Risk of herpes zoster in individuals on biologics, disease-modifying antirheumatic drugs, and/or corticosteroids for autoimmune diseases: A systematic review and meta-analysis

Open Forum Infectious Diseases

Volumn 3, Issue 4, 2016, Pages

  Marra, Fawziah ^a   Lo, Elaine ^b,c   Kalashnikov, Viktor ^a   Richardson, Kathryn ^d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Biologics; DMARDs; Herpes zoster; Immunocompromised; Rheumatoid arthritis

Indexed keywords

ABETIMUS; ALEFACEPT; ANAKINRA; ANTIRHEUMATIC AGENT; BIOLOGICAL PRODUCT; CORTICOSTEROID; CYCLOSPORINE; EFALIZUMAB; GOLIMUMAB; HYDROXYCHLOROQUINE; PLACEBO; SALAZOSULFAPYRIDINE; SIFALIMUMAB; TOCILIZUMAB; TOFACITINIB; TUMOR NECROSIS FACTOR; USTEKINUMAB;

ANKYLOSING SPONDYLITIS; ARTICLE; AUTOIMMUNE DISEASE; CONFIDENCE INTERVAL; DATA EXTRACTION; HERPES ZOSTER; HOSPITALIZATION; HUMAN; INFLAMMATORY BOWEL DISEASE; MANTEL HAENSZEL TEST; META ANALYSIS; PRIORITY JOURNAL; PSORIASIS; PSORIATIC ARTHRITIS; QUALITY CONTROL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RHEUMATOID ARTHRITIS; SYSTEMATIC REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; ULCERATIVE COLITIS;

EID: 85045073843     PISSN: None     EISSN: 23288957     Source Type: Journal    
DOI: 10.1093/ofid/ofw205     Document Type: Article

References (95)

