Italian consensus recommendations for the management of hepatitis C infection in patients with rheumatoid arthritis

References

• Polaris Observatory HCV Collaborators. Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study. Lancet Gastroenterol Hepatol. 2017;2(3):161–76.
   PubMed Web of Science ®Google Scholar
• Alberti A, Lacoin L, Morais E, Lefevre C, Abogunrin S, Iheanacho I. A literature review of the distribution of hepatitis C virus genotypes across Europe. J Med Virol. 2016;88(12):2157–69.
   PubMed Web of Science ®Google Scholar
• Aggiornamento dati registri AIFA DAAs - epatite C cronica. 27 Agosto [Chronic hepatitis C Registry data on Direct Antiviral Agents of Italian Drugs Agency] 2018.
   Google Scholar
• Rossini M, Rossi E, Bernardi D, Viapiana O, Gatti D, Idolazzi L, et al. Prevalence and incidence of rheumatoid arthritis in Italy. Rheumatol Int. 2014;34(5):659–64.
   PubMed Web of Science ®Google Scholar
• Su FH, Wu CS, Sung FC, Chang SN, Su CT, Shieh YH. Chronic hepatitis C virus infection is associated with the development of rheumatoid arthritis: a nationwide population-based study in taiwan. PLoS One. 2016;11(11):e0166508.
   PubMed Web of Science ®Google Scholar
• Dʼamico E, Palazzi C, Fratelli V, Matteo LD, Girolamo GD, Consoli G. High prevalence of hepatitis C virus infection in patients with rheumatoid arthritis. J Clin Rheumatol. 1996;2(4):233.
   PubMedGoogle Scholar
• Hsu FC, Starkebaum G, Boyko EJ, Dominitz JA. Prevalence of rheumatoid arthritis and hepatitis C in those age 60 and older in a US population based study. J Rheumatol. 2003;30(3):455–8.
   PubMed Web of Science ®Google Scholar
• Ferucci ED, Choromanski TL, Varney DT, Ryan HS, Townshend-Bulson LJ, McMahon BJ, Wener MH. Prevalence and correlates of hepatitis C virus-associated inflammatory arthritis in a population-based cohort. Semin Arthritis Rheum. 2017;47(3):445–50.
   PubMed Web of Science ®Google Scholar
• Cacoub P, Renou C, Rosenthal E, Cohen P, Loury I, Loustaud-Ratti V, et al. Extrahepatic manifestations associated with hepatitis C virus infection. A prospective multicenter study of 321 patients. The GERMIVIC. Groupe d'Etude et de Recherche en Medecine Interne et Maladies Infectieuses sur le Virus de l'Hepatite C. Medicine (Baltimore). 2000;79(1):47–56.
   PubMed Web of Science ®Google Scholar
• Kudaeva FM, Speechley MR, Pope JE. A systematic review of viral exposures as a risk for Rheumatoid arthritis. Semin Arthritis Rheum. 2018. doi:10.1016/j.semarthrit.2018.03.011.
   PubMed Web of Science ®Google Scholar
• RAMOS-CASALS MANUEL, MUÑOZ SANDRA, MEDINA FRANCISCO, JARA LUIS-JAVIER, ROSAS JOSÉ, CALVO-ALEN JAIME, et al. Systemic autoimmune diseases in patients with hepatitis C virus infection: characterization of 1020 cases (The HISPAMEC Registry). J Rheumatol. 2009;36(7):1442–8.
   PubMed Web of Science ®Google Scholar
• Patel R, Mikuls TR, Richards JS, Kerr G, Cannon GW, Baker JF. Disease characteristics and treatment patterns in veterans with rheumatoid arthritis and concomitant hepatitis C infection. Arthritis Care Res (Hoboken). 2015;67(4):467–74.
   PubMed Web of Science ®Google Scholar
• Mercer LK, Regierer AC, Mariette X, Dixon WG, Baecklund E, Hellgren K, et al. Spectrum of lymphomas across different drug treatment groups in rheumatoid arthritis: a European registries collaborative project. Ann Rheum Dis. 2017;76(12):2025–30.
   PubMed Web of Science ®Google Scholar
• Ferri C, Sebastiani M, Giuggioli D, Colaci M, Fallahi P, Piluso A, et al. Hepatitis C virus syndrome: a constellation of organ- and non-organ specific autoimmune disorders, B-cell non-Hodgkin's lymphoma, and cancer. World J Hepatol. 2015;7(3):327–43.
