Journal List > J Rheum Dis > v.22(5) > 1064210

Lee: Reactivation of Hepatitis B Virus in Patients with Rheumatologic Disease Treated with Biologic Disease Modifying Anti-rheumatic Drugs: Screening and Treatment

Abstract

Reactivation of hepatitis B virus (HBV) is not infrequently reported in patients with rheumatologic diseases treated with biologic disease modify anti-rheumatic drugs (DMARDs) such as a tumor necrosis factor-α inhibitor or a B cell depleting molecule. HBV reactivation is reported not only in patients with chronic hepatitis B but also in cases with resolved HBV where HBsAg is negative and anti-HBc positive. Studies suggest that with treatment using biologic DMARDs, the risk of HBV reactivation increases when HBsAg is positive independent of HBV DNA replication status, and in those with anti-HBc positive and serum HBV DNA positive. Therefore, testing for HBsAg as well as anti-HBc is important before initiating treatment with a biologic DMARD. In addition, evaluation of serum HBV DNA may be required when either HBsAg or anti-HBc turns out to be positive. Although series of reports suggest that prophylactic antiviral therapy in patients with higher risk of HBV reactivation would diminish morbidity and mortality from hepatic cause, solid guidelines pertaining to when to initiate and terminate HBV antiviral therapy and which agent should be used should be provided in the future.

REFERENCES

1. Jang JW. Hepatitis B virus reactivation in patients with hepatocellular carcinoma undergoing anticancer therapy. World J Gastroenterol. 2014; 20:7675–85.
crossref
2. Nard FD, Todoerti M, Grosso V, Monti S, Breda S, Rossi S, et al. Risk of hepatitis B virus reactivation in rheumatoid arthritis patients undergoing biologic treatment: Extending perspective from old to newer drugs. World J Hepatol. 2015; 7:344–61.
crossref
3. Ahn YO. A review study on descriptive epidemiology of HBs antigen positivity in Korea. Korean J Epidemiol. 1982; 4:35–45.
4. Sim JG, Seo JK, Suh SJ. Prevalence and its changes of hepatitis b viral markers from 1988 to 1993 in Korean children. J Korean Pediatr Soc. 1995; 38:1535–9.
5. Ministry of Health & Welfare. Korea health statistics 2011: Korea national health and nutrition examination survey (KNHANESV-2). Seoul: Ministry of Health & Welfare;2012.
6. Lok AS, McMahon BJ. Chronic hepatitis B. Hepatology. 2007; 45:507–39.
crossref
7. Hoofnagle JH, Doo E, Liang TJ, Fleischer R, Lok AS. Management of hepatitis B: summary of a clinical research workshop. Hepatology. 2007; 45:1056–75.
crossref
8. Tran TT. Immune tolerant hepatitis B: a clinical dilemma. Gastroenterol Hepatol (N Y). 2011; 7:511–6.
9. Lok AS, Lai CL. A longitudinal follow-up of asymptomatic hepatitis B surface antigen-positive Chinese children. Hepatology. 1988; 8:1130–3.
crossref
10. Chang MH, Hsu HY, Hsu HC, Ni YH, Chen JS, Chen DS. The significance of spontaneous hepatitis B e antigen seroconversion in childhood: with special emphasis on the clearance of hepatitis B e antigen before 3 years of age. Hepatology. 1995; 22:1387–92.
crossref
11. Hui CK, Leung N, Yuen ST, Zhang HY, Leung KW, Lu L, et al. Hong Kong Liver Fibrosis Study Group. Natural history and disease progression in Chinese chronic hepatitis B patients in immune-tolerant phase. Hepatology. 2007; 46:395–401.
crossref
12. Vierling JM. The immunology of hepatitis B. Clin Liver Dis. 2007; 11:727–59.
crossref
13. Lee PI, Chang MH, Lee CY, Hsu HY, Chen JS, Chen PJ, et al. Changes of serum hepatitis B virus DNA and aminotransferase levels during the course of chronic hepatitis B virus infection in children. Hepatology. 1990; 12:657–60.
crossref
14. Lok AS, Lai CL. Acute exacerbations in Chinese patients with chronic hepatitis B virus (HBV) infection. Incidence, predisposing factors and etiology. J Hepatol. 1990; 10:29–34.
