International Journal of Pediatric Otorhinolaryngology 90 (2016) 86e90

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International Journal of Pediatric Otorhinolaryngology

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Review Article

Bronchoscopy findings in recurrent croup: A systematic review and

meta-analysis
Jared C. Hiebert a, *, Yan Daniel Zhao b, Elena B. Willis a
a
Department of Otorhinolaryngology, The University of Oklahoma Health Sciences Center, 920 Stanton L. Young Blvd WP 1290, Oklahoma City, OK, 73104,
USA
b
Department of Biostatistics and Epidemiology, The University of Oklahoma Health Sciences Center, 801 NE 13th St, Room 327, Oklahoma City, OK, 73104,
USA

a r t i c l e i n f o a b s t r a c t

Article history: Importance: The etiology of recurrent croup is often anatomic. Currently there is no set criteria for
Received 6 July 2016 determining who should undergo diagnostic bronchoscopy and which patients are at most risk for
Received in revised form having a clinically significant finding. Few studies have addressed these questions.
3 August 2016
Objective: To identify risk factors for clinically significant findings on bronchoscopy in children with
Accepted 3 September 2016
Available online 5 September 2016
recurrent croup and the frequency of bronchoscopy findings in general.
Data sources: PUBMED, Ovid MEDLINE, EMBASE.
Study selection: Articles addressing bronchoscopy in children with recurrent croup, up to July 2016, were
Keywords:
Recurrent croup
reviewed. Related keywords and medical subject headings were used during the search. The abstracts
Bronchoscopy were reviewed to determine suitability for inclusion based on a set of criteria. Manual crosscheck of
Pediatric references was performed.
Data extraction: We analyzed the bronchoscopy findings of individual patients in each study and their
associated risk factors when available.
Results: We reviewed 11 articles, published between 1992 and 2016, including 885 patients (654 males,
237 females). Only 5 studies, including 455 patients, had sufficient data for meta-analysis. Our study
revealed that the three most common bronchoscopy findings were subglottic stenosis, reflux changes,
and broncho/tracheomalacia. Only 8.7% of patients were noted to have clinically significant findings on
bronchoscopy. Meta analysis showed an association between significant bronchoscopy findings and
History of Intubation [OR ¼ 5.17, 95% CI 2.65e10.09], Inpatient Consultation [OR ¼ 4.01, 95% CI 1.44
e11.20], Age < 3 [OR ¼ 3.22, 95% 1.66e6.27], Age < 1 [OR ¼ 2.86, 95% CI 1.28e6.40], and Prematurity
[OR ¼ 2.90, 95% CI 1.39e6.06]. Our study found a high incidence of a History of GERD (20%) and Asthma/
Allergies (35%) among patients with recurrent croup, but these variables did not reach statistical sig-
nificance in patients with significant bronchoscopy findings ([OR ¼ 1.62, 95% CI 0.79e3.30], [OR ¼ 0.57,
95% CI 0.30e1.08] respectively).
Conclusion: The risk factors most associated with clinically significant bronchoscopy findings in recur-
rent croup are Intubation, Inpatient Consultation, Age < 3, Age <1, and Prematurity. A History of GERD
and Asthma/Allergy, though highly prevalent in recurrent croup patients, were not statistically associ-
ated with significant bronchoscopy findings.
Relevance: The results should guide physicians in selecting which recurrent croup patients are most at
risk for significant findings and thus may warrant bronchoscopy.
© 2016 Elsevier Ireland Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
2. Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87

* Corresponding author.
E-mail address: Jared-hiebert@ouhsc.edu (J.C. Hiebert).

http://dx.doi.org/10.1016/j.ijporl.2016.09.003
0165-5876/© 2016 Elsevier Ireland Ltd. All rights reserved.
 J.C. Hiebert et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 86e90 87

2.1. Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88

3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
Conflicts of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