   PubMed Web of Science ®Google Scholar
• Varache S, Narbonne V, Jousse-Joulin S, Guennoc X, Dougados M, Daurès JP, et al. Is routine viral screening useful in patients with recent-onset polyarthritis of a duration of at least 6 weeks? Results from a nationwide longitudinal prospective cohort study. Arthritis Care Res (Hoboken). 2011;63(11):1565–70.
   PubMed Web of Science ®Google Scholar
• Ansemant T, Ornetti P, Garrot JF, Pascaud F, Tavernier C, Maillefert JF. Usefulness of routine hepatitis C and hepatitis B serology in the diagnosis of recent-onset arthritis. Systematic prospective screening in all patients seen by the rheumatologists of a defined area–brief report. Joint Bone Spine. 2012;79(3):268–70.
   PubMed Web of Science ®Google Scholar
• Sebastiani M, Giuggioli D, Colaci M, Fallahi P, Gragnani L, Antonelli A, et al. HCV-related rheumatic manifestations and therapeutic strategies. Curr Drug Targets. 2017;18(7):803–10.
   PubMed Web of Science ®Google Scholar
• Cacoub P, Commarmond C, Sadoun D, Desbois AC. Hepatitis C virus infection and rheumatic diseases: the impact of direct-acting antiviral agents. Rheum Dis Clin North Am. 2017;43:123–32.
   PubMed Web of Science ®Google Scholar
• Oxford Centre for Evidence-based Medicine – Levels of Evidence. 2009. Available from: http://www.cebm.net/index.aspx?o=1025 [last accessed 25 Aug 2018).
   Google Scholar
• Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988;31(3):315–24.
   PubMed Web of Science ®Google Scholar
• Aletaha D, Neogi T, Silman A, Funovits J, Felson D, Bingham CO, 3rd, et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism Collaborative Initiative. Arthritis Rheum. 2010;62(9):2569–81.
   PubMed Web of Science ®Google Scholar
• Curtis JR, Beukelman T, Onofrei A, Cassell S, Greenberg JD, Kavanaugh A, et al. Elevated liver enzyme tests among patients with rheumatoid arthritis or psoriatic arthritis treated with methotrexate and/or leflunomide. Ann Rheum Dis. 2010;69(01):43–7.
   PubMed Web of Science ®Google Scholar
• Tilling L, Townsend S, David J. Methotrexate and hepatic toxicity in rheumatoid arthritis and psoriatic arthritis. Clin Drug Investig. 2006;26(2):55–62.
   PubMed Web of Science ®Google Scholar
• Amital H, Arnson Y, Chodick G, Shalev V. Hepatotoxicity rates do not differ in patients with rheumatoid arthritis and psoriasis treated with methotrexate. Rheumatology. 2009;48(9):1107–10.
   PubMed Web of Science ®Google Scholar
• Burton MJ, Curtis JR, Yang S, Chen L, Singh JA, Mikuls TR, et al. Safety of biologic and nonbiologic disease-modifying antirheumatic drug therapy in veterans with rheumatoid arthritis and hepatitis C virus infection. J Rheumatol. 2017;44(5):565–70. May
   PubMed Web of Science ®Google Scholar
• Tang KT, Chen YH, Lin CH, Chen DY. Methotrexate is not associated with increased liver cirrhosis in a population-based cohort of rheumatoid arthritis patients with chronic hepatitis C. Sci Rep. 2016;6:33104.
   PubMed Web of Science ®Google Scholar
• Singh JA, Saag KG, Bridges SL, Jr, Akl EA, Bannuru RR, Sullivan MC, et al. 2015 American College of Rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Rheumatol. 2016;68(1):1–26.
   PubMed Web of Science ®Google Scholar
• Pritchard C. Etanercept and hepatitis C. J Clin Rheumatol. 1999;5(3):179.
   PubMed Web of Science ®Google Scholar
• Brunasso AM, Puntoni M, Gulia A, Massone C. Safety of anti-tumour necrosis factor agents in patients with chronic hepatitis C infection: a systematic review. Rheumatology. 2011;50(9):1700–11.
   PubMed Web of Science ®Google Scholar
• United States FDA. Safety alerts for drugs, biologics medical devices, and dietary supplements. Remicade (infliximab). Washington DC: FDA, 2004. Available from: http://www.fda.gov/Safety/MedWatch/SafetyInformation/SafetyAlertsforHumanMedicalProducts/ucm166901.htm
   Google Scholar
• Iannone F, La Montagna G, Bagnato G, Gremese E, Giardina A, Lapadula G. Safety of etanercept and methotrexate in patients with rheumatoid arthritis and hepatitis C virus infection: a multicenter randomized clinical trial. J Rheumatol. 2014;41(2):286–92.
