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The Other Causes of Severe Enteropathy with Villous Atrophy Non-Responsive to a Gluten-Free Diet

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Refractory Celiac Disease

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Abstract

The first step in approaching someone with refractory celiac disease is to confirm the original diagnosis of celiac disease. This involves reviewing haplotype testing, prior serologies, histology, family history, and the response both clinically and histologically to a gluten-free diet. If the original diagnosis is called into question, alternative causes of severe enteropathy with villous atrophy need to be considered. In this chapter we will focus on these alternative causes, and particularly focus on those that lead to clinical symptoms and signs of malabsorption and diarrhea, in addition to villous atrophy. For this reason, we will not review causes of villous atrophy with no accompanying malabsorption, such as peptic duodenitis. We will also not review very uncommon causes such as macroglobulinemia, lipid storage disorders, diffuse signet cell carcinoma, tuberculosis, lymphangiectasia, abetalipoproteinemia, and amyloidosis. Crohn’s disease is another potential cause of villous atrophy that will not be discussed.

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References

  1. Amadi B, Besa E, Zyambo K, Kaonga P, Louis-Auguste J, Chandwe K, et al. Impaired barrier function and autoantibody generation in malnutrition enteropathy in Zambia. EBioMedicine. 2017;22:191–9.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Guerrant R, DeBoer M, Moore S, Scharf R, Lima A. The impoverished gut - a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol. 2013;10:220–9.

    Article  PubMed  Google Scholar 

  3. Platts-Mills J, Babji S, Bodhidatta L, Gratz J, Haque R, Havt A, et al. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite bortih cohort study (MAL-ED). Lancet Glob Health. 2015;3(9):e564–75.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dewey K, Adu-Afarwuah S. Systematic review of the efficacy and effectiveness of complementary feeding interventions in developing countries. Matern Child Nutr. 2008;4:24–85.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bhutta Z, Ahmed T, Black R, Cousens S, Dewey K, Giugliani E, et al. What works? Interventions for maternal and child undernutrition and survival. Lancet. 2008;371:417–40.

    Article  PubMed  Google Scholar 

  6. Levine M. Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol. 2010;8:129.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Campbell D, Murch S, Elia M, Sullivan P, Sanyang M, Jobarteh B, et al. Chronic T cell-mediated enteropathy in rural West African children: relationship with nutritional status and small bowel function. Pediatr Res. 2003;54(3):306–11.

    Article  PubMed  Google Scholar 

  8. Akram S, Murray J, Pardi D, Alexander G, Schaffner J, Russo P, et al. Adult autoimmune enteropathy: Mayo Clinic Rochester experience. Clin Gastroenterol Hepatol. 2007 Nov;5(11):1282–90.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Sharma A, Choung R, Wang X, Russo P, Wu T, Nehra V, et al. Features of adult autoimmune enteropathy compared with refractory celiac disease. Clin Gastroenterol Hepatol. 2018;16(6):877–83.e1.

    Article  PubMed  Google Scholar 

  10. Mais D, Mulhall B, Adolphson K, Yamamoto K. Thymoma-associated autoimmune enteropathy. A report of two cases. Am J Clin Pathol. 1999;112(6):810–5.

    Article  CAS  PubMed  Google Scholar 

  11. Umetsu S, Brown I, Langner C, Lauwers G. Autoimmune enteropathies. Virchows Arch. 2018;472(1):55–66.

    Article  CAS  PubMed  Google Scholar 

  12. Duclaux-Loras R, Charbit-Henrion F, Neven B, Nowak J, Collardeau-Frachon S, Malcus C, et al. Clinical heterogeneity of immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome: a French multicenter retrospective study. Clin Transl Gastroenterol. 2018;9(10):201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Parlato M, Charbit-Henrion F, Abi Nader E, Begue B, Guegan N, Bruneau J, et al. Efficacy of ruxolitinib therapy in a patient with severe enterocolitis associated with a STAT3 gain-of-function mutation. Gastroenterology. 2019;156(4):1206–10.

