Review: Current status of antiviral therapy for hepatitis B

Therapeutic Advances in Gastroenterology

Volumn 1, Issue 1, 2008, Pages 61-75

  Lau, Daryl T Y ^a   Bleibel, Wissam ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

drug resistance; Hepatitis B virus; nucleos(t)ide analogues; pegylated interferon

Indexed keywords

EID: 84993661175     PISSN: 1756283X     EISSN: None     Source Type: Journal    
DOI: 10.1177/1756283X08093944     Document Type: Review

References (87)

1. Alward, W.L., McMahon, B.J., Hall, D.B., Heyward, W.L., Francis, D.P. and Bender, T.R. (1985) The long-term serological course of asymptomatic hepatitis B virus carriers and the development of primary hepatocellular carcinoma. J Infect Dis 151 (4): 604-609.
2. Arora, G. and Keeffe, E.B. (2007) Chronic hepatitis B with advanced fibrosis or cirrhosis: impact of antiviral therapy. Rev Gastroenterol Disord 7 (2): 63-73.
3. Bondini, S., Kallman, J., Wheeler, A., Prakash, S., Gramlich, T., Jondle, D.M. et al. (2007) Impact of non-alcoholic fatty liver disease on chronic hepatitis B. Liver Int 27 (5): 607-611.
4. Chan, H.L., Hui, A.Y., Wong, M.L., Tse, A.M., Hung, L.C., Wong, V.W. et al. (2004) Genotype C hepatitis B virus infection is associated with an increased risk of hepatocellular carcinoma. Gut 53 (10): 1494-1498.
5. Chen, C.J., Yang, H.I., Su, J., Jen, C.L., You, S.L., Lu, S.N. et al. (2006) Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. Jama 295 (1): 65-73.
6. Chu, C.M., Lin, D.Y. and Liaw, Y.F. (2007) Does increased body mass index with hepatic steatosis contribute to seroclearance of hepatitis B virus (HBV) surface antigen in chronic HBV infection? Int J Obes (Lond ) 31 (5): 871-875.
7. Colonno, R.J., Genovesi, E.V., Medina, I., Lamb, L., Durham, S.K., Huang, M.L. et al. (2001) Long-term entecavir treatment results in sustained antiviral efficacy and prolonged life span in the woodchuck model of chronic hepatitis infection. J Infect Dis 184 (10): 1236-1245.
8. Colonno, R.J., Rose, R., Baldick, C.J., Levine, S., Pokornowski, K., Yu, C.F. et al. (2006) Entecavir resistance is rare in nucleoside naive patients with hepatitis B. Hepatology 44 (6): 1656-1665.
9. Cooksley, W.G., Piratvisuth, T., Lee, S.D., Mahachai, V., Chao, Y.C., Tanwandee, T. et al. (2003) Peginterferon alpha-2a (40 kDa): an advance in the treatment of hepatitis B e antigen-positive chronic hepatitis B. J Viral Hepat 10 (4): 298-305.
10. Del Poggio, P., Zaccanelli, M., Oggionni, M., Colombo, S., Jamoletti, C. and Puhalo, V. (2007) Low-dose tenofovir is more potent than adefovir and is effective in controlling HBV viremia in chronic HBeAg-negative hepatitis B. World J Gastroenterol 13 (30): 4096-4099.
11. Doo, E. and Liang, T.J. (2001) Molecular anatomy and pathophysiologic implications of drug resistance in hepatitis B virus infection. Gastroenterology 120 (4): 1000-1008.
12. Fan, Y.F., Lu, C.C., Chen, W.C., Yao, W.J., Wang, H.C., Chang, T.T. et al. (2001) Prevalence and significance of hepatitis B virus (HBV) pre-S mutants in serum and liver at different replicative stages of chronic HBV infection. Hepatology 33 (1): 277-286.
13. Fung, S.K., Chae, H.B., Fontana, R.J., Conjeevaram, H., Marrero, J., Oberhelman, K. et al. (2006) Virologic response and resistance to adefovir in patients with chronic hepatitis B. J Hepatol 44 (2): 283-290.
14. Gish, R.G., Lau, D.T., Schmid, P. and Perrillo, R. (2007) A pilot study of extended duration peginterferon alfa-2a for patients with hepatitis B e antigen-negative chronic hepatitis B. Am J Gastroenterol 102 (12): 2718-2723.
15. Gish, R.G., Lok, A.S., Chang, T.T., de Man, R.A., Gadano, A., Sollano, J. et al. (2007) Entecavir therapy for up to 96 weeks in patients with HBeAg-positive chronic hepatitis B. Gastroenterology 133 (5): 1437-1444.
