Clinical implications of hepatitis B virus mutations: Recent advances

World Journal of Gastroenterology

Volumn 20, Issue 24, 2014, Pages 7653-7664

  Lazarevic, Ivana ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Drug resistance; Hepatitis B virus; Hepatitis B virus variability; Mutation; Vaccine escape

Indexed keywords

ADEFOVIR; ENTECAVIR; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; LAMIVUDINE; RNA DIRECTED DNA POLYMERASE; TELBIVUDINE; TENOFOVIR; VIRUS DNA; VIRUS PROTEIN; VITRONECTIN; ANTIVIRUS AGENT; CORE PROTEIN; HEPATITIS B ANTIGEN; HEPATITIS B VIRUS X PROTEIN; NUCLEOCAPSID PROTEIN, HEPATITIS C VIRUS; TRANSACTIVATOR PROTEIN;

ANTIVIRAL THERAPY; ARTICLE; CLINICAL FEATURE; DISEASE COURSE; DRUG RESISTANCE; GENETIC VARIABILITY; GENOME ANALYSIS; HEPATITIS B; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; LIFE CYCLE STAGE; LIVER CELL CARCINOMA; META ANALYSIS (TOPIC); NONHUMAN; TREATMENT OUTCOME; VACCINATION; VIRUS MORPHOLOGY; VIRUS MUTATION; ACUTE DISEASE; ANTIVIRAL RESISTANCE; DRUG EFFECTS; GENETICS; GENOTYPE; HEPATITIS B VIRUS; IMMUNOLOGY; MUTATION; PATHOGENICITY; PHENOTYPE; VIROLOGY;

ACUTE DISEASE; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; GENOTYPE; HEPATITIS B; HEPATITIS B ANTIGENS; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; MUTATION; PHENOTYPE; TRANS-ACTIVATORS; TREATMENT OUTCOME; VIRAL CORE PROTEINS;

EID: 84903124437     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i24.7653     Document Type: Article

References (131)

1. Lavanchy D. Worldwide epidemiology of HBV infection, disease burden, and vaccine prevention. J Clin Virol 2005; 34 Suppl 1: S1-S3 [PMID: 16461208 DOI: 10.1016/ S1386-6532(05)00384-7]
2. Nowak MA, Bonhoeffer S, Hill AM, Boehme R, Thomas HC, McDade H. Viral dynamics in hepatitis B virus infection. Proc Natl Acad Sci USA 1996; 93: 4398-4402 [PMID: 8633078 DOI: 10.1073/pnas.93.9.4398]
3. Okamoto H, Imai M, Kametani M, Nakamura T, Mayumi M. Genomic heterogeneity of hepatitis B virus in a 54-yearold woman who contracted the infection through maternofetal transmission. Jpn J Exp Med 1987; 57: 231-236 [PMID: 3430800]
4. Seeger C, Zoulim F, Mason WS. Hepadnaviruses. In: Knipe DM, Howley PM, Editors. Fields Virology, 5th ed. Philadelphia: Lippincott Williams Wilkins, 2007: 2977-3029
5. Rabe B, Vlachou A, Panté N, Helenius A, Kann M. Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc Natl Acad Sci USA 2003; 100: 9849-9854 [PMID: 12909718 DOI: 10.1073/pnas.1730940100]
6. Kann M, Bischof A, Gerlich WH. In vitro model for the nuclear transport of the hepadnavirus genome. J Virol 1997; 71: 1310-1316 [PMID: 8995655]
7. Bock CT, Schwinn S, Locarnini S, Fyfe J, Manns MP, Trautwein C, Zentgraf H. Structural organization of the hepatitis B virus minichromosome. J Mol Biol 2001; 307: 183-196 [PMID: 11243813 DOI: 10.1006/jmbi.2000.4481]
8. Tuttleman JS, Pourcel C, Summers J. Formation of the pool of covalently closed circular viral DNA in hepadnavirusinfected cells. Cell 1986; 47: 451-460 [PMID: 3768961 DOI: 10.1016/0092-8674(86)90602-1]
9. Lambert C, Döring T, Prange R. Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol 2007; 81: 9050-9060 [PMID: 17553870 DOI: 10.1128/JVI.00479-07]
10. Kay A, Zoulim F. Hepatitis B virus genetic variability and evolution. Virus Res 2007; 127: 164-176 [PMID: 17383765 DOI: 10.1016/j.virusres.2007.02.021]
11. Zanetti AR, Tanzi E, Manzillo G, Maio G, Sbreglia C, Caporaso N, Thomas H, Zuckerman AJ. Hepatitis B variant in Europe. Lancet 1988; 2: 1132-1133 [PMID: 2460710 DOI: 10.1016/S0140-6736(88)90541-7]
12. Carman WF, Zanetti AR, Karayiannis P, Waters J, Manzillo G, Tanzi E, Zuckerman AJ, Thomas HC. Vaccine-induced escape mutant of hepatitis B virus. Lancet 1990; 336: 325-329 [PMID: 1697396 DOI: 10.1016/0140-6736(90)91874-A]
13. Zuckerman JN, Zuckerman AJ. Mutations of the surface protein of hepatitis B virus. Antiviral Res 2003; 60: 75-78 [PMID: 14638401 DOI: 10.1016/j.antiviral.2003.08.013]
14. Hsu HY, Chang MH, Liaw SH, Ni YH, Chen HL. Changes of hepatitis B surface antigen variants in carrier children before and after universal vaccination in Taiwan. Hepatology 1999; 30: 1312-1317 [PMID: 10534356 DOI: 10.1002/hep.510300511]
15. François G, Kew M, Van Damme P, Mphahlele MJ, Meheus A. Mutant hepatitis B viruses: a matter of academic interest only or a problem with far-reaching implications? Vaccine 2001; 19: 3799-3815 [PMID: 11427251 DOI: 10.1016/S0264-410X(01)00108-6]
