Abstract
Porcine circovirus type 2 (PCV2) is considered the major etiological pathogen of porcine circovirus-associated diseases (PCVADs) in pigs. Recently, PCV2 was also found in non-porcine animals such as cattle, rats, and mice. However, there was no record of PCV2 in rats in China. The goal of this study was to investigate whether PCV2 was present in rats (Rattus norvegicus, RN) on three swine farms, using molecular tools. PCR results showed that 30 of 95 (31.6 %) rat samples were positive for PCV2. Moreover, further genotype analysis suggested that 10 of 30 (33.3 %) were positive for PCV2a, 19 of 30 (63.3 %) were positive for PCV2b, and only one sample (1/30, 3.33 %) was co-infected by PCV2a and PCV2b. To determine the possible origin of PCV2, 60 serum samples were also collected from weaned pigs on those swine farms, and 23 out of 60 samples were positive for PCV2. In addition, two distinct RN-origin and two distinct porcine-origin PCV2 full-length nucleotide sequences were obtained from the farms. Sequence and phylogenetic analysis indicated that they had the highest nucleotide similarity and closest genetic relationships to each other. In this study, we report the infection and genome characterization of PCV2 in rats and compare RN-origin and porcine-origin PCV2 sequences obtained from the same pig farm, revealing possible cross-species transmission of PCV2.
References
Blunt R, McOrist S, McKillen J, McNair I, Jiang T, Mellits K (2011) House fly vector for porcine circovirus 2b on commercial pig farms. Vet Microbiol 149:452–455
Cheung AK, Lager KM, Kohutyuk OI, Vincent AL, Henry SC, Baker RB, Rowland RR, Dunham AG (2007) Detection of two porcine circovirus type 2 genotypic groups in United States swine herds. Arch Virol 152:1035–1044
Cságola A, Cadar D, Tuboly T (2008) Replication and transmission of porcine circovirus type 2 in experimentally inoculated mice. Acta Vet Hung 55:421–427
Cságola A, Kecskeméti S, Kardos G, Kiss I, Tuboly T (2006) Genetic characterization of type 2 porcine circoviruses detected in Hungarian wild boars. Arch Virol 151:495–507
Davies B, Wang X, Dvorak CM, Marthaler D, Murtaugh MP (2016) Diagnostic phylogenetics reveals a new Porcine circovirus 2 cluster. Virus Res 217:32–37
Deng ZB, Wang ND, Xu DJ, Yuan AW, Ge M, Luo W, Xue LQ, Yu XL (2011) Viral distribution and lesions in Kunming mice experimentally infected with porcine circovirus type 2b. Vet Res Commun 35:181–192
Deng ZB, Yuan AW, Luo W, Wang ND, Gong QL, Yu XL, Xue LQ (2013) Transmission of porcine circovirus type 2b (PCV2b) in Kunming mice. Acta Vet Hung 61:234–243
Dezen D, Rijsewijk FA, Teixeira TF, Holz CL, Cibulski SP, Franco AC, Dellagostin OA, Roehe PM (2010) Multiply-primed rolling-circle amplification (MPRCA) of PCV2 genomes: applications on detection, sequencing and virus isolation. Res Vet Sci 88:436–440
Dupont K, Nielsen EO, Baekbo P, Larsen LE (2008) Genomic analysis of PCV2 isolates from Danish archives and a current PMWS case-control study supports a shift in genotypes with time. Vet Microbiol 128:56–64
Eddicks M, Fux R, Szikora F, Eddicks L, Majzoub-Altweck M, Hermanns W, Sutter G, Palzer A, Banholzer E, Ritzmann M (2015) Detection of a new cluster of porcine circovirus type 2b strains in domestic pigs in Germany. Vet Microbiol 176:337–343
Franzo G, Cortey M, de Castro AM, Piovezan U, Szabo MP, Drigo M, Segalés J, Richtzenhain LJ (2015) Genetic characterisation of Porcine circovirus type 2 (PCV2) strains from feral pigs in the Brazilian Pantanal: An opportunity to reconstruct the history of PCV2 evolution. Vet Microbiol 178:158–162
