A Historical Overview on the Role of Hepatitis B and C Viruses as Aetiological Factors for Hepatocellular Carcinoma
Abstract
:Simple Summary
Abstract
1. Introduction
2. Hepatitis B
2.1. Viral Cofactors
2.1.1. HCV Coinfection
2.1.2. HDV Coinfection
2.2. Non-Viral Cofactors
3. HBV Carcinogenesis
4. Prevention of HBV-Related HCC
4.1. Primary Prevention (For Subjects That Are Still Susceptible to HBV)
4.2. Secondary Prevention (For Subjects with Chronic HBV Infection)
5. Hepatitis C
6. Risk Factors for HCC in HCV Patients C
6.1. Viral Cofactors
6.2. Non-Viral Cofactors
7. HCV Carcinogenesis
8. Prevention of HCV-Related HCC
8.1. Primary Prevention (For Subjects That Are Still Susceptible to HCV)
8.2. Secondary Prevention (For Subjects Who Are Infected with HCV)
9. Future Scenarios
10. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424, Erratum in CA Cancer J. Clin. 2020, 70, 313. [Google Scholar] [CrossRef] [PubMed]
- Rumgay, H.; Ferlay, J.; de Martel, C.; Georges, D.; Ibrahim, A.S.; Zheng, R.; Wei, W.; Lemmens, V.E.; Soerjomataram, I. Global, regional, and national burden of primary liver cancer by subtype. Eur. J. Cancer 2022, 161, 108–118. [Google Scholar] [CrossRef] [PubMed]
- Fattovich, G.; Stroffolini, T.; Zagni, I.; Donato, F. Hepatocellular carcinoma in cirrhosis: Incidence and risk factors. Gastroenterology 2004, 127 (Suppl. S1), S35–S50. [Google Scholar] [CrossRef]
- Blumberg, B.S.; Alter, H.J.; Visnich, S.A. “new” antigen in leukemia sera. JAMA 1965, 191, 541–546. [Google Scholar] [CrossRef] [PubMed]
- Beasley, R.; Lin, C.-C.; Hwang, L.-Y.; Chien, C.-S. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22,707 men in Taiwan. Lancet 1981, 2, 1129–1133. [Google Scholar] [CrossRef]
- Szmuness, W.; Stevens, C.E.; Harley, E.J.; Zang, E.A.; Oleszko, W.R.; William, D.C.; Sadovsky, R.; Morrison, J.M.; Kellner, A. Hepatitis B vaccine: Demonstration of efficacy in a controlled clinical trial in a high-risk population in the United States. N. Engl. J. Med. 1980, 303, 833–841. [Google Scholar] [CrossRef]
- Chien, Y.-C.; Jan, C.-F.; Kuo, H.-S.; Chen, C.-J. Nationwide hepatitis B vaccination program in Taiwan: Effectiveness in the 20 years after it was launched. Epidemiol. Rev. 2006, 28, 126–135. [Google Scholar] [CrossRef]
- McMahon, B.J.; Bulkow, L.R.; Singleton, R.J.; Williams, J.; Snowball, M.; Homan, C.; Parkinson, A.J. Elimination of hepatocellular carcinoma and acute hepatitis B in children 25 years after a hepatitis B newborn and catch-up immunization program. Hepatology 2011, 54, 801–807. [Google Scholar] [CrossRef]
- Stroffolini, T.; Chiaramonte, M.; Tiribelli, C.; Villa, E.; Simonetti, R.; Rapicetta, M.; Stazi, M.; Bertin, T.; Crocè, S.; Trande, P.; et al. Hepatitis C virus infection, HBsAg carrier state and hepatocellular carcinoma: Relative risk and population attributable risk from a case-control study in Italy. J Hepatol. 1992, 16, 360–363. [Google Scholar] [CrossRef]
