Occurrence of hepatocellular carcinoma after direct-acting antiviral therapy for hepatitis C virus infection: literature review and risk analysis

References

• Aleman S, Rahbin N, Weiland O, et al. A risk for hepatocellular carcinoma persists long-term after sustained virologic response in patients with hepatitis C-associated liver cirrhosis. Clin Infect Dis. 2013;57:230–236.
   PubMed Web of Science ®Google Scholar
• El-Serag HB, Kanwal F, Richardson P, et al. Risk of hepatocellular carcinoma after sustained virological response in veterans with hepatitis C virus infection. Hepatology. 2016;64:130–137.
   PubMed Web of Science ®Google Scholar
• Van der Meer AJ, Feld JJ, Hofer H, et al. Risk of cirrhosis-related complications in patients with advanced fibrosis following hepatitis C virus eradication. J Hepatol. 2017;66:485–493.
   PubMed Web of Science ®Google Scholar
• Morgan RL, Baak B, Smith BD, et al. 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.
   PubMed Web of Science ®Google Scholar
• Kozbial K, Moser S, Schwarzer R, et al. Unexpected high incidence of hepatocellular carcinoma in cirrhotic patients with sustained virologic response following interferon-free direct-acting antiviral treatment. J Hepatol. 2016;65:856–858.
   PubMed Web of Science ®Google Scholar
• Conti F, Buonfiglioli F, Scuteri A, et al. Early occurrence and recurrence of hepatocellular carcinoma in HCV-related cirrhosis treated with direct-acting antivirals. J Hepatol. 2016;65:727–733.
   PubMed Web of Science ®Google Scholar
• Reig M, Marino Z, Perello C, et al. Unexpected high rate of early tumor recurrence in patients with HCV-related HCC undergoing interferon-free therapy. J Hepatol. 2016;65:719–726.
   PubMed Web of Science ®Google Scholar
• Lemon SM, McGivern DR. Is hepatitis C virus carcinogenic? Gastroenterology. 2012;142:1274–1278.
   PubMedGoogle Scholar
• Godfrey DI, Uldrich AP, McCluskey J, et al. The burgeoning family of unconventional T cells. Nat Immunol. 2015;16:1114–1123.
   PubMed Web of Science ®Google Scholar
• Martin B, Hennecke N, Lohmann V, et al. Restoration of HCV-specific CD8 + T cell function by interferon-free therapy. J Hepatol. 2014;61:538–543.
   PubMed Web of Science ®Google Scholar
• Serti E, Chepa-Lotrea X, Kim YJ, et al. Successful interferon-free therapy of chronic hepatitis C virus infection normalizes natural killer cell function. Gastroenterology. 2015;149:190–200.
   PubMed Web of Science ®Google Scholar
• Spaan M, van Oord G, Kreefft K, et al. Immunological analysis during interferon-free therapy for chronic hepatitis C virus infection reveals modulation of the natural killer cell compartment. J Infect Dis. 2016;213:216–223.
   PubMed Web of Science ®Google Scholar
• Guarino M, Viganò L, Ponziani FR, et al. Special Interest Group on Hepatocellular carcinoma and new anti-HCV therapies of the Italian Association for the Study of the Liver. Recurrence of hepatocellular carcinoma after direct acting antiviral treatment for hepatitis C virus infection: literature review and risk analysis. Dig Liver Dis. 2018 Nov;50(11):1105–1114.
   PubMedGoogle Scholar
• Nakao Y, Hashimoto S, Abiru S, et al. Rapidly growing, moderately differentiated HCC: a clinicopathological characteristic of HCC occurrence after IFN-free DAA therapy? J Hepatol. 2017 Nov 13. pii. [Epub ahead of print]. DOI: 10.1016/j.jhep.2017.11.011
   PubMed Web of Science ®Google Scholar
• Cammà C, Leandro G. Direct antiviral agents and risk of HCC: waiting for Godot. J Hepatol. 2018;68:614–616.
