Hepatocellular carcinoma in patients with chronic hepatitis C virus infection in the Asia-Pacific region

Journal of Gastroenterology

Volumn 48, Issue 6, 2013, Pages 681-688

  Kim, Mi Na ^a   Kim, Beom Kyung ^a   Han, Kwang Hyub ^a,b  

^a Yonsei University College of Medicine   (South Korea)

^b Liver Cirrhosis Clinical Research Centre   (South Korea)

Author keywords

Hepatitis C virus; Hepatocellular carcinoma

Indexed keywords

BEVACIZUMAB; BOCEPREVIR; BRIVANIB; CETUXIMAB; CORE PROTEIN; ERLOTINIB; INTERFERON; MONOCLONAL ANTIBODY; NONSTRUCTURAL PROTEIN 5A; PEGINTERFERON; PLACEBO; SORAFENIB; TELAPREVIR; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ADVANCED CANCER; ALOPECIA; ANOREXIA; ANTIVIRAL THERAPY; APOPTOSIS; ASIA; CANCER MORTALITY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RISK; CANCER SCREENING; CANCER SURVIVAL; CELL PROLIFERATION; CHEMORADIOTHERAPY; DESQUAMATION; DIARRHEA; DRUG COST; DRUG ERUPTION; DRUG SAFETY; FATIGUE; HAND FOOT SYNDROME; HEPATITIS C; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; HYPERTENSION; IMMUNE DEFICIENCY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER RESECTION; OXIDATIVE STRESS; PACIFIC ISLANDS; PREDICTION; PRIORITY JOURNAL; QUALITY OF LIFE; RADIOFREQUENCY ABLATION; REVIEW; RISK REDUCTION; UNSPECIFIED SIDE EFFECT;

ASIA; CARCINOMA, HEPATOCELLULAR; HEPATITIS C, CHRONIC; HUMANS; LIVER NEOPLASMS;

EID: 84879417093     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-013-0770-9     Document Type: Review

References (85)