1. Cohen JI. Clinical practice: herpes zoster. N Engl J Med 2013; 369:255-63.
2. Sampathkumar P, Drage LA, Martin DP. Herpes zoster (shingles) and postherpetic neuralgia. Mayo Clin Proc 2009; 84:274-80.
3. Kost RG, Straus SE. Postherpetic neuralgia-pathogenesis, treatment, and prevention. N Engl J Med 1996; 335:32-42.
4. Yawn BP, Gilden D. The global epidemiology of herpes zoster. Neurology 2013; 81:928-30.
5. Kawai K, Gebremeskel BG, Acosta CJ. Systematic review of incidence and complications of herpes zoster: towards a global perspective. BMJ Open 2014; 4:e004833.
6. Yawn BP, Itzler RF, Wollan PC, et al. Health care utilization and cost burden of herpes zoster in a community population. Mayo Clin Proc 2009; 84:787-94.
7. Hayward AR, Herberger M. Lymphocyte responses to varicella zoster virus in the elderly. J Clin Immunol 1987; 7:174-8.
8. Bongartz T, Sutton AJ, Sweeting MJ, et al. 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; 295:2275-85.
9. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009; 339:b2535.
10. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 2000; 283:2008-12.
11. Zorzela L, Golder S, Liu Y, et al. Quality of reporting in systematic reviews of adverse events: systematic review. BMJ 2014; 348:f7668.
12. Dechartres A, Trinquart L, Boutron I, Ravaud P. Influence of trial sample size on treatment effect estimates: meta-epidemiological study. BMJ 2013; 346:f2304.
13. Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane collaboration's tool for assessing risk of bias in randomised trials. BMJ 2011; 343:d5928.
14. Wells GA, Shea B, O'Connell D, et al. (2011) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analysis. Available at: www.ohri.ca/programs/clinical-epidemiology/oxford.asp. Accessed 24 October 2016.
15. Sweeting MJ, Sutton AJ, Lambert PC. What to add to nothing? Use and avoidance of continuity corrections in meta-analysis of sparse data. Stat Med 2004; 23:1351-75.
16. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327:557-60.
17. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629-34.
18. Spittal MJ, Pirkis J, Gurrin LC. Meta-analysis of incidence rate data in the presence of zero events. BMC Med Res Methodol 2015; 15:42.
19. Peto R, Pike MC, Armitage P, et al. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. Analysis and examples. Br J Cancer 1977; 35:1-39.
20. Alarcon-Segovia D, Tumlin JA, Furie RA, et al. LJP 394 for the prevention of renal flare in patients with systemic lupus erythematosus: results from a randomized, double-blind, placebo-controlled study. Arthritis Rheum 2003; 48:442-54.
21. Bachelez H, van de Kerkhof PC, Strohal R, et al. Tofacitinib versus etanercept or placebo in moderate-to-severe chronic plaque psoriasis: a phase 3 randomised non-inferiority trial. Lancet Lond Engl 2015; 386:552-61.
22. Bejarano V, Quinn M, Conaghan PG, et al. Effect of the early use of the anti-tumor necrosis factor adalimumab on the prevention of job loss in patients with early rheumatoid arthritis. Arthritis Rheum 2008; 59:1467-74.
23. Braun J, van der Horst-Bruinsma IE, Huang F, et al. Clinical efficacy and safety of etanercept versus sulfasalazine in patients with ankylosing spondylitis: a randomized, double-blind trial. Arthritis Rheum 2011; 63:1543-51.
24. Bresnihan B, Alvaro-Gracia JM, Cobby M, et al. Treatment of rheumatoid arthritis with recombinant human interleukin-1 receptor antagonist. Arthritis Rheum 1998; 41:2196-204.
25. Cardiel MH, Tumlin JA, Furie RA, et al. Abetimus sodium for renal flare in systemic lupus erythematosus: results of a randomized, controlled phase III trial. Arthritis Rheum 2008; 58:2470-80.
26. Chen XX, Dai Q, Huang AB, et al. A multicenter, randomized, double-blind clinical trial of combination therapy with Anbainuo, a novel recombinant human TNFRII:Fc fusion protein, plus methotrexate versus methotrexate alone or Anbainuo alone in Chinese patients with moderate to severe rheumatoid arthritis. Clin Rheumatol 2013; 32:99-108.
27. Emery P, Breedveld FC, Hall S, et al. Comparison of methotrexate monotherapy with a combination of methotrexate and etanercept in active, early, moderate to severe rheumatoid arthritis (COMET): a randomised, double-blind, parallel treatment trial. Lancet 2008; 372:375-82.
28. Emery P, Burmester GR, Bykerk VP, et al. Evaluating drug-free remission with abatacept in early rheumatoid arthritis: results from the phase 3b, multicentre, randomised, active-controlled AVERT study of 24 months, with a 12-month, double-blind treatment period. Ann Rheum Dis 2015; 74:19-26.
