Effects of antiviral therapy on the recurrence of hepatocellular carcinoma after curative resection or liver transplantation

Hepatitis Monthly

Volumn 12, Issue 10 HCC, 2012, Pages 1-10

  Du, Yan ^a   Su, Tong ^a   Ding, Yibo ^a   Cao, Guangwen ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Carcinoma; Hepatocellular; Operative; Recurrence; Surgical procedures; Survival

Indexed keywords

ADEFOVIR DIPIVOXIL; ALPHA INTERFERON; ALPHA INTERFERON A; ALPHA2B INTERFERON; BETA INTERFERON; ENTECAVIR; HEPATITIS B ANTIBODY; HEPATITIS B(E) ANTIGEN; LAMIVUDINE; PEGINTERFERON ALPHA2B; RIBAVIRIN; TELBIVUDINE; TENOFOVIR DISOPROXIL;

ANTIVIRAL THERAPY; ARTICLE; BONE MARROW SUPPRESSION; CANCER PROGNOSIS; CANCER RECURRENCE; DEPRESSION; DISEASE FREE SURVIVAL; FATIGUE; FLU LIKE SYNDROME; HEPATITIS B; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LIVER CELL CARCINOMA; LIVER RESECTION; LIVER TRANSPLANTATION; META ANALYSIS (TOPIC); NEUTROPENIA; OVERALL SURVIVAL; RADIOFREQUENCY ABLATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); THROMBOCYTOPENIA; VIRAL CLEARANCE; VIRUS LOAD; VIRUS MUTATION; VIRUS REPLICATION;

EID: 84871482978     PISSN: 1735143X     EISSN: 17353408     Source Type: Journal    
DOI: 10.5812/hepatmon.6031     Document Type: Article

References (80)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90.
2. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132(7):2557-76.
3. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, et al. Liver transplantation for the treatment of small heap-tocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334(11):693-9.
4. Llovet JM, Schwartz M, Mazzaferro V. Resection and liver trans-plantation for hepatocellular carcinoma. Semin Liver Dis. 2005;25(2):181-200.
5. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38(2):200-7.
6. Wu JC, Huang YH, Chau GY, Su CW, Lai CR, Lee PC, et al. Risk factors for early and late recurrence in hepatitis B-related hepatocellular carcinoma. J Hepatol. 2009;51(5):890-7.
7. Kim SR, Yang J, Kudo M, Hino O. Recent advances in the management of chronic hepatitis B. Hepat Mon. 2011;11(8):601-11.
8. Hoofnagle JH, Seeff LB. Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med. 2006;355(23):2444-51.
9. Emerit I. Cytogenetic methods for detection of oxidative stress and evaluation of antioxidant therapy in hepatitis C infection. Hepat Mon. 2011;11(6):434-9.
10. Sun HC, Zhang W, Qin LX, Zhang BH, Ye QH, Wang L, et al. Positive serum hepatitis B e antigen is associated with higher risk of early recurrence and poorer survival in patients after curative resection of hepatitis B-related hepatocellular carcinoma. J Hepatol. 2007;47(5):684-90.
11. Hung IF, Poon RT, Lai CL, Fung J, Fan ST, Yuen MF. Recurrence of hepatitis B-related hepatocellular carcinoma is associated with high viral load at the time of resection. Am J Gastroenterol. 2008;103(7):1663-73.
12. Xia F, Lai EC, Lau WY, Ma K, Li X, Bie P, et al. High Serum Hyaluronic Acid and HBV Viral Load are Main Prognostic Factors of Local Recurrence after Complete Radiofrequency Ablation of Hepatitis B-Related Small Hepatocellular Carcinoma. Ann Surg Oncol. 2011.
13. Hosaka T, Suzuki F, Kobayashi M, Hirakawa M, Kawamura Y, Yatsuji H, et al. HBcrAg is a predictor of post-treatment recurrence of hepatocellular carcinoma during antiviral therapy. Liver Int. 2010;30(10):1461-70.
14. Yamanaka N, Takada M, Tanaka T, Yamanaka J, Yasui C, Ando T, et al. Viral serostatus and coexisting inflammatory activity affect metachronous carcinogenesis after hepatectomy for hepatocellular carcinoma. A further report. J Gastroenterol. 2000;35(3):206-13.
