Mitrović Slobodan M.

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Strana 608 VOJNOSANITETSKI PREGLED Vojnosanit Pregl 2014; 71(6): 608–610.Correspondence to: Slobodan M. Mitroviý, Ear, Nose and Throat University Clinic, Clinical Center of Vojvodina, Hajduk Veljkova 1–3,21 000 Novi Sad, Serbia. Phone: +381 21 484 3 670. E-mail: mitroslo@eunet.rsHISTORY OF MEDICINE UDC: 61:[616.22-02:616.34-008.1(091)DOI: 10.2298/VSP1406608MTerminology, diagnostics and therapy of laryngopharyngeal reflux– A glimpse into the pastTerminologija, dijagnostika i terapija laringofarinksnog refluksa – pogled uprošlostSlobodan M. MitroviüPhoniatric Department, Ear, Nose and Throat University Clinic, Clinical Center ofVojvodina, Faculty of Medicine, University of Novi Sad, Novi Sad, SerbiaKey words:larynx; gastroesophageal reflux; diagnosis, differential;therapeutics; hydrochloric acid; pepsin a.Kljuÿne reÿi:larinks; gastroezofagusni refluks; dijagnoza,diferencijalna; leÿenje; hlorovodoniÿna kiselina;pepsin.IntroductionLaryngopharyngeal reflux (LPR) is the presence of re-fluxed gastric contents in the laryngopharyngeal space,where it is in close contact with the tissues of upper aerodi-gestive tract. Some authors consider it an entity, while othersas extraesophageal manifestation of gastroesophageal reflux.However, it is considered that its pathophysiology andsymptoms are different from gastroesophageal reflux. Mainsymptoms are: throat clearing, hoarseness, chronic cough,postnasal drip, halitosis, dysphagia, sense of foreign body inpharynx. As a confirmation of suspected LPR, indirect lar-yngoscopy shows: mucous edema, redness, ventricular oblit-eration, pseudoulcer, hypertrophy of posterior laryngeal re-gion and laryngeal granulomas. It is believed that the pres-ence of gastric contents in larynx and hypopharynx plays arole in the development of cancer lesions of this region. To-day, an influence of pepsin and hydrochlorid acid on manyother disorders in otorhinolaryngological region are beingconsidered 1.At the level of assumptionsAlthough in the middle of XIX century the only possi-ble way to visualize larynx was post mortem, negative im-pact of numerous factors on different laryngeal functions,predominantly phonation, were known. Singing teacher inParis, Manuel Garcia 2, wrote “Studies about human voice”in 1840, where he stated: “Gourmet dishes, oils from certainherbs, spirits, it all has negative impact on our apparatus.”Thus, he pointed out a possible influence of reflux on larynx,without actually being able to prove it. Guided by a wish toshow larynx, in 1854 Garcia performed the first “autolaryn-goscopy”, and managed to visualize this organ for the firsttime. By the end of the XIX century, changes of posteriorpart of larynx were confirmed histopathologically, whichcaused a series of researches on gastric contents reflux as anetiology factor in many laryngeal disorders in the XX cen-tury.In 1880, Rudolf Virchow wrote a descriptive term“pachydermia verrucosa laryngis“ for changes on arytenoidmucosa, which he associated with vocal abuse. In his origi-nal paper, Virchow described it as a state different from la-ryngeal leucoplacia and keratosis 3. In the same year, MorellMackenzie 4 identified the changes of arytenoid cartilagebased on the presence of ulceration. Journal of the Royal So-ciety of Medicine in 1908 published the abstract of W. Job-son Horne’s 5 presentation, in which he confirms that pachy-dermia is a consequence of hyperplasia due to persistent lar-yngitis, but he identified rather different causes. In the cutsof a 37-year old patient’s vocal cords, besides hyperplasia,he found excrescence with sulcus in front of and behind it.In 1928, Chevalier Jackson 6 observed 217 patientsduring a 4-year period, and named changes he found on ary-tenoids “contact ulcer”. It was almost 50 years afterMackenzie’s description. Jackson 6 emphasized that this termrefers strictly to nontuberculous lesions, but that any of themcan turn into cancer. He associated these lesion to excessivevocal use, occurring frequently among salesman, doctorswho gave lectures, priests, with the significant influence ofalcohol