Intensive Care Med (2012) 38:577–591
DOI 10.1007/s00134-012-2513-4
CO NFERENCE REPORTS AND EXPERT PANEL
International evidence-based
recommendations for point-of-care
lung ultrasound
Giovanni Volpicelli
Mahmoud Elbarbary
Michael Blaivas
Daniel A. Lichtenstein
Gebhard Mathis
Andrew W. Kirkpatrick
Lawrence Melniker
Luna Gargani
Vicki E. Noble
Gabriele Via
Anthony Dean
James W. Tsung
Gino Soldati
Roberto Copetti
Belaid Bouhemad
Angelika Reissig
Eustachio Agricola
Jean-Jacques Rouby
Charlotte Arbelot
Andrew Liteplo
Ashot Sargsyan
Fernando Silva
Richard Hoppmann
Raoul Breitkreutz
Armin Seibel
Luca Neri
Enrico Storti
Tomislav Petrovic
International Liaison Committee on Lung Ultrasound
(ILC-LUS) for the International
Consensus Conference on Lung Ultrasound (ICC-LUS)
Received: 29 October 2011
Accepted: 23 January 2012
Published online: 6 March 2012
! Copyright jointly held by Springer and
ESICM 2012
M. Blaivas
Department of Emergency Medicine,
Northside Hospital Forsyth,
Atlanta, GA, USA
e-mail:
[email protected]
Electronic supplementary material
The online version of this article
(doi:10.1007/s00134-012-2513-4) contains
supplementary material, which is available
to authorized users.
D. A. Lichtenstein
Service de Réanimation Médicale, Hôpital
Ambroise-Paré, Paris-Ouest, Boulogne,
France
e-mail:
[email protected]
L. Melniker
Clinical Epidemiology Unit, Division of
General Internal Medicine, Department
of Medicine, Weill Medical College of
Cornell University, New York, USA
e-mail:
[email protected]
L. Gargani
Institute of Clinical Physiology,
National Research Council, Pisa, Italy
e-mail:
[email protected]
V. E. Noble
G. Mathis
Internal Medicine Praxis, Rankweil, Austria Division of Emergency Ultrasound,
Department of Emergency Medicine,
e-mail:
[email protected]
Massachusetts General Hospital,
Boston, MA, USA
A. W. Kirkpatrick
e-mail:
[email protected]
Foothills Medical Centre, Calgary, AB,
Canada
G. Via
e-mail: andrew.kirkpatrick@
M. Elbarbary
1st Department of Anesthesia and Intensive
albertahealthservices.ca
National & Gulf Center for Evidence Based
Care Pavia, IRCCS Foundation Policlinico
Health Practice, King Saud University for
San Matteo, Pavia, Italy
Health Sciences, Riyadh, Saudi Arabia
e-mail:
[email protected]
e-mail:
[email protected]
G. Volpicelli ())
Department of Emergency Medicine,
San Luigi Gonzaga University Hospital,
10043 Orbassano, Torino, Italy
e-mail:
[email protected]
578
A. Dean
Division of Emergency Ultrasonography,
Department of Emergency Medicine,
University of Pennsylvania Medical Center,
Philadelphia, PA, USA
e-mail:
[email protected]
J. W. Tsung
Departments of Emergency Medicine and
Pediatrics, Mount Sinai School of Medicine,
New York, NY, USA
e-mail:
[email protected]
G. Soldati
Emergency Medicine Unit, Valle del
Serchio General Hospital, Lucca, Italy
e-mail:
[email protected]
R. Copetti
Medical Department, Latisana Hospital,
Udine, Italy
e-mail:
[email protected]
F. Silva
Department of Emergency Medicine,
UC Davis Medical Center,
Sacramento, CA, USA
e-mail:
[email protected]
R. Hoppmann
Internal Medicine, University of South
Carolina School of Medicine,
Columbia, SC, USA
e-mail:
[email protected]
R. Breitkreutz
Department of Anaesthesiology, Intensive
Care and Pain Therapy, University Hospital
of the Saarland and Frankfurt Institute of
Emergency Medicine and Simulation
Training (FINEST), Homburg, Germany
e-mail:
[email protected]
A. Seibel
Diakonie Klinikum jung-stilling,
Siegen, Germany
e-mail:
[email protected]
B. Bouhemad
Surgical Intensive Care Unit, Department
L. Neri
of Anesthesia and Critical Care, Groupe
Hospitalier Paris Saint-Joseph, Paris, France AREU EMS Public Regional Company,
Niguarda Ca’ Granda Hospital,
e-mail:
[email protected]
Milano, Italy
e-mail:
[email protected]
A. Reissig
Department of Pneumology and
E. Storti
Allergology, Medical University Clinic I,
Intensive Care Unit ‘‘G. Bozza,’’, Niguarda
Friedrich-Schiller University,
Ca’ Granda Hospital, Milan, Italy
Jena, Germany
e-mail:
[email protected] e-mail:
[email protected]
E. Agricola
Division of Noninvasive Cardiology,
San Raffaele Scientific Institute, IRCCS,
Milan, Italy
e-mail:
[email protected]
T. Petrovic
Samu 93, University Hospital Avicenne,
Bobigny, France
e-mail:
[email protected]
J.-J. Rouby ! C. Arbelot
Multidisciplinary Intensive Care Unit,
Department of Anesthesiology,
Pitié-Salpêtrière Hospital,
University Pierre and Marie Curie (UPMC),
Paris 6, France
e-mail:
[email protected]
Abstract Background: The purpose of this study is to provide
evidence-based and expert consensus
recommendations for lung ultrasound
with focus on emergency and critical
care settings. Methods: A multidisciplinary panel of 28 experts from
eight countries was involved. Literature was reviewed from January 1966
to June 2011. Consensus members
searched multiple databases including
Pubmed, Medline, OVID, Embase,
and others. The process used to
develop these evidence-based recommendations involved two phases:
determining the level of quality of
evidence and developing the recommendation. The quality of evidence is
C. Arbelot
e-mail:
[email protected]
A. Liteplo
Emergency Medicine, Massachusetts
General Hospital, Boston, MA, USA
e-mail:
[email protected]
A. Sargsyan
Wyle/NASA Lyndon B. Johnson Space
Center Bioastronautics Contract,
Houston, TX, USA
e-mail:
[email protected]
assessed by the grading of recommendation, assessment, development,
and evaluation (GRADE) method.
