JNS
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
JOURNAL OF NUTRITIONAL SCIENCE
RESEARCH ARTICLE
Ramadan during pregnancy and birth weight of newborns
Ary I. Savitri1*, Dwirani Amelia2, Rebecca C. Painter3, Mohammad Baharuddin2, Tessa J. Roseboom3,4,
Diederick E. Grobbee1 and Cuno S. P. M. Uiterwaal1
1
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands
Budi Kemuliaan Hospital, Jl. Budi Kemuliaan No. 25, Jakarta Pusat 10110, Indonesia
3
Department of Obstetrics and Gynecology, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
4
Department of Clinical Epidemiology, Biostatistics and Bioinformatics, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam,
The Netherlands
2
(Received 11 June 2017 – Final revision received 14 November 2017 – Accepted 15 November 2017)
Journal of Nutritional Science (2018), vol. 7, e5, page 1 of 9
doi:10.1017/jns.2017.70
Abstract
Previous studies suggest that Ramadan exposure during pregnancy might affect the health of women and their babies, particularly through the effect of
fasting. This study aimed to evaluate the association between Ramadan exposure and fasting during pregnancy on the birth weight of newborns. This study
concerned 1351 pregnant women from a prospective cohort in Jakarta, Indonesia. Ramadan exposure was based on the actual overlap between Ramadan
and pregnancy. Women’s fasting behaviour was recorded among 139 women who came for antenatal care between 10 July 2013 and 7 August 2013, and
those who had fasted for at least 1 d (n 110) were classified as exposed to Ramadan fasting. Furthermore, a 24 h dietary recall was performed and repeated 1
month later. Birth weight of newborns who were exposed to Ramadan during pregnancy did not significantly differ from those who were not, both in the
total and trimester-specific analysis. Maternal fasting did not seem to affect the birth weight of newborns (−72 (95 % CI −258, 114) g; P = 0·44), although
there was a non-significant trend towards lower birth weight with fasting in the second and third trimester. Women who fasted had significantly lower total
energy, macronutrient and water intake as compared with women who did not. Women’s intake was also lower during Ramadan (regardless of their fasting
behaviour) as compared with 1 month later. Lifestyle changes that occur with Ramadan and fasting during pregnancy are associated with lower reported
energy intake. We cannot conclude on the effect of fasting on birth weight due to low statistical power.
Key words: Ramadan: Fasting: Pregnancy: Birth weight
An adverse fetal environment could have serious consequences on health outcomes in offspring. Exposures such as
suboptimal maternal diet, smoking and stress could inhibit
fetal growth and development, which further cause lower
birth weight and other poor birth outcomes(1–3). Studies on
the long-term impact of fetal growth restriction, as represented
by lighter weight at birth, showed a greater risk of later chronic
diseases, including CHD, stroke, type 2 diabetes, hypertension,
and other cognitive and emotional problems(4–8).
During the month of Ramadan when daytime fasting is obligated to every adult Muslim, various degrees of behavioural
changes may occur among pregnant Muslim women. Meal
frequencies are usually reduced to two times per d; one large
meal when breaking the fast in the evening and another smaller meal during sahoor at dawn. Many seasonal meals which
consist of sugary and fatty foods are commonly served during
this month(9–13). Physical activities and sleeping pattern are
also affected, as people tend to be more active at night.
Ramadan lasts for 29–30 d and shifts forward by approximately 11 d each year, since it is based on the Islamic lunar
calendar(11–14).
Three out of every four pregnant Muslim women are
exposed to Ramadan(15). According to the Islamic rule, pregnant women, together with breastfeeding mothers, are
* Corresponding author: A. I. Savitri, email
[email protected]
© The Author(s) 2018. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is
properly cited.
1
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
journals.cambridge.org/jns
delivery. All pregnancies that overlapped with Ramadan in
any number of days were all classified as exposed. These
exposed pregnancies were, further, classified according to
the trimesters when the exposure occurred. They were consecutively classified as being exposed in the first, second and
third trimester if Ramadan started between the 1st and 93rd
day, the 94th to 186th day, and at 187th day or later of the
pregnancy.
Maternal fasting behaviour was measured using a selfadministered questionnaire in women who came to the hospital for antenatal care during Ramadan in 2013 (10 July
2013–7 August 2013). Women were classified as being
exposed to Ramadan fasting if she had fasted for at least 1
d during Ramadan. Fasted women were also classified according to their trimester when they fasted.
exempted from the obligation to fast during Ramadan. They
are permitted to postpone their fasting until after delivery or
to feed one poor person for each day they do not fast.
However, many women choose to fast during pregnancy to
share the spiritual experience with their family. The proportion
of fasting pregnant Muslim women varies globally, ranging
from 50–70 % (in Iran, The Netherlands)(16–18) to 70–90 %
(in England, Singapore, USA, Gambia and Yemen)(15,19–21).
Despite its widespread adherence, evidence on the health
effects of Ramadan fasting during pregnancy (both maternal
and fetal) is still limited. Dietary intake and weight gain of fasting pregnant women were reported to be less than in the nonfasting(22,23). Metabolic alterations associated with fasting have
also been reported, which include reduction in serum glucose
and insulin levels(24) and elevation in serum TAG, cortisol and
leptin concentrations(25,26). Several studies showed no association between Ramadan exposure during pregnancies with
birth weight, or the risk of low birth weight(16–18,22,26–31).
