Considerations for the long-term treatment of chronic hepatitis B with nucleos(t)ide analogs

Expert Review of Gastroenterology and Hepatology

Volumn 6, Issue 6, 2012, Pages 683-694

  Petersen, Jörg ^a   Buti, Maria ^b  

^a DEPARTMENT OF CARDIOLOGY   (Germany)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

chronic hepatitis B; entecavir; long term treatment; nucleos(t)ide analogs; real life data; tenofovir

Indexed keywords

ADEFOVIR; EMTRICITABINE; ENTECAVIR; LAMIVUDINE; NUCLEOSIDE ANALOG; RNA DIRECTED DNA POLYMERASE INHIBITOR; TELBIVUDINE; TENOFOVIR; VIRUS DNA; ZIDOVUDINE;

ANTIVIRAL ACTIVITY; ANTIVIRAL THERAPY; DISEASE SEVERITY; DRUG EFFICACY; DRUG POTENCY; DRUG SAFETY; DRUG TOLERABILITY; HEPATITIS B; HEPATITIS C; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFECTION RISK; LONG TERM CARE; MIXED INFECTION; MONOTHERAPY; NEPHROTOXICITY; NONHUMAN; PRACTICE GUIDELINE; RELAPSE; REVIEW; SEROCONVERSION; VIRAL CLEARANCE; VIRUS LOAD; VIRUS REACTIVATION; VIRUS RESISTANCE;

ADENINE; AGE FACTORS; ANTIVIRAL AGENTS; COMORBIDITY; DNA, VIRAL; DRUG RESISTANCE, VIRAL; GUANINE; HEPATITIS B, CHRONIC; HUMANS; LAMIVUDINE; LIFE STYLE; ORGANOPHOSPHONATES; SEVERITY OF ILLNESS INDEX; THYMIDINE; TIME FACTORS;

EID: 84871027805     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/egh.12.52     Document Type: Review

References (86)

1. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of chronic hepatitis B virus infection. J. Hepatol. 57(1), 167-185 (2012).
2. Liaw YF, Kao JH, Piratvisuth T et al. Asian-Pacific consensus statement on the management of chronic hepatitis B: a 2005 update. Hepatol. Int. 25(3), 472-489 (2005). (Pubitemid 40861895)
3. Lok AS, McMahon BJ. Chronic hepatitis B: update 2009. Hepatology 50(3), 661-662 (2009).
4. Keeffe EB, Dieterich DT, Han SH et al. A treatment algorithm for the management of chronic hepatitis B virus infection in the United States: 2008 update. Clin. Gastroenterol. Hepatol. 6(12), 1315-41; quiz 1286 (2008).
5. Tong MJ, Pan CQ, Hann HW et al. The management of chronic hepatitis B in Asian Americans. Dig. Dis. Sci. 56(11), 3143-3162 (2011).
6. Dienstag JL, Schiff ER, Wright TL et al. Lamivudine as initial treatment for chronic hepatitis B in the United States. N. Engl. J. Med. 341(17), 1256-1263 (1999). (Pubitemid 29489740)
7. Chang TT, Gish RG, de Man R et al.; BEHoLD AI463022 Study Group. A comparison of entecavir and lamivudine for HBeAg-positive chronic hepatitis B. N. Engl. J. Med. 354(10), 1001-1010 (2006). (Pubitemid 43357804)
8. Hadziyannis SJ, Tassopoulos NC, Heathcote EJ et al.; Adefovir Dipivoxil 438 Study Group. Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B. N. Engl. J. Med. 352(26), 2673-2681 (2005). (Pubitemid 41007822)
9. Shouval D, Lai CL, Chang TT et al. Relapse of hepatitis B in HBeAg-negative chronic hepatitis B patients who discontinued successful entecavir treatment: the case for continuous antiviral therapy. J. Hepatol. 50(2), 289-295 (2009).
10. Reijnders JG, Perquin MJ, Zhang N, Hansen BE, Janssen HL. Nucleos(t)ide analogues only induce temporary hepatitis B e antigen seroconversion in most patients with chronic hepatitis B. Gastroenterology 139(2), 491-498 (2010).
11. Chen CJ, Yang HI. Natural history of chronic hepatitis B REVEALed. J. Gastroenterol. Hepatol. 26(4), 628-638 (2011).
12. Yuen MF, Seto WK, Fung J, Wong DK, Yuen JC, Lai CL. Three years of continuous entecavir therapy in treatmentnaive chronic hepatitis B patients: VIRAL suppression, viral resistance, and clinical safety. Am. J. Gastroenterol. 106(7), 1264-1271 (2011).
13. Chae HB, Hann HW. Baseline HBV DNA level is the most important factor associated with virologic breakthrough in chronic hepatitis B treated with lamivudine. World J. Gastroenterol. 13(30), 4085-4090 (2007).
14. 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 34(4 Pt 1), 785-791 (2001). (Pubitemid 32928004)
15. Marcellin P, Heathcote EJ, Corsa A et al. No detectable resistance to tenofovir disoproxil fumarate (TDF) following up to 240 weeks of treatment in patients with HBeAg+ and HBeAg- chronic hepatitis B virus infection. Hepatology 54(4), Abstract 238 (2011).
16. Tenney DJ, Pokornoski KA, Rose RE et al. Entecavir maintains a high genetic barrier to HBV resistance through 6 years in naive patients. J. Hepatol. 50 (Suppl. 1), S10 (2009).
17. Flink HJ, van Zonneveld M, Hansen BE, de Man RA, Schalm SW, Janssen HL; HBV 99-01 Study Group. Treatment with Peg-interferon alpha-2b for HBeAg-positive chronic hepatitis B: HBsAg loss is associated with HBV genotype. Am. J. Gastroenterol. 101(2), 297-303 (2006). (Pubitemid 43381671)
18. Wiegand J, Hasenclever D, Tillmann HL. Should treatment of hepatitis B depend on hepatitis B virus genotypes? A hypothesis generated from an explorative analysis of published evidence. Antivir. Ther. 13(2), 211-220 (2008). (Pubitemid 351535372)
19. Gish RG, Chang TT, Lai CL et al. Loss of HBsAg antigen during treatment with entecavir or lamivudine in nucleoside-naive HBeAg-positive patients with chronic hepatitis B. J. Viral Hepat. 17(1), 16-22 (2010).
20. Lin CL, Kao JH. The clinical implications of hepatitis B virus genotype: recent advances. J. Gastroenterol. Hepatol. 26(Suppl. 1), 123-130 (2011).
21. Chan HL, Hui AY, Wong ML et al. Genotype C hepatitis B virus infection is associated with an increased risk of hepatocellular carcinoma. Gut 53(10), 1494-1498 (2004). (Pubitemid 39265273)
22. Kramvis A, Kew MC. Molecular characterization of subgenotype A1 (subgroup Aa) of hepatitis B virus. Hepatol. Res. 37(Suppl. 1), S37-S32 (2007).