However, the GRADE system does
not enforce a specific method on how
the panel should reach decisions
during the consensus process. Our
methodology committee decided to
utilize the RAND appropriateness
method for panel judgment and decisions/consensus. Results: Seventythree proposed statements were
examined and discussed in three
conferences held in Bologna, Pisa,
and Rome. Each conference included
two rounds of face-to-face modified
Delphi technique. Anonymous panel
voting followed each round. The
panel did not reach an agreement and
therefore did not adopt any recommendations for six statements. Weak/
conditional recommendations were
made for 2 statements, and strong
recommendations were made for the
remaining 65 statements. The statements were then recategorized and
grouped to their current format.
Internal and external peer-review
processes took place before submission of the recommendations.
Updates will occur at least every
4 years or whenever significant major
changes in evidence appear. Conclusions: This document reflects the
overall results of the first consensus
conference on ‘‘point-of-care’’ lung
ultrasound. Statements were discussed and elaborated by experts who
published the vast majority of papers
on clinical use of lung ultrasound in
the last 20 years. Recommendations
were produced to guide implementation, development, and
standardization of lung ultrasound in
all relevant settings.
Keywords Lung ultrasound !
Chest sonography ! Emergency
ultrasound ! Critical ultrasound !
Point-of-care ultrasound ! Guideline !
RAND ! GRADE !
Evidence-based medicine
579
Introduction
Table 1 Levels of quality of evidence
Modern lung ultrasound is mainly applied not only in
critical care, emergency medicine, and trauma surgery,
but also in pulmonary and internal medicine. Many
international authors have produced several studies on
the application of lung ultrasound in various settings.
The emergence of differences in approach, techniques
utilized, and nomenclature, however, provided the
stimulus to initiate a guideline/consensus process with
the aim of elaborating a unified approach and language
for six major areas, namely terminology, technology,
technique, clinical outcomes, cost effectiveness, and
future research. This process was conducted following a
rigorous scientific pathway to produce evidence-based
guidelines containing a list of recommendations for
clinical application of lung ultrasound [1]. A literature
search was performed, and a multidisciplinary, international panel of experts was identified. The proposed
recommendations represent a framework for ‘‘point-ofcare’’ lung ultrasound intended to standardize its
application around the globe and in different clinical
settings.
This report constitutes a concise, shortened version of
the original document. The electronic version, accessible
online as supplementary material, provides a full explanation of methods and a comprehensive discussion for
each recommendation (see Electronic Supplementary
Material 1).
Level Pointsb Quality
Methods
Grading of recommendation, assessment, development,
and evaluation (GRADE) method was used to develop
these evidence-based recommendations [2]. The process
involves two phases: (1) determining the level of quality
of evidence, and (2) developing the recommendation.
Relevant articles with clinical outcomes were classified
into three levels of quality based on the criteria of the
GRADE methodology for developing guidelines and
clinical recommendations (Table 1). RAND appropriateness method (RAM) was used within the GRADE steps
that required panel judgment and decisions/consensus [3].
RAM was also used in formulating the recommendations
based purely on expert consensus, such as recommendations related to terminology. Recommendations were
generated in two classes (strong or weak/conditional)
based on the GRADE criteria taking into consideration
preset rules that defined the panel agreement/consensus
and its degree. The transformation of evidence into recommendation depends on the evaluation by the panel for
outcome, benefit/cost, and benefit/harm ratios, and certainty about similarity in values/preferences [2].
A
C4
B
3
Ca
B2
Interpretation
High
Further research is very unlikely to
change our confidence in the estimate
of effect or accuracy
Moderate Further research is likely to have an
important impact on our confidence in
the estimate of effect or accuracy and
may change the estimate
Lowa
Further research is very likely to have
an important impact on our
confidence in the estimate of effect or
accuracy and is likely to change the
estimate. Any estimate of effect or
accuracy is very uncertain (very low)
This table was modified from Guyatt et al. [2]
a
Level C can be divided into low (points = 2) and very low
(points = 1 or less)
b
Points are calculated based on the nine GRADE quality factors
[2]
Panel selection
Experts were eligible for selection if they had published
as first author a peer-reviewed article on lung ultrasound
during the past 10 years in more than one main topic of
lung ultrasound (pneumothorax, interstitial syndrome,
lung consolidation, monitoring, neonatology, pleural
effusion), taking into consideration the proportionality as
determined by a MEDLINE literature search from 1966 to
October 2010. Methodologists with experience in evidence-based methodology and guideline development
were also included (see ‘‘Appendix’’ for list of participants, affiliations, and assignments).
Literature search strategy
The literature search was done in two tracks. The experts
themselves, with more than one expert search in each
domain to avoid selection bias, constituted the first track.
An epidemiologist assisted by a professional librarian
performed the second track by conducting literature
search of English-language articles from 1966 to October
2010. See Table 2 for search databases, terms, and the
MeSH headings used. The two bibliographies were
compared for thoroughness and consistency.
