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

Lung ultrasound systematic review shows its prognostic and


diagnostic role in acute viral bronchiolitis

Christos Kogias1 | Spyridon Prountzos2 |


2
Efthymia Alexopoulou | Konstantinos Douros3

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

1 | I NTRO D U C TI O N of the tracheobronchial tree, along with increased mucus produc-


tion and apoptosis of airway epithelial cells.4 A diagnosis of bron-
Acute viral bronchiolitis is a clinical syndrome with varying symp- chiolitis is based on medical history and physical examination. 5 The
toms. In developed countries, bronchiolitis is the most common disease lacks a pathognomonic radiological pattern.6 Radiographic
1,2
reason for hospitalisation in the first 12 months of life. Up to features suggesting viral bronchiolitis when using chest radiography
6% of these patients require admission to the paediatric intensive may include lung hyperinflation, peribronchial wall thickening often
care unit (PICU).3 It is characterised by inflammation and oedema symmetrical and bilateral, lack of focal consolidation in the lungs,

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

atelectasis and small lobular air-­trapping. Chest radiography can be


helpful in severe cases. The sensitivity of chest radiography for find-
Key Notes
ings consistent with bronchiolitis fluctuates and has been estimated
• Lung ultrasound (LUS) has not been included in current
between 20% and 96%.7 In typical cases, it does not add significantly
8 guidelines for the diagnosis of bronchiolitis so far, even
to the diagnostic process. Nevertheless, it is performed in 50% or
though data concerning its effectiveness have been
more of admitted infants with bronchiolitis,9,10 mainly to rule out
published.
bacterial pneumonia, resulting in exposure to ionising radiation11
• A systematic search identified 199 papers published up
and unnecessary antibiotic prescription.12
to December 2021, of which 18 were eligible for the
Lung ultrasound (LUS) has been proposed as a diagnostic tool for
review.
many neonatal and paediatric conditions.13-­15 It is performed using
• Sonographic findings as a useful adjunct to the clinical
either a high-­frequency linear probe (5–­15 MHz) when examining
ones could have both a diagnostic and prognostic role in
superficial structures or a low-­frequency micro-­convex probe (5–­
16-­19 bronchiolitis.
7.5 MHz) when assessing deeper structures. When using LUS to
diagnose bronchiolitis, suggestive findings may include liver-­like hy-
poechoic consolidations either small subpleural <10 mm in diameter
or >10 mm in diameter with air bronchogram, interstitial syndrome rs). After the first screening, the role of LUS in assessing the need for
with B-­lines and pleural effusion.17 PICU admission was added as an objective of the review. Ultimately,
The objective of our systematic review is to determine whether the diagnostic and prognostic value of the LUS was assessed by an-
definite conclusions can be made about the role of LUS scores in the swering five individual questions about whether LUS and chest radi-
diagnosis and prognosis of patients aged 0–­2 years with bronchiolitis. ography findings were comparable, whether LUS could predict the
admission to PICU, whether there was a correlation between LUS
scores and clinical course and whether LUS scores could predict the
2 | M E TH O D S length of hospital stay and the need for respiratory support.

