Vaccination of patients with autoimmune inflammatory rheumatic diseases

Key Points

  • As patients with an autoimmune inflammatory rheumatic disease (AIRD) are at increased risk of infection, vaccination could be of paramount importance

  • Vaccination of patients with an AIRD is complicated by possible decreased efficacy of the vaccine and the risk of exacerbating underlying disease

  • Most vaccinations of patients with an AIRD seem to be effective; however, efficacy is dependent on the vaccine used, the type of AIRD and the medication regimen

  • Although some vaccines have been reported to induce autoimmune disorders, disease activity was not increased after vaccination in studies evaluating vaccination of patients with an AIRD

  • More research on vaccination of patients with an AIRD is needed, in particular regarding infections, adverse effects of vaccination and the influence of immunomodulatory therapies on vaccination efficacy

Abstract

Patients with autoimmune inflammatory rheumatic diseases (AIRDs) are at increased risk of infections. This risk has been further increased by the introduction of biologic agents over the past two decades. One of the most effective strategies to prevent infection is vaccination. However, patients with an AIRD have a compromised immune system, which is further impaired by medication. Another important issue is the possibility of triggering a broad nonspecific response by vaccination, potentially resulting in increased activity of the underlying autoimmune disease. In this Review, we provide an analysis of data on vaccination of patients with an AIRD. Both the efficacy and the safety of vaccination are addressed, together with the epidemiology of vaccine-preventable infectious diseases in different subgroups of adults with AIRDs. Special attention is given to vaccination of patients who are treated with biologic agents.

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Figure 1: Treatment-related RR of herpes zoster in RA.
Figure 2: Recommended vaccinations for patients with an AIRD.

References

  1. 1

    Mandell, B. F. Vaccination: an option not to be ignored. Cleve. Clin. J. Med. 77, 151 (2010).

  2. 2

    Plotkin, S. A. Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47, 401–409 (2008).

  3. 3

    Touma, Z., Gladman, D. D. & Urowitz, M. B. Vaccination and auto-immune rheumatic diseases: lessons learnt from the 2009 H1N1 influenza virus vaccination campaign. Curr. Opin. Rheumatol. 25, 164–170 (2013).

  4. 4

    Murdaca, G. et al. Influenza and pneumococcal vaccinations of patients with systemic lupus erythematosus: current views upon safety and immunogenicity. Autoimmun. Rev. 13, 75–84 (2014).

  5. 5

    Van Assen, S. et al. Vaccination in adult patients with auto-immune inflammatory rheumatic diseases: a systematic literature review for the European League Against Rheumatism evidence-based recommendations for vaccination in adult patients with auto-immune inflammatory rheumatic diseases. Autoimmun. Rev. 10, 341–352 (2011).

  6. 6

    Hohensinner, P. J., Goronzy, J. J. & Weyand, C. M. Telomere dysfunction, autoimmunity and aging. Aging Dis. 2, 524–537 (2011).

  7. 7

    Stampfli, M. R. & Anderson, G. P. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol. 9, 377–384 (2009).

  8. 8

    Listing, J., Gerhold, K. & Zink, A. The risk of infections associated with rheumatoid arthritis, with its comorbidity and treatment. Rheumatology (Oxford) 52, 53–61 (2013).

  9. 9

    Germano, V. et al. Infection risk in rheumatoid arthritis and spondyloarthropathy patients under treatment with DMARDs, corticosteroids and TNF-α antagonists. J. Transl. Med. http://dx.doi.org/10.1186/1479-5876-12-77.

  10. 10

    Sciascia, S., Cuadrado, M. J. & Karim, M. Y. Management of infection in systemic lupus erythematosus. Best Pract. Res. Clin. Rheumatol. 27, 377–389 (2013).

  11. 11

    Curtis, J. R. et al. Risk of hospitalized bacterial infections associated with biologic treatment among US veterans with rheumatoid arthritis. Arthritis Care Res. (Hoboken) 66, 990–997 (2014).

  12. 12

    Ruiz-Irastorza, G. et al. Predictors of major infections in systemic lupus erythematosus. Arthritis Res. Ther. 11, R109 (2009).

  13. 13

    Nichol, K. L., Wuorenma, J. & von Sternberg, T. Benefits of influenza vaccination for low-, intermediate-, and high-risk senior citizens. Arch. Intern. Med. 158, 1769–1776 (1998).