Panel meetings and voting
The panel of experts met on three occasions: Bologna
(28–30 November 2009), Pisa (11–12 May 2010), and
Rome (7–9 October 2010). The panelists formulated draft
580
Table 2 Search terms used
MeSH
headings
Terms
Sonography (echographic OR echography OR sonographic OR
sonography OR ultrasonic OR ultrasonographic
OR ultrasonography OR ultrasound).ti
EM/CCM
(bedside OR critical OR intensive OR emergency OR
emergent OR urgency OR urgent OR critical OR
critically OR shock OR unstable OR hypotensive
OR hypoperfusion OR sepsis).ti
ECHO
(cardiac OR cardiologic OR cardiological
echocardiography OR echocardiographic OR heart
OR pacing OR chest OR lung OR congestive heart
failure OR CHF OR ADHF OR pressure).ti
LUNG
(lung OR chest OR thoracic OR transthoracic OR
cardiothoracic OR pleural OR pulmonary OR
pulmonic OR pneumology OR pneumonic OR
alveolar OR interstitial OR pneumothorax OR
hemothorax OR consolidation).ti
OTHER
(accuracy OR accurate OR sensitivity OR sensitive
OR specificity OR specific OR predictive OR
predict).ti
COST
(cost OR effective OR effectiveness OR efficacy OR
efficacious OR efficient OR efficiency OR benefit
OR value).ti
Search databases: Books@Ovid June 02, 2011; Journals@Ovid Full
Text June 2003, 2011; Your Journals@Ovid; AMED (Allied and
Comp Medicine) 1985 to May 2011; CAB Abstracts Archive
1910–1972; Embase 1980–2011 week 22; ERIC 1965 to May
2011; Health and Psychosocial Instruments 1985 to April 2011;
Ovid MEDLINE(R) In-Process and Other Non-Indexed Citations
and Ovid MEDLINE(R) 1948 to present; Ovid MEDLINE(R) 1948
to May week 4 2011; Social Work Abstracts 1968 to June 2011;
NASW Clinical Register 14th Edition
recommendations before the conferences, which laid the
foundation to work together and critique the recommendations during the conferences. At each plenary
conference, a representative of each domain presented
potentially controversial issues in the recommendations. A
face-to-face debate took place in two rounds of modified
Delphi technique; after each round, anonymous voting was
conducted. A standardized method for determining the
agreement/disagreement and the degree of agreement and
hence for deciding about the grade of recommendation
(weak versus strong) was then applied [3, 4].
Results
Literature search results
judgment about the quality of evidence-based recommendations was only done after assigning the articles to
each statement/question.
General results
A total number of 73 proposed statements were examined
by 28 experts and discussed in the three conferences.
Each statement was coded with an alphanumeric code,
which includes the following in order of appearance: the
location of the conference (Bologna, B; Pisa, P; Rome,
RL), the number assigned to the domain, and the number
assigned to the statement. Table 3 presents each statement
code with its grade of recommendation, degree of consensus, and level of quality of evidence.
Statements and discussion
Pneumothorax
Technique
Statement code B-D1-S1 (strong recommendation:
level A of evidence)
• The sonographic signs of pneumothorax include the
following:
–
–
–
–
Presence of lung point(s)
Absence of lung sliding
Absence of B-lines
Absence of lung pulse
B-D1-S2 (strong: level A)
• In the supine patient, the sonographic technique
consists of exploration of the least gravitationally
dependent areas progressing more laterally.
• Adjunct techniques such as M-mode and color
Doppler may be used.
B-D1-S3 (weak: level C)
• Ultrasound scanning for pneumothorax may be a basic
ultrasound technique with a steep learning curve.
P-D1-S2 (strong: level B)
• During assessment for pneumothorax in adults, a
microconvex probe is preferred. However, other
transducer (e.g., linear array, phased array, convex)
may be chosen based on physician preference and
clinical setting.
A total of 209 articles and two books were retrieved by
the first track search. An additional 110 articles were Clinical implications
added from the second track over a 1-year period. These
B-D1-S4 (strong: level A)
320 references (see Electronic Supplementary Material 1)
were individually appraised based on methodological • Lung ultrasound should be used in clinical settings
criteria to determine the initial quality level. The final
when pneumothorax is in the differential diagnosis.
