Hepatitis C virus infection, antiviral therapy, and risk of hepatocellular carcinoma

Seminars in Oncology

Volumn 42, Issue 2, 2015, Pages 329-338

  Hsu, Yao Chun ^a,b,c   Wu, Chun Ying ^a,d,e,f   Lin, Jaw Town ^g  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b E DA HOSPITAL   (Taiwan)

^c I SHOU UNIVERSITY   (Taiwan)

^d TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^e NATIONAL YANG MING UNIVERSITY   (Taiwan)

^f NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^g FU JEN CATHOLIC UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; PEGINTERFERON; RIBAVIRIN;

ANTIVIRAL THERAPY; CANCER RECURRENCE; CANCER RISK; DRUG EFFICACY; HEPATITIS C; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; PRIORITY JOURNAL; REVIEW; VIRAL CLEARANCE; CARCINOMA, HEPATOCELLULAR; COMPLICATION; LIVER NEOPLASMS; RISK FACTOR; VIROLOGY;

ANTIVIRAL AGENTS; CARCINOMA, HEPATOCELLULAR; HEPATITIS C; HUMANS; LIVER NEOPLASMS; RISK FACTORS;

EID: 84926330802     PISSN: 00937754     EISSN: 15328708     Source Type: Journal    
DOI: 10.1053/j.seminoncol.2014.12.023     Document Type: Review

References (108)

1. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J Clin 61 2011 69 90
2. H.B. El-Serag Epidemiology of viral hepatitis and hepatocellular carcinoma Gastroenterology 142 2012 1264 1273
3. H.B. El-Serag Hepatocellular carcinoma: recent trends in the United States Gastroenterology 127 2004 S27 S34
4. S.F. Altekruse, K.A. McGlynn, and M.E. Reichman Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005 J Clin Oncol 27 2009 1485 1491
5. H.B. El-Serag, and K.L. Rudolph Hepatocellular carcinoma: epidemiology and molecular carcinogenesis Gastroenterology 132 2007 2557 2576
6. F. Donato, A. Tagger, and U. Gelatti Alcohol and hepatocellular carcinoma: the effect of lifetime intake and hepatitis virus infections in men and women Am J Epidemiol 155 2002 323 331
7. P. Ferenci, M. Fried, and D. Labrecque Hepatocellular carcinoma (HCC): a global perspective J Clin Gastroenterol 44 2010 239 245
8. H.B. El-Serag Epidemiology of hepatocellular carcinoma in USA Hepatol Res 37 Suppl 2 2007 S88 S94
9. K. Mohd Hanafiah, J. Groeger, A.D. Flaxman, and S.T. Wiersma Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence Hepatology 57 2013 1333 1342
10. C. Frank, M.K. Mohamed, and G.T. Strickland The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt Lancet 355 2000 887 891
11. H. Hagan, N. Snyder, and E. Hough Case-reporting of acute hepatitis B and C among injection drug users J Urban Health 79 2002 579 585
12. J.M. Micallef, J.M. Kaldor, and G.J. Dore Spontaneous viral clearance following acute hepatitis C infection: a systematic review of longitudinal studies J Viral Hepat 13 2006 34 41
13. D.L. Thomas, C.L. Thio, and M.P. Martin Genetic variation in IL28B and spontaneous clearance of hepatitis C virus Nature 461 2009 798 801
14. D.L. Thomas, J. Astemborski, and R.M. Rai The natural history of hepatitis C virus infection: host, viral, and environmental factors JAMA 284 2000 450 456
15. R.Y. Dodd, E.P. Notari, and S.L. Stramer Current prevalence and incidence of infectious disease markers and estimated window-period risk in the American Red Cross blood donor population Transfusion 42 2002 975 979
16. M.J. Alter Prevention of spread of hepatitis C Hepatology 36 2002 S93 S98
17. F. Donato, P. Boffetta, and M. Puoti A meta-analysis of epidemiological studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma Int J Cancer 75 1998 347 354
18. H.B. El-Serag Hepatocellular carcinoma and hepatitis C in the United States Hepatology 36 2002 S74 S83
19. Y.T. Huang, C.L. Jen, and H.I. Yang Lifetime risk and sex difference of hepatocellular carcinoma among patients with chronic hepatitis B and C. J Clin Oncol 29 2011 3643 3650
20. F. Degos, C. Christidis, and N. Ganne-Carrie Hepatitis C virus related cirrhosis: time to occurrence of hepatocellular carcinoma and death Gut 47 2000 131 136
21. G. Fattovich Progression of hepatitis B and C to hepatocellular carcinoma in Western countries Hepatogastroenterology 45 Suppl 3 1998 1206 1213
22. T. Chiba, Y. Matsuzaki, and M. Abei Multivariate analysis of risk factors for hepatocellular carcinoma in patients with hepatitis C virus-related liver cirrhosis J Gastroenterol 31 1996 552 558
23. W.K. Sung, H. Zheng, and S. Li Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma Nat Genet 44 2012 765 769
24. T. Luedde, and R.F. Schwabe NF-kappaB in the liver - linking injury, fibrosis and hepatocellular carcinoma Nat Rev Gastroenterol Hepatol 8 2011 108 118
25. W.L. Tsai, and R.T. Chung Viral hepatocarcinogenesis Oncogene 29 2010 2309 2324
26. K. Moriya, H. Fujie, and Y. Shintani The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice Nat Med 4 1998 1065 1067
27. N. Tanaka, K. Moriya, K. Kiyosawa, K. Koike, F.J. Gonzalez, and T. Aoyama PPARalpha activation is essential for HCV core protein-induced hepatic steatosis and hepatocellular carcinoma in mice J Clin Invest 118 2008 683 694
