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Review

Update on the risk of lymphoma following immunosuppressive therapy for inflammatory bowel disease

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Pages 621-631 | Published online: 10 Jan 2014

References

  • Engels EA, Biggar RJ, Hall HI et al. Cancer risk in people infected with human immunodeficiency virus in the United States. Int. J. Cancer123(1), 187–194 (2008).
  • Mbulaiteye SM, Biggar RJ, Goedert JJ, Engels EA. Immune deficiency and risk for malignancy among persons with AIDS. J. Acquir. Immune Defic. Syndr.32(5), 527–533 (2003).
  • Biggar RJ, Chaturvedi AK, Goedert JJ, Engels EA, HIV/AIDS Cancer Match Study. AIDS-related cancer and severity of immunosuppression in persons with AIDS. J. Natl Cancer Inst.99(12), 962–972 (2007).
  • Kamel OW, van de Rijn M, Weiss LM et al. Brief report: reversible lymphomas associated with Epstein–Barr virus occurring during methotrexate therapy for rheumatoid arthritis and dermatomyositis. N. Engl. J. Med.328(18), 1317–1321 (1993).
  • Nalesnik MA, Jaffe R, Starzl TE et al. The pathology of posttransplant lymphoproliferative disorders occurring in the setting of cyclosporine A-prednisone immunosuppression. Am. J. Pathol.133(1), 173–192 (1988).
  • Paul C, Le Tourneau A, Cayuela JM et al. Epstein–Barr virus-associated lymphoproliferative disease during methotrexate therapy for psoriasis. Arch. Dermatol.133(7), 867–871 (1997).
  • Pietersma F, Piriou E, van Baarle D. Immune surveillance of EBV-infected B cells and the development of non-Hodgkin lymphomas in immunocompromised patients. Leuk. Lymphoma49(6), 1028–1041 (2008).
  • Dantal J, Pohanka E. Malignancies in renal transplantation: an unmet medical need. Nephrol. Dial. Transplant.22(Suppl. 1), i4–i10 (2007).
  • Buell JF, Gross TG, Woodle ES. Malignancy after transplantation. Transplantation80(2 Suppl.), S254–S264 (2005).
  • Bachman TR, Sawitzke AD, Perkins SL, Ward JH, Cannon GW. Methotrexate-associated lymphoma in patients with rheumatoid arthritis: report of two cases. Arthritis Rheum.39(2), 325–329 (1996).
  • Liote F, Pertuiset E, Cochand-Priollet B et al. Methotrexate related B lymphoproliferative disease in a patient with rheumatoid arthritis. Role of Epstein–Barr virus infection. J. Rheumatol.22(6), 1174–1178 (1995).
  • Hoshida Y, Xu JX, Fujita S et al. Lymphoproliferative disorders in rheumatoid arthritis: clinicopathological analysis of 76 cases in relation to methotrexate medication. J. Rheumatol.34(2), 322–331 (2007).
  • Salloum E, Cooper DL, Howe G et al. Spontaneous regression of lymphoproliferative disorders in patients treated with methotrexate for rheumatoid arthritis and other rheumatic diseases. J. Clin. Oncol.14(6), 1943–1949 (1996).
  • Viraben R, Brousse P, Lamant L. Reversible cutaneous lymphoma occurring during methotrexate therapy. Br. J. Dermatol.135(1), 116–118 (1996).
  • Dantal J, Hourmant M, Cantarovich D et al. Effect of long-term immunosuppression in kidney-graft recipients on cancer incidence: randomised comparison of two cyclosporin regimens. Lancet351(9103), 623–628 (1998).
  • Opelz G, Dohler B. Lymphomas after solid organ transplantation: a collaborative transplant study report. Am. J. Transplant.4(2), 222–230 (2004).
  • Gutierrez-Dalmau A, Campistol JM. Immunosuppressive therapy and malignancy in organ transplant recipients: a systematic review. Drugs67(8), 1167–1198 (2007).
  • Guba M, Graeb C, Jauch KW, Geissler EK. Pro- and anti-cancer effects of immunosuppressive agents used in organ transplantation. Transplantation77(12), 1777–1782 (2004).
