Hepatocellular carcinoma in patients with a sustained response to anti-hepatitis C therapy

International Journal of Molecular Sciences

Volumn 16, Issue 8, 2015, Pages 19698-19712

  D’Ambrosio, Roberta ^a   Della Corte, Cristina ^a   Colombo, Massimo ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Hepatitis C; Hepatocellular carcinoma; Interferon; Sustained virological response

Indexed keywords

ALBUMIN; ALPHA FETOPROTEIN; BILIRUBIN; HEMOGLOBIN A1C; INTERFERON; MICRORNA 122; NONSTRUCTURAL PROTEIN 5A; NONSTRUCTURAL PROTEIN 5B; RETINOBLASTOMA PROTEIN; SIMEPREVIR; SOFOSBUVIR; ANTIVIRUS AGENT;

ALCOHOL ABUSE; ANTIVIRAL THERAPY; CARCINOGENICITY; DISEASE ASSOCIATION; FATTY LIVER; GENETIC POLYMORPHISM; GENOMIC INSTABILITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FIBROSIS; META ANALYSIS (TOPIC); MRNA EXPRESSION ASSAY; MULTICENTER STUDY (TOPIC); OBESITY; OXIDATIVE STRESS; REVIEW; RISK FACTOR; SMOKING; SUSTAINED VIROLOGICAL RESPONSE; THROMBOCYTE COUNT; CARCINOMA, HEPATOCELLULAR; COMPLICATION; DRUG EFFECTS; HEPACIVIRUS; HEPATITIS C, CHRONIC; LIVER NEOPLASMS; TREATMENT OUTCOME; VIRUS LOAD;

HEPATITIS C VIRUS;

ANTIVIRAL AGENTS; CARCINOMA, HEPATOCELLULAR; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; INTERFERONS; LIVER NEOPLASMS; RISK FACTORS; TREATMENT OUTCOME; VIRAL LOAD;

EID: 84939863631     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160819698     Document Type: Review

References (55)

