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Archives of Virology

, Volume 164, Issue 5, pp 1361–1369 | Cite as

New variants of canine parvovirus in dogs in southern Brazil

  • Pablo Sebastian Britto de Oliveira
  • Juliana Felipetto Cargnelutti
  • Eduardo Kenji Masuda
  • Rudi Weiblen
  • Eduardo Furtado FloresEmail author
Original Article

Abstract

Carnivore protoparvovirus 1 (canine parvovirus 2, CPV-2) has undergone a rapid evolution through mutations in the capsid protein VP2, giving rise to variants associated with unique clinicopathological and immunological features. VP2 is a major capsid protein involved in key steps of virus biology, including interactions with cellular receptors and with the immune system. This study analyzed the complete VP2 coding sequence of 38 CPV-2 isolates obtained from dogs with clinical parvovirosis in southern Brazil. Amplicons encompassing the whole VP2 coding region were subjected to nucleotide sequencing, and predicted amino acid sequences were analyzed to identify molecular markers of viral variants. Viral variants were classified as CPV-2a, -2b or -2c based on the presence of the amino acid Asn, Asp or Glu, respectively, at VP2 residue 426. Amino acid sequence analysis identified 20 CPV-2c and four CPV-2b isolates. Eleven viruses were identified as New CPV-2a, two as New CPV-2b, and one resembled the original CPV-2 and was designated CPV-2-like. In addition to the mutation at amino acid 426 of VP2, new 2a/2b variants containing a Ser297Ala mutation at residue 297 were identified. CPV-2-like samples contained some mutations that were also present in the original CPV-2 isolate, including as Leu, Thr, Ala and Asp at residues 87, 101, 300 and 305, respectively. The New CPV-2a isolates had three additional mutations (Phe267Tyr, Tyr324Ile and Thr440Ala) associated with selective pressure and development of disease in vaccinated dogs. The resemblance of the CPV-2-like isolate to CPV-2 suggests reemergence of CPV-2 and/or evolution from vaccine strains. Phylogenetic analysis grouped the variants with their respective reference strains, in general, according to amino acid changes. These results demonstrate the high VP2 diversity of CPV circulating in dogs in southern Brazil and indicate the emergence of new viral variants that differ markedly from the current vaccine strains.

Notes

Acknowledgements

We thank the LPV (Veterinary Pathology Laboratory/UFSM), Axys Análises Laboratory and veterinary clinics for providing the clinical samples.

