First detection of porcine circovirus type 3 on commercial pig farms in Poland
01 Oct 2017-Transboundary and Emerging Diseases (John Wiley & Sons, Ltd)-Vol. 64, Iss: 5, pp 1350-1353
TL;DR: The results indicate that PCV3 is a common virus among Polish pigs but no links to unexplained disease conditions were established.
Abstract: Porcine circovirus type 3 (PCV3) is a novel circovirus species recently discovered in USA and China in cases of porcine dermatitis and nephropathy syndrome, reproductive failure, respiratory disease and multisystemic inflammation. This study reports on the first identification of PCV3 in Europe, in serum from pigs from Polish farms. A total of 1,050 serum samples were collected between 2014 and 2017 from sows and 3-20 weeks old pigs from 14 commercial farms representing different regions of Poland, different size and health status. The samples were pooled by 4-6 and tested with real-time PCR for PCV3. PCV3 DNA was detected in 12 of 14 farms (85.7%). On the PCV3-positive farms, the virus was detected in 5.9% to 65% serum pools. PCV3 was most common among weaned pigs and finishers (26.1% and 28.0% of serum pools, respectively). Sequence analysis of 359 nucleotide fragment of ORF2 showed highest identity of 99.7% to PCV3-US/SD2016 from USA. Our results indicate that PCV3 is a common virus among Polish pigs but no links to unexplained disease conditions were established.
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TL;DR: Two full-genome sequences of porcine circovirus type 3 (PCV3) are reported, recovered from pooled serum samples from sows who had just delivered litters with variable numbers of stillbirths.
Abstract: Two full-genome sequences of porcine circovirus type 3 (PCV3) are reported. The genomes were recovered from pooled serum samples from sows who had just delivered litters with variable numbers of stillbirths. The two circular genomes (PCV3-BR/RS/6 and PCV3-BR/RS/8) are 2,000 nucleotides long and contain two open reading frames (ORFs) oriented in opposite directions that encode the putative capsid (Cap) and replicase (Rep) proteins. The intergenic region contains a stem-loop motif, as reported for other circoviruses. Rolling circle replication motifs and putative helicase domains were identified in the Rep coding region. The degree of overall nucleotide similarity between the genomes reported here and those available at GenBank was higher than 97%. No PCV3 sequence was detected in pooled serum samples from sows which had no stillbirths on the same farms. However, further studies are necessary to confirm the association between PCV3 and the occurrence of stillbirths.
116 citations
TL;DR: For the first time successful reproduction of PDNS-like disease by PCV3 infection by intranasally inoculating 4- and 8-week-old specific-pathogen-free piglets is demonstrated and will provide significant information regarding the pathogenesis of PCV 3 in piglets.
Abstract: Porcine circovirus type 3 (PCV3) is an emerging porcine circovirus that has been associated with porcine dermatitis and nephropathy syndrome (PDNS)-like clinical signs, reproductive failure, cardiac pathologies, and multisystemic inflammation in piglets and sows. Many aspects of PCV3 infection biology and pathogenesis, however, remain unknown. Here, we used a PCV3 virus stock from the rescue of an infectious PCV3 DNA clone to intranasally inoculate 4- and 8-week-old specific-pathogen-free piglets for evaluation of PCV3 pathogenesis. For 4-week-old piglets, typical clinical signs resembling those of PDNS-like disease were observed when piglets were inoculated with PCV3 alone or PCV3 combined with immunostimulation by keyhole limpet hemocyanin, with a mortality of 40% (2/5) for both types of inoculated piglets during a 28-day observation period postinoculation. Both types of inoculated piglets showed similar progressive increases in viral loads in the sera and had seroconverted to PCV3 capsid antibody after inoculation. Pathological lesions and PCV3-specific antigen were detected in various tissues and organs, including the lung, heart, kidney, lymph nodes, spleen, liver, and small intestine, in both types of inoculated piglets. The levels of proinflammatory cytokines and chemokines, including interleukin 1 beta (IL-1β), IL-6, IL-23α, gamma interferon (IFN-γ), tumor necrosis factor alpha (TNF-α), and chemokine ligand 5 (CCL5), were significantly upregulated in both groups of inoculated piglets. Eight-week-old piglets also exhibited a similar PDNS-like disease but without death after PCV3 inoculation, as evidenced by pathological lesions and PCV3 antigen in various tissues and organs. These results show for the first time successful reproduction of PDNS-like