Advertisement

Individual Drugs in Rheumatology and the Risk of Infection

  • Konstantinos Thomas
  • Dimitrios Vassilopoulos
Chapter

Abstract

The advances in the therapeutics of rheumatic patients with the introduction of biologic therapies have led to a better control of diseases with inadequate response to conventional treatments and to an improvement of the functional status of these patients. Despite this progress, the risk of infections in patients under biologic or conventional treatments has not been reduced, partly because more elderly patients or patients with comorbidities are considered eligible for immunosuppressive or disease-modifying treatments. Rheumatologists should be aware of the specific patterns of infection risk that accompany these, especially the newer, treatments and should be vigilant for signs and symptoms of infection in patients with rheumatic diseases. Appropriate screening for and treatment of chronic hepatitis B virus infection and latent tuberculosis significantly reduce the risk for reactivation in patients under therapy. Chemoprophylaxis of patients susceptible for Pneumocystis jirovecii pneumonia eliminates almost completely the risk for acquisition of this potentially lethal infection in eligible patients. Appropriate vaccinations of rheumatic patients treated with antirheumatic therapies should be part of the daily clinical practice of physicians caring for patients with rheumatic diseases.

Abbreviations

AAV

ANCA-associated vasculitis

ABA

Abatacept

ADA

Adalimumab

ANA

Anakinra

ANCA

Antineutrophil cytoplasmic antibody

Anti-HBc

Antibody against hepatitis B core antigen

Anti-HBs

Antibody against hepatitis B surface antigen

AOSD

Adult-onset Still’s disease

AS

Ankylosing spondylitis

AZA

Azathioprine

BAFF

B-cell activating factor

BCG

Bacillus Calmette-Guérin

bDMARDs

Biologic disease-modifying antirheumatic drugs

CAPS

Cryopyrin-associated periodic syndromes

CD

Cluster of differentiation

CNS

Central nervous system

CRP

C-reactive protein

CsA

Cyclosporine A

csDMARDs

Conventional synthetic disease-modifying antirheumatic drugs

CYC

Cyclophosphamide

EDTA

European Dialysis and Transplantation Association

EMA

European Medicines Agency

ETN

Etanercept

EULAR

European League Against Rheumatism

FDA

Food and Drug Administration

GCA

Giant-cell arteritis

HBsAg

Hepatitis B surface antigen

HBV

Hepatitis B virus

HZ

Herpes zoster

Ig

Immunoglobulin

IGRA

Interferon-gamma releasing assay

IL

Interleukin

INFL

Infliximab

IV

Intravenous

IVIG

Intravenous immunoglobulin

JAK

Janus kinase

JIA

Juvenile idiopathic arthritis

LEF

Leflunomide

LN

Lupus nephritis

LON

Late-onset neutropenia

LTBI

Latent tuberculosis infection

LTE

Long-term extension

MMF

Mycophenolate mofetil

MTX

Methotrexate

NSAIDs

Nonsteroidal anti-inflammatory drugs

NTM

Nontuberculous mycobacteria

OIs

Opportunistic infections

PDE4

Phosphodiesterase-4

PJP

Pneumocystis jirovecii pneumonia

PML

Progressive multifocal leukoencephalopathy

PMR

Polymyalgia rheumatica

PsA

Psoriatic arthritis

RA

Rheumatoid arthritis

RCT

Randomized controlled trial

RTX

Rituximab

SC

Subcutaneous

SLE

Systemic lupus erythematosus

TB

Tuberculosis

TCZ

Tocilizumab

TMP/SMX

Trimethoprim/sulfamethoxazole

TNF

Tumor necrosis factor

TNFi

TNF inhibitors

TST

Tuberculin skin test

VZV

Varicella-zoster virus

References

  1. 1.
    Olofsson T, Petersson IF, Eriksson JK, et al. Predictors of work disability after start of anti-TNF therapy in a national cohort of Swedish patients with rheumatoid arthritis: does early anti-TNF therapy bring patients back to work? Ann Rheum Dis. 2017;76(7):1245–52.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Mikuls TR, Saag KG, Criswell LA, et al. Mortality risk associated with rheumatoid arthritis in a prospective cohort of older women: results from the Iowa women’s health study. Ann Rheum Dis. 2002;61:994–9.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Weaver A, Troum O, Hooper M, et al. Rheumatoid arthritis disease activity and disability affect the risk of serious infection events in RADIUS 1. J Rheumatol. 2013;40:1275–81.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Tektonidou MG, Wang Z, Dasgupta A, et al. Burden of serious infections in adults with systemic lupus erythematosus: a national population-based study, 1996–2011. Arthritis Care Res (Hoboken). 2015;67:1078–85.CrossRefGoogle Scholar
  5. 5.
    Rua-Figueroa I, Lopez-Longo J, Galindo-Izquierdo M, et al. Incidence, associated factors and clinical impact of severe infections in a large, multicentric cohort of patients with systemic lupus erythematosus. Semin Arthritis Rheum. 2017;47(1):38–45.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Flossmann O, Berden A, de Groot K, et al. Long-term patient survival in ANCA-associated vasculitis. Ann Rheum Dis. 2011;70:488–94.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Dougados M, Soubrier M, Antunez A, et al. Prevalence of comorbidities in rheumatoid arthritis and evaluation of their monitoring: results of an international, cross-sectional study (COMORA). Ann Rheum Dis. 2014;73:62–8.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Labarca C, Koster MJ, Crowson CS, et al. Predictors of relapse and treatment outcomes in biopsy-proven giant cell arteritis: a retrospective cohort study. Rheumatology (Oxford). 2016;55:347–56.CrossRefGoogle Scholar
