• 1.

    Allan GM, Ellis JA. Porcine circoviruses: a review. J Vet Diagn Invest 2000;12:314.

  • 2.

    Done S, Gresham A, Potter R, et al. PMWS and PDNS—two recently recognized diseases of pigs in the UK. In Pract 2001;15:1421.

  • 3.

    Segales J, Domingo M. Postweaning multisystemic wasting syndrome (PMWS) in pigs. A review. Vet Q 2002;24:109124.

  • 4.

    Gagnon CA, Tremblay D, Tijssen P, et al. The emergence of porcine circovirus 2b genotype (PCV-2b) in swine in Canada. Can Vet J 2007;48:811819.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cheung AK, Lager KM, Kohutyuk OI, et al. Detection of two porcine circovirus type 2 genotypic groups in United States swine herds. Arch Virol 2007;152:10351044.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Chianini F, Majo N, Segales J, et al. Immunohistochemical characterisation of PCV2 associated lesions in lymphoid and non-lymphoid tissues of pigs with natural postweaning multisystemic wasting syndrome (PMWS). Vet Immunol Immunopathol 2003;94:6375.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Krakowka S, Ellis JA, McNeilly F, et al. Immunologic features of porcine circovirus type 2 infection. Viral Immunol 2002;15:567582.

  • 8.

    Ellis J, Krakowka S, Lairmore M, et al. Reproduction of lesions of post-weaning multisystemic wasting syndrome in gnotobiotic piglets. J Vet Diagn Invest 1999;11:314.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Krakowka S, Ellis JA, Meehan B, et al. 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 2000;37:274282.

    • Search Google Scholar
    • Export Citation
  • 10.

    Dorr PM, Baker RB, Almond GW, et al. Epidemiologic assessment of porcine circovirus type 2 coinfection with other pathogens in swine. J Am Vet Med Assoc 2007;230:244250.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Harms PA, Sorden S, Halbur P, et al. 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 2001;38:528539.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Larochelle R, Magar R, D'Allaire S. Comparative serologic and virologic study of commercial swine herds with and without postweaning multisystemic wasting syndrome. Can J Vet Res 2003;67:114120.

    • Search Google Scholar
    • Export Citation
  • 13.

    Pogranichniy RM, Yoon KJ, Harms PA, et al. 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 2002;14:449456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Opriessnig T, Thacker EL, Yu S, et al. Experimental reproduction of postweaning multisystemic wasting syndrome in pigs by dual infection with Mycoplasma hyopneumoniae and porcine circovirus type 2. Vet Pathol 2004;41:624640.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Krakowka S, Ellis JA, McNeilly F, et al. Activation of the immune system is the pivotal event in the production of wasting disease in pigs infected with porcine circovirus-2 (PCV-2). Vet Pathol 2001;38:3142.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Krakowka S, Ellis J, McNeilly F, et al. Mycoplasma hyopneumoniae bacterins and porcine circovirus type 2 (PCV2) infection: Induction of postweaning multisystemic wasting syndrome (PMWS) in the gnotobiotic swine model of PCV2-associated disease. Can Vet J 2007;48:716724.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kyriakis SC, Saoulidis K, Lekkas S, et al. The effects of immuno-modulation on the clinical and pathological expression of postweaning multisystemic wasting syndrome. J Comp Pathol 2002;126:3846.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Kekarainen T, Sibila M, Segales J. Prevalence of swine torque teno virus in post-weaning multisystemic wasting syndrome (PMWS)-affected and non-PMWS-affected pigs in Spain. J Gen Virol 2006;87:833837.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Biagini P. Human circoviruses. Vet Microbiol 2004;98:95101.

  • 20.

    Hino S, Miyata H. Torque teno virus (TTV): current status. Rev Med Virol 2007;17:4557.

  • 21.

    Irshad M, Joshi YK, Sharma Y, et al. Transfusion transmitted virus: a review on its molecular characteristics and role in medicine. World J Gastroenterol 2006;12:51225134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Takahashi K, Iwasa Y, Hijikata M, et al. Identification of a new human DNA virus (TT-like mini virus, TLMV) intermediately related to TT virus and chicken anemia virus. Arch Virol 2000;145:979993.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Yzebe D, Xueref S, Baratin D, et al. TT virus. A review of the literature. Panminerva Med 2002;44:167177.

  • 24.

