Risk of tuberculosis in patients treated with TNF-α antagonists: A systematic review and meta-analysis of randomised controlled trials

BMJ Open

Volumn 7, Issue 3, 2017, Pages

  Zhang, Zheng ^a   Fan, Wei ^a   Yang, Gui ^a   Xu, Zhigao ^a   Wang, June ^a   Cheng, Qingyuan ^a   Yu, Mingxia ^a  

^a ZHONGNAN HOSPITAL OF WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; CERTOLIZUMAB PEGOL; ETANERCEPT; GOLIMUMAB; INFLIXIMAB; TUMOR NECROSIS FACTOR INHIBITOR; ANTIRHEUMATIC AGENT; RITUXIMAB; TUMOR NECROSIS FACTOR;

DISEASE ASSOCIATION; HUMAN; INFECTION RISK; META ANALYSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RHEUMATOID ARTHRITIS; RISK ASSESSMENT; SYSTEMATIC REVIEW; TUBERCULOSIS; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; RISK; STATISTICS AND NUMERICAL DATA;

ADALIMUMAB; ANTIRHEUMATIC AGENTS; CERTOLIZUMAB PEGOL; ETANERCEPT; HUMANS; INFLIXIMAB; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK; RITUXIMAB; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85016291407     PISSN: None     EISSN: 20446055     Source Type: Journal    
DOI: 10.1136/bmjopen-2016-012567     Document Type: Review

References (55)

