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Comparative analysis of rabbit hemorrhagic disease virus strains originating from outbreaks in the Russian Federation

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Abstract

Since the first introduction of rabbit hemorrhagic disease (RHD) in 1986, disease outbreaks have been continuously reported in different regions of Russia. Despite extensive vaccination, sporadic RHD cases are still reported. Here, we examine eleven RHDV strains originating from disease outbreaks occurring between 2003 and 2012 and one widely used vaccine strain. Notable phenotypic and genetic heterogeneity among RHDV strains was observed. The RHDV strains Tambov-2010, Perm-2010, Manihino-09 showed different hemagglutinating activity (HA) at 4 °C and room temperature. While all RHDV field strains were identified as hemagglutinating virulent viruses of the RHDVa variant, the vaccine strain was assigned as a “classical” RHDV. These data indicate that since 2003, RHDVa has become the predominant variant circulating in Russia.

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References

  1. Liu SJ, Xue HP, Pu BQ, Quian NH (1984) A new viral disease in rabbits. Anim Husb Vet Med 16:253–255

    Google Scholar 

  2. Abrantes J, van der Loo W, Le Pendu J, Esteves PJ (2012) Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review. Vet Res 43:12. doi:10.1186/1297-9716-43-12

    Article  PubMed  PubMed Central  Google Scholar 

  3. Alda F, Gaitero T, Suárez M, Merchán T, Rocha G, Doadrio I (2010) Evolutionary history and molecular epidemiology of rabbit haemorrhagic disease virus in the Iberian Peninsula and Western Europe. BMC Evol Biol 10:347

    Article  PubMed  PubMed Central  Google Scholar 

  4. Le Gall-Recule G, Zwingelstein F, Laurent S, de Boisseson C, Portejoie Y, Rasschaert D (2003) Phylogenetic analysis of rabbit haemorrhagic disease virus in France between 1993 and 2000, and the characterisation of RHDV antigenic variants. Arch Virol 148:65–81

    Article  PubMed  Google Scholar 

  5. Capucci L, Scicluna MT, Lavazza A (1991) Diagnosis of viral haemorrhagic disease of rabbits and the European brown hare syndrome. Rev Sci Tech 10:347–370

    CAS  PubMed  Google Scholar 

  6. Capucci L, Fusi P, Lavazza A, Pacciarini LM, Rossi C (1996) Detection and preliminary characterization of a new rabbit hemorrhagic disease virus but nonpathogenic. J Virol 70:8614–8623

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Chasey D, Lucas M, Westcott D, Williams M (1992) European brown hare syndrome in the U.K.; a calicivirus related to but distinct from that of viral haemorrhagic disease in rabbits. Arch Virol 124:363–370

    Article  CAS  PubMed  Google Scholar 

  8. Lavazza A, Capucci L (2008) How many caliciviruses are there in rabbits? A review on RHDV and correlated viruses. In: Alves PC, Ferrand N, Hackländer K (eds) Lagomorph biology. Evolution, ecology, and conservation. Springer, Netherlands, pp 263–279. doi:10.1007/978-3-540-72446-9_18

  9. Laurent S, Vautherot JF, Le Gall G, Madelaine MF, Rasschaert D (1997) Structural, antigenic and immunogenic relationships between European brown hare syndrome virus and rabbit haemorrhagic disease virus. J Gen Virol 78:2803–2811

    Article  CAS  PubMed  Google Scholar 

  10. Meyers G, Wirblich C, Thiel HJ (1991) Rabbit hemorrhagic disease virus-molecular cloning and nucleotide sequencing of a calicivirus genome. Virology 184:664–676

    Article  CAS  PubMed  Google Scholar 

  11. Capucci L, Fallacara F, Grazioli S, Lavazza A, Pacciarini ML, Brocchi E (1998) A further step in the evolution of rabbit hemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Res 58:115–126

    Article  CAS  PubMed  Google Scholar 

  12. Schirrmeier H, Reimann I, Kollner B, Granzow H (1999) Pathogenic, antigenic and molecular properties of rabbit haemorrhagic disease virus (RHDV) isolated from vaccinated rabbits: detection and characterization of antigenic variants. Arch Virol 144:719–735

    Article  CAS  PubMed  Google Scholar 

  13. Le Gall-Reculé G, Zwingelstein F, Boucher S, Le Normand B, Plassiart G, Portejoie Y, Decors A, Bertagnoli S, Guérin JL, Marchandeau S (2011) Detection of a new variant of rabbit haemorrhagic disease virus in France. Vet Rec 5:137–138

    Article  Google Scholar 

  14. Le Gall-Reculé G, Lavazza A, Marchandeau S, Bertagnoli S, Zwingelstein F, Cavadini P, Martinelli N, Lombardi G, Guérin JL, Lemaitre E, Decors A, Boucher S, Le Normand B, Capucci L (2013) Emergence of a new lagovirus related to rabbit haemorrhagic disease virus. Vet Res 44:81

    Article  PubMed  PubMed Central  Google Scholar 

  15. Dalton KP, Nicieza I, Balseiro A, Muguerza MA, Rosell JM, Casais R, Álvarez AL, Parra F (2012) Variant rabbit hemorrhagic disease virus in young rabbits, Spain. Emerg Infect Dis 18:2009–2012

    Article  PubMed  PubMed Central  Google Scholar 

  16. Baily JL, Dagleish MP, Graham M, Maley M, Rocchi MS (2014) RHDV variant 2 presence detected in Scotland. Vet Rec 19:174–190

