Abstract
Upon phylogenetic analysis of a partial S gene sequence [396 nucleotides (nt)], 928 hepatitis B virus (HBV) strains obtained from 899 viremic subjects in 28 major cities on 15 islands of Indonesia in 1989–2007 segregated into four HBV genotypes. Genotype B was predominant (66%), followed by genotype C (26%), genotype D (7%), and genotype A (0.8%). Comparative and phylogenetic analyses of the 396-nt S gene sequence of 928 HBV isolates and whole genomic sequences of 25 selected HBV isolates revealed a total of 14 subgenotypes within genotypes A–D: two (A1 and A2) in genotype A (HBV/A), five (B2, B3, B5, B7, and a novel subgenotype, tentatively designated B8) in HBV/B, five (C1, C2, C5, C6, and another novel subgenotype, C7) in HBV/C, and two (D1 and D3) in HBV/D. The distribution of HBV genotypes/subgenotypes, including B8 and C7, seems to be associated with ethnological origins in Indonesia.
Similar content being viewed by others
References
Achwan WA, Muttaqin Z, Zakaria E, Depamede SA, Mulyanto Sumoharjo S, Tsuda F, Takahashi K, Abe N, Mishiro S (2007) Epidemiology of hepatitis B, C, and E viruses and human immunodeficiency virus infections in Tahuna, Sangihe-Talaud Archipelago, Indonesia. Intervirology 50:408–411
Arauz-Ruiz P, Norder H, Visoná KA, Magnius LO (1997) Molecular epidemiology of hepatitis B virus in Central America reflected in the genetic variability of the small S gene. J Infect Dis 176:851–858
Arauz-Ruiz P, Norder H, Robertson BH, Magnius LO (2002) Genotype H: a new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 83:2059–2073
Bancroft WH, Mundon FK, Russell PK (1972) Detection of additional antigenic determinants of hepatitis B antigen. J Immunol 109:842–848
Bellwood P (1997) Prehistory of the Indo-Malaysian Archipelago, 2nd edn. University of Hawaii Press, Honolulu
Brandes JLA (1884) Contribution of the lexicon comparison to the western part of Malaysian-Polynesian Language Family. PhD Thesis, University of Utrecht, Utrecht, The Netherland (in Dutch)
Couroucé-Pauty AM, Plançon A, Soulier JP (1983) Distribution of HBsAg subtypes in the world. Vox Sang 44:197–211
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Hannoun C, Norder H, Lindh M (2006) An aberrant genotype revealed in recombinant hepatitis B virus strains from Vietnam. J Gen Virol 81:2267–2272
Horikita M, Itoh S, Yamamoto K, Shibayama T, Tsuda F, Okamoto H (1994) Differences in the entire nucleotide sequence between hepatitis B virus genomes from carriers positive for antibody to hepatitis B e antigen with and without active disease. J Med Virol 44:96–103
Ina Y (1994) ODEN: a program package for molecular evolutionary analysis and database search of DNA and amino acid sequences. Comput Appl Biosci 10:11–12
Inoue J, Takahashi M, Nishizawa T, Narantuya L, Sakuma M, Kagawa Y, Shimosegawa T, Okamoto H (2005) High prevalence of hepatitis delta virus infection detectable by enzyme immunoassay among apparently healthy individuals in Mongolia. J Med Virol 76:333–340
Khan M, Dong JJ, Acharya SK, Dhagwahdorj Y, Abbas Z, Jafri SMW, Mulyono DH, Tozun N, Sarin SK (2004) Hepatology issues in Asia: perspectives from regional leaders. J Gastroenterol Hepatol 19:S419–S430
Kramvis A, Kew M, François G (2005) Hepatitis B virus genotypes. Vaccine 23:2409–2423
Kramvis A, Arakawa K, Yu MC, Nogueira R, Stram DO, Kew MC (2008) Relationship of serological subtype, basic core promoter and precore mutations to genotypes/subgenotypes of hepatitis B virus. J Med Virol 80:27–46
Le Bouvier GL (1971) The heterogeneity of Australia antigen. J Infect Dis 123:671–675
Lee WM (1997) Hepatitis B virus infection. N Engl J Med 337:1733–1745
Lusida MI, Surayah, Sakugawa H, Nagano-Fujii M, Soetjipto, Mulyanto, Handajani R, Boediwarsono, Setiawan PB, Nidom CA, Ohgimoto S, Hotta H (2003) Genotype and subtype analysis of hepatitis B virus (HBV) and possible co-infection of HBV and hepatitis C virus (HCV) or hepatitis D virus (HDV) in blood donors, patients with chronic liver disease patients on hemodialysis in Surabaya, Indonesia. Microbiol Immunol 47:969–975
Lusida MI, Nugrahaputra VE, Soetjipto, Handajani R, Nagano-Fujii M, Sasayama T, Utsumi T, Hotta H (2008) Novel subgenotypes of hepatitis B virus genotypes C and D in Papua, Indonesia. J Clin Microbiol 46:2160–2166
Mazzur S, Bastiaans MJ, Nath N (1981) Hepatitis B virus (HBV) infection among children and adults in the Solomon Islands. Am J Epidemiol 113:510–519
Mulyanto, Tsuda F, Karossi AT, Soewignyo S, Roestamsjah, Sumarsidi D, Trisnamurti RH, Sumardi, Surayah K, Udin LZ, Melani-Wikanta, Kanai K, Mishiro S (1997) Distribution of the Hepatitis B surface antigen subtypes in Indonesia: implications for ethnic heterogeneity and infection control measures. Arch Virol 142:2121–2129
