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Correlation of Findings at Direct Laryngoscopy and Bronchoscopy With Gastroesophageal Reflux Disease in Children
A Prospective Study
Michele M. Carr, DDS, MD, MEd, FRCSC;
Mark L. Nagy, MD;
Michael P. Pizzuto, MD;
Christopher P. Poje, MD;
Linda S. Brodsky, MD
Arch Otolaryngol Head Neck Surg. 2001;127:369-374.
ABSTRACT
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Objective To correlate direct laryngoscopic and bronchoscopic findings with the
presence of positive test results for gastroesophageal reflux disease (GERD)
in children.
Design Prospective collection of structured data.
Setting An academic pediatric otolaryngology department.
Patients Seventy-seven consecutive patients who underwent direct laryngoscopy
and bronchoscopy between June and October 1999.
Interventions During direct laryngoscopy and bronchoscopy, descriptions of 7 laryngeal
and 6 cricotracheal findings were recorded on a 3-point scale (ie, absent,
mild, or severe). Medical records were later reviewed to obtain results of
the following tests, if they were part of the record: gastric scintiscan,
24-hour pH probe monitoring, upper gastrointestinal tract series, and esophageal
biopsy.
Main Outcome Measures Correlation of mucosal abnormalities with the presence or absence of
a positive test result for GERD.
Results Fifty (65%) of 77 patients had GERD diagnosed with at least 1 positive
test result, 21 (27%) had no clinical symptoms and no positive GERD test results,
and 5 (7%) had clinical symptoms but no positive test results. There were
significant differences for total laryngeal and cricotracheal scores (P<.001) between the groups with positive and negative
results. Significant differences were as follows: in the larynx—large
lingual tonsil (P<.001), postglottic edema (P<.001), arytenoid edema (P<.001),
ventricle obliteration (P = .03), and true vocal
fold edema (P = .001), and in the cricotracheal region—general
edema and erythema (P = .003) and blunting of the
carina (P<.001). Severe arytenoid edema, postglottic
edema, or enlargement of lingual tonsil were pathognomonic of GERD.
Conclusion Many direct laryngoscopic and bronchoscopic findings correlate well
with the diagnosis of GERD as determined by using other tests.
INTRODUCTION
MANY TESTS are useful to diagnose pathologic gastroesophageal reflux
disease (GERD). Even in the best hands, each test has a significant false-negative
rate.1, 2 The use of airway endoscopy
in children with extraesophageal reflux has not been clearly established although
it is well accepted that adults with GERD may have posterior laryngeal edema
and erythema. This study compared airway endoscopic findings in pediatric
patients with and without GERD to examine the usefulness in diagnosing GERD.
PATIENTS AND METHODS
All patients who underwent direct laryngoscopy and bronchoscopy (DLB)
in the Department of Pediatric Otolaryngology, Children's Hospital of Buffalo,
Buffalo, NY, between June and October 1999 had descriptions of endoscopic
appearance recorded on a checklist. The checklist was developed from a retrospective
analysis of endoscopic findings in a series of patients positive for GERD,
reported elsewhere.4 Findings were divided
into a laryngeal group, which could be assessed by direct laryngoscopy or
flexible laryngsocopy, and a cricotracheal group, which required bronchoscopy
for evaluation. There were 7 laryngeal factors and 6 cricotracheal factors,
each graded as absent, mild, or severe. A mild finding was assigned 1 point;
a severe finding was assigned 2 points. A list of these factors and severity
definitions is given in Table 1.
Some representative photographs are shown in Figure 1. Points were summed weighing each factor equally to determine
laryngeal and cricotracheal scores, with the total score being the sum of
these 2 scores. In most cases, evaluators were not blinded to the patient's
history.
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Table 1. Anatomic Factors Evaluated With Endoscopy
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A, Severe lingual tonsil hypertrophy. The laryngoscope is displaced
anteriorly to show the lingual tonsil filling the vallecula. B, Severe postglottic
edema. The posterior laryngeal mucosa is more than twice the usual width.
