Epizootiological surveillance of porcine circoviruses in free-ranging wild boars in China

Wenjie Gong; Haiying Du; Tong Wang; Heting Sun; Peng Peng; Siyuan Qin; Haidong Geng; Zheng Zeng; Wangwang Liang; Hongquan Ling; Changchun Tu; Zhongzhong Tu

doi:10.1016/j.virs.2023.08.008

October 2023

Citation: Wenjie Gong, Haiying Du, Tong Wang, Heting Sun, Peng Peng, Siyuan Qin, Haidong Geng, Zheng Zeng, Wangwang Liang, Hongquan Ling, Changchun Tu, Zhongzhong Tu. Epizootiological surveillance of porcine circoviruses in free-ranging wild boars in China .VIROLOGICA SINICA, 2023, 38(5) : 663-670. http://dx.doi.org/10.1016/j.virs.2023.08.008

Epizootiological surveillance of porcine circoviruses in free-ranging wild boars in China

Wenjie Gong ^a,b ,
Haiying Du ^b ,
Tong Wang ^b,c ,
Heting Sun ^d ,
Peng Peng ^d ,
Siyuan Qin ^d ,
Haidong Geng ^d ,
Zheng Zeng ^e ,
Wangwang Liang ^e ,
Hongquan Ling ^e ,
Changchun Tu ^{b,c
,,} ,
Zhongzhong Tu ^{b
,,}

a. State Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, 130062, China;
b. Changchun Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Changchun, 130122, China;
c. Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou University, Yangzhou, 225009, China;
d. Biological Disaster Control and Prevention Center, National Forestry and Grassland Administration, Shenyang, 110034, China;
e. Chongqing Animal Disease Prevention and Control Center, Chongqing, 401120, China

Corresponding author: Changchun Tu, changchun_tu@hotmail.com
Zhongzhong Tu, tudong890901@163.com
Received Date: 18 April 2023
Accepted Date: 28 August 2023
Available online: 01 September 2023

Abstract

Four species of porcine circoviruses (PCV1-4) have been reported to circulate in Chinese domestic pigs, while the epizootiology of these viruses in free-ranging wild boars in China remains unknown. In this study, tissue and serum samples collected from diseased or apparently healthy wild boars between 2018 and 2020 in 19 regions of China were tested for the prevalence of PCV1-4 infections. Positive rates of PCV1, PCV2, and PCV3 DNA in the tissue samples of Chinese wild boars were 1.6% (4/247), 58.3% (144/247), and 10.9% (27/247) respectively, with none positive for PCV4. Sequence analysis of viral genome showed that the four PCV1 strains distributed in Hunan and Inner Mongolia shared 97.5%-99.6% sequence identity with global distributed reference strains. Comparison of the ORF2 gene sequences showed that 80 PCV2 strains widely distributed in 18 regions shared 79.5%-100% sequence identity with reference strains from domestic pigs and wild boars, and were grouped into PCV2a (7), PCV2b (31) and PCV2d (42). For PCV3, 17 sequenced strains shared 97.2%-100% nucleotide identity at the genomic level and could be divided into PCV3a (3), PCV3b (2) and PCV3c (12) based on the phylogeny of ORF2 gene sequences. Serological data revealed antibody positive rates against PCV1 and PCV2 of 11.4% (19/167) and 53.9% (90/167) respectively. The data obtained in this study improved our understanding about the epidemiological situations of PCVs infection in free-ranging wild boars in China and will be valuable for the prevention and control of diseases caused by PCVs infection.
- Porcine circoviruses (PCVs)
- , Epizootiology
- , Wild boar
- , China

