Pharyngeal pH monitoring in patients with posterior

laryngitis
SECKIN O. ULUALP, MD, ROBERT J. TOOHILL, MD, RAYMOND HOFFMANN, PhD, and REZA SHAKER, MD, Milwaukee, Wisconsin

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 Reinkes 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

METHODS

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
OtolaryngologyHead 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
672

Otolaryngology
Head and Neck Surgery
Volume 120 Number 5

ULUALP et al

673

Table 1. Diagnostic workup results

Patient no.

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, VCN
PL
PL, LTS
PL, VCN
PL, LTS
PL, LTS
PL
PL
PL
PL
PL
PL, LTS
PL, VCN
PL
PL, LTS
PL
PL
PL, VFP
PL, VCN
PL

GER()
GER()
GER()
GER()
GER()
GER()
GER()
GER(+), HH
AM
GER()
AM
GER()
GER(+), HH
GER(+), AM, HH
GER(+)
AM
GER(+), 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, 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, Vocal cord nodules; LTS, laryngotracheal stenosis; HH, hiatal hernia; AM, abnormal motility; VFP, vocal fold polyp.

chronic cough and exhibited videostroboscopic findings of

erythema and edema of the arytenoids, erythema of interarytenoid tissue and posterior third of the vocal cords, pachyderma laryngis, hyperplastic interarytenoid tissue, or erythema of
the entire larynx. In addition to the above findings, videostroboscopy also documented vocal cord nodules in 4 patients,
vocal fold polyp in 1 patient, and laryngotracheal stenosis in
5 patients (Table 1).
Fifteen of the 20 PL patients underwent T-EGD.12 T-EGD
could not be performed in the remaining 5 PL patients
because of severe nasal septal deviation (2 patients), technical
difficulty in intubating the esophagus (1 patient), and vasovagal reaction (2 patients). All 20 PL patients had a standard barium esophagram findings.
All PL patients and healthy volunteers were studied for
occurrence of pharyngeal acid reflux by 3-site 24-hour
pharyngoesophageal pH monitoring.13
Barium esophagram was done after an overnight fasting.
Barium swallows were performed with a total of 200 to 250
mL of barium and water mixture. Radiographs and videofluoroscopic recordings were obtained. Spontaneous gastroesophageal reflux (GER) events throughout the examination
were evaluated. If no GER event was observed, the provocative maneuvers were performed while the PL patients were in
a supine position. Provocative maneuvers involved exercises
that increase the intra-abdominal pressure. For this, PL
patients were sequentially asked to perform the following
tasks: (1) coughing, (2) leg raising, and (3) the Valsalva
maneuver. GER was said to be present when barium was
observed to fill the esophageal lumen at least 3 cm.14 Barium

esophagram reports included the presence or absence of GER,

the extent of the barium in the esophagus, and the provocative
maneuver or maneuvers performed to observe GER.
T-EGD was done with an Olympus GIF-N30 endoscope
(Olympus Corp, Lake Success, NY) with volunteers or PL
patients sitting upright in a chair. 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. In cases of narrow passage caused by hypertrophied turbinates, 2 puffs of a nasal decongestant were
applied. In all cases the pharynx was anesthetized with
Cetacaine spray. Then the endoscope was passed through the
nose to the nasopharynx and pharynx. The larynx was
observed, and glottal closure during swallowing and phonation was evaluated. The scope was then introduced into the
esophagus through the upper esophageal sphincter under
direct vision. The gross appearance of esophageal mucosa was
evaluated. Subsequently, 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.
The ambulatory pH studies were done with pH recording
systems, with a single recording site and another with 2
recording sites that were 10 cm apart (Synectics Medical Inc,
Irving, TX). pH probes were placed at 3 manometrically
determined sites: pharynx (2 cm above the upper esophageal
sphincter), proximal esophagus (10 cm distal to the pharyngeal probe, approximately 4 to 5 cm below the upper esophageal sphincter), and distal esophagus (5 cm above the
lower esophageal sphincter). The probes were secured to the

674

ULUALP et al

Fig 1. Comparison of the number of pharyngeal acid

reflux episodes, acid exposure, and acid clearance time
between PL patients and healthy controls. Data for each
subject are depicted. As seen, PL patients as a group had
significantly more reflux events than controls. In addition,
the prevalence of pharyngeal acid reflux events was significantly higher in the patient group than in controls (*P
< 0.01).

