Gastrointestinal Lymphomas

  • Alma Aslan
  • Serkan Akın
  • Taner Babacan
  • Evren Özdemir


Primary gastrointestinal (GI) lymphomas constitute 1–4% of all gastrointestinal malignancies, and 90% are of B-cell type. The most commonly involved sites are as follows: stomach (60–75%), small intestine (9%), ileocecal region (7%), and colorectal region (<1%). Certain histological subtypes of lymphomas may preferentially involve specific sites in the gastrointestinal tract. There are several known risk factors for the development of primary GI lymphoma. Pretreatment work-up and tissue biopsy are necessary for definitive diagnosis and evaluation of the extent of the disease. There is limited consensus on the staging system of primary GI lymphoma, with three staging systems in use: Ann-Arbor staging with Musshoff modification, Lugano staging system, and Paris staging system. The treatment depends upon the patient’s clinical condition, histological subtype, and stage of the disease and may range from observation to stem cell transplantation. This chapter will focus on the most common primary GI lymphomas of the stomach, small intestine, and colon and extranodal involvement of the GI tract by systemic lymphomas. Epidemiology, etiology, risk factors, diagnostic procedures, staging, treatment, and follow-up of GI lymphomas will be discussed.


Lymphoma Non-Hodgkin’s lymphoma Gastrointestinal system Gastrointestinal tract Gastric lymphoma Intestinal lymphoma Extranodal lymphoma 


  1. 1.
    Paryani S, Hoppe RT, Burke JS, Sneed P, Dawley D, Cox RS, et al. Extralymphatic involvement in diffuse non-Hodgkin’s lymphoma. J Clin Oncol. 1983;1(11):682–8.CrossRefPubMedGoogle Scholar
  2. 2.
    Freeman C, Berg JW, Cutler SJ. Occurrence and prognosis of extranodal lymphomas. Cancer. 1972;29:252–60.CrossRefPubMedGoogle Scholar
  3. 3.
    Loehr WJ, Mujahed Z, Zahn FD, Gray GF, Thorbjarnarson B. Primary lymphoma of the gastrointestinal tract: a review of 100 cases. Ann Surg. 1969;170(2):232–8.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Gurney KA, Cartwright RA. Increasing incidence and descriptive epidemiology of extranodal non-Hodgkin lymphoma in parts of England and Wales. Hematol J. 2002;3(2):95–104.CrossRefPubMedGoogle Scholar
  5. 5.
    Dawson IM, Cornes JS, Morson BC. Primary malignant lymphoid tumors of the intestinal tract. Report of 37 cases with a study of factors influencing prognosis. Br J Surg. 1961;49:80.CrossRefPubMedGoogle Scholar
  6. 6.
    Lewin KJ, Ranchod M, Dorfman RF. Lymphomas of the gastrointestinal tract: a study of 117 cases presenting with gastrointestinal disease. Cancer. 1978;42:693.CrossRefPubMedGoogle Scholar
  7. 7.
    Koch P, del Valle F, Berdel WE, Willich NA, Reers B, Hiddemann W, et al; German Multicenter Study Group. Primary gastrointestinal non-Hodgkin’s lymphoma: I. Anatomic and histologic distribution, clinical features, and survival data of 371 patients registered in the German Multicenter Study GIT NHL 01/92. J Clin Oncol. 2001;19(18):3861–73.Google Scholar
  8. 8.
    Papaxoinis G, Papageorgiou S, Rontogianni D, Kaloutsi V, Fountzilas G, Pavlidis N, et al. Primary gastrointestinal non-Hodgkin’s lymphoma: a clinicopathologic study of 128 cases in Greece. A Hellenic Cooperative Oncology Group study (HeCOG). Leuk Lymphoma. 2006;47(10):2140–6.CrossRefPubMedGoogle Scholar
  9. 9.
    Cogliatti SB, Schmid U, Schumacher U, Eckert F, Hansmann ML, Hedderich J, et al. Primary B-cell gastric lymphoma: a clinicopathological study of 145 patients. Gastroenterology. 1991;101:1159–70.CrossRefPubMedGoogle Scholar
  10. 10.
    Müller AM, Ihorst G, Mertelsmann R, Engelhardt M. Epidemiology of non-Hodgkin’s lymphoma (NHL): trends, geographic distribution, and etiology. Ann Hematol. 2005;84:1–12.CrossRefPubMedGoogle Scholar
  11. 11.
    Brands F, Monig SP, Raab M. Treatment and prognosis of gastric lymphoma. Eur J Surg. 1997;163:803–13.PubMedGoogle Scholar
  12. 12.
    Zucca E, Bertoni F, Roggero E, Bosshard G, Cazzaniga G, Pedrinis E, et al. Molecular analysis of the progression from Helicobacter pylori-associated chronic gastritis to mucosa-associated lymphoid-tissue lymphoma of the stomach. N Engl J Med. 1998;338:804–10.CrossRefPubMedGoogle Scholar
  13. 13.
    Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet. 1991;338:1175.CrossRefPubMedGoogle Scholar
  14. 14.