1. European Association for Study of Liver. EASL Clinical Practice Guidelines: Management of hepatitis C virus infection. J. Hepatol. 2014, 60, 392–420. Erratum in: J. Hepatol. 2014, 61, 183–184
2. Yoshida, H.; Tateishi, R.; Arakawa, Y.; Sata, M.; Fujiyama, S.; Nishiguchi, S.; Ishibashi, H.; Yamada, G.; Yokosuka, O.; Shiratori, Y. et al. Benefit of interferon therapy in hepatocellular carcinoma prevention for individual patients with chronic hepatitis C. Gut 2004, 53, 425–430
3. Yu, M.L.; Lin, S.M.; Chuang, W.L.; Dai, C.Y.; Wang, J.H.; Lu, S.N.; Sheen, I.S.; Chang, W.Y.; Lee, C.M.; Liaw, Y.F. A sustained virological response to interferon or interferon/ribavirin reduces hepatocellular carcinoma and improves survival in chronic hepatitis C: A nationwide, multicentre study in Taiwan. Antivir. Ther. 2006, 11, 985–994
4. Bruno, S.; Stroffolini, T.; Colombo, M.; Bollani, S.; Benvegnù, L.; Mazzella, G.; Ascione, A.; Santantonio, T.; Piccinino, F.; Andreone, F. 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
5. Veldt, B.J.; Heathcote, E.J.; Wedemeyer, H.; Reichen, J.; Hofmann, W.P.; Zeuzem, S.; Manns, M.P.; Hansen, B.E.; Schalm, S.W.; Janssen, H.L. Sustained virologic response and clinical outcomes in patients with chronic hepatitis C and advanced fibrosis. Ann. Intern. Med.2007, 147, 677–684
6. Mallet, V.; Gilgenkrantz, H.; Serpaggi, J.; Verkarre, V.; Vallet-Pichard, A, Fontaine, H.; Pol, S Brief communication: The relationship of regression of cirrhosis to outcome in chronic hepatitis C Ann. Intern. Med. 2008, 149, 399–403
7. Van der, M.; Veldt, B.J.; Feld, J.J.; Wedemeyer, H.; Dufour, J.F.; Lammert, F.; Duarte-Rojo, A.; Heathcote, E.J.; Manns, M.P.; Kuske, L. et al. Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. JAMA 2012, 308, 2584–2593
8. Morgan, T.R.; Ghany, M.G.; Kim, H.Y.; Snow, K.K.; Shiffman, M.L.; de Santo, J.L; Lee, W.M.; di Bisceglie, A.M.; Bonkovsky, H.L.; HALT-C Trial Group. Outcome of sustained virological responders with histologically advanced chronic hepatitis C. Hepatology 2010, 52, 833–844
9. For Research, European Organization, and European Association for the Study of the Liver EASL–EORTC Clinical Practice Guidelines: Management of hepatocellular carcinoma. J. Hepatol 2012, 56, 908–943
10. Lemon, S.M. Is hepatitis C virus carcinogenic? Gastroenterology 2012, 142, 1274–1278
11. Trépo, E.; Nahon, P.; Bontempi, G.; Valenti, L.; Falleti, E.; Nischalke, H.D.; Hamza, S.; Corradini, S.G.; Burza, M.A.; Guyot, E. et al. Association between the PNPLA3 (rs738409 C>G) variant and hepatocellular carcinoma: Evidence from a meta-analysis of individual participant data. Hepatology 2014, 59, 2170–2177
12. Singal, A.G.; Volk, M.L.; Jensen, D.; di Bisceglie, A.M.; Schoenfeld, P.S. Sustained viral response is associated with reduced liver-related morbidity and mortality in patients with hepatitis C virus. Clin. Gastroenterol. Hepatol. 2010, 8, 280–288
13. Aleman, S.; Rahbin, N.; Weiland, O.; Davidsdottir, L.; Hedenstierna, M.; Rose, N.; Verbaan, H.; Stål P.; Carlsson, T.; Norrgren, H. 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
14. Lok, A.S.; Everhart, J.E.; Wright, E.C.; di Bisceglie, A.M.; Kim, H.Y.; Sterling, R.K.; Everson, G.T.; Lindsay, K.L.; Lee, W.M.; Bonkovsky, H.L. et al. Maintenance peginterferon therapy and other factors associated with hepatocellular carcinoma in patients with advanced hepatitis C Gastroenterology 2011, 140, 840–849