  • Herman M, Weinstein T, Korzets A et al. Effect of cyclosporin A on DNA repair and cancer incidence in kidney transplant recipients. J. Lab. Clin. Med.137(1), 14–20 (2001).
  • Starzl TE, Nalesnik MA, Porter KA et al. Reversibility of lymphomas and lymphoproliferative lesions developing under cyclosporin-steroid therapy. Lancet1(8377), 583–587 (1984).
  • Zijlmans JM, van Rijthoven AW, Kluin PM, Jiwa NM, Dijkmans BA, Kluin-Nelemans JC. Epstein–Barr virus-associated lymphoma in a patient with rheumatoid arthritis treated with cyclosporine. N. Engl. J. Med.326(20), 1363 (1992).
  • Watabe H, Soma Y, Obara W et al. Adult T-cell lymphoma/leukaemia developing in a patient with psoriasis treated with long-term cyclosporine. Acta Derm. Venereol.86(2), 184–185 (2006).
  • Lelievre JD, Sacre K, Adle-Biassette H, Molinier-Frenkel V, Gaulard P, Papo T. Epstein–Barr virus-associated lymphoproliferative disease after long-standing cyclosporine therapy for psoriasis: a case of spontaneous regression. J. Am. Acad. Dermatol.52(2 Suppl. 1), 24–27 (2005).
  • Corazza M, Zampino MR, Montanari A, Altieri E, Virgili A. Primary cutaneous CD30+ large T-cell lymphoma in a patient with psoriasis treated with cyclosporine. Dermatology206(4), 330–333 (2003).
  • Mahe E, Descamps V, Grossin M, Fraitag S, Crickx B. CD30+ T-cell lymphoma in a patient with psoriasis treated with ciclosporin and infliximab. Br. J. Dermatol.149(1), 170–173 (2003).
  • Cockburn IT, Krupp P. The risk of neoplasms in patients treated with cyclosporine A. J. Autoimmun.2(5), 723–731 (1989).
  • Birkeland SA, Hamilton-Dutoit S. Is posttransplant lymphoproliferative disorder (PTLD) caused by any specific immunosuppressive drug or by the transplantation per se? Transplantation76(6), 984–988 (2003).
  • Paul CF, Ho VC, McGeown C et al. Risk of malignancies in psoriasis patients treated with cyclosporine: a 5 y cohort study. J. Invest. Dermatol.120(2), 211–216 (2003).
  • Hannuksela-Svahn A, Pukkala E, Laara E, Poikolainen K, Karvonen J. Psoriasis, its treatment, and cancer in a cohort of Finnish patients. J. Invest. Dermatol.114(3), 587–590 (2000).
  • Farrell RJ, Ang Y, Kileen P et al. Increased incidence of non-Hodgkin’s lymphoma in inflammatory bowel disease patients on immunosuppressive therapy but overall risk is low. Gut47(4), 514–519 (2000).
  • Shibahara T, Miyazaki K, Sato D et al. Rectal malignant lymphoma complicating ulcerative colitis treated with long-term cyclosporine A. J. Gastroenterol. Hepatol.21(1 Pt 2), 336–338 (2006).
  • Schwartz LK, Kim MK, Coleman M, Lichtiger S, Chadburn A, Scherl E. Case report: lymphoma arising in an ileal pouch anal anastomosis after immunomodulatory therapy for inflammatory bowel disease. Clin. Gastroenterol. Hepatol.4(8), 1030–1034 (2006).
  • Ellman MH, Hurwitz H, Thomas C, Kozloff M. Lymphoma developing in a patient with rheumatoid arthritis taking low dose weekly methotrexate. J. Rheumatol.18(11), 1741–1743 (1991).
  • Kingsmore SF, Hall BD, Allen NB, Rice JR, Caldwell DS. Association of methotrexate, rheumatoid arthritis and lymphoma: report of 2 cases and literature review. J. Rheumatol.19(9), 1462–1465 (1992).
  • Thomason RW, Craig FE, Banks PM, Sears DL, Myerson GE, Gulley ML. Epstein–Barr virus and lymphoproliferation in methotrexate-treated rheumatoid arthritis. Mod. Pathol.9(3), 261–266 (1996).
