Analysis of canine parvoviruses circulating in Australia reveals predominance of variant 2b and identifies feline parvovirus-like mutations in the capsid proteins.


Journal

Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538

Informations de publication

Date de publication:
Mar 2021
Historique:
revised: 16 06 2020
received: 10 05 2020
accepted: 08 07 2020
pubmed: 14 7 2020
medline: 27 5 2021
entrez: 14 7 2020
Statut: ppublish

Résumé

Canine parvovirus (CPV) is a major enteric pathogen of dogs worldwide that emerged in the late 1970s from a feline parvovirus (FPV)-like ancestral virus. Shortly after its emergence, variant CPVs acquired amino acid (aa) mutations in key capsid residues, associated with biological and/or antigenic changes. This study aimed to identify and analyse CPV variants and their capsid mutations amongst Australian dogs, to gain insights into the evolution of CPV in Australia and to investigate relationships between the disease and vaccination status of dogs from which viruses were detected. CPV VP2 sequences were amplified from 79 faecal samples collected from dogs with parvoviral enteritis at 20 veterinary practices in five Australian states. The median age at diagnosis was 4 months (range 1-96 months). Only 3.7% of dogs with vaccination histories had completed recommended vaccination schedules, while 49% were incompletely vaccinated and 47.2% were unvaccinated. For the first time, CPV-2b has emerged as the dominant antigenic CPV variant circulating in dogs with parvoviral enteritis in Australia, comprising 54.4% of viruses, while CPV-2a and CPV-2 comprised 43.1% and 2.5%, respectively. The antigenic variant CPV-2c was not identified. Analysis of translated VP2 sequences revealed a vast repertoire of amino acid (aa) mutations. Several Australian CPV strains displayed signatures in the VP2 protein typical of Asian CPVs, suggesting possible introduction of CPV strains from Asia, and/or CPV circulation between Asia and Australia. Canine parvoviruses were identified containing aa residues typical of FPV at key capsid (VP2) positions, representing reverse mutations or residual mutations retained from CPV-2 during adaptation from an FPV-like ancestor, suggesting that evolutionary intermediates between CPV-2 and FPV are circulating in the field. Similarly, intermediates between CPV-2a-like viruses and CPV-2 were also identified. These findings help inform a better understanding of the evolution of CPV in dogs.

Identifiants

pubmed: 32657506
doi: 10.1111/tbed.13727
doi:

Substances chimiques

Antigens, Viral 0
Capsid Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

656-666

Subventions

Organisme : Boehringer Ingelheim
ID : University of Sydney ARC Seed Funding scheme

Informations de copyright

© 2020 Blackwell Verlag GmbH.