16. Coleman PF, Chen YC, Mushahwar IK. Immunoassay detection of hepatitis B surface antigen mutants. J Med Virol 1999; 59: 19-24 [PMID: 10440803]
17. Ireland JH, O'Donnell B, Basuni AA, Kean JD, Wallace LA, Lau GK, Carman WF. Reactivity of 13 in vitro expressed hepatitis B surface antigen variants in 7 commercial diagnostic assays. Hepatology 2000; 31: 1176-1182 [PMID: 10796895 DOI: 10.1053/he.2000.6407]
18. Lee KM, Kim YS, Ko YY, Yoo BM, Lee KJ, Kim JH, Hahm KB, Cho SW. Emergence of vaccine-induced escape mutant of hepatitis B virus with multiple surface gene mutations in a Korean child. J Korean Med Sci 2001; 16: 359-362 [PMID: 11410701]
19. Moerman B, Moons V, Sommer H, Schmitt Y, Stetter M. Evaluation of sensitivity for wild type and mutant forms of hepatitis B surface antigen by four commercial HBsAg assays. Clin Lab 2004; 50: 159-162 [PMID: 15074469]
20. Seddigh-Tonekaboni S, Lim WL, Young B, Hou JL, Waters J, Luo KX, Thomas HC, Karayiannis P. Hepatitis B surface antigen variants in vaccinees, blood donors and an interferon-treated patient. J Viral Hepat 2001; 8: 154-158 [PMID: 11264736 DOI: 10.1046/j.1365-2893.2001.00275.x]
21. Zuckerman AJ, Zuckerman JN. Molecular epidemiology of hepatitis B virus mutants. J Med Virol 1999; 58: 193-195 [PMID: 10447411]
22. Oon CJ, Chen WN, Goo KS, Goh KT. Intra-familial evidence of horizontal transmission of hepatitis B virus surface antigen mutant G145R. J Infect 2000; 41: 260-264 [PMID: 11120616 DOI: 10.1053/jinf.2000.0751]
23. Chakravarty R, Neogi M, Roychowdhury S, Panda CK. Presence of hepatitis B surface antigen mutant G145R DNA in the peripheral blood leukocytes of the family members of an asymptomatic carrier and evidence of its horizontal transmission. Virus Res 2002; 90: 133-141 [PMID: 12457969 DOI: 10.1016/S0168-1702(02)00147-8]
24. Chong-Jin O, Wei Ning C, Shiuan K, Gek Keow L. Identification of hepatitis B surface antigen variants with alterations outside the "a" determinant in immunized Singapore infants. J Infect Dis 1999; 179: 259-263 [PMID: 9841851 DOI: 10.1086/314553]
25. Ngui SL, O'Connell S, Eglin RP, Heptonstall J, Teo CG. Low detection rate and maternal provenance of hepatitis B virus S gene mutants in cases of failed postnatal immunoprophylaxis in England and Wales. J Infect Dis 1997; 176: 1360-1365 [PMID: 9359739 DOI: 10.1086/514133]
26. Carman WF. The clinical significance of surface antigen variants of hepatitis B virus. J Viral Hepat 1997; 4 Suppl 1: 11-20 [PMID: 9097273 DOI: 10.1111/j.1365-2893.1997.tb00155.x]
27. He C, Nomura F, Itoga S, Isobe K, Nakai T. Prevalence of vaccine-induced escape mutants of hepatitis B virus in the adult population in China: a prospective study in 176 restaurant employees. J Gastroenterol Hepatol 2001; 16: 1373-1377 [PMID: 11851835 DOI: 10.1046/j.1440-1746.2001.02654.x]
28. Hou J, Wang Z, Cheng J, Lin Y, Lau GK, Sun J, Zhou F, Waters J, Karayiannis P, Luo K. Prevalence of naturally occurring surface gene variants of hepatitis B virus in nonimmunized surface antigen-negative Chinese carriers. Hepatology 2001; 34: 1027-1034 [PMID: 11679975 DOI: 10.1053/ jhep.2001.28708]
29. Ho M, Mau Y, Lu C, Huang S, Hsu L, Lin S, Hsu H. Patterns of circulating hepatitis B surface antigen variants among vaccinated children born to hepatitis B surface antigen carrier and non-carrier mothers. A population-based comparative study. J Biomed Sci 1998; 5: 355-362 [PMID: 9758909 DOI: 10.1007/BF02253445]
30. Oon CJ, Tan KL, Harrison T, Zuckerman A. Natural history of hepatitis B surface antigen mutants in children. Lancet 1996; 348: 1524 [PMID: 8942816 DOI: 10.1016/ S0140-6736(05)65950-8]
31. Song BC, Kim SH, Kim H, Ying YH, Kim HJ, Kim YJ, Yoon JH, Lee HS, Cha CY, Kook YH, Kim BJ. Prevalence of naturally occurring surface antigen variants of hepatitis B virus in Korean patients infected chronically. J Med Virol 2005; 76: 194-202 [PMID: 15834881 DOI: 10.1002/jmv.20354]
32. Avellón A, Echevarria JM. Frequency of hepatitis B virus 'a' determinant variants in unselected Spanish chronic carriers. J Med Virol 2006; 78: 24-36 [PMID: 16299725 DOI: 10.1002/ jmv.20516]
33. Mendy M, D'Mello F, Kanellos T, Oliver S, Whittle H, Howard CR. Envelope protein variability among HBV-Infected asymptomatic carriers and immunized children with breakthrough infections. J Med Virol 2008; 80: 1537-1546 [PMID: 18649345 DOI: 10.1002/jmv.21221]