Electronic Supplementary Material

10.1016j.virs.2023.08.008-ESM.rtf
References
1. Allan G, McNeilly F, Kennedy S, Daft B, Clarke E, Ellis J, Haines D, Meehan B, Adair B. 1998. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and europe. Journal of veterinary diagnostic investigation, 10:3-10.
2. Amoroso M, Serra F, Esposito C, D'Alessio N, Ferrara G, Cioffi B, Anzalone A, Pagnini U, De Carlo E, Fusco G, Montagnaro S. 2021. Prevalence of infection with porcine circovirus types 2 and 3 in the wild boar population in the campania region (southern italy). Animals, 11:3215.
3. Auer A, Schweitzer L, Kübber-Heiss A, Posautz A, Dimmel K, Seitz K, Beiglböck C, Riedel C, Rümenapf T. 2022. Porcine circoviruses and herpesviruses are prevalent in an austrian game population. Pathogens (Basel, Switzerland), 11:305.
4. Barbosa C, Martins N, Freitas T, Lobato Z. 2016. Serological survey of porcine circovirus-2 in captive wild boars (sus scrofa) from registered farms of south and south-east regions of brazil. Transboundary and emerging diseases, 63:e278-280.
5. 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.
6. Chen S, Zhang L, Li X, Niu G, Ren L. 2021. Recent progress on epidemiology and pathobiology of porcine circovirus 3. Viruses, 13:1944.
7. Cságola A, Kecskeméti S, Kardos G, Kiss I, Tuboly T. 2006. Genetic characterization of type 2 porcine circoviruses detected in hungarian wild boars. Archives of virology, 151:495-507.
8. de Sousa Moreira A, Santos-Silva S, Mega J, Palmeira J, Torres R, Mesquita J. 2022. Epidemiology of porcine circovirus type 2 circulating in wild boars of portugal during the 2018-2020 hunting seasons suggests the emergence of genotype 2d. Animals, 12:451.
9. Dei Giudici S, Franzoni G, Bonelli P, Angioi P, Zinellu S, Deriu V, Carta T, Sechi A, Salis F, Balzano F, Oggiano A. 2020. Genetic characterization of porcine circovirus 3 strains circulating in sardinian pigs and wild boars. Pathogens (Basel, Switzerland), 9:344.
10. Dyk A, Hrk A, Jhpa C, Nyk A, Jmk A, Jkk A, Jhp A, Kkl B, Shk B, Wik D. 2021. Detection of a novel porcine circovirus 4 in korean pig herds using a loop-mediated isothermal amplification assay. J Virol Methods, 299:114350.
11. Ellis J. 2014. Porcine circovirus:A historical perspective. Veterinary pathology, 51:315-327.
12. Fanelli A, Pellegrini F, Camero M, Catella C, Buonavoglia D, Fusco G, Martella V, Lanave G. 2022. Genetic diversity of porcine circovirus types 2 and 3 in wild boar in italy. Animals, 12:953.
13. Franzo G, Tucciarone C, Drigo M, Cecchinato M, Martini M, Mondin A, Menandro M. 2018. 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. Transboundary and emerging diseases, 65:957-962.
14. 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. Transboundary and emerging diseases, 65:e296-e303.
15. Fux R, Söckler C, Link EK, 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.
16. Geng S, Luo H, Liu Y, Chen C, Xu W, Chen Y, Li X, Fang W. 2019. Prevalence of porcine circovirus type 3 in pigs in the southeastern chinese province of zhejiang. BMC Vet Res, 15:244.
17. Gillespie J, Opriessnig T, Meng X, Pelzer K, Buechner-Maxwell V. 2009. Porcine circovirus type 2 and porcine circovirus-associated disease. Journal of veterinary internal medicine, 23:1151-1163.
18. Gong W, Du H, Sun X, Sun H, Peng P, Qin S, Geng H, Zeng Z, Liang W, Ling H, Tu C, Tu Z. 2022. Genetic characterization of hepatitis e virus from wild boar in china. Transboundary and emerging diseases, 69:e3357-e3362.
