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Archives of Virology

, Volume 163, Issue 5, pp 1345–1349 | Cite as

The identification and characterization of novel rat hepatitis E virus strains in Bali and Sumbawa, Indonesia

  • Putu Prathiwi Primadharsini
  • Mulyanto
  • I. Dewa Nyoman Wibawa
  • Joko Anggoro
  • Tsutomu Nishizawa
  • Masaharu Takahashi
  • Suljid Jirintai
  • Hiroaki Okamoto
Brief Report
First Online:
Received:
Accepted:

Abstract

All three genetic groups of ratHEV have been found in Indonesia, suggesting the presence of additional variants of ratHEV in unexamined areas of Indonesia. A total of 242 wild rats were captured in Bali and Sumbawa, Indonesia, during 2014-2016. Among them, 4.1% were seropositive for anti-ratHEV IgG and two (0.8%) had detectable ratHEV RNA: ratESUMBAWA-140L and ratEBali2016D-047L, sharing 84.9-85.4% and 86.9-92.1% nucleotide identity with the reported G2 strains, respectively. The provisional criteria supported the notion that the ratEBali2016D-047L and ratESUMBAWA-140L strains were novel G2 variants. These results suggested the spatial distribution of further divergent ratHEV strains in Indonesia.

Keywords

Rat hepatitis E virus Bali Sumbawa Full-genome Genetic group 
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Notes

Acknowledgments

We thank Ms. Endang Wiwik Rochjati in Sumbawa-Besar town for her assistance in collecting wild rats. This study was supported in part by the Research Program on Hepatitis from the Japan Agency for Medical Research and Development, AMED (JP17fk0210301) and a MEXT-Supported Program for the Strategic Research Foundation at Private Universities, 2013-2017 (S13110340).

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest in association with the present study.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

705_2018_3736_MOESM1_ESM.pdf (123 kb)
Supplementary material 1 (PDF 123 kb)