29. Fleischmann R, Cutolo M, Genovese MC, et al. Phase IIb dose-ranging study of the oral JAK inhibitor tofacitinib (CP-690,550) or adalimumab monotherapy versus placebo in patients with active rheumatoid arthritis with an inadequate response to disease-modifying antirheumatic drugs. Arthritis Rheum 2012; 64:617-29.
30. Fleischmann RM, Halland AM, Brzosko M, et al. Tocilizumab inhibits structural joint damage and improves physical function in patients with rheumatoid arthritis and inadequate responses to methotrexate: LITHE study 2-year results. J Rheumatol 2013; 40:113-26.
31. Furie R, Nicholls K, Cheng TT, et al. Efficacy and safety of abatacept in lupus nephritis: a twelve-month, randomized, double-blind study. Arthritis Rheumatol 2014; 66:379-89.
32. Furst DE, Schiff MH, Fleischmann RM, et al. Adalimumab, a fully human anti tumor necrosis factor-alpha monoclonal antibody, and concomitant standard antirheumatic therapy for the treatment of rheumatoid arthritis: results of STAR (Safety Trial of Adalimumab in Rheumatoid Arthritis). J Rheumatol 2003; 30:2563-71.
33. Genovese MC, McKay JD, Nasonov EL, et al. Interleukin-6 receptor inhibition with tocilizumab reduces disease activity in rheumatoid arthritis with inadequate response to disease-modifying antirheumatic drugs: the tocilizumab in combination with traditional disease-modifying antirheumatic drug therapy study. Arthritis Rheum 2008; 58:2968-80.
34. Kameda H, Kanbe K, Sato E, et al. Continuation of methotrexate resulted in better clinical and radiographic outcomes than discontinuation upon starting etanercept in patients with rheumatoid arthritis: 52-week results from the JESMR study. J Rheumatol 2011; 38:1585-92.
35. 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.
36. Kremer JM, Bloom BJ, Breedveld FC, et al. The safety and efficacy of a JAK inhibitor in patients with active rheumatoid arthritis: Results of a double-blind, placebo-controlled phase IIa trial of three dosage levels of CP-690,550 versus placebo. Arthritis Rheum 2009; 60:1895-905.
37. Kremer J, Ritchlin C, Mendelsohn A, et al. Golimumab, a new human anti-tumor necrosis factor alpha antibody, administered intravenously in patients with active rheumatoid arthritis: forty-eight-week efficacy and safety results of a phase III randomized, double-blind, placebo-controlled study. Arthritis Rheum 2010; 62:917-28.
38. Kremer JM, Cohen S, Wilkinson BE, et al. A phase IIb dose-ranging study of the oral JAK inhibitor tofacitinib (CP-690,550) versus placebo in combination with background methotrexate in patients with active rheumatoid arthritis and an inadequate response to methotrexate alone. Arthritis Rheum 2012; 64:970-81.
39. Kremer J, Li ZG, Hall S, et al. Tofacitinib in combination with nonbiologic disease-modifying antirheumatic drugs in patients with active rheumatoid arthritis: a randomized trial. Ann Intern Med 2013; 159:253-61.
40. Leonardi CL, Kimball AB, Papp KA, et al. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet 2008; 371:1665-74.
41. Merrill JT, Wallace DJ, Petri M, et al. Safety profile and clinical activity of sifalimumab, a fully human anti-interferon α monoclonal antibody, in systemic lupus erythematosus: a phase I, multicentre, double-blind randomised study. Ann Rheum Dis 2011; 70:1905-13.
42. Moutsopoulos HM, Gallagher JD, Decker JL, Steinberg AD. Herpes zoster in patients with systemic lupus erythematosus. Arthritis Rheum 1978; 21:798-802.
43. Nishimoto N, Hashimoto J, Miyasaka N, et al. Study of active controlled monotherapy used for rheumatoid arthritis, an IL-6 inhibitor (SAMURAI): evidence of clinical and radiographic benefit from an x ray reader-blinded randomised controlled trial of tocilizumab. Ann Rheum Dis 2007; 66:1162-7.
44. Papp KA, Menter MA, Abe M, et al. Tofacitinib, an oral Janus kinase inhibitor, for the treatment of chronic plaque psoriasis: results from two randomized, placebo-controlled, phase III trials. Br J Dermatol 2015; 173:949-61.
45. 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.
46. Sandborn WJ, Colombel JF, Enns R, et al. Natalizumab induction and maintenance therapy for Crohn's disease. N Engl J Med 2005; 353:1912-25.
47. Sandborn WJ, Rutgeerts P, Feagan BG, et al. Colectomy rate comparison after treatment of ulcerative colitis with placebo or infliximab. Gastroenterology 2009; 137:1250-60; quiz 1520.
