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
Abstract
:1. Introduction
2. Results
- -
- strain 9607 originated from a recombination event between PCV-2d (region 0–350) and PCV-2a (region 351–699);
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- strain 16860 between PCV-2b (region 0–105 and 270–699) and PCV-2d (region 106–269);
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- strains 9473 and 13719 between PCV-2d (region 0–312) and PCV-2b (region 313–699).
3. Discussion
4. Material and Methods
4.1. Italian Samples
4.2. Sequence Analysis
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Segalés, J.; Kekarainen, T.; Cortey, M. The natural history of porcine circovirus type 2: From an inoffensive virus to a devastating swine disease? Vet. Microbiol. 2013, 165, 13–20. [Google Scholar] [CrossRef]
- Allan, G.M.; McNeilly, F.; Kennedy, S.; Daft, B.; Clarke, E.G.; Ellis, J.A.; Haines, D.M.; Meehan, B.M.; Adair, B.M. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and Europe. J. Vet. Diagnostic Investig. 1998, 10, 3–10. [Google Scholar] [CrossRef][Green Version]
- Harding, J.C.S.; Clark, E.T.G.; Strokappe, J.H.; Willson, P.I.; Ellis, J. A Postweaning multisystemic wasting syndrome: Epidemiology and clinical presentation. Swine Heal. Prod. 1998, 6, 249–254. [Google Scholar]
- Grau-Roma, L.; Fraile, L.; Segalés, J. Recent advances in the epidemiology, diagnosis and control of diseases caused by porcine circovirus type 2. Vet. J. 2011, 187, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Franzo, G.; Segalés, J. Porcine circovirus 2 (PCV-2) genotype update and proposal of a new genotyping methodology. PLoS ONE 2018, 13, e0208585. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Segalés, J. Porcine circovirus type 2 (PCV2) infections: Clinical signs, pathology and laboratory diagnosis. Virus Res. 2012, 164, 10–19. [Google Scholar] [CrossRef] [PubMed]
- Young, M.G.; Cunningham, G.L.; Sanford, S.E. Circovirus vaccination in pigs with subclinical porcine circovirus type 2 infection complicated by ileitis. J. Swine Heal. Prod. 2011, 19, 175–180. [Google Scholar]
- Jacobsen, B.; Krueger, L.; Seeliger, F.; Bruegmann, M.; Segalés, J.; Baumgaertner, W. Retrospective study on the occurrence of porcine circovirus 2 infection and associated entities in Northern Germany. Vet. Microbiol. 2009, 138, 27–33. [Google Scholar] [CrossRef][Green Version]
- Franzo, G.; Cortey, M.; Segalés, J.; Hughes, J.; Drigo, M. Phylodynamic analysis of porcine circovirus type 2 reveals global waves of emerging genotypes and the circulation of recombinant forms. Mol. Phylogenet. Evol. 2016, 100, 269–280. [Google Scholar] [CrossRef][Green Version]
- Zhai, S.-L.; Lu, S.-S.; Wei, W.-K.; Lv, D.-H.; Wen, X.-H.; Zhai, Q.; Chen, Q.-L.; Sun, Y.-W.; Xi, Y. Reservoirs of Porcine Circoviruses: A Mini Review. Front. Vet. Sci. 2019, 6, 319. [Google Scholar] [CrossRef][Green Version]
- Barbosa, C.N.; Martins, N.R.S.; Freitas, T.R.P.; Lobato, Z.I.P. Serological Survey of Porcine circovirus-2 in Captive Wild Boars (Sus scrofa) from Registered Farms of South and South-east Regions of Brazil. Transbound. Emerg. Dis. 2016, 63, e278–e280. [Google Scholar] [CrossRef] [PubMed]
- Hälli, O.; Ala-Kurikka, E.; Nokireki, T.; Skrzypczak, T.; Raunio-Saarnisto, M.; Peltoniemi, O.A.T.; Heinonen, M. Prevalence of and risk factors associated with viral and bacterial pathogens in farmed European wild boar. Vet. J. 2012, 194, 98–101. [Google Scholar] [CrossRef] [PubMed]
- Petrini, S.; Barocci, S.; Gavaudan, S.; Villa, R.; Briscolini, S.; Sabbatini, M.; Mattozzi, C.; Barchiesi, F.; Salamida, S.; Ferrari, M.; et al. Detection of porcine circovirus type 2 (PCV2) from wild boars in central Italy. Eur. J. Wildl. Res. 2009, 55, 465–469. [Google Scholar] [CrossRef]
- Turcitu, M.A.; Wellenberg, G.J.; Barboi, G.; Codreanu, M.D.; Vuta, V.B.; Nicolae, S.; Barbuceanu, F.; Coste, H.; Cioranu, R. Genetic diversity of porcine circovirus type 2 (PCV2) in the Romanian wild boar population. Res. Vet. Sci. 2011, 91, e103–e106. [Google Scholar] [CrossRef] [PubMed]
- Lv, Q.; Guo, K.; Zhang, Y. Current understanding of genomic DNA of porcine circovirus type 2. Virus Genes 2014, 49, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Choi, C.-Y.; Choi, Y.-C.; Park, I.-B.; Lee, C.-H.; Kang, S.-J.; Chun, T. The ORF5 protein of porcine circovirus type 2 enhances viral replication by dampening type I interferon expression in porcine epithelial cells. Vet. Microbiol. 2018, 226, 50–58. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Cao, J.; Zhou, N.; Jin, Y.; Wu, J.; Zhou, J. Identification and Functional Analysis of the Novel ORF4 Protein Encoded by Porcine Circovirus Type 2. J. Virol. 2013, 87, 1420–1429. [Google Scholar] [CrossRef][Green Version]
- Li, D.; Wang, J.; Xu, S.; Cai, S.; Ao, C.; Fang, L.; Xiao, S.; Chen, H.; Jiang, Y. Identification and functional analysis of the novel ORF6 protein of porcine circovirus type 2 in vitro. Vet. Res. Commun. 2018, 42, 1–10. [Google Scholar] [CrossRef]
- Liu, J.; Zhu, Y.; Chen, I.; Lau, J.; He, F.; Lau, A.; Wang, Z.; Karuppannan, A.K.; Kwang, J. The ORF3 Protein of Porcine Circovirus Type 2 Interacts with Porcine Ubiquitin E3 Ligase Pirh2 and Facilitates p53 Expression in Viral Infection. J. Virol. 2007, 81, 9560–9567. [Google Scholar] [CrossRef][Green Version]
- Xiao, C.T.; Harmon, K.M.; Halbur, P.G.; Opriessnig, T. PCV2d-2 is the predominant type of PCV2 DNA in pig samples collected in the U.S. during 2014–2016. Vet. Microbiol. 2016, 197, 72–77. [Google Scholar] [CrossRef][Green Version]
- Cortey, M.; Pileri, E.; Sibila, M.; Pujols, J.; Balasch, M.; Plana, J.; Segalés, J. Genotypic shift of porcine circovirus type 2 from PCV-2a to PCV-2b in Spain from 1985 to 2008. Vet. J. 2011, 187, 363–368. [Google Scholar] [CrossRef] [PubMed]
- Dupont, K.; Nielsen, E.O.; Bækbo, P.; Larsen, L.E. Genomic analysis of PCV2 isolates from Danish archives and a current PMWS case-control study supports a shift in genotypes with time. Vet. Microbiol. 2008, 128, 56–64. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Wang, F.; Guo, X.; Ge, X.; Wang, Z.; Chen, Y.; Cha, Z.; Yang, H. Genetic variation analysis of Chinese strains of porcine circovirus type 2. Virus Res. 2009, 145, 151–156. [Google Scholar] [CrossRef] [PubMed]
- Franzo, G.; Cortey, M.; Segalés, J.; Hughes, J.; Drigo, M. Phylodynamic analysis of porcine circovirus type 2: Methodological approach and datasets. DATA Br. 2016, 8, 549–552. [Google Scholar] [CrossRef]
- Franzo, G.; Tucciarone, C.M.; Dotto, G.; Gigli, A.; Ceglie, L.; Drigo, M. International trades, local spread and viral evolution: The case of porcine circovirus type 2 (PCV2) strains heterogeneity in Italy. Infect. Genet. Evol. 2015, 32, 409–415. [Google Scholar] [CrossRef]
- Dei Giudici, S.; Lo Presti, A.; Bonelli, P.; Angioi, P.P.; Sanna, G.; Zinellu, S.; Balzano, F.; Salis, F.; Ciccozzi, M.; Oggiano, A. Phylogenetic analysis of porcine circovirus type 2 in Sardinia, Italy, shows genotype 2d circulation among domestic pigs and wild boars. Infect. Genet. Evol. 2019, 71, 189–196. [Google Scholar] [CrossRef]
- Mur, L.; Atzeni, M.; Martínez-López, B.; Feliziani, F.; Rolesu, S.; Sanchez-Vizcaino, J.M. Thirty-Five-Year Presence of African Swine Fever in Sardinia: History, Evolution and Risk Factors for Disease Maintenance. Transbound. Emerg. Dis. 2016, 63, e165–e177. [Google Scholar] [CrossRef]
- Kwon, T.; Lee, D.U.; Yoo, S.J.; Je, S.H.; Shin, J.Y.; Lyoo, Y.S. Genotypic diversity of porcine circovirus type 2 (PCV2) and genotype shift to PCV2d in Korean pig population. Virus Res. 2017, 228, 24–29. [Google Scholar] [CrossRef]
- Guo, L.; Fu, Y.; Wang, Y.; Lu, Y.; Wei, Y.; Tang, Q.; Fan, P.; Liu, J.; Zhang, L.; Zhang, F.; et al. A porcine circovirus type 2 (PCV2) mutant with 234 amino acids in Capsid protein showed more virulence in vivo, compared with classical PCV2a/b strain. PLoS ONE 2012, 7, e41463. [Google Scholar] [CrossRef][Green Version]
