Drugs and hepatitis B virus reactivation_Journal of Biomedical Engineering

Authors：

DU Lingyao , MA Yuanji ,  TANG Hong

Center of Infectious Diseases, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

Keywords：

Hepatitis B virus; Reactivation; Drugs; Chemotherapy; Immunosuppression

DOI：

10.7507/1001-5515.202112003

Video：

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Abstract Full text Figures/Tables Video References Cited by

Drugs may induce hepatitis B virus (HBV) reactivation (HBV-R). Here we have reviewed the definition and harm of HBV-R, the risk drugs and their underlying mechanism, the influence factors, as well as the early intervention measures. It is shown that multiple drugs, including chemotherapy drugs, immunotherapy drugs, directly acting antivirals, cell therapy, etc., can induce HBV-R by affecting host immunity or directly activating HBV transcription factors. HBV-R could cause severe liver damage, even interruption of treatment of original diseases, affecting the prognosis of patients. Through precisely identifying risk drugs, monitoring the influence factors, and prescribing preventive anti-HBV regimen if necessary, the incidence of HBV-R can be significantly reduced. It is also suggested that clinical physicians should not only pay attention to the early identification and intervention of HBV-R, but also further study the mechanism of HBV-R in depth, especially the underlying mechanism between host, HBV and risk factors. This will help to promote the discovery of more valuable markers for risk prediction and targets for early intervention, and to further reduce the risk of HBV-R and improve the prognosis of patients.

Citation： DU Lingyao, MA Yuanji, TANG Hong. Drugs and hepatitis B virus reactivation. Journal of Biomedical Engineering, 2022, 39(3): 627-632. doi: 10.7507/1001-5515.202112003 Copy

