Association between immune checkpoint inhibitor antitumor therapy and hepatitis B virus reactivation

Shun CHEN; Youcheng XIE; Junke WANG; Baoyin ZHAO; Jiucong ZHANG; Pan WANG; Xiaohui YU

doi:10.3969/j.issn.1001-5256.2023.06.027

Volume 39 Issue 6

Jun. 2023

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Article Navigation > Journal of Clinical Hepatology > 2023 > 39(6): 1424-1430

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Association between immune checkpoint inhibitor antitumor therapy and hepatitis B virus reactivation

DOI: 10.3969/j.issn.1001-5256.2023.06.027

1.
Department of Gastroenterology, The 940 Hospital of Joint Logistic Support Force of PLA, Lanzhou 730050, China
2.
The Second Hospital of Lanzhou University, Lanzhou 730000, China

Research funding:

Gansu Provincial Key R&D Program (20YF8FA099);

Gansu Provincial Youth Science and Technology Fund (20JR10RA016);

Gansu Provincial Clinical Medical Research Centre for Non － infectious Liver Diseases (21JR7RA017)

More Information

Corresponding author: YU Xiaohui, yuxiaohui@126.com (ORCID: 0000-0002-8633-3281)
Received Date: 2022-09-30
Accepted Date: 2022-10-28
Published Date: 2023-06-20

Abstract

Abstract

In recent years, monotherapy and combination therapy with immune checkpoint inhibitors (ICIs) have achieved good efficacy in a variety of malignancies from solid tumors to lymphomas and have become a standardized and systematic treatment modality for many cancers. However, there is still a lack of studies on the safety of ICIs in hepatitis B virus (HBV)-infected patients with malignancies, and early studies have reported HBV reactivation due to ICI antitumor therapy in clinical practice. With reference to related literature, this article reviews the recent clinical trials and application of ICIs in cancer patients with chronic viral infection and clarifies the efficacy and safety of ICIs in this special population, in order to provide a reference for clinical medication.
- Liver Neoplasms,
- Hepatitis B, Chronic,
- Reinfection,
- Immune Checkpoint Inhibitors

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References(41)

