Best Practice & Research Clinical Gastroenterology
Volume 24, Issue 1 , Pages 43-56 , February 2010

Enteropathy associated T-cell lymphoma and its precursor lesions

  • Jolanda M.W. van de Water

      Affiliations

    • Department of Gastroenterology and Hepatology, VU University Medical Centre, P.O. Box 7057, 1005 MB Amsterdam, The Netherlands
    • Corresponding Author InformationCorresponding author. Tel.: +31 20 4440613; fax: +31 20 4440554.
  • ,
  • Saskia A.G.M. Cillessen

      Affiliations

    • Department of Pathology, VU University Medical Centre, Amsterdam, The Netherlands
  • ,
  • Otto J. Visser

      Affiliations

    • Department of Haematology, VU University Medical Centre, Amsterdam, The Netherlands
  • ,
  • Wieke H.M. Verbeek

      Affiliations

    • Department of Gastroenterology and Hepatology, VU University Medical Centre, P.O. Box 7057, 1005 MB Amsterdam, The Netherlands
  • ,
  • Chris J.L.M. Meijer

      Affiliations

    • Department of Pathology, VU University Medical Centre, Amsterdam, The Netherlands
  • ,
  • Chris J.J. Mulder

      Affiliations

    • Department of Gastroenterology and Hepatology, VU University Medical Centre, P.O. Box 7057, 1005 MB Amsterdam, The Netherlands