Références

Allison, A. B., Harbison, C. E., Pagan, I., Stucker, K. M., Kaelber, J. T., Brown, J. D., … Parrish, C. R. (2012). Role of multiple hosts in the cross-species transmission and emergence of a pandemic parvovirus. Journal of Virology, 86(2), 865-872. https://doi.org/10.1128/jvi.06187-11
Allison, A. B., Organtini, L. J., Zhang, S., Hafenstein, S. L., Holmes, E. C., & Parrish, C. R. (2016). Single mutations in the VP2 300 loop region of the three-fold spike of the carnivore parvovirus capsid can determine host range. Journal of Virology, 90(2), 753-767. https://doi.org/10.1128/jvi.02636-15
Battilani, M., Modugno, F., Mira, F., Purpari, G., Di Bella, S., Guercio, A., & Balboni, A. (2019). Molecular epidemiology of canine parvovirus type 2 in Italy from 1994 to 2017: Recurrence of the CPV-2b variant. BMC Veterinary Research, 15(1), 393. https://doi.org/10.1186/s12917-019-2096-1
Binn, L. N., Lazar, E. C., Eddy, G. A., & Kajima, M. (1970). Recovery and characterization of a minute virus of canines. Infection and Immunity, 1(5), 503-508.
Cavalli, A., Desario, C., Marinaro, M., Losurdo, M., Camero, M., Decaro, N., … Buonavoglia, C. (2020). Oral administration of modified live canine parvovirus type 2b induces systemic immune response. Vaccine, 38(2), 115-118. https://doi.org/10.1016/j.vaccine.2019.10.016
Cavalli, A., Martella, V., Desario, C., Camero, M., Bellacicco, A. L., De Palo, P., … Buonavoglia, C. (2008). Evaluation of the antigenic relationships among canine parvovirus type 2 variants. Clinical and Vaccine Immunology, 15(3), 534-539. https://doi.org/10.1128/cvi.00444-07
Chang, S. F., Sgro, J. Y., & Parrish, C. R. (1992). Multiple amino acids in the capsid structure of canine parvovirus coordinately determine the canine host range and specific antigenic and hemagglutination properties. Journal of Virology, 66(12), 6858-6867. https://doi.org/10.1128/JVI.66.12.6858-6867.1992
Clark, N. J., Seddon, J. M., Kyaw-Tanner, M., Al-Alawneh, J., Harper, G., McDonagh, P., & Meers, J. (2018). Emergence of canine parvovirus subtype 2b (CPV-2b) infections in Australian dogs. Infection, Genetics and Evolution, 58, 50-55.
Day, M. J., Horzinek, M. C., Schultz, R. D., & Squires, R. A. (2016). WSAVA guidelines for the vaccination of dogs and cats: WSAVA vaccination guidelines. Journal of Small Animal Practice, 57(1), 4-8. https://doi.org/10.1111/jsap.12431
Decaro, N., & Buonavoglia, C. (2012). Canine parvovirus-A review of epidemiological and diagnostic aspects, with emphasis on type 2c. Veterinary Microbiology, 155(1), 1-12. https://doi.org/10.1016/j.vetmic.2011.09.007
Decaro, N., Buonavoglia, C., & Barrs, V. R. (2020). Canine parvovirus vaccination and immunisation failures: Are we far from disease eradication? Veterinary Microbiology, 247, 108760. https://doi.org/10.1016/j.vetmic.2020.108760
Decaro, N., Desario, C., Addie, D. D., Martella, V., Vieira, M. J., Elia, G., … Buonavoglia, C. (2007). Molecular epidemiology of canine parvovirus, Europe. Emerging Infectious Diseases, 13(8), 1222-1224. https://doi.org/10.3201/eid1308.070505
Decaro, N., Desario, C., Elia, G., Martella, V., Mari, V., Lavazza, A., … Buonavoglia, C. (2008). Evidence for immunisation failure in vaccinated adult dogs infected with canine parvovirus type 2c. The New Microbiologica, 31(1), 125.
Decaro, N., Desario, C., Miccolupo, A., Campolo, M., Parisi, A., Martella, V., … Buonavoglia, C. (2008). Genetic analysis of feline panleukopenia viruses from cats with gastroenteritis. Journal of General Virology, 89(9), 2290-2298. https://doi.org/10.1099/vir.0.2008/001503-0
Decaro, N., Elia, G., Desario, C., Roperto, S., Martella, V., Campolo, M., … Buonavoglia, C. (2006). A minor groove binder probe real-time PCR assay for discrimination between type 2-based vaccines and field strains of canine parvovirus. Journal of Virological Methods, 136(1), 65-70. https://doi.org/10.1016/j.jviromet.2006.03.030
Department of Infrastructure, Transport, Regional Development and Communications (2020). Retrieved from: https://www.rda.gov.au/sites/default/files/images/rda-map-national-2020.jpg
Hafenstein, S., Palermo, L. M., Kostyuchenko, V. A., Xiao, C., Morais, M. C., Nelson, C. D. S., … Rossmann, M. G. (2007). Asymmetric binding of transferrin receptor to parvovirus capsids. Proceedings of the National Academy of Sciences, 104(16), 6585-6589. https://doi.org/10.1073/pnas.0701574104
Hoang, M., Lin, W.-H., Le, V. P., Nga, B. T. T., Chiou, M.-T., & Lin, C.-N. (2019). Molecular epidemiology of canine parvovirus type 2 in Vietnam from November 2016 to February 2018. Virology Journal, 16(1), https://doi.org/10.1186/s12985-019-1159-z
Hoelzer, K., & Parrish, C. R. (2010). The emergence of parvoviruses of carnivores. Veterinary Research, 41(6), 39. https://doi.org/10.1051/vetres/2010011
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547-1549. https://doi.org/10.1093/molbev/msy096
Lee, H., Callaway, H. M., Cifuente, J. O., Bator, C. M., Parrish, C. R., & Hafenstein, S. L. (2019). Transferrin receptor binds virus capsid with dynamic motion. Proceedings of the National Academy of Sciences, 116(41), 20462-20471. https://doi.org/10.1073/pnas.1904918116
Lin, Y. C., Chiang, S. Y., Wu, H. Y., Lin, J. H., Chiou, M. T., Liu, H. F., & Lin, C. N. (2017). Phylodynamic and genetic diversity of canine parvovirus type 2c in Taiwan. International Journal of Molecular Sciences, 18(12), https://doi.org/10.3390/ijms18122703
