Archives of Virology

, Volume 164, Issue 10, pp 2435–2449 | Cite as

The prevalence and genetic diversity of porcine circovirus types 2 and 3 in Northeast China from 2015 to 2018

  • Deli Xia
  • Liping Huang
  • Yongxing Xie
  • Xiaoqian Zhang
  • Yanwu Wei
  • Dan Liu
  • Hongzhen Zhu
  • Haiqiao Bian
  • Li Feng
  • Changming LiuEmail author
Original Article


A total of 472 samples from domestic pigs collected in China from 2015 to 2018 were tested for the presence of porcine circovirus types 2 and 3 (PCV2 and PCV3, respectively) by conventional polymerase chain reaction analysis. The prevalence of PCV2, PCV3, and PCV2/3 co-infection was 50.0%, 13.3%, and 6.78%, respectively. The complete genomic sequences of 66 PCV2 isolates and four PCV3 isolates were determined. Based phylogenetic analysis, the PCV2 isolates were assigned to three genotypes, PCV2a, PCV2b, and PCV2d, representing 13.6% (9/66), 25.8% (17/66), and 60.6% (40/66) of the total, respectively. All four PCV3 isolates shared a high degree of similarity in their complete nucleotide sequences (98.8–99.8% identity) and ORF2 amino acid sequences (98.6–99.5% identity). These results indicate that all three PCV2 genotypes (PCV2a, PCV2b, and PCV2d) are present on pig farms and that PCV2d has become the predominant genotype. The predicted amino acid sequences of the four PCV3 isolates indicated that PCV3-CN-JL53/PCV3-CN-LN56, PCV3-CN-HLJ3, and PCV3-CN-0710, belonged to the genotypes PCV3a, PCV3b, and PCV3a-IM, respectively. In view of the great harm that PCV2 causes to the pig industry, the epidemic trend of PCV3 should continue to be closely monitored. This study provides information about the prevalence, genetic diversity, and molecular epidemiology of PCV2 and PCV3 in China from 2015 to 2018.



This study was supported by the National Natural Science Foundation of China (Grant no. 31873012) and the National Key Research and Development Programs (Grant nos. 2017YFD0500903 and 2017YFD0501603)