References 

  1. Gough KR, Read AE, Naish JM. Intestinal reticulosis as a complication of idiopathic steatorrhoea. Gut. 1962 Sep;3:232–239
  2. Harris OD, Cooke WT, Thompson H, Waterhouse JA. Malignancy in adult coeliac disease and idiopathic steatorrhoea. Am J Med. 1967 Jun;42(6):899–912
  3. O'Farrelly C, Feighery C, O'Briain DS, et al. Humoral response to wheat protein in patients with coeliac disease and enteropathy associated T cell lymphoma. Br Med J (Clin Res Ed). 1986 Oct 11;293(6552):908–910
  4. Isaacson P, Chott A, Ott G, Stein H. Enteropathy-associated T-cell lymphoma. In:  Swerdlow SH,  Campo E,  Harris NL,  Jaffe ES,  Pileri SA,  Thiele J, et al. editor. WHO classification of tumours of haematopoietic and lymphoid tissue. 4th ed.. Lyon, France: IARC Press; 2008;p. 289–291
  5. Catassi C, Bearzi I, Holmes GK. Association of celiac disease and intestinal lymphomas and other cancers. Gastroenterology. 2005 Apr;128(4 Suppl. 1):S79–S86
  6. Al-Toma A, Verbeek WH, Hadithi M, et al. Survival in refractory coeliac disease and enteropathy-associated T-cell lymphoma: retrospective evaluation of single-centre experience. Gut. 2007 Oct;56(10):1373–1378
  7. Verbeek WH, Van De Water JM, Al-Toma A, et al. Incidence of enteropathy–associated T-cell lymphoma: a nation-wide study of a population-based registry in The Netherlands. Scand J Gastroenterol. 2008;43(11):1322–1328
  8. Di Sabatino A, Corazza GR. Coeliac disease. Lancet. 2009 Apr 25;373(9673):1480–1493
  9. Dube C, Rostom A, Sy R, et al. The prevalence of celiac disease in average-risk and at-risk Western European populations: a systematic review. Gastroenterology. 2005 Apr;128(4 Suppl. 1):S57–S67
  10. Fasano A, Catassi C. Current approaches to diagnosis and treatment of celiac disease: an evolving spectrum. Gastroenterology. 2001 Feb;120(3):636–651
  11. Daum S, Ullrich R, Heise W, et al. Intestinal non-Hodgkin's lymphoma: a multicenter prospective clinical study from the German Study Group on Intestinal non-Hodgkin's Lymphoma. J Clin Oncol. 2003 Jul 15;21(14):2740–2746
  12. Smedby KE, Akerman M, Hildebrand H, et al. Malignant lymphomas in coeliac disease: evidence of increased risks for lymphoma types other than enteropathy-type T cell lymphoma. Gut. 2005 Jan;54(1):54–59
  13. Swinson CM, Slavin G, Coles EC, Booth CC. Coeliac disease and malignancy. Lancet. 1983 Jan 15;1(8316):111–115
  14. Askling J, Linet M, Gridley G, et al. Cancer incidence in a population-based cohort of individuals hospitalized with celiac disease or dermatitis herpetiformis. Gastroenterology. 2002 Nov;123(5):1428–1435
  15. Silano M, Volta U, Mecchia AM, et al. Delayed diagnosis of coeliac disease increases cancer risk. BMC Gastroenterol. 2007;7:8
  16. Viljamaa M, Kaukinen K, Pukkala E, et al. Malignancies and mortality in patients with coeliac disease and dermatitis herpetiformis: 30-year population-based study. Dig Liver Dis. 2006 Jun;38(6):374–380
  17. Biagi F, Corazza GR. Defining gluten refractory enteropathy. Eur J Gastroenterol Hepatol. 2001 May;13(5):561–565
  18. Cellier C, Delabesse E, Helmer C, et al. Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma. French Coeliac Disease Study Group. Lancet. 2000 Jul 15;356(9225):203–208
  19. Daum S, Cellier C, Mulder CJ. Refractory coeliac disease. Best Pract Res Clin Gastroenterol. 2005 Jun;19(3):413–424
  20. Wahab PJ, Meijer JW, Goerres MS, Mulder CJ. Coeliac disease: changing views on gluten-sensitive enteropathy. Scand J Gastroenterol Suppl. 2002;236:60–65
  21. Vahedi K, Mascart F, Mary JY, et al. Reliability of antitransglutaminase antibodies as predictors of gluten-free diet compliance in adult celiac disease. Am J Gastroenterol. 2003 May;98(5):1079–1087
  22. Cellier C, Patey N, Mauvieux L, et al. Abnormal intestinal intraepithelial lymphocytes in refractory sprue. Gastroenterology. 1998 Mar;114(3):471–481
  23. Patey-Mariaud De SN, Cellier C, Jabri B, et al. Distinction between coeliac disease and refractory sprue: a simple immunohistochemical method. Histopathology. 2000 Jul;37(1):70–77
  24. Daum S, Weiss D, Hummel M, et al. Frequency of clonal intraepithelial T lymphocyte proliferations in enteropathy-type intestinal T cell lymphoma, coeliac disease, and refractory sprue. Gut. 2001 Dec;49(6):804–812