28. R.B. Ray, K. Meyer, and R. Ray Hepatitis C virus core protein promotes immortalization of primary human hepatocytes Virology 271 2000 197 204
29. H. Aoki, J. Hayashi, M. Moriyama, Y. Arakawa, and O. Hino Hepatitis C virus core protein interacts with 14-3-3 protein and activates the kinase Raf-1 J Virol 74 2000 1736 1741
30. J. Hayashi, H. Aoki, K. Kajino, M. Moriyama, Y. Arakawa, and O. Hino Hepatitis C virus core protein activates the MAPK/ERK cascade synergistically with tumor promoter TPA, but not with epidermal growth factor or transforming growth factor alpha Hepatology 32 2000 958 961
31. M. Hassan, D. Selimovic, H. Ghozlan, and O. Abdel-kader Hepatitis C virus core protein triggers hepatic angiogenesis by a mechanism including multiple pathways Hepatology 49 2009 1469 1482
32. T. Munakata, M. Nakamura, Y. Liang, K. Li, and S.M. Lemon Down-regulation of the retinoblastoma tumor suppressor by the hepatitis C virus NS5B RNA-dependent RNA polymerase Proc Natl Acad Sci U S A 102 2005 18159 18164
33. T. Munakata, Y. Liang, and S. Kim Hepatitis C virus induces E6AP-dependent degradation of the retinoblastoma protein PLoS Pathog 3 2007 1335 1347
34. M. Hassan, H. Ghozlan, and O. Abdel-Kader Activation of c-Jun NH2-terminal kinase (JNK) signaling pathway is essential for the stimulation of hepatitis C virus (HCV) non-structural protein 3 (NS3)-mediated cell growth Virology 333 2005 324 336
35. S.C. Wu, S.C. Chang, H.Y. Wu, P.J. Liao, and M.F. Chang Hepatitis C virus NS5A protein down-regulates the expression of spindle gene Aspm through PKR-p38 signaling pathway J Biol Chem 283 2008 29396 29404
36. Q.L. Choo, G. Kuo, A.J. Weiner, L.R. Overby, D.W. Bradley, and M. Houghton Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome Science 244 1989 359 362
37. F. Tine, S. Magrin, A. Craxi, and L. Pagliaro Interferon for non-A, non-B chronic hepatitis. A meta-analysis of randomised clinical trials J Hepatol 13 1991 192 199
38. R.L. Carithers Jr., and S.S. Emerson Therapy of hepatitis C: meta-analysis of interferon alfa-2b trials Hepatology 26 1997 83S 88SS
39. J.G. McHutchison, S.C. Gordon, and E.R. Schiff Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. Hepatitis Interventional Therapy Group N Engl J Med 339 1998 1485 1492
40. G.L. Davis, R. Esteban-Mur, and V. Rustgi Interferon alfa-2b alone or in combination with ribavirin for the treatment of relapse of chronic hepatitis C. International Hepatitis Interventional Therapy Group N Engl J Med 339 1998 1493 1499
41. M.W. Fried, M.L. Shiffman, and K.R. Reddy Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection N Engl J Med 347 2002 975 982
42. M.G. Ghany, D.B. Strader, D.L. Thomas, and L.B. Seeff Diagnosis, management, and treatment of hepatitis C: an update Hepatology 49 2009 1335 1374
43. I.M. Jacobson, J.G. McHutchison, and G. Dusheiko Telaprevir for previously untreated chronic hepatitis C virus infection N Engl J Med 364 2011 2405 2416
44. S. Zeuzem, P. Andreone, and S. Pol Telaprevir for retreatment of HCV infection N Engl J Med 364 2011 2417 2428
45. F. Poordad, J. McCone Jr., and B.R. Bacon Boceprevir for untreated chronic HCV genotype 1 infection N Engl J Med 364 2011 1195 1206
46. B.R. Bacon, S.C. Gordon, and E. Lawitz Boceprevir for previously treated chronic HCV genotype 1 infection N Engl J Med 364 2011 1207 1217
47. M.L. Yu, and W.L. Chuang Treatment of chronic hepatitis C in Asia: when East meets West J Gastroenterol Hepatol 24 2009 336 345
48. M.G. Swain, M.Y. Lai, and M.L. Shiffman A sustained virologic response is durable in patients with chronic hepatitis C treated with peginterferon alfa-2a and ribavirin Gastroenterology 139 2010 1593 1601
49. M.P. Manns, J.G. McHutchison, and S.C. Gordon Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial Lancet 358 2001 958 965
