Pharyngeal pH monitoring in patients with posterior


OBJECTIVE: To evaluate the diagnostic value of 3site 24-hour ambulatory pH monitoring in patients
with posterior laryngitis (PL) and the prevalence of
esophageal abnormalities in this patient group.
METHODS: Twenty patients with PL and 17 healthy
volunteers were studied as controls. Control subjects
had transnasal esophagogastroduodenoscopy
(T-EGD) and ambulatory pH monitoring. Patients
underwent T-EGD, ambulatory pH monitoring, and
barium esophagram.
RESULTS: T-EGD documented no abnormality in
controls. Esophagitis was present in 2 PL patients,
and hiatal hernia in 3. Ambulatory pH monitoring
showed that 15 PL patients and 2 controls exhibited
pharyngeal acid reflux. Barium esophagram documented gastroesophageal reflux in 5 PL patients.
However, none of these barium reflux events
reached the pharynx. All PL patients with barium
esophagram evidence of gastroesophageal reflux
also showed pharyngeal acid reflux by pH monitoring.
CONCLUSION: Pharyngeal acid reflux is more
prevalent in patients with PL than in healthy controls. Patients with PL infrequently have esophageal
sequelae of reflux disease. Ambulatory 24-hour
simultaneous 3-site pharyngoesophageal pH monitoring detects gastroesophagopharyngeal acid
reflux events in most patients with PL. (Otolaryngol
Head Neck Surg 1999;120:672-7.)

improved flexible and rigid instruments to perform
diagnostic laryngoscopy along with videostroboscopy,
abnormalities of the posterior larynx have been
increasingly recognized. These patients may report
chronic or intermittent hoarseness,1-4 voice fatigue and
breaks,3 frequent throat clearing,2,5,6 sore throat,2,3,7
excessive mucus8 or postnasal drip,8-10 cough,3,5 dyspnea,11 or dysphagia.5 Laryngeal examination may
reveal erythema and edema of arytenoids,8 hypertrophic mucosa of interarytenoid area,2,3 or pachyderma laryngis.1,2 Associated true vocal cord problems
such as contact ulcer or granuloma,6 edema and erythema,2,3 vocal cord nodules,8 Reinke’s edema,8 leukoplakia,8 and laryngotracheal stenosis11 may accompany
the PL. The typical symptoms of gastroesophageal
reflux disease (GERD), such as heartburn, regurgitation, and water brash, occur in a minority of patients
with PL.5,10 Therefore the possible role of refluxed
gastric acid in the pathogenesis of laryngeal disorders
may easily be overlooked.
Patients with suspected reflux-induced laryngeal
lesions have been evaluated for reflux disease by various
modalities such as upper gastrointestinal endoscopy,
barium esophagram, and ambulatory pH monitoring. In
this study we report the combined findings of upper
gastrointestinal endoscopy, barium esophagram, and
24-hour pharyngoesophageal pH monitoring in a group
of patients with subjective and objective findings suggestive of reflux-induced laryngitis.

Posterior laryngitis (PL) until recently was not well


recognized. Examiners frequently keyed on the true
vocal cords during evaluation. With the advent of

Twenty consecutive patients (13 male, 7 female) with PL,
aged 17 to 78 years (47 ± 4 yrs), and 17 healthy volunteers (5
male, 12 female), aged 19 to 85 years (46 ± 6 yrs), were studied. Studies were approved by the Human Research Review
Committee of the Medical College of Wisconsin, and participants gave written, informed consent before their studies. All
PL patients and healthy volunteers filled out a detailed health
questionnaire before their studies.
Healthy volunteers were recruited by advertisement and
did not have any esophageal or laryngeal symptoms. In addition, they underwent unsedated transnasal pharyngoesophagogastroduodenoscopy (T-EGD) and did not exhibit any
pathologic symptoms.
PL patients reported intermittent hoarseness, chronic
hoarseness, frequent throat clearing, sore throat, dyspnea, or