19. Guo HC, Ren ZW, Ding MM, Xiao WJ, Peng P, He B, Feng Y, Liu Y, Li XY, Cai JQ, Zhang BK, Luo QH, Tu CC. 2019. Serologic and molecular survey for major viral pathogens in grazing hybrid wild boars in northeast china. Journal of Integrative Agriculture, 18:2133-2140.
20. Han L, Yuan G, Chen S, Dai F, Hou L, Fan J, Zuo Y. 2021. Porcine circovirus type 2 (pcv2) infection in hebei province from 2016 to 2019:A retrospective study. Archives of virology, 166:2159-2171.
21. Hu X, Chen Z, Li Y, Ding Z, Zeng Q, Wan T, Wu H. 2022. Detection of porcine circovirus 1/2/3 and genetic analysis of porcine circovirus 2 in wild boar from jiangxi province of china. Animals (Basel), 12:2021.
22. Kim J, Han DU, Choi C, Chae C. 2001. Differentiation of porcine circovirus (pcv)-1 and pcv-2 in boar semen using a multiplex nested polymerase chain reaction. J Virol Methods, 98:25-31.
23. Klaumann F, Dias-Alves A, Cabezón O, Mentaberre G, Castillo-Contreras R, López-Béjar M, Casas-Díaz E, Sibila M, Correa-Fiz F, Segalés J. 2019. Porcine circovirus 3 is highly prevalent in serum and tissues and may persistently infect wild boar (sus scrofa scrofa). Transboundary and emerging diseases, 66:91-101.
24. 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, 64:703-708.
25. Li L, Ren Z, Wang Q, Ge S, Liu Y, Liu C, Liu F, Hu Y, Li J, Bao J, Ren W, Zhang Y, Xu T, Sun C, Li L, Wang S, Fan X, Wu Z, Huang B, Guo H, Wu X, Wang Z. 2019. Infection of african swine fever in wild boar, china, 2018. Transboundary and emerging diseases, 66:1395-1398.
26. Mahé D, Blanchard P, Truong C, Arnauld C, Le Cann P, Cariolet R, Madec F, Albina E, Jestin A. 2000. Differential recognition of orf2 protein from type 1 and type 2 porcine circoviruses and identification of immunorelevant epitopes. J Gen Virol, 81:1815-1824.
27. Mankertz A, Domingo M, Folch JM, LeCann P, Jestin A, Segalés J, Chmielewicz B, Plana-Durán J, Soike D. 2000. Characterisation of pcv-2 isolates from spain, germany and france. Virus Res, 66:65-77.
28. Meng X, Lindsay D, Sriranganathan N. 2009. Wild boars as sources for infectious diseases in livestock and humans. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 364:2697-2707.
29. Opriessnig T, Karuppannan A, Castro A, Xiao C. 2020. Porcine circoviruses:Current status, knowledge gaps and challenges. Virus research, 286:198044.
30. Palinski R, Piñeyro P, Shang P, Yuan F, Guo R, Fang Y, Byers E, Hause B. 2017. A novel porcine circovirus distantly related to known circoviruses is associated with porcine dermatitis and nephropathy syndrome and reproductive failure. Journal of virology, 91:e01879-16.
31. Phan T, Giannitti F, Rossow S, Marthaler D, Knutson T, 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. Virology journal, 13:184.
32. Prinz C, Stillfried M, Neubert L, Denner J. 2019. Detection of pcv3 in german wild boars. Virology journal, 16:25.
33. Risco D, Fernández-Llario P, García-Jiménez W, Gonçalves P, Cuesta J, Martínez R, Sanz C, Sequeda M, Gómez L, Carranza J, de Mendoza J. 2013. Influence of porcine circovirus type 2 infections on bovine tuberculosis in wild boar populations. Transboundary and emerging diseases:121-127.
34. Rudova N, Buttler J, Kovalenko G, Sushko M, Bolotin V, Muzykina L, Zinenko O, Stegniy B, Dunaiev Y, Sytiuk M, Gerilovych A, Drown D, Bortz E, Solodiankin O. 2022. Genetic diversity of porcine circovirus 2 in wild boar and domestic pigs in ukraine. Viruses, 14:924.