Ling, M., Norris, J. M., Kelman, M., & Ward, M. P. (2012). Risk factors for death from canine parvoviral-related disease in Australia. Veterinary Microbiology, 158(3-4), 280-290. https://doi.org/10.1016/j.vetmic.2012.02.034
Martella, V., Cavalli, A., Decaro, N., Elia, G., Desario, C., Campolo, M., … Buonavoglia, C. (2005). Immunogenicity of an intranasally administered modified live canine parvovirus type 2b vaccine in pups with maternally derived antibodies. Clinical and Diagnostic Laboratory Immunology, 12(10), 1243-1245. https://doi.org/10.1128/cdli.12.10.1243-1245.2005
Maya, L., Calleros, L., Francia, L., Hernández, M., Iraola, G., Panzera, Y., … Pérez, R. (2013). Phylodynamics analysis of canine parvovirus in Uruguay: Evidence of two successive invasions by different variants. Archives of Virology, 158(6), 1133-1141. https://doi.org/10.1007/s00705-012-1591-5
Meers, J., Kyaw-Tanner, M., Bensink, Z., & Zwijnenberg, R. (2007). Genetic analysis of canine parvovirus from dogs in Australia. Australian Veterinary Journal, 85(10), 392-396. https://doi.org/10.1111/j.1751-0813.2007.00206.x
Mira, F., Purpari, G., Lorusso, E., Di Bella, S., Gucciardi, F., Desario, C., … Guercio, A. (2018). Introduction of Asian canine parvovirus in Europe through dog importation. Transboundary and Emerging Diseases, 65(1), 16-21. https://doi.org/10.1111/tbed.12747
Ohneiser, S. A., Hills, S. F., Cave, N. J., Passmore, D., & Dunowska, M. (2015). Canine parvoviruses in New Zealand form a monophyletic group distinct from the viruses circulating in other parts of the world. Veterinary Microbiology, 178(3-4), 190-200. https://doi.org/10.1016/j.vetmic.2015.05.017
Parrish, C. R., Aquadro, C. F., Strassheim, M. L., Evermann, J. F., Sgro, J. Y., & Mohammed, H. O. (1991). Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. Journal of Virology, 65(12), 6544-6552. https://doi.org/10.1128/JVI.65.12.6544-6552.1991
Parrish, C. R., Have, P., Foreyt, W. J., Evermann, J. F., Senda, M., & Carmichael, L. E. (1988). The global spread and replacement of canine parvovirus strains. Journal of General Virology, 69(5), 1111-1116. https://doi.org/10.1099/0022-1317-69-5-1111
Pollock, R. V., & Carmichael, L. E. (1982). Maternally derived immunity to canine parvovirus infection: Transfer, decline, and interference with vaccination. Journal of the American Veterinary Medical Association, 180(1), 37-42.
Roth, J. A., & Spickler, A. R. (2010). Duration of immunity induced by companion animal vaccines. Animal Health Research Reviews, 11(2), 165-190. https://doi.org/10.1017/s1466252310000150
Shackelton, L. A., Parrish, C. R., Truyen, U., Holmes, E. C., & Berns, K. I. (2005). High rate of viral evolution associated with the emergence of carnivore parvovirus. Proceedings of the National Academy of Sciences, 102(2), 379-384. https://doi.org/10.1073/pnas.0406765102.
Stucker, K. M., Pagan, I., Cifuente, J. O., Kaelber, J. T., Lillie, T. D., Hafenstein, S. … Parrish, C. R. (2012). The role of evolutionary intermediates in the host adaptation of canine parvovirus. Journal of virology, 86(3), 1514-1521. https://doi.org/10.1128/JVI.06222-11
Tamura, K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution, 9(4), 678-687. https://doi.org/10.1093/oxfordjournals.molbev.a040752
Truyen, U., Agbandje, M., & Parrish, C. R. (1994). Characterization of the feline host range and a specific epitope of feline panleukopenia virus. Virology, 200(2), 494-503. https://doi.org/10.1006/viro.1994.1212
Truyen, U. W. E., Evermann, J. F., Vieler, E., & Parrish, C. R. (1996). Evolution of canine parvovirus involved loss and gain of feline host range. Virology, 215(2), 186-189. https://doi.org/10.1006/viro.1996.0021
Tsao, J., Chapman, M. S., Agbandje, M., Keller, W., Smith, K., Wu, H. … Compans, R. W. (1991). The three-dimensional structure of canine parvovirus and its functional implications. Science, 251(5000), 1456-1464.
Vannamahaxay, S., Vongkhamchanh, S., Intanon, M., Tangtrongsup, S., Tiwananthagorn, S., Pringproa, K., Chuammitri, P. (2017). Molecular characterization of canine parvovirus in Vientiane, Laos. Archives of Virology, 162(5), 1355-1361. https://doi.org/10.1007/s00705-016-3212-1
Voorhees, I. E. H., Lee, H., Allison, A. B., Lopez-Astacio, R., Goodman, L. B., Oyesola, O. O., … Parrish, C. R. (2019). Limited intra-host diversity and background evolution accompany 40 years of canine parvovirus host adaptation and spread. bioRxiv, 714683. https://doi.org/10.1101/714683
Wang, D., Yuan, W., Davis, I., & Parrish, C. R. (1998). Nonstructural protein-2 and the replication of canine parvovirus. Virology, 240(2), 273-281. https://doi.org/10.1006/viro.1997.8946
Wang, J., Lin, P., Zhao, H., Cheng, Y., Jiang, Z., Zhu, H., … Cheng, S. (2016). Continuing evolution of canine parvovirus in China: Isolation of novel variants with an Ala5Gly mutation in the VP2 protein. Infection, Genetics and Evolution, 38, 73-78. https://doi.org/10.1016/j.meegid.2015.12.009
Woolford, L., Crocker, P., Bobrowski, H., Baker, T., & Hemmatzadeh, F. (2017). Detection of the canine parvovirus 2c subtype in Australian dogs. Viral Immunology, 30(5), 371-376. https://doi.org/10.1089/vim.2017.0019