50. S.J. Hadziyannis, H. Sette Jr., and T.R. Morgan Peginterferon-alpha2a and ribavirin combination therapy in chronic hepatitis C: a randomized study of treatment duration and ribavirin dose Ann Intern Med 140 2004 346 355
51. D. Ge, J. Fellay, and A.J. Thompson Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance Nature 461 2009 399 401
52. A.J. Thompson, A.J. Muir, and M.S. Sulkowski Interleukin-28B polymorphism improves viral kinetics and is the strongest pretreatment predictor of sustained virologic response in genotype 1 hepatitis C virus Gastroenterology 139 2010 120 129
53. C.Y. Dai, J.F. Huang, and M.Y. Hsieh Insulin resistance predicts response to peginterferon-alpha/ribavirin combination therapy in chronic hepatitis C patients J Hepatol 50 2009 712 718
54. S. Nishiguchi, T. Kuroki, and S. Nakatani Randomised trial of effects of interferon-alpha on incidence of hepatocellular carcinoma in chronic active hepatitis C with cirrhosis Lancet 346 1995 1051 1055
55. D.C. Valla, M. Chevallier, and P. Marcellin Treatment of hepatitis C virus-related cirrhosis: a randomized, controlled trial of interferon alfa-2b versus no treatment Hepatology 29 1999 1870 1875
56. E. Bernardinello, L. Cavalletto, and L. Chemello Long-term clinical outcome after beta-interferon therapy in cirrhotic patients with chronic hepatitis C. TVVH Study Group Hepatogastroenterology 46 1999 3216 3222
57. F. Azzaroli, E. Accogli, and G. Nigro Interferon plus ribavirin and interferon alone in preventing hepatocellular carcinoma: a prospective study on patients with HCV related cirrhosis World J Gastroenterol 10 2004 3099 3102
58. K. Soga, K. Shibasaki, and Y. Aoyagi Effect of interferon on incidence of hepatocellular carcinoma in patients with chronic hepatitis C Hepatogastroenterology 52 2005 1154 1158
59. C.H. Zhang, G.L. Xu, W.D. Jia, J.S. Li, J.L. Ma, and Y.S. Ge Effects of interferon treatment on development and progression of hepatocellular carcinoma in patients with chronic virus infection: a meta-analysis of randomized controlled trials Int J Cancer 129 2011 1254 1264
60. Y.C. Shen, C. Hsu, C.C. Cheng, F.C. Hu, and A.L. Cheng A critical evaluation of the preventive effect of antiviral therapy on the development of hepatocellular carcinoma in patients with chronic hepatitis C or B: a novel approach by using meta-regression Oncology 82 2012 275 289
61. M.L. Yu, S.M. Lin, and W.L. Chuang 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 11 2006 985 994
62. A.J. van der Meer, B.J. Veldt, and J.J. Feld Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis JAMA 308 2012 2584 2593
63. A.K. Singal, A. Singh, and S. Jaganmohan Antiviral therapy reduces risk of hepatocellular carcinoma in patients with hepatitis C virus-related cirrhosis Clin Gastroenterol Hepatol 8 2010 192 199
64. V. Ng, and S. Saab Effects of a sustained virologic response on outcomes of patients with chronic hepatitis C Clin Gastroenterol Hepatol 9 2011 923 930
65. B.L. Pearlman, and N. Traub Sustained virologic response to antiviral therapy for chronic hepatitis C virus infection: a cure and so much more Clin Infect Dis 52 2011 889 900
66. R.L. Morgan, B. Baack, B.D. Smith, A. Yartel, M. Pitasi, and Y. Falck-Ytter Eradication of hepatitis C virus infection and the development of hepatocellular carcinoma: a meta-analysis of observational studies Ann Intern Med 158 2013 329 337
67. A.M. Di Bisceglie, M.L. Shiffman, and G.T. Everson Prolonged therapy of advanced chronic hepatitis C with low-dose peginterferon N Engl J Med 359 2008 2429 2441
68. J. Bruix, T. Poynard, and M. Colombo Maintenance therapy with peginterferon alfa-2b does not prevent hepatocellular carcinoma in cirrhotic patients with chronic hepatitis C Gastroenterology 140 2011 1990 1999
