Reactivation of occult hepatitis B virus infection in patients with rheumatic diseases: pathogenesis, risk assessment and prevention

Rheumatology International

Volumn 36, Issue 5, 2016, Pages 635-641

  Kato, Masaru ^a   Atsumi, Tatsuya ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Biologics; Hepatitis B virus reactivation; Immunosuppressive drugs; Occult hepatitis B virus infection; Rheumatic diseases

Indexed keywords

ABATACEPT; ANTIVIRUS AGENT; CIRCULAR DNA; COVALENTLY CLOSED CIRCULAR DNA; CYCLOPHOSPHAMIDE; GLUCOCORTICOID; HEPATITIS B CORE ANTIBODY; HEPATITIS B SURFACE ANTIBODY; HEPATITIS B SURFACE ANTIGEN; METHOTREXATE; RITUXIMAB; TACROLIMUS; TOCILIZUMAB; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR INHIBITOR; UNCLASSIFIED DRUG; USTEKINUMAB; VIRUS DNA; IMMUNOSUPPRESSIVE AGENT;

CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; HEPATITIS B; HUMAN; IMMUNE EVASION; IMMUNOLOGICAL TOLERANCE; INFECTION PREVENTION; INFECTION RISK; MORTALITY; NONHUMAN; PATIENT MONITORING; PRIORITY JOURNAL; PROGNOSIS; REACTIVATED OCCULT HEPATITIS B; RECURRENT VIRUS INFECTION; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATIC DISEASE; RISK ASSESSMENT; SCREENING; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS PATHOGENESIS; VIRUS REACTIVATION; VIRUS REPLICATION; CHEMICALLY INDUCED; DRUG EFFECTS; HEPATITIS B VIRUS; RHEUMATIC DISEASES; VIROLOGY; VIRUS ACTIVATION;

HEPATITIS B; HEPATITIS B VIRUS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; RHEUMATIC DISEASES; RISK ASSESSMENT; VIRUS ACTIVATION;

EID: 84947093611     PISSN: 01728172     EISSN: 1437160X     Source Type: Journal    
DOI: 10.1007/s00296-015-3395-x     Document Type: Review

References (60)

