1887

Abstract

A recent survey of pigs in Dong Thap province, Vietnam identified a high frequency of enterovirus species G (EV-G) infection (144/198; 72.7 %). Amongst these was a plethora of EV-G types (EV-G1, EV-G6 and four new types EV-G8–EV-G11). To better characterize the genetic diversity of EV-G and investigate the possible existence of further circulating types, we performed a larger-scale study on 484 pig and 45 farm-bred boar faecal samples collected in 2012 and 2014, respectively. All samples from the previous and current studies were also screened for kobuviruses. The overall EV infection frequency remained extremely high (395/484; 81.6 %), but with comparable detection rates and viral loads between healthy and diarrhoeic pigs; this contrasted with less frequent detection of EV-G in boars (4/45; 8.9 %). EV was most frequently detected in pigs ≤ 14 weeks old (∼95 %) and declined in older pigs. Infections with EV-G1 and EV-G6 were most frequent, whilst less commonly detected types included EV-G3, EV-G4 and EV-G8–EV-G11, and five new types (EV-G12–EV-G16). In contrast, kobuvirus infection frequency was significantly higher in diarrhoeic pigs (40.9 versus 27.6 %;  = 0.01). Kobuviruses also showed contrasting epizootiologies and age associations; a higher prevalence was found in boars (42 %) compared with domestic pigs (29 %), with the highest infection frequency amongst pigs >52 weeks old. Although genetically diverse, all kobuviruses identified belonged to the species . In summary, this study confirms infection with EV-G was endemic in Vietnamese domestic pigs and exhibits high genetic diversity and extensive inter-type recombination.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000366
2016-02-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/2/378.html?itemId=/content/journal/jgv/10.1099/jgv.0.000366&mimeType=html&fmt=ahah

References

  1. Alexandersen S., Donaldson A. I.. 2002; Further studies to quantify the dose of natural aerosols of foot-and-mouth disease virus for pigs. Epidemiol Infect128:313–323[PubMed]
    [Google Scholar]
  2. Alexandersen S., Zhang Z., Donaldson A. I.. 2002; Aspects of the persistence of foot-and-mouth disease virus in animals - the carrier problem. Microbes Infect4:1099–1110 [CrossRef][PubMed]
    [Google Scholar]
  3. Amimo J. O., Okoth E., Junga J. O., Ogara W. O., Njahira M. N., Wang Q., Vlasova A. N., Saif L. J., Djikeng A.. 2014; Molecular detection and genetic characterization of kobuviruses and astroviruses in asymptomatic local pigs in East Africa. Arch Virol159:1313–1319 [CrossRef][PubMed]
    [Google Scholar]
  4. Barry A. F., Ribeiro J., Alfieri A. F., van der Poel W. H. M., Alfieri A. A.. 2011; First detection of kobuvirus in farm animals in Brazil and the Netherlands. Infect Genet Evol11:1811–1814 [CrossRef][PubMed]
    [Google Scholar]
  5. Beld M., Minnaar R., Weel J., Sol C., Damen M., van der Avoort H., Wertheim-van Dillen P., van Breda A., Boom R.. 2004; Highly sensitive assay for detection of enterovirus in clinical specimens by reverse transcription-PCR with an armored RNA internal control. J Clin Microbiol42:3059–3064 [CrossRef][PubMed]
    [Google Scholar]
  6. Boros Á., Pankovics P., Reuter G.. 2011; Characterization of a novel porcine enterovirus in domestic pig in Hungary. Infect Genet Evol11:1096–1102 [CrossRef][PubMed]
    [Google Scholar]
  7. Boros A., Nemes C., Pankovics P., Bíró H., Kapusinszky B., Delwart E., Reuter G.. 2012a; Characterization of a novel porcine enterovirus in wild boars in Hungary. Arch Virol157:981–986 [CrossRef][PubMed]
    [Google Scholar]
  8. Boros A., Pankovics P., Knowles N. J., Reuter G.. 2012b; Natural interspecies recombinant bovine/porcine enterovirus in sheep. J Gen Virol93:1941–1951 [CrossRef][PubMed]
    [Google Scholar]
  9. Buitrago D., Cano-Gómez C., Agüero M., Fernandez-Pacheco P., Gómez-Tejedor C., Jiménez-Clavero M.Á.. 2010; A survey of porcine picornaviruses and adenoviruses in fecal samples in Spain. J Vet Diagn Invest22:763–766 [CrossRef][PubMed]