and tobacco use. In his work about laryngeal kerato-sis in 1946, Clerf 7 also said that pachydermia occurred moreVolumen 71, Broj 6 VOJNOSANITETSKI PREGLED Strana 609Mitroviý MS. Vojnosanit Pregl 2014; 71(6): 608–610.often at alcoholics or excessive vocal use, as in street sellers,for example.From posterior laryngitis to “silent“gastroesophageal refluxThe advance in understanding the posterior laryngealchanges happened in 1968, when first reports on posteriorlaryngitis caused by gastroesophageal reflux occurred. Thatyear Delahunty and Cherry 8 concluded on animal model thatdescribed changes on posterior larynx were caused by gas-troesophageal reflux, while Cherry and Margulies 9 treatedthree patients with posterior laryngitis, and changes disap-peared in six months. In 1970, Delahunty and Ardran 10 triedto explain globus hystericus as a possible manifestation ofreflux esophagitis. In 1972, Delahunty climbed one floorabove larynx, and in “Journal of Laryngology“ published thepaper titled “Acid laryngitis“ 11. In it, he stated as a postulatethat “patients with reflux esophagitis can regurgitate acidcontents even more, especially during the night, whichcauses inflammatory reaction of posterior larynx”.Searching PubMed data base showed a lack of papersuntil 1984, when a research of otorhinolaryngologists fromLjubljana, Vinko Kambiþ and Zora Radšel 12, “Acid poste-rior laryngitis” was published in the same journal in whichDelahunty published the results of his researches. They pub-lished the histological results of biopsy of mucosa in 44 pa-tients with chronic posterior laryngitis caused by acid. Fromphoniatric point of view, Živko Majdevac 13, student ofCzech phoniatric school and founder of Phoniatric Depart-ment of Otorhinolaryngology Clinic in Novi Sad, was alsointerested in these changes. At the VIII Congress of UEP(Union of European Phoniatrics) in 1979 in Köszeg (Hun-gary), he presented his “Classification of dysphonia regard-ing primary etiological factor”, and in the first group of dis-orders – functional disorders, described “contact hyperplasticdysphonia” as a condition which occurs in men whose voiceis in range of baritone or bas, and more often at militarycommanders and teachers. During phonation, posterior thirdsof vocal cords are overcontracted, which causes the appear-ance of circumscriptive yellowish thickening. At the time, heassociated the mentioned changes on vocal processes of ary-tenoid cartilage with gastric hyperacidity, considering it asignificant cofactor.In 1986, Benjamin 14 published a paper on extraesopha-geal complications of gastroesophageal reflux, stating thatgastric contents can get from esophagus into hypopharynxand lungs. In 1989, Wilson et al. 15 published a paper basedon a 23-hour long ambulatory measurement of pH and bi-opsy of posterior larynx in patients with hoarseness, throatburn and globus sensation.In 1991, Olson 16 mentioned laryngopharyngeal mani-festations of gastroesophageal disease. In the same year,James A. Koufman 17 published a paper on otolaryngealmanifestations of gastroesophageal disease in 225 patients,which was the highest number of patients up to the time. Atthat moment, he did not refer to the disorder as LPR yet, butcalled it “occult (silent) gastroeophageal reflux disease”. Apaper on measuring pH on children with gastroesophagealreflux was published in 1992 by Contencin et al. 18.Gastroesophageal vs laryngopharyngeal refluxIn 1996 in the Journal of Voice, Koufman, Sataloffand Toohil 19 published a report from consensus conferenceon LPR, and that was the first paper to refer to the term la-ryngopharyngeal reflux. In 1992, Kamel et al. 20 publishedthe results of prospective study on the use of omeprazole inthe therapy of reflux laryngitis, while Shaw et al. 21 in 1996published a paper with the special emphasis on laryngo-scopic findings before and after the therapy with omepra-zole. In 1997, Wo et al. 22 published a work on empiric useof high doses of omeprazole in patients with posterior lar-yngitis, while Habermann et al. 23 published a study on exiuvantibus therapy with pantoprazole in patients with poste-rior laryngitis in 