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Pathogens
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Porcine Circovirus Infections
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Porcine Circovirus Infections

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Viral Pathogens".

Deadline for manuscript submissions: closed (31 August 2020) | Viewed by 22822

Special Issue Editors

Prof. Michele Drigo

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Guest Editor
Department Animal Medicine, Production and Health (MAPS), University of Padova, Padova, Italy
Interests: swine infectious diseases and epidemiology; viral pathogens; circoviruses
Special Issues, Collections and Topics in MDPI journals
Dr. Enrico Brugnera

E-Mail Website
Guest Editor
Research Scientist/Project Leader, Department for Farm Animals, Division of Swine Medicine, University of Zurich, Zurich, Switzerland
Interests: transcription; immunology; porcine circovirus; vaccine
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

We are honored and delighted to have this opportunity to guest-edit a Special Issue on Porcine Circovirus Infections and Pathogenicity.

Porcine circoviruses (PCVs) belong to the genus Circovirus, family Circoviridae, and comprise PCV1, considered non-pathogenic, PCV2, one of the most economically relevant viruses for the swine industry worldwide and PCV3, a third member of the same genus, discovered in the last few years.

Since its emergence in the late 1990s, PCV2 has been recognized to be the primary causative agent of a variety of clinical-pathological manifestations grouped in the so-called porcine circovirus diseases (PCVD). The pathogenic role of this virus is profoundly linked to its tropism for lymphoid tissue and its presence in early development of the adaptive immune response. Interestingly, a similar pathogenicity mechanism was also described for chicken anaemia virus (CAV) of the genus Gyrovirus, another single stranded DNA virus that causes chicken anaemia. PCV2 has not been shown to cause severe disease symptoms on its own in contrary to CAV. Other cofactors that mimic either immunostimulation and/or immunosuppression together with PCV2 can lead to any of the PCVDs. Additionally, PCV-2 infections alone are responsible for immunosuppression, facilitating secondary infections.

Although substantial progress has been achieved in the understanding of PCV2 pathogenesis and immune interactions, epidemiological and experimental studies have evidenced that genetic diversity is potentially affecting the virulence of PCV2. Its high mutation rate as well as the presence of several genotype group members in the same pig, even in the same cell, bring other complexities that cannot easily be studied with another animal infection model. Therefore, further efforts should be made to achieve a better understanding of the associations between genetic, multi-member PCV2 infections and disease.

The recent discovery of PCV3 has caused some concerns among both the field veterinarians and the scientific world, likely because of some similarities with PCV2. Several reports of PCV3 detection all around the world in presence of different clinical conditions have been published to date, resulting in a priori emphasis on the association between PCV3 infection and clinical-pathological conditions, even if little evidence is currently available to sustain this association.

Studies on porcine circoviruses pathogenesis, immunity and epidemiology are more than warranted to give insights into complex biological mechanisms that cannot be addressed so easily in any of the other animal infection models and, in this Special Issue, we will summarize the current knowledge on porcine circovirus infections and pathogenicity.

Prof. Michele Drigo
Dr. Enrico Brugnera
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Pathogens is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Porcine circovirus
  • Gyrovirus molecular epidemiology
  • Pathogenesis
  • Immunity

Published Papers (8 papers)