15. McMahon BJ, Holck P, Bulkow L, Snowball M. Serologic and clinical outcomes of 1536 Alaska Natives chronically infected with hepatitis B virus. Ann Intern Med. 2001; 135:759–68.
crossref
16. Tsai SL, Chen PJ, Lai MY, Yang PM, Sung JL, Huang JH, et al. Acute exacerbations of chronic type B hepatitis are accompanied by increased T cell responses to hepatitis B core and e antigens. Implications for hepatitis B e antigen seroconversion. J Clin Invest. 1992; 89:87–96.
crossref
17. Martinot-Peignoux M, Boyer N, Colombat M, Akremi R, Pham BN, Ollivier S, et al. Serum hepatitis B virus DNA levels and liver histology in inactive HBsAg carriers. J Hepatol. 2002; 36:543–6.
crossref
18. Zacharakis GH, Koskinas J, Kotsiou S, Papoutselis M, Tzara F, Vafeiadis N, et al. Natural history of chronic HBV infection: a cohort study with up to 12 years follow-up in North Greece (part of the Interreg I-II/EC-project). J Med Virol. 2005; 77:173–9.
crossref
19. de Franchis R, Meucci G, Vecchi M, Tatarella M, Colombo M, Del Ninno E, et al. The natural history of asymptomatic hepatitis B surface antigen carriers. Ann Intern Med. 1993; 118:191–4.
crossref
20. Chen YC, Sheen IS, Chu CM, Liaw YF. Prognosis following spontaneous HBsAg seroclearance in chronic hepatitis B patients with or without concurrent infection. Gastroenterology. 2002; 123:1084–9.
crossref
21. Lok AS, McMahon BJ. Chronic hepatitis B: update 2009. Hepatology. 2009; 50:661–2.
crossref
22. Okamoto H, Tsuda F, Akahane Y, Sugai Y, Yoshiba M, Moriyama K, et al. Hepatitis B virus with mutations in the core promoter for an e antigen-negative phenotype in carriers with antibody to e antigen. J Virol. 1994; 68:8102–10.
crossref
23. Croagh CM, Bell SJ, Slavin J, Kong YX, Chen RY, Locarnini S, et al. Increasing hepatitis B viral load is associated with risk of significant liver fibrosis in HBeAg-negative but not HBeAg-positive chronic hepatitis B. Liver Int. 2010; 30:1115–22.
crossref
24. Yoo BC, Park JW, Kim HJ, Lee DH, Cha YJ, Park SM. Precore and core promoter mutations of hepatitis B virus and hepatitis B e antigen-negative chronic hepatitis B in Korea. J Hepatol. 2003; 38:98–103.
crossref
25. Gupta S, Govindarajan S, Fong TL, Redeker AG. Spontaneous reactivation in chronic hepatitis B: patterns and natural history. J Clin Gastroenterol. 1990; 12:562–8.
26. Yeo W, Johnson PJ. Diagnosis, prevention and management of hepatitis B virus reactivation during anticancer therapy. Hepatology. 2006; 43:209–20.
crossref
27. Yeo W, Zee B, Zhong S, Chan PK, Wong WL, Ho WM, et al. Comprehensive analysis of risk factors associating with Hepatitis B virus (HBV) reactivation in cancer patients undergoing cytotoxic chemotherapy. Br J Cancer. 2004; 90:1306–11.
crossref
28. Hwang JP, Lok AS. Management of patients with hepatitis B who require immunosuppressive therapy. Nat Rev Gastroenterol Hepatol. 2014; 11:209–19.
crossref
29. Chung SJ, Kim JK, Park MC, Park YB, Lee SK. Reactivation of hepatitis B viral infection in inactive HBsAg carriers following anti-tumor necrosis factor-alpha therapy. J Rheumatol. 2009; 36:2416–20.