1.	中华医学会感染病学分会. 中华医学会肝病学分会. 慢性乙型肝炎防治指南(2019年版). 中华肝脏病杂志, 2019, 27(12): 938-961.
2.	Lee H W, Lee J S, Ahn S H. Hepatitis B virus cure: targets and future therapies. Int J Mol Sci, 2020, 22(1): 213.
3.	Sarin S K, Kumar M, Lau G K, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int, 2016, 10(1): 1-98.
4.	Terrault N A, Lok A S, McMahon B J, et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology, 2018, 67(4): 1560-1599.
5.	Guo L, Wang D, Ouyang X, et al. Recent advances in HBV reactivation research. Biomed Res Int, 2018: 2931402.
6.	Sarin S K, Choudhury A. Management of acute-on-chronic liver failure: an algorithmic approach. Hepatol Int, 2018, 12(5): 402-416.
7.	Aygen B, Demir A M, Gümüş M, et al. Immunosuppressive therapy and the risk of hepatitis B reactivation: consensus report. Turk J Gastroenterol, 2018, 29(3): 259-269.
8.	Hwang J P, Barbo A G, Perrillo R P. Hepatitis B reactivation during cancer chemotherapy: an international survey of the membership of the American Association for the Study of Liver Diseases. J Viral Hepat, 2015, 22(3): 346-352.
9.	田文广, 何平, 万克强, 等. 核苷类似物防治化疗后乙肝病毒再激活的临床疗效分析. 中国新药与临床杂志, 2015, 34(7): 560-564.
10.	Yeo W, Chan P K, Hui P, et al. Hepatitis B virus reactivation in breast cancer patients receiving cytotoxic chemotherapy: a prospective study. J Med Virol, 2003, 70(4): 553-561.
11.	Huang Gang, Lai E C, Lau W Y, et al. Posthepatectomy HBV reactivation in hepatitis B-related hepatocellular carcinoma influences postoperative survival in patients with preoperative low HBV-DNA levels. Ann Surg, 2013, 257(3): 490-505.
12.	Shi Y, Zheng M. Hepatitis B virus persistence and reactivation. British Medical Journal, 2020, 370: m2200.
13.	Bukowski K, Kciuk M, Kontek R. Mechanisms of multidrug resistance in cancer chemotherapy. Int J Mol Sci, 2020, 21(9): 3233.
14.	马军, 秦叔逵, 缪晓辉, 等. 淋巴瘤免疫化疗HBV再激活预防和治疗中国专家共识. 临床肿瘤学杂志, 2013, 18(10): 935-942.
15.	Cao X, Wang Y, Li P, et al. HBV reactivation during the treatment of non-Hodgkin lymphoma and management strategies. Front Oncol, 2021, 11: 685706.
16.	Chen X, Hu Y, Zhang W, et al. Cisplatin induces autophagy to enhance hepatitis B virus replication via activation of ROS/JNK and inhibition of the Akt/mTOR pathway. Free Radic Biol Med, 2019, 131: 225-236.
17.	Li X, Pan E, Zhu J, et al. Cisplatin enhances hepatitis B virus replication and PGC-1α expression through endoplasmic reticulum stress. Sci Rep, 2018, 8(1): 3496.
18.	Zen Y, Yeh M M. Checkpoint inhibitor-induced liver injury: a novel form of liver disease emerging in the era of cancer immunotherapy. Semin Diagn Pathol, 2019, 36(6): 434-440.
19.	Pan C, Liu H, Robins E, et al. Next-generation immuno-oncology agents: current momentum shifts in cancer immunotherapy. J Hematol Oncol, 2020, 13(1): 29.
20.	Zhang X, Zhou Y, Chen C, et al. Hepatitis B virus reactivation in cancer patients with positive hepatitis B surface antigen undergoing PD-1 inhibition. J Immunother Cancer, 2019, 7(1): 322.
21.	Godbert B, Petitpain N, Lopez A, et al. Hepatitis B reactivation and immune check point inhibitors. Dig Liver Dis, 2021, 53(4): 452-455.
22.	Lee P C, Chao Y, Chen M H, et al. Risk of HBV reactivation in patients with immune checkpoint inhibitor-treated unresectable hepatocellular carcinoma. J Immunother Cancer, 2020, 8(2): e001072.
