Hepatitis B virus reactivation during immunosuppressive therapy: Appropriate risk stratification

World Journal of Hepatology

Volumn 7, Issue 6, 2015, Pages 825-830

  Seto, Wai Kay ^a,b,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b THE UNIVERSITY OF HONG KONG SHENZHEN HOSPITAL   (China)

^c THE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Antibody to hepatitis B core antigen; Antibody to tumor necrosis factor; Antigen CD20; Hematopoietic stem cell transplantation; Hepatitis B surface antigen; Hepatitis B virus; Occult; Rituximab

Indexed keywords

EID: 84928941488     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v7.i6.825     Document Type: Article

References (46)

1. Yuen MF, Seto WK, Fung J, Wong DK, Yuen JC, Lai CL. Three years of continuous entecavir therapy in treatment-naïve chronic hepatitis B patients: VIRAL suppression, viral resistance, and clinical safety. Am J Gastroenterol 2011; 106: 1264-1271 [PMID: 21364549 DOI: 10.1038/ajg.2011.45]
2. Marcellin P, Gane E, Buti M, Afdhal N, Sievert W, Jacobson IM, Washington MK, Germanidis G, Flaherty JF, Schall RA, Bornstein JD, Kitrinos KM, Subramanian GM, McHutchison JG, Heathcote EJ. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet 2013; 381: 468-475 [PMID: 23234725 DOI: 10.1016/S0140-6736(12)61425-1]
3. Chang TT, Liaw YF, Wu SS, Schiff E, Han KH, Lai CL, Safadi R, Lee SS, Halota W, Goodman Z, Chi YC, Zhang H, Hindes R, Iloeje U, Beebe S, Kreter B. Long-term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology 2010; 52: 886-893 [PMID: 20683932 DOI: 10.1002/hep.23785]
4. Yuen MF, Seto WK, Chow DH, Tsui K, Wong DK, Ngai VW, Wong BC, Fung J, Yuen JC, Lai CL. Long-term lamivudine therapy reduces the risk of long-term complications of chronic hepatitis B infection even in patients without advanced disease. Antivir Ther 2007; 12: 1295-1303 [PMID: 18240869]
5. Wong GL, Chan HL, Mak CW, Lee SK, Ip ZM, Lam AT, Iu HW, Leung JM, Lai JW, Lo AO, Chan HY, Wong VW. Entecavir treatment reduces hepatic events and deaths in chronic hepatitis B patients with liver cirrhosis. Hepatology 2013; 58: 1537-1547 [PMID: 23389810 DOI: 10.1002/hep.26301]
6. Tenney DJ, Rose RE, Baldick CJ, Pokornowski KA, Eggers BJ, Fang J, Wichroski MJ, Xu D, Yang J, Wilber RB, Colonno RJ. Long-term monitoring shows hepatitis B virus resistance to entecavir in nucleoside-naïve patients is rare through 5 years of therapy. Hepatology 2009; 49: 1503-1514 [PMID: 19280622 DOI: 10.1002/hep.22841]
7. Kitrinos KM, Corsa A, Liu Y, Flaherty J, Snow-Lampart A, Marcellin P, Borroto-Esoda K, Miller MD. No detectable resistance to tenofovir disoproxil fumarate after 6 years of therapy in patients with chronic hepatitis B. Hepatology 2014; 59: 434-442 [PMID: 23939953 DOI: 10.1002/hep.26686]
8. Seto WK, Lai CL, Yuen MF. Acute-on-chronic liver failure in chronic hepatitis B. J Gastroenterol Hepatol 2012; 27: 662-669 [PMID: 22098452 DOI: 10.1111/j.1440-1746.2011.06971.x]
9. Cui YL, Yan F, Wang YB, Song XQ, Liu L, Lei XZ, Zheng MH, Tang H, Feng P. Nucleoside analogue can improve the long-term prognosis of patients with hepatitis B virus infection-associated acute on chronic liver failure. Dig Dis Sci 2010; 55: 2373-2380 [PMID: 20512414 DOI: 10.1007/s10620-010-1257-7]
10. Garg H, Sarin SK, Kumar M, Garg V, Sharma BC, Kumar A. Tenofovir improves the outcome in patients with spontaneous reactivation of hepatitis B presenting as acute-on-chronic liver failure. Hepatology 2011; 53: 774-780 [PMID: 21294143 DOI: 10.1002/hep.24109]
11. Tan D, Tan SY, Lim ST, Kim SJ, Kim WS, Advani R, Kwong YL. Management of B-cell non-Hodgkin lymphoma in Asia: resourcestratified guidelines. Lancet Oncol 2013; 14: e548-e561 [PMID: 24176573]
12. Artz AS, Somerfield MR, Feld JJ, Giusti AF, Kramer BS, Sabichi AL, Zon RT, Wong SL. American Society of Clinical Oncology provisional clinical opinion: chronic hepatitis B virus infection screening in patients receiving cytotoxic chemotherapy for treatment of malignant diseases. J Clin Oncol 2010; 28: 3199-3202 [PMID: 20516452 DOI: 10.1200/JCO.2010.30.0673]
13. 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. Steroid-free chemotherapy decreases risk of hepatitis B virus (HBV) reactivation in HBV-carriers with lymphoma. Hepatology 2003; 37: 1320-1328 [PMID: 12774010 DOI: 10.1053/ jhep.2003.50220]
14. Lai CL, Yuen MF. Systemic corticosteroid and reactivation of chronic hepatitis B. Respirology 2010; 15: 1017-1018 [PMID: 20874743 DOI: 10.1111/j.1440-1843.2010.01822.x]
15. Evens AM, Jovanovic BD, Su YC, Raisch DW, Ganger D, Belknap SM, Dai MS, Chiu BC, Fintel B, Cheng Y, Chuang SS, Lee MY, Chen TY, Lin SF, Kuo CY. Rituximab-associated hepatitis B virus (HBV) reactivation in lymphoproliferative diseases: metaanalysis and examination of FDA safety reports. Ann Oncol 2011; 22: 1170-1180 [PMID: 21115603 DOI: 10.1093/annonc/mdq583]
16. Seto WK, Chan TS, Hwang YY, Wong DK, Fung J, Liu KS, Gill H, Lam YF, Lie AK, Lai CL, Kwong YL, Yuen MF. Hepatitis B reactivation in patients with previous hepatitis B virus exposure undergoing rituximab-containing chemotherapy for lymphoma: a prospective study. J Clin Oncol 2014; 32: 3736-3743 [PMID: 25287829 DOI: 10.1200/JCO.2014.56.7081]
17. Yeo W, Chan TC, Leung NW, Lam WY, Mo FK, Chu MT, Chan HL, Hui EP, Lei KI, Mok TS, Chan PK. Hepatitis B virus reactivation in lymphoma patients with prior resolved hepatitis B undergoing anticancer therapy with or without rituximab. J Clin Oncol 2009; 27: 605-611 [PMID: 19075267 DOI: 10.1200/ JCO.2008.18.0182]
18. Pérez-Alvarez R, Díaz-Lagares C, García-Hernández F, Lopez-Roses L, Brito-Zerón P, Pérez-de-Lis M, Retamozo S, Bové A, Bosch X, Sanchez-Tapias JM, Forns X, Ramos-Casals M. Hepatitis B virus (HBV) reactivation in patients receiving tumor necrosis factor (TNF)-targeted therapy: analysis of 257 cases. Medicine (Baltimore) 2011; 90: 359-371 [PMID: 22033451 DOI: 10.1097/ MD.0b013e3182380a76]
19. Jang JW, Choi JY, Bae SH, Kim CW, Yoon SK, Cho SH, Yang JM, Ahn BM, Lee CD, Lee YS, Chung KW, Sun HS. Transarterial chemo-lipiodolization can reactivate hepatitis B virus replication in patients with hepatocellular carcinoma. J Hepatol 2004; 41: 427-435 [PMID: 15336446 DOI: 10.1016/j.jhep.2004.05.014]
20. Locasciulli A, Bruno B, Alessandrino EP, Meloni G, Arcese W, Bandini G, Cassibba V, Rotoli B, Morra E, Majolino I, Alberti A, Bacigalupo A. Hepatitis reactivation and liver failure in haemopoietic stem cell transplants for hepatitis B virus (HBV)/ hepatitis C virus (HCV) positive recipients: a retrospective study by the Italian group for blood and marrow transplantation. Bone Marrow Transplant 2003; 31: 295-300 [PMID: 12621466 DOI: 10.1038/sj.bmt.1703826]
