The risk of cancer in patients with rheumatoid arthritis taking tumor necrosis factor antagonists: A nationwide cohort study

Arthritis Research and Therapy

Volumn 16, Issue 5, 2014, Pages

  Wu, Chun Ying ^a,b,c,d   Chen, Der Yuan ^a,b,d,e   Shen, Jui Lung ^b   Ho, Hsiu J ^b   Chen, Chih Chiang ^f   Kuo, Ken N ^g,h   Liu, Han Nan ^f   Chang, Yun Ting ^a,f   Chen, Yi Ju ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^f TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^g TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^h NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CORTICOSTEROID; CYCLOSPORIN; ETANERCEPT; HYDROXYCHLOROQUINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; METFORMIN; METHOTREXATE; RITUXIMAB; SALAZOSULFAPYRIDINE; ANTIRHEUMATIC AGENT; GOLIMUMAB; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR;

ADULT; AGE; ARTICLE; CANCER EPIDEMIOLOGY; CANCER INCIDENCE; CANCER RISK; COHORT ANALYSIS; COMORBIDITY; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE DURATION; DRUG USE; FEMALE; GENDER; HEALTH CARE UTILIZATION; HUMAN; LEUKEMIA; LYMPHOMA; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; RHEUMATOID ARTHRITIS; RISK FACTOR; RISK REDUCTION; TAIWAN; TREATMENT DURATION; AGED; ANTAGONISTS AND INHIBITORS; ARTHRITIS, RHEUMATOID; ASIAN CONTINENTAL ANCESTRY GROUP; COMPLICATION; ETHNOLOGY; INCIDENCE; INSURANCE; MULTIVARIATE ANALYSIS; NEOPLASMS; OUTCOME ASSESSMENT; PROPORTIONAL HAZARDS MODEL; STATISTICS AND NUMERICAL DATA;

ADALIMUMAB; ADULT; AGED; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; ASIAN CONTINENTAL ANCESTRY GROUP; COHORT STUDIES; CYCLOSPORINE; ETANERCEPT; FEMALE; HUMANS; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN G; INCIDENCE; INSURANCE; MALE; METHOTREXATE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASMS; OUTCOME ASSESSMENT (HEALTH CARE); PROPORTIONAL HAZARDS MODELS; RECEPTORS, TUMOR NECROSIS FACTOR; RISK FACTORS; TAIWAN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84969630247     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-014-0449-5     Document Type: Article

References (50)

