Eosinophilic esophagitis, efficacy of therapeutic alternatives in adults: a systematic review
e202308067
Keywords:
Eosinophilic esophagitis, Treatment, Efficacy, AdultAbstract
BACKGROUND // Eosinophilic esophagitis is actually the main cause of dysphagia in adults. The choise of therapy must be agreed with the patient. The objective of this study was to review the scientific literature to determine the efficacy of the different therapeutic options for eosinophilic esophagitis in adults.
METHODS // A search for articles was carried out during the month of February 2023 in the databases PubMed, Web of Science, Scopus and Scielo using the search terms: eosinophilic esophagitis, therapeutics and treatment. Clinical trials and observational studies published in the last ten years in adults were selected.
RESULTS // A total of 1,138 articles were obtained, of which 41 were selected after applying the eligibility criteria. Of the available therapies, the most frequently analyzed treatment was swallowed corticosteroids, followed by elimination diets and proton pump inhibitors. Clinical trials predominated. The studies show results on the efficacy of these therapies in histological and clinical remission, both in induction and in the long-term.
CONCLUSIONS // There are basically three therapies for eosinophilic esophagitis in adults, all of them are superior to placebo in histological and clinical response.
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References
Lucendo AJ, Molina-Infante J. Current treatment options and long-term outcomes in patients with eosinophilic esophagitis. Expert review of clinical immunology. 2022;18(8):859-872.
Lucendo AJ, Molina-Infante J, Arias Á, von Arnim U, Brede¬noord AJ, Bussmann C, Amil Dias J, Bove M, González-Cervera J, Larsson H, Miehlke S, Papadopoulou A, Rodríguez-Sánchez J, Ravelli A, Ronkainen J, Santander C, Schoepfer AM, Storr MA, Terreehorst I, Straumann A, Attwood SE. Guidelines on eosinophilic esophagitis: evidence-based statements and recommenda¬tions for diagnosis and management in children and adults. United European Gastroenterol J 2017;5:335-358.
Camargo-Abril N, Santiago-Barrios J, Varela L et al. Esofagitis eosinofílica. Med Int Mex. 2021;37(6):1094-1098.
Simon D, Cianferoni A, Spergel JM, Aceves S, Holbreich M, Venter C, Rothenberg ME, Terreehorst I, Muraro A, Lucendo AJ, Schoepfer A, Straumann A, Simon HU. Eosinophilic esophagitis is characterized by a non-IgE-mediated food hypersensitivity. Allergy 2016;71:611-620.
Pérez Martínez I. Esofagitis Eosinofílica: epidemiología poblacional y análisis del perfil de sensibilización en dos áreas geográficas españolas. 2016. [Tesis doctoral].
Prasad GA, Alexander JA, Schleck CD, Zinsmeister AR, Smyrk TC, Elias RM et al. Epidemiología de la esofagitis eosinofílica durante tres décadas en el condado de Olmsted, Minnesota. Clin Gastroenterol Hepatol. 2009; 7: 1055-1061.
Gutiérrez Junquera C, Fernández Fernández S, Domínguez-Ortega G, Vila Miravet V, García Puig R, García Romero R et al. Recomendaciones para el diagnóstico y manejo práctico de la esofagitis eosinofílica pediátrica. Anales de Pediatría 2020. Junio 2020;92(6):376. e1-376.e10.
Arias Á, Pérez-Martínez I, Tenías JM, Lucendo AJ. Systematic review with meta-analysis: the incidence and prevalence of eosinophilic oesophagitis in children and adults in population-based studies. Aliment Pharmacol Ther. 2016;43(1):3-15.
Furuta GT, Liacouras CA, Collins MH et al. Eosinophilic esophagitis in children and adults: a systematic review and consensus recommendations for diagnosis and treatment. Gastroenterology 2007; 133: 1342-1363.
Molina-Infante J, Bredenoord AJ, Cheng E et al. Proton pump inhibitor-responsive oesophageal eosinophilia: an entity challenging current diagnostic criteria for eosinophilic oesophagitis. Gut 2016; 65: 524-531.
Hudgens S, Evans C, Phillips E, Hill M. Psychometric validation of the Dysphagia Symptom Questionnaire in patients with eosinophilic esophagitis treated with budesonide oral suspension. J Patient Rep Outcomes. 2017;1(1):3.