15. Yeh CT, So M, Ng J, Yang HW, Chang ML, Lai MW, et al. Hepatitis B virus-DNA level and basal core promoter A1762T/G1764A mutation in liver tissue independently predict postoperative survival in hepatocellular carcinoma. Hepatology. 2010;52(6):1922-33.
16. An HJ, Jang JW, Bae SH, Choi JY, Cho SH, Yoon SK, et al. Sustained low hepatitis B viral load predicts good outcome after curative resection in patients with hepatocellular carcinoma. J Gastroenterol Hepatol. 2010;25(12):1876-82.
17. Tokuhisa Y, Iizuka N, Sakaida I, Moribe T, Fujita N, Miura T, et al. Circulating cell-free DNA as a predictive marker for distant metastasis of hepatitis C virus-related hepatocellular carcinoma. Br J Cancer. 2007;97(10):1399-403.
18. Kubo S, Nishiguchi S, Shuto T, Tanaka H, Tsukamoto T, Hirohashi K, et al. Effects of continuous hepatitis with persistent hepatitis C viremia on outcome after resection of hepatocellular carcinoma. Jpn J Cancer Res. 1999;90(2):162-70.
19. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883-99.
20. Bertuzzo VR, Cescon M, Ravaioli M, Grazi GL, Ercolani G, Del Gaudio M, et al. Analysis of factors affecting recurrence of hepatocellular carcinoma after liver transplantation with a special focus on inflammation markers. Transplantation. 2011;91(11):1279-85.
21. Fu J, Xu D, Liu Z, Shi M, Zhao P, Fu B, et al. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology. 2007;132(7):2328-39.
22. Liu L, Zhu XD, Wang WQ, Shen Y, Qin Y, Ren ZG, et al. Activation of beta-catenin by hypoxia in hepatocellular carcinoma contributes to enhanced metastatic potential and poor prognosis. Clin Cancer Res. 2010;16(10):2740-50.
23. Mun HS, Lee SA, Kim H, Hwang ES, Kook YH, Kim BJ. Novel F141L pre-S2 mutation in hepatitis B virus increases the risk of hepatocellular carcinoma in patients with chronic genotype C infections. J Virol. 2011;85(1):123-32.
24. Han YF, Zhao J, Ma LY, Yin JH, Chang WJ, Zhang HW, et al. Factors predicting occurrence and prognosis of hepatitis-B-virus-related hepatocellular carcinoma. World J Gastroenterol. 2011;17(38):4258-70.
25. Liu S, Xie J, Yin J, Zhang H, Zhang Q, Pu R, et al. A matched case-control study of hepatitis B virus mutations in the preS and core promoter regions associated independently with hepatocellular carcinoma. J Med Virol. 2011;83(1):45-53.
26. Liu S, Zhang H, Gu C, Yin J, He Y, Xie J, et al. Associations between hepatitis B virus mutations and the risk of hepatocellular carcinoma: a meta-analysis. J Natl Cancer Inst. 2009;101(15):1066-82.
27. Yin J, Xie J, Zhang H, Shen Q, Han L, Lu W, et al. Significant association of different preS mutations with hepatitis B-related cirrhosis or hepatocellular carcinoma. J Gastroenterol. 2010;45(10):1063-71.
28. Cao GW. Clinical relevance and public health significance of hepatitis B virus genomic variations. World J Gastroenterol. 2009;15(46):5761-9.
29. Kay A, Zoulim F. Hepatitis B virus genetic variability and evolution. Virus Res. 2007;127(2):164-76.
30. Tsai HW, Lin YJ, Lin PW, Wu HC, Hsu KH, Yen CJ, et al. A clustered ground-glass hepatocyte pattern represents a new prognostic marker for the recurrence of hepatocellular carcinoma after surgery. Cancer. 2011;117(13):2951-60.
31. Nakamoto S, Imazeki F, Fukai K, Fujiwara K, Arai M, Kanda T, et al. Association between mutations in the core region of hepatitis C virus genotype 1 and hepatocellular carcinoma development. J Hepatol. 2010;52(1):72-8.
32. Toyoda H, Kumada T, Kaneoka Y, Maeda A. Amino acid substitutions in the hepatitis C virus core region are associated with postoperative recurrence and survival of patients with HCV genotype 1b-associated hepatocellular carcinoma. Ann Surg. 2011;254(2):326-32.