581
Table 3 Summary table for the 73 statements with their level of evidence
SN Statement Recommendation
code
strength
Degree of
consensus
Level of quality SN Statement Recommendation
of evidence
code
strength
Degree of
consensus
Level of quality
of evidence
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
Very good
Very good
Some
Very good
Very good
Good
Good
No
Very good
Very good
Very good
Good
Very good
Very good
No
Very good
Very good
Very good
Very good
Some
Good
Very good
Very good
Good
No
Very good
Good
Very good
Very good
Very good
Very good
Very good
Very good
Good
No
No
Very good
A
A
C
A
B
A
C
C
A
A
B
B
B
B
C
C
N/A
N/A
C
C
N/A
A
A
B
C
A
A
A
A
A
B
B
A
C
N/A
C
B
Very good
Very good
Very good
No
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Very good
Good
N/A
B
B
C
A
A
B
B
B
B
A
B
B
B
B
B
B
B
A
A
B
A
A
B
B
B
B
B
B
B
A
A
A
N/A
N/A
B
B-D1-S1
B-D1-S2
B-D1-S3
B-D1-S4
B-D1-S5
B-D1-S6
B-D1-S7
B-D1-S8
B-D2-S1
B-D2-S2
B-D2-S3
B-D2-S4
B-D2-S5
B-D2-S6
B-D2-S7
B-D2-S8
B-D2-S9
B-D2-S10
B-D3-S1
B-D3-S2
B-D3-S3
B-D3-S4
B-D3-S5
B-D3-S6
B-D3-S7
B-D3-S8
B-D4-S1
B-D4-S2
B-D4-S3
B-D4-S4
B-D4-S5
B-D4-S6
B-D4-S7
B-D4-S8
B-D4-S9
P-D1-S1
P-D1-S2
Strong
Strong
Weak
Strong
Strong
Strong
Strong
No = disagreement
Strong
Strong
Strong
Strong
Strong
Strong
No = disagreement
Strong
Strong
Strong
Strong
Weak
Strong
Strong
Strong
Strong
No = disagreement
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
No = disagreement
No = disagreement
Strong
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
P-D2-S1
P-D2-S2
P-D2-S3
P-D2-S4
P-D3-S1
P-D3-S2
P-D3-S3
P-D3-S4
P-D3-S5
P-D3-S6
P-D3-S7
P-D4-S1
P-D4-S2
P-D4-S3
P-D4-S4
P-D4-S5
P-D4-S6
P-D4-S7
P-D4-S8
P-D4-S9
P-D5-S1
RL-D2-S1
RL-D2-S2
RL-D3-S1
RL-D3-S2
RL-D3-S3
RL-D3-S4
RL-D3-S5
RL-D4-S1
RL-D4-S2
RL-D4-S3
RL-D4-S4
RL-D4-S5
RL-D5-S1
RL-D5-S2
RL-D6-S1
Strong
Strong
Strong
No = disagreement
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
Strong
No statement for D1 in Rome (removed for duplication); RL-D6-S1 was a revision of P-D2-S4 due to new evidence presented; statement
B-D3-S1 covers information given by statements P-D3-S4 and P-D3-S5; these latter two are not presented in the document
B Bologna, P Pisa, RL Rome-Lung, D domain, S statement, SN statement number, N/A not applicable
Imaging strategies and outcomes
B-D1-S5 (strong: level B)
• Lung ultrasound more accurately rules in the diagnosis of pneumothorax than supine anterior chest
radiography (CXR).
B-D1-S6 (strong: level A)
suspected pneumothorax, and may lead to better
patient outcome.
B-D1-S8 (no consensus: level C)
• Lung ultrasound compares well with computerized tomography in assessment of pneumothorax
extension.
P-D1-S1 (no consensus: level C)
• Lung ultrasound more accurately rules out the diagnosis of pneumothorax than supine anterior chest
radiography.
B-D1-S7 (strong: level C)
• Bedside lung ultrasound is a useful tool to differentiate between small and large pneumothorax, using
detection of the lung point.
Comments The four sonographic signs useful to
• Lung ultrasound when compared with supine chest diagnose pneumothorax and their usefulness in ruling in
radiography may be a better diagnostic strategy as an and ruling out the condition are reported in Fig. 1 [5].
initial diagnostic study in critically ill patients with Lung sliding is the depiction of a regular rhythmic
582
interpretation of the combination of findings as lung
bullae, contusions, adhesions, and others that can result in
false positives.
Interstitial syndrome
Artifacts and physics
P-D2-S1 [strong: level not applicable (N/A)]
• B-lines are defined as discrete laser-like vertical
hyperechoic reverberation artifacts that arise from
the pleural line (previously described as ‘‘comet
tails’’), extend to the bottom of the screen without
fading, and move synchronously with lung sliding.
RL-D5-S1 (strong: level N/A)
• B-lines are artifacts.
Fig. 1 Flow chart on diagnosing pneumothorax. This flow chart
suggests the correct sequence and combination of the four
sonographic signs useful to rule out or rule in pneumothorax
RL-D5-S2 (strong: level N/A)
• The anatomic and physical basis of B-lines is not
known with certainty at this time.
B-D2-S9 (strong: level N/A)
movement synchronized with respiration that occurs • The term ‘‘sliding’’ (rather than ‘‘gliding’’) should be
between the parietal and visceral pleura that are either in
used in the description of pleural movement.
direct apposition or separated by a thin layer of intrapleural fluid [6–9]. The lung pulse refers to the subtle
rhythmic movement of the visceral upon the parietal
pleura with cardiac oscillations [6, 8, 10]. As B-lines Scanning and training methodology
(well defined elsewhere) originate from the visceral B-D2-S1 (strong: level A)
pleura, their simple presence proves that the visceral
pleura is opposing the parietal, thus excluding pneumo- • Multiple B-lines are the sonographic sign of lung
interstitial syndrome.
thorax at that point. The lung point refers to the depiction
of the typical pattern of pneumothorax, which is simply B-D2-S2 (strong: level A)
the absence of any sliding or moving B-lines at a physical
location where this pattern consistently transitions into an • In the evaluation of interstitial syndrome, the sonographic technique ideally consists of scanning
area of sliding, which represents the physical limit of
eight regions, but two other methods have been
pneumothorax as mapped on the chest wall [7, 11, 12].
described:
In extreme emergency, absence of any movement of
the pleural line, either horizontal (sliding) or vertical
– A more rapid anterior two-region scan may be
(pulse), coupled with absence of B-lines allows prompt
sufficient in some cases.
and safe diagnosis of pneumothorax without the need for
– The evaluation of 28 rib interspaces is an
searching the lung point.
alternative.
Lung ultrasound is more accurate than CXR particularly in ruling out pneumothorax [1, 6, 13–17]. There are • A positive region is defined by the presence of three or
more B-lines in a longitudinal plane between two ribs.
some settings where lung ultrasound for pneumothorax is
not only recommended but also essential: cardiac arrest/
unstable patient, radio-occult pneumothorax, and limited- B-D2-S4 (strong: level B)
resource areas.
