• 1.

    Suwignyo S, 1996. Seroepidemiology of hepatitis B and C in Indonesia. Int Hepatol Commun 5: 3037.

  • 2.

    Khan M, Dong JJ, Acharya SK, Dhagwardorj Y, Abbas Z, Jafri W, Mulyono DH, Tozun N, Sarin SK, 2004. Hepatology issues in Asia: perspective from regional leaders. J Gastroenterol Hepatol 19: S419S430.

    • Search Google Scholar
    • Export Citation
  • 3.

    Creati M, Saleh A, Ruff TA, Stewart T, Otto B, Sutanto A, Clements CJ, 2007. Implementing the birth dose of hepatitis B vaccine in rural Indonesia. Vaccine 25: 59855993.

    • Search Google Scholar
    • Export Citation
  • 4.

    World Health Organization, Regional Office for Southeast Asia, 2013. Regional Strategy for the Prevention and Control of Viral Hepatitis. Available at: http://www.searo.who.int/entity/emerging_diseases/topics/CD_282.pdf. Accessed March 16, 2015.

    • Search Google Scholar
    • Export Citation
  • 5.

    National Institute of Health Research and Development, Ministry of Health of the Republic Indonesia, 2008. Report on National Basic Health Research 2007. Available at: http://terbitan.litbang.depkes.go.id/penerbitan/index.php/blp/catalog/book/22. Accessed August 10, 2013.

    • Search Google Scholar
    • Export Citation
  • 6.

    Carman WF, 1997. The clinical significance of surface antigen variants of hepatitis B virus. J Viral Hep 4: 11S20S.

  • 7.

    Yamamoto K, Horikita M, Tsuda F, Itoh K, Akahane Y, Yotsumoto S, Okamoto H, Mikakawa Y, Mayumi M, 1994. Naturally occurring escape mutants of hepatitis B virus with various mutations in the S gene in carriers seropositive for antibody to hepatitis B surface antigen. J Virol 68: 26712676.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hsu HY, Chang MH, Ni YH, Chen HL, 2004. Survey of hepatitis B surface variant infection in children 15 years after a nationwide vaccination programe in Taiwan. Gut 53: 14991503.

    • Search Google Scholar
    • Export Citation
  • 9.

    Okamoto H, Tsuda F, Sakugawa H, Satrosoewignjo 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: 25752583.

    • Search Google Scholar
    • Export Citation
  • 10.

    Kramvis A, Kew M, Francois G, 2005. Hepatitis B genotypes. Vaccine 23: 24092423.

  • 11.

    Seeger C, Zoulim F, Mason WS, 2013. Hepadnaviruses. Knipe DM, Howley PM, eds. Fields Virology, 6th edition. Philadelphia, PA: Lippincott, Williams and Wilkins, 21852221.

    • Search Google Scholar
    • Export Citation
  • 12.

    Tatematsu K, Tanaka Y, Kurbanov F, Sagauchi F, Mano S, Maeshiro T, Nakayoshi T, Wakuta M, Miyakawa Y, Mizokami M, 2009. A genetic variant of hepatitis B virus divergent from known human and ape genotypes isolated from a Japanese patient and provisionally assigned to new genotype J. J Virol 83: 1053810547.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lusida MI, Nugrahaputra VE, Soetjipto, Handayani R, Naganofujii M, Sasayama M, Utsumi T, Hotta H, 2008. Novel subgentypes of hepatitis B virus genotype C and D in Papua, Indonesia. J Clin Microbiol 46: 21602166.

    • Search Google Scholar
    • Export Citation
  • 14.

    Utsumi T, Yano Y, Lusida MI, Amin M, Soetjipto, Hotta H, Hayashi Y, 2010. Serologic and molecular characteristics of hepatitis B virus among school children in East Java, Indonesia. Am J Trop Med Hyg 83: 189193.

    • Search Google Scholar
    • Export Citation
  • 15.

    Mulyanto, Depamede SN, Surayah K, Tsuda F, Ichiyama K, Takahashi M, Okamoto H, 2009. A nationwide molecular epidemiological study on hepatitis B virus in Indonesia: identification of two novel subgenotypes, B8, C7. Arch Virol 154: 10471059.

    • Search Google Scholar
    • Export Citation
  • 16.

    Juniastuti, Lusida MI, Nugrahaputra VE, Amin M, Utsumi T, Hayashi Y, Hotta H, 2011. Another novel subgenotype of hepatitis B virus genotype C from Papuans of Highland origin. J Med Virol 83: 225234.

    • Search Google Scholar
    • Export Citation
  • 17.

    Magnius LO, Norder H, 1995. Subtype, genotype and molecular epidemiology of the hepatitis B virus as reflected by sequence variability of the S gene. Intervirology 38: 2434.

