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03 Lung Ultrasound Review Shows Prognostic and Diagnostic Bronchiolitis 2023
03 Lung Ultrasound Review Shows Prognostic and Diagnostic Bronchiolitis 2023
03 Lung Ultrasound Review Shows Prognostic and Diagnostic Bronchiolitis 2023
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Received: 2 June 2022 | Revised: 14 October 2022 | Accepted: 18 October 2022
DOI: 10.1111/apa.16578
REVIEW ARTICLE
1
Faculty of Medicine, National and
Kapodistrian University of Athens, Athens, Abstract
Greece
Aim: Lung ultrasound (LUS) has not been included in the current guidelines for the
2
2nd Department of Radiology, National
and Kapodistrian University of Athens,
diagnosis of bronchiolitis so far, even though data concerning its effectiveness have
Faculty of Medicine, University General been published.
Hospital ‘Attikon’, Athens, Greece
3
Methods: A systematic literature review was carried out to determine the role of
3rd Department of Paediatrics, National
and Kapodistrian University of Athens, LUS scores in the diagnosis and prognosis of patients aged 0–2 years with bronchi-
Faculty of Medicine, University General olitis, using MEDLINE, Scopus and ScienceDirect databases from their inception to
Hospital ‘Attikon’, Athens, Greece
December 2021.
Correspondence Results: A total of 18 studies matching our eligibility criteria were analysed for the
Christos Kogias, National and Kapodistrian
University of Athens, Faculty of Medicine, purposes of this review and 1249 patients with bronchiolitis were included. The sono-
University General Hospital ‘Attikon’, graphic and radiological findings were comparable and chest radiography was found
Rimini 1, Chaidari 12462, Athens, Greece.
Email: christoskogias.ped@gmail.com to have a higher sensitivity in ruling out severe complications such as concomitant
pneumonia. The LUS scores were correlated to the clinical course of bronchiolitis and
it was able to predict the need of admission in paediatric intensive care unit, the dura-
tion of hospitalisation and the need for respiratory support.
Conclusion: This review suggests that LUS could have both a diagnostic and a prog-
nostic role in bronchiolitis during first evaluation in the emergency department and
hospitalisation. Physicians could adjust management according to sonographic find-
ings as a useful adjunct to the clinical ones.
KEYWORDS
bronchiolitis, diagnosis, infants, lung ultrasound, prognosis
Abbreviations: CPAP, continuous positive airway pressure; HFNC, high flow nasal cannula; LUS, lung ultrasound; OR, odds ratio; PED, paediatric emergency department; PICU,
paediatric intensive care unit.
© 2022 Foundation Acta Paediatrica. Published by John Wiley & Sons Ltd
222 |
wileyonlinelibrary.com/journal/apa Acta Paediatrica. 2023;112:222–232.
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KOGIAS et al. 223
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224 KOGIAS et al.
excluded as reviews, 21-25 2 due to lack of sonographic data, 26,27 and and by both paediatricians and radiologists/sonographers in six
1 as non-relevant to the topic because it presents diaphragm ultra- studies.32,33,39,41,44,45 One study did not state the interpretation
28 29-4 6
sound data. Finally, 18 of them were eligible for use in this method. 29 We sorted these studies into groups according to the ob-
systematic review. For detailed characteristics of each study see jective for further stratification of the results in our review.
Table 1.