1. Raimondo G, Allain JP, Brunetto MR, Buendia MA, Chen DS, Colombo M, Craxi A, Donato F, Ferrari C, Gaeta GB, Gerlich WH, Levrero M, Locarnini S, Michalak T, Mondelli MU, Pawlotsky JM, Pollicino T, Prati D, Puoti M, Samuel D, Shouval D, Smedile A, Squadrito G, Trepo C, Villa E, Will H, Zanetti AR, Zoulim F (2008) Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 49(4):652–657
2. Feeney SA, McCaughey C, Watt AP, Agnaf MR, McDougall N, Wend UC, Gerlich WH, Coyle PV (2013) Reactivation of occult hepatitis B virus infection following cytotoxic lymphoma therapy in an anti-HBc negative patient. J Med Virol 85(4):597–601
3. Webster A, Brenner MK, Prentice HG, Griffiths PD (1989) Fatal hepatitis B reactivation after autologous bone marrow transplantation. Bone Marrow Transplant 4(2):207–208
4. Dervite I, Hober D, Morel P (2001) Acute hepatitis B in a patient with antibodies to hepatitis B surface antigen who was receiving rituximab. New Engl J Med 344(1):68–69
5. Madonia S, Orlando A, Scimeca D, Olivo M, Rossi F, Cottone M (2007) Occult hepatitis B and infliximab-induced HBV reactivation. Inflamm Bowel Dis 13(4):508–509
6. Charpin C, Guis S, Colson P, Borentain P, Mattei JP, Alcaraz P, Balandraud N, Thomachot B, Roudier J, Gerolami R (2009) Safety of TNF-blocking agents in rheumatic patients with serology suggesting past hepatitis B state: results from a cohort of 21 patients. Arthritis Res Ther 11(6):R179
7. Caporali R, Bobbio-Pallavicini F, Atzeni F, Sakellariou G, Caprioli M, Montecucco C, Sarzi-Puttini P (2010) Safety of tumor necrosis factor alpha blockers in hepatitis B virus occult carriers (hepatitis B surface antigen negative/anti-hepatitis B core antigen positive) with rheumatic diseases. Arthritis Care Res (Hoboken) 62(6):749–754
8. Vassilopoulos D, Apostolopoulou A, Hadziyannis E, Papatheodoridis GV, Manolakopoulos S, Koskinas J, Manesis EK, Archimandritis AI (2010) Long-term safety of anti-TNF treatment in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis 69(7):1352–1355
9. Urata Y, Uesato R, Tanaka D, Kowatari K, Nitobe T, Nakamura Y, Motomura S (2011) Prevalence of reactivation of hepatitis B virus replication in rheumatoid arthritis patients. Mod Rheumatol 21(1):16–23
10. Tamori A, Koike T, Goto H, Wakitani S, Tada M, Morikawa H, Enomoto M, Inaba M, Nakatani T, Hino M, Kawada N (2011) Prospective study of reactivation of hepatitis B virus in patients with rheumatoid arthritis who received immunosuppressive therapy: evaluation of both HBsAg-positive and HBsAg-negative cohorts. J Gastroenterol 46(4):556–564
11. Lan JL, Chen YM, Hsieh TY, Chen YH, Hsieh CW, Chen DY, Yang SS (2011) 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 Rheumatol Dis 70(10):1719–1725
12. Kato M, Atsumi T, Kurita T, Odani T, Fujieda Y, Otomo K, Horita T, Yasuda S, Koike T (2011) Hepatitis B virus reactivation by immunosuppressive therapy in patients with autoimmune diseases: risk analysis in hepatitis B surface antigen-negative cases. J Rheumatol 38(10):2209–2214
13. Mori S (2011) Past hepatitis B virus infection in rheumatoid arthritis patients receiving biological and/or nonbiological disease-modifying antirheumatic drugs. Mod Rheumatol 21(6):621–627
14. Tan J, Zhou J, Zhao P, Wei J (2012) Prospective study of HBV reactivation risk in rheumatoid arthritis patients who received conventional disease-modifying antirheumatic drugs. Clin Rheumatol 31(8):1169–1175
15. Mitroulis I, Hatzara C, Kandili A, Hadziyannis E, Vassilopoulos D (2013) Long-term safety of rituximab in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis 72(2):308–310