    • Search Google Scholar
    • Export Citation
  • 18.

    Norder H, Courouce AM, Coursaget P, Echevaria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LO, 2004. Genetic diversity of hepatitis B virus strains derived worldwide: genotype, subgenotypes, HBsAg subtypes. Intervirology 47: 289309.

    • Search Google Scholar
    • Export Citation
  • 19.

    Purdy MA, Talekar G, Swenson P, Araujo A, Fields H, 2007. A new algorithm for deduction of hepatitis B surface antigen subtype determinants from the amino acid sequence. Intervirology 50: 4551.

    • Search Google Scholar
    • Export Citation
  • 20.

    Mulyanto, Tsuda F, Karossi AT, Soewignyo S, Roestamsjah, Sumarsidi D, Trisnamurti RH, Sumardi, Surayah, Udin LZ, Wikanta M, Kanai K, Mishiro S, 1997. Distribution of the hepatitis B virus in Indonesia: implication for heterogeneity and infection control measures. Arch Virol 142: 21212129.

    • Search Google Scholar
    • Export Citation
  • 21.

    Zuckerman AJ, Zuckeman JN, 1999. Molecular epidemiology of hepatitis B virus mutant. J Med Virol 58: 193195.

  • 22.

    Zuckerman AJ, 2000. Effect of hepatitis B virus mutants on efficacy of vaccination. Lancet 355: 13821384.

  • 23.

    Francois G, Kew M, van Damme P, Mphahlele MJ, Mehews A, 2001. Mutant hepatitis B viruses: a matter of academic interest only or a problem with far reaching implications? Vaccine 19: 37993815.

    • Search Google Scholar
    • Export Citation
  • 24.

    Arauz-Ruiz P, Norder H, Visona 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: 851858.

    • Search Google Scholar
    • Export Citation
  • 25.

    Norder H, Courouce AM, Magnius LO, 1994. Complete genome, phylogenetic relatedness and structural protein of six strains of hepatitis B virus, four of which represent two new genotypes. Virology 198: 489503.

    • Search Google Scholar
    • Export Citation
  • 26.

    Nelson CM, Wibisono H, Purwanto H, Mansyur I, Moniaga V, Widjaya A, 2004. Hepatitis B vaccine freezing in Indonesia cold chain: evidence and solutions. Bull World Health Organ 82: 99105.

    • Search Google Scholar
    • Export Citation
  • 27.

    Levin CE, Nelson CM, Widjaya A, Moniaga V, Anwar C, 2004. The costs of home delivery of a birth dose of hepatitis B vaccine in prefilled syringe in Indonesia. Bull World Health Organ 83: 456461.

    • Search Google Scholar
    • Export Citation
  • 28.

    Clements CJ, Baoping Y, Crouch A, Hipgrave D, Mansoor O, Nelson CB, Treleaven S, Konkelenberg RV, Wirsma S, 2006. Progress in the control of hepatitis B infection in the Western Pacific Region. Vaccine 24: 19751982.

    • Search Google Scholar
    • Export Citation
  • 29.

    Ruff TA, Gertig D, Otto BF, Gust ID, Sutanto A, Soewarso TI, Kandun N, Marschner IC, Maynard JE, 1995. Lombok hepatitis B model immunization project: toward universal infant hepatitis B immunization in Indonesia. J Infect Dis 171: 290296.

    • Search Google Scholar
    • Export Citation
  • 30.

    Chan CY, Lee SD, Lo KJ, 2004. Legend of hepatitis B vaccination: the Taiwan experience. J Gastroenterol Hepatol 19: 121126.

  • 31.

    Chen DS, 2009. Hepatitis B vaccination: the key towards elimination and eradication of Hepatitis B. J Hepatol 50: 805816.

  • 32.

    Hipgrave DB, Maynard JE, Beverley AB, 2006. Improving birth dose coverage of hepatitis B vaccine. Bull World Health Organ 84: 6571.

  • 33.

    Greenberg DP, 1993. Pediatric experience with recombinant hepatitis B vaccine in infants and relevant safety and immunogenicity studies. Pediatr Infect Dis J 12: 438445.

    • Search Google Scholar
    • Export Citation
  • 34.

    Otto BF, Suarnawa IM, Stewart T, Nelson C, Ruff TA, Widjaya A, Maynard JE, 2000. At birth immunization against hepatitis B using novel pre-filled immunization device stored outside the cold chain. Vaccine 18: 498502.

    • Search Google Scholar
    • Export Citation
  • 35.

