Skip to main content
Log in

Markers of Viral Hepatitis B in Blood–Plasma Samples of the Indigenous Population of the Far North of Russia. HBV Genotypes and HBsAg Subtypes

  • EXPERIMENTAL PAPERS
  • Published:
Molecular Genetics, Microbiology and Virology Aims and scope Submit manuscript

Abstract

Hepatitis B is a major public health problem worldwide. The indigenous population of remote regions with harsh living conditions, such as the Far North of Russia, with possibly unique genetic mutations in the local strains of this pathogen, remains poorly studied. The aim of the study was to determine the prevalence of serological HBV markers in blood–plasma samples of the population of the Far North of Russia and to determine HBV genotypes and HBsAg subtypes in blood–plasma samples containing HBsAg. We studied 702 blood–plasma samples taken from the indigenous population (Tundra Nenets) of the village of Gyda in the Tazovsky district of the Yamalo-Nenets autonomous okrug (YaNAO) (north of the Gydan Peninsula). Detection of serological HBV markers—HBsAg, anti-HBs, and anti-Hbcore—was carried out using JSC Vector-Best reagent kits. HBV genotypes and HBsAg subtypes in the samples were determined according to our own original procedure with monoclonal antibodies and by classical molecular-biological methods. The prevalence of HBsAg in the entire sample was 0.4% (3/702). For the subgroup of samples (persons older than 15 years during the first two expeditions, 300 samples), an extended analysis of the markers was carried out. The following frequencies were determined for them: HBsAg, 0.7% (2/300); anti-HBs, 63.7% (191/300); and anti-HBcore, 11.3% (34/300). HBV statuses were established for this subgroup: the presence of HBV infection (0.7%), past hepatitis B infection (9.3%), and immunity as result of vaccination (54.3%). Genotype D was established for two samples containing HBsAg (subtypes ayw2 and ayw3); the results of the two used methods coincided. The prevalence of HBsAg in the Tazovsky and adjacent Purovsky districts (the main population being Nenets, previously published data) differed (0.4% vs. 1.7%, p < 0.05), presumably due to vaccination (samples of the Purovsky district were collected almost 20 years earlier), as well as the distribution of HBV genotypes. The Tazovsky district of YaNAO is now a low endemic region in terms of HBV infection. The HBV isolates belong to the most common HBV genotype D in the Russian Federation (HBsAg subtypes ayw2, ayw3).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Notes

  1. Number in the GenBank database: AB675681.1 (Hepatitis B virus DNA, complete genome, isolate: 10B19).

REFERENCES

  1. World Health Organization. Hepatitis B. https://www.who.int/ru/news-room/fact-sheets/detail/hepatitis-b. Accessed October 31, 2021.

  2. Prikaz no. 229 ot 27 iyunya 2001 Ministerstva zdravookhraneniya Rossiiskoi Federatsii “O natsional’nom kalendare profilakticheskih privivok i kalendare profilakticheskih privivok po epidemicheskim pokazaniyam” (Order no. 1229 of Ministry of Healthcare of the Russian Federation of June 27, 2001 on National Prophylactic Immunization Schedule and Prophylactic Immunization Schedule According to Epidemic Conditions), Moscow, 2003. https://39.rospotrebnadzor.ru/content/prikaz-ot-27062001-no-229-o-nacionalnom-kalendare-profilakticheskih-privivok-i-kalendare. Accessed June 22, 2021.

  3. National Prophylactic Immunization Schedule. https://44.rospotrebnadzor.ru/profilaktika_infekci/158/%D1%8D. Accessed June 22, 2021.

  4. Le Bouvier, G.L., The heterogeneity of Australia antigen, J. Infect. Dis., 1971, vol. 123, no. 6, pp. 671–675. https://doi.org/10.1093/infdis/123.6.671

    Article  CAS  Google Scholar 

  5. Bancroft, W.H., Mundon, F.K., and Russell, P.K., Detection of additional antigenic determinants of hepatitis B antigen, J. Immunol., 1972, vol. 109, no. 4, pp. 842–848.