Albinsson S, Tuomi L, Wennerås C, Larsson H. Patient-Reported Dysphagia in Adults with Eosinophilic Esophagitis: Translation and Validation of the Swedish Eosinophilic Esophagitis Activity Index. Dysphagia. 2022;37(2):286-296.
Wechsler JB, Bolton SM, Amsden K, Wershil BK, Hirano I, Kagalwalla AF. Eosinophilic Esophagitis Reference Score Accurately Identifies Disease Activity and Treatment Effects in Children. Clinical gastroenterology and hepatology: the official clinical practice journal of the American Gastroenterological Association. 2018;16(7):1056-1063.
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Systematic Reviews. 2021;10(1):89.
Balshem H, Helfand M, Schünemann HJ, Oxman AD, Kunz R, Brozek J et al. GRADE guidelines: 3. Rating the quality of evidence. Journal of clinical epidemiology. 2011;64(4):401-406.
Dellon ES, Woosley JT, Arrington A, McGee SJ, Covington J, Moist SE et al. Efficacy of Budesonide vs Fluticasone for Initial Treatment of Eosinophilic Esophagitis in a Randomized Controlled Trial. Gastroenterology. 2019;157(1):65-73.
Miehlke S, Hruz P, Vieth M, Bussmann C, Von Arnim U, Bajbouj M et al. A randomised, double-blind trial comparing budesonide formulations and dosages for short-term treatment of eosinophilic oesophagitis. Gut. 2016;65(3):390-399.
Straumann A, Lucendo AJ, Miehlke S, Vieth M, Schlag C, Biedermann L et al. Budesonide Orodispersible Tablets Maintain Remission in a Randomized, Placebo-Controlled Trial of Patients With Eosinophilic Esophagitis. Gastroenterology. 2020;159(5):1672-1685.
Dellon ES, Lucendo AJ, Schlag C, Schoepfer AM, Falk GW, Eagle G et al. Fluticasone Propionate Orally Disintegrating Tablet (APT-1011) for Eosinophilic Esophagitis: Randomized Controlled Trial. Clinical Gastroenterology and Hepatology. 2022;20(11):2485-94.
Schupack DA, Johnson K, Akambase JA, Geno D, Lavey C, Lennon RJ et al. Histologic response to steroids in eosinophilic esophagitis is dependent on delivery compound. Diseases of the Esophagus. 2022;36(1).
Lucendo AJ, Miehlke S, Schlag C, Vieth M, von Arnim U, Molina-Infante J et al. Efficacy of Budesonide Orodispersible Tablets as Induction Therapy for Eosinophilic Esophagitis in a Randomized Placebo-Controlled Trial. Gastroenterology. 2019;157(1):74-86.
Miehlke S, Schlag C, Lucendo AJ, Biedermann L, Vaquero CS, Schmoecker C et al. Budesonide orodispersible tablets for induction of remission in patients with active eosinophilic oesophagitis: A 6-week open-label trial of the EOS-2 Programme. United European Gastroenterology Journal. 2022;10(3):330-343.
Bhardwaj N, Ishmael F, Lehman E, Bethards D, Ruggiero F, Ghaffari G. Effect of topical beclomethasone on inflammatory markers in adults with eosinophilic esophagitis: A pilot study. Allergy & Rhinology. 2017;8(2):E85-E94.
Kia L, Nelson M, Zalewski A, Gregory D, Gonsalves N, Straumann A et al. Oral delivery of fluticasone powder improves esophageal eosinophilic inflammation and symptoms in adults with eosinophilic esophagitis. Diseases of the Esophagus. 2018;31(12).
Tytor J, Larsson H, Bove M, Johansson L, Bergquist H. Topically applied mometasone furoate improves dysphagia in adult eosinophilic esophagitis - results from a double-blind, randomized, placebo-controlled trial. Scandinavian Journal of Gastroenterology. 2021;56(6):629-634.
Greuter T, Safroneeva E, Bussmann C, Biedermann L, Vavricka SR, Katzka DA et al. Maintenance Treatment Of Eosinophilic Esophagitis With Swallowed Topical Steroids Alters Disease Course Over A 5-Year Follow-up Period In Adult Patients. Clinical Gastroenterology and Hepatology. 2019;17(3):419-428.
Greuter T, Godat A, Ringel A, Almonte HS, Schupack D, Mendoza G et al. Effectiveness and Safety of High- vs Low-Dose Swallowed Topical Steroids for Maintenance Treatment of Eosinophilic Esophagitis: A Multicenter Observational Study. Clinical Gastroenterology and Hepatology. 2021;19(12):2514-2523.
