Skip to main content
Top
Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

Comparative quantitative monitoring of rabbit haemorrhagic disease viruses in rabbit kittens

Authors: Markus Matthaei, Peter J Kerr, Andrew J Read, Paul Hick, Stephanie Haboury, John D Wright, Tanja Strive

Published in: Virology Journal | Issue 1/2014

Login to get access

Abstract

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference Meyers G, Wirblich C, Thiel HJ: Rabbit hemorrhagic-disease virus - molecular-cloning and nucleotide sequencing of a calicivirus genome. Virology 1991, 184: 664-676. 10.1016/0042-6822(91)90436-FPubMedCrossRef Meyers G, Wirblich C, Thiel HJ: Rabbit hemorrhagic-disease virus - molecular-cloning and nucleotide sequencing of a calicivirus genome. Virology 1991, 184: 664-676. 10.1016/0042-6822(91)90436-FPubMedCrossRef
2.
go back to reference 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.PubMedPubMedCentral 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.PubMedPubMedCentral
3.
go back to reference Ohlinger VF, Haas B, Thiel HJ: Rabbit hemorrhagic disease (RHD): characterization of the causative calicivirus. Vet Res 1993, 24: 103-116.PubMed Ohlinger VF, Haas B, Thiel HJ: Rabbit hemorrhagic disease (RHD): characterization of the causative calicivirus. Vet Res 1993, 24: 103-116.PubMed
4.
go back to reference 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.PubMed 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.PubMed
5.
go back to reference 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.PubMed 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.PubMed
6.
go back to reference 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. 10.7589/0090-3558-34.3.429PubMedCrossRef 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. 10.7589/0090-3558-34.3.429PubMedCrossRef
7.
go back to reference 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. 10.7589/0090-3558-34.2.221PubMedCrossRef 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. 10.7589/0090-3558-34.2.221PubMedCrossRef
8.
go back to reference Xu ZJ, Chen WX: Viral haemorrhagic disease in rabbits: a review. Vet Res Commun 1989, 13: 205-212. 10.1007/BF00142046PubMedCrossRef Xu ZJ, Chen WX: Viral haemorrhagic disease in rabbits: a review. Vet Res Commun 1989, 13: 205-212. 10.1007/BF00142046PubMedCrossRef
9.
go back to reference 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. 10.1186/1743-422X-4-96PubMedPubMedCentralCrossRef 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. 10.1186/1743-422X-4-96PubMedPubMedCentralCrossRef
10.
go back to reference 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. 10.1111/j.1523-1739.2008.00993.xPubMedCrossRef 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. 10.1111/j.1523-1739.2008.00993.xPubMedCrossRef
11.
go back to reference 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. 10.1071/WR00089CrossRef 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. 10.1071/WR00089CrossRef
12.
go back to reference 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. 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.
go back to reference Cooke BD: Rabbits: manageable environmental pests or participants in new Australian ecosystems? Wildlife Res 2012, 39: 279-289.CrossRef Cooke BD: Rabbits: manageable environmental pests or participants in new Australian ecosystems? Wildlife Res 2012, 39: 279-289.CrossRef
14.
go back to reference Rolls EC: They all ran wild. Angus and Robertson: Melbourne; 1969. Rolls EC: They all ran wild. Angus and Robertson: Melbourne; 1969.
15.
go back to reference 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. 10.1071/WR02010CrossRef 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. 10.1071/WR02010CrossRef
16.
go back to reference 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. 10.1016/j.biocontrol.2009.06.014CrossRef 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. 10.1016/j.biocontrol.2009.06.014CrossRef
17.
go back to reference 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. 10.1017/S0950268899003994PubMedPubMedCentralCrossRef 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. 10.1017/S0950268899003994PubMedPubMedCentralCrossRef
18.
go back to reference 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. 10.1071/WR08137CrossRef 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. 10.1071/WR08137CrossRef
19.
go back to reference 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. 10.1111/j.1365-2664.2010.01844.xCrossRef 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. 10.1111/j.1365-2664.2010.01844.xCrossRef
20.
go back to reference 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. 10.1017/S0950268811002743PubMedCrossRef 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. 10.1017/S0950268811002743PubMedCrossRef
21.
go back to reference 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.CrossRef 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.CrossRef
22.
go back to reference 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. 10.1186/1297-9716-44-51PubMedPubMedCentralCrossRef 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. 10.1186/1297-9716-44-51PubMedPubMedCentralCrossRef
23.
go back to reference Strive T, Wright JD, Robinson AJ: Identification and partial characterisation of a new lagovirus in Australian wild rabbits. Virology 2009, 384: 97-105. 10.1016/j.virol.2008.11.004PubMedCrossRef Strive T, Wright JD, Robinson AJ: Identification and partial characterisation of a new lagovirus in Australian wild rabbits. Virology 2009, 384: 97-105. 10.1016/j.virol.2008.11.004PubMedCrossRef
24.
go back to reference 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. 10.1016/S0168-1702(98)00106-3PubMedCrossRef 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. 10.1016/S0168-1702(98)00106-3PubMedCrossRef
25.
26.
go back to reference 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. 10.1292/jvms.001519PubMedCrossRef 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. 10.1292/jvms.001519PubMedCrossRef
27.
go back to reference 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. 10.1007/s00705-012-1340-9PubMedCrossRef 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. 10.1007/s00705-012-1340-9PubMedCrossRef
28.
go back to reference 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. 10.1186/1471-2148-10-347PubMedPubMedCentralCrossRef 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. 10.1186/1471-2148-10-347PubMedPubMedCentralCrossRef
