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Retrospective surveillance of porcine circovirus 4 in pigs in Inner Mongolia, China, from 2016 to 2018

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Abstract

A novel circovirus designated "porcine circovirus type 4" (PCV4) was recently reported in pigs with severe clinical disease in Hunan Province, China. Relatively little is known about the molecular epidemiology of this recently discovered virus. In order to assess the prevalence of PCV4 infection in pigs and to analyze its genomic characteristics, 1683 clinical samples were collected in Inner Mongolia, China, from 2016 to 2018. The overall infection rate of PCV4 was 1.6% (27/1683) at the sample level and 21.6% (11/51) at the farm level, with rates ranging from 3.2% (1/31) to 20.0% (6/30) on different PCV4-positive pig farms. In addition, the PCV4 infection rates at both the sample and farm level increased from 2016 to 2018. This also showed that PCV4 was present in pigs in 2016 in China and therefore did not arrive later than this date. Additionally, our findings showed that PCV4 infections had no association with PCV2 or PCV3 infections. We sequenced the complete genomes of three PCV4 strains and found that the PCV4 strains had a high degree of genetic stability but shared less than 80% sequence identity with other circoviruses. We identified six amino acid mutations in the Rep protein and seven in the Cap protein. Phylogenetic analysis based on Cap and Rep sequences confirmed that the PCV4 strains grouped in an independent branch. Our findings provide important information about the prevalence and genetic characteristics of PCV4 strains.

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References

  1. Cao L, Sun W, Lu H, Tian M, Xie C, Zhao G, Han J, Wang W, Zheng M, Du R, Jin N, Qian A (2018) Genetic variation analysis of PCV1 strains isolated from Guangxi Province of China in 2015. BMC Vet Res 14:43

    Article  PubMed  PubMed Central  Google Scholar 

  2. Fenaux M, Opriessnig T, Halbur PG, Elvinger F, Meng XJ (2004) Two amino acid mutations in the capsid protein of type 2 porcine circovirus (PCV2) enhanced PCV2 replication in vitro and attenuated the virus in vivo. J Virol 78:13440–13446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Franzo G, Ruiz A, Grassi L, Sibila M, Drigo M, Segales J (2020) Lack of Porcine circovirus 4 genome detection in pig samples from Italy and Spain. Pathogens 9:433

    Article  PubMed Central  Google Scholar 

  4. 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 65:e296–e303

    Article  CAS  PubMed  Google Scholar 

  5. Gairu Li WH, Zhu H, Bi Y, Wang R, Xing G, Zhang C, Zhou J, Yuen K-Y, Gao GF, Shuo Su (2018) Origin, genetic diversity, and evolutionary dynamics of novel porcine circovirus 3. Adv Sci 5:1800275

    Article  Google Scholar 

  6. Ge X, Wang F, Guo X, Yang H (2012) Porcine circovirus type 2 and its associated diseases in China. Virus Res 164:100–106

    Article  CAS  PubMed  Google Scholar 

  7. 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 14:321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ha Z, Li J, Xie C, Yu C, Hao P, Zhang Y, Xu W, Nan F, Xie Y, Li Y, Rong F, Wang G, Guo Y, Lu H, Jin N (2020) Prevalence, pathogenesis, and evolution of porcine circovirus type 3 in China from 2016 to 2019. Vet Microbiol 247:108756

    Article  CAS  PubMed  Google Scholar 

  9. Ha Z, Li JF, Xie CZ, Li CH, Zhou HN, Zhang Y, Hao PF, Nan FL, Zhang JY, Han JC, Zhang H, Zhuang XY, Guo YC, Lu HJ, Jin NY (2020) First detection and genomic characterization of porcine circovirus 3 in mosquitoes from pig farms in China. Vet Microbiol 240:108522

    Article  CAS  PubMed  Google Scholar 

  10. He W, Zhao J, Xing G, Li G, Wang R, Wang Z, Zhang C, Franzo G, Su S, Zhou J (2019) Genetic analysis and evolutionary changes of Porcine circovirus 2. Mol Phylogenet Evol 139:106520

