Ecochard-Dugelay et al.

BMC Pediatrics 2014, 14:143

http://www.biomedcentral.com/1471-2431/14/143

RESEARCH ARTICLE Open Access

Clinical predictors of radiographic abnormalities

among infants with bronchiolitis in a paediatric
emergency department
Emmanuelle Ecochard-Dugelay1, Muriel Beliah2, Francis Perreaux2, Jocelyne de Laveaucoupet3, Jean Bouyer1,
Ralph Epaud4,5, Philippe Labrune2,8, Hubert Ducou-Lepointe6,7 and Vincent Gajdos1,2,8*

Abstract
Background: Acute viral respiratory exacerbation is one of the most common conditions encountered in a
paediatric emergency department (PED) during winter months. We aimed at defining clinical predictors of chest
radiography prescription and radiographic abnormalities, among infants with bronchiolitis in a paediatric
emergency department.
Methods: We conducted a prospective cohort study of children less than 2 years of age with clinical bronchiolitis,
who presented for evaluation at the paediatric emergency department of an urban general hospital in France.
Detailed information regarding historical features, examination findings, and management were collected. Clinical
predictors of interest were explored in multivariate logistic regression models.
Results: Among 410 chest radiographs blindly interpreted by two experts, 40 (9.7%) were considered as abnormal.
Clinical predictors of chest radiography achievement were age (under three months), feeding difficulties, fever over
38C, hypoxia under than 95% of oxygen saturation, respiratory distress, crackles, and bronchitis rales. Clinical
predictors of radiographic abnormalities were fever and close to significance hypoxia and conjunctivitis.
Conclusion: Our study provides arguments for reducing chest radiographs in infants with bronchiolitis. For infants
with clinical factors such as age less than three months, feeding difficulties, respiratory distress without hypoxia,
isolated crackles or bronchitis rales, careful clinical follow-up should be provided instead of chest radiography.
Keywords: Bronchiolitis, Chest radiography, Radiographic pneumonia, Clinical decision rule

Background diagnosis and management of bronchiolitis showed a CR

Acute viral respiratory exacerbation is one of the most rate of 72% that lead to an increased likelihood of anti-
common conditions encountered in a paediatric emer- biotic therapy and length of stay in hospital [2]. Recent
gency department (PED) during winter months [1]. It is studies showed that most of these CR were read as nega-
often difficult to distinguish viral from bacterial cause of tive, (ie consistent with a simple acute viral respiratory
dyspnea with only clinical features. The lack of reliable exacerbation), and that many of them might have been
clinical decision rule for management of bronchiolitis avoided, saving time, money, and children exposure to
often leads to perform chest radiography (CR) in order to ionizing radiations [3,4].
detect radiographic abnormalities inconsistent with this The aims of our study were to investigate historical
diagnosis, such as pneumonia or other cardio-respiratory features and clinical examination findings in the evalu-
disease. An American survey of clinical practices in the ation of infants with bronchiolitis that conduct to the
prescription of CR, and to determine clinical predictors
of radiographic abnormalities.
* Correspondence: [email protected]
1
INSERM U1018, Paris 94270, Le Kremlin Bictre, France
2
Paediatric Department, APHP, Hopital Antoine Bclre, BP 405, 92140 Cedex
Clamart, France
Full list of author information is available at the end of the article

2014 Ecochard-Dugelay et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the
Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public
Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this
article, unless otherwise stated.
Ecochard-Dugelay et al. BMC Pediatrics 2014, 14:143 Page 2 of 5
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Methods findings and the decision to realise CR or not. Clinical