- Opriessnig, T.; Gerber, P.F.; Xiao, C.T.; Halbur, P.G.; Matzinger, S.R.; Meng, X.J. Commercial PCV2a-based vaccines are effective in protecting naturally PCV2b-infected finisher pigs against experimental challenge with a 2012 mutant PCV2. Vaccine 2014, 32, 4342–4348. [Google Scholar] [CrossRef]
- Park, K.H.; Oh, T.; Yang, S.; Cho, H.; Kang, I.; Chae, C. Evaluation of a porcine circovirus type 2a (PCV2a) vaccine efficacy against experimental PCV2a, PCV2b, and PCV2d challenge. Vet. Microbiol. 2019, 231, 87–92. [Google Scholar] [CrossRef] [PubMed]
- Saha, D.; Huang, L.; Bussalleu, E.; Lefebvre, D.J.; Fort, M.; Van Doorsselaere, J.; Nauwynck, H.J. Antigenic subtyping and epitopes’ competition analysis of porcine circovirus type 2 using monoclonal antibodies. Vet. Microbiol. 2012, 157, 13–22. [Google Scholar] [CrossRef] [PubMed]
- Zhan, Y.; Wang, N.; Zhu, Z.; Wang, Z.; Wang, A.; Deng, Z.; Yang, Y. In silico analyses of antigenicity and surface structure variation of an emerging porcine circovirus genotype 2b mutant, prevalent in Southern China from 2013 to 2015. J. Gen. Virol. 2016, 97, 922–933. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Franzo, G.; Tucciarone, C.M.; Cecchinato, M.; Drigo, M. Porcine circovirus type 2 (PCV2) evolution before and after the vaccination introduction: A large scale epidemiological study. Sci. Rep. 2016, 6, 1–10. [Google Scholar] [CrossRef]
- Jeong, J.; Park, C.; Choi, K.; Chae, C. Comparison of three commercial one-dose porcine circovirus type 2 (PCV2) vaccines in a herd with concurrent circulation of PCV2b and mutant PCV2b. Vet. Microbiol. 2015, 177, 43–52. [Google Scholar] [CrossRef]
- Karuppannan, A.K.; Opriessnig, T. Porcine circovirus type 2 (PCV2) vaccines in the context of current molecular epidemiology. Viruses 2017, 9, 99. [Google Scholar] [CrossRef][Green Version]
- Opriessnig, T.; Xiao, C.T.; Halbur, P.G.; Gerber, P.F.; Matzinger, S.R.; Meng, X.J. A commercial porcine circovirus (PCV) type 2a-based vaccine reduces PCV2d viremia and shedding and prevents PCV2d transmission to naïve pigs under experimental conditions. Vaccine 2017, 35, 248–254. [Google Scholar] [CrossRef][Green Version]
- Opriessnig, T.; O’Neill, K.; Gerber, P.F.; de Castro, A.M.M.G.; Gimenéz-Lirola, L.G.; Beach, N.M.; Zhou, L.; Meng, X.J.; Wang, C.; Halbur, P.G. A PCV2 vaccine based on genotype 2b is more effective than a 2a-based vaccine to protect against PCV2b or combined PCV2a/2b viremia in pigs with concurrent PCV2, PRRSV and PPV infection. Vaccine 2013, 31, 487–494. [Google Scholar] [CrossRef]
- Edlefsen, P.T. Leaky vaccines protect highly exposed recipients at a lower rate: Implications for vaccine efficacy estimation and sieve analysis. Comput. Math. Methods Med. 2014, 2014. [Google Scholar] [CrossRef][Green Version]
- Franzo, G.; Dotto, G.; Cecchinato, M.; Pasotto, D.; Martini, M.; Drigo, M. Phylodynamic analysis of porcine reproductive and respiratory syndrome virus (PRRSV) in Italy: Action of selective pressures and interactions between different clades. Infect. Genet. Evol. 2015, 31, 149–157. [Google Scholar] [CrossRef]
- Franzo, G.; Massi, P.; Tucciarone, C.M.; Barbieri, I.; Tosi, G.; Fiorentini, L.; Ciccozzi, M.; Lavazza, A.; Cecchinato, M.; Moreno, A. Think globally, act locally: Phylodynamic reconstruction of infectious bronchitis virus (IBV) QX genotype (GI-19 lineage) reveals different population dynamics and spreading patterns when evaluated on different epidemiological scales. PLoS ONE 2017, 12, e0184401. [Google Scholar] [CrossRef] [PubMed]
- Lefeuvre, P.; Lett, J.-M.; Varsani, A.; Martin, D.P. Widely Conserved Recombination Patterns among Single-Stranded DNA Viruses. J. Virol. 2009, 83, 2697–2707. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Correa-Fiz, F.; Franzo, G.; Llorens, A.; Segalés, J.; Kekarainen, T. Porcine circovirus 2 (PCV-2) genetic variability under natural infection scenario reveals a complex network of viral quasispecies. Sci. Rep. 2018, 8, 1–11. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Vicente, J.; Segalés, J.; Höfle, U.; Balasch, M.; Plana-Durán, J.; Domingo, M.; Gortázar, C. Epidemiological study on porcine circovirus type 2 (PCV2) infection in the European wild boar (Sus scrofa). Vet. Res. 2004, 35, 243–253. [Google Scholar] [CrossRef][Green Version]