34. De Maddalena C, Giambelli C, Tanzi E, Colzani D, Schiavini M, Milazzo L, Bernini F, Ebranati E, Cargnel A, Bruno R, Galli M, Zehender G. High level of genetic heterogeneity in S and P genes of genotype D hepatitis B virus. Virology 2007; 365: 113-124 [PMID: 17451771 DOI: 10.1016/ j.virol.2007.03.015]
35. Roque-Afonso AM, Férey MP, Ly TD, Graube A, CostaFaria L, Samuel D, Dussaix E. Viral and clinical factors associated with surface gene variants among hepatitis B virus carriers. Antivir Ther 2007; 12: 1255-1263 [PMID: 18240865]
36. Lazarevic I, Cupic M, Delic D, Svirtlih NS, Simonovic J, Jovanovic T. Prevalence of hepatitis B virus MHR mutations and their correlation with genotypes and antiviral therapy in chronically infected patients in Serbia. J Med Virol 2010; 82: 1160-1167 [PMID: 20513079 DOI: 10.1002/jmv.21810]
37. Laoi BN, Crowley B. Molecular characterization of hepatitis B virus (HBV) isolates, including identification of a novel recombinant, in patients with acute HBV infection attending an Irish hospital. J Med Virol 2008; 80: 1554-1564 [PMID: 18649329 DOI: 10.1002/jmv.21273]
38. Dunford L, Carr MJ, Dean J, Nguyen LT, Ta Thi TH, Nguyen BT, Connell J, Coughlan S, Nguyen HT, Hall WW, Thi LA. A multicentre molecular analysis of hepatitis B and blood-borne virus coinfections in Viet Nam. PLoS One 2012; 7: e39027 [PMID: 22720022 DOI: 10.1371/journal.pone.0039027]
39. Chen DS. Hepatitis B vaccination: The key towards elimination and eradication of hepatitis B. J Hepatol 2009; 50: 805-816 [PMID: 19231008 DOI: 10.1016/j.jhep.2009.01.002]
40. Wilson JN, Nokes DJ, Carman WF. The predicted pattern of emergence of vaccine-resistant hepatitis B: a cause for concern? Vaccine 1999; 17: 973-978 [PMID: 10067705 DOI: 10.1016/S0264-410X(98)00313-2]
41. Chen CY, Hsu HY, Liu CC, Chang MH, Ni YH. Stable seroepidemiology of hepatitis B after universal immunization in Taiwan: A 3-year study of national surveillance of primary school students. Vaccine 2010; 28: 5605-5608 [PMID: 20598405 DOI: 10.1016/j.vaccine.2010.06.029]
42. Wiseman E, Fraser MA, Holden S, Glass A, Kidson BL, Heron LG, Maley MW, Ayres A, Locarnini SA, Levy MT. Perinatal transmission of hepatitis B virus: an Australian experience. Med J Aust 2009; 190: 489-492 [PMID: 19413519]
43. Ghaziasadi A, Alavian SM, Norouzi M, Fazeli Z, Jazayeri SM. Mutational analysis of HBs Ag-positive mothers and their infected children despite immunoprophylaxis. Iran J Allergy Asthma Immunol 2013; 12: 352-360 [PMID: 23996711]
44. Raimondo G, Allain JP, Brunetto MR, Buendia MA, Chen DS, Colombo M, Craxì A, Donato F, Ferrari C, Gaeta GB, Gerlich WH, Levrero M, Locarnini S, Michalak T, Mondelli MU, Pawlotsky JM, Pollicino T, Prati D, Puoti M, Samuel D, Shouval D, Smedile A, Squadrito G, Trépo C, Villa E, Will H, Zanetti AR, Zoulim F. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 2008; 49: 652-657 [PMID: 18715666 DOI: 10.1016/j.jhep.2008.07.014]
45. Raimondo G, Pollicino T, Cacciola I, Squadrito G. Occult hepatitis B virus infection. J Hepatol 2007; 46: 160-170 [PMID: 17112622 DOI: 10.1016/j.jhep.2006.10.007]
46. Dettori S, Candido A, Kondili LA, Chionne P, Taffon S, Genovese D, Iudicone P, Miceli M, Rapicetta M. Identification of low HBV-DNA levels by nucleic acid amplification test (NAT) in blood donors. J Infect 2009; 59: 128-133 [PMID: 19586663 DOI: 10.1016/j.jinf.2009.06.007]
47. Velati C, Romanò L, Fomiatti L, Baruffi L, Zanetti AR. Impact of nucleic acid testing for hepatitis B virus, hepatitis C virus, and human immunodeficiency virus on the safety of blood supply in Italy: a 6-year survey. Transfusion 2008; 48: 2205-2213 [PMID: 18631163 DOI: 10.1111/ j.1537-2995.2008.01813.x]
48. Brojer E, Grabarczyk P, Liszewski G, Mikulska M, Allain JP, Letowska M. Characterization of HBV DNA+/HBsAgblood donors in Poland identified by triplex NAT. Hepatology 2006; 44: 1666-1674 [PMID: 17133474 DOI: 10.1002/hep.21413]
49. Katsoulidou A, Paraskevis D, Magiorkinis E, Moschidis Z, Haida C, Hatzitheodorou E, Varaklioti A, Karafoulidou A, Hatzitaki M, Kavallierou L, Mouzaki A, Andrioti E, Veneti C, Kaperoni A, Zervou E, Politis C, Hatzakis A. Molecular characterization of occult hepatitis B cases in Greek blood donors. J Med Virol 2009; 81: 815-825 [PMID: 19319945 DOI: 10.1002/jmv.21499]