    Article  PubMed  Google Scholar 

  14. Charbit-Henrion F, Jeverica A, Begue B, Markelj G, Parlato M, Avcin S, et al. Deficiency in mucosa-associated lymphoid tissue lymphoma translocation 1: a novel cause of IPEX-like syndrome. J Pediatr Gastroenterol Nutr. 2017;64(3):378–84.

    Article  PubMed  Google Scholar 

  15. Boland B, Widjaja C, Banno A, Zhang B, Kim S, Stoven S, et al. Immunodeficiency and autoimmune enterocolopathy linked to NFAT5 haploinsufficiency. J Immunol. 2015;195(6):2551–60.

    Article  Google Scholar 

  16. Lei A, Azhari H, Raman M. A117 a case of adult autoimmune enteropathy and primary sclerosing cholangitis. J Can Assoc Gastroenterol. 2020;3(Supplement_1):135–7.

    Article  PubMed Central  Google Scholar 

  17. Malamut G, Verkarre V, Suarez F, Viallard J, Lascaux A-S, Cosnes J, et al. The enteropathy associated with common variable immunodeficiency: the delineated frontiers with celiac disease. Am J Gastroenterol. 2010;105(10):2262–75.

    Article  CAS  PubMed  Google Scholar 

  18. Martinez-Gallo M, Radigan L, Almejun M, Martinez-Pomar N, Matamoros N, Cunningham-Rundles C. TACI mutations and impaired B-cell function in subjects with CVID and healthy heterozygotes. J Allergy Clin Immunol. 2012;131(2):468–76.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Biagi F, Bianchi P, Zilli A, Marchese A, Luinetti O, Lougaris V, et al. The significance of duodenal mucosal atrophy in patients with common variable immunodeficiency: a clinical and histopathologic study. Am J Clin Pathol. 2012;138(2):185–9.

    Article  PubMed  Google Scholar 

  20. Venhoff N, Emmerich F, Neagu M, Salzer U, Koehn C, Driever S, et al. The role of HLA DQ2 and DQ8 in dissecting celiac-like disease in common variable immunodeficiency. J Clin Immunol. 2013;33(5):909–16.

    Article  CAS  PubMed  Google Scholar 

  21. Cunningham-Rundles C. How I treat common variable immune deficiency. Blood. 2010;116(1):7–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Skinnider B. Lymphoproliferative disorders of the gastrointestinal tract. Arch Pathol Lab Med. 2018;142:44–52.

    Article  CAS  PubMed  Google Scholar 

  23. Van Vliet C, Spagnolo D. T- and NK-cell lymphoproliferative disorders of the gastrointestinal tract: review and update. Pathology. 2020;52(1):128–41.

    Article  PubMed  Google Scholar 

  24. Sharma A, Oishi N, Boddicker R, Hu G, Benson H, Ketterling R, et al. Recurrent STAT3-JAK2 fusions in indolent T-cell lymphoproliferative disorder of the gastrointestinal tract. Blood. 2018;131(20):2262–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Matnani R, Ganapathi K, Lewis S, Green P, Alobeid B, Bhagat G. Indolent T- and NK-cell lymphoproliferative disorders of the gastrointestinal tract: a review and update. Hematol Oncol. 2017;35(1):3–16.

    Article  CAS  PubMed  Google Scholar 

  26. Hujoel I, Rubio-Tapia A. Sprue-like enteropathy associated with olmesartan: a new kid on the enteropathy block. GE Port J Gastroenterol. 2016 Mar;23(2):61–5.

    Article  PubMed  PubMed Central  Google Scholar 

  27. DeGaetani M, Tennyson C, Lebwohl B, Lewis S, Abu Daya H, Arguelles-Grande C, et al. Villous atrophy and negative celiac serology: a diagnostic and therapeutic dilemma. Am J Gastroenterol. 2013 May;108(5):647–53.