  10. 10.
    Youssef J, Novosad SA, Winthrop KL. Infection risk and safety of corticosteroid use. Rheum Dis Clin North Am. 2016;42:157.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Fardet L, Petersen I, Nazareth I. Common infections in patients prescribed systemic glucocorticoids in primary care: a population-based cohort study. PLoS Med. 2016;13:e1002024.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Dixon WG, Kezouh A, Bernatsky S, et al. The influence of systemic glucocorticoid therapy upon the risk of non-serious infection in older patients with rheumatoid arthritis: a nested case-control study. Ann Rheum Dis. 2011;70:956–60.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Grijalva CG, Chen L, Delzell E, et al. Initiation of tumor necrosis factor-alpha antagonists and the risk of hospitalization for infection in patients with autoimmune diseases. JAMA. 2011;306:2331–9.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Smitten AL, Choi HK, Hochberg MC, et al. The risk of hospitalized infection in patients with rheumatoid arthritis. J Rheumatol. 2008;35:387–93.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Wolfe F, Caplan L, Michaud K. Treatment for rheumatoid arthritis and the risk of hospitalization for pneumonia: associations with prednisone, disease-modifying antirheumatic drugs, and anti-tumor necrosis factor therapy. Arthritis Rheum. 2006;54:628–34.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Dixon WG, Abrahamowicz M, Beauchamp ME, et al. Immediate and delayed impact of oral glucocorticoid therapy on risk of serious infection in older patients with rheumatoid arthritis: a nested case-control analysis. Ann Rheum Dis. 2012;71:1128–33.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Strangfeld A, Eveslage M, Schneider M, et al. Treatment benefit or survival of the fittest: what drives the time-dependent decrease in serious infection rates under TNF inhibition and what does this imply for the individual patient? Ann Rheum Dis. 2011;70:1914–20.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Ruiz-Irastorza G, Olivares N, Ruiz-Arruza I, et al. Predictors of major infections in systemic lupus erythematosus. Arthritis Res Ther. 2009;11:R109.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Bosch X, Guilabert A, Pallares L, et al. Infections in systemic lupus erythematosus: a prospective and controlled study of 110 patients. Lupus. 2006;15(9):584.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Pagnoux C, Quemeneur T, Ninet J, et al. Treatment of systemic necrotizing vasculitides in patients aged sixty-five years or older: results of a multicenter, open-label, randomized controlled trial of corticosteroid and cyclophosphamide-based induction therapy. Arthritis Rheumatol. 2015;67:1117–27.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Petri H, Nevitt A, Sarsour K, et al. Incidence of giant cell arteritis and characteristics of patients: data-driven analysis of comorbidities. Arthritis Care Res (Hoboken). 2015;67:390–5.CrossRefGoogle Scholar
  22. 22.
    Schmidt J, Smail A, Roche B, et al. Incidence of severe infections and infection-related mortality during the course of giant cell arteritis: a multicenter, prospective, double-cohort study. Arthritis Rheumatol. 2016;68:1477–82.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Koutsianas C, Thomas K, Vassilopoulos D. Hepatitis B reactivation in rheumatic diseases: screening and prevention. Rheum Dis Clin North Am. 2017;43:133–49.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    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(8):1431.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Dooley MA, Jayne D, Ginzler EM, et al. Mycophenolate versus azathioprine as maintenance therapy for lupus nephritis. N Engl J Med. 2011;365:1886–95.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Strand V, Ahadieh S, French J, et al. Systematic review and meta-analysis of serious infections with tofacitinib and biologic disease-modifying antirheumatic drug treatment in rheumatoid arthritis clinical trials. Arthritis Res Ther. 2015;17:362.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Galloway JB, Hyrich KL, Mercer LK, et al. Anti-TNF therapy is associated with an increased risk of serious infections in patients with rheumatoid arthritis especially in the first 6 months of treatment: updated results from the British Society for Rheumatology biologics register with special emphasis on risks in the elderly. Rheumatology (Oxford). 2011;50:124–31.CrossRefGoogle Scholar
  28. 28.
