Eosinophilic esophagitis in Egyptian adult patients presenting with upper gastrointestinal symptoms

Shereen Shoukry Hunter, Dina Omar Helmy, Naglaa Aly Zayed, Tamer Mohamed El-Tayeb, Magdy Amin El-Serafy

Endemic Medicine Department and Gastrointestinal Endoscopy and Liver Unit, Faculty of Medicine, Cairo University, Cairo, Egypt.
Endoscopy Unit, New Kasr El-Ainy Teaching Hospital, Cairo, Egypt.
Pathology Department, Faculty of Medicine, Cairo University, Cairo, Egypt.

DOI: 10.4236/ojgas.2014.42015                

Abstract

Background and Study Aim: Eosinophilic esophagitis (EoE) is a clinicopathological disease characterized by esophageal dysfunction and marked esophageal eosinophilic infiltration. It shows a marked increase in incidence and prevalence and has been associated with gastroesophageal reflux disease (GERD). The aim of this work was to detect the prevalence of EoE in Egyptian adult patients presenting with upper gastrointestinal symptoms and to clarify its clinical pattern and the possibility of its overlap with GERD. Patients and Methods: The study included 91 adult patients presenting with various upper gastrointestinal symptoms. Upper gastrointestinal endoscopy was done and esophageal biopsies were taken. The presence of >15 eosinophils per high power field together with a history of intake of proton pump inhibitors for at least 3 weeks without improvement was used as prerequisite diagnostic criteria for EoE. Results: Classification of the patients was based on both endoscopic and histo-pathological findings. Accordingly, out of the 91 patients, 70 had GERD (76.9%); 58 of them had erosive reflux disease (ERD) and 12 had endoscopically normal esophagus but with histopathological changes compatible with reflux esophagitis and were classified as non erosive reflux disease (NERD). Eighteen patients had normal endoscopic and histopathological esophagus (19.8%), and 3 patients had EoE (3.3%), with an overlap between ERD and EoE in one patient. The mean age of EoE patients was 41.6 ± 11.7 years. Two of them were males and one was a female. All of the 3 patients complained of dysphagia and none complained of heartburn. The endoscopists did not report any endoscopic findings characteristic of EoE. Conclusion: The prevalence of EoE is low in adult Egyptian patients presenting with upper gastrointestinal symptoms. Dysphagia is the main presenting symptom of EoE while heartburn is not characteristic of the disease. Normal esophagus endoscopically does not exclude EoE.

Keywords

Eosinophilic Esophagitis (EoE); Adults; Gastroesophageal Reflux Disease (GERD); Egypt

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Liacouras, C.A., Furuta, G.T., Hirano, I., Atkins, D., Attwood, S.E., Bonis, P.A., Burks, A.W., Chehade, M., Collins, M.H., Dellon, E.S., Dohil, R., Falk, G.W., Gonsalves, N., Gupta, S.K., Katzka, D.A., Lucendo, A.J., Markowitz, J.E., Noel, R.J., Odze, R.D., Putnam, P.E., Richter, J.E., Romero, Y., Ruchelli, E., Sampson, H.A., Schoepfer, A., Shaheen, N.J., Sicherer, S.H., Spechler, S., Spergel, J.M., Straumann, A., Wershil, B.K., Rothenberg, M.E. and Aceves, S.S. (2011) Eosinophilic esophagitis: Updated consensus recommendations for children and adults. Journal of Allergy and Clinical Immunology, 128, 3-20. http://dx.doi.org/10.1016/j.jaci.2011.02.040
[2]	Croese, J., Fairley, S.K., Masson, J.W., Chong, A.K., Whitaker, D.A., Kanowski, P.A. and Walker, N.I. (2003) Clinical and endoscopic features of eosinophilic esophagitis in adults. Gastrointest Endosc, 58, 516-522. http://dx.doi.org/10.1067/S0016-5107(03)01870-4
[3]	Straumann, A. and Beglinger, C. (2006) Eosinophilic esophagitis: The endoscopist’s enigma. Gastrointest Endosc, 63, 13-15. http://dx.doi.org/10.1016/j.gie.2005.09.010
[4]	Dellon, E.S, Erichsen, R., Pedersen, L., Shaheen, N.J., Baron, J.A., Sørensen, H.T. and Vyberg, M. (2013) Development and validation of a registry-based definition of eosinophilic esophagitis in Denmark. World Journal of Gastroenterology, 19, 503-510. http://dx.doi.org/10.3748/wjg.v19.i4.503
[5]	Furuta, G.T., Liacouras, C.A., Collins, M.H., Gupta, S.K., Justinich, C., Putnam, P.E., Bonis, P., Hassall, E., Straumann, A., Rothenberg, M.E. and Members of the First International Gastrointestinal Eosinophil Research Symposium (FIGERS) Subcommittees (2007) Eosinophilic esophagitis in children and adults: A systematic review and consensus recommendations for diagnosis and treatment. Gastroenterology, 133, 1342-1363. http://dx.doi.org/10.1053/j.gastro.2007.08.017
[6]	Gonsalves, N. and Kahrilas, P.J. (2009) Eosinophilic oesophagitis in adults. Neurogastroenterology & Motility, 21, 1017-1026. http://dx.doi.org/10.1111/j.1365-2982.2009.01307.x
[7]	Sgouros, S.N. (2006) Refractory heartburn to proton pump inhibitors: Epidemiology, etiology and management. Digestion, 73, 218-227.