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17 pages, 1914 KiB  
Article
Porcine Circovirus Type 2 Pathogenicity Alters Host’s Central Tolerance for Propagation
by Xaver Sidler, Titus Sydler, José Maria Mateos, Stefanie Klausmann and Enrico Brugnera
Pathogens 2020, 9(10), 839; https://doi.org/10.3390/pathogens9100839 - 13 Oct 2020
Cited by 3 | Viewed by 2373
Abstract
Porcine circovirus type 2 (PCV2) infections and resulting diseases are a worldwide threat to pig production. PCV2 bears a uniqueness that allows for us to understand more about chronic infections and the immune system in general. The virus can be phylogenetically subdivided into [...] Read more.
Porcine circovirus type 2 (PCV2) infections and resulting diseases are a worldwide threat to pig production. PCV2 bears a uniqueness that allows for us to understand more about chronic infections and the immune system in general. The virus can be phylogenetically subdivided into PCV2a to PCV2h genotypes. Although vaccination against PCV2 has been seen to prevent the manifestation of PCV disease, PCV2 still lingers as subclinical infections in all developmental stages of pigs. The “slow and low” tactic gives PCV2 a particular advantage in a host’s immune surveillance. Since the inception of the PCV2 associated panzootic, research scientists have been trying to understand the pathogenicity of PCV2. Different research groups found that one genotype group member was more pathogenic than others. We found, in our weaner infection model with in vivo transfection of different recombinant PCV2 genotype group members that these viruses alter T cell maturation in the thymus, including host’s central tolerance. Here, we extend these original observations by showing that PCV2 infected cells were also found in proximity within the female and male reproductive organs of stillborn pig fetuses. These PCV2 pools were sufficient in infecting three and half-day-old embryos in sows. Furthermore, the dominant PCV2 group member was more pathogenic in our weaner infection model. PCV2 pre-immunocompetence infection makes PCV2 recognized by central immune tolerance as belonging to the host. This also explains why pathogenicity is not a genetically intrinsic characteristic of PCV2; however, the dominance of any one PCV2 genotype group member leads to a more efficient deletion of the T cells against that specific genotype group member in the thymus. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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8 pages, 886 KiB  
Article
Lack of Evidence on the Susceptibility of Ticks and Wild Rodent Species to PCV3 Infection
by Laura Grassi, Valentina Tagliapietra, Annapaola Rizzoli, Marco Martini, Michele Drigo, Giovanni Franzo and Maria Luisa Menandro
Pathogens 2020, 9(9), 682; https://doi.org/10.3390/pathogens9090682 - 21 Aug 2020
Cited by 3 | Viewed by 2484
Abstract
Porcine circovirus 3 (PCV3) is an emerging virus, first detected in 2016 and widespread in the swine industry. Although not considered a primary pathogen, PCV3 is potentially linked to several clinical conditions that threaten swine farming. Wild boars are considered the main reservoir [...] Read more.
Porcine circovirus 3 (PCV3) is an emerging virus, first detected in 2016 and widespread in the swine industry. Although not considered a primary pathogen, PCV3 is potentially linked to several clinical conditions that threaten swine farming. Wild boars are considered the main reservoir species for PCV3 infection in the wild, but recent detection in roe deer, chamois and associated ticks has complicated our understanding of its epidemiology. Much emphasis has been placed on ticks, as competent vectors, and wild rodents, which typically feed immature tick stages. The aim of this study was to clarify whether wild rodent species and associated ticks are susceptible to PCV3 infection and involved in its spread. Wild small mammals’ serum samples and hosted ticks were, therefore, collected from areas where no wild boars were present and tested by PCR, targeting the PCV3 rep gene. A total of 90 yellow-necked mice (Apodemus flavicollis), two wood mice (A. sylvaticus), 26 bank voles (Myodes glareolus) and 262 Ixodes spp. ticks were investigated. PCV3 DNA was not detected in serum or in tick samples. These findings support the hypothesis that the investigated species do not have an actual role as PCV3 reservoirs. Further studies would be necessary to state whether these species, or others that we did not test, are involved in PCV3 infection spread—in particular when susceptible species share the same habitat. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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12 pages, 2287 KiB  
Article
Genetic Diversity of Porcine Circovirus Isolated from Korean Wild Boars
by Sok Song, Gyu-Nam Park, SeEun Choe, Ra Mi Cha, Song-Yi Kim, Bang-Hun Hyun, Bong-Kyun Park and Dong-Jun An
Pathogens 2020, 9(6), 457; https://doi.org/10.3390/pathogens9060457 - 9 Jun 2020
Cited by 12 | Viewed by 2810
Abstract
In Korea, three genotypes of porcine circovirus type 2 (PCV2a, PCV2b, and PCV2d) have been identified on domestic pig farms, while two genotypes (PCV2a and PCV2b) have been identified in wild boar populations. Here, we investigated genotype diversity and genotypic shift in 91 [...] Read more.
In Korea, three genotypes of porcine circovirus type 2 (PCV2a, PCV2b, and PCV2d) have been identified on domestic pig farms, while two genotypes (PCV2a and PCV2b) have been identified in wild boar populations. Here, we investigated genotype diversity and genotypic shift in 91 PCV2 isolates from 1340 wild boars captured in South Korea between 2013 and 2017. Phylogenetic analyses based on the complete ORF2 showed that the 91 PCV2 strains were detected as four genotypes by qPCR screening assay: PCV2a (2.2%, 2/91), PCV2b (16.5%, 15/91), PCV2d (80.2%, 73/91), and PCV2h (1.1%, 1/91). Only one intergenotype recombinant event was detected between PCV2 ORF2 in wild boars (PCV2b) and domestic pigs (PCV2a). Amino acid positions 86–89 within ORF2, which distinguishes the different genotypes, were conserved in all PCV2 genotypes isolated from South Korean wild boars, including TNKI in PCV2a/PCV2h, SNPR in PCV2b, and SNPL in PCV2d. The estimated nucleotide substitution rates in the ORF2 region of viruses from South Korean wild boars and domestic pigs were 5.8145 × 10−4 and 4.5838 × 10−4 substitutions per site per year (s/s/y), respectively. The times to the most recent common ancestor (tMRCA) for South Korean domestic pig PCV2 were 1937 (PCV2a), 1972 (PCV2b), 1999 (PCV2d-1), and 2000 (PCV2d-2). By contrast, the tMRCA for South Korean wild boar PCV2b and PCV2d were 1989 and 2001, respectively. Thus, the PCV2d genotype is prevalent among South Korean wild boars and domestic pigs. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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6 pages, 228 KiB  
Communication
Lack of Porcine circovirus 4 Genome Detection in Pig Samples from Italy and Spain
by Giovanni Franzo, Albert Ruiz, Laura Grassi, Marina Sibila, Michele Drigo and Joaquim Segalés
Pathogens 2020, 9(6), 433; https://doi.org/10.3390/pathogens9060433 - 31 May 2020
Cited by 45 | Viewed by 2818
Abstract
The genus Circovirus includes several species and mostly causes asymptomatic infections. Porcine circovirus 2 (PCV-2) and, with increasing evidence, Porcine circovirus 3 (PCV-3), have been associated with different clinical conditions all over the world. In 2019, a new porcine circovirus (PCV-4) was identified [...] Read more.
The genus Circovirus includes several species and mostly causes asymptomatic infections. Porcine circovirus 2 (PCV-2) and, with increasing evidence, Porcine circovirus 3 (PCV-3), have been associated with different clinical conditions all over the world. In 2019, a new porcine circovirus (PCV-4) was identified from diseased animals in China. Because of the lessons learned from PCV-2 and PCV-3, it appears mandatory to investigate the actual distribution of this new virus and its potential association with clinical outcomes. To this purpose, an exploratory study to detect PCV-4 by molecular methods was performed in Italy and Spain by testing more than 300 samples of different types (serum and tissues), collected from both healthy and diseased pigs and wild boar as well. All samples, independently from the country, type, health status and host, tested PCV-4 negative. Therefore, no evidence of PCV-4 presence was found in Italy and Spain through this exploratory study. Considering the dense pig trade among European countries, its presence in the continent can similarly be considered unlikely. The reasons behind the restricted PCV-4 distribution compared to other porcine circoviruses will require further investigations. Careful surveillance might nevertheless be important since prompt recognition of PCV-4 would allow the implementation of effective countermeasures to prevent its spreading and potential economic losses. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
11 pages, 1093 KiB  
Article
Wide Range of the Prevalence and Viral Loads of Porcine Circovirus Type 3 (PCV3) in Different Clinical Materials from 21 Polish Pig Farms
by Aleksandra Woźniak, Dagmara Miłek and Tomasz Stadejek
Pathogens 2020, 9(5), 411; https://doi.org/10.3390/pathogens9050411 - 25 May 2020
Cited by 14 | Viewed by 2929
Abstract
Porcine circovirus type 3 (PCV3) was described in different clinical cases and healthy pigs. However, little is known about its circulation in pig farms. In order to assess PCV3 prevalence in 21 Polish farms, serum, feces, and oral fluid samples were examined by [...] Read more.
Porcine circovirus type 3 (PCV3) was described in different clinical cases and healthy pigs. However, little is known about its circulation in pig farms. In order to assess PCV3 prevalence in 21 Polish farms, serum, feces, and oral fluid samples were examined by quantitative real-time PCR. In total, 1451 pairs of serum and feces from the same animals, as well as 327 samples of oral fluids were analyzed. The results showed that PCV3 is more commonly detected in oral fluids (37.3% positives) than in serum (9.7% positives) or feces (15.0% positives) samples. The viral loads detected in these materials ranged from 102.5–107.2 genome equivalent copies/mL. Although in most farms PCV3 was detected post weaning, in nine farms, the virus was also found in groups of suckling piglets, and in six of them viremia was detected. In four farms with reproductive failure, fetal materials were also obtained. PCV3 was detected in 36.0% of fetuses or stillborn piglets (9/25) with viral loads of 103.1–1010.4 genome equivalent copies/mL. In summary, the virus circulation may show different patterns, and congenital or early infection is not uncommon. Precise quantification of PCV3 loads in clinical materials seems to be necessary for the study and diagnosis of the infection. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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12 pages, 1569 KiB  
Article
Genetic Characterization of Porcine Circovirus 3 Strains Circulating in Sardinian Pigs and Wild Boars
by Silvia Dei Giudici, Giulia Franzoni, Piero Bonelli, Pier Paolo Angioi, Susanna Zinellu, Viviana Deriu, Tania Carta, Anna Maria Sechi, Francesco Salis, Francesca Balzano and Annalisa Oggiano
Pathogens 2020, 9(5), 344; https://doi.org/10.3390/pathogens9050344 - 2 May 2020
Cited by 24 | Viewed by 2679
Abstract
Porcine circovirus 3 (PCV3) is a recently discovered member of the Circoviridae family. So far, its presence has been reported in North America, Asia, South America, and Europe. In this study, blood and tissue samples from 189 Sardinian suids (34 domestic pigs, 115 [...] Read more.
Porcine circovirus 3 (PCV3) is a recently discovered member of the Circoviridae family. So far, its presence has been reported in North America, Asia, South America, and Europe. In this study, blood and tissue samples from 189 Sardinian suids (34 domestic pigs, 115 feral free ranging pigs, and 39 wild boars) were used to genetically characterize the PCV3 strains from Sardinia. PCV3 infection in the animals was confirmed by real time PCR. The detection rate in the three groups analyzed was l7.64% in domestic pigs, 77.39% in free ranging pigs, and 61.54% in wild boars. Moreover, our results showed that co-infection of PCV3 with other viruses is quite a common occurrence. Molecular characterization of Sardinian PCV3 strains was performed by sequencing 6 complete genomes and 12 complete cap genes. Our results revealed that there is a high similarity between our strains and those identified in different countries, confirming the genetic stability of PCV3 regardless of geographical origin. Haplotype network analysis revealed the presence of 6 whole genomes or 12 unique ORF2 haplotypes and a nonsynonymous mutation in ORF2 that leads to an R14K amino acid substitution. Phylogenetic analysis of whole genome and ORF2 was also conducted. The Sardinian strains were allocated in three different clusters of phylogenetic trees of both complete genome and ORF2. With this study, we have provided a snapshot of PCV3 circulation in Sardinia. Our findings might help to achieve a deeper understanding of this emerging porcine virus. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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14 pages, 4814 KiB  
Article
Free to Circulate: An Update on the Epidemiological Dynamics of Porcine Circovirus 2 (PCV-2) in Italy Reveals the Role of Local Spreading, Wild Populations, and Foreign Countries
by Giovanni Franzo, Susanna Tinello, Laura Grassi, Claudia Maria Tucciarone, Matteo Legnardi, Mattia Cecchinato, Giorgia Dotto, Alessandra Mondin, Marco Martini, Daniela Pasotto, Maria Luisa Menandro and Michele Drigo