On the contrary, several other studies reported a lower birth
weight with Ramadan exposure(32,33). Many of these studies,
however, did not differentiate Ramadan exposure (as overlap
between pregnancy and the month of Ramadan) from actual
fasting exposure, which potentially leads to dilution of effects.
In the present study, we used data from a large prospective
cohort of Indonesian Muslim pregnant women to evaluate
both the effect of Ramadan exposure during pregnancy and
maternal fasting on the birth weight of newborns. Maternal
dietary intakes were evaluated during and after Ramadan,
both in the fasting and non-fasting women, in an attempt to
seek for possible explanatory factors.
Assessment of women’s dietary intakes was done by a nutrition officer using a single 24 h dietary recall, both in the fasting
and non-fasting women and was repeated 1 month later. A 24
h dietary recall is a retrospective method of dietary assessment
in which every individual is interviewed about his or her food
and beverage consumption during the previous 1 d or 24 h.
A computerised data analysis system (Nutrisurvey, 2007;
Indonesian version) was used to convert food intake into
nutrient intake based on the portion sizes, preparation of
recipes and food tables. The system is a translation from a
German nutrition software package (EBISpro), which has
been adapted to the local food tables.
Materials and methods
Outcome measurement
Study population
Newborn birth weight was investigated in relation to both
Ramadan exposure and maternal fasting. Birth weight was
measured using a standard infant scale (Tanita).
The present study was conducted within a cohort of pregnant
women in Budi Kemuliaan Hospital, Jakarta, Indonesia, a private municipal hospital that specialised in maternal and child
health care, training (midwives), education and research.
Recruitment of participants took place from July 2012 until
October 2014. Muslim pregnant women who were paying
antenatal care visits to the hospital were asked to participate
and provided a written informed consent. Women were examined and interviewed by the midwives according to the standard clinical care and followed on the subsequent antenatal care
visits until delivery. Pregnancies that ended with preterm birth
were excluded since they intrinsically had less chance to be
exposed to Ramadan and were more likely to result in
lower-birth-weight babies.
Ramadan and fasting exposure
The present study coincided with three Ramadan months,
which occurred on 21 July–18 August 2012, 10 July–7
August 2013, and 29 June–27 July 2014. Pregnancies were
classified as being exposed to Ramadan if the women’s last
menstrual period coincided with Ramadan or if Ramadan
started after the women’s last menstrual period and before
Dietary assessment
Data analysis
Maternal and babies’ characteristics were tabulated by Ramadan exposure and Ramadan fasting exposure separately, for
both descriptive purposes and for initial evaluation for possible confounding. First, we compared the birth weight of
newborns with Ramadan exposure during pregnancy with
the unexposed. Second, within the Ramadan-exposed newborns, we examined the effect of maternal fasting on birth
weight. A trimester-specific analysis was done to investigate
if the effect differs according to the timing of exposure.
We used linear regression analysis to analyse the association
between Ramadan exposure and maternal fasting on newborn
birth weight. Univariable analyses were first performed and
followed by multivariable analyses for adjustment for confounders. Potential confounders were secondhand smoking exposure, monthly family income and maternal education (as proxy
for socio-economic status), pre-pregnancy BMI, gestational
duration and parity. Secondhand smoking was used instead
of active smoking because few (<1 %) of these pregnant
women smoke. Family income was asked to the women as
2
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
journals.cambridge.org/jns
an estimate range. Women’s education was categorised as low
if the women had finished elementary or junior high school,
middle if they had finished senior high school, or high if
they attained education from university. Pre-pregnancy BMI
was calculated as women’s self-reported pre-pregnancy weight
in kg divided by the square of height in metres. Women’s
weight was measured at each antenatal care visit and at the
day of delivery using a standard weight scale (Camry).
Gestational durations were measured as the difference
between the last menstrual date and the date of delivery.
Women’s parity was classified into nulli- or multiparity.
Results are expressed as β coefficients from linear regression
with 95 % CI and corresponding P values. Statistical significance were considered to be a two-sided P < 0·05. All analyses
were done with SPSS version 21.0 for Windows (SPSS Inc.).
Results
The initial number of pregnant women in the total cohort was
2252. Thirty-five women withdrew their consent (drop outs),
168 women experienced miscarriage, and 282 women could
not be contacted for their pregnancy outcomes (loss to
follow-up). After excluding the women with missing data on
their last menstrual period and/or date of delivery (n 113),
miscoded gestational durations (n 11), twin pregnancies
(n 28), non-Muslim mothers (n 65) and preterm births
(n 199), the cohort included 1351 women for analysis. The
flowchart of the study population is shown in Fig. 1.
The baseline characteristics of women based on their exposure to Ramadan during their pregnancy and their fasting status
are shown in Table 1. The majority of women in this study
were exposed to Ramadan during their pregnancy. Gestational
duration was on average 4 d longer with Ramadan exposure.
Women who were exposed to Ramadan had a slightly higher
pre-pregnancy BMI as compared with the unexposed,
although not statistically significant. The exposed and unexposed women were similar with respect to age, education, family income, secondhand smoking exposure, parity, pregnancy
weight gain and babies’ sex.
There were 139 women who came to the hospital between
10 July and 7 August 2013, from whom data about fasting
behaviour were collected. As compared with Ramadanexposed women who did not come to the hospital during
the month, these women had higher gestational age (24·0 v.
