Optimal management of chronic hepatitis B patients with treatment failure and antiviral drug resistance

Liver International

Volumn 33, Issue SUPPL. 1, 2013, Pages 116-124

  Zoulim, Fabien ^a,b   Locarnini, Stephen ^c  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b HOSPICES CIVILS DE LYON   (France)

^c VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

Author keywords

Antiviral therapy; Combination chemotherapy; Drug resistance; Hepatitis B

Indexed keywords

ADEFOVIR DIPIVOXIL; ALPHA INTERFERON; ANTIVIRUS AGENT; DEOXYCYTIDINE; ENTECAVIR; LAMIVUDINE; PEGINTERFERON; TELBIVUDINE;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; CLINICAL EFFECTIVENESS; DRUG EFFICACY; HEPATITIS B; HUMAN; LIVER DISEASE; MULTIDRUG RESISTANCE; PATIENT COMPLIANCE; REVIEW; TREATMENT FAILURE; TREATMENT PLANNING; TREATMENT RESPONSE; VIREMIA; VIRUS LOAD; VIRUS REPLICATION;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; DRUG THERAPY, COMBINATION; GENOTYPE; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; PHENOTYPE; TIME FACTORS; TREATMENT FAILURE;

EID: 84872006797     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12069     Document Type: Review

References (71)

1. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of chronic hepatitis B. J Hepatol 2012; 57: 167-85.
2. Shaw T, Locarnini S. Entecavir for the treatment of chronic hepatitis B. Expert Rev Anti Infect Ther 2004; 2: 853-71.
3. Domingo E. Quasispecies and the development of new antiviral strategies. Prog Drug Res 2003; 60: 133-58.
4. Ahmed SNS, Tavan D, Pichoud C, Berby F, Stuyver L, et al. Early detection of viral resistance by determination of hepatitis B virus polymerase mutations in patients treated by lamivudine for chronic hepatitis B. Hepatology 2000; 32: 1078-88.
5. Yuen MF, Sablon E, Hui CK, et al. Factors associated with hepatitis B virus DNA breakthrough in patients receiving prolonged lamivudine therapy. Hepatology 2001; 34(4 Pt 1): 785-91.
6. Lai CL, Dienstag J, Schiff E, et al. Prevalence and clinical correlates of YMDD variants during lamivudine therapy for patients with chronic hepatitis B. Clin Infect Dis 2003; 36: 687-96.
7. Lok AS, Lai CL, Leung N, et al. Long-term safety of lamivudine treatment in patients with chronic hepatitis B. Gastroenterology 2003; 125: 1714-22.
8. Dienstag JL, Goldin RD, Heathcote EJ, et al. Histological outcome during long-term lamivudine therapy. Gastroenterology 2003; 124: 105-17.
9. Liaw YF, Sung JJ, Chow WC, et al. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med 2004; 351: 1521-31.
10. Hadziyannis SJ, Tassopoulos NC, Heathcote EJ, et al. Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B for up to 5 years. Gastroenterology 2006; 131: 1743-51.
11. Fung SK, Andreone P, Han SH, et al. Adefovir-resistant hepatitis B can be associated with viral rebound and hepatic decompensation. J Hepatol 2005; 43: 937-43.
12. Zoulim F, Poynard T, Degos F, et al. A prospective study of the evolution of lamivudine resistance mutations in patients with chronic hepatitis B treated with lamivudine. J Viral Hepat 2006; 13: 278-88.
13. Lai CL, Gane E, Liaw YF, et al. Telbivudine versus lamivudine in patients with chronic hepatitis B. N Engl J Med 2007; 357: 2576-88.
14. Gish R, Jia JD, Locarnini S, Zoulim F. Selection of chronic hepatitis B therapy with high barrier to resistance. Lancet Infect Dis [Research Support, Non-U.S. Gov't] 2012; 12: 341-53.
15. Zoulim F, Locarnini S. Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 2009; 137: 1593-608 e1-2.
16. Locarnini S, Mason WS. Cellular and virological mechanisms of HBV drug resistance. J Hepatol 2006; 44: 422-31.
17. Delaney WEt, Locarnini S, Shaw T. Resistance of hepatitis B virus to antiviral drugs: current aspects and directions for future investigation. Antivir Chem Chemother 2001; 12: 1-35.
18. Shaw T, Bartholomeusz A, Locarnini S. HBV drug resistance: mechanisms, detection and interpretation. J Hepatol 2006; 44: 593-606.
19. 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: 1318-26.
20. Ogata N, Fujii K, Takigawa S, et al. Novel patterns of amino acid mutations in the hepatitis B virus polymerase in association with resistance to lamivudine therapy in japanese patients with chronic hepatitis B. J Med Virol 1999; 59: 270-6.
21. Delaney WEt, Yang H, Westland CE, et al. The hepatitis B virus polymerase mutation rtV173L is selected during lamivudine therapy and enhances viral replication in vitro. J Virol 2003; 77: 11833-41.
22. Bartholomeusz A, Locarnini S, Ayres A, et al. Mechanistic basis for hepatitis B virus resistance to acyclic nucleoside phosphonate analogues, adefovir and tenofovir. Hepatology 2005; 42: 594A-A.
23. Tenney DJ, Levine SM, Rose RE, et al. Clinical emergence of entecavir-resistant hepatitis B virus requires additional substitutions in virus already resistant to Lamivudine. Antimicrob Agents Chemother 2004; 48: 3498-507.
24. Angus P, Vaughan R, Xiong S, et al. Resistance to adefovir dipivoxil therapy associated with the selection of a novel mutation in the HBV polymerase. Gastroenterology 2003; 125: 292-7.
25. Villeneuve JP, Durantel D, Durantel S, et al. Selection of a hepatitis B virus strain resistant to adefovir in a liver transplantation patient. J Hepatol 2003; 39: 1085-9.
26. Hadziyannis SJ, Tassopoulos NC, Heathcote EJ, et al. Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B. N Engl J Med 2005; 352: 2673-81.