   PubMed Web of Science ®Google Scholar
• Waziry R, Amin J, Law M, et al. Reply to: “Direct antiviral agents and risk of HCC: waiting for Godot”. J Hepatol. 2018;68:616–617.
   PubMed Web of Science ®Google Scholar
• Cardoso H, Vale AM, Rodrigues S, et al. High incidence of hepatocellular carcinoma following successful interferon-free antiviral therapy for hepatitis C associated cirrhosis. J Hepatol. 2016;65:1070–1071.
   PubMed Web of Science ®Google Scholar
• Waziry R, Hajarizadeh B, Grebely J, et al. Hepatocellular carcinoma risk following direct-acting antiviral HCV therapy: a systematic review, meta-analyses, and meta-regression. J Hepatol. 2017;67:1204–1212.
   PubMed Web of Science ®Google Scholar
• Ravi S, Axley P, Jones D, et al. Unusually high rates of hepatocellular carcinoma after treatment with direct-acting antiviral therapy for hepatitis c related cirrhosis. Gastroenterology. 2017 Mar;152(4):911–912.
   PubMed Web of Science ®Google Scholar
• Kanwal F, Kramer J, Asch SM, et al. Risk of hepatocellular cancer in HCV patients treated with direct-antiviral agents. Gastroenterology. 2017;153:996–1005.
   PubMed Web of Science ®Google Scholar
• Li DK, Ren Y, Fierer DS, et al. The short-term incidence of hepatocellular carcinoma is not increased after hepatitis C treatment with direct-acting antivirals: an ERCHIVES study. Hepatology. 2018;67:2244–2253.
   PubMed Web of Science ®Google Scholar
• Cheung MC, Walker AJ, Hudson BE, et al. Outcomes after successful direct-acting antiviral therapy for patients with chronic hepatitis C and decompensated cirrhosis. J Hepatol. 2016;65:741–747.
   PubMed Web of Science ®Google Scholar
• Renzulli M, Buonfiglioli F, Conti F, et al. Imaging features of microvascular invasion in hepatocellular carcinoma developed after direct-acting antiviral therapy in HCV-related cirrhosis. Eur Radiol. 2018;28:506–513.
   PubMed Web of Science ®Google Scholar
• Backus LI, Belperio PS, Shahoumian TA, et al. Impact of sustained virologic response with direct-acting antiviral treatment on mortality in patients with advanced liver disease. Hepatology. 2017 Jul 27. [Epub ahead of print]. DOI:10.1002/hep.29408
   PubMedGoogle Scholar
• Innes H, Barclay ST, Hayes PC, et al. The risk of hepatocellular carcinoma in cirrhotic patients with hepatitis C and sustained viral response: role of the treatment regimen. J Hepatol. 2017 Nov 16. [Epub ahead of print]. DOI:10.1016/j.jhep.2017.10.033
   Google Scholar
• Ida H, Hagiwara S, Kono M, et al. Hepatocellular carcinoma after achievement of sustained viral response with daclatasvir and asunaprevir in patients with chronic hepatitis C virus infection. Dig Dis. 2017;35:565–573.
   PubMed Web of Science ®Google Scholar
• Nahon P, Bourcier V, Layese R, et al. Eradication of hepatitis C virus infection in patients with cirrhosis reduces risk of liver and non-liver complications. Gastroenterology. 2017;152:142–156.
   PubMed Web of Science ®Google Scholar
• Faillaci F, Marzi L, Critelli R, et al. Liver Angiopoietin-2 is a key predictor of de novo or recurrenthepatocellular cancer after HCV direct-acting antivirals. Hepatology. 2018;68:1010–1024.
   PubMed Web of Science ®Google Scholar
• Ioannou GN, Green PK, Berry K. HCV eradication induced by direct-acting antiviral agents reduces the risk of hepatocellular carcinoma. J Hepatol. 2017 Sep 5. [Epub ahead of print]. DOI:10.1016/j.jhep.2017.08.030.
