Viruses in the genus Bocavirus are associated with respiratory and enteric disease in dogs and cattle. In addition, novel porcine bocaviruses (PBoVs) have been identified in domestic and wild pigs in recent years, but are of unknown relevance to date. The objectives of this study were to determine the prevalence ra
tes and genetic diversity of PBoVs in pigs in the USA. Using newly established multiplex real-time PCR assays, 385 lung, lymph node, serum and faecal samples from pigs with various disease conditions were investigated. A high PBoV prevalence rate ranging from 21.3 to 50.8 % was identified in the investigated samples and often two or more PBoV species were detected in the same sample. Cloning and sequencing analysis of the partial non-structural protein NS1 and the capsid proteins VP1 and VP2 of DNA samples positive for PBoV groups 1 (n = 6), 2 (n = 16) and 3 (n = 42), including subgroups 3A, 3B or 3C, revealed a high genetic diversity especially for the PBoV G3 VP2 gene, whereas the PBoV group 1 VP1 gene displayed a low nucleotide polymorphism. Using primer walking, 18 partial or nearly complete genomes of PBoVs were obtained and six of the 18 nearly complete genomes represented novel PBoV species. Recombination analysis using partial NS1, VP1 and VP2 genes and the nearly complete genomes indicated possible recombination events within and between PBoVs. Further studies will be required to reveal the possible pathogenic role of these diverse PBoVs.
AllanderT., EmersonS. U., EngleR. E., PurcellR. H., BukhJ.2001; A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. Proc Natl Acad Sci U S A 98:11609–11614 [View Article][PubMed]
AllanderT., TammiM. T., ErikssonM., BjerknerA., Tiveljung-LindellA., AnderssonB.2005; Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci U S A 102:12891–12896 [View Article][PubMed]
ArthurJ. L., HigginsG. D., DavidsonG. P., GivneyR. C., RatcliffR. M.2009; A novel bocavirus associated with acute gastroenteritis in Australian children. PLoS Pathog 5:e1000391 [View Article][PubMed]
BlomströmA. L., BelákS., FossumC., McKillenJ., AllanG., WallgrenP., BergM.2009; Detection of a novel porcine boca-like virus in the background of porcine circovirus type 2 induced postweaning multisystemic wasting syndrome. Virus Res 146:125–129 [View Article][PubMed]
DuffyS., ShackeltonL. A., HolmesE. C.2008; Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276 [View Article][PubMed]
GrigorasI., TimchenkoT., Grande-PérezA., KatulL., VettenH. J., GronenbornB.2010; High variability and rapid evolution of a nanovirus. J Virol 84:9105–9117 [View Article][PubMed]
HoelzerK., ShackeltonL. A., HolmesE. C., ParrishC. R.2008a; Within-host genetic diversity of endemic and emerging parvoviruses of dogs and cats. J Virol 82:11096–11105 [View Article][PubMed]
HoelzerK., ShackeltonL. A., ParrishC. R., HolmesE. C.2008b; Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. J Gen Virol 89:2280–2289 [View Article][PubMed]
KapoorA., SlikasE., SimmondsP., ChieochansinT., NaeemA., ShaukatS., AlamM. M., SharifS., AngezM.other authors2009; A newly identified bocavirus species in human stool. J Infect Dis 199:196–200 [View Article][PubMed]
KapoorA., MehtaN., EsperF., Poljsak-PrijateljM., QuanP. L., QaisarN., DelwartE., LipkinW. I.2010a; Identification and characterization of a new bocavirus species in gorillas. PLoS ONE 5:e11948 [View Article][PubMed]
KapoorA., MehtaN., DuboviE. J., SimmondsP., GovindasamyL., MedinaJ. L., StreetC., ShieldsS., LipkinW. I.2012; Characterization of novel canine bocaviruses and their association with respiratory disease. J Gen Virol 93:341–346 [View Article][PubMed]
LauS. K., YipC. C., QueT. L., LeeR. A., Au-YeungR. K., ZhouB., SoL. Y., LauY. L., ChanK. H.other authors2007; Clinical and molecular epidemiology of human bocavirus in respiratory and fecal samples from children in Hong Kong. J Infect Dis 196:986–993 [View Article][PubMed]