- Chiaramonte, M.; Stroffolini, T.; Vian, A.; Stazi, M.A.; Floreani, A.; Lorenzoni, U.; LoBello, S.; Farinati, F.; Naccarato, R. Rate of incidence of hepatocellular carcinoma in patients with compensated viral cirrhosis. Cancer 1999, 85, 2132–2137. [Google Scholar] [CrossRef]
- Rizzetto, M.; Canese, M.G.; Arico, S.; Crivelli, O.; Trepo, C.; Bonino, F.; Verme, G. Immunofluorescence detection of new antigen-antibody system (delta/anti-delta) associated to hepatitis B virus in liver and in serum of HBsAg carriers. Gut 1977, 18, 997–1003. [Google Scholar] [CrossRef] [PubMed]
- Sureau, C.; Negro, F. The hepatitis delta virus: Replication and pathogenesis. J. Hepatol. 2016, 64 (Suppl. S1), S102–S116. [Google Scholar] [CrossRef] [PubMed]
- Fattovich, G.; Giustina, G.; Christensen, E.; Pantalena, M.; Zagni, I.; Realdi, G.; Schalm, S.W. Influence of hepatitis delta virus infection on morbidity and mortality in compensated cirrhosis type B. The European Concerted Action on Viral Hepatitis (Eurohep). Gut 2000, 46, 420–426. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Baecker, A.; Wu, M.; Zhou, J.-Y.; Yang, J.; Han, R.-Q.; Wang, P.-H.; Jin, Z.-Y.; Liu, A.-M.; Gu, X.; et al. Interaction between tobacco smoking and hepatitis B virus infection on the risk of liver cancer in a Chinese population. Int. J. Cancer 2018, 142, 1560–1567. [Google Scholar] [CrossRef]
- Donato, F.; Tagger, A.; Gelatti, U.; Parrinello, G.; Boffetta, P.; Albertini, A.; Decarli, A.; Trevisi, P.; Ribero, M.L.; Martelli, C.; et al. Alcohol and hepatocellular carcinoma: The effect of lifetime intake and hepatitis virus infections in men and women. Am. J. Epidemiol. 2002, 155, 323–331. [Google Scholar] [CrossRef]
- Kim, K.; Choi, S.; Park, S.M. Association of High Body Mass Index and Hepatocellular Carcinoma in Patients with Chronic Hepatitis B Virus Infection: A Korean Population-Based Cohort Study. JAMA Oncol. 2018, 4, 737–739. [Google Scholar] [CrossRef]
- Tan, Y.; Wei, S.; Zhang, W.; Yang, J.; Yan, L. Type 2 diabetes mellitus increases the risk of hepatocellular carcinoma in subjects with chronic hepatitis B virus infection: A meta-analysis and systematic review. Cancer Manag. Res. 2019, 11, 705–713. [Google Scholar] [CrossRef]
- Raimondo, G.; Allain, J.-P.; Brunetto, M.R.; Buendia, M.-A.; Chen, D.-S.; Colombo, M.; Craxì, A.; Donato, F.; Ferrari, C.; Gaeta, G.B.; et al. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J. Hepatol. 2008, 49, 652–657. [Google Scholar] [CrossRef]
- Pollicino, T.; Saitta, C. Occult hepatitis B virus and hepatocellular carcinoma. World J. Gastroenterol. 2014, 20, 5951–5961. [Google Scholar] [CrossRef]
- Stroffolini, T.; Almasio, P.L.; Persico, M.; Bollani, S.; Benvegnù, L.; Di Costanzo, G.; Pastore, G.; Aghemo, A.; Stornaiuolo, G.; Mangia, A.; et al. Italian Association of the Study of the Liver Disease (AISF). Lack of correlation between serum anti-HBcore detectability and hepatocellular carcinoma in patients with HCV-related cirrhosis. Am. J. Gastroenterol. 2008, 103, 1966–1972. [Google Scholar] [CrossRef]