    Article  CAS  PubMed  Google Scholar 

  11. Jiang CG, Wang G, Tu YB, Liu YG, Wang SJ, Cai XH, An TQ (2017) Genetic analysis of porcine circovirus type 2 in China. Arch Virol 162:2715–2726

    Article  CAS  PubMed  Google Scholar 

  12. 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 (2019) Induction of porcine dermatitis and nephropathy syndrome in piglets by infection with porcine circovirus type 3. J Virol 93(4):e02045-18

    Article  PubMed  PubMed Central  Google Scholar 

  13. Karuppannan AK, Opriessnig T (2017) Porcine circovirus type 2 (PCV2) vaccines in the context of current molecular epidemiology. Viruses 9:99

    Article  PubMed Central  Google Scholar 

  14. Klaumann F, Franzo G, Sohrmann M, Correa-Fiz F, Drigo M, Nunez JI, Sibila M, Segales J (2018) Retrospective detection of Porcine circovirus 3 (PCV-3) in pig serum samples from Spain. Transbound Emerg Dis 65:1290–1296

    Article  CAS  PubMed  Google Scholar 

  15. Krakowka S, Allan G, Ellis J, Hamberg A, Charreyre C, Kaufmann E, Brooks C, Meehan B (2012) A nine-base nucleotide sequence in the porcine circovirus type 2 (PCV2) nucleocapsid gene determines viral replication and virulence. Virus Res 164:90–99

    Article  CAS  PubMed  Google Scholar 

  16. Li GWH, Wang S et al (2018) Insights into the genetic and host adaptability of emerging Porcine circovirus 3. Virulence 9:1301–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li J, Xing G, Zhang C, Yang H, Li G, Wang N, Wang R, Sun H, Shi Z, Lei J, Hu B, Gu J, Zhou J (2019) Cross-species transmission resulted in the emergence and establishment of circovirus in pig. Infect Genet Evol 75:103973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Liu X, Zhang X, Li X, Ouyang T, Niu G, Ouyang H, Ren L (2020) Genotyping based on complete coding sequences of porcine circovirus type 3 is stable and reliable. Infect Genet Evol 78:104116

    Article  CAS  PubMed  Google Scholar 

  19. Lv N, Zhu L, Li W, Li Z, Qian Q, Zhang T, Liu L, Hong J, Zheng X, Wang Y, Zhang Y, Chai J (2020) Molecular epidemiology and genetic variation analyses of porcine circovirus type 2 isolated from Yunnan Province in China from 2016–2019. BMC Vet Res 16:96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nawagitgul P, Morozov I, Bolin SR, Harms PA, Sorden SD, Paul PS (2000) Open reading frame 2 of porcine circovirus type 2 encodes a major capsid protein. J Gen Virol 81:2281–2287

    Article  CAS  PubMed  Google Scholar 

  21. Nguyen VG, Do HQ, Huynh TM, Park YH, Park BK, Chung HC (2021) Molecular-based detection, genetic characterization and phylogenetic analysis of porcine circovirus 4 from Korean domestic swine farms. Transbound Emerg Dis 1–11

  22. Opriessnig T, McKeown NE, Zhou EM, Meng XJ, Halbur PG (2006) Genetic and experimental comparison of porcine circovirus type 2 (PCV2) isolates from cases with and without PCV2-associated lesions provides evidence for differences in virulence. J Gen Virol 87:2923–2932

    Article  CAS  PubMed  Google Scholar 

  23. Opriessnig T, Meng XJ, Halbur PG (2007) Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J Vet Diagn Investig 19:591–615

    Article  Google Scholar 

  24. Opriessnig T, Karuppannan AK, Castro A, Xiao CT (2020) Porcine circoviruses: current status, knowledge gaps and challenges. Virus Res 286:198044

    Article  CAS  PubMed  Google Scholar 

  25. Ouyang T, Niu G, Liu X, Zhang X, Zhang Y, Ren L (2019) Recent progress on porcine circovirus type 3. Infect Genet Evol 73:227–233

    Article  PubMed  Google Scholar 

  26. Ouyang T, Zhang X, Liu X, Ren L (2019) Co-infection of swine with Porcine circovirus type 2 and other swine viruses. Viruses 11:185

