Variation in attributable fraction of hepatitis B virus and hepatitis C virus among primary liver cancer cases across mainland China: a systematic literature review and meta-analysis

Abstract

Aim: Our objective was to describe variations in attributable fractions (AFs) of hepatitis B virus (HBV) and hepatitis C virus (HCV) to primary liver cancer (PLC) across mainland China.

Methods: We conducted a systematic review and meta-analysis of studies published up to July 2024 in PubMed, Embase, WanFang, and China National Knowledge Infrastructure. Eligible studies reported the prevalence of HBV and HCV infection, alone and in combination, in PLC. AFs of HBV, HCV, and non-viral etiology in PLC were estimated by province and, when possible, by sex, age, histological diagnosis, and study periods. Regional and overall AFs were estimated by weighting by provincial and regional population size. Publication bias and heterogeneity were assessed by funnel plots of AFs of HBV, HCV, and non-viral etiology in PLC cases, using Egger test by study size.

Results: We included 240 studies with 71,905 PLC cases from 31 provinces, autonomous regions and municipalities across mainland China. AFs of HBV, HCV, and non-viral etiology for PLC across mainland China were 76.5%, 6.6%, and 16.9%, respectively. The AFs of HBV and HCV varied by region, with HBV AFs ranging from 68.7% in Northwest China to 82.9% in South Central China. Respective HCV AFs ranged from 12.7% in Northeast China down to 3.7% in South Central China. Non-viral AFs ranged from 13.4% to 21.0% by region. AFs of non-viral etiology were 57.9% in intrahepatic cholangiocarcinoma (ICC), and AF of HBV was double prevalence ratio (PR), 2.11 (95%CI: 1.89-2.34) in hepatocellular carcinoma (HCC, 76.3%) than ICC (37.3%) cases. Prevalence of HBV was higher in male (83.9%) than female (74.6%) PLC cases, and the mean age at diagnosis was 10 years higher for PLC with HCV (64.9 years) than HBV (54.4 years).

Conclusion: HBV, HCV, and non-viral AFs varied substantially by region across China, as well as by sex and age, which can inform strategies for liver cancer prevention and control.

Keywords

Hepatitis B virus / hepatitis C virus / primary liver cancer / meta-analysis

References

[1] Bray F,Sung H.Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin2024;74:229-63

[2] Zheng RS,Han BF.[Cancer incidence and mortality in China, 2022].Zhonghua Zhong Liu Za Zhi2024;46:221-31

[3] Rumgay H,de Martel C.Global, regional and national burden of primary liver cancer by subtype.Eur J Cancer2022;161:108-18

[4] Lin J,Yu H.Epidemiological characteristics of primary liver cancer in Mainland China from 2003 to 2020: a representative multicenter study.Front Oncol2022;12:906778 PMCID:PMC9253580

[5] McGlynn KA,El-Serag HB.Epidemiology of hepatocellular carcinoma.Hepatology2021;73 Suppl 1:4-13 PMCID:PMC7577946

[6] Martel C, Maucort-Boulch D, Plummer M, Franceschi S. World-wide relative contribution of hepatitis B and C viruses in hepatocellular carcinoma.Hepatology2015;62:1190-200 PMCID:PMC5019261

[7] Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis.Lancet Glob Health2020;8:e180-90

[8] Liu Z,Mao X.Changing prevalence of chronic hepatitis B virus infection in China between 1973 and 2021: a systematic literature review and meta-analysis of 3740 studies and 231 million people.Gut2023;72:2354-63 PMCID:PMC10715530

[9] Gao Y,Sun F.Prevalence of anti-HCV antibody among the general population in mainland china between 1991 and 2015: a systematic review and meta-analysis.Open Forum Infect Dis2019;6:ofz040 PMCID:PMC6408870

[10] Sievert W,Razavi HA.A systematic review of hepatitis C virus epidemiology in Asia, Australia and Egypt.Liver Int2011;31 Suppl 2:61-80

[11] Mei X.Prevalence, diagnosis, and treatment of hepatitis C in Mainland China.Glob Health Med2021;3:270-5 PMCID:PMC8562088

[12] Sui HT. Clinical characteristics and molecular mechanism of primary liver cancer in Yanbian area. Master thesis, Yanbian University, 2018. Available from: https://d.wanfangdata.com.cn/thesis/ChhUaGVzaXNOZXdTMjAyNDA5MjAxNTE3MjUSCFkzNDIyNDI4GggyZTh5Mnp0Zg%253D%253D. [Last accessed on 31 Dec 2024].