1. Yang JD, Roberts LR. Hepatocellular carcinoma: a global view. Nat Rev Gastroenterol Hepatol. 2010;7:448-58.
2. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74-108.
3. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557-76.
4. Bege T, Le Treut YP, Hardwigsen J, Ananian P, Richa H, Campan P, et al. Prognostic factors after resection for hepatocellular carcinoma in nonfibrotic or moderately fibrotic liver. A 116-case European series. J Gastrointest Surg. 2007;11:619-25.
5. Lawson A, Hagan S, Rye K, Taguri N, Ratib S, Zaitoun AM, et al. The natural history of hepatitis C with severe hepatic fibrosis. J Hepatol. 2007;47:37-45.
6. Bralet MP, Regimbeau JM, Pineau P, Dubois S, Loas G, Degos F, et al. Hepatocellular carcinoma occurring in nonfibrotic liver: epidemiologic and histopathologic analysis of 80 French cases. Hepatology. 2000;32:200-4.
7. Le Treut YP, Pons J, Hardwigsen J, Castellani P, Campan P, Hanna X, et al. Hepatocellular carcinoma in a non-cirrhotic liver: presentation of series of 77 operated patients. Chirurgie. 1999;124:485-93.
8. Nzeako UC, Goodman ZD, Ishak KG. Hepatocellular carcinoma in cirrhotic and noncirrhotic livers: a clinico-histopathologic study of 804 North American patients. Am J Clin Pathol. 1996;105:65-75.
9. Fung J, Lai CL, Yuen MF. Hepatitis B and C virus-related carcinogenesis. Clin Microbiol Infect. 2009;15:964-70.
10. Yamanaka N, Tanaka T, Tanaka W, Yamanaka J, Yasui C, Kuroda N, et al. Correlation of hepatitis virus serologic status with clinicopathologic features in patients undergoing hepatectomy for hepatocellular carcinoma. Cancer. 1997;79:1509-15.
11. Miyagawa S, Kawasaki S, Makuuchi M. Comparison of the characteristics of hepatocellular carcinoma between hepatitis B and C viral infection: tumor multicentricity in cirrhotic liver with hepatitis C. Hepatology. 1996;24:307-10.
12. Roayaie S, Haim MB, Emre S, Fishbein TM, Sheiner PA, Miller CM, et al. Comparison of surgical outcomes for hepatocellular carcinoma in patients with hepatitis B versus hepatitis C: a western experience. Ann Surg Oncol. 2000;7:764-70.
13. Moriya K, Fujie H, Shintani Y, Yotsuyanagi H, Tsutsumi T, Ishibashi K, et al. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med. 1998;4:1065-7.
14. Lerat H, Honda M, Beard MR, Loesch K, Sun J, Yang Y, et al. Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis C virus. Gastroenterology. 2002;122:352-65.
15. Yoshida T, Hanada T, Tokuhisa T, Kosai K, Sata M, Kohara M, et al. Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation. J Exp Med. 2002;196:641-53.
16. Lai MM, Ware CF. Hepatitis C virus core protein: possible roles in viral pathogenesis. Curr Top Microbiol Immunol. 2000;242:117-34.
17. Liang TJ, Heller T. Pathogenesis of hepatitis C-associated hepatocellular carcinoma. Gastroenterology. 2004;127:S62-71.
18. Yamashita T, Honda M, Takatori H, Nishino R, Minato H, Takamura H, et al. Activation of lipogenic pathway correlates with cell proliferation and poor prognosis in hepatocellular carcinoma. J Hepatol. 2009;50:100-10.
19. Yamashita T, Kaneko S, Hashimoto S, Sato T, Nagai S, Toyoda N, et al. Serial analysis of gene expression in chronic hepatitis C and hepatocellular carcinoma. Biochem Biophys Res Commun. 2001;282:647-54.
20. Honda M, Yamashita T, Ueda T, Takatori H, Nishino R, Kaneko S. Different signaling pathways in the livers of patients with chronic hepatitis B or chronic hepatitis C. Hepatology. 2006;44:1122-38.
21. Honda M, Kaneko S, Kawai H, Shirota Y, Kobayashi K. Differential gene expression between chronic hepatitis B and C hepatic lesion. Gastroenterology. 2001;120:955-66.
22. Akuta N, Suzuki F, Kawamura Y, Yatsuji H, Sezaki H, Suzuki Y, et al. Amino acid substitutions in the hepatitis C virus core region are the important predictor of hepatocarcinogenesis. Hepatology. 2007;46:1357-64.
23. Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, Matsuura Y, et al. Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J Gen Virol. 1997;78(Pt 7):1527-31.
24. Perlemuter G, Sabile A, Letteron P, Vona G, Topilco A, Chretien Y, et al. Hepatitis C virus core protein inhibits microsomal triglyceride transfer protein activity and very low density lipoprotein secretion: a model of viral-related steatosis. FASEB J. 2002;16:185-94.
25. Moriya K, Nakagawa K, Santa T, Shintani Y, Fujie H, Miyoshi H, et al. Oxidative stress in the absence of inflammation in a mouse model for hepatitis C virus-associated hepatocarcinogenesis. Cancer Res. 2001;61:4365-70.
26. Okuda M, Li K, Beard MR, Showalter LA, Scholle F, Lemon SM, et al. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology. 2002;122:366-75.
27. Kwun HJ, Jang KL. Dual effects of hepatitis C virus Core protein on the transcription of cyclin-dependent kinase inhibitor p21 gene. J Viral Hepat. 2003;10:249-55.
28. Miyamoto H, Moriishi K, Moriya K, Murata S, Tanaka K, Suzuki T, et al. Involvement of the PA28gamma-dependent pathway in insulin resistance induced by hepatitis C virus core protein. J Virol. 2007;81:1727-35.
29. Banerjee S, Saito K, Ait-Goughoulte M, Meyer K, Ray RB, Ray R. Hepatitis C virus core protein upregulates serine phosphorylation of insulin receptor substrate-1 and impairs the downstream akt/protein kinase B signaling pathway for insulin resistance. J Virol. 2008;82:2606-12.
30. Bugianesi E, Salamone F, Negro F. The interaction of metabolic factors with HCV infection: does it matter? J Hepatol. 2012;56(Suppl 1):S56-65.
31. Laron Z. Insulin-a growth hormone. Arch Physiol Biochem. 2008;114:11-6.
32. White DL, Ratziu V, El-Serag HB. Hepatitis C infection and risk of diabetes: a systematic review and meta-analysis. J Hepatol. 2008;49:831-44.
33. Jiang W, Zhu Z, Thompson HJ. Dietary energy restriction modulates the activity of AMP-activated protein kinase, Akt, and mammalian target of rapamycin in mammary carcinomas, mammary gland, and liver. Cancer Res. 2008;68:5492-9.
34. Villanueva A, Chiang DY, Newell P, Peix J, Thung S, Alsinet C, et al. Pivotal role of mTOR signaling in hepatocellular carcinoma. Gastroenterology (2008);135:1972-1883, 83e1-11.
35. Kwun HJ, Jung EY, Ahn JY, Lee MN, Jang KL. p53-dependent transcriptional repression of p21(waf1) by hepatitis C virus NS3. J Gen Virol. 2001;82:2235-41.
36. Reyes GR. The nonstructural NS5A protein of hepatitis C virus: an expanding, multifunctional role in enhancing hepatitis C virus pathogenesis. J Biomed Sci. 2002;9:187-97.
37. Tanji Y, Kaneko T, Satoh S, Shimotohno K. Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J Virol. 1995;69:3980-6.
38. Levrero M. Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene. 2006;25:3834-47.
39. Foucher J, Chanteloup E, Vergniol J, Castera L, Le Bail B, Adhoute X, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006;55:403-8.
40. Ziol M, Handra-Luca A, Kettaneh A, Christidis C, Mal F, Kazemi F, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology. 2005;41:48-54.
41. Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29:1705-13.
42. Ganne-Carrie N, Ziol M, de Ledinghen V, Douvin C, Marcellin P, Castera L, et al. Accuracy of liver stiffness measurement for the diagnosis of cirrhosis in patients with chronic liver diseases. Hepatology. 2006;44:1511-7.
43. Castera L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128:343-50.
44. Yeh WC, Li PC, Jeng YM, Hsu HC, Kuo PL, Li ML, et al. Elastic modulus measurements of human liver and correlation with pathology. Ultrasound Med Biol. 2002;28:467-74.
45. Masuzaki R, Tateishi R, Yoshida H, Sato S, Kato N, Kanai F, et al. Risk assessment of hepatocellular carcinoma in chronic hepatitis C patients by transient elastography. J Clin Gastroenterol. 2008;42:839-43.