Study design and setting predictors of radiographic abnormality were studied on
The study was approved by the ethical committee CPP patients that underwent CR. Continuous and ordinal vari-
(Comit de Protection des Personnes) Ile de France 3. ables were categorized: temperature was coded as <38C,
We performed a prospective cohort study of children 38 39C or > 39C, hypoxia was defined by an oxygen
less than 2 years of age with clinical bronchiolitis, who saturation <95%, age-related respiratory rate was de-
presented for evaluation to the PED of a urban general fined in accordance with Liu definition (Table 1) [6].
hospital (Antoine Beclere Clamart, Paris suburb, France) We created a global score of respiratory distress, using
between October 2006 and February 2007. According to weighted retraction signs widely used and that showed a
the American Academy of Pediatrics, bronchiolitis was good inter-observer reproducibility (Tables 2 and 3) [7].
defined as a constellation of clinical symptoms and signs Variables with a p-value 0.20 in univariate analysis
including a viral upper respiratory prodrome followed by were considered candidate variables for inclusion in the
increased respiratory effort and wheezing in children less multivariate model and p-values 0.05 were considered
than 2 years of age [5]. All children who had clinical bron- statistically significant.
chiolitis on examination were eligible to the study. All Because CR is a frequent event (about 50%), odds-
physicians working in the PED were asked and accepted ratio substantially overestimate the relative risk. We used
to participate. Physicians were oriented to the question- then Poisson regression to estimate relative risk, first for
naire before the start of the study and were continually performing CR, and then for radiographic abnormalities
informed of study details throughout the study period. [8]. To enhance power of our analysis, we used multiple
They completed a questionnaire for each patient included. imputation for missing values [9-11].
To prevent free text responses, fixed-choice format has All analyses were performed on Stata 11 Software
been chosen. (StataCorp. 2007. Stata Statistical Software: Release 11.
College Station, TX: StataCorp LP).
Clinical data collection
Detailed information regarding historical features and Results
examination findings at first evaluation were collected. Demographics data and clinical findings
Demographics data included age, gender, history of pre- Study forms were completed for 821 patients (Table 4).
maturity, known chronic illness, and previous wheezing One hundredand-seventy infants (21%) were less than
episodes. Historical features of interest included duration three months of age, 13% had prematurity history, and
of symptoms, history of fever, feeding difficulties, and anti- 60% had no wheezing history before this episode. The
biotics use before PED admission. Physicians were asked mean duration of symptoms was 4.1 days (SD 5.3 days),
to report temperature, respiratory rate, retraction signs 38% of children had feeding difficulties and about 15%
and wheezing, oxygen saturation, auscultation findings had antibiotic prescription before the emergency admis-
(bronchitis rales, crackles) and the presence of otitis, sion. Clinically, about half of children were febrile, 105
conjunctivitis or toxic appearing. Clinicians recorded the (14.1%) had oxygen saturation under 95%, 272 (33%)
following management: CR, antibiotic prescription, and had bronchitis rales and 104 (12.7%) crackles. 427 (52%)
decision of hospitalisation. of the children have had a chest radiography and 350
(42.6%) had been hospitalized. One hundred and four
Chest radiography interpretation (12.7%) children had otitis, 27 (3.3%) conjunctivitis. 215
All CR were performed by using standard equipment and (26%) received antibiotics (13.5% of children without CR
