1887

Abstract

Lagoviruses belong to the Caliciviridae family. They were first recognized as highly pathogenic viruses of the European rabbit (Oryctolagus cuniculus) and European brown hare (Lepus europaeus) that emerged in the 1970–1980s, namely, rabbit haemorrhagic disease virus (RHDV) and European brown hare syndrome virus (EBHSV), according to the host species from which they had been first detected. However, the diversity of lagoviruses has recently expanded to include new related viruses with varying pathogenicity, geographic distribution and host ranges. Together with the frequent recombination observed amongst circulating viruses, there is a clear need to establish precise guidelines for classifying and naming lagovirus strains. Therefore, here we propose a new nomenclature based on phylogenetic relationships. In this new nomenclature, a single species of lagovirus would be recognized and called Lagovirus europaeus. The species would be divided into two genogroups that correspond to RHDV- and EBHSV-related viruses, respectively. Genogroups could be subdivided into genotypes, which could themselves be subdivided into phylogenetically well-supported variants. Based on available sequences, pairwise distance cutoffs have been defined, but with the accumulation of new sequences these cutoffs may need to be revised. We propose that an international working group could coordinate the nomenclature of lagoviruses and any proposals for revision.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000840
2017-07-17
2019-11-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/7/1658.html?itemId=/content/journal/jgv/10.1099/jgv.0.000840&mimeType=html&fmt=ahah

References

  1. Gavier-Widén D, Mörner T. Epidemiology and diagnosis of the european brown hare syndrome in scandinavian countries: a review. Rev Sci Tech 1991;10:453–458 [CrossRef][PubMed]
    [Google Scholar]
  2. Liu SJ, Xue HP, Bq P, Quian NH. A new viral disease in rabbit. Anim Husb Vet Med 1984;16:235–255
    [Google Scholar]
  3. Marcato PS, Benazzi C, Vecchi G, Galeotti M, della Salda L et al. Clinical and pathological features of viral haemorrhagic disease of rabbits and the european brown hare syndrome. Rev Sci Tech 1991;10:371–392 [CrossRef][PubMed]
    [Google Scholar]
  4. Abrantes J, van der Loo W, Le Pendu J, Esteves PJ. Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review. Vet Res 2012;43:12–19 [CrossRef][PubMed]
    [Google Scholar]
  5. Parra F, Prieto M. Purification and characterization of a calicivirus as the causative agent of a lethal hemorrhagic disease in rabbits. J Virol 1990;64:4013–4015[PubMed]
    [Google Scholar]
  6. Ohlinger VF, Haas B, Meyers G, Weiland F, Thiel HJ. Identification and characterization of the virus causing rabbit hemorrhagic disease. J Virol 1990;64:3331–3336[PubMed]
    [Google Scholar]
  7. Lavazza A, Vecchi G. Osservazioni su alcuni episodi di mortalità nelle lepri. Evidenziazione Al Microscopio Elettronico Di Una particella virale. Nota Preliminare Sel Vet 1989;30:461–467
    [Google Scholar]
  8. Eskens U, Volmer K. Untersuchungen zur ätiologie der leberdystrophie des feldhasen (Lepus europaeus Pallas). Dtsch Tierärztl Wochenschr 1989;96:433–472
    [Google Scholar]
