Detection of antibodies to the hepatitis E virus in domestic reindeer (Rangifer tarandus) in the Republic of Sakha (Yakutia)

Cover Page

Cite item

Full Text

Abstract

Introduction. Although domestic pigs and wild boars are the main reservoir of zoonotic hepatitis E virus (HEV) genotypes in temperate countries, the presence of antibodies to HEV (anti-HEV) in the indigenous population of circumpolar territories, i.e. outside the habitat of wild and domestic pigs, indicates the presence of an alternative reservoir of the virus. Reindeer (Rangifer tarandus) may be a potential reservoir for HEV in the polar regions. The purpose of the study was to determine the prevalence of anti-HEV among domestic reindeer in the Republic of Sakha (Yakutia).

Materials and methods. Sera from 497 domestic reindeer from the Oymyakon (n = 425) and Ust-Yansky districts (n = 72) of the Republic of Sakha (Yakutia) were tested for anti-HEV. A commercial ELISA kit DS-ELISA-ANTI-HEV-G (Diagnostic Systems-Stolitsa LLC, Russia) was used for detection of anti-HEV IgG, but a rabbit polyclonal antibody against deer IgG labeled with horseradish peroxidase (KPL, USA) at a dilution of 1 : 100 in phosphate-buffered saline were used instead of the human specific conjugate from the kit.

Results. The average detection rate of anti-HEV in reindeer sera was 15.5% (95% CI: 12.6–19.0%). The detection rate of anti-HEV significantly increased with age, from 3.5% (95% CI: 1.1–9.0%) in calves aged 3–6 months to 25.0% (95% CI: 1.6 –36.5%) in deer aged 2–4 years (p < 0.0001). From this age group, anti-HEV detection rates reached a plateau, not differing significantly between older age groups (p > 0.05). The average anti-HEV detection rate among reindeer 2 years of age and older was 19.0% (95% CI: 15.3–23.4%). There were no statistically significant differences in the frequency of anti-HEV detection between female and male reindeer, both among adult animals and among calves.

Conclusion. The observed anti-HEV detection rates among domestic reindeer in the Republic of Sakha (Yakutia) indicate that infection caused by HEV or an antigenically similar virus is common in these animals. The dynamics of antibody accumulation in the reindeer population indicates that infection apparently occurs during the first two years of life.

About the authors

Vera S. Kichatova

Central Research Institute of Epidemiology; Mechnikov Research Institute of Vaccines and Sera; Russian Medical Academy of Continuing Professional Education

Author for correspondence.
Email: vera_kichatova@mail.ru
ORCID iD: 0000-0002-7838-6965

MD, PhD, Senior Research Fellow, Laboratory of Molecular Epidemiology of Viral Hepatitis of Central Research Institute of Epidemiology; Research Fellow, Laboratory of Viral Hepatitis of I. Mechnikov Research Institute of Vaccines and Sera; Senior Research Fellow, Laboratory of Socially Significant Viral Infections of Russian Medical Academy of Continuing Professional Education, Moscow, Russia

Russian Federation, 111123, Moscow; 105064, Moscow; 125993, Moscow

Ilya A. Potemkin

Central Research Institute of Epidemiology; Mechnikov Research Institute of Vaccines and Sera; Russian Medical Academy of Continuing Professional Education

Email: axi0ma@mail.ru
ORCID iD: 0000-0001-7559-4219

MD, PhD, Senior Research Fellow, Laboratory of Molecular Epidemiology of Viral Hepatitis of Central Research Institute of Epidemiology; Research Fellow, Laboratory of Viral Hepatitis of I. Mechnikov Research Institute of Vaccines and Sera; Senior Research Fellow, Laboratory of Socially Significant Viral Infections of Russian Medical Academy of Continuing Professional Education, Moscow, Russia

Russian Federation, 111123, Moscow; 105064, Moscow; 125993, Moscow

Fedor A. Asadi Mobarkhan

Central Research Institute of Epidemiology; Mechnikov Research Institute of Vaccines and Sera

Email: 1amfa@bk.ru
ORCID iD: 0000-0002-1838-8037

Research Fellow, Laboratory of Molecular Epidemiology of Viral Hepatitis of Central Research Institute of Epidemiology; Junior Research Fellow, Laboratory of Viral Hepatitis of I. Mechnikov Research Institute of Vaccines and Sera, Moscow, Russia

Russian Federation, 111123, Moscow; 105064, Moscow

Tatyana D. Rumyantseva

Arctic State Agrotechnological University

Email: tanya_rum@mail.ru
ORCID iD: 0000-0003-0997-5499

Leading Researcher, Arctic State Agrotechnological University, Yakutsk, Russia

Russian Federation, 677008, Yakutsk, Republic of Sakha (Yakutia)