Otolaryngology
Head and Neck Surgery
May 1999

nose. Studies were initiated in the morning after the manometric studies and terminated 22 to 24 hours later. Subjects ate
a standard meal that included the following: (1) breakfast, a
total of 504 kcal (78.6% carbohydrate, 12.1% protein, 9.3%
fat); (2) lunch, a total of 822 kcal (67.7% carbohydrate, 11.4%
protein, 20.9% fat); and (3) dinner, a total of 1199 kcal (58.2%
carbohydrate, 16.2% protein, 25.6% fat). Meals were provided through the Medical College of Wisconsin General Clinical
Research Center. All subjects kept a detailed diary indicating
the time of oral intakes and time of going to bed. They also
indicated position (upright or supine) and events such as
heartburn, belching, cough, chest pain, and exercise. For all 3
sites, a decrease in pH below 4, which was not related to
belching or to the time of eating or drinking, was considered
to be an acid reflux episode. To be considered a pharyngeal
reflux event, it had to be simultaneous or preceded by a
decrease in pH of similar or larger magnitude in the proximal
and distal esophageal sites. Earlier studies have shown that the
proximal distribution of refluxate is associated with a decline
in pH activity of refluxed material in the esophagus. Also,
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). These strict criteria were applied to
avoid counting in spurious readings induced by pharyngeal
pH probe movement, loss of complete mucosal contact, pH
change caused by aerodigestive tract residue and secretions,
and pH change caused by oral intake.
During the study, signals from pH electrodes were stored
by the portable data logger, and on completion of each study,
they were transferred to a computer for subsequent printing
and analysis. In addition, pH recordings were displayed on the
screen, 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. The 2 pH electrodes were calibrated in buffers of pH 1 and pH 7, before and
at the end of each study, and showed no significant drift in the
pH signal during the study. Using these techniques, we determined in the pharyngeal site the number of pH declines below
4, percent of study time that the pH was below 4, and average
acid clearance time of the acid reflux episodes. Percent acid
exposure time was calculated as the percentage of the study
period that the pH sensor was exposed to acid. Average acid
clearance time was derived by dividing the total acid exposure
time in minutes by the number of reflux episodes. We also
determined the presence or absence of hiatal hernia, esophagitis, esophageal dysmotility, reflux of barium, and clearance
during esophagography. Statistical comparison between
groups for acid reflux event exposure time was performed

Otolaryngology
Head and Neck Surgery
Volume 120 Number 5

with the nonparametric test (Wilcoxon rank sum test) and for
prevalence was performed by the 2 test.
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. In 3 of these 5 PL
patients the reflux events occurred spontaneously and
reached the thoracic inlet and aortic arch. In the other 2
PL patients they occurred with provocative maneuvers;
4 of these patients had hiatal hernias. Barium studies
did not exhibit any detectable structural abnormalities.
Four of 20 PL patients exhibited abnormal esophageal motility. These abnormalities included breaking of the primary wave in the mid to upper esophagus,
inadequate clearance of the distal esophagus by secondary peristalsis, and pooling of the barium in the distal esophagus. Among these PL patients, 3 had pharyngeal reflux episodes during pH monitoring. 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).
Findings of T-EGD

T-EGD in the healthy control group showed normal

laryngeal, esophageal, gastric, and duodenal mucosa.
Glottal closure during swallowing and phonation was
normal in all controls. There was no endoscopic evidence of hiatal hernia, esophagitis, neoplasm, or stricture formation among this group. In the PL patient
group, T-EGD could not be done in 5 patients, as
described in the Methods section. Among the remaining
15 PL patients, glottal closure during swallowing and
phonation was normal. Macroscopic esophagitis was
observed in 2 PL patients, and subsequent pH monitoring of these PL patients documented the occurrence of
pharyngeal acid reflux. Hiatal hernia was observed in 3
of the patients with PL, all of whom demonstrated pharyngeal acid reflux during pH monitoring (Table 1).
Barium esophagram also documented hiatal hernia in
these PL patients.
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, respectively). The number of pharyngeal reflux episodes among PL patients ranged from 0
to 12. In total, 53 pharyngeal acid reflux events were
recorded in PL patients. None of these episodes was
associated with belching. Except for 1 PL patient, all

