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GI.1b/GI.1b/GI.2 recombinant rabbit hemorrhagic disease virus 2 (Lagovirus europaeus/GI.2) in Morocco, Africa

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Abstract

Rabbit hemorrhagic disease virus (RHDV) is highly lethal to the European rabbit (Oryctolagus cuniculus). It was first reported in 1984 in China, but in 2010, a new variant of the virus was detected (GI.2) in France. Several recombination events with pathogenic and non-pathogenic strains have been described. Here, we report the first sequences of RHDV in Africa, isolated from Moroccan rabbits, and these resemble GI.1b/GI.1b/GI.2 recombinants found in the Iberian Peninsula. Monitoring and characterization of strains from future outbreaks are advised to guarantee the success of current programs on small-rabbit production for poverty alleviation in African countries.

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References

  1. 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

    Article  PubMed  PubMed Central  Google Scholar 

  2. Almeida T, Lopes AM, Magalhaes MJ, Neves F, Pinheiro A, Goncalves D, Leitao M, Esteves PJ, Abrantes J (2015) Tracking the evolution of the G1/RHDVb recombinant strains introduced from the Iberian Peninsula to the Azores islands, Portugal. Infect Genet Evol 34:307–313

    Article  PubMed  Google Scholar 

  3. Calvete C, Sarto P, Calvo AJ, Monroy F, Calvo JH (2014) Could the new rabbit haemorrhagic disease virus variant (RHDVb) be fully replacing classical RHD strains in the Iberian Peninsula? World Rabbit Sci 22:91

    Article  Google Scholar 

  4. Camarda A, Pugliese N, Cavadini P, Circella E, Capucci L, Caroli A, Legretto M, Mallia E, Lavazza A (2014) 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 97:642–645

    Article  PubMed  CAS  Google Scholar 

  5. Dalton KP, Nicieza I, Balseiro A, Muguerza MA, Rosell JM, Casais R, Alvarez 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 

  6. Hall RN, Mahar JE, Haboury S, Stevens V, Holmes EC, Strive T (2015) Emerging rabbit hemorrhagic disease virus 2 (RHDVb), Australia. Emerg Infect Dis 21:2276–2278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Hall RN, Mahar JE, Read AJ, Mourant R, Piper M, Huang N, Strive T (2018) A strain-specific multiplex RT-PCR for Australian rabbit haemorrhagic disease viruses uncovers a new recombinant virus variant in rabbits and hares. Transbound Emerg Dis 65:e444–e456

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  9. Le Gall-Recule G, Lemaitre E, Bertagnoli S, Hubert C, Top S, Decors A, Marchandeau S, Guitton JS (2017) Large-scale lagovirus disease outbreaks in European brown hares (Lepus europaeus) in France caused by RHDV2 strains spatially shared with rabbits (Oryctolagus cuniculus). Vet Res 48:70

    Article  PubMed  PubMed Central  Google Scholar 

  10. Le Gall-Reculé 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  CAS  Google Scholar 

  11. Le Gall-Reculé G, Zwingelstein F, Boucher S, Le Normand B, Plassiart G, Portejoie Y, Decors A, Bertagnoli S, Guerin JL, Marchandeau S (2011) Detection of a new variant of rabbit haemorrhagic disease virus in France. Vet Rec 168:137–138

    Article  PubMed  Google Scholar 

  12. Le Gall-Reculé G, Lavazza A, Marchandeau S, Bertagnoli S, Zwingelstein F, Cavadini P, Martinelli N, Lombardi G, Guerin 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  CAS  Google Scholar 

  13. Le Pendu J, Abrantes J, Bertagnoli S, Guitton JS, Le Gall-Recule G, Lopes AM, Marchandeau S, Alda F, Almeida T, Celio AP, Barcena J, Burmakina G, Blanco E, Calvete C, Cavadini P, Cooke B, Dalton K, Delibes Mateos M, Deptula W, Eden JS, Wang F, Ferreira CC, Ferreira P, Foronda P, Goncalves D, Gavier-Widen D, Hall R, Hukowska-Szematowicz B, Kerr P, Kovaliski J, Lavazza A, Mahar J, Malogolovkin A, Marques RM, Marques S, Martin-Alonso A, Monterroso P, Moreno S, Mutze G, Neimanis A, Niedzwiedzka-Rystwej P, Peacock D, Parra F, Rocchi M, Rouco C, Ruvoen-Clouet N, Silva E, Silverio D, Strive T, Thompson G, Tokarz-Deptula B, Esteves P (2017) Proposal for a unified classification system and nomenclature of lagoviruses. J Gen Virol 98:1658–1666

    Article  PubMed  CAS  Google Scholar 

  14. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160

    PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. Lopes AM, Dalton KP, Magalhaes MJ, Parra F, Esteves PJ, Holmes EC, Abrantes J (2015) Full genomic analysis of new variant rabbit hemorrhagic disease virus revealed multiple recombination events. J Gen Virol 96:1309–1319