27. Lok AS, Zoulim F, Locarnini S, et al. Antiviral drug-resistant HBV: standardization of nomenclature and assays and recommendations for management. Hepatology 2007; 46: 254-65.
28. Patterson SJ, George J, Strasser SI, et al. Tenofovir disoproxil fumarate rescue therapy following failure of both lamivudine and adefovir dipivoxil in chronic hepatitis B. Gut 2010; 60: 247-54.
29. van Bommel F, de Man RA, Wedemeyer H, et al. Long-term efficacy of tenofovir monotherapy for hepatitis B virus-monoinfected patients after failure of nucleoside/nucleotide analogues. Hepatology 2010; 51: 73-80.
30. Berg T, Marcellin P, Zoulim F, et al. Tenofovir is effective alone or with emtricitabine in adefovir-treated patients with chronic-hepatitis B virus infection. Gastroenterology 2010; 139: 1207-17.
31. Patterson SJ, George J, Strasser SI, et al. Tenofovir disoproxil fumarate rescue therapy following failure of both lamivudine and adefovir dipivoxil in chronic hepatitis B. Gut 2011; 60: 247-54.
32. Villet S, Pichoud C, Billioud G, et al. Impact of hepatitis B virus rtA181V/T mutants on hepatitis B treatment failure. J Hepatol 2008; 48: 747-55.
33. Levine S, Hernandez D, Yamanaka G, et al. Efficacies of entecavir against lamivudine-resistant hepatitis B virus replication and recombinant polymerases in vitro. Antimicrob Agents Chemother 2002; 46: 2525-32.
34. Colonno RJ, Rose R, Baldick CJ, et al. Entecavir resistance is rare in nucleoside naive patients with hepatitis B. Hepatology 2006; 44: 1656-65.
35. Tenney DJ, Rose RE, Baldick CJ, et al. Long-term monitoring shows hepatitis B virus resistance to entecavir in nucleoside-naive patients is rare through 5 years of therapy. Hepatology 2009; 49: 1503-14.
36. Villet S, Ollivet A, Pichoud C, et al. Stepwise process for the development of entecavir resistance in a chronic hepatitis B virus infected patient. J Hepatol 2007; 46: 531-8.
37. Yim HJ, Hussain M, Liu Y, et al. Evolution of multi-drug resistant hepatitis B virus during sequential therapy. Hepatology 2006; 44: 703-12.
38. Liu Y, Wang C, Zhong Y, et al. Evolution and suppression of HBV strains with multidrug resistance to lamivudine, adefovir dipivoxil and entecavir in a patient with chronic hepatitis B. Antivir Ther 2010; 15: 1185-90.
39. Villet S, Pichoud C, Villeneuve JP, Trepo C, Zoulim F. Selection of a multiple drug-resistant hepatitis B virus strain in a liver-transplanted patient. Gastroenterology 2006; 131: 1253-61.
40. Brunelle MN, Jacquard AC, Pichoud C, et al., et al. Susceptibility to antivirals of a human HBV strain with mutations conferring resistance to both lamivudine and adefovir. Hepatology 2005; 41: 1391-8.
41. Villet S, Billioud G, Pichoud C, et al., et al. In vitro characterization of viral fitness of therapy-resistant hepatitis B variants. Gastroenterology 2009; 136: 168-76 e2.
42. Warner N, Locarnini S. The antiviral drug selected hepatitis B virus rtA181T/sW172* mutant has a dominant negative secretion defect and alters the typical profile of viral rebound. Hepatology 2008; 48: 88-98.
43. Clavel F, Hance AJ. HIV drug resistance. N Engl J Med 2004; 350: 1023-35.
44. Locarnini S, Hatzakis A, Heathcote J, et al. Management of antiviral resistance in patients with chronic hepatitis B. Antivir Ther 2004; 9: 679-93.
45. Pawlotsky JM, Dusheiko G, Hatzakis A, et al. Virologic monitoring of hepatitis B virus therapy in clinical trials and practice: recommendations for a standardized approach. Gastroenterology 2008; 134: 405-15.
46. Carrouee-Durantel S, Durantel D, Werle-Lapostolle B, et al. Suboptimal response to adefovir dipivoxil therapy for chronic hepatitis B in nucleoside-naive patients is not due to pre-existing drug-resistant mutants. Antivir Ther 2008; 13: 381-8.
47. Zoulim F, Perrillo R. Hepatitis B: reflections on the current approach to antiviral therapy. J Hepatol 2008; 48(Suppl. 1): S2-19.
48. Liaw YF, Gane E, Leung N, et al. 2-Year GLOBE trial results: telbivudine Is superior to lamivudine in patients with chronic hepatitis B. Gastroenterology 2009; 136: 486-95.
49. Chang TT, Gish RG, de Man R, et al. A comparison of entecavir and lamivudine for HBeAg-positive chronic hepatitis B. N Engl J Med 2006; 354: 1001-10.