2.1 | Search process


2.3 | Appraisal tools
Systematic literature research was carried out in three different da-
tabases, MEDLINE, Scopus and ScienceDirect. The search included All potentially relevant full texts identified in the three electronic
the keywords ‘bronchiolitis’, ‘acute bronchiolitis’, ‘acute viral bron- databases were screened by two authors (CK, SP) independently of
chiolitis’, ‘lung ultrasound’, ‘lung ultrasonography’ and the Boolean one another and a third author (KD) confirmed the data obtained.
operators AND and OR. The initial search yielded 39 papers in Discrepancies were resolved by discussion. No attempts were made
MEDLINE, 56 in Scopus and 104 in ScienceDirect databases that to contact the study authors for identifying missing and confusing
were scanned for relevance. All databases were searched from data. Each study was evaluated based on the strength of the scien-
their inception to December 2021, and no restriction was imposed tific evidence provided, using the levels of evidence from the Centre
on language and date of publication. A manual search of the refer- for Evidence-­Based Medicine in Oxford. Level I included validat-
ences found in the selected papers and reviews was also performed. ing cohort studies with good reference tests that applied blindly
Inclusion criteria were papers including patients with bronchiolitis or objectively to all patients. Level II included exploratory cohort
and presented original data from the use of LUS in diagnosis and studies with good reference tests. Level III included studies with
prognosis of the patients with bronchiolitis. Exclusion criteria were non-­consecutive patients, or with the reference test not applied
papers without relation to the field of interest and without relevant to all patients. Level IV included case–­control studies, poor or non-­
conclusions and specific types of papers such as comments, reviews, independent reference tests that were not applied to all patients but
conference abstracts, case reports, contents, editorials, letters. still interpreted independently of the index test. Level V included
expert opinion without explicit critical appraisal, or based on physi-
ology, bench research or first principles. This review has been con-
2.2 | Statistics ducted according to the Preferred Reporting Items for Systematic
Review and Meta-­Analyses guidelines. 20
The diagnostic value of LUS was assessed by comparing LUS with
chest radiography as for their sensitivity, specificity, receiver oper-
ating characteristic curve, positive likelihood ratio (+LR) and area 3 | R E S U LT S
under the curve (AUC). Its prognostic value was defined by compar-
ing clinical scores with ultrasound scores and predicting the need for We identified 199 studies, of which 152 were screened by title and
respiratory support and hospital stay using odds ratio (OR), Cohen's κ abstract after removing duplicates (Figure 1). Twenty-­six (26) pa-
coefficient (k or K) and Spearman's rank correlation coefficient (rho or pers were assessed for eligibility by full text. Five (5) of them were
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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

Records identified from: Records removed before


MEDLINE (n = 39) screening:
Scopus (n = 56) Duplicate records removed
ScienceDirect (n = 104) (n = 47)

Records screened Records excluded


(n = 152) (n = 122)

Reports sought for retrieval Reports not retrieved


(n = 30)
Screening

(n = 4)

Full-text articles assessed for Reports excluded:


eligibility reviews (n = 5)
(n = 26) did not report sonographic
data (n = 2)
diaphragm ultrasound (n = 1)

Studies included in review


Included

(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

TA B L E 1 Characteristics of studies reported

Gender
Level of
References Country Study design N Age Males Females evidence

Elkhazragy et al. 29 Egypt Comparative 36 IV


cross-­sectional
Bobillo-­Perez et al.30 Spain Prospective, observational, 80 53 daysb 37 43 II
single-­centre
Regina et al.31 Italy Single-­centre, longitudinal, 63 2.7 monthsa 41 22 IV
prospective
Ruiz et al.32 Spain Observational 200 5.7 monthsa 116 84 IV
5 monthsb
Ingelse et al.33 Netherlands Prospective, observational 17 2.7 monthsb 6 11 III
34 a
Di Mauro et al. Italy Prospective, observational 83 4.5 months III
single-­centre 3 monthsb
Özkaya et al.35 Turkey Prospective observational 76 7.4 monthsa 46 30 II
6 monthsb
Supino et al.36 Italy Prospective 76 90 daysb 41 35 III
37 b
Bueno-­C ampaña et al. Spain Prospective multicentre 145 1.7 months 76 69 III
Garrote et al.38 Spain Prospective, observational 59 90 daysb 37 22 III
39 b
Biagi et al. Italy Prospective 87 5.7 months IV
Jaszczolt et al.40 Poland Retrospective 26 7.3 monthsa IV
7 monthsb
Taveira et al.41 France Prospective, observational 47 32 daysb 27 20 IV
single-­center
Cohen et al.42 USA Prospective, observational 29 291 daysa 18 11 IV
43 a
Kader et al. Egypt Prospective, observational 25 6.94 months 7 18 IV
Varshney et al.44 Canada Prospective cross-­sectional 94 11.1 monthsb 62 32 IV
45 a
Basile et al. Italy Observational cohort 106 87.4 days 59 47 IV
71 daysb
Caiulo et al.46 Italy Prospective observational 52 2.1 monthsb 28 24 IV
a
Value expressed as mean.
b
Value expressed as median.

