|
Indian Pediatr 2016;53: 1007-1011 |
 |
Comparison of Lung Ultrasonography and Chest
Radiography for Diagnosis of Childhood Pneumonia
|
Source Citation: Ambroggio L, Sucharew
H, Rattan MS, O’Hara SM, Babcock DS, Clohessy C, et al. Lung
ultrasonography: A viable alternative to chest radiography in children
with suspected pneumonia? J Pediatr. 2016;176:93-8.
Section Editor: Abhijeet Saha
|
Summary
This was a prospective cohort study to determine the
interrater reliability (IRR) of lung ultrasonography (LUS) and chest
radiography (CXR), and evaluate the accuracy of LUS compared with CXR
for detecting pediatric pneumonia compared with chest computed
tomography (CT) scan. Children aged 3 months to 18 years with a CXR and
LUS performed with or without a clinical diagnosis of pneumonia were
included in the study. Four pediatric radiologists blinded to clinical
information reported findings for the CXR and LUS images, and two
radiologists reviewed CT scans to determine an overall finding. IRR was
estimated for 50 LUS and CXR images. The main outcome was the finding
from CT ordered clinically or the probability of the CT finding for
patients clinically requiring CT. Latent class analysis was used to
evaluate the sensitivity and specificity for findings (eg,
consolidation) for LUS and CXR compared with CT.
Of the 132 patients in the cohort, 36 (27%) had CT
performed for a clinical reason. Pneumonia was clinically documented in
47 patients (36%). The IRR (95% CI) for lung consolidation was 0.55
(0.40, 0.70) for LUS and 0.36 (0.21, 0.51) for CXR. The sensitivity for
detecting consolidation, interstitial disease, and pleural effusion was
statistically similar for LUS and CXR compared with CT; however,
specificity was higher for CXR. The negative predictive value was
similar for CXR and LUS. The authors concluded that LUS has a
sufficiently high IRR for detection of consolidation; and compared with
CT, LUS and CXR have similar sensitivity, but CXR is more specific for
findings indicating pneumonia.
Commentaries
Evidence-based Medicine Viewpoint
Relevance: Chest radiographs are commonly done
for managing children with suspected lower respiratory tract conditions
including pneumonia, although their value in uncomplicated cases is
debatable. Diagnosis of pneumonia in developed countries relies heavily
on radiologic ‘confirmation’, whereas the WHO recommends (for developing
countries) clinical criteria alone. The crux of the problem is that
neither clinical criteria nor radiographic findings can be considered
foolproof for diagnosing pneumonia. Even attempts to introduce
objectivity to clinical as well as radiologic criteria have not improved
the situation. For example, the recent Community Acquired Pneumonia
Etiology Study (CAPES) [1] from India showed that only 44% children with
WHO/IMNCI-defined pneumonia had WHO Class I X-rays (i.e
consolidation and/or pleural effusion). Similarly other smaller studies
identified radiological features of pneumonia in less than 40% children
with clinical pneumonia [2]. In yet another study, almost half the
children with clinical pneumonia [3] had normal chest X-ray
(CXR); although two-thirds of those with normal CXR had crackles or
rales on auscultation. Even a recent Cochrane review [4] reported that
CXR do not affect the clinical outcome in children with clinical
pneumonia (although this conclusion was based on limited data). The
other major limitation with chest radiography is significant
inter-observer variation in interpreting images [5,6].
Lung ultrasonography (LUS) is emerging as a potential
alternative to CXR, being radiation-free, relatively affordable and
feasible at the point-of-care. The critical issue is whether it is
efficacious. Several studies [7-10] compared LUS against CXR, and
emerging data suggests a slight superiority of LUS over CXR [11]. LUS is
also reportedly superior to chest auscultation for identifying pneumonia
[12]. However, an important limitation in such studies is the absence of
appropriate reference standard(s) for labeling pneumonia. CXR findings
are not the ideal reference standard because they suggest (but not
necessarily confirm) pneumonia, but pneumonia can exist with normal CXR.
The same limitation holds for clinical diagnosis, and also clinical plus
radiographic diagnosis. Obviously, the WHO/IMNCI definition of pneumonia
cannot be used as the reference standard for pneumonia as it has
moderate sensitivity and poor specificity [13].
Some studies evaluating LUS vs CXR have the
limitation that the reference standard for pneumonia diagnosis includes
CXR findings as one of the criteria [14-16]. Even a recent meta-analysis
[17] of eight studies, reporting excellent sensitivity and specificity
of LUS, showed that the reference standards included clinical diagnosis
plus CXR in five studies and CXR alone in the other three. While such
data can give an overall impression of the utility of LUS, they are
inappropriate for comparing LUS against CXR.