69. A. Erhardt, U. Heinzel-Pleines, and W. Boecher Long-term treatment with PEG-IFN-alfa 2b reduces hepatocellular incidence and prevents clinical complications in hepatitis C cirrhosis - an interim analysis of a multicenter trial J Hepatol 46 2007 S93
70. N. Afdhal, B. Freilich, and R. Levine Colchicine versus PEGINTRON long term (COPILOT) trial: interim analysis of clinical outcomes at year 2 Hepatology 40 2004 239A
71. A.S. Lok, J.E. Everhart, and E.C. Wright Maintenance peginterferon therapy and other factors associated with hepatocellular carcinoma in patients with advanced hepatitis C Gastroenterology 140 2011 840 849
72. European Association for Study of the Liver EASL Clinical Practice Guidelines: management of hepatitis C virus infection J Hepatol 60 2014 392 420
73. R.T. Chung, and T.F. Baumert Curing chronic hepatitis C - the arc of a medical triumph N Engl J Med 370 2014 1576 1578
74. A. Makiyama, Y. Itoh, and A. Kasahara Characteristics of patients with chronic hepatitis C who develop hepatocellular carcinoma after a sustained response to interferon therapy Cancer 101 2004 1616 1622
75. H. Tokita, H. Fukui, and A. Tanaka 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 20 2005 752 758
76. K.C. Chang, C.H. Hung, and S.N. Lu 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 67 2012 2766 2772
77. C.F. Huang, M.L. Yeh, and P.C. Tsai Baseline gamma-glutamyl transferase levels strongly correlate with hepatocellular carcinoma development in non-cirrhotic patients with successful hepatitis C virus eradication J Hepatol 61 1 2014 67 74
78. Y. Nagaoki, H. Aikata, and D. Miyaki Clinical features and prognosis in patients with hepatocellular carcinoma that developed after hepatitis C virus eradication with interferon therapy J Gastroenterol 46 2011 799 808
79. D. Poon, B.O. Anderson, and L.T. Chen Management of hepatocellular carcinoma in Asia: consensus statement from the Asian Oncology Summit Lancet Oncol 10 2009 1111 1118
80. J. Bruix, and M. Sherman Management of hepatocellular carcinoma: an update Hepatology 53 2011 1020 1022
81. J. Yamamoto, T. Kosuge, and T. Takayama Recurrence of hepatocellular carcinoma after surgery Br J Surg 83 1996 1219 1222
82. Y. Sasaki, T. Yamada, and H. Tanaka Risk of recurrence in a long-term follow-up after surgery in 417 patients with hepatitis B- or hepatitis C-related hepatocellular carcinoma Ann Surg 244 2006 771 780
83. O. Morimoto, H. Nagano, and M. Sakon Diagnosis of intrahepatic metastasis and multicentric carcinogenesis by microsatellite loss of heterozygosity in patients with multiple and recurrent hepatocellular carcinomas J Hepatol 39 2003 215 221
84. I.O. Ng, X.Y. Guan, R.T. Poon, S.T. Fan, and J.M. Lee Determination of the molecular relationship between multiple tumour nodules in hepatocellular carcinoma differentiates multicentric origin from intrahepatic metastasis J Pathol 199 2003 345 353
85. T.S. Huang, Y.C. Shyu, H.Y. Chen, S.S. Yuan, J.N. Shih, and P.J. Chen A systematic review and meta-analysis of adjuvant interferon therapy after curative treatment for patients with viral hepatitis-related hepatocellular carcinoma J Viral Hepat 20 2013 729 743
86. K. Ikeda, Y. Arase, and S. Saitoh Interferon beta prevents recurrence of hepatocellular carcinoma after complete resection or ablation of the primary tumor - A prospective randomized study of hepatitis C virus-related liver cancer Hepatology 32 2000 228 232
87. S. Kubo, S. Nishiguchi, K. Hirohashi, H. Tanaka, T. Shuto, and H. Kinoshita Randomized clinical trial of long-term outcome after resection of hepatitis C virus-related hepatocellular carcinoma by postoperative interferon therapy Br J Surg 89 2002 418 422
88. Y. Shiratori, S. Shiina, and T. Teratani Interferon therapy after tumor ablation improves prognosis in patients with hepatocellular carcinoma associated with hepatitis C virus Ann Intern Med 138 2003 299 306