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.

3.3 | LUS scores and clinical course correlation


3.2 | LUS scores and PICU admission
Nine studies examined the correlation between sonographic and clini-
Four prospective studies attempted to evaluate the usefulness cal scores in children with bronchiolitis (Table 5).31,34,35,36,38,41,43,45,46
30,32,36,38
of LUS as a predictor of PICU admission (Table 4). LUS Four of them estimated a strong31,35,38,45 and two of them a weak34
scores and the need of PICU admission was found to correlate or no statistically significant correlation.41 A parallel correlation
38
with OR = 2.5. A study from Spain concluded that LUS scores was found between the clinical improvement or deterioration and
could predict the PICU admission more accurately than clini- the decrease or the increase in the number of consolidations.43,46
cal scores with both sensitivity and specificity close to 90% and Moreover, a prospective study from Italy noted a more severe sono-
30
+LR = 8.19. Moreover, a significant difference in LUS score was graphic and clinical score in infants who needed high flow nasal can-
found between infants who needed advanced respiratory support nula (HFNC) or helmet continuous positive airway pressure (CPAP)
on admission and those who did not. 36 Patients with a greater compared to those who did not need it.36 LUS score showed a mar-
LUS score were in need of respiratory support. The vast majority ginally better performance in predicting hospital admission with
TA B L E 2 Lung ultrasound scoring systems
| 226

No. of papers using


Author Ultrasound scoring system the scoring system

Basile et al.45 LUS Score 0 1 2 4


Anterolateral Normal lung sliding with Diffuse and Diffuse and dishomogeneous
data horizontal artefacts dishomogeneous interstitial syndrome and/or
(A-­lines) interstitial syndrome subpleural lung consolidations
with confluent, multiple
B-­lines and spared areas
Vertical artefacts (B-­lines)
in limited number or
absent
Paravertebral/ Interstitial Individual B-­line or absent Focal, multiple B-­lines Confluent, multiple B-­lines
posterior syndrome
data Extension on 0–­6 bilaterally involved 6–­12 bilaterally involved >12 bilaterally involved intercostal
interstitial intercostal spaces intercostal spaces spaces
syndrome
Presence of Absent Subcentimeter-­subpleural Subpleural lung consolidation of
subpleural lung lung consolidation 1 cm or more
consolidation
Copetti et al.14 LUS findings Alveolar-­interstitial Pleural-­line abnormalities Presence of ‘spared areas’ Presence of large consolidations Bilateral ‘white 10
syndrome lung’
Enghard et al.47 LUS Score 0 1–­5 6 7 8
LUS findings No B-­lines/ICS 1–­5 B-­lines/ICS Confluent B-­lines >50% Confluent B-­lines >75% ICS Confluent B-­lines 1
ICS 100% ICS
Taveira et al.41 LUS Score 0 1 2 1
LUS Finding Normal lung Severe AIS Consolidation
parenchyma or
Moderate AIS
Bobillo-­Perez LUSBRO 0 1 2 3 1
et al.30 Score
LUS Findings A-­line pattern with Non-­coalescent B-­line Coalescent B-­line Areas with >1 cm sub pulmonary
lung sliding. pattern. pattern without loss consolidation or presence of
of aeration or with atelectasis.
<1 cm sub pulmonary
consolidations.
KOGIAS et al.