• In the evaluation of interstitial syndrome, the followDisagreement on the steep learning curve of the
ing suggest a positive exam:
technique is based on the fact that the positive predictive
– Two or more positive regions (see B-D2-S2)
value of ultrasound and its specificity have tended to be
bilaterally.
slightly lower than the sensitivity in the studies on
– The 28 rib space technique may semiquantify the
pneumothorax. Consideration has been made that diaginterstitial syndrome: in each rib space, count the
nosis of pneumothorax can require more nuanced
583
number of B-lines from zero to ten, or if confluent,
assess the percentage of the rib space occupied by
B-lines and divide it by ten.
B-D2-S10 (strong: level N/A)
• The term ‘‘B-pattern’’ should be used (rather than
‘‘lung rockets’’ or ‘‘B-PLUS’’) in the description of
multiple B-lines in patients with interstitial syndrome.
B-D2-S3 (strong: level B)
• In the evaluation of interstitial syndrome, lung
ultrasound should be considered as a basic technique
with a steep learning curve.
Clinical implications
P-D5-S1 (strong: level B)
• The presence of multiple diffuse bilateral B-lines
indicates interstitial syndrome. Causes of interstitial
syndrome include the following conditions:
parenchymal lung disease
include the following:
(pulmonary
fibrosis)
– Pleural line abnormalities (irregular, fragmented
pleural line)
– Subpleural abnormalities (small echo-poor areas)
– B-lines in a nonhomogeneous distribution
RL-D3-S4 (strong: level B)
• In contrast to cardiogenic pulmonary edema, the
sonographic findings that are indicative of acute
respiratory distress syndrome (ARDS) include the
following:
–
–
–
–
Anterior subpleural consolidations
Absence or reduction of lung sliding
‘‘Spared areas’’ of normal parenchyma
Pleural line abnormalities (irregular thickened
fragmented pleural line)
– Nonhomogeneous distribution of B-lines
Imaging strategies
– Pulmonary edema of various causes
– Interstitial pneumonia or pneumonitis
B-D2-S5 (strong: level B)
– Diffuse parenchymal lung disease (pulmonary
• Lung ultrasound is superior to conventional chest
fibrosis)
radiography for ruling in significant interstitial
syndrome.
P-D2-S2 (strong: level B)
• Regarding B-lines, focal multiple B-lines may be
present in a normal lung, and a focal (localized)
sonographic pattern of interstitial syndrome may be
seen in the presence of any of the following:
–
–
–
–
–
–
B-D2-S6 (strong: level B)
• In patients with suspected interstitial syndrome, a
negative lung ultrasound examination is superior to
Pneumonia and pneumonitis
Atelectasis
Pulmonary contusion
Pulmonary infarction
Pleural disease
Neoplasia
RL-D3-S1 (strong: level B)
• Lung ultrasound is a reliable tool to evaluate diffuse
parenchymal lung disease (pulmonary fibrosis).
• The primary sonographic sign to be identified is the
presence of multiple B-lines in a diffuse and nonhomogeneous distribution.
• Pleural line abnormalities are often present.
RL-D3-S2 (strong: level B)
• In patients with diffuse parenchymal lung disease
(pulmonary fibrosis), the distribution of B-lines corre- Fig. 2 The four chest areas per side considered for complete eightlates with computed tomography (CT) signs of fibrosis. zone lung ultrasound examination. These areas are used to evaluate
for the presence of interstitial syndrome. Areas 1 and 2 denote the
RL-D3-S3 (strong: level B)
upper anterior and lower anterior chest areas, respectively. Areas 3
and 4 denote the upper lateral and basal lateral chest areas,
• In contrast to cardiogenic pulmonary edema, the respectively.
PSL parasternal line, AAL anterior axillary line, PAL
sonographic findings that are indicative of diffuse posterior axillary line (modified from Volpicelli et al. [19])
584
conventional chest radiography in ruling out signifi- Lung consolidation
cant interstitial syndrome.
Signs and clinical implications
B-D2-S7 (no consensus: level C)
B-D3-S1 (strong: level C) (this statement combines
• Lung ultrasound used as a first-line diagnostic statements P-D3-S4 and P-D3-S5)
approach in the evaluation of suspected interstitial • The sonographic sign of lung consolidation is a
syndrome, when compared with chest radiography,
subpleural echo-poor region or one with tissue-like
may lead to better patient outcomes.
echotexture.
P-D2-S3 (strong: level B)
• In resource-limited settings, lung ultrasound should be
considered as a particularly useful diagnostic modality
in the evaluation of interstitial syndrome.
Outcomes
B-D2-S8 (strong: level C)
• Use of sonography in diagnosis of interstitial syndrome is likely to improve the care of patients in
whom this diagnosis is a consideration.
B-D4-S5 (strong: level B)
• In suspected decompensated left-sided heart failure,
lung ultrasound should be considered because, with
other bedside tests, it provides additional diagnostic
information about this condition.
• Lung consolidations may have a variety of causes
including infection, pulmonary embolism, lung cancer
and metastasis, compression atelectasis, obstructive
atelectasis, and lung contusion. Additional sonographic signs that may help to determine the cause of lung
consolidation include the following:
– The quality of the deep margins of the consolidation
– The presence of comet-tail reverberation artifacts at
the far-field margin
– The presence of air bronchogram(s)
– The presence of fluid bronchogram(s)
– The vascular pattern within the consolidation.
B-D3-S4 (strong: level A)
• Lung ultrasound for detection of lung consolidation
can be used in any clinical setting including point-ofcare examination.
