1887

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Volume 97, Issue 12

Genetic diversity and phenotypic associations of feline caliciviruses from cats in Switzerland Free

Abstract

Feline calicivirus (FCV) is a common viral pathogen in domestic cats worldwide. The variable regions of the capsid (VP1) gene of FCV have one of the highest recorded rates of molecular evolution. Understanding the genetic diversity and phylogeny of FCV is a prerequisite to exploring the epidemiology and pathogenesis of this virus and to the development of efficacious vaccine strategies. In this study, we undertook a nationwide molecular characterization of FCV using for the first time nearly complete capsid (VP1) gene sequences. Sequences from 66 FCV samples were used to investigate the correlation between viral phylogeny and several traits, including geographic origin, signalment, husbandry, FCV vaccination and co-infections. Codon-based nucleotide alignment showed that individual nucleotides and their corresponding amino acid sites were either invariant or highly variable. Using a threshold of 20 % genetic distance in variable region E, FCV samples were grouped into 52 strains, 10 of which comprised two to three samples. Significant associations between FCV phylogeny and host characteristics were found, specifically the pedigree status of the cats, and two well-supported lineages were identified in which the current FCV strain definition was confounded. No correlation between viral genetic distances and geographic distances was evident. The greater resolution of the FCV phylogeny in this study compared to previous studies can be attributed to our use of more conserved regions of the capsid (VP1) gene; nonetheless, our results were still hampered by sequence saturation. The study highlights the need for whole-genome sequences for FCV phylogeny studies.

  • Received:
  • Accepted:
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Keyword(s): capsid (VP1) gene , Feline calicivirus , hypervariable region E , pedigree cat , phylogenetic analyses and trait correlation
© 2016 The Authors
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2016-12-16
2024-04-18
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References

  1. Abd-Eldaim M., Potgieter L., Kennedy M. 2005; Genetic analysis of feline caliciviruses associated with a hemorrhagic-like disease. J Vet Diagn Invest 17:420–429 [View Article][PubMed]
     [Google Scholar]
  2. Abd-Eldaim M. M., Wilkes R. P., Thomas K. V., Kennedy M. A. 2009; Development and validation of a TaqMan real-time reverse transcription-PCR for rapid detection of feline calicivirus. Arch Virol 154:555–560 [View Article][PubMed]
     [Google Scholar]
  3. Battilani M., Vaccari F., Carelle M. S., Morandi F., Benazzi C., Kipar A., Dondi F., Scagliarini A. 2013; Virulent feline calicivirus disease in a shelter in Italy: a case description. Res Vet Sci 95:283–290 [View Article][PubMed]
     [Google Scholar]
  4. Bennett D., Gaskell R. M., Mills A., Knowles J., Carter S., McArdle F. 1989; Detection of feline calicivirus antigens in the joints of infected cats. Vet Rec 124:329–332 [View Article][PubMed]
     [Google Scholar]
  5. Berger A., Willi B., Meli M. L., Boretti F. S., Hartnack S., Dreyfus A., Lutz H., Hofmann-Lehmann R. 2015; Feline calicivirus and other respiratory pathogens in cats with Feline calicivirus-related symptoms and in clinically healthy cats in Switzerland. BMC Vet Res 11:282 [View Article][PubMed]
     [Google Scholar]
  6. Binns S. H., Dawson S., Speakman A. J., Cuevas L. E., Hart C. A., Gaskell C. J., Morgan K. L., Gaskell R. M. 2000; A study of feline upper respiratory tract disease with reference to prevalence and risk factors for infection with feline calicivirus and feline herpesvirus. J Feline Med Surg 2:123–133 [View Article][PubMed]
     [Google Scholar]
  7. Bundesamt für Landestopographie 2015 http://www.swisstopo.admin.ch Swiss BOUNDARIES3D accessed on March 2015.
  8. Butts C. T. 2014; Sna: tools for social network analysis. http://CRAN.r-project.org/package=sna
  9. Carr D. 2015; Hexbin: hexagonal binning routines. http://CRAN.r-project.org/package=hexbin
  10. Centers for Disease Control and Prevention 2016 https://www.cdc.gov/epiinfo/index.html Epi InfoTM accessed on August 2016.
