Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
Shopping Cart: ( empty )
You are here: Home > Journals > WR > WR24122
RESEARCH ARTICLE (Open Access)
Contents Vol 52(1)

No evidence of rabbit haemorrhagic disease virus 2 infection in scavengers of wild rabbits in Australia

Ina L. Smith https://orcid.org/0000-0001-5807-3737 A * , Nina Huang A , Megan Pavy A , Alexander Gofton A , Omid Fahri A , Egi Kardia A B , Roslyn Mourant A , Sammi Chong A , Maria Jenckel A , Robyn N. Hall A C and Tanja Strive A
+ Author Affiliations
- Author Affiliations

A CSIRO, Clunies Ross Street, Acton, ACT 2601, Australia.

B Present address: School of Biomedical Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

C Present address: Ausvet, Bruce, ACT 2617, Australia.

* Correspondence to: Ina.Smith@csiro.au

Handling Editor: Peter Caley

Wildlife Research 52, WR24122 https://doi.org/10.1071/WR24122
Submitted: 26 July 2024  Accepted: 17 December 2024  Published: 14 January 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

Rabbit haemorrhagic disease virus 2 (RHDV2/b/GI.2) is the only representative of the genus Lagovirus that is known to fatally infect multiple lagomorph species. RHDV2 is the dominant lagovirus circulating in rabbits in Australia, where some lagoviruses are used for deliberate biological control of European rabbits, a major environmental and agricultural pest in this country. Evidence of exposure to lagoviruses has been reported for a range of species that feed on rabbits, and the reduced host specificity of RHDV2 compared with RHDV1 has occasionally raised concerns, especially in a biocontrol context.

Aim

We investigated evidence of exposure to RHDV2 in 99 individual feral foxes, cats, dogs and pigs and then we aimed to test these animals for evidence of a productive infection.

Methods

Sera were analysed for the presence of antibodies to RHDV2, and faeces and tissues for the presence of viral RNA. We made provisions for downstream analysis of liver tissues by reverse-transcription quantitative polymerase chain reaction (RT-qPCR) and histopathology should they return a positive RT-qPCR result, to further investigate any evidence of productive virus infection. We also infected RHDV2 in hepatobiliary organoids derived from cats and foxes to test for possible infection.

Key results

We detected serum antibodies and viral RNA in faeces indicative of ingestion of RHDV2-infected rabbits, but found no evidence for productive infection with RHDV2. Furthermore, no RHDV2 replication was seen in hepatobiliary organoids derived from foxes and cats after in vitro infection with RHDV2.

Conclusion

RHDV2 does not infect scavengers of rabbits, such as foxes, dogs, cats and pigs.

Implications

This study has provided insights into the safety of this strain.

Keywords: hares, hepatobiliary organoids, lagomorphs, predators, rabbit haemorrhagic disease virus 2, rabbits, RHDV2, scavengers.

References

Abade dos Santos FA, Pinto A, Burgoyne T, Dalton KP, Carvalho CL, Ramilo DW, Carneiro C, Carvalho T, Peleteiro MC, Parra F, Duarte MD (2022) Spillover events of rabbit haemorrhagic disease virus 2 (recombinant GI.4P-GI.2) from Lagomorpha to Eurasian badger. Transboundary and Emerging Diseases 69(3), 1030-1045.
| Crossref | Google Scholar |

Asin J, Rejmanek D, Clifford DL, Mikolon AB, Henderson EE, Nyaoke AC, Macías-Rioseco M, Streitenberger N, Beingesser J, Woods LW, Lavazza A, Capucci L, Crossley B, Uzal FA (2022) Early circulation of rabbit haemorrhagic disease virus type 2 in domestic and wild lagomorphs in southern California, USA (2020–2021). Transboundary and Emerging Diseases 69(4), e394-e405.
| Crossref | Google Scholar | PubMed |

Calvete C, Mendoza M, Sarto MP, Bagüés MPJ, Luján L, Molín J, Calvo AJ, Monroy F, Calvo JH (2019) Detection of Rabbit Hemorrhagic Disease Virus GI.2/RHDV2/b in the Mediterranean Pine Vole (Microtus duodecimcostatus) and White-Toothed Shrew (Crocidura russula). Journal of Wildlife Diseases 55(2), 467-472.
| Crossref | Google Scholar | PubMed |