    CAS  Google Scholar 

  6. Couroucé-Pauty, A.M., Plançon, A., and Soulier, J.P., Distribution of HBsAg subtypes in the world, Vox Sang., 1983, vol. 44, no. 4, pp. 197–211. https://doi.org/10.1111/j.1423-0410.1983.tb01885.x

    Article  Google Scholar 

  7. Norder, H., Couroucé, A.M., Coursaget, P., Echevarria, J.M., Lee, S.D., and Mushahwar, I.K., et al., Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes, Intervirology, 2004, vol. 47, no. 6, pp. 289–309. https://doi.org/10.1159/000080872

    Article  Google Scholar 

  8. Schaefer, S., Magnius, L., and Norder, H., Under construction: classification of hepatitis B virus genotypes and subgenotypes, Intervirology, 2009, vol. 52, no. 6, pp. 323–325. https://doi.org/10.1159/000242353

    Article  Google Scholar 

  9. Kurbanov, F., Tanaka, Y., and Mizokami, M., Geographical and genetic diversity of the human hepatitis B virus, Hepatol. Res., 2010, vol. 40, no. 1, pp. 14–30. https://doi.org/10.1111/j.1872-034X.2009.00601.x

    Article  Google Scholar 

  10. Krarup, H.B., Andersen, S., Madsen, P.H., Okkels, H., Hvingel, B.H., and Laurberg, P., Benign course of long-standing hepatitis B virus infection among Greenland Inuit?, Scand. J. Gastroenterol., 2008, vol. 43, no. 3, pp. 334–343. https://doi.org/10.1080/00365520701712198

    Article  Google Scholar 

  11. Baikie, M., Ratnam, S., Bryant, D.G., Jong, M., and Bokhout, M., Epidemiologic features of hepatitis B virus infection in northern Labrador, Can. Med. Assoc. J., 1989, vol. 141, no. 8, pp. 791–795.

    CAS  Google Scholar 

  12. Schreeder, M.T., Bender, T.R., McMahon, B.J., Moser, M.R., Murphy, B.L., Sheller, M.J., Heyward, W.L., Hall, D.B., and Maynard, J.E., Prevalence of hepatitis B in selected Alaskan Eskimo villages, Am. J. Epidemiol., 1983, vol. 118, pp. 543–549.

    Article  CAS  Google Scholar 

  13. Manuilov, V.A., Osipova, L.P., Netesova, I.G., Chub, E.V., Bezuglova, L.V., Norder, H., et al., The Prevalence of HBsAg subtypes and HBV of Siberia, Mol. Genet., Microbiol. Virol., 2015, vol. 30, no. 1, pp. 30–38. https://doi.org/10.3103/S089141681501005X

    Article  Google Scholar 

  14. Sleptsova, S.S., A role of the genotypes of hepatitis B, C and D viruses in primary liver cancer progression, VICh-Infekts. Immunosupr., 2012, vol. 4, no. 4, pp. 67–73.

    Google Scholar 

  15. Chulanov, V.P., The epidemiological and clinical significance of hepatitis A and B viruses genetic heterogeneity, Doctoral Sci (Med.) Dissertation, Moscow, 2013.

  16. Federal State Statistics Service. Population of the Russian Federation in Municipal Districts up to January 1, 2020 (Table no. 25). https://rosstat.gov.ru/compendium/document/13282. Accessed June 22, 2021.

  17. Bezuglova, L.V., Manuilov, V.A., Osipova, L.P., Mosina, Ya.D., Poryvaeva, V.A., Agafonova, O.A., et al., Trial results for ELISA test kits for HBsAg subtype and hepatitis B virus genotype identification in human blood plasma, Mol. Genet., Microbiol. Virol., 2020, vol. 35, no. 4, pp. 229–236. https://doi.org/10.3103/S0891416820040047

    Article  Google Scholar 

  18. Hawkins, T., O’Connor-Morin, T., Roy, A., and Santillan, C., DNA purification and isolation using a solid-phase, Nucleic Acids Res., 1994, vol. 22, no. 21, pp. 4543–4544. https://doi.org/10.1093/nar/22.21.4543

