Screening of Hepatitis B Virus Infection before Chemotherapy for Patients with Lymphoma_West China Medical Journal

Authors：

 MAOYin-yan , DENGYao-tiao ,  JIANGMing

Department of Oncology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

JIANGMing, Email: 307048372@qq.com

Keywords：

Lymphoma; Hepatitis B virus; Chemotherapy; Reactivation

DOI：

10.7507/1002-0179.20150130

Video：

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Objective To analyze the influencing factors for hepatitis B virus (HBV) infection screening in lymphoma patients prior to chemotherapy with a focus on HBV reactivation after chemotherapy. Methods The HBV infection screening data of 449 patients with lymphoma treated by chemotherapy between June 2010 and July 2012 were analyzed retrospectively. Results Among the 449 patients, 387 (86.2%) were screened for HBV before initiation of chemotherapy, and patients with elevated aminotransferase levels were more likely to receive pre-chemotherapy HBV testing (OR=2.509, P=0.040). HBV reactivation was observed in 16.1% (9/56) of the HBsAg-positive patients after chemotherapy, and it was more likely to occur in patients with the use of rituximab (29.2% vs. 6.3%; P=0.030). Prophylactic antiviral therapy can significantly reduce the incidence of chemotherapy-induced HBV reactivation (12.0% vs. 50.0%; P=0.046). Two cases of reactivation occurred in patients who were HBsAg negative and hepatitis B core antibody positive. Conclusion HBV reactivation, especially for people with the use of rituximab, is a common complication in patients with HBV infection. HBV infection testing should be considered for lymphoma patients who were planned for chemotherapy. Prophylactic antiviral therapy can greatly decrease the incidence of HBV reactivation.

Citation： MAOYin-yan, DENGYao-tiao, JIANGMing. Screening of Hepatitis B Virus Infection before Chemotherapy for Patients with Lymphoma. West China Medical Journal, 2015, 30(3): 455-459. doi: 10.7507/1002-0179.20150130 Copy