Sergey I. Semenov

North-Eastern Federal University named after. M.K. Ammosov

Email: insemenov@yandex.ru
ORCID iD: 0000-0001-8099-2270

MD, PhD, Leading Researcher, Research Center of the NEFU Medical Institute of the Federal State Autonomous Educational Institution of Higher Education “North-Eastern Federal University named after M.K. Ammosov”, Yakutsk, Russia

Russian Federation, 677010, Yakutsk, Republic of Sakha (Yakutia)

Karen K. Kyuregyan

Central Research Institute of Epidemiology; Mechnikov Research Institute of Vaccines and Sera

Email: karen-kyuregyan@yandex.ru
ORCID iD: 0000-0002-3599-117X

Doctor of Biol. Sci., PhD, Professor of Russ. Acad. Sci., Head of Laboratory of Molecular Epidemiology of Viral Hepatitis of Central Research Institute of Epidemiology; Leading Research Fellow, Laboratory of Viral Hepatitis of I. Mechnikov Research Institute of Vaccines and Sera, Moscow, Russia

Russian Federation, 111123, Moscow; 105064, Moscow

Mikhail I. Mikhailov

Central Research Institute of Epidemiology; Mechnikov Research Institute of Vaccines and Sera

Email: michmich2@yandex.ru
ORCID iD: 0000-0002-6636-6801

MD, PhD, Corr. Member of Russ. Acad. Sci., Chief Research Fellow, Laboratory of Molecular Epidemiology of Viral Hepatitis of Central Research Institute of Epidemiology; Head of Laboratory of Viral Hepatitis of I. Mechnikov Research Institute of Vaccines and Sera; Moscow, Russia