  • Ebeo CT, Girish MR, Byrd RP, Roy TM, Mehta JB. Methotrexate-induced pulmonary lymphoma. Chest123(6), 2150–2153 (2003).
  • Suzuki M, Hirano S, Ito H et al. Pulmonary lymphoma developed during long-term methotrexate therapy for psoriasis. Respirology12(5), 774–776 (2007).
  • Khopkar U, Bhor U. Hodgkin’s lymphoma in a patient of psoriasis treated with long-term, low-dose methotrexate therapy. Indian J. Dermatol. Venereol. Leprol.74(4), 379–382 (2008).
  • Gridley G, McLaughlin JK, Ekbom A et al. Incidence of cancer among patients with rheumatoid arthritis. J. Natl. Cancer Inst.85(4), 307–311 (1993).
  • Hakulinen T, Isomaki H, Knekt P. Rheumatoid arthritis and cancer studies based on linking nationwide registries in Finland. Am. J. Med.78(1A), 29–32 (1985).
  • Isomaki HA, Hakulinen T, Joutsenlahti U. Excess risk of lymphomas, leukemia and myeloma in patients with rheumatoid arthritis. J. Chronic Dis.31(11), 691–696 (1978).
  • Prior P. Cancer and rheumatoid arthritis: epidemiologic considerations. Am. J. Med.78(1A), 15–21 (1985).
  • Silman AJ, Petrie J, Hazleman B, Evans SJ. Lymphoproliferative cancer and other malignancy in patients with rheumatoid arthritis treated with azathioprine: a 20 year follow up study. Ann. Rheum. Dis.47(12), 988–992 (1988).
  • Symmons DP. Neoplasms of the immune system in rheumatoid arthritis. Am. J. Med.78(1A), 22–28 (1985).
  • Wolfe F, Michaud K. Lymphoma in rheumatoid arthritis: the effect of methotrexate and anti-tumor necrosis factor therapy in 18,572 patients. Arthritis Rheum.50(6), 1740–1751 (2004).
  • Santana V, Rose NR. Neoplastic lymphoproliferation in autoimmune disease: an updated review. Clin. Immunol. Immunopathol.63(3), 205–213 (1992).
  • Stern RS, Zierler S, Parrish JA. Methotrexate used for psoriasis and the risk of noncutaneous or cutaneous malignancy. Cancer50(5), 869–872 (1982).
  • Stern RS. Lymphoma risk in psoriasis: results of the PUVA follow-up study. Arch. Dermatol.142(9), 1132–1135 (2006).
  • Bernatsky S, Clarke AE, Suissa S. Hematologic malignant neoplasms after drug exposure in rheumatoid arthritis. Arch. Intern. Med.168(4), 378–381 (2008).
  • Buchbinder R, Barber M, Heuzenroeder L et al. Incidence of melanoma and other malignancies among rheumatoid arthritis patients treated with methotrexate. Arthritis Rheum.59(6), 794–799 (2008).
  • Salliot C, van der Heijde D. Long-term safety of methotrexate monotherapy in patients with rheumatoid arthritis: a systematic literature research. Ann. Rheum. Dis.68(7), 1100–1104 (2009).
  • Tiede I, Fritz G, Strand S et al. CD28-dependent Rac1 activation is the molecular target of azathioprine in primary human CD4+ T lymphocytes. J. Clin. Invest.111(8), 1133–1145 (2003).
  • Present DH, Meltzer SJ, Krumholz MP, Wolke A, Korelitz BI. 6-Mercaptopurine in the management of inflammatory bowel disease: short- and long-term toxicity. Ann. Intern. Med.111(8), 641–649 (1989).
  • Connell WR, Kamm MA, Dickson M, Balkwill AM, Ritchie JK, Lennard-Jones JE. Long-term neoplasia risk after azathioprine treatment in inflammatory bowel disease. Lancet343(8908), 1249–1252 (1994).
  • George J, Present DH, Pou R, Bodian C, Rubin PH. The long-term outcome of ulcerative colitis treated with 6-mercaptopurine. Am. J. Gastroenterol.91(9), 1711–1714 (1996).