    van Dartel SA, Fransen J, Kievit W, et al. Difference in the risk of serious infections in patients with rheumatoid arthritis treated with adalimumab, infliximab and etanercept: results from the Dutch rheumatoid arthritis monitoring (DREAM) registry. Ann Rheum Dis. 2013;72:895–900.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Dixon WG, Watson K, Lunt M, et al. Rates of serious infection, including site-specific and bacterial intracellular infection, in rheumatoid arthritis patients receiving anti-tumor necrosis factor therapy: results from the British Society for Rheumatology biologics register. Arthritis Rheum. 2006;54:2368–76.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    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. 2015;386:258–65.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Kavanaugh A, McInnes IB, Mease P, et al. Clinical efficacy, radiographic and safety findings through 5 years of subcutaneous golimumab treatment in patients with active psoriatic arthritis: results from a long-term extension of a randomised, placebo-controlled trial (the GO-REVEAL study). Ann Rheum Dis. 2014;73:1689–94.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Gottlieb AB, Gordon K, Giannini EH, et al. Clinical trial safety and mortality analyses in patients receiving etanercept across approved indications. J Drugs Dermatol. 2011;10:289–300.PubMedGoogle Scholar
  33. 33.
    Burmester GR, Panaccione R, Gordon KB, et al. 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;72:517–24.PubMedCrossRefGoogle Scholar
  34. 34.
    Kristensen LE, Gulfe A, Saxne T, et al. Efficacy and tolerability of anti-tumour necrosis factor therapy in psoriatic arthritis patients: results from the South Swedish arthritis treatment group register. Ann Rheum Dis. 2008;67:364–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Saad AA, Ashcroft DM, Watson KD, et al. Efficacy and safety of anti-TNF therapies in psoriatic arthritis: an observational study from the British Society for Rheumatology biologics register. Rheumatology (Oxford). 2010;49:697–705.CrossRefGoogle Scholar
  36. 36.
    van der Heijde D, Zack D, Wajdula J, et al. Rates of serious infections, opportunistic infections, inflammatory bowel disease, and malignancies in subjects receiving etanercept vs. controls from clinical trials in ankylosing spondylitis: a pooled analysis. Scand J Rheumatol. 2014;43:49–53.PubMedCrossRefGoogle Scholar
  37. 37.
    Deodhar A, Braun J, Inman RD, et al. Golimumab administered subcutaneously every 4 weeks in ankylosing spondylitis: 5-year results of the GO-RAISE study. Ann Rheum Dis. 2015;74:757–61.PubMedCrossRefGoogle Scholar
  38. 38.
    Wallis D, Thavaneswaran A, Haroon N, et al. Tumour necrosis factor inhibitor therapy and infection risk in axial spondyloarthritis: results from a longitudinal observational cohort. Rheumatology (Oxford). 2015;54:152–6.CrossRefGoogle Scholar
  39. 39.
    van Vollenhoven RF, Emery P, Bingham CO III, et al. Long-term safety of rituximab in rheumatoid arthritis: 9.5-year follow-up of the global clinical trial programme with a focus on adverse events of interest in RA patients. Ann Rheum Dis. 2013;72:1496–502.PubMedCrossRefGoogle Scholar
  40. 40.
    Curtis JR, Yang S, Patkar NM, et al. Risk of hospitalized bacterial infections associated with biologic treatment among US veterans with rheumatoid arthritis. Arthritis Care Res (Hoboken). 2014;66:990–7.CrossRefGoogle Scholar
  41. 41.
    Vassilopoulos D, Delicha EM, Settas L, et al. Safety profile of repeated rituximab cycles in unselected rheumatoid arthritis patients: a long-term, prospective real-life study. Clin Exp Rheumatol. 2016;34:893–900.PubMedGoogle Scholar
  42. 42.
    Johnston SS, Turpcu A, Shi N, et al. Risk of infections in rheumatoid arthritis patients switching from anti-TNF agents to rituximab, abatacept, or another anti-TNF agent, a retrospective administrative claims analysis. Semin Arthritis Rheum. 2013;43:39–47.PubMedCrossRefGoogle Scholar
  43. 43.
    Jones RB, Tervaert JW, Hauser T, et al. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N Engl J Med. 2010;363:211–20.PubMedCrossRefGoogle Scholar
  44. 44.
    McGregor JG, Hogan SL, Kotzen ES, et al. Rituximab as an immunosuppressant in antineutrophil cytoplasmic antibody-associated vasculitis. Nephrol Dial Transplant. 2015;30(Suppl 1):i123–31.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Pendergraft WF III, Cortazar FB, Wenger J, et al. Long-term maintenance therapy using rituximab-induced continuous B-cell depletion in patients with ANCA vasculitis. Clin J Am Soc Nephrol. 2014;9:736–44.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Alberici F, Smith RM, Jones RB, et al. Long-term follow-up of patients who received repeat-dose rituximab as maintenance therapy for ANCA-associated vasculitis. Rheumatology (Oxford). 2015;54:1153–60.CrossRefGoogle Scholar
  47. 47.