C, Arytenoid edema with loss of normal contour. D, Widespread tracheal cobblestoning.
E, Severe carinal blunting.
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Five patients were scored separately by 2 evaluators (M.M.C. and L.S.B.)
using videotape and photographs to establish the reliability of the scoring
system. The coefficient of correlation for the presence or absence of factors
as judged in the small group of patients by 2 observers blinded to the other's
scoring was 0.94 showing good reliability.
The following information was recorded for all patients: sex, age at
bronchoscopy, reason for bronchoscopy, and whether a tracheotomy was performed.
Medical records were reviewed at the study end point for the following results:
gastric scintiscan, an upper gastrointestinal tract series, 24-hour pH probe
monitoring, and esophageal biopsies. Any test positive for GERD resulted in
the patient being included in the GERD-positive (GERD[+]) group. Patients
who did not have symptoms suggestive of GERD and no positive test results
composed the GERD-negative (GERD[-]) group. Patients who had GERD symptoms
but no positive test results composed the GERD indeterminant group. Patients
with tracheal mucosal abnormalities underwent bronchial washings for the presence
of lipid-laden macrophages and elevated amylase levels.
Data were entered into an Excel 97 spreadsheet (Microsoft Corporation,
Seattle, Wash) and analyzed with SPSS 8.0 (SPSS Inc, Chicago, Ill). Comparisons
were made between the GERD(+) and GERD(-) groups for the number of laryngeal
and cricotracheal findings, the number of mild and severe findings, and scores
for each individual factor. Age, sex, and presence of tracheotomy were also
compared. For continuous data, t tests were used;
for categorical data, the Mann-Whitney tests were used.
RESULTS
Seventy-seven patients underwent DLB during the study period. There
were 51 male and 26 female patients who had an average age of 4.2 years (age
range, 0.01-15.1 years). Twenty-four (31%) had a tracheotomy present. Reasons
for endoscopy are given in Table 2.
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Table 2. Primary Indication for Endoscopy*
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Fifty patients (65%) had at least 1 positive GERD test result and were
included in the GERD(+) group (Table 3).
Twenty-one patients (27%) had no positive tests and were believed to be GERD
free on clinical grounds; they composed the GERD(-) group. Six patients
had no positive GERD test results but were believed to have GERD symptoms;
they made up the indeterminant group. The distribution of tracheotomies was
similar between the GERD(+) and GERD(-) groups. The average age of the
patient was 4.2 years (age range, 0.01-15.1 years), with the same age distribution
among groups. Overall, the incidence of GERD in this population of children
undergoing DLB was 65%, 69% in those younger than 2 years, and 63% in those
older than 2 years.
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Table 3. Test Results of 50 Pediatric Patients Who Had GERD Diagnosed
With at Least 1 Positive Test
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No statistical difference was noted between the groups for the findings
of lipid-laden macrophages and elevated amylase levels from tracheal washings,
which represents lower power to detect a difference owing to small sample
size. None of the patients in the GERD(-) group had positive tracheal
washings, but only 3 patients had these washings done. In the GERD(+) group,
27 patients had tracheal washings sent to the laboratory for analyses; the
results for 12 patients (44%) were positive for lipid-laden macrophages; 15
patients (55%) had elevated amylase levels.
The average number of laryngeal and cricotracheal findings is summarized
in Table 4. In all cases, the
number of findings was greater in the GERD(+) group than in the GERD(-)
group, and the difference was statistically significant.
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Table 4. Average Total Number and Scores for Direct Laryngeal and Cricotracheal
Findings in the GERD (+) and GERD (-) Groups*
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For laryngeal and cricotracheal factors, average scores on each were
higher for the GERD(+) group than for the GERD(-) group (except for
vocal fold lesions), and 5 of 7 laryngeal factors and 2 of 6 cricotracheal
factors were significantly different between these groups (Table 5).