48. 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.
49. Schreiber S, Rutgeerts P, Fedorak RN, et al. A randomized, placebo-controlled trial of certolizumab pegol (CDP870) for treatment of Crohn's disease. Gastroenterology 2005; 129:807-18.
50. Smolen JS, Kay J, Doyle MK, et al. Golimumab in patients with active rheumatoid arthritis after treatment with tumour necrosis factor alpha inhibitors (GO-AFTER study): a multicentre, randomised, double-blind, placebo-controlled, phase III trial. Lancet 2009; 374:210-21.
51. Smolen JS, Nash P, Durez P, et al. Maintenance, reduction, or withdrawal of etanercept after treatment with etanercept and methotrexate in patients with moderate rheumatoid arthritis (PRESERVE): a randomised controlled trial. Lancet 2013; 381:918-29.
52. Takeuchi T, Harigai M, Tanaka Y, et al. Golimumab monotherapy in Japanese patients with active rheumatoid arthritis despite prior treatment with disease-modifying antirheumatic drugs: results of the phase 2/3, multicentre, randomised, double-blind, placebo-controlled GO-MONO study through 24 weeks. Ann Rheum Dis 2013; 72:1488-95.
53. Tanaka Y, Harigai M, Takeuchi T, et al. Golimumab in combination with methotrexate in Japanese patients with active rheumatoid arthritis: results of the GO-FORTH study. Ann Rheum Dis 2012; 71:817-24.
54. Tanaka Y, Takeuchi T, Yamanaka H, et al. Efficacy and safety of tofacitinib as monotherapy in Japanese patients with active rheumatoid arthritis: a 12-week, randomized, phase 2 study. Mod Rheumatol 2015; 25:514-21.
55. van der Heijde D, Tanaka Y, Fleischmann R, et al. Tofacitinib (CP-690,550) in patients with rheumatoid arthritis receiving methotrexate: twelve-month data from a twenty-four-month phase III randomized radiographic study. Arthritis Rheum 2013; 65:559-70.
56. van Vollenhoven RF, Fleischmann R, Cohen S, et al. Tofacitinib or adalimumab versus placebo in rheumatoid arthritis. N Engl J Med 2012; 367:508-19.
57. Yamamoto K, Takeuchi T, Yamanaka H, et al. Efficacy and safety of certolizumab pegol without methotrexate co-administration in Japanese patients with active rheumatoid arthritis: the HIKARI randomized, placebo-controlled trial. Mod Rheumatol 2014; 24:552-60.
58. Dreiher J, Kresch FS, Comaneshter D, Cohen AD. Risk of herpes zoster in patients with psoriasis treated with biologic drugs. J Eur Acad Dermatol Venereol 2012; 26:1127-32.
59. Galloway JB, Mercer LK, Moseley A, et al. Risk of skin and soft tissue infections (including shingles) in patients exposed to anti-tumour necrosis factor therapy: results from the British Society for Rheumatology Biologics Register. Ann Rheum Dis 2013; 72:229-34.
60. McDonald JR, Zeringue AL, Caplan L, et al. Herpes zoster risk factors in a national cohort of veterans with rheumatoid arthritis. Clin Infect Dis 2009; 48:1364-71.
61. Nakajima A, Urano W, Inoue E, et al. Incidence of herpes zoster in Japanese patients with rheumatoid arthritis from 2005 to 2010. Mod Rheumatol Jpn Rheum Assoc 2015; 25:558-61.
62. Pappas DA, Hooper MM, Kremer JM, et al. Herpes zoster reactivation in patients with rheumatoid arthritis: analysis of disease characteristics and disease-modifying antirheumatic drugs. Arthritis Care Res (Hoboken) 2015; 67:1671-8.
63. Osterman MT, Haynes K, Delzell E, et al. Effectiveness and safety of immunomodulators with anti-tumor necrosis factor therapy in Crohn's disease. Clin Gastroenterol Hepatol 2015; 13:1293-301.e5; quiz e70, e72.
64. Segan J, Staples MP, March L, et al. Risk factors for herpes zoster in rheumatoid arthritis patients: the role of tumour necrosis factor-α inhibitors. Intern Med J 2015; 45:310-8.
65. Shah M, Chaudhari S, McLaughlin TP, et al. Cumulative burden of oral corticosteroid adverse effects and the economic implications of corticosteroid use in patients with systemic lupus erythematosus. Clin Ther 2013; 35:486-97.
66. Strangfeld A, Listing J, Herzer P, et al. Risk of herpes zoster in patients with rheumatoid arthritis treated with anti-TNF-alpha agents. JAMA 2009; 301:737-44.
67. Veetil BM, Myasoedova E, Matteson EL, et al. Incidence and time trends of herpes zoster in rheumatoid arthritis: a population-based cohort study. Arthritis Care Res (Hoboken) 2013; 65:854-61.
68. Winthrop KL, Baddley JW, Chen L, et al. Association between the initiation of antitumor necrosis factor therapy and the risk of herpes zoster. JAMA 2013; 309:887-95.