    [Google Scholar]
  10. Chen L., Zhu L., Zhou Y. C., Xu Z. W., Guo W. Z., Yang W. Y.. 2013; Molecular and phylogenetic analysis of the porcine kobuvirus VP1 region using infected pigs from Sichuan Province, China. Virol J10:281 [CrossRef][PubMed]
    [Google Scholar]
  11. Davis M., Sagan S. M., Pezacki J. P., Evans D. J., Simmonds P.. 2008; Bioinformatic and physical characterizations of genome-scale ordered RNA structure in mammalian RNA viruses. J Virol82:11824–11836 [CrossRef][PubMed]
    [Google Scholar]
  12. Di Bartolo I., Angeloni G., Tofani S., Monini M., Ruggeri F. M.. 2015; Infection of farmed pigs with porcine kobuviruses in Italy. Arch Virol160:1533–1536 [CrossRef][PubMed]
    [Google Scholar]
  13. Fan S., Sun H., Ying Y., Gao X., Wang Z., Yu Y., Li Y., Wang T., Yu Z., other authors. 2013; Identification and characterization of porcine kobuvirus variant isolated from suckling piglet in Gansu province, China. Viruses5:2548–2560 [CrossRef][PubMed]
    [Google Scholar]
  14. Frémont M., Coomans D., Massart S., De Meirleir K.. 2013; High-throughput 16S rRNA gene sequencing reveals alterations of intestinal microbiota in myalgic encephalomyelitis/chronic fatigue syndrome patients. Anaerobe22:50–56 [CrossRef][PubMed]
    [Google Scholar]
  15. Inaba M., Katayama H., Tran N. V. T., Furuami H.. 2014; Detection of genus Kobuvirus for evaluation as virus indicator for fecal contamination source track from Nhue River in Hanoi, Vietnam. In Southeast Asian Water Environment 5 pp61–66Edited by Yamamoto H., Furumai H., Katayama H., Chiemchaisri C., Puetpaiboon U., Visvanathan C., Satoh H.. London: IWA Publishing;
    [Google Scholar]
  16. Kaku Y., Sarai A., Murakami Y.. 2001; Genetic reclassification of porcine enteroviruses. J Gen Virol82:417–424 [CrossRef][PubMed]
    [Google Scholar]
  17. Khamrin P., Maneekarn N., Kongkaew A., Kongkaew S., Okitsu S., Ushijima H.. 2009; Porcine kobuvirus in piglets, Thailand. Emerg Infect Dis15:2075–2076 [CrossRef][PubMed]
    [Google Scholar]
  18. Khamrin P., Maneekarn N., Hidaka S., Kishikawa S., Ushijima K., Okitsu S., Ushijima H.. 2010; Molecular detection of kobuvirus sequences in stool samples collected from healthy pigs in Japan. Infect Genet Evol10:950–954 [CrossRef][PubMed]
    [Google Scholar]
  19. Knowles N. J.. 1988; The association of group III porcine enteroviruses with epithelial tissue. Vet Rec122:441–442 [CrossRef][PubMed]
    [Google Scholar]
  20. Knowles N. J.. 2006; Porcine enteric picornaviruses. In Diseases of Swine pp337–345Edited by Straw B. E., Zimmermann J. J., D'Allaine S. D., Taylor D. J.. Ames, IA: Blackwell;
    [Google Scholar]
  21. Krumbholz A., Dauber M., Henke A., Birch-Hirschfeld E., Knowles N. J., Stelzner A., Zell R.. 2002; Sequencing of porcine enterovirus groups II and III reveals unique features of both virus groups. J Virol76:5813–5821 [CrossRef][PubMed]
    [Google Scholar]
  22. McIntyre C. L., Knowles N. J., Simmonds P.. 2013; Proposals for the classification of human rhinovirus species A, B and C into genotypically assigned types. J Gen Virol94:1791–1806 [CrossRef][PubMed]
    [Google Scholar]
  23. McLeish N. J., Witteveldt J., Clasper L., McIntyre C., McWilliam Leitch E. C., Hardie A., Bennett S., Gunson R., Carman W. F., other authors. 2012; Development and assay of RNA transcripts of enterovirus species A to D, rhinovirus species a to C, and human parechovirus: assessment of assay sensitivity and specificity of real-time screening and typing methods. J Clin Microbiol50:2910–2917 [CrossRef][PubMed]
    [Google Scholar]
  24. Moon H. J., Song D., Seon B. H., Kim H. K., Park S. J., An D. J., Kim J. M., Kang B. K., Park B. K.. 2012; Complete genome analysis of porcine enterovirus B isolated in Korea. J Virol86:10250 [CrossRef][PubMed]
    [Google Scholar]
  25. Oberste M. S., Maher K., Kilpatrick D. R., Pallansch M. A.. 1999; Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol73:1941–1948[PubMed]