23.	Wang J, Du L, Tang H. Suppression of interferon-α treatment response by host negative factors in hepatitis B virus infection. Front Med (Lausanne), 2021, 8: 784172.
24.	Du L Y, Cui Y L, Chen E Q, et al. Correlation between the suppressor of cytokine signaling-1 and 3 and hepatitis B virus: possible roles in the resistance to interferon treatment, Virol J, 2014: 51.
25.	Mücke M M, Backus L, Mücke V T, et al. Hepatitis B virus reactivation during direct-acting antiviral therapy for hepatitis C: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol, 2018, 3(3): 172-180.
26.	Huang R, Li X, He Y, et al. Recent advances in CAR-T cell engineering. J Hematol Oncol, 2020, 13(1): 86.
27.	Yang C, Xie M, Zhang K, et al. Risk of HBV reactivation post CD19-CAR-T cell therapy in DLBCL patients with concomitant chronic HBV infection. Leukemia, 2020, 34(11): 3055-3059.
28.	Han L, Zhou J, Zhou K, et al. Safety and efficacy of CAR-T cell targeting BCMA in patients with multiple myeloma coinfected with chronic hepatitis B virus. J Immunother Cancer, 2020, 8(2): e000927.
29.	Li P, Zhou L, Ye S, et al. Risk of HBV reactivation in patients with resolved HBV infection receiving anti-CD19 chimeric antigen receptor T cell therapy without antiviral prophylaxis. Front Immunol, 2021, 12: 638678.
30.	Zhang S S, Liu J X, Zhu J, et al. Effects of TACE and preventive antiviral therapy on HBV reactivation and subsequent hepatitis in hepatocellular carcinoma: a meta-analysis. Jpn J Clin Oncol, 2019, 49(7): 646-655.
31.	Liu Shousheng, Lai Jinfa, Lyu N, et al. Effects of antiviral therapy on HBV reactivation and survival in hepatocellular carcinoma patients undergoing hepatic artery infusion chemotherapy. Front Oncol, 2020, 10: 582504.
32.	Ziogas D C, Kostantinou F, Cholongitas E, et al. Reconsidering the management of patients with cancer with viral hepatitis in the era of immunotherapy. J Immunother Cancer, 2020, 8(2): e000943.
33.	Karaca M, Tural D, Akar E, et al. Hepatitis B reactivation rate is higher undergoing some cytotoxic chemotherapy in patients with solid tumors: a large retrospective study. Chemotherapy, 2018, 63(5): 247-252.
34.	Shih C A, Chen W C, Yu H C, et al. Risk of severe acute exacerbation of chronic HBV infection cancer patients who underwent chemotherapy and did not receive anti-viral prophylaxis. PLoS One, 2015, 10(8): e0132426.
35.	Yang H C, Tsou H H, Pei S N, et al. Quantification of HBV core antibodies may help predict HBV reactivation in patients with lymphoma and resolved HBV infection. J Hepatol, 2018, 69(2): 286-292.
36.	European Association for the Study of the Liver. EASL 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection. J Hepatol, 2017, 67(2): 370-398.
37.	Pawłowska M, Flisiak R, Gil L, et al. Prophylaxis of hepatitis B virus (HBV) infection reactivation-recommendations of the working group for prevention of HBV reactivation. Clin Exp Hepatol, 2019, 5(3): 195-202.
38.	Su Y C, Lin P C, Yu H C, et al. Antiviral prophylaxis during chemotherapy or immunosuppressive drug therapy to prevent HBV reactivation in patients with resolved HBV infection: a systematic review and meta-analysis. Eur J Clin Pharmacol, 2018, 74(9): 1111-1119.
39.	Chauhan R, Lingala S, Gadiparthi C, et al. Reactivation of hepatitis B after liver transplantation: current knowledge, molecular mechanisms and implications in management. World J Hepatol, 2018, 10(3): 352-370.