1999. In 1999, Koufman 24 made a reportabout the treatment of LPR (for the first time with thisname) on I International Symposium about human pepsin,held at the University of York (England). The term of la-ryngeal reflux in children was first mentioned in 2000 byZalzal and Tran 25 in the paper titled “Pediatric gastro-esophageal reflux and laryngopharyngeal reflux”. The termLPR was not yet used in that year, but “laryngitis gastrica”was used instead.In 2000, Koufman et al. 26 found that reflux is observedin 50% of their examined patients with laryngeal and vocalproblems. In June 2001, Belafsky, Postma and Koufman 27published a paper in the Laryngoscope Journal, in which theyexplain their scoring system of reflux findings [Reflux Find-ing Score – (RFS)], questionnaire about the LPR symptomsnamed Reflux Simptom Index (RSI) and support the termLPR. In August of the same year, in the same journal, theyexplained the validity and usefulness of RFS in detail 28. Ayear later, the same team 29, (joined by Amin) made a de-tailed evaluation of RSI usefulness, while Koufman 30 de-finitively explained that LPR is different from classic gastro-esophageal reflux disease.Nissen’s fundoplication as a method for the treatmentof extraesophageal manifestations of gastroesophageal refluxdisease was promoted in the study by Lindstrom et al. 31 in2002. In 2003 Siupsinskiene and Adamonis 32 published apaper on ex iuvantibus diagnosis by administration of omep-razole and monitoring the response. In the same year, Galli etal. 33 published a study based on the hypothesis that biliaryreflux, as well as gastric reflux, has an influence on inflam-matory, precancerous and neoplastic changes of larynx. Thefirst paper on the quality of life in patients with LPR waspublished in 2007 34.In April 2011, during 132nd annual meeting of Ameri-can Laryngology Association (ALA), Jamie A. Koufman 35was awarded for extraordinary contribution to the researchand medical references in laryngology. It was a reward for alifelong work on explaining etiology, pathophysiology, clini-cal findings, diagnostics, therapy and prevention of laryngo-pharyngeal reflux. In order to grasp the importance of hercontribution, it should be mentioned that among the scien-Strana 610 VOJNOSANITETSKI PREGLED Volumen 71, Broj 6Mitroviý MS. Vojnosanit Pregl 2014; 71(6): 608–610.tists who got this award were Chevalier Jackson and JohnKirchner.ConclusionResearches on the influence of laryngopharyngeal re-flux on the organs of otorhinolaryngology region keep on,especially after understanding that this disorder can be astand-alone factor or cofactor in etiology of secretory otitis,chronic rhinitis, nose-sinus polyposis and cancer of aerodi-gestive ways. However, without looking back in the past andpaying tribute to everyone who explained the term and na-ture of laryngopharyngeal reflux, no new researches wouldhave the full sense.REFERENCES1. Ford CN. Evaluation and  management  of  laryngopharyngealreflux. JAMA 2005; 294(12): 1534î40.2. Garcia M.  The complete treatise  on the art of singing. 1stpart. 1st ed. New York: Da Capo Press; 1975î1984. (French)3. Grossman AA, Mathews WH. Keratosis of the larynx with pro-gression to malignancy. Can Med Assoc J 1952; 66(1): 39î41.4. MacKenzie M. Disease of the pharynx, larynx, and trachae. NewYork: William Wood & Co; 1880. p. 347.5. Horne JW. Specimens showing the Pathogenesis of Pachyder-mia laryngis verrucosa et diffusa. Proc R Soc Med. 1908;1(Laryngol Sect): 132–3.6. Jackcon LC. Symposium on the larynx: II.—Etiology andtreatment of contact ulcer of the larynx. Laryngoscope 1933;43(9): 718–21.7. Clerf HL. Keratosis of the larynx.  JAMA 1946;132(14): 823î6.8. Delahunty JE, Cherry J. Experimentally produced vocal cordgranulomas. Laryngoscope 1968; 78(11): 1941î7.9. Cherry J, Margulies S. Contact ulcer of the larynx. Laryngoscope1968; 78(11): 1937î40.10. Delahunty JE, Ardran GM. Globus hystericus-a manifestation ofreflux oesophagitis? J Laryngol Otol 1970; 84(10): 1049î5.11. Delahunty JE. Acid laryngitis. J Laryngol Otol 1972; 86(4): 335– 42.12. Kambiÿ V, Radšel Z. Acid posterior laryngitis. Aetiology, histol-ogy, diagnosis and treatment. J Laryngol Otol 1984; 98(12):1237î40.13. Majdevac Ž. Heiserkeit. In: Frint T, Hirschberg J, editors. Haupt-referate und vorträge. VIII Kongres der Union foniater Eu-ropae; 1979.  