1. Bradley JR. TNF-mediated inflammatory disease. J Pathol 2008;214:149-60.
2. Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 2001;344:907-16.
3. Baraliakos X, Listing J, Fritz C, et al. Persistent clinical efficacy and safety of infliximab in ankylosing spondylitis after 8 years-early clinical response predicts long-term outcome. Rheumatology (Oxford) 2011;50:1690-9.
4. Perrier C, Rutgeerts P. Cytokine blockade in inflammatory bowel diseases. Immunotherapy 2011;3:1341-52.
5. Bansback N, Sizto S, Sun H, et al. Efficacy of systemic treatments for moderate to severe plaque psoriasis: systematic review and meta-analysis. Dermatology (Basel) 2009;219:209-18.
6. Sánchez-Moya AI, García-Doval I, Carretero G, et al. Latent tuberculosis infection and active tuberculosis in patients with psoriasis: a study on the incidence of tuberculosis and the prevalence of latent tuberculosis disease in patients with moderate-severe psoriasis in Spain. BIOBADADERM registry. J Eur Acad Dermatol Venereol 2013;27:1366-74.
7. Yu M, Zhou X, Niu L, et al. Targeting transmembrane TNF-alpha suppresses breast cancer growth. Cancer Res 2013;73:4061-74.
8. Solovic I, Sester M, Gomez-Reino JJ, et al. The risk of tuberculosis related to tumour necrosis factor antagonist therapies: a TBNET consensus statement. Eur Respir J2010;36:1185-206.
9. Raval A, Akhavan-Toyserkani G, Brinker A, et al. Brief communication: characteristics of spontaneous cases of tuberculosis associated with infliximab. Ann Intern Med 2007;147:699-702.
10. Ai JW, Zhang S, Ruan QL, et al. The risk of tuberculosis in patients with rheumatoid arthritis treated with tumor necrosis factor-alpha antagonist: a meta-analysis of both randomized controlled trials and registry/cohort studies. J Rheumatol2015;42:2229-37.
11. Souto A, Maneiro JR, Salgado E, et al. Risk of tuberculosis in patients with chronic immune-mediated inflammatory diseases treated with biologics and tofacitinib: a systematic review and meta-analysis of randomized controlled trials and long-term extension studies. Rheumatology (Oxford) 2014;53:1872-85.
12. Xie X, Chen J, Peng Y, et al. [Meta-analysis of infection risks of anti-TNF-alpha treatment in rheumatoid arthritis]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2013;38:722-36.
13. Singh JA, Wells GA, Christensen R, et al. Adverse effects of biologics: a network meta-analysis and Cochrane overview. Cochrane Database Syst Rev2011;(2):Cd008794.
14. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009;339:b2535.
15. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336:924-6.
16. Kim H-Y, Lee S-K, Song YW, et al. A randomized, double-blind, placebo-controlled, phase III study of the human anti-tumor necrosis factor antibody adalimumab administered as subcutaneous injections in Korean rheumatoid arthritis patients treated with methotrexate. APLAR J Rheumatol 2007;10:9-16.
17. Rutgeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 2005;353:2462-76.
18. Baranauskaite A, Raffayová H, Kungurov NV, et al. Infliximab plus methotrexate is superior to methotrexate alone in the treatment of psoriatic arthritis in methotrexate-naive patients: the RESPOND study. Ann Rheum Dis 2012;71:541-8.
19. Barker J, Hoffmann M, Wozel G, et al. Efficacy and safety of infliximab vs. methotrexate in patients with moderate-to-severe plaque psoriasis: results of an open-label, active-controlled, randomized trial (RESTORE1). Br J Dermatol 2011;165:1109-17.
20. Braun J, Brandt J, Listing J, et al. Treatment of active ankylosing spondylitis with infliximab: a randomised controlled multicentre trial. Lancet 2002;359:1187-93.
21. Breedveld FC, Weisman MH, Kavanaugh AF, et al. 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 arthritis who had not had previous methotrexate treatment. Arthritis Rheum 2006;54:26-37.
22. Chen DY, Chou SJ, Hsieh TY, et al. 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;108:310-19.
23. Colombel JF, Sandborn WJ, Reinisch W, et al. Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 2010;362:1383-95.
24. Couriel DR, Saliba R, de Lima M, et al. A phase III study of infliximab and corticosteroids for the initial treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant 2009;15:1555-62.
25. Judson MA, Baughman RP, Costabel U, et al. Safety and efficacy of ustekinumab or golimumab in patients with chronic sarcoidosis. Eur Respir J 2014;44:1296-307.
26. Kavanaugh A, Fleischmann RM, Emery P, et al. Clinical, functional and radiographic consequences of achieving stable low disease activity and remission with adalimumab plus methotrexate or methotrexate alone in early rheumatoid arthritis: 26-week results from the randomised, controlled OPTIMA study. Ann Rheum Dis 2013;72:64-71.
27. Kennedy WP, Simon JA, Offutt C, et al. Efficacy and safety of pateclizumab (anti-lymphotoxin-alpha) compared to adalimumab in rheumatoid arthritis: a head-to-head phase 2 randomized controlled study (The ALTARA Study). Arthritis Res Ther 2014; 16:467.
28. Keystone EC, Kavanaugh AF, Sharp JT, et al. Radiographic, clinical, and functional outcomes of treatment with adalimumab (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;50:1400-11.
29. Keystone E, Heijde Dv, Mason D, Jr, et al. Certolizumab pegol plus methotrexate is significantly more effective than placebo plus methotrexate in active rheumatoid arthritis: findings of a fifty-two-week, phase III, multicenter, randomized, double-blind, placebo-controlled, parallel-group study. Arthritis Rheum 2008;58:3319-29.