From the Departments of Medicine (Division of Gastroenterology and
Hepatology) (Drs Ulualp and Shaker), Otolaryngology and Human
Communication (Drs Ulualp, Toohill, and Shaker), and Biostatistics (Dr Hoffmann), Medical College of Wisconsin.
Supported in part by NIH grant no. R01 DK25731.
Presented at the Annual Meeting of the American Academy of
Otolaryngology–Head and Neck Surgery, San Francisco, CA,
September 7-10, 1997.
Reprint requests: Reza Shaker, MD, Professor of Medicine, Division
of Gastroenterology and Hepatology, Froedtert Memorial Lutheran
Hospital, 9200 W Wisconsin Ave, Milwaukee, WI 53226.
Copyright © 1999 by the American Academy of Otolaryngology–
Head and Neck Surgery Foundation, Inc.
0194-5998/99/$8.00 + 0 23/1/91774

The probes were secured to the . Videostroboscopy Barium esophagram T-EGD esophageal findings Pharyngeal acid exposure 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 PL. GER was said to be present when barium was observed to fill the esophageal lumen at least 3 cm. In addition to the above findings. VFP.12 T-EGD could not be performed in the remaining 5 PL patients because of severe nasal septal deviation (2 patients). videostroboscopy also documented vocal cord nodules in 4 patients. pachyderma laryngis. HH GER(+). LTS PL. PL patients were sequentially asked to perform the following tasks: (1) coughing. The gross appearance of esophageal mucosa was evaluated. VCN PL PL. All 20 PL patients had a standard barium esophagram findings. and distal esophagus (5 cm above the lower esophageal sphincter). AM. hyperplastic interarytenoid tissue. LTS PL. laryngotracheal stenosis. HH. The ambulatory pH studies were done with pH recording systems. (2) leg raising. The more patent side of the nasal cavity was determined by nasal examination and was anesthetized by passing a cotton-tipped swab covered with Xylocaine gel. direct examination of the stomach and retroflexed examination of the gastroesophageal junction were followed by the evaluation of the bulb and second portion of the duodenum. Lake Success. Provocative maneuvers involved exercises that increase the intra-abdominal pressure. Irving. For this. and vasovagal reaction (2 patients). AM. or erythema of the entire larynx. If no GER event was observed. HH AM GER(–) AM GER(–) GER(+). Radiographs and videofluoroscopic recordings were obtained. abnormal motility. HH GER(–) GER(–) GER(–) No abnormality No abnormality No abnormality No abnormality No abnormality No abnormality No abnormality HH No abnormality No abnormality No abnormality — HH. VFP PL. T-EGD was done with an Olympus GIF-N30 endoscope (Olympus Corp. Fifteen of the 20 PL patients underwent T-EGD. Vocal cord nodules. Spontaneous gastroesophageal reflux (GER) events throughout the examination were evaluated. NY) with volunteers or PL patients sitting upright in a chair. TX). with a single recording site and another with 2 recording sites that were 10 cm apart (Synectics Medical Inc. Then the endoscope was passed through the nose to the nasopharynx and pharynx. HH GER(+) AM GER(+). and (3) the Valsalva maneuver. approximately 4 to 5 cm below the upper esophageal sphincter).14 Barium esophagram reports included the presence or absence of GER. VCN PL GER(–) GER(–) GER(–) GER(–) GER(–) GER(–) GER(–) GER(+). The larynx was observed. In cases of narrow passage caused by hypertrophied turbinates. 2 puffs of a nasal decongestant were applied. LTS PL PL PL. LTS PL PL PL PL PL PL. All PL patients and healthy volunteers were studied for occurrence of pharyngeal acid reflux by 3-site 24-hour pharyngoesophageal pH monitoring. VCN PL PL. and glottal closure during swallowing and phonation was evaluated. Esophagitis HH No abnormality Esophagitis — — — — Positive Positive Positive Negative Positive Negative Negative Positive Positive Negative Negative Positive Positive Positive Positive Positive Positive Positive Positive Positive VCN. and the provocative maneuver or maneuvers performed to observe GER. hiatal hernia. Barium swallows were performed with a total of 200 to 250 mL of barium and water mixture. technical difficulty in intubating the esophagus (1 patient). In all cases the pharynx was anesthetized with Cetacaine spray. LTS. and laryngotracheal stenosis in 5 patients (Table 1). erythema of interarytenoid tissue and posterior third of the vocal cords. chronic cough and exhibited videostroboscopic findings of erythema and edema of the arytenoids. LTS PL. proximal esophagus (10 cm distal to the pharyngeal probe.Otolaryngology– Head and Neck Surgery Volume 120 Number 5 ULUALP et al 673 Table 1. Subsequently. VCN PL. Diagnostic workup results Patient no. The scope was then introduced into the esophagus through the upper esophageal sphincter under direct vision. vocal fold polyp.13 Barium esophagram was done after an overnight fasting. pH probes were placed at 3 manometrically determined sites: pharynx (2 cm above the upper esophageal sphincter). vocal fold polyp in 1 patient. the provocative maneuvers were performed while the PL patients were in a supine position. the extent of the barium in the esophagus.