  25. Verbeek WH, von Blomberg BM, Coupe VM, et al. Aberrant T-lymphocytes in refractory coeliac disease are not strictly confined to a small intestinal intraepithelial localization. Cytometry B Clin Cytom. 2009 May 14;
  26. Verkarre V, Romana SP, Cellier C, et al. Recurrent partial trisomy 1q22-q44 in clonal intraepithelial lymphocytes in refractory celiac sprue. Gastroenterology. 2003 Jul;125(1):40–46
  27. Zettl A, Ott G, Makulik A, et al. Chromosomal gains at 9q characterize enteropathy-type T-cell lymphoma. Am J Pathol. 2002 Nov;161(5):1635–1645
  28. Farstad IN, Johansen FE, Vlatkovic L, et al. Heterogeneity of intraepithelial lymphocytes in refractory sprue: potential implications of CD30 expression. Gut. 2002 Sep;51(3):372–378
  29. Mention JJ, Ben AM, Begue B, et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology. 2003 Sep;125(3):730–745
  30. When is a coeliac a coeliac? report of a working group of the United European gastroenterology week in Amsterdam, 2001. Eur J Gastroenterol Hepatol. 2001 Sep;13(9):1123–1128
  31. Verbeek WH, Goerres MS, von Blomberg BM, et al. Flow cytometric determination of aberrant intra-epithelial lymphocytes predicts T-cell lymphoma development more accurately than T-cell clonality analysis in refractory celiac disease. Clin Immunol. 2008 Jan;126(1):48–56
  32. Ashton-Key M, Diss TC, Pan L, et al. Molecular analysis of T-cell clonality in ulcerative jejunitis and enteropathy-associated T-cell lymphoma. Am J Pathol. 1997 Aug;151(2):493–498
  33. Akiyama T, Okino T, Konishi H, et al. CD8+, CD56+ (natural killer-like) T-cell lymphoma involving the small intestine with no evidence of enteropathy: clinicopathology and molecular study of five Japanese patients. Pathol Int. 2008 Oct;58(10):626–634
  34. Kataoka I, Arima F, Nishimoto J, et al. Enteropathy-type T-cell lymphoma showing repeated small bowel rupture and refractoriness to chemotherapy: a case report. Jpn J Clin Oncol. 2002 Dec;32(12):546–549
  35. Chuang SS, Liao YL, Liu H, et al. The phenotype of intraepithelial lymphocytes in Taiwanese enteropathy-associated T-cell lymphoma is distinct from that of the West. Histopathology. 2008 Aug;53(2):234–236
  36. Nakamura S, Matsumoto T, Iida M, et al. Primary gastrointestinal lymphoma in Japan: a clinicopathologic analysis of 455 patients with special reference to its time trends. Cancer. 2003 May 15;97(10):2462–2473
  37. Gale J, Simmonds PD, Mead GM, et al. Enteropathy-type intestinal T-cell lymphoma: clinical features and treatment of 31 patients in a single center. J Clin Oncol. 2000 Feb;18(4):795–803
  38. Brousse N, Meijer JW. Malignant complications of coeliac disease. Best Pract Res Clin Gastroenterol. 2005 Jun;19(3):401–412
  39. Rooney N, Dogan A. Gastrointestinal lymphoma. Curr Diagn Pathol. 2004;10:69–78
  40. Chott A, Haedicke W, Mosberger I, et al. Most CD56+ intestinal lymphomas are CD8 + CD5-T-cell lymphomas of monomorphic small to medium size histology. Am J Pathol. 1998 Nov;153(5):1483–1490
  41. de Bruin PC, Connolly CE, Oudejans JJ, et al. Enteropathy-associated T-cell lymphomas have a cytotoxic T-cell phenotype. Histopathology. 1997 Oct;31(4):313–317
  42. Ilyas M, Niedobitek G, Agathanggelou A, et al. Non-Hodgkin's lymphoma, coeliac disease, and Epstein-Barr virus: a study of 13 cases of enteropathy-associated T- and B-cell lymphoma. J Pathol. 1995 Oct;177(2):115–122
  43. Quintanilla-Martinez L, Lome-Maldonado C, Ott G, et al. Primary non-Hodgkin's lymphoma of the intestine: high prevalence of Epstein-Barr virus in Mexican lymphomas as compared with European cases. Blood. 1997 Jan 15;89(2):644–651
  44. Walsh SV, Egan LJ, Connolly CE, et al. Enteropathy-associated T-cell lymphoma in the West of Ireland: low-frequency of Epstein-Barr virus in these tumors. Mod Pathol. 1995 Sep;8(7):753–757
  45. Bagdi E, Diss TC, Munson P, Isaacson PG. Mucosal intra-epithelial lymphocytes in enteropathy-associated T-cell lymphoma, ulcerative jejunitis, and refractory celiac disease constitute a neoplastic population. Blood. 1999 Jul 1;94(1):260–264
  46. de Mascarel A, Belleannee G, Stanislas S, et al. Mucosal intraepithelial T-lymphocytes in refractory celiac disease: a neoplastic population with a variable CD8 phenotype. Am J Surg Pathol. 2008 May;32(5):744–751