References

[1]	KONG X, LU P, LIU C, et al. A combination of PD-1/PD-L1 inhibitors: The prospect of overcoming the weakness of tumor immunotherapy (Review)[J]. Mol Med Rep, 2021, 23(5): 362. DOI: 10.3892/mmr.2021.12001.
[2]	HASLAM A, GILL J, PRASAD V. Estimation of the percentage of US patients with cancer who are eligible for immune checkpoint inhibitor drugs[J]. JAMA Netw Open, 2020, 3(3): e200423. DOI: 10.1001/jamanetworkopen.2020.0423.
[3]	SHI Y, ZHENG M. Hepatitis B virus persistence and reactivation[J]. BMJ, 2020, 370: m2200. DOI: 10.1136/bmj.m2200.
[4]	YUEN MF, CHEN DS, DUSHEIKO GM, et al. Hepatitis B virus infection[J]. Nat Rev Dis Primers, 2018, 4: 18036. DOI: 10.1038/nrdp.2018.36.
[5]	LOOMBA R, LIANG TJ. Hepatitis B reactivation associated with immune suppressive and biological modifier therapies: current concepts, management strategies, and future directions[J]. Gastroenterology, 2017, 152(6): 1297-1309. DOI: 10.1053/j.gastro.2017.02.009.
[6]	SMALLS DJ, KIGER RE, NORRIS LB, et al. Hepatitis B virus reactivation: risk factors and current management strategies[J]. Pharmacotherapy, 2019, 39(12): 1190-1203. DOI: 10.1002/phar.2340.
[7]	CHEN CY, TIEN FM, CHENG A, et al. Hepatitis B reactivation among 1962 patients with hematological malignancy in Taiwan[J]. BMC Gastroenterol, 2018, 18(1): 6. DOI: 10.1186/s12876-017-0735-1.
[8]	AKIYAMA S, COTTER TG, SAKURABA A. Risk of hepatitis B virus reactivation in patients with autoimmune diseases undergoing non-tumor necrosis factor-targeted biologics[J]. World J Gastroenterol, 2021, 27(19): 2312-2324. DOI: 10.3748/wjg.v27.i19.2312.
[9]	SAITTA C, POLLICINO T, RAIMONDO G. Occult hepatitis B virus infection: An update[J]. Viruses, 2022, 14(7): 1504. DOI: 10.3390/v14071504.
[10]	ASAI A, HIRAI S, YOKOHAMA K, et al. Effect of an electronic alert system on hepatitis B virus reactivation in patients receiving immunosuppressive drug therapy[J]. J Clin Med, 2022, 11(9): 2446. DOI: 10.3390/jcm11092446.
[11]	KUSUMOTO S, ARCAINI L, HONG X, et al. Risk of HBV reactivation in patients with B-cell lymphomas receiving obinutuzumab or rituximab immunochemotherapy[J]. Blood, 2019, 133(2): 137-146. DOI: 10.1182/blood-2018-04-848044.
[12]	VOICAN CS, MIR O, LOULERGUE P, et al. Hepatitis B virus reactivation in patients with solid tumors receiving systemic anticancer treatment[J]. Ann Oncol, 2016, 27(12): 2172-2184. DOI: 10.1093/annonc/mdw414.
[13]	LAU G, YU ML, WONG G, et al. APASL clinical practice guideline on hepatitis B reactivation related to the use of immunosuppressive therapy[J]. Hepatol Int, 2021, 15(5): 1031-1048. DOI: 10.1007/s12072-021-10239-x.
[14]	ANASTASOPOULOU A, ZIOGAS DC, SAMARKOS M, et al. Reactivation of tuberculosis in cancer patients following administration of immune checkpoint inhibitors: current evidence and clinical practice recommendations[J]. J Immunother Cancer, 2019, 7(1): 239. DOI: 10.1186/s40425-019-0717-7.
[15]	LIN G, ZHUANG W, CHEN XH, et al. Increase of programmed death ligand 1 in non-small-cell lung cancers with chronic hepatitis B[J]. Ann Oncol, 2018, 29(2): 516-517. DOI: 10.1093/annonc/mdx694.
[16]	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]. J Immunother Cancer, 2019, 7(1): 322. DOI: 10.1186/s40425-019-0808-5.
[17]	SCHÖNRICH G, RAFTERY MJ. The PD-1/PD-L1 axis and virus infections: a delicate balance[J]. Front Cell Infect Microbiol, 2019, 9: 207. DOI: 10.3389/fcimb.2019.00207.
[18]	European Association for the Study of the Liver. EASL 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection[J]. J Hepatol, 2017, 67(2): 370-398. DOI: 10.1016/j.jhep.2017.03.021.
[19]	MORENO-CUBERO E, LARRUBIA JR. Specific CD8(+) T cell response immunotherapy for hepatocellular carcinoma and viral hepatitis[J]. World J Gastroenterol, 2016, 22(28): 6469-6483. DOI: 10.3748/wjg.v22.i28.6469.
[20]	LI B, YAN C, ZHU J, et al. Anti-PD-1/PD-L1 Blockade immunotherapy employed in treating hepatitis B virus infection-related advanced hepatocellular carcinoma: a literature review[J]. Front Immunol, 2020, 11: 1037. DOI: 10.3389/fimmu.2020.01037.
[21]	WANG X, HE Q, SHEN H, et al. Genetic and phenotypic difference in CD8(+) T cell exhaustion between chronic hepatitis B infection and hepatocellular carcinoma[J]. J Med Genet, 2019, 56(1): 18-21. DOI: 10.1136/jmedgenet-2018-105267.
[22]	KUMAGAI S, TOGASHI Y, KAMADA T, et al. The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies[J]. Nat Immunol, 2020, 21(11): 1346-1358. DOI: 10.1038/s41590-020-0769-3.
[23]	KNOLLE PA, THIMME R. Hepatic immune regulation and its involvement in viral hepatitis infection[J]. Gastroenterology, 2014, 146(5): 1193-1207. DOI: 10.1053/j.gastro.2013.12.036.