- Raimondo, G.; Locarnini, S.; Pollicino, T.; Levrero, M.; Zoulim, F.; Lok, A.S.; Taormina Workshop on Occult HBV Infection Faculty Members. Update of the statements on biology and clinical impact of occult hepatitis B virus infection. J. Hepatol. 2019, 71, 397–408. [Google Scholar] [CrossRef] [PubMed]
- Sohn, W.; Chang, Y.; Cho, Y.K.; Hong, Y.S.; Ryu, S. Isolated Hepatitis B Core Antibody Positivity and Long-Term Liver-Related Mortality in Korea: A Cohort Study. Am. J. Gastroenterol. 2023, 118, 95–104. [Google Scholar] [CrossRef] [PubMed]
- Brechot, C.; Scotto, J.; Charnay, P.; Hadchouel, M.; Degos, F.; Trepo, C.; Tiollais, P. Detection of hepatitis B virus DNA in liver and serum: A direct appraisal of the chronic carrier state. Lancet 1981, 2, 765–768. [Google Scholar] [CrossRef] [PubMed]
- Chen, D.S.; Hoyer, B.H.; Nelson, J.; Purcell, R.H.; Gerin, J.L. Detection and properties of hepatitis B viral DNA in liver tissues from patients with hepatocellular carcinoma. Hepatology 1982, 2, 942–946. [Google Scholar]
- Chang, M.H.; Chen, D.S.; Hsu, H.C.; Hsu, H.Y.; Lee, C.Y. Maternal transmission of hepatitis B virus in childhood hepatocellular carcinoma. Cancer 1989, 64, 2377–2380. [Google Scholar] [CrossRef]
- Chang, M.H.; Chen, D.-S.; Hsu, H.-C.; Hsu, H.-Y.; Lee, C.-Y. Hepatitis B virus integration in hepatitis B virus-related hepatocellular carcinoma in childhood. Hepatology 1991, 13, 316–320. [Google Scholar] [CrossRef]
- Liang, T.J. Hepatitis B: The virus and disease. Hepatology 2009, 49, S13–S21. [Google Scholar] [CrossRef]
- Rizzo, G.E.M.; Cabibbo, G.; Craxì, A. Hepatitis B Virus-Associated Hepatocellular Carcinoma. Viruses 2022, 14, 986. [Google Scholar] [CrossRef]
- Stroffolini, T.; Morisco, F.; Ferrigno, L.; Pontillo, G.; Iantosca, G.; Cossiga, V.; Crateri, S.; Tosti, M.E.; The Seieva Collaborating Group. Effectiveness of Hepatitis B Vaccination Campaign in Italy: Towards the Control of HBV Infection for the First Time in a European Country. Viruses 2022, 14, 245. [Google Scholar] [CrossRef]
- Lemoine, M.; Eholié, S.; Lacombe, S. Reducing the neglected burden of viral hepatitis in Africa: Strategies for a global approach. J. Hepatol. 2015, 62, 469–476. [Google Scholar] [CrossRef]
- Lemoine, M.; Thursz, M.R. Battefield against hepatitis B and HCC in Africa. J. Hepatol. 2017, 66, 645–654. [Google Scholar] [CrossRef] [PubMed]
- Iqbal, K.; Klevens, R.M.; Kainer, M.A.; Baumgartner, J.; Gerard, K.; Poissant, T.; Sweet, K.; Vonderwahl, C.; Knickerbocker, T.; Khudyakov, Y.; et al. Epidemiology of Acute Hepatitis B in the United States from Population-Based Surveillance, 2006–2011. Clin. Infect. Dis. 2015, 61, 584–592. [Google Scholar] [CrossRef] [PubMed]
- Ly, K.N.; Xing, J.; Spradling, P.R. Trends in Prevalence and Characteristics of Resolved and Current Hepatitis B Among US-Born Persons: National Health and Nutrition Examination Survey, 2001–2018. J. Infect. Dis. 2021, 224, 804–812. [Google Scholar] [CrossRef] [PubMed]
- 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, 370–398. [Google Scholar] [CrossRef]