  14. 14

    Hak, E. et al. Influence of high-risk medical conditions on the effectiveness of influenza vaccination among elderly members of 3 large managed-care organizations. Clin. Infect. Dis. 35, 370–377 (2002).

  15. 15

    Blumentals, W. A., Arreglado, A., Napalkov, P. & Toovey, S. Rheumatoid arthritis and the incidence of influenza and influenza-related complications: a retrospective cohort study. BMC Musculoskelet. Disord. 13, 158 (2012).

  16. 16

    Wotton, C. J. & Goldacre, M. J. Risk of invasive pneumococcal disease in people admitted to hospital with selected immune-mediated diseases: record linkage cohort analyses. J. Epidemiol. Community Health 66, 1177–1181 (2012).

  17. 17

    Yee, A. M., Ng, S. C., Sobel, R. E. & Salmon, J. E. FcγRIIA polymorphism as a risk factor for invasive pneumococcal infections in systemic lupus erythematosus. Arthritis Rheum. 40, 1180–1182 (1997).

  18. 18

    Klippel, J. H. et al. A controlled study of pneumococcal polysaccharide vaccine in systemic lupus erythematosus. Arthritis Rheum. 22, 1321–1325 (1979).

  19. 19

    Naveau, C. & Houssiau, F. A. Pneumococcal sepsis in patients with systemic lupus erythematosus. Lupus 14, 903–906 (2005).

  20. 20

    Lu, T. Y. et al. A retrospective seven-year analysis of the use of B cell depletion therapy in systemic lupus erythematosus at University College London Hospital: the first fifty patients. Arthritis Rheum. 61, 482–487 (2009).

  21. 21

    Favalli, E. G. et al. Serious infections during anti-TNFα treatment in rheumatoid arthritis patients. Autoimmun. Rev. 8, 266–273 (2009).

  22. 22

    Strangfeld, A. et al. Risk of herpes zoster in patients with rheumatoid arthritis treated with anti-TNF-α agents. JAMA 301, 737–744 (2009).

  23. 23

    Antonelli, M. A., Moreland, L. W. & Brick, J. E. Herpes zoster in patients with rheumatoid arthritis treated with weekly, low-dose methotrexate. Am. J. Med. 90, 295–298 (1991).

  24. 24

    McDonald, J. R. et al. Herpes zoster risk factors in a national cohort of veterans with rheumatoid arthritis. Clin. Infect. Dis. 48, 1364–1371 (2009).

  25. 25

    Smitten, A. L. et al. The risk of herpes zoster in patients with rheumatoid arthritis in the United States and the United Kingdom. Arthritis Rheum. 57, 1431–1438 (2007).

  26. 26

    Speerstra, F. et al. Side-effects of azathioprine treatment in rheumatoid arthritis: analysis of 10 years of experience. Ann. Rheum. Dis. 41, (Suppl. 1) 37–39 (1982).

  27. 27

    Wolfe, F., Michaud, K. & Chakravarty, E. F. Rates and predictors of herpes zoster in patients with rheumatoid arthritis and non-inflammatory musculoskeletal disorders. Rheumatology (Oxford) 45, 1370–1375 (2006).

  28. 28

    Garcia-Doval, I. et al. Incidence and risk of hospitalisation due to shingles and chickenpox in patients with rheumatic diseases treated with TNF antagonists. Ann. Rheum. Dis. 69, 1751–1755 (2010).

  29. 29

    Winthrop, K. L. et al. Association between the initiation of anti-tumor necrosis factor therapy and the risk of herpes zoster. JAMA 309, 887–895 (2013).

  30. 30

    Ramiro, S. et al. Safety of synthetic and biological DMARDs: a systematic literature review informing the 2013 update of the EULAR recommendations for management of rheumatoid arthritis. Ann. Rheum. Dis. 73, 529–535 (2014).

  31. 31

    Kahl, L. E. Herpes zoster infections in systemic lupus erythematosus: risk factors and outcome. J. Rheumatol. 21, 84–86 (1994).

  32. 32

    Kang, T. Y., Lee, H. S., Kim, T. H., Jun, J. B. & Yoo, D. H. Clinical and genetic risk factors of herpes zoster in patients with systemic lupus erythematosus. Rheumatol. Int. 25, 97–102 (2005).

  33. 33

    Manzi, S. et al. Herpes zoster in systemic lupus erythematosus. J. Rheumatol. 22, 1254–1258 (1995).

  34. 34

    Chakravarty, E. F., Michaud, K., Katz, R. & Wolfe, F. Increased incidence of herpes zoster among patients with systemic lupus erythematosus. Lupus 22, 238–244 (2013).