    Article  CAS  PubMed  Google Scholar 

  28. Rubio-Tapia A, Herman M, Ludvigsson J, Kelly D, Mangan T, Wu T, et al. Severe spruelike enteropathy associated with olmesartan. Mayo Clin Proc. 2012 Aug;87(8):732–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Marietta E, Nadeau A, Cartee A, Singh I, Rishi A, Choung R, et al. Immunopathogenesis of olmesartan-associated enteropathy. Aliment Pharmacol Ther. 2015 Dec;42(11):1303–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Weclawiak H, Ould-Mohamed A, Bournet B, Guilbeau-Frugier C, Fortenfant F, Muscari F, et al. Duodenal villous atrophy: a cause of chronic diarrhea after solid-organ transplantation. Am J Transplant. 2011 Mar;11(3):575–82.

    Article  CAS  PubMed  Google Scholar 

  31. Tai F, McAlindon M. NSAIDs and the small bowel. Curr Opin Gastroenterol. 2018 May;34(3):175–82.

    Article  CAS  PubMed  Google Scholar 

  32. Shin S, Noh C, Lim S, Lee K, Lee K. Non-steroidal anti-inflammatory drug-induced enteropathy. Intest Res. 2017;15(4):446–55.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Bosca M, Anon R, Mayordomo E, Villagrasa R, Balza N, Amoros C, et al. Methotreate induced sprue-like syndrome. World J Gastroenterol. 2008;14(45):7009–11.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Houtman P, Hofstra S, Spoelstra P. Non-coeliac sprue possibly related to methotrexate in a rheumatoid arthritis patient. Neth J Med. 1995;47(3):113–6.

    Article  CAS  PubMed  Google Scholar 

  35. Ziegler T, Fernandez-Estivariz C, Gu L, Fried M, Leader L. Severe villus atrophy and chronic malabsorption induced by azathioprine. Gastroenterology. 2003;124:1950–7.

    Article  PubMed  Google Scholar 

  36. Gentile N, D'Souza A, Fujii L, Wu T, Murray J. Association between ipilimumab and celiac disease. Mayo Clin Proc. 2013;88(4):414–7.

    Article  CAS  PubMed  Google Scholar 

  37. Arnouk J, Mathew D, Nulton E, Rachakonda V. A celiac disease phenotype after checkpoint inhibitor exposure: an example of immune dysregulation after immunotherapy. ACG Case Rep J. 2019;6:1–3.

    Article  Google Scholar 

  38. Alsaadi D, Shah N, Charabaty A, Atkins M. A case of checkpoint inhibitor-induced celiac disease. J Immunother Cancer. 2019;7:203.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Duval L, Habes S, Chatellier T, Guerzider P, Bossard C, Masliah C, et al. Nivolumab-induced celiac-like enteropathy in patient with metastatic renal cell carcinoma: case report and review of the literature. Clin Case Rep. 2019;7:1689–93.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Staffas A, Burgos da Silva M, van den Brink M. The intestinal microbiota in allogeneic hematopoietic cell transplant and graft-versus-host disease. Blood. 2017;129(8):927–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Nalle S, Zuo L, Ong M, Singh G, Worthylake A, Choi W, et al. Graft-versus-host disease propagation depends on increased intestinal epithelial tight junction permeability. J Clin Invest. 2019;129(2):902–14.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Borges L, Vilela E, Ferrari M, Cunha A, Vasconcelos A, Torres H. Diagnosis of acute graft-versus-host disease in the gastrointestinal tract of patietns undergoing allogeneic hematopoietic stem cell transplantation. A descriptive and critical study of diagnostic tests. Hematol Transfus Cell Ther. 2020;42(3):245–51.

    Article  PubMed  Google Scholar 

  43. de Serre N, Reijasse D, Verkarre V, Canioni D, Colomb V, Haddad E, et al. Chronic intestinal graft-versus-host disease: clinical, histological and immunohistochemical analysis of 17 children. Bone Marrow Transplant. 2002;29:223–30.

    Article  Google Scholar 

  44. Chen Y, Shah N, Renteria A, Cutler C, Jansson J, Akbari M, et al. Vedolizumab for prevention of gravt-versus-host disease after allogeneic hematopoietic stem cell transplantation. Blood Adv. 2019;3(23):4136–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jones J, Avritscher E, Cooksley C, Michelet M, Bekele B, Elting L. Epidemiology of treatment-associated mucosal injury after treatment with newer regimens for lymphoma, breast, lung, or colorectal cancer. Support Care Cancer. 2006;14(6):505–15.