50. Svicher V, Cento V, Bernassola M, Neumann-Fraune M, Van Hemert F, Chen M, Salpini R, Liu C, Longo R, Visca M, Romano S, Micheli V, Bertoli A, Gori C, Ceccherini-Silberstein F, Sarrecchia C, Andreoni M, Angelico M, Ursitti A, Spanò A, Zhang JM, Verheyen J, Cappiello G, Perno CF. Novel HBsAg markers tightly correlate with occult HBV infection and strongly affect HBsAg detection. Antiviral Res 2012; 93: 86-93 [PMID: 22086128 DOI: 10.1016/j.antiviral.2011.10.022]
51. Huang CH, Yuan Q, Chen PJ, Zhang YL, Chen CR, Zheng QB, Yeh SH, Yu H, Xue Y, Chen YX, Liu PG, Ge SX, Zhang J, Xia NS. Influence of mutations in hepatitis B virus surface protein on viral antigenicity and phenotype in occult HBV strains from blood donors. J Hepatol 2012; 57: 720-729 [PMID: 22634131 DOI: 10.1016/j.jhep.2012.05.009]
52. Yuan Q, Ou SH, Chen CR, Ge SX, Pei B, Chen QR, Yan Q, Lin YC, Ni HY, Huang CH, Yeo AE, Shih JW, Zhang J, Xia NS. Molecular characteristics of occult hepatitis B virus from blood donors in southeast China. J Clin Microbiol 2010; 48: 357-362 [PMID: 19940057 DOI: 10.1128/JCM.01781-09]
53. Huang X, Qin Y, Li W, Shi Q, Xue Y, Li J, Liu C, Hollinger FB, Shen Q. Molecular analysis of the hepatitis B virus presurface and surface gene in patients from eastern China with occult hepatitis B. J Med Virol 2013; 85: 979-986 [PMID: 23588723 DOI: 10.1002/jmv.23556]
54. Cassini R, De Mitri MS, Gibellini D, Urbinati L, Bagaglio S, Morsica G, Domenicali M, Verucchi G, Bernardi M. A novel stop codon mutation within the hepatitis B surface gene is detected in the liver but not in the peripheral blood mononuclear cells of HIV-infected individuals with occult HBV infection. J Viral Hepat 2013; 20: 42-49 [PMID: 23231083 DOI: 10.1111/j.1365-2893.2012.01623.x]
55. Chen SJ, Zhao YX, Fang Y, Xu WZ, Ma YX, Song ZW, Teng X, Gu HX. Viral deletions among healthy young Chinese adults with occult hepatitis B virus infection. Virus Res 2012; 163: 197-201 [PMID: 21963662 DOI: 10.1016/ j.virusres.2011.09.029]
56. Tong S, Kim KH, Chante C, Wands J, Li J. Hepatitis B Virus e Antigen Variants. Int J Med Sci 2005; 2: 2-7 [PMID: 15968333 DOI: 10.7150/ijms.2.2]
57. Hadziyannis SJ, Lieberman HM, Karvountzis GG, Shafritz DA. Analysis of liver disease, nuclear HBcAg, viral replication, and hepatitis B virus DNA in liver and serum of HBeAg Vs. anti-HBe positive carriers of hepatitis B virus. Hepatology 1983; 3: 656-662 [PMID: 6618432 DOI: 10.1002/ hep.1840030505]
58. Funk ML, Rosenberg DM, Lok AS. World-wide epidemiology of HBeAg-negative chronic hepatitis B and associated precore and core promoter variants. J Viral Hepat 2002; 9: 52-61 [PMID: 11851903 DOI: 10.1046/j.1365-2893.2002.00304.x]
59. Buckwold VE, Xu Z, Yen TS, Ou JH. Effects of a frequent double-nucleotide basal core promoter mutation and its putative single-nucleotide precursor mutations on hepatitis B virus gene expression and replication. J Gen Virol 1997; 78 (Pt 8): 2055-2065 [PMID: 9267007]
60. Li J, Buckwold VE, Hon MW, Ou JH. Mechanism of suppression of hepatitis B virus precore RNA transcription by a frequent double mutation. J Virol 1999; 73: 1239-1244 [PMID: 9882327]
61. Baumert TF, Rogers SA, Hasegawa K, Liang TJ. Two core promotor mutations identified in a hepatitis B virus strain associated with fulminant hepatitis result in enhanced viral replication. J Clin Invest 1996; 98: 2268-2276 [PMID: 8941643 DOI: 10.1172/JCI119037]
62. Parekh S, Zoulim F, Ahn SH, Tsai A, Li J, Kawai S, Khan N, Trépo C, Wands J, Tong S. Genome replication, virion secretion, and e antigen expression of naturally occurring hepatitis B virus core promoter mutants. J Virol 2003; 77: 6601-6612 [PMID: 12767980 DOI: 10.1128/JVI.77.12.6601-6612.2003]
63. Brunetto MR, Stemler M, Bonino F, Schodel F, Oliveri F, Rizzetto M, Verme G, Will H. A new hepatitis B virus strain in patients with severe anti-HBe positive chronic hepatitis B. J Hepatol 1990; 10: 258-261 [PMID: 2332598 DOI: 10.1016/016 8-8278(90)90062-V]
64. Carman WF, Jacyna MR, Hadziyannis S, Karayiannis P, McGarvey MJ, Makris A, Thomas HC. Mutation preventing formation of hepatitis B e antigen in patients with chronic hepatitis B infection. Lancet 1989; 2: 588-591 [PMID: 2570285 DOI: 10.1016/S0140-6736(89)90713-7]