33. Huang L, Li J, Lau WY, Yan J, Zhou F, Liu C, et al. Perioperative reactivation of hepatitis B virus replication in patients undergoing partial hepatectomy for hepatocellular carcinoma. J Gastroenterol Hepatol. 2012;27(1):158-64.
34. Breitenstein S, Dimitroulis D, Petrowsky H, Puhan MA, Mullhaupt B, Clavien PA. Systematic review and meta-analysis of interferon after curative treatment of hepatocellular carcinoma in patients with viral hepatitis. Br J Surg. 2009;96(9):975-81.
35. Ikeda K, Arase Y, Saitoh S, Kobayashi M, Suzuki Y, Suzuki F, et al. 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. 2000;32(2):228-32.
36. Kubo S, Nishiguchi S, Hirohashi K, Tanaka H, Shuto T, Kinoshita H. Randomized clinical trial of long-term outcome after resection of hepatitis C virus-related hepatocellular carcinoma by postoperative interferon therapy. Br J Surg. 2002;89(4):418-22.
37. Shiratori Y, Shiina S, Teratani T, Imamura M, Obi S, Sato S, et al. Interferon therapy after tumor ablation improves prognosis in patients with hepatocellular carcinoma associated with hepatitis C virus. Ann Intern Med. 2003;138(4):299-306.
38. Lin SM, Lin CJ, Hsu CW, Tai DI, Sheen IS, Lin DY, et al. Prospective randomized controlled study of interferon-alpha in preventing hepatocellular carcinoma recurrence after medical ablation therapy for primary tumors. Cancer. 2004;100(2):376-82.
39. Sun HC, Tang ZY, Wang L, Qin LX, Ma ZC, Ye QH, et al. Postoperative interferon alpha treatment postponed recurrence and improved overall survival in patients after curative resection of HBV-related hepatocellular carcinoma: a randomized clinical trial. J Cancer Res Clin Oncol. 2006;132(7):458-65.
40. Mazzaferro V, Romito R, Schiavo M, Mariani L, Camerini T, Bhoori S, et al. Prevention of hepatocellular carcinoma recurrence with alpha-interferon after liver resection in HCV cirrhosis. Hepatology. 2006;44(6):1543-54.
41. Lo CM, Liu CL, Chan SC, Lam CM, Poon RT, Ng IO, et al. A randomized, controlled trial of postoperative adjuvant interferon therapy after resection of hepatocellular carcinoma. Ann Surg. 2007;245(6):831-42.
42. Singal AG, Volk ML, Jensen D, Di Bisceglie AM, Schoenfeld PS. A sustained viral response is associated with reduced liver-related morbidity and mortality in patients with hepatitis C virus. Clin Gastroenterol Hepatol. 2010;8(3):280-8, 8 e1.
43. Miao RY, Zhao HT, Yang HY, Mao YL, Lu X, Zhao Y, et al. Postoperative adjuvant antiviral therapy for hepatitis B/C virus-related hepatocellular carcinoma: a meta-analysis. World J Gastroenterol. 2010;16(23):2931-42.
44. Suou T, Mitsuda A, Koda M, Matsuda H, Maruyama S, Tanaka H, et al. Interferon alpha inhibits intrahepatic recurrence in hepatocellular carcinoma with chronic hepatitis C: a pilot study. Hepatol Res. 2001;20(3):301-11.
45. Hung CH, Lee CM, Wang JH, Tung HD, Chen CH, Lu SN. Antiviral therapy after non-surgical tumor ablation in patients with hepatocellular carcinoma associated with hepatitis C virus. J Gastroenterol Hepatol. 2005;20(10):1553-9.
46. Sakaguchi Y, Kudo M, Fukunaga T, Minami Y, Chung H, Kawasaki T. Low-dose, long-term, intermittent interferon-alpha-2b therapy after radical treatment by radiofrequency ablation delays clinical recurrence in patients with hepatitis C virus-related hepatocellular carcinoma. Intervirology. 2005;48(1):64-70.
47. Akamatsu M, Yoshida H, Shiina S, Teratani T, Obi S, Tateishi R, et al. Sustained viral response prolonged survival of patients with C-viral hepatocellular carcinoma. Liver Int. 2006;26(5):536-42.