Comments Many studies showed a tight correlation B-D3-S8 (strong: level A)
between interstitial involvement of lung diseases and
B-lines [10, 18–20]. The consensus process defined the • Lung ultrasound should be used in the evaluation of
lung consolidation because it can differentiate conbasic eight-region sonographic technique (Fig. 2) and the
solidations due to pulmonary embolism, pneumonia,
criteria for positive scan and positive examination [19–
or atelectasis.
21]. In the critically ill, a more rapid anterior two-region
scan may be sufficient to rule out interstitial syndrome in P-D3-S6 (strong: level B)
cardiogenic acute pulmonary edema [12]. A positive
examination for sonographic diffuse interstitial syndrome • Lung ultrasound is a clinically useful diagnostic tool
in patients with suspected pulmonary embolism.
allows bedside distinction between a cardiogenic versus a
respiratory cause of acute dyspnea [22–24]. For more P-D3-S7 (strong: level A)
precise quantification of interstitial syndrome, the
28-scanning-site technique can be useful, especially in • Lung ultrasound is an alternative diagnostic tool to
computerized tomography in diagnosis of pulmonary
cardiology and nephrology settings [25]. In acute
embolism when CT is contraindicated or unavailable.
decompensated heart failure, semiquantification of the
severity of congestion can be calculated by counting the P-D3-S3 (strong: level B)
total number of B-lines (28-scanning-site technique) or
the number of positive scans (eight-region technique) [26, • Lung ultrasound is a clinically useful tool to rule in
pneumonia; however, lung ultrasound does not rule
27]. A focal sonographic pattern of interstitial syndrome
out consolidations that do not reach the pleura.
should be differentiated from a diffuse interstitial syndrome [21]. Similar B-patterns are observed in many B-D4-S8 (strong: level C)
acute and chronic conditions with diffuse interstitial
involvement [1, 19, 20, 25, 28, 29]. However, some so- • Lower-frequency ultrasound scanning may allow for
better evaluation of the extent of a consolidation.
nographic signs other than B-lines are useful to
differentiate the B-pattern of cardiogenic pulmonary
edema, ARDS, and pulmonary fibrosis [10]. The sonographic technique for diagnosis of interstitial syndrome is
a basic technique [30–32] with superiority over conven- Imaging strategies and learning curve
tional CXR [33].
B-D3-S5 (strong: level A)
585
• Lung ultrasound should be considered as an accurate good accuracy compared with CXR [43, 45–48]. In
tool in ruling in lung consolidation when compared pleuritic pain, lung ultrasound is superior to CXR and
with chest radiography.
may allow visualization of radio-occult pulmonary conditions [47, 48]. In mechanically ventilated patients,
B-D3-S6 (strong: level B)
lung ultrasound is more accurate than CXR in detecting
• Lung ultrasound may be considered as an accurate and distinguishing various types of consolidations
tool in ruling out lung consolidation in comparison [49, 50].
with chest radiography.
B-D3-S7 (no consensus: level C)
• Use of lung ultrasound as an initial diagnostic strategy
in the evaluation of lung consolidation improves
outcomes in comparison with chest radiography.
B-D3-S3 (strong: level N/A)
• Ultrasound diagnosis of lung consolidation may be
considered as a basic sonographic technique with a
steep learning curve.
B-D4-S6 (strong: level B)
• Lung ultrasound should be considered in the detection
of radio-occult pulmonary conditions in patients with
pleuritic pain.
B-D3-S2 (weak: level C)
• In the evaluation of lung consolidation, the sonographic technique should commence with the
examination of areas of interest (if present, e.g., area
of pain) then progress to the entire lung, as needed.
B-D4-S3 (strong: level A)
• In mechanically ventilated patients, lung ultrasound
should be considered because it is more accurate than
chest radiography in distinguishing various types of
consolidations.
B-D4-S4 (strong: level A)
• In mechanically ventilated patients lung ultrasound
should be considered as it is more accurate than
portable chest radiography in the detection of
consolidation.
B-D4-S9 (no consensus: level N/A)
• Lung ultrasound is accurate in distinguishing various
types of consolidations in comparison with CT scan in
mechanically ventilated patients.
Comments The consolidated region of the lung is
visualized at lung ultrasound as an echo-poor or tissuelike image, depending on the extent of air loss and fluid
predominance, which is clearly different from the normal
pattern [34–38]. The cause of lung consolidation can be
diagnosed by analyzing the sonographic features of the
lesion [39, 40]. Accuracy of lung ultrasound in the diagnosis and differential diagnosis of lung consolidation has
been tested in different settings [36, 41–44] and showed
Monitoring lung diseases
B-D4-S1 (strong: level A)
• In patients with cardiogenic pulmonary edema, semiquantification of disease severity may be obtained by
evaluating the number of B-lines as this is directly
proportional to the severity of congestion.
B-D4-S2 (strong: level A)
• In patients with cardiogenic pulmonary edema,
B-lines should be evaluated because it allows monitoring of response to therapy.
P-D3-S1 (strong: level A)
• In patients with increased extravascular lung water,
assessment of lung reaeration can be assessed by
demonstrating a change (decrease) in the number of
B-lines.
P-D3-S2 (strong: level A)
• In the majority of cases of acute lung injury or ARDS,
ultrasound quantification of lung reaeration may be
assessed by tracking changes in sonographic findings.
• Sonographic findings should include assessment of
lung consolidation and B-lines.
RL-D2-S1 (strong: level A)
• In critically ill patients with acute lung injury or
ARDS, ultrasound changes in lung aeration can be
semiquantitatively assessed (at a given location on the
chest) using the following four sonographic findings,
often in progression:
–
–
–
–
Normal pattern
Multiple spaced B-lines
Coalescent B-lines
Consolidation
RL-D2-S2 (strong: level A)
• Lung ultrasound is able to monitor aeration changes
and the effects of therapy in a number of acute lung
diseases, including the following:
–
–
–
–
–
Acute pulmonary edema
Acute respiratory distress syndrome
Acute lung injury
Community-acquired pneumonia
Ventilator-associated pneumonia
586
– Recovery from lavage of alveolar proteinosis
RL-D3-S5 (strong: level B)
• Serial evaluation of B-lines allows monitoring of
pulmonary congestion in patients on hemodialysis, but
is of undetermined clinical utility.