Russian Federation, 111123, Moscow; 105064, Moscow

References

  1. Purdy M.A., Drexler J.F., Meng X.J., Norder H., Okamoto H., Van der Poel W.H.M., et al. ICTV virus taxonomy profile: Hepeviridae 2022. J. Gen. Virol. 2022; 103(9). https://doi.org/10.1099/jgv.0.001778
  2. Pischke S., Hartl J., Pas S.D., Lohse A.W., Jacobs B.C., Van der Eijk A.A. Hepatitis E virus: Infection beyond the liver? J. Hepatol. 2017; 66(5): 1082–95. https://doi.org/10.1016/j.jhep.2016.11.016.
  3. WHO. Hepatitis E: Fact Sheet; 2020. Available at: https://www.who.int/news-room/fact-sheets/detail/hepatitis-e
  4. Kamar N., Izopet J., Pavio N., Aggarwal R., Labrique A., Wedemeyer H., et al. Hepatitis E virus infection. Nat. Rev. Dis. Primers. 2017; 3: 17086. https://doi.org/10.1038/nrdp.2017.86
  5. Mikhailov M.I., Karlsen A.A., Potemkin I.A., Isaeva O.V., Kichatova V.S., Malinnikova E.Y., et al. Geographic and temporal variability of hepatitis E virus circulation in the Russian Federation. Viruses. 2022; 15(1): 37. https://doi.org/10.3390/v15010037
  6. Smith D.B., Izopet J., Nicot F., Simmonds P., Jameel S., Meng X.J., et al. Update: proposed reference sequences for subtypes of hepatitis E virus (species Orthohepevirus A). J. Gen. Virol. 2020; 101(7): 692–8. https://doi.org/10.1099/jgv.0.001435
  7. Nelson K.E., Labrique A.B., Kmush B.L. Epidemiology of genotype 1 and 2 hepatitis E virus infections. Cold Spring Harb. Perspect. Med. 2019; 9(6): a031732. https://doi.org/10.1101/cshperspect.a031732
  8. Pallerla S.R., Harms D., Johne R., Todt D., Steinmann E., Schemmerer M., et al. Hepatitis E virus infection: circulation, molecular epidemiology, and impact on global health. Pathogens. 2020; 9(10): 856. https://doi.org/10.3390/pathogens9100856
  9. Grange Z.L., Goldstein T., Johnson C.K., Anthony S., Gilardi K., Daszak P., et al. Ranking the risk of animal-to-human spillover for newly discovered viruses. Proc. Natl Acad. Sci. USA. 2021; 118(15): e2002324118. https://doi.org/10.1073/pnas.2002324118
  10. Reuter G., Boros Á., Pankovics P. Review of hepatitis E virus in rats: evident risk of species Orthohepevirus C to human zoonotic infection and disease. Viruses. 2020; 12(10): 1148. https://doi.org/10.3390/v12101148
  11. Minuk G.Y., Sun A., Sun D.F., Uhanova J., Nicolle L.E., Larke B., et al. Serological evidence of hepatitis E virus infection in an indigenous North American population. Can. J. Gastroenterol. 2007; 21(7): 439–42. https://doi.org/10.1155/2007/289059
  12. Di Profio F., Sarchese V., Palombieri A., Fruci P., Lanave G., Robetto S., et al. Current knowledge of Hepatitis E Virus (HEV) epidemiology in ruminants. Pathogens. 2022; 11(10): 1124. https://doi.org/10.3390/pathogens11101124
  13. Lin J., Karlsson M., Olofson A.S., Belák S., Malmsten J., Dalin A.M., et al. High prevalence of hepatitis e virus in Swedish moose – a phylogenetic characterization and comparison of the virus from different regions. PLoS One. 2015; 10(4): e0122102. https://doi.org/10.1371/journal.pone.0122102
  14. Weger S., Elkin B., Lindsay R., Bollinger T., Crichton V., Andonov A. Hepatitis E virus seroprevalence in free-ranging deer in Canada. Transbound. Emerg. Dis. 2017; 64(3): 1008–11. https://doi.org/10.1111/tbed.12462
  15. Sacristán C., Madslien K., Sacristán I., Klevar S., das Neves C.G. Seroprevalence of hepatitis E virus in moose (Alces alces), reindeer (Rangifer tarandus), red deer (Cervus elaphus), roe deer (Capreolus capreolus), and muskoxen (Ovibos moschatus) from Norway. Viruses. 2021; 13(2): 224. https://doi.org/10.3390/v13020224
  16. Rinaldo C.H., Nymo I.H., Sánchez Romano J., Breines E.M., Murguzur F.J.A., Tryland M. Serological evidence of hepatitis E virus infection in semi-domesticated Eurasian tundra reindeer (Rangifer tarandus tarandus) in Norway. Pathogens. 2021; 10(12): 1542. https://doi.org/10.3390/pathogens10121542
  17. Slukinova O.S., Kyuregyan K.K., Karlsen A.A., Potemkin I.A., Kichatova V.S., Semenov S.I., et al. Serological evidence of hepatitis E virus circulation among reindeer and reindeer herders. Vector. Borne Zoonotic Dis. 2021; 21(7): 546–51. https://doi.org/10.1089/vbz.2020.2727
  18. Kodani M., Kamili N.A., Tejada-Strop A., Poe A., Denniston M.M., Drobeniuc J., et al. Variability in the performance characteristics of IgG anti-HEV assays and its impact on reliability of seroprevalence rates of hepatitis E. J. Med. Virol. 2017; 89(6): 1055–61. https://doi.org/10.1002/jmv.24741
  19. Haqshenas G., Huang F.F., Fenaux M., Guenette D.K., Pierson F.W., Larsen C.T., et al. The putative capsid protein of the newly identified avian hepatitis E virus shares antigenic epitopes with that of swine and human hepatitis E viruses and chicken big liver and spleen disease virus. J. Gen. Virol. 2002; 83(Pt. 9): 2201–9. https://doi.org/10.1099/0022-1317-83-9-2201
  20. Zhou X., Kataoka M., Liu Z., Takeda N., Wakita T., Li T.C. Characterization of self-assembled virus-like particles of dromedary camel hepatitis E virus generated by recombinant baculoviruses. Virus Res. 2015; 210: 8–17. https://doi.org/10.1016/j.virusres.2015.06.022
  21. Kubickova B., Schenk J.A., Ramm F., Markuškienė K., Reetz J., Dremsek P., et al. A broadly cross-reactive monoclonal antibody against hepatitis E virus capsid antigen. Appl. Microbiol. Biotechnol. 2021; 105(12): 4957–73. https://doi.org/10.1007/s00253-021-11342-7
  22. Sánchez Romano J., Omazic A., Leijon M., Hagström Å., Tryland M., Kantanen J., et al. Screening of Eurasian tundra reindeer for viral sequences by next-generation sequencing. Int. J. Environ. Res. Public Health. 2021; 18(12): 6561. https://doi.org/10.3390/ijerph18126561
  23. Feng R., Zhao C., Li M., Harrison T.J., Qiao Z., Feng Y., et al. Infection dynamics of hepatitis E virus in naturally infected pigs in a Chinese farrow-to-finish farm. Infect. Genet. Evol. 2011; 11(7): 1727–31. https://doi.org/10.1016/j.meegid.2011.07.009

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure. Frequency rates of anti-HEV detection in different age groups of reindeer.

Download (103KB)
Indexing metadata

Copyright (c) 2023 Kichatova V.S., Potemkin I.A., Asadi Mobarkhan F.A., Rumyantseva T.D., Semenov S.I., Kyuregyan K.K., Mikhailov M.I.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies