Combination Therapy with Lamivudine and HBIG versus Lamivudine Monotherapy in Prevention of Hepatitis B Virus Recurrence after Liver Transplantation: A Systematic Review_Chinese Journal of Evidence-Based Medicine

Authors：

JIANG Zicheng ,  JIANG Jianning

Department of Infectious Diseases, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, China;

Corresponding author：

JIANG Jianning, Email: jjianning@163.com

Keywords：

Liver transplantation; Hepatitis B; Recurrence; Lamivudine; Hepatitis B immunoglobulin; Meta-analysis

DOI：

10.7507/1672-2531.20100527

Video：

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Objective To evaluate the effectiveness of combination therapy with lamivudine (LAM) and hepatitis B immunoglobulin (HBIG) versus LAM monotherapy in prevention of hepatitis B virus recurrence after liver transplantation.
Methods Databases including MEDLINE (Ovid), PubMed, EMbase, Cochrane Central Register of Controlled Trials (CENTRAL), CBM, VIP, and CNKI were searched up to Dec. 2008. Clinical trials including randomized controlled, non-randomized concurrent-control and case-control studies about combination therapy with HBIG and LAM versus LAM monotherapy in prevention of hepatitis B virus recurrence after liver transplantation were screened. Trial selection and data extraction were conducted by two reviewers independently. Meta-analysis was performed using RevMan 5.0.18 software.
Results Eleven non-randomized concurrent-control studies involving 1 421 patients (1 035 patients in combination therapy group, and 386 patients in LAM monotherapy group) were included. The results of meta-analyses showed: Compared with LAM monotherapy group, the risks of hepatitis B virus recurrence, YMDD mutation, and death associated with HBV recurrence were significantly reduced by 73% (RR=0.27, 95%CI 0.20 to 0.37, P lt;0.000 01), 72% (RR=0.28, 95%CI 0.15 to 0.53, P=0.000 01), and 79% (RR=0.21, 95%CI 0.09 to 0.49, P=0.000 3) respectively in combination therapy group after liver transplantation; overall survival rates of both recipients and grafts in combination therapy group were similar to LAM monotherapy group (RR=1.03, 95%CI 0.95 to 1.11, P=0.51; RR=1.04, 95%CI 0.97 to 1.12, P=0.26).
Conclusion Current evidence indicates that compared with LAM monotherapy, combination therapy with LAM and HBIG could reduce the risks of hepatitis B virus recurrence, YMDD mutation, and death associated with HBV recurrence after liver transplantation.

Citation： JIANG Zicheng,JIANG Jianning. Combination Therapy with Lamivudine and HBIG versus Lamivudine Monotherapy in Prevention of Hepatitis B Virus Recurrence after Liver Transplantation: A Systematic Review. Chinese Journal of Evidence-Based Medicine, 2010, 10(8): 964-971. doi: 10.7507/1672-2531.20100527 Copy