    Google Scholar 

  17. Moss SR, Turner SL, Trout RC, White PJ, Hudson PJ, Desai A, Armesto M, Forrester NL, Gould EA (2002) Molecular epidemiology of rabbit haemorrhagic disease virus. J Gen Virol 83:2461–2467

    Article  CAS  PubMed  Google Scholar 

  18. Vlasov NA (1998) Fiziko-khimicheskie svojstva i antigennaya struktura virusa gemorragicheskoj bolezni krolikov, Doctoral dissertation. VNIIVViM, Pokrov (in Russian)

    Google Scholar 

  19. Gall A, Hoffmann B, Teifke JP, Lange B, Schirrmeier H (2007) Persistence of viral RNA in rabbits which overcome an experimental RHDV infection detected by a highly sensitive multiplex real-time RT-PCR. Vet Microbiol 120:17–32

    Article  CAS  PubMed  Google Scholar 

  20. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (2010) Chapter 2.6.2. Rabbit haemorrhagic disease virus. World Organization for Animal Health, Paris

    Google Scholar 

  21. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  22. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Neill JD (1992) Nucleotide sequence of the capsid protein gene of two serotype of San Miguel sea lion virus: identification of conserved and non conserved amino acid sequences among calicivirus capsid protein. Virus Res 24:211–222

    Article  CAS  PubMed  Google Scholar 

  24. Esteves PJ, Abrantes J, Carneiro M, Muller A, Thompson G, van der Loo W (2008) Detection of positive selection in the major capsid protein VP60 of the rabbit haemorrhagic disease virus (RHDV). Virus Res 137:253–256

    Article  CAS  PubMed  Google Scholar 

  25. Elsworth P, Cooke BD, Kovaliski J, Sinclair R, Holmes EC, Strive T (2014) Increased virulence of rabbit haemorrhagic disease virus associated with genetic resistance in wild Australian rabbits (Oryctolagus cuniculus). Virol Vol 464–465:415–423

    Article  Google Scholar 

  26. Lopes AM, Correia J, Abrantes J, Melo P, Ramada M, Magalhães MJ, Esteves PJ (2015) Is the new variant RHDV replacing genogroup 1 in Portuguese wild rabbit populations? Viruses 7(1):27–36

    Article  Google Scholar 

  27. Mitro S, Kraus H (1993) Rabbit hemorrhagic disease: a review with special reference to its epizootiology. Eur J Epidemiol 9:70–78

    Article  CAS  PubMed  Google Scholar 

  28. Ohlinger VF, Haas B, Meyers G, Weiland F, Thiel HJ (1990) Identification and characterization of the virus causing rabbit hemorrhagic disease. J Virol 64:3331–3336

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Schwensow NI, Cooke B, Kovaliski J, Sinclair R, Peacock D, Fickel J, Sommer S (2014) Rabbit haemorrhagic disease: virus persistence and adaptation in Australia. Evol Appl 7(9):1056–1067

    Article  PubMed  PubMed Central  Google Scholar 

  30. Esteves PJ, Abrantes J, Bertagnoli S, Cavadini P, Gavier-Widén D et al (2015) Emergence of pathogenicity in lagoviruses: evolution from pre-existing nonpathogenic strains or through a species jump? Emergence of pathogenicity in lagoviruses: evolution from pre-existing nonpathogenic strains or through a species jump? PLoS Pathog 11(11):e1005087

    Article  PubMed  PubMed Central  Google Scholar 

  31. McIntosh MT, Behan SC, Mohamed FM, Lu Z, Moran KE, Burrage TG, Neilan JG, Ward GB, Botti G, Capucci L, Metwally SA (2007) A pandemic strain of calicivirus threatens rabbit industries in the Americas. Virol J 4:96–110

    Article  PubMed  PubMed Central  Google Scholar 

  32. Oem JK, Lee KN, Roh IS, Lee KK, Kim SH, Kim HR, Park CK, Joo YS (2009) Identification and characterization of rabbit hemorrhagic disease virus genetic variants isolated in Korea. J Vet Med Sci 71(11):1519–1523

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We acknowledge Edan Tulman and Gustavo Delhon for critical reading the manuscript and useful comments. The authors thank the Russian State Veterinary Service and The All-Russian State Center for Quality and Standardization of Veterinary Drugs and Feed (VGNKI) for providing RHDV strains. Our special thanks to Zhivoderov Sergej, Bobrovskaya Nina, and Glukhareva Elena for help with animal handling, and all technicians involved in these studies. Financial support was provided by the Council of the President of the Russian Federation (grant no. MK-9335.2016.11).

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Authors and Affiliations

  1. Molecular Virology Laboratory, National Research Institute of Veterinary Virology and Microbiology (VNIIVViM), Russian Academy of Agricultural Science, Pokrov, 601125, Russia

    Galina Burmakina, Nina Malogolovkina, Andrey Lunitsin, Ilya Titov, Sodnom Tsybanov & Alexander Malogolovkin

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  1. Galina Burmakina
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Correspondence to Alexander Malogolovkin.

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The authors declare no conflict of interest. None of the authors of this publication have any financial or personal relationships with other people or organizations that could inappropriately influence this work.

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Burmakina, G., Malogolovkina, N., Lunitsin, A. et al. Comparative analysis of rabbit hemorrhagic disease virus strains originating from outbreaks in the Russian Federation. Arch Virol 161, 1973–1979 (2016). https://doi.org/10.1007/s00705-016-2864-1

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  • DOI: https://doi.org/10.1007/s00705-016-2864-1

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