46. Masuzaki R, Tateishi R, Yoshida H, Goto E, Sato T, Ohki T, et al. Prospective risk assessment for hepatocellular carcinoma development in patients with chronic hepatitis C by transient elastography. Hepatology. 2009;49:1954-61.
47. Jung KS, Kim SU. Clinical applications of transient elastography. Clin Mol Hepatol. 2012;18:163-73.
48. Poca M, Puente A, Graupera I, Villanueva C. Prognostic markers in patients with cirrhosis and portal hypertension who have not bled. Dis Markers. 2011;31:147-54.
49. Robic MA, Procopet B, Metivier S, Peron JM, Selves J, Vinel JP, et al. Liver stiffness accurately predicts portal hypertension related complications in patients with chronic liver disease: a prospective study. J Hepatol. 2011;55:1017-24.
50. Pesce A, Scilletta R, Branca A, Nigro L, Montineri A, Larocca L, et al. Does transient elastography (FibroScan(R)) have a role in decision making in hepatocellular carcinoma? HPB (Oxford). 2012;14:403-8.
51. Motosugi U, Ichikawa T, Koshiishi T, Sano K, Morisaka H, Ichikawa S, et al. Liver stiffness measured by magnetic resonance elastography as a risk factor for hepatocellular carcinoma: a preliminary case-control study. Eur Radiol. 2013;23(1):156-62.
52. Masuzaki R, Tateishi R, Yoshida H, Arano T, Uchino K, Enooku K, et al. Assessment of disease progression in patients with transfusion-associated chronic hepatitis C using transient elastography. World J Gastroenterol. 2012;18:1385-90.
53. McHutchison JG, Poynard T, Esteban-Mur R, Davis GL, Goodman ZD, Harvey J, et al. Hepatic HCV RNA before and after treatment with interferon alone or combined with ribavirin. Hepatology. 2002;35:688-93.
54. McHutchison JG, Patel K. Future therapy of hepatitis C. Hepatology. 2002;36:S245-52.
55. Shiratori Y, Imazeki F, Moriyama M, Yano M, Arakawa Y, Yokosuka O, et al. Histologic improvement of fibrosis in patients with hepatitis C who have sustained response to interferon therapy. Ann Intern Med. 2000;132:517-24.
56. Lok AS, Everhart JE, Wright EC, Di Bisceglie AM, Kim HY, Sterling RK, et al. Maintenance peginterferon therapy and other factors associated with hepatocellular carcinoma in patients with advanced hepatitis C. Gastroenterology 2011;140:840-9; quiz e12
57. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989;244:359-62.
58. Kim JL, Morgenstern KA, Lin C, Fox T, Dwyer MD, Landro JA, et al. Crystal structure of the hepatitis C virus NS3 protease domain complexed with a synthetic NS4A cofactor peptide. Cell. 1996;87:343-55.
59. Bressanelli S, Tomei L, Roussel A, Incitti I, Vitale RL, Mathieu M, et al. Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. Proc Natl Acad Sci USA. 1999;96:13034-9.
60. McHutchison JG, Everson GT, Gordon SC, Jacobson IM, Sulkowski M, Kauffman R, et al. Telaprevir with peginterferon and ribavirin for chronic HCV genotype 1 infection. N Engl J Med. 2009;360:1827-38.
61. Hezode C, Forestier N, Dusheiko G, Ferenci P, Pol S, Goeser T, et al. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med. 2009;360:1839-50.
62. Kwo PY, Lawitz EJ, McCone J, Schiff ER, Vierling JM, Pound D, et al. Efficacy of boceprevir, an NS3 protease inhibitor, in combination with peginterferon alfa-2b and ribavirin in treatment-naive patients with genotype 1 hepatitis C infection (SPRINT-1): an open-label, randomised, multicentre phase 2 trial. Lancet. 2010;376:705-16.
63. Singal AK, Freeman DH Jr, Anand BS. Meta-analysis: interferon improves outcomes following ablation or resection of hepatocellular carcinoma. Aliment Pharmacol Ther. 2010;32:851-8.
64. Ueno Y, Sollano JD, Farrell GC. Prevention of hepatocellular carcinoma complicating chronic hepatitis C. J Gastroenterol Hepatol. 2009;24:531-6.
65. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359:378-90.
