Molecular features of hepatitis E virus from farmed rabbits in Shandong province, China

Authors

  • Hongna Zhang Hebei University of Economics and Business
  • Yufa Zhou Center for Disease Control, Daiyue Bureau of Animal Husbandry
  • Jingbo Liu Institute of Microbiology Research, Baolai-Leelai Bio-Tech. Ltd.

DOI:

https://doi.org/10.4995/wrs.2018.10225

Keywords:

HEV, farmed rabbit, RT-nPCR, phylogenetic analysis, nucleotide identity

Abstract

This study was undertaken to investigate the genetic variability of hepatitis E virus (HEV) from farmed rabbits in Shandong province, China. A total of 50 fresh faecal samples from 5 rabbit farms were collected and subjected to reverse transcription and nested polymerase chain reaction (RT-nPCR) for a fragment sequence of HEV capsid gene. The results demonstrated that HEV RNA was observed in 6 faecal samples (6/50, 12.0%). In addition, the result of phylogenetic analysis showed that the 6 HEV isolates were classified into HEV-3 genotype with other rabbit HEV isolates from other countries, and shared 85.2-87.2%, 81.5-83.1%, and 77.0-78.6% nucleotide similarities with rabbit HEV isolates from Korea, the United States and France, respectively. To sum up, the HEV isolated in this study from farmed rabbits belongs to the HEV-3 genotype, and the zoonotic ability and pathogenesis of the rabbit HEV merit further study due to the fact that HEV-3 genotype has the potential to trigger zoonotic infections.

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Author Biography

Hongna Zhang, Hebei University of Economics and Business

Department of Teaching Affairs

References

Ahn H.S., Park B.J., Han S.H., Kim Y.H., Kim D.H., Kim B.S., Lee J.B., Park S.Y., Song C.S., Lee S.W., Choi I.S. 2017. Prevalence and genetic features of rabbit hepatitis E virus in Korea. J. Med. Virol., 89: 1995-2002. https://doi.org/10.1002/jmv.24875

Burt S.A., Veltman J., Hakze-van der Honing R., Schmitt H., Poel W.H. 2016. Hepatitis E Virus in Farmed Rabbits, Wild Rabbits and Petting Farm Rabbits in the Netherlands. Food Environ. Virol., 84: 313. https://doi.org/10.1007/s12560-016-9257-1

Cossaboom C.M., Córdoba L., Dryman B.A., Meng X.J. 2011. Hepatitis E virus in rabbits, Virginia, USA. Emerg. Infect. Dis., 17: 2047-2049. https://doi.org/10.3201/eid1711.110428

Cossaboom C.M., Córdoba L., Cao D., Ni Y.Y., Meng X.J. 2012. Complete genome sequence of hepatitis E virus from rabbits in the United States. J. Virol., 86: 13124-13125. https://doi.org/10.1128/JVI.02414-12

Di Bartolo I., De Sabato L., Marata A., Martinelli N., Magistrali C., Monini M., Ponterio E., Ostanello F., Ruggeri F. 2016. Serological survey of hepatitis E virus infection in farmed and pet rabbits in Italy. Arch. Virol., 161: 1343-1346. https://doi.org/10.1007/s00705-016-2778-y

Eiden M., Vina-Rodriguez A., Schlosser J., Schirrmeier H., Groschup M.H. 2016. Detection of Hepatitis E Virus in Archived Rabbit Serum Samples, Germany 1989. Food Environ. Virol., 8: 105-107. https://doi.org/10.1007/s12560-015-9222-4

Emerson S.U., Purcell R.H. 2003. Hepatitis E virus. Rev. Med.Virol., 13: 145-154. https://doi.org/10.1002/rmv.384

Frias M., López-López P., Rivero A., Rivero-Juarez A. 2018. Role of Hepatitis E Virus Infection in Acute-on-Chronic Liver Failure. Biomed. Res. Int., 9098535. https://doi.org/10.1155/2018/9098535

Fujiwara S., Yokokawa Y., Morino K., Hayasaka K., Kawabata M., Shimizu T. 2014. Chronic hepatitis E: a review of the literature. J. Viral Hepat., 21: 78-89. https://doi.org/10.1111/jvh.12156

Geng J., Wang L., Wang X., Fu H., Bu Q, Liu P., Zhu Y., Wang M., Sui Y., Zhuang H. 2011. Potential risk of zoonotic transmission from young swine to human: seroepidemiological and genetic characterization of hepatitis E virus in human and various animals in Beijing, China. J. Viral Hept., 18: 583-590. https://doi.org/10.1111/j.1365-2893.2011.01472.x

Huang F., Li Y., Yu W., Jing S., Wang J., Long F., He Z., Yang C., Bi Y., Cao W., Liu C., Hua X., Pan Q. 2016. Excretion of infectious hepatitis E virus into milk in cows imposes high risks of zoonosis. Hepatology, 64: 350-359. https://doi.org/10.1002/hep.28668

