International Journal of Pediatric Otorhinolaryngology 79 (2015) 749–752

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International Journal of Pediatric Otorhinolaryngology

journal homepage: www.elsevier.com/locate/ijporl

Pediatric patients with chronic cough and recurrent croup:

The case for a multidisciplinary approach
Melanie Greifer a,b, Maria T. Santiago a,c, Kalliope Tsirilakis a,c, Jeffrey C. Cheng a,d,
Lee P. Smith a,d,*
a
Hofstra North Shore LIJ School of Medicine, United States
b
Division of Gastroenterology and Nutrition, The Steven and Alexandra Cohen Children’s Medical Center of New York, United States
c
Division of Pulmonology, The Steven and Alexandra Cohen Children’s Medical Center of New York, United States
d
Division of Pediatric Otolaryngology, The Steven and Alexandra Cohen Children’s Medical Center of New York, United States

A R T I C L E I N F O A B S T R A C T

Article history: Objective: To evaluate the results of our multidisciplinary approach to recurrent croup and chronic
Received 20 December 2014 cough.
Received in revised form 4 March 2015 Methods: Retrospective chart review of all patients with recurrent croup and chronic cough managed at
Accepted 7 March 2015
a tertiary care children’s hospital by our Comprehensive Airway, Respiratory, and Esophageal (CARE)
Available online 14 March 2015
Team. Charts were reviewed for all patients who carried a diagnosis of recurrent croup or chronic cough.
Patients were excluded if they did not receive a full workup, including micro-direct laryngoscopy,
Keywords:
flexible and/or rigid bronchoscopy, bronchioalveolar lavage (BAL), and upper endoscopy with biopsies.
Croup
Cough
We reviewed the records for the presence of gastrointestinal complaints, abdominal pain and failure to
Recurrent thrive (FTT) and compared the children with documented esophagitis to the remaining children.
Airway Results: Forty patients met inclusion criteria. 53% had airway abnormalities; the most common was
Subglottic tracheomalacia, followed by enlarged adenoids. 38% had esophagitis (group 1) while 62% had normal
Aerodigestive esophageal biopsies (group 2). Among the children in group 1, 27% met criteria for eosinophilic
esophagitis (>15 eosinophils per high powered field). There was no significant difference between
groups 1 and 2 based on the presence of gastrointestinal complaints, abdominal pain and/or FTT
(p > 0.05). There was no significant difference between the groups based on the location or presence of
an airway abnormality (p > 0.05).
Conclusions: Children with recurrent croup and chronic cough may benefit from a multidisciplinary
approach to management. Our CARE Team approach led to a specific diagnosis in almost 95% of patients.
ß 2015 Elsevier Ireland Ltd. All rights reserved.

Introduction recurrent croup or chronic cough without a multidisciplinary

Pediatric patients with chronic cough and recurrent croup may
present a diagnostic and treatment dilemma. The etiology of
chronic cough and recurrent croup may result from disease
processes normally treated by pulmonologists, otolaryngologists
or gastroenterologists. Our institution has created a multidisci-
plinary team in order to efficiently address the unique needs of
these patients. We hypothesize that despite detailed history and
physical exams, it is difficult to determine a priori the cause of
* Corresponding author at: 430 Lakeville Road, New Hyde Park, New York 11042,
United States. Tel.: +1 516 470 7550; fax: +1 516 470 7814.
E-mail address: LSmith8@nshs.edu (L.P. Smith).
evaluation.
Croup is the most common cause of stridor in the febrile child. It
typically presents in children ages 6–36 months and is usually mild
and self-limited. Typical infectious croup should happen no more
than once or twice in child’s life. Children with a prolonged course,
multiple recurrent episodes, severe symptoms or age outside of the
typical range (6–36 months) would be considered to have atypical
or recurrent croup. Cough will often be associated with an acute
upper respiratory infection and usually resolves within one to
two weeks. A cough that persists beyond six weeks would be
considered a chronic cough.
Several recent studies have highlighted the diverse causes of
atypical croup [1,2]. These studies have highlighted the broncho-
scopic findings associated with recurrent or atypical croup and
even attempted to diagnose reflux disease based on a subjective

http://dx.doi.org/10.1016/j.ijporl.2015.03.007
0165-5876/ß 2015 Elsevier Ireland Ltd. All rights reserved.
750 M. Greifer et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 749–752