[8]	Richter, J.E. (2007) How to manage refractory GERD. Nature Clinical Practice Gastroenterology & Hepatology, 4, 658-664. http://dx.doi.org/10.1038/ncpgasthep0979
[9]	Fass, R. and Gasiorowska, A. (2008) Refractory GERD: What is it? Current Gastroenterology Reports, 10, 252-257. http://dx.doi.org/10.1007/s11894-008-0052-5
[10]	Fox, V.L., Nurko, S. and Furuta, G.T. (2002) Eosinophilic esophagitis: It’s not just kid’s stuff. Gastrointest Endosc, 56, 260-270. http://dx.doi.org/10.1016/S0016-5107(02)70188-0
[11]	Vasilopoulos, S., Murphy, P., Auerbach, A., Massey, B.T., Shaker, R., Stewart, E., Komorowski, R.A. and Hogan, W.J. (2002) The small-caliber esophagus: An unappreciated cause of dysphagia for solids in patients with eosinophilic esophagitis. Gastrointest Endosc, 55, 99-106. http://dx.doi.org/10.1067/mge.2002.118645
[12]	Straumann, A., Spichtin, H.P., Grize, L., Bucher, K.A., Beglinger, C. and Simon, H.U. (2003) Natural history of primary eosinophilic esophagitis: A follow-up of 30 adult patients for up to 11.5 years. Gastroenterology, 125, 1660-1669. http://dx.doi.org/10.1053/j.gastro.2003.09.024
[13]	Ruchelli, E., Wenner, W., Voytek, T., Brown, K. and Liacouras, C. (1999) Severity of esophageal eosinophilia predicts response to conventional gastroesophageal reflux therapy. Pediatric and Developmental Pathology, 2, 15-18. http://dx.doi.org/10.1007/s100249900084
[14]	Sgouros, S.N., Bergele, C. and Mantides, A. (2006) Eosinophilic esophagitis in adults: A systematic review. European Journal of Gastroenterology & Hepatology, 18, 211-217. http://dx.doi.org/10.1097/00042737-200602000-00015
[15]	Dellon, E.S., Gibbs, W.B., Fritchie, K.J., Rubinas, T.C., Wilson, L.A., Woosley, J.T. and Shaheen, N.J. (2009) Clinical, endoscopic, and histologic findings distinguish eosinophilic esophagitis from gastroesophageal reflux disease. Clinical Gastroenterology and Hepatology, 7, 1305-1313. http://dx.doi.org/10.1016/j.cgh.2009.08.030
[16]	Armstrong, D., Bennett, J.R., Blum, A.L., Dent, J., De Dombal, F.T., Galmiche, J.P., Lundell, L., Margulies, M., Richter, J.E., Spechler, S.J., Tytgat, G.N. and Wallin, L. (1996) The endoscopic assesment of esophagitis: A progress report on observer agreement. Gastroenterology, 111, 85-92. http://dx.doi.org/10.1053/gast.1996.v111.pm8698230
[17]	Straumann, A. and Simon, H.U. (2005) Eosinophilic esophagitis: Escalating epidemiology? Journal of Allergy and Clinical Immunology, 115, 418-419. http://dx.doi.org/10.1016/j.jaci.2004.11.006
[18]	Spergel, J.M., Brown-Whitehorn, T.F., Beausoleil, J.L., Franciosi, J., Shuker, M., Verma, R. and Liacouras, C.A. (2009) 14 years of eosinophilic esophagitis: Clinical features and prognosis. Journal of Pediatric Gastroenterology and Nutrition, 48, 30-36. http://dx.doi.org/10.1097/MPG.0b013e3181788282
[19]	Almansa, C., Devault, K.R. and Achem, S.R. (2011) A comprehensive review of eosinophilic esophagitis in adults. Journal of Clinical Gastroenterology, 45, 658-664. http://dx.doi.org/10.1097/MCG.0b013e318211f95b
[20]	Ronkainen, J., Talley, N.J., Aro, P., Storskrubb, T., Johansson, S.E., Lind, T., Bolling-Sternevald, E., Vieth, M., Stolte, M., Walker, M.M. and Agréus, L. (2007) Prevalence of oesophageal eosinophils and eosinophilic oesophagitis in adults: The population-based Kalixanda study. Gut, 56, 615-620. http://dx.doi.org/10.1136/gut.2006.107714