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Table 5. Percentage With Direct Laryngeal and Cricotracheal Findings
and Average Scores for GERD(+) and GERD(-) Groups and P Values for Comparison Between Average Scores*
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The presence of either severe arytenoid edema, severe postglottic edema,
or a severely enlarged lingual tonsil was always associated with GERD. Twenty-five
(50%) of the 77 patients with GERD had at least 1 severe finding from among
these 3 factors. Forty-three (86%) of the 77 patients with GERD had at least
2 of these findings (mild or severe) present, and 49 patients (98%) had at
least 1 factor. Seventeen (81%) of the patients who were GERD(-) had
only 1 or none of these findings present, and none of these patients had severe
scores for these factors.
Calculations of sensitivity and specificity were done. The presence
of at least 1 severe finding among lingual tonsil enlargement, postglottic
edema, or arytenoid edema had a sensitivity of 50% and a specificity of 100%.
Finding at least 2 of these at a mild or severe level had a sensitivity of
87.5% and a specificity of 68%. A laryngeal score of 4 or more had a sensitivity
of 74% and a specificity of 81%. A cricotracheal score of 2 or more had a
sensitivity of 82% and a specificity of 67%. A total score of 7 or more had
a sensitivity of 76% and a specificity of 86%.
The small indeterminant group (n = 6) was compared pairwise with the
GERD(+) and GERD(-) groups. There were no statistically significant
differences between the indeterminant group and the GERD(+) group. However,
the following several factors were different (P<.05)
between the indeterminant group and the GERD(-) group: the total number
of laryngeal and cricotracheal findings, the number of severe cricotracheal
findings, and findings of posterior laryngeal edema, arytenoid edema, generalized
tracheal edema, and blunt carina. For these factors, and most of the others
(except subglottic stenosis and ventricular obliteration), the indeterminant
group had higher scores than did the GERD(-) group. One patient in the
indeterminant group had significant levels of lipid-laden macrophages in a
tracheal aspirate, suggesting aspiration.
COMMENT
Posterior laryngitis, ranging from erythema and edema to pachyderm changes
in the interarytenoid region, and from contact granuloma formation to diffuse
vocal fold edema,5 has had a recognized association
with GERD in adults since Cherry and Margulies6
reported on this topic in 1968. The mucosa in this region does not have defenses
against acid exposure and brief acidifications can result in significant pathology.7 Adult patients with GERD and laryngeal symptoms (ie,
dysphonia, cough, globus, throat clearing, or sore throat) had significantly
more proximal esophageal acidification than did patients who had GERD with
no laryngeal symptoms, but only 40% of those patients with GERD laryngitis
had laryngeal findings on flexible laryngsocopy.8
This may be related to variable definitions of posterior laryngitis. In another
study,5 75% of the adult patients with symptomatic
posterior laryngitis had pharyngeal acid reflux despite being free of typical
GERD symptoms. Matthews et al9 recently reported
the presence of pharyngeal acid reflux in all of a group of 24 children with
laryngomalacia. Some of their patients would not have been considered to have
pathologic condition using North American Society of Pediatric Gastroenterology
and Nutrition10 criteria for evaluating pH
monitoring since they had very few episodes of reflux. This evidence supports
the concept that even a small amount of pharyngeal acid can cause edema of
the posterior larynx and resultant symptoms. In the study by Deveney et al,11
gastroesophageal reflex–related posterior laryngitis and hoarseness
resolved in 73% of the adult patients within 3 months of Nissen fundoplication,
showing a relationship with the resolution of reflux. Our group of pediatric
patients shows a very strong correlation between posterior laryngeal pathology
and GERD; virtually all of the patients with GERD(+) exhibited this.
There are few reports of tracheal findings in patients with GERD. In
this group of patients with respiratory symptoms, tracheal findings of GERD
are probably more common than in a group without such symptoms. We found that
diffuse tracheal edema including a blunt carina was associated with GERD.