19·0 weeks; P < 0·01). There were 110 (79 %) women who
fasted to some extent during Ramadan and twenty-nine (21
%) women who did not fast at all. Among women who fasted,
the median number of days fasted was 14 d. Fasting women
had significantly higher pre-pregnancy BMI and less pregnancy
weight gain than the non-fasting. There were also fewer fasting
women in the lowest income category. The two groups were
not different with respect to age, education, secondhand
smoking exposure, parity, gestational duration and babies’ sex.
The Ramadan-unexposed pregnancies consisted of all pregnancies in the cohort that did not overlap with Ramadan and
were taken as the reference group. Birth weight of Ramadanexposed babies was on average 3107·5 (SD 545·7) g while that
of unexposed was 3022·4 (SD 545·7) g. In Table 2, we show
the association between Ramadan exposure during pregnancy
and newborn birth weight. Newborn birth weight was not
Fig. 1. Overview of the study population.
3
journals.cambridge.org/jns
Table 1. Baseline characteristics of women based on Ramadan exposure and their fasting status
(Numbers of subjects and percentages; mean values with their standard errors; medians and interquartile ranges)
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
Ramadan exposure
Yes
Subjects
Maternal age (years)
Mean
Ramadan fasting
No
Fasting
n
%
n
%
1099
81·3
252
18·7
P
Non-fasting
n
%
n
%
110
79
29
21
P
0·38*
SE
Maternal pre-pregnancy BMI (kg/m2)†
Median
Interquartile range
Maternal weight gain (kg)
Mean
28·2
0·2
28·6
0·4
22·2
5·6
21·5
5·5
12·3
0·3
12·2
0·6
0·30*
28·8
0·6
27·4
1·4
22·6
5·3
21·1
2·7
11·6
0·9
17·6
1·6
0·09‡
0·03‡
0·96*
SE
Maternal education
Low
Middle
High
Monthly family income
<1 million IDR
1–2·5 million IDR
2·5–5 million IDR
> 5 million IDR
Secondhand smoking exposure
Yes, every day
Yes, sometimes
No
Nulliparity
Gestational duration (d)†
Median
Interquartile range
Baby’s sex (boy)
<0·01*
0·13§
204
695
197
18·6
63·4
18·0
53
143
56
21·0
56·7
22·2
104
481
341
69
9·5
43·8
31·0
6·3
15
113
83
12
6·0
44·8
32·9
4·8
234
66
198
323
47·0
13·3
39·8
38·0
61
12
47
81
50·8
10·0
39·2
38·2
0·74ǁ
10
70
30
9·1
63·6
27·3
4
18
7
13·8
62·1
24·1
3
47
45
7
2·7
42·7
40·9
6·4
5
14
8
1
17·2
48·3
27·6
3·4
12
4
16
46
37·5
12·5
50·0
42·6
4
0
3
13
57·1
0·0
42·9
44·8
0·31§
0·03ǁ
0·57§
278
14·0
562
0·48ǁ
0·97§
<0·01‡
274
12·0
51·3
134
276
11·5
53·2
0·59§
54
0·83§
0·60‡
277
12·5
49·1
13
44·8
0·68§
IDR, Indonesian Rupiah.
* Independent-samples t test.
† Skewed data.
‡ Mann–Whitney test.
§ χ2 Test.
ǁ Fisher’s exact test.
different between Ramadan-exposed and -unexposed groups,
neither in crude nor in adjusted analysis. Similarly, Ramadan
exposure in the first and second trimesters did not influence
newborn birth weight. With exposure in the third trimester,
birth weight was shown on average 73 g higher in the crude
analysis and model 1, but this association was reduced in the
fully adjusted analysis.
Within women who were exposed to Ramadan during their
pregnancy, comparison of their newborns’ birth weight was
made according to the fasting status. Average birth weight
of babies who were exposed to Ramadan fasting during pregnancy was 3201·5 (SD 377·6) g and 3190·6 (SD 606·7) g in
babies who were not. As shown in Table 3, birth weight of
newborns of the fasted women was not significantly different
Table 2. Total and trimester-specific associations between Ramadan exposure during pregnancy and the birth weight of newborns†
(Regression coefficients and 95 % confidence intervals)
Crude model
Ramadan unexposed
Ramadan exposed (at any trimester)
Ramadan exposed at first trimester
Ramadan exposed at second
trimester
Ramadan exposed at third trimester
n
Regression
coefficient
252
1099
350
386
54·6
30·7
58·7
363
73·2*
95 % CI
Reference
−3·4. 112·5
−37·8, 99·2
−8·4, 125·9
5·2, 141·2
Model 1‡
Regression
coefficient
54·9
34·5
57·3
95 % CI
Model 2§
Regression
coefficient
95 % CI
Reference
−3·1, 113·0
−34·1, 103·1
−9·9, 124·5
46·4
22·9
61·9
Reference
−12·4, 105·2
−46·2, 92·0
−6·5, 130·4
4·1, 140·5
53·8
−15·5, 123·0
72·3*
* P < 0·05.
† Linear regression coefficients indicated the difference in birth weight (g) compared with the reference category.
‡ Model 1 is adjusted for secondhand smoking exposure, family income categories and maternal education categories.
§ Model 2 is adjusted for as model 1 and for pre-pregnancy BMI, gestational duration and parity.