65. Li JS, Tong SP, Wen YM, Vitvitski L, Zhang Q, Trépo C. Hepatitis B virus genotype A rarely circulates as an HBeminus mutant: possible contribution of a single nucleotide in the precore region. J Virol 1993; 67: 5402-5410 [PMID: 8350403]
66. Yin J, Xie J, Liu S, Zhang H, Han L, Lu W, Shen Q, Xu G, Dong H, Shen J, Zhang J, Han J, Wang L, Liu Y, Wang F, Zhao J, Zhang Q, Ni W, Wang H, Cao G. Association between the various mutations in viral core promoter region to different stages of hepatitis B, ranging of asymptomatic carrier state to hepatocellular carcinoma. Am J Gastroenterol 2011; 106: 81-92 [PMID: 20959817 DOI: 10.1038/ajg.2010.399]
67. Yang HI, Yeh SH, Chen PJ, Iloeje UH, Jen CL, Su J, Wang LY, Lu SN, You SL, Chen DS, Liaw YF, Chen CJ. Associations between hepatitis B virus genotype and mutants and the risk of hepatocellular carcinoma. J Natl Cancer Inst 2008; 100: 1134-1143 [PMID: 18695135 DOI: 10.1093/jnci/djn243]
68. Liao Y, Hu X, Chen J, Cai B, Tang J, Ying B, Wang H, Wang L. Precore mutation of hepatitis B virus may contribute to hepatocellular carcinoma risk: evidence from an updated metaanalysis. PLoS One 2012; 7: e38394 [PMID: 22675557 DOI: 10.1371/journal.pone.0038394]
69. Hou J, Lin Y, Waters J, Wang Z, Min J, Liao H, Jiang J, Chen J, Luo K, Karayiannis P. Detection and significance of a G1862T variant of hepatitis B virus in Chinese patients with fulminant hepatitis. J Gen Virol 2002; 83: 2291-2298 [PMID: 12185284]
70. Inoue J, Ueno Y, Nagasaki F, Wakui Y, Kondo Y, Fukushima K, Niitsuma H, Shimosegawa T. Enhanced intracellular retention of a hepatitis B virus strain associated with fulminant hepatitis. Virology 2009; 395: 202-209 [PMID: 19850315 DOI:10.1016/j.virol.2009.09.028]
71. Andrisani OM, Barnabas S. The transcriptional function of the hepatitis B virus X protein and its role in hepatocarcinogenesis (Review). Int J Oncol 1999; 15: 373-379 [PMID: 10402250]
72. Bouchard MJ, Schneider RJ. The enigmatic X gene of hepatitis B virus. J Virol 2004; 78: 12725-12734 [PMID: 15542625 DOI: 10.1128/JVI.78.23.12725-12734.2004]
73. Terradillos O, Billet O, Renard CA, Levy R, Molina T, Briand P, Buendia MA. The hepatitis B virus X gene potentiates c-myc-induced liver oncogenesis in transgenic mice. Oncogene 1997; 14: 395-404 [PMID: 9053836 DOI: 10.1038/ sj.onc.1200850]
74. Madden CR, Finegold MJ, Slagle BL. Hepatitis B virus X protein acts as a tumor promoter in development of diethylnitrosamine-induced preneoplastic lesions. J Virol 2001; 75: 3851-3858 [PMID: 11264374 DOI: 10.1128/ JVI.75.8.3851-3858.2001]
75. Buendia MA. Genetics of hepatocellular carcinoma. Semin Cancer Biol 2000; 10: 185-200 [PMID: 10936068 DOI: 10.1006/ scbi.2000.0319]
76. Lee TH, Elledge SJ, Butel JS. Hepatitis B virus X protein interacts with a probable cellular DNA repair protein. J Virol 1995; 69: 1107-1114 [PMID: 7815490]
77. Xu C, Zhou W, Wang Y, Qiao L. Hepatitis B virus-induced hepatocellular carcinoma. Cancer Lett 2014; 345: 216-222 [PMID: 23981576 DOI: 10.1016/j.canlet.2013.08.035]
78. Sirma H, Giannini C, Poussin K, Paterlini P, Kremsdorf D, Bréchot C. Hepatitis B virus X mutants, present in hepatocellular carcinoma tissue abrogate both the antiproliferative and transactivation effects of HBx. Oncogene 1999; 18: 4848-4859 [PMID: 10490818 DOI: 10.1038/sj.onc.1202867]
79. Iavarone M, Trabut JB, Delpuech O, Carnot F, Colombo M, Kremsdorf D, Bréchot C, Thiers V. Characterisation of hepatitis B virus X protein mutants in tumour and nontumour liver cells using laser capture microdissection. J Hepatol 2003; 39: 253-261 [PMID: 12873823 DOI: 10.1016/ S0168-8278(03)00217-4]
80. Sung WK, Zheng H, Li S, Chen R, Liu X, Li Y, Lee NP, Lee WH, Ariyaratne PN, Tennakoon C, Mulawadi FH, Wong KF, Liu AM, Poon RT, Fan ST, Chan KL, Gong Z, Hu Y, Lin Z, Wang G, Zhang Q, Barber TD, Chou WC, Aggarwal A, Hao K, Zhou W, Zhang C, Hardwick J, Buser C, Xu J, Kan Z, Dai H, Mao M, Reinhard C, Wang J, Luk JM. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet 2012; 44: 765-769 [PMID: 22634754]
81. Toh ST, Jin Y, Liu L, Wang J, Babrzadeh F, Gharizadeh B, Ronaghi M, Toh HC, Chow PK, Chung AY, Ooi LL, Lee CG. Deep sequencing of the hepatitis B virus in hepatocellular carcinoma patients reveals enriched integration events, structural alterations and sequence variations. Carcinogenesis 2013; 34: 787-798 [PMID: 23276797 DOI: 10.1093/carcin/bgs406]