    Rovin BH, Furie R, Latinis K, et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the lupus nephritis assessment with rituximab study. Arthritis Rheum. 2012;64:1215–26.PubMedCrossRefGoogle Scholar
  48. 48.
    Witt M, Grunke M, Proft F, et al. Clinical outcomes and safety of rituximab treatment for patients with systemic lupus erythematosus (SLE)–results from a nationwide cohort in Germany (GRAID). Lupus. 2013;22:1142–9.PubMedCrossRefGoogle Scholar
  49. 49.
    Mease PJ, McInnes IB, Kirkham B, et al. Secukinumab inhibition of interleukin-17A in patients with psoriatic arthritis. N Engl J Med. 2015;373:1329–39.PubMedCrossRefGoogle Scholar
  50. 50.
    McInnes IB, Mease PJ, Kirkham B, et al. Secukinumab, a human anti-interleukin-17A monoclonal antibody, in patients with psoriatic arthritis (FUTURE 2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2015;386:1137–46.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Baeten D, Sieper J, Braun J, et al. Secukinumab, an interleukin-17A inhibitor, in ankylosing spondylitis. N Engl J Med. 2015;373:2534–48.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Yamamoto K, Goto H, Hirao K, et al. Longterm safety of tocilizumab: results from 3 years of followup postmarketing surveillance of 5573 patients with rheumatoid arthritis in Japan. J Rheumatol. 2015;42:1368–75.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Sakai R, Cho SK, Nanki T, et al. Head-to-head comparison of the safety of tocilizumab and tumor necrosis factor inhibitors in rheumatoid arthritis patients (RA) in clinical practice: results from the registry of Japanese RA patients on biologics for long-term safety (REAL) registry. Arthritis Res Ther. 2015;17:74.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Salmon JH, Gottenberg JE, Ravaud P, et al. Predictive risk factors of serious infections in patients with rheumatoid arthritis treated with abatacept in common practice: results from the Orencia and rheumatoid arthritis (ORA) registry. Ann Rheum Dis. 2016;75:1108–13.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Fleischmann RM, Tesser J, Schiff MH, et al. Safety of extended treatment with anakinra in patients with rheumatoid arthritis. Ann Rheum Dis. 2006;65:1006–12.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Galloway JB, Hyrich KL, Mercer LK, et al. The risk of serious infections in patients receiving anakinra for rheumatoid arthritis: results from the British Society for Rheumatology biologics register. Rheumatology (Oxford). 2011;50:1341–2.CrossRefGoogle Scholar
  57. 57.
    Manzi S, Sanchez-Guerrero J, Merrill JT, et al. Effects of belimumab, a B lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two phase III trials. Ann Rheum Dis. 2012;71:1833–8.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Merrill JT, Ginzler EM, Wallace DJ, et al. Long-term safety profile of belimumab plus standard therapy in patients with systemic lupus erythematosus. Arthritis Rheum. 2012;64:3364–73.PubMedCrossRefGoogle Scholar
  59. 59.
    McInnes IB, Kavanaugh A, Gottlieb AB, et al. Efficacy and safety of ustekinumab in patients with active psoriatic arthritis: 1 year results of the phase 3, multicentre, double-blind, placebo-controlled PSUMMIT 1 trial. Lancet. 2013;382:780–9.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Ritchlin C, Rahman P, Kavanaugh A, et al. Efficacy and safety of the anti-IL-12/23 p40 monoclonal antibody, ustekinumab, in patients with active psoriatic arthritis despite conventional non-biological and biological anti-tumour necrosis factor therapy: 6-month and 1-year results of the phase 3, multicentre, double-blind, placebo-controlled, randomised PSUMMIT 2 trial. Ann Rheum Dis. 2014;73:990–9.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Ritchlin CT, Gottlieb AB, Menter A, Mease PJ, Kalia S, Kerdel F, et al. Serious infections in psoriasis patients with psoriatic arthritis in the psoriasis longitudinal assessment and registry study. Arthritis Rheumatol. 2015;67(suppl 10):2084–5.Google Scholar
  62. 62.
    Kavanaugh AF, Geier J, Bingham CO III, Chen C, Reed GW, Saunders KC, et al. Real world results from a post-approval safety surveillance of tofacitinib (Xeljanz): over 3 year results from an ongoing US-based rheumatoid arthritis registry. Arthritis Rheumatol. 2016;68(suppl 10):2595.Google Scholar
  63. 63.
    Greenberg JD, Reed G, Kremer JM, et al. Association of methotrexate and tumour necrosis factor antagonists with risk of infectious outcomes including opportunistic infections in the CORRONA registry. Ann Rheum Dis. 2010;69:380–6.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Richter A, Listing J, Schneider M, et al. Impact of treatment with biologic DMARDs on the risk of sepsis or mortality after serious infection in patients with rheumatoid arthritis. Ann Rheum Dis. 2016;75:1667–73.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Beutler B, Milsark IW, Cerami AC. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science. 1985;229:869–71.