50. Lai CL, Shouval D, Lok AS, et al. Entecavir versus lamivudine for patients with HBeAg-negative chronic hepatitis B. N Engl J Med 2006; 354: 1011-20.
51. Zoutendijk R, Reijnders JG, Brown A, et al. Entecavir treatment for chronic hepatitis B: adaptation is not needed for the majority of naive patients with a partial virological response. Hepatology 2011; 54: 443-51.
52. Heathcote EJ, Marcellin P, Buti M, et al. Three-year efficacy and safety of tenofovir disoproxil fumarate treatment for chronic hepatitis B. Gastroenterology 2011; 140: 132-43.
53. Keeffe EB, Zeuzem S, Koff RS, et al. Report of an international workshop: Roadmap for management of patients receiving oral therapy for chronic hepatitis B. Clin Gastroenterol Hepatol 2007; 5: 890-7.
54. Zoulim F. Hepatitis: treatment failure in chronic hepatitis B. Nat Rev Gastroenterol Hepatol [News] 2011; 8: 366-7.
55. Pol S, Sogni P. Treatment of chronic hepatitis B: adherence and safety. Gastroenterol Clin Biol 2010; 34(Suppl. 2): S142-8.
56. Chotiyaputta W, Peterson C, Ditah FA, Goodwin D, Lok AS. Persistence and adherence to nucleos(t)ide analogue treatment for chronic hepatitis B. J Hepatol 2010; 54: 12-8.
57. Krummenacher I, Cavassini M, Bugnon O, Schneider MP. An interdisciplinary HIV-adherence program combining motivational interviewing and electronic antiretroviral drug monitoring. AIDS Care 2011; 23: 550-61.
58. Zhou T, Saputelli J, Aldrich CE, et al. Emergence of drug-resistant populations of woodchuck hepatitis virus in woodchucks treated with the antiviral nucleoside lamivudine [In Process Citation]. Antimicrob Agents Chemother 1999; 43: 1947-54.
59. Lampertico P, Vigano M, Manenti E, et al. Low resistance to adefovir combined with lamivudine: a 3-year study of 145 lamivudine-resistant hepatitis B patients. Gastroenterology 2007; 133: 1445-51.
60. Fournier C, Zoulim F. Antiviral therapy of chronic hepatitis B: prevention of drug resistance. Clin Liver Dis 2007; 11: 869-92, ix.
61. Marcellin P, Heathcote EJ, Buti M, et al. Tenofovir disoproxil fumarate versus adefovir dipivoxil for chronic hepatitis B. N Engl J Med 2008; 359: 2442-55.
62. Chan HL, Heathcote EJ, Marcellin P, et al. Treatment of hepatitis B e antigen positive chronic hepatitis with telbivudine or adefovir: a randomized trial. Ann Intern Med 2007; 147: 745-54.
63. Snow-Lampart A, Chappell B, Curtis M, et al. No resistance to tenofovir disoproxil fumarate detected after up to 144 weeks of therapy in patients monoinfected with chronic hepatitis B virus. Hepatology 2011; 53: 763-73.
64. Chang TT, Liaw YF, Wu SS, et al. Long-term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology 2010; 52: 886-93.
65. Delmas J, Schorr O, Jamard C, et al. Inhibitory effect of adefovir on viral DNA synthesis and covalently closed circular DNA formation in duck hepatitis B virus-infected hepatocytes in vivo and in vitro. Antimicrob Agents Chemother 2002; 46: 425-33.
66. Kock J, Baumert TF. Delaney WEt, Blum HE, von Weizsacker F. Inhibitory effect of adefovir and lamivudine on the initiation of hepatitis B virus infection in primary tupaia hepatocytes. Hepatology 2003; 38: 1410-8.
67. Si-Ahmed SN, Pradat P, Zoutendijk R, et al. Efficacy and tolerance of a combination of tenofovir disoproxil fumarate plus emtricitabine in patients with chronic hepatitis B: a European multicenter study. Antiviral research [Clinical Trial Multicenter Study Research Support, Non-U.S. Gov't] 2011; 92: 90-5.
68. Reijnders JG, Deterding K, Petersen J, et al. Antiviral effect of entecavir in chronic hepatitis B: influence of prior exposure to nucleos(t)ide analogues. J Hepatol 2010; 52: 493-500.
69. Petersen J, Ratziu V, Buti M, et al. Entecavir plus tenofovir combination as rescue therapy in pre-treated chronic hepatitis B patients: an international multicenter cohort study. J Hepatolo [Multicenter Study] 2012; 56: 520-6.
70. Zoulim F. Are novel combination therapies needed for chronic hepatitis B? Antiviral Res 2012; 96: 256-9.
71. Zoulim F, Locarnini S. Management of treatment failure in chronic hepatitis B. J Hepatol [Review] 2012; 56(Suppl. 1): S112-22.