History

Internists and otolaryngologists have reported possible airway involvement in adult patients with upper digestive disorders. By the end of the 19th century, Osler mentioned the occurrence of dyspnea in the postprandial period when the gastric cavity is full. From the early 1970s, with the description of “hiatal hernia” in adults, to more recent pediatric studies, it has become obvious that some laryngeal inflammatory processes develop in conjunction with upper digestive malfunctions, including GER.

The first modern clinical demonstration of GER-related laryngeal harm was made by Ward and colleagues¹ in glottic granulomas and contact ulcers in adults, and by Little and colleagues² in subglottic stenosis in an animal model. In infants and children, GER was initially shown through barium studies to be responsible for recurrent croup.³ Similarly, apnea in premature newborns and various forms of laryngitis were linked to GER by means of esophageal and pharyngeal pH monitoring.^4,5 Finding decreases in pharyngeal pH to 2 at the laryngeal inlet or above in cases of pediatric chronic rhinitis/laryngitis raises a high index of suspicion of the role of acid reflux in these disorders of the airway. There was a statistically significant difference in upper and lower pH monitoring data between these patients and controls.⁶ Some control patients and even gastroenterology patients might have pH variations that were close to each other, however, without any rhinolaryngologic symptoms. Since those studies were performed, control infants and children could not ethically be tested. Many studies focused on in vitro tests and on the efficacy of anti-GER treatments in patients.

Definition

GER is an abnormal and repeated ascent of gastric content into the esophagus (and possibly above it). There is a physiologic GER that occurs mainly in the postprandial period. Small amounts of refluxed material may cause burping at any age and a small degree of emesis in the infant. Sometimes it is also called “functional” GER because esophageal pH monitoring may show a few acid periods (<5% of recorded time at pH less than 4 on a 20-hour basis) that are considered unharmful to the esophagus. In this case, no other digestive symptom is noted, and upper digestive endoscopy is normal.

GER disease (GERD) is believed to have gastrointestinal or extragastrointestinal signs. Gastrointestinal signs include emesis, dysphagia, choking, gagging, and failure to thrive in children. Extragastrointestinal signs include chronic coughing, wheezing, hoarseness, sore throat, stridor, recurrent croup, and obstructive apnea. Heartburn is extremely rare.

GERD was defined using gastrointestinal criteria; normal values for GER tests were established according to this definition. These criteria are not entirely appropriate in cases of a laryngeal disorder (also improperly called “laryngopharyngeal reflux” in adults). An extensive assessment for GER with “normal” results may be associated with chronic laryngeal inflammation; however, abnormal results indicating GERD may be found in cases of asymptomatic and endoscopically normal larynges. Many authors emphasized the particular pH profile of “airway-linked” GER. In a cohort of 90 children with pH monitoring, Zalesska-Krecicka and coworkers⁷ found a high prevalence of daytime refluxes when patients with laryngeal disorders were in the upright position.

Physiopathology

The anatomic proximity and the neurofunctional collusion of the human larynx to the hypopharynx and upper esophagus lead to its unique vulnerability.⁸ In no other mammal species is the larynx so caudal compared with the digestive tract organs. This positioning can explain the diffusion of the gastric juice up to the laryngeal mucosa.⁹ Although many patients have GER, why do so few have true laryngeal disorders? It seems that a mechanism peculiar to the larynx is involved, and this can be due to direct contact with the gastric juice or to a vague mediated reflex.

Studies by Willging and Thompson¹⁰ emphasized the role of laryngeal sensitivity in the development of pediatric anomalies such as laryngomalacia and GER-induced laryngeal reflexes. Paradoxical vocal cord motion, laryngospasm, and saliva and food aspiration are associated with abnormal thresholds of local chemoreceptors and mechanoreceptors. It has been shown that premature infants develop progressive swallowing ability and control of the lower esophageal sphincter postnatally, depending on the status of their respiratory and neurologic systems. GER and laryngeal sensitivity are intimately related and involved in cases of prematurity.¹¹

Lipan and associates⁹ discussed possible mechanisms of potential harm of the larynx by GER. They stated that, compared with classic intraesophageal reflux, cranial involvement by GER may be the result of four failing “barriers” including upper esophageal sphincter and pharyngolaryngeal mucosal resistance. These two domains warrant specialized interest and involvement of gastroenterologists, pathologists, and immunologists to know what exactly differentiates patients with gastrointestinal symptoms from patients with head and neck symptoms affected by GER. In 1998, an experimental rabbit model–based study emphasized the role of hydrogen chloride and pepsin inducing a chemical trauma and the individual laryngeal chemosensitivity.¹² In 2003, Altman and colleagues¹³ found expression of a proton pump in the laryngeal mucosa. These mechanisms are held responsible for inflammatory laryngeal pediatric processes and for adult laryngeal carcinomas.¹⁴ Eventually, in an “in vitro” model of laryngeal cultures, Ylitalo and Thibeault¹⁵ showed more changes in gene expression of postcricoidal fibroblasts after 60 seconds of exposure to pepsin at low pH. Some authors denied the role of acid secretions in this domain, however, considering the inefficacy of gastric acid suppressors (i.e., proton pump inhibitors) in healing chronic laryngitis in adults.¹⁶

Diagnosis

A patient history of combined digestive and respiratory symptoms may help suggest the diagnosis of GERD. In infants, feeding difficulties with tears, apparent life-threatening events with hypotonia, and rise of refluxed food while supine are useful signs that may lead to empirical treatment. Radiographic studies with barium swallow, a search for lipid-laden macrophages at bronchial lavage, and a thoracic scintiscan with ingestion of nuclide elements are not routinely performed. Esophagoscopy with a flexible fiberscope may show esophagitis and large hiatal hernia. These abnormalities are rare, however, in cases with no gastrointestinal symptoms. It is unclear whether laryngoscopy and bronchoscopy can point to marks of GER because no specific features are described other than cobblestoning of the posterior supraglottic or subglottic area.^17,18

Esophageal pH monitoring is considered by gastroenterologists to be the gold standard for diagnosing GER. Acid periods recorded over 18 to 24 hours can be correlated with airway manifestations (e.g., cough, stridor). An abnormal percentage of the recorded time at a pH less than 4 allows the physician to manage the GER. The question is what percentage should be considered abnormal in the absence of gastrointestinal signs and symptoms. It is unknown whether nonacid or weakly acid reflux may also play a role in the pathogenesis of GER-related laryngeal disorders.^19,20 A negative test does not rule out GER without esophageal lesion, however. Combined pharyngeal and esophageal pH records showed that brief refluxes can reach the laryngeal inlet and cause problems, whereas classic standards for this pH test are considered normal with a poor total acid time. Pharyngeal pH recordings are subject to drifts by dryness, however, and are not used routinely. Many studies have shown that brief diurnal refluxes are usual features of airway-disordered GER. Brief, pharyngeal and nonacid refluxes may be diagnosed easily by a promising test: esophageal impedance recording. This technique, which includes pH monitoring, allows recording of any refluxate, and is expected to enter routine practice.²¹

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