Köszeg: Ungarn; 1979. p. 97î118.14. Benjamin SB. Extra-esophageal complications of gastroesopha-geal reflux. J Clin Gastroenterol 1986; 8(Suppl 1): 68î71.15. Wilson JA, White A, von Haacke NP, Maran AG, Heading RC,Pryde A, et al. Gastroesophageal reflux and posterior laryngitis.Ann Otol Rhinol Laryngol 1989; 98(6): 405î10.16. Olson NR. Laryngopharyngeal manifestations of gastroesophagealreflux disease. Otolaryngol Clin North Am 1991; 24(5): 1201î13.17. Koufman JA. The otolaryngologic manifestations of gastro-esophageal  reflux disease (GERD): a clinical investiogation of225 patients using ambulatory 24-hour pH monitoring and anexperimental investigation of the role of acid pepsin in the de-velopment of laryngeal injury. Laryngoscope 1991; 101(4 Pt 2Suppl 53): 1î78.18. Contencin P, Adjoua P, Viala P, Erminy M, Narcy P. Long-termesophageal and oropharyngeal pH-metry in ORL manifesta-tions of gastroesophageal reflux in children. Ann OtolaryngolChir Cervicofac 1992; 109(3): 129î33. (French)19. Koufman J,  Sataloff RT,  Toohill R. Laryngopharyngeal reflux:consensus conference report. J Voice 1996; 10(3): 215î6.20. Kamel P, Kahrilas PJ, Hanson DG, McMahon J, Brenic S. Prospec-tive trial of omeprazole in the treatment of “reflux laryngitis”.Gastroenterology 1992; 102: A93.21. Shaw GY, Searl JP, Young JL, Minner PB. Subjective, laryngo-scopic and acoustic measurements of laryngeal reflux, beforeand after treatment with omeprazole. J Voice 1996; 10(4):410î8.22. Wo JM, Grist WJ, Gussack G, Delgaudio JM, Waring JP. Empirictrial of high- dose omeprazole in patients with posterior laryn-gitis: a prospective study. Am J Gastroenterol 1997; 92(12):2160î5.23. Habermann W, Eherer A, Lindbichler F, Raith J, Friedrich G. Exjuvantibus approach for chronic posterior laryngitis: results ofshort-term pantoprazole therapy.  J Laryngol Otol 1999;113(8): 734î9.24. Koufman JA. Treatment of laryngopharyngeal reflux (LPR).[Abstract]. Presented at the 1st International Symposium onHuman Pepsin; 1999 October 1-2; London: University ofYork; 1999.25. Zalzal GH, Tran LP. Pediatric gastroesophageal reflux and la-ryngopharyngeal reflux. Otolaryngol Clin Nort Am 2000;33(1): 151î61.26. Koufman JA, Amin MR, Panetti M. Prevalence of reflux in 113consecutive patients with laryngeal and voice disorders.Otolaryngol Head Neck Surg 2000; 123(4): 385î8.27. Belafsky CP, Postma NG, Koufman JA. Laryngopharyngeal refluxsymptoms improve before changes in physical findings. La-ryngoscope 2001;111(6): 979î81.28. Belafsky PC, Postma GN, Koufman JA. The validitiy and reliabil-ity of the reflux finding score (RFS). Laryngoscope 2001;111(8): 1313î7.29. Belafsky PC, Postma GN, Amin MR, Koufman JA. Symptoms andfindings of laryngopharyngeal reflux. Ear Nose Troat J 2002;81(9 Suppl 2): 10î3.30. Koufman JA. Laryngopharyngeal reflus is different from classicgastroesophageal reflux disease. Ear Nose Throat J 2002; 81(9Suppl 2): 7î9.31. Lindstrom DR, Wallace J, Loehrl TA, Merati AL, Toohil RJ. Nis-sen fundoplication surgery for extraesophageal manifestationof gastroesophageal reflux (EER). Laryngoscope 2002;112(10): 1762î5.32. Siupsinskiene N, Adamonis K. Diagnostic test with omeprazole inpatients with posterior laryngitis. Medicina (Kaunas) 2003;39(1): 47î55.33. Galli J, Calo L, Agostino S, Cadoni G, Sergi B, Cianci R, et al. Bilereflux as possible risk factor in laryngopharyngeal inflamma-tory and neoplastic lesions. Acta Otorinolaryngol Ital 2003;23(5): 377î82.34. Siupsinskiene N, Adamonis K, Toohil RJ. Quality of life in laryn-gopharyngeal reflux patients. Laryngoscope 2007; 117(3):480î4.35. Kaufman JA.  Biography and facts. Available from:http://www.whoislog.info/profile/charlie-kaufman.htmlReceived on November 3, 2012.Revised on February 28, 2013.Accepted on February 12, 2013.OnLine-First February, 2014.

Terminology, diagnostics and therapy of laryngopharyngeal reflux: A glimpse into the past

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