1. Askling J, Fored CM, Baecklund E, Brandt L, Backlin C, Ekbom A, Sundström C, Bertilsson L, Cöster L, Geborek P, Jacobsson LT, Lindblad S, Lysholm J, Rantapää-Dahlqvist S, Saxne T, Klareskog L, Feltelius N: Haematopoietic malignancies in rheumatoid arthritis: lymphoma risk and characteristics after exposure to tumour necrosis factor antagonists. Ann Rheum Dis 2005, 64:1414-1420.
2. Askling J, Fored CM, Brandt L, Baecklund E, Bertilsson L, Feltelius N, Cöster L, Geborek P, Jacobsson LT, Lindblad S, Lysholm J, Rantapää-Dahlqvist S, Saxne T, Klareskog L: Risks of solid cancers in patients with rheumatoid arthritis and after treatment with tumour necrosis factor antagonists. Ann Rheum Dis 2005, 64:1421-1426.
3. Chen YJ, Chang YT, Wang CB, Wu CY: The risk of cancer in patients with rheumatoid arthritis: a nationwide cohort study in Taiwan. Arthritis Rheum 2011, 63:352-358.
4. Mellemkjaer L, Linet MS, Gridley G, Frisch M, Moller H, Olsen JH: Rheumatoid arthritis and cancer risk. Eur J Cancer 1996, 32A:1753-1757.
5. Abasolo L, Judez E, Descalzo MA, Gonzalez-Alvaro L, Jover JA, Carmona L: Cancer in rheumatoid arthritis: occurrence, mortality, and associated factors in a South European population. Semin Arthritis Rheum 2008, 37:388-397.
6. Thomas E, Brewster DH, Black RJ, Macfarlane GJ: Risk of malignancy among patients with rheumatic conditions. Int J Cancer 2000, 88:497-502.
7. Geborek P, Bladstrom A, Turesson C, Gulfe A, Petersson IF, Saxne T, Olsson H, Jacobsson LT: Tumour necrosis factor blockers do not increase overall tumour risk in patients with rheumatoid arthritis, but may be associated with an increased risk of lymphomas. Ann Rheum Dis 2005, 64:699-703.
8. Baecklund E, Ekbom A, Sparen P, Feltelius N, Klareskog L: Disease activity and risk of lymphoma in patients with rheumatoid arthritis: nested case-control study. BMJ 1998, 317:180-181.
9. Arber N, Levin B: Chemoprevention of colorectal neoplasia: the potential for personalized medicine. Gastroenterology 2008, 134:1224-1237.
10. Thun MJ, Henley SJ, Patrono C: Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 2002, 94:252-266.
11. Salloum E, Cooper DL, Howe G, Lacy J, Tallini G, Crouch J, Schultz M, Murren J: Spontaneous regression of lymphoproliferative disorders in patients treated with methotrexate for rheumatoid arthritis and other rheumatic diseases. J Clin Oncol 1996, 14:1943-1949.
12. Balkwill F: TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev 2006, 25:409-416.
13. Larmonier N, Cathelin D, Larmonier C, Nicolas A, Merino D, Janikashvili N, Audia S, Bateman A, Thompson J, Kottke T, Hartung T, Katsanis E, Vile R, Bonnotte B: The inhibition of TNF-alpha anti-tumoral properties by blocking antibodies promotes tumor growth in a rat model. Exp Cell Res 2007, 313:2345-2355.
14. Bongartz T, Warren FC, Mines D, Matteson EL, Abrams KR, Sutton AJ: Etanercept therapy in rheumatoid arthritis and the risk of malignancies: a systematic review and individual patient data meta-analysis of randomised controlled trials. Ann Rheum Dis 2009, 68:1177-1183.
15. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V: Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA 2006, 295:2275-2285.
16. Lopez-Olivo MA, Tayar JH, Martinez-Lopez JA, Pollono EN, Cueto JP, Gonzales-Crespo MR, Gonzales-Crespo MR, Fulton S, Sauraz-Almazor ME: Risk of malignancies in patients with rheumatoid arthritis treated with biologic therapy: a meta-analysis. JAMA 2012, 308:898-908.
17. Askling J, Fahrbach K, Nordstrom B, Ross S, Schmid CH, Symmons D: Cancer risk with tumor necrosis factor alpha (TNF) inhibitors: meta-analysis of randomized controlled trials of adalimumab, etanercept, and infliximab using patient level data. Pharmacoepidemiol Drug Saf 2011, 20:119-130.
18. Wolfe F, Michaud K: Biologic treatment of rheumatoid arthritis and the risk of malignancy: analyses from a large US observational study. Arthritis Rheum 2007, 56:2886-2895.