[13] Liu Y,Hao J.Global burden of primary liver cancer by five etiologies and global prediction by 2035 based on global burden of disease study 2019.Cancer Med2022;11:1310-23 PMCID:PMC8894698

[14] Tan DJH,Ng CH.Global burden of liver cancer in males and females: changing etiological basis and the growing contribution of NASH.Hepatology2023;77:1150-63

[15] Alberts CJ,Georges D.Worldwide prevalence of hepatitis B virus and hepatitis C virus among patients with cirrhosis at country, region, and global levels: a systematic review.Lancet Gastroenterol Hepatol2022;7:724-35 PMCID:PMC9259503

[16] Maucort-Boulch D,Franceschi S.Fraction and incidence of liver cancer attributable to hepatitis B and C viruses worldwide.Int J Cancer2018;142:2471-7

[17] Wang M,Feng X.Contribution of hepatitis B virus and hepatitis C virus to liver cancer in China north areas: experience of the Chinese National Cancer Center.Int J Infect Dis2017;65:15-21

[18] Wang Y,Gu D.Hepatitis B and C virus infections and the risk of biliary tract cancers: a meta-analysis of observational studies.Infect Agent Cancer2022;17:45 PMCID:PMC9420284

[19] Li H,Zhou ZQ,Zhang ZY.Hepatitis C virus infection and the risk of intrahepatic cholangiocarcinoma and extrahepatic cholangiocarcinoma: evidence from a systematic review and meta-analysis of 16 case-control studies.World J Surg Oncol2015;13:161 PMCID:PMC4419416

[20] Tan JH,Zhou L,Zhang GW.Viral hepatitis B and C infections increase the risks of intrahepatic and extrahepatic cholangiocarcinoma: evidence from a systematic review and meta-analysis.Turk J Gastroenterol2020;31:246-56 PMCID:PMC7197930

[21] Lin B,Lu Y,Jin J.Viral hepatitis increases the risk of cholangiocarcinoma: a systematic review and meta-analysis.Transl Cancer Res2023;12:1602-16 PMCID:PMC10331712

[22] Huang DQ,Kanwal F.Hepatocellular carcinoma surveillance - utilization, barriers and the impact of changing aetiology.Nat Rev Gastroenterol Hepatol2023;20:797-809

[23] Xiao L,Zhang H.Comparison of the clinical characteristics and survival between Uyghur patients with hepatitis virus-related and non-B, non-C hepatocellular carcinoma in Xinjiang, China.Chin J Cancer Res2015;27:279-87 PMCID:PMC3726712

[24] He J, Wei WQ. China cancer registry annual report (2019). People’s Medical Publishing House; 2023. pp. 349. Available from: https://oaepublishstorage.blob.core.windows.net/manuscript11828/Scanned-file-of-reference-24-in-main-text-0811.pdf. [Last accessed on 30 Dec 2024].

[25] Ni YQ,Mao R,Wen H.[Clinical epidemiological analysis of 3602 cases of primary liver cancer in Xinjiang].Zhonghua Zhong Liu Za Zhi2012;34:374-7

[26] Li Q,Qin Y,Hao X.Comparison of surgical outcomes for small hepatocellular carcinoma in patients with hepatitis B versus hepatitis C: a Chinese experience.J Gastroenterol Hepatol2007;22:1936-41

[27] Lu SN,Yang SS.Secular trends and geographic variations of hepatitis B virus and hepatitis C virus-associated hepatocellular carcinoma in Taiwan.Int J Cancer2006;119:1946-52

[28] Wang AC,Wang CW,Chen SC.Sex difference in the associations among risk factors with hepatitis B and C infections in a large Taiwanese population study.Front Public Health2022;10:1068078 PMCID:PMC9748294