15. Fattovich, G.; Giustina, G.; Degos, F.; Diodati, G.; Tremolada, F.; Nevens, F.; Almasio, P.; Solinas, A.; Brouwer, J.T. Effectiveness of interferon α on incidence of hepatocellular carcinoma and decompensation in cirrosi type C. J. Hepatol. 1997, 27, 201–205
16. Cardoso, A.C.; Rami, M.R.; Figueiredo-Mendes, C.; Ripault, M.P.; Giuily, N.; Castelnau, C.; Boyer, N.; Tarik, A.T.; Martinot-Peignoux, M.; Maylin, S. et al. Impact of peginterferon and ribavirin therapy on hepatocellular carcinoma: Incidence and survival in hepatitis C patients with advanced fibrosis. J. Hepatol. 2010, 52, 652–657
17. Shiratori, Y.; Ito, Y.; Yokosuka, O.; Imazeki, F.; Nakata, R.; Tanaka, N.; Arakawa, Y.; Hashimoto, E.; Hirota, K.; Yoshida, H. et al. Antiviral therapy for cirrhotic hepatitis C: association with reduced hepatocellular carcinoma development and improved survival Ann. Intern. Med. 2005, 142, 105–114
18. European Association for the Study of the Liver. EASL Recommendations on Treatment of Hepatitis C 2015. J. Hepatol. 2015, doi:10.1016/ j.jhep.2015.03.025
19. Charlton, M.; Everson, G.T.; Flamm, S.L.; Kumar, P.; Landis, C.; Brown, R.S.,; Fried, M.W.; Terrault, N.A.; O'Leary, J.G.; Vargas, H.E. et al. Ledipasvir and Sofosbuvir Plus Ribavirin for Treatment of HCV Infection in Patients with Advanced Liver DiseaseSOLAR-1 Investigators Gastroenterology2015, doi:10.1053/j.gastro.2015.05.010
20. Bunchorntavakul, C.; Reddy, K.R. Review article: The efficacy and safety of daclatasvir in the treatment of chronic hepatitis C virus infection. Aliment. Pharmacol. Ther. 2015, doi:10.1111/apt.13264
21. Afdhal, N.; Zeuzem, S.; Kwo, P.; Chojkier, M.; Gitlin, N.; Puoti, M.; Romero-Gomez, M.; Zarski, J.P.; Agarwal, K.; Buggisch, P. et al. ION-1 Investigators. Ledipasvir and sofosbuvir for untreated HCV genotype 1 infection. N. Engl. J. Med. 2014, 370, 1889–1898
22. Papatheodoridis, G.V.; Lampertico, P.; Manolakopoulos, S.; Lok, A. Incidence of hepatocellular carcinoma in chronic hepatitis B patients receiving nucleos(t)ide therapy: A systematic review J. Hepatol. 2010, 53, 348–356
23. Papatheodoridis, G.V.; Manolakopoulos, S.; Touloumi, G.; Vourli, G.; Raptopoulou-Gigi, M.; Vafiadis-Zoumbouli, I.; Vasiliadis, T.; Mimidis, K.; Gogos, C.; Ketikoglou, I.; et al. Virological suppression does not prevent the development of hepatocellular carcinoma in HBeAg-negative chronic hepatitis B patients with cirrhosis receiving oral antiviral(s) starting with lamivudine monotherapy: Results of the nationwide HEPNET. Greece cohort study. Gut 2011, 60, 1109–1116
24. Chang, K.C.; Hung, C.H.; Lu, S.N.; Wang, J.H.; Lee, C.M.; Chen, C.H.; Yen, M.F.; Lin, S.C.; Yen, Y.H.; Tsai, M.C. et al. A novel predictive score for hepatocellular carcinoma development in patients with chronic hepatitis C after sustained response to pegylated interferon and ribavirin combination therapy. J. Antimicrob. Chemother. 2012, 67, 2766–2777
25. Van der Meer, A.; Feld, J.; Hofer, H.; Almasio, P.; Calvaruso, V.; Fernandez-Rodriguez, C.; Aleman, S.; Ganne-Carrie, N.; D’Ambrosio, R. The risk for hepatocellular carcinoma among patients with chronic HCV infection and advanced hepatic fibrosis following sustained virological response Hepatology 2013, 58, 280A