    Article  CAS  Google Scholar 

  19. DeAngelis, M., Wang, D., Hawkins, T., Solid-phase reversible immobilization for the isolation of PCR products, Nucleic Acids Res., 1995, vol. 23, no. 22, pp. 4742–4743. https://doi.org/10.1093/nar/23.22.4742

    Article  CAS  Google Scholar 

  20. MEGA. Molecular Evolutionary Genetics Analysis. https://www.megasoftware.net. Accessed June 16, 2021.

  21. Norder, H., Hammas, B., Losfdahl, S., Courouce, A.M., and Magnius, L.O., Comparison of the amino acid sequences of nine different serotypes of hepatitis B surface antigen and genomic classification of the corresponding hepatitis B virus strains, J. Gen. Virol., 1992, vol. 73, no. 5, pp. 1201–1208. https://doi.org/10.1099/0022-1317-73-5-1201

    Article  CAS  Google Scholar 

  22. Magnius, L.O. and Norder, H., Subtypes, genotypes and molecular epidemiology of the hepatitis B virus as reflected by sequence variability of the S-gene, Intervirology, 1995, vol. 38, pp. 24–34. https://doi.org/10.1159/000150411

    Article  CAS  Google Scholar 

  23. Purdy, M., Talekar, G., Swenson, P., Araujo, A., and Fields, H., A new algorithm for deduction of hepatitis B surface antigen subtype determinants from the amino acid sequence, Intervirology, 2007, vol. 50, pp. 45–51. https://doi.org/10.1159/000096312

    Article  CAS  Google Scholar 

  24. Analysis of Four-Fold Tables by Means of Non-Parametric Statistical Criteria (Online-Calculator). https://medstatistic.ru/calculators/calchi.html. Accessed June 22, 2021.

  25. Calculation of Mann-Whitney Test (Online-Calculator). https://medstatistic.ru/calculators/calcmann.html. Accessed June 22, 2021.

  26. Directorate of Russian Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing for Yamalo-Nenets Autonomous Okrug. May 19 - International Day Against Hepatitis B. https://89.rospotrebnadzor.ru/press/public/73356/. Accessed June 22, 2021.

  27. European Association for the Study of the Liver. EASL 2017 clinical practice guidelines on the management of hepatitis B virus infection, J. Hepatol., 2017, vol. 67, no. 2, pp. 370–398. https://doi.org/10.1016/j.jhep.2017.03.021

    Article  Google Scholar 

  28. Caviglia, G.P., Abate, M.L., Tandoi, F., Ciancio, A., Amoroso, A., Salizzoni, M., et al., Quantitation of HBV cccDNA in anti-HBc-positive liver donors by droplet digital PCR: A new tool to detect occult infection, J. Hepatol., 2018, vol. 69, no. 2, pp. 301–307. https://doi.org/10.1016/j.jhep.2018.03.021

    Article  CAS  Google Scholar 

  29. Sofian, M., Aghakhani, A., Izadi, N., Banifazl, M., Kalantar, E., Eslamifar, A., et al., Lack of occult hepatitis B virus infection among blood donors with isolated hepatitis B core antibody living in an HBV low prevalence region of Iran, Int. J. Infect. Dis., 2010, vol. 14, no. 4, pp. 308–310. https://doi.org/10.1016/j.ijid.2009.05.011

    Article  Google Scholar 

  30. Altunay, H., Kosan, E., Birinci, I., Aksoy, A., Kirali, K., Saribas, S., et al., Are isolated anti-HBc blood donors in high-risk group? The detection of HBV DNA in isolated anti-HBc cases with nucleic acid amplification test (NAT) based on transcription-mediated amplification (TMA) and HBV discrimination, Transfus. Apheresis Sci., 2010, vol. 43, no. 3, pp. 265–268. https://doi.org/10.1016/j.transci.2010.09.012

    Article  Google Scholar 

  31. Sowole, L., Labbett, W., Patel, M., O’Riordan, A., Cross, J., Davenport, A., et al., The prevalence of occult hepatitis B virus (HBV) infection in a large multi-ethnic haemodialysis cohort, BMC Nephrol., 2015, vol. 16, p. 12. https://doi.org/10.1186/s12882-015-0010-z