23. Hou J, Xu D, Shi G et al. Five-year telbivudine treatment with effective viral suppression results in resolution of liver inflammation and fibrosis regression in patients with chonic hepatitis B. J. Hepatol. 54, S287 (2011).
24. 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 52(3), 886-893 (2010).
25. Liaw YF, Raptopoulou-Gigi M, Cheinquer H et al. Efficacy and safety of entecavir versus adefovir in chronic hepatitis B patients with hepatic decompensation: a randomized, open-label study. Hepatology 54(1), 91-100 (2011).
26. Liaw YF, Sheen IS, Lee CM et al. Tenofovir disoproxil fumarate (TDF), emtricitabine/ TDF, and entecavir in patients with decompensated chronic hepatitis B liver disease. Hepatology 53(1), 62-72 (2011).
27. Zoutendijk R, Reijnders JG, Zoulim F et al. Virologic response to entecavir is associated with a lower probability of disease progression in chronic hepatitis B. Gut doi:10.1136/gutjnl-2012-302024 (2011) (Epub ahead of print).
28. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27(5), 1047-1053 (2004). (Pubitemid 38579764)
29. Li-Ng M, Tropp S, Danoff A, Bini EJ. Association between chronic hepatitis B virus infection and diabetes among Asian Americans and Pacific Islanders. Dig. Liver Dis. 39(6), 549-556 (2007). (Pubitemid 46746648)
30. Gomez P, Ruilope LM, Barrios V et al.; FATH Study Group. Prevalence of renal insufficiency in individuals with hypertension and obesity/overweight: the FATH study. J. Am. Soc. Nephrol. 17(12 Suppl. 3), S194-S200 (2006). (Pubitemid 44865248)
31. Deterding K, Lampe N, Reijnders JG et al. Prevalence and severity of kidney dysfunction in patients with chronic hepatitis B in Europe: data from the European VIRGIL cohort. J. Hepatol. 54(Suppl. 1), S147 (2011).
32. Diamond T, Stiel D, Lunzer M, Wilkinson M, Roche J, Posen S. Osteoporosis and skeletal fractures in chronic liver disease. Gut 31(1), 82-87 (1990). (Pubitemid 20037985)
33. Chung NS, Kwon OS, Park CH et al. [A comparative cross-sectional study of the development of hepatocellular carcinoma in patients with liver cirrhosis caused by hepatitis B virus, alcohol, or combination of hepatitis b virus and alcohol]. Korean J. Gastroenterol. 49(6), 369-375 (2007).
34. Mallat A, Lotersztajn S. Cigarette smoke exposure: a novel cofactor of NAFLD progression? J. Hepatol. 51(3), 430-432 (2009).
35. Wang CS, Yao WJ, Chang TT, Wang ST, Chou P. The impact of type 2 diabetes on the development of hepatocellular carcinoma in different viral hepatitis statuses. Cancer Epidemiol. Biomarkers Prev. 18(7), 2054-2060 (2009).
36. Loomba R, Rowley A, Wesley R et al. Systematic review: the effect of preventive lamivudine on hepatitis B reactivation during chemotherapy. Ann. Intern. Med. 148(7), 519-528 (2008). (Pubitemid 351665421)
37. Ahn HJ, Kim MS, Kim YS et al. Clinical outcome of renal transplantation in patients with positive pre-transplant hepatitis B surface antigen. J. Med. Virol. 79(11), 1655-1663 (2007).
38. Xi ZF, Xia Q, Zhang JJ et al. The role of entecavir in preventing hepatitis B recurrence after liver transplantation. J. Dig. Dis. 10(4), 321-327 (2009).
39. Fung J, Cheung C, Chan SC et al. Entecavir monotherapy is effective in suppressing hepatitis B virus after liver transplantation. Gastroenterology 141(4), 1212-1219 (2011).
40. Jiménez-Pérez M, Sáez-Gómez AB, Mongil Poce L, Lozano-Rey JM, de la Cruz- Lombardo J, Rodrigo-López JM. Efficacy and safety of entecavir and/or tenofovir for prophylaxis and treatment of hepatitis B recurrence post-liver transplant. Transplant. Proc. 42(8), 3167-3168 (2010).
41. Kamar N, Milioto O, Alric L et al. Entecavir therapy for adefovir-resistant hepatitis B virus infection in kidney and liver allograft recipients. Transplantation 86(4), 611-614 (2008).
42. Yim HJ, Lok AS. Natural history of chronic hepatitis B virus infection: what we knew in 1981 and what we know in 2005. Hepatology 43(2 Suppl. 1), S173-S181 (2006).
43. Lin PF, Nowicka-Sans B, Terry B et al. Entecavir exhibits inhibitory activity against human immunodeficiency virus under conditions of reduced viral challenge. Antimicrob. Agents Chemother. 52(5), 1759-1767 (2008). (Pubitemid 351614670)