  • Bouhnik Y, Lemann M, Mary JY et al. Long-term follow-up of patients with Crohn’s disease treated with azathioprine or 6-mercaptopurine. Lancet347(8996), 215–219 (1996).
  • Korelitz BI, Mirsky FJ, Fleisher MR, Warman JI, Wisch N, Gleim GW. Malignant neoplasms subsequent to treatment of inflammatory bowel disease with 6-mercaptopurine. Am. J. Gastroenterol.94(11), 3248–3253 (1999).
  • Fraser AG, Orchard TR, Robinson EM, Jewell DP. Long-term risk of malignancy after treatment of inflammatory bowel disease with azathioprine. Aliment. Pharmacol. Ther.16(7), 1225–1232 (2002).
  • Glazier KD, Palance AL, Griffel LH, Das KM. The ten-year single-center experience with 6-mercaptopurine in the treatment of inflammatory bowel disease. J. Clin. Gastroenterol.39(1), 21–26 (2005).
  • Lewis JD, Bilker WB, Brensinger C, Deren JJ, Vaughn DJ, Strom BL. Inflammatory bowel disease is not associated with an increased risk of lymphoma. Gastroenterology121(5), 1080–1087 (2001).
  • Armstrong RG, West J, Card TR. Risk of cancer in inflammatory bowel disease treated with azathioprine: a UK population-based case–control study. Am. J. Gastroenterol. (2010) (Epub ahead of print).
  • Beaugerie L, Brousse N, Bouvier AM et al. Lymphoproliferative disorders in patients receiving thiopurines for inflammatory bowel disease: a prospective observational cohort study. Lancet374(9701), 1617–1625 (2009).
  • 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. Gut54(8), 1121–1125 (2005).
  • Masunaga Y, Ohno K, Ogawa R, Hashiguchi M, Echizen H, Ogata H. Meta-analysis of risk of malignancy with immunosuppressive drugs in inflammatory bowel disease. Ann. Pharmacother.41(1), 21–28 (2007).
  • Dayharsh GA, Loftus EV Jr, Sandborn WJ et al. Epstein–Barr virus-positive lymphoma in patients with inflammatory bowel disease treated with azathioprine or 6-mercaptopurine. Gastroenterology122(1), 72–77 (2002).
  • Bewtra M, Lichtenstein GR. Infliximab use in Crohn’s disease. Expert Opin. Biol. Ther.5(4), 589–599 (2005).
  • Cohen RD, Tsang JF, Hanauer SB. Infliximab in Crohn’s disease: first anniversary clinical experience. Am. J. Gastroenterol.95(12), 3469–3477 (2000).
  • Ricart E, Panaccione R, Loftus EV, Tremaine WJ, Sandborn WJ. Infliximab for Crohn’s disease in clinical practice at the Mayo Clinic: the first 100 patients. Am. J. Gastroenterol.96(3), 722–729 (2001).
  • Seiderer J, Goke B, Ochsenkuhn T. Safety aspects of infliximab in inflammatory bowel disease patients. A retrospective cohort study in 100 patients of a German University Hospital. Digestion70(1), 3–9 (2004).
  • Wenzl HH, Reinisch W, Jahnel J et al. Austrian infliximab experience in Crohn’s disease: a nationwide cooperative study with long-term follow-up. Eur. J. Gastroenterol. Hepatol.16(8), 767–773 (2004).
  • Sands BE, Anderson FH, Bernstein CN et al. Infliximab maintenance therapy for fistulizing Crohn’s disease. N. Engl. J. Med.350(9), 876–885 (2004).
  • Rutgeerts P, Sandborn WJ, Feagan BG et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N. Engl. J. Med.353(23), 2462–2476 (2005).
  • Caspersen S, Elkjaer M, Riis L et al. Infliximab for inflammatory bowel disease in Denmark 1999–2005: clinical outcome and follow-up evaluation of malignancy and mortality. Clin. Gastroenterol. Hepatol.6(11), 1212–1217; quiz 1176 (2008).
