Patterns of hepatitis b virus immune escape and pol/rt mutations across clinical cohorts of patients with genotypes a, e and occult hepatitis b infection in Nigeria: A multi-centre study

References

• World Health Organisation Global Health Sector Strategies on respectively, HIV, Viral hepatitis and sexually transmitted infections for the period 2022-2023, 2016-2021. Accessed on 24 November, 2021.
   Google Scholar
• Mokaya J, McNaughton AL, Hadley MJ, et al. A systematic review of hepatitis B virus (HBV) drug and vaccine escape mutations in Africa. A call for urgent action. PLoS Negl Trop Dis. 2018;12(8):e0006629.
   PubMed Web of Science ®Google Scholar
• Han YF, Zhao J, Ma LY, et al. Factors predicting occurrence and prognosis of hepatitis B related hepatocellular carcinoma. World J Gastroenterol. 2011 Oct 14;17(38):4258–18. DOI:10.3748/wjg.v17.i38.4258
   PubMed Web of Science ®Google Scholar
• Burns GS, Thompson AJ. Viral hepatitis B: clinical and epidemiological characteristics. Cold Spring Harb Perspect Med. 2014 Oct 30;4(12):a024935. PMID: 25359547; PMCID: PMC4292086. DOI:10.1101/cshperspect.a024935
   PubMed Web of Science ®Google Scholar
• Noordeen F. Hepatitis B virus infection: An insight into infection outcomes and recent treatment options. VirusDis. 2015 Jun;26(1–2):1–8. Epub 2015 Apr 5. PMID: 26436115; PMCID: PMC4585049. DOI:10.1007/s13337-015-0247-y
   PubMedGoogle Scholar
• Kramvis A, Kew MC. Epidemiology of hepatitis B virus in Africa, its genotypes and clinical associations of genotypes. Hepatol Res. 2007 Jul;37(s1):S9–S19. PMID: 17627641. DOI:10.1111/j.1872-034X.2007.00098.x
   PubMedGoogle Scholar
• Olayinka AT, Oyemakinde A, Balogun MS, et al. Seroprevalence of hepatitis b infection in Nigeria: A national survey. Am J Trop Med Hyg. 2016 Oct 5;95(4):902–907. Epub 2016 Aug 15. PMID: 27527630; PMCID: PMC5062798. DOI:10.4269/ajtmh.15-0874
   PubMed Web of Science ®Google Scholar
• Krajden M, McNabb G, Petric M. The laboratory diagnosis of hepatitis B virus. Can J Infect Dis Med Microbiol. 2005 Mar;16(2):65–72. PMID: 18159530; PMCID: PMC2095015. DOI:10.1155/2005/450574
   PubMedGoogle Scholar
• Kwak MS, Kim YJ. Occult hepatitis B virus infection. WJH. 6(12): PMID: 25544873; PMCID: PMC4269905:860–869. 2014 Dec 27. DOI:10.4254/wjh.v6.i12.860
   Google Scholar
• Schaefer S. Hepatitis B virus taxonomy and hepatitis B virus genotypes world J. Gastroenterol. 2007. Jan 7;13(1):14–21. DOI:10.3748/wjg.v13.i1.14
   PubMed Web of Science ®Google Scholar
• Ganem D, Schneider R. Hepadnaviridae : the viruses and their replication. In: Howley P, editor knipe Dm. Fields Virology.Philadelphia: Lippincott-Raven; 2001. pp. 2923–2970.
   Google Scholar
• Utsumi T, Yano Y, Hotta H. Molecular epidemiology of hepatitis B virus in Asia. WJMG. 2014;4(2):19–26.
   Google Scholar
• Sunbul M. Hepatitis B virus genotypes: global distribution and clinical importance. World J Med Genetics. 2014;4(2):19–26.