view of the airway. Unfortunately, neither of these studies Table 1

systematically evaluated their patients for reflux disease using
esophagoscopy or pH probe. We know from previous studies that
the subjective findings of inflammation on laryngoscopy do not
correlate well with actual pathological reflux disease [3]. Interest-
ingly, significant airway findings were identified in less than half of
patients who undergo bronchoscopy for recurrent croup
[1,2,4]. The remaining patients have no identifiable airway
abnormality and are thus left without an explanation following
bronchoscopy. Indeed, one recent study demonstrated abnormal
pH probe findings indicative of GERD in 60% of children with a
diagnosis of recurrent croup [5]. Others have demonstrated the
association between chronic cough and reflux or eosinophilic
esophagitis [6,7]. With this in mind, we set out to retrospectively
review the patients with chronic cough and recurrent croup that
were managed by the Comprehensive Airway, Respiratory and
Esophageal (CARE) Team at the Steven and Alexandra Cohen’s
Children Medical Center. The CARE Team is our multidisciplinary
service designed to collaboratively evaluate and manage patients
with complex challenges related to the upper aerodigestive tract.
Methods
A retrospective chart review of all patients seen by our CARE
Team physicians was performed between September 1, 2009 and
December 31, 2011. Patients who carried a diagnosis of either
chronic cough and/or recurrent croup were evaluated. Chronic
cough was defined as any cough present for greater than 6 weeks.
Patients with recurrent croup had three or more episodes of croup
in their lifetime, with each episode characterized by either the
presence of a bark-like cough or stridor. Patients were excluded if
they did not receive the full CARE team workup, which included
micro-direct laryngoscopy, flexible and/or rigid bronchoscopy and
upper endoscopy with biopsies. Bronchioalveolar lavage (BAL) was
performed at the time of bronchoscopy. If subglottic stenosis was
suspected on micro-direct laryngoscopy, the airway was formally
sized using the Cotton-Myer grading system.
We reviewed the charts for the presence of gastrointestinal
complaints at the time of the initial history, including vomiting and
spitting up (‘‘GER’’), abdominal pain and failure to thrive (FTT). We
then compared the children with biopsy proven esophagitis to the
remaining children to attempt to determine if physicians could
determine a priori based on history and physical whether
esophagitis is likely to be present on endoscopy. The two groups
were compared using T-test for statistical significance. Statistical
significance was defined as p < 0.05. The study was approved by
the institutional review board of the North Shore Long Island
Jewish Health System.
Results
We identified 40 patients who met inclusion criteria. Twenty-
one patients met the criteria for recurrent croup and 19 patients
had chronic cough as diagnosed by one of two pediatric
pulmonologists on our team (MS or KT). Mean age was
5.76  3.9 years. There were 29 males and 11 females. Twenty-one
patients (53%) had 33 airway abnormalities (Table 1). Ten patients
were diagnosed with two airway abnormalities and two patients had
three airway abnormalities. The most common diagnosis was
tracheomalacia, followed by enlarged adenoids.
Number and percent of airway diagnoses.
Airway diagnosis Number of abnormalities Percent
Tracheomalacia 10 30
Adenoid enlargement 8 24
Bronchomalacia 5 15
Subglottic stenosis 2 6
Laryngomalacia 2 6
Innominate artery compression 2 6
Tracheoesophageal fistula 1 3
Unilateral vocal cord immobility 1 3
Subglottic cyst 1 3
Tracheal bronchus 1 3
Total 33 100
their adenoids removed (including the three children who also had
their tonsils removed).
Fifteen patients (38%) had esophagitis noted on biopsy (group
1) while 25 (62%) had normal esophageal biopsies (group 2).
Among the children with biopsy proven esophagitis (group 1), 4/15
(27%) met criteria for eosinophilic esophagitis based on the
presence of greater than 15 eosinophils per high powered field.
There was no significant difference in ages between groups
1 and 2 (p > 0.05). There was no significant difference between
groups 1 and 2 based on the presence of ‘‘GER’’ related complaints,
abdominal pain and FTT (p > 0.05). There was no significant
difference between the groups based on the location or presence of
an airway abnormality (p > 0.05). Bacterial pathogens (abnormal
bronchoalveolar lavage) were found in 33% of the patients we
evaluated. BAL findings were also not significantly different
between the 2 groups (p > 0.05) (Table 2). The most common
pathogens were Staphyloccus aureus and Streptococcus
pneumoniae. Antibiotic therapy in these patients resulted in
clinical improvement of their chronic cough with decreased
episodes of croup. Overall, our multidisciplinary approach to
patients with recurrent croup and chronic cough led to a specific
diagnosis in approximately 95% of patients evaluated
Discussion
Recurrent croup and chronic cough are challenging conditions
to evaluate and manage. Pediatric patients with these complaints
may be referred to either pediatric pulmonologists and/or pediatric
otolaryngologists for evaluation. Interestingly, these complaints
may result from a variety of causes spanning at least three different
sub-specialty providers, the pediatric gastroenterologist, pulmo-
nologist and otolaryngologist. When a pediatrician evaluates a
child with recurrent croup or chronic cough, they must consider
the symptoms to determine how best to manage the complaints or
to whom to refer the patient. We evaluated the cause of recurrent
croup and chronic cough in patients who were seen by the
Table 2
Comparison between patients with biopsy proven esophagitis (Group 1) and
patients with no evidence of esophageal inflammation (Group 2). There was no
statistically significant difference between the two groups for any of the metrics
tested.
Group 1 Group 2