    Aull MJ, Buell JF, Peddi VR, Trofe J, Beebe TM, Hanaway MJ, et al; Israel Penn International Transplant Tumor Registry. MALToma: a Helicobacter pylori-associated malignancy in transplant patients: a report from the Israel Penn International Transplant Tumor Registry with a review of published literature. Transplantation. 2003;75(2):225–8.CrossRefPubMedGoogle Scholar
  15. 15.
    McTamaney JP, Neifeld JP, Mendez-Picon G, Lee HM. Primary gastric lymphoma following renal transplantation. J Surg Oncol. 1981;18:265.CrossRefPubMedGoogle Scholar
  16. 16.
    Heise W, Arastéh K, Mostertz P, Skörde J, Schmidt W, Obst C, et al. Malignant gastrointestinal lymphomas in patients with AIDS. Digestion. 1997;58:218.CrossRefPubMedGoogle Scholar
  17. 17.
    Whooley BP, Bernik S, Sarkis AY, Wallack MK. Primary gastrointestinal non-Hodgkin’s lymphoma: increasingly AIDS-related. Am Surg. 1998;64:137.PubMedGoogle Scholar
  18. 18.
    Andrews CN, John Gill M, Urbanski SJ, Stewart D, Perini R, Beck P. Changing epidemiology and risk factors for gastrointestinal non-Hodgkin’s lymphoma in a North American population: population-based study. Am J Gastroenterol. 2008;103:1762.CrossRefPubMedGoogle Scholar
  19. 19.
    Catassi C, Fabiani E, Corrao G, Barbato M, De Renzo A, Carella AM, et al. Risk of non-Hodgkin lymphoma in celiac disease. JAMA. 2002;287:1413.CrossRefPubMedGoogle Scholar
  20. 20.
    Kandiel A, Fraser AG, Korelitz BI, Brensinger C, Lewis JD. Increased risk of lymphoma among inflammatory bowel disease patients treated with azathioprine and 6-mercaptopurine. Gut. 2005;54:1121.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Geborek P, Bladström A, Turesson C, Gulfe A, Petersson IF, Saxne T, et al. Tumor necrosis factor blockers do not increase overall tumor risk in patients with rheumatoid arthritis, but may be associated with an increased risk of lymphomas. Ann Rheum Dis. 2005;64(5):699–703.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Baecklund E, Iliadou A, Askling J, Ekbom A, Backlin C, Granath F, et al. Association of chronic inflammation, not its treatment, with increased lymphoma risk in rheumatoid arthritis. Arthritis Rheum. 2006;54(3):692–701.CrossRefGoogle Scholar
  23. 23.
    Mathus-Vliegen EMH, Van Halteren H, Tytgat GNJ. Malignant lymphoma in coeliac disease: various manifestations with distinct symptomatology and prognosis? J Intern Med. 1994;236:43–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Radaszkiewicz T, Dragosics B, Bauer P. Gastrointestinal malignant lymphomas of the mucosa-associated lymphoid tissue: factors relevant to prognosis. Gastroenterology. 1992;102:1628.CrossRefPubMedGoogle Scholar
  25. 25.
    Wang T, Gui W, Shen Q. Primary gastrointestinal non-Hodgkin’s lymphoma: clinicopathological and prognostic analysis. Med Oncol. 2010;27:661.CrossRefPubMedGoogle Scholar
  26. 26.
    Caletti G, Ferrari A, Brocchi E, Barbara L. Accuracy of endoscopic ultrasonography in the diagnosis and staging of gastric cancer and lymphoma. Surgery. 1993;113:14.PubMedGoogle Scholar
  27. 27.
    Fujishima H, Misawa T, Maruoka A, Chijiiwa Y, Sakai K, Nawata H. Staging and follow-up of primary gastric lymphoma by endoscopic ultrasonography. Am J Gastroenterol. 1991;86:719.PubMedGoogle Scholar
  28. 28.
    Vilmann P, Hancke S, Henriksen FW, Jacobsen GK. Endoscopic ultrasonography-guided fine-needle aspiration biopsy of lesions in the upper gastrointestinal tract. Gastrointest Endosc. 1995;41:230.CrossRefPubMedGoogle Scholar
  29. 29.
    Spinelli P, Lo Gullo C, Pizzetti P. Endoscopic diagnosis of gastric lymphomas. Endoscopy. 1980;12:211.CrossRefPubMedGoogle Scholar
  30. 30.
    Fork FT, Haglund U, Högström H, Wehlin L. Primary gastric lymphoma versus gastric cancer. An endoscopic and radiographic study of differential diagnostic possibilities. Endoscopy. 1985;17:5.CrossRefPubMedGoogle Scholar
  31. 31.
    Suekane H, Iida M, Yao T, Matsumoto T, Masuda Y, Fujishima M. Endoscopic ultrasonography in primary gastric lymphoma: correlation with endoscopic and histologic findings. Gastrointest Endosc. 1993;39:139–45.CrossRefPubMedGoogle Scholar
  32. 32.
    Novak U, Basso K, Pasqualucci L, Dalla-Favera R, Bhagat G. Genomic analysis of non-splenic marginal zone lymphomas (MZL) indicates similarities between nodal and extranodal MZL and supports their derivation from memory B-cells. Br J Haematol. 2011;155:362.CrossRefPubMedGoogle Scholar
  33. 33.