1. 中华医学会感染病学分会. 中华医学会肝病学分会. 慢性乙型肝炎防治指南(2019年版). 中华肝脏病杂志, 2019, 27(12): 938-961.
2. Lee H W, Lee J S, Ahn S H. Hepatitis B virus cure: targets and future therapies. Int J Mol Sci, 2020, 22(1): 213.
3. Sarin S K, Kumar M, Lau G K, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int, 2016, 10(1): 1-98.
4. Terrault N A, Lok A S, McMahon B J, et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology, 2018, 67(4): 1560-1599.
5. Guo L, Wang D, Ouyang X, et al. Recent advances in HBV reactivation research. Biomed Res Int, 2018: 2931402.
6. Sarin S K, Choudhury A. Management of acute-on-chronic liver failure: an algorithmic approach. Hepatol Int, 2018, 12(5): 402-416.
7. Aygen B, Demir A M, Gümüş M, et al. Immunosuppressive therapy and the risk of hepatitis B reactivation: consensus report. Turk J Gastroenterol, 2018, 29(3): 259-269.
8. Hwang J P, Barbo A G, Perrillo R P. Hepatitis B reactivation during cancer chemotherapy: an international survey of the membership of the American Association for the Study of Liver Diseases. J Viral Hepat, 2015, 22(3): 346-352.
9. 田文广, 何平, 万克强, 等. 核苷类似物防治化疗后乙肝病毒再激活的临床疗效分析. 中国新药与临床杂志, 2015, 34(7): 560-564.
10. Yeo W, Chan P K, Hui P, et al. Hepatitis B virus reactivation in breast cancer patients receiving cytotoxic chemotherapy: a prospective study. J Med Virol, 2003, 70(4): 553-561.
11. Huang Gang, Lai E C, Lau W Y, et al. Posthepatectomy HBV reactivation in hepatitis B-related hepatocellular carcinoma influences postoperative survival in patients with preoperative low HBV-DNA levels. Ann Surg, 2013, 257(3): 490-505.
12. Shi Y, Zheng M. Hepatitis B virus persistence and reactivation. British Medical Journal, 2020, 370: m2200.
13. Bukowski K, Kciuk M, Kontek R. Mechanisms of multidrug resistance in cancer chemotherapy. Int J Mol Sci, 2020, 21(9): 3233.
14. 马军, 秦叔逵, 缪晓辉, 等. 淋巴瘤免疫化疗HBV再激活预防和治疗中国专家共识. 临床肿瘤学杂志, 2013, 18(10): 935-942.
15. Cao X, Wang Y, Li P, et al. HBV reactivation during the treatment of non-Hodgkin lymphoma and management strategies. Front Oncol, 2021, 11: 685706.
16. Chen X, Hu Y, Zhang W, et al. Cisplatin induces autophagy to enhance hepatitis B virus replication via activation of ROS/JNK and inhibition of the Akt/mTOR pathway. Free Radic Biol Med, 2019, 131: 225-236.
17. Li X, Pan E, Zhu J, et al. Cisplatin enhances hepatitis B virus replication and PGC-1α expression through endoplasmic reticulum stress. Sci Rep, 2018, 8(1): 3496.
18. Zen Y, Yeh M M. Checkpoint inhibitor-induced liver injury: a novel form of liver disease emerging in the era of cancer immunotherapy. Semin Diagn Pathol, 2019, 36(6): 434-440.
19. Pan C, Liu H, Robins E, et al. Next-generation immuno-oncology agents: current momentum shifts in cancer immunotherapy. J Hematol Oncol, 2020, 13(1): 29.
20. Zhang X, Zhou Y, Chen C, et al. Hepatitis B virus reactivation in cancer patients with positive hepatitis B surface antigen undergoing PD-1 inhibition. J Immunother Cancer, 2019, 7(1): 322.
21. Godbert B, Petitpain N, Lopez A, et al. Hepatitis B reactivation and immune check point inhibitors. Dig Liver Dis, 2021, 53(4): 452-455.
22. Lee P C, Chao Y, Chen M H, et al. Risk of HBV reactivation in patients with immune checkpoint inhibitor-treated unresectable hepatocellular carcinoma. J Immunother Cancer, 2020, 8(2): e001072.
23. Wang J, Du L, Tang H. Suppression of interferon-α treatment response by host negative factors in hepatitis B virus infection. Front Med (Lausanne), 2021, 8: 784172.
24. Du L Y, Cui Y L, Chen E Q, et al. Correlation between the suppressor of cytokine signaling-1 and 3 and hepatitis B virus: possible roles in the resistance to interferon treatment, Virol J, 2014: 51.
25. Mücke M M, Backus L, Mücke V T, et al. Hepatitis B virus reactivation during direct-acting antiviral therapy for hepatitis C: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol, 2018, 3(3): 172-180.
26. Huang R, Li X, He Y, et al. Recent advances in CAR-T cell engineering. J Hematol Oncol, 2020, 13(1): 86.
27. Yang C, Xie M, Zhang K, et al. Risk of HBV reactivation post CD19-CAR-T cell therapy in DLBCL patients with concomitant chronic HBV infection. Leukemia, 2020, 34(11): 3055-3059.
28. Han L, Zhou J, Zhou K, et al. Safety and efficacy of CAR-T cell targeting BCMA in patients with multiple myeloma coinfected with chronic hepatitis B virus. J Immunother Cancer, 2020, 8(2): e000927.
29. Li P, Zhou L, Ye S, et al. Risk of HBV reactivation in patients with resolved HBV infection receiving anti-CD19 chimeric antigen receptor T cell therapy without antiviral prophylaxis. Front Immunol, 2021, 12: 638678.
30. Zhang S S, Liu J X, Zhu J, et al. Effects of TACE and preventive antiviral therapy on HBV reactivation and subsequent hepatitis in hepatocellular carcinoma: a meta-analysis. Jpn J Clin Oncol, 2019, 49(7): 646-655.
31. Liu Shousheng, Lai Jinfa, Lyu N, et al. Effects of antiviral therapy on HBV reactivation and survival in hepatocellular carcinoma patients undergoing hepatic artery infusion chemotherapy. Front Oncol, 2020, 10: 582504.
32. Ziogas D C, Kostantinou F, Cholongitas E, et al. Reconsidering the management of patients with cancer with viral hepatitis in the era of immunotherapy. J Immunother Cancer, 2020, 8(2): e000943.
33. Karaca M, Tural D, Akar E, et al. Hepatitis B reactivation rate is higher undergoing some cytotoxic chemotherapy in patients with solid tumors: a large retrospective study. Chemotherapy, 2018, 63(5): 247-252.
34. Shih C A, Chen W C, Yu H C, et al. Risk of severe acute exacerbation of chronic HBV infection cancer patients who underwent chemotherapy and did not receive anti-viral prophylaxis. PLoS One, 2015, 10(8): e0132426.
35. Yang H C, Tsou H H, Pei S N, et al. Quantification of HBV core antibodies may help predict HBV reactivation in patients with lymphoma and resolved HBV infection. J Hepatol, 2018, 69(2): 286-292.
36. European Association for the Study of the Liver. EASL 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection. J Hepatol, 2017, 67(2): 370-398.
37. Pawłowska M, Flisiak R, Gil L, et al. Prophylaxis of hepatitis B virus (HBV) infection reactivation-recommendations of the working group for prevention of HBV reactivation. Clin Exp Hepatol, 2019, 5(3): 195-202.
38. Su Y C, Lin P C, Yu H C, et al. Antiviral prophylaxis during chemotherapy or immunosuppressive drug therapy to prevent HBV reactivation in patients with resolved HBV infection: a systematic review and meta-analysis. Eur J Clin Pharmacol, 2018, 74(9): 1111-1119.
39. Chauhan R, Lingala S, Gadiparthi C, et al. Reactivation of hepatitis B after liver transplantation: current knowledge, molecular mechanisms and implications in management. World J Hepatol, 2018, 10(3): 352-370.

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