16. Gordillo, R.M., Gutierrez, J. and Casal, M. (2005) Evaluation of the COBAS TaqMan 48 real-time PCR system for quantitation of hepatitis B virus DNA. J Clin Microbiol 43 (7): 3504-3507.
17. Hadziyannis, S.J. and Vassilopoulos, D. (2001) Hepatitis B e antigen-negative chronic hepatitis B. Hepatology 34(4 Pt 1): 617-624.
18. Hadziyannis, S.J., Papatheodoridis, G.V. and Vassilopoulos, D. (2003) Treatment of HBeAg-negative chronic hepatitis B. Semin Liver Dis 23 (1): 81-88.
19. Hadziyannis, S.J., Tassopoulos, N.C., Heathcote, E.J., Chang, T.T., Kitis, G., Rizzetto, M. et al. (2003) Adefovir dipivoxil for the treatment of hepatitis B e antigen-negative chronic hepatitis B. N Engl J Med 348 (9): 800-807.
20. Hadziyannis, S.J., Tassopoulos, N.C., Heathcote, E.J., Chang, T.T., Kitis, G., Rizzetto, M. et al. (2005) Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B. N Engl J Med 352 (26): 2673-2681.
21. Hollinger, F.B. and Lau, D.T. (2006) Hepatitis B: the pathway to recovery through treatment. Gastroenterol Clin North Am 35 (4): 895-931.
22. Hoofnagle, J.H., Doo, E., Liang, T.J., Fleischer, R. and Lok, A.S. (2007) Management of hepatitis B: summary of a clinical research workshop. Hepatology 45 (4): 1056-1075.
23. Hoofnagle, J.H., Shafritz, D.A. and Popper, H. (1987) Chronic type B hepatitis and the ‘healthy‘ HBsAg carrier state. Hepatology 7 (4): 758-763.
24. Hu, K.Q., Currie, S.L., Shen, H., Cheung, R.C., Ho, S.B., Bini, E.J. et al. (2007) Clinical implications of hepatic steatosis in patients with chronic hepatitis C: a multicenter study of US veterans. Dig Dis Sci 52 (2): 570-578.
25. Hunt, C.M., McGill, J.M., Allen, M.I. and Condreay, L.D. (2000) Clinical relevance of hepatitis B viral mutations. Hepatology 31 (5): 1037-1044.
26. Iloeje, U.H., Yang, H.I., Su, J., Jen, C.L., You, S.L. and Chen, C.J. (2006) Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology 130 (3): 678-686.
27. Izzedine, H., Launay-Vacher, V. and Deray, G. (2005) Antiviral drug-induced nephrotoxicity. Am J Kidney Dis 45 (5): 804-817.
28. Janssen, H.L., van Zonneveld, M., Senturk, H., Zeuzem, S., Akarca, US, Cakaloglu, Y. et al. (2005) Pegylated interferon alfa-2b alone or in combination with lamivudine for HBeAg-positive chronic hepatitis B: a randomised trial. Lancet 365 (9454): 123-129.
29. Keeffe, E.B., Dieterich, D.T., Pawlotsky, J.M. and Benhamou, Y. (2008) Chronic hepatitis B: preventing, detecting, and managing viral resistance. Clin Gastroenterol Hepatol 6 (3): 268-274.
30. Keeffe, E.B., Zeuzem, S., Koff, R.S., Dieterich, D.T., Esteban-Mur, R., Gane, E.J. et al. (2007) Report of an international workshop: roadmap for management of patients receiving oral therapy for chronic hepatitis B. Clin Gastroenterol Hepatol 5 (8): 890-897.
31. Kidd-Ljunggren, K., Miyakawa, Y. and Kidd, A.H. (2002) Genetic variability in hepatitis B viruses. J Gen Virol 83(Pt 6): 1267-1280.
32. Kim, H.C., Nam, C.M., Jee, S.H., Han, K.H., Oh, D.K. and Suh, I. (2004) Normal serum aminotransferase concentration and risk of mortality from liver diseases: prospective cohort study. BMJ 328 (7446): 983.
33. Kim, J.H., Yu, S.K., Seo, Y.S., Yim, H.J., Yeon, J.E., Park, J.J. et al. (2007) Clinical outcomes of chronic hepatitis B patients with persistently detectable serum hepatitis B virus DNA during lamivudine therapy. J Gastroenterol Hepatol 22 (8): 1220-1225.