    Cui F, Li L, Hadler SC, Wang F, Zheng H, Chen Y, Gong X, Hutin YJ, Cairns KL, Liang X, Yang W, 2010. Factors associated with effectiveness of the first dose of vaccine in China: 1992–2005. Vaccine 28: 59735978.

    • Search Google Scholar
    • Export Citation
  • 36.

    Ministry of Health of the Republic Indonesia, 2004. National Guideline of Vaccination Implementation. Available at: http://www.hukor.depkes.go.id. Accessed August 20, 2012.

    • Search Google Scholar
    • Export Citation
  • 37.

    World Health Organization, 2013. Global Policy Report on the Prevention and Control of Viral Hepatitis. Available at: http://www.who.int/csr/disease/hepatitis/global_report/en/. Accessed March 16, 2015.

    • Search Google Scholar
    • Export Citation
  • 38.

    National Center for Statistics of the Republic Indonesia, 2010. Life Time Migration: 1971–2010. Available at: http://www.bps.go.id/linkTableDinamis/view/id/855. Accessed October 27, 2015.

    • Search Google Scholar
    • Export Citation
  • 39.

    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: 20592073.

    • Search Google Scholar
    • Export Citation
  • 40.

    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 the two blood donors carrying a surface antigen of compound subtype adyr or adwr. J Virol 61: 30303034.

    • Search Google Scholar
    • Export Citation
  • 41.

    Norder H, Courouce AM, Magnius LO, 1992. Molecular basis of hepatitis B virus serotype variations within the four major subtypes. J Gen Virol 73: 31413145.

    • Search Google Scholar
    • Export Citation
  • 42.

    Waters JA, O'Rourke SM, Richardson SC, Papavengelou G, Thomas HC, 1987. Quantitative analysis of the humoral immune response to the “a” determinant of HBs antigen after inoculation with plasma derived or recombinant vaccine. J Med Virol 21: 155160.

    • Search Google Scholar
    • Export Citation
  • 43.

    Carman WF, Van Deursen FJ, Mimms LT, Hardie D, Coppola R, Decker R, Sanders R, 1997. The prevalence of surface antigen variants of hepatitis B virus in Papua New Guinea, South Africa and Sardinia. Hepatology 26: 16581666.

    • Search Google Scholar
    • Export Citation
  • 44.

    Carman WF, Zanetti AR, Karayiannis P, Waters J, Manzillo G, Tanzi E, Zuckerman AJ, Thomas HC, 1990. Vaccine induced escape mutant of hepatitis B virus. Lancet 336: 325329.

    • Search Google Scholar
    • Export Citation
  • 45.

    Coleman PF, 2006. Detecting hepatitis B surface antigen mutants. Emerg Infect Dis 12: 198203.

  • 46.

    Horvat RT, 2011. Diagnostic and clinical relevance of HBV mutations. LabMedicine 42: 488496.

  • 47.

    Hsu HY, Chang MH, Liaw SH, Ni YH, Chen HL, 1999. Changes of hepatitis B surface antigen variants in carrier children before and after vaccination in Taiwan. Hepatology 30: 13121317.

    • Search Google Scholar
    • Export Citation
  • 48.

    Gerin JL, Alexander H, Shih JW, Purcell RH, Dapolito G, Engle R, Green N, Sutcliffe JG, Shinnick TM, Lerner RA, 1983. Chemically synthesized peptides of hepatitis B surface antigen duplicate the d/y specificities and induced subtype-specific antibodies in chimpanzees. Proc Natl Acad Sci USA 80: 23652369.

    • Search Google Scholar
    • Export Citation
  • 49.

    Song BC, Kim SH, Kim H, Ying YH, Kim HJ, Kim YJ, Yoon JH, Lee HS, Cha CY, Kook YH, Kim BJ, 2005. Prevalence of naturally occurring surface antigen variants of hepatitis B virus in Korea patients infected chronically. J Med Virol 76: 194202.

    • Search Google Scholar
    • Export Citation
  • 50.

    Thedja MD, Roni M, Harahap AR, Siregar NC, Ie SI, Muljono DH, 2010. Occult hepatitis B in blood donors in Indonesia: altered antigenicity of the hepatitis B virus surface protein. Hepatol Int 4: 608614.

    • Search Google Scholar
    • Export Citation
  • 51.

    Utsumi T, Lusida MI, Yano Y, Purwono PB, Amin M, Soetjipto, Hotta H, Hayashi Y, 2014. Progress in the control of hepatitis B virus infection among children in Indonesia. J Vaccines Vaccin 5: 247.

    • Search Google Scholar
    • Export Citation
  • 52.

    Ie SI, Thedja MD, Roni M, Muljono DH, 2010. Prediction of conformational changes by single mutation in the hepatitis B virus surface antigen (HBsAg) identified in HBsAg-negative blood donors. Virol J 7: 326.

