Review article: Success and failure of nucleoside and nucleotide analogues in chronic hepatitis B

Alimentary Pharmacology and Therapeutics

Volumn 26, Issue SUPPL. 2, 2007, Pages 171-182

  Leemans, W F ^a   Ter Borg, M J ^a   De Man, R A ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADEFOVIR; ADEFOVIR DIPIVOXIL; ENTECAVIR; HEPATITIS B(E) ANTIGEN; LAMIVUDINE; NUCLEOSIDE; NUCLEOTIDE DERIVATIVE; TENOFOVIR DISOPROXIL;

CONFERENCE PAPER; CROSS RESISTANCE; DRUG EFFICACY; DRUG SAFETY; DRUG WITHDRAWAL; HEPATITIS B; HEPATITIS B VIRUS; HOST; HUMAN; PRIORITY JOURNAL; RELAPSE; RISK FACTOR; TREATMENT FAILURE; TREATMENT OUTCOME; VIRUS MUTATION; VIRUS REACTIVATION; VIRUS RESISTANCE;

ADENINE; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; GUANINE; HEPATITIS B, CHRONIC; HUMANS; LAMIVUDINE; NUCLEOSIDES; NUCLEOTIDES; PHOSPHONIC ACIDS; REVERSE TRANSCRIPTASE INHIBITORS; RISK FACTORS; VIRUS REPLICATION;

EID: 36849024400     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/j.1365-2036.2007.03481.x     Document Type: Conference Paper

References (96)

1. Lok AS. Chronic hepatitis B. N Engl J Med 2002 346 : 1682 3.
2. Mahoney FJ. Update on diagnosis, management, and prevention of hepatitis B virus infection. Clin Microbiol Rev 1999 12 : 351 66.
3. Lee WM. Hepatitis B virus infection. N Engl J Med 1997 337 : 1733 45.
4. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001 94 : 153 6.
5. Chen CJ, Yang HI, Su J, et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 2006 295 : 65 73.
6. Iloeje UH, Yang HI, Su J, Jen CL, You SL, Chen CJ. Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology 2006 130 : 678 86.
7. de Franchis R, Hadengue A, Lau G, et al. EASL International Consensus Conference on Hepatitis B. 13-14 September, 2002 Geneva, Switzerland. Consensus statement (long version). J Hepatol 2003 39 (Suppl. 1 S3 25.
8. Janssen HL, van Zonneveld M, Senturk H, et al. Pegylated interferon alfa-2b alone or in combination with lamivudine for HBeAg-positive chronic hepatitis B: a randomised trial. Lancet 2005 365 : 123 9.
9. Lau GK, Piratvisuth T, Luo KX, et al. Peginterferon alfa-2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N Engl J Med 2005 352 : 2682 95.
10. Marcellin P, Lau GK, Bonino F, et al. Peginterferon alfa-2a alone, lamivudine alone, and the two in combination in patients with HBeAg-negative chronic hepatitis B. N Engl J Med 2004 351 : 1206 17.
11. Thomas H, Foster G, Platis D. Mechanisms of action of interferon and nucleoside analogues. J Hepatol 2003 39 (Suppl. 1 S93 8.
12. Nowak MA, Bonhoeffer S, Hill AM, Boehme R, Thomas HC, McDade H. Viral dynamics in hepatitis B virus infection. Proc Natl Acad Sci U S A 1996 93 : 4398 402.
13. Locarnini S. Molecular virology of hepatitis B virus. Semin Liver Dis 2004 24 (Suppl. 1 3 10.
14. Doong SL, Tsai CH, Schinazi RF, Liotta DC, Cheng YC. Inhibition of the replication of hepatitis B virus in vitro by 2',3'-dideoxy-3'-thiacytidine and related analogues. Proc Natl Acad Sci U S A 1991 88 : 8495 9.
15. Dienstag JL, Schiff ER, Wright TL, et al. Lamivudine as initial treatment for chronic hepatitis B in the United States. N Engl J Med 1999 341 : 1256 63.
16. Lai CL, Chien RN, Leung NW, et al. A one-year trial of lamivudine for chronic hepatitis B. Asia Hepatitis Lamivudine Study Group. N Engl J Med 1998 339 : 61 8.
17. 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.
18. 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.