1.	Rohit L, Rowley AK, Wesley R, et al. Hepatitis B immunoglobulin and lamivudine improve hepatitis B related outcomes after liver transplantation: meta-analysis. Clinical Gastroenterology and Hepatolog, 2008, 6(6): 696-700.
2.	Alter MJ. Epidemiology of hepatitis B in Europe and worldwide. J Hepatol, 2003, 39(Suppl 1): S64-69.
3.	全国人群乙肝血清流行病学调查结果.卫生部与中国疾病预防控制中心, 2008. http://www.chinacdc.net.cn/n272442/n272530/n3246177 /23316.html.
4.	Seehofer D, Rayes N, Neuhaus P. Prophylaxis and treatment of hepatitis B recurrence after liver transplantation in the antiviral era. Expert Rev Anti Infect Ther, 2003, 1(2): 307-318.
5.	Konig V, Hopf U, Neuhaus P, et al. Long-term follow-up of hepatitis B virus-infected recipients after orthotopic liver transplantation. Transplantation, 1994, 58(5): 553-559.
6.	Samuel D, Muller R, Alexander G, et al. Liver transplantation in European patients with the hepatitis B surface antigen. N Engl J Med, 1993, 329(25): 1842-1847.
7.	Large, muticenter, European retrospective study of more than 300 transplant patients illustrating that the risk of recurrence among patients with hepatitis B decreased with hepatitis B immunoglobulin (HBIG) usage.
8.	Fontana RJ, Lok AS. Combination of HBIG and lamivudineresistant mutations: a formula for trouble? Liver Transpl, 2002, 8: 1082-1084.
9.	Saab S, Kim M, Wright TL, et al. Successful orthotopic liver transplantation for lamivudine-associatied YMDD mutant hepatitis B virus. Gastroenterology, 2000, 119(5): 1382-1384.
10.	Dumortier J, Le Derf Y, Guillem P, et al. Favorable outcome of livertransplantation despite a high hepatitis B virus replication: beyond the limits? Transpl Infect Dis, 2006, 8(3): 182-184.
11.	Kamath PS, Wiesner RH, Malinchoc M, et al. A model to predict survival in patients with end-stage liver disease. Hepatology, 2001, 33(2): 464-470.
12.	吴泰相, 刘关键. 隐蔽分组(分配隐藏)和盲法的概念、实施与报告.中国循证医学杂志, 2007, 7(3): 222-225.
13.	王家良, 主编. 循证医学. 北京: 人民卫生出版社, 2005: 60-72.
14.	Sutton AJ, Abrams KR, Jones DR, et al. Methods for meta-analysis in medical research. Wiley: Chichester, 2000.
15.	Hedges LV. Modeling Publication selection effects in meta-analysis. Stat Sci, 1992, 7(2): 246-265.
16.	Freshwater DA, Dudley T, Cane P, et al. Viral persistence after liver transplantation for hepatitis B virus: a cross-sectional study. Transplantation, 2008, 85(8): 1105-1111.
17.	Neff,GW, O’Brien CB, Nery J, et al. Outcomes in liver transplant recipients with hepatitis B virus: Resistance and recurrence patterns from a large transplant center over the last decade. Liver Transplantation, 2004, 10(11): 1372-1378.
18.	Buti M, Mas A, Prieto M, et al. Adherence to lamivudine after an early withdrawal of hepatitis B immune globulin Plays an important role in the long-term prevention of hepatitis B virus recurrence. Transplantation, 2007, 84(5): 650-654.
19.	陈耀敏, 郑树森, 王伟林, 等. 拉米夫定联合乙型肝炎免疫球蛋白防治肝移植后乙型肝炎复发的疗效研究. 浙江医学, 2008, 30(9): 989-990.
20.	朱建平, 李磊, 张同琳, 等. 拉米夫定及乙型肝炎免疫球蛋白预防肝移植后乙型肝炎复发的疗效观察. 外科理论与实践, 2003, 8(6): 479-481.
21.	Zhu JP, Zhang TL, Li L, et al. Prevention and treatment of hepatitis B recurrence after liver transplantation. Hepatobillary & Pancreatic Diseases International, 2003, 2(4): 500-503.
22.	Oldakowska-Jedynak U, Paczek L, Foroncewicz B, et al. Prevention of hepatitis B recurrence after liver transplantation using lamivudine and hepatitis B immune globulin. Ann Transplant, 2007, 12(3): 28-32.
23.	Anselmo DM, Ghobrial RM, Jung LC, et al. New era of liver transplantation for hepatitis B: a 17-year single-center experience. Ann Surg, 2002, 235(5): 611-620.
24.	焦作义, 严律南, 李波, 等. 拉米夫定联合小剂量乙型肝炎免疫球蛋白预防肝移植术后乙型肝炎复发. 中华肝脏病杂志, 2007, 15(11): 804-808.
25.	史宪杰, 周宁新, 纪文斌, 等. 肝移植术后乙型肝炎病毒再感染的预防. 中华医院感染学杂志, 2007, 17(5): 527-529.
26.	王正昕, 丁国善, 付宏, 等. 173例肝移植术后乙型肝炎病毒再感染防治经验回顾. 中华肝胆外科杂志, 2006, 12(9): 616-618.
27.	夏杰, 杨占宇, 陈佳, 等. 肝移植术后乙型肝炎病毒再感染的预防与诊治. 中华消化外科杂志, 2007, 6(5): 348-351.
28.	Zheng S, Chen YM, Liang TB, et al. Prevention of hepatitis B recurrence after liver transplantation using lamivudine or lamivudine combined with hepatitis B Immunoglobulin prophylaxis. Liver Transpl, 2006, 12(2): 253-258.
29.	朱建平, 李磊, 张同琳, 等. 小剂量乙型肝炎免疫球蛋白与拉米夫定联合使用对肝移植后乙肝复发的疗效. 实用临床医药杂志, 2003, 7(3): 239-242.
30.	孙丽莹, 沈中阳, 朱志军, 等. 肝移植后乙型肝炎复发的回顾性分析. 外科理论与实践, 2008, 13(4): 326-329.
31.	张相良, 朱晓峰, 石慧娟, 等. 肝移植术后乙肝复发的预防和治疗. 广东医学, 2008, 29(1): 115-117.
32.	Yoshida H, Kato T, Levi DM, et al. Lamivudine monoprophylaxis for liver transplant recipients with non-replicating hepatitis B virus infection. Clinical Transplantation, 2007, 21(2): 166-171.
33.	巫林伟, 何晓顺, 朱晓峰, 等. 乙肝免疫球蛋白预防肝移植后乙肝复发. 热带医学杂志, 2006, 6(7): 788-790.
34.	Rao W, Wu X, Xiu D. Lamivudine or lamivudine combined with hepatitis B immunoglobulin in Prophylaxis of hepatitis B recurrence after liver transplantation: a meta-analysis. Transpl Int, 2009, 22(4): 387-394.
35.	Lo CM, Fung JT, Lau GK, et al. Development of antibody to hepatitis B surfae antigen after liver transplantation for chronic hepatitis B. Hepatology, 2003, 37(1): 36-43.