    • Search Google Scholar
    • Export Citation
  • 53.

    Scheiblauer H, El Nageh M, Diaz S, Nick S, Zeichhardt H, Grunert HP, Prince A, 2010. Performance evaluation of 70 hepatitis B virus (HBV) surface antigen (HBsAg) assays from around the world by a geographically diverse panel with an array of HBV genotypes and HBsAg subtypes. Vox Sang 98: 403414.

    • Search Google Scholar
    • Export Citation
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Hepatitis B Virus Infection in Indonesia 15 Years After Adoption of a Universal Infant Vaccination Program: Possible Impacts of Low Birth Dose Coverage and a Vaccine-Escape Mutant

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  • 1 Department of Microbiology, Faculty of Medicine, Airlangga University, Surabaya, Indonesia.
  • | 2 Department of Biochemistry, Faculty of Medicine, Airlangga University, Surabaya, Indonesia.
  • | 3 Indonesia-Japan Collaborative Research Center for Emerging and Re-emerging Infectious Diseases, Institute of Tropical Disease, Airlangga University, Surabaya, Indonesia.
  • | 4 Local Health Office, Kota Sorong, Indonesia.
  • | 5 Bahteramas Hospital, Kendari, Indonesia.
  • | 6 Health Polytechnics of Ministry of Health, Kupang, Indonesia.
  • | 7 Center for Infectious Diseases, Kobe University Graduate School of Medicine, Kobe, Japan.
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A universal hepatitis B vaccination program for infants was adopted in Indonesia in 1997. Before its implementation, the prevalence of hepatitis B surface antigen (HBsAg)–positive individuals in the general population was approximately 5–10%. The study aimed to investigate the hepatitis B virus (HBV) serological status and molecular profile among children, 15 years after adoption of a universal infant vaccination program in Indonesia. According to the Local Health Office data in five areas, the percentages of children receiving three doses of hepatitis B vaccine are high (73.9–94.1%), whereas the birth dose coverage is less than 50%. Among 967 children in those areas, the seropositive rate of HBsAg in preschool- and school-aged children ranged from 2.1% to 4.2% and 0% to 5.9%, respectively. Of the 61 HBV DNA–positive samples, the predominant genotype/subtype was B/adw2. Subtype adw3 was identified in genotype C for the first time in this population. Six samples (11.5%) had an amino acid substitution within the a determinant of the S gene region, and one sample had T140I that was suggested as a vaccine-escape mutant type. The low birth dose coverage and the presence of a vaccine-escape mutant might contribute to the endemicity of HBV infection among children in Indonesia.

Author Notes

* Address correspondence to Maria Inge Lusida, Institute of Tropical Disease, Airlangga University, Campus C, Jalan Mulyorejo, Surabaya 60115, Indonesia. E-mail: ingelusida@yahoo.com

Financial support: This work was supported by grants from the National Institute of Health Research and Development, Ministry of Health and Ministry of Research and Technology of the Republic Indonesia and by the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID), the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.

Authors' addresses: Priyo Budi Purwono, Juniastuti, Mochammad Amin, Rury Mega Wahyuni, Soetjipto, and Maria Inge Lusida, Institute of Tropical Disease (ITD), Airlangga University, Surabaya, Indonesia, E-mails: priyo_budi@yahoo.com, juniastutisyafik@yahoo.com, amin_tdc@yahoo.co.id, rury_mega@yahoo.com, soetjiptobr@sby.centrin.net.id, and ingelusida@yahoo.com. Rendra Bramanthi, Local Health Office, Kota Sorong, Indonesia, E-mail: rendra.bramanthi@gmail.com. Nursidah, Bahteramas Hospital, Kendari, Indonesia, E-mail: idhamikro@gmail.com. Erika Maria Resi, Health Polytechnics of Ministry of Health, Kupang, Indonesia, E-mail: mkorebima@yahoo.co.id. Yoshihiko Yano, Hak Hotta, and Yoshitake Hayashi, Center for Infectious Diseases, Kobe University Graduate School of Medicine, Kobe, Japan, E-mails: yanoyo@med.kobe-u.ac.jp, hotta@kobe-u.ac.jp, and hayashiy@med.kobe-u.ac.jp. Takako Utsumi, Indonesian-Japan Collaborative Research Center for Emerging and Re-emerging Infectious Diseases, Institute of Tropical Disease (ITD), Airlangga University, Surabaya, Indonesia, and Center for Infectious Diseases, Kobe University Graduate School of Medicine, Kobe, Japan, E-mail: tutsumi@people.kobe-u.ac.jp.

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