34. Lai, C.L., Gane, E., Liaw, Y.F., Hsu, C.W., Thongsawat, S., Wang, Y. et al. (2007) Telbivudine versus lamivudine in patients with chronic hepatitis B. N Engl J Med 357 (25): 2576-2588.
35. Lai, C.L., Shouval, D., Lok, A.S., Chang, T.T., Cheinquer, H., Goodman, Z. et al. (2006) Entecavir versus lamivudine for patients with HBeAg-negative chronic hepatitis B. N Engl J Med 354 (10): 1011-1020.
36. Lampertico, P., Vigano, M., Manenti, E., Iavarone, M., Sablon, E. and Colombo, M. (2007) Low resistance to adefovir combined with lamivudine: a 3-year study of 145 lamivudine-resistant hepatitis B patients. Gastroenterology 133 (5): 1445-1451.
37. Laras, A., Koskinas, J., Dimou, E., Kostamena, A. and Hadziyannis, S.J. (2006) Intrahepatic levels and replicative activity of covalently closed circular hepatitis B virus DNA in chronically infected patients. Hepatology 44 (3): 694-702.
38. Lau, D.T., Everhart, J., Kleiner, D.E., Park, Y., Vergalla, J., Schmid, P. et al. (1997) Long-term follow-up of patients with chronic hepatitis B treated with interferon alfa. Gastroenterology 113 (5): 1660-1667.
39. Lau, D.T., Khokhar, M.F., Doo, E., Ghany, M.G., Herion, D., Park, Y. et al. (2000) Long-term therapy of chronic hepatitis B with lamivudine. Hepatology 32(4 Pt 1): 828-834.
40. Lau, G.K., Piratvisuth, T., Luo, K.X., Marcellin, P., Thongsawat, S., Cooksley, G. et al. (2005)
41. Peginterferon Alfa- 2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N Engl J Med 352 (26): 2682-2695.
42. Lau, G.K., Tsiang, M., Hou, J., Yuen, S., Carman, W.F., Zhang, L. et al. (2000) Combination therapy with lamivudine and famciclovir for chronic hepatitis B-infected Chinese patients: a viral dynamics study. Hepatology 32 (2): 394-399.
43. Leandro, G., Mangia, A., Hui, J., Fabris, P., Rubbia-Brandt, L., Colloredo, G. et al. (2006) Relationship between steatosis, inflammation, and fibrosis in chronic hepatitis C: a meta-analysis of individual patient data. Gastroenterology 130 (6): 1636-1642.
44. Lee, W.M. (1997) Hepatitis B virus infection. N Engl J Med 337 (24): 1733-1745.
45. Leemans, W.F., Ter Borg, M.J. and de Man, R.A. (2007) Review article: Success and failure of nucleoside and nucleotide analogues in chronic hepatitis B. Aliment Pharmacol Ther 26 Suppl 2: 171-182.
46. Leung, N.W., Lai, C.L., Chang, T.T., Guan, R., Lee, C.M., Ng, K.Y. et al. (2001) Extended lamivudine treatment in patients with chronic hepatitis B enhances hepatitis B e antigen seroconversion rates: results after 3 years of therapy. Hepatology 33 (6): 1527-1532.
47. Liaw, Y.F., Leung, N.W., Chang, T.T., Guan, R., Tai, D.I., Ng, K.Y. et al. (2000) Effects of extended lamivudine therapy in Asian patients with chronic hepatitis B. Asia Hepatitis Lamivudine Study Group. Gastroenterology 119 (1): 172-180.
48. Liaw, Y.F., Sung, J.J., Chow, W.C., Farrell, G., Lee, C.Z., Yuen, H. et al. (2004) Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med 351 (15): 1521-1531.
49. Lin, S.M., Sheen, I.S., Chien, R.N., Chu, C.M. and Liaw, Y.F. (1999) Long-term beneficial effect of interferon therapy in patients with chronic hepatitis B virus infection. Hepatology 29 (3): 971-975.
50. Liu, C.J., Chen, P.J., Lai, M.Y., Kao, J.H. and Chen, D.S. (2001) Hepatitis B virus variants in patients receiving lamivudine treatment with breakthrough hepatitis evaluated by serial viral loads and full-length viral sequences. Hepatology 34 (3): 583-589.
51. Livingston, S.E., Simonetti, J.P., McMahon, B.J., Bulkow, L.R., Hurlburt, K.J., Homan, C.E. et al. (2007) Hepatitis B virus genotypes in Alaska Native people with hepatocellular carcinoma: preponderance of genotype F. J Infect Dis 195 (1): 5-11.
