TNF blockers show distinct patterns of immune response to the pandemic influenza A H1N1 vaccine in inflammatory arthritis patients

Ivan Leonardo Avelino França, Ana Cristina Medeiros Ribeiro, Nádia Emi Aikawa, Carla Gonçalves Schain Saad, Julio Cesar Bertacine Moraes, Cláudia Goldstein-Schainberg, Ieda Maria Magalhães Laurindo, Alexander Roberto Precioso, Maria Akiko Ishida, Ana Marli Christovam Sartori, Clovis Artur Silva, Eloisa Bonfa, Ivan Leonardo Avelino França, Ana Cristina Medeiros Ribeiro, Nádia Emi Aikawa, Carla Gonçalves Schain Saad, Julio Cesar Bertacine Moraes, Cláudia Goldstein-Schainberg, Ieda Maria Magalhães Laurindo, Alexander Roberto Precioso, Maria Akiko Ishida, Ana Marli Christovam Sartori, Clovis Artur Silva, Eloisa Bonfa

Abstract

Objective: To evaluate the immunogenicity of the anti-influenza A H1N1/2009 vaccine in RA and spondyloarthritis (SpA) patients receiving distinct classes of anti-TNF agents compared with patients receiving DMARDs and healthy controls.

Methods: One hundred and twenty patients (RA, n = 41; AS, n = 57; PsA, n = 22) on anti-TNF agents (monoclonal, n = 94; soluble receptor, n = 26) were compared with 116 inflammatory arthritis patients under DMARDs and 117 healthy controls. Seroprotection, seroconversion (SC), geometric mean titre, factor increase in geometric mean titre and adverse events were evaluated 21 days after vaccination.

Results: After immunization, SC rates (58.2% vs 74.3%, P = 0.017) were significantly lower in SpA patients receiving anti-TNF therapy, whereas no difference was observed in RA patients receiving this therapy compared with healthy controls (P = 0.067). SpA patients receiving mAbs (infliximab/adalimumab) had a significantly lower SC rate compared with healthy controls (51.6% vs 74.3%, P = 0.002) or those on DMARDs (51.6% vs 74.7%, P = 0.005), whereas no difference was observed for patients on etanercept (86.7% vs 74.3%, P = 0.091). Further analysis of non-seroconverting and seroconverting SpA patients revealed that the former group had a higher mean age (P = 0.003), a higher frequency of anti-TNF (P = 0.031) and mAbs (P = 0.001) and a lower frequency of MTX (P = 0.028). In multivariate logistic regression, only older age (P = 0.015) and mAb treatment (P = 0.023) remained significant factors for non-SC in SpA patients.

Conclusion: This study revealed a distinct disease pattern of immune response to the pandemic influenza vaccine in inflammatory arthritis patients receiving anti-TNF agents, illustrated by a reduced immunogenicity solely in SpA patients using mAbs.

Trial registration: ClinicalTrials.gov, www.clinicaltrials.gov, NCT01151644.

