature regimes to support malaria parasite
were completed for the current study on 1 June 2010. The development within anopheline vectors [35]. All grids were
clipped to a standard regional extent that incorporated Indonesia
completed database was subjected to various levels of exclusion in
and that matched the grids defined for the spatial limits of
order to obtain the final input data set for modelling as follows:
transmission, and subject to an automated pre-processing
removing surveys located only to large (.100 km2) and small
algorithm that used per-pixel resampling and/or nearest neigh-
polygons (.25 km2), removing those surveys that could not be
bour interpolation to ensure identical spatial resolution and
precisely geo-positioned, removing those that could not be
definition of land versus sea pixels.
temporally disaggregated into independent surveys or for which
the date was unknown. The dataset was then stratified into two
regions for descriptive purposes (Figure 1), since western and Defining an optimum suite of environmental covariates
eastern Indonesia are biogeographically distinct regions of the The environmental data library described above consists of
archipelago, typically demarked by the Wallace Line [23]. around 90 potential covariates. A variable selection procedure was
implemented to identify an optimum subset of 20 covariates, a
number chosen to representing an appropriate trade-off between
Assembling Indonesia human population data
gaining maximum informative power from the covariates whilst
The Global Rural Urban Mapping Project (GRUMP) beta
retaining computational feasibility and avoiding over-fitting. The
version provides gridded population counts and population density
Bayesian Information Criteria (BIC) [36,38] is a model compar-
estimates at 161 km spatial resolution for the years 1990, 1995 and
ison metric which provides an objective means of quantifying the
2000, both adjusted and unadjusted to the United Nationsnational
trade-off described above: predictive accuracy (which tends to
population estimates [24,25]. The adjusted population counts for
increase with more covariates) is scored against model parsimony
the year 2000 were projected to 2010 by applying the relevant
(which decreases with more covariates) and an optimum
national urban and rural growth rates by country [26] using
compromise is suggested. A total set-analysis was undertaken
methods described previously [27]. The urban growth rates were
whereby models were built using all possible combinations of 20
applied to populations residing within the GRUMP-defined urban
covariate sets, and the BIC statistic calculated for each. The set
extents [25], and the rural rates were applied elsewhere. National
with the optimum (i.e. lowest) BIC value was then identified.
2010 totals were then adjusted to match those estimated by the
Because of their very large computational expense, this prelimi-
United Nations [28]. These population counts were then stratified
nary analysis could not be conducted using full geostatistical
nationally by age group using United Nations-defined [28]
models and, in line with previous studies [38], was instead based
population age structures for the year 2010 to obtain population
on comparison of simpler non-spatial generalised linear regression
count surfaces for the 05 years, 514 years and $15 years age
models. The final selected suite consisted of the two indicator grids
groups. This population surface was extracted for Indonesia and
defining areas that were urban or peri-urban; the bespoke
aligned to all other spatial data grids used in the analysis.
temperature suitability index; six products from the TFA
processed WorldClim precipitation data; and five, four, and two
Defining the limits of Plasmodium falciparum from the TFA processed AVHRR NDVI, land surface temper-
transmission ature, and MIR data sets, respectively.
Following previously defined protocols [21,29,30], PfAPI data
were mapped to the lowest available administrative unit and used Bayesian space-time geostatistical modelling
to classify areas as either no risk (zero cases over three years), and Building on approaches described previously for global
either unstable or stable risk if the mean annual number of prevalence mapping [21]. The underlying value of PfPR210 in
confirmed cases over three years was lower or higher than 0.1 per 2010, Pf 2P2R2{10 xi , at each location xi was modelled as a
1,000 people per annum respectively. These polygon-based data transformation g: of a spatiotemporally structured field super-
were then rasterised to 161 km spatial grids. A biological model imposed with unstructured (random) variation [xi . The number
that identified areas where low temperatures were likely to of P. falciparum positive responses Ni z from a total sample of Ni
preclude transmission [31] was used to identify further risk-free individuals at each survey location was modelled as a conditionally
areas, and merged onto the same 161 km grid to create a single independent binomial variate given the unobserved underlying
surface defining areas of no risk, unstable, and stable transmission age-standardized PfPR210 value [39]. An age-standardisation
at high spatial resolution. procedure [21,40] was implemented to allow surveys conducted in
participants of any age range to be converted to the epidemio-
Assembling environmental covariates logically informative two-up-to-ten-year age range using an
The MAP maintains a large library of globally mapped algorithm based on catalytic conversion models first adapted for
environmental data that represent potentially useful covariates of malaria by Pull and Grab [41]. Each survey was referenced

temporally using the mid-point (in decimal years) between the The ability of the model to predict the correct endemicity class
recorded start and end months. The spatiotemporal component at un-sampled locations was assessed by (1) using the area of under
was represented by a stationary Gaussian process f xi ,ti with curve (AUC) of a receiver-operating characteristics (ROC) curve
mean m and covariance defined by a spatially anisotropic version and (2) calculating the overall percentage of validation points
of the space-time covariance function proposed by Stein [42]. A predicted to the correct class and those grossly mis-assigned (with a
modification was made to the Stein covariance function to allow low endemicity point being classed as high, and vice-versa). These
the time-marginal model to include a periodic component of assessments indicated the reliability of endemicity class assignment
wavelength 12 months, providing the capability to model seasonal [21,43,44,45]. The interpretation of AUC was defined by
effects in the observed temporal covariance structure. These effects established cut-off values, whereby an AUC of one indicates the
arise when studies performed in different years but during similar model is perfect in differentiating a given endemicity class, values
calendar months have a tendency to be more similar to each other above 0.9 regarded as excellent discrimination and between 0.7
than would be expected in the absence of seasonality. The mean and 0.9 as fair to good discrimination. An AUC value of 0.5
component m was modelled as a linear function of a vector of the represents a model with no ability to differentiate endemicity
final selected suite of twenty environmental covariates, classes above a random allocation.
k : m~bx zbkx: The unstructured component [xi was The ability of the model to generate appropriate credible
represented as Gaussian with zero mean and variance V . Bayesian intervals was tested via a coverage plot. Working through 100
inference was implemented using Markov Chain Monte Carlo to progressively narrower credible intervals (CIs), from the 99% CI to
generate 100,000 samples from the posterior distribution of: the the 1% CI, each was tested by computing the actual proportion of
Gaussian field f xi ,ti at each data location: the unobserved held-out prevalence observations that fell within the predicted CI.
parameters bx ,b, and V as stated above and further unobserved Plotting these actual proportions against each predicted CI level
parameters defining the structure and anisotropy of the exponen- allows the overall fidelity of the posterior probability distributions
tial space-time covariance function. Distances between locations predicted at the held-out data locations to be assessed.
were computed in great-circle distance to incorporate the effect of
the curvature of the Earth, which becomes important for a nation Measuring area and population at risk
as large as Indonesia. Samples were generated from the 2010 The modelled surface defining the limits of stable transmission
annual mean of the posterior distribution of f xi ,ti at each was combined with that defining the binned endemicity classes
prediction location. For each sample of the joint posterior, within this limit to produce a single five-category map delineating
predictions were made using space-time conditional simulation areas within Indonesia: those at zero risk; at risk of unstable
over the 12 months of 2010 {t = 2010Jan, ..., 2010Dec}. These transmission; and those at risk of stable transmission experiencing
predictions were made at points on a regular 161 km spatial grid. infection prevalence of between 0% and 5%; 5% and 40%, and
Model output therefore consisted of samples from the predicted 40% to 100% PfPR210. The quantification of areas within each
posterior distribution of the 2010 annual mean PfPR210 at each category was undertaken by first projecting the predicted class
grid location, which were used to generate point estimates and map from geographic to Mollweide equal area projection in
uncertainty metrics (computed as the mean and standard ArcGIS 9.3. The areas covered by each category were then
deviation, respectively, of the set of posterior samples at each calculated in km2. To derive population at risk within each zone,
pixel). Additionally each pixel was also classified into one of three this categorical map was overlaid with the GRUMP-beta 2010
endemicity classes defined previously [21] as of particular gridded population surface using an exact bespoke algorithm
relevance for control: PfPR210#5%; 5%,PfPR210,40%; written in Fortran90, and the total population living in each risk
PfPR210$40%. Classification was based on the class with the category was calculated. These totals were further disaggregated
highest posterior probability of membership. by provincial level.
Evaluating model performance Results

An empirical model assessment exercise was carried out by first
selecting 10% (252) of the full data set using a spatially de-clustered Summaries of P. falciparum malaria prevalence survey
stratified random sampling algorithm, described previously [21], data
and then re-running the model in full using the remaining 90% A total of 2,581 temporally independent community PfPR were
(2,264) of data to make predictions at the space-time locations of identified nationally from 27 of the 33 P. falciparum malaria
these held-out data. Model performance was then evaluated using endemic provinces from a total of 79 different sources between
three criteria: the ability of the model to (1) predict point-values of 1985 and 2009 (Figure 2). The three data richest provinces were
PfPR210 at un-sampled locations, (2) predict the correct Papua (n = 643), East Nusa Tenggara (n = 516) and Aceh
endemicity class at un-sampled locations and (3) to generate (n = 288). A total of 65 survey locations were excluded from
credible intervals that capture appropriately the uncertainty analysis because they were polygon data (n = 6), could not be geo-
associated with predictions at each location. positioned (n = 6), were longitudinal surveys that could not be
The ability of model to predict point-values of PfPR210 at un- disaggregated temporally (n = 39) or were missing information on
sampled locations was then evaluated by comparing observed the month of survey (n = 14).
values to those predicted (using the posterior mean) by the model Of the remaining 2,516 data points, Table 1 shows the
at the equivalent locations. Assessment was made using three summaries of PfPR by region. The presence of P. falciparum was
summary statistics: (1) the mean prediction error (ME), (2) the observed in 75% of total data points. PfPR was generally higher in
mean prediction absolute error (MAE) and (3) the linear surveys in the eastern than the western region. The majority of the
correlation coefficient. The ME measures the bias of prediction PfPR data incorporated resulted from surveys conducted in 2008
and the MAE measures the accuracy of predictions. The (57%). Most surveys included the upper age.20 years (89%). A
correlation coefficient indicates the linear association between total of 85% of the total number of records resulted from direct
predicted and observed values, which was also visualised using a communication with malaria specialists across Indonesia and with
scatter plot. the Indonesian National Malaria Control Program. Twelve

