Abstract
European brown hare syndrome (EBHS) is characterised by high mortality of European brown hares (Lepus europaeus) and mountain hares (Lepus timidus). European brown hare syndrome virus (EBHSV) and the closely related rabbit haemorrhagic disease virus (RHDV) comprise the genus Lagovirus, family Caliciviridae. In contrast to RHDV, which is well studied, with more than 30 complete genome sequences available, the only complete genome sequence available for EBHSV was obtained from a strain isolated in 1989 in France. EBHS was originally diagnosed in Sweden in 1980. Here, we report the complete coding sequences of two EBHSV strains isolated from European brown hares that died with liver lesions characteristic of EBHS in Sweden in 1982. These sequences represent the oldest complete coding sequences of EBHSV isolated from the original area of virus diagnosis. The genomic organisation is similar to that of the published French sequence. Comparison with this sequence revealed several nucleotide substitutions, corresponding to 6 % divergence. At the amino acid level, the Swedish strains are 2 % different from the French strain. Most amino acid substitutions were located within the major capsid protein VP60, but when considering the amino acid sequence length of each protein, VP10 is the protein with the highest percentage of amino acid differences. The same result was obtained when Swedish strains were compared. This evolutionary pattern has not been described previously for members of the genus Lagovirus.
Similar content being viewed by others
References
Abrantes J, Esteves PJ, van der Loo W (2008) Evidence for recombination in the major capsid gene VP60 of the rabbit haemorrhagic disease virus (RHDV). Arch Virol 153:329–335
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
Bascunana CR, Nowotny N, Belak S (1997) Detection and differentiation of rabbit hemorrhagic disease and European brown hare syndrome viruses by amplification of VP60 genomic sequences from fresh and fixed tissue specimens. J Clin Microbiol 35:2492–2495
Billinis C, Psychas V, Tontis DK, Spyrou V, Birtsas PK, Sofia M, Likotrafitis F, Maslarinou OM, Kanteres D (2005) European brown hare syndrome in wild European brown hares from Greece. J Wildl Dis 41:783–786
Cancellotti FM, Renzi M (1991) Epidemiology and current situation of viral haemorrhagic disease of rabbits and the European brown hare syndrome in Italy. Rev Sci Tech 10:409–422
Chasey D, Duff P (1990) European brown hare syndrome and associated virus particles in the UK. Vet Rec 126:623–624
Drews B, Szentiks CA, Roellig K, Fickel J, Schroeder K, Duff JP, Lavazza A, Hildebrandt TB, Goeritz F (2011) Epidemiology, control and management of an EBHS outbreak in captive hares. Vet Microbiol 154:37–48
Duff JP, Chasey D, Munro R, Wooldridge M (1994) European brown hare syndrome in England. Vet Rec 134:669–673
Duff JP, Whitwell K, Chase D (1997) The emergence and epidemiology of European brown hare syndrome in the UK. In: 1st International Symposium on Caliciviruses ESVV, Reading, UK, pp 176–181
Forrester NL, Moss SR, Turner SL, Schirrmeier H, Gould EA (2008) Recombination in rabbit haemorrhagic disease virus: possible impact on evolution and epidemiology. Virology 376:390–396
Frolich K, Meyer HH, Pielowski Z, Ronsholt L, von Seck-Lanzendorf S, Stolte M (1996) European brown hare syndrome in free-ranging hares in Poland. J Wildl Dis 32:280–285
Frolich K, Haerer G, Bacciarini L, Janovsky M, Rudolph M, Giacometti M (2001) European brown hare syndrome in free-ranging European brown and mountain hares from Switzerland. J Wildl Dis 37:803–807
Frolich K, Kujawski OE, Rudolph M, Ronsholt L, Speck S (2003) European brown hare syndrome virus in free-ranging European brown hares from Argentina. J Wildl Dis 39:121–124
Frolich K, Fickel J, Ludwig A, Lieckfeldt D, Streich WJ, Jurcik R, Slamecka J, Wibbelt G (2007) New variants of European brown hare syndrome virus strains in free-ranging European brown hares (Lepus europaeus) from Slovakia. J Wildl Dis 43:89–96
Gavier-Widen D, Morner T (1991) Epidemiology and diagnosis of the European brown hare syndrome in Scandinavian countries: a review. Rev Sci Tech 10:453–458
Gavier-Widen D (1994) Morphologic and immunohistochemical characterization of the hepatic lesions associated with European brown hare syndrome. Vet Pathol 31:327–334
Le Gall-Recule G, Zwingelstein F, Laurent S, Portejoie Y, Rasschaert D (2006) Molecular epidemiology of European brown hare syndrome virus in France between 1989 and 2003. Arch Virol 151:1713–1721
Le Gall G, Huguet S, Vende P, Vautherot JF, Rasschaert D (1996) European brown hare syndrome virus: molecular cloning and sequencing of the genome. J Gen Virol 77(Pt 8):1693–1697
Lenghaus C, Studdert M, Gavier-Widen D (2001) Calicivirus infections. In: Baker IK, Williams ES (eds) Infectious diseases of wild mammals. Wiley, New York, pp 280–291
Loliger HC, Eskens U (1991) Incidence, epizootiology and control of viral haemorrhagic disease of rabbits and the European brown hare syndrome in Germany. Rev Sci Tech 10:423–434
MacLeod NS, Greig A, Nettleton PF (1992) Suspected European brown hare syndrome in Scotland. Vet Rec 130:543
Meyers G, Wirblich C, Thiel HJ, Thumfart JO (2000) Rabbit hemorrhagic disease virus: genome organization and polyprotein processing of a calicivirus studied after transient expression of cDNA constructs. Virology 276:349–363
Salmela P, Belak K, Gavier-Widen D (1993) The occurrence of European brown hare syndrome in Finland. Acta Vet Scand 34:215–217
Wirblich C, Meyers G, Ohlinger VF, Capucci L, Eskens U, Haas B, Thiel HJ (1994) European brown hare syndrome virus: relationship to rabbit hemorrhagic disease virus and other caliciviruses. J Virol 68:5164–5173
Wirblich C, Sibilia M, Boniotti MB, Rossi C, Thiel HJ, Meyers G (1995) 3C-like protease of rabbit hemorrhagic disease virus: identification of cleavage sites in the ORF1 polyprotein and analysis of cleavage specificity. J Virol 69:7159–7168
Acknowledgments
The Portuguese Foundation for Science and Technology (FCT) supported the doctoral fellowship of Ana M. Lopes (SFRH/BD/78738/2011) and the postdoctoral fellowship of Joana Abrantes (SFRH/BPD/73512/2010). The FCT Project PTDC/CVT/108490/2008 supported this work.
Conflict of interest
None of the authors has any personal or financial conflict of interest that would bias the results of this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lopes, A.M., Gavier-Widén, D., Le Gall-Reculé, G. et al. Complete coding sequences of European brown hare syndrome virus (EBHSV) strains isolated in 1982 in Sweden. Arch Virol 158, 2193–2196 (2013). https://doi.org/10.1007/s00705-013-1714-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-013-1714-7