  47. Carbonnel F, Grollet-Bioul L, Brouet JC, et al. Are complicated forms of celiac disease cryptic T-cell lymphomas?. Blood. 1998 Nov 15;92(10):3879–3886
  48. Polvi A, Arranz E, Fernandez-Arquero M, et al. HLA-DQ2-negative celiac disease in Finland and Spain. Hum Immunol. 1998 Mar;59(3):169–175
  49. Sollid LM, Markussen G, Ek J, et al. Evidence for a primary association of celiac disease to a particular HLA-DQ alpha/beta heterodimer. J Exp Med. 1989 Jan 1;169(1):345–350
  50. Sollid LM. Molecular basis of celiac disease. Annu Rev Immunol. 2000;18:53–81
  51. Vader W, Stepniak D, Kooy Y, et al. The HLA-DQ2 gene dose effect in celiac disease is directly related to the magnitude and breadth of gluten-specific T cell responses. Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12390–12395
  52. Louka AS, Nilsson S, Olsson M, et al. HLA in coeliac disease families: a novel test of risk modification by the ‘other’ haplotype when at least one DQA1*05-DQB1*02 haplotype is carried. Tissue Antigens. 2002 Aug;60(2):147–154
  53. Ploski R, Ek J, Thorsby E, Sollid LM. On the HLA-DQ(alpha 1*0501, beta 1*0201)-associated susceptibility in celiac disease: a possible gene dosage effect of DQB1*0201. Tissue Antigens. 1993 Apr;41(4):173–177
  54. Al-Toma A, Goerres MS, Meijer JW, et al. Human leukocyte antigen-DQ2 homozygosity and the development of refractory celiac disease and enteropathy-associated T-cell lymphoma. Clin Gastroenterol Hepatol. 2006 Mar;4(3):315–319
  55. van Heel DA, Franke L, Hunt KA, et al. A genome-wide association study for celiac disease identifies risk variants in the region harboring IL2 and IL21. Nat Genet. 2007 Jul;39(7):827–829
  56. Djilali-Saiah I, Schmitz J, Harfouch-Hammoud E, et al. CTLA-4 gene polymorphism is associated with predisposition to coeliac disease. Gut. 1998 Aug;43(2):187–189
  57. Hunt KA, McGovern DP, Kumar PJ, et al. A common CTLA4 haplotype associated with coeliac disease. Eur J Hum Genet. 2005 Apr;13(4):440–444
  58. Monsuur AJ, de Bakker PI, Alizadeh BZ, et al. Myosin IXB variant increases the risk of celiac disease and points toward a primary intestinal barrier defect. Nat Genet. 2005 Dec;37(12):1341–1344
  59. Wolters VM, Verbeek WH, Zhernakova A, et al. The MYO9B gene is a strong risk factor for developing refractory celiac disease. Clin Gastroenterol Hepatol. 2007 Dec;5(12):1399–14051405
  60. Giordano M, Marano C, Mellai M, et al. A family-based study does not confirm the association of MYO9B with celiac disease in the Italian population. Genes Immun. 2006 Oct;7(7):606–608
  61. Hunt KA, Monsuur AJ, McArdle WL, et al. Lack of association of MYO9B genetic variants with coeliac disease in a British cohort. Gut. 2006 Jul;55(7):969–972
  62. Nunez C, Marquez A, Varade J, et al. No evidence of association of the MYO9B polymorphisms with celiac disease in the Spanish population. Tissue Antigens. 2006 Dec;68(6):489–492
  63. Sadlack B, Merz H, Schorle H, et al. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell. 1993 Oct 22;75(2):253–261
  64. Monteleone G, Monteleone I, Fina D, et al. Interleukin-21 enhances T-helper cell type I signaling and interferon-gamma production in Crohn's disease. Gastroenterology. 2005 Mar;128(3):687–694
  65. Hunt KA, van Heel DA. Recent advances in coeliac disease genetics. Gut. 2009 Apr;58(4):473–476
  66. Zhernakova A, Alizadeh BZ, Bevova M, et al. Novel association in chromosome 4q27 region with rheumatoid arthritis and confirmation of type 1 diabetes point to a general risk locus for autoimmune diseases. Am J Hum Genet. 2007 Dec;81(6):1284–1288
  67. Hunt KA, Zhernakova A, Turner G, et al. Newly identified genetic risk variants for celiac disease related to the immune response. Nat Genet. 2008 Apr;40(4):395–402
  68. Baumgartner AK, Zettl A, Chott A, et al. High frequency of genetic aberrations in enteropathy-type T-cell lymphoma. Lab Invest. 2003 Oct;83(10):1509–1516
  69. Deleeuw RJ, Zettl A, Klinker E, et al. Whole-genome analysis and HLA genotyping of enteropathy-type T-cell lymphoma reveals 2 distinct lymphoma subtypes. Gastroenterology. 2007 May;132(5):1902–1911
  70. Cejkova P, Zettl A, Baumgartner AK, et al. Amplification of NOTCH1 and ABL1 gene loci is a frequent aberration in enteropathy-type T-cell lymphoma. Virchows Arch. 2005 Apr;446(4):416–420