    [Google Scholar]
  26. Oberste M. S., Peñaranda S., Pallansch M. A.. 2004; RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol78:2948–2955 [CrossRef][PubMed]
    [Google Scholar]
  27. Okitsu S., Khamrin P., Thongprachum A., Hidaka S., Kongkaew S., Kongkaew A., Maneekarn N., Mizuguchi M., Hayakawa S., Ushijima H.. 2012; Sequence analysis of porcine kobuvirus VP1 region detected in pigs in Japan and Thailand. Virus Genes44:253–257 [CrossRef][PubMed]
    [Google Scholar]
  28. Park S.-J., Kim H.-K., Moon H.-J., Song D.-S., Rho S.-M., Han J.-Y., Nguyen V.-G., Park B.-K.. 2010; Molecular detection of porcine kobuviruses in pigs in Korea and their association with diarrhea. Arch Virol155:1803–1811 [CrossRef][PubMed]
    [Google Scholar]
  29. Prodělalová J.. 2012; The survey of porcine teschoviruses, sapeloviruses and enteroviruses B infecting domestic pigs and wild boars in the Czech Republic between 2005 and 2011. Infect Genet Evol12:1447–1451 [CrossRef][PubMed]
    [Google Scholar]
  30. Reuter G., Boldizsár A., Kiss I., Pankovics P.. 2008; Candidate new species of Kobuvirus in porcine hosts. Emerg Infect Dis14:1968–1970 [CrossRef][PubMed]
    [Google Scholar]
  31. Reuter G., Nemes C., Boros A., Kapusinszky B., Delwart E., Pankovics P.. 2013; Porcine kobuvirus in wild boars (Sus scrofa). Arch Virol158:281–282 [CrossRef][PubMed]
    [Google Scholar]
  32. Simmonds P.. 2006; Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J Virol80:11124–11140 [CrossRef][PubMed]
    [Google Scholar]
  33. Simmonds P.. 2012; sse: a nucleotide and amino acid sequence analysis platform. BMC Res Notes5:50 [CrossRef][PubMed]
    [Google Scholar]
  34. Simmonds P., Midgley S.. 2005; Recombination in the genesis and evolution of hepatitis B virus genotypes. J Virol79:15467–15476 [CrossRef][PubMed]
    [Google Scholar]
  35. Simmonds P., Tuplin A., Evans D. J.. 2004; Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: Implications for virus evolution and host persistence. RNA10:1337–1351 [CrossRef][PubMed]
    [Google Scholar]
  36. Sisay Z., Wang Q., Oka T., Saif L.. 2013; Prevalence and molecular characterization of porcine enteric caliciviruses and first detection of porcine kobuviruses in US swine. Arch Virol158:1583–1588 [CrossRef][PubMed]
    [Google Scholar]
  37. Sozzi E., Barbieri I., Lavazza A., Lelli D., Moreno A., Canelli E., Bugnetti M., Cordioli P.. 2010; Molecular characterization and phylogenetic analysis of VP1 of porcine enteric picornaviruses isolates in Italy. Transbound Emerg Dis57:434–442 [CrossRef][PubMed]
    [Google Scholar]
  38. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  39. Van Dung N., Anh P. H., Van Cuong N., Hoa N. T., Carrique-Mas J., Hien V. B., Campbell J., Baker S., Farrar J., other authors. 2014; Prevalence, genetic diversity and recombination of species G enteroviruses infecting pigs in Vietnam. J Gen Virol95:549–556 [CrossRef][PubMed]
    [Google Scholar]
  40. Wang T. H., Donaldson Y. K., Brettle R. P., Bell J. E., Simmonds P.. 2001; Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. J Virol75:11686–11699 [CrossRef][PubMed]
    [Google Scholar]
  41. Yang S., Wang Y., Shen Q., Zhang W., Hua X.. 2013; Prevalence of porcine enterovirus 9 in pigs in middle and eastern China. Virol J10:99 [CrossRef][PubMed]
    [Google Scholar]
  42. Zell R., Dauber M., Krumbholz A., Henke A., Birch-Hirschfeld E., Stelzner A., Prager D., Wurm R.. 2001; Porcine teschoviruses comprise at least eleven distinct serotypes: molecular and evolutionary aspects. J Virol75:1620–1631 [CrossRef][PubMed]
    [Google Scholar]
  43. Zhang W., Yang S., Shen Q., Ren L., Shan T., Wei J., Cui L., Hua X.. 2012; Complete genome sequence of a novel porcine enterovirus strain in China. J Virol86:7008–7009 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000366
Loading
/content/journal/jgv/10.1099/jgv.0.000366
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error