Auteurs

Emily Kwan (E)

Faculty of Science, Sydney School of Veterinary Science, University of Sydney, Camperdown, NSW, Australia.

Maura Carrai (M)

Faculty of Science, Sydney School of Veterinary Science, University of Sydney, Camperdown, NSW, Australia.

Gianvito Lanave (G)

Department of Veterinary Medicine, University of Bari, Valenzano (Bari), Italy.

Jennifer Hill (J)

Vetpath Laboratory Services, Ascot, WA, Australia.

Kylie Parry (K)

NorthWest Vets, Coonamble, NSW, Australia.

Mark Kelman (M)

Faculty of Science, Sydney School of Veterinary Science, University of Sydney, Camperdown, NSW, Australia.

Joanne Meers (J)

School of Veterinary Science, The University of Queensland, Saint Lucia, QLD, Australia.

Nicola Decaro (N)

Department of Veterinary Medicine, University of Bari, Valenzano (Bari), Italy.

Julia A Beatty (JA)

Faculty of Science, Sydney School of Veterinary Science, University of Sydney, Camperdown, NSW, Australia.
Department of Veterinary Clinical Sciences, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China.

Vito Martella (V)

Department of Veterinary Medicine, University of Bari, Valenzano (Bari), Italy.

Vanessa R Barrs (VR)

Faculty of Science, Sydney School of Veterinary Science, University of Sydney, Camperdown, NSW, Australia.
Department of Veterinary Clinical Sciences, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China.

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