The otorhinolaryngologic manifestations of esophagitis: peptic laryngitis
R.T. Sataloff, D.O. Castell, M.J. Hawkshaw, J.R. Spiegel (Philadelphia)
Occult chronic gastroesophageal reflux (GER) is an etiologic factor in a high percentage of patients with laryngological complaints. Patients with reflux laryngitis (RL) frequently have characteristic histories and physical findings which lead to the diagnosis. Although it is seen in general otolaryngologic practice in patients of all ages, the problem is particularly common in professional singers. In 1991, Sataloff et al. reported reflux in 265 of the 583 consecutive professional voice users (45%) who sought medical care during a 12-month period, although RL was often diagnosed incidentally and was not always responsible for the patient's primary voice complaint . The incidence may be lower in patients with other vocations. However, it is interesting to note that Koufman, et al. found increased GER in 78% of patients with hoarseness . Nevertheless, convincing studies of the prevalence of RL are not available.
Professional voice users: a special case
Acid reflux is especially common in singers for several reasons. First, the technique of singing involves "support," forceful compression of the abdominal muscles designed to push the abdominal contents superiorly and pull the sternum down. This compresses the air in the thorax and generates force for the stream of expired air. However, it also compresses the stomach and works against the lower esophageal sphincter (LES). Singing is an athletic endeavor, and the mechanism responsible for reflux in voice users is similar to that associated with reflux following other athletic activities, lifting, and pregnancy (in addition to hormonal factors). Secondly, many singers do not eat before performing because a full stomach interferes with abdominal support and promotes reflux. Performances usually take place at night. Consequently, the singer returns home hungry and eats a large meal before bed. Thirdly, performance careers are particularly stressful, and this factor may be associated with increased acid production. Fourthly, many singers pay little attention to good nutrition, frequently consuming caffeine, fatty foods, spicy foods, citrus products (especially lemons), tomatoes (including pizza and spaghetti), and fatty "fast foods."
Common symptoms of RL include morning hoarseness, prolonged warm up time (greater than 20-30 min), halitosis, excessive phlegm, frequent throat clearing, dry mouth, coated tongue, sensation of a lump in the throat, throat tickle, dysphagia, chronic sore throat, nocturnal cough, chronic or recurrent cough, difficulty breathing (especially at night), closing off of the airway ("laryngospasm"), regurgitation of food, poorly controlled asthma (which causes dysphonia by interfering with the support mechanism), pneumonia, and occasionally dyspepsia. However, dyspepsia is frequently absent. Interestingly, if patients stop reflux treatment after a period of a couple of months or more, classic dyspepsia is frequently present when symptoms recur. In addition to prolonged vocal warm up time, professional singers and actors may also complain of voice practice intolerance. This involves frequent throat clearing and excessive phlegm especially during the first 10 to 20 min of vocal exercises or songs. Although the majority of otolaryngologists have only begun to acknowledge the importance of reflux in causing otolaryngologic disease recently, many authors have recognized the association over a period of more than 2 decades [3-27].
Laryngoscopic examination typically reveals erythema and edema of the mucosa overlying the arytenoid cartilages, the posterior aspect of the larynx, and often the posterior portion of the true vocal folds. In severe cases, the erythema and edema may be more extensive. Mild, nonspecific laryngitis and halitosis are also commonly
present. In some patients with laryngitis severe enough to involve the oral cavity, there is also loss of dental enamel. Transparency of the lower portion of the central incisors may be seen occasionally in reflux patients, although it is more common in patients with bulimia.
In addition to erythema and edema, more significant vocal fold pathology may be caused by reflux laryngitis. In 1968, Cherry and Margulies  recognized that reflux laryngitis might be a causative factor in contact ulcers and granulomas of the posterior portion of the vocal folds. They also observed that treatment of peptic esophagitis resulted in resolution of vocal process granulomas. Delahunty and Cherry  followed up on this observation by applying gastric juice to the vocal processes of two dogs, and applying saliva in a similar fashion to the vocal processes of a third dog who was used as a control. The control dogs' vocal folds remained normal, the other dogs developed granulomas at the sites of repeated acid application. Since then, numerous authors have recognized the importance of reflux laryngitis as a causative factor in laryngeal ulcers and granulomas, including intubation granuloma [2,4,7,8, 30-36]. In addition to its etiological involvement in intubation granuloma, reflux laryngitis has long been recognized as contributing to posterior glottic stenosis, especially following intubation . Olson has suggested that it may also be involved in causing cricoarytenoid joint arthritis through chronic inflammation and ulceration, beginning on the mucosa and involving the synovial cricoarytenoid joint . In addition to posterior glottic and supraglottic stenosis, subglottic stenosis has also been reported as a complication of reflux [3,38].
Vocal fold pathology may also occur secondary to aspiration of gastric juice. Severe coughing may cause vocal fold hemorrhage or mucosal tears, sometimes leading to permanent dysphonia. Aspiration also makes reactive airway disease difficult to control. Even mild pulmonary obstruction impairs voice support. Consequently, afflicted patients subconsciously strain to compensate with muscles in the neck and throat, designed for delicate control, not for power source functions . This behavior is typically responsible for vocal nodules and other voice abuse lesions.