Pathogens 2020, 9(3), 221; https://doi.org/10.3390/pathogens9030221 - 17 Mar 2020
Cited by 19 | Viewed by 3275
Abstract
Porcine circovirus 2 (PCV-2) is one of the most impactful and widespread pathogens of the modern swine industry. Unlike other DNA viruses, PCV-2 is featured by a remarkable genetic variability, which has led to the emergence and recognition of different genotypes, some of [...] Read more.
Porcine circovirus 2 (PCV-2) is one of the most impactful and widespread pathogens of the modern swine industry. Unlike other DNA viruses, PCV-2 is featured by a remarkable genetic variability, which has led to the emergence and recognition of different genotypes, some of which (PCV-2a, 2b, and 2d) have alternated over time. Currently, PCV-2d is considered the most prevalent genotype, and some evidence of differential virulence and vaccine efficacy have been reported. Despite the potential practical relevance, the data on PCV-2 epidemiology in Italy are quite outdated and do not quantify the actual circulation of this genotype in Italy. In the present study, 82 complete ORF2 sequences were obtained from domestic pigs and wild boars sampled in Northern Italy in the period 2013–2018 and merged with those previously obtained from Italy and other countries. A combination of phylogenetic, haplotype network, and phylodynamic analyses were used to genotype the collected strains and evaluate the temporal trend and the spatial and host spread dynamics. A rising number of PCV-2d detections was observed in domestic pigs, particularly since 2013, reaching a detection frequency comparable to PCV-2b. A similar picture was observed in wild boars, although a lower sequence number was available. Overall, the present study demonstrates the extreme complexity of PCV-2 molecular epidemiology in Italy, the significant spread across different regions, the recurrent introduction from foreign countries, and the frequent occurrence of recombination events. Although a higher viral flux occurred from domestic to wild populations than vice versa, wild boars seem to maintain PCV-2 infection and spread it over relatively long distances. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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6 pages, 699 KiB  
Short Communication
Detection of Porcine Circovirus 3 in Wildlife Species in Spain
by Ewelina Czyżewska-Dors, José I. Núñez, Viviane Saporiti, Eva Huerta, Carme Riutord, Oscar Cabezón, Joaquim Segalés and Marina Sibila
Pathogens 2020, 9(5), 341; https://doi.org/10.3390/pathogens9050341 - 1 May 2020
Cited by 14 | Viewed by 2517
Abstract
Porcine circovirus 3 (PCV-3) is the third member of the family Circoviridae, genus Circovirus, able to infect swine. A high prevalence of viral DNA has been recorded in wild boars. Recently, PCV-3 DNA was identified in Italian wild ruminants. Based on [...] Read more.
Porcine circovirus 3 (PCV-3) is the third member of the family Circoviridae, genus Circovirus, able to infect swine. A high prevalence of viral DNA has been recorded in wild boars. Recently, PCV-3 DNA was identified in Italian wild ruminants. Based on these previous results, this study assessed the frequency of PCV-3 DNA detection in free-ranging ruminants and Lagomorpha species in Spain. In addition, the genetic characterization of the PCV-3 PCR-positive samples was performed. A total of 801 serum samples, including red deer (Cervus elaphus, [CE]; n = 108), roe deer (Capreolus capreolus, [CC]; n = 87), Pyrenean chamois (Rupicapra pyrenaica, [RP]; n = 133), Iberian ibex (Capra pyrenaica, [CP]; n = 92), mouflon (Ovis aries, [OA]; n = 91), fallow deer (Dama dama, [DD]; n = 104), European rabbit (Oryctolagus cuniculus, [OC]; n = 101), and European hare (Lepus europaeus, [LE]; n = 85) from Catalonia (northeast Spain) were tested by conventional polymerase chain reaction (PCR) and, when positive, sequenced. Overall, PCV-3 DNA was found in three out of 801 analyzed sera (0.37%) corresponding to one red deer (1/108, 0.9%), one mouflon (1/91, 1.1%), and one fallow deer (1/104, 0.96%). None of the samples collected from Lagomorpha species resulted PCR positive. The partial genome sequences detected in positive samples displayed high identity with some PCV-3 sequences detected in wild boars and domestic pigs (99.7% and 100%, respectively). In conclusion, the present study indicated that free-ranging ruminant and Lagomorpha species are not relevant in the epidemiology of PCV-3 in Spain. Full article
(This article belongs to the Special Issue Porcine Circovirus Infections)
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