Association between use of thiopurines or tumor necrosis factor antagonists alone or in combination and risk of lymphoma in patients with inflammatory bowel disease

JAMA - Journal of the American Medical Association

Volumn 318, Issue 17, 2017, Pages 1679-1686

  Lemaitre, Magali ^a   Kirchgesner, Julien ^a,b,c   Rudnichi, Annie ^a   Carrat, Fabrice ^b,d   Zureik, Mahmoud ^a   Carbonnel, Franck ^e   Dray Spira, Rosemary ^a  

^a Agence Nationale de Sécurité des Médicaments et des Produits de Santé ANSM French National Agency for Medicines and Health Products Safety   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d HÔPITAL SAINT ANTOINE   (France)

^e BICÊTRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MERCAPTOPURINE; TUMOR NECROSIS FACTOR INHIBITOR; ANTIINFLAMMATORY AGENT; AZATHIOPRINE; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR;

ADULT; ARTICLE; CANCER RISK; COHORT ANALYSIS; COMBINATION DRUG THERAPY; CONTROLLED STUDY; DISEASE ASSESSMENT; DISEASE ASSOCIATION; FEMALE; FOLLOW UP; HIGH RISK PATIENT; HUMAN; INCIDENCE; INFLAMMATORY BOWEL DISEASE; LYMPHOMA; MAJOR CLINICAL STUDY; MALE; MONOTHERAPY; OBSERVATIONAL STUDY; PRIORITY JOURNAL; RISK REDUCTION; TREATMENT OUTCOME; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; MIDDLE AGED;

ADULT; ANTI-INFLAMMATORY AGENTS; ANTIBODIES, MONOCLONAL; AZATHIOPRINE; COHORT STUDIES; DRUG THERAPY, COMBINATION; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; LYMPHOMA; MALE; MIDDLE AGED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85034661471     PISSN: 00987484     EISSN: 15383598     Source Type: Journal    
DOI: 10.1001/jama.2017.16071     Document Type: Article

References (31)