  35. 35

    Ginzler, E. et al. Computer analysis of factors influencing frequency of infection in systemic lupus erythematosus. Arthritis Rheum. 21, 37–44 (1978).

  36. 36

    Nagaoka, S. et al. Herpes zoster in patients with polymyositis and dermatomyositis. Kansenshogaku Zasshi 64, 1394–1399 (1990).

  37. 37

    Nagasawa, K. et al. High incidence of herpes zoster in patients with systemic lupus erythematosus: an immunological analysis. Ann. Rheum. Dis. 49, 630–633 (1990).

  38. 38

    Wang, F., Chua, C. T. & Bosco, J. Herpes zoster in patients with systemic lupus erythematosus. Singapore Med. J. 24, 218–220 (1983).

  39. 39

    Dubois, E. L. & Tuffanelli, D. L. Clinical manifestations of systemic lupus erythematosus. Computer analysis of 520 cases. JAMA 190, 104–111 (1964).

  40. 40

    Ishikawa, O., Abe, M. & Miyachi, Y. Herpes zoster in Japanese patients with systemic lupus erythematosus. Clin. Exp. Dermatol. 24, 327–328 (1999).

  41. 41

    Janwityanuchit, S., Totemchokchyakarn, K., Krachangwongchai, K. & Vatanasuk, M. Infection in systemic lupus erythematosus. J. Med. Assoc. Thai. 76, 542–548 (1993).

  42. 42

    Moutsopoulos, H. M., Gallagher, J. D., Decker, J. L. & Steinberg, A. D. Herpes zoster in patients with systemic lupus erythematosus. Arthritis Rheum. 21, 798–802 (1978).

  43. 43

    Borba, E. F. et al. Incidence, risk factors, and outcome of Herpes zoster in systemic lupus erythematosus. J. Clin. Rheumatol. 16, 119–122 (2010).

  44. 44

    Della-Torre, E. et al. Individualized therapy provides better outcome in patients with proliferative lupus nephritis: follow up of a cohort of Italian patients [abstract]. Ann. Rheum. Dis. 68 (Suppl. 3), 247 (2009).

  45. 45

    Tokunaga, M. et al. Efficacy of rituximab (anti-CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann. Rheum. Dis. 66, 470–475 (2007).

  46. 46

    Mak, A. et al. Mycophenolate mofetil is as efficacious as, but safer than, cyclophosphamide in the treatment of proliferative lupus nephritis: a meta-analysis and meta-regression. Rheumatology (Oxford) 48, 944–952 (2009).

  47. 47

    Merrill, J. T. et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 62, 222–233 (2010).

  48. 48

    Wung, P. K. et al. Herpes zoster in immunocompromised patients: incidence, timing, and risk factors. Am. J. Med. 118, 1416 (2005).

  49. 49

    Tam, L. S., Chan, A. Y., Chan, P. K., Chang, A. R. & Li, E. K. Increased prevalence of squamous intraepithelial lesions in systemic lupus erythematosus: association with human papillomavirus infection. Arthritis Rheum. 50, 3619–3625 (2004).

  50. 50

    Nath, R. et al. High risk of human papillomavirus type 16 infections and of development of cervical squamous intraepithelial lesions in systemic lupus erythematosus patients. Arthritis Rheum. 57, 619–625 (2007).

  51. 51

    Lee, Y. H. et al. Prevalence of human papilloma virus infections and cervical cytological abnormalities among Korean women with systemic lupus erythematosus. J. Korean Med. Sci. 25, 1431–1437 (2010).

  52. 52

    Tam, L. S. et al. Natural history of cervical papilloma virus infection in systemic lupus erythematosus - a prospective cohort study. J. Rheumatol. 37, 330–340 (2010).

  53. 53

    Stojanovich, L. Influenza vaccination of patients with systemic lupus erythematosus (SLE) and rheumatoid arthritis (RA). Clin. Dev. Immunol. 13, 373–375 (2006).

  54. 54

    Kobashigawa, T. et al. Vaccination against seasonal influenza is effective in Japanese patients with rheumatoid arthritis enrolled in a large observational cohort. Scand. J. Rheumatol. 42, 445–450 (2013).

  55. 55

    Kostianovsky, A. et al. Immunogenicity and safety of seasonal and 2009 pandemic A/H1N1 influenza vaccines for patients with autoimmune diseases: a prospective, monocentre trial on 199 patients. Clin. Exp. Rheumatol. 30 (1 Suppl. 70), S83–S89 (2012).