  • Lichtenstein GR, Cohen R, Feagan BG et al. Safety of infliximab and other Crohn’s disease therapies: TREAT™ registry data with 24,575 patient-years of follow-up. Am. J. Gastroenterol.103(S1), (2008).
  • Hanauer SB, Feagan BG, Lichtenstein GR et al. Maintenance infliximab for Crohn’s disease: the ACCENT I randomised trial. Lancet359(9317), 1541–1549 (2002).
  • Ljung T, Karlen P, Schmidt D et al. Infliximab in inflammatory bowel disease: clinical outcome in a population based cohort from Stockholm County. Gut53(6), 849–853 (2004).
  • Colombel JF, Loftus EV Jr, Tremaine WJ et al. The safety profile of infliximab in patients with Crohn’s disease: the Mayo clinic experience in 500 patients. Gastroenterology126(1), 19–31 (2004).
  • Lees CW, Ali AI, Thompson AI et al. The safety profile of anti-tumour necrosis factor therapy in inflammatory bowel disease in clinical practice: analysis of 620 patient-years follow-up. Aliment. Pharmacol. Ther.29(3), 286–297 (2009).
  • Brown SL, Greene MH, Gershon SK, Edwards ET, Braun MM. Tumor necrosis factor antagonist therapy and lymphoma development: twenty-six cases reported to the Food and Drug Administration. Arthritis Rheum.46(12), 3151–3158 (2002).
  • FDA Board Document. Update on the TNF-α blocking agents; 2003 (2009).
  • Khanna D, McMahon M, Furst DE. Safety of tumour necrosis factor-α antagonists. Drug Saf.27(5), 307–324 (2004).
  • Mikuls TR, Weaver AL. Lessons learned in the use of tumor necrosis factor-α inhibitors in the treatment of rheumatoid arthritis. Curr. Rheumatol. Rep.5(4), 270–277 (2003).
  • Scheinfeld N. A comprehensive review and evaluation of the side effects of the tumor necrosis factor α blockers etanercept, infliximab and adalimumab. J. Dermatolog. Treat.15(5), 280–294 (2004).
  • Schiff MH, Burmester GR, Kent JD et al. Safety analyses of adalimumab (HUMIRA) in global clinical trials and US postmarketing surveillance of patients with rheumatoid arthritis. Ann. Rheum. Dis.65(7), 889–894 (2006).
  • Hanauer SB, Sandborn WJ, Rutgeerts P et al. Human anti-tumor necrosis factor monoclonal antibody (adalimumab) in Crohn’s disease: the CLASSIC-I trial. Gastroenterology130(2), 323–333 (2006).
  • Colombel JF, Sandborn WJ, Rutgeerts P et al. Adalimumab for maintenance of clinical response and remission in patients with Crohn’s disease: the CHARM trial. Gastroenterology132(1), 52–65 (2007).
  • Sandborn WJ, Feagan BG, Stoinov S et al. Certolizumab pegol for the treatment of Crohn’s disease. N. Engl. J. Med.357(3), 228–238 (2007).
  • Rosh JR, Lerer T, Markowitz J et al. Retrospective Evaluation of the Safety and Effect of Adalimumab Therapy (RESEAT) in pediatric Crohn’s disease. Am. J. Gastroenterol.104(12), 3042–3049 (2009).
  • Humira® Injection Prescribing Information and Medication Guide. Abbot Laboratories, IL, USA (2009).
  • Schreiber S, Rutgeerts P, Fedorak RN et al. A randomized, placebo-controlled trial of certolizumab pegol (CDP870) for treatment of Crohn’s disease. Gastroenterology129(3), 807–818 (2005).
  • Schreiber S, Khaliq-Kareemi M, Lawrance IC et al. Maintenance therapy with certolizumab pegol for Crohn’s disease. N. Engl. J. Med.357(3), 239–250 (2007).
  • Peyrin-Biroulet L, Deltenre P, de Suray N et al. Efficacy and safety of tumor necrosis factor antagonists in Crohn’s disease: meta-analysis of placebo-controlled trials. Clin. Gastroenterol. Hepatol.6(6), 644–653 (2008).