4
journals.cambridge.org/jns
Table 3. Total and trimester-specific associations between maternal fasting during pregnancy and the birth weight of newborns*
(Regression coefficients and 95 % confidence intervals)
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
Crude model
n
Did not fast
Fasted (at any trimester)
Fasted at first trimester
Fasted at second
trimester
Fasted at third
trimester
29
110
23
47
40
Regression
coefficient
Model 1†
95 % CI
Reference
−63·7
−230·5, 103·0
−23·4
−246·8, 200·1
−35·3
−224·2, 153·7
−121·8
−318·0, 74·4
Regression
coefficient
Model 2‡
95 % CI
Regression
coefficient
Reference
−62·3
−241·2, 116·6
−17·1
−274·6, 240·4
−31·5
−233·2, 170·2
−116·2
95 % CI
Reference
−72·1
−257·6, 113·5
−0·7
−260·8, 259·4
−38·1
−244·6, 168·3
−326·4, 94·1
−144·1
−360·2, 72·0
* Linear regression coefficients indicated the difference in birth weight (g) compared with the reference category.
† Model 1 is adjusted for secondhand smoking exposure, family income categories and maternal education categories.
‡ Model 2 is adjusted for as model 1 and for pre-pregnancy BMI, gestational duration and parity.
from those who did not fast, both in the crude and adjusted
analysis. Although not statistically significant, trimester-specific
analysis shows a trend towards reduced birth weight with fasting, especially in women who fasted in the second and third
trimesters. Furthermore, within fasted women, we also
explored if birth weight differed according to fasting intensity.
Fig. 2 shows a boxplot that illustrates the association between
tertiles of fasting days with newborn birth weight. The first tertile of fasting days consists of women who fasted for 1 to 8 d,
while the second and third tertiles include women who fasted
for 10 to 23 and 24 to 30 d.
During Ramadan, we performed a 24 h dietary recall in
ninety-six women. There were forty-two women who were
fasting and fifty-four women who were not fasting at the
day of the interview. The median of gestational age was not
different between the fasting and non-fasting women (33 v.
30 weeks; P = 0·46). Table 4 shows the comparison of intake
between these two groups. Women who were fasting reported
significantly lower percentage of energy intakes from protein
than the non-fasting. They reported lower total energy and
protein intake, although borderline statistically significant.
Fig. 2. Boxplot showing the relationship between tertiles of fasting days and
birth weight. Tertile 1 (n 33), tertile 2 (n 40) and tertile 3 (n 35). The horizontal
lines represent medians, the boxes interquartile ranges, the whiskers are minima and maxima and the circles are outliers.
They also, in general, reported lower intakes of carbohydrates,
water, vitamin A, Na and K, although none was statistically
significant. There was no difference in consumption of fat,
dietary fibre, PUFA, cholesterol, carotene, vitamin E, vitamin
B1, vitamin B2, vitamin B6, folic acid, vitamin C, Ca, Mg, P, Fe
and Zn, as well as percentage of energy from fat and
carbohydrates.
In Table 5, we compared dietary intake of the fasting
women during Ramadan with their intake 1 month later.
Table 4. Maternal dietary intake on one Ramadan day based on fasting
status*
(Mean values with their standard errors; medians and interquartile ranges)
Fasting (n 42)
Total energy
kcal
kJ
Water (g)
Protein (g)†
Fat (g)†
Carbohydrates (g)
Dietary fibre (g)†
PUFA (g)†
Cholesterol (mg)†
Vitamin A (mg)†
Carotene (mg)†
Vitamin E (mg)†
Vitamin B1 (mg)†
Vitamin B2 (mg)†
Vitamin B6 (mg)†
Folic acid (μg)†
Vitamin C (mg)†
Na (mg)†
K (mg)
Ca (mg)†
Mg (mg)
P (mg)†
Fe (mg)†
Zn (mg)
Protein (% TE)
Fat (% TE)
Carbohydrates (% TE)
Non-fasting (n 54)
Mean
SE
Mean
SE
1646·1
6887·3
1870·2
50·9
55·5
215·2
10·4
11·2
227·5
1076·2
0·0
0·0
0·6
0·9
1·2
0·0
63·6
384·2
1793·2
588·6
255·6
843·2
10·4
7·2
12·9
29·3
52·2
60·5
253·1
92·5
25·7
48·3
9·3
7·2
15·6
266·3
1244·2
245·4
3·6
0·6
0·6
0·9
339·4
87·5
627·8
142·6
507·8
17·4
472·4
13·1
0·4
0·6
2·5
1·3
1831·7
7663·8
1940·1
63·6
58·1
232·8
9·8
8·9
217·4
1377·0
0·0
0·0
0·7
1·1
1·2
0·8
76·0
632·3
1906·9
571·4
264·5
937·7
11·5
8·3
15·0
29·8
51·6
80·8
338·1
114·3
39·13
48·0
9·9
5·7
15·0
264·5
2093·9
398·2
2·4
0·6
0·92
1·0
260·8
114·6
911·0
104·3
569·9
15·5
865·7
12·4
0·5
0·4
1·9
1·1
P
0·07
0·64
0·07
0·53
0·21
0·62
0·55
0·30
0·16
0·47
0·94
0·81
0·63
0·66
0·67
0·60
0·14
0·51
0·96
0·70
0·45
0·98
0·14
<0·01
0·86
0·73
% TE, percentage of total energy.
* Results are based on estimation using 24 h nutrition recall. P values are based on
Student’s t test or the Mann–Whitney U test in the case of skewed data.
† Skewed data. Medians and interquartile ranges.