Funding

Funding and scholarships were received from the Brazilian Council for Research (CNPq) (PSBO-Process: 131335/2017-0, EFF-Process: 301363/2017-0, RW-Process: 304153/2014-1) and JFC received a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Parrish CR, O’Connell PH, Evermann JF, Carmichael LE (1985) Natural variation of canine parvovirus. Science (80-) 230:1046–1048CrossRefGoogle Scholar
  2. 2.
    Agbandje M, Parrish CR, Rossmann MG et al (1995) The recognition of parvovirus capsids by antibodies. Academic Press, San DiegoCrossRefGoogle Scholar
  3. 3.
    Decaro N, Buonavoglia C (2012) Canine parvovirus—a review of epidemiological and diagnostic aspects, with emphasis on type 2c. Vet Microbiol 155:1–12.  https://doi.org/10.1016/j.vetmic.2011.09.007 CrossRefGoogle Scholar
  4. 4.
    Shackelton LA, Parrish CR, Truyen U, Holmes EC (2005) High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci USA 102:379–384.  https://doi.org/10.1073/pnas.0406765102 CrossRefGoogle Scholar
  5. 5.
    Parrish CR, Aquadro CF, Strassheim ML et al (1991) Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. J Virol 65:6544–6552Google Scholar
  6. 6.
    Truyen U (2006) Evolution of canine parvovirus–a need for new vaccines? Vet Microbiol 117:9–13.  https://doi.org/10.1016/j.vetmic.2006.04.003 CrossRefGoogle Scholar
  7. 7.
    Parrish CR, Have P, Foreyt WJ et al (1988) The global spread and replacement of canine parvovirus strains. J Gen Virol 69:1111–1116.  https://doi.org/10.1099/0022-1317-69-5-1111 CrossRefGoogle Scholar
  8. 8.
    Buonavoglia C, Martella V, Pratelli A et al (2001) Evidence for evolution of canine parvovirus type 2 in Italy. J Gen Virol 82:3021–3025.  https://doi.org/10.1099/0022-1317-82-12-3021 CrossRefGoogle Scholar
  9. 9.
    Streck AF, de Souza CK, Gonçalves KR et al (2009) First detection of canine parvovirus type 2c in Brazil. Braz J Microbiol 40:465–469.  https://doi.org/10.1590/S1517-83822009000300008 CrossRefGoogle Scholar
  10. 10.
    de Oliveira PSB, Cargnelutti JF, Masuda EK et al (2018) Epidemiological, clinical and pathological features of canine parvovirus 2c infection in dogs from southern Brazil. Pesqui Vet Bras 38:113–118.  https://doi.org/10.1590/1678-5150-pvb-5122 CrossRefGoogle Scholar
  11. 11.
    Miranda C, Thompson G (2016) Canine parvovirus: the worldwide occurrence of antigenic variants. J Gen Virol 97:2043–2057.  https://doi.org/10.1099/jgv.0.000540 CrossRefGoogle Scholar
  12. 12.
    Zhou P, Zeng W, Zhang X, Li S (2017) The genetic evolution of canine parvovirus—a new perspective. PLoS One 12:e0175035.  https://doi.org/10.1371/journal.pone.0175035 CrossRefGoogle Scholar
  13. 13.
    Mira F, Dowgier G, Purpari G et al (2018) Molecular typing of a novel canine parvovirus type 2a mutant circulating in Italy. Infect Genet Evol 61:67–73.  https://doi.org/10.1016/j.meegid.2018.03.010 CrossRefGoogle Scholar
  14. 14.
    Monteiro K, Allendorf SD, Vicente AF et al (2016) Viral type characterization and clinical aspects of canine parvovirus in naturally infected dogs in São Paulo State, Brazil. Pesqui Vet Bras 36:1181–1185.  https://doi.org/10.1590/s0100-736x2016001200007 CrossRefGoogle Scholar
  15. 15.
    Maya L, Calleros L, Francia L et al (2013) Phylodynamics analysis of canine parvovirus in Uruguay: evidence of two successive invasions by different variants. Arch Virol 158:1133–1141.  https://doi.org/10.1007/s00705-012-1591-5 CrossRefGoogle Scholar
  16. 16.
    Calderón MG, Romanutti C, Wilda M et al (2015) Resurgence of canine parvovirus 2a strain in the domestic dog population from Argentina. J Virol Methods 222:145–149.  https://doi.org/10.1016/j.jviromet.2015.06.012 CrossRefGoogle Scholar
  17. 17.
    Wu J, Gao X-T, Hou S-H et al (2015) Molecular epidemiological and phylogenetic analyses of canine parvovirus in domestic dogs and cats in Beijing, 2010–2013. J Vet Med Sci 77:2010–2013.  https://doi.org/10.1292/jvms.14-0665 CrossRefGoogle Scholar
  18. 18.