44. Duarte-Rojo A, Heathcote EJ. Efficacy and safety of tenofovir disoproxil fumarate in patients with chronic hepatitis B. Therap. Adv. Gastroenterol. 3(2), 107-119 (2010).
45. Woo G, Tomlinson G, Nishikawa Y et al. Tenofovir and entecavir are the most effective antiviral agents for chronic hepatitis B: a systematic review and Bayesian meta-analyses. Gastroenterology 139(4), 1218-1229 (2010).
46. Lai CL, Shouval D, Lok AS et al.; BEHoLD AI463027 Study Group. Entecavir versus lamivudine for patients with HBeAg-negative chronic hepatitis B. N. Engl. J. Med. 354(10), 1011-1020 (2006). (Pubitemid 43357805)
47. Leung N, Peng CY, Hann HW et al. Early hepatitis B virus DNA reduction in hepatitis B e antigen-positive patients with chronic hepatitis B: a randomized international study of entecavir versus adefovir. Hepatology 49(1), 72-79 (2009).
48. Chang TT, Lai CL, Kew Yoon S et al. Entecavir treatment for up to 5 years in patients with hepatitis B e antigen-positive chronic hepatitis B. Hepatology 51(2), 422-430 (2010).
49. Lampertico P, Vigano M, Soffredini R et al. Entecavir monotherapy for nuc-naive chronic hepatitis B patients from field practice: high efficacy and favorable safety profile over 3 years. Hepatology 54 (Suppl. 1), Abstract 1436 (2011).
50. Seto WK, Lai CL, Fung J, Yuen JC, Wong DK, Yuen MF. Outcome of 4-year treatment of entecavir for treatment-naive chronic hepatitis B. J. Hepatol. 54, S301 (2011).
51. Yokosuka O, Takaguchi K, Fujioka S et al. Long-term use of entecavir in nucleosidenaive Japanese patients with chronic hepatitis B infection. J. Hepatol. 52(6), 791-799 (2010).
52. Marcellin P, Heathcote EJ, Buti M et al. Tenofovir disoproxil fumarate versus adefovir dipivoxil for chronic hepatitis B. N. Engl. J. Med. 359(23), 2442-2455 (2008).
53. Marcellin P, Buti M, Gane EJ et al. Five years of treatment with tenofovir DF (TDF) for chronic hepatitis B (Chb) infection is associated with sustained viral suppression and significant regression of histological fibrosis and cirrhosis. Hepatology 54 (Suppl. 1), Abstract 1375 (2011).
54. Lampertico P, Soffredini R, Viganò M et al. 2-year effectiveness and safety of tenofovir in 302 NUC-naive patients with chronic hepatitis B: a multicenter European study in clinical practice. Hepatology 54 (Suppl.), 1041A (2011).
55. Zoulim F, Locarnini S. Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 137(5), 1593-608.e1 (2009).
56. Yuen MF, Seto WK, Chow DH et al. Long-term lamivudine therapy reduces the risk of long-term complications of chronic hepatitis B infection even in patients without advanced disease. Antivir. Ther. 12(8), 1295-1303 (2007).
57. Lai CL, Gane E, Liaw YF et al.; Globe Study Group. Telbivudine versus lamivudine in patients with chronic hepatitis B. N. Engl. J. Med. 357(25), 2576-2588 (2007). (Pubitemid 350294224)
58. Liaw YF, Gane E, Leung N et al.; GLOBE Study Group. 2-Year GLOBE trial results: telbivudine Is superior to lamivudine in patients with chronic hepatitis B. Gastroenterology 136(2), 486-495 (2009).
59. Marcellin P, Chang TT, Lim SG et al. Long-term efficacy and safety of adefovir dipivoxil for the treatment of hepatitis B antigen-positive chronic hepatitis B. Hepatology 48(3), 750-758 (2008).
60. Hadziyannis SJ, Tassopoulos NC, Heathcote EJ et al.; Adefovir Dipivoxil 438 Study Group. Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B for up to 5 years. Gastroenterology 131(6), 1743-1751 (2006). (Pubitemid 44958517)
61. van Bömmel F, de Man RA, Wedemeyer H et al. Long-term efficacy of tenofovir monotherapy for hepatitis B virusmonoinfected patients after failure of nucleoside/nucleotide analogues. Hepatology 51(1), 73-80 (2010).
62. Reijnders JG, Deterding K, Petersen J et al.; VIRGIL Surveillance Study Group. Antiviral effect of entecavir in chronic hepatitis B: influence of prior exposure to nucleos(t)ide analogues. J. Hepatol. 52(4), 493-500 (2010).
63. Tenney DJ, Rose RE, Baldick CJ et al. Long-term monitoring shows hepatitis B virus resistance to entecavir in nucleosidenaive patients is rare through 5 years of therapy. Hepatology 49(5), 1503-1514 (2009).
64. 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 60(2), 247-254 (2011).
