ORIGINAL ARTICLE. Correlation of Findings at Direct Laryngoscopy and Bronchoscopy With Gastroesophageal Reflux Disease in Children
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1 Correlation of Findings at Direct Laryngoscopy and Bronchoscopy With Gastroesophageal Reflux Disease in Children A Prospective Study ORIGINAL ARTICLE Michele M. Carr, DDS, MD, MEd, FRCSC; Mark L. Nagy, MD; Michael P. Pizzuto, MD; Christopher P. Poje, MD; Linda S. Brodsky, MD 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 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. Arch Otolaryngol Head Neck Surg. 2001;127: 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. 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. 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, years). Twenty-four (31%) had a tracheotomy present. Reasons for endoscopy are given in Table 2. Fifty patients (65%) had at least 1 positive GERD test result and were included in the GERD(+) group (Table 3). Twentyone 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, years), with the same age distribution among groups. Overall, the incidence of GERD in 369
2 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 the Figure. 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. 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. this population of children undergoing DLB was 65%, 69% in those younger than 2 years, and 63% in those older than 2 years. 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. 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). 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. 370
3 Table 1. Anatomic Factors Evaluated With Endoscopy Anatomic Region Mild Finding Severe Finding Larynx and Supraglottic Regions Lingual tonsil Enlarged but vallecula visible Fills vallecula Postglottic edema and erythema 1.5 to 2 times normal anteroposterior width 2 Times normal anteroposterior width Arytenoid edema and erythema Loss of contour of arytenoid area Obvious swelling or redundancy of arytenoid mucosa Ventricle Constricted Effaced True vocal fold edema Loss of whiteness of true vocal fold or loss Obvious edema of sharpness of edge Vocal fold lesions Unilateral Bilateral Posterior cobblestoning Few areas seen Confluent 2cm Cricotracheal Region General edema and erythema Rings visible but red or decreased contour Loss of ring contour throughout Cobblestoning Few scattered areas Throughout Subglottic stenosis Size 50% of diameter Size 50% of diameter Blunt carina Loss of carina sharpness Carina round Increased secretions Localized to 1 bronchi Generalized Stomal granuloma Size 50% of lumen Size 50% lumen or friable A B C D E 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. 371
4 Table 2. Primary Indication for Endoscopy* Reason GERD(+) COMMENT GERD( ) Indeterminant Dysphonia Noisy breathing Tracheostomy surveillance Chronic cough Desaturations Tracheal or subglottic stenosis Bronchial biopsy Recurrent pneumonia Laryngotracheal reconstruction follow-up Vocal fold paralysis surveillance Respiratory papillomatosis Airway trauma Total *GERD(+) indicates pediatric patients who tested positive for gastroesophageal reflux disease (GERD); GERD( ), pediatric patients who tested negative for GERD; and Indeterminant, pediatric patients who had GERD symptoms but no positive test result for GERD. Table 3. Test Results of 50 Pediatric Patients Who Had GERD Diagnosed With at Least 1 Positive Test Type of Test* Finding: Abnormal Finding: Normal Upper gastrointestial tract series 9 6 Scintiscan Gastric emptying Reflux h ph monitoring 17 3 Esophageal biopsy *The criteria for positive test result for each of the tests were as follows: upper gastrointestinal tract series, reflux evident; scintiscan; gastric emptying of 25% or less or evidence of reflux; 24-h/pH monitoring, any drop in ph of 4 or less in the upper probe or lower probe ph drops of 4 or less according to the criteria of Boyle 3 or an esophageal biopsy specimen showing basal cell hyperplasia, papillary elongation, and/or an inflammatory cell infiltrate. 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 Margulies 6 reported on this topic in 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 Table 4. Average Total Number and Scores for Direct Laryngeal and Cricotracheal Findings in the GERD (+) and GERD ( ) s* Factor GERD(+) GERD( ) P No. of larynx findings No. of mild larynx findings No. of severe larynx findings Total laryngeal score No. of cricotracheal findings No. of mild cricotracheal findings No. of severe cricotracheal findings Total cricotracheal score Overall scores *GERD(+) indicates pediatric patients who tested positive for gastroesophageal reflux disease (GERD); GERD( ), pediatric patients who tested negative for GERD. Statistical significance was set at P.05 for t (continuous data) and Mann-Whitney (categorical data) tests. reflux despite being free of typical GERD symptoms. Matthews et al 9 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 Nutrition 10 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 lipidladen 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 al 13 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 372
5 Table 5. Percentage With Direct Laryngeal and Cricotracheal Findings and Average Scores for GERD(+) and GERD( ) s and P Values for Comparison Between Average Scores* GERD(+) (n = 50) GERD( ) (n = 21) Parameter % Present Average Score % Present Average Score P Larynx and Supraglottic Regions Lingual tonsil Postglottic edema and erythema Arytenoid edema and erythema Ventricle obliteration True vocal fold edema Vocal fold lesion Hypopharyngeal cobblestoning Cricotracheal Region General edema and erythema Cobblestoning SGS Blunt carina Increased secretions Stomal granuloma (N = 24) 38 (n = 21) (n = 5) *GERD(+) indicates pediatric patients who tested positive for gastroesophageal reflux disease (GERD); GERD( ), pediatric patients who tested negative for GERD. Statistical significance was set at P.05 for t (continuous data) and Mann-Whitney (categorical data) tests. 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. Accepted for publication September 22, 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 ( mm.carr@utoronto.ca). 373
6 REFERENCES 1. Orenstein S. Controversies in pediatric gastroesophageal reflux. J Pediatr Gastroenterol Nutr. 1992:14: Meyers WF, Roberts CC, Johnson DG, Herbst JJ. Value of tests for evaluation of gastroesophageal reflux in children. J Pediatr Surg. 1985;20: Boyle JT. Gastroesophageal reflux in the pediatric patient. Gastroentol Clin North Am. 1989;18: 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;10: Ulualp SO, Toohill RJ, Hoffmann R, Shaker R. Pharyngeal ph monitoring in patients with posterior laryngitis. Otolaryngol Head Neck Surg. 1999;120: Cherry J, Margulies SI. Contact ulcer of the larynx. Laryngoscope. 1968;78: Delahunty JE, Cherry J. Experimentally produced vocal cord granulomas. Laryngoscope. 1968;78: Jacob P, Kahrilas PJ, Herzon G. Proximal esophageal ph-metry in patients with reflux laryngitis. Gastroenterology. 1991;100: 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: 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: ph_probe.html. Accessed November 9, Deveney CW, Benner K, Cohen J. Gastroesophageal reflux and laryngeal disease. Arch Surg. 1993;128: Contencin P, Narcy P. Gastropharyngeal reflux in infants and children: a pharyngeal ph monitoring study. Arch Otolaryngol Head Neck Surg. 1992;118: Altman KW, Wetmore RF, Marsh RR. Congenital airway abnormalities in patients requiring hospitalization. Arch Otolaryngol Head Neck Surg. 1999:125: Meyers WF, Roberts CC, Johnson DG, Herbst JJ. Value of tests for evaluation of gastroesophageal reflux in children. J Pediatr Surg. 1985;20: Seibert JJ, Byrne WJ, Euler AR. Gastric emptying in children: unusual patterns detected by scintigraphy. AJR Am J Roentgenol. 1983;141: Orenstein SR, Orenstein DM. Gastroesophageal reflux and respiratory disease in children. J Pediatr. 1988;112:
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