1.	Lavanchy D. Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures[J]. J Viral Hepat, 2004, 11(2):97-107.
2.	Lu FM, Zhuang H. Management of hepatitis B in China[J]. Chin Med J (Engl), 2009, 122(1):3-4.
3.	Yeo W, Chan PK, Ho WM, et al. Lamivudine for the prevention of hepatitis B virus reactivation in hepatitis B s-antigen seropositive cancer patients undergoing cytotoxic chemotherapy[J]. J Clin Oncol, 2004, 22(5):927-934.
4.	Cheng AL, Hsiung CA, Su IJ, et al. Steroid-free chemotherapy decreases risk of hepatitis B virus (HBV) reactivation in HBV-carriers with lymphoma[J]. Hepatology, 2003, 37(6):1320-1328.
5.	贾杰, 林锋. 拉米夫定预防化疗诱发乙型肝炎病毒再活动的初步研究[J]. 中华肝脏病杂志, 2004, 12(10):628-629.
6.	Lau GK, Yiu HH, Fong DY, et al. Early is superior to deferred preemptive lamivudine therapy for hepatitis B patients undergoing chemotherapy[J]. Gastroenterology, 2003, 125(6):1742-1749.
7.	Kim JH, Bang YJ, Park BJ, et al. Hepatitis B virus infection and B-cell non-Hodgkin's lymphoma in a hepatitis B endemic area:a case-control study[J]. Jpn J Cancer Res, 2002, 93(5):471-477.
8.	Chen MH, Hsiao LT, Chiou TJ, et al. High prevalence of occult hepatitis B virus infection in patients with B cell non-Hodgkin's lymphoma[J]. Ann Hematol, 2008, 87(6):475-480.
9.	European Association For The Study Of The Liver. EASL clinical practice guidelines:management of chronic hepatitis B[J]. J Hepatol, 2009, 50(2):227-242.
10.	Weinbaum CM, Williams I, Mast EE, et al. Recommendations for identification and public health management of persons with chronic hepatitis B virus infection[J]. MMWR Recomm Rep, 2008, 57(RR/8):1-20.
11.	Yeo W, Chan PK, Zhong S, et al. Frequency of hepatitis B virus reactivation in cancer patients undergoing cytotoxic chemotherapy:a prospective study of 626 patients with identification of risk factors[J]. J Med Virol, 2000, 62(3):299-307.
12.	Lee R, Vu K, Bell CM, et al. Screening for hepatitis B surface antigen before chemotherapy:current practice and opportunities for improvement[J]. Curr Oncol, 2010, 17(6):32-38.
13.	Hwang J, Fisch M, Zhang H, et al. Predictors of hepatitis B screening among patients with cancer[J]. J Clin Oncol, 2011, 29(Suppl 4):180.
14.	中华医学会血液学分会, 中国抗癌协会淋巴瘤专业委员会, 中华医学会肝病学分会. 中国淋巴瘤合并HBV感染患者管理专家共识[J]. 中华血液学杂志, 2013, 34(11):988-993.
15.	Zurawska U, Hicks LK, Woo G, et al. Hepatitis B virus screening before chemotherapy for lymphoma:a cost-effectiveness analysis[J]. J Clin Oncol, 2012, 30(26):3167-3173.
16.	Wang Y, Luo XM, Yang D, et al. Testing for hepatitis B infection in prospective chemotherapy patients:a retrospective study[J]. World J Gastroenterol, 2013, 19(6):923-930.
17.	Hwang J, Fisch M, Zhang H, et al. Hepatitis B screening and positivity prior to chemotherapy[J]. J Clin Oncol, 2010, 28(Suppl 15):9008.
18.	Méndez-Navarro J, Corey KE, Zheng H, et al. Hepatitis B screening, prophylaxis and re-activation in the era of rituximab-based chemotherapy[J]. Liver Int, 2011, 31(3):330-339.
19.	Wang F, Xu RH, Han B, et al. High incidence of hepatitis B virus infection in B-cell subtype non-Hodgkin lymphoma compared with other cancers[J]. Cancer, 2007, 109(7):1360-1364.
20.	Marcucci F, Mele A, Spada E, et al. High prevalence of hepatitis B virus infection in B-cell non-Hodgkin's lymphoma[J]. Haematologica, 2006, 91(4):554-557.
21.	Liang X, Bi S, Yang W, et al. Reprint of:epidemiological serosurvey of hepatitis B in china:declining HBV prevalence due to hepatitis B vaccination[J]. Vaccine, 2013, 31(Suppl 9):J21-J28.
22.	Lok AS, McMahon BJ. Chronic hepatitis B[J]. Hepatology, 2007, 45(2):507-539.
23.	Ji D, Cao J, Hong X, et al. Low incidence of hepatitis B virus reactivation during chemotherapy among diffuse large B-cell lymphoma patients who are HBsAg-negative/HBcAb-positive:a multicenter retrospective study[J]. Eur J Haematol, 2010, 85(3):243-250.
24.	Yeo W, Chan TC, Leung NW, et al. Hepatitis B virus reactivation in lymphoma patients with prior resolved hepatitis B undergoing anticancer therapy with or without rituximab[J]. J Clin Oncol, 2009, 27(4):605-611.
25.	Kusumoto S, Tanaka Y, Mizokami M, et al. Reactivation of hepatitis B virus following systemic chemotherapy for malignant lymphoma[J]. Int J Hematol, 2009, 90(1):13-23.
26.	Johnson P, Glennie M. The mechanisms of action of rituximab in the elimination of tumor cells[J]. Semin Oncol, 2003, 30(1 Suppl 2):3-8.
27.	Wilson WH, Gutierrez M, O'connor P, et al. The role of rituximab and chemotherapy in aggressive B-cell lymphoma:a preliminary report of dose-adjusted EPOCH-R[J]. Semin Oncol, 2002, 29(Suppl 2):41-47.
28.	Ghetie MA, Bright H, Vitetta ES. Homodimers but not monomers of rituxan (chimeric anti-CD20) induce apoptosis in human B-lymphoma cells and synergize with a chemotherapeutic agent and an immunotoxin[J]. Blood, 2001, 97(5):1392-1398.
29.	Demidem A, Lam T, Alas S, et al. Chimeric anti-CD20(IDEC-C2B8) monoclonal antibody sensitizes a B cell lymphoma cell line to cell killing by cytotoxic drugs[J]. Cancer Biother Radiopharm, 1997, 12(3):177-186.
30.	Evens AM, Jovanovic BD, Su YC, et al. Rituximab-associated hepatitis B virus (HBV) reactivation in lymphoproliferative diseases:meta-analysis and examination of FDA safety reports[J]. Ann Oncol, 2011, 22(5):1170-1180.
31.	Dong HJ, Ni LN, Sheng GF, et al. Risk of hepatitis B virus (HBV) reactivation in non-Hodgkin lymphoma patients receiving rituximab-chemotherapy:a meta-analysis[J]. J Clin Virol, 2013, 57(3):209-214.
32.	Tsutsumi Y, Tanaka J, Kawamura T, et al. Possible efficacy of lamivudine treatment to prevent hepatitis B virus reactivation due to rituximab therapy in a patient with non-Hodgkin's lymphoma[J]. Ann Hematol, 2004, 83(1):58-60.
33.	Dai MS, Chao TY, Kao WY, et al. Delayed hepatitis B virus reactivation after cessation of preemptive lamivudine in lymphoma patients treated with rituximab plus CHOP[J]. Ann Hematol, 2004, 83(12):769-774.
34.	Wang YH, Fan L, Wang L, et al. Efficacy of prophylactic lamivudine to prevent hepatitis B virus reactivation in B-cell lymphoma treated with rituximab-containing chemotherapy[J]. Support Care Cancer, 2013, 21(5):1265-1271.
35.	Chen XQ, Peng JW, Lin GN, et al. The effect of prophylactic lamivudine on hepatitis B virus reactivation in HBsAg-positive patients with diffuse large B-cell lymphoma undergoing prolonged rituximab therapy[J]. Med Oncol, 2012, 29(2):1237-1241.
36.	Martyak LA, Taqavi E, Saab S. Lamivudine prophylaxis is effective in reducing hepatitis B reactivation and reactivation-related mortality in chemotherapy patients:a meta-analysis[J]. Liver Int, 2008, 28(1):28-38.
37.	Lau GK. Hepatitis B reactivation after chemotherapy:two decades of clinical research[J]. Hepatol Int, 2008, 2(2):152-162.

