Abstract
Two distinct genotypes responsible for rabbit hemorrhagic disease (RHD) are reported, GI.1 (RHDV) and GI.2 (RHDV2). Vaccines based on these two genotypes are only partially cross-protective. Hence, knowing which genotype is circulating is important for appropriate control measures. We have investigated 25 field samples isolated between 2015 and 2018 from rabbits with clinical signs of RHD. Only GI.2 (RHDV2) is currently circulating in Tunisia. All Tunisian samples were grouped together with typical genotypic and phenotypic mutations. Therefore, we recommend initiating an extensive preventive vaccination program based on GI.2 vaccines in addition to a regular monitoring of the circulating lagoviruses.
References
Meyers G, Wirblich C, Thiel H-J (1991) Genomic and subgenomic RNAs of rabbit hemorrhagic disease virus are both protein-linked and packaged into particles. Virology 184:677–686
Oem J-K, Lee K-N, Roh IS et al (2009) Identification and characterization of rabbit hemorrhagic disease virus genetic variants isolated in Korea. J Vet Med Sci 71:1519–1523
Ohlinger VF, Haas B, Meyers G, Weiland F, Thiel H-J (1990) Identification and characterization of the virus causing rabbit hemorrhagic disease. J Virol 64:6
Le Pendu J, Abrantes J, Bertagnoli S et al (2017) Proposal for a unified classification system and nomenclature of lagoviruses. J Gen Virol 98:1658–1666
Liu SJ, Xue HP, Pu BQ, Qian NH (1984) A new viral disease in rabbits. Anim Husb Vet Med Xumu Yu Shouyi 16:253–255
Kesy A, Fitzner A, Niedbalski W, Paprocka G, Walkowiak B (1996) A new variant of the viral haemorrhagic disease of rabbits virus. Rev Sci Tech Int Off Epizoot 15:1029–1035
Capucci L, Fallacara F, Grazioli S et al (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
Schirrmeier H, Reimann I, Köllner 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
Capucci L, Fusi P, Lavazza A, Pacciarini ML, Rossi C (1996) Detection and preliminary characterization of a new rabbit calicivirus related to rabbit hemorrhagic disease virus but nonpathogenic. J Virol 70:8614–8623
Capucci L, Cavadini P, Schiavitto M, Lombardi G, Lavazza A (2017) Increased pathogenicity in rabbit haemorrhagic disease virus type 2 (RHDV2). Vet Rec 180:426
Dalton KP, Nicieza I, Balseiro A et al (2012) Variant rabbit hemorrhagic disease virus in young rabbits, Spain. Emerg Infect Dis 18:2009–2012
Gall-Reculé GL, Zwingelstein F, Boucher S et al (2011) Detection of a new variant of rabbit haemorrhagic disease virus in France. Vet Rec 168:137–138
Le Gall-Reculé G, Lavazza A, Marchandeau S et al (2013) Emergence of a new lagovirus related to rabbit haemorrhagic disease virus. Vet Res 44:81
Lopes AM, Correia J, Abrantes J et al (2015) Is the new variant RHDV replacing genogroup 1 in Portuguese wild rabbit populations? Viruses 7:27–36
Mahar JE, Hall RN, Peacock D et al (2018) Rabbit hemorrhagic disease virus 2 (RHDV2; GI.2) is replacing endemic strains of RHDV in the Australian landscape within 18 months of its arrival. J Virol 92:e01374-17
Neimanis AS, Ahola H, Zohari S et al (2018) Arrival of rabbit haemorrhagic disease virus 2 to northern Europe: Emergence and outbreaks in wild and domestic rabbits (Oryctolagus cuniculus) in Sweden. Transbound Emerg Dis 65:213–220
Fitzner A, Niedbalski W (2017) Phylogenetic analysis of rabbit haemorrhagic disease virus (RHDV) strains isolated in Poland. Arch Virol 162:3197–3203
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
WOAH (2015) Rabbit haemorrhagic disease. https://www.oie.int/fileadmin/Home/eng/Animal_Health_in_the_World/docs/pdf/Disease_cards/RHD.pdf
Ben Slimen H, Suchentrunk F, Memmi A, Ben Ammar Elgaaied A (2005) Biochemical genetic relationships among Tunisian hares (Lepus sp.), South African cape hares (L. capensis), and European brown hares (L. europaeus). Biochem Genet 43:577–596. https://doi.org/10.1007/s10528-005-9115-6
Lebas F, Bolet G (2008) Impressions sur l’élevage du Lapin en Tunisie. Cunicult Mag 35:68–76
Bouslama A, Mia GMD, Hammami S et al (1996) Identification of the virus of rabbit haemorrhagic disease in Tunisia. Vet Rec 138:108–110
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
WOAH (2015) Rabbit haemorrhagic disease, Benin. http://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport&reportid=19109
Martin-Alonso A, Martin-Carrillo N, Garcia-Livia K, Valladares B, Foronda P (2016) Emerging rabbit haemorrhagic disease virus 2 (RHDV2) at the gates of the African continent. Infect Genet Evol 44:46–50
Lopes AM, Rouco C, Esteves PJ, Abrantes J (2019) GI.1b/GI.1b/GI.2 recombinant rabbit hemorrhagic disease virus 2 (Lagovirus europaeus/GI.2) in Morocco, Africa. Arch Virol 164:279–283
Chakroun C, Ben Hamouda W, Khaled K, Sghaier S (2015) La nouvelle forme de la maladie hémorragique virale (VHD en Tunisie due au virus variant). Group Interprofessionnel ProdAvic Cunic GIPAC Bull Inf Avic 56:23–26
Peacock D, Kovaliski J, Sinclair R, Mutze G, Iannella A, Capucci L (2017) RHDV2 overcoming RHDV immunity in wild rabbits (Oryctolagus cuniculus) in Australia. Vet Rec 180:280
Acknowledgments
We would like to acknowledge the highly valuable help of Prof. Helmi Mardassi for providing us sequencing reagents, Mrs. Dhouha Haj Slimène (MMVDB) and Mrs. Roukaya Yaakoubi (LTCI) for helping with the nucleotide sequencing experiments, and Mrs. Neila Khabouchi for technical assistance with automated sequencing. Finally, we would like to strongly thank the Veterinary Service of the Tunisian Ministry of Agriculture and Water Resources and the veterinary practitioners who performed and collected biopsy samples from the field. We would like to acknowledge the help of Mrs. Peggy Weiss, a USA native and an English language teacher in AMIDEAST, Tunis, Tunisia, for language editing of the manuscript.
Author information
Authors and Affiliations
Contributions
NR performed all molecular biology experiments and phylogenetic analysis and was involved in the manuscript. SS provided the liver biopsies and helped in drafting of the manuscript. HK and AZ participated in molecular biology experiments. CB contributed by designing the work, drafting the manuscript, and carrying out the phylogenetic analysis.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Reimar Johne.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rahali, N., Sghaier, S., Kbaier, H. et al. Genetic characterization and phylogenetic analysis of rabbit hemorrhagic disease virus isolated in Tunisia from 2015 to 2018. Arch Virol 164, 2327–2332 (2019). https://doi.org/10.1007/s00705-019-04311-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-019-04311-z