  9. Rodák L, Smíd B, Valícek L, Veselý T, Stĕpánek J et al. Enzyme-linked immunosorbent assay of antibodies to rabbit haemorrhagic disease virus and determination of its major structural proteins. J Gen Virol 1990;71:1075–1080 [CrossRef][PubMed]
    [Google Scholar]
  10. Capucci L, Scicluna MT, Lavazza A. Diagnosis of viral haemorrhagic disease of rabbits and the european brown hare syndrome. Rev Sci Tech 1991;10:347–370 [CrossRef][PubMed]
    [Google Scholar]
  11. Wirblich C, Meyers G, Ohlinger VF, Capucci L, Eskens U et al. European brown Hare syndrome virus: relationship to rabbit hemorrhagic disease virus and other caliciviruses. J Virol 1994;68:5164–5173[PubMed]
    [Google Scholar]
  12. Meyers G, Wirblich C, Thiel HJ. Rabbit hemorrhagic disease virus-molecular cloning and nucleotide sequencing of a calicivirus genome. Virology 1991;184:664–676 [CrossRef][PubMed]
    [Google Scholar]
  13. Capucci L, Fusi P, Lavazza A, Pacciarini ML, Rossi C. Detection and preliminary characterization of a new rabbit calicivirus related to rabbit hemorrhagic disease virus but nonpathogenic. J Virol 1996;70:8614–8623[PubMed]
    [Google Scholar]
  14. Le Gall-Reculé G, Zwingelstein F, Fages MP, Bertagnoli S, Gelfi J et al. Characterisation of a non-pathogenic and non-protective infectious rabbit lagovirus related to RHDV. Virology 2011;410:395–402 [CrossRef][PubMed]
    [Google Scholar]
  15. Strive T, Wright JD, Robinson AJ. Identification and partial characterisation of a new Lagovirus in Australian wild rabbits. Virology 2009;384:97–105 [CrossRef][PubMed]
    [Google Scholar]
  16. Forrester NL, Trout RC, Gould EA. Benign circulation of rabbit haemorrhagic disease virus on Lambay Island, Eire. Virology 2007;358:18–22 [CrossRef][PubMed]
    [Google Scholar]
  17. Mahar JE, Nicholson L, Eden JS, Duchêne S, Kerr PJ et al. Benign rabbit caliciviruses exhibit evolutionary dynamics similar to those of their virulent relatives. J Virol 2016;90:9317–9329 [CrossRef][PubMed]
    [Google Scholar]
  18. Capucci L, Fallacara F, Grazioli S, Lavazza A, Pacciarini ML et al. A further step in the evolution of rabbit hemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Res 1998;58:115–126 [CrossRef][PubMed]
    [Google Scholar]
  19. Le Gall-Reculé G, Zwingelstein F, Boucher S, Le Normand B, Plassiart G et al. Detection of a new variant of rabbit haemorrhagic disease virus in France. Vet Rec 2011;168:137–138 [CrossRef][PubMed]
    [Google Scholar]
  20. Dalton KP, Nicieza I, Abrantes J, Esteves PJ, Parra F. Spread of new variant RHDV in domestic rabbits on the Iberian Peninsula. Vet Microbiol 2014;169:67–73 [CrossRef][PubMed]
    [Google Scholar]
  21. Le Gall-Reculé G, Lavazza A, Marchandeau S, Bertagnoli S, Zwingelstein F et al. Emergence of a new lagovirus related to Rabbit Haemorrhagic Disease Virus. Vet Res 2013;44:81 [CrossRef][PubMed]
    [Google Scholar]
  22. Lopes AM, Correia J, Abrantes J, Melo P, Ramada M et al. Is the new variant RHDV replacing genogroup 1 in Portuguese wild rabbit populations?. Viruses 2014;7:27–36 [CrossRef][PubMed]
    [Google Scholar]
  23. Calvete C, Sarto P, Calvo AJ, Monroy F, Calvo JH. Letter – Could the new rabbit haemorrhagic disease virus variant (RHDVb) be fully replacing classical RHD strains in the Iberian Peninsula?. World Rabbit Science 2014;22:91 [CrossRef]
    [Google Scholar]