LauS. K., WooP. C., YipC. C., LiK. S., FuC. T., HuangY., ChanK. H., YuenK. Y.2011; Co-existence of multiple strains of two novel porcine bocaviruses in the same pig, a previously undescribed phenomenon in members of the family Parvoviridae, and evidence for inter- and intra-host genetic diversity and recombination. J Gen Virol 92:2047–2059 [View Article][PubMed]
ManningA., RussellV., EastickK., LeadbetterG. H., HallamN., TempletonK., SimmondsP.2006; Epidemiological profile and clinical associations of human bocavirus and other human parvoviruses. J Infect Dis 194:1283–1290 [View Article][PubMed]
MartinD. P., LemeyP., LottM., MoultonV., PosadaD., LefeuvreP.2010; RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463 [View Article][PubMed]
McKillenJ., McNeillyF., DuffyC., McMenamyM., McNairI., HjertnerB., MillarA., McKayK., LaganP.other authors2011; Isolation in cell cultures and initial characterisation of two novel bocavirus species from swine in Northern Ireland. Vet Microbiol 152:39–45 [View Article][PubMed]
MochizukiM., HashimotoM., HajimaT., TakiguchiM., HashimotoA., UneY., RoerinkF., OhshimaT., ParrishC. R., CarmichaelL. E.2002; Virologic and serologic identification of minute virus of canines (canine parvovirus type 1) from dogs in Japan. J Clin Microbiol 40:3993–3998 [View Article][PubMed]
ParkerJ. S. L., ParrishC. R.1997; Canine parvovirus host range is determined by the specific conformation of an additional region of the capsid. J Virol 71:9214–9222[PubMed]
ParrishC. R., KawaokaY.2005; The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59:553–586 [View Article][PubMed]
SchwartzD., GreenB., CarmichaelL. E., ParrishC. R.2002; The canine minute virus (minute virus of canines) is a distinct parvovirus that is most similar to bovine parvovirus. Virology 302:219–223 [View Article][PubMed]
ShackeltonL. A., ParrishC. R., TruyenU., HolmesE. C.2005; High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci U S A 102:379–384 [View Article][PubMed]
ShanT., LanD., LiL., WangC., CuiL., ZhangW., HuaX., ZhuC., ZhaoW., DelwartE.2011a; Genomic characterization and high prevalence of bocaviruses in swine. PLoS ONE 6:e17292 [View Article][PubMed]
ShanT., LiL., SimmondsP., WangC., MoeserA., DelwartE.2011b; The fecal virome of pigs on a high-density farm. J Virol 85:11697–11708 [View Article][PubMed]
SharpC. P., LeBretonM., KantolaK., NanaA., DiffoJ. D., DjokoC. F., TamoufeU., KiyangJ. A., BabilaT. G.other authors2010; Widespread infection with homologues of human parvoviruses B19, PARV4, and human bocavirus of chimpanzees and gorillas in the wild. J Virol 84:10289–10296 [View Article][PubMed]
TijssenP., Agbandje-McKennaM., AlmendralJ. M., BergoinM., FlegelT. W., HedmanK., KleinschmidtJ., LiY., PintelD. J., others. 2011; Family Parvoviridae
. In Virus Taxonomy9th report of the International Committee on Taxonomy of Viruses pp. 405–425 Edited by KingA. M. Q., AdamsM. J., CarstensE. B., LefkowitzE. J. London: Academic Press;
TijssenP., Agbandje-McKennaM., AlmendralJ. M., BergoinM., FlegelT. W., HedmanK., KleinschmidtJ., LiY., PintelD. J., TattersallP.2011; Family Parvoviridae. in KingA. M. Q., AdamsM. J., CarstensE. B., LefkowitzE. J.(Eds.) Virus Taxonomy. 9th report of the International Committee on Taxonomy of Viruses. Academic Press; London: pp. 405–425 [View Article][PubMed]
XiaoC. T., Giménez-LirolaL., HuangY. W., MengX. J., HalburP. G., OpriessnigT.2012; The prevalence of Torque teno sus virus (TTSuV) is common and increases with the age of growing pigs in the United States. J Virol Methods 183:40–44 [View Article][PubMed]
XiaoC. T., GerberP. F., Giménez-LirolaL. G., HalburP. G., OpriessnigT.2013a; Characterization of porcine parvovirus type 2 (PPV2) which is highly prevalent in the USA. Vet Microbiol 161:325–330 [View Article][PubMed]
XuL., HeX., ZhangD. M., FengF. S., WangZ., GuanL. L., WuJ. H., ZhouR., ZhengB. J.other authors2012; Surveillance and genome analysis of human bocavirus in patients with respiratory infection in Guangzhou, China. PLoS ONE 7:e44876 [View Article][PubMed]