    Nakamura S, Matsumoto T, Nakamura S, Jo Y, Fujisawa K, Suekane H, Yao T, Tsuneyoshi M, Iida M. Chromosomal translocation t(11;18)(q21;q21) in gastrointestinal mucosa associated lymphoid tissue lymphoma. J Clin Pathol. 2003;56:36–42.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Bertoni F, Zucca E. Delving deeper into MALT lymphoma biology. J Clin Invest. 2006;116:22.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Dierlamm J, Baens M, Wlodarska I, Stefanova-Ouzounova M, Hernandez JM, Hossfeld DK, et al. The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18) (q21;q21) associated with mucosa-associated lymphoid tissue lymphomas. Blood. 1999;93:3601–9.PubMedGoogle Scholar
  36. 36.
    Yeh KH, Kuo SH, Chen LT, Mao TL, Doong SL, Wu MS, et al. Nuclear expression of BCL10 or nuclear factor kappa B helps predict Helicobacter pylori-independent status of low-grade gastric mucosa-associated lymphoid tissue lymphomas with or without t(11;18)(q21;q21). Blood. 2005;106:1037–41.CrossRefPubMedGoogle Scholar
  37. 37.
    Park YH, Kim WS, Bang SM, Lee SI, Uhm JE, Kang HJ, et al. Prognostic factor analysis and proposed prognostic model for conventional treatment of high-grade primary gastric lymphoma. Eur J Haematol. 2006;77:304–8.CrossRefPubMedGoogle Scholar
  38. 38.
    Klapproth K, Wirth T. Advances in the understanding of MYC-induced lymphomagenesis. Br J Haematol. 2010;149:484–97.CrossRefPubMedGoogle Scholar
  39. 39.
    Iqbal J, Neppalli VT, Wright G, Dave BJ, Horsman DE, Rosenwald A, et al. BCL2 expression is a prognostic marker for the activated B-cell-like type of diffuse large B-cell lymphoma. J Clin Oncol. 2006;24:961–8.CrossRefPubMedGoogle Scholar
  40. 40.
    Johnson NA, Slack GW, Savage KJ, Connors JM, Ben-Neriah S, Rogic S, et al. Concurrent expression of MYC and BCL2 in diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol. 2012;30:3452–9.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Perry C, Herishanu Y, Metzer U, Bairey O, Ruchlemer R, Trejo L, et al. Diagnostic accuracy of PET/CT in patients with extranodal marginal zone MALT lymphoma. Eur J Haematol. 2007;79:205.CrossRefPubMedGoogle Scholar
  42. 42.
    Zucca E, Copie-Bergman C, Ricardi U, Thieblemont C, Raderer M, Ladetto M, Ladetto M, ESMO Guidelines Working Group. Gastric marginal zone lymphoma of MALT type: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2013;24(Suppl 6):vi144–8.CrossRefPubMedGoogle Scholar
  43. 43.
    Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, Lister TA. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059–68.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Musshoff K, Schmidt-Vollmer H. Proceedings: prognosis of non-Hodgkin’s lymphomas with special emphasis on the staging classification. Z Krebsforsch Klin Onkol Cancer Res Clin Oncol. 1975;83(4):323–41.CrossRefPubMedGoogle Scholar
  45. 45.
    Rohatiner A, d’Amore F, Coiffier B, Crowther D, Gospodarowicz M, Isaacson P, et al. Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994;5(5):397–400.CrossRefPubMedGoogle Scholar
  46. 46.
    Ruskoné-Fourmestraux A, Dragosics B, Morgner A, Wotherspoon A, De Jong D. Paris staging system for primary gastrointestinal lymphomas. Gut. 2003;52(6):912–3.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Inagaki H, Nakamura T, Li C, Sugiyama T, Asaka M, Kodaira J, et al. Gastric MALT lymphomas are divided into three groups based on responsiveness to Helicobacter Pylori eradication and detection of API2-MALT1 fusion. Am J Surg Pathol. 2004;28:1560–7.CrossRefPubMedGoogle Scholar
  48. 48.
    Xia B, Zhang L, Guo SQ, Li XW, Qu FL, Zhao HF, et al. Coexpression of MYC and BCL-2 predicts prognosis in primary gastrointestinal diffuse large B-cell lymphoma. World J Gastroenterol. 2015;21:2433–42.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Nakamura S, Sugiyama T, Matsumoto T, Iijima K, Ono S, Tajika M, et al. Long-term clinical outcome of gastric MALT lymphoma after eradication of Helicobacter pylori: a multicentre cohort follow-up study of 420 patients in Japan. Gut. 2012;61:507–13.CrossRefPubMedGoogle Scholar
  50. 50.
    Alpen B, Neubauer A, Dierlamm J, Marynen P, Thiede C, Bayerdörfer E, et al. Translocation t(11;18) absent in early gastric marginal zone B-cell lymphoma of MALT type responding to eradication of Helicobacter pylori infection. Blood. 2000;95:4014–5.PubMedGoogle Scholar
  51. 51.