[21]	Veerappan, G.R., Perry, J.L., Duncan, T.J., Baker, T.P., Maydonovitch, C., Lake, J.M., Wong, R.K. and Osgard, E.M. (2009) Prevalence of eosinophilic esophagitis in an adult population undergoing upper endoscopy: A prospective study. Clinical Gastroenterology and Hepatology, 7, 420-426. http://dx.doi.org/10.1016/j.cgh.2008.10.009
[22]	Gupta, S.K., Fitzgerald, J.F., Chong, S.K., Croffie, J.M. and Collins, M.H. (1997) Vertical lines in distal esophageal mucosa (VLEM): A true endoscopic manifestation of esophagitis in children? Gastrointest Endosc, 45, 485-489. http://dx.doi.org/10.1016/S0016-5107(97)70178-0
[23]	Moy, N., Heckman, M.G., Gonsalves, N., Achem, S.R. and Hirano, I. (2011) Inter-observer agreement on endoscopic esophageal findings in eosinophilic esophagitis (EoE). Gastroenterology, 140, S236.
[24]	Peery, A.F., Cao, H., Dominik, R., Shaheen, N.J. and Dellon, E.S. (2011) Variable reliability of endoscopic findings with white-light and narrow-band imaging for patients with suspected eosinophilic esophagitis. Clinical Gastroenterology and Hepatology, 9, 475-480. http://dx.doi.org/10.1016/j.cgh.2011.02.026
[25]	Parfitt, J.R., Gregor, J.C., Suskin, N.G., Jawa, H.A. and Driman, D.K. (2006) Eosinophilic esophagitis in adults: Distinguishing features from gastroesophageal reflux disease: A study of 41 patients. Modern Pathology, 19, 90-96. http://dx.doi.org/10.1038/modpathol.3800498
[26]	Mikhak, Z. and Luster, D. (2009) Chemokines in cell movement and allergic inflammation. In: Adkinson Jr., N.F., Busse, W.W., Bochner, B.S., Holgate, S.T., Simons, E.R. and Lemanske Jr., R.F., Eds., Middleton’s Allergy Principles & Practice, 7th Edition, Mosby Elsevier, New York, 181-201. http://dx.doi.org/10.1016/B978-0-323-05659-5.00011-5
[27]	Potter, J.W., Saeian, K., Staff, D., Massey, B.T., Komorowski, R.A., Shaker, R. and Hogan, W.J. (2004) Eosinophilic esophagitis in adults: An emerging problem with unique esophageal features. Gastrointest Endosc, 59, 355-361. http://dx.doi.org/10.1016/S0016-5107(03)02713-5
[28]	Carr, S. and Watson, W. (2011) Eosinophilic esophagitis. Allergy Asthma Clinical Immunology, 7, S8. http://dx.doi.org/10.1186/1710-1492-7-S1-S8
[29]	Noel, R.J., Putnam, P.E. and Rothenberg, M.E. (2004) Eosinophilic esophagitis. The New England Journal of Medicine, 351, 940-941. http://dx.doi.org/10.1056/NEJM200408263510924
[30]	Brown-Whitehorn, T.F. and Spergel, J.M. (2010) The link between allergies and eosinophilic esophagitis: Implications for management strategies. Expert Review of Clinical Immunology, 6, 101-109. http://dx.doi.org/10.1586/eci.09.74
[31]	Klauser, A.G., Schindlbeck, N.E. and Muller-Lissner, S.A. (1990) Symptoms in gastrooesophageal reflux disease. Lancet, 335, 205-208. http://dx.doi.org/10.1016/0140-6736(90)90287-F
[32]	Kapel, R.C., Miller, J.K., Torres, C., Aksoy, S., Lash, R. and Katzka, D.A. (2008) Eosinophilic esophagitis: A prevalent disease in the United States that affects all age groups. Gastroenterology, 134, 1316-1321. http://dx.doi.org/10.1053/j.gastro.2008.02.016