Franzo G, Tucciarone CM, Dotto G, Gigli A, Ceglie L, Drigo M (2015) International trades, local spread and viral evolution: the case of porcine circovirus type 2 (PCV2) strains heterogeneity in Italy. Infect Genet Evol 32:409–415
Garcia LA, Viancelli A, Rigotto C, Pilotto MR, Esteves PA, Kunz A, Barardi CR (2012) Surveillance of human and swine adenovirus, human norovirus and swine circovirus in water samples in Santa Catarina, Brazil. J Water Health 10:445–452
Grierson SS, King DP, Wellenberg GJ, Banks M (2004) Genome sequence analysis of 10 Dutch porcine circovirus type 2 (PCV-2) isolates from a PMWS case-control study. Res Vet Sci 77:265–268
Halami MY, Müller H, Böttcher J, Vahlenkamp TW (2014) Whole-genome sequences of two strains of porcine circovirus 2 isolated from calves in Germany. Genome Announc 2:e01150-13
Halami MY, Freick M, Shehata AA, Müller H, Vahlenkamp TW (2014) Susceptibility of calves to porcine circovirus-2 (PCV2). Vet Microbiol 173:125–131
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:e01315-15
Hu J, Zhai SL, Zeng SY, Sun BB, Deng SF, Chen HL, Zheng Y, Wang HX, Li XP, Liu JK, Cheng S, Zhou X, Zhai JQ, Luo ML (2015) Identification of natural recombinants derived from PCV2a and PCV2b. Genet Mol Res 14:11780–11790
Kappe EC, Halami MY, Schade B, Alex M, Hoffmann D, Gangl A, Meyer K, Dekant W, Schwarz BA, Johne R, Buitkamp J, Böttcher J, Müller H (2010) Bone marrow depletion with haemorrhagic diathesis in calves in Germany: characterization of the disease and preliminary investigations on its aetiology. Berl Munch Tierarztl Wochenschr 123:31–41
Kiupel M, Stevenson GW, Choi J, Latimer KS, Kanitz CL, Mittal SK (2001) Viral replication and lesions in BALB/c mice experimentally inoculated with porcine circovirus isolated from a pig with postweaning multisystemic wasting disease. Vet Pathol 38:74–82
Kiupel M, Stevenson GW, Galbreath EJ, North A, HogenEsch H, Mittal SK (2005) Porcine circovirus type 2 (PCV2) causes apoptosis in experimentally inoculated BALB/c mice. BMC Vet Res 1:7
Li L, Kapoor A, Slikas B, Bamidele OS, Wang C, Shaukat S, Masroor MA, Wilson ML, Ndjango JB, Peeters M, Gross-Camp ND, Muller MN, Hahn BH, Wolfe ND, Triki H, Bartkus J, Zaidi SZ, Delwart E (2010) Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84:1674–1682
Li J, Yuan X, Zhang C, Miao L, Wu J, Shi J, Xu S, Cui S, Wang J, Ai H (2010) A mouse model to study infection against porcine circovirus type 2: viral distribution and lesions in mouse. Virol J 7:158
Li L, Shan T, Soji OB, Alam MM, Kunz TH, Zaidi SZ, Delwart E (2011) Possible cross-species transmission of circoviruses and cycloviruses among farm animals. J Gen Virol 92:768–772
Lohse L, Bøtner A, Hansen AS, Frederiksen T, Dupont K, Christensen CS, Baekbo P, Nielsen J (2008) Examination for a viral co-factor in postweaning multisystemic wasting syndrome (PMWS). Vet Microbiol 129:97–107
Lorincz M, Cságola A, Biksi I, Szeredi L, Dán A, Tuboly T (2010) Detection of porcine circovirus in rodents - short communication. Acta Vet Hung 58:265–268
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
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 79:2171–2179
Morozov I, Sirinarumitr T, Sorden SD, Halbur PG, Morgan MK, Yoon KJ, Paul PS (1998) Detection of a novel strain of porcine circovirus in pigs with postweaning multisystemic wasting syndrome. J Clin Microbiol 36:2535–2541