- Franzo, G.; Tucciarone, C.M.; Drigo, M.; Cecchinato, M.; Martini, M.; Mondin, A.; Menandro, M.L. First report of wild boar susceptibility to Porcine circovirus type 3: High prevalence in the Colli Euganei Regional Park (Italy) in the absence of clinical signs. Transbound. Emerg. Dis. 2018, 65, 957–962. [Google Scholar] [CrossRef]
- Franzo, G.; Grassi, L.; Tucciarone, C.M.; Drigo, M.; Martini, M.; Pasotto, D.; Mondin, A.; Menandro, M.L. A wild circulation: High presence of Porcine circovirus 3 in different mammalian wild hosts and ticks. Transbound. Emerg. Dis. 2019, 66, 1548–1557. [Google Scholar] [CrossRef]
- Opriessnig, T.; Yu, S.; Gallup, J.M.; Evans, R.B.; Fenaux, M.; Pallares, F.; Thacker, E.L.; Brockus, C.W.; Ackermann, M.R.; Thomas, P.; et al. Effect of vaccination with selective bacterins on conventional pigs infected with type 2 porcine circovirus. Vet. Pathol. 2003, 40, 521–529. [Google Scholar] [CrossRef][Green Version]
- Standley, K. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability.(outlines version 7). Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar]
- Abascal, F.; Zardoya, R.; Telford, M.J. TranslatorX: Multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 2010, 38, W7–W13. [Google Scholar] [CrossRef][Green Version]
- Martin, D.P.; Murrell, B.; Golden, M.; Khoosal, A.; Muhire, B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015, 1, 1–5. [Google Scholar] [CrossRef][Green Version]
- Trifinopoulos, J.; Nguyen, L.-T.; von Haeseler, A.; Minh, B.Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016, 44, W232–W235. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Xia, X. DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Mol. Biol. Evol. 2013, 30, 1720–1728. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Paradis, E. Pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics 2010, 26, 419–420. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Drummond, A.J.; Suchard, M.A.; Xie, D.; Rambaut, A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29, 1969–1973. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Baele, G.; Lemey, P.; Bedford, T.; Rambaut, A.; Suchard, M.A.; Alekseyenko, A.V. Improving the Accuracy of Demographic and Molecular Clock Model Comparison While Accommodating Phylogenetic Uncertainty. Mol. Biol. Evol. 2012, 29, 2157–2167. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Bielejec, F.; Baele, G.; Vrancken, B.; Suchard, M.A.; Rambaut, A.; Lemey, P. SpreaD3: Interactive Visualization of Spatiotemporal History and Trait Evolutionary Processes. Mol. Biol. Evol. 2016, 33, 2167–2169. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Li, W.; Godzik, A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22, 1658–1659. [Google Scholar] [CrossRef][Green Version]
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Franzo, G.; Tinello, S.; Grassi, L.; Tucciarone, C.M.; Legnardi, M.; Cecchinato, M.; Dotto, G.; Mondin, A.; Martini, M.; Pasotto, D.; Menandro, M.L.; Drigo, M. 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. Pathogens 2020, 9, 221. https://doi.org/10.3390/pathogens9030221
Franzo G, Tinello S, Grassi L, Tucciarone CM, Legnardi M, Cecchinato M, Dotto G, Mondin A, Martini M, Pasotto D, Menandro ML, Drigo M. 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. Pathogens. 2020; 9(3):221. https://doi.org/10.3390/pathogens9030221
Chicago/Turabian StyleFranzo, Giovanni, 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. 2020. "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" Pathogens 9, no. 3: 221. https://doi.org/10.3390/pathogens9030221