disease by PCV3 infection and further provide significant information regarding the pathogenesis of PCV3 in piglets.IMPORTANCE Porcine circovirus type 3 (PCV3), an emerging porcine circovirus, is considered the cause of porcine dermatitis and nephropathy syndrome (PDNS)-like clinical signs and other systemic diseases in piglets and sows. To evaluate the pathogenesis of PCV3 infection in vivo, we used a PCV3 virus stock from the rescue of an infectious PCV3 DNA clone to intranasally inoculate 4- and 8-week-old specific-pathogen-free piglets and demonstrated successful reproduction of PDNS-like disease in animals that were inoculated with PCV3 alone or PCV3 combined with immunostimulation by keyhole limpet hemocyanin. Both 4- and 8-week-old PCV3-inoculated piglets showed similar increases in viral loads in the sera and had seroconverted to PCV3 capsid antibody. Pathological lesions and PCV3-specific antigen were detected in various tissues and organs, while numerous proinflammatory cytokines and chemokines in the sera were significantly upregulated after PCV3 inoculation. These results will provide significant information regarding the pathogenesis of PCV3 in piglets.
108 citations
TL;DR: The preliminary screening of the data from three European countries confirmed a rather wide PCV3 distribution in Europe, and the analysis of the six obtained complete EuropeanPCV3 genomes and their comparison with the public available sequences seems to support a remarkable worldwide PCV 3 circulation.
Abstract: Porcine circovirus 3 (PCV3) is a new species of the Circovirus genus, which has recently been associated with different clinical syndromes. Its presence has been reported in different countries of North and South America, Asia and recently also Europe (Poland). However, different from the other continents, no European PCV3 sequence is currently available in public databases. There is a strong need of epidemiological data and full-genome sequences from Europe because of its relevance in the understanding of PCV3 molecular epidemiology and control. To fill this lack of information, samples collected in Denmark, Italy and Spain in 2016 and 2017 were screened for PCV3. Of the Danish samples, 36 of 38 the lymph nodes, six of 20 serum samples and two of 20 lung samples tested positive. Similarly, 10 of 29 lungs, 20 of 29 organ pools, six of 33 sera and one of eight nasal swabs tested PCV3 positive in Italy. Fourteen of 94 serum pools from seven of 14 Spanish farms were also positive. Despite the convenience nature of the sampling prevents any precise prevalence estimation, the preliminary screening of the data from three European countries confirmed a rather wide PCV3 distribution in Europe. Furthermore, the analysis of the six obtained complete European PCV3 genomes and their comparison with the public available sequences seems to support a remarkable worldwide PCV3 circulation. These results underline once more the urgency of more extensive epidemiological studies to refine the current knowledge on PCV3 evolution, transmission, spreading patterns and impact on pig health.
102 citations
TL;DR: The results suggested that PCV3 is widely distributed in southern China and has been circulating in swine herds for nearly half a century, and has evolved into different clades caused by mutations in cap proteins; thus, further research on PCV 3 epidemiology should be conducted.
Abstract: Porcine circovirus type 3 (PCV3) is a newly identified circovirus from swine in the USA, China and Poland. This novel circovirus has been associated with porcine dermatitis and nephropathy syndrome (PDNS), reproductive failure and multisystemic inflammation; moreover, PCV3 poses a potential threat to the swine industry. In this retrospective study, a phylogenetic analysis was conducted to address the epidemiology and evolutionary dynamics of this novel circovirus. The total positive sample rate of PCV3 was 26.7% (76/285) and has increased gradually over the past 3 years. Of these PCV3-positive samples, 22.3% (17/76) were coinfected with PCV2. PCV3 can be detected in multiple sample types with different positive rates, and the positive rate is highest among stillborn. We also divide PCV3 into three clades (PCV3a, PCV3b and PCV3c) based on two amino acid mutations (A24V and R27K) on the cap protein in this study. In addition, the origin of PCV3 was approximately 1966 and may have originated from a bat-associated circovirus. Our results suggested that PCV3 is widely distributed in southern China and has been circulating in swine herds for nearly half a century. PCV3 has evolved into different clades caused by mutations in cap proteins; thus, further research on PCV3 epidemiology should be conducted.