89. V. Mazzaferro, R. Romito, and M. Schiavo Prevention of hepatocellular carcinoma recurrence with alpha-interferon after liver resection in HCV cirrhosis Hepatology 44 2006 1543 1554
90. T. Ishikawa, K. Higuchi, and T. Kubota Combination PEG-IFN a-2b/ribavirin therapy following treatment of hepatitis C virus-associated hepatocellular carcinoma is capable of improving hepatic functional reserve and survival Hepatogastroenterology 59 2012 529 532
91. A.K. Singal, and D.H. Freeman Jr Anand BS. Meta-analysis: interferon improves outcomes following ablation or resection of hepatocellular carcinoma Aliment Pharmacol Ther 32 2010 851 858
92. Y.C. Shen, C. Hsu, L.T. Chen, C.C. Cheng, F.C. Hu, and A.L. Cheng Adjuvant interferon therapy after curative therapy for hepatocellular carcinoma (HCC): a meta-regression approach J Hepatol 52 2010 889 894
93. H. Yano, S. Ogasawara, and S. Momosaki Growth inhibitory effects of pegylated IFN alpha-2b on human liver cancer cells in vitro and in vivo Liver Int 26 2006 964 975
94. Y. Tanimoto, H. Tashiro, and H. Aikata Impact of pegylated interferon therapy on outcomes of patients with hepatitis C virus-related hepatocellular carcinoma after curative hepatic resection Ann Surg Oncol 19 2012 418 425
95. H. Hagihara, K. Nouso, and Y. Kobayashi Effect of pegylated interferon therapy on intrahepatic recurrence after curative treatment of hepatitis C virus-related hepatocellular carcinoma Int J Clin Oncol 16 2011 210 220
96. Y.C. Hsu, H.J. Ho, M.S. Wu, J.T. Lin, and C.Y. Wu Postoperative peg-interferon plus ribavirin is associated with reduced recurrence of hepatitis C virus-related hepatocellular carcinoma Hepatology 58 2013 150 157
97. C.Y. Wu, Y.J. Chen, and H.J. Ho Association between nucleoside analogues and risk of hepatitis B virus-related hepatocellular carcinoma recurrence following liver resection JAMA 308 2012 1906 1914
98. E. Lawitz, A. Mangia, and D. Wyles Sofosbuvir for previously untreated chronic hepatitis C infection N Engl J Med 368 2013 1878 1887
99. M.W. Fried, M. Buti, and G.J. Dore Once-daily simeprevir (TMC435) with pegylated interferon and ribavirin in treatment-naive genotype 1 hepatitis C: the randomized PILLAR study Hepatology 58 2013 1918 1929
100. J. Grebely, J. Bryant, and P. Hull Factors associated with specialist assessment and treatment for hepatitis C virus infection in New South Wales, Australia J Viral Hepat 18 2011 e104 e116
101. N. Papadopoulos, S. Manolakopoulos, and M. Deutsch Frequency and predictors of no treatment in anti-hepatitis C virus-positive patients at tertiary liver centers in Greece Eur J Gastroenterol Hepatol 25 2013 587 593
102. S. Lattimore, W. Irving, and S. Collins Using surveillance data to determine treatment rates and outcomes for patients with chronic hepatitis C virus infection Hepatology 59 2014 1343 1350
103. N. Afdhal, K.R. Reddy, and D.R. Nelson Ledipasvir and sofosbuvir for previously treated HCV genotype 1 infection N Engl J Med 370 2014 1483 1493
104. I.M. Jacobson, S.C. Gordon, and K.V. Kowdley Sofosbuvir for hepatitis C genotype 2 or 3 in patients without treatment options N Engl J Med 368 2013 1867 1877
105. F. Poordad, C. Hezode, and R. Trinh ABT-450/r-ombitasvir and dasabuvir with ribavirin for hepatitis C with cirrhosis N Engl J Med 370 2014 1973 1982
106. M.S. Sulkowski, D.F. Gardiner, and M. Rodriguez-Torres Daclatasvir plus sofosbuvir for previously treated or untreated chronic HCV infection N Engl J Med 370 2014 211 221
107. N. Afdhal, S. Zeuzem, and P. Kwo Ledipasvir and sofosbuvir for untreated HCV genotype 1 infection N Engl J Med 370 2014 1889 1898
108. J.H. Hoofnagle, and A.H. Sherker Therapy for hepatitis C - the costs of success N Engl J Med 370 2014 1552 1553