We did not routinely evaluate and document tonsillar Number Percent Number Percent
hypertrophy; however, three children underwent tonsillectomy GER complaints 7 47 7 28
at the time of the surgical procedure. Thus, these three children Abdominal pain 1 7 4 16
had concomitant and symptomatic tonsillar hypertrophy. There Failure to thrive 1 7 2 8
may have been other children with asymptomatic tonsillar Airway abnormality 7 47 14 56
Abnormal BAL 5 33 6 24
hypertrophy. All nine children with adenoid enlargement had
 M. Greifer et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 749–752
multidisciplinary aerodigestive team (CARE Team) at our tertiary
care referral children’s hospital.
Approximately half of our patients (21/40) had an airway
problem which was either primarily responsible or contributing to
their recurrent croup or chronic cough. Not surprisingly, tracheo-
malacia was the most common abnormality identified, followed by
adenoid hypertrophy and bronchomalacia. Children with tracheo-
and/or broncho-malacia commonly present with stridor, wheez-
ing, recurrent barking cough, or frequent respiratory infections.
The severity of the symptoms may correlate with the degree of
collapse. Conventional radiographic techniques are usually not
helpful and diagnosis of both of these conditions often requires
bronchoscopy, preferably flexible bronchoscopy performed under
spontaneous ventilation conditions. Before the diagnosis is
established, these children may be mistakenly treated for reactive
airway disease. When the diagnosis of tracheo-malacia is
established, medical (or rarely surgical) therapy may be very
effective at improving symptoms. Our patients with moderate to
severe primary tracheo- or broncho-malacia may be placed on a
medical regimen that includes bethanecol which improves
expiratory flow rates by stabilizing airway smooth muscle tone
[8]. Abnormal bacterial pathogens were found on bronchoalveolar
lavage in 33% of the patients. In these cases, antibiotic therapy
resulted in significant clinical improvement.
Approximately 9% of our patients had a significant subglottic
pathology identified, including either subglottic stenosis (6%) or
subglottic cyst (3%). Other studies have identified subglottic
airway abnormalities in a similar cohort of patients in more than
32% of cases [9–11]. Subglottic pathology in this series may be
slightly lower than represented by these conditions, since the
patients reviewed for this series were pre-selected to undergo a
multidisciplinary evaluation. If a child presented to the otolaryn-
gologist with recurrent croup and high suspicion for subglottic
pathology based on history, physical exam or fiberoptic exam, then
the otolaryngologist may have performed direct laryngoscopy and
rigid bronchoscopy without the involvement of the rest of the
multidisciplinary team and these patients would have been
excluded from the analysis. Subglottic pathology, including cysts
and stenosis, is often amenable to endoscopic treatment. Rigid
bronchoscopy performed by a well-trained pediatric otolaryngol-
ogist will assist in the diagnosis and management of these
conditions.
Twenty percent of patients had significant adenoid hypertrophy
and underwent adenoidectomy. Anecdotally, we believe that
removing the adenoids in these cases may decrease post-nasal drip
and improve nasal airflow, resulting in improvement in chronic
cough and recurrent croup symptoms. Previous studies have
demonstrated that addressing sinonasal symptoms will indepen-
dently improve pulmonary function in asthmatic patients. This
finding, in addition findings of various basic science studies has led
to the development of the unified airway concept [12]. Our
decision to perform adenoidectomy for those pediatric patients
with symptomatic adenoid hypertrophy was rooted in the unified
airway concept and based on our belief that it may improve
symptoms of recurrent croup and chronic cough; although this has
not been demonstrated in the literature and our study was not
designed to assess this intervention.
In more complex cases of recurrent croup and chronic cough,
we believe a multidisciplinary approach to management may
improve our ability to diagnose and treat these conditions. Our
data suggests that the pulmonologist is integral in evaluating and
managing malacia and performing BAL to determine the presence
of pathogenic bacteria. The otolaryngologist is required to evaluate
the adenoids, glottis and subglottis. The question may remain as to
what role the gastroenterologist plays in this multidisciplinary
approach? Our data suggests that gastrointestinal pathology may
751
be found in approximately one-third of patients with complaints of
