Evaluation of induction of porcine dermatitis and nephropathy syndrome in gnotobiotic pigs with negative results for porcine circovirus type 2

Krakowka, Steven; Hartunian, Catherine; Hamberg, Alexander; Shoup, David I.; Rings, Michael; Zhang, Yan; Allan, Gordon; Ellis, John

doi:10.2460/ajvr.69.12.1615

Cited by 93 publications

(57 citation statements)

References 33 publications

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“…Attempts to reproduce PDNS experimentally with PCV2 have been unsuccessful; however, PDNS has been reproduced experimentally in the absence of PCV2 with PRRSV and a tissue homogenate containing TTV (28). Relatively little is known about the clinical significance of TTV infection.…”

Section: Discussionmentioning

confidence: 99%

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A Novel Porcine Circovirus Distantly Related to Known Circoviruses Is Associated with Porcine Dermatitis and Nephropathy Syndrome and Reproductive Failure

Palinski

Piñeyro

Shang

et al. 2017

J Virol

465

744

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Porcine circovirus-associated disease (PCVAD) is clinically manifested by postweaning multisystemic wasting syndrome (PMWS), respiratory and enteric disease, reproductive failure, and porcine dermatitis and nephropathy syndrome (PDNS). Porcine circovirus 2 (PCV2) is an essential component of PCVAD, although an etiologic role in PDNS is not well established. Here, a novel circovirus, designated porcine circovirus 3 (PCV3), was identified in sows that died acutely with PDNS-like clinical signs. The capsid and replicase proteins of PCV3 are only 37% and 55% identical to PCV2 and bat circoviruses, respectively. Aborted fetuses from sows with PDNS contained high levels of PCV3 (7.57 ϫ 10 7 genome copies/ml), and no other viruses were detected by PCR and metagenomic sequencing. Immunohistochemistry (IHC) analysis of sow tissue samples identified PCV3 antigen in skin, kidney, lung, and lymph node samples localized in typical PDNS lesions, including necrotizing vasculitis, glomerulonephritis, granulomatous lymphadenitis, and bronchointerstitial pneumonia. Further study of archived PDNS tissue samples that were negative for PCV2 by IHC analysis identified 45 of 48 that were PCV3 positive by quantitative PCR (qPCR), with 60% of a subset also testing positive for PCV3 by IHC analysis. Analysis by qPCR of 271 porcine respiratory disease diagnostic submission samples identified 34 PCV3-positive cases (12.5%), and enzyme-linked immunosorbent assay detection of anti-PCV3 capsid antibodies in serum samples found that 46 (55%) of 83 samples tested were positive. These results suggest that PCV3 commonly circulates within U.S. swine and may play an etiologic role in reproductive failure and PDNS. Because of the high economic impact of PCV2, this novel circovirus warrants further studies to elucidate its significance and role in PCVAD.IMPORTANCE While porcine circovirus 2 (PCV2) was first identified in sporadic cases of postweaning multisystemic wasting syndrome in Canada in the early 1990s, an epidemic of severe systemic disease due to PCV2 spread worldwide in the ensuing decade. Despite being effectively controlled by commercial vaccines, PCV2 remains one of the most economically significant viruses of swine. Here, a novel porcine circovirus (PCV3) that is distantly related to known circoviruses was identified in sows with porcine dermatitis and nephropathy syndrome (PDNS) and reproductive failure. PCV2, which has previously been associated with these clinical presentations, was not identified. High levels of PCV3 nucleic acid were observed in aborted fetuses by quantitative PCR, and PCV3 antigen was localized in histologic lesions typical of PDNS in sows by immunohistochemistry (IHC) analysis. PCV3 was also identi- Citation Palinski R, Piñeyro P, Shang P, Yuan F, Guo R, Fang Y, Byers E, Hause BM. 2017. A novel porcine circovirus distantly related to known circoviruses is associated with porcine dermatitis and nephropathy syndrome and reproductive failure. J Virol 91:e01879-16.

