Skip to main content

Advertisement

SpringerLink
Log in

Retrospective study of porcine circovirus 3 (PCV3) in swine tissue from Brazil (1967–2018)

  • Veterinary Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

In this study, we report the molecular diagnosis and retrospective study of porcine circovirus 3 (PCV3) in frozen and formalin-fixed paraffin-embedded swine tissues (FFPE) collected from 1967 to 2018 in southeastern Brazil (Espírito Santo and Rio de Janeiro states). Frozen tissues from 35 pigs and FFPE tissues from 143 pigs were tested by nested PCR, targeting the PCV3 partial capsid gene. Bidirectional sequencing of 16 positive samples was performed, followed by sequence analysis and haplotype networks. A total of 26/178 samples (14.6%) tested positive for PCV3: 14/35 (40%) frozen tissue and 12/143 (8.4%) FFPE tissue. PCV3 was detected in the 1960s, 1970s, 2000s, and 2010s with the characterization of types PCV3a and PCV3b. A star-like distribution was observed in the grid of haplotypes, with a low haplotype diversity and more recent dispersal of the virus. A total of 40% of asymptomatic animals considered fit for slaughter tested positive for PCV3. In conclusion, PCV3 DNA was detected over 51 years of study, prior to initial reports and, so far, the sample detected in 1967 is the oldest partial capsid sequence described. The circulation of two different genotypes was reported, suggesting more than one introduction event of this virus into Brazil. Moreover, taken together, our studies indicated an ancient origin of PCV3 and its circulation in asymptomatic animals in Brazilian herds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Palinski R, Pineyro 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(1):1879–1816

    Article  Google Scholar 

  2. Phan TG, Giannitti F, Rossow S, Marthaler D, Knutson TP, Li L, Deng X, Resende T, Vannucci F, Delwart E (2016) Detection of a novel circovirus PCV-3 in pigs with cardiac and multi-systemic inflammation. Virol J 13:184

    Article  PubMed  PubMed Central  Google Scholar 

  3. Klaumann F, Correa-Fiz F, Franzo G, Sibila M, Nunez JI, Segales J (2018) Current knowledge on porcine circovirus 3 (PCV-3): a novel virus with a yet unknown impact on the swine industry. Front Vet Sci 5:315

    Article  PubMed  PubMed Central  Google Scholar 

  4. ICTV Taxonomy history: Porcine circovirus 3. International Committee on Taxonomy of Viruses (ICTV) Publishing.https://talk.ictvonline.org//taxonomy/p/taxonomy-history?taxnode_id=201855768. Accessed 04 April 2020

  5. Zhao D, Wang X, Gao Q, Huan C, Wang W, Gao S, Liu X (2018) Retrospective survey and phylogenetic analysis of porcine circovirus type 3 in Jiangsu province, China, 2008 to 2017. Arch Virol 163:2531–2538

    Article  CAS  PubMed  Google Scholar 

  6. Tochetto C, Lima DA, Varela APM, Loiko MR, Paim WP, Scheffer CM, Roehe PM (2018) Full-genome sequence of porcine circovirus type 3 recovered from serum of sows with stillbirths in Brazil. Transbound Emerg Dis 6(5):5–9

    Article  Google Scholar 

  7. Li G, He W, Zhu H, Bi Y, Wang R, Xing G, Zhang C, Zhou J, Yuen KY, Gao GF, Su S (2018) Origin, genetic diversity, and evolutionary dynamics of novel porcine circovirus 3. AdvSci (Weinh) 5:1800275

    Google Scholar 

  8. Saraiva GL, Vidigal PMP, Assao VS, Fajardo MLM, Loreto ANS, Fietto JLR, Bressan GC, Lobato ZIP, Almeida MR, Silva-Junior A (2019) Retrospective detection and genetic characterization of porcine circovirus 3 (PCV-3) strains identified between 2006 and 2007 in Brazil. Viruses 11(3):201

    Article  CAS  PubMed Central  Google Scholar 

  9. Dal Santo AC, Cezario KC, Bennemann PE, Machado SA, Martins M (2020) Full-genome sequences of porcine circovirus 3 (PCV3) and high prevalence in mummified fetuses from commercial farms in Brazil. Microb Pathog 141:104027

    Article  CAS  PubMed  Google Scholar 

  10. Souza AE (2019) Detecção molecular de circovírus suíno (PCV-2), torque tenovirus suíno 1 e 2 (TTSUV-1 e TTSUV-2) e achados histopatológicos em vísceras de suínos sumetidos ao abate regular no estado do Espírito Santo. [Dissertação]. Pós-Graduação em Microbiologia e Parasitologia Aplicadas do Instituto Biomédico: Universidade Federal Fluminense

  11. Boom R, Sol CJA, Salimans MMM, Jansen CL, Wertheim D, Noordaa J (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ku X, Chen F, Li P, Wang Y, Yu X, Fan S, Qian P, Wu M, He Q (2017) Identification and genetic characterization of porcine circovirus type 3 in China. Transbound Emerg Dis 64(3):703–708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Res 40(15):115

    Article  Google Scholar 

  14. Cruz ACM. (2019) Quantificação do circovirus suíno tipo 2 e detecção molecular do circovirus suíno tipo 3 em soro de suínos dos estados do Rio de Janeiro e Espírito Santo, Brasil. [Tese]. Pós-Graduação em Microbiologia e Parasitologia Aplicadas do Instituto Biomédico: Universidade Federal Fluminense