   Google Scholar
• Norder H, Courance AM, Coursaget P, et al. Genetic Diversity of hepatitis b virus strains derived worldwide: Genotypes, subgenotypes, and HBsAg subtypes. Intervirology. 2004;47(6):289–309. DOI:10.1159/000080872
   PubMed Web of Science ®Google Scholar
• Kramvis A. Genotypes and genetic variability of hepatitis B virus. Intervirology. 2014;57(3–4):141–150. DOI:10.1159/000360947. Epub 2014 Jul 15. PMID: 25034481.
   PubMed Web of Science ®Google Scholar
• Cuestas ML, Mathet VL, Ruiz V, et al. Unusual naturally occurring humoral and cellular mutated epitopes of hepatitis B virus in a chronically infected argentine patient with anti-HBs antibodies. J Clin Microbiol. 2006 Jun;44(6):2191–2198. PMID: 16757620; PMCID: PMC1489447. DOI:10.1128/JCM.00057-06
   PubMed Web of Science ®Google Scholar
• Romanò L, Paladini S, Galli C, et al. Hepatitis B vaccination. Hepatitis B Vaccination Hum Vaccin Immunother. 2015;11(1):53–57. DOI:10.4161/hv.34306. Epub 2014 Nov 1. PMID: 25483515; PMCID: PMC4514213.
   PubMed Web of Science ®Google Scholar
• Yano Y, Azuma T, Hayashi Y. Variations and mutations in the hepatitis B virus genome and their associations with clinical characteristics. WJH. 2015;7(3):583–592.
   PubMedGoogle Scholar
• Salpini R, Colagrossi L, Bellocchi MC, et al. Hepatitis B surface antigen genetic elements critical for immune escape correlate with hepatitis B virus reactivation upon immunosuppression. Hepatology. 2015;61:823–833. CrossRef. DOI:10.1002/hep.27604
   PubMed Web of Science ®Google Scholar
• Zanetti AR, Tanzi E, Manzillo G, et al. Hepatitis B variant in Europe. Lancet. 1988;2(8620):1132–1133. DOI:10.1016/S0140-6736(88)90541-7.
   PubMed Web of Science ®Google Scholar
• Weber B. Genetic variability of the S gene of hepatitis B virus: Clinical and diagnostic impact. J Clin Virol. 2005;32(2):102–112.
   PubMed Web of Science ®Google Scholar
• Kreutz C. Molecular, immunological and clinical properties of mutated hepatitis B virus. J Cell Mol Med. 2022;6(1):113–143.
   Google Scholar
• Faleye TO, Adewumi OM, Ifeorah IM, et al. Detection and circulation of hepatitis B virus immune escape mutants among asymptomatic community dwellers in Ibadan, southwestern Nigeria. Int J Infect Dis. 2015;39:102–109. Epub 2015 Aug 14. PMID: 26283552. DOI:10.1016/j.ijid.2015.08.008
   PubMed Web of Science ®Google Scholar
• Adesina OA, Akanbi OA, Opaleye OO, et al. Detection of Q129H immune escape mutation in apparently healthy hepatitis B virus carriers in southwestern Nigeria. Viruses. 2021;1273(7):29. DOI:10.3390/v13071273. PMID: 34210073; PMCID: PMC8310067.
   Google Scholar
• Forbi JC, Vaughan G, Purdy MA, et al. Epidemic history and evolutionary dynamics of hepatitis b virus infection in two remote communities in rural Nigeria. PLoS ONE. 2011;5(7):e11615. DOI:10.1371/journal.pone.0011615
   Web of Science ®Google Scholar
• Faleye TOC, Adewumi MO, Ifeorah IM, et al. Detection of hepatitis B virus isolates with mutations associated with immune escape mutants among pregnant women in Ibadan, southwestern Nigeria. SpringerPlus. 2015;4(1):43. DOI:10.1186/s40064-015-0813-1
   PubMedGoogle Scholar
• Koyaweda GW, Ongus JR, Machuka E, et al. Detection of circulating hepatitis B virus immune escape and polymerase mutants among HBV-positive patients attending institut pasteur de Bangui, central African republic. Int J Infect Dis. 2020; Jan;90:138–144. DOI:10.1016/j.ijid.2019.10.039. Epub 2019 Nov 1. PMID: 31682960; PMCID: PMC6912157.