    Neubauer A, Thiede C, Morgner A, Alpen B, Ritter M, Neubauer B, et al. Cure of Helicobacter pylori infection and duration of remission of low-grade gastric mucosa-associated lymphoid tissue lymphoma. J Natl Cancer Inst. 1997;89:1350–5.CrossRefPubMedGoogle Scholar
  52. 52.
    Conconi A, Martinelli G, Thiéblemont C, Ferreri AJ, Devizzi L, Peccatori F, et al. Clinical activity of rituximab in extranodal marginal zone B-cell lymphoma of MALT type. Blood. 2003;102:2741–5.CrossRefPubMedGoogle Scholar
  53. 53.
    Martinelli G, Laszlo D, Ferreri AJ, Pruneri G, Ponzoni M, Conconi A, et al. Clinical activity of rituximab in gastric marginal zone non-Hodgkin’s lymphoma resistant to or not eligible for anti-Helicobacter pylori therapy. J Clin Oncol. 2005;23:1979–83.CrossRefPubMedGoogle Scholar
  54. 54.
    Raderer M, Streubel B, Wöhrer S, Häfner M, Chott A. Successful antibiotic treatment of Helicobacter pylori negative gastric mucosa associated lymphoid tissue lymphomas. Gut. 2006;55:616–8.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Daum S, Ullrich R, Heise W, Dederke B, Foss HD, Stein H, 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;21:2740–6.CrossRefPubMedGoogle Scholar
  56. 56.
    Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993;342:575–7.CrossRefPubMedGoogle Scholar
  57. 57.
    Shiozawa E, Norose T, Kaneko K, Yamochi-Onizuka T, Takimoto M, Imawari M, et al. Clinicopathological comparison of the World Health Organization/Wotherspoon score to the Grouped’Etude des Lymphomes de l’Adult grade for the post-treatment evaluation of gastric mucosa-associated lymphoid tissue lymphoma. J Gastroenterol Hepatol. 2009;24:307–15.CrossRefPubMedGoogle Scholar
  58. 58.
    Ruskoné-Fourmestraux A, Fischbach W, Aleman BM, Boot H, Du MQ, Megraud F, EGILS group. EGILS consensus report. Gastric extranodal marginal zone B-cell lymphoma of MALT. Gut. 2011;60:747–58.CrossRefPubMedGoogle Scholar
  59. 59.
    Zucca E, Dreyling M, ESMO Guideline Working Group. Gastric marginal zone lymphoma of MALT type: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2010;21:175–6.CrossRefGoogle Scholar
  60. 60.
    Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65(1):5–29.CrossRefGoogle Scholar
  61. 61.
    Schottenfeld D, Beebe-Dimmer JL, Vigneau FD. The epidemiology and pathogenesis of neoplasia in the small intestine. Ann Epidemiol. 2009;19(1):58–69.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Isaacson PG. Gastrointestinal lymphoma. Hum Pathol. 1994;25(10):1020–9.CrossRefPubMedGoogle Scholar
  63. 63.
    Al-Saleem T, Al-Mondhiry H. Immunoproliferative small intestinal disease (IPSID): a model for mature B-cell neoplasms. Blood. 2005;105(6):2274–80.CrossRefPubMedGoogle Scholar
  64. 64.
    Bibas M, Antinori A. EBV and HIV-Related Lymphoma. Mediterr J Hematol Infect Dis. 2009;1(2):e2009032.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Delabie J, Holte H, Vose JM, Ullrich F, Jaffe ES, Savage KJ, et al. Enteropathy-associated T-cell lymphoma: clinical and histological findings from the international peripheral T-cell lymphoma project. Blood. 2011;118(1):148–55.CrossRefPubMedGoogle Scholar
  66. 66.
    Quintanilla-Martinez L, Lome-Maldonado C, Ott G, Gschwendtner A, Gredler E, Angeles-Angeles A, et al. Primary intestinal non-Hodgkin’s lymphoma and Epstein-Barr virus: high frequency of EBV-infection in T-cell lymphomas of Mexican origin. Leuk Lymphoma. 1998;30(1–2):111–21.CrossRefPubMedGoogle Scholar
  67. 67.
    Lecuit M, Abachin E, Martin A, Poyart C, Pochart P, Suarez F, Bengoufa D, et al. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med. 2004;350(3):239–48.CrossRefPubMedGoogle Scholar
  68. 68.
    Nikbin B, Banisadre M, Ala F, Mojtabai A. HLA AW19, B12 in immunoproliferative small intestinal disease. Gut. 1979;20(3):226–8.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer. 2001;91(4):854–62.CrossRefPubMedGoogle Scholar
  70. 70.
    Cooper BT, Holmes GK, Ferguson R, Cooke WT. Celiac disease and malignancy. Medicine (Baltimore). 1980;59(4):249–61.CrossRefGoogle Scholar
  71. 71.
    Asano N, Kato S, Nakamura S. Epstein-Barr virus-associated natural killer/T-cell lymphomas. Best Pract Res Clin Haematol. 2013;26(1):15–21.CrossRefPubMedGoogle Scholar
  72. 72.
    Heise W. GI-lymphomas in immunosuppressed patients (organ transplantation; HIV). Best Pract Res Clin Gastroenterol. 2010;24(1):57–69.CrossRefPubMedGoogle Scholar
  73. 73.