1. Fraser AG, Orchard TR, Jewell DP. The efficacy of azathioprine for the treatment of inflammatory bowel disease: a 30 year review. Gut. 2002;50(4): 485-489.
2. Colombel JF, Sandborn WJ, Reinisch W, et al; SONIC Study Group. Infliximab, azathioprine, or combination therapy for Crohn’s disease. N Engl J Med. 2010;362(15):1383-1395.
3. Reinisch W, Sandborn WJ, Hommes DW, et al. Adalimumab for induction of clinical remission in moderately to severely active ulcerative colitis: results of a randomised controlled trial. Gut. 2011; 60(6):780-787.
4. Rutgeerts P, Van Assche G, Sandborn WJ, et al; EXTEND Investigators. Adalimumab induces and maintains mucosal healing in patients with Crohn’s disease: data from the EXTEND trial. Gastroenterology. 2012;142(5):1102-1111.e2.
5. D’Haens G, Baert F, van Assche G, et al; Belgian Inflammatory Bowel Disease Research Group; North-Holland Gut Club. Early combined immunosuppression or conventional management in patients with newly diagnosed Crohn’s disease: an open randomised trial. Lancet. 2008;371(9613): 660-667.
6. Jones JL, Kaplan GG, Peyrin-Biroulet L, et al. Effects of concomitant immunomodulator therapy on efficacy and safety of anti-tumor necrosis factor therapy for Crohn’s disease: a meta-analysis of placebo-controlled trials. Clin Gastroenterol Hepatol. 2015;13(13):2233-2240.e1.
7. Pasternak B, Svanström H, Schmiegelow K, Jess T, Hviid A. Use of azathioprine and the risk of cancer in inflammatory bowel disease. Am J Epidemiol. 2013;177(11):1296-1305.
8. 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 (8):1121-1125.
9. Beaugerie L, Brousse N, Bouvier AM, et al; CESAME Study Group. Lymphoproliferative disorders in patients receiving thiopurines for inflammatory bowel disease: a prospective observational cohort study. Lancet. 2009;374 (9701):1617-1625.
10. Nyboe Andersen N, Pasternak B, Basit S, et al. Association between tumor necrosis factor-α antagonists and risk of cancer in patients with inflammatory bowel disease. JAMA. 2014;311(23): 2406-2413.
11. 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. 2009;7(8):874-881.
12. Herrinton LJ, Liu L, Weng X, Lewis JD, Hutfless S, Allison JE. Role of thiopurine and anti-TNF therapy in lymphoma in inflammatory bowel disease. Am J Gastroenterol. 2011;106(12):2146-2153.
13. Osterman MT, Sandborn WJ, Colombel J-F, et al. Increased risk of malignancy with adalimumab combination therapy, compared with monotherapy, for Crohn’s disease. Gastroenterology. 2014;146(4): 941-949.
14. Kirchgesner J, Lemaitre M, Rudnichi A, et al. Therapeutic management of inflammatory bowel disease in real-life practice in the current era of anti-TNF agents: analysis of the French administrative health databases 2009-2014. Aliment Pharmacol Ther. 2017;45(1):37-49. doi:10 .1111/apt.13835
15. Weill A, Vallier N, Salanave B, et al. Frequency of thirty long-term illnesses for beneficiaries of the French general health insurance scheme in 2004. Pratiques et Organisation des Soins. 2006;37:173-188.
16. Bouillon K, Bertrand M, Maura G, Blotière P-O, Ricordeau P, Zureik M. Risk of bleeding and arterial thromboembolism in patients with non-valvular atrial fibrillation either maintained on a vitamin K antagonist or switched to a non-vitamin K-antagonist oral anticoagulant: a retrospective, matched-cohort study. Lancet Haematol. 2015;2(4): e150-e159.
17. Colas S, Collin C, Piriou P, Zureik M. Association between total hip replacement characteristics and 3-year prosthetic survivorship: a population-based study. JAMA Surg. 2015;150(10):979-988.
18. Weill A, Dalichampt M, Raguideau F, et al. Low dose oestrogen combined oral contraception and risk of pulmonary embolism, stroke, and myocardial infarction in five million French women: cohort study. BMJ. 2016;353:i2002.
19. Raguideau F, Lemaitre M, Dray-Spira R, Zureik M. Association between oral fluoroquinolone use and retinal detachment. JAMA Ophthalmol. 2016; 134(4):415-421.
20. Miranda S, Chaignot C, Collin C, Dray-Spira R, Weill A, Zureik M. Human papillomavirus vaccination and risk of autoimmune diseases: a large cohort study of over 2 million young girls in France. Vaccine. 2017;35(36):4761-4768.
21. Swoger JM, Regueiro M. Stopping, continuing, or restarting immunomodulators and biologics when an infection or malignancy develops. Inflamm Bowel Dis. 2014;20(5):926-935.
22. Annese V, Beaugerie L, Egan L, et al; ECCO. European evidence-based consensus: inflammatory bowel disease and malignancies. J Crohns Colitis. 2015;9(11):945-965.
23. Kotlyar DS, Lewis JD, Beaugerie L, et al. Risk of lymphoma in patients with inflammatory bowel disease treated with azathioprine and 6-mercaptopurine: a meta-analysis. Clin Gastroenterol Hepatol. 2015;13(5):847-58.e4.
24. Dulai PS, Siegel CA. The risk of malignancy associated with the use of biological agents in patients with inflammatory bowel disease. Gastroenterol Clin North Am. 2014;43(3):525-541.
25. Williams CJM, Peyrin-Biroulet L, Ford AC. Systematic review with meta-analysis: malignancies with anti-tumour necrosis factor-α therapy in inflammatory bowel disease. Aliment Pharmacol Ther. 2014;39(5):447-458.
26. Lichtenstein GR, Rutgeerts P, Sandborn WJ, et al. A pooled analysis of infections, malignancy, and mortality in infliximab- and immunomodulator-treated adult patients with inflammatory bowel disease. Am J Gastroenterol. 2012;107(7):1051-1063.
27. Nocturne G, Boudaoud S, Ly B, Pascaud J, Paoletti A, Mariette X. Impact of anti-TNF therapy on NK cells function and on immunosurveillance against B-cell lymphomas. J Autoimmun. 2017;80 (February):56-64.
28. Harris NL, Jaffe ES, Diebold J, et al. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting—Airlie House, Virginia, November 1997. J Clin Oncol. 1999;17(12):3835-3849.
29. Baecklund E, Iliadou A, Askling J, et al. Association of chronic inflammation, not its treatment, with increased lymphoma risk in rheumatoid arthritis. Arthritis Rheum. 2006;54(3): 692-701.
30. Beaugerie L, Itzkowitz SH. Cancers complicating inflammatory bowel disease. N Engl J Med. 2015;372(15):1441-1452.
31. Lewis JD, Bilker WB, Brensinger C, Deren JJ, Vaughn DJ, Strom BL. Inflammatory bowel disease is not associated with an increased risk of lymphoma. Gastroenterology. 2001;121(5):1080-1087.