1. Introduction often not significant and do not alter clinical management. In an era
of evidence based medicine and healthcare cost-consciousness, it
Croup is a common pediatric condition affecting children be- would be advantageous to identify which patient s are at highest
tween 6 months and 3 years. Typically a self-limited viral illness, it risk for having a clinically significant finding on bronchoscopy and
presents with a barky cough, stridor, and respiratory distress. who should be taken to the operating room for bronchoscopy.
Recurrent croup, however, is a different entity affecting 6.4% of Several recent studies have attempted to answer this question and
children before the age of 4 and is defined as 2 or more croup-like identify pertinent risk factors [6,7,8]. The objective of this study was
episodes [1]. It should not be considered a definitive diagnosis as to systematically review the literature and identify risk factors that
there is often an underlying etiology to the condition, whether it is may predict clinically significant findings on bronchoscopy in
a congenital anatomic abnormality or other pathophysiological children with recurrent croup and also note the frequency of
process causing narrowing or obstruction of the airway. Multiple bronchoscopy findings in general.
studies have shown a high incidence of both asthma/allergies and
gastroesophageal reflux (GERD) in patients with recurrent croup 2. Materials and methods
[2,3,4,5]. Many children with recurrent croup are taken for direct
laryngoscopy and bronchoscopy to evaluate the airway for an un- Pubmed, Ovid MEDLINE, and EMBASE database searches were
derlying etiology. Abnormalities are sometimes found but they are conducted to include all articles that addressed bronchoscopy
IDENTIFICATON

Articles identified through database Additional records from manual

search (n=255) reference crosscheck (n=1)
SCREENNG

Articles included for abstract review (n=14) Records excluded (n=241)

ELIGIBILITY

Full-text articles assessed for eligibility Full-text articles excluded (n=1)

(n=12)
INCLUDED

Articles included in systematic review Articles included in meta-analysis (n=5)

(n=11)

Fig. 1. Flow diagram describing the search strategy used to include articles in the systematic review and meta-analysis.
88 J.C. Hiebert et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 86e90

findings in pediatric patients with recurrent croup, up to July 2016.
The PRISMA Statement was taken into account when developing
the systematic review [9]. The search terms “recurrent croup” OR
“croup” AND “bronchoscopy” were used. The articles were
screened by title and abstract based on set criteria. To ensure that
all relevant published articles were captured, the reference lists
from the selected articles were searched for additional publica-
tions. Prospective or retrospective studies were included that
addressed pediatric patients with recurrent croup, defined as two
or more episodes of croup, who underwent rigid bronchoscopy. The
articles were analyzed to determine bronchoscopy findings as well
as patient risk factors associated with clinically significant bron-
choscopy findings. A clinically significant bronchoscopy finding was
one that alters the clinical management of the patient and defined
as grade II or greater subglottic stenosis, or requiring surgical
intervention, or repeat bronchoscopy for surveillance. This defini-
tion was based on previous criteria established by Jabbour et al. [8].
In the event that the above criteria could not be met due to
incomplete data from a study but reported findings were deemed
significant by the authors they were also included. This occurred
only in two patients. Subglottic stenosis was graded according to
the Cotton-Myer scale. When the grade of stenosis was not
explicitly reported in a study, those patients were included in the
total number of patients with subglottic stenosis but not in the
individual subglottic stenosis subgroups (i.e. I,II,III,IV). Patients with
a diagnosis of asthma or allergies were combined. All studies in
which children with recurrent croup underwent bronchoscopy
with reported findings were included in the systematic review but
only those studies with identifiable risk factors that could be linked
to individual patients were able to be used in the meta-analysis.
Risk factors studied included Inpatient Consultation, Age <3, Age
<1, Prematurity, History of Gastroesophageal Reflux Disease, and
History of Asthma/Allergies. These were the only consistent re-
ported risk factors across studies. Non-English studies, adult
populations, and case reports were excluded. Articles judged to
meet inclusion criteria were then studied.
2.1. Statistical analysis
For each risk factor associated with recurrent croup, the overall
odds ratio and its 95% confidence interval across relevant studies
was summarized using meta-analysis. The homogeneity of the
odds ratios across relevant studies was tested using Cochran's Q
statistics. If the homogeneity was not rejected at 0.1 level, then the
odds ratios were treated as random effects and the overall odds
ratio was computed using the C-M-H method; otherwise, the odds
ratios were treated as fixed effects and the overall odds ratio was
computed using the Der Simonian-Laird method. Additionally, in
the systematic review, the bronchoscopy findings were noted and
categorized into common themes to identify the most common
pathology.
3. Results
The process of article screening and selection is summarized in
Fig. 1. We only reviewed articles written in the English literature
that included Pediatric patients diagnosed with recurrent croup
who underwent bronchoscopy.
We reviewed 11 articles, published between 1992 and 2016,
including 885 patients with 654 males and 237 females (Table 1).
Six patients from Farmer et al. [10] did not undergo bronchoscopy
resulting in 885 patients with bronchoscopy findings. Only 5
studies [6,7,8,9,11], including 455 patients, had sufficient and spe-
cific data for meta-analysis. Our study revealed that the most
commonly reported bronchoscopy finding was subglottic stenosis
(30.6%). The next three most common bronchoscopy findings were
reflux changes (24.6%), broncho/tracheomalacia (4.6%), and vocal
fold pathology (3.7%), which includes vocal fold paralysis,

