1887

Journal of General Virology header logo

Volume 95, Issue 8

Genetic variability of porcine circovirus 2 in vaccinating and non-vaccinating commercial farms Free

Abstract

Vaccines against porcine circovirus 2 (PCV2) are now widely used to control the diseases caused by the virus. Although the vaccines protect pigs against the disease, they do not lead to sterilizing immunity and therefore infections with PCV2 continue in farms. It is expected that, due to its high evolutionary rate, PCV2 can adapt quickly to environmental pressures such as vaccination. The goal of this study was to elucidate the molecular variation of PCV2 in relation to vaccination. PCV2 variability was investigated from samples of infected pigs from five farms where vaccination had never been applied and two farms where pigs had been vaccinated for at least 2 years. For the genetic analysis, full PCV2 genomes were amplified and subsequently pooled by vaccination status from serum of eight vaccinated, infected pigs and 16 non-vaccinated, infected pigs. Variability of viral populations was quantified using next-generation sequencing and subsequent bioinformatics analysis. The number of segregating sites was similar in the non-vaccinated ( = 109) and vaccinated pools ( = 96), but the distribution of these sites in the genome differed. Most notably, in the capsid gene, the number of segregating sites was observed only in the non-vaccinated population. Based on the structural analysis, it is expected that some low-frequency amino acids result in biologically low-fit viruses. On the contrary, D294 in replicase represents a novel amino acid which was dominant and unique in the vaccinated pool. This work showed that variable PCV2 populations were circulating in commercial farms, and that this variability was different in samples obtained from vaccinating and non-vaccinating farms.

  • Received:
  • Accepted:
  • Published Online:
© 2014 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.065318-0
2014-08-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/8/1734.html?itemId=/content/journal/jgv/10.1099/vir.0.065318-0&mimeType=html&fmt=ahah