   PubMed Web of Science ®Google Scholar
• Lin KM, Cheng TT, Lin JC, Chen CJ. Tumor necrosis factor-α antagonist therapy for concomitant rheumatoid arthritis and hepatitis C virus infection: a case series study. Clin Rheumatol. 2015;34(6):1039–46.
   PubMed Web of Science ®Google Scholar
• Pompili M, Biolato M, Miele L, Grieco A. Tumor necrosis factor-a inhibitors and chronic hepatitis C: a comprehensive literature review. World J Gastroenterol. 2013;19(44):7867–73.
   PubMed Web of Science ®Google Scholar
• Chen YM, Chen HH, Chen YH, Hsieh TY, Hsieh CW, Hung WT, et al. A comparison of safety profiles of tumour necrosis factor α inhibitors and rituximab therapy in patients with rheumatoid arthritis and chronic hepatitis C. Ann Rheum Dis. 2015;74(3):626–7.
   PubMed Web of Science ®Google Scholar
• Gandhi NP, Manadan AM, Block JA. Retrospective Study of Patients on Etanercept Therapy for Rheumatic Diseases in Patients With Chronic Hepatitis C Virus. J Clin Rheumatol. 2017;23(5):252–7.
   PubMed Web of Science ®Google Scholar
• Temel T, Cansu DÜ, Korkmaz C, Kaşifoğlu T, Özakyol A. The long-term effects of anti-TNF-a agents on patients with chronic viral hepatitis C and B infections. Int J Rheum Dis 2015;18(1):40–5.
   PubMed Web of Science ®Google Scholar
• Ghavami S, Hashemi M, Kadkhoda K, Alavian SM, Bay GH, Los M. Apoptosis in liver diseases-detection and therapeutic applications. Med Sci Monit. 2005;11(11):RA337–45.
   PubMed Web of Science ®Google Scholar
• Calabrese LH, Zein N, Vassilopoulos D. Safety of antitumour necrosis factor (anti-TNF) therapy in patients with chronic viral infections: hepatitis C, hepatitis B, and HIV infection. Ann Rheum Dis. 2004;63(Suppl 2):ii18.
   PubMedGoogle Scholar
• Tsai SL, Liaw YF, Chen MH, Huang CY, Kuo GC. Detection of type 2-like T-helper cells in hepatitis C virus infection: implications for hepatitis C virus chronicity. Hepatology. 1997;25(2):449–58.
   PubMed Web of Science ®Google Scholar
• Zein NN. Etanercept Study Group. Etanercept as an adjuvant to interferon and ribavirin in treatment naive patients with chronic hepatitis C virus infection: a phase 2 randomized, double-blind, placebo-controlled study. J Hepatol. 2005;42:315–22.
   PubMed Web of Science ®Google Scholar
• Roccatello D, Baldovino S, Rossi D, Giachino O, Mansouri M, Naretto C, et al. Rituximab as a therapeutic tool in severe mixed cryoglobulinemia. Clin Rev Allergy Immunol. 2008;34(1):111–7.
   PubMed Web of Science ®Google Scholar
• Lin KM, Lin JC, Tseng WY, Cheng TT. Rituximab-induced hepatitis C virus reactivation in rheumatoid arthritis. J Microbiol Immunol Infect. 2013;46(1):65–7.
   PubMedGoogle Scholar
• Oldfield V, Dhillon S, Plosker GL. Tocilizumab: a review of its use in the management of rheumatoid arthritis. Drugs 2009;69(5):609–32.
   PubMed Web of Science ®Google Scholar
• Forestier E, Pasquali JL. Long-term safety of tocilizumab treatment on chronic active hepatitis C in a patient with adult onset Still's disease. Joint Bone Spine. 2015;82(2):136–7.
   PubMed Web of Science ®Google Scholar
• Nagashima T, Maruyama A, Kamata Y, Minota S. Unchanged serum viral load and liver function during tocilizumab treatment in a patient with rheumatoid arthritis and hepatitis C virus infection. Rheumatol Int. 2012;32(7):2231–2.
   PubMed Web of Science ®Google Scholar
• Iebba F, Di Sora F, Tarasi A, Leti W, Montella T, Montella F. Case report: safety and efficacy of tocilizumab in a patient with rheumatoid arthritis and chronic hepatitis C. Case Rep Med. 2012;2012:1.