26. Huang, C.F.; Yeh, M.L.; Tsai, P.C.; Hsieh, M.H.; Yang, H.L.; Hsieh, M.Y.; Yang, J.F.; Lin, Z.Y.; Chen, S.C.; Wang, L.Y. et al. Baseline gamma-glutamyl transferase levels strongly correlate with hepatocellular carcinoma development in non-cirrhotic patients with successful hepatitis C virus eradication. J. Hepatol. 2014, 61, 67–74
27. D'Ambrosio, R.; Aghemo, A.; Rumi, M.G.; Ronchi, G.; Donato, M.F.; Paradis, V.; Colombo, M.; Bedossa, P. A morphometric and immunohistochemical study to assess the benefit of a sustained virological response in hepatitis C virus patients with cirrhosis. Hepatology 2012, 56, 532–543
28. Maylin, S.; Martinot-Peignoux, M.; Moucari, R.; Boyer, N.; Ripault, M.P.; Cazals-Hatem, D.; Giuily, N.; Castelnau, C.; Cardoso, A.C.; Asselah, T. et al. Eradication of hepatitis C virus in patients successfully treated for chronic hepatitis C. Gastroenterology 2008, 135, 821–829
29. Calle, E.E.; Rodriguez, C.; Walker-Thurmond, K.; Thun, M.J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 2003, 348, 1625–1638
30. Koh, W.P.; Robien, K.; Wang, R.; Govindarajan, S.; Yuan, J.M.; Yu, M.C. Smoking as an independent risk factor for hepatocellular carcinoma: the Singapore Chinese Health Study Br. J. Cancer 2011, 105, 1430–1435
31. Baffy, G.; Brunt, E.M.; Caldwel, S.H. Hepatocellular carcinoma in non-alcoholic fatty liver disease, an emerging menace. J. Hepatol. 2012, 56, 1384–1391
32. El-Serag, H.B.; Mason, A.C. Risk factors for the rising rates of primary liver cancer in the United States. Arch. Intern. Med. 2000, 160, 3227–3230
33. Hassan, M.M.; Hwang, L.Y; Hatten, C.J.; Swaim, M.; Li, D.; Abbruzzese, J.L.; Beasley, P.; Patt, Y.Z Risk Factors for Hepatocellular Carcinoma, Synergism of Alcohol With Viral Hepatitis and Diabetes Mellitus. Hepatology 2002, 36, 1206–1213
34. Allen, E.; Beral, V.; Casabonne, D.; Kan, S.W.; Reeves, G.K.; Brown, A.; Green, J. Million Women Study Collaborators. Moderate alcohol intake and cancer incidence in women. JNCI 2009, 101, 296–305
35. Baan, R.; Straif, K.; Grosse, Y.; Secretan, B.; El Ghissassi, F.; Bouvard, V.; Altieri, A.; Cogliano, V.; WHO International Agency for Research on Cancer Monograph Working Group. Carcinogenicity of alcoholic beverages. Lancet Oncol. 2007, 8, 292–293
36. Lieber, C.S.; Seitz, H.K.; Garro, A.J.; Worner, T.M. Alcohol-related diseases and carcinogenesis Cancer Res. 1979, 39, 2863–2886
37. Lieber, C.S. Mechanism of ethanol induced hepatic injury. Pharmacol. Ther.1990, 46, 1–41
38. Iwasaki, Y.; Takaguchi, K.; Ikeda, H.; Makino, Y.; Araki, Y.; Ando, M.; Kobashi, H.; Kobatake, T.; Tanaka, R.; Tomita, M. et al. Risk factors for hepatocellular carcinoma in Hepatitis C patients with sustained virologic response to interferon therapy. Liver Int. 2004, 24, 603–610
39. Tokita, H; Fukui, H.; Tanaka, A.; Kamitsukasa, H.; Yagura, M.; Harada, H, Okamoto, H. Risk factors for the development of hepatocellular carcinoma among patients with chronic hepatitis C who achieved a sustained virological response to interferon therapy. J. Gastroenterol. Hepatol. 2005, 20, 752–758
40. Arase, Y.; Kobayashi, M.; Suzuki, F.; Suzuki, Y.; Kawamura, Y.; Akuta, N.; Kobayashi, M.; Sezaki, H.; Saito, S.; Hosaka, T. et al. Effect of type 2 diabetes on risk for malignancies includes hepatocellular carcinoma in chronic hepatitis C. Hepatology 2013, 57, 964–973