52. Locarnini, S. (2005) Molecular virology and the development of resistant mutants: implications for therapy. Semin Liver Dis 25(Suppl 1): 9-19.
53. Locarnini, S. and Mason, W.S. (2006) Cellular and virological mechanisms of HBV drug resistance. J Hepatol 44 (2): 422-431.
54. Locarnini, S., Hatzakis, A., Heathcote, J., Keeffe, E.B., Liang, T.J., Mutimer, D. et al. (2004) Management of antiviral resistance in patients with chronic hepatitis B. Antivir Ther 9 (5): 679-693.
55. Lok, A.S. and McMahon, B.J. (2007) Chronic hepatitis B. Hepatology 45 (2): 507-539.
56. Lok, A.S., Chung, H.T., Liu, V.W. and Ma, O.C. (1993) Long-term follow-up of chronic hepatitis B patients treated with interferon alfa. Gastroenterology 105 (6): 1833-1838.
57. Lok, A.S., Heathcote, E.J. and Hoofnagle, J.H. (2001) Management of hepatitis B: 2000-summary of a workshop. Gastroenterology 120 (7): 1828-1853.
58. Lole, K.S. and Arankalle, V.A. (2006) Quantitation of hepatitis B virus DNA by real-time PCR using internal amplification control and dual TaqMan MGB probes. J Virol Methods 135 (1): 83-90.
59. Magnius, L.O. and Norder, H. (1995) Subtypes, genotypes and molecular epidemiology of the hepatitis B virus as reflected by sequence variability of the S-gene. Intervirology 1995; 38(1-2): 24-34.
60. Manesis, E.K. and Hadziyannis, S.J. (2001) Interferon alpha treatment and retreatment of hepatitis B e antigen-negative chronic hepatitis B. Gastroenterology 121 (1): 101-109.
61. Marcellin, P., Lau, G.K., Bonino, F., Farci, P., Hadziyannis, S., Jin, R. et al. (2004) Peginterferon alfa-2a alone, lamivudine alone, and the two in combination in patients with HBeAg-negative chronic hepatitis B. N Engl J Med 351 (12): 1206-1217.
62. Margolis, H.S., Alter, M.J. and Hadler, S.C. (1991) Hepatitis B: evolving epidemiology and implications for control. Semin Liver Dis 11 (2): 84-92.
63. McMahon, B.J., Alward, W.L., Hall, D.B., Heyward, W.L., Bender, T.R., Francis, D.P. et al. (1985) Acute hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent development of the carrier state. J Infect Dis 151 (4): 599-603.
64. McQuillan, G.M., Coleman, P.J., Kruszon-Moran, D., Moyer, L.A., Lambert, S.B. and Margolis, H.S. (1999) Prevalence of hepatitis B virus infection in the United States: the national health and nutrition examination surveys, 1976 through 1994. Am J Public Health 89 (1): 14-18.
65. Niederau, C., Heintges, T., Lange, S., Goldmann, G., Niederau, C.M., Mohr, L. et al. (1996) Long-term follow-up of HBeAg-positive patients treated with interferon alfa for chronic hepatitis B. N Engl J Med 334 (22): 1422-1427.
66. Okamoto, H., Tsuda, F., Akahane, Y., Sugai, Y., Yoshiba, M., Moriyama, K. et al. (1994) Hepatitis B virus with mutations in the core promoter for an e antigen-negative phenotype in carriers with antibody to e antigen. J Virol 68 (12): 8102-8110.
67. Okamoto, H., Yotsumoto, S., Akahane, Y., Yamanaka, T., Miyazaki, Y., Sugai, Y. et al. (1990) Hepatitis B viruses with precore region defects prevail in persistently infected hosts along with seroconversion to the antibody against e antigen. J Virol 64 (3): 1298-1303.
68. Ono-Nita, S.K., Kato, N., Shiratori, Y., Lan, K.H., Yoshida, H., Carrilho, F.J. et al. (1999) Susceptibility of lamivudine-resistant hepatitis B virus to other reverse transcriptase inhibitors. J Clin Invest 103 (12): 1635-1640.
69. Papatheodoridis, G.V., Dimou, E., Dimakopoulos, K., Manolakopoulos, S., Rapti, I., Kitis, G. et al. (2005) Outcome of hepatitis B e antigen-negative chronic hepatitis B on long-term nucleos(t)ide analog therapy starting with lamivudine. Hepatology 42 (1): 121-129.