- Papatheodoridis, G.V.; Idilman, R.; Dalekos, G.N.; Buti, M.; Chi, H.; van Boemmel, F.; Calleja, J.L.; Sypsa, V.; Goulis, J.; Manolakopoulos, S.; et al. The risk of hepatocellular carcinoma decreases after the first 5 years of entecavir or tenofovir in Caucasians with chronic hepatitis B. Hepatology 2017, 66, 1444–1453. [Google Scholar] [CrossRef]
- Lopatin, U. Drugs in the Pipeline for HBV. Clin. Liver Dis. 2019, 23, 535–555. [Google Scholar] [CrossRef]
- Yu, T.; Zhang, M.; Zhang, H.; Zheng, J.; Shen, C.; Jiang, N.; Zou, L.; Wang, J.; Yu, Y.; Zhang, Q.; et al. Evidence of Residual Ongoing Viral Replication in Chronic Hepatitis B Patients Successfully Treated with Nucleos(t)ide Analogues. J. Infect. Dis. 2023, 227, 675–685. [Google Scholar] [CrossRef]
- Kuo, G.; Choo, Q.-L.; Alter, H.; Gitnick, G.; Redeker, A.; Purcell, R.; Miyamura, T.; Dienstag, J.; Stevens, C.; Tegtmeier, G.E.; et al. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 1989, 244, 362–364. [Google Scholar] [CrossRef]
- Alter, H.J. The hepatitis C virus and its relationship to the clinical spectrum of NANB hepatitis. J. Gastroenterol. Hepatol. 1990, 5 (Suppl. S1), 78–94. [Google Scholar] [CrossRef]
- Yu, M.C.; Tong, M.J.; Coursaget, P.; Ross, R.K.; Govindarajan, S.; Henderson, B.E. Prevalence of hepatitis B and C viral markers in black and white patients with hepatocellular carcinoma in the United States. J. Natl. Cancer Inst. 1990, 82, 1038–1041. [Google Scholar] [CrossRef]
- Simonetti, R.G.; Cammà, C.; Fiorello, F.; Cottone, M.; Rapicetta, M.; Marino, L.; Fiorentino, G.; Craxi, A.; Ciccaglione, A.; Giuseppetti, R.; et al. Hepatitis C virus infection as a risk factor for hepatocellular carcinoma in patients with cirrhosis. A case-control study. Ann. Intern. Med. 1992, 116, 97–102. [Google Scholar] [CrossRef] [PubMed]
- Akinyemiju, T.; Abera, S.; Ahmed, M.; Alam, N.; Alemayohu, M.A.; Allen, C.; Al-Raddadi, R.; Alvis-Guzman, N.; Amoako, Y.; Global Burden of Disease Liver Cancer Collaboration; et al. The Burden of Primary Liver Cancer and Underlying Etiologies From 1990 to 2015 at the Global, Regional, and National Level: Results from the Global Burden of Disease Study 2015. JAMA Oncol. 2017, 3, 1683–1691. [Google Scholar] [CrossRef] [PubMed]
- Graham, C.S.; Baden, L.R.; Yu, E.; Mrus, J.M.; Carnie, J.; Heeren, T.; Koziel, M.J. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: A meta-analysis. Clin. Infect. Dis. 2001, 33, 562–569. [Google Scholar] [CrossRef] [PubMed]
- Tovo, C.V.; Becker, S.C.D.C.; de Almeida, P.R.L.; Galperim, B.; Chaves, S. Progression of liver fibrosis in monoinfected patients by hepatitis C virus and coinfected by HCV and human immunodeficiency virus. Arq. Gastroenterol. 2013, 50, 19–22. [Google Scholar] [CrossRef] [PubMed]
- Puoti, M.; Prestini, K.; Putzolu, V.; Zanini, B.; Baiguera, C.; Antonini, M.G.; Pagani, P.; Airoldi, M.; Carosi, G. HIV/HCV co-infection: Natural history. J. Biol. Regul. Homeost. Agents 2003, 17, 144–146. [Google Scholar]