16. Nakamura J, Nagashima T, Nagatani K, Yoshio T, Iwamoto M, Minota S (2014) Reactivation of hepatitis B virus in rheumatoid arthritis patients treated with biological disease-modifying antirheumatic drugs. Int J Rheum Dis. doi:10.1111/1756-185X.12359
17. Barone M, Notarnicola A, Lopalco G, Viggiani MT, Sebastiani F, Covelli M, Iannone F, Avolio AW, Di Leo A, Cantarini L, Lapadula G (2015) Safety of long-term biologic therapy in rheumatologic patients with a previously resolved hepatitis B viral infection. Hepatology 62(1):40–46
18. Hui CK, Cheung WW, Zhang HY, Au WY, Yueng YH, Leung AY, Leung N, Luk JM, Lie AK, Kwong YL, Liang R, Lau GK (2006) Kinetics and risk of de novo hepatitis B infection in HBsAg-negative patients undergoing cytotoxic chemotherapy. Gastroenterology 131(1):59–68
19. Umemura T, Tanaka E, Kiyosawa K, Kumada H, Japan de novo Hepatitis BRG (2008) Mortality secondary to fulminant hepatic failure in patients with prior resolution of hepatitis B virus infection in Japan. Clin Infect Dis 47(5):e52–e56
20. Winthrop KL, Calabrese LH (2011) Let the fog be lifted: screening for hepatitis B virus before biological therapy. Ann Rheumatol Dis 70(10):1701–1703
21. Harigai M, Mochida S, Mimura T, Koike T, Miyasaka N (2014) A proposal for management of rheumatic disease patients with hepatitis B virus infection receiving immunosuppressive therapy. Mod Rheumatol 24(1):1–7
22. Stine JG, Khokhar OS, Charalambopoulos J, Shanmugam VK, Lewis JH (2010) Rheumatologists’ awareness of and screening practices for hepatitis B virus infection prior to initiating immunomodulatory therapy. Arthritis Care Res (Hoboken) 62(5):704–711
23. Yuki N, Nagaoka T, Yamashiro M, Mochizuki K, Kaneko A, Yamamoto K, Omura M, Hikiji K, Kato M (2003) Long-term histologic and virologic outcomes of acute self-limited hepatitis B. Hepatology 37(5):1172–1179
24. Lucifora J, Xia Y, Reisinger F, Zhang K, Stadler D, Cheng X, Sprinzl MF, Koppensteiner H, Makowska Z, Volz T, Remouchamps C, Chou WM, Thasler WE, Huser N, Durantel D, Liang TJ, Munk C, Heim MH, Browning JL, Dejardin E, Dandri M, Schindler M, Heikenwalder M, Protzer U (2014) Specific and nonhepatotoxic degradation of nuclear hepatitis B virus cccDNA. Science 343(6176):1221–1228
25. Isogawa M, Robek MD, Furuichi Y, Chisari FV (2005) Toll-like receptor signaling inhibits hepatitis B virus replication in vivo. J Virol 79(11):7269–7272
26. Kamatani Y, Wattanapokayakit S, Ochi H, Kawaguchi T, Takahashi A, Hosono N, Kubo M, Tsunoda T, Kamatani N, Kumada H, Puseenam A, Sura T, Daigo Y, Chayama K, Chantratita W, Nakamura Y, Matsuda K (2009) A genome-wide association study identifies variants in the HLA-DP locus associated with chronic hepatitis B in Asians. Nat Genet 41(5):591–595
27. Thimme R, Wieland S, Steiger C, Ghrayeb J, Reimann KA, Purcell RH, Chisari FV (2003) CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 77(1):68–76
28. Wu J, Meng Z, Jiang M, Pei R, Trippler M, Broering R, Bucchi A, Sowa JP, Dittmer U, Yang D, Roggendorf M, Gerken G, Lu M, Schlaak JF (2009) Hepatitis B virus suppresses toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells. Hepatology 49(4):1132–1140
29. Boni C, Fisicaro P, Valdatta C, Amadei B, Di Vincenzo P, Giuberti T, Laccabue D, Zerbini A, Cavalli A, Missale G, Bertoletti A, Ferrari C (2007) Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J Virol 81(8):4215–4225
30. van der Molen RG, Sprengers D, Binda RS, de Jong EC, Niesters HG, Kusters JG, Kwekkeboom J, Janssen HL (2004) Functional impairment of myeloid and plasmacytoid dendritic cells of patients with chronic hepatitis B. Hepatology 40(3):738–746