65. Carey I, Harrison PM. Monotherapy versus combination therapy for the treatment of chronic hepatitis B. Expert Opin. Investig. Drugs 18(11), 1655-1666 (2009).
66. 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. Hepatol. 56(3), 520-526 (2012).
67. Elefsiniotis I, Buti M, Jardi R, Vezali E, Esteban R. Clinical outcome of lamivudine-resistant chronic hepatitis B patients with compensated cirrhosis under adefovir salvage treatment. Importance of HCC surveillance. Eur. J. Intern. Med. 20(5), 478-481 (2009).
68. Fontana RJ. Side effects of long-term oral antiviral therapy for hepatitis B. Hepatology 49(Suppl. 5), S185-S195 (2009).
69. Mazzucco CE, Hamatake RK, Colonno RJ, Tenney DJ. Entecavir for treatment of hepatitis B virus displays no in vitro mitochondrial toxicity or DNA polymerase gamma inhibition. Antimicrob. Agents Chemother. 52(2), 598-605 (2008). (Pubitemid 351170833)
70. But DY, Yuen MF, Fung J, Lai CL. Safety evaluation of telbivudine. Expert Opin. Drug Saf. 9(5), 821-829 (2010).
71. Lange CM, Bojunga J, Hofmann WP et al. Severe lactic acidosis during treatment of chronic hepatitis B with entecavir in patients with impaired liver function. Hepatology 50(6), 2001-2006 (2009).
72. Lange CM, Sprinzl K, Vermerhren J, Zeuzem S, Sarrazin C. Prospektive untersuchung von laktat-konzentrationen im blut von patienten mit chronischer hepatitis B und dekompensierter Leberzirrhose während der Therapie mit Nukleos(t)id-Analoga. Medizinische Klinik 105(Suppl. 1), PS25 (2010).
73. Manns MP, Akarca US, Chang TT et al. Long-term safety and tolerability of entecavir in patients with chronic hepatitis B in the rollover study ETV-901. Expert Opin. Drug Saf. 11(3), 361-368 (2012).
74. Mauss S, Berger F, Filmann N et al. Effect of HBV polymerase inhibitors on renal function in patients with chronic hepatitis B. J. Hepatol. 55(6), 1235-1240 (2011).
75. Hadziyannis SJ, Tassopoulos NC, Heathcote EJ et al.; Adefovir Dipivoxil 438 Study Group. Adefovir dipivoxil for the treatment of hepatitis B e antigen-negative chronic hepatitis B. N. Engl. J. Med. 348(9), 800-807 (2003). (Pubitemid 36245756)
76. Marcellin P, Chang TT, Lim SG et al.; Adefovir Dipivoxil 437 Study Group. Adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. N. Engl. J. Med. 348(9), 808-816 (2003). (Pubitemid 36245757)
77. Lampertico P, Vigano M, Yurdaydin C et al. Effectiveness and safety of tenofovir disproxil fumarate in field practice: a multicentre European cohort study of 737 patients with chronic hepatitis B. Hepatology 52(Suppl. 1), 436A (2010).
78. Viread® (tenofovir), European summary of product characteristics. Gilead Sciences International Limited, Madrid, Spain, April 2011.
79. Kwon H, Lok AS. Hepatitis B therapy. Nat. Rev. Gastroenterol. Hepatol. 8(5), 275-284 (2011).
80. Jeng RW-J, Sheen I-S, Chien R-N et al. Consolidation duration influences the relapse rate post entecavir treatment in HBeAg negative non-cirrhotic patients with CHB. Hepatol. Int. 6(1), Abstract PP09-003 (2012).
81. Sonneveld MJ, Zoutendijk R, Janssen HL. Hepatitis B surface antigen monitoring and management of chronic hepatitis B. J. Viral Hepat. 18(7), 449-457 (2011).
82. Brunetto MR, Colombatto P, Bonino F. Bio-mathematical models of viral dynamics to tailor antiviral therapy in chronic viral hepatitis. World J. Gastroenterol. 15(5), 531-537 (2009).
83. Hadziyannis S, Sevastianos V, Rapti I. Outcome of HBeAg-negative chroic hepatitis B (CHB) 5 years after discontinuation of long term adefovir dipivoxil (ADV) treatment. J. Hepatol. 50(Suppl. 1), S9-S10 (2009).
84. Petersen J, Buggisch P, Stoehr A et al. Stopping long-term nucleos(t)ide analogue therapy before HBsAg loss or seroconversion in HBeAg negative patients: experience from four referral centers in Germany. J. Hepatol. 54, S299 (2011).
85. Papatheodoridis GV, Lampertico P, Manolakopoulos S, Lok A. Incidence of hepatocellular carcinoma in chronic hepatitis B patients receiving nucleos(t)ide therapy: a systematic review. J. Hepatol. 53(2), 348-356 (2010).
86. Bruix J, Sherman M; American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma: an update. Hepatology 53(3), 1020-1022 (2011).