- Salmon-Ceron, D.; Nahon, P.; Layese, R.; Bourcier, V.; Sogni, P.; Bani-Sadr, F.; Audureau, E.; Merchadou, L.; Dabis, F.; Wittkop, L.; et al. ANRS CO12 CirVir and ANRS CO13 HEPAVIH study groups. Human Immunodeficiency Virus/Hepatitis C Virus (HCV) Co-infected Patients with Cirrhosis Are No Longer at Higher Risk for Hepatocellular Carcinoma or End-Stage Liver Disease as Compared to HCV Mono-infected Patients. Hepatology 2019, 70, 939–954. [Google Scholar] [CrossRef]
- Chuang, S.-C.; Lee, Y.-C.A.; Hashibe, M.; Dai, M.; Zheng, T.; Boffetta, P. Interaction between cigarette smoking and hepatitis B and C virus infection on the risk of liver cancer: A meta-analysis. Cancer Epidemiol. Biomark. Prev. 2010, 19, 1261–1268. [Google Scholar] [CrossRef]
- Dyal, H.K.; Aguilar, M.; Bartos, G.; Holt, E.W.; Bhuket, T.; Liu, B.; Cheung, R.; Wong, R.J. Diabetes Mellitus Increases Risk of Hepatocellular Carcinoma in Chronic Hepatitis C Virus Patients: A Systematic Review. Dig. Dis. Sci. 2016, 61, 636–645. [Google Scholar] [CrossRef]
- Castera, L.; Hézode, C.; Roudot-Thoraval, F.; Bastie, A.; Zafrani, E.-S.; Pawlotsky, J.-M.; Dhumeaux, D. Worsening of steatosis is an independent factor of fibrosis progression in untreated patients with chronic hepatitis C and paired liver biopsies. Gut 2003, 52, 288–292. [Google Scholar] [CrossRef]
- Poynard, T.; Bedossa, P.; Opolon, P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 1997, 349, 825–832. [Google Scholar] [CrossRef]
- Ikeda, K.; Saitoh, S.; Suzuki, Y.; Kobayashi, M.; Tsubota, A.; Koida, I.; Arase, Y.; Fukuda, M.; Chayama, K.; Murashima, N.; et al. Disease progression and hepatocellular carcinogenesis in patients with chronic viral hepatitis: A prospective observation of 2215 patients. J. Hepatol. 1998, 28, 930–938. [Google Scholar] [CrossRef] [PubMed]
- Tagger, A.; Donato, F.; Ribero, M.L.; Chiesa, R.; Portera, G.; Gelatti, U.; Albertini, A.; Fasola, M.; Boffetta, P.; Nardi, G. Case-control study on hepatitis C virus (HCV) as a risk factor for hepatocellular carcinoma: The role of HCV genotypes and the synergism with hepatitis B virus and alcohol. Brescia HCC Study. Int. J. Cancer 1999, 81, 695–699. [Google Scholar] [CrossRef]
- Vandenbulcke, H.; Moreno, C.; Colle, I.; Knebel, J.-F.; Francque, S.; Sersté, T.; George, C.; de Galocsy, C.; Laleman, W.; Delwaide, J.; et al. Alcohol intake increases the risk of HCC in hepatitis C virus-related compensated cirrhosis: A prospective study. J. Hepatol. 2016, 65, 543–551. [Google Scholar] [CrossRef] [PubMed]
- Aloman, C.; Gehring, S.; Wintermeyer, P.; Kuzushita, N.; Wands, J.R. Chronic ethanol consumption impairs cellular immune responses against HCV NS5 protein due to dendritic cell dysfunction. Gastroenterology 2007, 132, 698–708. [Google Scholar] [CrossRef] [PubMed]
- Pianko, S.; Patella, S.; Sievert, W. Alcohol consumption induces hepatocyte apoptosis in patients with chronic hepatitis C infection. J. Gastroenterol. Hepatol. 2000, 15, 798–805. [Google Scholar] [CrossRef] [PubMed]
- Stroffolini, T.; Sagnelli, E.; Sagnelli, C.; Morisco, F.; Babudieri, S.; Furlan, C.; Pirisi, M.; Russello, M.; Smedile, A.; Pisaturo, M.; et al. Characteristics and Changes over Time of Alcohol-Related Chronic Liver Diseases in Italy. Can. J. Gastroenterol. Hepatol. 2018, 2018, 9151820. [Google Scholar] [CrossRef]