Frandsen LT, Westmark S, Melgaard D, Krarup AL. Effectiveness of PPI treatment and guideline adherence in 236 patients with eosinophilic oesophagitis—Results from the population-based DanEoE cohort shows a low complication rate. United European Gastroenterology Journal. 2021;9(8):910-918.
Vazquez-Elizondo G, Ngamruengphong S, Khrisna M, Devault KR, Talley NJ, Achem SR. The outcome of patients with oesophageal eosinophilic infiltration after an eight-week trial of a proton pump inhibitor. Alimentary Pharmacology and Therapeutics. 2013;38(10):1312-1319.
Gõmez-Torrijos E, García-Rodríguez R, Castro-Jiménez A, Rodríguez-Sanchez J, Méndez Díaz Y, Molina-Infante J. The efficacy of step-down therapy in adult patients with proton pump inhibitor-responsive oesophageal eosinophilia. Alimentary Pharmacology and Therapeutics. 2016;43(4):534-540.
Thakkar KP, Fowler M, Keene S, Iuga A, Dellon ES. Long-term efficacy of proton pump inhibitors as a treatment modality for eosinophilic esophagitis. Digestive and Liver Disease. 2022;54(9):1179-1185.
Visaggi P, Svizzero FB, Del Corso G, Bellini M, Savarino E, de Bortoli N. Efficacy of a Second PPI Course After Steroid-Induced Remission in Eosinophilic Esophagitis Refractory to Initial PPI Therapy. American Journal of Gastroenterology. 2022;117(10):1702-1705.
Kuzumoto T, Tanaka F, Sawada A, Nadatani Y, Otani K, Hosomi S et al. Vonoprazan shows efficacy similar to that of proton pump inhibitors with respect to symptomatic, endoscopic, and histological responses in patients with eosinophilic esophagitis. Esophagus. 2021;18(2):372-379.
Lucendo AJ, Arias A, Gonzalez-Cervera J, Yague-Compadre JL, Guagnozzi D, Angueira T et al. Empiric 6-food elimination diet induced and maintained prolonged remission in patients with adult eosinophilic esophagitis: A prospective study on the food cause of the disease. Journal of Allergy and Clinical Immunology. 2013;131(3):797-804.
Wang L, Mara KC, Ravi K, Wu TT, Smyrk TC, Katzka DA et al. Predictors of histologic response to dietary therapy in eosinophilic oesophagitis. Alimentary Pharmacology and Therapeutics. 2022;56(10):1444-1452.
Zalewski A, Doerfler B, Krause A, Hirano I, Gonsalves N. Long-Term Outcomes of the Six-Food Elimination Diet and Food Reintroduction in a Large Cohort of Adults With Eosinophilic Esophagitis. American Journal of Gastroenterology. 2022;117(12):1963-1970.
Reed CC, Fan C, Koutlas NT, Shaheen NJ, Dellon ES. Food elimination diets are effective for long-term treatment of adults with eosinophilic oesophagitis. Alimentary Pharmacology and Therapeutics. 2017;46(9):836-844.
Molina-Infante J, Arias A, Barrio J, Rodriguez-Sanchez J, Sanchez-Cazalilla M, Lucendo AJ. Four-food group elimination diet for adult eosinophilic esophagitis: A prospective multicenter study. Journal of Allergy and Clinical Immunology. 2014;134(5):1093-1099.
Wolf WA, Jerath MR, Sperry SLW, Shaheen NJ, Dellon ES. Dietary Elimination Therapy Is an Effective Option for Adults With Eosinophilic Esophagitis. Clinical Gastroenterology and Hepatology. 2014;12(8):1272-1279.
Rodríguez-Sánchez J, Gómez Torrijos E, López Viedma B, de la Santa Belda E, Martín Dávila F, García Rodríguez C et al. Efficacy of IgE-targeted vs empiric six-food elimination diets for adult eosinophilic oesophagitis. Allergy. 2014;69(7):936-942.
Dellon ES, Guo R, McGee SJ, Hamilton DK, Nicolai E, Covington J et al. A Novel Allergen-Specific Immune Signature-Directed Approach to Dietary Elimination in Eosinophilic Esophagitis. Clinical and Translational Gastroenterology. 2019;10.
De Rooij WE, Vlieg-Boerstra B, Warners MJ, Van Ampting MTJ, Van Esch B, Eussen S et al. Effect of amino acid-based formula added to four-food elimination in adult eosinophilic esophagitis patients: A randomized clinical trial. Neurogastroenterology and Motility. 2022;34(7).