25. cough. We also determined the presence or absence of hiatal hernia. Data for each subject are depicted.1% protein. a decrease in pH below 4. 12. 20. Earlier studies have shown that the proximal distribution of refluxate is associated with a decline in pH activity of refluxed material in the esophagus. pH recordings were displayed on the screen. Average acid clearance time was derived by dividing the total acid exposure time in minutes by the number of reflux episodes. was considered to be an acid reflux episode. the prevalence of pharyngeal acid reflux events was significantly higher in the patient group than in controls (*P < 0. they were transferred to a computer for subsequent printing and analysis. percent of study time that the pH was below 4. and exercise. esophageal dysmotility. The 2 pH electrodes were calibrated in buffers of pH 1 and pH 7. and a computer program was used to create a smaller time scale for determination of the temporal relationship among pH declines registered at various sites.9% fat). determination of the temporal relationship between the onset of pH decline among recording sites differentiated pH declines induced by oral intake (in which pharyngeal decline precedes distal esophageal pH drops) from true gastroesophagopharyngeal acid reflux episodes (in which pharyngeal pH decline occurs either simultaneously or after the esophageal pH decline). Studies were initiated in the morning after the manometric studies and terminated 22 to 24 hours later. and (3) dinner. and average acid clearance time of the acid reflux episodes. 16. Using these techniques. Meals were provided through the Medical College of Wisconsin General Clinical Research Center. acid exposure. Otolaryngology– Head and Neck Surgery May 1999 nose. PL patients as a group had significantly more reflux events than controls. belching. pH change caused by aerodigestive tract residue and secretions.674 ULUALP et al Fig 1. and showed no significant drift in the pH signal during the study. Percent acid exposure time was calculated as the percentage of the study period that the pH sensor was exposed to acid.3% fat).7% carbohydrate. reflux of barium. 9. a total of 1199 kcal (58. Statistical comparison between groups for acid reflux event exposure time was performed .6% carbohydrate. chest pain. and clearance during esophagography. For all 3 sites.4% protein. which was not related to belching or to the time of eating or drinking. (2) lunch. signals from pH electrodes were stored by the portable data logger. They also indicated position (upright or supine) and events such as heartburn. 11. These strict criteria were applied to avoid counting in spurious readings induced by pharyngeal pH probe movement.6% fat). and acid clearance time between PL patients and healthy controls. In addition. esophagitis. before and at the end of each study. and on completion of each study. All subjects kept a detailed diary indicating the time of oral intakes and time of going to bed.2% carbohydrate. and pH change caused by oral intake. a total of 504 kcal (78.2% protein. In addition. Also. During the study. a total of 822 kcal (67. it had to be simultaneous or preceded by a decrease in pH of similar or larger magnitude in the proximal and distal esophageal sites. As seen. Comparison of the number of pharyngeal acid reflux episodes. loss of complete mucosal contact. To be considered a pharyngeal reflux event. we determined in the pharyngeal site the number of pH declines below 4.01). Subjects ate a standard meal that included the following: (1) breakfast.