    Nishizawa T, Okamoto H, Konishi K, et al. A novel DNA virus (TTV) associated with elevated transaminase levels in post-transfusion hepatitis of unknown etiology. Biochem Biophys Res Commun 1997;241:9297.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Inami T, Obara T, Moriyama M, et al. Full-length nucleotide sequence of a simian TT virus isolate obtained from a chimpanzee: evidence for a new TT virus-like species. Virology 2000;277:330335.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Leary TP, Erker JC, Chalmers ML, et al. Improved detection systems for TT virus reveal high prevalence in humans, non-human primates and farm animals. J Gen Virol 1999;80:21152120.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Okamoto H, Takahashi M, Nishizawa T, et al. Genomic characterization of TT viruses (TTVs) in pigs, cats and dogs and their relatedness with species-specific TTVs in primates and tupaias. J Gen Virol 2002;83:12911297.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Niel C, Diniz-Mendes L, Devalle S. Rolling-circle amplification of torque teno virus (TTV): complete genomes from human and swine sera and identification of a novel swine TTV genogroup. J Gen Virol 2005;86:13431347.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Bigarre L, Beven L, de Boisseson C, et al. Pig anelloviruses are highly prevalent in swine herds in France. J Gen Virol 2005;86:631635.

  • 30.

    Martinez L, Kekarainen T, Sibila M, et al. Torque teno virus (TTV) is highly prevalent in the European wild boar (Sus scrofa). Vet Microbiol 2006;20:223229.

    • Search Google Scholar
    • Export Citation
  • 31.

    McKeown NE, Fenaux M, Halbur PG, et al. Molecular characterization of porcine TT virus, an orphan virus, in pigs from six different countries. Vet Microbiol 2004;104:113117.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Gallian P, Biagini P, Attoui H, et al. High genetic diversity revealed by the study of TLMV infection in French hemodialysis patients. J Med Virol 2002;67:630635.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Niel C, Saback L, Lampe E. Co-infection with multiple TTV virus strains belonging to different genotypes is a common event in healthy Brazilian adults. J Clin Microbiol 2000;38:19261930.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Peng YH, Nishizawa T, Takahashi M, et al. Analysis of the entire genomes of thirteen TT virus variants classifiable into the fourth and fifth genetic groups, isolated from viremic infants. Arch Virol 2002;147:2141.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Simmonds P, Prescott LE, Logur C, et al. TT virus–part of the normal human flora? J Infect Dis 1999;180:17481750.

  • 36.

    Zein NN. TT virus infection: an emerging pathogen in search of its identity. J Pediatr 2000;136:573575.

  • 37.

    Krakowka S, Ellis JA. Evaluation of the effects of porcine geno-group 1 torque teno virus in gnotobiotic swine. Am J Vet Res 2008;69:xxxxxx.

    • Search Google Scholar
    • Export Citation
  • 38.

    Krakowka S, Eaton KA. Helicobacter pylori infection in gnotobiotic piglets: a model of human gastric bacterial disease. In: Tumbleson M, Schook L, eds. Advances in swine in biomedical research II. New York: Plenum Press, 1996;779810.

    • Search Google Scholar
    • Export Citation
  • 39.

    Feinstone SM, Mihalik KB, Kamimura T, et al. Inactivation of hepatitis B virus and non-A, non-B hepatitis by chloroform. Infect Immun 1983;41:816821.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    McIntosh KA, Harding JCS, Ellis JA, et al. Detection of porcine circovirus type 2 viremia and seroconversion in naturally infected pigs in a farrow-to-finish barn. Can J Vet Res 2006;70:5861.

    • Search Google Scholar
    • Export Citation
  • 41.

    Brunborg IM, Moldal T, Jonassen CM. Quantitation of porcine circovirus type 2 isolated from serum/plasma and tissue samples of healthy pigs and pigs with postweaning multisystemic wasting syndrome using a TaqMan-based real-time PCR. J Virol Methods 2004;122:171178.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Fort M, Sibila M, Allepuz A, et al. Porcine circovirus type 2 (PCV2) vaccination of conventional pigs prevents viremia against PCV2 isolated of different genotypes and geographic origins. Vaccine 2007;26:10631071.

    • Search Google Scholar
    • Export Citation
  • 43.