  71. Deftos ML, Bevan MJ. Notch signaling in T cell development. Curr Opin Immunol. 2000 Apr;12(2):166–172
  72. Ellisen LW, Bird J, West DC, et al. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell. 1991 Aug 23;66(4):649–661
  73. Jundt F, Anagnostopoulos I, Forster R, et al. Activated Notch1 signaling promotes tumor cell proliferation and survival in Hodgkin and anaplastic large cell lymphoma. Blood. 2002 May 1;99(9):3398–3403
  74. Isaacson PG, Du MQ. Gastrointestinal lymphoma: where morphology meets molecular biology. J Pathol. 2005 Jan;205(2):255–274
  75. Joyce AM, Burns DL, Marcello PW, et al. Capsule endoscopy findings in celiac disease associated enteropathy-type intestinal T-cell lymphoma. Endoscopy. 2005 Jun;37(6):594–596
  76. Fry LC, Bellutti M, Neumann H, et al. Utility of double-balloon enteroscopy for the evaluation of malabsorption. Dig Dis. 2008;26(2):134–139
  77. Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc. 2001 Feb;53(2):216–220
  78. Hadithi M, Al-Toma A, Oudejans J, et al. The value of double-balloon enteroscopy in patients with refractory celiac disease. Am J Gastroenterol. 2007 May;102(5):987–996
  79. van Weyenberg SJB, Mallant M, Al-Toma A, et al. Magnetic Resonance Enteroclysis in adult coeliac disease: findings and comparisons between subtypes with different prognosis. Gut. 2007;56(Suppl.3):A56
  80. Matsumoto T, Nakamura S, Esaki M, et al. Double-balloon endoscopy depicts diminutive small bowel lesions in gastrointestinal lymphoma. Dig Dis Sci. 2010 Jan;55(1):158–165
  81. Tomei E, Diacinti D, Marini M, et al. Abdominal CT findings may suggest coeliac disease. Dig Liver Dis. 2005 Jun;37(6):402–406
  82. Mallant M, Hadithi M, Al-Toma AB, et al. Abdominal computed tomography in refractory coeliac disease and enteropathy associated T-cell lymphoma. World J Gastroenterol. 2007 Mar 21;13(11):1696–1700
  83. Hadithi M, Mallant M, Oudejans J, et al. 18F-FDG PET versus CT for the detection of enteropathy-associated T-cell lymphoma in refractory celiac disease. J Nucl Med. 2006 Oct;47(10):1622–1627
  84. Hoffmann M, Vogelsang H, Kletter K, et al. 18F-fluoro-deoxy-glucose positron emission tomography (18F-FDG-PET) for assessment of enteropathy-type T cell lymphoma. Gut. 2003 Mar;52(3):347–351
  85. Csizmadia CG, Mearin ML, von Blomberg BM, et al. An iceberg of childhood coeliac disease in the Netherlands. Lancet. 1999 Mar 6;353(9155):813–814
  86. Lohi S, Mustalahti K, Kaukinen K, et al. Increasing prevalence of coeliac disease over time. Aliment Pharmacol Ther. 2007 Nov 1;26(9):1217–1225
  87. Holmes GK, Prior P, Lane MR, et al. Malignancy in coeliac disease–effect of a gluten free diet. Gut. 1989 Mar;30(3):333–338
  88. Marsh MN. Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity ('celiac sprue'). Gastroenterology. 1992 Jan;102(1):330–354
  89. Rostami K, Kerckhaert J, Tiemessen R, et al. Sensitivity of antiendomysium and antigliadin antibodies in untreated celiac disease: disappointing in clinical practice. Am J Gastroenterol. 1999 Apr;94(4):888–894
  90. Babel N, Paragi P, Chamberlain RS. Management of enteropathy associated T-cell lymphoma: an algorithmic approach. Case Rep Oncol. 2009;2:36–43
  91. Verbeek WH, Schreurs MWJ, Visser OJ, et al. Novel approaches in the management of refractory celiac disease. Expert Rev Clin Immunol. 2008;42(2):205–219
  92. Corrao G, Corazza GR, Bagnardi V, et al. Mortality in patients with coeliac disease and their relatives: a cohort study. Lancet. 2001 Aug 4;358(9279):356–361
  93. Egan LJ, Walsh SV, Stevens FM, et al. Celiac-associated lymphoma. A single institution experience of 30 cases in the combination chemotherapy era. J Clin Gastroenterol. 1995 Sep;21(2):123–129
  94. Bishton MJ, Haynes AP. Combination chemotherapy followed by autologous stem cell transplant for enteropathy-associated T cell lymphoma. Br J Haematol. 2007 Jan;136(1):111–113
  95. Blystad AK, Enblad G, Kvaloy S, et al. High-dose therapy with autologous stem cell transplantation in patients with peripheral T cell lymphomas. Bone Marrow Transplant. 2001 Apr;27(7):711–716
  96. Jantunen E, Juvonen E, Wiklund T, et al. High-dose therapy supported by autologous stem cell transplantation in patients with enteropathy-associated T-cell lymphoma. Leuk Lymphoma. 2003 Dec;44(12):2163–2164