    Article  Google Scholar 

  32. Weber, B., Melchior, W., Gehrke, R., Doerr, H.W., Berger, A., and Rabenau, H., Hepatitis B virus markers in anti-HBc only positive individuals, J. Med. Virol., 2001, vol. 64, no. 3, pp. 312–319. https://doi.org/10.1002/jmv.1052

    Article  CAS  Google Scholar 

  33. Hollinger, F.B., Hepatitis B virus infection and transfusion medicine: science and the occult, Transfusion, 2008, vol. 48, pp. 1001–1026. https://doi.org/10.1111/j.1537-2995.2008.01701.x

    Article  CAS  Google Scholar 

  34. Raimondo, G., Locarnini, S., Pollicino, T., Levrero, M., Zoulim, F., Lok, A.S., and the Taormina Workshop on Occult HBV Infection Faculty Members, Update of the statements on biology and clinical impact of occult hepatitis B virus infection, J. Hepatol., 2019, vol. 71, pp. 397–408. https://doi.org/10.1016/j.jhep.2019.03.034

    Article  Google Scholar 

  35. Jilg, W., Sieger, E., Zachoval, R., and Schatzl, H., Individuals with antibodies against hepatitis B core antigen as the only serological marker for hepatitis B infection: high percentage of carriers of hepatitis B and C virus, J. Hepatol., 1995, vol. 23, pp. 14–20. https://doi.org/10.1016/0168-8278(95)80305-x

    Article  CAS  Google Scholar 

  36. Koike, K., Kobayashi, M., Gondo, M., Hayashi, I., Osuga, T., and Takada, S., Hepatitis B virus DNA is frequently found in liver biopsy samples from hepatitis C virus-infected chronic hepatitis patients, J. Med. Virol., 1998, vol. 54, no. 4, pp. 249–255. https://doi.org/10.1002/(SICI)1096-9071(199804)54:4<249::AID-JMV3>3.0.CO;2-4

    Article  CAS  Google Scholar 

  37. Coppola, N., Onorato, L., Pisaturo, M., Macera, M., Sagnelli, C., Martini, S., et al., Role of occult hepatitis B virus infection in chronic hepatitis C, World J. Gastroenterol., 2015, vol. 21, no. 42, pp. 11931–11940. https://doi.org/10.3748/wjg.v21.i42.11931

    Article  CAS  Google Scholar 

  38. WHO International Standard. Third International Standard for HBsAg (HBV Genotype B4, HBsAg Subtypes ayw1/adw2). NIBSC Code: 12/226. https://www.nibsc.org/products/brm_product_catalogue/detail_page.aspx?catid=12/226. Accessed June 22, 2021.

  39. Netesova, I.G., Yaroslavtseva, O.A., Dryga, S.A., et al., Degree of incidence of hepatitis A, B, C viral markers in the native-borne population at the North of Western Siberia, Vopr. Virusol., 1995, vol. 4, pp. 172–174.

    Google Scholar 

Download references

Funding

The work was carried out mainly without special financial support. The participation of S.V. Netesov was supported within the framework of state order for financing research at Novosibirsk State University no. FSUS-2020-0035 and the TOP-100 NSU “Program for Increasing the Competitiveness of Russian Universities.” The participation of L.P. Osipova and L.E. Tabikhanova was supported by the budget project of the Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, no. 0259-2021-0014.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. V. Bezuglova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individuals involved in the study.

Conflict of Interest

The authors declare that they have no conflicts of interest.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bezuglova, L.V., Osipova, L.P., Sergeeva, E.I. et al. Markers of Viral Hepatitis B in Blood–Plasma Samples of the Indigenous Population of the Far North of Russia. HBV Genotypes and HBsAg Subtypes. Mol. Genet. Microbiol. Virol. 37, 146–152 (2022). https://doi.org/10.3103/S0891416822030041

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0891416822030041

Keywords:

Navigation