    Article  PubMed  Google Scholar 

  46. Dranitsaris G, Maroun J, Shah A. Severe chemotherapy-induced diarrhea in patients with colorectal cancer: a cost of illness analysis. Support Care Cancer. 2005;13(5):318–24.

    Article  PubMed  Google Scholar 

  47. Keefe D, Brealey J, Goland G, Cummins A. Chemotherapy for cancer causes apoptosis that precedes hypoplasia in crypts of the small intestine in humans. Gut. 2000;47(5):632–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ribeiro R, Wanderley C, Wong D, Mota J, Leite C, Souza M, Cunha FQ, et al. Irinotecan- and 5-fluorouracil-induced intestinal mucositis: insights into pathogenesis and therapeutic perspectives. Cancer Chemother Pharmacol. 2016;78:881–93.

    Article  CAS  PubMed  Google Scholar 

  49. Shukla P, Gupta D, Bisht S, Pant M, Bhatt M, Gupta R, et al. Circadian variation in radiation-induced intestinal mucositis in patients with cervical carcinoma. Cancer. 2010;116(8):2031–5.

    Article  PubMed  Google Scholar 

  50. Levinson J, Nastro L. Giardiasis with total villous atrophy. Gastroenterology. 1978;74(2 Pt 1):271–5.

    Article  CAS  PubMed  Google Scholar 

  51. Duncombe V, Bolin T, Davis A, Cummins A, Crouch R. Histopathology in giardiasis: a correlation with diarrhoea. Aust NZ J Med. 1978;8(4):392–6.

    Article  CAS  Google Scholar 

  52. Arevalo F, Aragon V, Morales L, Morales Caramutti D, Arandia J, Alcocer G. Duodenal villous atrophy, an unexpectedly common finding in giardia lamblia infestation. Rev Gastroenterol Peru. 2010;30(4):272–6.

    PubMed  Google Scholar 

  53. Koot B, ten Kate F, Juffrie M, Rosalina I, Taminiau J, Benninga M. Does giardia lamblia cause villous atrophy in children?: a retrospective cohort study of the histological abnormalities in giardiasis. J Pediatr Gastroenterol Nutr. 2009;49(3):304–8.

    Article  PubMed  Google Scholar 

  54. Langford D, Housley M, Boes M, Chen J, Kagnoff M, Gillin F, et al. Central importance of immunoglobulin a in host defense against Giardia spp. Infect Immun. 2002;70(1):11–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Gillon J. Clinical studies in adults presenting with giardiasis to a gastrointestinal unit. Scott Med J. 1985;30(2):89–95.

    Article  CAS  PubMed  Google Scholar 

  56. Dolmans R, Boel C, Lacle M, Kusters J. Clinical manifestations, treatment, and diagnosis of tropheryma whipplei infections. Clin Microbiol Rev. 2017;30(2):529–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Fenollar F, Trani M, Davoust B, Salle B, Birg M, Rolain J, et al. Prevalence of asymptomatic tropheryma whipplei carriage among humans and nonhuman primates. J Infect Dis. 2008;197(6):880–7.

    Article  CAS  PubMed  Google Scholar 

  58. Schoniger-Hekele M, Petermann D, Weber B, Muller C. Tropheryma whipplei in the environment: survey of sewage plant influxes and sewage plant workers. Appl Environ Microbiol. 2007 Mar;73(6):2033–5.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Keita A, Brouqui P, Badiaga S, Benkouiten S, Ratmanov P, Raoult D, et al. Tropheryma whipplei prevalence strongly suggests human transmission in homeless shelters. Int J Infect Dis. 2013 Jan;17(1):e67–8.

    Article  PubMed  Google Scholar 

  60. Fenollar F, Keita A, Buffet S, Raoult D. Intrafamilial circulation of tropheryma whipplei. France Emerg Infect Dis. 2012;18(6):949–55.