recurrent croup and chronic cough. Indeed, other authors have
previously shown that gastroenterology pathology including reflux
disease may cause upper airway challenges [13]. Patients with
eosinophilic esophagitis may also present with complaints related
solely to the upper aerodigestive tract [14,15].
We examined our patients with recurrent croup and chronic
cough caused by a primary esophageal pathology to evaluate
whether an astute clinician could have suspected the presence of a
gastroenterology pathology based on history and physical alone.
Our data suggests that we were not able to predict whether a
primary gastroenterology pathology was contributing to the
symptoms. Other studies examining similar patients with recurrent
croup and chronic cough where a gastroenterologist did not
routinely perform esophagoscopy demonstrated that about half of
patients remain undiagnosed at the end of their evaluation; a
finding which is in line with our results [1,2,4]. Perhaps, in those
studies, a diagnosis may have been achieved if a full gastrointestinal
evaluation were performed. In our study, when a full multidisci-
plinary operative evaluation was performed, a diagnosis was
established in 95% of cases. Indeed, smaller studies have
demonstrated the presence of GERD by esophageal biopsy,
scintiscan, pH probe or barium swallow in over 47% of patients
with recurrent croup [11,16,17]. In this series, the diagnosis of
esophagitis was based on biopsy. We feel that this approach has the
benefit of being objective. It is possible that some children in our
series had laryngopharyngeal reflux disease without pathological
esophagitis and this could represent a limitation of this study.
The association between recurrent croup, gastroesophageal
reflux disease and airway hyper-responsiveness has previously
been reported. A large epidemiologic study revealed that asthmatic
patients with recurrent croup had significantly decreased expira-
tory flow rates in small to mid-sized airways compared to patients
who did not have recurrent croup [18]. Seventy-five percent of our
patients had a history of asthma and/or recurrent wheezing.
Kwong et al. questioned the association between recurrent croup
and asthma in a small retrospective review of 17 patients who
were not responding to asthma therapy and did not have
symptoms of wheezing or other symptoms of lower respiratory
tract disease [10]. Of these non-responders, 82% had endoscopic
findings suspicious for or consistent with laryngopharyngeal
reflux, although no patients had esophageal biopsies or pH probe
studies [10]. Indeed, instillation of synthetic gastric juice with a pH
1.4 causes severe mucosal irritation and necrosis of rabbit tracheas
demonstrating the potential for GERD to contribute to airway
pathology including subglottic stenosis [19].
It is worth noting, that not all of the patients evaluated by our
team receive operative intervention. Our unpublished data reveals
that about 40% of patients who receive an initial office visit from
two or more of our CARE Team providers go on to an operative
intervention. The cohort of patients who receive operative
intervention for recurrent croup and/or chronic cough would
likely skew toward those patients with more severe symptoms.
Two limitations of this study are its retrospective nature, and the
fact that we limited our review to patients who received a full
operative evaluation. In addition, while we were able to achieve a
diagnosis in 95% of patients, we can never know for sure if that
diagnosis is responsible for the clinical symptom. However, our
anecdotal experience is that the vast majority of patients improve
or respond to the treatment directed at the pathology we
identified.
Conclusions
Children with recurrent croup and chronic cough may benefit
from a multidisciplinary approach to management. Our CARE
752 M. Greifer et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 749–752
Team approach led to a specific diagnosis in almost 95% of patients.
Our data demonstrates that about half the patients will have
primary airway challenges treated by either the pulmonologist or
otolaryngologist. Approximately one-third of the patients will have
gastrointestinal pathology contributing to their symptoms, and our
data suggests that it is very difficult to predict a priori based on
history, which patients will have gastrointestinal pathology. We
advocate for a combined multidisciplinary approach for complex
patients with recurrent croup and chronic cough.
Funding
No author has any financial disclosures to make. No grants were
used in the funding of this manuscript
Conflict of interest
None.
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