    Article  PubMed  CAS  Google Scholar 

  17. Lopes AM, Blanco-Aguiar J, Martin-Alonso A, Leitao M, Foronda P, Mendes M, Goncalves D, Abrantes J, Esteves PJ (2018) Full genome sequences are key to disclose RHDV2 emergence in the Macaronesian islands. Virus Genes 54:1–4

    Article  PubMed  CAS  Google Scholar 

  18. Mahar JE, Hall RN, Peacock D, Kovaliski J, Piper M, Mourant R, Huang N, Campbell S, Gu X, Read A, Urakova N, Cox T, Holmes EC, Strive T (2017) Rabbit haemorrhagic disease virus 2 (GI.2) is replacing endemic strains of RHDV in the Australian landscape within 18 months of its arrival. J Virol. https://doi.org/10.1128/JVI.01374-17

    Article  PubMed  Google Scholar 

  19. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Morisse JP, Le Gall G, Boilletot E (1991) Hepatitis of viral origin in Leporidae: introduction and aetiological hypotheses. Rev Sci Tech 10:283–295

    Article  Google Scholar 

  21. Oseni SO, Lukefahr SD (2014) Rabbit production in low-input systems in Africa: situation, knowledge and perspectives—a review. World Rabbit Sci 22:147–160

    Article  Google Scholar 

  22. Puggioni G, Cavadini P, Maestrale C, Scivoli R, Botti G, Ligios C, Le Gall-Reculé G, Lavazza A, Capucci L (2013) The new French 2010 Rabbit Hemorrhagic Disease Virus causes an RHD-like disease in the Sardinian Cape hare (Lepus capensis mediterraneus). Vet Res 44:96

    Article  PubMed  PubMed Central  Google Scholar 

  23. Rouco C, Abrantes J, Serronha A, Lopes AM, Maio E, Magalhaes MJ, Blanco E, Barcena J, Esteves PJ, Santos N, Alves PC, Monterroso P (2018) Epidemiology of RHDV2 (Lagovirus europaeus/GI.2) in free-living wild European rabbits in Portugal. Transbound Emerg Dis 65:e373–e382

    Article  PubMed  CAS  Google Scholar 

  24. Silvério D, Lopes AM, Melo-Ferreira J, Magalhães MJ, Monterroso P, Serronha A, Maio E, Alves PC, Esteves PJ, Abrantes J (2018) Insights into the evolution of the new variant rabbit haemorrhagic disease virus (GI.2) and the identification of novel recombinant strains. Transbound Emerg Dis 65:983–992

    Article  PubMed  CAS  Google Scholar 

  25. Soriguer RC (1981) Biologia y dinamica de una populacion de conejos (Oryctolagus cuniculus L.) en Andalucia Occidental. Rev Verterbrados Estac Biol Doñana 8–3:379

    Google Scholar 

  26. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Velarde R, Cavadini P, Neimanis A, Cabezon O, Chiari M, Gaffuri A, Lavin S, Grilli G, Gavier-Widen D, Lavazza A, Capucci L (2017) 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 64:1750–1761

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Fundação para a Ciência e Tecnologia (FCT) supported the Post-doc Grant of A.M. Lopes (SFRH/BPD/115211/2016) and the FCT Investigator Grants of P.J. Esteves (IF/00376/2015) and J. Abrantes (IF/01396/2013). C. Rouco was supported by XXII Propio de Investigación of the University of Córdoba and “Programa Operativo de fondos FEDER Andalucía”. This work is a result of the project AGRIGEN—NORTE-01-0145-FEDER-000007, supported by Norte Portugal Regional Operational Programme (NORTE2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF).

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Authors and Affiliations

  1. CIBIO/InBio-UP, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Vairão, Portugal

    Ana M. Lopes, Pedro J. Esteves & Joana Abrantes

  2. Instituto de Ciências Biomédicas Abel Salazar (ICBAS)/Unidade Multidisciplinar de Investigação Biomédica (UMIB), Universidade do Porto, Porto, Portugal

    Ana M. Lopes

  3. Departamento de Zoología, Facultad de Ciencias de la Universidad de Córdoba, Córdoba, Spain

    Carlos Rouco

  4. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, Portugal

    Pedro J. Esteves

Authors
  1. Ana M. Lopes
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  2. Carlos Rouco
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  3. Pedro J. Esteves
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  4. Joana Abrantes
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Corresponding author

Correspondence to Joana Abrantes.

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Handling Editor: Tim Skern.

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Lopes, A.M., Rouco, C., Esteves, P.J. et al. GI.1b/GI.1b/GI.2 recombinant rabbit hemorrhagic disease virus 2 (Lagovirus europaeus/GI.2) in Morocco, Africa. Arch Virol 164, 279–283 (2019). https://doi.org/10.1007/s00705-018-4052-y

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  • DOI: https://doi.org/10.1007/s00705-018-4052-y

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