  15. Hui RK, Zeng F, Chan CM, Yuen KY, Peiris JS, Leung FC (2004) Reverse transcriptase PCR diagnostic assay for the coronavirus associated with severe acute respiratory syndrome. J Clin Microbiol 42(5):1994–1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Drummond AJ, Rambaut A, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Librado PJR, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  19. Bandelt HJ, Forter P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  20. Fux R, Söckler C, Kathrin EL, Renken C, Krejci R, Sutter G, Ritzmann M, Eddicks M (2018) Full genome characterization of porcine circovirus type 3 isolates reveals the existence of two distinct groups of virus strains. Virol J 15(25):1–9

    Google Scholar 

  21. Mesquita RA, Anzai EK, Oliveira RN, Nunes FD (2001) Avaliação de três métodos de extração de DNA de material parafinado para amplificação de DNA genômico pela técnica da PCR. Pesqui Odontol Bras 15(4):314–319

    Article  CAS  PubMed  Google Scholar 

  22. Ye X, Berg N, Fossum C, Wallgren P, Blomstrom A (2018) Detection and genetic characterization of porcine circovirus 3 from pigs in Sweden. Virus Genes 54(4):466–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sun J, Wei L, Lu Z, Mi S, Bao F, Guo H, Tu C, Zhu Y, Gong W (2018) Retrospective study of porcine circovirus 3 infection in China. Transbound Emerg Dis 65:607–613

    Article  CAS  PubMed  Google Scholar 

  24. Fu X, Fang B, Ma J, Liu Y, Bu D, Zhou P, Wang H, Jia K, Zhang G (2018) Insights into the epidemic characteristics and evolutionary history of the novel porcine circovirus type 3 in southern China. Transbound Emerg Dis 3(65):296–303

    Article  Google Scholar 

  25. Yuzhakov AG, Raev SA, Alekseev KP, Grebennikova TV, Verkhovsky OA, Zaberezhny AD, Aliper TI (2018) First detection and full genome sequence of porcine circovirus type 3 in Russia. Virus Genes 54:608–611

    Article  CAS  PubMed  Google Scholar 

  26. Klaumann F, Correa-Fiz F, Sibila M (2019) Infection dynamics of porcine circovirus 3 (PCV3) in longitudinally sampled pigs from four Spanish farms. Vet Rec 184:619. https://doi.org/10.1136/vr.105219

    Article  PubMed  Google Scholar 

  27. Franzo G, Grassi L, Tucciarone CM, Drigo M, Martini M, Pasotto D, Mondin A, Menandro ML (2019) A wild circulation: high presence of porcine circovirus 3 in different mammalian wild hosts and ticks. Transbound Emerg Dis 66:1548.Disponívelem. https://doi.org/10.1111/tbed.13180

    Article  Google Scholar 

  28. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Stadejek T, Wozniak A, Mitek D, Biernacka K (2017) First detection of porcine circovirus type 3 on commercial pig farms in Poland. Transbound Emerg Dis 64(5):1350–1353

    Article  CAS  PubMed  Google Scholar 

  30. Zheng S, Wu X, Zhang L, Xin C, Liu Y, Shi J, Peng Z, Xu S, Fu F, Yu J, Sun W, Xu S, Li J, Wang J (2017) The occurrence of porcine circovirus 3 without clinical infection signs in Shandong Province. Transbound Emerg Dis 64:1337–1341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wen S, Sun W, Li Z, Zhuang X, Zhao G, Xie C, Zheng M, Jing J, Xiao P, Wang M, Han J, Ren J, Liu H, Lu H, Jin N (2018) The detection of porcine circovirus 3 in Guangxi, China. Transbound Emerg Dis 65:27–31

    Article  CAS  PubMed  Google Scholar 

  32. Arruda B, Piñeyro P, Derscheid R, Hause B, Byers E, Dion K, Long D, Sievers C, Tangen T, Williams T, Schwartz K (2019) PCV-3 associated disease in the United States swine herd. Emerg Microbes Infect 8(1):684–698. https://doi.org/10.1080/22221751.2019.1613176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by CAPES. We thank the veterinarian Márcio Figueiredo, who made the collection of slaughtered pig samples possible. We also thank the State Center for Research in Animal Health, Agricultural Research Company of the State of Rio de Janeiro-Pesagro-Rio, which allowed access to its collection enabling the execution of this work.

Author information

Authors and Affiliations

  1. Department of Microbiology and Parasitology, Biomedical Institute, Fluminense Federal University, Rua Prof. Hernani Melo, Niterói, Rio de Janeiro, 24210-130, Brazil

    I. L. F. Rodrigues, A. C. M. Cruz, A. E. Souza, R. L. Silveira & T. X. Castro

  2. Escola de Ciências da Saúde, Medicina Veterinária, Unigranrio, Duque de Caxias, RJ, Brazil

    F. B. Knackfuss

  3. Pathological Anatomy Laboratory, State Center for Research in Animal Health, Agricultiural Research Company of the State of Rio de Janeiro-Pesagro-Rio, Alameda São Boaventura, Niterói, Rio de Janeiro, Brazil

    C. H. C. Costa

  4. Department of Morphology, Fluminense Federal University, Rua Prof. Hernani Melo, Niterói, Rio de Janeiro, 24210-130, Brazil

    R. L. Silveira

Authors
  1. I. L. F. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. C. M. Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. E. Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. B. Knackfuss
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. H. C. Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. L. Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. T. X. Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. L. F. Rodrigues.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Responsible Editor: Giliane Souza Trindade.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 19 kb).

ESM 2

(PDF 208 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodrigues, I.L.F., Cruz, A.C.M., Souza, A.E. et al. Retrospective study of porcine circovirus 3 (PCV3) in swine tissue from Brazil (1967–2018). Braz J Microbiol 51, 1391–1397 (2020). https://doi.org/10.1007/s42770-020-00281-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-020-00281-6

Keywords

Search

Navigation