41. Davila, J.A.; Morgan, R.O.; Shaib, Y.; McGlynn, K.A.; El-Serag, H.B. Diabetes increases the risk of hepatocellular carcinoma in the United States, a population based case control study. Gut 2005, 54, 533–539
42. Polesel, J.; Zucchetto, A.; Montella, M.; Dal Maso, L.; Crispo, A.; La Vecchia, C.; Serraino, D.; Franceschi, S.; Talamini, R. The impact of obesity and diabetes mellitus on the risk of hepatocellular carcinoma. Ann. Oncol. 2009, 20, 353–357
43. Bianchini, F.; Kaaks, R.; Vainio, H. Overweight, obesity, and cancer risk. Lancet Oncol.2002, 3, 565–574
44. Chen, C.L.; Yang, H.I.; Yang, W.S.; Liu, C.J.; Chen, P.J.; You, S.L.; Wang, L.Y.; Sun, C.A.; Lu, S.N.; Chen, D.S. et al. Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection, a follow-up study in Taiwan. Gastroenterology 2008, 135, 111–121
45. Angulo, P. Nonalcoholic fatty liver disease. N. Engl. J. Med.2002, 346, 1221–1231
46. Dyson, J.; Jaques, B.; Chattopadyhay, D.; Lochan, R.; Graham, J.; Das, D.; Aslam, T.; Patanwala, I.; Gaggar, S.; Cole, M. et al. Hepatocellular cancer, The impact of obesity, type 2 diabetes and a multidisciplinary team. J. Hepatol. 2014, 60, 110–117
47. Guzman, G.; Brunt, E.M.; Petrovic, L.M.; Chejfec, G.; Layden, T.J.; Cotler, S.J. Does nonalcoholic fatty liver disease predispose patients to hepatocellular carcinoma in the absence of cirrhosis? Arch. Pathol. Lab. Med. 2008, 132, 1761–1766
48. Tanaka, A.; Uegaki, S.; Kurihara, H.; Aida, K.; Mikami, M.; Nagashima I.; Shiga J.; Takikawa, H Hepatic steatosis as a possible risk factor for the development of hepatocellular carcinoma after eradication of hepatitis C virus with antiviral therapy in patients with chronic hepatitis C World J. Gastroenterol. 2007, 13, 5180–5187
49. El-Zayadi, A.R. Heavy smoking and liver. World J. Gastroenterol. 2006, 12, 6098–6101
50. Wu, W.K.K.; Wong, H.P.S.; Yu, L.; Cho, C.H. Nicotine and Cancer, in Alcohol Tobacco and Cancer; Cho, C.H., Purohit, V., Eds.; Karger: Basel, Switzerland, 2006; pp. 253–267
51. Gandini, S.; Botteri, E.; Iodice, S.; Boniol, M.; Lowenfels, A.; Maisonneuve, P.; Boyle, P. Tobacco smoking and cancer: a metaanalysis. Int. J. Cancer 2008, 122, 155–164
52. Wang, L.Y.; You, S.L.; Lu, S.N.; Ho, H.C.; Wu, M.H.; Sun, C.A.; Yang, H.I.; Chien-Jen, C. Risk of hepatocellular carcinoma and habits of alcohol drinking, betel quid chewing and cigarette smoking, a cohort of 2416 HBsAg seropositive and 9421 HBsAg-seronegative male residents in Taiwan Cancer Causes Control2003, 14, 241–250
53. Mori, M.; Hara, M.; Wada, I.; Hara, T.; Yamamoto, K.; Honda, M.; Naramoto, J. Prospective study of hepatitis B and C viral infections, cigarette smoking, alcohol consumption, and other factors associated with hepatocellular carcinoma risk in Japan. Am. J. Epidemiol. 2000, 151, 131–139
54. Chen, Z.M.; Liu, B.Q.; Boreham, J.; Wu, Y.P.; Chen, J.S.; Peto, R. Smoking and Liver Cancer in China, Case-Control Comparison of 36,000 Liver Cancer Deaths vs. 17,000 Cirrhosis Deaths Int. J. Cancer 2003, 107, 106–112
55. Franceschi, S.; Montella, M.; Polesel, J.; La Vecchia, C.; Crispo, A.; dal Maso, L.; Casarin, P.; Izzo, F.; Tommasi, L.G.; Chemin, I. et al. Hepatitis viruses, alcohol, and tobacco in the etiology of hepatocellular carcinoma in Italy. Cancer Epidemiol. Biomark. Prev. 2006, 15, 683–689