Figure 2. The spatial limits of Plasmodium falciparum defined by Annual Parasite Incidence and the temperature mask. Areas were
defined as stable (dark grey areas, where PfAPI$0.1 per 1,000 pa), unstable (medium grey areas, where PfAPI,0.1 per 1,000 pa), or no risk (light grey,
where PfAPI = 0 per 1,000 pa). The 2,516 community surveys of P. falciparum prevalence conducted between 01 January 1985 and 31 May 2010 are
plotted.
percent of surveys were geo-positioned by Global Positioning falciparum shows a high degree of heterogeneity ranging from 0.3%
Systems (GPS). Surveys with small sample sizes (n,50) represent- to about 41%. The frequency distribution of both input data and
ed 12% of the total data archived whilst 38% had sample sizes predicted PfPR210 in 2010 for Indonesia were visualised using
between 100 and 500. The median sample size was 187. violin plots (Figure 4). These plots display a smoothed distribution
Microscopy was the most commonly recorded diagnostic tech- of PfPR210 overlaid on a central bar showing median and inter-
nique (66% of all surveys). quartile range values. The median of predicted PfPR210 was
Overall, more malaria surveys were conducted in Eastern regions 11.9% (range 0.4%39.5%).
compared to Western regions (60% vs. 40%). The distribution of P. The map of the predicted malaria endemicity class of PfPR210 is
falciparum malaria surveys was not uniform among main islands in presented in Figure 5. Each pixel was also classified into one of three
the archipelago (Figure 2). The islands of Sumatra (Western), Papua endemicity classes defined previously [21,46] as of particular
(Eastern) and Lesser Sundas (Eastern) were reported as the three relevance for control: PfPR210#5%; 5%,PfPR210,40%;
richest PfPR data islands with proportion of 34.7%, 25.4% and PfPR210$40%. We refer to these as low, intermediate and high
24.6%, respectively. Kalimantan was reported as the island with the stable risk. Of those exposed to stable P. falciparum risk, the largest
sparsest PfPR data (0.8%) followed by Sulawesi (1.2%). In Java area was at low risk (0.967 million km2, 50.8% of total area at risk),
where more districts reported no-risk of malaria, only 4.8% of PfPR followed by intermediate risk (0.216 million km2, 11.4%) and high
data were collected between 1985 and 2009. risk (864 km2, 0.05%). Further regional stratifications of areas at risk
are provided in Table 2 and provincial level estimates in Table S1.
The spatial limits of Plasmodium falciparum transmission
The Plasmodium falciparum malaria risk defined by API and the The estimation of population at risk of Plasmodium
temperature mask is shown in Figure 2. The clear demarcation of falciparum malaria
no P. falciparum risk in the Papuan highland is the most striking Table 2 shows the estimated population at risk of P. falciparum
feature; the aridity mask [21] was not used as it did not modify risk malaria in Indonesia in 2010. We have estimated 132.8 million
in any areas of Indonesia. Of a total land area of 1.9 million km2, people (57.1%) lived at any risk of P. falciparum transmission in
0.2 million km2 (11.4%) was classified at no risk of malaria Indonesia in 2010. Of these, 93.5 million (70.3%) inhabited areas
transmission, 0.5 million km2 (26.4%) as unstable transmission and of unstable and 39.3 million (29.7%) in stable transmission.
1.2 million km2 (62.2%) as stable transmission (Table 2). Further Among those exposed to stable P. falciparum risk the vast majority
regional stratifications of areas at risk are provided in Table 2. were at low risk (36.7 million, 93.3%) with the reminder at
intermediate (2.6 million, 6.6%) and high risk (0.006 million,
The spatial distribution of Plasmodium falciparum malaria 0.01%). Further provincial level estimates of population at risk are
endemicity provided in Table S2.
The continuous predicted surface of P. falciparum is presented in In the Western region, 112.1 million people (54.7%) live at any
Figure 3. In stable transmission areas, the distribution of P. risk of P. falciparum transmission. Of these, 87.9 million (78.5%)

Table 1. Summary of the most important aspects of the PfPR data by main region.
Total records of input data set Western Eastern Total Percentage
(n = 1,013) (n = 1,503) (n = 2,516) (100%)
Number selected for model

Population sample size 264,304 674,753 939,057
Number of PfPR.0 520 1,355 1,875 74.5
Mean (standar deviation) PfPR (%) 3.06 (6.64) 8.14 (9.57) 6.09 (8.87)
Median (range) PfPR (%) 0.16 (061.3) 5.02 (081.7) 2.63 (081.7)
Primary source of PfPR data
Peer reviewed sources 95 150 245 9.7
Unpublished work 819 1,343 2,162 85.9
Reports{ 99 10 109 4.4
Source of spatial coordinates
Personal communication 35 39 74 2.9
GPS 129 165 294 11.7
Encarta 106 142 248 9.9
Combination 661 1,070 1,731 68.8
Other digital gazetteers 36 29 65 2.6
Paper source 4 1 5 0.2
Map 42 57 99 3.9
Time period
19851989 104 12 116 4.6
19901994 58 64 122 4.9
19951999 35 60 95 3.8
20002004 81 115 196 7.8
20052009 735 1,252 1,987 78.9
Upper age sampled
, = 10 18 42 60 2.4
.10 and , = 15 70 10 80 3.2
.15 and , = 20 - 117 117 4.6
.20 925 1,334 2,259 89.8
Diagnostic method
Microscopy 806 866 1,672 66.5
RDT 207 637 844 33.5
Denominator
149 216 72 288 11.5
50100 282 252 534 21.2
101500 305 662 967 38.4
.500 210 517 727 29.9
Median (IQR) 104 (53424) 245 (108725) 187 (84581)
{Ministry of Health reports, theses and other unpublished sources.

doi:10.1371/journal.pone.0021315.t001
inhabited areas of unstable and 24.2 million (21.5%) in stable stable transmission zone, 100% of people in Java lived in low
transmission. Within the area of stable P. falciparum risk, 23.5 endemicity risk, 98.8% in Sumatra and 92.7% in Kalimantan.
million lived in low risk (97.3%) and 0.65 million in intermediate In the Eastern region, 20.7 million (75%) people live at any risk
risk (2.7%). Alternatively, more people in western Indonesia lived of P. falciparum transmission. Of these, 5.5 million (26.7%)
in unstable transmission zone than those of stable transmission inhabited unstable transmission areas and 15.2 million (73.3%)
zone (78% vs 22%). The distribution of the population at risk was stable. Within areas stable P. falciparum risk, 13.2 million (87.1%)
not uniform across the islands of the western region: 80.4 million lived in low risk, 1.9 million (12.8%) in intermediate risk and 0.005
in Java, 23.3 million in Sumatra and 8.5 million in Kalimantan. million (0.04%) in high endemicity risk. In other words, less people
The proportion of unstable to stable risk was 96% vs. 4% in Java, lived in unstable transmission areas than those of stable
38% vs. 62% in Sumatra and 23% vs. 77% in Kalimantan. In the transmission areas (27% vs 73%). All of 10.2 million people lived

Table 2. Areas and population at risk of Plasmodium falciparum malaria in 2010 throughout the Indonesian archipelago.
Area and population at risk Region Total

Western Eastern
Value % Value % Value %

2
Area (km ) 1,153,945 100.0 748,886 100.0 1,902,831 100.0
No-risk 145,516 12.6 71,373 9.5 216,889 11.4
At-risk 1,008,429 87.4 677,513 90.5 1,685,942 88.6
Unstable 402,204 34.9 99,427 13.3 501,631 26.4
Stable 606,225 52.5 578,086 77.2 1,184,311 62.2
PfPR210#5% 588,510 51.0 378,317 50.5 966,827 50.8
5%,PfPR210,40% 17,715 1.5 198,905 26.6 216,620 11.4
PfPR210$40% 0 0 864 0.1 864 0.05
Population 204,915,987 100.0 27,628,308 100.0 232,544,295 100.0
No-risk 92,753,767 45.3 6,912,056 25.0 99,665,823 42.9
At-risk 112,162,220 54.7 20,716,252 75.0 132,878,472 57.1
Unstable 87,994,775 42.9 5,538,611 20.0 93,533,386 40.2
Stable 24,167,445 11.8 15,177,641 54.9 39,345,086 16.9
PfPR210#5% 23,517,672 11.5 13,225,290 47.9 36,742,962 15.8
5%,PfPR210,40% 649,773 0.3 1,946,790 7.0 2,596,563 1.1
PfPR210$40% 0 0 5,561 0.02 5,561 0.02
Free, unstable and stable risk areas were corresponded to PfAPI = 0 per 1,000 pa, 0,PfAPI,0.1 per 1,000 pa and PfAPI$0.1 per 1,000 pa.
Figure 3. The Plasmodium falciparum malaria PfPR210 endemicity map. Model-based geostatistical point estimates of the annual mean PfPR210
for 2010 within the stable spatial limits of P. falciparum malaria transmission, displayed as a continuum of yellow to red from 0%50% (see map legend).
The rest of the land area was defined as unstable risk (medium grey areas, where PfAPI,0.1 per 1,000 pa) or no risk (light grey, where PfAPI = 0 per
1,000 pa).

endemicity risk in Sulawesi, Maluku and Lesser Sundas. However,

in Papua, a high proportion of population at-risk are observed to
be at intermediate risk (50%).
Model performance
Table 3 shows the outcomes of the model validation exercise. In
predicting point-values of PfPR210 at un-sampled locations, the
estimated mean error was 0.08% (in units of PfPR210), indicating
very small systematic bias. Mean absolute error (i.e average model
precision) was estimated at 4.7% PfPR210. The correlation
coefficient between predicted and observed values was 0.77
indicating strong linear agreement (see also the corresponding
scatter plot, Figure 6A). Overall, 77% of held-out data were
predicted to their correct endemicity class. Only 1.2% of points
were assigned to a non-adjacent endemicity class. ROC curves for
each endemicity class are plotted in Figure 6B. The AUC values
were 0.90 for PfPR210#5%; 0.87 for 5%,PfPR210,40% and
0.96 for PfPR210$40%, indicating good or excellent class
discrimination for all classes. Figure 6C shows the coverage plot
comparing predicted to actual credible intervals. The plotted line
Figure 4. Violin plots showing for each region frequency is close to the ideal 1:1 line throughout the range indicating that
distributions of PfPR210 data. The width of each polygon illustrates predicted credible intervals provided an appropriate measure of
the relative frequency of different PfPR210 values. The background is model uncertainty.
coloured to match the endemicity classes shown in Figure 5. The black
central bar indicates the inter-quartile range and white circles indicate
the median values.
Discussion
doi:10.1371/journal.pone.0021315.g004 A Bayesian model-based geostatistical spatial-temporal platform
[21,30] was used to define the spatial limits of P. falciparum and its
at any risk of P. falciparum transmission in Sulawesi, followed by 6.6 endemicity level in Indonesia. The resulting maps at 161 km
million in Lesser Sundas, 1.9 million each in Maluku and Papua. spatial resolution provide a continuous surface of P. falciparum
Uniformly, the proportion of people inhabited in stable transmis- malaria risk from an evidence-base of over 2,500 independent
sion areas among all main islands in this region. Within stable estimates of P. falciparum malaria prevalence. These resulting
transmission, between 84.6% and 99.9% of people lived in low estimates of area and population at risk of P. falciparum represent a
Figure 5. The Plasmodium falciparum malaria PfPR210 predictions stratified by endemicity class. They are categorized as low risk
(PfPR210#5%), intermediate risk (5%,PfPR210,40%) and high risk (PfPR210$40%). The rest of the land area was defined as unstable risk (medium
grey areas, where PfAPI,0.1 per 1,000 pa) or no risk (light grey).