  11. Coyne K. P., Dawson S., Radford A. D., Cripps P. J., Porter C. J., McCracken C. M., Gaskell R. M. 2006a; Long-term analysis of feline calicivirus prevalence and viral shedding patterns in naturally infected colonies of domestic cats. Vet Microbiol 118:12–25 [View Article][PubMed]
     [Google Scholar]
  12. Coyne K. P., Jones B. R., Kipar A., Chantrey J., Porter C. J., Barber P. J., Dawson S., Gaskell R. M., Radford A. D. 2006b; Lethal outbreak of disease associated with feline calicivirus infection in cats. Vet Rec 158:544–550 [View Article][PubMed]
     [Google Scholar]
  13. Coyne K. P., Reed F. C., Porter C. J., Dawson S., Gaskell R. M., Radford A. D. 2006c; Recombination of feline calicivirus within an endemically infected cat colony. J Gen Virol 87:921–926 [View Article][PubMed]
     [Google Scholar]
  14. Coyne K. P., Edwards D., Radford A. D., Cripps P., Jones D., Wood J. L., Gaskell R. M., Dawson S. 2007a; Longitudinal molecular epidemiological analysis of feline calicivirus infection in an animal shelter: a model for investigating calicivirus transmission within high-density, high-turnover populations. J Clin Microbiol 45:3239–3244 [View Article][PubMed]
     [Google Scholar]
  15. Coyne K. P., Gaskell R. M., Dawson S., Porter C. J., Radford A. D. 2007b; Evolutionary mechanisms of persistence and diversification of a calicivirus within endemically infected natural host populations. J Virol 81:1961–1971 [View Article][PubMed]
     [Google Scholar]
  16. Coyne K. P., Christley R. M., Pybus O. G., Dawson S., Gaskell R. M., Radford A. D. 2012; Large-scale spatial and temporal genetic diversity of feline calicivirus. J Virol 86:11356–11367 [View Article][PubMed]
     [Google Scholar]
  17. Darriba D., Taboada G. L., Doallo R., Posada D. 2012; jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772 [View Article][PubMed]
     [Google Scholar]
  18. Fernandez M., Manzanilla E. G., Lloret A., León M., Thibault J. C. 2016; Prevalence of feline herpesvirus-1, feline calicivirus, Chlamydophila felis and Mycoplasma felis DNA and associated risk factors in cats in Spain with upper respiratory tract disease, conjunctivitis and/or gingivostomatitis. J Feline Med Surg Epub ahead of print 2016 Feb 26 [View Article][PubMed]
     [Google Scholar]
  19. Foley J., Hurley K., Pesavento P. A., Poland A., Pedersen N. C. 2006; Virulent systemic feline calicivirus infection: local cytokine modulation and contribution of viral mutants. J Feline Med Surg 8:55–61 [View Article][PubMed]
     [Google Scholar]
  20. Geissler K., Schneider K., Platzer G., Truyen B., Kaaden O. R., Truyen U. 1997; Genetic and antigenic heterogeneity among feline calicivirus isolates from distinct disease manifestations. Virus Res 48:193–206 [View Article][PubMed]
     [Google Scholar]
  21. Glenn M., Radford A. D., Turner P. C., Carter M., Lowery D., DeSilver D. A., Meanger J., Baulch-Brown C., Bennett M., Gaskell R. M. 1999; Nucleotide sequence of UK and Australian isolates of feline calicivirus (FCV) and phylogenetic analysis of FCVs. Vet Microbiol 67:175–193 [View Article][PubMed]
     [Google Scholar]
  22. GlobeFeed 2014 http://distancecalculator.globefeed.com Switzerland Distance Calculator, accessed on June 2015
  23. Helps C., Lait P., Tasker S., Harbour D. 2002; Melting curve analysis of feline calicivirus isolates detected by real-time reverse transcription PCR. J Virol Methods 106:241–244 [View Article][PubMed]
     [Google Scholar]
  24. Hofmann-Lehmann R., Holznagel E., Ossent P., Lutz H. 1997; Parameters of disease progression in long-term experimental feline retrovirus (feline immunodeficiency virus and feline leukemia virus) infections: hematology, clinical chemistry, and lymphocyte subsets. Clin Diagn Lab Immunol 4:33–42[PubMed]
     [Google Scholar]