1. Lavanchy D. Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures[J]. J Viral Hepat, 2004, 11(2):97-107.
2. Lu FM, Zhuang H. Management of hepatitis B in China[J]. Chin Med J (Engl), 2009, 122(1):3-4.
3. Yeo W, Chan PK, Ho WM, et al. Lamivudine for the prevention of hepatitis B virus reactivation in hepatitis B s-antigen seropositive cancer patients undergoing cytotoxic chemotherapy[J]. J Clin Oncol, 2004, 22(5):927-934.
4. Cheng AL, Hsiung CA, Su IJ, et al. Steroid-free chemotherapy decreases risk of hepatitis B virus (HBV) reactivation in HBV-carriers with lymphoma[J]. Hepatology, 2003, 37(6):1320-1328.
5. 贾杰, 林锋. 拉米夫定预防化疗诱发乙型肝炎病毒再活动的初步研究[J]. 中华肝脏病杂志, 2004, 12(10):628-629.
6. Lau GK, Yiu HH, Fong DY, et al. Early is superior to deferred preemptive lamivudine therapy for hepatitis B patients undergoing chemotherapy[J]. Gastroenterology, 2003, 125(6):1742-1749.
7. Kim JH, Bang YJ, Park BJ, et al. Hepatitis B virus infection and B-cell non-Hodgkin's lymphoma in a hepatitis B endemic area:a case-control study[J]. Jpn J Cancer Res, 2002, 93(5):471-477.
8. Chen MH, Hsiao LT, Chiou TJ, et al. High prevalence of occult hepatitis B virus infection in patients with B cell non-Hodgkin's lymphoma[J]. Ann Hematol, 2008, 87(6):475-480.
9. European Association For The Study Of The Liver. EASL clinical practice guidelines:management of chronic hepatitis B[J]. J Hepatol, 2009, 50(2):227-242.
10. Weinbaum CM, Williams I, Mast EE, et al. Recommendations for identification and public health management of persons with chronic hepatitis B virus infection[J]. MMWR Recomm Rep, 2008, 57(RR/8):1-20.
11. Yeo W, Chan PK, Zhong S, et al. Frequency of hepatitis B virus reactivation in cancer patients undergoing cytotoxic chemotherapy:a prospective study of 626 patients with identification of risk factors[J]. J Med Virol, 2000, 62(3):299-307.
12. Lee R, Vu K, Bell CM, et al. Screening for hepatitis B surface antigen before chemotherapy:current practice and opportunities for improvement[J]. Curr Oncol, 2010, 17(6):32-38.
13. Hwang J, Fisch M, Zhang H, et al. Predictors of hepatitis B screening among patients with cancer[J]. J Clin Oncol, 2011, 29(Suppl 4):180.
14. 中华医学会血液学分会, 中国抗癌协会淋巴瘤专业委员会, 中华医学会肝病学分会. 中国淋巴瘤合并HBV感染患者管理专家共识[J]. 中华血液学杂志, 2013, 34(11):988-993.
15. Zurawska U, Hicks LK, Woo G, et al. Hepatitis B virus screening before chemotherapy for lymphoma:a cost-effectiveness analysis[J]. J Clin Oncol, 2012, 30(26):3167-3173.
16. Wang Y, Luo XM, Yang D, et al. Testing for hepatitis B infection in prospective chemotherapy patients:a retrospective study[J]. World J Gastroenterol, 2013, 19(6):923-930.
17. Hwang J, Fisch M, Zhang H, et al. Hepatitis B screening and positivity prior to chemotherapy[J]. J Clin Oncol, 2010, 28(Suppl 15):9008.
18. Méndez-Navarro J, Corey KE, Zheng H, et al. Hepatitis B screening, prophylaxis and re-activation in the era of rituximab-based chemotherapy[J]. Liver Int, 2011, 31(3):330-339.
19. Wang F, Xu RH, Han B, et al. High incidence of hepatitis B virus infection in B-cell subtype non-Hodgkin lymphoma compared with other cancers[J]. Cancer, 2007, 109(7):1360-1364.
20. Marcucci F, Mele A, Spada E, et al. High prevalence of hepatitis B virus infection in B-cell non-Hodgkin's lymphoma[J]. Haematologica, 2006, 91(4):554-557.
21. Liang X, Bi S, Yang W, et al. Reprint of:epidemiological serosurvey of hepatitis B in china:declining HBV prevalence due to hepatitis B vaccination[J]. Vaccine, 2013, 31(Suppl 9):J21-J28.