Table 3. Summary of the validation statistics for predicting

point values PfPR210 and endemicity class.
Evaluation measure Indonesia
Predicting point values PfPR210

Mean prediction error 0.08%
Mean absolute prediction error 4.7%
Correlation between the predicted and observed data 0.77
Predicting PfPR210 endemicity class
AUC (#5%) 0.898
AUC (.5% to,40%) 0.866
AUC ($40%) 0.964
Overall % correct 77.2%
#5% classed as $40% (%) 0.3%
$40% classed as#5% (%) 0.9%
refinement and update for Indonesia of an earlier estimate made

for 2007 [21,30]. The substantive difference in methods used to
generate the maps means that a comparison between the two is
not a valid method for tracking change. The operational
importance of such methods in an elimination context is
acknowledged, and specific methods are being developed to
facilitate the process of tracking change in malaria risk over the
time.
P. falciparum maps and the control and elimination

objectives of Indonesia
The maps presented here provide detailed insights into spatially
varying risk that, in turn, can support a range of strategic planning
and wider decision making within the Indonesia Ministry of
Health and among its many partners in malaria control and
elimination. By means of example we discuss here utility with
respect to a comparison of two regions of Indonesia at opposing
ends of the transmission intensity spectrum: Java and Papua.
The three provinces of Java (which exclude the national capital
area of Jakarta and a special administrative area of the city of
Yogyakarta) are densely populated: West Java (42 million), East
Java (39.9 million) and Central Java (35.2 million) (Table S2).
These three provinces contribute 71.6 million people (54%) of
total population at risk of P. falciparum in the whole of Indonesia. In
contrast, the three provinces constitute only 4.9% (83.163 km2) of
the total area at risk (Table S1) with the vast majority living under
unstable transmission (68.9 million; 96.3%). The remainder
inhabit low endemicity areas (2.6 million; 4.7%). Efforts focused
upon Java would result in relatively large gains in reducing the Figure 6. Evaluation of model performance. (A) Scatter plot of
actual versus predicted point-values of PfPR210. (B) Receiver-Operating-
population at risk of P. falciparum malaria in all of Indonesia. This is
Characteristic curves for each PfPR210 endemicity class (PfPR210,5%;
not inconsistent with national plans, both historically and 5%,PfPR210,40%; PfPR210$40%) and associated AUC statistics. (C)
currently, with elimination of malaria from Java planned by Probability-probability plot comparing predicted credible intervals with
2015. The absolute feasibility of this goal would need to be further the actual percentage of true values lying inside those intervals. In the
assessed with additional work [47]. top and bottom plots the 1:1 line is also shown (dashed line) for
The situation of malaria in Papua island is entirely different to reference.
Java. Papua (the western half of the island of New Guinea)
comprises two provinces contributing only 1.4% (1.85 million) of
total population at risk of P. falciparum in the whole of Indonesia, essentially similar. Altogether these two endemicity classes
whilst they occupied over a fifth of total area at risk of P. falciparum contributed 99.7% (1.78 million) of total population at stable risk.
in this country. About 96% of the population at risk inhabited The remainder reside in high risk areas (0.3%). Therefore
areas of stable transmission. Among those exposed to stable risk, maintaining aggressive control in Papua is critical and will be
the proportion of people living in between low and medium risk is necessary to continue for the foreseeable future. It is clear that

similar evidence-based guides will help untangle the complexity of of malaria infection in the Indonesian archipelago and Figures 7
the malaria epidemiology in Indonesia and that this will need to be and 8 produced here will help to indicate the spatial accuracy of
augmented by additional work on morbidity and mortality malaria intensity at detailed tourist destinations. However, the
estimation, as well as on P. vivax malaria. The prospects for information should not be used directly to estimate risk to
elimination of malaria on Papua by 2030 will hinge upon long- individual travellers risk and should never be used as an alternative
term progress in reducing high risk among relatively low numbers to formal travel advice. The risk to malaria infection can
of people scattered across wide and often remote areas. This in substantially differ for different travellers taking into account their
turn depends largely upon broader development of healthcare personal protection and prophylactic measure. The longer they
systems delivering prompt diagnosis and effective treatment, stay in malaria areas, the higher the risk of contracting malaria.
especially at the fringe of reach for such services. Maps like those Precautionary measures to prevent mosquito bites should be
presented here may bring focus to the placement of resources advised although visiting malaria free zones.
aimed at this objective.
Indonesian challenges to control and elimination
Spatial variation in map accuracy Hay et al. [49] suggested a framework of milestones on the path
The precision of the predicted map (Figures 7 and 8) is to malaria elimination in the context of MAP outputs. The five
influenced strongly by the density of data points used for analysis stages and their corresponding endemicity levels include: attack
as well as the inherent variability of the underlying survey data (PfPR210$40%), sustain (PfPR210.5%,40%), transition
[48]. About 85% of PfPR data is supplied by three main islands (PfPR210#5%), consolidate (PfAPI,0.01) and maintain
(Sumatra, Papua and Lesser Sundas) which covered 48.7% of 1.68 (PfAPI = 0). In attack and sustain phases, the suggested actions
million km2 of area at risk of P. falciparum in Indonesia. However, are aggressive, combined and extensive interventions, such as total
only two percent of total PfPR data was assembled from two coverage of artemisinin combination therapies (ACTs), insecticide
islands (Kalimantan and Sulawesi) which occupied 40.9% of total treated nets (ITNs), indoor residual spraying, and intermittent
area at risk. These maps can help direct future parasitological preventive treatment. When PfPR210#5%, specific and targeted
surveys to areas of maximal uncertainty. At the time of writing, intervention should be implemented, guided by efficient active and
The Global Fund for AIDS, Tuberculosis and Malaria has funded passive case detection through surveillance and foci of deliberate
the Indonesian Ministry of Health to conduct a series of malaria control measures. In the consolidation phase, the foci of infection
surveys covering 51 of 128 districts in Kalimantan and Sulawesi must be eliminated through sustained specific and targeted
Islands. The assembled data described here guided that commit- interventions. After the malaria-free stage is achieved, the ability
ment of survey resources. Future maps, informed by additional to detect cases and respond with ACT therapies and other
and well-placed data gathering, will similarly do so and yield measures, e.g., vector control, will be absolutely necessary.
increasingly reliable distributions of risk. Adapting such a generic schema to an Indonesia-specific
The reliable distribution of local risk can facilitate travel context is required to make progress and this adaptation is on-
medicine professionals and travellers in their assessment of the risk going. The obstacles and opportunities of malaria control in
Figure 7. The standard deviation map of predicted PfPR2-10 within the stable transmission areas. These values indicate an index of
relative uncertainty. Dark blue areas represent where predictions were made with large uncertainty. Yellow areas represent where predictions were
made with small uncertainty.


Figure 8. The predicted probability of PfPR210 falling in each endemicity class within the Plasmodium falciparum stable transmission
areas. (A) The map of predicted probability of PfPR210 falling in the PfPR210#5% endemicity class. (B) The map of predicted probability of PfPR210
falling in the 5%,PfPR210,40% endemicity class. (C) The map of predicted probability of PfPR210 falling in the PfPR210$40% endemicity class.
Indonesia have been recently described in detail [4] and include other possible interventions aimed at reducing human-anopheline
case detection and surveillance, diagnosis, treatment, and vector contact. The selection and investment in specific tools for doing so
control. In addition to substantially increasing access to diagnostic hinges upon the distribution, density, behaviour and physiology
services, the establishment of a robust quality assurance program (i.e., resistance to insecticides) of the local anopheline species. The
in support of such services may be essential [50]. Progress in combination of sub-national endemicity maps with maps of the
diagnostics is certainly required to to overcome the high distribution of the dominant Anopheles vectors of malaria could
proportion of clinically diagnosed malaria cases (87%) [4]. The empower malaria control managers to formulate evidence-based
persistent use of chloroquine or sulfadoxine/pyrimethamine, both intervention strategy appropriate to the bionomics of their local
known to be widely ineffective, to treat clinically diagnosed vectors [21,58]. This is another significant area of on-going
malaria should be immediately minimized and ultimately activity.
abandoned. This requires aggressive strategies for expanding the The assembled survey data described in this report also revealed
reach of reliable diagnostic services. the almost ubiquitous presence of P. vivax malaria in Indonesia.
The biological complexity of P. vivax relative to P. falciparum
Future work imposes obstacles to mapping endemicity [29,30] but the 1,732
There are inherent uncertainties in any use of routine malaria data points in hand for this parasite represent a wealth of
case reports to measure risk, driven largely by the completeness information for working through the technical challenges. That
and representativeness of data sources [18,51]. While biological important work is in progress. Malaria elimination aims at all
masks can help differentiate areas of incomplete reporting from species and the fielding of interventions effective against that
areas of true zero risk, significant efforts will need to be devoted biological range will provide conspicuous and likely necessary
into improving the precision of our estimates in low transmission economies of scale in reaching success.
zones. It is certainly true that people charged with conducting
blood surveys in search of malaria parasites are guided by instinct
Supporting Information
and information to areas where they are most likely to be found.
Overcoming this tendency will become especially important as Table S1
Indonesia progresses towards elimination. (DOCX)
The population at risk estimates represent the denominator in
Table S2
deriving morbidity and mortality estimates [52]. Hay et al. [5]
presented a new cartographic technique to estimate national, (DOCX)
regional and global scales of clinical burden of P. falciparum
malaria. A modelled relationship between prevalence and clinical Acknowledgments
incidence [53], together with P. falciparum malaria endemicity The national assembly of parasite prevalence surveys was dependent on the
maps were used to estimate incidence in areas of stable generous contributions of data by a large number of people in the malaria
transmission. Geostatistical joint simulation was then used to research and control communities, and these individuals are listed on the
quantify uncertainty in these estimates. However, this work did not MAP website (http://www.map.ac.uk/acknowledgements.html). We thank
provide sub-national level estimates and deriving these would help Catherine Moyes for comments and Jennie Charlton for proofreading this
the Indonesian malaria control agencies forecasting the area- paper. The authors additionally acknowledge the support of the colleagues
specific requirements for antimalarial drugs, and thereby minimize from the Sub-Directorate of Indonesian Malaria Control including
Achmad Farchanny, Adhi Sambodo, Ali Romzan, Aris Munanto, Bangkit
both health-costly stock-outs and financially costly loss of therapies
Hutajulu, Budi Pramono, Charles Tobing, Elvieda Samoedro, Niken W.
to expiration [54]. Palupi, Nur Asni and Saktiyono. The authors also thank the support of the
The population at risk estimates will allow malaria control Eijkman Institute of Molecular Biology, Jakarta.
managers to tailor vector control interventions. This can help
forecast the number of long-lasting insecticide treated nets (LLINs)
Author Contributions
that need to be procured and distributed [55]. The cost estimates
of scaling up LLIN coverage can also be calculated [56]. This Conceived and designed the experiments: IE SIH. Performed the
LLIN intervention has important implications in those areas where experiments: PWG APP. Analyzed the data: IE. Contributed reagents/
materials/analysis tools: PWG APP. Wrote the paper: IE SIH JKB.
the interruption of malaria transmission could be achieved with
Assembled and managed the PfAPI data: HR IE. Provided context
universal coverage of LLIN in medium transmission intensity regarding the Indonesian malaria control strategy: RK DMW SNT.
(PfPR210,40%) [49,57]. However, the distribution of the Commented on the final draft of the manuscript: IE PWG APP HR RK
Anopheles vectors and their bionomics need evaluating before the DMW SNT JKB SIH.
scale up any LLIN intervention. This is also true of the myriad
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Table S1. Areas at risk of Plasmodium falciparum malaria in Indonesia by provincial, main islands and region level in 2010.
Risk area (km2) Total area