  • Siegel CA, Marden SM, Persing SM, Larson RJ, Sands BE. Risk of lymphoma associated with combination anti-tumor necrosis factor and immunomodulator therapy for the treatment of Crohn’s disease: a meta-analysis. Clin. Gastroenterol. Hepatol.7(8), 874–881 (2009).
  • Targan SR, Feagan BG, Fedorak RN et al. Natalizumab for the treatment of active Crohn’s disease: results of the ENCORE Trial. Gastroenterology132(5), 1672–1683 (2007).
  • Schweikert A, Kremer M, Ringel F et al. Primary central nervous system lymphoma in a patient treated with natalizumab. Ann. Neurol.66(3), 403–406 (2009).
  • Khan WA, Yu L, Eisenbrey AB et al. Hepatosplenic γ/δ T-cell lymphoma in immunocompromised patients. Report of two cases and review of literature. Am. J. Clin. Pathol.116(1), 41–50 (2001).
  • Ochenrider MG, Patterson DJ, Aboulafia DM. Hepatosplenic T-cell lymphoma in a young man with Crohn’s disease: case report and literature review. Clin. Lymphoma Myeloma Leuk.10(2), 144–148 (2010).
  • Mackey AC, Green L, Leptak C, Avigan M. Hepatosplenic T cell lymphoma associated with infliximab use in young patients treated for inflammatory bowel disease: update. J. Pediatr. Gastroenterol. Nutr.48(3), 386–388 (2009).
  • Mackey AC, Green L, Liang LC, Dinndorf P, Avigan M. Hepatosplenic T cell lymphoma associated with infliximab use in young patients treated for inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr.44(2), 265–267 (2007).
  • Thayu M, Markowitz JE, Mamula P, Russo PA, Muinos WI, Baldassano RN. Hepatosplenic T-cell lymphoma in an adolescent patient after immunomodulator and biologic therapy for Crohn disease. J. Pediatr. Gastroenterol. Nutr.40(2), 220–222 (2005).
  • Zeidan A, Sham R, Shapiro J, Baratta A, Kouides P. Hepatosplenic T-cell lymphoma in a patient with Crohn’s disease who received infliximab therapy. Leuk. Lymphoma48(7), 1410–1413 (2007).
  • Humphreys MR, Cino M, Quirt I, Barth D, Kukreti V. Long-term survival in two patients with hepatosplenic T cell lymphoma treated with interferon-α. Leuk. Lymphoma49(7), 1420–1423 (2008).
  • Lewis JD, Gelfand JM, Troxel AB et al. Immunosuppressant medications and mortality in inflammatory bowel disease. Am. J. Gastroenterol.103(6), 1428–1435; quiz 1436 (2008).
  • Siegel CA, Hur C, Korzenik JR, Gazelle GS, Sands BE. Risks and benefits of infliximab for the treatment of Crohn’s disease. Clin. Gastroenterol. Hepatol.4(8), 1017–1024 (2006).
  • Lewis JD, Schwartz JS, Lichtenstein GR. Azathioprine for maintenance of remission in Crohn’s disease: benefits outweigh the risk of lymphoma. Gastroenterology118(6), 1018–1024 (2000).
  • Johnson FR, Ozdemir S, Mansfield C et al. Crohn’s disease patients’ risk-benefit preferences: serious adverse event risks versus treatment efficacy. Gastroenterology133(3), 769–779 (2007).
  • Toruner M, Loftus EV Jr, Harmsen WS et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology134(4), 929–936 (2008).
  • Van Assche G, Magdelaine-Beuzelin C, D’Haens G et al. Withdrawal of immunosuppression in Crohn’s disease treated with scheduled infliximab maintenance: a randomized trial. Gastroenterology134(7), 1861–1868 (2008).
  • Sandborn WJ, Rutgeerts PJ, Reinisch W et al. One year data from the SONIC study: a randomized, double-blind trial comparing infliximab and infliximab plus azathioprine to azathioprine in patients with Crohn’s disease naive to immunomodulators and biologic therapy. Presented at: Digestive Disease Week 2009. 30 May–4 June 2009, Chicago, IL, USA (Abstract 751f).

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