Genetic and experimental comparison of porcine circovirus type 2 (PCV2) isolates from cases with and without PCV2-associated lesions provides evidence for differences in virulence Free

Abstract

There are marked differences in the clinical expression of diseases associated with porcine circovirus type 2 (PCV2) in the field. The objective of this study was to compare the sequences and pathogenicity of PCV2 isolates from field cases with and without PCV2-associated lesions. Forty-two specific-pathogen-free (SPF) pigs were assigned randomly to three groups of 14 pigs each. At 7 weeks of age, group 1 pigs were mock-inoculated with saline, group 2 pigs were inoculated with PCV2-4838 (isolated from a pig with no evidence of PCV2-associated lymphoid lesions) and group 3 pigs were inoculated with PCV2-40895 (isolated from a pig with PCV2-associated lymphoid lesions and disease). The PCV2-4838 and PCV2-40895 isolates shared approximately 98.9 % nucleotide sequence identity across the entire genome. A total of nine amino acid changes in ORF2 and two amino acid changes in ORF1 were identified between the two isolates. PCV2-4838-inoculated pigs had significantly more genomic copy numbers of PCV2 in their sera at 7 days post-inoculation (p.i.) (<0.0001) and significantly fewer genomic copy numbers at 14, 21 and 28 days p.i. (<0.05) compared with pigs inoculated with the PCV2-40895 isolate. Microscopic lesions in lymphoid tissues were significantly less severe (<0.05) and the amount of PCV2 antigen associated with these lesions was significantly lower (<0.05) in pigs inoculated with PCV2-4838. The results of this study suggest that PCV2 isolates from the USA differ in virulence in an SPF pig model.

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2006-10-01
2024-03-28
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References

  1. Allan G. M., Ellis J. A. 2000; Porcine circoviruses: a review. J Vet Diagn Invest 12:3–14 [CrossRef]
    [Google Scholar]
  2. Allan G. M., McNeilly F., Kennedy S., Daft B., Clarke E. G., Ellis J. A., Haines D. M., Meehan B. M., Adair B. M. 1998; Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and Europe. J Vet Diagn Invest 10:3–10 [CrossRef]
    [Google Scholar]
  3. Allan G. M., Kennedy S., McNeilly F., Foster J. C., Ellis J. A., Krakowka S. J., Meehan B. M., Adair B. M. 1999; Experimental reproduction of severe wasting disease by co-infection of pigs with porcine circovirus and porcine parvovirus. J Comp Pathol 121:1–11 [CrossRef]
    [Google Scholar]
  4. Allan G. M., McNeilly F., Ellis J., Krakowka S., Meehan B., McNair I., Walker I., Kennedy S. 2000a; Experimental infection of colostrum deprived piglets with porcine circovirus 2 (PCV2) and porcine reproductive and respiratory syndrome virus (PRRSV) potentiates PCV2 replication. Arch Virol 145:2421–2429 [CrossRef]
    [Google Scholar]
  5. Allan G. M., McNeilly F., Kennedy S., Meehan B., Ellis J., Krakowka S. 2000b; Immunostimulation, PCV-2 and PMWS. Vet Rec 147:170–171
    [Google Scholar]
  6. Bereiter M., Young T. F., Joo H. S., Ross R. F. 1990; Evaluation of the ELISA and comparison of the complement fixation test and radial immunodiffusion enzyme assay for detection of antibodies against Mycoplasma hyopneumoniae in swine serum. Vet Microbiol 25:177–192 [CrossRef]
    [Google Scholar]
  7. Cheung A. K. 2003; Comparative analysis of the transcriptional patterns of pathogenic and nonpathogenic porcine circoviruses. Virology 310:41–49 [CrossRef]
    [Google Scholar]
  8. Choi J., Stevenson G. W., Kiupel M., Harrach B., Anothayanontha L., Kanitz C. L., Mittal S. K. 2002; Sequence analysis of old and new strains of porcine circovirus associated with congenital tremors in pigs and their comparison with strains involved with postweaning multisystemic wasting syndrome. Can J Vet Res 66:217–224
    [Google Scholar]