References

  1. 1.
    Hsu IW, Tsai HJ (2014) Avian hepatitis E virus in chickens, Taiwan, 2013. Emerg Infect Dis 20:149–151CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Inoue J, Takahashi M, Yazaki Y, Tsuda F, Okamoto H (2006) Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. J Virol Methods 137:325–333CrossRefPubMedGoogle Scholar
  3. 3.
    Johne R, Heckel G, Plenge-Bönig A, Kindler E, Maresch C, Reetz J, Schielke A, Ulrich RG (2010) Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 16:1452–1455CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Johne R, Dremsek P, Kindler E, Schielke A, Plenge-Bonig A, Gregersen H, Wessels U, Schmidt K, Rietschel W, Groschup MH, Guenther S, Heckel G, Ulrich RG (2012) Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infect Genet Evol 12:947–956CrossRefPubMedGoogle Scholar
  5. 5.
    Kamar N, Dalton HR, Abravanel F, Izopet J (2014) Hepatitis E virus infection. Clin Microbiol Rev 27:116–138CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Kanai Y, Miyasaka S, Uyama S, Kawami S, Kato-Mori Y, Tsujikawa M, Yunoki M, Nishiyama S, Ikuta K, Hagiwara K (2012) Hepatitis E virus in Norway rats (Rattus norvegicus) captured around a pig farm. BMC Res Notes 5:4CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  8. 8.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  9. 9.
    Lack JB, Volk K, Van Den Bussche RA (2012) Hepatitis E virus genotype 3 in wild rats, United States. Emerg Infect Dis 18:1268–1273CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Li TC, Yoshimatsu K, Yasuda SP, Arikawa J, Koma T, Kataoka M, Ami Y, Suzaki Y, le Mai TQ, Hoa NT, Yamashiro T, Hasebe F, Takeda N, Wakita T (2011) Characterization of self-assembled virus-like particles of rat hepatitis E virus generated by recombinant baculoviruses. J Gen Virol 92:2830–2837CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Li TC, Ami Y, Suzaki Y, Yasuda SP, Yoshimatsu K, Arikawa J, Takeda N, Takaji W (2013) Characterization of full genome of rat hepatitis E virus strain from Vietnam. Emerg Infect Dis 19:115–118CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Li TC, Yoshizaki S, Ami Y, Suzaki Y, Yasuda SP, Yoshimatsu K, Arikawa J, Takeda N, Wakita T (2013) Susceptibility of laboratory rats against genotypes 1, 3, 4, and rat hepatitis E viruses. Vet Microbiol 163:54–61CrossRefPubMedGoogle Scholar
  13. 13.
    Li W, Guan D, Su J, Takeda N, Wakita T, Li TC, Ke CW (2013) High prevalence of rat hepatitis E virus in wild rats in China. Vet Microbiol 165:275–280CrossRefPubMedGoogle Scholar
  14. 14.
    Mulyanto, Depamede SN, Sriasih M, Takahashi M, Nagashima S, Jirintai S, Nishizawa T, Okamoto H (2013) Frequent detection and characterization of hepatitis E virus variants in wild rats (Rattus rattus) in Indonesia. Arch Virol 158:87–96CrossRefPubMedGoogle Scholar
  15. 15.
    Mulyanto, Suparyatmo JB, Andayani IG, Khalid Takahashi M, Ohnishi H, Jirintai S, Nagashima S, Nishizawa T, Okamoto H (2014) Marked genomic heterogeneity of rat hepatitis E virus strains in Indonesia demonstrated on a full-length genome analysis. Virus Res 179:102–112CrossRefPubMedGoogle Scholar
  16. 16.
    Obana S, Shimizu K, Yoshimatsu K, Hasebe F, Hotta K, Isozumi R, Nguyen HT, Le MQ, Yamashiro T, Tsuda Y, Arikawa J (2017) Epizootiological study of rodent-borne hepatitis E virus HEV-C1 in small mammals in Hanoi, Vietnam. J Vet Med Sci 79:76–81CrossRefPubMedGoogle Scholar
  17. 17.
    Okamoto H (2007) Genetic variability and evolution of hepatitis E virus. Virus Res 127:216–228CrossRefPubMedGoogle Scholar
  18. 18.
    Park SJ, Lee BW, Moon HW, Sung HW, Yoon BI, Meng XJ, Kwon HM (2015) Construction of an infectious cDNA clone of genotype 1 avian hepatitis E virus: characterization of its pathogenicity in broiler breeders and demonstration of its utility in studying the role of the hypervariable region in virus replication. J Gen Virol 96:1015–1026CrossRefPubMedGoogle Scholar
  19. 19.
    Purcell RH, Engle RE, Rood MP, Kabrane-Lazizi Y, Nguyen HT, Govindarajan S, St Claire M, Emerson SU (2011) Hepatitis E virus in rats, Los Angeles, California, USA. Emerg Infect Dis 17:2216–2222CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Purdy MA, Harrison TJ, Jameel S, Meng XJ, Okamoto H, Van der Poel WHM, Smith DB, ICTV Report C (2017) ICTV virus taxonomy profile: Hepeviridae. J Gen Virol 98:2645–2646CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Raj VS, Smits SL, Pas SD, Provacia LB, Moorman-Roest H, Osterhaus AD, Haagmans BL (2012) Novel hepatitis E virus in ferrets, The Netherlands. Emerg Infect Dis 18:1369–1370CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Ryll R, Bernstein S, Heuser E, Schlegel M, Dremsek P, Zumpe M, Wolf S, Pepin M, Bajomi D, Muller G, Heiberg AC, Spahr C, Lang J, Groschup MH, Ansorge H, Freise J, Guenther S, Baert K, Ruiz-Fons F, Pikula J, Knap N, Tsakmakidis I, Dovas C, Zanet S, Imholt C, Heckel G, Johne R, Ulrich RG (2017) Detection of rat hepatitis E virus in wild Norway rats (Rattus norvegicus) and Black rats (Rattus rattus) from 11 European countries. Vet Microbiol 208:58–68CrossRefPubMedGoogle Scholar
  23. 23.
    Smith DB, Simmonds P, 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 95:2223–2232CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    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 97:537–542CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Sugono D (2008) The mapping of languages in Indonesia. Language Center Press, Jakarta, p 8Google Scholar
  26. 26.
    Tam AW, Smith MM, Guerra ME, Huang CC, Bradley DW, Fry KE, Reyes GR (1991) Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185:120–131CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Division of Virology, Department of Infection and ImmunityJichi Medical University School of MedicineShimotsukeJapan
  2. 2.West Nusa Tenggara Hepatitis LaboratoryMataramIndonesia
  3. 3.Immunobiology Laboratory, Faculty of MedicineUniversity of MataramMataramIndonesia
  4. 4.Division of Gastroenterology and Hepatology, Department of Internal MedicineSanglah Hospital of Udayana UniversityDenpasarIndonesia
  5. 5.Division of Pathology, Department of Basic Veterinary MedicineInner Mongolia Agricultural University College of Veterinary MedicineHohhotChina

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