30. Kim YJ, Bae SC, Sung YK, Kim TH, Jun JB, Yoo DH, et al. Possible reactivation of potential hepatitis B virus occult infection by tumor necrosis factor-alpha blocker in the treatment of rheumatic diseases. J Rheumatol. 2010; 37:346–50.
31. Lee YH, Bae SC, Song GG. Hepatitis B virus reactivation in HBsAg-positive patients with rheumatic diseases undergoing anti-tumor necrosis factor therapy or DMARDs. Int J Rheum Dis. 2013; 16:527–31.
crossref
32. Pérez-Alvarez R, Díaz-Lagares C, García-Hernández F, Lopez-Roses L, Brito-Zerón P, Pérez-de-Lis M, et al. BIO-GEAS Study Group. Hepatitis B virus (HBV) reactivation in patients receiving tumor necrosis factor (TNF)-targeted therapy: analysis of 257 cases. Medicine (Baltimore). 2011; 90:359–71.
33. Nakamura J, Nagashima T, Nagatani K, Yoshio T, Iwamoto M, Minota S. Reactivation of hepatitis B virus in rheumatoid arthritis patients treated with biological disease-modifying antirheumatic drugs. Int J Rheum Dis. 2014 Apr 4; [Epub].DOI: DOI: 10.1111/1756-185X.12359.
crossref
34. Liu HL, Zhao Z, Yang H, Liu FF, Liu Q, Luo Q, et al. The effects of nucleoside analogue prophylactic treatment on HBV activation in HBcAb+ patients undergoing immunosuppressive therapy. J Viral Hepat. 2013; 20:645–9.
crossref
35. Cheng AL, Hsiung CA, Su IJ, Chen PJ, Chang MC, Tsao CJ, et al. Lymphoma Committee of Taiwan Cooperative Oncology Group. Steroid-free chemotherapy decreases risk of hepatitis B virus (HBV) reactivation in HBV-carriers with lymphoma. Hepatology. 2003; 37:1320–8.
crossref
36. Yeo W, Chan TC, Leung NW, Lam WY, Mo FK, Chu MT, et al. Hepatitis B virus reactivation in lymphoma patients with prior resolved hepatitis B undergoing anticancer therapy with or without rituximab. J Clin Oncol. 2009; 27:605–11.
crossref
37. Kim SJ, Hsu C, Song YQ, Tay K, Hong XN, Cao J, et al. Hepatitis B virus reactivation in B-cell lymphoma patients treated with rituximab: analysis from the Asia Lymphoma Study Group. Eur J Cancer. 2013; 49:3486–96.
crossref
38. Hsu C, Tsou HH, Lin SJ, Wang MC, Yao M, Hwang WL, et al. Taiwan Cooperative Oncology Group. Chemotherapy-induced hepatitis B reactivation in lymphoma patients with resolved HBV infection: a prospective study. Hepatology. 2014; 59:2092–100.
crossref
39. Dong HJ, Ni LN, Sheng GF, Song HL, Xu JZ, Ling Y. Risk of hepatitis B virus (HBV) reactivation in non-Hodgkin lymphoma patients receiving rituximab-chemotherapy: a meta-analysis. J Clin Virol. 2013; 57:209–14.
crossref
40. Chen XQ, Peng JW, Lin GN, Li M, Xia ZJ. The effect of prophylactic lamivudine on hepatitis B virus reactivation in HBsAg-positive patients with diffuse large B-cell lymphoma undergoing prolonged rituximab therapy. Med Oncol. 2012; 29:1237–41.
crossref
41. Pyrpasopoulou A, Douma S, Vassiliadis T, Chatzimichaili-dou S, Triantafyllou A, Aslanidis S. Reactivation of chronic hepatitis B virus infection following rituximab administration for rheumatoid arthritis. Rheumatol Int. 2011; 31:403–4.
crossref
42. Ghrénassia E, Mékinian A, Rouaghe S, Ganne N, Fain O. Reactivation of resolved hepatitis B during rituximab therapy for rheumatoid arthritis. Joint Bone Spine. 2012; 79:100–1.
crossref
43. Gigi E, Georgiou T, Mougiou D, Boura P, Raptopoulou-Gigi M. Hepatitis B reactivation in a patient with rheumatoid arthritis with antibodies to hepatitis B surface antigen treated with rituximab. Hippokratia. 2013; 17:91–3.