   PubMed Web of Science ®Google Scholar
• Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10(3):512–526.
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Li M, et al. Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–1549.
   PubMed Web of Science ®Google Scholar
• Letunic I, Bork P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2 July 2019;47(W1):W256–W259. DOI:10.1093/nar/gkz239
   PubMed Web of Science ®Google Scholar
• Forbi JC, Ben-Ayed Y, Xia GL, et al. Disparate distribution of hepatitis B virus genotypes in four sub-Saharan African countries. J Clin Virol. 2013 Sep;58(1):59–66. Epub 2013 Jul 17. PMID: 23871163; PMCID: PMC4591023. DOI:10.1016/j.jcv.2013.06.028
   PubMed Web of Science ®Google Scholar
• Velkov S, Protzer U, Michler T. Global occurrence of clinically relevant hepatitis B Virus variants as found by analysis of publicly available sequencing data. Viruses. 12(11): PMID: 33238650; PMCID: PMC7700573:1344. 2020 Nov 23. DOI:10.3390/v12111344
   PubMed Web of Science ®Google Scholar
• Schädler S, Hildt E. HBV life cycle: entry and morphogenesis. Viruses. 2009 Sep;1(2):185–209. Epub 2009 Sep 1. PMID: 21994545; PMCID: PMC3185491. DOI:10.3390/v1020185
   PubMed Web of Science ®Google Scholar
• Kedar Mukthinuthalapati VVP, Sewram V, Ndlovu N, et al. Hepatocellular carcinoma in Sub-Saharan Africa. JCO Glob Oncol. 2021 May;7(7):756–766. PMID: 34043413; PMCID: PMC8457845. DOI:10.1200/GO.20.00425
   PubMedGoogle Scholar
• Lazarevic I, Banko A, Miljanovic D, et al. Immune-escape hepatitis B virus mutations associated with viral reactivation upon Immunosuppression. Viruses. 11(9): PMID: 31450544; PMCID: PMC6784188:778. 2019 Aug 24. DOI:10.3390/v11090778
   PubMed Web of Science ®Google Scholar
• Elkady A, Iijima S, Aboulfotuh S, et al. Characteristics of escape mutations from occult hepatitis B virus infected patients with hematological malignancies in South Egypt. WJH. 9(9): PMID: 28396718; PMCID: PMC5368625:477–486. 2017 Mar 28. DOI:10.4254/wjh.v9.i9.477
   Google Scholar
• Locarnini S. Molecular virology of hepatitis B virus. Semin Liver Dis. 2004;24:3–10. DOI:10.1055/s-2004-828672. [PubMed Google Scholar].
   PubMed Web of Science ®Google Scholar
• Mathet VL, Feld M, Espínola L, et al. 69.Hepatitis B virus S gene mutants in a patient with chronic active hepatitis with circulating anti-HBs antibodies. J Med Virol. 2003;69(1):18–26. PubMed] [Google Scholar. DOI:10.1002/jmv.10267
   PubMed Web of Science ®Google Scholar
• Thakur V, Kazim SN, Guptan RC, et al. 70.Transmission of G145R mutant of HBV to an unrelated contact. J Med Virol. 2005;76(1):40–46. PubMed] [Google Scholar. DOI:10.1002/jmv.20321
   PubMed Web of Science ®Google Scholar
• Carman WF, Zanetti AR, Karayiannis P, et al. Vaccine induced escape mutants of hepatitis B virus. Lancet. 1990;336:325–329.
   PubMed Web of Science ®Google Scholar
• Zhang JM, Xu Y, Wang XY, et al. Co-existence of hepatitis B surface antigen (HBsAg) and heterologous subtype specific antibodies to HBsAg among patients with chronic hepatitis B virus infection. Clin Infect Dis. 2007;44(9):1161–1169.