  56. 56

    De Jong, J. C. et al. Haemagglutination-inhibiting antibody to influenza virus. Dev. Biol. (Basel) 115, 63–73 (2003).

  57. 57

    Chalmers, A. et al. Immunization of patients with rheumatoid arthritis against influenza: a study of vaccine safety and immunogenicity. J. Rheumatol. 21, 1203–1206 (1994).

  58. 58

    Del Porto, F. et al. Influenza vaccine administration in patients with systemic lupus erythematosus and rheumatoid arthritis. Safety and immunogenicity. Vaccine 24, 3217–3223 (2006).

  59. 59

    Denman, E. J., Denman, A. M., Greenwood, B. M., Gall, D. & Heath, R. B. Failure of cytotoxic drugs to suppress immune responses of patients with rheumatoid arthritis. Ann. Rheum. Dis. 29, 220–231 (1970).

  60. 60

    Fomin, I. et al. Vaccination against influenza in rheumatoid arthritis: the effect of disease modifying drugs, including TNF α blockers. Ann. Rheum. Dis. 65, 191–194 (2006).

  61. 61

    Gelinck, L. B. et al. The effect of anti-tumour necrosis factor α treatment on the antibody response to influenza vaccination. Ann. Rheum. Dis. 67, 713–716 (2008).

  62. 62

    Herron, A. et al. Influenza vaccination in patients with rheumatic diseases. Safety and efficacy. JAMA 242, 53–56 (1979).

  63. 63

    Kaine, J. L., Kivitz, A. J., Birbara, C. & Luo, A. Y. Immune responses following administration of influenza and pneumococcal vaccines to patients with rheumatoid arthritis receiving adalimumab. J. Rheumatol. 34, 272–279 (2007).

  64. 64

    Kubota, 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. 17, 531–533 (2007).

  65. 65

    Nii, T. et al. Reevaluation of antibody titers 1 year after influenza vaccination in patients with rheumatoid arthritis receiving TNF blockers. Mod. Rheumatol. 19, 216–218 (2009).

  66. 66

    Turner-Stokes, L., Cambridge, G., Corcoran, T., Oxford, J. S. & Snaith, M. L. In vitro response to influenza immunisation by peripheral blood mononuclear cells from patients with systemic lupus erythematosus and other autoimmune diseases. Ann. Rheum. Dis. 47, 532–535 (1988).

  67. 67

    Van Assen, S. et al. Humoral responses after influenza vaccination are severely reduced in patients with rheumatoid arthritis treated with rituximab. Arthritis Rheum. 62, 75–81 (2010).

  68. 68

    Elkayam, O. Safety and efficacy of vaccination against influenza in patients with rheumatoid arthritis. Clin. Dev. Immunol. 13, 349–351 (2006).

  69. 69

    Kapetanovic, M. C., Saxne, T., Nilsson, J. A. & Geborek, P. Influenza vaccination as model for testing immune modulation induced by anti-TNF and methotrexate therapy in rheumatoid arthritis patients. Rheumatology (Oxford) 46, 608–611 (2007).

  70. 70

    Kivitz, A. J. et al. Vaccine responses in patients with rheumatoid arthritis treated with certolizumab pegol: results from a single-blind randomized phase IV trial. J. Rheumatol. 41, 648–657 (2014).

  71. 71

    Elkayam, O. 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. 39, 442–447 (2010).

  72. 72

    Gelinck, L. B. et al. Poor serological responses upon influenza vaccination in patients with rheumatoid arthritis treated with rituximab. Ann. Rheum. Dis. 66, 1402–1403 (2007).

  73. 73

    Kapetanovic, M. C. Further evidence for influenza and pneumococcal vaccination in patients treated with disease modifying antirheumatic drugs and anti-tumor necrosis factor agents. J. Rheumatol. 41, 626–628 (2014).

  74. 74

    Kapetanovic, M. C. et al. Impact of anti-rheumatic treatment on immunogenicity of pandemic H1N1 influenza vaccine in patients with arthritis. Arthritis Res. Ther. 16, R2 (2014).

  75. 75

    Oren, S. et al. Vaccination against influenza in patients with rheumatoid arthritis: the effect of rituximab on the humoral response. Ann. Rheum. Dis. 67, 937–941 (2008).

  76. 76

    Elkayam, O. et al. Efficacy and safety of vaccination against pandemic 2009 influenza A (H1N1) virus among patients with rheumatic diseases. Arthritis Care Res. (Hoboken) 63, 1062–1067 (2011).