[33]	Attwood, S.E., Smyrk, T.C., Demeester, T.R. and Jones, J.B. (1993) Esophageal eosinophilia with dysphagia. A distinct clinicopathologic syndrome. Digestive Diseases and Sciences, 38, 109-116. http://dx.doi.org/10.1007/BF01296781
[34]	Kim, H.P., Vance, R.B., Shaheen, N.J. and Dellon, E.S. (2012) The prevalence and diagnostic utility of endoscopic features of eosinophilic esophagitis: A meta-analysis. Clinical Gastroenterology and Hepatology, 10, 988-996. http://dx.doi.org/10.1016/j.cgh.2012.04.019
[35]	Mackenzie, S.H., Go, M., Chadwick, B., Thomas, K., Fang, J., Kuwada, S., Lamphier, S., Hilden, K. and Peterson, K. (2008) Eosinophilic oesophagitis in patients presenting with dysphagia—A prospective analysis. Alimentary Pharmacology & Therapeutics, 28, 1140-1146. http://dx.doi.org/10.1111/j.1365-2036.2008.03795.x
[36]	Orenstein, S.R., Shalaby, T.M., Di Lorenzo, C., Putnam, P.E., Sigurdsson, L., Mousa, H. and Kocoshis, S.A. (2000) The spectrum of pediatric eosinophilic esophagitis beyond infancy: A clinical series of 30 children. American Journal of Gastroenterology, 95, 1422-1430. http://dx.doi.org/10.1111/j.1572-0241.2000.02073.x
[37]	Rothenberg, M.E., Mishra, A., Collins, M.H. and Putnam, P.E. (2001) Pathogenesis and clinical features of eosinophilic esophagitis. Journal of Allergy and Clinical Immunology, 108, 891-894. http://dx.doi.org/10.1067/mai.2001.120095
[38]	Lee, R.G. (1985) Marked eosinophilia in esophageal mucosal biopsies. American Journal of Surgical Pathology, 9, 475-479. http://dx.doi.org/10.1097/00000478-198507000-00002
[39]	Steiner, S.J., Gupta, S.K., Croffie, J.M. and Fitzgerald, J.F. (2004) Correlation between number of eosinophils and reflux index on same day esophageal biopsy and 24 hour esophageal pH monitoring. American Journal of Gastroenterology, 99, 801-805. http://dx.doi.org/10.1111/j.1572-0241.2004.04170.x
[40]	Desai, T.K., Stecevic, V., Chang, C.H., Goldstein, N.S., Badizadegan, K. and Furuta, G.T. (2005) Association of eosinophilic inflammation with esophageal food impaction in adults. Gastrointestinal Endoscopy, 61, 795-801. http://dx.doi.org/10.1016/S0016-5107(05)00313-5
[41]	Remedios, M., Campbell, C., Jones, D.M. and Kerlin, P. (2006) Eosinophilic esophagitis in adults: Clinical, endoscopic, histologic findings, and response to treatment with fluticasone propionate. Gastrointestinal Endoscopy, 63, 3-12. http://dx.doi.org/10.1016/j.gie.2005.07.049
[42]	Morrow, J.B., Vargo, J.J., Goldblum, J.R. and Richter, J.E. (2001) The ringed esophagus: Histological features of GERD. American Journal of Gastroenterology, 96, 984-989. http://dx.doi.org/10.1111/j.1572-0241.2001.03682.x
[43]	Dent, J., El-Serag, H.B., Wallander, M.A. and Johansson, S. (2005) Epidemiology of gastrooesophageal reflux disease: A systematic review. Gut, 54, 710-717. http://dx.doi.org/10.1136/gut.2004.051821
[44]	Voutilainen, M., Sipponen, P., Mecklin, J.P., Juhola, M. and Färkkilä, M. (2000) Gastroesophageal reflux disease: Prevalence, clinical, endoscopic and histopathologic findings in 1,128 consecutive patients referred for endoscopy due to dyspeptic and reflux symptoms. Digestion, 61, 6-13. http://dx.doi.org/10.1159/000007730