The quality assessment showed that none of the studies met
level I evidence criteria, 2 met level II, 5 met level III and the remain- 3.1 | LUS and chest radiography
ing 11 level IV criteria. Thus, the majority of studies had a low quality findings comparison
of evidence. Of these studies, fifteen were prospective observa-
tional studies,30,31,32,33,34,35,36,37,38,40,41,42,43,45,46 one was retrospec- Seven studies examined the accuracy of the two diagnostic methods
tive observational study40 and two were cross-sectional studies. 29,44 (Table 3). 29,31,35,39,40,43,46 Five of them showed that LUS was more
37
Except for one multi-centre study, all others were single-centre accurate than chest radiography in identifying lung consolidations as
studies. One study was published in French,41 one in Spanish,38 and a marker of bronchiolitis. 29,31,35,40,46 LUS was found to be more sen-
the remainder were published in English. sitive than chest radiography. Two prospective observational stud-
Lung ultrasound was performed using either a high-frequency lin- ies showed that LUS could recognise more accurately a pathological
ear probe when examining superficial structures or a low-frequency pattern in patients with bronchiolitis indicating that it was more val-
micro-convex probe when assessing deeper structures. Different uable as a diagnostic tool compared to chest radiography.35,46 One 46
LUS scoring systems were used among the studies included in this found that nine patients whose clinical scores was consistent with
review, which can be found in Table 2 in detail. While the number the diagnosis of bronchiolitis had negative chest radiography, though
of scoring systems used in the studies was high (n = 6) each scoring a positive LUS. The other study included 76 infants with bronchioli-
system in its essence was scrutinising the B-line pattern, its occur- tis, seventy-four (97%) had a positive LUS and forty-t wo (55.3%) had
rence and density per intercostal space and the presence of sub- positive chest radiography.35 A strong correlation between chest
pleural consolidations. LUS findings interpretation was performed radiography and LUS (rs = 0.638) and good accuracy of LUS in diag-
only by non-radiologists/sonographers in six studies, 30,36,37,38,40,42 nosing bacterial pneumonia in children with clinical bronchiolitis was
only by radiologists/sonographers in five studies31,34,35,43,46 shown. When only consolidation size >1 cm was considered positive
Identification
(n = 4)
(n = 18)
F I G U R E 1 Preferred reporting items
for systematic reviews flow diagram of
selection process
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KOGIAS et al. 225
Gender
Level of
References Country Study design N Age Males Females evidence
for pneumonia, the correlation in the study grew further (rs = 0.684) (87.5%) of infants needing non-invasive ventilation in PICU upon
and specificity of LUS was higher than CXR (98.4% vs. 87.1%) with arrival and at 48 h had an abnormal LUS pattern. 32 Interstitial pat-
39
+LR = 5, comparable to the CXR's. These data suggested that a tern along with consolidation tended to be the main predictor of
positive lung ultrasound with consolidations >1 cm may avoid the worse outcome.
need to perform chest radiography in these patients.
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KOGIAS et al. 227
Depth ≥ 10 mm
findings and the need for hospital stay. A Spanish prospective study
that enrolled 59 patients estimated that the median LUS score in the
patients who did not require hospital admission was six points (2–8),
in those who admitted to the ward was nine points (5–13.7), and
in the patients who needed to be transferred from the ward to the
C
consolidation
consolidation
pattern with
Abbreviations: AIS, alveolar-interstitial syndrome; ICS, intercostal space; LUS, lung ultrasound.
found that the need for supplemental oxygen was more frequent in
(b) Moderate interstitial
(a) Moderate interstitial
± small subpleural
intercostal spaces
the patients with higher LUS scores31,33,34,37 and that LUS can identify
Moderate interstitial
and/or confluent
pattern without
(depth < 10 mm)
consolidation
consolidation
consolidation
limited number
of focal B-lines
sliding without
as normal lung
Normal or almost
gen therapy was more frequent in patients with higher LUS score.31
Author
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228 KOGIAS et al.
Studies N Age LUS CXR LUS CXR LUS CXR LUS CXR
29 c c c c c
Elkhazragy et al. 36 9/36 (25%) 3/36 (8%) 91.7% 77.8% 95.9% 89.7% 22.4 7.55c
Regina et al.31 63 2.7 monthsa 54/63 (85%) 14/23 (61%)
35 a
Özkaya et al. 76 7.4 months 75/76 (99%) 5/76 (6.5%) 50%d 91.2%d 5.68d
6 monthsb
Biagi et al.39 87 5.7 monthsb 100%e 96%e 83.9%e 87.1%e 6.21 e 7.44 e
80%f 98.4%f 5f
Jaszczolt et al.40 26 7.3 monthsa 19/26 (73%) 4/26 (15%)
7 monthsb
Kader et al.43 25 6.94 monthsa 3/25 (12%) 4/25 (16%)
46 b
Caiulo et al. 52 2.1 months 44/63 (70%) 16/63 (25%)
Abbreviations: CXR, chest X-ray; +LR, positive likelihood ratio; LUS, lung ultrasound; N, number of children with bronchiolitis.
a
Value expressed as mean.
b
Value expressed as median.
c
In diagnosing bronchiolitis.
d
In predicting hospital admission.
e
In identifying children with bronchiolitis affected by a concomitant bacterial pneumonia.
f
When only >1 cm consolidations were considered positive for concomitant pneumonia.