Province
No risk Unstable Stable PfPR2-10 < 5% 5% < PfPR2-10 < 40% PfPR2-10 > 40% (km2)
Western 145,516 402,204 606,225 588,510 17,715 0 1,153,945
Sumatra 96,790 156,673 223,048 221,529 1,519 0 476,511

Aceh 7,930 6,351 42,787 41,642 1,145 0 57,068
Sumatra Utara 36,276 5,217 30,357 30,251 106 0 71,850
Sumatra Barat 13,524 21,976 6,295 6,284 11 0 41,795
Riau 1,618 63,619 24,799 24,799 0 0 90,036
Kepulauan Riau 0 0 9,021 9,021 0 0 9,021
Jambi 2,347 25,101 21,981 21,807 174 0 49,429
Bengkulu 1,156 13,013 9,655 6,932 23 0 21,124
Sumatra Selatan 24,287 89 61,793 61,765 28 0 86,169
Bangka Belitung 358 0 15,952 15,952 0 0 16,310
Lampung 9,294 21,307 3,108 3,076 32 0 33,709
Java/Bali 41,854 90,629 6,231 6,231 0 0 138,714

Jakarta 681 0 0 0 0 0 681
Banten 3,374 6,013 0 0 0 0 9,387
1
Province
Jawa Barat 14,000 23,162 0 0 0 0 37,162

Jawa Tengah 4,947 27,318 2,086 2,086 0 0 34,351
Yogyakarta 10 2,547 604 604 0 0 3,161
Jawa Timur 17,710 27,921 2,677 2,677 0 0 48,308
Bali 1,132 3,668 864 864 0 0 5,664
Kalimantan 6,872 154,902 376,946 360,750 16,196 0 538,720

Kalimantan Barat 1,685 5,926 140,432 140,424 8 0 148,043
Kalimantan Tengah 593 35,445 118,501 118,107 394 0 154,539
Kalimantan Selatan 1,015 4,047 32,521 17,006 15,515 0 37,583
Kalimantan Timur 3,579 109,484 85,492 85,213 279 0 198,555
Eastern 71,373 99,427 578,086 378,317 198,905 864 748,886
Sulawesi 30,349 86,853 71,028 71,013 15 0 188,230

Sulawesi Utara 96 0 14,687 14,672 15 0 14,783
Gorontalo 6,430 275 5,454 5,454 0 0 12,159
Sulawesi Tenggara 1,515 31,167 4,437 4,437 0 0 37,119
Sulawesi Barat 2,148 13,222 991 991 0 0 16,361
2
Province
Sulawesi Tengah 5,011 11,958 44,264 44,264 0 0 61,233

Sulawesi Selatan 15,149 30,231 1,195 1,195 0 0 46,575
Maluku 504 0 78,509 65,875 12,634 0 79,013

Maluku 487 0 46,471 37,465 9,006 0 46,958
Maluku Utara 17 0 32,038 28,410 3,628 0 32,055
Lesser Sundas 1,630 0 64,803 52,236 12,567 0 66,433

Nusa Tenggara Barat 1,358 0 18,526 18,523 3 0 19,884
Nusa Tenggara Timur 272 0 46,277 33,713 12,564 0 46,549
Papua 38,890 12,574 363,746 189,193 173,689 864 415,210

Papua 35,608 12,574 269,681 126,723 142,094 864 317,863
Papua Barat 3,282 0 94,065 62,470 31,595 0 97,347
Indonesia 216,889 501,631 1,184,311 966,827 216,620 864 1,902,831
3
Table S2. Population at risk of Plasmodium falciparum malaria in Indonesia by provincial, main islands and region level in 2010.
Population (people) Total

Region/Province population
No risk Unstable Stable 0%< PfPR2-10 <5% 5%< PfPR2-10 <40% PfPR2-10 >40%
(people)
Western 92,753,767 87,994,775 24,167,445 23,517,672 649,773 0 204,915,987
Sumatra 22,425,463 8,850,714 14,451,840 14,278,834 173,006 0 45,728,017

Aceh 854,080 140,671 2,879,917 2,776,794 103,123 0 3,874,668
Sumatra Utara 9,750,071 726,676 2,579,869 2,544,255 35,614 0 13,056,616
Sumatra Barat 2,847,845 1,491,937 100,563 100,448 115 0 4,440,345
Riau 893,711 2,235,767 859,715 859,715 0 0 3,989,193
Kepulauan Riau 0 0 1,219,190 1,219,190 0 0 1,219,190
Jambi 800,579 931,711 791,463 783,587 7,876 0 2,523,753
Bengkulu 276,492 782,066 483,820 483,304 516 0 1,542,378
Sumatra Selatan 3,490,456 85,793 3,749,463 3,746,572 2,892 0 7,325,713
Bangka Belitung 164,738 0 739,955 739,955 0 0 904,693
Lampung 3,347,491 2,456,093 1,047,884 1,025,014 22,870 0 6,851,468
Java/Bali 67,047,647 77,173,997 3,220,112 3,220,112 0 0 147,441,756

Jakarta 12,523,487 0 0 0 0 0 12,523,487
Banten 8,103,144 1,985,916 0 0 0 0 10,089,060
1
Province population
No risk Unstable Stable 0% < PfPR2-10 < 5% 5 % < PfPR2-10 < 40% PfPR2-10 > 40%
(people)
Jawa Barat 25,129,619 16,926,878 0 0 0 0 42,056,497

Jawa Tengah 5,184,617 28,526,288 1,493,949 1,493,949 0 0 35,204,854
Yogyakarta 3,688 3,372,344 353,670 353,670 0 0 3,729,702
Jawa Timur 15,328,777 23,537,524 1,121,942 1,121,942 0 0 39,988,243
Bali 774,315 2,825,047 250,551 250,551 0 0 3,849,913
Kalimantan 3,280,657 1,970,064 6,495,493 6,018,726 476,767 0 11,746,214

Kalimantan Barat 927,565 233,352 2,940,593 2,940,297 296 0 4,101,510
Kalimantan Tengah 57,002 176,962 1,526,361 1,511,421 14,940 0 1,760,325
Kalimantan Selatan 1,367,435 422,531 1,485,498 1,025,365 460,133 0 3,275,464
Kalimantan Timur 928,655 1,137,219 543,041 541,643 1,398 0 2,608,915
Eastern 6,912,056 5,538,611 15,177,641 13,225,290 1,946,790 5,561 27,628,308
Sulawesi 5,168,936 5,470,351 4,800,531 4,798,886 1,645 0 15,439,818

Sulawesi Utara 4,701 0 2,140,889 2,139,244 1,645 0 2,145,590
Gorontalo 174,384 173,575 497,286 497,286 0 0 845,245
Sulawesi Tenggara 311,887 1,229,676 260,800 260,800 0 0 1,802,363
Sulawesi Barat 145,211 625,637 92,963 92,963 0 0 863,811
2
Province population
No risk Unstable Stable 0% < PfPR2-10 < 5% 5 % < PfPR2-10 < 40% PfPR2-10 > 40%
(people)
Sulawesi Tengah 298,205 157,262 1,714,339 1,714,339 0 0 2,169,806

Sulawesi Selatan 4,234,548 3,284,201 94,254 94,254 0 0 7,613,003
Maluku 5,189 0 1,949,145 1,649,279 299,866 0 1,954,333

Maluku 3,519 0 1,218,172 1,079,806 138,366 0 1,221,691
Maluku Utara 1,670 0 730,973 569,473 161,500 0 732,643
Lesser Sundas 1,410,305 0 6,643,165 5,890,218 752,947 0 8,053,470

Nusa Tenggara Barat 1,367,195 0 2,788,796 2,788,778 18 0 4,155,991
Nusa Tenggara Timur 43,110 0 3,854,369 3,101,440 752,929 0 3,897,479
Papua 327,626 68,260 1,784,800 886,907 892,332 5,561 2,180,685