  24. Dalton KP, Nicieza I, Balseiro A, Muguerza MA, Rosell JM et al. Variant rabbit hemorrhagic disease virus in young rabbits, Spain. Emerg Infect Dis 2012;18:2009–2012 [CrossRef][PubMed]
    [Google Scholar]
  25. Le Gall-Reculé G, Zwingelstein F, Laurent S, de Boisséson C, Portejoie Y et al. Phylogenetic analysis of rabbit haemorrhagic disease virus in France between 1993 and 2000, and the characterisation of RHDV antigenic variants. Arch Virol 2003;148:65–81 [CrossRef][PubMed]
    [Google Scholar]
  26. Kerr PJ, Kitchen A, Holmes EC. Origin and phylodynamics of rabbit hemorrhagic disease virus. J Virol 2009;83:12129–12138 [CrossRef][PubMed]
    [Google Scholar]
  27. Strive T, Wright J, Kovaliski J, Botti G, Capucci L. The non-pathogenic Australian Lagovirus RCV-A1 causes a prolonged infection and elicits partial cross-protection to rabbit haemorrhagic disease virus. Virology 2010;398:125–134 [CrossRef][PubMed]
    [Google Scholar]
  28. Le Gall-Reculé G, Lemaitre E, Briand F-X, Marchandeau S. Characterization in France of non-pathogenic lagoviruses closely related to the Australian Rabbit calicivirus RCV-A1: confirmation of the European origin of RCV-A1. In Xth International Congress for Veterinary Virology Changing Viruses in a Changing World France: Montpellier; 2015; pp.183–185
    [Google Scholar]
  29. Moss SR, Turner SL, Trout RC, White PJ, Hudson PJ et al. Molecular epidemiology of rabbit haemorrhagic disease virus. J Gen Virol 2002;83:2461–2467 [CrossRef][PubMed]
    [Google Scholar]
  30. Bergin IL, Wise AG, Bolin SR, Mullaney TP, Kiupel M et al. Novel calicivirus identified in rabbits, Michigan, USA. Emerg Infect Dis 2009;15:1955–1962 [CrossRef][PubMed]
    [Google Scholar]
  31. Abrantes J, Esteves PJ. Not-so-novel Michigan rabbit calicivirus. Emerg Infect Dis 2010;16:1331–1332 [CrossRef][PubMed]
    [Google Scholar]
  32. Puggioni G, Cavadini P, Maestrale C, Scivoli R, Botti G et al. The new French 2010 rabbit hemorrhagic disease virus causes an RHD-like disease in the Sardinian Cape hare (Lepus capensis mediterraneus). Vet Res 2013;44:96 [CrossRef][PubMed]
    [Google Scholar]
  33. Le Gall-Reculé G, Zwingelstein F, Laurent S, Portejoie Y, Rasschaert D. Molecular epidemiology of European brown hare syndrome virus in France between 1989 and 2003. Arch Virol 2006;151:1713–1721 [CrossRef][PubMed]
    [Google Scholar]
  34. Lopes AM, Capucci L, Gavier-Widén D, Le Gall-Reculé G, Brocchi E et al. Molecular evolution and antigenic variation of European brown hare syndrome virus (EBHSV). Virology 2014;468-470:104–112 [CrossRef][PubMed]
    [Google Scholar]
  35. Cavadini P, Molinari S, Pezzoni G, Chiari M, Brocchi E et al. Identification of a new non-pathogenic lagovirus in brown hares (Lepus europeaus). In Kelly P, Phillips S, Smith A, Browning C. (editors) 5th World Lagomorph Conference Turlock, CA: California State University Stanislaus; 2016
    [Google Scholar]
  36. Abrantes J, Esteves PJ, van der Loo W. Evidence for recombination in the major capsid gene VP60 of the rabbit haemorrhagic disease virus (RHDV). Arch Virol 2008;153:329–335 [CrossRef][PubMed]
    [Google Scholar]
  37. Forrester NL, Moss SR, Turner SL, Schirrmeier H, Gould EA. Recombination in rabbit haemorrhagic disease virus: possible impact on evolution and epidemiology. Virology 2008;376:390–396 [CrossRef][PubMed]
    [Google Scholar]