   Web of Science ®Google Scholar
• Calvaruso V, Cabibbo G, Cacciola I, et al. Incidence of hepatocellular carcinoma in patients with HCV-associated cirrhosis treated with direct-acting antiviral agents. Gastroenterology. 2018;155:411–421.
   PubMed Web of Science ®Google Scholar
• Kobayashi M, Suzuki F, Fujiyama S, et al. Sustained virologic response by direct antiviral agents reduces the incidence of hepatocellular carcinoma in patients with HCV infection. J Med Virol. 2017;89:476–483.
   PubMed Web of Science ®Google Scholar
• Nagaoki Y, Imamura M, Aikata H, et al. The risks of hepatocellular carcinoma development after HCV eradication are similar between patients treated with peg-interferon plus ribavirin and direct-acting antiviral therapy. PLoSOne. 2017 Aug 10;12(8):e0182710.
   PubMed Web of Science ®Google Scholar
• Ogawa E, Furusyo N, Nomura H, et al. Short-term risk of hepatocellular carcinoma after hepatitis C virus eradication following direct-acting anti-viral treatment. Aliment Pharmacol Ther. 2018;47:104–113.
   PubMed Web of Science ®Google Scholar
• Foster GR, Irving WL, Cheung MC, et al. Impact of direct acting antiviral therapy in patients with chronic hepatitis C and decompensated cirrhosis. J Hepatol. 2016;64:1224–1231.
   PubMed Web of Science ®Google Scholar
• Nagata H, Nakagawa M, Asahina Y, et al. Effect of interferon-based and -free therapy on early occurrence and recurrence of hepatocellular carcinoma in chronic hepatitis C. J Hepatol. 2017;67:933–939.
   PubMed Web of Science ®Google Scholar
• Finkelmeier F, Dultz G, Peiffer KH, et al. Risk of de novo hepatocellular carcinoma after HCV treatment with direct-acting antivirals. Liver Cancer. 2018 May;7(2):190–204.
   PubMed Web of Science ®Google Scholar
• Calleja JL, Crespo J, Rincón D, et al. Effectiveness, safety and clinical outcomes of direct-acting antiviral therapy in HCV genotype 1 infection: results from a Spanish real-world cohort. J Hepatol. 2017 Jun;66(6):1138–1148.
   PubMed Web of Science ®Google Scholar
• Axley P, Ahmed Z, Ravi S, et al. Hepatitis C virus and hepatocellular carcinoma: a narrative review. J Clin Transl Hepatol. 2018;28(6):79–84.
   Google Scholar
• Konjeti VR, John BV. Interaction between hepatocellular carcinoma and hepatitis C eradication with direct-acting antiviral therapy. Curr Treat Options Gastroenterol. 2018;16:203–214.
   PubMedGoogle Scholar
• Butt AS, Sharif F, Abid S. Impact of direct acting antivirals on occurrence and recurrence of hepatocellular carcinoma: biologically plausible or an epiphenomenon? World J Hepatol. 2018;27(10):267–276.
   Google Scholar
• Maida M, Cabibbo G, Cammà C. Increased incidence or recurrence of hepatocellular carcinoma in hepatitis C virus cirrhotic patients treated with direct-acting antivirals: myth or fact? Expert Rev Anticancer Ther. 2018;18:307–309.
   PubMed Web of Science ®Google Scholar
• Roche B, Coilly A, Duclos-Vallee JC, et al. The impact of treatment of hepatitis C with DAAs on the occurrence of HCC. Liver Int. 2018;38:139–145.
   PubMed Web of Science ®Google Scholar
• Robert SB Jr. The possible association between DAA treatment for HCV infection and HCC recurrence. Gastroenterol Hepatol (N Y). 2016;12:776–779.
   PubMedGoogle Scholar
• Grandhe S, Frenette CT. Occurrence and recurrence of hepatocellular carcinoma after successful direct-acting antiviral therapy for patients with chronic hepatitis C virus infection. Gastroenterol Hepatol (N Y). 2017;13:421–425.