[24]	EL-KHOUEIRY AB, SANGRO B, YAU T, et al. Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): an open-label, non-comparative, phase 1/2 dose escalation and expansion trial[J]. Lancet, 2017, 389(10088): 2492-2502. DOI: 10.1016/S0140-6736(17)31046-2.
[25]	ZHU AX, FINN RS, EDELINE J, et al. Pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib (KEYNOTE-224): a non-randomised, open-label phase 2 trial[J]. Lancet Oncol, 2018, 19(7): 940-952. DOI: 10.1016/S1470-2045(18)30351-6.
[26]	PU D, YIN L, ZHOU Y, et al. Safety and efficacy of immune checkpoint inhibitors in patients with HBV/HCV infection and advanced-stage cancer: A systematic review[J]. Medicine (Baltimore), 2020, 99(5): e19013. DOI: 10.1097/MD.0000000000019013.
[27]	TERRAULT NA, LOK A, MCMAHON BJ, et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance[J]. Hepatology, 2018, 67(4): 1560-1599. DOI: 10.1002/hep.29800.
[28]	ZIOGAS DC, KOSTANTINOU F, CHOLONGITAS E, et al. Reconsidering the management of patients with cancer with viral hepatitis in the era of immunotherapy[J]. J Immunother Cancer, 2020, 8(2). DOI: 10.1136/jitc-2020-000943.
[29]	TIO M, RAI R, EZEOKE OM, et al. Anti-PD-1/PD-L1 immunotherapy in patients with solid organ transplant, HIV or hepatitis B/C infection[J]. Eur J Cancer, 2018, 104: 137-144. DOI: 10.1016/j.ejca.2018.09.017.
[30]	KOTHAPALLI A, KHATTAK MA. Safety and efficacy of anti-PD-1 therapy for metastatic melanoma and non-small-cell lung cancer in patients with viral hepatitis: a case series[J]. Melanoma Res, 2018, 28(2): 155-158. DOI: 10.1097/CMR.0000000000000434.
[31]	SHAH NJ, AL-SHBOOL G, BLACKBURN M, et al. Safety and efficacy of immune checkpoint inhibitors (ICIs) in cancer patients with HIV, hepatitis B, or hepatitis C viral infection[J]. J Immunother Cancer, 2019, 7(1): 353. DOI: 10.1186/s40425-019-0771-1.
[32]	SCHEINER B, KIRSTEIN MM, HUCKE F, et al. Programmed cell death protein-1 (PD-1)-targeted immunotherapy in advanced hepatocellular carcinoma: efficacy and safety data from an international multicentre real-world cohort[J]. Aliment Pharmacol Ther, 2019, 49(10): 1323-1333. DOI: 10.1111/apt.15245.
[33]	PERTEJO-FERNANDEZ A, RICCIUTI B, HAMMOND SP, et al. Safety and efficacy of immune checkpoint inhibitors in patients with non-small cell lung cancer and hepatitis B or hepatitis C infection[J]. Lung Cancer, 2020, 145: 181-185. DOI: 10.1016/j.lungcan.2020.02.013.
[34]	LEE PC, CHAO Y, CHEN MH, et al. Risk of HBV reactivation in patients with immune checkpoint inhibitor-treated unresectable hepatocellular carcinoma[J]. J Immunother Cancer, 2020, 8(2): e001072. DOI: 10.1136/jitc-2020-001072.
[35]	ZHANG X, TIAN D, CHEN Y, et al. Association of hepatitis B virus infection status with outcomes of non-small cell lung cancer patients undergoing anti-PD-1/PD-L1 therapy[J]. Transl Lung Cancer Res, 2021, 10(7): 3191-3202. DOI: 10.21037/tlcr-21-455.
[36]	HE MK, PENG C, ZHAO Y, et al. Comparison of HBV reactivation between patients with high HBV-DNA and low HBV-DNA loads undergoing PD-1 inhibitor and concurrent antiviral prophylaxis[J]. Cancer Immunol Immunother, 2021, 70(11): 3207-3216. DOI: 10.1007/s00262-021-02911-w.
[37]	WONG GL, WONG VW, HUI VW, et al. Hepatitis flare during immunotherapy in patients with current or past hepatitis B virus infection[J]. Am J Gastroenterol, 2021, 116(6): 1274-1283. DOI: 10.14309/ajg.0000000000001142.
[38]	ZHONG L, ZHONG P, LIU H, et al. Hepatitis B virus infection does not affect the clinical outcome of anti-programmed death receptor-1 therapy in advanced solid malignancies: Real-world evidence from a retrospective study using propensity score matching[J]. Medicine (Baltimore), 2021, 100(49): e28113. DOI: 10.1097/MD.0000000000028113.
[39]	YOO S, LEE D, SHIM JH, et al. Risk of hepatitis b virus reactivation in patients treated with immunotherapy for anti-cancer treatment[J]. Clin Gastroenterol Hepatol, 2022, 20(4): 898-907. DOI: 10.1016/j.cgh.2021.06.019.
[40]	PAN S, YU Y, WANG S, et al. Correlation of HBV DNA and hepatitis B surface antigen levels with tumor response, liver function and immunological indicators in liver cancer patients with HBV infection undergoing PD-1 inhibition combinational therapy[J]. Front Immunol, 2022, 13: 892618. DOI: 10.3389/fimmu.2022.892618.
[41]	HAGIWARA S, NISHIDA N, IDA H, et al. Clinical implication of immune checkpoint inhibitor on the chronic hepatitis B virus infection[J]. Hepatol Res, 2022, 52(9): 754-761. DOI: 10.1111/hepr.13798.

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Association between immune checkpoint inhibitor antitumor therapy and hepatitis B virus reactivation

DOI: 10.3969/j.issn.1001-5256.2023.06.027

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Association between immune checkpoint inhibitor antitumor therapy and hepatitis B virus reactivation

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