99 citations
TL;DR: Investigation of the presence of PCV3 in pigs from a farm in Thailand suffering from porcine respiratory disease complex (PRDC) showed that the PRDC-affected pigs exhibited higher prevalence ofPCV3 infection and higher PCV 3 titers comparing with the clinically healthy pigs.
92 citations
References
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TL;DR: The diagnosis of PCV2-associated disease is based on the direct demonstration ofPCV2 antigens or nucleic acid in affected tissues, as is the role of the immune response in controlling or augmenting disease.
Abstract: Porcine circoviruses (PCV) are small nonenveloped DNA viruses containing a unique single-stranded circular genome. Previously, no recognized link was found between PCV infection of pigs and disease, and PCV was considered a nonpathogenic agent. Over the last 5 years, a "novel" PCV, designated PCV2, has been associated with various disease syndromes in pigs, primarily postweaning multisystemic wasting syndrome (PMWS). Pigs with PMWS have a variety of clinical signs, including debility, dyspnea, palpable lymphadenopathy, diarrhea, and pallor or icterus. Lesions associated with the presence of PCV2 in a variety of cell types include lymphohistiocytic to granulomatous interstitial pneumonia, hepatitis, nephritis, myocarditis, enteritis, and pancreatitis. The lesions of PMWS have been reproduced experimentally after inoculation of piglets with PCV2 cell culture isolates, although the full expression of the disease syndrome may require the presence of other agents such as porcine parvovirus or porcine reproductive and respiratory syndrome (PRRS) virus. Recent reports have linked PCV2 to other disorders in pigs, ranging from abortion and reproductive failure to "atypical" PRRS. Available data indicate high seroprevalence of antibodies to PCV2 worldwide. The diagnosis of PCV2-associated disease is based on the direct demonstration of PCV2 antigens or nucleic acid in affected tissues. PCV2 is now regarded as an important emerging pathogen. Although vertical transmission has been documented, the epidemiology of PCV2 infections is poorly understood, as is the role of the immune response in controlling or augmenting disease.
785 citations
"First detection of porcine circovir..." refers background in this paper
...In China, PCV3 was detected in piglets with respiratory disease and fever >40°C, negative for PCV2, porcine reproductive and respiratory syndrome virus (PRRSV) and pseudorabies virus (Shen et al., 2017)....
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...PCV1 is generally considered non-pathogenic while PCV2 infection can be either asymptomatic or cause a variety of clinical symptoms known as porcine circovirus disease (PCVD) with significant economic impact (Segales, 2012)....
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...To date, two porcine circovirus (PCV) species were well studied, PCV1 and PCV2 (Allan & Ellis, 2000; Ellis, 2014)....
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...All the farms, except for farm B, vaccinated piglets, or sows and piglets, against PCV2 (Table 1)....
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...On farm KS, an increase in the number of abortion cases was observed and PCV2 DNA was detected by PCR in foetal tissues....
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TL;DR: The objective of the present review is to update the current knowledge on the clinical and pathological scope of PCV2 infections, as well as on their diagnosis, and a proposal on a unified PCVD/PCVAD terminology and clearly defined diagnostic criteria for these conditions are given.
450 citations
"First detection of porcine circovir..." refers background in this paper
...PCV1 is generally considered non-pathogenic while PCV2 infection can be either asymptomatic or cause a variety of clinical symptoms known as porcine circovirus disease (PCVD) with significant economic impact (Segales, 2012)....
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TL;DR: Results suggest that PCV3 commonly circulates within U.S. swine and may play an etiologic role in reproductive failure and PDNS and further studies are needed to elucidate its significance and role in PCVAD.