The mechanism of this may be repeated microaspiration of refluxate.12 About half of those in the GERD(+) group who had
tracheal aspirates examined for lipid-laden macrophages or elevated amylase
levels were positive, suggesting aspiration in about a quarter of this group.
In this group of pediatric patients undergoing DLB, we found the incidence
of GERD to be 65%, much higher than that reported by Altman et al13 in their group of 174 children with congenital airway
abnormalities who required hospitalization. They reported an incidence of
28%. We suspect that we may be still be underdiagnosing because of the limitations
of existing GERD tests. The endoscopic appearance in most of our indeterminant
cases was similar to that found in our GERD(+) group, suggesting that they
may in fact have GERD with secondary airway symptoms. This study does not
give evidence that allows us to conclude that GERD has a causal relationship
with airway problems, but it does allow us to conclude that GERD is present
in a significant proportion of pediatric patients with airway symptoms, more
than we would expect by chance.
How useful is DLB to diagnose GERD? Commonly used tests for diagnosing
GERD include barium esophagram, gastric scintiscan, 24-hour pH monitoring,
and esophageal biopsy. Each has its limitations and drawbacks. Barium esophagram
had a sensitivity of 86% and a specificity of 69%, extended 24-hour pH monitoring
had a sensitivity of 88% and specificity of 94%, and esophagoscopy had a sensitivity
of 54% and a specificity of 100% in one study.14
Compare these with the best values for gastric scintiscans with a sensitivity
of 79% and a specificity of 93% when any reflux episode is considered a positive
test, and where a true-positive test is defined according to 24-hour pH monitoring.15 In our study, finding at least 1 instance of severe
arytenoid edema, postglottic edema, or enlargement of lingual tonsil was always
associated with the presence of GERD, but only half of the patients displayed
at least 1 of these findings. Finding at least 2 of these at a mild or severe
level had a sensitivity of 87.5% and a specificity of 68%. Overall, laryngeal
appearance is very useful in the diagnosis of GERD in patients with airway
symptoms, but less useful to rule it out; this makes sense since some patients
may not have refluxate up to the level of the larynx, but may have reflex-mediated
respiratory symptoms, such as bronchospasm, laryngospasm, central apnea, or
bradycardia.16 Direct laryngoscopy and bronchoscopy
have the drawback of requiring a general anesthetic, but these pediatric patients
with reports of respiratory symptoms usually require this study to characterize
their disease. The findings with the strongest association with GERD can be
evaluated with flexible laryngsocopy done at the bedside. We believe that
careful observation of the airway appearance can provide strong evidence to
make a diagnosis of GERD in pediatric patients with airway symptoms.
CONCLUSIONS
In summary, we conclude that 65% of children in this group who underwent
DLB for any reason ultimately had GERD diagnosed by having at least 1 positive
traditional test. There were significant differences for laryngeal and cricotracheal
abnormalities between the GERD(+) and GERD(-) groups. Laryngeal findings
associated with GERD were as follows: large lingual tonsil (P<.001), postglottic edema (P<.001),
arytenoid edema (P<.001), ventricle obliteration
(P = .03), and true vocal fold edema (P = .001). Severe arytenoid edema, postglottic edema, or enlargement
of the lingual tonsil were pathognomonic of GERD. Cricotracheal findings associated
with GERD were general edema and erythema (P = .003)
and blunting of the carina (P<.001). Laryngeal
findings associated with GERD can be assessed with flexible laryngoscopy.
Bronchoscopy is less likely to have a high yield of information supporting
a diagnosis of GERD except in the most severe cases. The incidence of GERD
is high enough in children with airway symptoms that these specific mucosal
abnormalities should be evaluated in each case.
AUTHOR INFORMATION
Accepted for publication September 22, 2000.
From the Department of Pediatric Otolaryngology, Children's Hospital
of Buffalo, Buffalo, NY. Dr Carr is now with the Department of Otolaryngology,
Toronto General Hospital, Toronto, Ontario.