Against this backdrop, the recent study by Ambroggio,
et al. [18] is different from previous studies in that LUS and
CXR have not been directly compared against each other, but against
another reference standard (viz CT scan). Briefly, the
investigators included children with various respiratory illnesses, and
performed CXR as well as LUS in them. A few of the children required CT
for clinical reasons and this could be used as the reference test. In
the others, a statistical method called latent class modeling was used
to estimate the likelihood of CT findings and this was used as the
reference standard. The twin objectives were to (i) calculate
inter-observer concordance of LUS and CXR reports; and (ii)
compare LUS versus CXR for diagnosis of pneumonia.
It should be recognized that this is not the first
such study. A recent report from Iran [19] compared LUS and CXR against
CT in children with suspected pneumonia; both showed good correlation
with CT, although LUS was slightly superior for complicated cases,
whereas CXR was superior in uncomplicated cases. Overall concordance was
best when combination of LUS and CXR findings was compared against CT.
Another study from Taiwan [20] showed that LUS finding of impaired lung
perfusion correlated well with the severity of lung necrosis on CT; and
the degree of impairment could reliably predict the extent of necrosis.
Critical appraisal: Table I
presents the methodological characteristics of the study. The study [18]
had several methodological refinements. LUS and CXR images were stripped
of identification details and observers were blinded to clinical
details. Efforts were made to prevent observers from linking LUS
findings with CXR findings of individual patients by assigning codes.
Both index tests were performed within 36 hours of each other, which is
reasonable although not ideal. Detailed description of LUS procedure has
been provided, as well as clear definitions for the terms used to
describe findings. Similarly CXR was done obtaining both
antero-posterior as well as lateral films and interpreted using
objective criteria. Both LUS and CXR interpretation were done taking
care to report findings in multiple lung/pleural regions. At least two
radiologists reported each LUS and CXR image; and 50 images selected
randomly were reviewed by four radiologists. All the radiologists
involved in this study were highly trained experts, enhancing
reliability of the observations.
Table I Critical Appraisal of the Study
Parameter
|
Comments |
Validity |
Are the results of the study valid?
|
The investigators applied two index tests (CXR and LUS) in 132
children (3 mo to 18 y) hospitalized with various respiratory
illnesses including (but not confined to) pneumonia, and
compared the results against CT scan findings (reference
standard). The presence of consolidation and/or pleural effusion
on CT was labeled as pneumonia. However, actual scans were
available in only 36 (27%) children, and latent class modeling
was used to estimate the CT results in the rest. Infants younger
than 3 mo were excluded. It is unclear whether eligible
participants were enrolled consecutively or an element of
selection bias existed.
|
Was the reference standard appliedregardless of the index test
result? |
This study has the distinction that the index test(s) did not
form part of the reference standard. Although 73% children did
not have the actual reference test (CT scan), the methodology
applied to impute the reference test result (latent class
modeling) is valid and acceptable. The results in the total
cohort (n=132) and those with the actual CT scans (n=36) are not
very different. The primary objective of inter-observer
concordance was appropriately measured by each index test (LUS
and CXR) being read by 4 observers independently in a sub-cohort
of 50 patients selected through an unspecified randomization
process. |
Was there an independent, blind comparison between the index
test and an appropriate reference (‘gold’) standard of
diagnosis? |
The reference standard (CT) was read by two independent experts
and showed total concordance. The index tests (LUS and CXR) were
interpreted by two of four expert pediatric radiologists,
although it is unclear whether these were the same (or
different) ones who interpreted the CT scan images. The study
specifies that the radiologists were blinded to clinical data,
but it is not explicitly mentioned whether they were blinded to
the results of the reference standard.
|
Results |
Test characteristics and measures |
LUS vs actual CT (n=36) |
|
•Consolidation: Sn 0.63, Sp 0.75, LR+ 2.52, LR– 0.49 |
|
•Pleural effusion: Sn 0.80, Sp 0.78, LR+ 3.64, LR– 0.26 |
|
•Interstitial disease: Sn NA, Sp 0.57, LR+ NA, LR– NA |
|
CXR vs actual CT (n=36) |
|
•Consolidation: Sn 0.58, Sp 0.85, LR+ 3.87, LR– 0.49 |
|
•Pleural effusion: Sn 0.60, Sp 0.92, LR+ 7.5, LR– 0.43 |
|
•Interstitial disease: Sn NA, Sp 0.85, LR+ NA, LR– NA |
|
LUS vs reference standard and CXR vs reference standard
(n=132) |
|
•Numeric data not provided for sensitivity and specificity;
these are shown only in a figure. Hence LR cannot be calculated
p
|
|
•Positive and negative predictive values are presented in a
Table in the study.
