Comparative quantitative monitoring of rabbit haemorrhagic disease viruses in rabbit kittens

Virology Journal

Tanja Strive¹  John D Wright²  Stephanie Haboury²  Paul Hick²  Andrew J Read²  Peter J Kerr²  Markus Matthaei² 

[1]CSIRO – Ecosystem Sciences, GPO Box 1700, Canberra ACT 2600, Australia

[2]Invasive Animals Cooperative Research Centre, University of Canberra, Canberra ACT 2601, Australia

关键词: Calicivirus;    Biological pest control;    Invasive species;    RHD;    Resistance;    Time course;    Oryctolagus cuniculus;    RHDVa;   

Others  :  802689
DOI  :  10.1186/1743-422X-11-109

 received in 2014-02-12, accepted in 2014-05-23,  发布年份 2014

【 摘 要 】

Background

Only one strain (the Czech CAPM-v351) of rabbit haemorrhagic disease virus (RHDV) has been released in Australia and New Zealand to control pest populations of the European rabbit O. cuniculus. Antigenic variants of RHDV known as RHDVa strains are reportedly replacing RHDV strains in other parts of the world, and Australia is currently investigating the usefulness of RHDVa to complement rabbit biocontrol efforts in Australia and New Zealand. RHDV efficiently kills adult rabbits but not rabbit kittens, which are more resistant to RHD the younger they are and which may carry the virus without signs of disease for prolonged periods. These different infection patterns in young rabbits may significantly influence RHDV epidemiology in the field and hence attempts to control rabbit numbers.

Methods

We quantified RHDV replication and shedding in 4–5 week old rabbits using quantitative real time PCR to assess their potential to shape RHDV epidemiology by shedding and transmitting virus. We further compared RHDV-v351 with an antigenic variant strain of RHDVa in kittens that is currently being considered as a potential RHDV strain for future release to improve rabbit biocontrol in Australia.

Results

Kittens were susceptible to infection with virus doses as low as 10 ID₅₀. Virus growth, shedding and transmission after RHDVa infection was found to be comparable or non-significantly lower compared to RHDV. Virus replication and shedding was observed in all kittens infected, but was low in comparison to adult rabbits. Both viruses were shed and transmitted to bystander rabbits. While blood titres indicated that 4–5 week old kittens mostly clear the infection even in the absence of maternal antibodies, virus titres in liver, spleen and mesenteric lymph node were still high on day 5 post infection.

Conclusions

Rabbit kittens are susceptible to infection with very low doses of RHDV, and can transmit virus before they seroconvert. They may therefore play an important role in RHDV field epidemiology, in particular for virus transmission within social groups during virus outbreaks.