Abbreviations: AUC, area under the curve; HCPAP, helmet continuous positive airway pressure;
+LR, positive likelihood ratio; LUS, lung ultrasound; N, number of children with bronchiolitis; NICU,
neonatal intensive care unit; OR, odds ratio; PICU, paediatric intensive care unit.
a
Value expressed as mean.
b
Value expressed as median.
c
16/200 patients admitted to PICU/NICU.
length of low flow nasal cannula.41 Though, a significant correlation with bronchiolitis or concomitant pneumonia or both. Some LUS find-
was noted between the number of affected intercostal spaces on the ings, such as consolidations sized >1 cm, could be used as a useful tool
right and the length of oxygen supply. to diagnose complex cases of bronchiolitis with concomitant pneu-
monia and avoid the need to perform chest radiography.39,48 Fewer
false-
negative results indicated that LUS could have a significant
4 | DISCUSSION complementary role in the primary assessment of bronchiolitis. Thus,
a greater ability to exclude bronchiolitis as a possible diagnosis in chil-
Our review examined five topics about the diagnostic and prognostic dren with no sonographic findings. It would be reasonable to consider
value of LUS. Topics 3.1 and 3.3 reported on a direct comparison be- LUS as a first-line examination in children who present with moderate
tween LUS scores and both chest radiography and clinical course in di- or severe bronchiolitis in the PED to rule out further adverse complica-
agnosing bronchiolitis. LUS compared to chest radiography was found tions such as concomitant pneumonia. Furthermore, LUS served as a
more sensitive and specific in detecting lung abnormalities compatible good prognostic tool in the context of predicting the clinical course of
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KOGIAS et al. 229
Abbreviations: HFNC, high flow nasal cannula; K, Cohen's κ; LUS, lung ultrasound; N, number of
children with bronchiolitis; rs, Spearman's rs; ΗCPAP, helmet continuous positive airway pressure.
a
Value expressed as mean.
b
Value expressed as median.
c
At admission.
d
At discharge.
e
Using the Wood Down Ferres clinical scale.
f
Using the Hospital San Joan de Deu clinical scale.
Abbreviations: LUS, lung ultrasound; N, number of children with bronchiolitis; PICU, paediatric
intensive care unit; rs, Spearman's rs.
a
Value expressed as mean.
b
Value expressed as median.
patients and was quicker to interpret compared to chest radiography.46 Though there was a discrepancy of available data, which pointed to
Several studies successfully showed a good correlation between so- the non-uniformity of bronchiolitis as a disease, possibly due to the
nographic scores and the clinical course of the disease.31,35,36,43,45,46 nature of its causative factors.34,38,41 However, this lack of correlation
|
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230 KOGIAS et al.
Abbreviations: HFNC: high flow nasal cannula; LFNC: low flow nasal cannula; +LR: positive
likelihood ratio; LUS: lung ultrasound; N: number of children with bronchiolitis; RR: risk ratio; rs:
Spearman's rs.
a
Value expressed as mean.
b
Value expressed as median.
c
Correlation between LUS counting B-line score and OSI on day 1.
d
Correlation between LUS aeration score and OSI on day 1.
e
Correlation between the number of the affected intercostal spaces on the right and the duration
of oxygen supply.
may, at least in part, have been due to the fact that clinical scores had stay in patients with bronchiolitis. All30,31,34,37,38 but one 41 of the
moderate sensitivity and specificity and thus they could not predict studies that examined this issue found a correlation between the
accurately the severity of the disease.49 severity of LUS scores with the need of hospital stay. One study
Topics 3.2, 3.4 and 3.5 elaborated on the prognostic value estimated the average additional in-h ospital days for a certain LUS
of LUS as a predictor of PICU admission and the need for hos- score increase. 38 Higher LUS scores were correlated with longer
pital stay and respiratory support. Four studies supported hospital stays. A higher LUS score in the PED could predict a worse
that the LUS scores could predict more accurately than the outcome when patients needed hospital admittance30,32,35,36 and
clinical scores the need for PICU admission or advanced re- also correlated to the need for advanced respiratory support in
30,32,36,38
spiratory support in patients with bronchiolitis. Ten stud- the form of HFNC or helmet CPAP of inpatients. 30
30,31,32,33,34,36,37,38,41,46
ies found an evident correlation between Upon synthesising we came across many LUS scoring systems
LUS and the need for respiratory support and two found a signif- with variations. In their essence, they all examined the B-line pat-
icant correlation36,38 between LUS scores and the duration of re- tern, its occurrence, density per intercostal space and the presence
spiratory support. It seemed that combining lung ultrasonography of subpleural consolidations. Factors contributing to limitations of
findings with oxygen saturation measurements could help predict this study had to be the number of varying clinical and LUS scoring
the need for oxygen supplementation. Another firm conclusion systems used by each author, which in its turn leaded to the fluc-
was that lung ultrasonography could predict the length of hospital tuations in sensitivity and specificity between these scores. To our
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KOGIAS et al. 231
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232 KOGIAS et al.
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