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. 1.
    Bao F, Mi S, Luo Q, Guo H, Tu C, Zhu G, Wang W (2017) Retrospective study of porcine circovirus type 2 infection reveals a novel genotype PCV2f. Transbound Emerg Dis 65(2):432–440CrossRefGoogle Scholar
  2. 2.
    Chen GH, Mai KJ, Zhou L, Wu RT, Tang XY, Wu JL, He LL, Lan T, Xie QM, Sun Y, Ma JY (2017) Detection and genome sequencing of porcine circovirus 3 in neonatal pigs with congenital tremors in South China. Transbound Emerg Dis 64(6):1650–1654CrossRefGoogle Scholar
  3. 3.
    Cheung AK (2015) Specific functions of the Rep and Rep proteins of porcine circovirus during copy-release and rolling-circle DNA replication. Virology 481:43–50CrossRefGoogle Scholar
  4. 4.
    Collins PJ, McKillen J, Allan G (2017) Porcine circovirus type 3 in the UK. Vet Rec 181:599CrossRefGoogle Scholar
  5. 5.
    Davies B, Wang X, Dvorak CMT, Marthaler D, Murtaugh MP (2016) Diagnostic phylogenetics reveals a new Porcine circovirus 2 cluster. Virus Res 217:32–37CrossRefGoogle Scholar
  6. 6.
    Faccini S, Barbieri I, Gilioli A, Sala G, Gibelli LR, Moreno A, Sacchi C, Rosignoli C, Franzini G, Nigrelli A (2017) Detection and genetic characterization of Porcine circovirus type 3 in Italy. Transbound Emerg Dis 64(6):1661–1664CrossRefGoogle Scholar
  7. 7.
    Franzo G, Segalés J (2018) Porcine circovirus 2 (PCV-2) genotype update and proposal of a new genotyping methodology. PLoS One 13(12):e0208585CrossRefGoogle Scholar
  8. 8.
    Guo LJ, Lu YH, Huang LP, Wei YW, Wu HL, Liu CM (2011) First construction of infectious clone for newly emerging mutation porcine circovirus type 2 (PCV2) followed by comparison with PCV2a and PCV2b genotypes in biological characteristics in vitro. Virol J 8:291CrossRefGoogle Scholar
  9. 9.
    Guo LJ, Lu YH, Wei YW, Huang LP, Liu CM (2010) Porcine circovirus type 2 (PCV2): genetic variation and newly emerging genotypes in China. Virol J 7:273CrossRefGoogle Scholar
  10. 10.
    Hayashi S, Ohshima Y, Furuya Y, Nagao A, Oroku K, Tsutsumi N, Sasakawa C, Sato T (2018) First detection of porcine circovirus type 3 in Japan. J Vet Med Sci 80(9):1468–1472CrossRefGoogle Scholar
  11. 11.
    Harmon KM, Gauger PC, Zhang J, Piñeyro PE, Dunn DD, Chriswell AJ (2015) Whole-genome sequences of novel porcine circovirus type 2 viruses detected in swine from Mexico and the United States. Genome Announc 3(6):e01315CrossRefGoogle Scholar
  12. 12.
    Ha Z, Xie CZ, Li JF, Wen SB, Zhang KL, Nan FL, Zhang H, Guo YC, Wang W, Lu HJ, Jin NY (2018) Molecular detection and genomic characterization of porcine circovirus 3 in pigs from Northeast China. BMC Vet Res 14(1):321CrossRefGoogle Scholar
  13. 13.
    He J, Cao J, Zhou N, Jin Y, Wu J, Zhou J (2013) Identification and functional analysis of the novel ORF4 protein encoded by porcine circovirus type 2. J Virol 87(3):1420–1429CrossRefGoogle Scholar
  14. 14.
    Jiang H, Wang D, Wang J, Zhu S, She R, Ren X, Tian J, Quan R, Hou L, Li Z, Chu J, Guo Y, Xi Y, Song H, Yuan F, Wei L, Liu J (2018) Induction of porcine dermatitis and nephropathy syndrome in piglets by infection with porcine circovirus type 3. J Virol 93(4):e02045-18CrossRefGoogle Scholar
  15. 15.
    Kwon T, Yoo SJ, Park CK, Lyoo YS (2017) Prevalence of novel porcine circovirus 3 in Korean pig populations. Vet Microbiol 207:178–180CrossRefGoogle Scholar
  16. 16.
    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):703–708CrossRefGoogle Scholar
  17. 17.
    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. Adv Sci 5(9):1800275CrossRefGoogle Scholar
  18. 18.
    Liu C, Wei Y, Zhang C, Lu Y, Kong X (2007) Construction and characterization of porcine circovirus type 2 carrying a genetic marker strain. Virus Res 127(1):95–99CrossRefGoogle Scholar
  19. 19.
    Liu J, Chen I, Du Q, Chua H, Kwang J (2006) The ORF3 protein of porcine circovirus type 2 is involved in viral pathogenesis in vivo. J Virol 80:5065–5073CrossRefGoogle Scholar
  20. 20.
    Meehan BM, McNeilly F, Todd D, Kennedy S, Jewhurst VA, Ellis JA, Hassard LE, Clark EG, Haines DM, Allan GM (1998) Characterization of novel circovirus DNAs associated with wasting syndromes in pigs. J Gen Virol 79(9):2171–2179CrossRefGoogle Scholar
  21. 21.
    Nawagitgul P, Morozov I, Bolin SR, Harms FA, Sorden SD, Paul PS (2000) Open reading frame 2 of porcine circovirus type 2 encodes a major capsid protein. J Gen Virol 81(9):2281–2287CrossRefGoogle Scholar
  22. 22.
    Meehan BM, McNeilly F, Todd D, Kennedy S, Jewhurst VA, Ellis JA, Hassard LE, Clark EG, Haines DM, Allan GM (2007) Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J Vet Diagn Invest 19(6):591–615CrossRefGoogle Scholar
  23. 23.