【 授权许可】

   
2014 Matthaei et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Meyers G, Wirblich C, Thiel HJ: Rabbit hemorrhagic-disease virus - molecular-cloning and nucleotide sequencing of a calicivirus genome. Virology 1991, 184:664-676.
• [2]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.
• [3]Ohlinger VF, Haas B, Thiel HJ: Rabbit hemorrhagic disease (RHD): characterization of the causative calicivirus. Vet Res 1993, 24:103-116.
• [4]Chasey D, Trout RC, Edwards S: Susceptibility of wild rabbits (Oryctolagus cuniculus) in the United Kingdom to rabbit haemorrhagic disease (RHD). Vet Res 1997, 28:271-276.
• [5]Lavazza A, Scicluna MT, Capucci L: Susceptibility of hares and rabbits to the European brown hare syndrome virus (EBHSV) and rabbit haemorrhagic disease virus (RHDV) under experimental conditions. Zentralbl Veterinarmed B 1996, 43:401-410.
• [6]Marchandeau S, Chantal J, Portejoie Y, Barraud S, Chaval Y: Impact of viral hemorrhagic disease on a wild population of European rabbits in France. J Wildl Dis 1998, 34:429-435.
• [7]Mutze G, Cooke B, Alexander P: The initial impact of rabbit hemorrhagic disease on European rabbit populations in South Australia. J Wildl Dis 1998, 34:221-227.
• [8]Xu ZJ, Chen WX: Viral haemorrhagic disease in rabbits: a review. Vet Res Commun 1989, 13:205-212.
• [9]McIntosh MT, Behan SC, Mohamed FM, Lu Z, Moran KE, Burrage TG, Neilan JG, Ward GB, Botti G, Capucci L, Metwally SA: A pandemic strain of calicivirus threatens rabbit industries in the Americas. Virol J 2007, 4:96. BioMed Central Full Text
• [10]Delibes-Mateos M, Delibes M, Ferreras P, Villafuerte R: Key role of European rabbits in the conservation of the Western Mediterranean basin hotspot. Conserv Biol 2008, 22:1106-1117.
• [11]Sandell PR: Implications of rabbit haemorrhagic disease for the short-term recovery of semi-arid woodland communities in north-west Victoria. Wildlife Res 2002, 29:591-598.
• [12]Ward VK, Cooke BD, Strive T: Rabbit Haemorrhagic Disease Virus and other Lagoviruses. In Caliciviruses. Edited by Green K, Hansman G. Norfolk, UK: Caister Academic Press; 2011.
• [13]Cooke BD: Rabbits: manageable environmental pests or participants in new Australian ecosystems? Wildlife Res 2012, 39:279-289.
• [14]Rolls EC: They all ran wild. Angus and Robertson: Melbourne; 1969.
• [15]Cooke BD, Fenner F: Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildlife Res 2002, 29:689-706.
• [16]Saunders G, Cooke B, McColl K, Shine R, Peacock T: Modern approaches for the biological control of vertebrate pests: an Australian perspective. Biol Control 2010, 52:288-295.
• [17]Cooke BD, Robinson AJ, Merchant JC, Nardin A, Capucci L: Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiol Infect 2000, 124:563-576.
• [18]McPhee SR, Butler KL, Kovaliski J, Mutze G, Capucci L, Cooke BD: Antibody status and survival of Australian wild rabbits challenged with rabbit haemorrhagic disease virus. Wildlife Res 2009, 36:447-456.
• [19]Mutze G, Kovaliski J, Butler K, Capucci L, McPhee S: The effect of rabbit population control programmes on the impact of rabbit haemorrhagic disease in south-eastern Australia. J Appl Ecol 2010, 47:1137-1146.
• [20]Elsworth PG, Kovaliski J, Cooke BD: Rabbit haemorrhagic disease: are Australian rabbits (Oryctolagus cuniculus) evolving resistance to infection with Czech CAPM 351 RHDV? Epidemiol Infect 2012, 140:1972-1981.
• [21]Nystrom K, Le Gall-Recule G, Grassi P, Abrantes J, Ruvoen-Clouet N, Le Moullac-Vaidye B, Lopes AM, Esteves PJ, Strive T, Marchandeau S, Dell A, Haslam SM, LePendu J: Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PloS Pathog 2011, 7:8.
• [22]Strive T, Elsworth P, Liu JN, Wright JD, Kovaliski J, Capucci L: 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. BioMed Central Full Text
• [23]Strive T, Wright JD, Robinson AJ: Identification and partial characterisation of a new lagovirus in Australian wild rabbits. Virology 2009, 384:97-105.
• [24]Capucci L, Fallacara F, Grazioli S, Lavazza A, Pacciarini ML, Brocchi E: 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.
• [25]Kerr PJ, Kitchen A, Holmes EC: Origin and phylodynamics of rabbit hemorrhagic disease virus. J Virol 2009, 83:12129-12138.
• [26]Oem JK, Lee KN, Roh IS, Lee KK, Kim SH, Kim HR, Park CK, Joo YS: Identification and characterization of rabbit hemorrhagic disease virus genetic variants isolated in Korea. J Vet Med Sci 2009, 71:1519-1523.
• [27]Wang X, Hao H, Qiu L, Dang R, Du E, Zhang S, Yang Z: Phylogenetic analysis of rabbit hemorrhagic disease virus in China and the antigenic variation of new strains. Arch Virol 2012, 157:1523-1530.
• [28]Alda F, Gaitero T, Suarez M, Merchan T, Rocha G, Doadrio I: Evolutionary history and molecular epidemiology of rabbit haemorrhagic disease virus in the Iberian Peninsula and Western Europe. BMC Evol Biol 2010, 10:347. BioMed Central Full Text
• [29]Abrantes J, Lopes AM, Dalton KP, Melo P, Correia JJ, Ramada M, Alves PC, Parra F, Esteves PJ: New variant of rabbit hemorrhagic disease virus, Portugal, 2012–2013. Emerg Infect Dis 2013, 19:1900-1902.
• [30]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. BioMed Central Full Text