44. Droz N, Gilardin L, Cacoub P, Berenbaum F, Wendling D, Godeau B, et al. Kinetic profiles and management of hepatitis B virus reactivation in patients with immunemediated inflammatory diseases. Arthritis Care Res (Hoboken). 2013; 65:1504–14.
crossref
45. Mitroulis I, Hatzara C, Kandili A, Hadziyannis E, Vassilopoulos D. 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.
crossref
46. Germanidis G, Hytiroglou P, Zakalka M, Settas L. Reactivation of occult hepatitis B virus infection, following treatment of refractory rheumatoid arthritis with abatacept. J Hepatol. 2012; 56:1420–1.
crossref
47. Kim PS, Ho GY, Prete PE, Furst DE. Safety and efficacy of abatacept in eight rheumatoid arthritis patients with chronic hepatitis B. Arthritis Care Res (Hoboken). 2012; 64:1265–8.
crossref
48. Kishida D, Okuda Y, Onishi M, Takebayashi M, Matoba K, Jouyama K, et al. Successful tocilizumab treatment in a patient with adult-onset Still's disease complicated by chronic active hepatitis B and amyloid A amyloidosis. Mod Rheumatol. 2011; 21:215–8.
crossref
49. Yeo W, Chan PK, Ho WM, Zee B, Lam KC, Lei KI, et al. Lamivudine for the prevention of hepatitis B virus reactivation in hepatitis B s-antigen seropositive cancer patients undergoing cytotoxic chemotherapy. J Clin Oncol. 2004; 22:927–34.
crossref
50. Rossi G, Pelizzari A, Motta M, Puoti M. Primary prophylaxis with lamivudine of hepatitis B virus reactivation in chronic HbsAg carriers with lymphoid malignancies treated with chemotherapy. Br J Haematol. 2001; 115:58–62.
crossref
51. Lau GK, He ML, Fong DY, Bartholomeusz A, Au WY, Lie AK, et al. Preemptive use of lamivudine reduces hepatitis B exacerbation after allogeneic hematopoietic cell transplantation. Hepatology. 2002; 36:702–9.
crossref
52. Lau GK, Yiu HH, Fong DY, Cheng HC, Au WY, Lai LS, et al. Early is superior to deferred preemptive lamivudine therapy for hepatitis B patients undergoing chemotherapy. Gastroenterology. 2003; 125:1742–9.
crossref
53. Hsu C, Hsiung CA, Su IJ, Hwang WS, Wang MC, Lin SF, et al. A revisit of prophylactic lamivudine for chemotherapy-associated hepatitis B reactivation in non-Hodgkin's lymphoma: a randomized trial. Hepatology. 2008; 47:844–53.
crossref
54. Lan JL, Chen YM, Hsieh TY, Chen YH, Hsieh CW, Chen DY, 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.
crossref
55. Saab S, Dong MH, Joseph TA, Tong MJ. Hepatitis B prophylaxis in patients undergoing chemotherapy for lymphoma: a decision analysis model. Hepatology. 2007; 46:1049–56.
crossref
56. Hui CK, Cheung WW, Au WY, Lie AK, Zhang HY, Yueng YH, et al. Hepatitis B reactivation after withdrawal of preemptive lamivudine in patients with haematological malignancy on completion of cytotoxic chemotherapy. Gut. 2005; 54:1597–603.
crossref
57. Li HR, Huang JJ, Guo HQ, Zhang X, Xie Y, Zhu HL, et al. Comparison of entecavir and lamivudine in preventing hepatitis B reactivation in lymphoma patients during chemotherapy. J Viral Hepat. 2011; 18:877–83.
crossref

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