82. Jung SY, Kim YJ. C-terminal region of HBx is crucial for mitochondrial DNA damage. Cancer Lett 2013; 331: 76-83 [PMID: 23246371 DOI: 10.1016/j.canlet.2012.12.004]
83. Yuan HJ, Lee WM. Molecular mechanisms of resistance to antiviral therapy in patients with chronic hepatitis B. Curr Mol Med 2007; 7: 185-197 [PMID: 17346170 DOI: 10.2174/156 652407780059159]
84. Bartholomeusz A, Locarnini SA. Antiviral drug resistance: clinical consequences and molecular aspects. Semin Liver Dis 2006; 26: 162-170 [PMID: 16673294 DOI: 10.1055/ s-2006-939758]
85. Zoulim F, Locarnini S. Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 2009; 137: 1593-608. e1-2 [PMID: 19737565 DOI: 10.1053/j.gastro.2009.08.063]
86. Litwin S, Toll E, Jilbert AR, Mason WS. The competing roles of virus replication and hepatocyte death rates in the emergence of drug-resistant mutants: theoretical considerations. J Clin Virol 2005; 34 Suppl 1: S96-S107 [PMID: 16461233 DOI: 10.1016/S1386-6532(05)80018-6]
87. Papatheodoridis GV, Manolakopoulos S, Dusheiko G, Archimandritis AJ. Therapeutic strategies in the management of patients with chronic hepatitis B virus infection. Lancet Infect Dis 2008; 8: 167-178 [PMID: 18053766 DOI: 10.1016/S1473-3099(07)70264-5]
88. Lai CL, Dienstag J, Schiff E, Leung NW, Atkins M, Hunt C, Brown N, Woessner M, Boehme R, Condreay L. Prevalence and clinical correlates of YMDD variants during lamivudine therapy for patients with chronic hepatitis B. Clin Infect Dis 2003; 36: 687-696 [PMID: 12627352 DOI: 10.1086/368083]
89. Liaw YF, Gane E, Leung N, Zeuzem S, Wang Y, Lai CL, Heathcote EJ, Manns M, Bzowej N, Niu J, Han SH, Hwang SG, Cakaloglu Y, Tong MJ, Papatheodoridis G, Chen Y, Brown NA, Albanis E, Galil K, Naoumov NV. 2-Year GLOBE trial results: telbivudine Is superior to lamivudine in patients with chronic hepatitis B. Gastroenterology 2009; 136: 486-495 [PMID: 19027013 DOI: 10.1053/j.gastro.2008.10.026]
90. Marcellin P, Chang TT, Lim SG, Sievert W, Tong M, Arterburn S, Borroto-Esoda K, Frederick D, Rousseau F. Longterm efficacy and safety of adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. Hepatology 2008; 48: 750-758 [PMID: 18752330 DOI: 10.1002/ hep.22414]
91. Chang TT, Lai CL, Kew Yoon S, Lee SS, Coelho HS, Carrilho FJ, Poordad F, Halota W, Horsmans Y, Tsai N, Zhang H, Tenney DJ, Tamez R, Iloeje U. Entecavir treatment for up to 5 years in patients with hepatitis B e antigen-positive chronic hepatitis B. Hepatology 2010; 51: 422-430 [PMID: 20049753 DOI: 10.1002/hep.23327]
92. Snow-Lampart A, Chappell B, Curtis M, Zhu Y, Myrick F, Schawalder J, Kitrinos K, Svarovskaia ES, Miller MD, Sorbel J, Heathcote J, Marcellin P, Borroto-Esoda K. 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: 763-773 [PMID: 21374657 DOI: 10.1002/hep.24078]
93. Tenney DJ, Rose RE, Baldick CJ, Pokornowski KA, Eggers BJ, Fang J, Wichroski MJ, Xu D, Yang J, Wilber RB, Colonno RJ. Long-term monitoring shows hepatitis B virus resistance to entecavir in nucleoside-naïve patients is rare through 5 years of therapy. Hepatology 2009; 49: 1503-1514 [PMID: 19280622 DOI: 10.1002/hep.22841]
94. Sheldon J, Camino N, Rodés B, Bartholomeusz A, Kuiper M, Tacke F, Núñez M, Mauss S, Lutz T, Klausen G, Locarnini S, Soriano V. Selection of hepatitis B virus polymerase mutations in HIV-coinfected patients treated with tenofovir. Antivir Ther 2005; 10: 727-734 [PMID: 16218172]
95. Margeridon-Thermet S, Svarovskaia ES, Babrzadeh F, Martin R, Liu TF, Pacold M, Reuman EC, Holmes SP, BorrotoEsoda K, Shafer RW. Low-level persistence of drug resistance mutations in hepatitis B virus-infected subjects with a past history of Lamivudine treatment. Antimicrob Agents Chemother 2013; 57: 343-349 [PMID: 23114756 DOI: 10.1128/ AAC.01601-12]
96. Borroto-Esoda K, Miller MD, Arterburn S. Pooled analysis of amino acid changes in the HBV polymerase in patients from four major adefovir dipivoxil clinical trials. J Hepatol 2007; 47: 492-498 [PMID: 17692425 DOI: 10.1016/j.jhep.2007.06.011]
97. Schildgen O, Sirma H, Funk A, Olotu C, Wend UC, Hartmann H, Helm M, Rockstroh JK, Willems WR, Will H, Gerlich WH. Variant of hepatitis B virus with primary resistance to adefovir. N Engl J Med 2006; 354: 1807-1812 [PMID: 16641397 DOI: 10.1056/NEJMoa051214]