  38. Lopes AM, Dalton KP, Magalhães MJ, Parra F, Esteves PJ et al. Full genomic analysis of new variant rabbit hemorrhagic disease virus revealed multiple recombination events. J Gen Virol 2015;96:1309–1319 [CrossRef][PubMed]
    [Google Scholar]
  39. Hu B, Wang F, Fan Z, Song Y, Abrantes J et al. Recombination between G2 and G6 strains of rabbit hemorrhagic disease virus (RHDV) in China. Arch Virol 2017;162:269–272 [CrossRef][PubMed]
    [Google Scholar]
  40. Clarke IN, Estes MK, Green KY, Hansman GS, Knowles NJ et al. Family Caliciviridae. In King AMQ, Adams MJ, Carstens EB. (editors) Virus Taxonomy Classification and Nomenclature of Viruses Ninth Report of the International Committee on Taxonomy of Viruses Lefkowitz, EJ: Elsevier Academic Press; 2012
    [Google Scholar]
  41. Strive T, Elsworth P, Liu J, Wright JD, Kovaliski J et al. The non-pathogenic Australian rabbit calicivirus RCV-A1 provides temporal and partial cross protection to lethal rabbit haemorrhagic disease virus infection which is not dependent on antibody titres. Vet Res 2013;44:51 [CrossRef][PubMed]
    [Google Scholar]
  42. Nyström K, Le Gall-Reculé G, Grassi P, Abrantes J, Ruvoën-Clouet N et al. Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PLoS Pathog 2011;7:e1002188 [CrossRef][PubMed]
    [Google Scholar]
  43. Lopes AM, Marques S, Silva E, Magalhães MJ, Pinheiro A et al. Detection of RHDV strains in the Iberian hare (Lepus granatensis): earliest evidence of rabbit lagovirus cross-species infection. Vet Res 2014;45:94 [CrossRef][PubMed]
    [Google Scholar]
  44. Camarda A, Pugliese N, Cavadini P, Circella E, Capucci L et al. Detection of the new emerging rabbit haemorrhagic disease type 2 virus (RHDV2) in Sicily from rabbit (Oryctolagus cuniculus) and Italian hare (Lepus corsicanus). Res Vet Sci 2014;97:642–645 [CrossRef][PubMed]
    [Google Scholar]
  45. Velarde R, Cavadini P, Neimanis A, Cabezón O, Chiari M et al. Spillover events of infection of brown hares (Lepus europaeus) with rabbit haemorrhagic disease type 2 virus (RHDV2) Caused sporadic cases of an European brown hare syndrome-like disease in Italy and Spain. Transbound Emerg Dis 2016; [CrossRef][PubMed]
    [Google Scholar]
  46. Hall RN, Peacock DE, Kovaliski J, Mahar JE, Mourant R et al. Detection of RHDV2 in European brown hares (Lepus europaeus) in Australia. Vet Rec 2017;180:121.2–12121 [CrossRef]
    [Google Scholar]
  47. Le Gall-Reculé G, Lemaitre E, Bertagnoli S, Hubert C, Top S et al. Large scale detection of the rabbit haemorrhagic disease virus RHDV2 in European hare (Lepus europaeus) populations in France causing European brown hare syndrome EBHS-like outbreaks. In Kelly P, Phillips S, Smith A, Browning C. (editors) 5th World Lagomorph Conference Turlock, CA: California State University Stanislaus; 2016; pp.68
    [Google Scholar]
  48. Ellertz I. Rabbit hemorrhagic disease – Sweden: (Skane) mountain hare, OIE. OIE, WAHID (World Animal Health Information Database 2017
    [Google Scholar]
  49. Guberti V, De Marco AM, Riga F, Lavazza A, Trocchi V et al. Virology and species conservation: the case of EBHSV and the Italian hare (Lepus corsicanus). In Vth International Congress of Veterinary Virology Brescia: Italy; 2000; pp.198–199
    [Google Scholar]