30. Maini R, St Clair EW, Breedveld F, et al. Infliximab (chimeric anti-tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial. ATTRACT Study Group. Lancet 1999;354:1932-9.
31. Nam JL, Villeneuve E, Hensor EM, et al. Remission induction comparing infliximab and high-dose intravenous steroid, followed by treat-to-target: a double-blind, randomised, controlled trial in new-onset, treatment-naive, rheumatoid arthritis (the IDEA study). Ann Rheum Dis 2014;73:75-85.
32. Reich K, Ortonne JP, Gottlieb AB, et al. Successful treatment of moderate to severe plaque psoriasis with the PEGylated Fab' certolizumab pegol: results of a phase II randomized, placebo-controlled trial with a re-treatment extension. Br J Dermatol 2012;167:180-90.
33. Schiff M, Weinblatt ME, Valente R, et al. Head-to-head comparison of subcutaneous abatacept versus adalimumab for rheumatoid arthritis: two-year efficacy and safety findings from AMPLE trial. Ann Rheum Dis 2014;73:86-94.
34. Schiff M, Keiserman M, Codding C, et al. Efficacy and safety of abatacept or infliximab vs placebo in ATTEST: a phase III, multi-centre, randomised, double-blind, placebo-controlled study in patients with rheumatoid arthritis and an inadequate response to methotrexate. Ann Rheum Dis 2008;67:1096-103.
35. Sieper J, Lenaerts J, Wollenhaupt J, et al. Efficacy and safety of infliximab plus naproxen versus naproxen alone in patients with early, active axial spondyloarthritis: results from the double-blind, placebo-controlled INFAST study, Part 1. Ann Rheum Dis 2014;73:101-7.
36. Smolen J, Landewé RB, Mease P, et al. Efficacy and safety of certolizumab pegol plus methotrexate in active rheumatoid arthritis: the RAPID 2 study. A randomised controlled trial. Ann Rheum Dis 2009;68:797-804.
37. St Clair EW, van der Heijde DM, Smolen JS, et al. Combination of infliximab and methotrexate therapy for early rheumatoid arthritis: a randomized, controlled trial. Arthritis Rheum 2004;50:3432-43.
38. Suzuki Y, Motoya S, Hanai H, et al. Efficacy and safety of adalimumab in Japanese patients with moderately to severely active ulcerative colitis. J Gastroenterol 2014;49:283-94.
39. Tam LS, Shang Q, Li EK, et al. Infliximab is associated with improvement in arterial stiffness in patients with early rheumatoid arthritis-a randomized trial. J Rheumatol 2012;39:2267-75.
40. Van Den Bosch F, Kruithof E, Baeten D, et al. Randomized double-blind comparison of chimeric monoclonal antibody to tumor necrosis factor alpha (infliximab) versus placebo in active spondylarthropathy. Arthritis Rheum 2002;46:755-65.
41. van der Heijde D, Klareskog L, Landewé R, et al. Disease remission and sustained halting of radiographic progression′ with combination etanercept and methotrexate in patients with rheumatoid arthritis. Arthritis Rheum 2007;56:3928-39.
42. van Vollenhoven RF, Kinnman N, Vincent E, et al. Atacicept in patients with rheumatoid arthritis and an inadequate response to methotrexate: results of a phase II, randomized, placebo-controlled trial. Arthritis Rheum 2011;63:1782-92.
43. Wenzel SE, Barnes PJ, Bleecker ER, et al. A randomized, double-blind, placebo-controlled study of tumor necrosis factor-alpha blockade in severe persistent asthma. Am J Respir Crit Care Med 2009;179:549-58.
44. Westhovens R, Yocum D, Han J, et al. The safety of infliximab, combined with background treatments, among patients with rheumatoid arthritis and various comorbidities: a large, randomized, placebo-controlled trial. Arthritis Rheum 2006;54:1075-86.
45. Carmona L, Hernández-García C, Vadillo C, et al. Increased risk of tuberculosis in patients with rheumatoid arthritis. J Rheumatol 2003;30:1436-9.
46. Doran MF, Crowson CS, Pond GR, et al. Frequency of infection in patients with rheumatoid arthritis compared with controls: a population-based study. Arthritis Rheum 2002;46:2287-93.
47. Arkema EV, Jonsson J, Baecklund E, et al. Are patients with rheumatoid arthritis still at an increased risk of tuberculosis and what is the role of biological treatments? Ann Rheum Dis 2015;74:1212-17.
48. Bekker LG, Freeman S, Murray PJ, et al. TNFα controls intracellular mycobacterial growth by both inducible nitric oxide synthase-dependent and inducible nitric oxide synthase-independent pathways. J Immunol 2001;166:6728-34.
49. Kindler V, Sappino AP, Grau GE, et al. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell 1989;56:731-40.
50. Murdaca G, Spanò F, Contatore M, et al. Infection risk associated with anti-TNF-alpha agents: a review. Expert Opin Drug Saf 2015;14:571-82.
51. Danielsen AV, Fløe A, Lillebaek T, et al. An interferon-gamma release assay test performs well in routine screening for tuberculosis. Dan Med J 2014;61:A4856.
52. Carmona L, Gómez-Reino JJ, Rodríguez-Valverde V, et al. Effectiveness of recommendations to prevent reactivation of latent tuberculosis infection in patients treated with tumor necrosis factor antagonists. Arthritis Rheum 2005;52:1766-72.
53. Yun JW, Lim SY, Suh GY, et al. Diagnosis and treatment of latent tuberculosis infection in arthritis patients treated with tumor necrosis factor antagonists in Korea. J Korean Med Sci 2007;22:779-83.
54. Hauck FR, Neese BH, Panchal AS, et al. Identification and management of latent tuberculosis infection. Am Fam Physician 2009;79:879-86.
55. Lorenzetti R, Zullo A, Ridola L, et al. Higher risk of tuberculosis reactivation when anti-TNF is combined with immunosuppressive agents: a systematic review of randomized controlled trials. Ann Med 2014;46:547-54.