  9. De Boisséson C., Béven V., Bigarré L., Thiéry R., Rose N., Eveno E., Madec F., Jestin A. 2004; Molecular characterization of Porcine circovirus type 2 isolates from post-weaning multisystemic wasting syndrome-affected and non-affected pigs. J Gen Virol 85:293–304 [CrossRef]
    [Google Scholar]
  10. Ellis J., Hassard L., Clark E. & 9 other authors 1998; Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Can Vet J 39:44–51
    [Google Scholar]
  11. Farnham M. W., Choi Y. K., Goyal S. M., Joo H. S. 2003; Isolation and characterization of porcine circovirus type-2 from sera of stillborn fetuses. Can J Vet Res 67:108–113
    [Google Scholar]
  12. Fenaux M., Halbur P. G., Gill M., Toth T. E., Meng X.-J. 2000; Genetic characterization of type 2 porcine circovirus (PCV-2) from pigs with postweaning multisystemic wasting syndrome in different geographic regions of North America and development of a differential PCR-restriction fragment length polymorphism assay to detect and differentiate between infections with PCV-1 and PCV-2. J Clin Microbiol 38:2494–2503
    [Google Scholar]
  13. Fenaux M., Halbur P. G., Haqshenas G., Royer R., Thomas P., Nawagitgul P., Gill M., Toth T. E., Meng X.-J. 2002; Cloned genomic DNA of type 2 porcine circovirus is infectious when injected directly into the liver and lymph nodes of pigs: characterization of clinical disease, virus distribution, and pathologic lesions. J Virol 76:541–551 [CrossRef]
    [Google Scholar]
  14. Fenaux M., Opriessnig T., Halbur P. G., Meng X.-J. 2003; Immunogenicity and pathogenicity of chimeric infectious DNA clones of pathogenic porcine circovirus type 2 (PCV2) and nonpathogenic PCV1 in weanling pigs. J Virol 77:11232–11243 [CrossRef]
    [Google Scholar]
  15. Fenaux M., Opriessnig T., Halbur P. G., Elvinger F., Meng X.-J. 2004a; A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the genomic backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 78:6297–6303 [CrossRef]
    [Google Scholar]
  16. Fenaux M., Opriessnig T., Halbur P. G., Elvinger F., Meng X.-J. 2004b; Two amino acid mutations in the capsid protein of type 2 porcine circovirus (PCV2) enhanced PCV2 replication in vitro and attenuated the virus in vivo . J Virol 78:13440–13446 [CrossRef]
    [Google Scholar]
  17. Grierson S. S., King D. P., Wellenberg G. J., Banks M. 2004; Genome sequence analysis of 10 Dutch porcine circovirus type 2 (PCV-2) isolates from a PMWS case-control study. Res Vet Sci 77:265–268 [CrossRef]
    [Google Scholar]
  18. Haines D. M., Waters E. H., Clark E. G. 1993; Immunohistochemical detection of swine influenza A virus in formalin-fixed and paraffin-embedded tissues. Can J Vet Res 57:33–36
    [Google Scholar]
  19. Halbur P. G., Paul P. S., Frey M. L., Landgraf J., Eernisse K., Meng X. J., Lum M. A., Andrews J. J., Rathje J. A. 1995; Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 32:648–660 [CrossRef]
    [Google Scholar]
  20. Hamel A. L., Lin L. L., Nayar G. P. S. 1998; Nucleotide sequence of porcine circovirus associated with postweaning multisystemic wasting syndrome. J Virol 72:5262–5267
    [Google Scholar]
  21. Harding J. C. S., Clark E. G. 1997; Recognizing and diagnosing postweaning multisystemic wasting syndrome (PMWS). J Swine Health Prod 5:201–203
    [Google Scholar]
  22. Harms P. A., Sorden S. D., Halbur P. G., Bolin S. R., Lager K. M., Morozov I., Paul P. S. 2001; Experimental reproduction of severe disease in CD/CD pigs concurrently infected with type 2 porcine circovirus and porcine reproductive and respiratory syndrome virus. Vet Pathol 38:528–539 [CrossRef]
    [Google Scholar]
  23. Harms P. A., Halbur P. G., Sorden S. D. 2002; Three cases of porcine respiratory disease complex associated with porcine circovirus type 2 infection. J Swine Health Prod 10:27–30
    [Google Scholar]