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KOGIAS et al. 227

AUC of 0.814 (95%CI 0.71–­0.91, p < 0.001) in comparison with clini-


No. of papers using
the scoring system
cal score with AUC of 0.804 (95%CI 0.71–­0.89, p < 0.001).35

1 3.4 | LUS scores and the length of hospital stay

Eight studies managed to determine the correlation between LUS


scores and hospital stay (Table 6).30,31,34,35,37,38,41,45 A Spanish study
that enrolled 80 patients found a more significant correlation be-
tween the LUS score and the length of hospital stay in comparison
with a clinical score.30 Similarly, a Turkish study found that the most
effective parameter in determining hospital admission among sev-
eral variables was LUS score with OR = 1.859.35 Two studies found
a moderate correlation31,37 and one study a weak correlation34 vali-
dating a previously published ultrasound score for bronchiolitis by
(a) Depth < 10 mm (b)

Basile et al.45 They first underlined the correlation between LUS


Isolated consolidation

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

PICU was 17 points (14.5–­18) (p = 0.001).38 Nevertheless, the study


≥4 intercostal spaces) ±
lung consolidation with

of Taveira et al found no such correlation.41


Severe interstitial pattern

lines and/or confluent


B-­lines, which involve
(generalised focal B-­

(b) Severe interstitial


(a) Severe interstitial
pattern without
depth ≥10 mm

consolidation

consolidation
pattern with

3.5 | LUS scores and the need for


respiratory support

Ten studies examined the prognostic value of LUS in predicting the


B2

Abbreviations: AIS, alveolar-­interstitial syndrome; ICS, intercostal space; LUS, lung ultrasound.

need for respiratory support (Table 7).30,31,32,33,34,36,37,38,41,45 It was


B-­lines, which involve
≤3 intercostal spaces)
pattern (focal B-­lines,

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

which involve <8

and/or confluent

pattern without
(depth < 10 mm)
consolidation

consolidation

consolidation

those infants who require supplementary oxygen with a sensitivity of


pattern with

96.6%, a specificity of 98.7% and +LR of 7.43.45 Four prospective stud-


ies found a positive correlation between LUS score and the duration
of any respiratory support.30,36,37,41 One study found a strong,30 two
B1

studies a medium36,37 and one study a weak41 correlation. A study from


Spain32 that included 200 infants with bronchiolitis estimated that
B-­lines or with a
normal defined

limited number
of focal B-­lines
sliding without
as normal lung
Normal or almost

among infants in need of O2/high flow oxygen, 86.7% had an abnormal


LUS at admission and 77.8% at 48 h after admission. Among the ones
Ultrasound scoring system

in need of non-­invasive ventilation, 87.5% had an abnormal LUS both at


admission and 48 h after admission. Furthermore, a team of research-
A

ers from Spain designed a new LUS score depending on ultrasound


findings along with clinical predictors, such as age <1 month and Wood
LUS Findings

Down-­Ferres score ≥6 points.37 It found that sensitivity improved


to 89.1%, though specificity was reduced to 56% when compared to
Group
TA B L E 2 (Continued)

these same predictors studied individually. The high value of sensitiv-


ity allowed the new LUS score to be used as a screening tool, with a
high negative predictive value (88.7%). A study from Italy that included
63 infants with a mean age of 2.7 months found that the need of oxy-
Ruiz et al.32

gen therapy was more frequent in patients with higher LUS score.31
Author

However, LUS score calculated by Taveira et al on admission did not


correlate significantly with the length of non-­invasive ventilation or the
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228 KOGIAS et al.

TA B L E 3 Characteristics of studies comparing lung ultrasound and chest radiography

Lung consolidations Sensitivity Specificity +LR

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.

TA B L E 4 Lung ultrasound prognostic


Studies N Age Findings
value for admission to paediatric intensive
Bobillo-­Perez 80 53 daysb AUC: 0.932 (95%CI 0.873–­0.990) for LUS care unit
et al.30 score, 0.675 (95%CI 0.556–­0.794)
for clinical score; Sensitivity: 90,9%,
specificity: 88.9%; +LR: 8.19
Ruiz et al.32 200 5.7 monthsa PICU/NICU admissionc: 2/16 patients
5 monthsb with normal LUS, 14/16 patients with
pathological LUS.
Supino et al.36 76 90 daysb Infants who needed ventilation with
HCPAP had a more severe ultrasound
score [2 (3–­4) vs 1 (1–­3), p = 0.028]
Garrote et al.38 59 90 daysb OR: 2.5 (95%CI 1.1–­5.9, p = 0.035)