radiographic techniques. They were blindly and independ- versus 38.8% of children with CR, p < 0.001).
ently reviewed in digital format by 2 paediatric radiologists.
CR was read as either normal or abnormal. Abnormalities Chest radiographs
were lobar consolidation, segmental or lobar atelectasia, or Among the 427 chest radiographs performed, 410 were
cardiomegaly. Others findings (prominent bronchial opaci- interpreted by both experts. Two chest radiographs were
ties, peribronchial infiltrates, hyperinflation or sub-segmental excluded because of their poor quality and 15 could not
atelectasia) were considered as consistent with the diagnosis
of bronchiolitis and therefore had no impact on therapeutic Table 1 Age related respiratory rate from Liu et al. [6]
decision. For CR whose interpretation differed between both Respiratory rate (/min)
radiologists, we organized a consensus meeting. 1 point 2 points 3 points
Age < 2 months 60 61-69 70
Statistical analysis
Age 2 12 months 50 51-59 60
Analyses were performed on the whole study population
Age 12 24 months 40 41-44 45
to assess the relationship between history and clinical
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Table 2 Clinical score of weighted retraction signs Table 4 Description of the study population (n = 821)
(total /8) N n (%)
None Moderate Important First wheezing episode 801 492 (59.9)
Intercostal indrawing 0 1 2 Sex (male/female) 821 476/345
Sub-costal indrawing 0 1 2 Age under 3 months 821 170 (20.7)
Nasal flaring 0 1 2 Prematurity <37 weeks 780 108 (13.1)
Thoraco-abdominal movement 0 1 2 Respiratory symptom length (j) mean (SD) 806 4.1 (5.3)
Feeding difficulties 799 309 (37.6)
be retrieved (Figure 1). Consistency rate between both Temperature 738
blinded radiologists was 84.3%. < 38C 373 (45.4)
Most infants had prominent bronchial opacities, peri-
[38-39C] 211 (25.7)
bronchial infiltrates and/or hyperinflation. These CR
were considered to be consistent with the diagnosis of 39C 154 (18.8)
bronchiolitis or viral acute exacerbation. Forty (9.7%) CR Previous antibiotherapy 816 124 (15.1)
were considered as abnormal: 39 with lobar or alveolar Age-related respiratory rate [6] 747
condensations and one with lobar atelectasia. 1 point 427 (52.0)
2 points 101 (12.3)
CR achievement
3 points 219 (26.7)
Univariate analysis identified nine variables that were
significantly related to the realisation of a chest radiog- Global score for retraction signs 798
raphy: age 3 months (p = 0.03), feeding difficulties (p < 0 point 233 (29.2)
0.001), fever (p < 0.001), tachypnea (p = 0.002), global 1 point 454 (56.9)
score of respiratory distress (p < 0.001), hypoxia (SpO2 < 2 points 83 (10.4)
95%, p < 0.001), crackles (p < 0.001), bronchitis rales (p = 3 points 28 (3.5)
0.04) and toxic appearing (p = 0.04). All these variables
Oxygen saturation 747
were included in the multivariate model (Table 5) which
found a significant association between the realisation of 95% 642 (85.9)
CR and age 3 months (p = 0.003), feeding difficulties <95% 105 (14.1)
(p = 0.01), presence of fever (p < 0.001), hypoxia (p = 0.04), Crackles 814 81 (9.9)
global score of respiratory distress (p = 0.03), crackles Bronchitis rales 814 272 (33.1)
(p = 0.003) or bronchitis rales (p = 0.004) (Table 4). Otitis 789 104 (12.7)
Conjunctivitis 802 27 (3.3)
Radiographic abnormalities
Univariate analysis only identified fever as significantly Toxic appearing 817 35 (4.3)
related to the presence of radiographic abnormality (p = Chest radiography 821 427 (52.0)
0.02). Finally, multivariate analysis only identified fever Hospitalisation 821 350 (42.6)
as an independent clinical predictor of radiographic ab-
normalities (p = 0.04) (Table 6). Presence of crackles was
not an independent predictor in our population (p = 0.1).