- Matsuzaki, K.; Murata, M.; Yoshida, K.; Sekimoto, G.; Uemura, Y.; Sakaida, N.; Kaibori, M.; Kamiyama, Y.; Nishizawa, M.; Fujisawa, J.; et al. Chronic inflammation associated with hepatitis C virus infection perturbs hepatic transforming growth factor beta signaling, promoting cirrhosis and hepatocellular carcinoma. Hepatology 2007, 46, 48–57. [Google Scholar] [CrossRef]
- Hino, O.; Kajino, K.; Umeda, T.; Arakawa, Y. Understanding the hypercarcinogenic state in chronic hepatitis: A clue to the prevention of human hepatocellular carcinoma. J. Gastroenterol. 2002, 37, 883–887. [Google Scholar] [CrossRef]
- Andriulli, A.; Stroffolini, T.; Mariano, A.; Valvano, M.R.; Grattagliano, I.; Ippolito, A.M.; Grossi, A.; Brancaccio, G.; Coco, C.; Russello, M.; et al. Declining prevalence and increasing awareness of HCV infection in Italy: A population-based survey in five metropolitan areas. Eur. J. Intern. Med. 2018, 53, 79–84. [Google Scholar] [CrossRef]
- Stroffolini, T.; Lombardi, A.; Ciancio, A.; Fontana, R.; Colloredo, G.; Marignani, M.; Vinci, M.; Morisco, F.; Babudieri, S.; Ferrigno, L.; et al. Hepatitis B vaccine coverage and risk factors for lack of vaccination in subjects with HBsAg negative liver cirrhosis in Italy: Still, much work should be done. Dig. Liver Dis. 2021, 53, 1315–1319. [Google Scholar] [CrossRef]
- Khan, F.; Peltekian, K.M.; Peterson, T.C. Effect of interferon-alpha, ribavirin, pentoxifylline, and interleukin-18 antibody on hepatitis C sera-stimulated hepatic stellate cell proliferation. J. Interferon Cytokine Res. 2008, 28, 643–651. [Google Scholar] [CrossRef] [PubMed]
- Bruno, S.; Stroffolini, T.; Colombo, M.; Bollani, S.; Benvegnù, L.; Mazzella, G.; Ascione, A.; Santantonio, T.; Piccinino, F.; Andreone, P.; et al. Italian Association of the Study of the Liver Disease (AISF). Sustained virological response to interferon-alpha is associated with improved outcome in HCV-related cirrhosis: A retrospective study. Hepatology 2007, 45, 579–587. [Google Scholar] [CrossRef] [PubMed]
- Morgan, R.L.; Baack, B.; Smith, B.D.; Yartel, A.; Pitasi, M.; Falck-Ytter, Y. Eradication of hepatitis C virus infection and the development of hepatocellular carcinoma: A meta-analysis of observational studies. Ann. Intern. Med. 2013, 158, 329–337. [Google Scholar] [CrossRef] [PubMed]
- Everson, G.T.; Jensen, D.M.; Craig, J.R.; van Leeuwen, D.J.; Bain, V.G.; Ehrinpreis, M.N.; Albert, D.; Joh, T.; Witt, K.; the Consensus Interferon Study Group. Efficacy of interferon treatment for patients with chronic hepatitis C: Comparison of response in cirrhotics, fibrotics, or nonfibrotics. Hepatology 1999, 30, 271–276. [Google Scholar] [CrossRef]
- Falade-Nwulia, O.; Suarez-Cuervo, C.; Nelson, D.R.; Fried, M.W.; Segal, J.B.; Sulkowski, M.S. Oral Direct-Acting Agent Therapy for Hepatitis C Virus Infection: A Systematic Review. Ann. Intern. Med. 2017, 166, 637–648. [Google Scholar] [CrossRef]