Izopet J., Dubois M., Bertagnoli S., Lhomme S., Marchandeau S., Boucher S., Kamar N., Abravanel F., Guérin J.L. 2012. Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg. Infect. Dis., 18: 1274-1281. https://doi.org/10.3201/eid1808.120057

Jirintai S., Manglai D., Takahashi M., Nagashima S., Kobayashi T., Nishizawa T., Okamoto H. 2012. Molecular analysis of hepatitis E virus from farm rabbits in Inner Mongolia, China and its successful propagation in A549 and PLC/PRF/5 cells. Virus Res., 170: 126-137. https://doi.org/10.1016/j.virusres.2012.09.015

Johne R., Dremsek P., Reetz J., Heckel G., Hess M., Ulrich R.G. 2014. Hepeviridae: an expanding family of vertebrate viruses. Infect. Genet. Evol., 27: 212-229. https://doi.org/10.1016/j.meegid.2014.06.024

Kaiser M., Delaune D., Chazouillères O., Blümel J., Roque-Afonso A.M., Baylis S.A. 2018. A World Health Organization Human Hepatitis E Virus Reference Strain Related to Similar Strains Isolated from Rabbits. Genome Announc., 6: e00292-18. https://doi.org/10.1128/genomeA.00292-18

Kamar N., Selves J., Mansuy J.M., Ouezzani L., Peron J.M., Guitard J., Cointault O., Esposito L., Abravanel F., Danjoux M., Durand D., Vinel J.P., Izopet J., Rostaing L. 2008. Hepatitis E virus and chronic hepatitis in organtransplant recipients. N. Engl. J. Med., 358: 811-817. https://doi.org/10.1056/NEJMoa0706992

King N.J., Hewitt J., Perchec-Merien A.M. Hiding in Plain Sight? It’s Time to Investigate Other Possible Transmission Routes for Hepatitis E Virus (HEV) in Developed Countries. Food Environ. Virol., 10: 225-252. https://doi.org/10.1007/s12560-018-9342-8

Krzowska-Firych J.M., Lucas C., Lucas G., Tomasiewicz K. 2018. Hepatitis E-A new era in understanding. Ann. Agric. Environ. Med., 25: 250-254. https://doi.org/10.26444/aaem/75142

Lee G.H., Tan B.H., Teo E.C., Lim S.G., Dan Y.Y., Wee A., Aw P.P., Zhu Y., Hibberd M.L., Tan C.K., Purdy M.A., Teo C.G. 2016. Chronic Infection With Camelid Hepatitis E Virus in a Liver Transplant Recipient Who Regularly Consumes Camel Meat and Milk. Gastroenterology, 150: 355-357. https://doi.org/10.1053/j.gastro.2015.10.048

Lhomme S., Dubois M., Abravanel F., Top S., Bertagnoli S., Guerin J.L., Izopet J. Risk of zoonotic transmission of HEV from rabbits. J. Clin. Virol., 58: 357-362. https://doi.org/10.1016/j.jcv.2013.02.006

Lhomme S., Top S., Bertagnoli S., Dubois M., Guerin J.-L., Izopet J. 2015. Wildlife reservoir for hepatitis E virus, Southwestern France. Emerg Infect. Dis., 21: 1224. https://doi.org/10.3201/eid2107.141909

Li S., Liu M., Cong J., Zhou Y., Miao Z. 2017. Detection and characterization of Hepatitis E Virus in goats at slaughterhouse in Tai’an Region, China. Biomed. Res. Int., 3723650. https://doi.org/10.1155/2017/3723650

Liu P., Bu Q.N., Wang L., Han J., Du R.J., Lei Y.X., Ouyang Y.Q., Li J., Zhu Y.H., Lu F.M. 2013. Transmission of hepatitis E virus from rabbits to cynomolgus macaques. Emerg. Infect. Dis., 19: 559-565. https://doi.org/10.3201/eid1904.120827

Meng X.J. 2010a. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet. Microbiol., 140: 256-265. https://doi.org/10.1016/j.vetmic.2009.03.017

Meng X.J. 2010b. Novel strains of hepatitis E virus identified from humans and other animal species: is hepatitis E a zoonosis? J. Hepatol., 33: 842-845. https://doi.org/10.1016/S0168-8278(00)80319-0

Meng X.J. 2011. From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res., 161: 23-30. https://doi.org/10.1016/j.virusres.2011.01.016

Pavio N., Meng X.J., Doceul V. 2015. Zoonotic origin of hepatitis E. Curr. Opin. Virol., 10: 34-41. https://doi.org/10.1016/j.coviro.2014.12.006