P-D2-S4 (no consensus: level C)
• The semiquantitative techniques of B-line evaluation
(see B-D2-S2 and B-D2-S4) are useful as a prognostic
indicator of outcomes or mortality in patients with
left-sided heart failure.
RL-D6-S1 (strong: level B)
• Semiquantitative B-line assessment is a prognostic
indicator of adverse outcomes and mortality in
patients with acute decompensated heart failure.
Comments The concept of using lung ultrasound for
monitoring the patient is one of the major innovations that
emerged from recent studies. Pulmonary congestion may
be semiquantified using lung ultrasound [22, 25, 27, 51–
55]. In the clinical arena, lung ultrasound can therefore be
employed as a bedside, easy-to-use, alternative tool for
monitoring pulmonary congestion changes in heart failure
patients, as they disappear or clear upon adequate medical
treatment [27, 56–60]. More generally, any significant
change in lung aeration resulting from any therapy aimed
at reversing aeration loss might be detected by corresponding changes in lung ultrasound patterns [61, 62].
P-D4-S5 (strong: level B)
• The sonographic signs for transient tachypnea of the
newborn are bilateral confluent B-lines in the dependent areas of the lung (‘‘white lung’’) and normal or
near-normal appearance of the lung in the superior
fields.
P-D4-S6 (strong: level B)
• Lung ultrasound is as accurate as chest radiography in
diagnosis of TTN.
P-D4-S7 (strong: level B)
• Lung ultrasound is a clinically useful diagnostic tool
in pediatric patients with suspected pneumonia.
P-D4-S8 (strong: level A)
• The ultrasound signs of lung and pleural diseases
described in adults are also found in pediatric patients.
P-D4-S9 (strong: level A)
• Lung ultrasound is as accurate as chest radiography in
diagnosis of pneumonia in pediatric patients.
Comments In newborns, lung ultrasound signs are
similar to those previously described in adults, although
these signs will be context specific. Lung ultrasound
allows diagnosis of RDS with accuracy similar to CXR
even if there is no correlation between the different
radiographic stages of RDS and ultrasound findings [63].
Lung ultrasound demonstrates very unique findings in the
diagnosis of TTN, whereas CXR is nonspecific [64].
Many studies showed that the ultrasound signs of lung
and pleural diseases described in adults are also found in
Neonatology and pediatrics
pediatric patients [45, 65–68]. In suspected pneumonia,
P-D4-S1 (strong: level B)
lung ultrasound has demonstrated to be no less accurate
• Lung ultrasound is a clinically useful diagnostic tool than CXR. These data suggest that, when there is clinical
in neonates with suspected respiratory distress syn- suspicion of pneumonia, a positive lung ultrasound
drome (RDS).
excludes the need to perform CXR.
P-D4-S2 (strong: level B)
• All the following sonographic signs are likely to be Pleural effusion
present in neonates with respiratory distress syndrome:
RL-D4-S3 (strong: level A)
– Pleural line abnormalities
• Both of the following signs are present in almost all
– Absence of spared areas
free effusions:
– Bilateral confluent B-lines
– A space (usually anechoic) between the parietal and
P-D4-S3 (strong: level B)
visceral pleura
– Respiratory movement of the lung within the
• Lung ultrasound is as accurate as chest radiography in
effusion (‘‘sinusoid sign’’)
the diagnosis of respiratory distress syndrome in
neonates.
RL-D4-S5 (strong: level A)
P-D4-S4 (strong: level B)
• A pleural effusion with internal echoes suggests that it
is an exudate or hemorrhage. While most transudates
• Lung ultrasound is a clinically useful diagnostic tool
are anechoic, some exudates are also anechoic. Thoin suspected transient tachypnea of the newborn
racentesis may be needed for further characterization.
(TTN).
587
RL-D4-S1 (strong: level B)
Conclusions
• In the evaluation of pleural effusion in adults, the
microconvex transducer is preferable. If not available, a This is the first document reporting evidence-based recommendations on clinical use of point-of-care lung
phased array or a convex transducer can be used.
ultrasound. Experts who published the vast majority of
RL-D4-S2 (strong: level B)
papers on clinical use of lung ultrasound in the last
• The optimal site to detect a nonloculated pleural 20 years elaborated these specific 73 recommendations. A
effusion is at the posterior axillary line above the number of these recommendations will potentially
reshape the future practice and knowledge of this rapidly
diaphragm.
expanding field. These applications will benefit patients
RL-D4-S4 (strong: level A)
worldwide as rigorous assessment, classification, and
• For the detection of effusion, lung ultrasound is more publication efforts continue to make this critical inforaccurate than supine radiography and is as accurate as mation available to all clinicians. The advantages of
correct use of bedside lung ultrasound in the emergency
CT.
setting are striking, particularly in terms of saving from
B-D4-S7 (strong: level A)
radiation exposure, delaying or even avoiding transpor• In opacities identified by chest radiography, lung tation to the radiology suite, and guiding life-saving
ultrasound should be used because it is more accurate therapies in extreme emergency. This document was
than chest radiography in distinguishing between elaborated to guide implementation, development, and
training on use of lung ultrasound in all relevant settings;
effusion and consolidation.
it will also serve as the basis for further research and to
Comments Pleural effusion is usually visualized as an influence and enhance the associated standards of care.
anechoic space between the parietal and visceral pleura.