Mulyanto, Surayah K, Depamede SN, Lestarini IA, Budianto W, Hafiludin, Umi K, Tsuda F, Takahashi M, Okamoto H (2008) Hepatitis B virus infection in Eastern part of Indonesia. Abstract book of the second China–Indonesia joint international symposium on hepatobiliary medicine and surgery, Chongqing, China
Nishioka K (1984) Predominant mode of transmission of hepatitis B virus: perinatal transmission in Asia. In: Vyas GN, Dienstag JL, Hoofnagle JB (eds) Viral hepatitis and liver disease. Grune & Stratton, Orlando, pp 423–432
Norder H, Couroucé AM, Magnius LO (1994) Complete genomes, phylogenetic relatedness, and structural proteins of six strains of the hepatitis B virus, four of which represent two new genotypes. Virology 198:489–503
Norder H, Couroucé AM, Coursaget P, Echevarria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LO (2004) Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes. Intervirology 47:289–309
Nurainy N, Muljono DH, Sudoyo H, Marzuki S (2008) Genetic study of hepatitis B virus in Indonesia reveals a new subgenotype of genotype B in east Nusa Tenggara. Arch Virol 153:1057–1065
Okamoto H, Imai M, Tsuda F, Tanaka T, Miyakawa Y, Mayumi M (1987) Point mutation in the S gene of hepatitis B virus for a d/y or w/r subtypic change in two blood donors carrying a surface antigen of compound subtype adyr or adwr. J Virol 61:3030–3034
Okamoto H, Imai M, Miyakawa Y, Mayumi M (1987) Site-directed mutagenesis of hepatitis B surface antigen sequence at codon 160 from arginine to lysine for conversion of subtypic determinant from r to w. Biochem Biophys Res Commun 148:500–504
Okamoto H, Tsuda F, Sakugawa H, Sastrosoewignjo RI, Imai M, Miyakawa Y, Mayumi M (1988) Typing hepatitis B virus by homology in nucleotide sequence: comparison of surface antigen subtypes. J Gen Virol 69:2575–2583
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sakamoto S, Tanaka Y, Orito E, Co J, Clavio J, Ito K, Ozasa A, Quino A, Ueda R, Sollano J, Mizokami M (2006) Novel subtypes (subgenotypes) of hepatitis B virus genotypes B and C among chronic liver disease patients in the Philippines. J Gen Virol 87:1873–1882
Sakamoto T, Tanaka Y, Simonetti J, Osiowy C, Borresen ML, Koch A, Kurbanov F, Sugiyama M, Minuk GY, McMahon BJ, Joh T, Mizokami M (2007) Classification of hepatitis B virus genotype B into 2 major types based on characterization of a novel subgenotype in Arctic indigenous populations. J Infect Dis 196:1487–1492
Sastrosoewignjo RI, Sandjaja B, Okamoto H (1991) Molecular epidemiology of hepatitis B virus in Indonesia. J Gastroenterol Hepatol 6:491–498
Shibayama T, Masuda G, Ajisawa A, Hiruma K, Tsuda F, Nishizawa T, Takahashi M, Okamoto H (2005) Characterization of seven genotypes (A to E, G and H) of hepatitis B virus recovered from Japanese patients infected with human immunodeficiency virus type 1. J Med Virol 76:24–32
Stuyver L, De Gendt S, Van Geyt C, Zoulim F, Fried M, Schinazi RF, Rossau R (2000) A new genotype of hepatitis B virus: complete genome and phylogenetic relatedness. J Gen Virol 81:67–74
Sugauchi F, Mizokami M, Orito E, Ohno T, Kato H, Suzuki S, Kimura Y, Ueda R, Butterworth LA, Cooksley WG (2001) A novel variant genotype C of hepatitis B virus identified in isolates from Australian Aborigines: complete genome sequence and phylogenetic relatedness. J Gen Virol 82:883–892
Sugono D (2008) The mapping of languages in Indonesia. Language Center Press, Jakarta, p 7
Summer Institute of Linguistics (2006) Languages in Indonesia. SIL, Jakarta
Takahashi M, Nishizawa T, Gotanda Y, Tsuda F, Komatsu F, Kawabata T, Hasegawa K, Altankhuu M, Chimedregzen U, Narantuya L, Hoshino H, Hino K, Kagawa Y, Okamoto H (2004) High prevalence of antibodies to hepatitis A and E viruses and viremia of hepatitis B, C, and D viruses among apparently healthy populations in Mongolia. Clin Diagn Lab Immunol 11:392–398
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Wang Z, Huang Y, Wen S, Zhou B, Hou J (2007) Hepatitis B virus genotypes and subgenotypes in China. Hepatol Res 37(s1):S36–S41
Acknowledgments
This study was supported in part by a grant from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The authors are grateful to Dr. Patiiha and Dr. Achwan WA as well as all of the people who helped us to collect blood samples for their invaluable contributions.
Author information
Authors and Affiliations
Corresponding author
Additional information
The nucleotide sequence data reported in this study have been assigned DDBJ/EMBL/GenBank accession numbers AP011084–AP011108 for 25 entire HBV genomes and AB466339–AB467266 for 928 partial HBV sequences.
Rights and permissions
About this article
Cite this article
Mulyanto, Depamede, S.N., Surayah, K. et al. A nationwide molecular epidemiological study on hepatitis B virus in Indonesia: identification of two novel subgenotypes, B8 and C7. Arch Virol 154, 1047–1059 (2009). https://doi.org/10.1007/s00705-009-0406-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-009-0406-9