ULUALP et al

675

pharyngeal acid reflux events in both patients and

healthy controls occurred in the upright position. None
of the pharyngeal acid reflux events was associated with
cough. Four patients with PL reported heartburn (1, 1,
2, and 4 episodes, respectively) during the 24-hour
study period. However, none of these heartburn events
was associated with a distal esophageal reflux event.
The number of pharyngeal acid reflux events in the PL
patient group was significantly more than in controls (P
< 0.0005). Similarly, the percent acid exposure time and
the average acid clearance time were significantly
greater in PL patients than in healthy controls (P <
0.005, P = 0.001, respectively). The prevalence of pharyngeal acid reflux was significantly higher in the PL
patients than in controls (P < 0.05).
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. Since
then GER has been implicated in the pathogenesis of a
large number of aerodigestive tract disorders. However,
the cause-and-effect relationship between the majority
of these disorders and gastric refluxate has not been systematically studied. In practice, to determine the role of
GER in the pathogenesis of these disorders, patients are
evaluated by various modalities such as esophageal
endoscopy, barium esophagram, and 24-hour pH monitoring. Except for pharyngeal pH monitoring, esophageal occurrence of reflux or its sequela is evaluated
by these techniques, and findings are extrapolated to
assess the role of reflux in the pathogenesis of supraesophageal lesions.
In this study we report the combined findings of barium esophagram, 24-hour pH monitoring, and endoscopic evaluation of the esophagus in a group of
patients with objectively documented PL. We also compared the pharyngoesophageal distribution of refluxed
gastric acid between these patients and healthy controls.
GER events have been reported to occur spontaneously or may be provoked during standard barium
esophagography. However, 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%,14,16 respectively. Gastroesophagopharyngeal
reflux of acid barium in patients with PL has been
reported in some studies.1,6 In our study, barium
esophagram revealed GER in 25% of patients, but pharyngeal reflux of barium was not observed in any
patients.
Although previous studies using barium have reported a 61%5 to 80%2 incidence of hiatal hernia in patients

676

Otolaryngology
Head and Neck Surgery
May 1999

ULUALP et al

with laryngitis, hiatal hernia was documented in only

20% of PL patients in our investigation.
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.17,18 However, our study
demonstrated endoscopic esophagitis in only 10% of
these PL patients at the time of investigation. Recent
use of acid-suppressive therapy may account for this
difference.
Ambulatory pH monitoring has been used to document the role of acid reflux in the pathogenesis of posterior acid laryngitis.5,13,17-19 Various techniques have
been used for this purpose. They have recorded from
either a single site within the esophagus4,18,20 or from
the pharynx and proximal or distal esophagus.5,17,19
These studies reported different degrees of GER. In a
recent study using concurrent recording from the pharynx, proximal, and distal esophagus, gastroesophagopharyngeal distribution of refluxed gastric acid in
patients with PL was found to be significantly different
from that in patients with GERD and healthy controls.13
Findings of our study are in agreement with this observation.
Although esophageal barium studies are frequently
performed, their value in determining patients with PL
has not been systematically evaluated. The findings of
this studythat only 25% of PL patients demonstrated esophageal reflux events during barium studies,
whereas 75% of them exhibited pharyngeal acid reflux
documented by pH monitoringsuggest 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.
Although the mechanism of the esophagopharyngeal
reflux was not studied in this report, previous studies
have shown that in patients with GERD and healthy
controls, esophagopharyngeal acid reflux events occur
most commonly during belching. 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, pharyngeal
reflux events, documented in our investigation, also
occurred overwhelmingly in the upright position, but
were not related to belching.
Although in this study the frequency of pharyngeal
acid reflux was measured, the injurious effect of the
gastric refluxate in addition to hydrochloric acid is
dependent on its various components, including pepsin,
pancreatic enzyme, bile acids, and byproducts of diges-