    Castellano G, Moreno D, Galvao O, Ballestín C, Colina F, Mollejo M, et al. Malignant lymphoma of jejunum with common variable hypogammaglobulinemia and diffuse nodular hyperplasia of the small intestine. A case study and literature review. J Clin Gastroenterol. 1992;15(2):128–35.CrossRefPubMedGoogle Scholar
  74. 74.
    Ghai S, Pattison J, Ghai S, O’Malley ME, Khalili K, Stephens M. Primary gastrointestinal lymphoma: spectrum of imaging findings with pathologic correlation. Radiographics. 2007;27(5):1371–88.CrossRefPubMedGoogle Scholar
  75. 75.
    Juweid M, Stroobants S, Hoekstra OS, Mottaghy FM, Dietlein M, Guermazi A, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol. 2007;25(5):571–8.CrossRefPubMedGoogle Scholar
  76. 76.
    Cronin CG, Scott J, Kambadakone A, Catalano OA, Sahani D, Blake MA, et al. Utility of positron emission tomography/CT in the evaluation of small bowel pathology. Br J Radiol. 2012;85(1017):1211–21.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Chung HH, Kim YH, Kim JH, Cha SH, Kim BH, Kim TK, et al. Imaging findings of mantle cell lymphoma involving gastrointestinal tract. Yonsei Med J. 2003;44(1):49–57.CrossRefPubMedGoogle Scholar
  78. 78.
    Schmatz AI, Streubel B, Kretschmer-Chott E, Püspök A, Jäger U, Mannhalter C, et al. Primary follicular lymphoma of the duodenum is a distinct mucosal/submucosal variant of follicular lymphoma: a retrospective study of 63 cases. J Clin Oncol. 2011;29(11):1445–51.CrossRefPubMedGoogle Scholar
  79. 79.
    Joyce AM, Burns DL, Marcello PW, Tronic B, Scholz FJ. Capsule endoscopy findings in celiac disease associated enteropathy-type intestinal T-cell lymphoma. Endoscopy. 2005;37(6):594–6.CrossRefPubMedGoogle Scholar
  80. 80.
    Yamamoto S, Nakase H, Yamashita K, Matsuura M, Takada M, Kawanami C, et al. Gastrointestinal follicular lymphoma: review of the literature. J Gastroenterol. 2010;45(4):370–88.CrossRefPubMedGoogle Scholar
  81. 81.
    Al-Saleem TI, Qadiry WA, Issa FS, King J. The immunoselection technic in laboratory diagnosis of alpha heavy-chain disease. Am J Clin Pathol. 1979;72(1):132–3.CrossRefPubMedGoogle Scholar
  82. 82.
    Suzuki R. NK/T-cell lymphomas: pathobiology, prognosis and treatment paradigm. Curr Oncol Rep. 2012;14(5):395–402.CrossRefPubMedGoogle Scholar
  83. 83.
    Kim SJ, Kang HJ, Kim JS, Oh SY, Choi CW, Lee SI, et al. Comparison of treatment strategies for patients with intestinal diffuse large B-cell lymphoma: surgical resection followed by chemotherapy versus chemotherapy alone. Blood. 2011;117(6):1958–65.CrossRefPubMedGoogle Scholar
  84. 84.
    Aleman BM, Haas RL, van der Maazen RW. Role of radiotherapy in the treatment of lymphomas of the gastrointestinal tract. Best Pract Res Clin Gastroenterol. 2010;24(1):27–34.CrossRefPubMedGoogle Scholar
  85. 85.
    Azab MB, Henry-Amar M, Rougier P, Bognel C, Theodore C, Carde P, et al. Prognostic factors in primary gastrointestinal non-Hodgkin’s lymphoma. A multivariate analysis, report of 106 cases, and review of the literature. Cancer. 1989;64(6):1208–17.CrossRefPubMedGoogle Scholar
  86. 86.
    Ben-Ayed F, Halphen M, Najjar T, Boussene H, Jaafoura H, Bouguerra A, et al. Treatment of alpha chain disease. Results of a prospective study in 21 Tunisian patients by the Tunisian-French intestinal Lymphoma Study Group. Cancer. 1989;63(7):1251–6.CrossRefPubMedGoogle Scholar
  87. 87.
    el Saghir NS. Combination chemotherapy with tetracycline and aggressive supportive care for immunoproliferative small-intestinal disease lymphoma. J Clin Oncol. 1995;13(3):794–5.CrossRefPubMedGoogle Scholar
  88. 88.
    Shih L, Liaw SJ, Dunn P, Kuo TT. Primary small-intestinal lymphomas in Taiwan: immunoproliferative small-intestinal disease and nonimmunoproliferative small-intestinal disease. J Clin Oncol. 1994;12(7):1375–82.CrossRefPubMedGoogle Scholar
  89. 89.
    Lee J, Kim WS, Kim K, Ahn JS, Jung CW, Lim HY, et al. Prospective clinical study of surgical resection followed by CHOP in localized intestinal diffuse large B cell lymphoma. Leuk Res. 2007;31(3):359–64.CrossRefPubMedGoogle Scholar
  90. 90.