48. Someya T, Ikeda K, Saitoh S, Kobayashi M, Hosaka T, Sezaki H, et al. Interferon lowers tumor recurrence rate after surgical resection or ablation of hepatocellular carcinoma: a pilot study of patients with hepatitis B virus-related cirrhosis. J Gastroenterol. 2006;41(12):1206-13.
49. Kudo M, Sakaguchi Y, Chung H, Hatanaka K, Hagiwara S, Ishikawa E, et al. Long-term interferon maintenance therapy improves survival in patients with HCV-related hepatocellular carcinoma after curative radiofrequency ablation. A matched case-control study. Oncology. 2007;72 (Suppl 1):132-8.
50. Jeong SC, Aikata H, Katamura Y, Azakami T, Kawaoka T, Saneto H, et al. Effects of a 24-week course of interferon-alpha therapy after curative treatment of hepatitis C virus-associated hepatocellular carcinoma. World J Gastroenterol. 2007;13(40):5343-50.
51. Jeong S, Aikata H, Katamura Y, Azakami T, Kawaoka T, Saneto H, et al. Low-dose intermittent interferon-alpha therapy for HCV-related liver cirrhosis after curative treatment of hepatocellular carcinoma. World J Gastroenterol. 2007;13(39):5188-95.
52. Qu LS, Jin F, Huang XW, Shen XZ. Interferon-alpha therapy after curative resection prevents early recurrence and improves survival in patients with hepatitis B virus-related hepatocellular carcinoma. J Surg Oncol. 2010;102(7):796-801.
53. Chan AC, Chok KS, Yuen WK, Chan SC, Poon RT, Lo CM, et al. Impact of antiviral therapy on the survival of patients after major hepatectomy for hepatitis B virus-related hepatocellular carcinoma. Arch Surg. 2011;146(6):675-81.
54. Ishikawa T, Higuchi K, Kubota T, Seki KI, Honma T, Yoshida T, et al. 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. 2011;59(115-116).
55. von Marschall Z, Scholz A, Cramer T, Schafer G, Schirner M, Oberg K, et al. Effects of interferon alpha on vascular endothelial growth factor gene transcription and tumor angiogenesis. J Natl Cancer Inst. 2003;95(6):437-48.
56. Wang L, Wu WZ, Sun HC, Wu XF, Qin LX, Liu YK, et al. Mechanism of interferon alpha on inhibition of metastasis and angiogenesis of hepatocellular carcinoma after curative resection in nude mice. J Gastrointest Surg. 2003;7(5):587-94.
57. Wang L, Tang ZY, Qin LX, Wu XF, Sun HC, Xue Q, et al. High-dose and long-term therapy with interferon-alfa inhibits tumor growth and recurrence in nude mice bearing human hepatocellular carcinoma xenografts with high metastatic potential. Hepatology. 2000;32(1):43-8.
58. Keng VW, Tschida BR, Bell JB, Largaespada DA. Modeling hepatitis B virus X-induced hepatocellular carcinoma in mice with the Sleeping Beauty transposon system. Hepatology. 2011;53(3):781-90.
59. Lee HH, Uen YH, Tian YF, Sun CS, Sheu MJ, Kuo HT, et al. Wnt-1 protein as a prognostic biomarker for hepatitis B-related and hepatitis C-related hepatocellular carcinoma after surgery. Cancer Epidemiol Biomarkers Prev. 2009;18(5):1562-9.
60. Thompson MD, Dar MJ, Monga SP. Pegylated interferon alpha targets Wnt signaling by inducing nuclear export of beta-catenin. J Hepatol. 2011;54(3):506-12.
61. Hwang S, Ahn CS, Song GW, Kim KH, Moon DB, Oh HB, et al. Post-transplantation prophylaxis with primary high-dose hepatitis B immunoglobulin monotherapy and complementary preemptive antiviral add-on. Liver Transpl. 2011;17(4):456-65.
62. Bihl F, Russmann S, Gurtner V, Di Giammarino L, Pizzi-Bosman L, Michel M, et al. Hyperimmune anti-HBs plasma as alternative to commercial immunoglobulins for prevention of HBV recurrence after liver transplantation. BMC Gastroenterol. 2010;10:71.
63. Ahn J, Cohen SM. Prevention of Hepatitis B Recurrence in Liver Transplant Patients Using Oral Antiviral Therapy without Long-Term Hepatitis B Immunoglobulin. Hepat Mon. 2011;11(8):638-45.