Table 1
Bronchscopy findings of included studies. Abbreviations: No. ¼ number of patients, M/F ¼ male/female, Sig. ¼ significant, FB ¼ foreign body.

Author No. M/F Sig. SGS Tracheomalacia/ Vocal fold Laryngomalacia Subglottic Congenital Vallecular FB Reflux Otherb
Findings Bronchomalacia Pathologyd cyst/ Airway cyst
hemangioma stenosis

Chun 30 20/ 2 6-Ia, 1-II 1 1 1

[15] 10
Delaney 103 81/ 9 19-I, 5-II, 1-III 2 8 3 2
[7] 22
Duval 235 174/ 27 68-I, 8-II, 1-III 25 11 11 2 111
[6] 61
Jabbour 81 59/ 8 17-I, 4-II, 1-III 5 9 4 3 1 4
[8] 22
Hoa [5] 47 29/ 12 34-I, 12-II 41
18
Rankin 90 72/ 6 11-I, 4-II, 1-III 4 7 1 1 23
[13] 18
Waki 32 19/ 0 5-I 1 1 2
[16] 13
Kwong 17 13/4 4 17-I 14
[14]
Farmer 47 40/ 5 13-I, 1-II 9 1 9 1 9 2
[10] 13
Tan [11] 6 6/0 2 1-I 2 1
Hodnett 197 141/ 2 39-I, 1-II, 1-III
[12] 56
885c 654/ 77 271-total (30.6%) 212-I 41 (4.6%) 33 (3.7%) 24 (2.7%) 12 (1.3%) 10 (1.1%) 1 (0.11% 1 218 5
237 (8.7%) (23.9%), 36-II (4.1%), 5-III (0.11%) (24.6%) (0.56%)
(0.56%)
a
I, II, III indicates grade of subglottic stenosis.
b
Includes subglottic edema, abnormal mucosa, pseudosulci, thick secretions.
c
6 patients from Farmer et al. did not undergo endoscopy but had gender assigned.
d
Includes vocal fold paralysis, asymmetry, granulation tissue, nodule.
 J.C. Hiebert et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 86e90 89

1. Risk factor: Intubaon asymmetry, granulation tissue, and nodules. Only 77 (8.7%) patients
were noted to have clinically significant findings on bronchoscopy.
Intubation No Odds Ratio Our meta-analysis (Fig. 2) showed an association between signifi-
cant bronchoscopy findings and History of Intubation [OR ¼ 5.17,
Study Events Total Events Total OR 95% -CI W(fixed)

Jabbour 2011 6 19 2 62 13.85 [2.51; 76.47] 8.6%

Delaney 2015 7 31 2 72 10.21 [1.98; 52.54] 12.5% 95% CI 2.65e10.09], Inpatient Consultation [OR ¼ 4.01, 95% CI
Duval 2015 17 86 10 149 3.42 [1.49; 7.88] 78.9%
1.44e11.20], Age < 3 [OR ¼ 3.22, 95% 1.66e6.27], Age < 1
[OR ¼ 2.86, 95% CI 1.28e6.40], and Prematurity [OR ¼ 2.90, 95% CI
Fixed effect model 136 283 5.17 [2.65; 10.09] 100%

0.01 0.1 0.5 1 2 10 76.47 1.39e6.06]. Our study found a high incidence of a History of GERD
2. Risk Factor: Prematurity
(20%) and Asthma/Allergies (35%) among patients with recurrent
croup, but these variables did not reach statistical significance in
patients with significant bronchoscopy findings ([OR ¼ 1.62, 95% CI
Study
Prematurity No
Events Total Events Total
Odds Ratio
OR 95% -CI W(fixed)
0.79e3.30], [OR ¼ 0.57, 95% CI 0.30e1.08] respectively).
Jabbour 2011 4 11 4 70 9.43 [1.92; 46.23] 9.8%
Duval 2015 10 54 17 181 2.19 [0.94; 5.12] 90.2%