  77. 77

    Mori, S. et al. Impact of tocilizumab therapy on antibody response to influenza vaccine in patients with rheumatoid arthritis. Ann. Rheum. Dis. 71, 2006–2010 (2012).

  78. 78

    Ribeiro, A. C. et al. Abatacept and reduced immune response to pandemic 2009 influenza A/H1N1 vaccination in patients with rheumatoid arthritis. Arthritis Care Res. (Hoboken) 65, 476–480 (2013).

  79. 79

    Williams, G. W. et al. Influenza immunization in systemic lupus eruthematosus. A double-blind trial. Ann. Intern. Med. 88, 729–734 (1978).

  80. 80

    Holvast, A. et al. Safety and efficacy of influenza vaccination in systemic lupus erythematosus patients with quiescent disease. Ann. Rheum. Dis. 65, 913–918 (2006).

  81. 81

    Mercado, U., Acosta, H. & Avendano, L. Influenza vaccination of patients with systemic lupus erythematosus. Rev. Invest. Clin. 56, 16–20 (2004).

  82. 82

    Wiesik-Szewczyk, E. et al. Anti-influenza vaccination in systemic lupus erythematosus patients: an analysis of specific humoral response and vaccination safety. Clin. Rheumatol. 29, 605–613 (2010).

  83. 83

    Brodman, R., Gilfillan, R., Glass, D. & Schur, P. H. Influenzal vaccine response in systemic lupus erythematosus. Ann. Intern. Med. 88, 735–740 (1978).

  84. 84

    Louie, J. S. et al. Clinical and antibody responses after influenza immunization in systemic lupus erythematosus. Ann. Intern. Med. 88, 790–792 (1978).

  85. 85

    Pons, V. G., Reinertsen, J. L., Steinberg, A. D. & Dolin, R. Decreased cell-mediated cytotoxicity against virus-infected cells in systemic lupus erythematosus. J. Med. Virol. 4, 15–23 (1979).

  86. 86

    Ristow, S. C., Douglas, R. G. Jr & Condemi, J. J. Influenza vaccination of patients with systemic lupus erythematosus. Ann. Intern. Med. 88, 786–789 (1978).

  87. 87

    Abu-Shakra, M. et al. Specific antibody response after influenza immunization in systemic lupus erythematosus. J. Rheumatol. 29, 2555–2557 (2002).

  88. 88

    Crowe, S. R. et al. Influenza vaccination responses in human systemic lupus erythematosus: impact of clinical and demographic features. Arthritis Rheum. 63, 2396–2406 (2011).

  89. 89

    Holvast, A. et al. Effect of a second, booster, influenza vaccination on antibody responses in quiescent systemic lupus erythematosus: an open, prospective, controlled study. Rheumatology (Oxford) 48, 1294–1299 (2009).

  90. 90

    Holvast, A. et al. Wegener's granulomatosis patients show an adequate antibody response to influenza vaccination. Ann. Rheum. Dis. 68, 873–878 (2009).

  91. 91

    Zycinska, K. et al. Antibody response to inactivated subunit influenza vaccine in patients with Wegener's granulomatosis. J. Physiol. Pharmacol. 58 (Suppl. 5), 819–828 (2007).

  92. 92

    Setti, M. et al. Flu vaccination with a virosomal vaccine does not affect clinical course and immunological parameters in scleroderma patients. Vaccine 27, 3367–3372 (2009).

  93. 93

    Saad, C. G. 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. 70, 1068–1073 (2011).

  94. 94

    Gabay, 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. 63, 1486–1496 (2011).

  95. 95

    Iwamoto, M. et al. Low level of seroconversion after a novel influenza A/H1N1/2009 vaccination in Japanese patients with rheumatoid arthritis in the 2009 season. Rheumatol. Int. 32, 3691–3694 (2012).

  96. 96

    Mathian, 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. 63, 3502–3511 (2011).

  97. 97

    Lu, C. C. et al. A/H1N1 influenza vaccination in patients with systemic lupus erythematosus: safety and immunity. Vaccine 29, 444–450 (2011).

  98. 98

    Pasoto, S. G. et al. Short and long-term effects of pandemic unadjuvanted influenza A(H1N1)pdm09 vaccine on clinical manifestations and autoantibody profile in primary Sjögren's syndrome. Vaccine 31, 1793–1798 (2013).