   PubMed Web of Science ®Google Scholar
• Aydin N, Kirdar S, Uzun N, et al. Atypical serological profiles in hepatitis B infections: investigations of S gene mutations in cases with concurrently positive for HBsAg and anti-HBs. Mikrobiyoloji bulteni. 2016;50(4):533–543.
   Web of Science ®Google Scholar
• Ponde RA. Atypical Serological Profiles in Hepatitis B virus infection. Er J Clin Microbiol Inf Dis. 2013;32(4):461–476.
   PubMed Web of Science ®Google Scholar
• Tedder RS, Wilson Croome R. IgM antibody response to the hepatitis B core antigen in acute and chronic hepatitis B. J Hyg. 1981;86(2):163–173.
   PubMedGoogle Scholar
• Konerman MA, Lok AS. Epidemiology, Diagnosis and Natural History of Hepatitis B. Lok in zakim and boyer’s hepatology. 7th ed. Amsterdam, Netherlands: Elsevier; 2018.
   Google Scholar
• Lesi OA, Audu RA, Okwuraiwe AP, et al. Serological and virological markers of nigerian patients with hepatitis B infection. Niger J Clin Pract. 2019 Apr;22(4):534–538. PMID: 30975959. DOI:10.4103/njcp.njcp_273_17
   PubMed Web of Science ®Google Scholar
• Forbi JC, Iperepolu OH, Zungwe T, et al. Prevalence of hepatitis B e antigen in chronic HBV carriers in North-central Nigeria. J Health Popul Nutr. 2012 Dec;30(4):377–382. PMID: 23304903; PMCID: PMC3763608. DOI:10.3329/jhpn.v30i4.13289
   PubMed Web of Science ®Google Scholar
• Anaedobe CG, Fowotade A, Omoruyi CE, et al. Prevalence, sociodemographic features and risk factors of hepatitis B virus infection among pregnant women in Southwestern Nigeria. Pan Afr Med J. 20 PMID: 26301010; PMCID: PMC4524914 2015 Apr 24: 406. DOI:10.11604/pamj.2015.20.406.6206
   PubMedGoogle Scholar
• Miller RH, Robinson WS. Integrated hepatitis B virus DNA sequences specifying the major viral core polypeptide are methylated in PLC/PRF/5 cells. Proc Natl Acad Sci U S A. 1983 May;80(9):2534–2538. PMID: 6302693; PMCID: PMC393860. DOI:10.1073/pnas.80.9.2534
   PubMed Web of Science ®Google Scholar
• Vivekanandan P, Thomas D, Torbenson M. Hepatitis B viral DNA is methylated in liver tissues. J Viral Hepat. 2008 Feb;15(2):103–107. PMID: 18184192. DOI:10.1111/j.1365-2893.2007.00905.x
   PubMed Web of Science ®Google Scholar
• Raimondo G, Burk RD, Lieberman HM, et al. Interrupted replication of hepatitis B virus in liver tissue of HBsAg carriers with hepatocellular carcinoma. Virology. 1988 Sep;166(1):103–112. PMID: 2842938. DOI:10.1016/0042-6822(88)90151-1
   PubMed Web of Science ®Google Scholar
• Coleman PF. Detecting hepatitis B surface antigen mutants. Emerg Infect Dis. 2006 Feb;12(2):198–203. PMID: 16494742; PMCID: PMC3293431. DOI:10.3201/eid1203.050038
   PubMed Web of Science ®Google Scholar
• Araujo NM, Teles SA, Spitz N. Spitz comprehensive analysis of clinically significant hepatitis B virus mutations in relation to genotype, subgenotype and geographic region. Front Microbiol. 2020;11. DOI:10.3389/fmicb.2020.616023
   Web of Science ®Google Scholar
• Lello D, A F, Ridruejo E, et al. Molecular epidemiology of hepatitis B virus mutants associated with vaccine escape, drug resistance and diagnosis failure. J Viral Hepat. 2019;26(5):552–560.