    Opriessnig T, Xiao CT, Halbur PG, Gerber PF, Matzinger SR, Meng XJ (2017) A commercial porcine circovirus (PCV) type 2a-based vaccine reduces PCV2d viremia and shedding and prevents PCV2d transmission to naive pigs under experimental conditions. Vaccine 35(2):248–254CrossRefGoogle Scholar
  24. 24.
    Palinski R, Pineyro P, Shang P, Yuan F, GuoR Fang Y, Byers E, Hause BM (2016) A novel porcine circovirus distantly related to known circoviruses is associated with porcine dermatitis and nephropathy syndrome and reproductive failure. J Virol 91(1):01879-16Google Scholar
  25. 25.
    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 PCV3 in pigs with cardiac and multi-systemic inflammation. Virol J 13(1):184CrossRefGoogle Scholar
  26. 26.
    Pringle CR (1999) Virus taxonomy at the XIth International Congress of Virology, Sydney, Australia. Adv Virol 144:2065–2070Google Scholar
  27. 27.
    Qi S, Su M, Guo D, Li C, Wei S, Feng L, Sun D (2019) Molecular detection and phylogenetic analysis of porcine circovirus type 3 in 21 Provinces of China during 2015–2017. Transbound Emerg Dis 66(2):1004–1015CrossRefGoogle Scholar
  28. 28.
    Qu T, Li R, Yan M, Luo B, Yang T, Yu X (2018) High prevalence of PCV2d in Hunan province, China: a retrospective analysis of samples collected from 2006 to 2016. Adv Virol 163(7):1897–1906Google Scholar
  29. 29.
    Saha D, Huang L, Bussalleu E, Lefebvre DJ, Fort M, Van Doorsselaere J, Nauwynck HJ (2012) Antigenic subtyping and epitopes’ competition analysis of porcine circovirus type 2 using monoclonal antibodies. Vet Microbiol 157(1–2):13–22CrossRefGoogle Scholar
  30. 30.
    Shang SB, Jin YL, Jiang XT, Zhou JY, Zhang X, Xing G, He JL, Yan Y (2009) Fine mapping of antigenic epitopes on capsid proteins of porcine circovirus, and antigenic phenotype of porcine circovirus type 2. Mol Immunol 46(3):327–334CrossRefGoogle Scholar
  31. 31.
    Shuai J, Wei W, Li X, Chen N, Zhang Z, Chen X, Fang W (2007) Genetic characterization of porcine circovirus type 2 (pcv2) from pigs in high-seroprevalence areas in southeastern China. Virus Genes 35(3):619–627CrossRefGoogle Scholar
  32. 32.
    Segalés J, Olvera A, Grau-Roma L, Charreyre C, Nauwynck H, Larsen L, Dupont K, McCullough K, Ellis J, Krakowka S, Mankertz A, Fredholm M, Fossum C, Timmusk S, Stockhofe-Zurwieden N, Beattie V, Armstrong D, Grassland B, Baekbo P, Allan G (2008) PCV-2 genotype definition and nomenclature. Vet Rec 162(26):867–868CrossRefGoogle Scholar
  33. 33.
    Stadejek T, Wozniak A, Milek D, Biernacka K (2017) First detection of porcine circovirus type 3 on commercial pig farms in Poland. Transbound Emerg Dis 64(5):1350–1353CrossRefGoogle Scholar
  34. 34.
    Tischer I, Rasch R, Tochtermann G (1974) Characterization of papovavirus-and picornavirus-like particles in permanent pig kidney cell lines. Zentralbl Bakteriol Orig A 226(2):153–156Google Scholar
  35. 35.
    Tochetto C, Lima DA, Varela APM, Loiko MR, Paim WP, Scheffer CM, Herpich JI, Cerva C, Schmitd C, Cibulski SP, Santos AC, Mayer FQ, Roehe PM (2018) Full-Genome Sequence of Porcine Circovirus type 3 recovered from serum of sows with stillbirths in Brazil. Transbound Emerg Dis 65(1):5–9CrossRefGoogle Scholar
  36. 36.
    Takahagi Y, Nishiyama Y, Toki S, Yonekita T, Morimatsu F, Murakami H (2008) Genotypic change of porcine circovirus type 2 on japanese pig farms as revealed by restriction fragment length polymorphism analysis. J Vet Med Sci 70(6):603–606CrossRefGoogle Scholar
  37. 37.
    Wang H, Gu J, Xing G, Qiu X, An S, Wang Y, Zhang C, Liu C, Gong W, Tu C, Su S, Zhou J (2018) Genetic diversity of porcine circovirus type 2 in China between 1999–2017. Transbound Emerg Dis 66(1):599–605CrossRefGoogle Scholar
  38. 38.
    Xiao CT, Halbur PG, Opriessnig T (2015) Global molecular genetic analysis of porcine circovirus type 2 (PCV2) sequences confirms the presence of four main PCV2 genotypes and reveals a rapid increase of PCV2d. J Gen Virol 96(7):1830–1841CrossRefGoogle Scholar
  39. 39.
    Zhai SL, Chen SN, Xu ZH, Tang MH, Wang FG, Li XJ, Sun BB, Deng SF, Hu J, Lv DH, Wen XH, Yuan J, Luo ML, Wei WK (2014) Porcine circovirus type 2 in China: an update on and insights to its prevalence and control. Virol J 11:88CrossRefGoogle Scholar
  40. 40.
    Zhang L, Luo Y, Liang L, Li J, Cui S (2018) Phylogenetic analysis of porcine circovirus type 3 and porcine circovirus type 2 in china detected by duplex nanoparticle-assisted pcr. Infect Genet Evol 60:1–6CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of Swine Digestive System Infectious Diseases, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research InstituteChinese Academy of Agricultural SciencesHarbinChina
  2. 2.College of Life Science and TechnologyHarbin Normal UniversityHarbinChina
  3. 3.College of Veterinary MedicineJi Lin UniversityChangchunChina

Personalised recommendations