Abstract: 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 (757 × 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 (125%), 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 US 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 identified in archival PDNS diagnostic samples that previously tested negative for PCV2 by IHC analysis The emergence of PCV3 warrants further investigation
410 citations
"First detection of porcine circovir..." refers background or methods in this paper
...Moreover, PCV3 DNA was detected in heart lesions by in situ hybridization, and PCV3 antigen in skin, kidney, lung and lymph node samples from sows with PDNS lesions by immunohistochemistry (Palinski et al., 2017; Phan et al., 2016)....
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...The reports from USA and China described a frequent incidence of PCV3 in samples from pigs with different disease signs, free from other known pathogens (Phan et al., 2016; Palinski et al., 2017; Shen et al., 2017; Ku et al., 2017)....
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...Selected samples with the lowest Ct value were subjected to PCR targeting an ORF2 fragment and the amplicons were submitted for nucleotide sequencing (Palinski et al., 2017)....
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...More recently, Palinski et al. (2017) identified PCV3 in sows with skin lesions consistent with porcine dermatitis and nephropathy syndrome (PDNS), as well as in mummified foetuses aborted from such sows....
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...Additionally, PCV3 was detected in samples from 45 of 48 cases with lesions consistent with PDNS from 2010 to 2016, as well as in 34 of 271 lung, oral fluid or nasal swabs samples from respiratory disease cases (Palinski et al., 2017)....
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TL;DR: The pathogenicity and molecular epidemiology of this new circovirus, alone or in the context of co-infections, warrants further investigations.
Abstract: Porcine circovirus 2 causes different clinical syndromes resulting in a significant economic loss in the pork industry. Three pigs with unexplained cardiac and multi-organ inflammation that tested negative for PCV2 and other known porcine pathogens were further analyzed. Histology was used to identify microscopic lesions in multiple tissues. Metagenomics was used to detect viral sequences in tissue homogenates. In situ hybridization was used to detect viral RNA expression in cardiac tissue. In all three cases we characterized the genome of a new circovirus we called PCV3 with a replicase and capsid proteins showing 55 and 35 % identities to the genetically-closest proteins from a bat-feces associated circovirus and were even more distant to those of porcine circovirus 1 and 2. Common microscopic lesions included non-suppurative myocarditis and/or cardiac arteriolitis. Viral mRNA was detected intralesionally in cardiac cells. Deep sequencing in tissues also revealed the presence of porcine astrovirus 4 in all three animals as well as rotavirus A, porcine cytomegalovirus and porcine hemagglutinating encephalomyelitis virus in individual cases. The pathogenicity and molecular epidemiology of this new circovirus, alone or in the context of co-infections, warrants further investigations.
298 citations
"First detection of porcine circovir..." refers background in this paper
...PCV3 was detected in different states of USA in suckling piglet and 9–10 weeks old fatteners with myocarditis or respiratory disease (Phan et al., 2016)....
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...The reports from USA and China described a frequent incidence of PCV3 in samples from pigs with different disease signs, free from other known pathogens (Phan et al., 2016; Palinski et al., 2017; Shen et al., 2017; Ku et al., 2017)....
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...Moreover, PCV3 DNA was detected in heart lesions by in situ hybridization, and PCV3 antigen in skin, kidney, lung and lymph node samples from sows with PDNS lesions by immunohistochemistry (Palinski et al., 2017; Phan et al., 2016)....
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...In 2016, a novel porcine circovirus species named PCV3 was discovered (Phan et al., 2016)....
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TL;DR: This study reports on the first identification, widely epidemic, different phylogenetic clusters, potential role in sow reproductive failure and possible origins of PCV3 in China.
Abstract: A novel circovirus called porcine circovirus type 3 (PCV3) was recently reported to exist in the USA. This circovirus is associated with porcine dermatitis, nephropathy syndrome and reproductive failure. This study reports on the first identification, widely epidemic, different phylogenetic clusters, potential role in sow reproductive failure and possible origins of PCV3 in China.
172 citations