[45]	Foroutan, M., Norouzi, A., Molaei, M., Mirbagheri, S.A., Irvani, S., Sadeghi, A., Derakhshan, F., Tavassoli, S., Besharat, S. and Zali, M. (2010) Eosinophilic esophagitis in patients with refractory gastroesophageal reflux disease. Digestive Diseases and Sciences, 55, 28-31. http://dx.doi.org/10.1007/s10620-008-0706-z
[46]	Molina-Infante, J., Ferrando-Lamana, L., Mateos-Rodriguez, J.M., Pérez-Gallardo, B. and Prieto-Bermejo, A.B. (2008) Overlap of reflux and eosinophilic esophagitis in two patients requiring different therapies: A review of the literature. World Journal of Gastroenterology, 14, 1463-1466. http://dx.doi.org/10.3748/wjg.14.1463
[47]	Lind, T., Havelund, T., Carlsson, R., Anker-Hansen, O., Glise, H., Hernqvist, H., Junghard, O., Lauritsen, K., Lundell, L., Pedersen, S.A. and Stubberöd, A. (1997) Heartburn without oesophagitis: Efficacy of omeprazole therapy and features determining therapeutic response. Scandinavian Journal of Gastroenterology, 32, 974-979. http://dx.doi.org/10.3109/00365529709011212
[48]	Smout, A.J.P.M. (1997) Endoscopy-negative acid reflux disease. Alimentary Pharmacology & Therapeutics, 11, 81-85. http://dx.doi.org/10.1111/j.1365-2036.1997.tb00798.x
[49]	Modlin, I.M., Hunt, R.H., Malfertheiner, P., Moayyedi, P., Quigley, E.M., Tytgat, G.N., Tack, J., Heading, R.C., Holtman, G., Moss, S.F. and Vevey NERD Consensus Group (2009) Diagnosis and management of non-erosive reflux disease—The Vevey NERD Consensus Group. Digestion, 80, 74-88.
[50]	Weusten, B.L., Akkermans, L.M., vanBerge-Henegouwen, G.P. and Smout, A.J. (1995) Symptom perception in gastroesophageal reflux disease is dependent on spatiotemporal reflux characteristics. Gastroenterology, 108, 1739-1744. http://dx.doi.org/10.1016/0016-5085(95)90135-3
[51]	Cicala, M., Emerenziani, S., Caviglia, R., Guarino, M.P., Vavassori, P., Ribolsi, M., Carotti, S., Petitti, T. and Pallone, F. (2003) Intraoesophageal distribution and perception of acid reflux in patients with non-erosive gastro-oesophageal reflux disease. Alimentary Pharmacology & Therapeutics, 18, 605-613. http://dx.doi.org/10.1046/j.1365-2036.2003.01702.x
[52]	Cicala, M., Gabbrielli, A., Emerenziani, S., Guarino, M.P., Ribolsi, M., Caviglia, R. and Costamagna, G. (2005) Effect of endoscopic augmentation of the lower oesophageal sphincter (Gatekeeper reflux repair system) on intra-oesophageal dynamic characteristics of acid reflux. Gut, 54, 183-186. http://dx.doi.org/10.1136/gut.2004.040501
[53]	Emerenziani, S., Zhang, X., Blondeau, K., Silny, J., Tack, J., Janssens, J. and Sifrim, D. (2005) Gastric fullness, physical activity, and proximal extent of gastroesophageal reflux. American Journal of Gastroenterology, 100, 1251-1256. http://dx.doi.org/10.1111/j.1572-0241.2005.41695.x
[54]	Bredenoord, A.J., Weusten, B.L., Curvers, W.L., Timmer, R. and Smout, A.J. (2006) Determinants of perception of heartburn and regurgitation. Gut, 55, 313-318. http://dx.doi.org/10.1136/gut.2005.074690
[55]	Bredenoord, A.J., Weusten, B.L., Timmer, R. and Smout, A.J. (2006) Characteristics of gastroesophageal reflux in symptomatic patients with and without excessive esophageal acid exposure. American Journal of Gastroenterology, 101, 2470-2475. http://dx.doi.org/10.1111/j.1572-0241.2006.00945.x