Papua 307,133 68,260 1,262,771 520,074 737,136 5,561 1,638,164
Papua Barat 20,493 0 522,029 366,833 155,196 0 542,522
Indonesia 99,665,823 93,533,386 39,345,086 36,742,962 2,596,563 5,561 232,544,295
3
Plasmodium vivax Malaria Endemicity in Indonesia in
2010
Iqbal R. F. Elyazar1*, Peter W. Gething2, Anand P. Patil2, Hanifah Rogayah3, Elvieda Sariwati3,
Niken W. Palupi3, Siti N. Tarmizi3, Rita Kusriastuti3, J. Kevin Baird1,4, Simon I. Hay2
1 Eijkman-Oxford Clinical Research Unit, Jakarta, Indonesia, 2 Spatial Ecology and Epidemiology Group, Department of Zoology, University of Oxford, Oxford, United
Kingdom, 3 Directorate of Vector-Borne Diseases, Indonesian Ministry of Health, Jakarta, Indonesia, 4 Centre for Tropical Medicine, Nuffield Department of Medicine,
University of Oxford, Oxford, United Kingdom
Abstract
Background: Plasmodium vivax imposes substantial morbidity and mortality burdens in endemic zones. Detailed
understanding of the contemporary spatial distribution of this parasite is needed to combat it. We used model based
geostatistics (MBG) techniques to generate a contemporary map of risk of Plasmodium vivax malaria in Indonesia in 2010.
Methods: Plasmodium vivax Annual Parasite Incidence data (20062008) and temperature masks were used to map P. vivax
transmission limits. A total of 4,658 community surveys of P. vivax parasite rate (PvPR) were identified (19852010) for
mapping quantitative estimates of contemporary endemicity within those limits. After error-checking a total of 4,457 points
were included into a national database of age-standardized 199 year old PvPR data. A Bayesian MBG procedure created a
predicted PvPR199 endemicity surface with uncertainty estimates. Population at risk estimates were derived with reference
to a 2010 human population surface.
Results: We estimated 129.6 million people in Indonesia lived at risk of P. vivax transmission in 2010. Among these, 79.3%
inhabited unstable transmission areas and 20.7% resided in stable transmission areas. In western Indonesia, the predicted P.
vivax prevalence was uniformly low. Over 70% of the population at risk in this region lived on Java and Bali islands, where
little malaria transmission occurs. High predicted prevalence areas were observed in the Lesser Sundas, Maluku and Papua.
In general, prediction uncertainty was relatively low in the west and high in the east.
Conclusion: Most Indonesians living with endemic P. vivax experience relatively low risk of infection. However, blood
surveys for this parasite are likely relatively insensitive and certainly do not detect the dormant liver stage reservoir of
infection. The prospects for P. vivax elimination would be improved with deeper understanding of glucose-6-phosphate
dehydrogenase deficiency (G6PDd) distribution, anti-relapse therapy practices and manageability of P. vivax importation
risk, especially in Java and Bali.
Citation: Elyazar IRF, Gething PW, Patil AP, Rogayah H, Sariwati E, et al. (2012) Plasmodium vivax Malaria Endemicity in Indonesia in 2010. PLoS ONE 7(5): e37325.
doi:10.1371/journal.pone.0037325
Editor: Erika Martins Braga, Universidade Federal de Minas Gerais, Brazil
Received February 21, 2012; Accepted April 18, 2012; Published May 17, 2012
Copyright: 2012 Elyazar et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: IE is funded by grants from the University of Oxford - Li Ka Shing Foundation Global Health Program and the Oxford Tropical Network. SIH is funded by
a Senior Research Fellowship from the Wellcome Trust (#095066), which also supports PWG. SIH also acknowledges funding support from the RAPIDD program
of the Science & Technology Directorate, Department of Homeland Security, and the Fogarty International Center, National Institutes of Health. APP is funded by a
grant from the Wellcome Trust (#091835). HR, ES, NWP, SNT, and RK are funded by the Indonesian Ministry of Health. JKB is funded by a grant from the Wellcome
Trust (#B9RJIXO). This work forms part of the output of the Malaria Atlas Project (MAP, http://www.map.ox.ac.uk), principally funded by the Wellcome Trust, U.K.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected]
Introduction against acute attack, chloroquine, has failed in Indonesia [12,13]

and parts of Oceania [14], and resistance now threatens the
Plasmodium vivax malaria is the most widely distributed species of Mekong region [15,16,17,18] and the Indian sub-continent [19],
human malaria, threatening nearly 3 billion people in 95 countries where .90% of P.vivax malaria occurs [20]. Although several
ranging from temperate to tropical in the Americas, Africa, and artemisinin combination therapies (ACT) have shown good
Asia [1,2]. Unlike the other common cause of malaria, Plasmodium efficacy against acute P. vivax [21], only primaquine can eliminate
falciparum, dormant liver stages of P. vivax cause relapses of acute the hypnozoite reservoir of infection [22,23]. The safety and
malaria [3]. Despite the reputation of P. vivax as a benign infection efficacy of primaquine, especially when used with an ACT, is
with very low risk of death, contemporary studies demonstrate virtually unknown in 2012 [24]. The distribution of risk of this
substantial morbidity [4,5,6,7] and mortality [8,9,10,11] burdens infection emerges as a vital consideration in developing strategies
in endemic zones. that may mitigate this potentially serious threat. This may be
Drug resistance and neglect of its research in P. vivax especially true in places like the vast number of islands scattered
exacerbates the threat of this infection. The first line therapy
PLoS ONE | www.plosone.org 1 May 2012 | Volume 7 | Issue 5 | e37325

Vivax Malaria Endemicity in Indonesia in 2010
within the Indonesian archipelago, and those with very limited Assembling Indonesia human population data
resources for dealing with such problems. Gridded population counts and population density estimates at
Other nations have developed such maps. Brooker et al. [25] 161 km spatial resolution for the years 1990, 1995 and 2000, both
developed a P. vivax map for Afghanistan in 2006 at a spatial adjusted and unadjusted to the United Nations national
resolution of 868 km using logistic regression models and malaria population estimates were provided by The Global Rural Urban
surveys from 269 endemic villages. Manh et al. [26] derived a P. Mapping Project (GRUMP) beta version [32,33]. The adjusted
vivax distribution map in Vietnam for 2010 using zero-inflated population counts for the year 2000 were projected to 2010 by
Poisson regression models in a Bayesian framework from 12 applying the relevant national urban and rural growth rates by
months of P. vivax malaria reported cases from 670 districts. Reid et country [34] using methods described previously [35]. The urban
al. [27] produced a P. vivax prevalence map on Tanna Island, growth rates were applied to populations residing within the
Vanuatu in 2008 at 161 km resolution using 220 geo-referenced GRUMP-defined urban extents [33], and the rural rates were
villages and the Bayesian geostatistical logistic regression model. applied elsewhere. National 2010 totals were then adjusted to
Dogan et al. [28] developed P. vivax malaria incidence maps at match those estimated by the United Nations [36]. These
0.460.4 km resolution in Turkey using malaria data from 81 population counts were then stratified nationally by age group
provinces for over 34 years (19752008) using a kriging method. using United Nations-defined [36] population age structures for
This report describes the first use of a Bayesian model-based the year 2010 to obtain population count surfaces for the 05
geostatistics (MBG) approach [29] to predict the risk of P. vivax years, 514 years and $15 years age groups. This population
malaria in Indonesia in 2010 at a spatial resolution of 161 km, surface was extracted for Indonesia and aligned to all other spatial
using the largest assembled contemporary empirical evidence for data grids used in the analysis.
any country in Asia. This collaborative effort between the Ministry
of Health in the Republic of Indonesia and the Malaria Atlas
Defining the limits of Plasmodium vivax transmission
Project (MAP, http://www.map.ox.ac.uk) aims to equip those
Annual Parasite Incidence data at district level in 33 endemic
responsible for national planning and implementation of malaria
provinces were sourced to define the spatial limits of P. vivax
control and elimination strategies with an evidence base for the
distribution of risk of vivax malaria in Indonesia. transmission in 2010. Following previously defined protocols [1],
classification of risk based on PvAPI data assigned areas at no risk
(zero annual incidence over three years), unstable (mean annual
Methods incidence less than 0.1 per 1,000 people per annum) or stable risk
Assembling a national database of Plasmodium vivax (mean annual incidence higher than 0.1 per 1,000 people per
Annual Parasite Incidence data annum). These polygon-based data were then rasterised to
The Sub-Directorate of Malaria Control at the Directorate of 161 km spatial grids. A temperature mask was then applied on
Vector-borne Diseases, Indonesia Ministry of Health in Jakarta PvAPI data-defined limits of transmission [29]. This biological
routinely collected P. vivax Annual Parasite Incidence (PvAPI) at mask delineated areas where low temperatures were likely to
the district level between 2006 and 2008. The reported cases of inhibit parasite development in anopheline vectors [37]. We
confirmed P. vivax malaria per 1,000 people were computed for further modified a decision rule for stable transmission. Within
each year by district and averaged over the number of reporting stable transmission limits, pixels predicted with high certainty
years. Each PvAPI summary estimate was mapped by matching it (probability .90%) of being less than 1% PvPR199 were
to its corresponding first (provincial) and second level (district) downgraded from stable to unstable class. This extremely low
administrative unit in a geographic information system (GIS; prediction was caused by a great abundance of survey data
ArcView GIS 9.3, ESRI, 2008). reporting zero prevalence in those areas.
Assembling a national database of Plasmodium vivax Environmental covariates

malariometric prevalence A minimal set of covariates were included to inform prediction
The process of assembling community-based survey parasite of the mean function, based on a priori expectations of the major
prevalence data undertaken since 1985 has been described environmental factors modulating transmission. These were (i) an
previously [30]. Data searches for P. vivax parasite rate (PvPR) indicator variable defining areas as urban or rural based on the
aimed to retrieve data from published and unpublished sources. GRUMP urban extent product [32,33]; (ii) a long-term average
These searches are an on-going activity of the Malaria Atlas vegetation index product as an indicator of overall moisture
Project (MAP, http://www.map.ox.ac.uk) and were completed for availability for vector oviposition and survival [38,39]; and (iii) a P.
the current iteration on 25 November 2011. The completed vivax specific index of temperature suitability derived from the
database was checked via various levels of exclusion criteria in same model used to delineate suitable areas on the basis of vector
order to obtain the final input data set for modelling as follows: survival and sporogony [37].
removing surveys located only to large (.100 km2) and small
polygons (.25 km2), removing those surveys that could not be Bayesian space-time geostatistical modelling
precisely geo-positioned and removing those that could not be Bayesian space-time geostatistical modelling for disease preva-
temporally disaggregated into independent surveys or for which lence mapping has been fully described [29] and implemented at
the survey date was unknown. The entire database was then the national [40] and global scales [29]. The underlying value of
checked to ensure all survey sites were located precisely on grid PvPR199 in 2010, PvPR1{99 xi , at each location xi was
squares identified as land and within the border of the country. modelled as a transformation g: of a spatiotemporally structured
Finally, the database was checked for any spatio-temporal field superimposed with unstructured (random) variation [xi .
duplicates. The dataset was then stratified into two regions for The number of P. vivax positive responses Ni z from a total sample
descriptive purposes, since western and eastern Indonesia are of Ni individuals at each survey location was modelled as a
biogeographically distinct regions of the archipelago, typically conditionally independent binomial variate given the unobserved
demarked by the Wallace Line [31]. underlying age-standardized PvPR199 value [41]. An age-

