Genomic Characterization of a Circovirus Associated with Fatal Hemorrhagic Enteritis in Dog, Italy

Decaro, Nicola; Martella, Vito; Desario, Costantina; Lanave, Gianvito; Circella, Elena; Cavalli, Alessandra; Elia, Gabriella; Camero, Michele; Buonavoglia, Canio

doi:10.1371/journal.pone.0105909

Cited by 82 publications

(83 citation statements)

References 34 publications

(44 reference statements)

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“…Phylogenetic analysis suggests a closest evolutionary relationship between PCV3 and CanineCV. Interestingly, CanineCV was identified in the liver of a dog displaying necrotizing vasculitis and granulomatous lymphadenitis, both of which were observed in PCV3-infected sows, as well as reported in PCV2 infections (22,73,74). Similar to CanineCV, attempts to propagate PCV3 in vitro were unsuccessful.…”

Section: Discussionmentioning

confidence: 82%

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

436

653

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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: 82%

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

436

653

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“…A novel circovirus suspected to cause fatal haemorrhagic diarrhoea in dogs was recently described (Li and others 2013, Decaro and others 2014). Aside from directly damaging enterocytes, viral infections might predispose to an overgrowth of clostridial bacteria, which might contribute to the pathogenesis of the disease (Turk and others 1992).…”

Section: Discussionmentioning

confidence: 99%

“…Although several articles reported CanineCV DNA in a subset of dogs with vasculitis, haemorrhage and haemorrhagic enteritis (Li and others 2013, Decaro and others 2014), enteric shedding of CanineCV was also present in a relatively high number of healthy dogs. In a study from the USA, faecal samples from 6.9 per cent of healthy dogs were PCR-positive for CanineCV (Li and others 2013).…”

Section: Discussionmentioning

confidence: 99%

“…In 2012, a canine circovirus (canine circovirus genotype 1 (CaCV-1)) was detected in serum samples of dogs (Kapoor and others 2012). Currently, little is known about the exact pathogenic role of this novel canine agent, although some case series suggest that this virus might cause haemorrhagic diarrhoea in dogs (Li and others 2013, Decaro and others 2014). Recently, a closely related variant of CaCV-1 was detected in an outbreak of fatal enteritis in puppies in Italy (Decaro and others 2014).…”

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confidence: 99%

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Role of canine circovirus in dogs with acute haemorrhagic diarrhoea

et al. 2017

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Canine circovirus (CanineCV) has been detected in some dogs with severe haemorrhagic diarrhoea, but its pathogenic role is unclear. This study evaluated a suspected association between the presence of CanineCV and acute haemorrhagic diarrhoea syndrome (AHDS) in dogs. The prevalence of CanineCV in dogs with AHDS was compared with that in healthy dogs and those infected with canine parvovirus (CPV). Additionally, time to recovery and mortality rate were compared between CanineCV-positive and CanineCV-negative dogs. Faecal samples of dogs with AHDS (n=55), healthy dogs (n=66) and dogs infected with CPV (n=54) were examined by two real-time TaqMan PCR assays targeting the replicase and capsid genes of CanineCV. CanineCV was detected in faecal samples of two dogs with AHDS, three healthy controls and seven dogs infected with CPV. Among the three groups, there was no significant difference in prevalence of CanineCV. CPV-infected animals that were coinfected with CanineCV had a significantly higher mortality rate compared with those negative for CanineCV. CanineCV does not appear to be the primary causative agent of AHDS in dogs, but might play a role as a negative co-factor in disease outcome in dogs with CPV infection.

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“…Viruses from the genus Cyclovirus have been found in humans and chimpanzees 2. Circoviruses have a wide host range, including human,2, 3 birds,4, 5 pigs,6, 7 dogs,8 and cattle 9, 10. Before to 2015, porcine circovirus 1 (PCV1) and PCV2 were considered the only types of porcine circoviruses.…”

Section: Introductionmentioning

confidence: 99%

Origin, Genetic Diversity, and Evolutionary Dynamics of Novel Porcine Circovirus 3

Zhu

et al. 2018

Advanced Science

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Porcine circovirus 3 (PCV3) is a novel virus associated with acute PDNS (porcine dermatitis and nephropathy syndrome)‐like clinical signs identified by metagenomic sequencing from swine. Its high occurrence may pose a potential threat to the swine industry worldwide. The processes resulting in the emergence and spread of PCV3 remain poorly understood. Herein, the possible origin, genotypes, and evolutionary dynamics of PCV3 based on available genomic sequences are determined. The closest ancestor of PCV3 is found to be within the clade 1 bat CVs. Using different phylogenetic methods, two major genotypes are identified, PCV3a and PCV3b. It is found that the effective population size of PCV3 increased rapidly during late 2013 to early 2014 and this is associated with the diversification of PCV3a and PCV3b. A relatively high effective reproductive number (Re) value and higher evolutionary rate were found compared to other single‐stranded DNA viruses, and positive selection on codons 122 and 320 (24 of ORF2) is identified. It is hypothesized that this, together with the prediction of a potential change of an antigenic epitope at position 320, might have allowed PCV3 to escape from the host immune response. Overall, this study has important implications for understanding the ongoing PCV3 cases worldwide and will guide future efforts to develop effective preventive and control measures.

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Genomic Characterization of a Circovirus Associated with Fatal Hemorrhagic Enteritis in Dog, Italy

Cited by 82 publications

References 34 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

Role of canine circovirus in dogs with acute haemorrhagic diarrhoea

Origin, Genetic Diversity, and Evolutionary Dynamics of Novel Porcine Circovirus 3

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