    Article  CAS  PubMed Central  Google Scholar 

  27. 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):e01879-16

    Article  PubMed  Google Scholar 

  28. 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 13:184

    Article  PubMed  PubMed Central  Google Scholar 

  29. Rodrigues ILF, Cruz ACM, Souza AE, Knackfuss FB, Costa CHC, Silveira RL, Castro TX (2020) Retrospective study of porcine circovirus 3 (PCV3) in swine tissue from Brazil (1967–2018). Braz J Microbiol 51:1391–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Saha D, Lefebvre DJ, Ducatelle R, Doorsselaere JV, Nauwynck HJ (2011) Outcome of experimental porcine circovirus type 1 infections in mid-gestational porcine foetuses. BMC Vet Res 7:64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Saporiti V, Cruz TF, Correa-Fiz F, Nunez JI, Sibila M, Segales J (2020) Similar frequency of Porcine circovirus 3 (PCV-3) detection in serum samples of pigs affected by digestive or respiratory disorders and age-matched clinically healthy pigs. Transbound Emerg Dis 67:199–205

    Article  CAS  PubMed  Google Scholar 

  32. Saporiti V, Huerta E, Correa-Fiz F, Grosse Liesner B, Duran O, Segales J, Sibila M (2020) Detection and genotyping of Porcine circovirus 2 (PCV-2) and detection of Porcine circovirus 3 (PCV-3) in sera from fattening pigs of different European countries. Transbound Emerg Dis 67:2521–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Segales 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 162:867–868

    Article  CAS  PubMed  Google Scholar 

  34. Segales J (2012) Porcine circovirus type 2 (PCV2) infections: clinical signs, pathology and laboratory diagnosis. Virus Res 164:10–19

    Article  CAS  PubMed  Google Scholar 

  35. Segales J, Kekarainen T, Cortey M (2013) The natural history of porcine circovirus type 2: from an inoffensive virus to a devastating swine disease? Vet Microbiol 165:13–20

    Article  CAS  PubMed  Google Scholar 

  36. Sukmak M, Thanantong N, Poolperm P, Boonsoongnern A, Ratanavanichrojn N, Jirawattanapong P, Woonwong Y, Soda N, Kaminsonsakul T, Phuttapatimok S, Wajjwalku W (2019) The retrospective identification and molecular epidemiology of porcine circovirus type 3 (PCV3) in swine in Thailand from 2006 to 2017. Transbound Emerg Dis 66:611–616

    Article  CAS  PubMed  Google Scholar 

  37. 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 

  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Tian RB, Zhao Y, Cui JT, Zheng HH, Xu T, Hou CY, Wang ZY, Li XS, Zheng LL, Chen HY (2020) Molecular detection and phylogenetic analysis of Porcine circovirus 4 in Henan and Shanxi Provinces of China. Transbound Emerg Dis 66:1004–1015

    Google Scholar 

  40. Tischer I, Gelderblom H, Vettermann W, Koch MA (1982) A very small porcine virus with circular single-stranded DNA. Nature 295:64–66

    Article  CAS  PubMed  Google Scholar 

  41. Wei R, Xie J, Theuns S, Nauwynck HJ (2019) Changes on the viral capsid surface during the evolution of porcine circovirus type 2 (PCV2) from 2009 till 2018 may lead to a better receptor binding. Virus Evol 5:vez026

    Article  PubMed  PubMed Central  Google Scholar 

  42. Xia D, Huang L, Xie Y, Zhang X, Wei Y, Liu D, Zhu H, Bian H, Feng L, Liu C (2019) The prevalence and genetic diversity of porcine circovirus types 2 and 3 in Northeast China from 2015 to 2018. Arch Virol 164:2435–2449

    Article  CAS  PubMed  Google Scholar 

  43. 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 96:1830–1841

    Article  CAS  PubMed  Google Scholar 

  44. 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 11:88

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zhai SL, Lu SS, Wei WK, Lv DH, Wen XH, Zhai Q, Chen QL, Sun YW, Xi Y (2019) Reservoirs of Porcine circoviruses: a mini review. Front Vet Sci 6:319