References

  1. Archer J., Baillie G., Watson S. J., Kellam P., Rambaut A., Robertson D. L. 2012a; Analysis of high-depth sequence data for studying viral diversity: a comparison of next generation sequencing platforms using Segminator II. BMC Bioinformatics 13:47 [View Article][PubMed]
     [Google Scholar]
  2. Archer J., Weber J., Henry K., Winner D., Gibson R., Lee L., Paxinos E., Arts E. J., Robertson D. L.other authors 2012b; Use of four next-generation sequencing platforms to determine HIV-1 coreceptor tropism. PLoS ONE 7:e49602 [View Article][PubMed]
     [Google Scholar]
  3. Beach N. M., Meng X.-J. 2012; Efficacy and future prospects of commercially available and experimental vaccines against porcine circovirus type 2 (PCV2). Virus Res 164:33–42 [View Article][PubMed]
     [Google Scholar]
  4. Blankenberg D., Gordon A., Von Kuster G., Coraor N., Taylor J., Nekrutenko A.Galaxy Team 2010; Manipulation of FASTQ data with Galaxy. Bioinformatics 26:1783–1785 [View Article][PubMed]
     [Google Scholar]
  5. Cai L., Ni J., Xia Y., Zi Z., Ning K., Qiu P., Li X., Wang B., Liu Q.other authors 2012; Identification of an emerging recombinant cluster in porcine circovirus type 2. Virus Res 165:95–102 [View Article][PubMed]
     [Google Scholar]
  6. Carman S., McEwen B., DeLay J., van Dreumel T., Lusis P., Cai H., Fairles J. 2006; Porcine circovirus-2 associated disease in swine in Ontario (2004 to 2005). Can Vet J 47:761–762[PubMed]
     [Google Scholar]
  7. Cheung A. K., Lager K. M., Kohutyuk O. I., Vincent A. L., Henry S. C., Baker R. B., Rowland R. R., Dunham A. G. 2007; Detection of two porcine circovirus type 2 genotypic groups in United States swine herds. Arch Virol 152:1035–1044 [View Article][PubMed]
     [Google Scholar]
  8. Cortey M., Olvera A., Grau-Roma L., Segalés J. 2011a; Further comments on porcine circovirus type 2 (PCV2) genotype definition and nomenclature. Vet Microbiol 149:522–523 [View Article][PubMed]
     [Google Scholar]
  9. Cortey M., Pileri E., Sibila M., Pujols J., Balasch M., Plana J., Segalés J. 2011b; Genotypic shift of porcine circovirus type 2 from PCV-2a to PCV-2b in Spain from 1985 to 2008. Vet J 187:363–368 [View Article][PubMed]
     [Google Scholar]
  10. Dupont K., Nielsen E. O., Baekbo P., Larsen L. E. 2008; Genomic analysis of PCV2 isolates from Danish archives and a current PMWS case-control study supports a shift in genotypes with time. Vet Microbiol 128:56–64 [View Article][PubMed]
     [Google Scholar]
  11. Dupont K., Hjulsager C. K., Kristensen C. S., Baekbo P., Larsen L. E. 2009; Transmission of different variants of PCV2 and viral dynamics in a research facility with pigs mingled from PMWS-affected herds and non-affected herds. Vet Microbiol 139:219–226 [View Article][PubMed]
     [Google Scholar]
  12. Firth C., Charleston M. A., Duffy S., Shapiro B., Holmes E. C. 2009; Insights into the evolutionary history of an emerging livestock pathogen: porcine circovirus 2. J Virol 83:12813–12821 [View Article][PubMed]
     [Google Scholar]
  13. Fort M., Sibila M., Allepuz A., Mateu E., Roerink F., Segalés J. 2008; Porcine circovirus type 2 (PCV2) vaccination of conventional pigs prevents viremia against PCV2 isolates of different genotypes and geographic origins. Vaccine 26:1063–1071 [View Article][PubMed]
     [Google Scholar]
  14. Gerber P. F., Johnson J., Shen H., Striegel D., Xiao C.-T., Halbur P. G., Opriessnig T. 2013; Association of concurrent porcine circovirus (PCV) 2a and 2b infection with PCV associated disease in vaccinated pigs. Res Vet Sci 95:775–781 [View Article][PubMed]
     [Google Scholar]
  15. Gorbalenya A. E., Koonin E. V., Donchenko A. P., Blinov V. M. 1989; Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17:4713–4730 [View Article][PubMed]
     [Google Scholar]
  16. Grau-Roma L., Crisci E., Sibila M., López-Soria S., Nofrarias M., Cortey M., Fraile L., Olvera A., Segalés J. 2008; A proposal on porcine circovirus type 2 (PCV2) genotype definition and their relation with postweaning multisystemic wasting syndrome (PMWS) occurrence. Vet Microbiol 128:23–35 [View Article][PubMed]
     [Google Scholar]
  17. Grau-Roma L., Hjulsager C. K., Sibila M., Kristensen C. S., López-Soria S., Enøe C., Casal J., Bøtner A., Nofrarías M.other authors 2009; Infection, excretion and seroconversion dynamics of porcine circovirus type 2 (PCV2) in pigs from post-weaning multisystemic wasting syndrome (PMWS) affected farms in Spain and Denmark. Vet Microbiol 135:272–282 [View Article][PubMed]
     [Google Scholar]
  18. Kekarainen T., McCullough K., Fort M., Fossum C., Segalés J., Allan G. M. 2010; Immune responses and vaccine-induced immunity against Porcine circovirus type 2. Vet Immunol Immunopathol 136:185–193 [View Article][PubMed]
     [Google Scholar]
  19. Khaiseb S., Sydler T., Zimmermann D., Pospischil A., Sidler X., Brugnera E. 2011; Coreplication of the major genotype group members of porcine circovirus type 2 as a prerequisite to coevolution may explain the variable disease manifestations. J Virol 85:11111–11120 [View Article][PubMed]