66. Wilhelm S, Chien DS. BAY 43-9006: preclinical data. Curr Pharm Des. 2002;8:2255-7.
67. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 2004;64:7099-109.
68. Carlomagno F, Anaganti S, Guida T, Salvatore G, Troncone G, Wilhelm SM, et al. BAY 43-9006 inhibition of oncogenic RET mutants. J Natl Cancer Inst. 2006;98:326-34.
69. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2009;10:25-34.
70. Lee HC. Systemic chemotherapy of hepatocellular carcinoma-Korean experience. Oncology. 2008;75(Suppl 1):114-8.
71. Shim JH, Park JW, Choi JI, Park BJ, Kim CM. Practical efficacy of sorafenib monotherapy for advanced hepatocellular carcinoma patients in a Hepatitis B virus-endemic area. J Cancer Res Clin Oncol. 2009;135:617-25.
72. Yeung YP, Lo CM, Liu CL, Wong BC, Fan ST, Wong J. Natural history of untreated nonsurgical hepatocellular carcinoma. Am J Gastroenterol. 2005;100:1995-2004.
73. Park KW, Park JW, Choi JI, Kim TH, Kim SH, Park HS, et al. Survival analysis of 904 patients with hepatocellular carcinoma in a hepatitis B virus-endemic area. J Gastroenterol Hepatol. 2008;23:467-73.
74. Cancer of the Liver Italian Program (CLIP) investigators. A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients: the Cancer of the Liver Italian Program (CLIP) investigators. Hepatology 1998;28:751-5.
75. Llovet JM, Bustamante J, Castells A, Vilana R, Ayuso Mdel C, Sala M, et al. Natural history of untreated nonsurgical hepatocellular carcinoma: rationale for the design and evaluation of therapeutic trials. Hepatology. 1999;29:62-7.
76. Han KH, Seong J, Kim JK, Ahn SH, Lee do Y, Chon CY. Pilot clinical trial of localized concurrent chemoradiation therapy for locally advanced hepatocellular carcinoma with portal vein thrombosis. Cancer. 2008;113:995-1003.
77. Mazzella G, Accogli E, Sottili S, Festi D, Orsini M, Salzetta A, et al. Alpha interferon treatment may prevent hepatocellular carcinoma in HCV-related liver cirrhosis. J Hepatol. 1996;24:141-7.
78. Valla DC, Chevallier M, Marcellin P, Payen JL, Trepo C, Fonck M, et al. Treatment of hepatitis C virus-related cirrhosis: a randomized, controlled trial of interferon alfa-2b versus no treatment. Hepatology. 1999;29:1870-5.
79. Bernardinello E, Cavalletto L, Chemello L, Mezzocolli I, Donada C, Benvegnu L, et al. Long-term clinical outcome after beta-interferon therapy in cirrhotic patients with chronic hepatitis C: TVVH Study Group. Hepatogastroenterology. 1999;46:3216-22.
80. Nishiguchi S, Shiomi S, Nakatani S, Takeda T, Fukuda K, Tamori A, et al. Prevention of hepatocellular carcinoma in patients with chronic active hepatitis C and cirrhosis. Lancet. 2001;357:196-7.
81. Planas R, Quer JC, Enriquez J, Barrera JM, Dalmau B, Casanovas T, et al. Induction therapy with interferon alfa-2a in compensated hepatitis C virus-related cirrhosis. Randomized, multicenter study. Med Clin (Barc). 2002;118:641-4.
82. Azzaroli F, Accogli E, Nigro G, Trere D, Giovanelli S, Miracolo A, et al. Interferon plus ribavirin and interferon alone in preventing hepatocellular carcinoma: a prospective study on patients with HCV related cirrhosis. World J Gastroenterol. 2004;10:3099-102.
83. Soga K, Shibasaki K, Aoyagi Y. Effect of interferon on incidence of hepatocellular carcinoma in patients with chronic hepatitis C. Hepatogastroenterology. 2005;52:1154-8.
84. Fartoux L, Degos F, Trepo C, Goria O, Cales P, Tran A, et al. Effect of prolonged interferon therapy on the outcome of hepatitis C virus-related cirrhosis: a randomized trial. Clin Gastroenterol Hepatol. 2007;5:502-7.
85. Bruix J, Poynard T, Colombo M, Schiff E, Burak K, Heathcote EJ, et al. Maintenance therapy with peginterferon alfa-2b does not prevent hepatocellular carcinoma in cirrhotic patients with chronic hepatitis C. Gastroenterology. 2011;140:1990-9.