19. Askling J, van Vollenhoven RF, Granath F, Raaschou P, Fored CM, Baecklund E, Dackhammar C, Feltelius N, Cöster L, Geborek P, Jacobsson LT, Lindblad S, Rantapää-Dahlqvist S, Saxne T, Klareskog L: Cancer risk in patients with rheumatoid arthritis treated with anti-tumor necrosis factor alpha therapies: does the risk change with the time since start of treatment? Arthritis Rheum 2009, 60:3180-3189.
20. Wu CY, Chen YJ, Ho HJ, Hsu YC, Kuo KN, Wu MS, Lin JT: Association between nucleoside analogues and risk of hepatitis B virus-related hepatocellular carcinoma recurrence following liver resection. JAMA 2012, 308:1906-1914.
21. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, Medsger TA Jr, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988, 31:315-324.
22. National Health Insurance Payment System, National Health Insurance Adminstration, Ministry of Health and Welfare. [ http://www.nhi.gov.tw/ ]
23. Tsan YT, Lee CH, Wang JD, Chen PC: Statins and the risk of hepatocellular carcinoma in patients with hepatitis B virus infection. J Clin Oncol 2012, 30:623-630.
24. Chen HP, Shieh JJ, Chang CC, Chen TT, Lin JT, Wu MS, Wu CY: Metformin decreases hepatocellular carcinoma risk in a dose-dependent manner: population-based and in vitro studies. Gut 2013, 62:606-615.
25. Ruan PK, Gray RJ: Analyses of cumulative incidence functions via non-parametric multiple imputation. Stat Med 2008, 27:5709-5724.
26. Kuk D, Varadhan R: Model selection in competing risks regression. Stat Med 2013, 32:3077-3088.
27. cmprsk: Subdistribution Analysis of Competing Risks. [ http://cran.r-project.org/web/packages/cmprsk/index.html ]
28. Mercer LK, Lunt M, Low ALS, Dixon WG, Watson KD, Symmons DPM, Hyrich KL, BSRBR Control Centre Consortium: Risk of solid cancer in patients exposed to anti-tumor necrosis factor therapy: results from the British Society for Rheumatology Biologics Register for Rheumatoid Arthritis. Ann Rheum Dis 2014, doi: 10.1136/annrheumdis-2013-204851.
29. Lan JL, Shou SJ, Chen DY, Chen YH, Hsieh TY, Young M Jr: A comparative study of etanercept plus methotrexate and methotrexate alone in Taiwanese patients with active rheumatoid arthritis: a 12-week, double-blind, randomized, placebo-controlled study. J Formos Med Assoc 2004, 103:618-623.
30. Chen DY, Chou SJ, Hsieh TY, Chen YH, Chen HH, Hsieh CW, Lan JL: Randomized, double-blind, placebo-controlled, comparative study of human anti-TNF antibody adalimumab in combination with methotrexate and methotrexate alone in Taiwanese patients with active rheumatoid arthritis. J Formos Med Assoc 2009, 108:310-319.
31. Combe B, Codreanu C, Fiocco U, Gaubitz M, Geusens PP, Kvien TK, Pavelka K, Sambrook PN, Smolen JS, Khandker R, Singh A, Wajdula J, Fatenejad S, Etanercept European Investigators Network: Efficacy, safety and patient-reported outcomes of combination etanercept and sulfasalazine versus etanercept alone in patients with rheumatoid arthritis: a double-blind randomized 2-year study. Ann Rheum Dis 2009, 68:1146-1152.
32. Emery P, Breedveld F, van der Heijde D, Ferraccioli G, Dougados M, Robertson D, Pedersen R, Koenig AS, Freundlich B, Combination of Methotrexate and Etanercept in Early Rheumatoid Arthritis Trial Group: Two-year clinical and radiographic results with combination etanercept-methotrexate thearpy versus monotherapy in early rheumatoid arthritis: a two-year, double-blind, randomized study. Arthritis Rheum 2010, 62:674-682.
33. Keystone EC, Kavanaugh AF, Sharp JT, Tannenbaum H, Hua Y, Teoh LS, Fischkoff SA, Chartash EK: Radiographic, clinical, and functional outcomes of treatment with adalimumuab (a human anti-tumor necrosis factor monoclonal antibody) in patients with active rheumatoid arthritis receiving concomitant methotrexate therapy: a randomized, placebo-controlled, 52-week trial. Arthritis Rheum 2004, 50:1400-1411.