  24. Kennedy S., Moffett D., McNeilly F., Meehan B., Ellis J., Krakowka S., Allan G. M. 2000; Reproduction of lesions of postweaning multisystemic wasting syndrome by infection of conventional pigs with porcine circovirus type 2 alone or in combination with porcine parvovirus. J Comp Pathol 122:9–24 [CrossRef]
    [Google Scholar]
  25. Kim J., Ha Y., Jung K., Choi C., Chae C. 2004; Enteritis associated with porcine circovirus 2 in pigs. Can J Vet Res 68:218–221
    [Google Scholar]
  26. Krakowka S., Ellis J. A., Meehan B., Kennedy S., McNeilly F., Allan G. 2000; Viral wasting syndrome of swine: experimental reproduction of postweaning multisystemic wasting syndrome in gnotobiotic swine by coinfection with porcine circovirus 2 and porcine parvovirus. Vet Pathol 37:254–263 [CrossRef]
    [Google Scholar]
  27. Larochelle R., Magar R., D'Allaire S. 2002; Genetic characterization and phylogenetic analysis of porcine circovirus type 2 (PCV2) strains from cases presenting various clinical conditions. Virus Res 90:101–112 [CrossRef]
    [Google Scholar]
  28. Larochelle R., Magar R., D'Allaire S. 2003; Comparative serology and virologic study of commercial swine herds with and without postweaning multisystemic wasting syndrome. Can J Vet Res 67:114–120
    [Google Scholar]
  29. Liu J., Chen I., Kwang J. 2005; Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J Virol 79:8262–8274 [CrossRef]
    [Google Scholar]
  30. Magar R., Müller P., Larochelle R. 2000; Retrospective serological survey of antibodies to porcine circovirus type 1 and type 2. Can J Vet Res 64:184–186
    [Google Scholar]
  31. 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
    [Google Scholar]
  32. Mankertz A., Mankertz J., Wolf K., Buhk H.-J. 1998; Identification of a protein essential for replication of porcine circovirus. J Gen Virol 79:381–384
    [Google Scholar]
  33. Mankertz A., Domingo M., Folch J. M., LeCann P., Jestin A., Segalés J., Chmielewicz B., Plana-Durán J., Soike D. 2000; Characterisation of PCV-2 isolates from Spain, Germany and France. Virus Res 66:65–77 [CrossRef]
    [Google Scholar]
  34. Meehan B. M., McNeilly F., Todd D. & 7 other authors 1998; Characterization of novel circovirus DNAs associated with wasting syndromes in pigs. J Gen Virol 79:2171–2179
    [Google Scholar]
  35. Meehan B. M., McNeilly F., McNair I., Walker I., Ellis J. A., Krakowka S., Allan G. M. 2001; Isolation and characterization of porcine circovirus 2 from cases of sow abortion and porcine dermatitis and nephropathy syndrome. Arch Virol 146:835–842 [CrossRef]
    [Google Scholar]
  36. Meerts P., Misinzo G., McNeilly F., Nauwynck H. J. 2005; Replication kinetics of different porcine circovirus 2 strains in PK-15 cells, fetal cardiomyocytes and macrophages. Arch Virol 150:427–441 [CrossRef]
    [Google Scholar]
  37. Mengeling W. L., Ridpath J. F., Vorwald A. C. 1988; Size and antigenic comparisons among the structural proteins of selected autonomous parvoviruses. J Gen Virol 69:825–837 [CrossRef]
    [Google Scholar]
  38. Morozov I., Sirinarumitr T., Sorden S. D., Halbur P. G., Morgan M. G., Yoon K.-J., Paul P. S. 1998; Detection of a novel strain of porcine circovirus in pigs with postweaning multisystemic wasting syndrome. J Clin Microbiol 36:2535–2541
    [Google Scholar]
  39. Nawagitgul P., Morozov I., Bolin S. R., Harms P. A., Sorden S. D., Paul P. S. 2000; Open reading frame 2 of porcine circovirus type 2 encodes a major capsid protein. J Gen Virol 81:2281–2287
    [Google Scholar]
  40. Nawagitgul P., Harms P. A., Morozov I., Thacker B. J., Sorden S. D., Lekcharoensuk C., Paul P. S. 2002; Modified indirect porcine circovirus (PCV) type 2-based and recombinant capsid protein (ORF2)-based enzyme-linked immunosorbent assays for detection of antibodies to PCV. Clin Diagn Lab Immunol 9:33–40
    [Google Scholar]
  41. Opriessnig T., Yu S., Gallup J. M. & 9 other authors 2003; Effect of vaccination with selective bacterins on conventional pigs infected with type 2 porcine circovirus. Vet Pathol 40:521–529 [CrossRef]