  99. 99

    Arad, U. et al. The cellular immune response to influenza vaccination is preserved in rheumatoid arthritis patients treated with rituximab. Vaccine 29, 1643–1648 (2011).

  100. 100

    Holvast, A. et al. Studies of cell-mediated immune responses to influenza vaccination in systemic lupus erythematosus. Arthritis Rheum. 60, 2438–2447 (2009).

  101. 101

    Coulson, E. et al. Pneumococcal antibody levels after pneumovax in patients with rheumatoid arthritis on methotrexate. Ann. Rheum. Dis. 70, 1289–1291 (2011).

  102. 102

    Visvanathan, S., Keenan, G. F., Baker, D. G., Levinson, A. I. & Wagner, C. L. Response to pneumococcal vaccine in patients with early rheumatoid arthritis receiving infliximab plus methotrexate or methotrexate alone. J. Rheumatol. 34, 952–957 (2007).

  103. 103

    Kapetanovic, M. C. et al. Influence of methotrexate, TNF blockers and prednisolone on antibody responses to pneumococcal polysaccharide vaccine in patients with rheumatoid arthritis. Rheumatology (Oxford) 45, 106–111 (2006).

  104. 104

    Bingham, C. O. 3rd et al. Immunization responses in rheumatoid arthritis patients treated with rituximab: results from a controlled clinical trial. Arthritis Rheum. 62, 64–74 (2010).

  105. 105

    Elkayam, O. et al. Immunogenicity and safety of pneumococcal vaccination in patients with rheumatoid arthritis or systemic lupus erythematosus. Clin. Infect. Dis. 34, 147–153 (2002).

  106. 106

    Elkayam, O., Caspi, D., Reitblatt, T., Charboneau, D. & Rubins, J. B. The effect of tumor necrosis factor blockade on the response to pneumococcal vaccination in patients with rheumatoid arthritis and ankylosing spondylitis. Semin. Arthritis Rheum. 33, 283–288 (2004).

  107. 107

    Kapetanovic, M. C. et al. Antibody response is reduced following vaccination with 7-valent conjugate pneumococcal vaccine in adult methotrexate-treated patients with established arthritis, but not those treated with tumor necrosis factor inhibitors. Arthritis Rheum. 63, 3723–3732 (2011).

  108. 108

    Kapetanovic, M. C., Roseman, C., Jönsson, G. & Truedsson, L. Heptavalent pneumococcal conjugate vaccine elicits similar antibody response as standard 23-valent polysaccharide vaccine in adult patients with RA treated with immunomodulating drugs. Clin. Rheumatol. 30, 1555–1561 (2011).

  109. 109

    Mori, S. et al. Pneumococcal polysaccharide vaccination in rheumatoid arthritis patients receiving tocilizumab therapy. Ann. Rheum. Dis. 72, 1362–1366 (2013).

  110. 110

    Bingham, C. O. 3rd et al. Humoral immune response to vaccines in patients with rheumatoid arthritis treated with tocilizumab: results of a randomised controlled trial (VISARA). Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis-2013-204427.

  111. 111

    Croft, S. M. et al. Specific antibody response after in vivo antigenic stimulation in systemic lupus erythematosus. J. Rheumatol. 11, 141–146 (1984).

  112. 112

    Lipnick, R. N. et al. Pneumococcal immunization in patients with systemic lupus erythematosus treated with immunosuppressives. J. Rheumatol. 12, 1118–1121 (1985).

  113. 113

    Battafarano, D. F. et al. Antigen-specific antibody responses in lupus patients following immunization. Arthritis Rheum. 41, 1828–1834 (1998).

  114. 114

    Jarrett, M. P., Schiffman, G., Barland, P. & Grayzel, A. I. Impaired response to pneumococcal vaccine in systemic lupus erythematosus. Arthritis Rheum. 23, 1287–1293 (1980).

  115. 115

    McDonald, E., Jarrett, M. P., Schiffman, G. & Grayzel, A. I. Persistence of pneumococcal antibodies after immunization in patients with systemic lupus erythematosus. J. Rheumatol. 11, 306–308 (1984).

  116. 116

    Tarjan, P. et al. No short-term immunological effects of Pneumococcus vaccination in patients with systemic lupus erythematosus. Scand. J. Rheumatol. 31, 211–215 (2002).

  117. 117

    Franco Salinas, G. et al. TNF blockade impairs T cell dependent antibody responses [abstract]. Ann. Rheum. Dis. 68 (Suppl. 3), 238 (2009).