Fixed effect model 65 251 2.90 [1.39; 6.06] 100%

4. Discussion

0.02 0.1 0.5 1 2 10 46.23 Recurrent croup is a relatively common entity encountered by
3. Risk Factor: GERD History
the otolaryngologist and may indicate an underlying congenital
abnormality or pathological process causing airway narrowing or
obstruction. The quandary for the otolaryngologist is determining
Study
GERD History No
Events Total Events Total
Odds Ratio
OR 95% -CI W(fixed)
which recurrent croup patients warrant bronchoscopy evaluation
Delaney 2015 6 62 3 41 1.36 [0.32; 5.76] 27.9%
in the operating room. The current study represents the largest
Duval 2015 12 78 15 157 1.72 [0.76; 3.88] 72.1% review of recurrent croup patients and the incidence of bronchos-
Fixed effect model 140 198 1.62 [0.79; 3.30] 100%
copy findings and can help guide the otolaryngologist in the clinical
0.2 0.5 1 2 5
management of these patients.
An inherent challenge and weakness of this review study is the
4. Risk Factor: Asthma/Allergy History heterogeneity between studies and the lack of specificity in patient
reporting. This is more so for the meta-analysis aspect than the
review of bronchoscopy findings since there were not consistently
Odds Ratio
Study
Asthma/Allergy No
Events Total Events Total OR 95% -CI W(fixed)
reported risk factors across studies. The most homogenous studies
Delaney 2015 6 115 12 91 0.36 [0.13; 1.01] 49.4%
included those by Duval, Delaney, and Jabbour which was beneficial
Duval 2015 10 100 17 135 0.77 [0.34; 1.76] 50.6%
since these also represented the largest patient cohorts. However,
Fixed effect model 215 226 0.57 [0.30; 1.08] 100%
analysis is still limited by what risk factors studies report. The study
0.2 0.5 1 2 5
by Duval, for example, found that chronic cough was a significant
risk factor for clinically significant bronchoscopy findings but this
was not included in meta-analysis due to its singularity. Addition-
5. Risk Factor: Inpaent Consult ally, all included studies were retrospective in nature.
Another weakness of the study is the selection bias of the pa-
Odds Ratio
tients. We are only able to evaluate those patients with recurrent
Inpat Consult No
Study Events Total Events Total OR 95% -CI W(random) croup who underwent bronchoscopy at tertiary care facilities
Jabbour 2011
Delaney 2015
4
4
16
12
3
5
63
91
6.67 [1.32; 33.69]
8.60 [1.92; 38.59]
25.2%
27.7%
which likely represent a population of sicker and higher acuity
Duval 2015 11 65 16 169 1.95 [0.85; 4.46] 47.1% patients. There are many children with a diagnosis of recurrent
Random effects model 93 323 4.01 [1.44; 11.20] 100%
croup who were observed and we will never know the bronchos-
0.1 0.5 1 2 10 copy findings in those patients, which might drastically affect the
overall incidence of clinically significant bronchoscopy findings,
which was 8.7% in our study. Performing bronchoscopy on all
6. Risk Factor: Age < 1 children with recurrent croup is not a viable option and a true
incidence will likely never be known.
Age < 1 No Odds Ratio
Although our study did not show a statistical association be-
Study Events Total Events Total OR 95% -CI W(fixed)
tween significant bronchoscopy findings and a history of GERD and
Jabbour 2011 5 17 3 64 8.47 [1.78; 40.30] 15.6%
Delaney 2015 2 16 4 87 2.96 [0.50; 17.74] 19.1%
Asthma/Allergies, these co-morbidities are often seen in conjunc-
Duval 2015 3 18 24 217 1.61 [0.43; 5.96] 53.7%
Tan 1992 1 3 1 3 1.00 [0.03; 29.81] 11.7%
tion with recurrent croup and warrant discussion. Our study
Fixed effect model 54 371 2.86 [1.28; 6.40] 100% showed a high incidence of both conditions, but should be viewed
with caution because most studies do not provide objective evi-
0.1 0.5 1 2 10
dence of either condition such as allergy testing or pH probe.
Additionally, there is no uniform reporting of GERD findings on
7. Risk Factor: Age < 3
bronchoscopy but instead studies report non-specific findings such
as “erythema,” “edema,” or “cobblestoning.” The study by Hodnett
Age < 3 No Odds Ratio
Study Events Total Events Total OR 95% -CI W(fixed) is one of the few to include objective data, including bron-
Jabbour 2011 6 42 2 39 3.08 [0.58; 16.29] 17.3% choalveolar lavage (BAL) and esophageal biopsy, attempting to
Delaney 2015 6 53 0 50 13.82 [0.76; 252.09] 4.4%
Duval 2015 16 93 11 142 2.47 [1.09; 5.61] 70.2%
Chun 2009 2 14 0 16 6.60 [0.29; 150.07] 3.8%
Tan 1992 2 5 0 1 2.14 [0.06; 77.54] 4.3%