    Article  PubMed  PubMed Central  Google Scholar 

  46. Zhang HH, Hu WQ, Li JY, Liu TN, Zhou JY, Opriessnig T, Xiao CT (2020) Novel circovirus species identified in farmed pigs designated as Porcine circovirus 4, Hunan province, China. Transbound Emerg Dis 67:1057–1061

    Article  CAS  PubMed  Google Scholar 

  47. Zheng G, Lu Q, Wang F, Xing G, Feng H, Jin Q, Guo Z, Teng M, Hao H, Li D, Wei X, Zhang Y, Deng R, Zhang G (2020) Phylogenetic analysis of porcine circovirus type 2 (PCV2) between 2015 and 2018 in Henan Province, China. BMC Vet Res 16:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by grants from the National Key Research and Development Program of China (Grant numbers 2017YFD0500101 and 2016YFD0500401). The funders did not play any role in the design, conclusions, or interpretation of the study.

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Author notes

  1. Zhuo Ha and Chengdong Yu contributed equally to this work.

Authors and Affiliations

  1. Institute of Military Veterinary medicine, Academy of Military Medical Sciences, Changchun, 130122, China

    Zhuo Ha, Chengdong Yu, Changzhan Xie, Pengfei Hao, Jinfeng Li, Zhuoxin Li, Fulong Nan, He Zhang, Xinyu Zhuang, Yubiao Xie, Ning Shi, Huijun Lu & Ningyi Jin

  2. Hulunbuir Animal Disease Control Center, Hulunbuir, 021000, China

    Guanyu Wang

  3. College of Veterinary Medicine, Jilin University, Changchun, 130012, China

    Ying Zhang

  4. National Engineering Research Center of Veterinary Biologics, Harbin, 150001, China

    Yanwei Li

  5. Harbin Pharmaceutical Group Bio-vaccine Co., Ltd, Harbin, 150030, China

    Fulong Rong

  6. Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou University, Yangzhou, 225009, China

    Huijun Lu & Ningyi Jin

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  1. Zhuo Ha
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Contributions

NYJ and HJL designed the experiments. ZH, CDY, CZX, and GYW performed the experiments. ZH, YZ, PFH, JFL, ZXL, YWL, and FLR analyzed the data. ZH, FLN, HZ, XYZ, YBX, and NS drew the graphs. ZH, YWL, PFH, and HJL wrote the paper. All authors approved the final manuscript.

Corresponding authors

Correspondence to Huijun Lu or Ningyi Jin.

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Conflict of interest

All authors have declared no conflict of interest.

Ethical approval

The clinical samples used in this study were obtained with written permission from the farm owners, and sampling was carried out in strict accordance with the Animal Ethics Procedures and Guidelines of the People's Republic of China. All of the animal protocols used in this study were approved by the Ethics Committee of the Military Veterinary Medicine Institute.

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Supplementary Information

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Supplementary Fig. S1

The genomic organization of PCV4. Complete genome sequences of PCV4/NM1 (MT882410) with 1770 nt, containing two inversely arranged ORFs. ORF1 encodes the replicase protein (REP), and ORF2 encodes the capsid protein (CAP). (TIF 14054 KB)

Supplementary Fig. S2

Phylogenetic analysis of the three PCV4 Cap protein genes from this study, together with those of two PCV4 strains and 24 related circoviruses obtained from GenBank. The three PCV4 strains from this study are indicated by red triangles. The tree was constructed using MEGA version 6.06 with 1000 bootstraps replicates and a p-distance model. (a) Neighbor-joining method. (b) Maximum-likelihood method (JPG 2206 KB)

Supplementary Fig. S3

Phylogenetic analysis of the three PCV4 Rep protein genes from this study, together with those of two PCV4 strains and 24 related circoviruses obtained from GenBank. The three PCV4 strains from this study are indicated by red triangles. The tree was constructed using MEGA version 6.06 with 1000 bootstrap replicates and a p-distance model. (a) Neighbor-joining method. (b) Maximum-likelihood method (JPG 1906 KB)

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Ha, Z., Yu, C., Xie, C. et al. Retrospective surveillance of porcine circovirus 4 in pigs in Inner Mongolia, China, from 2016 to 2018. Arch Virol 166, 1951–1959 (2021). https://doi.org/10.1007/s00705-021-05088-w

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