98. Schildgen O, Olotu C, Funk A, Zöllner B, Helm M, Rockstroh JK, Sirma H. Selection and counterselection of the rtI233V adefovir resistance mutation during antiviral therapy. J Clin Microbiol 2010; 48: 631-634 [PMID: 20007398 DOI: 10.1128/JCM.01073-09]
99. Curtis M, Zhu Y, Borroto-Esoda K. Hepatitis B virus containing the I233V mutation in the polymerase reversetranscriptase domain remains sensitive to inhibition by adefovir. J Infect Dis 2007; 196: 1483-1486 [PMID: 18008227 DOI: 10.1086/522521]
100. Ismail AM, Sharma OP, Kumar MS, Kannangai R, Abraham P. Impact of rtI233V mutation in hepatitis B virus polymerase protein and adefovir efficacy: Homology modeling and molecular docking studies. Bioinformation 2013; 9: 121-125 [PMID: 23423477 DOI: 10.6026/97320630009121]
101. Delaney WE, Ray AS, Yang H, Qi X, Xiong S, Zhu Y, Miller MD. Intracellular metabolism and in vitro activity of tenofovir against hepatitis B virus. Antimicrob Agents Chemother 2006; 50: 2471-2477 [PMID: 16801428 DOI: 10.1128/ AAC.00138-06]
102. Amini-Bavil-Olyaee S, Herbers U, Sheldon J, Luedde T, Trautwein C, Tacke F. The rtA194T polymerase mutation impacts viral replication and susceptibility to tenofovir in hepatitis B e antigen-positive and hepatitis B e antigen-negative hepatitis B virus strains. Hepatology 2009; 49: 1158-1165 [PMID: 19263474 DOI: 10.1002/hep.22790]
103. Qin B, Budeus B, Cao L, Wu C, Wang Y, Zhang X, Rayner S, Hoffmann D, Lu M, Chen X. The amino acid substitutions rtP177G and rtF249A in the reverse transcriptase domain of hepatitis B virus polymerase reduce the susceptibility to tenofovir. Antiviral Res 2013; 97: 93-100 [PMID: 23261845 DOI: 10.1016/j.antiviral.2012.12.007]
104. Kitrinos KM, Corsa A, Liu Y, Flaherty J, Snow-Lampart A, Marcellin P, Borroto-Esoda K, Miller MD. No detectable resistance to tenofovir disoproxil fumarate after 6 years of therapy in patients with chronic hepatitis B. Hepatology 2014; 59: 434-442 [PMID: 23939953 DOI: 10.1002/hep.26686]
105. Villet S, Pichoud C, Billioud G, Barraud L, Durantel S, Trépo C, Zoulim F. Impact of hepatitis B virus rtA181V/T mutants on hepatitis B treatment failure. J Hepatol 2008; 48: 747-755 [PMID: 18331765 DOI: 10.1016/j.jhep.2008.01.027]
106. 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 [PMID: 18537180 DOI: 10.1002/ hep.22295]
107. Lai MW, Yeh CT. The oncogenic potential of hepatitis B virus rtA181T/ surface truncation mutant. Antivir Ther 2008; 13: 875-879 [PMID: 19043921]
108. Lee GH, Aung MO, Dan YY, Lee YM, Mak B, Low HC, Lim K, Thwin MA, Tan PS, Lim SG. Do different lamivudine-resistant hepatitis B genotypes carry the same risk of entecavir resistance? J Med Virol 2013; 85: 26-33 [PMID: 23023992 DOI: 10.1002/jmv.23392]
109. Yim HJ, Hussain M, Liu Y, Wong SN, Fung SK, Lok AS. Evolution of multi-drug resistant hepatitis B virus during sequential therapy. Hepatology 2006; 44: 703-712 [PMID: 16941700 DOI: 10.1002/hep.21290]
110. Liu Y, Wang C, Zhong Y, Chen L, Li X, Ji D, Wang H, Xin S, Zoulim F, Xu D. 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: 1185-1190 [PMID: 21149926 DOI: 10.3851/ IMP1679]
111. Kim SS, Cho SW, Kim SO, Hong SP, Cheong JY. Multidrug-resistant hepatitis B virus resulting from sequential monotherapy with lamivudine, adefovir, and entecavir: clonal evolution during lamivudine plus adefovir therapy. J Med Virol 2013; 85: 55-64 [PMID: 23096938 DOI: 10.1002/ jmv.23440]
112. Yeh CT. Development of HBV S gene mutants in chronic hepatitis B patients receiving nucleotide/nucleoside analogue therapy. Antivir Ther 2010; 15: 471-475 [PMID: 20516567 DOI: 10.3851/IMP1552]
113. Torresi J, Earnest-Silveira L, Civitico G, Walters TE, Lewin SR, Fyfe J, Locarnini SA, Manns M, Trautwein C, Bock TC. Restoration of replication phenotype of lamivudine-resistant hepatitis B virus mutants by compensatory changes in the "fingers" subdomain of the viral polymerase selected as a consequence of mutations in the overlapping S gene. Virology 2002; 299: 88-99 [PMID: 12167344 DOI: 10.1006/ viro.2002.1448]
114. Villet S, Pichoud C, Villeneuve JP, Trépo C, Zoulim F. Selection of a multiple drug-resistant hepatitis B virus strain in a liver-transplanted patient. Gastroenterology 2006; 131: 1253-1261 [PMID: 17030194 DOI: 10.1053/ j.gastro.2006.08.013]
