Skip to main content

Advertisement

Log in

Natural infection of captive cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus genotype 4

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Data on natural HEV infection of infection in monkeys are limited. We report a case of hepatitis E virus genotype 4 infection in captive non-human primates (cynomolgus monkeys) imported from Vietnam. Phylogenetic analysis demonstrated that HEV infection was not the result of spillover from single source of infection, but rather the persistent circulation of HEV-4 among cynomolgus monkeys or multiple infections by related strains from a human or swine reservoir.

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.

Fig. 1

References

  1. Smith DB, Simmonds P, International Committee on Taxonomy of Viruses Hepeviridae Study Group, Jameel S, Emerson SU, Harrison TJ, Meng XJ, Okamoto H, Van der Poel WH, Purdy MA (2014) Consensus proposals for classification of the family Hepeviridae. J Gen Virol 95:2223–2232. https://doi.org/10.1099/vir.0.068429-0

    Article  PubMed  PubMed Central  Google Scholar 

  2. Woo PC, Lau SK, Teng JL, Cao KY, Wernery U, Schountz T, Chiu TH, Tsang AK, Wong PC, Wong EY, Yuen KY (2013) New hepatitis E virus genotype in bactrian camels, Xinjiang, China, 2013. Emerg Infect Dis 22(12):2219–2221. https://doi.org/10.3201/eid2212.160979

    Article  CAS  Google Scholar 

  3. Tsarev SA, Emerson SU, Tsareva TS, Yarbough PO, Lewis M, Govindarajan S, Reyes GR, Shapiro M, Purcell RH (1993) Variation in course of hepatitis E in experimentally infected cynomolgus monkeys. J Infect Dis 167(6):1302–1306

    Article  CAS  PubMed  Google Scholar 

  4. de Carvalho LG, Marchevsky RS, dos Santos DR, de Oliveira JM, de Paula VS, Lopes LM et al (2013) Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis. BMC Infect Dis 13:495. https://doi.org/10.1186/1471-2334-13-495

    Article  PubMed  PubMed Central  Google Scholar 

  5. Huang F, Yang C, Zhou X, Yu W, Pan Q (2016) Rhesus macaques persistently infected with hepatitis E shed virus into urine. J Hepatol 64(6):1446–1447. https://doi.org/10.1016/j.jhep.2015.12.026

    Article  PubMed  Google Scholar 

  6. Huang F, Yu W, Hua X, Jing S, Zeng W, He Z (2011) Seroepidemiology and molecular characterization of hepatitis E virus in Macaca mulatta from a village in Yunnan, China, where infection with this virus is endemic. Hepat Mon 11(9):745–749. https://doi.org/10.5812/kowsar.1735143x.730

    Article  PubMed  PubMed Central  Google Scholar 

  7. Spahr C, Knauf-Witzens T, Dahnert L, Enders M, Muller M, Johne R, Ulrich R (2018) Detection of HEV-specific antibodies in four non-human primate species, including great apes, from different zoos in Germany. Epidemiol Infect 146(1):119–124. https://doi.org/10.1017/S0950268817002606

    Article  CAS  PubMed  Google Scholar 

  8. Yamamoto H, Suzuki J, Matsuda A, Ishida T, Ami Y, Suzaki Y, Adachi I, Wakita T, Takeda N, Li T (2012) Hepatitis E virus outbreak in monkey facility, Japan. EID 18(12):2032–2034. https://doi.org/10.3201/eid1812.120884

    Article  Google Scholar 

  9. Lapin BA, Yakovleva LA, Dzhikidze EK, Gvozdik TE, Agumava AA, Stasilevich ZK, Danilova IG (2015) An enzootic outbreak of acute disease associated with pathogenic E. coli in Adler monkey colony. J Med Primatol 44:355–363. https://doi.org/10.1111/jmp.12184