22. Lok AS, McMahon BJ. Chronic hepatitis B[J]. Hepatology, 2007, 45(2):507-539.
23. Ji D, Cao J, Hong X, et al. Low incidence of hepatitis B virus reactivation during chemotherapy among diffuse large B-cell lymphoma patients who are HBsAg-negative/HBcAb-positive:a multicenter retrospective study[J]. Eur J Haematol, 2010, 85(3):243-250.
24. Yeo W, Chan TC, Leung NW, et al. Hepatitis B virus reactivation in lymphoma patients with prior resolved hepatitis B undergoing anticancer therapy with or without rituximab[J]. J Clin Oncol, 2009, 27(4):605-611.
25. Kusumoto S, Tanaka Y, Mizokami M, et al. Reactivation of hepatitis B virus following systemic chemotherapy for malignant lymphoma[J]. Int J Hematol, 2009, 90(1):13-23.
26. Johnson P, Glennie M. The mechanisms of action of rituximab in the elimination of tumor cells[J]. Semin Oncol, 2003, 30(1 Suppl 2):3-8.
27. Wilson WH, Gutierrez M, O'connor P, et al. The role of rituximab and chemotherapy in aggressive B-cell lymphoma:a preliminary report of dose-adjusted EPOCH-R[J]. Semin Oncol, 2002, 29(Suppl 2):41-47.
28. Ghetie MA, Bright H, Vitetta ES. Homodimers but not monomers of rituxan (chimeric anti-CD20) induce apoptosis in human B-lymphoma cells and synergize with a chemotherapeutic agent and an immunotoxin[J]. Blood, 2001, 97(5):1392-1398.
29. Demidem A, Lam T, Alas S, et al. Chimeric anti-CD20(IDEC-C2B8) monoclonal antibody sensitizes a B cell lymphoma cell line to cell killing by cytotoxic drugs[J]. Cancer Biother Radiopharm, 1997, 12(3):177-186.
30. Evens AM, Jovanovic BD, Su YC, et al. Rituximab-associated hepatitis B virus (HBV) reactivation in lymphoproliferative diseases:meta-analysis and examination of FDA safety reports[J]. Ann Oncol, 2011, 22(5):1170-1180.
31. Dong HJ, Ni LN, Sheng GF, et al. Risk of hepatitis B virus (HBV) reactivation in non-Hodgkin lymphoma patients receiving rituximab-chemotherapy:a meta-analysis[J]. J Clin Virol, 2013, 57(3):209-214.
32. Tsutsumi Y, Tanaka J, Kawamura T, et al. Possible efficacy of lamivudine treatment to prevent hepatitis B virus reactivation due to rituximab therapy in a patient with non-Hodgkin's lymphoma[J]. Ann Hematol, 2004, 83(1):58-60.
33. Dai MS, Chao TY, Kao WY, et al. Delayed hepatitis B virus reactivation after cessation of preemptive lamivudine in lymphoma patients treated with rituximab plus CHOP[J]. Ann Hematol, 2004, 83(12):769-774.
34. Wang YH, Fan L, Wang L, et al. Efficacy of prophylactic lamivudine to prevent hepatitis B virus reactivation in B-cell lymphoma treated with rituximab-containing chemotherapy[J]. Support Care Cancer, 2013, 21(5):1265-1271.
35. Chen XQ, Peng JW, Lin GN, et al. The effect of prophylactic lamivudine on hepatitis B virus reactivation in HBsAg-positive patients with diffuse large B-cell lymphoma undergoing prolonged rituximab therapy[J]. Med Oncol, 2012, 29(2):1237-1241.
36. Martyak LA, Taqavi E, Saab S. Lamivudine prophylaxis is effective in reducing hepatitis B reactivation and reactivation-related mortality in chemotherapy patients:a meta-analysis[J]. Liver Int, 2008, 28(1):28-38.
37. Lau GK. Hepatitis B reactivation after chemotherapy:two decades of clinical research[J]. Hepatol Int, 2008, 2(2):152-162.

West China Medical Journal

Screening of Hepatitis B Virus Infection before Chemotherapy for Patients with Lymphoma

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