  25. Hou J., Sánchez-Vizcaíno F., McGahie D., Lesbros C., Almeras T., Howarth D., O'Hara V., Dawson S., Radford A. D. 2016; European molecular epidemiology and strain diversity of feline calicivirus. Vet Rec 178:114–115 [View Article][PubMed]
     [Google Scholar]
  26. Huelsenbeck J. P., Ronquist F. 2001; MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755 [View Article][PubMed]
     [Google Scholar]
  27. Katoh K., Standley D. M. 2013; MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 [View Article][PubMed]
     [Google Scholar]
  28. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S. et al. 2012; Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649 [View Article][PubMed]
     [Google Scholar]
  29. Maine Coon Association 2016 http://www.mca.ch/unsere-zuechter/schweiz List of Maine Coon breeders in Switzerland, accessed on August 2016
  30. Meyer A., Kershaw O., Klopfleisch R. 2011; Feline calicivirus-associated virulent systemic disease: not necessarily a local epizootic problem. Vet Rec 168:589 [View Article][PubMed]
     [Google Scholar]
  31. O'Brien S. J., Roelke M. E., Marker L., Newman A., Winkler C. A., Meltzer D., Colly L., Evermann J. F., Bush M., Wildt D. E. 1985; Genetic basis for species vulnerability in the cheetah. Science 227:1428–1434 [View Article][PubMed]
     [Google Scholar]
  32. Ohe K., Sakai S., Sunaga F., Murakami M., Kiuchi A., Fukuyama M., Furuhata K., Hara M., Soma T. et al. 2006; Detection of feline calicivirus (FCV) from vaccinated cats and phylogenetic analysis of its capsid genes. Vet Res Commun 30:293–305 [View Article][PubMed]
     [Google Scholar]
  33. Ohe K., Sakai S., Takahasi T., Sunaga F., Murakami M., Kiuchi A., Fukuyama M., Furuhata K., Hara M. et al. 2007; Genogrouping of vaccine breakdown strains (VBS) of feline calicivirus in Japan. Vet Res Commun 31:497–507 [View Article][PubMed]
     [Google Scholar]
  34. Ossiboff R. J., Sheh A., Shotton J., Pesavento P. A., Parker J. S. 2007; Feline caliciviruses (FCVs) isolated from cats with virulent systemic disease possess in vitro phenotypes distinct from those of other FCV isolates. J Gen Virol 88:506–517 [View Article][PubMed]
     [Google Scholar]
  35. Paradis E., Claude J., Strimmer K. 2004; APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290 [View Article][PubMed]
     [Google Scholar]
  36. Parker J., Rambaut A., Pybus O. G. 2008; Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 8:239–246 [View Article][PubMed]
     [Google Scholar]
  37. Pedersen N. C., Hawkins K. F. 1995; Mechanisms for persistence of acute and chronic feline calicivirus infections in the face of vaccination. Vet Microbiol 47:141–156 [View Article][PubMed]
     [Google Scholar]
  38. Pedersen N. C., Elliott J. B., Glasgow A., Poland A., Keel K. 2000; An isolated epizootic of hemorrhagic-like fever in cats caused by a novel and highly virulent strain of feline calicivirus. Vet Microbiol 73:281–300 [View Article][PubMed]
     [Google Scholar]
  39. Pesavento P. A., MacLachlan N. J., Dillard-Telm L., Grant C. K., Hurley K. F. 2004; Pathologic, immunohistochemical, and electron microscopic findings in naturally occurring virulent systemic feline calicivirus infection in cats. Vet Pathol 41:257–263 [View Article][PubMed]
     [Google Scholar]
  40. Pet Food Manufacturers' Association 2012 http://www.pfma.org.uk/pet-population-2008-2012 Pet population 2008 to 2012, accessed on June 2016
  41. Poulet H., Brunet S., Soulier M., Leroy V., Goutebroze S., Chappuis G. 2000; Comparison between acute oral/respiratory and chronic stomatitis/gingivitis isolates of feline calicivirus: pathogenicity, antigenic profile and cross-neutralisation studies. Arch Virol 145:243–261 [View Article][PubMed]
     [Google Scholar]