tion. The role of pepsin, a primary component of gastric

secretion, in inducing esophageal and supraesophageal
lesions has been reported previously.22,23 However, an
acidic pH is required for proteolytic activities of pepsin.
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, whereas pharyngeal acid reflux events
are more prevalent among patients with PL, they are
rare among healthy controls. Esophageal complications
of reflux are rare among patients with posterior acid
laryngitis. Reflux events detected during barium esophagography poorly correlate with the existence of PL and
pharyngeal acid reflux. Among the 3 modalities used in
this study, pharyngeal acid reflux events recorded by pH
monitoring are more frequently detected in patients
with PL than esophageal sequela of reflux disease
detected by endoscopy or occurrence of reflux during
esophageal barium studies.
REFERENCES
1. Delahunty JE. Acid laryngitis. J Laryngol Otol 1972;86:335-42.
2. Ward PH, Berci G. Observations on the pathogenesis of chronic
nonspecific pharyngitis and laryngitis. Laryngoscope 1982;92:
1377-82.
3. Kambic V, Radsel Z. Acid posterior laryngitis: aetiology, histology, diagnosis and treatment. J Laryngol Otol 1984;98:1237-40.
4. Wilson JA, White A, Von Haacke NP, et al. Gastroesophageal
reflux and posterior laryngitis. Ann Otol Rhinol Laryngol 1989;
98:405-10.
5. Koufman JA. 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. Laryngoscope 1991;101(Suppl 53):
1-78.
6. Cherry J, Margulies SI. Contact ulcer of the larynx. Laryngoscope 1968;78:1937-40.
7. Deveney CW, Benner K, Cohen J. Gastroesophageal reflux and
laryngeal disease. Arch Surg 1993;128:1021-5.
8. Koufman JA. Gastroesophageal reflux and voice disorders. In:
Rubin JS, et al, editors. Diagnosis and treatment of voice disorders. New York: Igaku-Shoin; 1995. p. 161-75.
9. Hanson DG, Kamel PL, Kahrilas PJ. Outcomes of antireflux
therapy for the treatment of chronic laryngitis. Ann Otol Rhinol
Laryngol 1995;104:550-5.
10. Toohill RJ, Mushtag E, Grossman TW, et al. Pharyngeal, laryngeal, and tracheobronchial manifestations of gastroesophageal
reflux. Proceedings of the XXIV World Congress of OtolaryngologyHead and Neck Surgery. Berkeley (CA): Kugler and
Ghedini; 1990. p. 3005-9.
11. Jindal JR, Milbrath MM, Shaker R, et al. Idiopathic subglottic
stenosis and gastroesophageal reflux. Ann Otol Rhinol Laryngol
1994;103:186-91.
12. Shaker R. Unsedated trans-nasal pharyngoesophagogastroduodenoscopy (T-EGD): technique. Gastrointest Endosc 1994;40;
3:346-7.
13. Shaker R, Milbrath M, Ren J, et al. Esophagopharyngeal distribution of refluxed gastric acid in patients with reflux laryngitis.
Gastroenterology 1995;109:1575-82.
14. Thompson JK, Koehler RE, Richter JE. Detection of gastroe-

Otolaryngology
Head and Neck Surgery
Volume 120 Number 5

15.
16.
17.
18.
19.

sophageal reflux: value of barium studies compared with 24 hr

pH monitoring. AJR Am J Roentgenol 1994;192:621-6.
Ott DJ, Gelfand DW, Wu WC. Reflux esophagitis: radiographic
and endoscopic correlation. Radiology 1979;130:583-8.
Sellor RJ, DeCaestecker JS, Heading RC. Barium radiology: a
sensitive test for gastroesophageal reflux. Clin Radiol 1987;38:
303-7.
Jacob P, Kahrilas PJ, Herzon G. Proximal esophageal pH-metry
in patients with reflux laryngitis. Gastroenterology 1991;100:
305-10.
McNally PR, Maydonovitch CL, Prosek RA, et al. Evaluation of
gastroesophageal reflux as a cause of idiopathic hoarseness. Dig
Dis Sci 1989;34:1900-4.
Wiener GJ, Koufman JA, Wu WC, et al. Chronic hoarseness sec-

ULUALP et al

20.
21.
22.
23.

677

ondary to gastroesophageal reflux disease: documentation with 24

h ambulatory pH monitoring. Am J Gastroenterol 1989;84:1503-8.
Metz D, Childs ML, Ruiz C, et al. Pilot study of the omeprazole
test for reflux laryngitis. Otolaryngology Head Neck Surg 1997;
116;1:41-6.
Shaker R, Dodds WJ, Hogan WJ, et al. Mechanisms of esophago-pharyngeal acid regurgitation [abstract]. Gastroenterology
1991;100:A494.
Goldberg HI, Dodds WJ, Montgomery C, et al. Controlled production of acute esophagitis. Experimental animal model. Am J
Roentgenol Rad Ther Nucl Med 1970;110:288-94.
Dodds WJ, Goldberg HI, Montgomery C, et al. Sequential gross,
microscopic and roentgenographic features of acute feline
esophagitis. Invest Radiol 1970;5:209-19.

Management of the Tinnitus Patient

This seventh annual conference, sponsored by the University of Iowa

Departments of OtolaryngologyHead and Neck Surgery and Speech Pathology and
Audiology, will be held September 30October 2, 1999, at the University of Iowa
Hospitals and Clinics, Iowa City, IA.
For further information, contact the Center for Conferences and Institutes,
University of Iowa, 249 Iowa Memorial Union, Iowa City, IA 52242-1317; phone,
900-551-9029; fax, 319-335-3533.