19. Chang TT, Lai CL, Chien RN, et al. Four years of lamivudine treatment in Chinese patients with chronic hepatitis B. J Gastroenterol Hepatol 2004 19 : 1276 82.
20. Schalm SW, Heathcote J, Cianciara J, et al. Lamivudine and alpha interferon combination treatment of patients with chronic hepatitis B infection: a randomised trial. Gut 2000 46 : 562 8.
21. Liaw YF, Leung NW, Chang TT, et al. Effects of extended lamivudine therapy in Asian patients with chronic hepatitis B. Asia Hepatitis Lamivudine Study Group. Gastroenterology 2000 119 : 172 80.
22. Leung NW, Lai CL, Chang TT, et al. Extended lamivudine treatment in patients with chronic hepatitis B enhances hepatitis B e antigen seroconversion rates: results after 3 years of therapy. Hepatology 2001 33 : 1527 32.
23. Guan R, Lai CL, Liaw YF, Lim SG, Lee CM. Efficacy and safety of 5 years lamivudine treatment of Chinese patients with chronic hepatitis B. J Gastroenterol Hepatol 2001 16 (Suppl. 1 A60 1.
24. Dienstag JL, Cianciara J, Karayalcin S, et al. Durability of serologic response after lamivudine treatment of chronic hepatitis B. Hepatology 2003 37 : 748 55.
25. Song BC, Suh DJ, Lee HC, Chung YH, Lee YS. Hepatitis B e antigen seroconversion after lamivudine therapy is not durable in patients with chronic hepatitis B in Korea. Hepatology 2000 32 (4 Pt 1 803 6.
26. Ryu SH, Chung YH, Choi MH, et al. Long-term additional lamivudine therapy enhances durability of lamivudine-induced HBeAg loss: a prospective study. J Hepatol 2003 39 : 614 9.
27. Lee HC, Suh DJ, Ryu SH, et al. Quantitative polymerase chain reaction assay for serum hepatitis B virus DNA as a predictive factor for post-treatment relapse after lamivudine induced hepatitis B e antigen loss or seroconversion. Gut 2003 52 : 1779 83.
28. Liaw YF, Chien RN, Yeh CT. No benefit to continue lamivudine therapy after emergence of YMDD mutations. Antivir Ther 2004 9 : 257 62.
29. 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.
30. Dienstag JL, Goldin RD, Heathcote EJ, et al. Histological outcome during long-term lamivudine therapy. Gastroenterology 2003 124 : 105 17.
31. 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 : 567 72.
32. 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.
33. de Man RA, Bartholomeusz AI, Niesters HG, Zondervan PE, Locarnini SA. The sequential occurrence of viral mutations in a liver transplant recipient re-infected with hepatitis B: hepatitis B immune globulin escape, famciclovir non-response, followed by lamivudine resistance resulting in graft loss. J Hepatol 1998 29 : 669 75.
34. Hadziyannis SJ, Papatheodoridis GV, Dimou E, Laras A, Papaioannou C. Efficacy of long-term lamivudine monotherapy in patients with hepatitis B e antigen-negative chronic hepatitis B. Hepatology 2000 32 (4 Pt 1 847 51.
35. Gaia S, Marzano A, Smedile A, et al. Four years of treatment with lamivudine: clinical and virological evaluations in HBe antigen-negative chronic hepatitis B. Aliment Pharmacol Ther 2004 20 : 281 7.
36. Scotto G, Fazio V, Campanozzi F, D'Adduzio A. Efficacy of treatment with lamivudine in patients with chronic active E-minus variant hepatitis B virus infection: a non-randomized, open label study. Curr Ther Res 2000 61 : 321 30.
37. Rizzetto M. Efficacy of lamivudine in HBeAg-negative chronic hepatitis B. J Med Virol 2002 66 : 435 51.
38. Shouval D, Lai CL, Cheinquer H, et al. Entacavir demonstrates superior histologic and virologic efficacy over lamivudine in nucleoside-naïve HBeAg(-) chronic hepatitis B: results of phase III trial ETV-027. Hepatology 2004 40 (4 Suppl. 1 728A.
39. Simsek H, Schiff E, Goodman Z, Brett-Smith H, Klesczewski K, Kreter B. Effects of entecavir and lamivudine on advanced liver fibrosis after 48 weeks of treatment in patients with CHB infection: results of three pivotal trials. J Hepatol 2006 44 (Suppl. 2 S191.