    Foon KA, Takeshita K, Zinzani PL. Novel therapies for aggressive B-cell lymphoma. Adv Hematol. 2012;2012:302570.PubMedPubMedCentralGoogle Scholar
  91. 91.
    Yamaguchi M, Suzuki R, Kwong YL, Kim WS, Hasegawa Y, Izutsu K, et al. Phase I study of dexamethasone, methotrexate, ifosfamide, L-asparaginase, and etoposide (SMILE) chemotherapy for advanced-stage, relapsed or refractory extranodal natural killer (NK)/T-cell lymphoma and leukemia. Cancer Sci. 2008;99(5):1016–20.CrossRefPubMedGoogle Scholar
  92. 92.
    Schmitz N, Trümper L, Ziepert M, Nickelsen M, Ho AD, Metzner B, et al. Treatment and prognosis of mature T-cell and NK-cell lymphoma: an analysis of patients with T-cell lymphoma treated in studies of the German High-Grade Non-Hodgkin Lymphoma Study Group. Blood. 2010;116(18):3418–25.CrossRefPubMedGoogle Scholar
  93. 93.
    Sieniawski M, Angamuthu N, Boyd K, Chasty R, Davies J, Forsyth P, et al. Evaluation of enteropathy-associated T-cell lymphoma comparing standard therapies with a novel regimen including autologous stem cell transplantation. Blood. 2010;115(18):3664–70.CrossRefPubMedGoogle Scholar
  94. 94.
    Nijeboer P, Malamut G, Mulder CJ, Cerf-Bensussan N, Sibon D, Bouma G, et al. Enteropathy-associated T-cell lymphoma: improving treatment strategies. Dig Dis. 2015;33(2):231–5.CrossRefPubMedGoogle Scholar
  95. 95.
    Dionigi G, Annoni M, Rovera F, Boni L, Villa F, Castano P, et al. Primary colorectal lymphomas: review of the literature. Surg Oncol. 2007;16(Suppl 1):S169–71.CrossRefPubMedGoogle Scholar
  96. 96.
    Kim YH, Lee JH, Yang SK, Kim TI, Kim JS, Kim HJ, et al. Primary colon lymphoma in Korea: a KASID (Korean Association for the Study of Intestinal Diseases) Study. Dig Dis Sci. 2005;50(12):2243–7.CrossRefPubMedGoogle Scholar
  97. 97.
    Doolabh N, Anthony T, Simmang C, Bieligk S, Lee E, Huber P, et al. Primary colonic lymphoma. J Surg Oncol. 2000;74(4):257–62.CrossRefPubMedGoogle Scholar
  98. 98.
    Yu H, Wang Y, Peng L, Lia A, Zhang Y. Endoscopic manifestations of primary colorectal lymphoma. Hepato-Gastroenterology. 2014;61(129):76–8.PubMedGoogle Scholar
  99. 99.
    Mendelson RM, Fermoyle S. Primary gastrointestinal lymphomas: a radiological-pathological review. Part 1: stomach, oesophagus and colon. Australas Radiol. 2005;49(5):353–64.CrossRefPubMedGoogle Scholar
  100. 100.
    Koniaris LG, Drugas G, Katzman PJ, Salloum R. Management of gastrointestinal lymphoma. J Am Coll Surg. 2003;197(1):127–41.CrossRefPubMedGoogle Scholar
  101. 101.
    Maddocks K, Blum KA. Treatment strategies in mantle cell lymphoma. Cancer Treat Res. 2015;165:251–70.CrossRefPubMedGoogle Scholar
  102. 102.
    Stanojevic GZ, Nestorovic MD, Brankovic BR, Stojanovic MP, Jovanovic MM, Radojkovic MD. Primary colorectal lymphoma: an overview. World J Gastrointest Oncol. 2011;3(1):14–8.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Ghimire P, Wu GY, Zhu L. Primary gastrointestinal lymphoma. World J Gastroenterol. 2011;17:697–707.CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Arora N, Manipadam MT, Pulimood A, Ramakrishna BS, Chacko A, Kurian SS, et al. Gastrointestinal lymphomas: pattern of distribution and histological subtypes: 10 years experience in a tertiary centre in South India. Indian J Pathol Microbiol. 2011;54(4):712–9.PubMedGoogle Scholar
  105. 105.
    Vetro C, Romano A, Amico I, Conticello C, Motta G, Figuera A, et al. Endoscopic features of gastro-intestinal lymphomas: from diagnosis to follow-up. World J Gastroenterol. 2014;20(36):12993–3005.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Morton LM, Wang SS, Devesa SS, Hartge P, Weisenburger DD, Linet MS. Lymphoma incidence patterns by WHO subtype in the United States, 1992–2001. Blood. 2006;107:265–76.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Sant M, Allemani C, Tereanu C, De Angelis R, Capocaccia R, Visser O, et al. Incidence of hematologic malignancies in Europe by morphologic subtype: results of the HAEMACARE project. Blood. 2010;116:3724–34.CrossRefPubMedGoogle Scholar
  108. 108.