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). Research in Veterinary Science 97(3), 642-645.
| Crossref | Google Scholar | PubMed |

Campbell SJ, Ashley W, Gil-Fernandez M, Newsome TM, Di Giallonardo F, Ortiz-Baez AS, Mahar JE, Towerton AL, Gillings M, Holmes EC, Carthey AJR, Geoghegan JL (2020) Red fox viromes in urban and rural landscapes. Virus Evolution 6(2), veaa065.
| Crossref | Google Scholar |

Chiari M, Molinari S, Cavadini P, Bertasi B, Zanoni M, Capucci L, Lavazza A (2016) Red foxes (Vulpes vulpes) feeding brown hares (Lepus europaeus) infected by European brown hare syndrome virus (EBHSv) might be involved in the spread of the virus. European Journal of Wildlife Research 62(6), 761-765.
| Crossref | Google Scholar |

Chong R, Shi M, Grueber CE, Holmes EC, Hogg CJ, Belov K, Barrs VR (2019) Fecal viral diversity of captive and wild tasmanian devils characterized using virion-enriched metagenomics and metatranscriptomics. Journal of Virology 93(11), e00205-e00219.
| Crossref | Google Scholar |

Cooke BD, Fenner F (2002) Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildlife Research 29(6), 689-706.
| Crossref | Google Scholar |

Di Profio F, Melegari I, Sarchese V, Robetto S, Bermudez Sanchez S, Carella E, Orusa R, Cavadini P, Lavazza A, Marsilio F, Martella V, Di Martino B (2018) Potential role of wolf (Canis lupus) as passive carrier of European brown hare syndrome virus (EBHSV). Research in Veterinary Science 117, 81-84.
| Crossref | Google Scholar | PubMed |

Du Plessis J (2022) Update on the disease killing our rabbits: rabbit haemorrhagic disease virus. Available at https://ewt.org.za/update-on-the-disease-killing-our-rabbits/

Duarte MD, Carvalho CL, Barros SC, Henriques AM, Ramos F, Fagulha T, Luís T, Duarte EL, Fevereiro M (2015) A real time Taqman RT-PCR for the detection of rabbit hemorrhagic disease virus 2 (RHDV2). Journal of Virological Methods 219, 90-95.
| Crossref | Google Scholar | PubMed |

Frölich K, Kiima F, Dedek J (1998) Antibodies against rabbit hemorrhagic disease virus in free-ranging red foxes from Germany. Journal of Wildlife Diseases 34(3), 436-442.
| Google Scholar | PubMed |

Henning J, Meers J, Davies PR, Morris RS (2005) Survival of rabbit haemorrhagic disease virus (RHDV) in the environment. Epidemiology and Infection 133(4), 719-730.
| Crossref | Google Scholar | PubMed |

Henning J, Davies PR, Meers J (2006) Seropositivity to rabbit haemorrhagic disease virus in non-target mammals during periods of viral activity in a population of wild rabbits in New Zealand. Wildlife Research 33(4), 305-311.
| Crossref | Google Scholar |

Kardia E, Fakhri O, Pavy M, Mason H, Huang N, Smertina E, Jenckel M, Peng NYG, Estes MK, Strive T, Frese M, Smith I, Hall RN (2023) Hepatobiliary organoids derived from leporids support the replication of hepatotropic lagoviruses. Journal of General Virology 104(8), 001874.
| Crossref | Google Scholar |

Kennedy A, Britton L, Byrne AW, Byrne C, Casey M, Flynn O, Lozano JM, Marnell F, McElroy M, Reid N, Wilson M, FitzGerald W (2021) First detected case of rabbit Haemorrhagic disease virus 2 (RHDV2) in the Irish hare (Lepus timidus hibernicus). Irish Veterinary Journal 74(1), 25.
| Crossref | Google Scholar |