5
journals.cambridge.org/jns
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
Table 5. Maternal dietary intake on one Ramadan day as compared with
1 month after Ramadan within fasting women*
(Mean values with their standard errors; medians and interquartile ranges)
During Ramadan
(n 15)
Total energy
kcal
kJ
Water (g)
Protein (g)
Fat (g)†
Carbohydrates (g)
Dietary fibre (g)
PUFA (g)†
Cholesterol (mg)
Vitamin A (mg)†
Carotene (mg)†
Vitamin E (mg)†
Vitamin B1 (mg)†
Vitamin B2 (mg)
Vitamin B6 (mg)
Folic acid (μg)†
Vitamin C (mg)
Na (mg)†
K (mg)
Ca (mg)
Mg (mg)
P (mg)†
Fe (mg)†
Zn (mg)
Protein (% TE)
Fat (% TE)†
Carbohydrates (% TE)
Table 6. Maternal dietary intake on one Ramadan day as compared with
1 month later in women who were not fasting*
(Mean values with their standard errors; medians and interquartile ranges)
After Ramadan
(n 15)
Mean
SE
Mean
SE
1527·3
6390·2
1686·5
52·5
42·0
196·3
10·4
11·6
234·7
1049·8
0·0
0·0
0·6
0·8
1·2
0·0
62·4
383·9
1583·4
485·9
240·1
835·2
8·2
6·3
13·9
29·8
50·8
103·2
431·8
110·9
5·0
63·3
16·4
0·9
12·0
45·3
1224·3
356·3
2·4
0·4
0·10
0·14
210·0
12·0
644·9
153·7
71·7
25·6
448·4
12·4
0·6
1·1
38·1
2·3
1744·1
7297·3
2255·3
54·8
58·1
246·9
10·1
7·7
228·8
2011·5
0·0
0·0
0·5
0·8
1·2
0·0
78·7
285·9
1589·0
378·9
222·6
646·5
8·0
6·5
13·0
29·5
56·4
165·3
691·6
152·6
5·0
34·2
26·0
1·2
8·1
40·5
1581·7
0·0
0·3
0·4
0·14
0·16
6·5
16·2
906·8
191·1
71·5
25·2
321·4
4·4
0·6
0·7
7·9
1·5
P
0·22
<0·01
0·69
0·02
0·07
0·80
0·41
0·93
0·02
0·06
0·51
0·87
0·82
0·97
0·95
0·40
0·78
0·98
0·26
0·59
0·39
0·23
0·81
0·49
0·09
0·01
Total energy
kcal
kJ
Water (g)
Protein (g)†
Fat (g)
Carbohydrates (g)
Dietary fibre (g)†
PUFA (g)†
Cholesterol (mg)†
Vitamin A (mg)†
Carotene (mg)†
Vitamin E (mg)†
Vitamin B1 (mg)†
Vitamin B2 (mg)†
Vitamin B6 (mg)†
Folic acid (μg)†
Vitamin C (mg)†
Na (mg)†
K (mg)
Ca (mg)†
Mg (mg)
P (mg)†
Fe (mg)†
Zn (mg)†
Protein (% TE)
Fat (% TE)†
Carbohydrates (% TE)
During Ramadan
(n 27)
After Ramadan
(n 27)
Mean
SE
Mean
SE
1888·3
7900·6
1965·7
68·7
62·2
245·6
9·0
9·6
234·4
1743·9
0·0
0·5
0·8
1·2
1·6
2·8
58·7
560·4
1978·2
530·6
282·7
1151·9
14·3
9·7
15·4
28·2
52·8
132·7
555·2
179·1
56·7
7·8
16·5
7·7
16·6
274·3
2573·6
8·0
3·6
0·8
1·2
1·1
351·2
118·3
580·0
165·3
659·7
25·3
893·0
12·7
8·2
0·6
11·9
1·8
1986·9
8313·2
2462·8
58·9
69·2
281·7
9·8
11·0
247·6
2442·4
0·0
0·1
0·9
1·1
1·7
4·0
73·7
533·8
1839·3
620·6
279·2
958·9
10·4
7·8
13·0
30·7
56·2
112·4
470·3
90·6
26·6
4·7
18·2
8·0
10·2
203·8
1541·6
0·0
3·1
0·7
0·6
1·2
350·0
83·5
672·7
164·3
753·1
20·0
498·5
10·3
4·7
0·6
8·9
1·5
P
0·56
<0·01
0·26
0·44
0·10
0·48
0·98
0·55
0·52
<0·01
0·79
0·87
0·51
0·80
0·82
0·60
0·85
0·45
0·88
0·91
0·14
0·06
0·34
0·01
0·41
0·14
% TE, percentage of total energy.
* Results are based on estimation using 24 h nutrition recall. P values are based on
the paired-samples t test or Wilcoxon signed-ranks test in the case of skewed data.
† Skewed data. Medians and interquartile ranges.
% TE, percentage of total energy.
* Results are based on estimation using 24 h nutrition recall. P values are based on
the paired-samples t test or Wilcoxon signed-ranks test in the case of skewed data.
† Skewed data. Medians and interquartile ranges.
There were fifteen women who could be re-interviewed for
this purpose. During Ramadan, fasting women reported significantly less consumption of water, fat and vitamin A, and
had a lower percentage of energy intake from carbohydrates.
Water and fat intakes were significantly lower than 1 month
later by on average 570 and 16 g while carbohydrate intake
was approximately 50 g lower. Intakes of total energy, carbohydrates, vitamin C, Na, Ca and P, as well as percentage of
energy from protein and fat were not significantly different.