    Article  PubMed  Google Scholar 

  61. Hujoel I, Johnson D, Lebwohl B, Leffler D, Kupfer S, Tsung-Teh W, et al. Tropheryma whipplei infection (Whipple disease) in the United States. Dig Dis Sci. 2019;64(1):213–23.

    Article  PubMed  Google Scholar 

  62. Schneider T, Moos V, Loddenkemper C, Marth T, Fenollar F, Raoult D. Whipple's disease: new aspects of pathogenesis and treatment. Lancet Infect Dis. 2008;8(3):179–90.

    Article  CAS  PubMed  Google Scholar 

  63. Fenollar F, Puechal X, Raoult D. Whipple's disease. N Engl J Med. 2007;356(1):55–66.

    Article  CAS  PubMed  Google Scholar 

  64. Sakai E, Higurashi T, Ohkubo H, Hosono K, Ueda A, Matsuhashi N, et al. Investigation of small bowel abnormalities in HIV-infected patients using capsule endoscopy. Gastroenterol Res Pract. 2017;2017:1932647.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Epple H, Allers K, Troger H, Kuhl A, Erben U, Fromm M, et al. Acute HIV infection induces mucosal infiltration with CD4+ and CD8+ T cells, epithelial apoptosis, and a mucosal barrier defect. Gastroenterology. 2010;139(4):1289–300.

    Article  CAS  PubMed  Google Scholar 

  66. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, McNeil A, et al. Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration folowing highly active antiretroviral therapy. J Virol. 2003;77(21):11708–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Wang H, Kotler D. HIV enteropathy and aging: gastrointestinal immunity, mucosal epithelial barrier, and microbial translocation. Curr Opin HIV AIDS. 2014;9(4):309–16.

    Article  PubMed  Google Scholar 

  68. Greenson J, Belitsos P, Yardley J, Bartlett J. AIDS enteropathy: occult enteric infections and duodenal mucosal alterations in chronic diarrhea. Ann Intern Med. 1991;114(5):366–72.

    Article  CAS  PubMed  Google Scholar 

  69. Utay N, Somasunderam A, Hinkle J, Petschow B, Detzel C, Somsouk M, et al. Serum bovine immunogloblins improve inflammation and gut barrier function in persons with HIV and enteropathy on suppressive ART. Pathog Immun. 2019;4(1):124–46.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Troseid M, Manner I, Pedersen K, Haissman J, Kvale D, Nielsen S. Microbial translocation and cardiometabolic risk factors in HIV infection. AIDS Res Hum Retrovir. 2014;30(6):514–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Pipaliya N, Ingle M, Rathi C, Poddar P, Pandav N, Sawant P. Spectrum of chronic small bowel diarrhea with malabsorption in Indian subcontinent: is the trend really changing? Intest Res. 2016;14(1):75–82.

    Article  PubMed  PubMed Central  Google Scholar 

  72. McCarroll M, Riddle M, Gutierrez R, Porter C. Infectious gastroenteritis as a risk factor for tropical sprue and malabsorption: a case-control study. Dig Dis Sci. 2015;60(11):3379–85.

    Article  PubMed  Google Scholar 

  73. Langenberg M, Wismans P, van Genderen P. Distinguishing tropical sprue from celiac disease in returning travellers with chronic diarrhoea: a diagnostic challenge? Travel Med Infect Dis. 2014;12(4):401–5.

    Article  PubMed  Google Scholar 

  74. Nath S. Tropical sprue. Curr Gastroenterol Rep. 2005;7:343–9.

    Article  PubMed  Google Scholar 

  75. Jacobs C, Coss Adame E, Attaluri A, Valestin J, Rao S. Dysmotility and proton pump inhibitor use are independent risk factors for small intestinal bacterial and/or fungal overgrowth. Aliment Pharmacol Ther. 2013;37(11):1103–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Choung R, Ruff K, Malhotra A, Herrick L, Locke GR, Harmsen W, et al. clinical predictors of small intestinal bacterial overgrowth by duodenal aspirate culture. Aliment Pharmacol Ther. 2011;33(9):1059–67.