40. Buti M, Cotrina M, Jardi R, et al. Two years of lamivudine therapy in anti-HBe-positive patients with chronic hepatitis B. J Viral Hepat 2001 8 : 270 5.
41. Tassopoulos NC, Anagnostopoulos GD. Long-term lamivudine treatment of patients with pre-core mutant profile (HBEAg(-)/Anti-HBe+) chronic hepatitis B. Antivir Ther 2000 5 (Suppl. 1 34.
42. Dimou E, Papatheodoridis GV, Laras A, Hadziyannis SJ Efficacy of long-term lamivudine monotherapy in HBeAg negative chronic hepatitis B. 2000 5 (Suppl. 1 44.
43. Santantonio T, Mazzola M, Iacovazzi T, Miglietta A, Guastadisegni A, Pastore G. Long-term follow-up of patients with anti-HBe/HBV DNA-positive chronic hepatitis B treated for 12 months with lamivudine. J Hepatol 2000 32 : 300 6.
44. Tassopoulos NC, Volpes R, Pastore G, et al. Efficacy of lamivudine in patients with hepatitis B e antigen-negative/hepatitis B virus DNA-positive (precore mutant) chronic hepatitis B. Lamivudine Precore Mutant Study Group. Hepatology 1999 29 : 889 96.
45. Rizzetto M, Tassopoulos NC, Goldin RD, et al. Extended lamivudine treatment in patients with HBeAg-negative chronic hepatitis B. J Hepatol 2005 42 : 173 9.
46. Fung SK, Wong F, Hussain M, Lok AS. Sustained response after a 2-year course of lamivudine treatment of hepatitis B e antigen-negative chronic hepatitis B. J Viral Hepat 2004 11 : 432 8.
47. Marcellin P, Chang TT, Lim SG, et al. Adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. N Engl J Med 2003 348 : 808 16.
48. Izzedine H, Hulot JS, Launay-Vacher V, et al. Renal safety of adefovir dipivoxil in patients with chronic hepatitis B: two double-blind, randomized, placebo-controlled studies. Kidney Int 2004 66 : 1153 8.
49. 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.
50. Mao YM, Zheng MD, Yao GB, et al. Efficacy and safety of two years therapy with adefovir dipixoxil (ADV) in Chinese subjects with HBeAg positive chronic hepatitis B (CHB). J. Hepatology 2006 44 (Suppl. 2 S185.
51. Durantel S, Werle B, Durantel D, et al. Different profiles of response to adefovir dipivoxil and factors that may influence response in patients with chronic hepatitis B. Hepatology 2004 40 (4 Suppl. 1 654A.
52. Marcellini P, Chang TT, Lim SG, et al. Increasing serologic, virologic and biochemical response over time to adefovir dipivoxil (ADV) 10 mg in HBeAg+ chronic hepatitis B (CHB) patients. J Hepatol 2005 42 (Suppl. 2 31 2.
53. Chang TT, Schiffman ML, Tong M, et al. Durability of HBeAg seroconversion following adefovir dipivoxil treatment for chronic hepatitis B. J Hepatol 2006 44 (Suppl. 2 S187.
54. Ratziu V, Thibault V, Benhamou Y, Poynard T. Successful rescue therapy with tenofovir in a patient with hepatic decompensation and adefovir resistant HBV mutant. Comp Hepatol 2006 5 : 1.
55. Yeon JE, Yoo W, Hong SP, et al. Resistance to adefovir dipivoxil (ADV) in lamivudine-resistant chronic hepatitis B patients treated with ADV. Gut 2006 55 : 1488 95.
56. 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.
57. Hadziyannis SJ, Tassopoulos NC, Heathcote EJ, et al. Adefovir dipivoxil for the treatment of hepatitis B e antigen-negative chronic hepatitis B. N Engl J Med 2003 348 : 800 7.
58. Hadziyannis SJ, Tassopoulos NC, Chang TT, et al. Two state modeling of virological and biochemical efficacy plus liver biopsies demonstrate efficacy of adefovir dipivoxil in HBeAg-negative chronic hepatitis B over 4 or 5 years. J. Hepatology 2006 44 (Suppl. 2 S184.
59. Hadziyannis SJ, Tassopoulos NC, Chang TT, et al. Long-term adefovir dipivoxil treatment induces regression of liver fibrosis in patients with HBeAg-negative chronic hepatitis B: results after 5 years of therapy. Hepatology 2005 42 (4 Suppl. ) 754A.