    Fenaux M, Opriessnig T, Halbur PG, et al. A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 2004;78:62976303.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Allan GM, McNeilly F, Ellis JA, et al. Experimental infection of colostrum-deprived piglets with porcine circovirus type 2 (PCV-2) and porcine respiratory and reproductive syndrome virus (PRRSV) potentiates PCV-2 replication. Arch Virol 2000;145:24212429.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Wallgren P, Hasslung F, Bergström G, et al. Postweaning multisystemic wasting syndrome—PMWS. The first year with the disease in Sweden. Vet Q 2004;26:170187.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Vigre H, Baekbo P, Jorsal SE, et al. Spatial and temporal patterns of pig herds diagnosed with postweaning multisystemic wasting syndrome (PMWS) during the first two years of its occurrence in Denmark. Vet Microbiol 2005;110:1726.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Woodbine KA, Medley GF, Slevin J, et al. Spatiotemporal patterns and risks of herd breakdowns in pigs with postweaning multisystemic wasting syndrome. Vet Rec 2007;160:751762.

    • Crossref
    • Search Google Scholar
    • Export Citation

Advertisement

Effect of coinfection with genogroup 1 porcine torque teno virus on porcine circovirus type 2–associated postweaning multisystemic wasting syndrome in gnotobiotic pigs

John A. Ellis DVM, PhD1, Gordon Allan PhD2, and Steven Krakowka DVM, PhD3
View More View Less
  • 1 Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK S7N 5B4, Canada
  • | 2 Queens University Belfast and Agri-Food and Biosciences Institute, Belfast, BT4 3SD, Northern Ireland
  • | 3 Department of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210

Abstract

Objective—To determine whether genogroup 1 porcine torque teno virus (g1-TTV) can potentiate clinical disease associated with porcine circovirus type 2 (PCV2).

Sample population—33 gnotobiotic baby pigs.

Procedures—Pigs were allocated into 7 groups: group A, 5 uninoculated control pigs from 3 litters; group B, 4 pigs oronasally inoculated with PCV2 alone; group C, 4 pigs inoculated IP with first-passage g1-TTV alone; group D, 4 pigs inoculated IP with fourth-passage g1-TTV alone; group E, 6 pigs inoculated IP with first-passage g1-TTV and then oronasally inoculated with PCV2 7 days later; group F, 6 pigs inoculated IP with fourth-passage g1-TTV and then inoculated oronasally with PCV2 7 days later; and group G, 4 pigs inoculated oro-nasally with PCV2 and then inoculated IP with fourth-passage g1-TTV 7 days later.

Results—6 of 12 pigs inoculated with g1-TTV prior to PCV2 developed acute onset of postweaning multisystemic wasting syndrome (PMWS). None of the pigs inoculated with g1-TTV alone or PCV2 alone or that were challenge exposed to g1-TTV after establishment of infection with PCV2 developed clinical illness. Uninoculated control pigs remained healthy.

Conclusions and Clinical Relevance—These data implicated g1-TTV as another viral infection that facilitates PCV2-induced PMWS. This raises the possibility that torque teno viruses in swine may contribute to disease expression currently associated with only a single infectious agent.

Abstract

Objective—To determine whether genogroup 1 porcine torque teno virus (g1-TTV) can potentiate clinical disease associated with porcine circovirus type 2 (PCV2).

Sample population—33 gnotobiotic baby pigs.

Procedures—Pigs were allocated into 7 groups: group A, 5 uninoculated control pigs from 3 litters; group B, 4 pigs oronasally inoculated with PCV2 alone; group C, 4 pigs inoculated IP with first-passage g1-TTV alone; group D, 4 pigs inoculated IP with fourth-passage g1-TTV alone; group E, 6 pigs inoculated IP with first-passage g1-TTV and then oronasally inoculated with PCV2 7 days later; group F, 6 pigs inoculated IP with fourth-passage g1-TTV and then inoculated oronasally with PCV2 7 days later; and group G, 4 pigs inoculated oro-nasally with PCV2 and then inoculated IP with fourth-passage g1-TTV 7 days later.

Results—6 of 12 pigs inoculated with g1-TTV prior to PCV2 developed acute onset of postweaning multisystemic wasting syndrome (PMWS). None of the pigs inoculated with g1-TTV alone or PCV2 alone or that were challenge exposed to g1-TTV after establishment of infection with PCV2 developed clinical illness. Uninoculated control pigs remained healthy.

Conclusions and Clinical Relevance—These data implicated g1-TTV as another viral infection that facilitates PCV2-induced PMWS. This raises the possibility that torque teno viruses in swine may contribute to disease expression currently associated with only a single infectious agent.

Contributor Notes

Supported by a grant from Cerebus Biologicals and a grant from the National Institutes of Health, Public Health Service (R01 A1053120).

The authors thank Susan S. Ringler, Judith Younger, and Sara Schmitz for technical assistance.

Address correspondence to Dr. Ellis.