    Article  CAS  PubMed  Google Scholar 

  77. Lasa J, Zubiaurre I, Fanjul I, Olivera P, Soifer L. Small intestinal bacterial overgrowth prevalence in celiac disease patients is similar in healthy subjects and lower in irritable bowel syndrome patients. Revista de Gastroenterologia de Mexico. 2015;80(2):171–4.

    Article  CAS  PubMed  Google Scholar 

  78. Lappinga P, Abraham S, Murray J, Vetter E, Patel R, Wu T. Small intestinal bacterial overgrowth: histopathologic features and clinical correlates in an underrecognized entity. Arch Pathol Lab Med. 2010;134(2):264–170.

    Article  PubMed  Google Scholar 

  79. Erdogan A, Rao S, Gulley D, Jacobs C, Lee Y, Badger C. Small intestinal bacterial overgrowth: duodenal aspiration vs glucose breath test. Neurogastroenterol Motil. 2015;27(4):481–9.

    Article  CAS  PubMed  Google Scholar 

  80. Ghoshal U, Ghoshal U. Small intestinal bacterial overgrowth and other intestinal disorders. Gastroenterol Clin N Am. 2017;46(1):103–20.

    Article  Google Scholar 

  81. Rezaie A, Buresi M, Lembo A, Lin H, McCallum R, Rao S, et al. Hydrogen and methane-based breath testing in gastrointestinal disorders: the North American consensus. Am J Gastroenterol. 2017;112(5):775–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Gatta L, Scarpignato C. Systematic review with meta-analysis: rifaximin is effective and safe for the treatment of small intestine bacterial overgrowth. Aliment Pharmacol Ther. 2017;45:604–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Zhong C, Qu C, Wang B, Liang S, Zeng B. Probiotics for preventing and treating small intestinal bacterial overgrowth: a meta-analysis and systematic review of current evidence. J Clin Gastroenterol. 2017;51(4):300–11.

    Article  CAS  PubMed  Google Scholar 

  84. Vakiani E, Arguelles-Grande C, Mansukhani M, Lewis S, Rotterdamn H, Green P, et al. Collagenous sprue is not always associated with dismal outcomes: a clinicopathological study of 19 patients. Mod Pathol. 2010;23(1):12–26.

    Article  PubMed  Google Scholar 

  85. Nielsen J, Steephen A, Lewin M. Angiotensin-II inhibitor (olmesartan)-induced collagenosu sprue with resolution following discontinuation of drug. World J Gastroenterol. 2013;19(40):6928–30.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Vasant D, Hayes S, Bucknall R, Lal S. Clinical and histological resolution fo collagenous sprue following gluten-free diet and discontinuation of non-steroidal anti-inflammatory drugs (NSAIDs). BMJ Case Rep. 2013;2013:bcr2013200097.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Rubio-Tapia A, Talley N, Gurudu S, Wu T, Murray J. Gluten-free diet and steroid treatment are effective therapy for most patients with collagenous sprue. Clin Gastroenterol Hepatol. 2010;8(4):344–9.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Freeman H. Hyposplenism, antiendomysial antibodies and lymphocytic colitis in collagenous sprue. Can J Gastroenterol. 1999;13(4):347–50.

    Article  CAS  PubMed  Google Scholar 

  89. Maguire A, Greenson J, Lauwers G, Ginsburg R, Williams G, Brown I, et al. Collagenous sprue: a clinicopathologic study of 12 cases. Am J Surg Pathol. 2009;33(10):1440–9.

    Article  PubMed  Google Scholar 

  90. Robert M, Ament M, Weinstein W. The histologic spectrum and clinical outcome of refractory and unclassified sprue. Am J Surg Pathol. 2000;24(5):676–87.

    Article  CAS  PubMed  Google Scholar 

  91. Schmidt C, Kasim E, Schlake W, Gerken G, Giese T, Stallmach A. TNF-alpha antibody treatment in refractory collagenous sprue: report of a case and review of the literature. Z Gastroenterol. 2009;47(6):575–8.