• [31]Muller A, Freitas J, Silva E, Le Gall-Recule G, Zwingelstein F, Abrantes J, Esteves PJ, Alves PC, Loo WD, Kolodziejek J, Nowotny N, Thompson G: Evolution of rabbit haemorrhagic disease virus (RHDV) in the European rabbit (Oryctolagus cuniculus) from the Iberian Peninsula. Vet Microbiol 2009, 135:368-373.
• [32]Le Gall-Recule G, Zwingelstein F, Laurent S, de Boisseson C, Portejoie Y, Rasschaert D: 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.
• [33]Le Gall-Recule G, Lavazza A, Marchandeau S, Bertagnoli S, Zwingelstein F, Cavadini P, Martinelli N, Lombardi G, Guerin J-L, Lemaitre E, Decors A, Boucher S, Le Normand B, Capucci L: Emergence of a new lagovirus related to rabbit haemorrhagic disease virus. Vet Res 2013, 44:1-13. BioMed Central Full Text
• [34]Schirrmeier H, Reimann I, Kollner B, Granzow H: Pathogenic, antigenic and molecular properties of rabbit haemorrhagic disease virus (RHDV) isolated from vaccinated rabbits: detection and characterization of antigenic variants. Arch Virol 1999, 144:719-735.
• [35]Nystrom K, Le Moullac-Vaidye B, Ruvoen-Clouet N, Le Pendu J: Shared human/rabbit ligands for rabbit hemorrhagic disease virus. Emerg Infect Dis 2012, 18:518-519.
• [36]Morisse JP, Le Gall G, Boilletot E: Hepatitis of viral origin in Leporidae: introduction and aetiological hypotheses. Rev Sci Tech 1991, 10:269-310.
• [37]Villafuerte R, Calvete C, Gortazar C, Moreno S: First epizootic of rabbit hemorrhagic disease in free living populations of Oryctolagus cuniculus at Donana National Park, Spain. J Wildl Dis 1994, 30:176-179.
• [38]Robinson AJ, So PTM, Muller WJ, Cooke BD, Capucci L: Statistical models for the effect of age and maternal antibodies on the development of rabbit haemorrhagic disease in Australian wild rabbits. Wildlife Res 2002, 29:663-671.
• [39]Marques RM, Teixeira L, Aguas AP, Ribeiro JC, Costa-e-Silva A, Ferreira PG: Immunosuppression abrogates resistance of young rabbits to Rabbit Haemorrhagic Disease (RHD). Vet Res 2014, 45:14. BioMed Central Full Text
• [40]Prieto JM, Fernandez F, Alvarez V, Espi A, Garcia Marin JF, Alvarez M, Martin JM, Parra F: Immunohistochemical localisation of rabbit haemorrhagic disease virus VP-60 antigen in early infection of young and adult rabbits. Res Vet Sci 2000, 68:181-187.
• [41]Mikami O, Park JH, Kimura T, Ochiai K, Itakura C: Hepatic lesions in young rabbits experimentally infected with rabbit haemorrhagic disease virus. Res Vet Sci 1999, 66:237-242.
• [42]Shien JH, Shieh HK, Lee LH: Experimental infections of rabbits with rabbit haemorrhagic disease virus monitored by polymerase chain reaction. Res Vet Sci 2000, 68:255-259.
• [43]Ferreira PG, Dinis M, Costa ESA, Aguas AP: Adult rabbits acquire resistance to lethal calicivirus infection by adoptive transfer of sera from infected young rabbits. Vet Immunol Immunopathol 2008, 121:364-369.
• [44]Duizer E, Bijkerk P, Rockx B, De Groot A, Twisk F, Koopmans M: Inactivation of caliciviruses. Appl Environ Microbiol 2004, 70:4538-4543.
• [45]Baert L, Wobus CE, Van Coillie E, Thackray LB, Debevere J, Uyttendaele M: Detection of murine norovirus 1 by using plaque assay, transfection assay, and real-time reverse transcription-PCR before and after heat exposure. Appl Environ Microbiol 2008, 74:543-546.
• [46]Ferreira PG, Costa ESA, Oliveira MJ, Monteiro E, Aguas AP: Leukocyte-hepatocyte interaction in calicivirus infection: differences between rabbits that are resistant or susceptible to rabbit haemorrhagic disease (RHD). Vet Immunol Immunopathol 2005, 103:217-221.
• [47]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.
• [48]Gall A, Hoffmann B, Teifke JP, Lange B, Schirrmeier H: Persistence of viral RNA in rabbits which overcome an experimental RHDV infection detected by a highly sensitive multiplex real-time RT-PCR. Vet Microbiol 2007, 120:17-32.
• [49]Gall A, Schirrmeier H: Persistence of rabbit haemorrhagic disease virus genome in vaccinated rabbits after experimental infection. J Vet Med B Infect Dis Vet Public Health 2006, 53:358-362.
• [50]Kovaliski J, Sinclair R, Mutze G, Peacock D, Strive T, Abrantes J, Esteves P, Holmes E: Molecular epidemiology of rabbit haemorrhagic disease virus (RHDV) in Australia: when one became many. Mol Ecol 2014, 23:408-420.
• [51]Dalton KP, Nicieza I, Balseiro A, Muguerza MA, Rosell JM, Casais R, Alvarez AL, Parra F: Variant rabbit hemorrhagic disease virus in young rabbits, Spain. Emerg Infect Dis 2012, 18:2009-2012.
• [52]Le Gall-Recule 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: Emergence of a new lagovirus related to rabbit haemorrhagic disease virus. Vet Res 2013, 44:81. BioMed Central Full Text
• [53]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.
• [54]Liu J, Kerr PJ, Wright JD, Strive T: Serological assays to discriminate rabbit haemorrhagic disease virus from Australian non-pathogenic rabbit calicivirus. Vet Microbiol 2012, 157:345-354.
• [55]Capucci L, Frigoli G, Ronshold L, Lavazza A, Brocchi E, Rossi C: Antigenicity of the rabbit hemorrhagic disease virus studied by its reactivity with monoclonal antibodies. Virus Res 1995, 37:221-238.