  42. Prikhodko V. G., Sandoval-Jaime C., Abente E. J., Bok K., Parra G., Rogozin I. B., Ostlund E. N., Green K. Y., Sosnovtsev S. 2014; Genetic characterization of feline calicivirus strains associated with varying disease manifestations during an outbreak season in Missouri (1995–1996). Virus Genes 48:96–110 [View Article][PubMed]
     [Google Scholar]
  43. QGIS Development Team 2015 http://qgis.osgeo.org QGIS geographic information system. Open source geospatial foundation project, accessed on March 2015
  44. Radford A. D., Bennett M., McArdle F., Dawson S., Turner P. C., Glenn M. A., Gaskell R. M. 1997; The use of sequence analysis of a feline calicivirus (FCV) hypervariable region in the epidemiological investigation of FCV related disease and vaccine failures. Vaccine 15:1451–1458 [View Article][PubMed]
     [Google Scholar]
  45. Radford A. D., Turner P. C., Bennett M., McArdle F., Dawson S., Glenn M. A., Williams R. A., Gaskell R. M. 1998; Quasispecies evolution of a hypervariable region of the feline calicivirus capsid gene in cell culture and in persistently infected cats. J Gen Virol 79:1–10 [View Article][PubMed]
     [Google Scholar]
  46. Radford A. D., Willoughby K., Dawson S., McCracken C., Gaskell R. M. 1999; The capsid gene of feline calicivirus contains linear B-cell epitopes in both variable and conserved regions. J Virol 73:8496–8502[PubMed]
     [Google Scholar]
  47. Radford A. D., Dawson S., Wharmby C., Ryvar R., Gaskell R. M. 2000; Comparison of serological and sequence-based methods for typing feline calcivirus isolates from vaccine failures. Vet Rec 146:117–123 [View Article][PubMed]
     [Google Scholar]
  48. Radford A. D., Sommerville L. M., Dawson S., Kerins A. M., Ryvar R., Gaskell R. M. 2001; Molecular analysis of isolates of feline calicivirus from a population of cats in a rescue shelter. Vet Rec 149:477–481 [View Article][PubMed]
     [Google Scholar]
  49. Radford A. D., Dawson S., Ryvar R., Coyne K., Johnson D. R., Cox M. B., Acke E. F., Addie D. D., Gaskell R. M. 2003; High genetic diversity of the immunodominant region of the feline calicivirus capsid gene in endemically infected cat colonies. Virus Genes 27:145–155[PubMed] [CrossRef]
     [Google Scholar]
  50. Radford A. D., Dawson S., Coyne K. P., Porter C. J., Gaskell R. M. 2006; The challenge for the next generation of feline calicivirus vaccines. Vet Microbiol 117:14–18 [View Article][PubMed]
     [Google Scholar]
  51. Radford A. D., Coyne K. P., Dawson S., Porter C. J., Gaskell R. M. 2007; Feline calicivirus. Vet Res 38:319–335 [View Article][PubMed]
     [Google Scholar]
  52. Radford A. D., Addie D., Belák S., Boucraut-Baralon C., Egberink H., Frymus T., Gruffydd-Jones T., Hartmann K., Hosie M. J. et al. 2009; Feline calicivirus infection. ABCD guidelines on prevention and management. J Feline Med Surg 11:556–564 [View Article][PubMed]
     [Google Scholar]
  53. Radford A. D., Chapman D., Dixon L., Chantrey J., Darby A. C., Hall N. 2012; Application of next-generation sequencing technologies in virology. J Gen Virol 93:1853–1868 [View Article][PubMed]
     [Google Scholar]
  54. Rambaut A., Lam T. T., Max Carvalho L., Pybus O. G. 2016; Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2: [View Article][PubMed]
     [Google Scholar]
  55. Reubel G. H., George J. W., Higgins J., Pedersen N. C. 1994; Effect of chronic feline immunodeficiency virus infection on experimental feline calicivirus-induced disease. Vet Microbiol 39:335–351 [View Article][PubMed]
     [Google Scholar]
  56. Reynolds B. S., Poulet H., Pingret J. L., Jas D., Brunet S., Lemeter C., Etievant M., Boucraut-Baralon C. 2009; A nosocomial outbreak of feline calicivirus associated virulent systemic disease in France. J Feline Med Surg 11:633–644 [View Article][PubMed]
     [Google Scholar]