  118. 118

    Mease, P. J. et al. Pneumococcal vaccine response in psoriatic arthritis patients during treatment with etanercept. J. Rheumatol. 31, 1356–1361 (2004).

  119. 119

    Mercado, U., Acosta, H. & Diaz-Molina, R. Antibody response to pneumococcal polysaccharide vaccine in systemic sclerosis. J. Rheumatol. 36, 1549–1550 (2009).

  120. 120

    Kuruma, K. A., Borba, E. F., Lopes, M. H., de Carvalho, J. F. & Bonfá, E. Safety and efficacy of hepatitis B vaccine in systemic lupus erythematosus. Lupus 16, 350–354 (2007).

  121. 121

    Erkek, E., Ayaslioglu, E., Erkek, A. B., Kurtipek, G. S. & Bagci, Y. Response to vaccination against hepatitis B in patients with Behcet's disease. J. Gastroenterol. Hepatol. 20, 1508–1511 (2005).

  122. 122

    Devey, M. E., Bleasdale, K. & Isenberg, D. A. Antibody affinity and IgG subclass of responses to tetanus toxoid in patients with rheumatoid arthritis and systemic lupus erythematosus. Clin. Exp. Immunol. 68, 562–569 (1987).

  123. 123

    Abe, T. & Homma, M. Immunological reactivity in patients with systemic lupus erythematosus. Humoral antibody and cellular immune responses. Acta Rheumatol. Scand. 17, 35–46 (1971).

  124. 124

    Kashef, S., Ghazizadeh, F., Derakhshan, A., Farjadian, S. & Alyasin, S. Antigen-specific antibody response in juvenile-onset SLE patients following routine immunization with tetanus toxoid. Iran. J. Immunol. 5, 181–184 (2008).

  125. 125

    Nies, K., Boyer, R., Stevens, R. & Louie, J. Anti-tetanus toxoid antibody synthesis after booster immunization in systemic lupus erythematosus. Comparison of the in vitro and in vivo responses. Arthritis Rheum. 23, 1343–1350 (1980).

  126. 126

    Askling, H. H. et al. Hepatitis A vaccine for immunosuppressed patients with rheumatoid arthritis: a prospective, open-label, multi-centre study. Travel Med. Infect. Dis. 12, 134–142 (2014).

  127. 127

    Mok, C. C., Ho, L. Y., Fong, L. S. & To, C. H. Immunogenicity and safety of a quadrivalent human papillomavirus vaccine in patients with systemic lupus erythematosus: a case–control study. Ann. Rheum. Dis. 72, 659–664 (2013).

  128. 128

    Soybilgic, A., Onel, K. B., Utset, T., Alexander, K. & Wagner-Weiner, L. Safety and immunogenicity of the quadrivalent HPV vaccine in female systemic lupus erythematosus patients aged 12 to 26 years. Pediatr. Rheumatol. Online J. 11, 29 (2013).

  129. 129

    Van Assen, S. et al. EULAR recommendations for vaccination in adult patients with autoimmune inflammatory rheumatic diseases. Ann. Rheum. Dis. 70, 414–422 (2011).

  130. 130

    Singh, J. A. et al. 2012 update of the 2008 American College of Rheumatology recommendations for the use of disease-modifying antirheumatic drugs and biologic agents in the treatment of rheumatoid arthritis. Arthritis Care. Res. (Hoboken) 64, 625–639 (2012).

  131. 131

    Zhang, J. et al. Association between vaccination for herpes zoster and risk of herpes zoster infection among older patients with selected immune-mediated diseases. JAMA 308, 43–49 (2012).

  132. 132

    Guthridge, J. M. et al. Herpes zoster vaccination in SLE: a pilot study of immunogenicity. J. Rheumatol. 40, 1875–1880 (2013).

  133. 133

    Shoenfeld, Y. & Agmon-Levin, N. 'ASIA' - autoimmune/inflammatory syndrome induced by adjuvants. J. Autoimmun. 36, 4–8 (2011).

  134. 134

    Colafrancesco, S., Perricone, C., Priori, R., Valesini, G. & Shoenfeld, Y. Sjögren's syndrome: another facet of the autoimmune/inflammatory syndrome induced by adjuvants (ASIA). J. Autoimmun. 51, 10–16 (2014).

  135. 135

    Perricone, C. et al. Autoimmune/inflammatory syndrome induced by adjuvants (ASIA) 2013: unveiling the pathogenic, clinical and diagnostic aspects. J. Autoimmun. 47, 1–16 (2013).