In Table 6, we compared the dietary intake of the nonfasting women on 1 d of Ramadan with 1 month later.
There were twenty-seven women who were accessible for
this analysis. As compared with 1 month later, these women
reported a consumption of significantly less water and had a
lower percentage of energy intakes from protein. Intakes of
all other nutrients were similar during Ramadan as compared
with 1 month later.
with newborn birth weight. Furthermore, within the
Ramadan exposed, babies’ birth weight of the fasted women
was not significantly different from that of the babies of nonfasted women. In the present study, we showed that fasted
women reported a significantly lower intake of total energy,
macronutrients and water as compared with women who did
not fast. Women’s intakes were also generally lower during
Ramadan as compared with 1 month later, both in the fasted
and non-fasted group.
To the best of our knowledge, we are the first to study the
effect of Ramadan during pregnancy on birth weight by looking both on the effects of Ramadan overlap and maternal fasting behaviour. We are also among the first to evaluate
women’s dietary intake during and after Ramadan, both in
the fasting and non-fasting group.
There were some limitations of the present study. First,
interviews about women’s fasting behaviour were limited
only to women who came to the hospital during the period
of data collection. The relatively small number of women analysed in the association between fasting and babies’ birth
weight could limit statistical power, thus requiring cautious
interpretation of the findings. Women with available data on
fasting behaviour were at a later stage of gestation as compared
with women without. Furthermore, women with available data
Discussion
Approximately 81 % of all women in our study had Ramadan
exposure at any time during their pregnancies and about 79 %
of them fasted to some extent during the month. Ramadan
exposure during pregnancy was not significantly associated
6
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
journals.cambridge.org/jns
on nutritional intake were also at a later gestational age (24 v.
19 weeks; P < 0·01) and had lower pre-pregnancy BMI (22·2 v.
23·2 kg/m2; P = 0·05) as compared with women without
nutritional data. The average pregnancy weight gain was not
different in women with available nutrition data as compared
with those without (12·9 v. 12·3 kg, P = 0·88). The difference
in gestational age could be caused by the fact that women at
later gestational age had more visits to the hospital, while we
can only speculate about the difference in BMI. Gestational
diabetes mellitus, notably, could confound the relationship
between Ramadan fasting and newborn birth weight; however,
we could not adjust for it in the analysis due to the absence of
gestational diabetes mellitus screening in our cohort.
Furthermore, the use of single 24 h dietary recall as nutritional
assessment may give some disadvantages since it relies on subjects’ memory, cooperation and communication ability, and it
may not have captured the day-to-day variation in nutrient
intake.
We are aware of the possibility of reverse causation, where
babies with longer gestational duration (and therefore higher
birth weight) had higher chance to be exposed to Ramadan.
We dealt with it by restricting the analyses to the full-term
babies. Although we had excluded the preterm babies, we
still found that pregnancies with Ramadan overlap were on
average 4 d longer than those without (Table 1). Thus, gestational length was an important potential confounder to be
adjusted for in our main analysis.
Several other possible confounders were included in our
model as those variables were found to be associated both
with the exposure and with the outcome. Secondhand smoking exposure, lower family income and low maternal education
were slightly more common in the non-fasting women. Fasting
women also had a significantly higher pre-pregnancy BMI and
lower gestational weight gain than the non-fasting. These
women may feel healthier and therefore more prone to fast.
In the previous studies, several maternal characteristics have
been shown to predict maternal fasting during Ramadan,
such as pre-pregnancy BMI, parity, maternal age and socioeconomic status(17,32,34,35).
Our finding of no significant difference in birth weight of
babies with or without Ramadan overlap during pregnancy is
in accordance with several previous studies(15,27,36). These
studies were, however, mostly based on registry data with limited information on women’s religion and might therefore
have included non-Muslim women in their analysis. Our finding of no significant difference in babies’ birth weight in the
fasting women as compared with the non-fasting women is
also in line with several earlier studies(16–18,26,29,30), although
different from our previous study among pregnant Muslim
women in Amsterdam (The Netherlands). In the previous
study, a lower birth weight was found with maternal fasting
in the first trimester(32). The difference in the finding could
be attributed to the contrast in cultural and dietary habits of
these women, who were mostly of Turkish and Moroccan
background. Variation in the climate, duration and the number
of fasting days could also influence the degree of exposure.
Our dietary assessments showed that women who were fasting during Ramadan in general reported lower percentage of
total energy intake from protein, intake of total energy and
macronutrients, as well as water, vitamin A, Na and K as compared with the non-fasting women. The differences in
women’s intakes were unlikely to be caused by the difference
in their gestational age since women in both groups had similar
gestational age at the interview. This result is in accordance
with findings from previous studies on dietary intake of pregnant women during Ramadan which found significantly lower
energy intake among women who fasted as compared with
those who did not(22), and lower energy intake during
Ramadan as compared with outside Ramadan(37). In contrast,
our result is different from a study conducted among Saudi
families which reported weight gains due to higher consumption of carbohydrates and fat-rich food during Ramadan(9).