31. Xu D, Fu J, Jin L, Zhang H, Zhou C, Zou Z, Zhao JM, Zhang B, Shi M, Ding X, Tang Z, Fu YX, Wang FS (2006) Circulating and liver resident CD4+ CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B. J Immunol 177(1):739–747
32. Droz N, Gilardin L, Cacoub P, Berenbaum F, Wendling D, Godeau B, Piette AM, Dernis E, Ebbo M, Fautrel B, Le Guenno G, Mekinian A, Bernard-Chabert B, Costedoat-Chalumeau N, Descloux E, Michot JM, Radenne S, Rigolet A, Riviere S, Yvin JL, Thibault V, Thabut D, Pol S, Guillevin L, Mouthon L, Terrier B (2013) Kinetic profiles and management of hepatitis B virus reactivation in patients with immune-mediated inflammatory diseases. Arthritis Care Res (Hoboken) 65(9):1504–1514
33. Oshima Y, Tsukamoto H, Tojo A (2013) Association of hepatitis B with antirheumatic drugs: a case–control study. Mod Rheumatol 23(4):694–704
34. Reddy KR, Beavers KL, Hammond SP, Lim JK, Falck-Ytter YT, American Gastroenterological Association I (2015) American Gastroenterological Association Institute guideline on the prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy. Gastroenterology 148(1):215–219
35. Pei SN, Ma MC, Wang MC, Kuo CY, Rau KM, Su CY, Chen CH (2012) Analysis of hepatitis B surface antibody titers in B cell lymphoma patients after rituximab therapy. Ann Hematol 91(7):1007–1012
36. Tur-Kaspa R, Burk RD, Shaul Y, Shafritz DA (1986) Hepatitis B virus DNA contains a glucocorticoid-responsive element. Proc Natl Acad Sci USA 83(6):1627–1631
37. Cheng J, Li JB, Sun QL, Li X (2011) Reactivation of hepatitis B virus after steroid treatment in rheumatic diseases. J Rheumatol 38(1):181–182
38. Gwak GY, Koh KC, Kim HY (2007) Fatal hepatic failure associated with hepatitis B virus reactivation in a hepatitis B surface antigen-negative patient with rheumatoid arthritis receiving low dose methotrexate. Clin Exp Rheumatol 25(6):888–889
39. Watanabe K, Takase K, Ohno S, Ideguchi H, Nozaki A, Ishigatsubo Y (2012) Reactivation of hepatitis B virus in a hepatitis B surface antigen-negative patient with rheumatoid arthritis treated with methotrexate. Mod Rheumatol 22(3):470–473
40. Flowers MA, Heathcote J, Wanless IR, Sherman M, Reynolds WJ, Cameron RG, Levy GA, Inman RD (1990) Fulminant hepatitis as a consequence of reactivation of hepatitis B virus infection after discontinuation of low-dose methotrexate therapy. Ann Intern Med 112(5):381–382
41. Ito S, Nakazono K, Murasawa A, Mita Y, Hata K, Saito N, Kikuchi M, Yoshida K, Nakano M, Gejyo F (2001) Development of fulminant hepatitis B (precore variant mutant type) after the discontinuation of low-dose methotrexate therapy in a rheumatoid arthritis patient. Arthritis Rheumatol 44(2):339–342
42. Hagiyama H, Kubota T, Komano Y, Kurosaki M, Watanabe M, Miyasaka N (2004) Fulminant hepatitis in an asymptomatic chronic carrier of hepatitis B virus mutant after withdrawal of low-dose methotrexate therapy for rheumatoid arthritis. Clin Exp Rheumatol 22(3):375–376
43. Perez-Alvarez R, Diaz-Lagares C, Garcia-Hernandez F, Lopez-Roses L, Brito-Zeron P, Perez-de-Lis M, Retamozo S, Bove A, Bosch X, Sanchez-Tapias JM, Forns X, Ramos-Casals M, Group BS (2011) Hepatitis B virus (HBV) reactivation in patients receiving tumor necrosis factor (TNF)-targeted therapy: analysis of 257 cases. Medicine (Baltimore) 90(6):359–371
44. Matsumoto T, Marusawa H, Dogaki M, Suginoshita Y, Inokuma T (2010) Adalimumab-induced lethal hepatitis B virus reactivation in an HBsAg-negative patient with clinically resolved hepatitis B virus infection. Liver Int 30(8):1241–1242