- Backus, L.I.; Belperio, P.S.; Shahoumian, T.A.; Mole, L.A. Impact of Sustained Virologic Response with Direct-Acting Antiviral Treatment on Mortality in Patients with Advanced Liver Disease. Hepatology 2019, 69, 487–497. [Google Scholar] [CrossRef]
- Calvaruso, V.; Cabibbo, G.; Cacciola, I.; Petta, S.; Madonia, S.; Bellia, A.; Tinè, F.; Distefano, M.; Licata, A.; Giannitrapani, L.; et al. Rete Sicilia Selezione Terapia–HCV (RESIST-HCV). Incidence of Hepatocellular Carcinoma in Patients With HCV-Associated Cirrhosis Treated with Direct-Acting Antiviral Agents. Gastroenterology 2018, 155, 411–421.e4. [Google Scholar] [CrossRef]
- Stroffolini, T.; Sagnelli, E.; Sagnelli, C.; Morisco, F.; Babudieri, S.; Furlan, C.; Pirisi, M.; Russello, M.; Smedile, A.; Pisaturo, M.; et al. Decreasing role of HCV and HBV infections as aetiological factors of hepatocellular carcinoma in Italy. Infection 2019, 47, 805–810. [Google Scholar] [CrossRef]
- Vitale, A.; Svegliati-Baroni, G.; Ortolani, A.; Cucco, M.; Riva, G.V.D.; Giannini, E.G.; Piscaglia, F.; Rapaccini, G.; Di Marco, M.; Caturelli, E.; et al. Epidemiological trends and trajectories of MAFLD-associated hepatocellular carcinoma 2002–2023: The ITA.LI.CA database. Gut 2023, 72, 141–152. [Google Scholar] [CrossRef]
- Mittal, S.; El-Serag, H.B.; Sada, Y.H.; Kanwal, F.; Duan, Z.; Temple, S.; May, S.B.; Kramer, J.R.; Richardson, P.A.; Davila, J.A. Hepatocellular Carcinoma in the Absence of Cirrhosis in United States Veterans is Associated with Nonalcoholic Fatty Liver Disease. Clin. Gastroenterol. Hepatol. 2016, 14, 124–131.e1. [Google Scholar] [CrossRef]
- Piscaglia, F.; Svegliati-Baroni, G.; Barchetti, A.; Pecorelli, A.; Marinelli, S.; Tiribelli, C.; Bellentani, S.; HCC-NAFLD Italian Study Group. Clinical patterns of hepatocellular carcinoma in nonalcoholic fatty liver disease: A multicenter prospective study. Hepatology 2016, 63, 827–838. [Google Scholar] [CrossRef] [PubMed]
- Pais, R.; Fartoux, L.; Goumard, C.; Scatton, O.; Wendum, D.; Rosmorduc, O.; Ratziu, V. Temporal trends, clinical patterns and outcomes of NAFLD-related HCC in patients undergoing liver resection over a 20-year period. Aliment. Pharm. Ther. 2017, 46, 856–863. [Google Scholar] [CrossRef] [PubMed]
- Chen, B.; Garmire, L.; Calvisi, D.F.; Chua, M.-S.; Kelley, R.K.; Chen, X. Harnessing big ‘omics’ data and AI for drug discovery in hepatocellular carcinoma. Nat. Rev. Gastroenterol. Hepatol. 2020, 17, 238–251, Erratum in Nat. Rev. Gastroenterol. Hepatol. 2020. https://doi.org/10.1038/s41575-020-0288-6. [Google Scholar] [CrossRef] [PubMed]
- Song, G.; Shi, Y.; Zhang, M.; Goswami, S.; Afridi, S.; Meng, L.; Ma, J.; Chen, Y.; Lin, Y.; Zhang, J.; et al. Global immune characterization of HBV/HCV-related hepatocellular carcinoma identifies macrophage and T-cell subsets associated with disease progression. Cell Discov. 2020, 6, 90. [Google Scholar] [CrossRef]