Ramadan also appeared to influence dietary intakes of
women both in the fasting and non-fasting groups. It was
shown by lower intakes of total energy, carbohydrates, fat
and water during Ramadan as compared with intakes of the
same women 1 month later, both in the fasting and nonfasting groups. More substantial changes of the intake during
Ramadan as compared with 1 month later, however, were evident among fasting women. We suggest that in the non-fasting
women, dietary habits were also influenced by their fasting
families, as seen by the reduction of the frequency and/or
the portion size of women’s meals. Furthermore, as compared
with the Indonesian estimated average requirement for pregnant women, we found that the mean intakes of protein and
fat of women in our study consistently exceeded the recommendation, while carbohydrate intakes were generally lower
than recommended. The estimated average requirements for
protein, fat and carbohydrate are 43–52, 40–42 and 270–
285 g, respectively(38,39).
Despite the nutrition restriction during Ramadan, a significant reduction of (secondhand) smoke exposure is expected
since Muslims are not allowed to smoke during daylight(40,41).
This temporary change may, to some extent, influence the
birth weight of Ramadan-exposed babies. Furthermore,
Ramadan is followed afterwards by several days of Eid celebration. During this celebration, people gather with family and
friends and usually have meals with high fat and sugar contents. Eid celebration, which is less likely to be experienced
by women who did not have Ramadan in their pregnancy,
may enable the exposed pregnant women to compensate.
Our study showed that women who were exposed to
Ramadan and did not fast had the highest weight gain during
pregnancy (17·6 (SE 1·6) kg), as compared with women who
fasted (11·6 (SE 0·9) kg) and Ramadan-unexposed women
(12·2 (SE 0·6) kg). This finding is consistent with several studies(16,22,23,42) which reported significantly lower weight gain in
women who fasted during pregnancy as compared with
women who did not. Furthermore, women who were exposed
to Ramadan and did not fast might have had the highest fat or
sugar intake, through the consumption of seasonal meals during and shortly after Ramadan.
In conclusion, in Indonesian Muslim women lifestyle
changes that occur with Ramadan are associated with lower
reported energy intake. Ramadan overlap during pregnancy
was not significantly associated with offspring birth weight
7
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
journals.cambridge.org/jns
while we cannot conclude on the effect of fasting on birth
weight due to limited statistical power. Further studies with larger sample size focusing on other pregnancy outcomes and the
offspring’s long-term health are needed.
18.
19.
20.
Acknowledgements
The authors have indicated they have no financial relationships
relevant in this article to disclose.
A. I. S. and C. S. P. M. U. formulated the research question
and designed the study; A. I. S. acquired the data; A. I. S. and
C. S. P. M. U. analysed and interpreted the data and drafted
the manuscript; D. A., R. C. P., M. B., T. J. R. and
D. E. G. critically reviewed the manuscript for important intellectual content. All authors read and approved the final
manuscript.
The authors declared no potential conflicts of interest with
respect to the authorship and/or publication of this article.
21.
22.
23.
24.
25.
26.
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
Abu-Saad K & Fraser D (2010) Maternal nutrition and birth outcomes. Epidemiol Rev 32, 5–25.
Rush D (2001) Maternal nutrition and perinatal survival. Nutr Rev
59, 315–326.
Wu G, Imhoff-Kunsch B & Girard AW (2012) Biological mechanisms for nutritional regulation of maternal health and fetal development. Paediatr Perinat Epidemiol 26, Suppl. 1, 4–26.
Barker DJP (2007) The origins of the developmental origins theory.
J Intern Med 261, 412–417.
Barker DJP, Lampl M, Roseboom T, et al. (2012) Resource allocation in utero and health in later life. Placenta 33, Suppl. 2, e30–e34.
Gluckman PD, Hanson M & Beedle A (2007) Early life events and
their consequences for later disease: a life history and evolutionary
perspective. Am J Hum Biol 19, 1–19.
Jaddoe VW (2008) Fetal nutritional origins of adult diseases: challenges for epidemiological research. Eur J Epidemiol 23, 767–771.
Roseboom TJ, Painter RC, van Abeelen AFM, et al. (2011) Hungry
in the womb: what are the consequences? Lessons from the Dutch
famine. Maturitas 70, 141–145.
Bakhotmah BA (2011) The puzzle of self-reported weight gain in a
month of fasting (Ramadan) among a cohort of Saudi families in
Jeddah, Western Saudi Arabia. Nutr J 10, 84.
Alkandari JR, Maughan RJ, Karli U, et al. (2012) The implications
of Ramadan fasting for human health and well-being. J Sports Sci
30, Suppl. 1, S9–S19.
Trepanowski JF & Bloomer RJ (2010) The impact of religious fasting on human health. Nutr J 9, 57.
Roky R, Chapotot F, Hakkou F, et al. (2001) Sleep during Ramadan
intermittent fasting. J Sleep Res 10, 319–327.
Alwasel SH, Harrath A, Aljarallah JS, et al. (2013) Intergenerational
effects of in utero exposure to Ramadan in Tunisia. Am J Hum Biol
25, 341–343.
Leiper JB, Molla A & Molla A (2003) Effects on health of fluid
restriction during fasting in Ramadan. Eur J Clin Nutr 57, Suppl.
2, S30–S38.
Almond D & Mazumder B (2011) Health capital and the prenatal
environment: the effect of Ramadan observance during pregnancy.
Am Econ J 3, 56–85.
Ziaee V, Kihanidoost Z, Younesian M, et al. (2010) The effect of
Ramadan fasting on outcome of pregnancy. Iran J Pediatr 20,
181–186.
Kavehmanesh Z & Abolghasemi H (2004) Maternal Ramadan fasting and neonatal health. J Perinatol 24, 748–750.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
Arab M & Nasrollahi S (2001) Interrelation of Ramadan fasting and
birthweight. Med J Islam Acad Sci 14, 91–95.