    Warrick J, Luo J, Robirds D, Branson J, Frater JL, Kreisel F, et al. Gastrointestinal lymphomas in a North American population: clinicopathologic features from one major Central-Midwestern United States tertiary care medical center. Diagn Pathol. 2012;28(7):76.CrossRefGoogle Scholar
  109. 109.
    Ekstrom-Smedby K. Epidemiology and etiology of Non-Hodgkin lymphoma: a review. Acta Oncol. 2006;45:258–71.CrossRefPubMedGoogle Scholar
  110. 110.
    Solal-Céligny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, et al. Follicular lymphoma international prognostic index. Blood. 2004;104:1258–65.CrossRefPubMedGoogle Scholar
  111. 111.
    Aschebrook-Kilfoy B, Caces DB, Ollberding NJ, Smith SM, Chiu BC. An upward trend in the age-specific incidence patterns for mantle cell lymphoma in the USA. Leuk Lymphoma. 2013;54(8):1677–83.CrossRefPubMedGoogle Scholar
  112. 112.
    Romaguera JE, Medeiros LJ, Hagemeister FB, Fayad LE, Rodriguez MA, Pro B, et al. Frequency of gastrointestinal involvement and its clinical significance in mantle cell lymphoma. Cancer. 2003;97:586–91.CrossRefPubMedGoogle Scholar
  113. 113.
    Salar A, Juanpere N, Bellosillo B, Domingo-Domenech E, Espinet B, Seoane A, et al. Gastrointestinal involvement in mantle cell lymphoma: a prospective clinic, endoscopic, and pathologic study. Am J Surg Pathol. 2006;30:1274–80.CrossRefPubMedGoogle Scholar
  114. 114.
    Ruskoné-Fourmestraux A, Delmer A, Lavergne A, Molina T, Brousse N, Audouin J, et al. Multiple lymphomatous polyposis of the gastrointestinal tract: prospective clinicopathologic study of 31 cases. Groupe D’étude des Lymphomes Digestifs. Gastroenterology. 1997;112(1):7–16.CrossRefPubMedGoogle Scholar
  115. 115.
    Leoncini L, et al. Burkitt lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoid tissues. 4th ed. Lyon: IARC; 2008. p. 262–4.Google Scholar
  116. 116.
    Hartge P, Wang S. Overview of the etiology and epidemiology of lymphoma. In: Mauch PMAJOCB, Dalla-Favera R, Harris NL, editors. Non-Hodgkin’s lymphomas. New York: Lippincott, Williams andWilkins; 2004. p. 711–27.Google Scholar
  117. 117.
    Vianna NJ. The malignant lymphomas: epidemiology and related aspects. Pathobiology Annual. 1977;7:231–55.PubMedGoogle Scholar
  118. 118.
    Raphael M, Said J, Borisch B, Cesarman E, Harris NL. Lymphomas associated with HIV infection. In: Swerdlow SH, Campo E, HarrisNL JES, Pileri SA, Stein H, et al., editors. WHO classification oftumors of haematopoietic and lymphoid tissues. 4th ed. Lyon: IARCPress; 2008. p. 340–1.Google Scholar
  119. 119.
    Oyama T, Ichimura K, Suzuki R, Suzumiya J, Ohshima K, Yatabe Y, et al. Senile EBV+ B-cell lymphoproliferative disorders: a clin-icopathologic study of 22 patients. Am J Surg Pathol. 2003;27(1):16–26.CrossRefPubMedGoogle Scholar
  120. 120.
    De Vita S, Sacco C, Sansonno D, Gloghini A, Dammacco F, Crovatto M, et al. Characterization of overt B-cell lymphomas in patients withhepatitis C virus infection. Blood. 1997;90(2):776–82.PubMedGoogle Scholar
  121. 121.
    Wu W, Doan N, Said J, Karunasiri D, Pullarkat ST. Strong expression of chemokine receptor CCR9 in diffuse large B-cell lymphoma and follicular lymphoma strongly correlates with gastrointestinal involvement. Hum Pathol. 2014;45(7):1451–8.CrossRefPubMedGoogle Scholar
  122. 122.
    Ma S. Risk Factors of Follicular Lymphoma. Expert Opin Med Diagn. 2012;6(4):323–33.CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    De Sanjose S, Benavente Y, Vajdic CM, Engels EA, Morton LM, Bracci PM, et al. Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepatol. 2008;6:451–8.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Bertoni F, Rinaldi A, Zucca E, Cavalli F. Update on the molecular biology of mantle cell lymphoma. Hematol Oncol. 2006;24:22–7.CrossRefPubMedGoogle Scholar
  125. 125.
    Orem J, Mbidde EK, Lambert B, de Sanjose S, Weiderpass E. Burkitt’s lymphoma in Africa, a review of the epidemiology and etiology. Afr Health Sci. 2007;7(3):166–75.PubMedPubMedCentralGoogle Scholar
  126. 126.
    Tilly H, Gomes da Silva M, Vitolo U, Jack A, Meignan M, Lopez-Guillermo A, et al; ESMO Guidelines Committee. Diffuse large B-cell lymphoma (DLBCL): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2015;26 Suppl 5:v116–25.CrossRefPubMedGoogle Scholar
  127. 127.