70. Patton, H.M., Patel, K., Behling, C., Bylund, D., Blatt, L.M., Vallee, M. et al. (2004) The impact of steatosis on disease progression and early and sustained treatment response in chronic hepatitis C patients. J Hepatol 40 (3): 484-490.
71. Pawlotsky, J.M., Dusheiko, G., Hatzakis, A., Lau, D., Lau, G., Liang, T.J. et al. (2008) Virologic monitoring of hepatitis B virus therapy in clin trials and practice: recommendations for a standardized approach. Gastroenterology 134 (2): 405-415.
72. Perazella, M.A. (2003) Drug-induced renal failure: update on new medications and unique mechanisms of nephrotoxicity. Am J Med Sci 325 (6): 349-362.
73. Perrillo, R.P. (2001) Acute flares in chronic hepatitis B: the natural and unnatural history of an immunologically mediated liver disease. Gastroenterology 120 (4): 1009-1022.
74. Sablon, E. and Shapiro, F. (2005) Advances in molecular diagnosis of HBV infection and drug resistance. Int J Med Sci 2 (1): 8-16.
75. Sablon, E., Shapiro, F. and Zoulim, F. (2003) Early detection of hepatitis B drug resistance: implications for patient management. Expert Rev Mol Diagn 3 (5): 535-547.
76. Sugauchi, F., Ohno, T., Orito, E., Sakugawa, H., Ichida, T., Komatsu, M. et al. (2003) Influence of hepatitis B virus genotypes on the development of preS deletions and advanced liver disease. J Med Virol 70 (4): 537-544.
77. Tacke, F., Manns, M.P. and Trautwein, C. (2004) Influence of mutations in the hepatitis B virus genome on virus replication and drug resistance- implications for novel antiviral strategies. Curr Med Chem 11 (20): 2667-2677.
78. Tan, J., Degertekin, B., Wong, S.N., Husain, M., Oberhelman, K. and Lok, A.S. (2008) Tenofovir monotherapy is effective in hepatitis B patients with antiviral treatment failure to adefovir in the absence of adefovir-resistant mutations. J Hepatol 48 (3): 391-398.
79. Tenney, D.J., Levine, S.M., Rose, R.E., Walsh, A.W., Weinheimer, S.P., Discotto, L. et al. (2004) Clinical emergence of entecavir-resistant hepatitis B virus requires additional substitutions in virus already resistant to Lamivudine. Antimicrob Agents Chemother 48 (9): 3498-3507.
80. Tsiang, M., Rooney, J.F., Toole, J.J. and Gibbs, C.S. (1999) Biphasic clearance kinetics of hepatitis B virus from patients during adefovir dipivoxil therapy. Hepatology 29 (6): 1863-1869.
81. Villet, S., Pichoud, C., Billioud, G., Barraud, L., Durantel, S., Trepo, C. et al. (2008) Impact of hepatitis B virus rtA181V/T mutants on hepatitis B treatment failure. J Hepatol 48 (5): 747-755.
82. Werle-Lapostolle, B., Bowden, S., Locarnini, S., Wursthorn, K., Petersen, J., Lau, G. et al. (2004) Persistence of cccDNA during the natural history of chronic hepatitis B and decline during adefovir dipivoxil therapy. Gastroenterology 126 (7): 1750-1758.
83. Yang, H., Qi, X., Sabogal, A., Miller, M., Xiong, S. and Delaney, W.E. 4th. (2005) Cross-resistance testing of next-generation nucleoside and nucleotide analogues against lamivudine-resistant HBV. Antivir Ther 10 (5): 625-633.
84. Yuen, M.F., Hui, C.K., Cheng, C.C., Wu, C.H., Lai, Y.P. and Lai, C.L. (2001) Long-term follow-up of interferon alfa treatment in Chinese patients with chronic hepatitis B infection: The effect on hepatitis B e antigen seroconversion and the development of cirrhosis-related complications. Hepatology 34 (1): 139-145.
85. Yuen, M.F., Tanaka, Y., Mizokami, M., Yuen, J.C., Wong, D.K., Yuan, H.J. et al. (2004) Role of hepatitis B virus genotypes Ba and C, core promoter and precore mutations on hepatocellular carcinoma: a case control study. Carcinogenesis 25 (9): 1593-1598.
86. Zoulim, F. (2005) Combination of nucleoside analogues in the treatment of chronic hepatitis B virus infection: lesson from experimental models. J Antimicrob Chemother 55 (5): 608-611.
87. Zoulim, F. (2006) In vitro models for studying hepatitis B virus drug resistance. Semin Liver Dis 26 (2): 171-180.