Warners MJ, Vlieg-Boerstra BJ, Verheij J, Van Hamersveld PHP, Van Rhijn BD, Van Ampting MTJ et al. Esophageal and Small Intestinal Mucosal Integrity in Eosinophilic Esophagitis and Response to an Elemental Diet. American Journal of Gastroenterology. 2017;112(7):1061-1071.
Peterson KA, Byrne KR, Vinson LA, Ying J, Boynton KK, Fang JC et al. Elemental diet induces histologic response in adult eosinophilic esophagitis. American Journal of Gastroenterology. 2013;108(5):759-766.
Hirano I, Collins MH, Assouline-Dayan Y, Evans L, Gupta S, Schoepfer AM et al. RPC4046, a Monoclonal Antibody Against IL13, Reduces Histologic and Endoscopic Activity in Patients With Eosinophilic Esophagitis. Gastroenterology. 2019;156(3):592-603.
Dellon ES, Collins MH, Rothenberg ME, Assouline-Dayan Y, Evans L, Gupta S et al. Long-term Efficacy and Tolerability of RPC4046 in an Open-Label Extension Trial of Patients With Eosinophilic Esophagitis. Clinical Gastroenterology and Hepatology. 2021;19(3):473-483.
Rothenberg ME, Wen T, Greenberg A, Alpan O, Enav B, Hirano I et al. Intravenous anti-IL-13 mAb QAX576 for the treatment of eosinophilic esophagitis. Journal of Allergy and Clinical Immunology. 2015;135(2):500-507.
Hirano I, Dellon ES, Hamilton JD, Collins MH, Peterson K, Chehade M et al. Efficacy of Dupilumab in a Phase 2 Randomized Trial of Adults With Active Eosinophilic Esophagitis. Gastroenterology. 2020;158(1):111-122.
Alexander JA, Ravi K, Enders FT, Geno DM, Kryzer LA, Mara KC et al. Montelukast Does not Maintain Symptom Remission After Topical Steroid Therapy for Eosinophilic Esophagitis. Clinical Gastroenterology and Hepatology. 2017;15(2):214-221.
Straumann A, Hoesli S, Bussmann C, Stuck M, Perkins M, Collins LP et al. Anti-eosinophil activity and clinical efficacy of the CRTH2 antagonist OC000459 in eosinophilic esophagitis. Allergy. 2013;68(3):375-385.
Kavitt RT, Ates F, Slaughter JC, Higginbotham T, Shepherd BD, Sumner EL et al. Randomized controlled trial comparing esophageal dilation to no dilation among adults with esophageal eosinophilia and dysphagia. Diseases of the Esophagus. 2016;29(8):983-991.
Schoepfer AM, Henchoz S, Biedermann L, Schreiner P, Greuter T, Reinhard A et al. Technical feasibility, clinical effectiveness, and safety of esophageal stricture dilation using a novel endoscopic attachment cap in adults with eosinophilic esophagitis. Gastrointestinal Endoscopy. 2021;94(5):912-919.
Kim SJ, Park MI, Kim GH, Lee MW, Jung K, Lee J et al. Practice Patterns for Eosinophilic Esophagitis Patients in Busan and Gyeongnam: A Korean Multicenter Database Study. Journal of Neurogastroenterology and Motility. 2021;27(1):71-77.
Navarro P, Laserna-Mendieta EJ, Guagnozzi D, Casabona S, Perello A, Savarino E et al. Proton pump inhibitor therapy reverses endoscopic features of fibrosis in eosinophilic esophagitis. Digestive and Liver Disease. 2021;53(11):1479-1485.
Moawad FJ, Veerappan GR, Dias JA, Baker TP, Maydonovitch CL, Wong RKH. Randomized Controlled Trial Comparing Aerosolized Swallowed Fluticasone to Esomeprazole for Esophageal Eosinophilia. American Journal of Gastroenterology. 2013;108(3):366-372.
Philpott H, Nandurkar S, Royce SG, Thien F, Gibson PR. A prospective open clinical trial of a proton pump inhibitor, elimination diet and/or budesonide for eosinophilic oesophagitis. Alimentary Pharmacology and Therapeutics. 2016;43(9):985-993.
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Copyright (c) 2023 Silvia Espina Cadena, Patricia Camo Monterde, María Badía Martínez, Yolanda Martínez Santos
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