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Lanternier F, Tubach F, Ravaud P, et al. Incidence and risk factors of Legionella pneumophila pneumonia during anti-tumor necrosis factor therapy: a prospective French study. Chest. 2013;144:990–8.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Slifman NR, Gershon SK, Lee JH, et al. Listeria monocytogenes infection as a complication of treatment with tumor necrosis factor alpha-neutralizing agents. Arthritis Rheum. 2003;48:319–24.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Winthrop KL, Iseman M. Bedfellows: mycobacteria and rheumatoid arthritis in the era of biologic therapy. Nat Rev Rheumatol. 2013;9:524–31.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Tubach F, Salmon D, Ravaud P, et al. Risk of tuberculosis is higher with anti-tumor necrosis factor monoclonal antibody therapy than with soluble tumor necrosis factor receptor therapy: the three-year prospective French research axed on tolerance of biotherapies registry. Arthritis Rheum. 2009;60:1884–94.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Carmona L, Gomez-Reino JJ, Rodriguez-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.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Wong SH, Gao Q, Tsoi KK, et al. Effect of immunosuppressive therapy on interferon gamma release assay for latent tuberculosis screening in patients with autoimmune diseases: a systematic review and meta-analysis. Thorax. 2016;71:64–72.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Singh JA, Saag KG, Bridges SL Jr, et al. 2015 American college of rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Rheumatol. 2016;68:1–26.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Kleinert S, Tony HP, Krueger K, et al. Screening for latent tuberculosis infection: performance of tuberculin skin test and interferon-gamma release assays under real-life conditions. Ann Rheum Dis. 2012;71:1791–5.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Winthrop KL, Weinblatt ME, Daley CL. You can’t always get what you want, but if you try sometimes (with two tests–TST and IGRA–for tuberculosis) you get what you need. Ann Rheum Dis. 2012;71:1757–60.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Winthrop KL, Baxter R, Liu L, et al. Mycobacterial diseases and antitumour necrosis factor therapy in USA. Ann Rheum Dis. 2013;72:37–42.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Perez-Alvarez R, Diaz-Lagares C, Garcia-Hernandez F, et al. Hepatitis B virus (HBV) reactivation in patients receiving tumor necrosis factor (TNF)-targeted therapy: analysis of 257 cases. Medicine (Baltimore). 2011;90:359–71.CrossRefGoogle Scholar
  77. 77.
    Lan JL, Chen YM, Hsieh TY, et al. Kinetics of viral loads and risk of hepatitis B virus reactivation in hepatitis B core antibody-positive rheumatoid arthritis patients undergoing anti-tumour necrosis factor alpha therapy. Ann Rheum Dis. 2011;70:1719–25.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Ryu HH, Lee EY, Shin K, et al. Hepatitis B virus reactivation in rheumatoid arthritis and ankylosing spondylitis patients treated with anti-TNFalpha agents: a retrospective analysis of 49 cases. Clin Rheumatol. 2012;31(6):931.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Ye H, Zhang XW, Mu R, et al. Anti-TNF therapy in patients with HBV infection–analysis of 87 patients with inflammatory arthritis. Clin Rheumatol. 2014;33:119–23.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Lee YH, Bae SC, Song GG. Hepatitis B virus (HBV) reactivation in rheumatic patients with hepatitis core antigen (HBV occult carriers) undergoing anti-tumor necrosis factor therapy. Clin Exp Rheumatol. 2013;31:118–21.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Fukuda W, Hanyu T, Katayama M, et al. Incidence of hepatitis B virus reactivation in patients with resolved infection on immunosuppressive therapy for rheumatic disease: a multicentre, prospective, observational study in Japan. Ann Rheum Dis. 2017;76(6):1051.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Reddy KR, Beavers KL, Hammond SP, et al. American gastroenterological association institute guideline on the prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy. Gastroenterology. 2015;148:215–9.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Vassilopoulos D, Apostolopoulou A, Hadziyannis E, et al. Long-term safety of anti-TNF treatment in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis. 2010;69:1352–5.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Winthrop KL, Baddley JW, Chen L, et al. Association between the initiation of anti-tumor necrosis factor therapy and the risk of herpes zoster. JAMA. 2013;309:887–95.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Curtis JR, Xie F, Yun H, et al. Real-world comparative risks of herpes virus infections in tofacitinib and biologic-treated patients with rheumatoid arthritis. Ann Rheum Dis. 2016;75:1843–7.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    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.CrossRefGoogle Scholar
  88. 88.