Discussion
To our knowledge, this study is one of the largest pro-
spective cohorts of infants under two years of age who
have been admitted to a PED for bronchiolitis. We have
been able to determine clinical predictors of CR pre-
scription and radiographic abnormalities. We observed a
high rate of CR (52.7%) with a rate of abnormalities of

Table 3 Global score of respiratory distress

Global score of respiratory distress
0 point 1 point 2 points 3 points
Clinical score of retraction signs 0 1 or 2 3 or 4 5 to 8 Figure 1 Description of chest radiographs in the study.
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Table 5 Factors associated with CR achievement: use [17]. Limiting the number of CR is important for
multivariate analysis several reasons: although the radiation associated with
RR IC.95 p achieving a CR is negligible (0.02 mSv, whereas natural ex-
Age 3 months 1.4 [1.1 1.8] 0.003 posure is estimated at about 0.05 mSv per week), a recent
Prematurity 1.3 [1.0 1.6] 0.08 report on the French population exposure to ionizing
radiation related to acts of medical diagnosis, reports a
Feeding difficulties 1.3 [1.1 1.6] 0.01
number of CR equal to 0.2 acts per year per child under
Fever
one year (approximately 160,000 procedures per year for a
[38-39C] 1.4 [1.1 1.8] <0.001 country with 800,000 births per year) [20]. Furthermore,
39C 1.9 [1.5 2.5] CR achievement appears to be associated with an in-
SpO2 < 95% 1.3 [1.0 1.7] 0.04 creased likelihood of prescribing unnecessary antibiotic
Age related respiratory rate* [2,18,21]. To reduce the number of unnecessary CR, it is
important to understand which clinical variables are asso-
score = 2 1.2 [0.9 1.7] 0.2
ciated with the realisation of this diagnostic test, and to
score = 3 1.2 [1.0 1.5]
compare these clinical variables with those associated with
Global score of respiratory distress radiographic abnormalities. In our study, clinical features
score = 1 1.4 [1.1 1.8] 0.03 such as age (less than 3 months), hypoxia, conjunctivitis,
score =2 1.7 [1.2 2.4] feeding difficulties, retraction signs, and presence of bron-
score =3 1.7 [1.1 2.8] chitis rales and crackles were independent clinical predic-
tors of CR, while these variables did not appear to predict
Toxic-appearing 1.0 [0.6 1.5] 0.9
a greater risk of radiographic abnormalities. Thus, our re-
Crackles 1.5 [1.2 2.0] 0.003
sults encourage to restrict CR prescription to infants with
Bronchitis rales 1.4 [1.1 1.7] 0.004 fever. Those clinical predictors of radiographic abnormal-
*According to Liu et al. [6]. ities are consistent with previous studies [3,4,12,13,16-18].
Neuman et al. conducted a large prospective cohort study
9.7% (4.9% of the whole study population). Our study to assess the relation between historical features and phys-
found a great difference between clinical predictors of ical examination findings and radiographic pneumonia
CR prescription (age 3 months, feeding difficulties, fever, [4]. Fever, duration of fever, hypoxia and focal rales
presence of retraction signs, hypoxia, crackles, bronchial emerged as significant predictors of pneumonia on the
rales and toxic appearing) and the only clinical factor subgroup of patients younger than five years. Further-
predictive of radiographic abnormalities (fever). Others more they attempted to stratify children in low and high
clinical factors such hypoxia and conjunctivitis were not risk for pneumonia by recursive partitioning analysis
predictive of radiographic abnormalities. but they were unable to characterize a low risk popula-
The prevalence of pneumonia in previous investigations tion among children of this subgroup.
varied widely, ranging from 0.75 to 63% [3,4,12-19]. These As recommended, no microbiological testing has been
variations may be due to several factors (age of patients, performed in these patients. Indeed, the question of the
inclusion of patients with or without history of wheezing, benefit of their implementation for limiting antibiotics
percentage of children who underwent CR, considered prescriptions or chest radiographs arises (even if a sec-
abnormalities). Wide variations in prescription rates of CR ondary bacterial infection may be a complication of an
(ranging from 42 to 72 [2,15-17]) reflect lack of consensus, authentic viral bronchiolitis and that the presence of
even if recent guidelines recommend to limit their routine RSV does not exclude a bacterial superinfection).
Our study had several limitations. First it was a mono-
centric study and our results could be considered repre-
Table 6 Clinical predictors of radiographic abnormalities:
multivariate analysis
sentative of all PED. As CR has only been performed in
52% of infants, the scope of our assessment of factors asso-
RR IC.95 p
ciated with radiographic abnormalities was limited. How-
Fever
ever, the number of CR studied (410) represented a large
[38-39C] 1.1 [0.4 2.7] 0.04 population compared with previous studies. Moreover,
39C 2.4 [1.1 5.1] given the current data in the literature and recommenda-
SpO2 < 95% 1.8 [0.9 3.5] 0.08 tions, it would be unethical to practice systematic CR in