    Tsao J, Chapman MS, Agbandje M et al (1991) The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456–1464.  https://doi.org/10.2210/pdb2dpv/pdb CrossRefGoogle Scholar
  19. 19.
    Hueffer K, Parker JSL, Weichert WS et al (2003) The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J Virol 77:1718–1726.  https://doi.org/10.1128/JVI.77.3.1718-1726.2003 CrossRefGoogle Scholar
  20. 20.
    Pinto LD, Streck AF, Gonçalves KR et al (2012) Typing of canine parvovirus strains circulating in Brazil between 2008 and 2010. Virus Res 165:29–33.  https://doi.org/10.1016/J.VIRUSRES.2012.01.001 CrossRefGoogle Scholar
  21. 21.
    Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241CrossRefGoogle Scholar
  22. 22.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  23. 23.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  24. 24.
    Truyen U (1999) Emergence and recent evolution of canine parvovirus. Vet Microbiol 69:47–50.  https://doi.org/10.1016/S0378-1135(99)00086-3 CrossRefGoogle Scholar
  25. 25.
    Li C, Tang J, Chen Z et al (2018) Genetic characterization of the complete genome of a mutant canine parvovirus isolated in China. Arch Virol 163:521–525.  https://doi.org/10.1007/s00705-017-3586-8 CrossRefGoogle Scholar
  26. 26.
    Pereira CAD, Leal ÉS, Durigon ÉL (2007) Selective regimen shift and demographic growth increase associated with the emergence of high-fitness variants of canine parvovirus. Infect Genet Evol 7:399–409.  https://doi.org/10.1016/j.meegid.2006.03.007 CrossRefGoogle Scholar
  27. 27.
    Mittal M, Chakravarti S, Mohapatra JK et al (2014) Molecular typing of canine parvovirus strains circulating from 2008 to 2012 in an organized kennel in India reveals the possibility of vaccination failure. Infect Genet Evol 23:1–6CrossRefGoogle Scholar
  28. 28.
    Gagnon CA, Allard V, Cloutier G (2016) Canine parvovirus type 2B is the most prevalent genomic variant strain found in parvovirus antigen positive diarrheic dog feces samples across Canada. Can Vet J 57:29–31Google Scholar
  29. 29.
    Geng Y, Guo D, Li C et al (2015) Co-circulation of the rare CPV-2c with unique Gln370Arg substitution, new CPV-2b with unique Thr440Ala substitution, and new CPV-2a with high prevalence and variation in Heilongjiang Province, Northeast China. PLoS One 10:e0137288.  https://doi.org/10.1371/journal.pone.0137288 CrossRefGoogle Scholar
  30. 30.
    Li G, Ji S, Zhai X et al (2017) Evolutionary and genetic analysis of the VP2 gene of canine parvovirus. BMC Genomics 18:534.  https://doi.org/10.1186/s12864-017-3935-8 CrossRefGoogle Scholar
  31. 31.
    Fontana DS, Rocha PRD, Cruz RAS et al (2013) A phylogenetic study of canine parvovirus type 2c in midwestern Brazil. Pesqui Vet Bras 33:214–218.  https://doi.org/10.1590/S0100-736X2013000200013 CrossRefGoogle Scholar
  32. 32.
    Hernández B, Catala-López F (2015) Are licensed canine parvovirus (CPV2 and CPV2b) vaccines able to elicit protection against CPV2c subtype in puppies? A systematic review of controlled clinical trials. Vet Microbiol 180:1–9.  https://doi.org/10.1016/J.VETMIC.2015.07.027 CrossRefGoogle Scholar
  33. 33.
    Pérez R, Calleros L, Marandino A et al (2014) Phylogenetic and genome-wide deep-sequencing analyses of canine parvovirus reveal co-infection with field variants and emergence of a recent recombinant strain. PLoS One 9:e111779.  https://doi.org/10.1371/journal.pone.0111779 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Setor de Virologia, Departamento de Medicina Veterinária Preventiva, Centro de Ciências RuraisUniversidade Federal de Santa Maria (UFSM)Santa MariaBrazil
  2. 2.Axys Análises Laboratório Veterinário e ConsultoriaPorto AlegreBrazil
  3. 3.Laboratório de Bacteriologia, Departamento de Medicina Veterinária Preventiva, Centro de Ciências RuraisUniversidade Federal de Santa Maria (UFSM)Santa MariaBrazil
  4. 4.Programa de Pós-Graduação em Medicina VeterináriaUniversidade Federal de Santa Maria (UFSM)Santa MariaBrazil

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