|
Applicability |
Do the methods described permit replication?
|
The methods described for performing, as well as interpreting
LUS and CXR are replicable. The details of CT scan (for example
with or without contrast, high resolution or otherwise, etc.)
are not mentioned. |
CT: Computed tomography; CXR: Chest X-ray; LR+: Positive
likelihood ratio; LR–: Negative likelihood ratio; LUS: Lung
ultrasound; Sn: Sensitivity; Sp: Specificity |
The major limitation in this study [18] is the
absence of a radiographic definition for the diagnosis of pneumonia,
both for LUS as well as CXR; although to be fair, pneumonia is not a
‘radiological diagnosis.’ In this study, four individual radiographic
findings have been evaluated on LUS and CXR (viz consolidation,
interstitial disease, effusion and other), without clearly defining a
priori which of these (singly or in combination) is to be considered
diagnostic of pneumonia. Although the authors correctly emphasized that
consolidation and pleural effusion are most suggestive of pneumonia,
this does not automatically mean that consolidation and pneumonia are
synonymous. In the paper [18], the objective in the abstract section
stated that LUS was compared with CXR for diagnosing ‘pneumonia’,
whereas the Objective in the text stated comparison to detect ‘disease’.
This subtle ambivalence is reflected in title of the paper also,
wondering whether LUS could be an alternative to CXR in diagnosing
pneumonia (which is the issue of interest); rather than stating a mere
comparison between LUS and CXR for specific radiologic findings (which
is what the investigators did).
Another important limitation is that the term
‘interstitial disease’ has not been defined at all; therefore it could
refer to interstitial pattern of radiographic findings (often seen in
viral lower respiratory tract infections), or true interstitial disease
of childhood (which can be of infective or non-infective origin).
Assuming that the authors intended the former, it is pertinent that this
pattern is seen in 30% xrays among children with clinically defined
pneumonia [1]. Further the sonographic definition of interstitial
disease in this study [18] is one of the criteria for diagnosing
pneumonia in some other studies. In fact, a Canadian study reported that
the pattern defined as ‘interstitial disease’ in this study [18] was the
predominant LUS finding among infants with lower respiratory infection
and wheezing. This suggests that the interstitial pattern on LUS or CXR
should also contribute to the definition of radiologic pneumonia. This
has been completely omitted in this study [18]. This is especially
pertinent because the results showed that CXR had higher sensitivity and
specificity than LUS for interstitial disease; and also better
inter-observer concordance. It is possible that if radiographic
pneumonia had been defined including the criteria for interstitial
disease, the superiority of LUS highlighted by the authors would be
negated.
Yet another limitation is that, not all the 132 LUS
and CXR images were examined for inter-observer concordance. The
reason(s) for this are not elaborated. It would have also been
interesting to examine the LUS and CXR data of the 36 children with
clinical pneumonia, to study whether either modality correlated with the
clinical diagnosis.
The authors emphasized the superiority of LUS over
CXR for detecting consolidation and pleural effusion, as well as better
inter-observer concordance for these findings. However, careful analysis
of the data shows overlapping confidence intervals (CI) for almost all
parameters (specific findings as well as inter-observer concordance),
suggesting comparability of the two modalities. In fact the only clear
differences (i.e. non-overlapping CI) were superior
inter-observer concordance of CXR for interstitial findings, and also
greater specificity of CXR for pleural effusion as well as interstitial
disease, and higher sensitivity (but lower specificity) of CXR for other
findings. These data suggest a slight edge of CXR over LUS.
Extendibility: The CXR protocol in this
study [18] included interpretation of both antero-posterior and lateral
films; this is rarely done in our setting, making it difficult to
extrapolate the findings directly. Last but not the least, the observers
in this study were trained pediatric radiologists, whereas in real life,
most CXR in emergency rooms are read by clinicians managing patients.
Previous studies have documented that inter-observer variation is
minimized with high level of training and expertise [21,22]. In our
setting, the relative ease and low cost of chest radiography (in urban
settings), and interpretation at the point-of-care by professionals not
trained to interpret radiologic images, creates the dual problems of
overuse and potential for incorrect interpretation. Lung ultrasonography
has not become popular in our setting as yet; however the same problems
are anticipated with this modality also.