60. Gish RG, Chang TT, de Man RA, et al. Entecavir results in substantial virologic and biochemical improvement and HBeAg seroconversion through 96 weeks of treatment in HBeAg(+) chronic hepatitis B patients (study ETV-022). Hepatology 2005 42 (4 Suppl. 1 267A.
61. Colonno RJ, Rose RE, Baldick CJ, Levine SM, Klesczewski K, Tenney DJ. High barrier to resistance results in no emergence of entecavir resistance in nucleoside-naïve subjects during the first two years of therapy. J Hepatol 2006 44 (Suppl. 2 S182.
62. Huang ZM, Huang QW, Qin YQ, et al. YMDD mutations in patients with chronic hepatitis B untreated with antiviral medicines. World J Gastroenterol 2005 11 : 867 70.
63. Schildgen O, Sirma H, Funk A, et al. Primary resistance of a novel hepatitis B virus variant to adefovir. J Hepatol 2006 44 (Suppl. 2 S190.
64. Chien RN, Liaw YF, Atkins M. Pretherapy alanine transaminase level as a determinant for hepatitis B e antigen seroconversion during lamivudine therapy in patients with chronic hepatitis B. Asian Hepatitis Lamivudine Trial Group. Hepatology 1999 30 : 770 4.
65. Perrillo RP, Lai CL, Liaw YF, et al. Predictors of HBeAg loss after lamivudine treatment for chronic hepatitis B. Hepatology 2002 36 : 186 94.
66. Villeneuve J, Willems B, Zoulim F. Efficacy of tenofovir in patients with chronic hepatitis B and resistance or sub-optimal response to adefovir. Hepatology 2005 42 (4 Suppl. 1 588A.
67. Delaney WE 4th., Yang H, Miller MD, Gibbs CS, Xiong S. Combinations of adefovir with nucleoside analogs produce additive antiviral effects against hepatitis B virus in vitro. Antimicrob Agents Chemother 2004 48 : 3702 10.
68. Ide T, Kumashiro R, Koga Y, et al. A real-time quantitative polymerase chain reaction method for hepatitis B virus in patients with chronic hepatitis B treated with lamivudine. Am J Gastroenterol 2003 98 : 2048 51.
69. Yuen MF, Sablon E, Hui CK, Yuan HJ, Decraemer H, Lai CL. Factors associated with hepatitis B virus DNA breakthrough in patients receiving prolonged lamivudine therapy. Hepatology 2001 34 (4 Pt 1 785 91.
70. Fung SK, Chae HB, Fontana RJ, et al. Virologic response and resistance to adefovir in patients with chronic hepatitis B. J Hepatol 2006 44 : 283 90.
71. Lee CH, Yeon JE, Pyo S, et al. More frequent and earlier emergence of adefovir (ADV) resistance mutations in lamivudine resistant patients treated with ADV compared to previously reported nucleoside-treatment naïve patients. Hepatology 2005 42 (Suppl. 1 593A.
72. Locarnini S, Qi X, Arterburn S, et al. Incidence and predictors of emergence of adefovir resistant HBV during four years of adefovir dipivoxil (ADV) therapy for patients with chronic hepatitis B (CHB). J Hepatol 2005 42 (Suppl. 2 17.
73. Colonno R, Rose R, Levine S, et al. Entecavir two year resistance update: no resistance observed in nucleotide naïve patients and low frequency resistance emergence in lamivudine refractory patients. Hepatology 2005 42 (Suppl. 1 573A.
74. Locarnini S, Hatzakis A, Heathcote J, et al. Management of antiviral resistance in patients with chronic hepatitis B. Antivir Ther 2004 9 : 679 93.
75. Lok AS, McMahon BJ. Chronic hepatitis B. Hepatology 2001 34 : 1225 41.
76. Lok AS, McMahon BJ. AASLD Practice Guidelines Chronic hepatitis B: update of therapeutic guidelines. Rom J Gastroenterol 2004 13 : 150 4.
77. Papatheodoridis GV, Dimou E, Laras A, Papadimitropoulos V, Hadziyannis SJ. Course of virologic breakthroughs under long-term lamivudine in HBeAg-negative precore mutant HBV liver disease. Hepatology 2002 36 : 219 26.