This condition can be obvious in patients with substantial
effusion. In other conditions, such as complex effusion
and in patients where pleural effusion is suspected, the Appendix
sonographic technique can benefit from standardized Organizing society
criteria to improve diagnostic accuracy. The sinusoid sign
is a dynamic sign showing the variation of the interpleural World Interactive Network Focused on Critical Ultradistance during the respiratory cycles [69, 70]. This var- sound (WINFOCUS)
iation is easily visualized on M-mode as a sinusoid
movement of the visceral pleura [70].
Lung ultrasound has the potential also for diagnosing Consensus conference participants and affiliations
the nature of the effusion [71]. Visualization of internal Working subgroup leaders
echoes, either of mobile particles or septa, is highly
suggestive of exudate or hemothorax [72–76]. However, Writing committee: G Volpicelli (Emergency Medicine,
when faced with an anechoic effusion, the only way to San Luigi Gonzaga University Hospital, Torino, Italy)
differentiate between transudate and exudate is to use
Document reviewers: M Blaivas (Department of
thoracentesis or alternatively to evaluate effusion in the Emergency Medicine, Northside Hospital Forsyth, Atlanta,
clinical context [71, 77–79].
GA, USA)
Lung ultrasound accuracy is proved to be higher than
Methodology committee: M Elbarbary (National & Gulf
CXR, particularly when anterior–posterior view in the Center for Evidence Based Health Practice, King Saud
supine patient is considered [49, 69, 70]. Lung ultrasound University for Health Sciences, Riyadh, Saudi Arabia)
performance is nearly as good as CT scan [49, 80].
Organizing committee: L Neri (AREU EMS Public
Update plan
Regional Company, Niguarda Ca’ Granda Hospital, Milano, Italy)
New research and knowledge will give impetus to update
these guidelines by renewing the development process at Working committees
least every 4 years or whenever a significant major change
in evidence appears. A professional librarian will review Writing committee:
literature on a regular basis and send any updates to the
corresponding author. The panel is open to new inputs, and • DA Lichtenstein (Service de Réanimation Médicale,
Hôpital Ambroise-Paré, Boulogne, Paris-Ouest,
the position of new researchers and experts will be conFrance)
sidered in the future before the next revision.
588
• G Mathis (Internal Medicine Praxis, Rankweil, Austria)
• A Kirkpatrick (Foothills Medical Centre, Calgary, AB,
Canada)
• L Gargani (Institute of Clinical Physiology, National
Research Council, Pisa, Italy)
• VE Noble (Division of Emergency Ultrasound, Department of Emergency Medicine, Massachusetts General
Hospital, Boston, MA, USA)
• R Copetti (Medical Department, Latisana Hospital,
Udine, Italy)
• G Soldati (Emergency Medicine Unit, Valle del
Serchio General Hospital, Lucca, Italy)
• B Bouhemad (Surgical Intensive Care Unit, Department of Anesthesia and Critical Care, Groupe
Hospitalier Paris Saint-Joseph, Paris, France)
• A Reissig (Department of Pneumology and Allergology, Medical University Clinic I, Friedrich-Schiller
University, Jena, Germany)
• JJ Rouby (Multidisciplinary Intensive Care Unit,
Department of Anesthesiology, Pitié-Salpêtrière Hospital, University Pierre and Marie Curie, Paris, France)
Document reviewers:
• G Via (IRCCS Foundation Policlinico San Matteo,
Pavia, Italy)
• E Agricola (Division of Noninvasive Cardiology, San
Raffaele Scientific Institute, IRCCS, Milan, Italy)
• JW Tsung (Mount Sinai School of Medicine, Departments of Emergency Medicine and Pediatrics, New
York, NY, USA)
• A Dean (Division of Emergency Ultrasonography,
Department of Emergency Medicine, University of
Pennsylvania Medical Center, Philadelphia, PA, USA)
• R Breitkreutz [Department of Anaesthesiology, Intensive Care and Pain therapy, University Hospital of the
Saarland and Frankfurt Institute of Emergency Medicine and Simulation Training (FINEST), Germany]
• A Seibel (Diakonie Klinikum jung-stilling, Siegen,
Germany)
Organizing committee:
• E Storti (Intensive Care Unit ‘‘G. Bozza,’’ Niguarda
Ca’ Granda Hospital, Milan, Italy)
• T Petrovic (Samu 93, University Hospital Avicenne,
Bobigny, France)
Other consensus conference members:
• C Arbelot (Multidisciplinary Intensive Care Unit,
Department of Anesthesiology, Pitié-Salpêtrière Hospital, University Pierre and Marie Curie, Paris, France)
• A Liteplo (Emergency Medicine, Massachusetts General Hospital, Boston, MA, USA)
• A Sargsyan (Wyle/NASA Lyndon B. Johnson Space
Center Bioastronautics Contract, Houston, TX, USA)
• F Silva (UC Davis Medical Center, Emergency Medicine, Sacramento, CA, USA)
• R Hoppmann (Internal Medicine, University of South
Carolina School of Medicine)
Acknowledgments Special thanks to the Cornell library staff for
conducting the literature search, to Ms. Maddalena Bracchetti for
her outstanding organizational and administrative support, and to
• L Melniker (Department of Emergency Medicine, New all the secretariat staff. This study was endorsed by the World
York Methodist Hospital and Clinical Epidemiology Interactive Network Focused on Critical Ultrasound (WINFOCUS).
Methodology committee:
Unit, Division of General Internal Medicine, Department of Medicine, Weill Medical College of Cornell Conflicts of interest The authors declare that they have no
competing interests.
University, NY, USA)
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