35. 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, 157:13-22.
36. 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, 35:619-627.
37. Song S, Park G, Choe S, Cha R, Kim S, Hyun B, Park B, An D. 2020. Genetic diversity of porcine circovirus isolated from korean wild boars. Pathogens (Basel, Switzerland), 9:457.
38. Souza T, Gava D, Schaefer R, Leme R, Porto G, Alfieri A. 2021. Porcine circovirus 3a field strains in free-living wild boars in paraná state, brazil. Animals, 11:1634.
39. Sun W, Du Q, Han Z, Bi J, Lan T, Wang W, Zheng M. 2021. Detection and genetic characterization of porcine circovirus 4 (pcv4) in guangxi, china. Gene, 773:145384.
40. Tian R, Zhao Y, Cui J, Zheng H, Xu T, Hou C, Wang Z, Li X, Zheng L, Chen H. 2020. Molecular detection and phylogenetic analysis of porcine circovirus 4 in henan and shanxi provinces of china. Transboundary and emerging diseases, 68:276-282.
41. Tischer I, Rasch R, Tochtermann G. 1974. Characterization of papovavirus-and picornavirus-like particles in permanent pig kidney cell lines. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Erste Abteilung Originale. Reihe A:Medizinische Mikrobiologie und Parasitologie, 226:153-167.
42. Touloudi A, Valiakos G, Athanasiou L, Birtsas P, Giannakopoulos A, Papaspyropoulos K, Kalaitzis C, Sokos C, Tsokana C, Spyrou V, Petrovska L, Billinis C. 2015. A serosurvey for selected pathogens in greek european wild boar. Veterinary record open, 2:e000077.
43. Turlewicz-Podbielska H, Augustyniak A, Pomorska-Mól M. 2022. Novel porcine circoviruses in view of lessons learned from porcine circovirus type 2-epidemiology and threat to pigs and other species. Viruses, 14:261.
44. Vicente J, Segalés J, Höfle U, Balasch M, Plana-Durán J, Domingo M, Gortázar C. 2004. Epidemiological study on porcine circovirus type 2 (pcv2) infection in the european wild boar (sus scrofa). Veterinary research, 35:243-253.
45. 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. Transboundary and emerging diseases, 65:27-31.
46. Wu H, Hou C, Wang Z, Meng P, Chen H, Cao H. 2022. First complete genomic sequence analysis of porcine circovirus type 4 (pcv4) in wild boars. Vet Microbiol, 273:109547.
47. 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. Archives of virology, 164:2435-2449.
48. Xu Q, Zhang Y, Sun W, Chen H, Zhu D, Lu C, Yin Y, Rai K, Chen J, Chen Y. 2022. Epidemiology and genetic diversity of pcv2 reveals that pcv2e is an emerging genotype in southern china:A preliminary study. Viruses, 14:724.
49. Xu T, Zhang Y, Tian R, Hou C, Li X, Zheng L, Wang L, Chen H. 2021. Prevalence and genetic analysis of porcine circovirus type 2 (pcv2) and type 3 (pcv3) between 2018 and 2020 in central china. Infection, genetics and evolution:journal of molecular epidemiology and evolutionary genetics in infectious diseases, 94:105016.
50. 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.
51. Zhang H, Hu W, Li J, Liu T, Zhou J, Opriessnig T, Xiao C. 2020. Novel circovirus species identified in farmed pigs designated as porcine circovirus 4, hunan province, china. Transboundary and emerging diseases, 67:1057-1061.
52. Zheng X, Nie S, Feng WH. 2022. Regulation of antiviral immune response by african swine fever virus (asfv). Virol Sin, 37:157-167.
53. Zhuo H, Yu C, Xie C, Wang G, Jin N. 2021. Retrospective surveillance of porcine circovirus 4 in pigs in inner mongolia, china, from 2016 to 2018. Archives of Virology:1-9.
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