- Lou, W.; Liu, J.; Ding, B.; Chen, D.; Xu, L.; Ding, J.; Jiang, D.; Zhou, L.; Zheng, S.; Fan, W. Identification of potential miRNA-mRNA regulatory network contributing to pathogenesis of HBV-related HCC. J. Transl. Med. 2019, 17, 7. [Google Scholar] [CrossRef]
- Sun, S.; Li, Y.; Han, S.; Jia, H.; Li, X.; Li, X. A comprehensive genome-wide profiling comparison between HBV and HCV infected hepatocellular carcinoma. BMC Med. Genom. 2019, 12, 147. [Google Scholar] [CrossRef]
- Andrisani, O. Epigenetic mechanisms in hepatitis B virus-associated hepatocellular carcinoma. Hepatoma Res. 2021, 7, 12. [Google Scholar] [CrossRef]
- Zeisel, M.B.; Guerrieri, F.; Levrero, M. Host Epigenetic Alterations and Hepatitis B Virus-Associated Hepatocellular Carcinoma. J. Clin. Med. 2021, 10, 1715. [Google Scholar] [CrossRef]
- Hamdane, N.; Jühling, F.; Crouchet, E.; El Saghire, H.; Thumann, C.; Oudot, M.A.; Bandiera, S.; Saviano, A.; Ponsolles, C.; Roca Suarez, A.A.R.; et al. HCV-Induced Epigenetic Changes Associated with Liver Cancer Risk Persist After Sustained Virologic Response. Gastroenterology 2019, 156, 2313–2329.e7. [Google Scholar] [CrossRef]
- Perez, S.; Kaspi, A.; Domovitz, T.; Davidovich, A.; Lavi-Itzkovitz, A.; Meirson, T.; Alison Holmes, J.; Dai, C.-Y.; Huang, C.-F.; Chung, R.T.; et al. Hepatitis C virus leaves an epigenetic signature post cure of infection by direct-acting antivirals. PLoS Genet. 2019, 15, e1008181. [Google Scholar] [CrossRef]
- Lupberger, J.; Croonenborghs, T.; Suarez, A.A.R.; Van Renne, N.; Jühling, F.; Oudot, M.A.; Virzì, A.; Bandiera, S.; Jamey, C.; Meszaros, G.; et al. Combined Analysis of Metabolomes, Proteomes, and Transcriptomes of Hepatitis C Virus-Infected Cells and Liver to Identify Pathways Associated with Disease Development. Gastroenterology 2019, 157, 537–551.e9. [Google Scholar] [CrossRef] [PubMed]
HBsAg | Anti-HCV | OR (CI 95%) |
---|---|---|
− | − | 1 |
+ | − | 13.3 (5.5–32.2) |
− | + | 21.3 (8.8–51.5) |
+ | + | 77.0 (3.8–142.1) |
Ever-Smoker | HBsAg+ | OR (CI 95%) |
---|---|---|
No | No | 1 |
No | Yes | 7.66 (6.05–9.71) |
Yes | No | 1.25 (1.03–1.52) |
Yes | Yes | 15.68 (12.06–20.39) |
Primary prevention |
|
Secondary prevention |
|
Alcohol Intake (g/day) | O.R. (95% CI) for HCC in HCV-Positive Subjects |
---|---|
0–40 | 26.1 (12.6–54.0) |
41–80 | 62.6 (23.3–168.0) |
>80 | 126.0 (42.8–379.0) |
Primary prevention |
|
Secondary prevention |
|
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Stroffolini, T.; Stroffolini, G. A Historical Overview on the Role of Hepatitis B and C Viruses as Aetiological Factors for Hepatocellular Carcinoma. Cancers 2023, 15, 2388. https://doi.org/10.3390/cancers15082388
Stroffolini T, Stroffolini G. A Historical Overview on the Role of Hepatitis B and C Viruses as Aetiological Factors for Hepatocellular Carcinoma. Cancers. 2023; 15(8):2388. https://doi.org/10.3390/cancers15082388
Chicago/Turabian StyleStroffolini, Tommaso, and Giacomo Stroffolini. 2023. "A Historical Overview on the Role of Hepatitis B and C Viruses as Aetiological Factors for Hepatocellular Carcinoma" Cancers 15, no. 8: 2388. https://doi.org/10.3390/cancers15082388