  50. Syrjälä P, Nylund M, Heinikainen S. European brown hare syndrome in free-living mountain hares (Lepus timidus) and European brown hares (Lepus europaeus) in Finland 1990–2002. J Wildl Dis 2005;41:42–47 [CrossRef][PubMed]
    [Google Scholar]
  51. Frölich K, Haerer G, Bacciarini L, Janovsky M, Rudolph M et al. European brown hare syndrome in free-ranging European brown and mountain hares from Switzerland. J Wildl Dis 2001;37:803–807 [CrossRef][PubMed]
    [Google Scholar]
  52. Lavazza A, Cavadini P, Barbieri I, Tizzani P, Pinheiro A et al. Field and experimental data indicate that the eastern cottontail (Sylvilagus floridanus) is susceptible to infection with European brown hare syndrome (EBHS) virus and not with rabbit haemorrhagic disease (RHD) virus. Vet Res 2015;46:13 [CrossRef][PubMed]
    [Google Scholar]
  53. Sasse C. Ecological consequences of the introduction of the American cottontail, Sylvilagus floridanus, into Europe. Report Council of Europe SN-US, 83 Leersum, The Netherlands: Research Institute for Nature Management; 1983; pp.33
    [Google Scholar]
  54. Esteves PJ, Abrantes J, Bertagnoli S, Cavadini P, Gavier-Widén D et al. Emergence of pathogenicity in lagoviruses: evolution from pre-existing nonpathogenic strains or through a species Jump?. PLoS Pathog 2015;11:e1005087 [CrossRef][PubMed]
    [Google Scholar]
  55. Merchán T, Rocha G, Alda F, Silva E, Thompson G et al. Detection of rabbit haemorrhagic disease virus (RHDV) in nonspecific vertebrate hosts sympatric to the European wild rabbit (Oryctolagus cuniculus). Infect Genet Evol 2011;11:1469–1474 [CrossRef][PubMed]
    [Google Scholar]
  56. Rocha G, Alda F, Pagés A, Merchán T. Experimental transmission of rabbit haemorrhagic disease virus (RHDV) from rabbit to wild mice (Mus spretus and Apodemus sylvaticus) under laboratory conditions. Infect Genet Evol 2017;47:94–98 [CrossRef][PubMed]
    [Google Scholar]
  57. Kroneman A, Vega E, Vennema H, Vinjé J, White PA et al. Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 2013;158:2059–2068 [CrossRef][PubMed]
    [Google Scholar]
  58. Smíd B, Valícek L, Stĕpánek J, Jurák E, Rodák L. Experimental transmission and electron microscopic demonstration of the virus of haemorrhagic disease of rabbits in Czechoslovakia. Zentralbl Veterinarmed B 1989;36:237–240 [CrossRef][PubMed]
    [Google Scholar]
  59. Ohlinger VF, Haas B, Ahl R, Weiland F. Die infektiöse hämorrhagische Kranheit der Kaninchen: eine Durch ein calicivirus verursachte tierseuche. Tieräztl Umsch 1989;44:284–294
    [Google Scholar]
  60. Plana Duran J, Vayreda Casadevall M, Baston Prat M, Molas V X. Calicivirus: firme candidato como agente inductor de la enfermedad vírica hemorrágica del conejo. Med Vet 1989;6:87–88
    [Google Scholar]
  61. Kuhn JH, Bào Y, Bavari S, Becker S, Bradfute S et al. Virus nomenclature below the species level: a standardized nomenclature for filovirus strains and variants rescued from cDNA. Arch Virol 2014;159:1229–1237 [CrossRef][PubMed]
    [Google Scholar]
  62. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  63. Jahnke M, Holmes EC, Kerr PJ, Wright JD, Strive T. Evolution and phylogeography of the nonpathogenic calicivirus RCV-A1 in wild rabbits in Australia. J Virol 2010;84:12397–12404 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000840
Loading
/content/journal/jgv/10.1099/jgv.0.000840
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error