   PubMed Web of Science ®Google Scholar
• Yan B, Lu J, Feng Y, et al. Temporal trend of hepatitis B surface mutations in the post-immunization period: 9 years of surveillance (2005–2013) in eastern China. Sci Rep. 2017;7(1):6669. DOI:10.1038/s41598-017-07085-z
   PubMedGoogle Scholar
• Ma Q, Wang Y. Comprehensive analysis of the prevalence of hepatitis B virus escape mutations in the major hydrophilic region of surface antigen. J Med Virol. 2012;84(2):198–206.
   PubMed Web of Science ®Google Scholar
• Kay A, Zoulim F. Hepatitis B virus genetic variability and evolution. Virus Res. 2007;127(2):164–176.
   PubMedGoogle Scholar
• Echevarría JM, Avellón A. Hepatitis B virus genetic diversity. J Med Virol. 2006;78(S1):S36–S42. DOI:10.1002/jmv.20605. [PubMed] [CrossRef] [Google Scholar] [Ref list].
   PubMedGoogle Scholar
• Purdy MA. Hepatitis B virus S gene escape mutants. Asian J Transfus Sci. 2007 Jul;1(2):62–70. PMID: 21938236; PMCID: PMC3168123. DOI:10.4103/0973-6247.33445
   PubMedGoogle Scholar
• Chen WN, Oon CJ. Mutation “hot spot” in HLA class I-restricted T cell epitope on hepatitis B surface antigen in chronic carriers and hepatocellular carcinoma. Biochem Biophys Res Commun. 1999;262(3):757–761.
   PubMed Web of Science ®Google Scholar
• Oon CJ, Chen WN. Current aspects of hepatitis B surface antigen mutants in Singapore. J Viral Hepat. 1998;5(s2):17–23.
   PubMedGoogle Scholar
• Hsu HY, Chang MH, Liaw SH, et al. Changes of hepatitis B surface antigen variants in carrier children before and after universal vaccination in Taiwan. Hepatology. 1999;30:1312–1317.
   PubMed Web of Science ®Google Scholar
• Sureau C, Salisse J. A conformational heparan sulfate binding site essential to infectivity overlaps with the conserved hepatitis B virus a-determinant. Hepatology. 2013;57(3):985–994.
   PubMed Web of Science ®Google Scholar
• Rezaee R, Poorebrahim M, Najafi S, et al. Impacts of the G145R mutation on the structure and immunogenic activity of the hepatitis B surface antigen: A computational analysis. Hepat Mon. 2016;16(7):e39097.
   PubMed Web of Science ®Google Scholar
• Colson P, Borentain P, Coso D, et al. Hepatitis B virus reactivation in HBsAg-negative patients is associated with emergence of viral strains with mutated HBsAg and reverse transcriptase. Virology. 2015;484:354–463. Google Scholar] [CrossRef. DOI:10.1016/j.virol.2015.06.017
   PubMed Web of Science ®Google Scholar
• Inoue J, Kondo Y, Wakui Y, et al. Reactivation of resolved hepatitis B virus infection with immune escape mutations after long-term corticosteroid therapy. Clin J Gastroenterol. 2016;9(2):93–98.
   PubMedGoogle Scholar
• Yang JX, Liu BM, Li XG, et al. Profile of HBV antiviral resistance mutations with distinct evolutionary pathways against nucleoside/nucleotide analogue treatment among Chinese chronic hepatitis B patients. Antivir Ther. 2010;15(8):1171–1178. PMID: 21149924. DOI:10.3851/IMP1677
   PubMed Web of Science ®Google Scholar
• Lazarevic I. Clinical implications of hepatitis B virus mutations: recent advances. WJG. 2814;20(24):7653–7664. [PMC free article] [PubMed] [CrossRef] [Google Scholar] [Ref list]. DOI:10.3748/wjg.v20.i24.7653
   Google Scholar
• Lok AS, Zoulim F, Locarnini S, et al.Antiviral drug-resistant HBV: standardization of nomenclature and assays and recommendations for management. Hepatology. 2007; Jul;46(1):254–265. PMID: 17596850. DOI:10.1002/hep.21698
   PubMed Web of Science ®Google Scholar
• Liu BM, Li T, Xu J, et al. Characterization of potential antiviral resistance mutations in hepatitis B virus reverse transcriptase sequences in treatment-naïve Chinese patients. Antiviral Res. 2010 Mar;85(3):512–519. Epub 2009 Dec 23. PMID: 20034521. DOI:10.1016/j.antiviral.2009.12.006
   PubMed Web of Science ®Google Scholar
• Deng L, Tang H. Hepatitis B virus drug resistance to current nucleos(t)ide analogs: Mechanisms and mutation sites. Hepatol Res. 2011;41(11):1017–1024.