    Stone JH, Merkel PA, Spiera R, et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N Engl J Med. 2010;363:221–32.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Guillevin L, Pagnoux C, Karras A, et al. Rituximab versus azathioprine for maintenance in ANCA-associated vasculitis. N Engl J Med. 2014;371:1771–80.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Salmon JH, Cacoub P, Combe B, et al. Late-onset neutropenia after treatment with rituximab for rheumatoid arthritis and other autoimmune diseases: data from the AutoImmunity and rituximab registry. RMD Open. 2015;1:e000034.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Tesfa D, Ajeganova S, Hagglund H, et al. Late-onset neutropenia following rituximab therapy in rheumatic diseases: association with B lymphocyte depletion and infections. Arthritis Rheum. 2011;63:2209–14.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Abdulkader R, Dharmapalaiah C, Rose G, et al. Late-onset neutropenia in patients with rheumatoid arthritis after treatment with rituximab. J Rheumatol. 2014;41:858–61.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Knight A, Sundstrom Y, Borjesson O, et al. Late-onset neutropenia after rituximab in ANCA-associated vasculitis. Scand J Rheumatol. 2016;45:404–7.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Besada E, Koldingsnes W, Nossent JC. Serum immunoglobulin levels and risk factors for hypogammaglobulinaemia during long-term maintenance therapy with rituximab in patients with granulomatosis with polyangiitis. Rheumatology (Oxford). 2014;53:1818–24.CrossRefGoogle Scholar
  95. 95.
    Roberts DM, Jones RB, Smith RM, et al. Rituximab-associated hypogammaglobulinemia: incidence, predictors and outcomes in patients with multi-system autoimmune disease. J Autoimmun. 2015;57:60–5.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Venhoff N, Niessen L, Kreuzaler M, et al. Reconstitution of the peripheral B lymphocyte compartment in patients with ANCA-associated vasculitides treated with rituximab for relapsing or refractory disease. Autoimmunity. 2014;47:401–8.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Besada E. Risk factors and adverse events poorly predict infections and hypogammaglobulinemia in granulomatosis with polyangiitis patients receiving rituximab. Autoimmune Dis. 2016;2016:8095695.PubMedPubMedCentralGoogle Scholar
  98. 98.
    Reddy V, Martinez L, Isenberg DA, et al. Pragmatic treatment of patients with systemic lupus erythematosus with rituximab: long-term effects on serum immunoglobulins. Arthritis Care Res (Hoboken). 2016;69(6):857–66.CrossRefGoogle Scholar
  99. 99.
    Mitroulis I, Hatzara C, Kandili A, et al. Long-term safety of rituximab in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis. 2013;72:308–10.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Varisco V, Vigano M, Batticciotto A, et al. Low risk of hepatitis B virus reactivation in HBsAg-negative/anti-HBc-positive carriers receiving rituximab for rheumatoid arthritis: a retrospective multicenter Italian study. J Rheumatol. 2016;43:869–74.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Molloy ES, Calabrese CM, Calabrese LH. The risk of progressive multifocal leukoencephalopathy in the biologic era: prevention and management. Rheum Dis Clin North Am. 2017;43:95–109.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Clifford DB, Ances B, Costello C, et al. Rituximab-associated progressive multifocal leukoencephalopathy in rheumatoid arthritis. Arch Neurol. 2011;68:1156–64.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Besada E, Nossent JC. Should Pneumocystis jiroveci prophylaxis be recommended with rituximab treatment in ANCA-associated vasculitis? Clin Rheumatol. 2013;32:1677–81.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Kronbichler A, Jayne DR, Mayer G. Frequency, risk factors and prophylaxis of infection in ANCA-associated vasculitis. Eur J Clin Invest. 2015;45:346–68.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Weinblatt ME, Moreland LW, Westhovens R, et al. Safety of abatacept administered intravenously in treatment of rheumatoid arthritis: integrated analyses of up to 8 years of treatment from the abatacept clinical trial program. J Rheumatol. 2013;40:787–97.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Alten R, Kaine J, Keystone E, et al. Long-term safety of subcutaneous abatacept in rheumatoid arthritis: integrated analysis of clinical trial data representing more than four years of treatment. Arthritis Rheumatol. 2014;66:1987–97.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Bigbee CL, Gonchoroff DG, Vratsanos G, et al. Abatacept treatment does not exacerbate chronic Mycobacterium tuberculosis infection in mice. Arthritis Rheum. 2007;56:2557–65.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Zink A, Manger B, Kaufmann J, et al. Evaluation of the RABBIT risk score for serious infections. Ann Rheum Dis. 2014;73:1673–6.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Moots RJ, Sebba A, Rigby W, et al. Effect of tocilizumab on neutrophils in adult patients with rheumatoid arthritis: pooled analysis of data from phase 3 and 4 clinical trials. Rheumatology (Oxford). 2017;56:541–9.CrossRefGoogle Scholar