     [Google Scholar]
  20. Khayat R., Brunn N., Speir J. A., Hardham J. M., Ankenbauer R. G., Schneemann A., Johnson J. E. 2011; The 2.3-angstrom structure of porcine circovirus 2. J Virol 85:7856–7862 [View Article][PubMed]
     [Google Scholar]
  21. Kim D., Kim C. H., Han K., Seo H. W., Oh Y., Park C., Kang I., Chae C. 2011; Comparative efficacy of commercial Mycoplasma hyopneumoniae and porcine circovirus 2 (PCV2) vaccines in pigs experimentally infected with M. hyopneumoniae and PCV2. Vaccine 29:3206–3212 [View Article][PubMed]
     [Google Scholar]
  22. Lekcharoensuk P., Morozov I., Paul P. S., Thangthumniyom N., Wajjawalku W., Meng X. J. 2004; Epitope mapping of the major capsid protein of type 2 porcine circovirus (PCV2) by using chimeric PCV1 and PCV2. J Virol 78:8135–8145 [View Article][PubMed]
     [Google Scholar]
  23. Librado P., Rozas J. 2009; DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452 [View Article][PubMed]
     [Google Scholar]
  24. Mahé D., Blanchard P., Truong C., Arnauld C., Le Cann P., Cariolet R., Madec F., Albina E., Jestin A. 2000; Differential recognition of ORF2 protein from type 1 and type 2 porcine circoviruses and identification of immunorelevant epitopes. J Gen Virol 81:1815–1824[PubMed]
     [Google Scholar]
  25. Meng X.-J. 2013; Porcine circovirus type 2 (PCV2): pathogenesis and interaction with the immune system. Annu Rev Anim Biosci 1:43–64 [View Article]
     [Google Scholar]
  26. Olvera A., Sibila M., Calsamiglia M., Segalés J., Domingo M. 2004; Comparison of porcine circovirus type 2 load in serum quantified by a real time PCR in postweaning multisystemic wasting syndrome and porcine dermatitis and nephropathy syndrome naturally affected pigs. J Virol Methods 117:75–80 [View Article][PubMed]
     [Google Scholar]
  27. Opriessnig T., Ramamoorthy S., Madson D. M., Patterson A. R., Pal N., Carman S., Meng X. J., Halbur P. G. 2008; Differences in virulence among porcine circovirus type 2 isolates are unrelated to cluster type 2a or 2b and prior infection provides heterologous protection. J Gen Virol 89:2482–2491 [View Article][PubMed]
     [Google Scholar]
  28. Opriessnig T., Patterson A. R., Madson D. M., Pal N., Halbur P. G. 2009; Comparison of efficacy of commercial one dose and two dose PCV2 vaccines using a mixed PRRSV–PCV2–SIV clinical infection model 2–3-months post vaccination. Vaccine 27:1002–1007 [View Article][PubMed]
     [Google Scholar]
  29. Opriessnig T., Xiao C.-T., Gerber P. F., Halbur P. G. 2013; Emergence of a novel mutant PCV2b variant associated with clinical PCVAD in two vaccinated pig farms in the U.S. concurrently infected with PPV2. Vet Microbiol 163:177–183 [View Article][PubMed]
     [Google Scholar]
  30. Opriessnig T., Gerber P. F., Xiao C.-T., Mogler M., Halbur P. G. 2014; A commercial vaccine based on PCV2a and an experimental vaccine based on a variant mPCV2b are both effective in protecting pigs against challenge with a 2013 U.S. variant mPCV2b strain. Vaccine 32:230–237 [View Article][PubMed]
     [Google Scholar]
  31. Quintana J., Balasch M., Segalés J., Calsamiglia M., Rodríguez-Arrioja G. M., Plana-Durán J., Domingo M. 2002; Experimental inoculation of porcine circoviruses type 1 (PCV1) and type 2 (PCV2) in rabbits and mice. Vet Res 33:229–237 [View Article][PubMed]
     [Google Scholar]
  32. Segalés J., Olvera A., Grau-Roma L., Charreyre C., Nauwynck H., Larsen L., Dupont K., McCullough K., Ellis J.other authors 2008; PCV-2 genotype definition and nomenclature. Vet Rec 162:867–868 [View Article][PubMed]
     [Google Scholar]
  33. Segalés J., Allan G., Domingo M. 2012). Porcine circoviruses. In Diseases of Swine, 10th edn. pp. 405–417 Edited by Zimmerman J. J., Karriker L., Ramirez H., Schwartz K. J., Stevenson G. W. Oxford: Wiley-Blackwell;
     [Google Scholar]
  34. Shang S.-B., Jin Y.-L., Jiang X. T., Zhou J.-Y., Zhang X., Xing G., He J. L., Yan Y. 2009; Fine mapping of antigenic epitopes on capsid proteins of porcine circovirus, and antigenic phenotype of porcine circovirus type 2. Mol Immunol 46:327–334 [View Article][PubMed]
     [Google Scholar]
  35. Shen H.-G., Halbur P. G., Opriessnig T. 2012; Prevalence and phylogenetic analysis of the current porcine circovirus 2 genotypes after implementation of widespread vaccination programmes in the USA. J Gen Virol 93:1345–1355 [View Article][PubMed]
     [Google Scholar]
  36. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  37. Zhai S.-L., Chen S.-N., Wei Z.-Z., Zhang J.-W., Huang L., Lin T., Yue C., Ran D.-L., Yuan S.-S.other authors 2011; Co-existence of multiple strains of porcine circovirus type 2 in the same pig from China. Virol J 8:517 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.065318-0
Loading
Genetic variability of porcine circovirus 2 in vaccinating and non-vaccinating commercial farms
J. Gen. Virol. 95, 1734 (2014); https://doi.org/10.1099/vir.0.065318-0
/content/journal/jgv/10.1099/vir.0.065318-0
/content/journal/jgv/10.1099/vir.0.065318-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error