78. Hussain M, Fung S, Libbrecht E, et al. Sensitive line probe assay that simultaneously detects mutations conveying resistance to lamivudine and adefovir. J Clin Microbiol 2006 44 : 1094 7.
79. Sertoz RY, Erensoy S, Pas S, et al. Comparison of sequence analysis and INNO-LiPA HBV DR line probe assay in patients with chronic hepatitis B. J Chemother 2005 17 : 514 20.
80. Peters MG, Hann Hw H, Martin P, et al. Adefovir dipivoxil alone or in combination with lamivudine in patients with lamivudine-resistant chronic hepatitis B. Gastroenterology 2004 126 : 91 101.
81. Perrillo R, Hann HW, Mutimer D, et al. Adefovir dipivoxil added to ongoing lamivudine in chronic hepatitis B with YMDD mutant hepatitis B virus. Gastroenterology 2004 126 : 81 90.
82. Lampertico P, Vigano M, Manenti E, Iavarone M, Lunghi G, Colombo M. Adefovir rapidly suppresses hepatitis B in HBeAg-negative patients developing genotypic resistance to lamivudine. Hepatology 2005 42 : 1414 9.
83. Vassiliadis T, Nikolaidis N, Giouleme O, et al. Adefovir dipivoxil added to ongoing lamivudine therapy in patients with lamivudine-resistant hepatitis B e antigen-negative chronic hepatitis B. Aliment Pharmacol Ther 2005 21 : 531 7.
84. Lee Y, Suh DJ, Lim YS, et al. Emergence of rtA181V/T and rtN236T mutations after 48 weeks of adefovir dipivoxil therapy in patients with lamivudine-resistant chronic hepatitis B. Hepatology 2005 42 (Suppl. 1 578A.
85. Snow A, Thibault V, Qi X, Zhu Y, Westland C, Arterburn S. Combination of adefovir (ADV) and lamivudine (LAM) prevented emergence of adefovir resistance mutations in chronic hepatitis B patients with lamivudine-resistant HBV. Gastroenterology 2005 128 : M945.
86. Sherman M, Yurdaydin C, Sollano J, et al. Entecavir is superior to continued lamivudine for the treatment of lamivudine-refractory, HBeAg(+) chronic hepatitis B: results of phase III study ETV-026. Hepatology 2004 40 (4 Suppl. 1 664A.
87. Yurdaydin C, Sollano J, Hadziyannis SJ, et al. Entecavir results in continued virologic and biochemical improvement and HBeAg seroconversion through 96 weeks of treatment in lamivudine-refractory, HBeAg(+) chronic hepatitis B patients (ETV-026). J Hepatol 2006 44 (Suppl. 2 S36.
88. 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.
89. Yang H, Qi X, Sabogal A, Miller M, Xiong S, Delaney WE 4th. Cross-resistance testing of next-generation nucleoside and nucleotide analogues against lamivudine-resistant HBV. Antivir Ther 2005 10 : 625 33.
90. van Bommel F, Wunsche T, Mauss S, et al. Comparison of adefovir and tenofovir in the treatment of lamivudine-resistant hepatitis B virus infection. Hepatology 2004 40 : 1421 5.
91. van Bömmel F, Mauss S, Zollner B, et al. Long-term effect of tenofovir in the treatment of lamivudine-resistant hepatitis B virus infections in comparison to adefovir. Hepatology 2005 42 (4 Suppl. 1 269A.
92. Brunelle MN, Jacquard AC, Pichoud C, et al. Susceptibility to antivirals of a human HBV strain with mutations conferring resistance to both lamivudine and adefovir. Hepatology 2005 41 : 1391 8.
93. 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.
94. Zoulim F. Combination of nucleoside analogues in the treatment of chronic hepatitis B virus infection: lesson from experimental models. J Antimicrob Chemother 2005 55 : 608 11.
95. Villet V, Pichoud C, Ollivet A, Villeneuve J, Trepo C, Zoulim F. Sequential antiviral therapy leads to the emergence of multiple drug resistant hepatitis B virus. Hepatology 2005 42 (Suppl. 1 581A.
96. Lampertico P, Marzano A, Levrero M, et al. A multicenter Italian study of rescue adefovir dipivoxil therapy in lamivudine resistant patients: a 2-year analysis of 604 patients. Hepatology 2005 42 (4 Suppl. 1 591A.