    Article  CAS  PubMed  Google Scholar 

  92. Jensen E, Martin C, Kappelman M, Dellon E. Prevalence of eosinophilic gastritis, gastroenteritis, and colitis: estimates from a national administrative database. J Pediatr Gastroenterol Nutr. 2016;62(1):36–42.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Spergel J, Book W, Mays E, Song L, Shah S, Talley N, et al. Variation in prevalence, diagnostic criteria, and initial management options for eosinophilic gastrointestinal diseases in the United States. J Pediatr Gastroenterol Nutr. 2011;52(3):300–6.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Talley N, Shorter R, Phillips S, Zinsmeister A. Eosinophilic gastroenteritis: a clinicopathological study of patients with disease of the mucosa, muscle layer, and subserosal tissues. Gut. 1990;31(1):54–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Klein N, Hargrove R, Sleisenger M, Jeffries G. Eosinophilic gastroenteritis. Medicine (Baltimore). 1970;49(4):299–319.

    Article  CAS  Google Scholar 

  96. Chang J, Choung R, Lee R, Locke GR, Schleck C, Zinsmeister A, et al. A shift in the clinical spectrum of eosinophliic gastroenteritis toward the mucosal disease type. Clin Gastroenterol Hepatol. 2010;8(8):669–75.

    Article  PubMed  Google Scholar 

  97. Reed C, Woosley J, Dellon E. Clinical characteristics, treatment outcomes, and resource utilization in children and adults with eosinophilic gastroenteritis. Dig Liver Dis. 2015;47(3):197–201.

    Article  PubMed  Google Scholar 

  98. Butterfield J, Murray J. Eosinophilic gastroenteritis and gluten-sensitive enteropathy in the same patient. J Clin Gastroenterol. 2002;34(5):552–3.

    Article  PubMed  Google Scholar 

  99. Tien F, Wu J, Jeng Y, Hsu H, Ni Y, Chang M, et al. Clinical features and treatment responses of children with eosinophilic gastroenteritis. Pediatr Neonatol. 2011;52(5):272–8.

    Article  PubMed  Google Scholar 

  100. Zheng X, Cheng J, Pan K, Yang K, Wang H, Wu E. Eosinophilic enteritis: CT features. Abdom Imaging. 2008;33(2):191–5.

    Article  PubMed  Google Scholar 

  101. Wong G, Lim K, Wan W, Low S, Kong S. Eosinophilic gastroenteritis: clinical profiles and treatment outcomes, a retrospective study of 18 adult patients in a Singapore tertiary hospital. Med J Malaysia. 2015;70(4):232–7.

    PubMed  Google Scholar 

  102. Hurrell J, Genta R, Melton S. Histopathologic diagnosis of eosinophilic conditions in the gastrointestinal tract. Adv Anat Pathol. 2011;18(5):335–48.

    Article  CAS  PubMed  Google Scholar 

  103. Pineton de Chambrun G, Gonzalez F, Canva J, Gonzalez S, Houssin L, Desremaux P, et al. Natural history of eosinophilic gastroenteritis. Clin Gastroenterol Hepatol. 2011;9(11):950–6.

    Article  PubMed  Google Scholar 

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  1. Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, USA

    Isabel A. Hujoel & Joseph A. Murray

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  1. Isabel A. Hujoel
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  2. Joseph A. Murray
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Correspondence to Joseph A. Murray .

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  1. Department of Gastroenterology, AP-HP. Centre-Université de Paris Hôpital Cochin, Paris, France

    Georgia Malamut

  2. Laboratory of Intestinal Immunity, Université de Paris, INSERM UMR 1163 and Imagine Institute, Paris, France

    Nadine Cerf-Bensussan

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Hujoel, I.A., Murray, J.A. (2022). The Other Causes of Severe Enteropathy with Villous Atrophy Non-Responsive to a Gluten-Free Diet. In: Malamut, G., Cerf-Bensussan, N. (eds) Refractory Celiac Disease. Springer, Cham. https://doi.org/10.1007/978-3-030-90142-4_8

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  • DOI: https://doi.org/10.1007/978-3-030-90142-4_8

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  • Print ISBN: 978-3-030-90141-7

  • Online ISBN: 978-3-030-90142-4

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