Except for pharyngeal pH monitoring. but pharyngeal reflux of barium was not observed in any patients. The number of pharyngeal reflux episodes among PL patients ranged from 0 to 12. patients are evaluated by various modalities such as esophageal endoscopy.001. Similarly. The number of pharyngeal acid reflux events in the PL patient group was significantly more than in controls (P < 0. These abnormalities included breaking of the primary wave in the mid to upper esophagus. Among the remaining 15 PL patients. Barium esophagram also documented hiatal hernia in these PL patients. Four patients with PL reported heartburn (1. In the PL patient group.Otolaryngology– Head and Neck Surgery Volume 120 Number 5 with the nonparametric test (Wilcoxon rank sum test) and for prevalence was performed by the χ2 test. glottal closure during swallowing and phonation was normal. esophagitis.14. Hiatal hernia was observed in 3 of the patients with PL. The prevalence of pharyngeal acid reflux was significantly higher in the PL patients than in controls (P < 0. 4 of these patients had hiatal hernias. 53 pharyngeal acid reflux events were recorded in PL patients.05). or stricture formation among this group. and findings are extrapolated to assess the role of reflux in the pathogenesis of supraesophageal lesions. In 3 of these 5 PL patients the reflux events occurred spontaneously and reached the thoracic inlet and aortic arch. and endoscopic evaluation of the esophagus in a group of patients with objectively documented PL. the sensitivity and specificity of this technique for documentation of GERD have been reported to range from 20% to 70%14-16 and 74% to 94%. GER events have been reported to occur spontaneously or may be provoked during standard barium esophagography. All PL patients who exhibited GER on esophageal barium studies were subsequently found to have pharyngeal acid reflux events during 24-hour pH monitoring (Table 1). In total. 3 had pharyngeal reflux episodes during pH monitoring. esophageal. Macroscopic esophagitis was observed in 2 PL patients. and duodenal mucosa. Except for 1 PL patient. DISCUSSION The association between GER and laryngeal disorders was first reported in patients with contact ulcer of the larynx by Cherry and Margulies6 in 1968. However. neoplasm. esophageal occurrence of reflux or its sequela is evaluated by these techniques. 2. and 4 episodes. None of the pharyngeal acid reflux events was associated with cough. However. all ULUALP et al 675 pharyngeal acid reflux events in both patients and healthy controls occurred in the upright position. Findings of 24-hour pH Monitoring Pharyngeal acid reflux episodes occurred in 15 of 20 patients with PL (Fig 1) and 2 of the 17 healthy controls (1 and 2 episodes.0005). 1. Barium studies did not exhibit any detectable structural abnormalities. barium esophagram revealed GER in 25% of patients. However. as described in the Methods section. There was no endoscopic evidence of hiatal hernia.005. Glottal closure during swallowing and phonation was normal in all controls.1. and pooling of the barium in the distal esophagus. all of whom demonstrated pharyngeal acid reflux during pH monitoring (Table 1). RESULTS Findings of Barium Esophagram Esophageal barium studies showed GER in 5 of 20 patients with PL. Barium refluxate did not reach the pharynx in any of these PL patients. and 24-hour pH monitoring. In the other 2 PL patients they occurred with provocative maneuvers. respectively). 24-hour pH monitoring. Since then GER has been implicated in the pathogenesis of a large number of aerodigestive tract disorders. T-EGD could not be done in 5 patients. Although previous studies using barium have reported a 61%5 to 80%2 incidence of hiatal hernia in patients . and subsequent pH monitoring of these PL patients documented the occurrence of pharyngeal acid reflux.6 In our study. In this study we report the combined findings of barium esophagram. inadequate clearance of the distal esophagus by secondary peristalsis. the percent acid exposure time and the average acid clearance time were significantly greater in PL patients than in healthy controls (P < 0. Among these PL patients. the cause-and-effect relationship between the majority of these disorders and gastric refluxate has not been systematically studied. None of these episodes was associated with belching. to determine the role of GER in the pathogenesis of these disorders. Findings of T-EGD T-EGD in the healthy control group showed normal laryngeal.16 respectively. Gastroesophagopharyngeal reflux of acid barium in patients with PL has been reported in some studies. P = 0. respectively). We also compared the pharyngoesophageal distribution of refluxed gastric acid between these patients and healthy controls. gastric. In practice. Four of 20 PL patients exhibited abnormal esophageal motility. barium esophagram. respectively) during the 24-hour study period. none of these heartburn events was associated with a distal esophageal reflux event.