69. Wolfe F, Michaud K, Chakravarty EF. Rates and predictors of herpes zoster in patients with rheumatoid arthritis and non-inflammatory musculoskeletal disorders. Rheumatology (Oxford) 2006; 45:1370-5.
70. Yun H, Xie F, Delzell E, et al. Risks of herpes zoster in patients with rheumatoid arthritis according to biologic disease-modifying therapy. Arthritis Care Res (Hoboken) 2015; 67:731-6.
71. Zhang J, Xie F, Delzell E, et al. Association between vaccination for herpes zoster and risk of herpes zoster infection among older patients with selected immune-mediated diseases. JAMA 2012; 308:43-9.
72. Zisman D, Bitterman H, Shalom G, et al. Psoriatic arthritis treatment and the risk of herpes zoster. Ann Rheum Dis 2016; 75:131-5.
73. Gupta G, Lautenbach E, Lewis JD. Incidence and risk factors for herpes zoster among patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2006; 4:1483-90.
74. Long MD, Martin C, Sandler RS, Kappelman MD. Increased risk of herpes zoster among 108 604 patients with inflammatory bowel disease. Aliment Pharmacol Ther 2013; 37:420-9.
75. Smitten AL, Choi HK, Hochberg MC, et al. The risk of herpes zoster in patients with rheumatoid arthritis in the United States and the United Kingdom. Arthritis Rheum 2007; 57:1431-8.
76. Kourbeti IS, Ziakas PD, Mylonakis E. Biologic therapies in rheumatoid arthritis and the risk of opportunistic infections: a meta-analysis. Clin Infect Dis 2014; 58:1649-57.
77. Che H, Lukas C, Morel J, Combe B. Risk of herpes/herpes zoster during anti-tumor necrosis factor therapy in patients with rheumatoid arthritis. Systematic review and meta-analysis. Joint Bone Spine 2014; 81:215-21.
78. Singh JA, Cameron C, Noorbaloochi S, et al. Risk of serious infection in biological treatment of patients with rheumatoid arthritis: a systematic review and meta-analysis. Lancet Lond Engl 2015; 386:258-65.
79. Winthrop KL, Novosad SA, Baddley JW, et al. Opportunistic infections and biologic therapies in immune-mediated inflammatory diseases: consensus recommendations for infection reporting during clinical trials and postmarketing surveillance. Ann Rheum Dis 2015; 74:2107-16.
80. Dixon WG. Rheumatoid arthritis: biological drugs and risk of infection. Lancet 2015; 386:224-5.
81. Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 2001; 344:907-16.
82. Brenner D, Blaser H, Mak TW. Regulation of tumour necrosis factor signalling: live or let die. Nat Rev Immunol 2015; 15:362-74.
83. Moreland L, Bate G, Kirkpatrick P. Abatacept. Nat Rev Drug Discov 2006; 5:185-6.
84. Weiner GJ. Rituximab: mechanism of action. Semin Hematol 2010; 47:115-23.
85. Winthrop KL, Park SH, Gul A, et al. Tuberculosis and other opportunistic infections in tofacitinib-treated patients with rheumatoid arthritis. Ann Rheum Dis 2016; 75:1133-8.
86. Genovese MC, Kremer J, Zamani O, et al. Baricitinib in patients with refractory rheumatoid arthritis. N Engl J Med 2016; 374:1243-52.
87. Gupta V, Harrison C, Hexner EO, et al. The impact of anemia on overall survival in patients with myelofibrosis treated with ruxolitinib in the COMFORT studies. Haematologica. doi: 10.3324/haematol.2016.151449.
88. Cutolo M, Seriolo B, Pizzorni C, et al. Use of glucocorticoids and risk of infections. Autoimmun Rev 2008; 8:153-5.
89. Dixon WG, Suissa S, Hudson M. The association between systemic glucocorticoid therapy and the risk of infection in patients with rheumatoid arthritis: systematic review and meta-analyses. Arthritis Res Ther 2011; 13:R139.
90. Hoes JN, Jacobs JW, Boers M, et al. EULAR evidence-based recommendations on the management of systemic glucocorticoid therapy in rheumatic diseases. Ann Rheum Dis 2007; 66:1560-7.
91. Youssef J, Novosad SA, Winthrop KL. Infection risk and safety of corticosteroid use. Rheum Dis Clin North Am 2016; 42:157-76, ix-x.
92. Oxman MN, Levin MJ, Johnson GR, et al. A vaccine to prevent herpes zoster and postherpetic neuralgia in older adults. N Engl J Med 2005; 352:2271-84.
93. Lal H, Cunningham AL, Godeaux O, et al. Efficacy of an adjuvanted herpes zoster subunit vaccine in older adults. N Engl J Med 2015; 372:2087-96.
94. Harpaz R, Ortega-Sanchez IR, Seward JF; Advisory Committee on Immunization Practices (ACIP) Centers for Disease Control and Prevention (CDC). Prevention of herpes zoster: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2008; 57:1-30; quiz CE2-4.
95. Oxman MN, Schmader KE. Editorial commentary: zoster vaccine in immunocompromised patients: time to reconsider current recommendations. Clin Infect Dis 2014; 59:920-2.