   PubMedGoogle Scholar
• Maan R, Feld JJ. Risk for hepatocellular carcinoma after hepatitis C virus antiviral therapy with direct-acting antivirals: case closed? Gastroenterology. 2017;153:890–892.
   PubMed Web of Science ®Google Scholar
• Ogata F, Kobayashi M, Akuta N, et al. Outcome of all-oral direct-acting antiviral regimens on the rate of development of hepatocellular carcinoma in patients with hepatitis C virus genotype 1-related chronic liver disease. Oncology. 2017;93:92–98.
   PubMed Web of Science ®Google Scholar
• Romano A, Angeli P, Piovesan S, et al. Newly diagnosed hepatocellular carcinoma in patients with advanced hepatitis C treated with DAAs: a prospective population study. J Hepatol. 2018;69(2):345–352.
   PubMed Web of Science ®Google Scholar
• Veldt BJ, Chen W, Heathcote EJ, et al. Increased risk of hepatocellular carcinoma among patients with hepatitis C cirrhosis and diabetes mellitus. Hepatology. 2008;47:1856–1862.
   PubMed Web of Science ®Google Scholar
• Cucchetti A, D’Amico G, Trevisani F, et al. Effect of direct-acting antivirals on furure occurrence of hepatocellular carcinoma in compensated cirrhotic patients. Dig Dis. 2018;50:156–162.
   Google Scholar
• Kozbial K, Moser S, Al-Zoairy R, et al. Follow-up of sustained virologic responders with hepatitis C and advanced liver disease after interferon/ribavirin-free treatment. Liver Int. 2017;38:1028–1035.
   PubMed Web of Science ®Google Scholar
• D’Amico G, Pasta L, Morabito A, et al. Competing risks and prognostic stages of cirrhosis: a 25-year inception cohort study of 494 patients. Aliment Pharmacol Ther. 2014;39:1180–1193.
   PubMed Web of Science ®Google Scholar
• Lu M, Li J, Rupp LB, et al. CHeCS Investigators. Hepatitis C treatment failure is associated with increased risk of hepatocellular carcinoma. J Viral Hepat. 2016 Sep;23(9):718–729.
   PubMed Web of Science ®Google Scholar
• Nahon P, Layese R, Bourcier V, et al. ANRS CO12 CirVir group. Incidence of hepatocellular carcinoma after direct antiviral therapy for HCV in patients with cirrhosis included in surveillance programs. Gastroenterology. 2018 Nov;155(5):1436–1450.e6.
   PubMed Web of Science ®Google Scholar
• Chen MF, Liaw YF, Chen MF. Alpha fetoprotein and hepatic regeneration. Gastroenterology. 1979;76:660.
   PubMed Web of Science ®Google Scholar
• Asahina Y, Tsuchiya K, Nishimura T, et al. α-fetoprotein levels after interferon therapy and risk of hepatocarcinogenesis in chronic hepatitis C. Hepatology. 2013;58:1253–1262.
   PubMed Web of Science ®Google Scholar
• Villani R, Facciorusso A, Bellanti F, et al. DAAs rapidly reduce inflammation but increase serum VEGF level: a rationale for tumor risk during Anti-HCV treatment. PLoSOne. 2016 Dec 20;11(12):e0167934.
   PubMed Web of Science ®Google Scholar
• Chu PS, Nakamoto N, Taniki N, et al. On-treatment decrease of NKG2D correlates to early emergence of clinically evident hepatocellular carcinoma after interferon-free therapy for chronic hepatitis C. PLoS One. 2017 Jun 15;12(6):e0179096.
   PubMed Web of Science ®Google Scholar
• European Association for the Study of the Liver clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236.
   PubMed Web of Science ®Google Scholar
• Heimbach JK, Kulik LM, Finn RS, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology. 2018 Jan;67(1):358–380.
   PubMed Web of Science ®Google Scholar
• Bruix J, Reig M, Sherman M. Evidence-based diagnosis, staging, and treatment of patients with hepatocellular carcinoma. Gastroenterology. 2016;150:835–853.
   PubMed Web of Science ®Google Scholar