   Google Scholar
• Dragonas C, Ehrenstein B, Fleck M. Tocilizumab treatment in a patient suffering from rheumatoid arthritis and concomitant chronic hepatitis C infection. Rheumatology (Oxford). 2012;51(8):1520–1.
   PubMed Web of Science ®Google Scholar
• Mori S, Fujiyama S. Comment on: tocilizumab treatment in a patient suffering from rheumatoid arthritis and concomitant chronic hepatitis C infection. Rheumatology (Oxford). 2012;51(12):2300–2.
   PubMed Web of Science ®Google Scholar
• Giannitti C, Fineschi I, Frediani B, Fioravanti A, Galeazzi M. Efficacy and safety of tocilizumab combined with cyclosporine A in a patient with rheumatoid arthritis and concomitant chronic hepatitis C virus infection. Clin Exp Rheumatol. 2013;31:816.
   PubMed Web of Science ®Google Scholar
• Nakagawa H, Maeda S, Yoshida H, Tateishi R, Masuzaki R, Ohki T, et al. Serum IL-6 levels and the risk for hepatocarcinogenesis in chronic hepatitis C patients: an analysis based on gender differences. Int J Cancer. 2009;125(10):2264–9.
   PubMed Web of Science ®Google Scholar
• Mahajan TD, Hooker R, Maher L, Brown G, Reimold A. Abatacept therapy for rheumatoid arthritis in the setting of hepatitis C infection. J Clin Rheumatol. 2010;16(7):332–4.
   PubMed Web of Science ®Google Scholar
• Rivellese F, Lobasso A, Barbieri L, Liccardo B, De Paulis A, Rossi FW. Novel therapeutic approaches in rheumatoid arthritis: role of Janus kinases inhibitors. Curr Med Chem. 2018. doi:10.2174/0929867325666180209145243.
   PubMed Web of Science ®Google Scholar
• Turan S, Walker S. Janus kinase inhibitors for the treatment of rheumatoid arthritis. Hosp Pharm. 2017;52(10):667–8. Nov
   PubMedGoogle Scholar
• Boor PPC, de Ruiter PE, Asmawidjaja PS, Lubberts E, van der Laan LJW, Kwekkeboom J. JAK-inhibitor tofacitinib suppresses interferon alfa production by plasmacytoid dendritic cells and inhibits arthrogenic and antiviral effects of interferon alfa. Transl Res. 2017;188:67–79.
   PubMed Web of Science ®Google Scholar
• Giner Galvañ V, Oltra MR, Rueda D, Esteban MJ, Redón J, Severe acute hepatitis related to hydroxychloroquine in a woman with mixed connective tissue disease. Clin Rheumatol. 2007,26:971–2.
   PubMed Web of Science ®Google Scholar
• Ohtani T, Hiroi A, Sakurane M, Furukawa F. Slow acetylator genotypes as a possible risk factor for infectious mononucleosis-like syndrome induced by salazosulfapyridine. Br J Dermatol. 2003;148(5):1035–9.
   PubMed Web of Science ®Google Scholar
• Soejima M, Kawaguchi Y, Hara M, Kamatani N. Prospective study of the association between NAT2 gene haplotypes and severe adverse events with sulfasalazine therapy in patients with rheumatoid arthritis. J Rheumatol. 2008;35(4):724.
   PubMed Web of Science ®Google Scholar
• Jobanputra P, Amarasena R, Maggs F, Homer D, Bowman S, Rankin E, et al. Hepatotoxicity associated with sulfasalazine in inflammatory arthritis: a case series from a local surveillance of serious adverse events. BMC Musculoskelet Disord. 2008;11:48.
   Web of Science ®Google Scholar
• Inoue K, Sekiyama K, Yamada M, Watanabe T, Yasuda H, Yoshiba M. Combined interferon alpha2b and cyclosporin A in the treatment of chronic hepatitis C: controlled trial. J Gastroenterol. 2003;38(6):567–72.
   PubMed Web of Science ®Google Scholar
• Galeazzi M, Bellisai F, Manganelli S, Morozzi G, Sebastiani GD. Cyclosporine A for the treatment of autoimmune disorders in HCV infected patients. Autoimmun Rev. 2006;5(7):493–8.
   PubMed Web of Science ®Google Scholar
• Chandran V, Schentag CT, Gladman DD. Reappraisal of the effectiveness of methotrexate in psoriatic arthritis: results from a longitudinal observational cohort. J Rheumatol. 2008;35(3):469–71.