It appears likely that RL is also causally related to laryngeal carcinoma. The association of GERD with Barrett's esophagus and esophageal carcinoma has been well established. Delahunty biopsied the posterior laryngeal mucosa in a RL patient and reported epithelial hyperplasia with parakeratosis and papillary downgrowth . Olson reported five patients with posterior laryngeal carcinoma, in whom he believed reflux to be a cofactor . This issue was also addressed by Morrison . Although the causal relationship between reflux and laryngeal cancer has not been established with absolute certainty, it appears likely.
In addition to its possible carcinogenic potential, the chronic irritation of reflux laryngitis may be responsible for failure of wound healing, another sign of reflux. Reflux appears to delay the resolution not only of vocal process ulcers and granulomas, but also of surgical vocal fold disruptions. For this reason, otolaryngologists are becoming increasingly aggressive about diagnosing and treating reflux before subjecting patients to vocal fold surgery, even for conditions unrelated to the reflux.
Tests to confirm the presence of reflux laryngitis are discussed elsewhere in this book, and will not be reviewed in this chapter. However, a couple of points are worth special consideration. At present, 24-h pH monitoring is considered the most definitive study and should be used to confirm abnormal reflux in many of these patients. Studies in our laboratory have shown that dual electrode pH recording can document abnormal distal and proximal esophageal reflux induced by singing (Fig. 1). However, occasionally patients will show abnormalities on barium swallow with water siphon-age, but normal 24-h pH monitor studies. Although this is usually regarded as a "false-positive" barium study, this assumption may require further investigation. In professional singers and actors especially, barium swallow with water siphonage provides a good clinical approximation of daily activities. In order to optimize mucosal function, it is essential for singers and actors to remain well hydrated. Consequently they drink large quantities of water, routinely carry water bottles with them, and drink substantial quantities shortly before they sing. This routine behavior is similar to the water siphon portion of the barium swallow, and this raises the question of whether positive water siphonage tests may provide useful information
Figure 1. .Dual electrode pH probe monitoring while singing for a 30 min period of the 1 h shown. The patient experienced typical heartburn, and increased proximal and distal acid exposure was prominent during singing.
at least in professional voice users, even when 24-h pH monitor studies are normal, much like the singing challenge (Fig. 1).
Other otolaryngologic manifestations of GERD
Other otolaryngologic manifestations of GERD are beyond the scope of this chapter. However, chronic recurrent sore throat, "globus hystericus," chronic aspiration, recurrent airway problems in infants, Zenker's diverticulum, oropharyngeal dysphagia, halitosis, possibly geographical tongue, and other problems encountered commonly by laryngologists may all be caused by, or associated with, reflux. Otolaryngologists are becoming increasingly diligent about recognizing GERD as the underlying problem, and beginning to treat it as the primary approach to these conditions, as well as to the many laryngeal abnormalities discussed above.
Treatment considerations in reflux patients are discussed elsewhere in this book. However, it should be noted that patients with reflux laryngitis frequently require more intensive therapy with higher doses of H2 blockers than patients with dyspepsia in the absence of laryngeal symptoms and signs. In addition to monitoring symptoms and signs of RL, response to treatment is best judged by combined intraesophageal and intragastric pH monitoring of patients while they are receiving treatment. Research into appropriate treatment regimens is ongoing, and extensive additional investigation is needed on the consequences of reflux upon the larynx, and upon all of the other mucosal surfaces above the cricopharyngeus muscle.
8. Ward PH, Zwitman D, Hanson D, et al. Contact ulcers and granulomas of the larynx: New insights into their etiology as a basis for more rational treatment. Otolaryngol Head Neck Surg 1980;88:262-269.
16. Wiener CJ, Koufman JA, Wu WC, Cooper JB, Richter JE, Castell DO. Chronic hoarseness secondary to gastroesophageal reflux disease: Documentation with 24-h ambulatory pH monitoring. Am J Gastroenterol 1989;84(12):1503-1507.
20. Koufman JA. Otolaryngologic manifestations of gastroesophageal reflux disease (GERD): A clinical investigation of 225 patients using ambulatory 24 hr pH monitoring and an experimental investigation of the role of acid and pepsin in the development of laryngeal injury. Laryngoscope 1991;101(4)(suppl 53):2.
21. Pesce G, Caligaris F. Posterior laryngitis in the pathology of the digestive system (Le laringiti posteriori nella pathologia dell'apparato digerente). Arch Ital Laringol 1966;74(2):77-92 (in Italian).
38. Fligny I, Francois M, Aigrain Y, Polonovski JM, Contencin P, Narcy P. Subglottic stenosis and gastroesophageal reflux (Stenoses sous-glottiques et reflux gastro-oesophagien). Ann Otolaryngol Chir Cervicofac 1989;106(3):193-196.