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Section: Discussionmentioning

confidence: 99%

“…The pathogenesis of this systemic vasculitis, as well as the fibrinous glomerulonephritis, is thought to be immune complex mediated. Importantly, PDNS has been reproduced experimentally without PCV2 by using PRRSV and a tissue homogenate containing torque teno virus (TTV) (28).…”

mentioning

confidence: 99%

A Novel Porcine Circovirus Distantly Related to Known Circoviruses Is Associated with Porcine Dermatitis and Nephropathy Syndrome and Reproductive Failure

Palinski

Piñeyro

Shang

et al. 2017

J Virol

465

744

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“…First evidence highlighted the high prevalence of TTSuV2 infection in postweaning multisystemic syndrome (PMWS), although in most cases, such co-infection does not lead to a disease; however, it is subclinical, suggesting that the disease association is possibly a matter of viral load [66]. Recent reports showed that porcine TTV partially contributed to inducing porcine reproductive and respiratory syndrome, porcine dermatitis and nephropathy syndrome, and hepatitis [82,83]. The latest research indicating that TTSuV2 but not TTSuV1 seems to benefit from the host's disease status suggests that TTSuVs may act as triggers for diseases that cause immune system impairment.…”

Section: Innocent Bystanders or Something Else?mentioning

confidence: 99%

Global impact of Torque teno virus infection in wild and domesticated animals

Mallus

Macera

Maggi

et al. 2015

J Infect Dev Ctries

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Infection with Torque teno viruses (TTVs) is not restricted to humans. Different domestic and wild animal species are naturally infected with species-specific TTVs worldwide. Due to the global spread of the infection, it is likely that essentially all animals are naturally infected with species-specific TTVs, and that co-evolution of TTVs with their hosts probably occurred. Although TTVs are potentially related to many diseases, the evidence of the widespread infection in healthy human and nonhuman hosts raised doubts about their pathogenic potential. Nonetheless, their role as superimposed agents of other diseases or as triggers for impairment of immune surveillance is currently under debate. The possible contribution of animal TT viruses to interspecies transmission and their role as zoonotic agents are currently topics of discussion.

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“…4 Both TTV-1 and -2 have been implicated by some authors as another virus that facilitates PCV-2-induced systemic disease. 9,20 Lesions of porcine dermatitis and nephropathy syndrome were detected in pigs with combined experimental infection with TTV and PRRSV, 24 and there may be a relationship between TTV-2 infection and reproductive failure in sows. 47 Other studies demonstrated that pigs with PCVAD were similarly more likely infected with TTV-2 than nonaffected pigs.…”

Section: Discussionmentioning

confidence: 99%

Experimental co-infection of pigs withBovine viral diarrhea virus 1andPorcine circovirus-2

et al. 2011

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The role of Bovine viral diarrhea virus (BVDV) in the development of Porcine circovirus-2 (PCV-2)-associated disease (PCVAD) was investigated in 2 experimental studies. In the first, separate groups of germ-free pigs were inoculated with filtered tissue homogenate (from diseased pigs) containing PCV-2b + BVDV-1–like virus (group 1), PCV-2a + BVDV-1–like virus (group 4), BVDV-1–like virus only (group 3), or PCV-2b + BVDV-1–like virus following a BVDV vaccination protocol (group 2). This last group was used to test if BVDV vaccination would prevent clinical PCVAD in this model. Many of the inoculated pigs had mild multisystemic inflammation consistent with classic PCVAD. One vaccinated, dually inoculated pig had acute respiratory distress followed by death at 21 days postinfection. Lesions in this pig resembled the severe form of PCVAD observed in the field since the fall of 2004, suggesting a role of ruminant pestiviruses and/or vaccination in the development of this disease. In the second study, cesarean-derived, colostrum-deprived pigs were inoculated with PCV-2b and a cytopathic strain of BVDV-1 (cpBVDV-NADL) either alone or in combination. Clinical signs of PCVAD were seen in a single animal inoculated only with PCV-2b. This pig had growth retardation followed by acute respiratory distress leading to death 30 days postinfection. Pulmonary lesions in this animal were similar to those seen in the pig that died in the first study. Infection with cpBVDV-NADL did not enhance PCV-2b replication or lesion formation.

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Evaluation of induction of porcine dermatitis and nephropathy syndrome in gnotobiotic pigs with negative results for porcine circovirus type 2

Abstract: These data suggested that PDNS is a manifestation of disseminated intravascular coagulation in swine. For the experimental conditions reported here, combined infection with g1-TTV and PRRSV was implicated in the genesis of these lesions.

Cited by 93 publications

References 33 publications

A Novel Porcine Circovirus Distantly Related to Known Circoviruses Is Associated with Porcine Dermatitis and Nephropathy Syndrome and Reproductive Failure

A Novel Porcine Circovirus Distantly Related to Known Circoviruses Is Associated with Porcine Dermatitis and Nephropathy Syndrome and Reproductive Failure

Global impact of Torque teno virus infection in wild and domesticated animals

Experimental co-infection of pigs withBovine viral diarrhea virus 1andPorcine circovirus-2

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