Conjunctivitis 2.7 [0.9 7.9] 0.07 bronchiolitis. Finally, our population was heterogeneous
History of wheezing 1.5 [0.8 2.8] 0.3
regarding the episode of bronchiolitis considered for our
study: 40% of the patients already had a wheezing episode.
Crackles 1.7 [0.8 3.4] 0.1
Our work reflected current practices in emergency room.
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Conclusion 8. McNutt LA, Wu C, Xue X, Hafner JP: Estimating the relative risk in cohort
Our study provides arguments for reducing CR achieve- studies and clinical trials of common outcomes. Am J Epidemiol 2003,
157(10):940943.
ment in infants admitted to PED for bronchiolitis. Espe- 9. Royston P: Multiple imputation of missing values: update. Stata J 2005,
cially, clinical factors such as age less than three months, 5(2):188201.
feeding difficulties, presence of retraction signs without 10. Rubin D: Multiple Imputation for Nonresponse in Surveys. New York: Wiley;
1987.
hypoxia, or isolated rales and crackles are not considered 11. Van Buuren S, Boshuizen H, Knook D: Multiple imputation of missing
as predictive of radiographic abnormalities and should blood pressure covariates in survival analysis. Stat Med 1999,
not lead to the prescription of CR. For those patients, 18(6):681694.
12. Farah MM, Padgett LB, McLario DJ, Sullivan KM, Simon HK: First-time
careful clinical follow-up is recommended as an alterna- wheezing in infants during respiratory syncytial virus season: chest
tive. Moreover further studies are required to evaluate radiograph findings. Pediatr Emerg Care 2002, 18(5):333336.
the real link between the achievement of CR and antibi- 13. Garcia Garcia ML, Calvo Rey C, Quevedo Teruel S, Martinez Perez M,
Sanchez Ortega F, Martin del Valle F, Verjano Sanchez F, Perez-Brena P:
otics prescription. Chest radiograph in bronchiolitis: is it always necessary? An Pediatr (Barc)
2004, 61(3):219225.
Abbreviations 14. Gershel JC, Goldman HS, Stein RE, Shelov SP, Ziprkowski M: The usefulness
CR: Chest radiography; PED: Pediatric emergency department. of chest radiographs in first asthma attacks. N Engl J Med 1983,
309(6):336339.
Competing interests 15. Kneyber MC, Moons KG, de Groot R, Moll HA: Predictors of a normal chest
The authors declare that they have no competing interests. x-ray in respiratory syncytial virus infection. Pediatr Pulmonol 2001,
31(4):277283.
Authors contributions 16. Mahabee-Gittens EM, Bachman DT, Shapiro ED, Dowd MD: Chest
EDE, JB, RE, PL and VG conceived the study and its design. MB and FP radiographs in the pediatric emergency department for children < or =
coordinated inclusions in the study. JDL and HDL reviewed all chest X-rays. 18 months of age with wheezing. Clin Pediatr 1999, 38(7):395399.
EDE, JB, PL and VG helped drafting the manuscript. All authors read and 17. Roback MG, Dreitlein DA: Chest radiograph in the evaluation of first time
approved the final manuscript. wheezing episodes: review of current clinical practice and efficacy.
Pediatr Emerg Care 1998, 14(3):181184.
Acknowledgements 18. Schuh S, Lalani A, Allen U, Manson D, Babyn P, Stephens D, MacPhee S,
The authors are grateful to the participants and their care takers/families as Mokanski M, Khaikin S, Dick P: Evaluation of the utility of radiography in
well as the staffs at the emergency pediatric ward of Hpital Antoine acute bronchiolitis. J Pediatr 2007, 150(4):429433.
Bclre. This study received no funding. 19. Walsh-Kelly CM, Kim MK, Hennes HM: Chest radiography in the initial
episode of bronchospasm in children: can clinical variables predict
Author details pathologic findings? Ann Emerg Med 1996, 28(4):391395.
1
INSERM U1018, Paris 94270, Le Kremlin Bictre, France. 2Paediatric 20. Etard C, Sinno-Tellier S, Aubert B: Exposition de la population franaise
Department, APHP, Hopital Antoine Bclre, BP 405, 92140 Cedex Clamart, aux rayonnements ionisants lis aux actes de diagnostic mdical en
France. 3Department of Paediatric Radiology, APHP, Hopital Antoine Bclre, 2007. Institut de veille sanitaire 2010, http://www.invs.sante.fr/publications/
BP 405, 92140 Cedex Clamart, France. 4Paediatric Department, Centre 2010/rayonnements_ionisants_diagnostic_medical/rapport_expri.pdf.
Intercommunal de Crteil, 94000 Crteil, France. 5University Paris Est Crteil, 21. Swingler GH, Hussey GD, Zwarenstein M: Randomised controlled trial
94000 Crteil, France. 6Department of Paediatric Radiology, APHP, Hopital of clinical outcome after chest radiograph in ambulatory acute
Trousseau, 75012 Paris, France. 7University Pierre et Marie Curie, 75005 Paris, lower-respiratory infection in children. Lancet 1998, 351(9100):404408.
France. 8University Paris Sud, UFR Kremlin Bictre, Chtenay-Malabry 94276
Cedex, Le Kremlin Bictre, France.
doi:10.1186/1471-2431-14-143
Cite this article as: Ecochard-Dugelay et al.: Clinical predictors of
Received: 17 December 2013 Accepted: 28 May 2014 radiographic abnormalities among infants with bronchiolitis in a
Published: 6 June 2014 paediatric emergency department. BMC Pediatrics 2014 14:143.

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