standardisation procedure [42,43] was implemented to allow (2) the mean prediction absolute error, and (3) the linear
surveys conducted in participants of any age range to be converted correlation coefficient. The mean prediction error measures the
to the epidemiologically informative 1 to 99 year age range using bias of prediction and the mean prediction absolute error
an algorithm based on catalytic conversion models first adapted measures the accuracy of predictions. The correlation coefficient
for malaria by Pull and Grab [44]. This age-standardisation indicates the linear association between predicted and observed
procedure has been previously adopted for P. falciparum [29,40], values, which was also visualised using a scatter plot [47].
but the model form has been reparameterised using assembled A sample semi-variogram was calculated from standardised
age-stratified PvPR surveys. Each survey was referenced tempo- model residuals to assess the presence of residual spatial
rally using the mid-point (in decimal years) between the recorded autocorrelation unexplained by the model output. Standardised
start and end months. The spatio-temporal component was Pearson residuals were calculated for each validation location
represented by a stationary Gaussian process f xi ,ti with mean [48,49]. This sample semi-variograms was compared to a Monte
m and covariance defined by a spatially anisotropic version of the Carlo envelope computed from 99 random permutations of the
space-time covariance function proposed by Stein [45]. A same residual set [50]. Where the semi-variogram of standardized
modification was made to the Stein covariance function to allow model Pearson residuals lies entirely within this envelope, it can be
the time-marginal model to include a periodic component of considered as the absence of spatial structure.
wavelength 12 months, providing the capability to model seasonal The ability of the model to generate appropriate credible
effects in the observed temporal covariance structure. These effects intervals was tested via a coverage plot. Working through 100
arise when studies performed in different years but during similar progressively narrower credible intervals, from the 99% CI to the
calendar months have a tendency to be more similar to each other 1% CI, each was tested by computing the actual proportion of
than would be expected in the absence of seasonality. The mean held-out prevalence observations that fell within the predicted CI.
component m was modelled as a linear function of a vector of the Plotting these actual proportions against each predicted CI level
selected suite of environmental covariates, k : m~bx zbkx. The allows the overall fidelity of the posterior probability distributions
unstructured component [xi was represented as Gaussian with predicted at the held-out data locations to be assessed.
zero mean and variance V . Bayesian inference was implemented
using Markov Chain Monte Carlo to generate 100,000 samples Measuring area and population at risk
from the posterior distribution of: the Gaussian field f xi ,ti at The quantification of areas within no risk, unstable and stable
each data location, the unobserved parameters bx , b, and V as category was undertaken by first projecting the predicted class
stated above and further unobserved parameters defining the map from geographic to Mollweide equal area projection in
structure and anisotropy of the exponential space-time covariance ArcGIS 9.3. The areas covered by each category were then
function. Distances between locations were computed in great- calculated in km2. To derive population at risk within each zone,
circle distance to incorporate the effect of the curvature of the this categorical map was overlaid with the GRUMP-beta 2010
Earth, which becomes important for a nation as large as gridded population surface using an exact bespoke algorithm
Indonesia. Samples were generated from the 2010 annual mean written in Fortran90, and the total population living in each risk
of the posterior distribution of f xi ,ti at each prediction location. category was calculated. These totals were further disaggregated
For each sample of the joint posterior, predictions were made by province level.
using space-time conditional simulation over the 12 months of
2010 {t = 2010Jan, , 2010Dec}. These predictions were made at Results
points on a regular 161 km spatial grid. Model output therefore
consisted of samples from the predicted posterior distribution of The spatial limits of Plasmodium vivax transmission
the 2010 annual mean PvPR199 at each grid location, which were The 2010 Plasmodium vivax malaria risk limits in Indonesia are
used to generate point estimates. The uncertainty metric was shown in Figure 1. We have estimated that 1.7 million km2
computed by calculating the ratio of posterior distribution (89.8%) of a total land area of 1.9 million km2 were endemic for P.
interquartile range to its mean. This standardized metric produced vivax malaria (Table 1). These endemic areas, a land area of 0.695
an uncertainty index which less influenced by underlying million km2 (40.7%) were unstable transmission zones and 1.014
prevalence levels. million km2 (59.3%) were stable transmission zones. Stable vivax
transmission zones were more common in eastern than western
Evaluating model performance Indonesia (83.5% vs. 33.7%). Further provincial level estimates of
An empirical model assessment was carried out by first selecting areas at risk are provided in Table S1.
a validation set. Ten percent (n = 445) of the full data points were
selected using a spatially de-clustered stratified random sampling Summaries of P. vivax malaria prevalence survey data
algorithm, described previously [29]. Those surveys located A total of 80 different sources from between 1985 and 2010
outside the stable limits of transmission were excluded from documented a total of 4,658 independent community surveys of
selection. Using the remaining 90% (n = 4,012) of data points the PvPR from 33 P. vivax malaria endemic provinces (Figure 2).
model was then re-run to make predictions at the space-time Provinces of Papua/West Papua (n = 1,021), East Nusa Tenggara
locations of these held-out data. Model performance was then (n = 734) and Aceh (n = 434) contributed 47% of total data points.
evaluated using two criteria: the ability of the model to (1) predict After database fidelity checks, a total of 201 survey locations were
point-values of PvPR199 at validation locations, and (2) to excluded from modelling because they were polygon data (n = 6),
generate credible intervals (CI) that capture appropriately the could not be geo-positioned (n = 87), surveys could not be
uncertainty associated with predictions at each location. disaggregated temporally (n = 39), were spatio-temporal duplicates
The ability of model to predict point-values of PvPR199 at (n = 50) or were missing information on the month of survey
validation locations was then evaluated by comparing observed (n = 19).
values to those predicted (using the posterior mean) by the model Table 2 summarizes the remaining 4,457 data points PvPR by
at the corresponding locations. Assessment was made using three region. More PvPR surveys were conducted in the eastern region
summary statistics [29,46] including (1) the mean prediction error, compared to the western region (58% vs. 42%). Over half of the

Figure 1. The spatial limits of Plasmodium vivax defined by Annual Parasite Incidence and the temperature mask. Areas were defined
as stable (dark grey areas, where PvAPI$0.1 per 1,000 pa), unstable (medium grey areas, where PvAPI,0.1 per 1,000 pa), or no risk (light grey, where
PvAPI = 0 per 1,000 pa).
total data points (57.4%) documented the presence of P. vivax. In Development. Most of the data incorporated resulted from PvPR
eastern Indonesia, 73.4% of the surveys reported presence records, surveys conducted between 2005 and 2010 (88.4%). The great
compared to 35.6% in western region. Mean PvPR was higher in majority of surveys included an upper age .20 years (94.3%).
the eastern than the western region (5.6% vs. 1.5%). The great About seven percent of surveys were geo-positioned by Global
majority of the PvPR data (91.8%) were obtained from unpub- Positioning Systems (GPS) whilst over 70% of the survey sites were
lished works. Peer-reviewed sources only contributed about 6% of geo-positioned using a combination of paper source, map and geo-
the total data points. A total of 92% of the full number of PvPR referencing techniques. Surveys with small sample sizes (n,50)
records were obtained from direct communication with malaria represented 8.95% of the total data. The median sample size was
specialists across Indonesia, the Indonesian National Malaria 136. The most common sample size in western region was 50100
Control Program and National Health Institute of Research and people (38.8%) whilst in eastern region was 100500 people
Table 1. Area and population at risk of Plasmodium vivax malaria in 2010 throughout the Indonesian archipelago.
Area and population at risk Region Total
Western Eastern
Value % Value % Value %

2
Area (km ) 1,153,945 100.0 748,886 100.0 1,902,831 100.0
No risk 143,050 12.4 50,261 6.7 193,311 10.2
At risk 1,010,895 87.6 698,625 93.3 1,709,520 89.8
Unstable 922,284 53.9 73,035 9.8 695,319 36.5
Stable 388,611 33.7 625,590 83.5 1,014,201 53.3
Population 204,915,987 100.0 27,628,308 100.0 232,544,295 100.0
No risk 96,726,120 47.2 6,157,027 22.3 102,926,147 44.3
At risk 108,146,867 52.8 21,471,281 77.7 129,618,148 55.7
Unstable 96,586,342 47.1 6,176,858 22.4 102,763,200 44.2
Stable 11,560,525 5.7 15,294,423 55.3 26,854,948 11.5
No risk, unstable and stable risk areas correspond to PvAPI = 0 per 1,000 pa, 0,PvAPI,0.1 per 1,000 pa and PvAPI$0.1 per 1,000 pa.