   PubMed Web of Science ®Google Scholar
• Harris BJ, Holzmayer V, Qureshi H, et al. Hepatitis B genotypes and surface antigen mutants present in Pakistani blood donors. PLoS ONE. 2017 Jun 5;12(6):e0178988. PMID: 28582431; PMCID: PMC5459465. DOI:10.1371/journal.pone.0178988
   PubMed Web of Science ®Google Scholar
• Archampong TN, Boyce CL, Lartey M, et al. HBV genotypes and drug resistance mutation in anti-retroviral treatment naïve and treatment experienced HBV-HIV-Co-infected patients. Antivir Ther. 2017;22(1):13–20.
   PubMed Web of Science ®Google Scholar
• Arrese E, Basaras M, Blanco S, et al. Evolution of hepatitis B virus during long-term therapy in patients with chronic hepatitis B. Ann Hepatol. 2011 Oct-Dec;10(4):434–440.
   PubMed Web of Science ®Google Scholar
• Mokaya J, Vasylyeva TI, Barnes E, et al. Global prevalence and phylogeny of hepatitis B virus (HBV) drug and vaccine resistance mutations. J Viral Hepat. 2021 Aug;28(8):1110–1120. Epub 2021 May 7. PMID: 33893696; PMCID: PMC8581767. DOI:10.1111/jvh.13525
   PubMed Web of Science ®Google Scholar
• Andernach IE, Hübschen JM, Muller CP. Hepatitis B virus: the genotype E puzzle. Rev Med Virol. 2009 Jul;19(4):231–240. PMID: 19475565. DOI:10.1002/rmv.618
   PubMed Web of Science ®Google Scholar
• Forbi JC, Vaughan G, Purdy MA, et al. Epidemic history and evolutionary dynamics of hepatitis b virus infection in two remote communities in rural Nigeria. PLoS ONE. 2010 Jul 19;5(7):e11615. PMID: 20657838; PMCID: PMC2906510. DOI:10.1371/journal.pone.0011615
   PubMed Web of Science ®Google Scholar
• Andernach IE, Nolte C, Pape JW, et al. Slave trade and hepatitis B virus genotypes and subgenotypes in Haiti and Africa. Emerg Infect Dis. 2009 Aug;15(8):1222–1228. PMID: 19751583; PMCID: PMC3467954. DOI:10.3201/eid1508.081642
   PubMed Web of Science ®Google Scholar
• Central Intelligence Agency. 2022.[cited August16 2022]. World factbook. https://www.cia.gov/library/publications/the-world-factbook/index.html
   Google Scholar
• Ampah KA, Pinho-Nascimento CA, Kerber S, et al. Limited genetic diversity of hepatitis b virus in the general population of the offin river valley in Ghana. PLoS ONE. 2016;11(6):e0156864. [PMC free article] [PubMed] [Google Scholar] [Ref list]. DOI:10.1371/journal.pone.0156864
   PubMed Web of Science ®Google Scholar
• Lago BV, Mello FC, Ribas FS, et al. Analysis of complete nucleotide sequences of angolan hepatitis B virus isolates reveals the existence of a separate lineage within genotype E. PLoS ONE. 2014;9(3):e92223. [PMC free article] [PubMed] [Google Scholar] [Ref list]. DOI:10.1371/journal.pone.0092223
   PubMed Web of Science ®Google Scholar