Conclusion: This study showed that LUS is
comparable to CXR for detection of certain findings suggestive of
pneumonia in children (viz consolidation and pleural effusion),
but is inferior for detecting interstitial patterns. The overall utility
for diagnosis of pneumonia and potential for replacing CXR as the
primary imaging modality cannot be gauged from the data presented in
this study.
Funding: None; Competing interest: None
stated.
Joseph L Mathew
Department of Pediatrics, PGIMER, Chandigarh, India.
Email: [email protected]
References
1. Mathew JL, Singhi S, Ray P, Hagel E,
Saghafian-Hedengren S, Bansal A, et al. Etiology of community
acquired pneumonia among children in India: prospective, cohort
study. J Glob Health. 2015;5:050418.
2. Simbalista R, Andrade DC, Borges IC, Araújo M,
Nascimento-Carvalho CM. Differences upon admission and in hospital
course of children hospitalized with community-acquired pneumonia
with or without radiologically-confirmed pneumonia: a retrospective
cohort study. BMC Pediatr. 2015;15:166.
3. Nahir B, Zimmerman DR, Applebaum Y, Kovalski
N. New guidelines to decreasex-ray use may increase unnecessary
antibiotic use. Harefuah. 2013; 152:713-5.
4. Cao AM, Choy JP, Mohanakrishnan LN, Bain RF,
van Driel ML. Chest radiographs for acute lower respiratory tract
infections. Cochrane Database Syst Rev. 2013;12:CD009119.
5. Williams GJ, Macaskill P, Kerr M, Fitzgerald
DA, Isaacs D, Codarini M, et al. Variability and accuracy in
interpretation of consolidation on chest radiography for diagnosing
pneumonia in children under 5 years of age. Pediatr Pulmonol.
2013;48:1195-200.
6. Bada C, Carreazo NY, Chalco JP, Huicho L.
Inter-observer agreement in interpreting chest X-rays on children
with acute lower respiratory tract infections and concurrent
wheezing. Sao Paulo Med J. 2007;125:150-4.
7. Urbankowska E, Krenke K, Drobczyński Ł,
Korczyński P, Urbankowski T, Krawiec M, et al. Lung
ultrasound in the diagnosis and monitoring of community acquired
pneumonia in children. Respir Med. 2015;109:1207-12.
8. Ho MC, Ker CR, Hsu JH, Wu JR, Dai ZK, Chen IC.
Usefulness of lung ultrasound in the diagnosis of community-acquired
pneumonia in children. Pediatr Neonatol. 2015;56:40-5.
9. Esposito S, Papa SS, Borzani I, Pinzani R,
Giannitto C, Consonni D, et al. Performance of lung
ultrasonography in children with community-acquired pneumonia. Ital
J Pediatr. 2014;40:37.
10. Shah VP, Tunik MG, Tsung JW. Prospective
evaluation of point-of-care ultrasonography for the diagnosis of
pneumonia in children and young adults. JAMA Pediatr.
2013;167:119-25.
11. Guerra M, Crichiutti G, Pecile P, Romanello
C, Busolini E, Valent F, et al. Ultrasound detection of
pneumonia in febrile children with respiratory distress: a
prospective study. Eur J Pediatr. 2016;175:163-70.
12. Lovrenski J, Petrović S, Balj-Barbir S, Jokić
R, Vilotijević-Dautović G. Stethoscope vs. ultrasound probe - which
is more reliable in children with suspected pneumonia? Acta Med
Acad. 2016;45:39-50.
13. Chavez MA, Naithani N, Gilman RH, Tielsch JM,
Khatry S, Ellington LE, et al. Agreement between the world
health organization algorithm and lung consolidation identified
using point-of-care ultrasound for the diagnosis of childhood
pneumonia by general practitioners. Lung. 2015;193:531-8.
14. Iorio G, Capasso M, De Luca G, Prisco S,
Mancusi C, Laganŕ B, et al. Lung ultrasound in the diagnosis
of pneumonia in children: proposal for a new diagnostic algorithm.
Peer J. 2015;3:e1374.
15. Reali F, Sferrazza Papa GF, Carlucci P,
Fracasso P, Di Marco F, et al. Can lung ultrasound replace
chest radiography for the diagnosis of pneumonia in hospitalized
children? Respiration. 2014;88:112-5.