Figure 2. The distribution of Plasmodium vivax prevalence surveys in Indonesia between 1985 and 2010. The 4,457 community surveys
of P. vivax prevalence conducted between 01 January 1985 and 25 November 2011 are plotted. The survey data are shown in white (PvPR = 0%),
yellow (PvPR.0%5%) and red (PvPR.5%). Areas were defined as stable (dark grey areas, where PvAPI$0.1 per 1,000 pa), unstable (medium grey
areas, where PvAPI,0.1 per 1,000 pa), or no risk (light grey, where PvAPI = 0 per 1,000 pa).
(48.9%). The most commonly recorded malaria diagnostic million people (55.7%) lived at risk of P. vivax transmission. Of
technique in these PvPR surveys was microscopy method (54%). these, 102.8 million (79.3%) and 26.8 million (20.7%) inhabited
The distribution of P. vivax malaria surveys was not uniform areas of unstable and stable transmission respectively. Further
among the main islands in the archipelago (Figure 2). The islands provincial level estimates of population at risk are provided in
of Sumatra (western), Papua (eastern) and Lesser Sundas (eastern) Table S1.
were reported as the three richest PvPR data islands with In the western region, 108.1 million people (52.8%) live at risk
proportions of 32.8%, 22.4% and 19.1%, respectively. Kaliman- of P. vivax transmission.
tan was reported as the island with the sparsest PvPR data (3%) On Java and Bali islands, (representing 7% of the land area of
followed by Sulawesi (4.6%). In Java, where more districts Indonesia) nearly 77 million people lived in areas of P. vivax
reported no-risk of vivax malaria, 6.5% of PvPR data were tranmission, accounting for 71% of all people at risk in western
collected between 1985 and 2010. region. More people in western Indonesia lived in unstable
transmission than those of stable transmission (89.3% vs.10.7%).
The spatial distribution of Plasmodium vivax malaria The proportion of the population living in unstable versus stable
endemicity risk was 99% vs. 1% in Java, 63% vs. 37% in Sumatra and 62%
The continuous predicted surface of P. vivax malaria endemicity vs. 38% in Kalimantan.
within the limits of stable transmission is presented in Figure 3. In the eastern region, 21.5 million (77.7%) people live at risk of
The mean of predicted PvPR199 was 1.6% with a high degree of P. vivax transmission.
heterogeneity ranging from 0.2% to about 11%. In western Less people lived in unstable transmission than stable transmis-
Indonesia, the predicted P. vivax prevalence was uniformly low. sion (28.8% vs. 71.2%). All of 10.8 million people lived at risk of P.
Spots of intermediate prevalence PvPR199 were observed in vivax transmission in Sulawesi, followed by 6.7 million in Lesser
eastern Kalimantan. High PvPR199 areas were observed in Lesser Sundas, 1.9 million each in both Maluku and Papua. The
Sundas, Maluku and Papua. Uncertainty in predicted PvPR199 proportion of the population living in unstable versus stable risk
was relatively low in areas with low endemicity and abundance of was 49% vs. 51% in Sulawesi, 8% vs. 92% in Maluku, 9% vs. 91%
surveys, such as in parts of Sumatra and Kalimantan (Figure 4). in Lesser Sundas and 3% vs. 97% in Papua.
However in areas with high variability of prevalence, such as
Papua, certainty of predicted PvPR199 was relatively lower than Model performance
other main western islands (Figure 4.). In predicting point-values of PvPR199 at validation locations,
the mean prediction error was 20.43% (in units of PvPR199),
The estimation of population at risk of Plasmodium vivax indicating low bias in predicted PvPR. This value also represented
malaria the tendecy to underestimate P. vivax prevalence by just under
Table 1 shows the estimated population at risk of P. vivax 0.5%. Mean prediction absolute error, which measured the model
malaria in Indonesia in 2010. We have estimated that 129.6 precision, was estimated at 3.4% PvPR199. This value represented

Table 2. Summary of the most important aspects of the PvPR data by main region.
Total records of input data set Western Eastern Total Percentage
(n = 1,886) (n = 2,571) (n = 4,457) (100%)
Number selected for model

Population sample size 426,341 955,469 1,381,810
Number of PvPR.0 672 1,886 2,558 57.39
Mean (standard deviation) PvPR (%) 1.49 (3.97) 5.57 (9.27) 3.84 (7.76)
Median (range) PvPR (%) 0 (045.9) 1.87 (086.1) 0.62 (086.1)
Primary source of PvPR data
Peer reviewed sources 104 156 260 5.83
Unpublished work 1,688 2,405 4,093 91.83
Reports{ 94 10 104 2.34
Source of spatial coordinates
Personal communication 35 39 74 1.66
GPS 129 165 294 6.60
Encarta 235 329 564 12.65
Combination 1,333 1,817 3,150 70.68
Other digital gazettes 112 161 273 6.12
Paper source 4 1 5 0.11
Map 38 59 97 2.18
Time period
19851989 99 11 110 2.47
19901994 58 60 118 2.65
19951999 35 60 95 2.13
20002004 81 115 196 4.39
20052010 1,613 2,325 3,938 88.36
Upper age sampled
#10 17 40 57 1.28
.10 and #15 70 10 80 1.79
.15 and #20 - 117 117 2.63
.20 1,799 2,404 4,203 94.30
Diagnostic method
Microscopy 1,064 1,336 2,400 53.85
RDT 822 1,235 2,057 46.15
Denominator
149 272 127 399 8.95
50100 732 507 1,290 28.94
101500 572 1,258 1,779 39.91
.500 310 679 989 22.19
Median (Inter Quartile Range; IQR) 95 (65321) 197 (100538) 136 (83450)
{
Ministry of Health reports, theses and other unpublished sources.
the variance between predicted and observed endemicity in each throughout the range indicating that predicted credible intervals
pixel, which is probably due to heterogenity of prevalence in short- provided an appropriate measure of model uncertainty.
range areas or sparsity of data points. The correlation coefficient
between predicted and observed values was 0.58, indicating strong Discussion
linear agreement (see also the corresponding scatter plot,
Figure 5A). The semi-variograms of the standardized model This report describes the spatial limits and level of endemicity of
Pearson residuals lie entirely within Monte Carlo envelope Plasmodium vivax in Indonesia. The continous surface P. vivax
(Figure 5B) which indicated no significant spatial structure. malaria endemicity maps at 161 km spatial resolution were
Figure 5C shows the coverage plot comparing predicted to actual generated from an evidence base of nearly 4,500 independent
credible intervals. The plotted line is close to the ideal 1:1 line estimates of P. vivax malaria prevalence across this archipelago and
the use of a Bayesian model-based geostatistical spatial-temporal

Figure 3. The Plasmodium vivax malaria PvPR199 endemicity map. Model-based geostatistical point estimates of the annual mean PvPR199 for
2010 within the stable spatial limits of P. vivax malaria transmission, displayed as a continuum of light green to red from 0% to 7% (see map legend).
Areas within the stable limits in Figure 1 that were predicted with high certainty (.0.9) to have PvPR199 less than 1% were classified as unstable areas
(shaded medium grey areas). The rest of the land area was defined as unstable risk (medium grey areas, where PvAPI,0.1 per 1,000 pa) or no risk
(light grey, where PvAPI = 0 per 1,000 pa).
Figure 4. The uncertainty map of predicted PvPR199 within the stable transmission areas. These values indicate the uncertainty of
prediction by using the ratio of posterior inter-quartile range to the posterior mean prediction at each pixel. Large values indicate greater uncertainty.
Smaller values indicate higher degree of certainty in the prediction. The rest of the land area was defined as unstable risk (medium grey areas, where
PvAPI,0.1 per 1,000 pa) or no risk (light grey, where PvAPI = 0 per 1,000 pa).

platform, similar to that applied for P. falciparum [29,40]. These

estimates of area and population at risk of P. vivax represent
improved and updated estimates from those made for 2009 [1].
The detection of P. vivax using the Rapid Diagnostic Tests (RDTs)
accounted for 46% of assembled malaria prevalence surveys.
RDTs are known to be less sensitive than expert microscopy and
molecular detection, especially at low parasite densities, which
tends to result in higher false-negative rates and, thus, lower
observed PvPR [51,52,53,54]. However, precise quantitative
adjustments for these factors are not readily available and we
have not assessed the impact of this low sensitivity of RDTs on our
endemicity estimates.
Indonesian challenges to control and elimination

Options for malaria preventive measures [55] to reduce the risk
of P. vivax malaria in Indonesia are limited. No contemporary work
has demonstrated the impact of district or nationwide implemen-
tation of larvicides, larvivorous fish, or source reduction by
environmental management upon malaria transmission. Low
coverage rates of insecticide-treated nets (ITN) and their usage,
low proportions of houses with screening in endemic zones,
variable practices in personal protection represent obstacles to
efforts to eliminate malaria transmission in Indonesia. The
challenge is further complicated by the unusually diverse mix of
20 Anopheles vectors with varying bionomics [56] and interspersed
distributions, as recently shown by comprehensive distribution
maps of dominant malaria vectors [57]. Another important
problem is the availability of reliable diagnostics, which may
currently identify fewer than 20% of malaria attacks [12]. A
clinical diagnosis in Indonesia prompts therapy with chloroquine
or sulfadoxine-pyramethamine, despite widespread resistance to
these drugs by both P. falciparum and P. vivax malaria [12].
Indonesian authorities acknowledge diagnostics as their primary
challenge in malaria control.
In the context of controlling or, especially eliminating endemic
P. vivax, chemotherapeutic attack on the hypnozoite reservoir of
infection may be a key consideration. However, the only drug
available for this purpose, primaquine, threatens to potentially
seriously harm patients with G6PDd [58]. Laboratory screening of
those at risk of this harm is not currently practical as part of
routine care in Indonesia. The G6PDd prevalences were
documented between 18% in this archipelago [59,60,61,62,63].
Although most authoritative agencies recommend a daily dose of
primaquine of 0.5 mg/kg for 14 days [64], especially in Southeast
Asia [65,66], this regimen is relatively threatening without G6PDd
screening, and the Indonesian authorities thus recommend
0.25 mg/kg for 14 days [67]. Even this lower dose, however, is
potentially dangerous and many providers in Indonesia may be
reluctant to prescribe it, much less encourage patients to be fully
adherent. It may thus be appreciated that G6PDd constitutes a
very significant challenge to the Indonesian authorities striving to
achieve their declared elimination goals [68].
This risk map of P. vivax malaria in Indonesia provides an
evidence base which the Indonesian authorities may refer to when
developing strategies for the systematic elimination of malaria
transmission. The steep challenges imposed by diagnosis, resis-
Figure 5. Evaluation of model performance. (A) Scatter plot of tance to chloroquine, and the potential harm caused by
actual versus predicted point-values of PvPR199. (B) Sample semi- primaquine may be rationally considered beyond nation-wide
variogram of standardized model Pearson residuals estimated at solutions. Instead, the resources required to overcome these
discrete lag and a Monte Carlo envelope (dashed line) representing challenges may be focused upon specific sites where control
the range of values expected by chance in the absence of spatial
autocorrelation. (C) Probability-probability plot comparing predicted measures are most needed or where elimination may be
credible intervals with the actual percentage of true values lying inside realistically within reach. Further, maps of G6PDd prevalence,
those intervals. In the top and bottom plots the 1:1 line is also shown and some understanding of the distribution of the most vulnerable
(dashed line) for reference. variants, may also guide balance of risk and benefit with

primaquine strategy, policy and practice brought to bear by the Conclusions

authorities [69]. The maps presented in this report constitute part of a suite of
GIS tools aimed at providing the authorities in Indonesia
Further work responsible for malaria contol with evidence-based means of
The Malaria Atlas Project developed cartographic techniques to focusing their resources to where they are most needed and may
estimate clinical burden of P. falciparum malaria by using a be most effectively applied. Maps of endemicity of both important
continuous relationship model between paired P. falciparum species of parasite, coupled with estimates of population at risk and
prevalence and clinical incidence [70,71]. A non-parametric clinical burden, along with the geographic distribution of G6PDd
Bayesian inference was chosen to define this relationship [71]. prevalence and patterns of internal migration compose that
Space-time joint simulation was then used to measure uncertainty envisioned suite.
of these clinical burden estimates [70]. In order to achieve similar
estimates for P. vivax, further work is needed to resolve the Supporting Information
association between prevalence of P. vivax and clinical incidence.
Table S1 Areas and population at risk of Plasmodium
This is especially challenging with the added dimension of relapse vivax malaria in Indonesia by province, main islands
and further clinical attacks from a single infectious event. and region level in 2010.
Nonetheless, such estimates constitute vital evidence in rational (DOCX)
allocation of limited resources in a nation facing multiple infectious
disease threats to the public health.
Acknowledgments
A glance at the geography of Indonesia reveals yet another
challenge faced by the authorities in realizing and maintaining the The national assembly of parasite prevalence surveys was dependent on the
elimination of malaria from any given island. People from the generous contributions of data by a large number of people in the malaria
research and control communities. These individuals are listed on the MAP
heavily populated islands of Java and Bali represent a significant
website. (http://www.map.ac.uk/acknowledgements/). We thank Kather-
proportion of those engaged in the economic development of the ine Battle and David Pigott for proofreading this paper. The authors
many sparsely populated outer islands of the archipelago and it is additionally acknowledge the support of colleagues from the Sub-
unknown how many travel back and forth between these islands. Directorate of Indonesian Malaria Control including Achmad Farchanny,
These movements incur substantial risk of importing and re- Adhi Sambodo, Ali Romzan, Aris Munanto, Budi Pramono, the late
establishing malaria transmission on Java and Bali. MAP and its Charles Tobing, Nur Asni and Saktiyono. We also thank to Trihono and
Indonesian partners will explore techniques to estimate specific Suparmi from National Health Institute of Research and Development for
their contribution of Basic Health Research data.
patterns and numbers of human movements among the islands in
order to identify specific and high priority threats to elimination.
The feasibility of such exploration has been facilitated by the Author Contributions
advance of geographical information systems, spatial statistics, and Conceived and designed the experiments: IE SIH. Performed the
anonimized mobile phone records [72,73,74] allowing for the experiments: PWG AP. Analyzed the data: IE. Contributed reagents/
tracking of movement of mobile phones among the communica- materials/analysis tools: PWG APP. Wrote the paper: IE PWG SIH JKB.
Assembled and managed the PvAPI data: HR IE. Provided context
tions masts that serve them. regarding the Indonesian malaria control strategy: ES NWP SNT RK.
Commented on the final draft of the manuscript: IE PWG APP HR ES
NWP SNT RK JKB SIH.
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Table S1. Area and population at risk of Plasmodium vivax malaria in Indonesia by province, main islands and region level in 2010.
Risk area (km2) Population (people) Total

Total area
Province population
No risk Unstable Stable (km2) No risk Unstable Stable
(people)
Western 143,050 622,284 388,611 1,153,945 96,769,120 96,586,342 11,560,525 204,915,987
Sumatra 93,689 259,269 123,553 476,511 22,543,764 14,707,432 8,476,821 45,728,017

Aceh 4,783 27,678 24,607 57,068 786,431 1,224,321 1,863,916 3,874,668
Sumatra Utara 35,594 31,357 4,899 71,850 9,729,105 2,690,212 637,299 13,056,616
Sumatra Barat 12,941 27,729 1,125 41,795 2,833,041 1,593,423 13,881 4,440,345
Riau 1,618 88,418 0 90,036 893,711 3,095,482 0 3,989,193
Kepulauan Riau 0 6,059 2,962 9,021 0 1,135,788 83,402 1,219,190
Jambi 1,243 19,108 29,078 49,429 748,227 800,072 975,454 2,523,753
Bengkulu 494 267 20,363 21,124 251,027 12,786 1,278,565 1,542,378
Sumatra Selatan 23,536 26,237 36,396 86,169 3,461,870 1,151,292 2,712,551 7,325,713
Bangka Belitung 357 15,944 9 16,310 164,738 739,871 84 904,693
Lampung 13,123 16,472 4,114 33,709 3,675,614 2,264,185 911,669 6,851,468
Java/Bali 44,542 93,809 363 138,714 70,511,604 76,865,382 64,770 147,441,756

Jakarta 681 0 0 681 12,523,487 0 0 12,523,487
Banten 3,334 6,053 0 9,387 8,100,547 1,988,513 0 10,089,060
1
Total area
Province population
(people)
Jawa Barat 13,446 23,716 0 37,162 24,925,194 17,131,303 0 42,056,497

Jawa Tengah 5,490 28,861 0 34,351 5,846,771 29,358,083 0 35,204,854
Yogyakarta 526 2,635 0 3,161 1,576,124 2,153,578 0 3,729,702
Jawa Timur 19,605 28,340 363 48,308 16,906,146 23,017,327 64,770 39,988,243
Bali 1,460 4,204 0 5,664 633,335 3,216,578 0 3,849,913
Kalimantan 4,819 269,206 264,695 538,720 3,713,752 5,013,528 3,018,934 11,746,214

Kalimantan Barat 1,534 86,280 60,229 148,043 927,269 2,581,801 592,440 4,101,510
Kalimantan Tengah 370 70,994 83,175 154,539 56,944 532,859 1,170,522 1,760,325
Kalimantan Selatan 999 17,176 19,408 37,583 1,382,456 1,253,595 639,413 3,275,464
Kalimantan Timur 1,916 94,756 101,883 198,555 1,347,083 645,273 616,559 2,608,915
Eastern 50,261 73,035 625,590 748,886 6,157,027 6,716,858 15,294,423 27,628,308
Sulawesi 21,621 54,524 112,085 188,230 4,577,945 5,345,801 5,516,072 15,439,818

Sulawesi Utara 2 8,009 6,772 14,783 89 942,211 1,203,290 2,145,590
Gorontalo 6,385 275 5,499 12,159 173,400 173,575 498,270 845,245
Sulawesi Tenggara 1,031 9,101 26,987 37,119 304,388 292,971 1,205,004 1,802,363
Sulawesi Barat 1,232 5,063 10,066 16,361 123,083 457,237 283,491 863,811
2
Total area
Region/Province population
(people)
Sulawesi Tengah 1,890 483 58,860 61,233 264,188 129,147 1,776,471 2,169,806
Sulawesi Selatan 11,081 31,593 3,901 46,575 3,712,797 3,350,660 549,546 7,613,003
Maluku 202 9,057 69,754 79,013 1,431 147,241 1,805,662 1,954,333

Maluku 196 9,057 37,705 46,958 1,347 147,241 1,073,103 1,221,691
Maluku Utara 6 0 32,049 32,055 84 0 732,559 732,643
Lesser Sundas 1,038 1,018 64,377 66,433 1,355,225 634,739 6,063,506 8,053,470
Nusa Tenggara Barat 999 1,018 17,867 19,884 1,344,784 634,739 2,176,468 4,155,991
Nusa Tenggara Timur 39 0 46,510 46,549 10,441 0 3,887,038 3,897,479
Papua 27,400 8,436 379,374 415,210 222,426 49,077 1,909,183 2,180,685

Papua 26,105 8,436 283,322 317,863 213,471 49,077 1,375,616 1,638,164
Papua Barat 1,295 0 96,052 97,347 8,955 0 533,567 542,522
Indonesia 193,311 695,319 1,014,201 1,902,831 102,926,147 102,763,200 26,854,948 232,544,295

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KOMPILASI PUBLIKASI ILMIAH

TENTANG MALARIA DI INDONESIA

Mengendalikan dan memberantas malaria di wilayah kepulauan terbesar di dunia, membentang

Iqbal Elyazar, MPH, DPhil

Ucapan Terima Kasih

Prof Simon Hay, Univ. Oxford Dr Rita Kusriastuti, Depkes RI

Contents 2.1. Introduction 42

* Eijkman-Oxford Clinical Research Unit, Jakarta, Indonesia

Advances in Parasitology, Volume 74 # 2011 Elsevier Ltd.

2.5. Outlook for Malaria Research in Indonesia 149

Abstract Approximately 230 million people live in Indonesia. The country is

2.2. EPIDEMIOLOGY OF MALARIA

FIGURE 2.1 The map of Indonesian archipelago.

Household Health Survey estimated an illiteracy rate of 7%, with more

2.2.1.3. Healthcare delivery systems

Indicators Year Cambodia Indonesia Thailand Malaysia Singapore

2.2.1.4. Infections research and surveillance systems operated by

and delivery (Soemantri et al., 2005). In addition, the National Family

The assembled data reveal that P. falciparum and P. vivax infections

2.2.2.2. Reported versus actual malaria morbidity and mortality

The discrepancies in these numbers were also reflected in the World

Reported malaria cases Reported malaria deaths

1994 145,920 145,920 No data No data

stable transmission, they used a modelled relationship between clinical

2.2.2.3. Occurrence of epidemic malaria

2.2.2.4. Malaria treatment policy and practice

1991 CQ First line: CQ (IV or IM) CQ PQ CQPQ CQPQ CQ CQ

diagnostic test (RDT) confirmation (World Health Organization, 2008e).

A combination of DHA and PP was administered at a dosage of 2.25 and

2.2.2.4.2. Treatment of complicated P. falciparum The first line of treat-

course of 7 days (as per guidelines detailed above). If the IV administra-

2.2.2.4.3. Treatment of P. vivax The current first line of treatment for

2.2.2.4.4. Treatment of P. malariae and P. ovale The treatment for

2.2.2.4.5. Chemoprophylaxis As a chemoprophylaxis against P. falciparum

2.2.2.5. Resistance to antimalarials

uncomplicated malaria into a severe and potentially fatal disease, reduces

In vivo test In vitro test

Year of No. No. No. Resistance No. No. No. Resistance

Sumatra 19732002 29 439 176 40 19 226 149 66

In vivo test In vitro test

Sumatra 19842001 6 302 43 14 10 121 79 65

Table 2.7 summarizes the distribution of P. falciparum resistance to QN

2.2.2.5.1. Evaluations prior to 1985

In vivo test In vitro test

TABLE 2.8 Plasmodium vivax resistance to chloroquine throughout the Indonesian

et al., 1983). Tjitra et al. reported that P. falciparum was resistant to CQ in

2.2.2.5.2. Evaluations since 1985

Western Indonesia Eastern Indonesia

P. falciparum CQ In vivo 961 417 43 2006 1122 56 < 0.001

p-value < 0.05, significant.

Prior 1985 Since 1985

P. falciparum CQ In vivo 252 64 25 2715 1475 54 <0.001

p-value < 0.05, significant.

2.3. MALARIA CONTROL IN INDONESIA

2.3.1. Control before independence (pre-1945)

recorded by European colonists indicates that malaria was a serious

on disease prevention, studying, amongst other things, the development

to combating malaria by specifically targeting only the breeding places of

Schuffner introduced a new form of species sanitation in 19161917

of three ponds (6 7 m) was allocated as treatment and control ponds.