    Article  PubMed  Google Scholar 

  10. Drobeniuc J, Meng J, Reuter G, Greene-Montfort T, Khudyakova N, Dimitrova Z, Kamili S, Teo CG (2010) Serologic assays specific to immunoglobulin M antibodies against hepatitis E virus: pangenotypic evaluation of performances. Clin Infect Dis 51(3):24–27. https://doi.org/10.1086/654801

    Article  Google Scholar 

  11. Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, Haynes JS, Thacker BJ, Emerson SU (1997) A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci USA 94:9860–9865

    Article  CAS  PubMed  Google Scholar 

  12. Lu L, Drobeniuc J, Kobylnikov N, Usmanov RK, Robertson BH, Favorov MO, Margolis HS (2004) Complete sequence of a Kyrgyzstan swine hepatitis E virus (HEV) isolated from a piglet thought to be experimentally infected with human HEV. J Med Virol 74:556–562. https://doi.org/10.1002/jmv.20214

    Article  CAS  PubMed  Google Scholar 

  13. Smith DB, Simmonds P, Izopet J, Oliveira-Filho EF, Ulrich RG, Johne R, Koenig M, Jameel S, Harrison TJ, Meng XJ, Okamoto H, Van der Poel WH, Purdy MA (2016) Proposed reference sequences for hepatitis E virus subtypes. J Gen Virol 97(3):537–542. https://doi.org/10.1099/jgv.0.000393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zehender G, Ebranati E, Lai A, Luzzago C, Paladini S, Tagliacarne C, Galli C, Galli M, Ciccozzi M, Zanetti AR, Romanò L (2014) Phylogeography and phylodynamics of European genotype 3 hepatitis E virus. Infect Genet Evol 25:138–143. https://doi.org/10.1016/j.meegid.2014.04.016

    Article  PubMed  Google Scholar 

  15. Mirazo S, Mir D, Bello G, Ramos N, Musto H, Arbiza J (2016) New insights into the hepatitis E virus genotype 3 phylodynamics and evolutionary history. Infect Genet Evol 43:267–273. https://doi.org/10.1016/j.meegid.2016.06.003

    Article  PubMed  Google Scholar 

  16. Mikhailov MI, Malinnikova EYu, Kyuregyan KK, Isaeva OV (2016) A case of importation of genotype 4 hepatitis E virus in Russia. Zh Mikrobiol Epidemiol Immunobiol 3:64–69 (in Russian)

    Google Scholar 

  17. Korzaia LI, Keburia VV, Dogadov DI, Lapin BA, Kyuregyan KK, Mikhailov MI (2016) Markers of hepatitis E among the population of the Greater Sochi and in monkeys of the Adler primate center. Voprosy Virusologii 61(4):176–180 (in Russian)

    Google Scholar 

  18. Jeblaoui A, Haim-Boukobza S, Marchadier E, Mokhtari C, Roque-Afonso A (2013) Genotype 4 hepatitis E virus in France: an autochthonous infection with a more severe presentation. Clin Infect Dis 57:122–126. https://doi.org/10.1093/cid/cit291

    Article  Google Scholar 

  19. Lhomme S, Abravanel F, Dubois M, Chapuy-Regaud S, Sandres-Saune K, Mansuy JM, Rostaing L, Kamar N, Izopet J (2015) Temporal evolution of the distribution of hepatitis E virus genotypes in Southwestern France. Infect Genet Evol 35:50–55. https://doi.org/10.1016/j.meegid.2015.07.028

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Saleem Kamili, Michael A. Purdy, and Jan Drobeniuc for review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dmitriy I. Dogadov.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving animals

The care and use of the monkeys comply with the rules on humane care of animals and with approved experimental protocols, which were also approved by the local ethics committee. No interventions except routine blood and fecal sampling during the quarantine period were made in this study.

Additional information

Handling Editor: Michael A. Purdy.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 2980 kb)

Supplementary material 2 (DOC 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dogadov, D.I., Korzaya, L.I., Kyuregyan, K.K. et al. Natural infection of captive cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus genotype 4. Arch Virol 164, 2515–2518 (2019). https://doi.org/10.1007/s00705-019-04337-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-019-04337-3

Navigation