1. Rohit L, Rowley AK, Wesley R, et al. Hepatitis B immunoglobulin and lamivudine improve hepatitis B related outcomes after liver transplantation: meta-analysis. Clinical Gastroenterology and Hepatolog, 2008, 6(6): 696-700.
2. Alter MJ. Epidemiology of hepatitis B in Europe and worldwide. J Hepatol, 2003, 39(Suppl 1): S64-69.
3. 全国人群乙肝血清流行病学调查结果.卫生部与中国疾病预防控制中心, 2008. http://www.chinacdc.net.cn/n272442/n272530/n3246177 /23316.html.
4. Seehofer D, Rayes N, Neuhaus P. Prophylaxis and treatment of hepatitis B recurrence after liver transplantation in the antiviral era. Expert Rev Anti Infect Ther, 2003, 1(2): 307-318.
5. Konig V, Hopf U, Neuhaus P, et al. Long-term follow-up of hepatitis B virus-infected recipients after orthotopic liver transplantation. Transplantation, 1994, 58(5): 553-559.
6. Samuel D, Muller R, Alexander G, et al. Liver transplantation in European patients with the hepatitis B surface antigen. N Engl J Med, 1993, 329(25): 1842-1847.
7. Large, muticenter, European retrospective study of more than 300 transplant patients illustrating that the risk of recurrence among patients with hepatitis B decreased with hepatitis B immunoglobulin (HBIG) usage.
8. Fontana RJ, Lok AS. Combination of HBIG and lamivudineresistant mutations: a formula for trouble? Liver Transpl, 2002, 8: 1082-1084.
9. Saab S, Kim M, Wright TL, et al. Successful orthotopic liver transplantation for lamivudine-associatied YMDD mutant hepatitis B virus. Gastroenterology, 2000, 119(5): 1382-1384.
10. Dumortier J, Le Derf Y, Guillem P, et al. Favorable outcome of livertransplantation despite a high hepatitis B virus replication: beyond the limits? Transpl Infect Dis, 2006, 8(3): 182-184.
11. Kamath PS, Wiesner RH, Malinchoc M, et al. A model to predict survival in patients with end-stage liver disease. Hepatology, 2001, 33(2): 464-470.
12. 吴泰相, 刘关键. 隐蔽分组(分配隐藏)和盲法的概念、实施与报告.中国循证医学杂志, 2007, 7(3): 222-225.
13. 王家良, 主编. 循证医学. 北京: 人民卫生出版社, 2005: 60-72.
14. Sutton AJ, Abrams KR, Jones DR, et al. Methods for meta-analysis in medical research. Wiley: Chichester, 2000.
15. Hedges LV. Modeling Publication selection effects in meta-analysis. Stat Sci, 1992, 7(2): 246-265.
16. Freshwater DA, Dudley T, Cane P, et al. Viral persistence after liver transplantation for hepatitis B virus: a cross-sectional study. Transplantation, 2008, 85(8): 1105-1111.
17. Neff,GW, O’Brien CB, Nery J, et al. Outcomes in liver transplant recipients with hepatitis B virus: Resistance and recurrence patterns from a large transplant center over the last decade. Liver Transplantation, 2004, 10(11): 1372-1378.
18. Buti M, Mas A, Prieto M, et al. Adherence to lamivudine after an early withdrawal of hepatitis B immune globulin Plays an important role in the long-term prevention of hepatitis B virus recurrence. Transplantation, 2007, 84(5): 650-654.
19. 陈耀敏, 郑树森, 王伟林, 等. 拉米夫定联合乙型肝炎免疫球蛋白防治肝移植后乙型肝炎复发的疗效研究. 浙江医学, 2008, 30(9): 989-990.
20. 朱建平, 李磊, 张同琳, 等. 拉米夫定及乙型肝炎免疫球蛋白预防肝移植后乙型肝炎复发的疗效观察. 外科理论与实践, 2003, 8(6): 479-481.
21. Zhu JP, Zhang TL, Li L, et al. Prevention and treatment of hepatitis B recurrence after liver transplantation. Hepatobillary & Pancreatic Diseases International, 2003, 2(4): 500-503.
22. Oldakowska-Jedynak U, Paczek L, Foroncewicz B, et al. Prevention of hepatitis B recurrence after liver transplantation using lamivudine and hepatitis B immune globulin. Ann Transplant, 2007, 12(3): 28-32.
23. Anselmo DM, Ghobrial RM, Jung LC, et al. New era of liver transplantation for hepatitis B: a 17-year single-center experience. Ann Surg, 2002, 235(5): 611-620.
24. 焦作义, 严律南, 李波, 等. 拉米夫定联合小剂量乙型肝炎免疫球蛋白预防肝移植术后乙型肝炎复发. 中华肝脏病杂志, 2007, 15(11): 804-808.
25. 史宪杰, 周宁新, 纪文斌, 等. 肝移植术后乙型肝炎病毒再感染的预防. 中华医院感染学杂志, 2007, 17(5): 527-529.
26. 王正昕, 丁国善, 付宏, 等. 173例肝移植术后乙型肝炎病毒再感染防治经验回顾. 中华肝胆外科杂志, 2006, 12(9): 616-618.
27. 夏杰, 杨占宇, 陈佳, 等. 肝移植术后乙型肝炎病毒再感染的预防与诊治. 中华消化外科杂志, 2007, 6(5): 348-351.
28. Zheng S, Chen YM, Liang TB, et al. Prevention of hepatitis B recurrence after liver transplantation using lamivudine or lamivudine combined with hepatitis B Immunoglobulin prophylaxis. Liver Transpl, 2006, 12(2): 253-258.
29. 朱建平, 李磊, 张同琳, 等. 小剂量乙型肝炎免疫球蛋白与拉米夫定联合使用对肝移植后乙肝复发的疗效. 实用临床医药杂志, 2003, 7(3): 239-242.
30. 孙丽莹, 沈中阳, 朱志军, 等. 肝移植后乙型肝炎复发的回顾性分析. 外科理论与实践, 2008, 13(4): 326-329.
31. 张相良, 朱晓峰, 石慧娟, 等. 肝移植术后乙肝复发的预防和治疗. 广东医学, 2008, 29(1): 115-117.
32. Yoshida H, Kato T, Levi DM, et al. Lamivudine monoprophylaxis for liver transplant recipients with non-replicating hepatitis B virus infection. Clinical Transplantation, 2007, 21(2): 166-171.
33. 巫林伟, 何晓顺, 朱晓峰, 等. 乙肝免疫球蛋白预防肝移植后乙肝复发. 热带医学杂志, 2006, 6(7): 788-790.
34. Rao W, Wu X, Xiu D. Lamivudine or lamivudine combined with hepatitis B immunoglobulin in Prophylaxis of hepatitis B recurrence after liver transplantation: a meta-analysis. Transpl Int, 2009, 22(4): 387-394.
35. Lo CM, Fung JT, Lau GK, et al. Development of antibody to hepatitis B surfae antigen after liver transplantation for chronic hepatitis B. Hepatology, 2003, 37(1): 36-43.

Chinese Journal of Evidence-Based Medicine

Combination Therapy with Lamivudine and HBIG versus Lamivudine Monotherapy in Prevention of Hepatitis B Virus Recurrence after Liver Transplantation: A Systematic Review

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