  110. 110.
    Strangfeld A, Richter A, Siegmund B, et al. Risk for lower intestinal perforations in patients with rheumatoid arthritis treated with tocilizumab in comparison to treatment with other biologic or conventional synthetic DMARDs. Ann Rheum Dis. 2017;76:504–10.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Lang VR, Englbrecht M, Rech J, et al. Risk of infections in rheumatoid arthritis patients treated with tocilizumab. Rheumatology (Oxford). 2012;51:852–7.CrossRefGoogle Scholar
  112. 112.
    Loricera J, Blanco R, Hernandez JL, et al. Tocilizumab in giant cell arteritis: multicenter open-label study of 22 patients. Semin Arthritis Rheum. 2015;44:717–23.PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Regent A, Redeker S, Deroux A, et al. Tocilizumab in giant cell arteritis: a multicenter retrospective study of 34 patients. J Rheumatol. 2016;43:1547–52.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Villiger PM, Adler S, Kuchen S, et al. Tocilizumab for induction and maintenance of remission in giant cell arteritis: a phase 2, randomised, double-blind, placebo-controlled trial. Lancet. 2016;387:1921–7.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 115.
    Stone JH, Tuckwell K, Dimonaco S, et al. Trial of tocilizumab in giant-cell arteritis. N Engl J Med. 2017;377:317–28.PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Beukelman T, Xie F, Baddley JW, et al. The risk of hospitalized infection following initiation of biologic agents versus methotrexate in the treatment of juvenile idiopathic arthritis. Arthritis Res Ther. 2016;18:210.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Salliot C, Dougados M, Gossec L. Risk of serious infections during rituximab, abatacept and anakinra treatments for rheumatoid arthritis: meta-analyses of randomised placebo-controlled trials. Ann Rheum Dis. 2009;68:25–32.PubMedCrossRefPubMedCentralGoogle Scholar
  118. 118.
    Orrock JE, Ilowite NT. Canakinumab for the treatment of active systemic juvenile idiopathic arthritis. Expert Rev Clin Pharmacol. 2016;9:1015–24.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Ruperto N, Brunner HI, Quartier P, et al. Two randomized trials of canakinumab in systemic juvenile idiopathic arthritis. N Engl J Med. 2012;367:2396–406.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    Fanouriakis A, Boumpas DT, Bertsias GK. Balancing efficacy and toxicity of novel therapies in systemic lupus erythematosus. Expert Rev Clin Pharmacol. 2011;4:437–51.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Navarra SV, Guzman RM, Gallacher AE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet. 2011;377:721–31.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Furie R, Petri M, Zamani O, et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 2011;63:3918–30.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Kalb RE, Fiorentino DF, Lebwohl MG, et al. Risk of serious infection with biologic and systemic treatment of psoriasis: results from the Psoriasis Longitudinal Assessment and Registry (PSOLAR). JAMA Dermatol. 2015;151(9):961.PubMedCrossRefPubMedCentralGoogle Scholar
  124. 124.
    Almirall M, Rodriguez J, Mateo L, et al. Treatment with ustekinumab in a Spanish cohort of patients with psoriasis and psoriatic arthritis in daily clinical practice. Clin Rheumatol. 2017;36:439–43.PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Chiu HY, Chen CH, Wu MS, et al. The safety profile of ustekinumab in the treatment of patients with psoriasis and concurrent hepatitis B or C. Br J Dermatol. 2013;169:1295–303.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    van de Kerkhof PC, Griffiths CE, Reich K, et al. Secukinumab long-term safety experience: a pooled analysis of 10 phase II and III clinical studies in patients with moderate to severe plaque psoriasis. J Am Acad Dermatol. 2016;75:83–98.PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Romani L. Immunity to fungal infections. Nat Rev Immunol. 2011;11:275–88.PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Mease PJ, van der Heijde D, Ritchlin CT, et al. Ixekizumab, an interleukin-17A specific monoclonal antibody, for the treatment of biologic-naive patients with active psoriatic arthritis: results from the 24-week randomised, double-blind, placebo-controlled and active (adalimumab)-controlled period of the phase III trial SPIRIT-P1. Ann Rheum Dis. 2017;76:79–87.PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
    Gordon KB, Blauvelt A, Papp KA, et al. Phase 3 trials of ixekizumab in moderate-to-severe plaque psoriasis. N Engl J Med. 2016;375:345–56.PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Winthrop KL. The emerging safety profile of JAK inhibitors in rheumatic disease. Nat Rev Rheumatol. 2017;13:234–43.PubMedCrossRefPubMedCentralGoogle Scholar