  57. Robilotti E., Deresinski S., Pinsky B. A. 2015; Norovirus. Clin Microbiol Rev 28:134–164 [View Article][PubMed]
     [Google Scholar]
  58. Rong S., Slade D., Floyd-Hawkins K., Wheeler D. 2006; Characterization of a highly virulent feline calicivirus and attenuation of this virus. Virus Res 122:95–108 [View Article][PubMed]
     [Google Scholar]
  59. Ruch-Gallie R. A., Veir J. K., Hawley J. R., Lappin M. R. 2011; Results of molecular diagnostic assays targeting feline herpesvirus-1 and feline calicivirus in adult cats administered modified live vaccines. J Feline Med Surg 13:541–545 [View Article][PubMed]
     [Google Scholar]
  60. Schliep K. P. 2011; phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593 [View Article][PubMed]
     [Google Scholar]
  61. Schorr-Evans E. M., Poland A., Johnson W. E., Pedersen N. C. 2003; An epizootic of highly virulent feline calicivirus disease in a hospital setting in New England. J Feline Med Surg 5:217–226 [View Article][PubMed]
     [Google Scholar]
  62. Schulz B. S., Hartmann K., Unterer S., Eichhorn W., Majzoub M., Homeier-Bachmann T., Truyen U., Ellenberger C., Huebner J. 2011; Two outbreaks of virulent systemic feline calicivirus infection in cats in Germany. Berl Munch Tierarztl Wochenschr 124:186–193[PubMed]
     [Google Scholar]
  63. Schweizer Tierschutz 2005 http://www.tierschutz.com/publikationen STS Merkblatt Heimtiere, accessed on June 2016
  64. Seal B. S., Ridpath J. F., Mengeling W. L. 1993; Analysis of feline calicivirus capsid protein genes: identification of variable antigenic determinant regions of the protein. J Gen Virol 74:2519–2524 [View Article][PubMed]
     [Google Scholar]
  65. Stamatakis A. 2006; RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690 [View Article][PubMed]
     [Google Scholar]
  66. Tandon R., Cattori V., Pepin A. C., Riond B., Meli M. L., McDonald M., Doherr M. G., Lutz H., Hofmann-Lehmann R. 2008; Association between endogenous feline leukemia virus loads and exogenous feline leukemia virus infection in domestic cats. Virus Res 135:136–143 [View Article][PubMed]
     [Google Scholar]
  67. Tohya Y., Yokoyama N., Maeda K., Kawaguchi Y., Mikami T. 1997; Mapping of antigenic sites involved in neutralization on the capsid protein of feline calicivirus. J Gen Virol 78:303–305 [View Article][PubMed]
     [Google Scholar]
  68. Wardley R. C., Povey R. C. 1977; The clinical disease and patterns of excretion associated with three different strains of feline caliciviruses. Res Vet Sci 23:7–14[PubMed]
     [Google Scholar]
  69. Willi B., Spiri A. M., Meli M. L., Samman A., Hoffmann K., Sydler T., Cattori V., Graf F., Diserens K. A. et al. 2016; Molecular characterization and virus neutralization patterns of severe, non-epizootic forms of feline calicivirus infections resembling virulent systemic disease in cats in Switzerland and in Liechtenstein. Vet Microbiol 182:202–212 [View Article][PubMed]
     [Google Scholar]
  70. Xia X. 2013; DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30:1720–1728 [View Article][PubMed]
     [Google Scholar]
  71. Xia X., Lemey P. 2009; Assessing substitution saturation with DAMBE. In The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny Lemey P., Salemi M., Vandamme A. M. New York: Cambridge University Press;
     [Google Scholar]
  72. Xia X., Xie Z., Salemi M., Chen L., Wang Y. 2003; An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7 [View Article][PubMed]
     [Google Scholar]
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Genetic diversity and phenotypic associations of feline caliciviruses from cats in Switzerland
J. Gen. Virol. 97, 3253 (2016); https://doi.org/10.1099/jgv.0.000622
/content/journal/jgv/10.1099/jgv.0.000622
/content/journal/jgv/10.1099/jgv.0.000622
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