Corresponding author: Michele M. Carr, DDS, MD, MEd, FRCSC, EN7-238,
Department of Otolaryngology, Toronto General Hospital, 200 Elizabeth St,
Toronto, Ontario, Canada M5G 2C4 (e-mail: mm.carr{at}utoronto.ca).
REFERENCES
| |
1. Orenstein S. Controversies in pediatric gastroesophageal reflux. J Pediatr Gastroenterol Nutr. 1992;14:338-348.
ISI
| PUBMED
2. Meyers WF, Roberts CC, Johnson DG, Herbst JJ. Value of tests for evaluation of gastroesophageal reflux in children. J Pediatr Surg. 1985;20:515-520.
FULL TEXT
|
ISI
| PUBMED
3. Boyle JT. Gastroesophageal reflux in the pediatric patient. Gastroentol Clin North Am. 1989;18:315-337.
4. Carr MM, Nguyen A, Poje C, Pizzuto M, Nagy M, Brodsky L. Correlation of findings on direct laryngoscopy and bronchoscopy with
presence of extraesophageal reflux disease. Laryngoscope. 2000;110:1560-1562.
FULL TEXT
|
ISI
| PUBMED
5. Ulualp SO, Toohill RJ, Hoffmann R, Shaker R. Pharyngeal pH monitoring in patients with posterior laryngitis. Otolaryngol Head Neck Surg. 1999;120:672-677.
FULL TEXT
|
ISI
| PUBMED
6. Cherry J, Margulies SI. Contact ulcer of the larynx. Laryngoscope. 1968;78:1937-1940.
FULL TEXT
|
ISI
| PUBMED
7. Delahunty JE, Cherry J. Experimentally produced vocal cord granulomas. Laryngoscope. 1968;78:1941-1947.
FULL TEXT
|
ISI
| PUBMED
8. Jacob P, Kahrilas PJ, Herzon G. Proximal esophageal pH-metry in patients with "reflux laryngitis." Gastroenterology. 1991;100:305-310.
ISI
| PUBMED
9. Matthews BL, Little JP, Mcguirt WF Jr, Koufman JA. Reflux in infants with laryngomalacia: results of 24-hour double-probe
pH monitoring. Otolaryngol Head Neck Surg. 1999;120:860-864.
FULL TEXT
|
ISI
| PUBMED
10. Colletti RB, Christie DL, Orenstein SR. Indications for pediatric esophageal pH monitoring: a medical position
statement of the North American Society for Pediatric Gastroenterology and
Nutrition. Available at:
http://www.naspgn.org/ph_probe.htm.
Accessed November 9, 1999.
11. Deveney CW, Benner K, Cohen J. Gastroesophageal reflux and laryngeal disease. Arch Surg. 1993;128:1021-1027.
FREE FULL TEXT
12. Contencin P, Narcy P. Gastropharyngeal reflux in infants and children: a pharyngeal pH monitoring
study. Arch Otolaryngol Head Neck Surg. 1992;118:1028-1030.
FREE FULL TEXT
13. Altman KW, Wetmore RF, Marsh RR. Congenital airway abnormalities in patients requiring hospitalization. Arch Otolaryngol Head Neck Surg. 1999;125:525-528.
FREE FULL TEXT
14. Meyers WF, Roberts CC, Johnson DG, Herbst JJ. Value of tests for evaluation of gastroesophageal reflux in children. J Pediatr Surg. 1985;20:515-520.
15. Seibert JJ, Byrne WJ, Euler AR. Gastric emptying in children: unusual patterns detected by scintigraphy. AJR Am J Roentgenol. 1983;141:49-51.
FREE FULL TEXT
16. Orenstein SR, Orenstein DM. Gastroesophageal reflux and respiratory disease in children. J Pediatr. 1988;112:847-858.
FULL TEXT
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ISI
| PUBMED
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