   PubMed Web of Science ®Google Scholar
• Visser K, van der Heijde DM. Risk and management of liver toxicity during methotrexate treatment in rheumatoid and psoriatic arthritis: a systematic review of the literature. Clin Exp Rheumatol. 2009;27:1017–25.
   PubMed Web of Science ®Google Scholar
• Beyeler C, Reichen J, Thomann SR, Lauterburg BH, Gerber NJ. Quantitative liver function in patients with rheumatoid arthritis treated with low-dose methotrexate: a longitudinal study. Br J Rheumatol. 1997;36(3):338–44.
   PubMedGoogle Scholar
• Salliot C, van der Heijde D. Long-term safety of methotrexate monotherapy in patients with rheumatoid arthritis: a systematic literature research. Ann Rheum Dis. 2009;68(7):1100–4.
   PubMed Web of Science ®Google Scholar
• Sokolove J, Strand V, Greenberg JD, Curtis JR, Kavanaugh A, Kremer JM, et al.; CORRONA Investigators. Risk of elevated liver enzymes associated with TNF inhibitor utilisation in patients with rheumatoid arthritis. Ann Rheum Dis. 2010;69(9):1612–7.
   PubMed Web of Science ®Google Scholar
• Taylor WJ, Korendowych E, Nash P, Helliwell PS, Choy E, Krueger GG, et al. Drug use and toxicity in psoriatic disease: focus on methotrexate. J Rheumatol. 2008;35(7):1454–7.
   PubMed Web of Science ®Google Scholar
• Alcorn N, Saunders S, Madhok R. Benefit-risk assessment of leflunomide: an appraisal of leflunomide in rheumatoid arthritis 10 years after licensing. Drug Saf. 2009;32(12):1123–34.
   PubMed Web of Science ®Google Scholar
• Jazwinski AB, Jezsik J, Ardoin SP, McCallum RM, Tillmann HL. Etanercept treatment to enable successful hepatitis C virus clearance in a patient with rheumatoid arthritis. Gastroenterol Hepatol (N Y). 2011;7:772–4.
   PubMedGoogle Scholar
• Roux CH, Brocq O, Breuil V, Albert C, Euller-Ziegler L. Safety of anti-TNF-alpha therapy in rheumatoid arthritis and spondylarthropathies with concurrent B or C chronic hepatitis. Rheumatology (Oxford). 2006;45(10):1294–7.
   PubMed Web of Science ®Google Scholar
• Fleischmann RM. Safety of biologic therapy in rheumatoid arthritis and other autoimmune diseases: focus on rituximab. Semin Arthritis Rheum. 2009;38(4):265–80.
   PubMed Web of Science ®Google Scholar
• Varisco V, Viganò M, Batticciotto A, Lampertico P, Marchesoni A, Gibertini P, 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(5):869–74.
   PubMed Web of Science ®Google Scholar
• Padovan M, Filippini M, Tincani A, Lanciano E, Bruschi E, Epis O, et al. Safety of abatacept in rheumatoid arthritis with serologic evidence of past or present hepatitis B virus infection. Arthritis Care Res (Hoboken). 2016;68(6):738–43.
   PubMed Web of Science ®Google Scholar
• Cacoub P, Ahmed SN S, Ferfar Y, Pol S, Thabut D, Hezode C, et al. Long-term efficacy of interferon-free antiviral treatment regimens in patients with hepatitis C virus-associated cryoglobulinemia vasculitis. Clin Gastroenterol Hepatol. 2018. doi:10.1016/j.cgh.2018.05.021.
   PubMed Web of Science ®Google Scholar
• Sise ME, Bloom AK, Wisocky J, Lin MV, Gustafson JL, Lundquist AL, et al. Treatment of hepatitis C virus-associated mixed cryoglobulinemia with direct-acting antiviral agents. Hepatology. 2016;63(2):408–17.
   PubMed Web of Science ®Google Scholar
• Bonacci M, Lens S, Mariño Z, Londoño MC, Rodriguez-Tajes S, Sánchez-Tapias JM, et al. Long-term outcomes of patients with HCV-associated cryoglobulinemic vasculitis after virologic cure. Gastroenterology. 2018;155(2):311–5.e6.
   PubMed Web of Science ®Google Scholar
• Sollima S, Milazzo L, Antinori S, Galli M. Direct-acting antivirals and mixed cryoglobulinemia vasculitis: long-term outcome of patients achieving HCV eradication. Am J Gastroenterol. 2017;112(11):1753–4.
   PubMed Web of Science ®Google Scholar