  97. Okuda M, Nomura J, Tateno H, et al. CD56 positive intestinal T-cell lymphoma: treatment with high dose chemotherapy and autologous peripheral blood stem cell transplantation. Intern Med. 2002 Sep;41(9):734–737
  98. Rongey C, Micallef I, Smyrk T, Murray J. Successful treatment of enteropathy-associated T cell lymphoma with autologous stem cell transplant. Dig Dis Sci. 2006 Jun;51(6):1082–1086
  99. Al-Toma A, Verbeek WH, Visser OJ, et al. Disappointing outcome of autologous stem cell transplantation for enteropathy-associated T-cell lymphoma. Dig Liver Dis. 2007 Jul;39(7):634–641
  100. Doocey RT, Toze CL, Connors JM, et al. Allogeneic haematopoietic stem-cell transplantation for relapsed and refractory aggressive histology non-Hodgkin lymphoma. Br J Haematol. 2005 Oct;131(2):223–230
  101. van Besien KW, Mehra RC, Giralt SA, et al. Allogeneic bone marrow transplantation for poor-prognosis lymphoma: response, toxicity and survival depend on disease histology. Am J Med. 1996;100:299–307
  102. Hosing C, Saliba RM, McLaughlin P, et al. Long-term results favor allogeneic over autologous hematopoietic stem cell transplantation in patients with refractory or recurrent indolent non-Hodgkin's lymphoma. Ann Oncol. 2003 May;14(5):737–744
  103. Dearden CE, Matutes E. Alemtuzumab in T-cell lymphoproliferative disorders. Best Pract Res Clin Haematol. 2006;19(4):795–810
  104. Dearden CE, Matutes E, Cazin B, et al. High remission rate in T-cell prolymphocytic leukemia with CAMPATH-1H. Blood. 2001 Sep 15;98(6):1721–1726
  105. Gallamini A, Zaja F, Patti C, et al. Alemtuzumab (Campath-1H) and CHOP chemotherapy as first-line treatment of peripheral T-cell lymphoma: results of a GITIL (Gruppo Italiano Terapie Innovative nei Linfomi) prospective multicenter trial. Blood. 2007 Oct 1;110(7):2316–2323
  106. Jiang L, Yuan CM, Hubacheck J, et al. Variable CD52 expression in mature T cell and NK cell malignancies: implications for alemtuzumab therapy. Br J Haematol. 2009 Feb 18;
  107. Kircher SM, Gurbuxani S, Smith SM. CHOP plus alemtuzumab can induce metabolic response by FDG-PET but has minimal long-term benefits: a case report and literature review. J Gastrointest Cancer. 2007;38(1):59–62
  108. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell. 2002 Jan 25;108(2):153–164
  109. Kitada S, Pedersen IM, Schimmer AD, Reed JC. Dysregulation of apoptosis genes in hematopoietic malignancies. Oncogene. 2002 May 13;21(21):3459–3474
  110. Green PH, Jabri B. Coeliac disease. Lancet. 2003 Aug 2;362(9381):383–391
  111. Catassi C, Fabiani E, Corrao G, et al. Risk of non-Hodgkin lymphoma in celiac disease. JAMA. 2002 Mar 20;287(11):1413–1419
  112. Collin P. Should adults be screened for celiac disease? What are the benefits and harms of screening?. Gastroenterology. 2005 Apr;128(4 Suppl. 1):S104–S108
  113. Logan RF. Malignancy in unrecognised coeliac disease: a nail in the coffin for mass screening?. Gut. 2009 May;58(5):618–619
  114. Lohi S, Maki M, Montonen J, et al. Malignancies in cases with screening-identified evidence of coeliac disease: a long-term population-based cohort study. Gut. 2009 May;58(5):643–647
  115. Hallert C, Granno C, Grant C, et al. Quality of life of adult coeliac patients treated for 10 years. Scand J Gastroenterol. 1998 Sep;33(9):933–938
  116. Mustalahti K, Lohiniemi S, Collin P, et al. Gluten-free diet and quality of life in patients with screen-detected celiac disease. Eff Clin Pract. 2002 May;5(3):105–113
  117. Casellas F, Rodrigo L, Vivancos JL, et al. Factors that impact health-related quality of life in adults with celiac disease: a multicenter study. World J Gastroenterol. 2008 Jan 7;14(1):46–52
  118. Johnston SD, Rodgers C, Watson RG. Quality of life in screen-detected and typical coeliac disease and the effect of excluding dietary gluten. Eur J Gastroenterol Hepatol. 2004 Nov;16(12):1281–1286
  119. The Non-Hodgkin's Lymphoma Classification Project: A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin's lymphoma. Blood. 1997;89:3909–3918

PII: S1521-6918(09)00152-8

doi: 10.1016/j.bpg.2009.11.002

Best Practice & Research Clinical Gastroenterology
Volume 24, Issue 1 , Pages 43-56 , February 2010