  136. 136

    Borchers, A. T., Keen, C. L., Shoenfeld, Y., Silva, J. Jr & Gershwin, M. E. Vaccines, viruses, and voodoo. J. Investig. Allergol. Clin. Immunol. 12, 155–168 (2002).

  137. 137

    Bengtsson, C. et al. Common vaccinations among adults do not increase the risk of developing rheumatoid arthritis: results from the Swedish EIRA study. Ann. Rheum. Dis. 69, 1831–1833 (2010).

  138. 138

    Grimaldi-Bensouda, L. et al. The risk of systemic lupus erythematosus associated with vaccines: an international case–control study. Arthritis Rheumatol. 66, 1559–1567 (2014).

  139. 139

    Perdan-Pirkmajer, K. et al. Autoimmune response following influenza vaccination in patients with autoimmune inflammatory rheumatic disease. Lupus 21, 175–183 (2012).

  140. 140

    Lu, C. C. et al. A/H1N1 influenza vaccination in patients with systemic lupus erythematosus: safety and immunity. Vaccine 29, 444–450 (2011).

  141. 141

    Urowitz, M. B., Anton, A., Ibanez, D. & Gladman, D. D. Autoantibody response to adjuvant and nonadjuvant H1N1 vaccination in systemic lupus erythematosus. Arthritis Care Res. (Hoboken) 63, 1517–1520 (2011).

  142. 142

    Milanetti, F. et al. Safety and immunogenicity of co-administered MF59-adjuvanted 2009 pandemic and plain 2009–10 seasonal influenza vaccines in rheumatoid arthritis patients on biologicals. Clin. Exp. Immunol. 177, 287–294 (2014).

  143. 143

    Aikawa, N. E. et al. Effective seroconversion and safety following the pandemic influenza vaccination (anti-H1N1) in patients with juvenile idiopathic arthritis. Scand. J. Rheumatol. 42, 34–40 (2013).

  144. 144

    Stassen, P. M., Sanders, J. S., Kallenberg, C. G. & Stegeman, C. A. Influenza vaccination does not result in an increase in relapses in patients with ANCA-associated vasculitis. Nephrol. Dial. Transplant. 23, 654–658 (2008).

  145. 145

    Karsh, J., Pavlidis, N., Schiffman, G. & Moutsopoulos, H. M. Immunization of patients with Sjögren's syndrome with pneumococcal polysaccharide vaccine: a randomized trial. Arthritis Rheum. 23, 1294–1298 (1980).

  146. 146

    Grimaldi-Bensouda, L. et al. Autoimmune disorders and quadrivalent human papillomavirus vaccination of young female subjects. J. Intern. Med. 275, 398–408 (2014).

  147. 147

    Gatto, M. et al. Human papillomavirus vaccine and systemic lupus erythematosus. Clin. Rheumatol. 32, 1301–1307 (2013).

  148. 148

    Soldevilla, H. F., Briones, S. F. & Navarra, S. V. Systemic lupus erythematosus following HPV immunization or infection? Lupus 21, 158–161 (2012).

  149. 149

    Zhang, J. et al. The use, safety, and effectiveness of herpes zoster vaccination in individuals with inflammatory and autoimmune diseases: a longitudinal observational study. Arthritis Res. Ther. 13, R174 (2011).

  150. 150

    Heijstek, M. W. et al. EULAR recommendations for vaccination in paediatric patients with rheumatic diseases. Ann. Rheum. Dis. 70, 1704–1712 (2011).

  151. 151

    Galloway, J. B. 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. 72, 229–234 (2013).

  152. 152

    Centers for Disease Control and Prevention. Recommendations on the use of quadrivalent human papillomavirus vaccine in males—Advisory Committee on Immunization Practices (ACIP). Morbidity and Mortality Weekly Report (MMWR) [online], (2011).

  153. 153

    Centers for Disease Control and Prevention. FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP). Morbidity and Mortality Weekly Report (MMWR) [online], (2011).

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J.W. and S.v.A. researched data for the article. J.W., S.v.A. and M.B. substantially contributed to discussion of content and all authors contributed to writing and review/editing of the manuscript before submission.

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Correspondence to Marc Bijl.

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Westra, J., Rondaan, C., van Assen, S. et al. Vaccination of patients with autoimmune inflammatory rheumatic diseases. Nat Rev Rheumatol 11, 135–145 (2015). https://doi.org/10.1038/nrrheum.2014.206

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