64. Pallier C, Castera L, Soulier A, Hezode C, Nordmann P, Dhumeaux D, et al. Dynamics of hepatitis B virus resistance to lamivudine. J Virol. 2006;80(2):643-53.
65. Lok AS, McMahon BJ. Chronic hepatitis B. Hepatology. 2007;45(2):507-39.
66. Piao CY, Fujioka S, Iwasaki Y, Fujio K, Kaneyoshi T, Araki Y, et al. Lamivudine treatment in patients with HBV-related hepatocellular carcinoma--using an untreated, matched control cohort. Acta Med Okayama. 2005;59(5):217-24.
67. Kuzuya T, Katano Y, Kumada T, Toyoda H, Nakano I, Hirooka Y, et al. Efficacy of antiviral therapy with lamivudine after initial treatment for hepatitis B virus-related hepatocellular carcinoma. J Gastroenterol Hepatol. 2007;22(11):1929-35.
68. Kubo S, Tanaka H, Takemura S, Yamamoto S, Hai S, Ichikawa T, et al. Effects of lamivudine on outcome after liver resection for hepatocellular carcinoma in patients with active replication of hepatitis B virus. Hepatol Res. 2007;37(2):94-100.
69. Yoshida H, Goto E, Sato T, Ohki T, Masuzaki R, Tateishi R, et al. Safety and efficacy of lamivudine after radiofrequency ablation in patients with hepatitis B virus-related hepatocellular carcinoma. Hepatol Int. 2008;2(1):89-94.
70. Li N, Lai EC, Shi J, Guo WX, Xue J, Huang B, et al. A comparative study of antiviral therapy after resection of hepatocellular carcinoma in the immune-active phase of hepatitis B virus infection. Ann Surg Oncol. 2010;17(1):179-85.
71. Zimmerman MA, Ghobrial RM, Tong MJ, Hiatt JR, Cameron AM, Busuttil RW. Antiviral prophylaxis and recurrence of hepatocellular carcinoma following liver transplantation in patients with hepatitis B. Transplant Proc. 2007;39(10):3276-80.
72. Ling R, Mutimer D, Ahmed M. Selection of mutations in the hepatitis B virus polymerase during therapy of transplant recipients with lamivudine. Hepatology. 1996;24:711-13.
73. Liaw YF, Chien RN, Yeh CT, Tsai SL, Chu CM. Acute exacerbation and hepatitis B virus clearance after emergence of YMDD motif mutation during lamivudine therapy. Hepatology. 1999;30(2):567-72.
74. Lai CL, Dienstag J, Schiff E, Leung NW, Atkins M, Hunt C, et al. Prevalence and clinical correlates of YMDD variants during lamivudine therapy for patients with chronic hepatitis B. Clin Infect Dis. 2003;36(6):687-96.
75. Yeh CT, Chien RN, Chu CM, Liaw YF. Clearance of the original hepatitis B virus YMDD-motif mutants with emergence of distinct lamivudine-resistant mutants during prolonged lamivudine therapy. Hepatology. 2000;31(6):1318-26.
76. Sayan M, Akhan SC, Senturk O. Frequency and Mutation Patterns of Resistance in Patients with Chronic Hepatitis B Infection Treated with Nucleos(t)ide Analogs in Add-On and Switch Strategies. Hepat Mon. 2011;11(10):835-42.
77. Sherman M, Yurdaydin C, Sollano J, Silva M, Liaw YF, Cianciara J, et al. Entecavir for treatment of lamivudine-refractory, HBeAgpositive chronic hepatitis B. Gastroenterology. 2006;130(7):2039-49.
78. Yang H, Qi X, Das K. In vitro characterization and molecular modeling analysis of a novel adefovir resistance mutation rtN236T in the HBV polymerase. J Hepatol. 2004;40:114.
79. Lai CL, Gane E, Liaw YF, Hsu CW, Thongsawat S, Wang Y, et al. Telbivudine versus lamivudine in patients with chronic hepatitis B. N Engl J Med. 2007;357(25):2576-88.
80. Yeh CT, Chen T, Hsu CW, Chen YC, Lai MW, Liang KH, et al. Emergence of the rtA181T/sW172* mutant increased the risk of hepatoma occurrence in patients with lamivudine-resistant chronic hepatitis B. BMC Cancer. 2011;11:398.