34. Breedveld FC, Weisman MH, Kavanaugh AF, Cohen SB, Pavelka K, van Vollenhoven R, Sharp J, Perez JL, Spencer-Green GT: The PREMIER study: a multicenter, randomized, double-blind clinical trial of combination therapy with adalimumab plus methotrexate versus methotrexate alone or adalimumab alone in patients with early, aggressive rheumatoid artritis who had not had previous methotrexate treatment. Arthritis Rheum 2006, 54:26-37.
35. Bejarano V, Quinn M, Conaghan PG, Reece R, Keenan A-M, Walker D, Gough A, Green M, McGonagle D, Adebajo A, Jarrett S, Doherty S, Hordon L, Melsom R, Unnebrink K, Kupper H, Emery P, Yorkshire Early Arthritis Register Consortium: Effect of the early use of the anti-tumor necrosis factor adalimumab on the prevention of job loss in patients with early rheuatmoid arhritis. Arthritis Rheum 2008, 59:1467-1474.
36. Wolfe F, Michaud K: Lymphoma in rheumatoid arthritis: the effect of methotrexate and anti-tumor necrosis factor therapy in 18,572 patients. Arthritis Rheum 2004, 50:1740-1751.
37. Setoguchi S, Solomon DH, Weinblatt ME, Katz JN, Avorn J, Glynn RJ, Cook EF, Carney G, Schneeweiss S: Tumor necrosis factor alpha antagonist use and cancer in patients with rheumatoid arthritis. Arthritis Rheum 2006, 54:2757-2764.
38. 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 2002, 46:3151-3158.
39. Burmester GR, Panaccione R, Gordon KB, Mcllraith MJ, Lacerda AP: Adalimumab: long-term safety in 23 458 patients from global clinical trials in rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, psoriatic arthritis, psoriasis and Crohn's disease. Ann Rheum Dis 2013, 72:517-524.
40. Theophile H, Schaeverbeke T, Miremont-Salame G, Abouelfath A, Kahn V, Haramburu F, Bégaud B: Sources of information on lymphoma associated with anti-tumour necrosis factor agents: comparison of published case reports and cases reported to the French pharmacovigilance system. Drug Saf 2011, 34:577-585.
41. Grivennikov SI, Greten FR, Karin M: Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
42. Chou CT, Pei L, Chang DM, Lee CF, Schumacher HR, Liang MH: Prevalence of rheumatoid diseases in Taiwan: a population study of urban, suburban and rural differences. J Rheumatol 1994, 21:302-306.
43. Beasley RP, Bennett PH, Lin CC: Low prevalence of rheumatoid arthritis in Chinese. Prevalence survey in a rural community. J Rheumatol Suppl 1983, 10:11-15.
44. Shickikawa K, Inoue K, Hirota S, Maeda A, Ota H, Kimura M: Changes in the incidence and prevalence of rheumatoid arthritis in Kamitonda, Kawayama, Japan, 1965-1996. Ann Rheum Dis 1999, 58:751-756.
45. Kim YJ, Shim JS, Choi CB, Bae SC: Mortality and incidence of malignancy in Korean patients with rheumatoid arthritis. J Rheumatol 2012, 39:226-232.
46. Chen YJ, Chang YT, Shen JL, Chen TT, Wang CB, Chen CM, Wu CY: Association between systemic antipsoriatic drugs and cardiovascular risk in patients with psoriasis with or without psoriatic arthritis: a nationwide cohort study. Arthritis Rheum 2012, 64:1879-1887.
47. Mariette X, Matucci-Cerinic M, Pavelka K, Taylor P, van Vollenhoven R, Heatley R, Walsh C, Lawson R, Reynolds A, Emery P: Malignancies associated with tumor necrosis factor inhibitors in registries and prospective observational studies: a systemic reiew and meta-analysis. Ann Rheum Dis 2011, 70:1895-1904.
48. De Giorgi V, Gandini S, Grazzini M, Benemei S, Marchionni N, Geppetti P: Effect of β-blockers and other antihypertensive drugs on the risk of melanoma recurrence and death. Mayo Clin Proc 2013, 88:1196-1203.
49. Sørensen GV, Ganz PA, Cole SW, Pedersen LA, Sørensen HT, Cronin-Fenton DP, Garne JP, Christiansen PM, Lash TL, Ahern TP: Use of β-blockers, angiotensin-converting enzyme inhibitors, angiotensin II receptor blockers, and risk of breast cancer recurrence: a Danish nationwide prospective cohort study. J Clin Oncol 2013, 31:2265-2272.
50. Ji Y, Chen S, Xiao X, Zheng S, Li K: β-blockers: a novel class of antitumor agents. Onco Targets Ther 2012, 5:391-401.