References

    1. Silva CA, Terreri MT, Aikawa NE, et al. Vaccination practice in children with rheumatic disease. Rev Bras Reumatol. 2010;50:351–61.
    1. Rahier JF, Moutschen M, Van Gompel A, et al. Vaccinations in patients with immune-mediated inflammatory diseases. Rheumatology. 2010;49:1815–27.
    1. Furst DE. The risk of infections with biologic therapies for rheumatoid arthritis. Semin Arthritis Rheum. 2010;39:327–46.
    1. Van Assen S, Agon-Levin N, Elkayam O, et al. EULAR recommendations for vaccination in adult patients with autoimmune inflammatory rheumatic diseases. Ann Rheum Dis. 2011;70:414–22.
    1. Centers for Disease Control and Prevention (CDC) Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP) 2010 (19 March 2012, date last accessed)
    1. Estratégia Nacional De Vacinação—Ministério Da Saúde—Brasil. [National vacinnation strategy—The Ministery of Health—Brazil]. (19 March 2012, date last accessed)
    1. Saad CG, Borba EF, Aikawa Ne, et al. Immunogenicity and safety of the 2009 non-adjuvanted influenza A/H1N1 vaccine in a large cohort of autoimmune rheumatic diseases. Ann Rheum Dis. 2011;70:1068–73.
    1. Ribeiro AC, Guedes LK, Moraes JC, et al. Reduced seroprotection after pandemic H1N1 influenza adjuvant-free vaccination in patients with rheumatoid arthritis: implications for clinical practice. Ann Rheum Dis. 2011;70:2144–47.
    1. Gabay C, Bel M, Combescure C, et al. Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum. 2011;63:1486–96.
    1. Elkayam O, Amir S, Mendelson E, et al. Efficacy and safety of vaccination against pandemic 2009 influenza A (H1N1) virus among patients with rheumatic diseases. Arthritis Care Res (Hoboken) 2011;63:1062–7.
    1. Haraoui B, Pope J. Treatment of early rheumatoid arthritis: concepts in management. Semin Arthritis Rheum. 2011;40:371–88.
    1. Arnett FC, Edworthy SM, Bloch DA, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988;31:315–24.
    1. van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum. 1984;27:361–8.
    1. Taylor W, Gladman D, Helliwell P, et al. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum. 2006;54:2665–73.
    1. Kendal AP, Pereira MS, Skehel JJ, editors. Concepts and procedures from laboratory-based influenza surveillance. Atlanta, GA: Centers for Disease Control and Prevention; 1982.
    1. Shoenfeld Y, Agmon-Levin N. ‘ASIA’ - autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36:4–8.
    1. Mathian A, Devilliers H, Krivine A, et al. Factors influencing the efficacy of two injections of a pandemic 2009 influenza A (H1N1) nonadjuvanted vaccine in systemic lupus erythematosus. Arthritis Rheum. 2011;63:3502–11.
    1. Lu CC, Wang YC, Lai JH, et al. A/H1N1 influenza vaccination in patients with systemic lupus erythematosus. safety and immunity. Vaccine. 2011;29:444–50.
    1. Urowitz MB, Anton A, Ibanez D, Gladman DD. Autoantibody response to adjuvant and nonadjuvant H1N1 vaccination in systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2011;63:1517–20.
    1. Lertdumrongluk P, Changsirikulchai S, Limkunakul C, et al. Safety and immunogenicity of a 2009 influenza A (H1N1) vaccine in hemodialysis patients. Vaccine. 2012;30:1108–14.
    1. Fomin I, Caspi D, Levy V, et al. Vaccination against influenza in rheumatoid arthritis: the effect of disease modifying drugs, including TNF alpha blockers. Ann Rheum Dis. 2006;65:191–4.
    1. Kubota T, Nii T, Nanki T, et al. Anti-tumor necrosis factor therapy does not diminish the immune response to influenza vaccine in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2007;17:531–3.
    1. Elkayam O, Bashkin A, Mandelboim M, et al. The effect of infliximab and timing of vaccination on the humoral response to influenza vaccination in patients with rheumatoid arthritis and ankylosing spondylitis. Semin Arthritis Rheum. 2010;39:442–7.
    1. Kapetanovic MC, Saxne T, Nilsson JA, Geborek P. Influenza vaccination as model for testing immune modulation induced by anti-TNF and methotrexate therapy in rheumatoid arthritis patients. Rheumatology. 2007;46:608–11.
    1. Gelinck LB, Van Der Bijl AE, Beyer WE, et al. The effect of anti-tumour necrosis factor alpha treatment on the antibody response to influenza vaccination. Ann Rheum Dis. 2008;67:713–6.
    1. Salemi S, Picchianti-Diamanti A, Germano V, et al. Influenza vaccine administration in rheumatoid arthritis patients under treatment with TNF alpha blockers: safety and immunogenicity. Clin Immunol. 2010;134:113–20.
    1. Kaine JL, Kivitz AJ, Birbara C, Luo AY. Immune responses following administration of influenza and pneumococcal vaccines to patients with rheumatoid arthritis receiving adalimumab. J Rheumatol. 2007;34:272–9.
    1. 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;18(301):737–44.
    1. Wallis RS. Tumour necrosis factor antagonists: structure, function, and tuberculosis risks. Lancet Infect Dis. 2008;8:601–11.
    1. Scallon B, Cai A, Solowski N, et al. Binding and functional comparisons of two types of tumor necrosis factor antagonists. J Pharmacol Exp Ther. 2002;301:418–26.
    1. Young F, Marra F. A systematic review of intradermal influenza vaccines. Vaccine. 2001;29:8788–801.
    1. Borba EF, Saad CG, Pasoto SG, et al. Antimalarials: a window of opportunity to improve the influenza A/H1N1 vaccine response in lupus patients under immunosuppressive agents. Rheumatology. 2011;51:1061–9.
    1. Aikawa NE, Campos LM, Silva CA, et al. Glucocorticoid: major factor for reduced immunogenicity of 2009 influenza a (H1N1) vaccine in patients with juvenile autoimmune rheumatic disease. J Rheumatol. 2012;39:167–73.
    1. Rahier JF, Papay P, Salleron J, et al. H1N1 vaccines in a large observational cohort of patients with inflammatory bowel disease treated with immunomodulators and biological therapy. Gut. 2011;60:456–62.
    1. Crowe SR, Merrill JT, Vista E S, et al. Influenza vaccination responses in human systemic lupus erythematosus: impact of clinical and demographic features. Arthritis Rheum. 2011;63:2396–406.
    1. European Committee for Medicinal Products for Human Use. London: European Medicines Agency; 2004. Guideline on dossier structure and content for pandemic influenza vaccine marketing authorisation application. Publication no. EMEA/CPMP/VEG/4717/2003-Rev.1. (19 March 2012, date last accessed)
    1. Department of Health and Human Services, Food and Drug Administration, Center for Biologics Evaluation and Research. Guidance for industry: clinical data needed to support the licensure of pandemic influenza vaccines. May 2007. .

Source: PubMed

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