Pérez-Gracia M.T., Suay B., Mateos-Lindemann M.L. 2014. Hepatitis E: an emerging disease. Infect. Genet. Evol., 22: 40-59. https://doi.org/10.1016/j.meegid.2014.01.002

Purcell R., Emerson S. 2008. Hepatitis E: an emerging awareness of an old disease. J. Hepatol., 48: 494-503. https://doi.org/10.1016/j.jhep.2007.12.008

Purdy M.A., Khudyakov Y.E. 2010. Evolutionary history and population dynamics of hepatitis E virus. PLoS One, 5:e14376. https://doi.org/10.1371/journal.pone.0014376

Ryll R., Eiden M., Heuser E., Weinhardt M., Ziege M., Höper D., Groschup M.H., Heckel G., Johne R., Ulrich R.G. 2018. Hepatitis E virus in feral rabbits along a rural-urban transect in Central Germany. Infect. Genet Evol., 61: 155-159. https://doi.org/10.1016/j.meegid.2018.03.019

Shuai J.B., Li L.H., Li A.Y., He Y.Q., Zhang X.F. 2017. Full genome analysis of swine genotype 3 hepatitis E virus isolated from eastern China. J. Zhejiang Univ. Sci. B, 18: 549-554. https://doi.org/10.1631/jzus.B1600419

Smith D.B., Simmonds P. 2014. International Committee on Taxonomy of Viruses Hepeviridae Study G., Jameel S., Emerson S.U., Harrison T.J., Meng X.J., Okamoto H., Van der Poel W.H., Purdy M.A. Consensus proposals for classification of the family Hepeviridae. J. Gen. Virol., 95: 2223-2232. https://doi.org/10.1099/vir.0.068429-0

Sridhar S., Teng J.L.L., Chiu T.H., Lau S.K.P., Woo P.C.Y. 2017. Hepatitis E Virus Genotypes and Evolution: Emergence of Camel Hepatitis E Variants. Int. J. Mol. Sci., 18: E869. https://doi.org/10.3390/ijms18040869

Syed S.F., Zhao Q., Umer M., Alagawany M., Ujjan I.A., Soomro F., Bangulzai N., Baloch A.H, Abd El-Hack M., Zhou E.M. 2018. Past, present and future of hepatitis E virus infection: Zoonotic perspectives. Microb. Pathog., 119: 103-108. https://doi.org/10.1016/j.micpath.2018.03.051

Tei S., Kitajima N., Takahashi K., Mishiro S. 2003. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet, 362: 371-373. https://doi.org/10.1016/S0140-6736(03)14025-1

Wang L., Gong W., Fu H., Li M., Zhang Y., Luo Z., Xu Q., Wang L. 2018. Hepatitis E virus detected from Chinese laboratory ferrets and farmed mink. Transbound Emerg. Dis., 65: 219-223. https://doi.org/10.1111/tbed.12720

Woo P.C., Lau S.K., Teng J.L., Tsang A.K., Joseph M., Wong E.Y., Tang Y., Sivakumar S., Xie J., Bai R., Wernery R., Wernery U., Yuen K.Y. 2014. New hepatitis E virus genotype in camels, the Middle East. Emerg .Infect. Dis., 20: 1044-1048. https://doi.org/10.3201/eid2006.140140

Xia J., Zeng H., Liu L., Zhang Y., Liu P., Geng J., Wang L., Wang L., Zhuang H. 2015. Swine and rabbits are the main reservoirs of hepatitis E virus in China: detection of HEV RNA in feces of farmed and wild animals. Arch. Virol., 160: 2791-2798. https://doi.org/10.1007/s00705-015-2574-0

Yazaki Y., Mizuo H., Takahashi M., Nishizawa T., Sasaki N., Gotanda Y., Okamoto H. 2003. Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J. Gen. Virol., 84: 2351-2357. https://doi.org/10.1099/vir.0.19242-0

Zhang X.X., Qin S.Y., Zhang Y., Meng Q.F., Jiang J., Yang G.L., Zhao Q., Zhu X.Q. 2015. First report of hepatitis E virus infection in sika deer in China. Biomed. Res. Int., 502846. https://doi.org/10.1155/2015/502846

Zhao C., Ma Z., Harrison T.J., Feng R., Zhang C., Qiao Z., Fan J., Ma H., Li M., Song A., Wang Y. 2009. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J. Med. Virol., 81: 1371-1379. https://doi.org/10.1002/jmv.21536

Zheng Y., Ge S., Zhang J., Guo Q., Ng M.H., Wang F., Xia N., Jiang Q. 2006. Swine as a principal reservoir of hepatitis E virus that infects humans in eastern China. J. Infect. Dis., 193: 1643-1649. https://doi.org/10.1086/504293

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Published

2018-12-27

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Section

Pathology