Ewijk RJG V, Painter RC & Roseboom TJ (2013) Associations of
prenatal exposure to Ramadan with small stature and thinness in
adulthood: results from a large Indonesian population-based
study. Am J Epidemiol 177, 729–736.
Makki AM (2002) Impact of Ramadan fasting on birth weight in 4
hospitals in Sana’a city, Yemen. Saudi Med 23, 1419–1420.
Robinson T & Raisler J (2005) “Each one is a doctor for herself”:
Ramadan fasting among pregnant Muslim women in The United
States. Ethn Dis 15, 99–103.
Kiziltan G, Karabudak E, Tuncay G, et al. (2005) Dietary intake
and nutritional status of Turkish pregnant women during
Ramadan. Saudi Med J 26, 1782–1787.
Khoshdel A, Kheiri S, Hashemi-Dehkordi E, et al. (2014) The
effect of Ramadan fasting on LH, FSH, oestrogen, progesterone
and leptin in pregnant women. J Obstet Gynaecol 34, 634–638.
Mirghani HM, Weerasinghe DS, Ezimokhai M, et al. (2003) The
effect of maternal fasting on the fetal biophysical profile. Int J
Gynecol Obstet 81, 17–21.
Dikensoy E, Balat O, Cebesoy B, et al. (2009) The effect of
Ramadan fasting on maternal serum lipids, cortisol levels and
fetal development. Arch Gynecol Obstet 279, 119–123.
Hızlı D, Yılmaz SS, Onaran Y, et al. (2012) Impact of maternal fasting during Ramadan on fetal Doppler parameters, maternal lipid
levels and neonatal outcomes. J Matern Neonatal Med 25, 975–977.
Cross H, Eminson J & Wharton BA (1990) Ramadan and birth
weight at full term in Asian Moslem pregnant women in
Birmingham. Arch Dis Child 65, 1053–1056.
Naderi T & Kamyabi Z (2004) Determinationof fundal height
increase in fasting and non-fasting pregnant women during
Ramadan. Saudi Med J 25, 809–815.
Ozturk E, Balat O, Ugur MG, et al. (2011) Effect of Ramadan fasting on maternal oxidative stress during the second trimester: a preliminary study. J Obstet Gynaecol Res 37, 729–733.
Shahgheibi S, Ghadery E, Pauladi A, et al. (2005) Effects of fasting
during the third trimester of pregnancy on neonatal growth indices.
Ann Alquds Med 2, 58–62.
Faris MA-IE & Al-Holy MA (2014) Implications of Ramadan intermittent fasting on maternal and fetal health and nutritional status: a
review. Med J Nutr Metab 7, 107–118.
Savitri AI, Yadegari N, Bakker J, et al. (2014) Ramadan fasting and
newborn’s birth weight in pregnant Muslim women in The
Netherlands. Br J Nutr 112, 1503–1509.
Almond D & Mazumder B (2008) Health Capital and the Prenatal
Environment: The Effect of Maternal Fasting during Pregnancy.
http://www.nber.org/papers/w14428
(accessed
December
2017).
Joosoph J, Abu J & Yu SL (2004) A survey of fasting during pregnancy. Singapore Med J 45, 583–586.
Petherick ES, Tuffnell D & Wright J (2014) Experiences and outcomes of maternal Ramadan fasting during pregnancy: results from
a sub-cohort of the Born in Bradford birth cohort study. BMC
Pregnancy Childbirth 14, 335.
Alwasel SH, Abotalib Z, Aljarallah JS, et al. (2010) Changes in placental size during Ramadan. Placenta 31, 607–610.
Al-Hourani H & Atoum M (2007) Body composition, nutrient
intake and physical activity patterns in young women during
Ramadan. Singapore Med J 48, 906–910.
Muhilal (2002) Peran Gizi Dalam Meningkatkan Kualitas Sumber Daya
Manusia: Telaah Dari Aspek Biokimia Gizi Hingga Pedoman Gizi
Seimbang. Pidato Pengukuhan Jabatan Guru Besar Dalam Ilmu Gizi
(The Role of Nutrition in Improving the Quality of Human Resources: A
Study of the Nutritional Biochemical Aspect to a Balanced Nutrition
Guideline. Inaugural Speech of Professorship in Nutrition Science).
Bandung: Padjadjaran University.
Muhilal, Jalal F & Hardiansyah (1998) Angka kecukupan yang dianjurkan (RDA). In Prosiding Widyakarya Nasional Pangan Dan Gizi
VI, Serpong, 17–20 Februari 1998 (Proceedings of National Symposium
8
Downloaded from https://www.cambridge.org/core. IP address: 54.70.40.11, on 07 Sep 2019 at 11:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jns.2017.70
journals.cambridge.org/jns
40.
on Food and Nutrition VI, Serpong, 17–20 February 1998). Jakarta:
Lembaga Ilmu Pengetahuan Indonesia.
Aveyard P, Begh R, Sheikh, et al. (2011) Promoting smoking cessation through smoking reduction during Ramadan. Addiction 106,
1379–1380.
41.
42.
Ghouri N, Atcha M & Sheikh A (2006) Influence of Islam on
smoking among Muslims. BMJ 332, 291–294.
Awwad J, Usta IM, Succar J, et al. (2012) The effect of maternal
fasting during Ramadan on preterm delivery: a prospective cohort
study. BJOG 119, 1379–1386.
9