21. Tamori A, Koike T, Goto H, Wakitani S, Tada M, Morikawa H, Enomoto M, Inaba M, Nakatani T, Hino M, Kawada N. 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 2011; 46: 556-564 [PMID: 21246383 DOI: 10.1007/s00535-010-0367-5]
22. Ling WH, Soe PP, Pang AS, Lee SC. Hepatitis B virus reactivation risk varies with different chemotherapy regimens commonly used in solid tumours. Br J Cancer 2013; 108: 1931-1935 [PMID: 23652302 DOI: 10.1038/bjc.2013.225]
23. Lai GM, Yan SL, Chang CS, Tsai CY. Hepatitis B reactivation in chronic myeloid leukemia patients receiving tyrosine kinase inhibitor. World J Gastroenterol 2013; 19: 1318-1321 [PMID: 23483799 DOI: 10.3748/wjg.v19.i8.1318]
24. Navarro R, Vilarrasa E, Herranz P, Puig L, Bordas X, Carrascosa JM, Taberner R, Ferrán M, García-Bustinduy M, Romero-Maté A, Pedragosa R, García-Diez A, Daudén E. Safety and effectiveness of ustekinumab and antitumour necrosis factor therapy in patients with psoriasis and chronic viral hepatitis B or C: a retrospective, multicentre study in a clinical setting. Br J Dermatol 2013; 168: 609-616 [PMID: 22985451 DOI: 10.1111/bjd.12045]
25. Raimondo G, Pollicino T, Cacciola I, Squadrito G. Occult hepatitis B virus infection. J Hepatol 2007; 46: 160-170 [PMID: 17112622 DOI: 10.1016/j.jhep.2006.10.007]
26. Yuen MF, Wong DK, Fung J, Ip P, But D, Hung I, Lau K, Yuen JC, Lai CL. HBsAg Seroclearance in chronic hepatitis B in Asian patients: replicative level and risk of hepatocellular carcinoma. Gastroenterology 2008; 135: 1192-1199 [PMID: 18722377 DOI: 10.1053/j.gastro.2008.07.008]
27. Matsue K, Kimura S, Takanashi Y, Iwama K, Fujiwara H, Yamakura M, Takeuchi M. Reactivation of hepatitis B virus after rituximab-containing treatment in patients with CD20-positive B-cell lymphoma. Cancer 2010; 116: 4769-4776 [PMID: 20597091 DOI: 10.1002/cncr.25253]
28. Kim SJ, Hsu C, Song YQ, Tay K, Hong XN, Cao J, Kim JS, Eom HS, Lee JH, Zhu J, Chang KM, Reksodiputro AH, Tan D, Goh YT, Lee J, Intragumtornchai T, Chng WJ, Cheng AL, Lim ST, Suh C, Kwong YL, Kim WS. Hepatitis B virus reactivation in B-cell lymphoma patients treated with rituximab: analysis from the Asia Lymphoma Study Group. Eur J Cancer 2013; 49: 3486-3496 [PMID: 23910494 DOI: 10.1016/j.ejca.2013.07.006]
29. Hsu C, Tsou HH, Lin SJ, Wang MC, Yao M, Hwang WL, Kao WY, Chiu CF, Lin SF, Lin J, Chang CS, Tien HF, Liu TW, Chen PJ, Cheng AL. Chemotherapy-induced hepatitis B reactivation in lymphoma patients with resolved HBV infection: a prospective study. Hepatology 2014; 59: 2092-2100 [PMID: 24002804 DOI: 10.1002/hep.26718]
30. Hammond SP, Borchelt AM, Ukomadu C, Ho VT, Baden LR, Marty FM. Hepatitis B virus reactivation following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2009; 15: 1049-1059 [PMID: 19660717 DOI: 10.1016/ j.bbmt.2009.05.001]
31. Ceneli O, Ozkurt ZN, Acar K, Rota S, Aki SZ, Yeğin ZA, Yağci M, Ozenirler S, Sucak GT. Hepatitis B-related events in autologous hematopoietic stem cell transplantation recipients. World J Gastroenterol 2010; 16: 1765-1771 [PMID: 20380010 DOI: 10.3748/ wjg.v16.i14.1765]
32. Viganò M, Vener C, Lampertico P, Annaloro C, Pichoud C, Zoulim F, Facchetti F, Poli F, Scalamogna M, Deliliers GL, Colombo M. Risk of hepatitis B surface antigen seroreversion after allogeneic hematopoietic SCT. Bone Marrow Transplant 2011; 46: 125-131 [PMID: 20383209 DOI: 10.1038/bmt.2010.70]