    Scott DW, Wright GW, Williams PM, Lih CJ, Walsh W, Jaffe ES, et al. Determining cell-of-origin subtypes of diffuse large B-cell lymphoma using gene expression in formalin-fixed paraffin-embedded tissue. Blood. 2014;123:1214–7.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Akasaka T, Lossos IS, Levy R. BCL6 gene translocation in follicular lymphoma: a harbinger of eventual transformation to diffuse aggressive lymphoma. Blood. 2003;102:1443.CrossRefPubMedGoogle Scholar
  129. 129.
    Dreyling M, Ghielmini M, Marcus R, Salles G, Vitolo U, Ladetto M, ESMO Guidelines Working Group. Newly diagnosed and relapsed follicular lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25(Suppl 3):iii76–82.CrossRefPubMedGoogle Scholar
  130. 130.
    Vose JM. Mantle cell lymphoma: 2015 update on diagnosis, risk-stratification, and clinical management. Am J Hematol. 2015;90(8):739–45.CrossRefPubMedGoogle Scholar
  131. 131.
    Fernàndez V, Salamero O, Espinet B, Solé F, Royo C, Navarro A, et al. Genomic and gene expression profiling defines indolent forms of mantle cell lymphoma. Cancer Res. 2010;70:1408–18.CrossRefPubMedGoogle Scholar
  132. 132.
    Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. Report of the committee on Hodgkin lymphoma staging classification. Cancer Res. 1971;31(11):1860–1.PubMedGoogle Scholar
  133. 133.
    Martelli M, Ferreri AJ, Agostinelli C, Di Rocco A, Pfreundschuh M, Pileri SA. Diffuse large B-cell lymphoma. Crit Rev Oncol Hematol. 2013;87(2):146–71.CrossRefGoogle Scholar
  134. 134.
    Cheson BD. Role of functional imaging in the management of lym-phoma. J Clin Oncol. 2011;29(14):1844–54.CrossRefPubMedGoogle Scholar
  135. 135.
    Miller TP. The limits of limited stage lymphoma. J Clin Oncol. 2004;22(15):2982–4.CrossRefPubMedGoogle Scholar
  136. 136.
    Dunleavy K, Pittaluga S, Czuczman MS, Dave SS, Wright G, Grant N, et al. Differential efficacy of bortezomib plus chemotherapy within molecular subtypes of diffuse large B-cell lymphoma. Blood. 2009;113:6069–76.CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Hernandez-Ilizaliturri FJ, Deeb G, Zinzani PL, Pileri SA, Malik F, Macon WR, et al. Higher response to lenalidomide in relapsed/refractory diffuse large B-cell lymphoma in nongerminal center B-cell-like than in germinal center B-cell-like phenotype. Cancer. 2011;117:5058–66.CrossRefPubMedGoogle Scholar
  138. 138.
    Van Oers MH, Klasa R, Marcus RE, Wolf M, Kimby E, Gascoyne RD, et al. Rituximab maintenance improves clinical outcome of relapsed/resistant follicular non-Hodgkin lymphoma in patients both with and without rituximab during induction: results of a prospective randomized phase 3 intergroup trial. Blood. 2006;108:3295–301.CrossRefPubMedGoogle Scholar
  139. 139.
    Hoster E, Dreyling M, Klapper W, Gisselbrecht C, van Hoof A, Kluin-Nelemans HC, et al. A new prognostic index (MIPI) for patients with advanced mantle cell lymphoma. Blood. 2008;111:558–65.CrossRefPubMedGoogle Scholar
  140. 140.
    Rummel M, Niederle N, Maschmeyer G, Banat GA, von Grünhagen U, Losem C, et al. Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment for patients with indolent and mantle-cell lymphomas: an open-label, muticentre, randomised, phase 3 non-inferiority trial. Lancet. 2013;381:1203–10.CrossRefPubMedGoogle Scholar
  141. 141.
    Romaguera JE, Fayad L, Rodriguez MA, Broglio KR, Hagemeister FB, Pro B, et al. High rate of durable remission after treatment of newly diagnosed aggressive mantle-cell lymphoma with rituximab plus Hyper-CVAD alternating with rituximab plus high-dose methotrexate and cytarabine. J Clin Oncol. 2005;23:7013–23.CrossRefPubMedGoogle Scholar
  142. 142.
    Wang L, Rule S, Martin P, Goy A, Auer R, Kahl BS, et al. Targeting BTK with ibruitinib in relapsed or refractory mantle cell lymphoma. N Engl J Med. 2014;369:507–16.CrossRefGoogle Scholar
  143. 143.
    Thomas DA, Faderl S, O’Brien S, Bueso-Ramos C, Cortes J, Garcia-Manero G, et al. Chemoimmunotherapy with hyper-CVAD plus rituximab for the treatment of adult Burkitt and Burkitt-type lymphoma or acute lymphoblastic leukemia. Cancer. 2006;106(7):1569–80.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alma Aslan
    • 1
  • Serkan Akın
    • 1
  • Taner Babacan
    • 1
  • Evren Özdemir
    • 1
  1. 1.Department of Medical OncologyHacettepe University Institute of CancerSıhhiyeTurkey

Personalised recommendations