    [Google Scholar]
  42. Opriessnig T., Thacker E. L., Yu S., Fenaux M., Meng X.-J., Halbur P. G. 2004a; Experimental reproduction of postweaning multisystemic wasting syndrome in pigs by dual-infection with Mycoplasma hyopneumoniae and porcine circovirus type 2. Vet Pathol 41:624–640 [CrossRef]
    [Google Scholar]
  43. Opriessnig T., Fenaux M., Yu S. & 8 other authors 2004b; Effect of porcine parvovirus vaccination on the development of PMWS in segregated early weaned pigs coinfected with type 2 porcine circovirus and porcine parvovirus. Vet Microbiol 98:209–220 [CrossRef]
    [Google Scholar]
  44. Opriessnig T., Yu S., Thacker E. L., Halbur P. G. 2004c; Derivation of porcine circovirus type 2-negative pigs from positive breeding herds. J Swine Health Prod 12:186–191
    [Google Scholar]
  45. Opriessnig T., Fenaux M., Thomas P., Hoogland M. J., Rothschild M. F., Meng X.-J., Halbur P. G. 2006a; Evidence of breed-dependent differences in susceptibility to porcine circovirus type 2 associated disease and lesions. Vet Pathol 43:281–293 [CrossRef]
    [Google Scholar]
  46. Opriessnig T., Halbur P. G., Yu S., Thacker E. L., Fenaux M., Meng X.-J. 2006b; Effects of the timing of the administration of Mycoplasma hyopneumoniae bacterin on the development of lesions associated with porcine circovirus type 2. Vet Rec 158:149–154 [CrossRef]
    [Google Scholar]
  47. Pogranichniy R. M., Yoon K. J., Harms P. A., Sorden S. D., Daniels M. 2002; Case-control study on the association of porcine circovirus type 2 and other swine viral pathogens with postweaning multisystemic wasting syndrome. J Vet Diagn Invest 14:449–456 [CrossRef]
    [Google Scholar]
  48. Rosell C., Segalés J., Ramos-Vara J. A., Folch J. M., Rodríguez-Arrioja G. M., Duran C. O., Balasch M., Plana-Durán J., Domingo M. 2000; Identification of porcine circovirus in tissues of pigs with porcine dermatitis and nephropathy syndrome. Vet Rec 146:40–43 [CrossRef]
    [Google Scholar]
  49. Rovira A., Balasch M., Segalés J., García L., Plana-Durán J., Rosell C., Ellerbrok H., Mankertz A., Domingo M. 2002; Experimental inoculation of conventional pigs with porcine reproductive and respiratory syndrome virus and porcine circovirus 2. J Virol 76:3232–3239 [CrossRef]
    [Google Scholar]
  50. Sorden S. D. 2000; Update on porcine circovirus and postweaning multisystemic wasting syndrome (PMWS). Swine Health Prod 8:133–136
    [Google Scholar]
  51. Sorden S. D., Harms P. A., Nawagitgul P., Cavanaugh D., Paul P. S. 1999; Development of a polyclonal-antibody-based immunohistochemical method for the detection of type 2 porcine circovirus in formalin-fixed, paraffin-embedded tissue. J Vet Diagn Invest 11:528–530 [CrossRef]
    [Google Scholar]
  52. Tischer I., Rasch R., Tochtermann G. 1974; Characterization of papovavirus- and picornavirus-like particles in permanent pig kidney cell lines. Zentralbl Bakteriol [orig A] 226153–167
    [Google Scholar]
  53. Tischer I., Glederblom H., Vettermann W., Koch M. A. 1982; A very small porcine virus with circular single-stranded DNA. Nature 295:64–66 [CrossRef]
    [Google Scholar]
  54. Todd D., Scott A. N., Ball N. W., Borghmans B. J., Adair B. M. 2002; Molecular basis of the attenuation exhibited by molecularly cloned highly passaged chicken anemia virus isolates. J Virol 76:8472–8474 [CrossRef]
    [Google Scholar]
  55. West K. H., Bystrom J. M., Wojnarowicz C. & 10 other authors 1999; Myocarditis and abortion associated with intrauterine infection of sows with porcine cirocovirus 2. J Vet Diagn Invest 11:530–532 [CrossRef]
    [Google Scholar]
  56. Yamaguchi S., Imada T., Kaji N., Mase M., Tsukamoto K., Tanimura N., Yuasa N. 2001; Identification of a genetic determinant of pathogenicity in chicken anaemia virus. J Gen Virol 82:1233–1238
    [Google Scholar]
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