Lavazza A, Capucci L, Cavadini P (2023) Rabbit haemorrhagic disease. Manual of diagnostic tests and vaccines for terrestrial animals, Chapter 3.7.2, pp. 1–20. World Organisation for Animal Health. Available at https://www.woah.org/en/what-we-do/standards/codes-and-manuals/terrestrial-manual-online-access/

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. Veterinary Record 168(5), 137-138.
| Crossref | Google Scholar |

Leighton FA, Artois M, Capucci L, Gavier-Widen D, Morisse J-P (1995) Antibody response to rabbit viral hemorrhagic disease virus in red foxes (Vulpes vulpes) consuming livers of infected rabbits (Oryctolagus cuniculus). Journal of Wildlife Diseases 31(4), 541-544.
| Crossref | Google Scholar | PubMed |

Liu SJ, Xue HP, Pu BQ, Qian NH (1984) A new viral disease in rabbits. Animal Husbandry and Veterinary Medicine 16(6), 253-255.
| Google Scholar |

Neimanis AS, Ahola H, Larsson Pettersson U, Lopes AM, Abrantes J, Zohari S, Esteves PJ, Gavier-Widén D (2018) Overcoming species barriers: an outbreak of Lagovirus europaeus GI.2/RHDV2 in an isolated population of mountain hares (Lepus timidus). BMC Veterinary Research 14(1), 367.
| Crossref | Google Scholar | PubMed |

Parkes JP, Heyward RP, Henning J, Motha MXJ (2004) Antibody responses to rabbit haemorrhagic disease virus in predators, scavengers, and hares in New Zealand during epidemics in sympatric rabbit populations. New Zealand Veterinary Journal 52(2), 85-89.
| Crossref | Google Scholar | PubMed |

Peng NYG, Hall RN, Huang N, West P, Cox TE, Mahar JE, Mason H, Campbell S, O’Connor T, Read AJ, Patel KK, Taggart PL, Smith IL, Strive T, Jenckel M (2023) Utilizing and citizen science for the surveillance of lagoviruses in Australia. Viruses 15(12), 2348.
| Crossref | Google Scholar |

Philbey AW, Kirkland PD, Saunders GR (2005) Assessment of antibodies to rabbit haemorrhagic disease virus in fox serum as an indicator of infection in sympatric rabbit populations. Australian Veterinary Journal 83(1–2), 97-100.
| Crossref | Google Scholar | PubMed |

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). Veterinary Research 44(1), 96.
| Crossref | Google Scholar | PubMed |

Ramsey DS, Patel KK, Campbell S, Hall RN, Taggart PL, Strive T (2023) Sustained impact of RHDV2 on wild rabbit populations across Australia eight years after its initial detection. Viruses 15(5), 1159.
| Crossref | Google Scholar |

Rouco C, Abrantes J, Serronha A, Lopes AM, Maio E, Magalhães MJ, Blanco E, Bárcena 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. Transboundary and Emerging Diseases 65(2), e373-e382.
| Crossref | Google Scholar | PubMed |

Simón M, Muguruza R, Alonso J, Muzquiz J, Gironés O, Haffar A (1994) Recherche du virus de la maladie hémorragique virale du lapin (RHD) chez le renard et rôle des canidés domestiques dans la transmission de la maladie. Recueil de Medecine Veterinaire 170, 841-845.
| Google Scholar |

Strive T, Piper M, Huang N, Mourant R, Kovaliski J, Capucci L, Cox TE, Smith I (2020) Retrospective serological analysis reveals presence of the emerging lagovirus RHDV2 in Australia in wild rabbits at least five months prior to its first detection. Transboundary and Emerging Diseases 67(2), 822-833.
| Crossref | Google Scholar |

Vinjé J, Estes MK, Esteves P, Green KY, Katayama K, Knowles NJ, L’Homme Y, Martella V, Vennema H, White PA (2019) ICTV Virus Taxonomy Profile: Caliciviridae. Journal of General Virology 100(11), 1469-1470.
| Crossref | Google Scholar | PubMed |

Zheng T, Lu G, Napier AM, Lockyer SJ (2003) No virus replication in domestic cats fed with RHDV-infected rabbit livers. Veterinary Microbiology 95(1–2), 61-73.
| Crossref | Google Scholar | PubMed |