45. Kasahara S, Ando K, Saito K, Sekikawa K, Ito H, Ishikawa T, Ohnishi H, Seishima M, Kakumu S, Moriwaki H (2003) Lack of tumor necrosis factor alpha induces impaired proliferation of hepatitis B virus-specific cytotoxic T lymphocytes. J Virol 77(4):2469–2476
46. Anolik JH, Ravikumar R, Barnard J, Owen T, Almudevar A, Milner EC, Miller CH, Dutcher PO, Hadley JA, Sanz I (2008) Cutting edge: anti-tumor necrosis factor therapy in rheumatoid arthritis inhibits memory B lymphocytes via effects on lymphoid germinal centers and follicular dendritic cell networks. J Immunol 180(2):688–692
47. Westhoff TH, Jochimsen F, Schmittel A, Stoffler-Meilicke M, Schafer JH, Zidek W, Gerlich WH, Thiel E (2003) Fatal hepatitis B virus reactivation by an escape mutant following rituximab therapy. Blood 102(5):1930
48. Skrabs C, Muller C, Agis H, Mannhalter C, Jager U (2002) Treatment of HBV-carrying lymphoma patients with Rituximab and CHOP: a diagnostic and therapeutic challenge. Leukemia 16(9):1884–1886
49. Hernandez JA, Diloy R, Salat D, del Rio N, Martinez X, Castellvi JM (2003) Fulminant hepatitis subsequent to reactivation of precore mutant hepatitis B virus in a patient with lymphoma treated with chemotherapy and rituximab. Haematologica 88 (6):ECR22
50. Zell JA, Yoon EJ, Ignatius Ou SH, Hoefs JC, Chang JC (2005) Precore mutant hepatitis B reactivation after treatment with CHOP-rituximab. Anticancer Drugs 16(1):83–85
51. Germanidis G, Hytiroglou P, Zakalka M, Settas L (2012) Reactivation of occult hepatitis B virus infection, following treatment of refractory rheumatoid arthritis with abatacept. J Hepatol 56(6):1420–1421
52. Fanouriakis A, Vassilopoulos D, Repa A, Boumpas DT, Sidiropoulos P (2014) Hepatitis B reactivation following treatment with abatacept in a patient with past hepatitis B virus infection. Rheumatology (Oxford) 53(1):195–196
53. Kim PS, Ho GY, Prete PE, Furst DE (2012) Safety and efficacy of abatacept in eight rheumatoid arthritis patients with chronic hepatitis B. Arthritis Care Res (Hoboken) 64(8):1265–1268
54. Thio CL, Mosbruger TL, Kaslow RA, Karp CL, Strathdee SA, Vlahov D, O’Brien SJ, Astemborski J, Thomas DL (2004) Cytotoxic T-lymphocyte antigen 4 gene and recovery from hepatitis B virus infection. J Virol 78(20):11258–11262
55. Nagashima T, Minota S (2008) Long-term tocilizumab therapy in a patient with rheumatoid arthritis and chronic hepatitis B. Rheumatology (Oxford) 47(12):1838–1840
56. Koskinas J, Tampaki M, Doumba PP, Rallis E (2013) Hepatitis B virus reactivation during therapy with ustekinumab for psoriasis in a hepatitis B surface-antigen-negative anti-HBs-positive patient. Br J Dermatol 168(3):679–680
57. Chiu HY, Chen CH, Wu MS, Cheng YP, Tsai TF (2013) The safety profile of ustekinumab in the treatment of patients with psoriasis and concurrent hepatitis B or C. Br J Dermatol 169(6):1295–1303
58. Gong ZJ, De Meyer S, Clarysse C, Verslype C, Neyts J, De Clercq E, Yap SH (1999) Mycophenolic acid, an immunosuppressive agent, inhibits HBV replication in vitro. J Viral Hepat 6(3):229–236
59. Huang H, Li X, Zhu J, Ye S, Zhang H, Wang W, Wu X, Peng J, Xu B, Lin Y, Cao Y, Li H, Lin S, Liu Q, Lin T (2014) Entecavir vs lamivudine for prevention of hepatitis B virus reactivation among patients with untreated diffuse large B-cell lymphoma receiving R-CHOP chemotherapy: a randomized clinical trial. JAMA 312(23):2521–2530
60. Cheng AL, Hsiung CA, Su IJ, Chen PJ, Chang MC, Tsao CJ, Kao WY, Uen WC, Hsu CH, Tien HF, Chao TY, Chen LT, Whang-Peng J, Lymphoma Committee of Taiwan Cooperative Oncology Group (2003) Steroid-free chemotherapy decreases risk of hepatitis B virus (HBV) reactivation in HBV-carriers with lymphoma. Hepatology 37(6):1320–1328