33. Seto WK, Chan TS, Hwang YY, Choi O, Wong DK, Fung J, Lie AK, Lai CL, Kwong YL, Yuen MF. Interim analysis of hepatitis B reactivation in patients with prior HBV exposure undergoing hematopoietic stem cell transplant: a prospective study (abstract). Hepatology 2013; 58 (S1): 650A [DOI: 10.1002/hep.26727]
34. 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: 118-121 [PMID: 23111095]
35. Peng JW, Lin GN, Xiao JJ, Jiang XM. Hepatitis B virus reactivation in hepatocellular carcinoma patients undergoing transcatheter arterial chemoembolization therapy. Asia Pac J Clin Oncol 2012; 8: 356-361 [PMID: 22897940 DOI: 10.1111/j.1743-7563.2012.01534.x]
36. European Association For The Study Of The Liver. EASL clinical practice guidelines: Management of chronic hepatitis B virus infection. J Hepatol 2012; 57: 167-185 [PMID: 22436845]
37. Lok AS, McMahon BJ. Chronic hepatitis B: update 2009. Hepatology 2009; 50: 661-662 [PMID: 19714720 DOI: 10.1002/ hep.23190]
38. Zurawska U, Hicks LK, Woo G, Bell CM, Krahn M, Chan KK, Feld JJ. Hepatitis B virus screening before chemotherapy for lymphoma: a cost-effectiveness analysis. J Clin Oncol 2012; 30: 3167-3173 [PMID: 22711851 DOI: 10.1200/JCO.2011.40.7510]
39. Yeo W, Chan PK, Ho WM, Zee B, Lam KC, Lei KI, Chan AT, Mok TS, Lee JJ, Leung TW, Zhong S, Johnson PJ. 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: 927-934 [PMID: 14990649 DOI: 10.1200/JCO.2004.05.161]
40. Loomba R, Rowley A, Wesley R, Liang TJ, Hoofnagle JH, Pucino F, Csako G. Systematic review: the effect of preventive lamivudine on hepatitis B reactivation during chemotherapy. Ann Intern Med 2008; 148: 519-528 [PMID: 18378948 DOI: 10.7326/0003-4819-148-7-200804010-00008]
41. 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. 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 2014; 312: 2521-2530 [PMID: 25514302 DOI: 10.1001/jama.2014.15704]
42. Chen CJ, Yang HI, Su J, Jen CL, You SL, Lu SN, Huang GT, Iloeje UH. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 2006; 295: 65-73 [PMID: 16391218 DOI: 10.1001/jama.295.1.65]
43. Iloeje UH, Yang HI, Su J, Jen CL, You SL, Chen CJ. Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology 2006; 130: 678-686 [PMID: 16530509 DOI: 10.1053/j.gastro.2005.11.016]
44. Huang YH, Hsiao LT, Hong YC, Chiou TJ, Yu YB, Gau JP, Liu CY, Yang MH, Tzeng CH, Lee PC, Lin HC, Lee SD. Randomized controlled trial of entecavir prophylaxis for rituximab-associated hepatitis B virus reactivation in patients with lymphoma and resolved hepatitis B. J Clin Oncol 2013; 31: 2765-2772 [PMID: 23775967 DOI: 10.1200/JCO.2012.48.5938]
45. Shen LP, Zhang Y, Wang F, Zhang S, Yang JY, Fang KX, Yu T, Wang XY, Zhang WY, Bi SL. Epidemiological changes in hepatitis B prevalence in an entire population after 20 years of the universal HBV vaccination programme. Epidemiol Infect 2011; 139: 1159-1165 [PMID: 21156099 DOI: 10.1017/S0950268810002827]
46. Zhang H, Li Q, Sun J, Wang C, Gu Q, Feng X, Du B, Wang W, Shi X, Zhang S, Li W, Jiang Y, Feng J, He S, Niu J. Seroprevalence and risk factors for hepatitis B infection in an adult population in Northeast China. Int J Med Sci 2011; 8: 321-331 [PMID: 21611114 DOI: 10.7150/ijms.8.321]