115. Cento V, Van Hemert F, Neumann-Fraune M, Mirabelli C, Di Maio VC, Salpini R, Bertoli A, Micheli V, Gubertini G, Romano S, Visca M, De Sanctis GM, Berkhout B, Marino N, Mazzotta F, Cappiello G, Spanò A, Sarrecchia C, CeccheriniSilberstein F, Andreoni M, Angelico M, Verheyen J, Perno CF, Svicher V. Anti-HBV treatment induces novel reverse transcriptase mutations with reflective effect on HBV S antigen. J Infect 2013; 67: 303-312 [PMID: 23796863 DOI: 10.1016/ j.jinf.2013.05.008]
116. Pastore G, Santantonio T, Monno L, Milella M, Luchena N, Angarano G. Effects of HIV superinfection on HBV replication in a chronic HBsAg carrier with liver disease. J Hepatol 1988; 7: 164-168 [PMID: 3192920]
117. Cassino L, Torres C, Mbayed V, Laufer N, Campos RH, Quarleri J. Comparative analysis of hepatitis B virus genotype a molecular evolution in patients infected with HBV and in patients co-infected with HBV and HIV. J Med Virol 2012; 84: 562-569 [PMID: 22337294 DOI: 10.1002/jmv.23233]
118. Pal A, Panigrahi R, Biswas A, Datta S, Sarkar N, Guha SK, Saha B, Banerjee A, Chakrabarti S, Chakravarty R. Influence of HIV-associated degree of immune suppression on molecular heterogeneity of hepatitis B virus among HIV co-infected patients. Virology 2013; 436: 134-142 [PMID: 23228859 DOI: 10.1016/j.virol.2012.11.003]
119. Lacombe K, Boyd A, Lavocat F, Pichoud C, Gozlan J, Miailhes P, Lascoux-Combe C, Vernet G, Girard PM, Zoulim F. High incidence of treatment-induced and vaccine-escape hepatitis B virus mutants among human immunodeficiency virus/hepatitis B-infected patients. Hepatology 2013; 58: 912-922 [PMID: 23468093 DOI: 10.1002/hep.26374]
120. Filippini P, Coppola N, Pisapia R, Scolastico C, Marrocco C, Zaccariello A, Nacca C, Sagnelli C, De Stefano G, Ferraro T, De Stefano C, Sagnelli E. Impact of occult hepatitis B virus infection in HIV patients naive for antiretroviral therapy. AIDS 2006; 20: 1253-1260 [PMID: 16816553 DOI: 10.1097/01. aids.0000232232.41877.2a]
121. Núñez M, Ríos P, Pérez-Olmeda M, Soriano V. Lack of 'occult' hepatitis B virus infection in HIV-infected patients. AIDS 2002; 16: 2099-2101 [PMID: 12370518 DOI: 10.1097/000 02030-200210180-00024]
122. Santos EA, Yoshida CF, Rolla VC, Mendes JM, Vieira IF, Arabe J, Gomes SA. Frequent occult hepatitis B virus infection in patients infected with human immunodeficiency virus type 1. Eur J Clin Microbiol Infect Dis 2003; 22: 92-98 [PMID: 12627282]
123. Jardim RN, Gonçales NS, Pereira JS, Fais VC, Gonçales Junior FL. Occult hepatitis B virus infection in immunocompromised patients. Braz J Infect Dis 2008; 12: 300-305 [PMID: 19030729 DOI: 10.1590/S1413-86702008000400008]
124. Shih CM, Lo SJ, Miyamura T, Chen SY, Lee YH. Suppression of hepatitis B virus expression and replication by hepatitis C virus core protein in HuH-7 cells. J Virol 1993; 67: 5823-5832 [PMID: 8396658]
125. Schüttler CG, Fiedler N, Schmidt K, Repp R, Gerlich WH, Schaefer S. Suppression of hepatitis B virus enhancer 1 and 2 by hepatitis C virus core protein. J Hepatol 2002; 37: 855-862 [PMID: 12445429 DOI: 10.1016/S0168-8278(02)00296-9]
126. Carreño V, Bartolomé J, Castillo I, Quiroga JA. Occult hepatitis B virus and hepatitis C virus infections. Rev Med Virol 2009; 18: 139-157 [PMID: 18265423 DOI: 10.1002/rmv.569]
127. Arababadi MK, Hassanshahi G, Yousefi H. HBV-DNA in hemodialysis patients infected by HCV. Saudi J Kidney Dis Transpl 2009; 20: 398-401 [PMID: 19414941]
128. Yeh CT, Chiu CT, Tsai SL, Hong ST, Chu CM, Liaw YF. Absence of precore stop mutant in chronic dual (B and C) and triple (B, C, and D) hepatitis virus infection. J Infect Dis 1994; 170: 1582-1585 [PMID: 7995999 DOI: 10.1093/ infdis/170.6.1582]
129. Yeh CT, Chu CM, Liaw YF. Progression of the proportion of hepatitis B virus precore stop mutant following acute superinfection of hepatitis C. J Gastroenterol Hepatol 1998; 13: 131-136 [PMID: 10221813 DOI: 10.1111/j.1440-1746.1998. tb00627.x]
130. De Mitri MS, Morsica G, Cassini R, Bagaglio S, Andreone P, Bianchi G, Loggi E, Bernardi M. Low replication and variability of HBV pre-core in concomitant infection with hepatitis B and hepatitis C viruses. Arch Virol 2007; 152: 395-404 [PMID: 16953307 DOI: 10.1007/s00705-006-0836-6]
131. Hung CH, Chen CH, Lu SN, Wang JH, Hu TH, Huang CM, Tsai MC, Lee CM. Precore/core promoter mutations and hepatitis B virus genotype in hepatitis B and C dually infected patients treated with interferon-based therapy. Antiviral Res 2012; 93: 55-63 [PMID: 22061616 DOI: 10.1016/j.antiviral]