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

TA B L E 5 Correlation between lung


Studies N Age Findings
ultrasound score and clinical course
31 a
Regina et al. 63 2.7 months rs = 0.62, p = 0.01
34 a
Di Mauro et al. 83 4.5 months rs = 0.23, p = 0.036c
3 monthsb rs = 0.3, p = 0.01d
Özkaya et al.35 76 7.41 monthsa rs = 0.698, p < 0.001
6 monthsb
Supino et al.36 76 90 daysb Infants who needed ventilation with HCPAP
had a more severe sonographic (2 vs
1, p = 0.028) and clinical score (7 vs 5,
p = 0.004) than the other patients
Garrote et al.38 59 90 daysb rs = 0.504, p < 0.001 e
rs = 0.518, p < 0.001f
Taveira et al.41 47 32 daysb rs = 0.09, p = 0.57
43 a
Kader et al. 25 6.94 months Sonographic signs of improvement correlated
with improved clinical course
Basile et al.45 106 87.4 daysa Κ = 0.8, p < 0.001
71 daysb
Caiulo et al.46 52 2.1 monthsb In 38/44 patients with lung consolidations
improvement of clinical score related to a
decrease in the number of consolidations

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.

TA B L E 6 Lung ultrasound prognostic


Studies N Age Findings
value for length of hospital stay
30 b
Bobillo-­Perez et al. 80 53 days rs = 0.764 for LUS score, rs = 0.477
for clinical score
Regina et al.31 63 2.7 monthsa rs = 0.42, p < 0.01
34 a
Di Mauro et al. 83 4.5 months rs = 0.3, p < 0.001
3 monthsb
Özkaya et al.35 76 7.4 monthsa OR: 1.859 (95%CI 1.016–­3.404,
6 monthsb p = 0.044)
Bueno-­C ampaña et al.37 145 1.7 monthsb rs = 0.401, p < 0.001
Zoido Garrote et al.38 59 90 daysb Each 5-­point increase in the LUS
score was correlated to a longer
hospital stay of 1.2 days (95%CI
0.55–­1.86, p = 0.001)
Taveira et al.41 47 32 daysb rs = 0.13, p = 0.38
Basile et al.45 106 87.4 daysa LUS reflects the clinical respiratory
71 daysb status and can be used as a
screening tool in identifying
infants in need of hospitalisation.

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.

TA B L E 7 Lung ultrasound prognostic


Studies N Age Findings
value for respiratory support
Bobillo-­Perez et al.30 80 53 daysb rs = 0.763 for LUS score, rs = 0.462 for
clinical score
Regina et al.31 63 2.7 monthsa Νo patient with mild LUS score performed
oxygen therapy. 29% of patients
with moderate LUS score performed
oxygen therapy with HFNC or LFNC.
86% of patients with severe LUS score
performed oxygen therapy with HFNC
or LFNC
Ruiz et al.32 200 5.7 monthsa Among patients with normal LUS, 3/89
5 monthsb (3.4%) were in need of respiratory
support at admission and 6/89 (6.7%)
at 48 h
Ingelse et al.33 17 2.7 monthsb rs = 0.517, p = 0.034c; rs = 0.570,
p = 0.017d; no correlation on days 2
and 6
Di Mauro et al.34 83 4.5 monthsa OR: 2.2 (95% CI 1.5–­3.3), p < 0.001
3 monthsb
Supino et al.36 76 90 daysb rs = 0.35, p = 0.003
Bueno-­C ampaña 145 1.7 monthsb rs = 0.448, p < 0.001; RR: 2.5 (95% CI:
et al.37 1.6–­4), p < 0.001
Garrote et al.38 59 90 daysb LUS was associated with the duration of
oxygen therapy: +0.87 days for every
5-­point increase in LUS score (95% CI:
0.26–­1.48), p = 0.006
Taveira et al.41 47 32 daysb rs = 0.318, p = 0.037 e
45 a
Basile et al. 106 87.4 days Sensitivity: 96.6% (95%CI: 82.2%–­99.4%),
71 daysb specificity: 98.7% (95% CI: 93%–­
99.8%), +LR: 7.43

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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