  131. 131.
    Cohen S, Radominski SC, Gomez-Reino JJ, et al. Analysis of infections and all-cause mortality in phase II, phase III, and long-term extension studies of tofacitinib in patients with rheumatoid arthritis. Arthritis Rheumatol. 2014;66:2924–37.PubMedCrossRefPubMedCentralGoogle Scholar
  132. 132.
    Winthrop KL, Yamanaka H, Valdez H, et al. Herpes zoster and tofacitinib therapy in patients with rheumatoid arthritis. Arthritis Rheumatol. 2014;66:2675–84.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  134. 134.
    Sokka T, Abelson B, Pincus T. Mortality in rheumatoid arthritis: 2008 update. Clin Exp Rheumatol. 2008;26:S35–61.PubMedPubMedCentralGoogle Scholar
  135. 135.
    van den Hoek J, Boshuizen HC, Roorda LD, et al. Mortality in patients with rheumatoid arthritis: a 15-year prospective cohort study. Rheumatol Int. 2017;37:487–93.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Hmamouchi I, Winthrop K, Launay O, et al. Low rate of influenza and pneumococcal vaccine coverage in rheumatoid arthritis: data from the international COMORA cohort. Vaccine. 2015;33:1446–52.PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Huang Y, Wang H, Wan L, et al. Is systemic lupus erythematosus associated with a declined immunogenicity and poor safety of influenza vaccination?: a systematic review and meta-analysis. Medicine (Baltimore). 2016;95:e3637.CrossRefGoogle Scholar
  139. 139.
    Del PF, Lagana B, Biselli R, et al. Influenza vaccine administration in patients with systemic lupus erythematosus and rheumatoid arthritis. Safety and immunogenicity. Vaccine. 2006;24:3217–23.CrossRefGoogle Scholar
  140. 140.
    Thomas K, Vassilopoulos D. Immunization in patients with inflammatory rheumatic diseases. Best Pract Res Clin Rheumatol. 2016;30:946–63.PubMedCrossRefGoogle Scholar
  141. 141.
    Yates M, Watts RA, Bajema IM, et al. EULAR/ERA-EDTA recommendations for the management of ANCA-associated vasculitis. Ann Rheum Dis. 2016;75:1583–94.PubMedCrossRefGoogle Scholar
  142. 142.
    Bodro M, Paterson DL. Has the time come for routine trimethoprim-sulfamethoxazole prophylaxis in patients taking biologic therapies? Clin Infect Dis. 2013;56:1621–8.PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    Wissmann G, Morilla R, Martin-Garrido I, et al. Pneumocystis jirovecii colonization in patients treated with infliximab. Eur J Clin Invest. 2011;41:343–8.PubMedCrossRefPubMedCentralGoogle Scholar
  144. 144.
    Ponce CA, Gallo M, Bustamante R, et al. Pneumocystis colonization is highly prevalent in the autopsied lungs of the general population. Clin Infect Dis. 2010;50:347–53.PubMedCrossRefPubMedCentralGoogle Scholar
  145. 145.
    Fritzsche C, Riebold D, Munk-Hartig A, et al. High prevalence of Pneumocystis jirovecii colonization among patients with autoimmune inflammatory diseases and corticosteroid therapy. Scand J Rheumatol. 2012;41:208–13.PubMedCrossRefPubMedCentralGoogle Scholar
  146. 146.
    Mori S, Sugimoto M. Pneumocystis jirovecii infection: an emerging threat to patients with rheumatoid arthritis. Rheumatology (Oxford). 2012;51:2120–30.CrossRefGoogle Scholar
  147. 147.
    Katsuyama T, Saito K, Kubo S, et al. Prophylaxis for pneumocystis pneumonia in patients with rheumatoid arthritis treated with biologics, based on risk factors found in a retrospective study. Arthritis Res Ther. 2014;16:R43.PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Fillatre P, Decaux O, Jouneau S, et al. Incidence of Pneumocystis jirovecii pneumonia among groups at risk in HIV-negative patients. Am J Med. 2014;127:1242–7.PubMedCrossRefPubMedCentralGoogle Scholar
  149. 149.
    Vananuvat P, Suwannalai P, Sungkanuparph S, et al. Primary prophylaxis for Pneumocystis jirovecii pneumonia in patients with connective tissue diseases. Semin Arthritis Rheum. 2011;41:497–502.PubMedCrossRefPubMedCentralGoogle Scholar
  150. 150.
    Liebling M, Rubio E, Ie S. Prophylaxis for Pneumocystis jirovecii pneumonia: is it a necessity in pulmonary patients on high-dose, chronic corticosteroid therapy without AIDS? Expert Rev Respir Med. 2015;9:171–81.PubMedCrossRefPubMedCentralGoogle Scholar
  151. 151.
    Limper AH, Knox KS, Sarosi GA, et al. An official American Thoracic Society statement: treatment of fungal infections in adult pulmonary and critical care patients. Am J Respir Crit Care Med. 2011;183:96–128.PubMedCrossRefPubMedCentralGoogle Scholar
  152. 152.
    Cortazar FB, Pendergraft WF III, Wenger J, et al. Effect of continuous B cell depletion with rituximab on pathogenic autoantibodies and total IgG levels in antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 2017;69:1045–53.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Joint Rheumatology Program, Clinical Immunology-Rheumatology Unit, 2nd Department of Medicine and LaboratoryNational and Kapodistrian University of Athens, School of Medicine, Hippokration General HospitalAthensGreece

Personalised recommendations