Diagnosis and treatment of voice disorders. and distal esophagus. also occurred overwhelmingly in the upright position.23 However. 6. esophagopharyngeal acid reflux events occur most commonly during belching. whereas pharyngeal acid reflux events are more prevalent among patients with PL. Grossman TW.86:335-42. an acidic pH is required for proteolytic activities of pepsin. et al. their value in determining patients with PL has not been systematically evaluated.18. Ann Otol Rhinol Laryngol 1995. whereas 75% of them exhibited pharyngeal acid reflux documented by pH monitoring—suggest the generally accepted notion that the role of the barium esophagram for documenting GER in patients with supraesophageal complications of reflux disease is quite limited.18 However.40. 14. Kambic V. 161-75. 12. Although the mechanism of the esophagopharyngeal reflux was not studied in this report.104:550-5. Laryngoscope 1982.109:1575-82. a primary component of gastric secretion. Gastroesophageal reflux and laryngeal disease. White A.5. Richter JE. p. Ren J. Esophagopharyngeal distribution of refluxed gastric acid in patients with reflux laryngitis. Ann Otol Rhinol Laryngol 1994. They have recorded from either a single site within the esophagus4. hiatal hernia was documented in only 20% of PL patients in our investigation. Because recording of the reflux of other components of gastric refluxate is not widely available at this time. documentation of acid reflux is used as a marker or indicator of reflux of gastric content In conclusion. previous studies have shown that in patients with GERD and healthy controls. Arch Surg 1993.676 Otolaryngology– Head and Neck Surgery May 1999 ULUALP et al with laryngitis. 10. Benner K. Outcomes of antireflux therapy for the treatment of chronic laryngitis. J Laryngol Otol 1984. pharyngeal reflux events. 9. Kahrilas PJ. J Laryngol Otol 1972. Acid laryngitis. Although esophageal barium studies are frequently performed. 13. et al. 5.17. Ann Otol Rhinol Laryngol 1989. Koehler RE. including pepsin. 4.17-19 Various techniques have been used for this purpose.103:186-91.13. Gastroenterology 1995. Koufman JA. but were not related to belching.17. our study demonstrated endoscopic esophagitis in only 10% of these PL patients at the time of investigation. Koufman JA. Jindal JR. pancreatic enzyme. Laryngoscope 1968. The otolaryngologic manifestations of gastroesophageal reflux disease (GERD): a clinical investigation of 225 patients using ambulatory 24 hour pH monitoring and an experimental investigation of the role of acid and pepsin in the development of laryngeal injury. Hanson DG. they are rare among healthy controls. and tracheobronchial manifestations of gastroesophageal reflux. 1995. 3. Deveney CW. Detection of gastroe- . The findings of this study—that only 25% of PL patients demonstrated esophageal reflux events during barium studies. Shaker R. 11. Acid posterior laryngitis: aetiology. 1990. Contact ulcer of the larynx. Toohill RJ. the injurious effect of the gastric refluxate in addition to hydrochloric acid is dependent on its various components. laryngeal. in inducing esophageal and supraesophageal lesions has been reported previously. Ward PH. Laryngoscope 1991. Although in this study the frequency of pharyngeal acid reflux was measured. 98:405-10. Margulies SI. 8. p. Cherry J.13 Findings of our study are in agreement with this observation. documented in our investigation. et al. Idiopathic subglottic stenosis and gastroesophageal reflux. Thompson JK.128:1021-5. et al. Cohen J. Ambulatory pH monitoring has been used to document the role of acid reflux in the pathogenesis of posterior acid laryngitis. Gastroesophageal reflux and voice disorders. Gastroesophageal reflux and posterior laryngitis. Observations on the pathogenesis of chronic nonspecific pharyngitis and laryngitis. Von Haacke NP. bile acids. and byproducts of diges- tion. The role of pepsin. Esophageal complications of reflux are rare among patients with posterior acid laryngitis. proximal. Esophagopharyngeal reflux events may also occur during the transient low upper esophageal sphincter resting pressure or at the early stages of swallowing if the esophagus contains gastric acid.21 Similar to prior studies. editors. Gastrointest Endosc 1994. Previous studies of patients with laryngeal symptoms with and without objective findings have reported a history of recent esophagitis detected by endoscopy in 50% to 67% of cases. 3005-9. Milbrath M. et al.78:1937-40. Delahunty JE. Pharyngeal. Proceedings of the XXIV World Congress of Otolaryngology–Head and Neck Surgery. 7. Berkeley (CA): Kugler and Ghedini. 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Kamel PL. Berci G. Recent use of acid-suppressive therapy may account for this difference. Radsel Z. New York: Igaku-Shoin. 2.

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