Nayar GP, Hamel AL, Lin L, Sachvie C, Grudeski E, Spearman G (1999) Evidence for circovirus in cattle with respiratory disease and from aborted bovine fetuses. Can Vet J 40:277–278
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 Invest 19:591–615
Opriessnig T, Ramamoorthy S, Madson DM, Patterson AR, Pal N, Carman S, Meng XJ, Halbur PG (2008) Differences in virulence among porcine circovirus type 2 isolates are unrelated to cluster type 2a or 2b and prior infection provides heterologous protection. J Gen Virol 89:2482–2491
Pinheiro AL, Bulos LH, Onofre TS, de Paula Gabardo M, de Carvalho OV, Fausto MC, Guedes RM, de Almeida MR, Silva Júnior A (2013) Verification of natural infection of peridomestic rodents by PCV2 on commercial swine farms. Res Vet Sci 94:764–768
Quintana J, Balasch M, Segalés J, Calsamiglia M, Rodríguez-Arrioja GM, Plana-Durán J, Domingo M (2002) Experimental inoculation of porcine circoviruses type 1 (PCV1) and type 2 (PCV2) in rabbits and mice. Vet Res 33:229–237
Segalés J (2012) Porcine circovirus type 2 (PCV2) infections: clinical signs, pathology and laboratory diagnosis. Virus Res 164:10–19
Truong QL, Seo TW, Yoon BI, Kim HC, Han JH, Hahn TW (2013) Prevalence of swine viral and bacterial pathogens in rodents and stray cats captured around pig farms in Korea. J Vet Med Sci 75:1647–1650
Wang F, Guo X, Ge X, Wang Z, Chen Y, Cha Z, Yang H (2009) Genetic variation analysis of Chinese strains of porcine circovirus type 2. Virus Res 145:151–156
Xiao CT, Halbur PG, Opriessnig T (2012) Complete genome sequence of a novel porcine circovirus type 2b variant present in cases of vaccine failures in the United States. J Virol 86:12469
Yang X, Hou L, Ye J, He Q, Cao S (2012) Detection of porcine circovirus type 2 (PCV2) in mosquitoes from pig farms by PCR. Pak Vet J 32:134–135
Zhai SL, He DS, Qi WB, Chen SN, Deng SF, Hu J, Li XP, Li L, Chen RA, Luo ML, Wei WK (2014) Complete genome characterization and phylogenetic analysis of three distinct buffalo-origin PCV2 isolates from China. Infect Genet Evol 28:278–282
Zhai SL, Chen RA, Chen SN, Wen XH, Lv DH, Wu DC, Yuan J, Huang Z, Zhou XR, Luo ML, He DS, Wei WK (2014) First molecular detection of porcine circovirus type 2 in bovids in China. Virus Genes 49:507–511
Zhai SL, Chen SN, Wei ZZ, Zhang JW, Huang L, Lin T, Yue C, Ran DL, Yuan SS, Wei WK, Long JX (2011) Co-existence of multiple strains of porcine circovirus type 2 in the same pig from China. Virol J 8:517
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
Zhan Y, Wang N, Zhu Z, Wang Z, Wang A, Deng Z, Yang Y (2016) 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 97:922–933
Acknowledgments
We are very grateful to three anonymous reviewers for the critical review. This study was supported by Grants (No. 2013B060500063, No. 2014B040404061, No. 2016A040401012 and No. 2015A020208008) from the Guangdong Provincial Department of Science and Technology and a Grant (No. 201508020055) from the Guangzhou Science Technology and Innovation Commission.
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S.-L. Zhai, S.-N. Chen and W. Liu contributed equally to this study.
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Zhai, SL., Chen, SN., Liu, W. et al. Molecular detection and genome characterization of porcine circovirus type 2 in rats captured on commercial swine farms. Arch Virol 161, 3237–3244 (2016). https://doi.org/10.1007/s00705-016-3004-7
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DOI: https://doi.org/10.1007/s00705-016-3004-7