16. Caiulo VA, Gargani L, Caiulo S, Fisicaro A,
Moramarco F, Latini G, et al. Lung ultrasound characteristics
of community-acquired pneumonia in hospitalized children. Pediatr
Pulmonol. 2013;48:280-7.
17. Pereda MA, Chavez MA, Hooper-Miele CC, Gilman
RH, Steinhoff MC, Ellington LE, et al. Lung ultrasound for
the diagnosis of pneumonia in children: a meta-analysis. Pediatrics.
2015;135:714-22.
18. Ambroggio L, Sucharew H, Rattan MS, O’Hara
SM, Babcock DS, Clohessy C, et al. Lung ultrasonography: A
viable alternative to chest radiography in children with suspected
pneumonia? J Pediatr. 2016; 176:93-98.
19. Hajalioghli P, Nemati M, Dinparast Saleh L,
Fouladi DF. Can chest computed tomography be replaced by lung
ultrasonography with or without plain chest radiography in pediatric
pneumonia? J Thorac Imaging. 2016;31:247-52.
20. Lai SH, Wong KS, Liao SL. Value of lung ultrasonography in the diagnosis and outcome prediction of pediatric
community-acquired pneumonia with necrotizing change. PLoS One.
2015;10:e0130082.
21. Xavier-Souza G, Vilas-Boas AL, Fontoura MS,
Araújo-Neto CA, Andrade SC, Cardoso MR, et al. The
inter-observer variation of chest radiograph reading in acute lower
respiratory tract infection among children. Pediatr Pulmonol.
2013;48:464-9.
22. Johnson J, Kline JA. Intraobserver and
interobserver agreement of the interpretation of pediatric chest
radiographs. Emerg Radiol. 2010;17:285-90.
Pediatric Emergency Medicine Physician’s Viewpoint
The most useful finding of this article is the
moderate inter-rater reliability (IRR) of lung ultrasound (LUS) for
pneumonia and relatively poor IRR for chest X-ray (CXR). The
calculated operating characteristics of LUS compared with CXR, using
computed tomography as the gold standard, is less dependable and less
useful due to the low rate of gold standard testing and the fact that
other studies report much higher sensitivities and specificities [1].
When comparing patient-centered outcomes, a randomized controlled trial
by Tsung, et al. [2] demonstrated that when LUS is used in the
pediatric emergency department to evaluate for pneumonia, there is
decreased CXR utilization and likely decreased length of stay.
They report a 30% decrease in CXR use by novice
sonographers, and a 60% decrease by experienced sonographers, without
misdiagnoses or adverse events.
Pediatric emergency medicine physicians are often in
the challenging position of evaluating the child with clinical features
concerning for pneumonia. The differential diagnoses in these cases are
extensive – from a viral triggered asthma exacerbation to influenza or
bacterial pneumonia with effusion. The IRR findings in this study
support the growing body of evidence that point-of-care LUS may supplant
CXR in cases of "rule out pneumonia" [3,4].
By wheeling the ultrasound machine to the bedside, the
clinician can rapidly document the presence or absence of a pleural
effusion and/or consolidation, without exposure to radiation. Bedside
LUS decreases length of stay, cost and radiation for our patients and is
indispensable to the busy clinician in search of immediate answers.
Funding: None; Competing interest: None
stated.
Sathyaseelan Subramaniam and *Jennifer
H Chao
SUNY Downstate Medical Center, Kings County Hospital
Center,
Brooklyn, New York, US.
Email:
[email protected]
References
1. Pereda MA, Chavez MA, Hooper-Miele CC, Gilman RH,
Steinhoff MC, Ellington LE, et al. Lung ultrasound for the
diagnosis of pneumonia in children: a meta-analysis. Pediatrics
2015;135:714-22.
2. Jones BP, Tay ET, Elikashvili I, Sanders JE, Paul
AZ, Nelson BP, et al. Feasibility and safety of substituting lung
ultrasonography for chest radiography when diagnosing pneumonia in
children: a randomized controlled trial. Chest. 2016;150:131-8.
3. Shah VP, Tunik MG, Tsung JW. Prospective
evaluation of point-of-care ultrasonography for the diagnosis of
pneumonia in children and young adults. JAMA Pediatr. 2013;167:119-25.
4. Samson F, Gorostiza I, Gonzalez A, Landa M, Ruiz L, Grau M, et
al. Prospective evaluation of clinical lung ultrasonography in the
diagnosis of community-acquired pneumonia in a pediatric emergency
department. Eur J Emerg Med. 2016 Aug 17. [Epub ahead of print].
|
|
 |
|