29.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
30.
go back to reference 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. 10.1186/1297-9716-43-12PubMedPubMedCentralCrossRef 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. 10.1186/1297-9716-43-12PubMedPubMedCentralCrossRef
31.
go back to reference 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. 10.1016/j.vetmic.2008.09.057PubMedCrossRef 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. 10.1016/j.vetmic.2008.09.057PubMedCrossRef
32.
go back to reference 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. 10.1007/s00705-002-0908-1PubMedCrossRef 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. 10.1007/s00705-002-0908-1PubMedCrossRef
33.
go back to reference 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. 10.1186/1297-9716-44-1CrossRef 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. 10.1186/1297-9716-44-1CrossRef
34.
go back to reference 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. 10.1007/s007050050538PubMedCrossRef 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. 10.1007/s007050050538PubMedCrossRef
35.
go back to reference 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. 10.3201/eid1803.111402PubMedPubMedCentralCrossRef 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. 10.3201/eid1803.111402PubMedPubMedCentralCrossRef
36.
go back to reference Morisse JP, Le Gall G, Boilletot E: Hepatitis of viral origin in Leporidae: introduction and aetiological hypotheses. Rev Sci Tech 1991, 10: 269-310.PubMed Morisse JP, Le Gall G, Boilletot E: Hepatitis of viral origin in Leporidae: introduction and aetiological hypotheses. Rev Sci Tech 1991, 10: 269-310.PubMed
37.
go back to reference 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. 10.7589/0090-3558-30.2.176PubMedCrossRef 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. 10.7589/0090-3558-30.2.176PubMedCrossRef
38.
go back to reference 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. 10.1071/WR00119CrossRef 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. 10.1071/WR00119CrossRef
39.
go back to reference 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. 10.1186/1297-9716-45-14PubMedPubMedCentralCrossRef 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. 10.1186/1297-9716-45-14PubMedPubMedCentralCrossRef
40.
go back to reference 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. 10.1053/rvsc.1999.0357PubMedCrossRef 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. 10.1053/rvsc.1999.0357PubMedCrossRef
41.
go back to reference 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. 10.1053/rvsc.1998.0266PubMedCrossRef 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. 10.1053/rvsc.1998.0266PubMedCrossRef
42.
go back to reference 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. 10.1053/rvsc.1999.0372PubMedCrossRef 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. 10.1053/rvsc.1999.0372PubMedCrossRef
43.
go back to reference 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. 10.1016/j.vetimm.2007.09.005PubMedCrossRef 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. 10.1016/j.vetimm.2007.09.005PubMedCrossRef
44.
go back to reference Duizer E, Bijkerk P, Rockx B, De Groot A, Twisk F, Koopmans M: Inactivation of caliciviruses. Appl Environ Microbiol 2004, 70: 4538-4543. 10.1128/AEM.70.8.4538-4543.2004PubMedPubMedCentralCrossRef Duizer E, Bijkerk P, Rockx B, De Groot A, Twisk F, Koopmans M: Inactivation of caliciviruses. Appl Environ Microbiol 2004, 70: 4538-4543. 10.1128/AEM.70.8.4538-4543.2004PubMedPubMedCentralCrossRef
45.
go back to reference 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. 10.1128/AEM.01039-07PubMedPubMedCentralCrossRef 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. 10.1128/AEM.01039-07PubMedPubMedCentralCrossRef
46.
go back to reference 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. 10.1016/j.vetimm.2004.09.028PubMedCrossRef 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. 10.1016/j.vetimm.2004.09.028PubMedCrossRef
47.
go back to reference 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. 10.1016/j.virol.2009.11.045PubMedCrossRef 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. 10.1016/j.virol.2009.11.045PubMedCrossRef
48.
go back to reference 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. 10.1016/j.vetmic.2006.10.006PubMedCrossRef 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. 10.1016/j.vetmic.2006.10.006PubMedCrossRef
49.
go back to reference 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. 10.1111/j.1439-0450.2006.00986.xPubMedCrossRef 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. 10.1111/j.1439-0450.2006.00986.xPubMedCrossRef
50.
go back to reference 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. 10.1111/mec.12596PubMedPubMedCentralCrossRef 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. 10.1111/mec.12596PubMedPubMedCentralCrossRef
51.
go back to reference 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. 10.3201/eid1812.120341PubMedPubMedCentralCrossRef 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. 10.3201/eid1812.120341PubMedPubMedCentralCrossRef
52.
go back to reference 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. 10.1186/1297-9716-44-81PubMedPubMedCentralCrossRef 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. 10.1186/1297-9716-44-81PubMedPubMedCentralCrossRef
53.
go back to reference 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. 10.1016/j.vetmic.2013.12.015PubMedCrossRef 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. 10.1016/j.vetmic.2013.12.015PubMedCrossRef
54.
go back to reference 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. 10.1016/j.vetmic.2012.01.018PubMedCrossRef 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. 10.1016/j.vetmic.2012.01.018PubMedCrossRef
55.
go back to reference 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. 10.1016/0168-1702(95)00033-MPubMedCrossRef 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. 10.1016/0168-1702(95)00033-MPubMedCrossRef
Metadata
Title
Comparative quantitative monitoring of rabbit haemorrhagic disease viruses in rabbit kittens
Authors
Markus Matthaei
Peter J Kerr
Andrew J Read
Paul Hick
Stephanie Haboury
John D Wright
Tanja Strive
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-11-109

Other articles of this Issue 1/2014

Virology Journal 1/2014 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.