Fixed effect model 207 248 3.22 [1.66; 6.27] 100% Fig. 2. Results of the meta-analysis showing a statistically significant association be-
tween significant bronchoscopy findings and History of Intubation, Inpatient Consul-
0.01 0.1 1 10 100 tation, Age <3, Age <1, and Prematurity. A History of Gastroesophageal Reflux Disease
and History of Asthma/Allergy did not reach statistical significance.
90 J.C. Hiebert et al. / International Journal of Pediatric Otorhinolaryngology 90 (2016) 86e90
diagnose GERD in patients with recurrent croup. Interestingly,
abnormal BAL and esophageal biopsy results did not correlate with
the presence of subglottic stenosis in their study. GERD likely plays
a role in the pathology of recurrent croup as several studies have
shown objective improvement in subglottic stenosis following
GERD treatment [5,13,14]. Some individual studies did show that
history of allergies was associated with significant bronchoscopy
findings [7] but Rankin et al. discouraged the use of RAST or com-
plement testing unless there is suspicion for a specific allergen or
angioedema as the cause for recurrent croup [13]. This high inci-
dence of GERD and Asthma/Allergies relative to the low incidence
of significant findings may provide support for initial conservative
medical management in recurrent croup patients who are at low-
risk for significant bronchoscopy findings.
The remaining analyzed risk factors of Intubation, Inpatient
Consultation, Age <3, Age <1, and Prematurity all showed associ-
ation with clinically significant findings on bronchoscopy. A pre-
vious history of intubation makes intuitive sense as a significant
risk factor because it is a known cause of subglottic stenosis and
subglottic cysts. Patients seen as inpatient consults with recent
diagnosis of croup likely have more severe symptoms and this may
indicate more significant findings such as airway stenosis and
obstruction. Younger patients and those with a history of prema-
turity have a smaller caliber airway with little reserve for
obstruction, putting them at greater risk for clinically significant
subglottic stenosis. Additionally, a history of prematurity may
confer additional risk as premature infants may have an increased
incidence of intubation.
The low incidence of clinically significant bronchoscopy findings
(8.7%) should also be interpreted in light of the fact that a signifi-
cant portion of patients did not undergo a surgical intervention but
only repeat bronchoscopy surveillance. Most studies did not have
clear indications for repeat bronchoscopy but appeared to be
mostly for subglottic stenosis. The necessity of repeat bronchos-
copy in these patients needs to be considered, especially if they are
asymptomatic.
Based on our study results, there should be a higher threshold
for bronchoscopy in recurrent croup patients, especially if they do
not have significant risk factors, and initial conservative medical
management of comorbid conditions should be considered in low
risk patients. Further prospective studies examining both obser-
vation and bronchoscopy cohorts would be useful in developing a
more robust treatment algorithm of these patients.
5. Conclusion
The majority of patients with recurrent croup will not have
clinically significant findings on bronchoscopy. The risk factors
most associated with clinically significant bronchoscopy findings
are Intubation, Inpatient Consultation, Age <3, Age <1, and Pre-
maturity. A History of GERD and Asthma/Allergy, though highly
prevalent in recurrent croup patients, are not associated with sta-
tistically significant bronchoscopy findings. These results should
guide physicians in selecting which recurrent croup patients are
most at risk for significant findings and therefore warrant
bronchoscopy.
Conflicts of interest
None.
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