1887

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Volume 94, Issue 9

Diversity of picornaviruses in rural Bolivia Free

Abstract

The family is a large and diverse group of viruses that infect humans and animals. Picornaviruses are among the most common infections of humans and cause a wide spectrum of acute human disease. This study began as an investigation of acute flaccid paralysis (AFP) in a small area of eastern Bolivia, where surveillance had identified a persistently high AFP rate in children. Stools were collected and diagnostic studies ruled out poliovirus. We tested stool specimens from 51 AFP cases and 34 healthy household or community contacts collected during 2002–2003 using real-time and semi-nested reverse transcription polymerase chain reaction assays for enterovirus, parechovirus, cardiovirus, kobuvirus, salivirus and cosavirus. Anecdotal reports suggested a temporal association with neurological disease in domestic pigs, so six porcine stools were also collected and tested with the same set of assays, with the addition of an assay for porcine teschovirus. A total of 126 picornaviruses were detected in 73 of 85 human individuals, consisting of 53 different picornavirus types encompassing five genera (all except ). All six porcine stools contained porcine and/or human picornaviruses. No single virus, or combination of viruses, specifically correlated with AFP; however, the study revealed a surprising complexity of enteric picornaviruses in a single community.

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© Microbiology Society
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2013-09-01
2024-04-16
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References

  1. Abed Y., Boivin G. 2008; New Saffold cardioviruses in 3 children, Canada. Emerg Infect Dis 14:834–836 [View Article][PubMed]
     [Google Scholar]
  2. Adams M. J., King A. M., Carstens E. B. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2013). Arch Virol (In Press) [View Article][PubMed]
     [Google Scholar]
  3. Anonymous 2006; Poliomyelitis eradication field guide. Washington, DC: Pan American Health Organization; http://www1.paho.org/english/ad/fch/im/fieldguide_polio.pdf Accessed 11 June 2012
    [Google Scholar]
  4. Anonymous. 2011; Porcine enteroviral encephalomyelitis (Teschen disease, Talfan disease, porcine polioencephalomyelitis).. In The Merck Veterinary Manual. Edited by Kahn C. M. Whitehouse Station, NJ: Merck Sharp & Dohme;
     [Google Scholar]
  5. Anonymous 2012a; Bolivia/Aujeszky's disease. Multiannual animal disease status. Paris: World Organization for Animal Health; http://web.oie.int/hs2/sit_pays_mald_pl.asp?c_pays=25&c_mald=21 Accessed 16 January 2013
    [Google Scholar]
  6. Anonymous 2012b; Bolivia/classical swine fever. Multiannual animal disease status. Paris: World Organization for Animal Health; http://web.oie.int/hs2/sit_pays_mald_pl.asp?c_pays=25&c_mald=14 Accessed 16 January 2013
    [Google Scholar]
  7. Begier E. M., Oberste M. S., Landry M. L., Brennan T., Mlynarski D., Mshar P. A., Frenette K., Rabatsky-Ehr T., Purviance K.& other authors ( 2008; An outbreak of concurrent echovirus 30 and coxsackievirus A1 infections associated with sea swimming among a group of travelers to Mexico. Clin Infect Dis 47:616–623 [View Article][PubMed]
     [Google Scholar]
  8. Benschop K., Thomas X., Serpenti C., Molenkamp R., Wolthers K. C. 2008; High prevalence of human Parechovirus (HPeV) genotypes in the Amsterdam region and identification of specific HPeV variants by direct genotyping of stool samples. J Clin Microbiol 46:3965–3970 [View Article][PubMed]
     [Google Scholar]
  9. Bingjun T., Yoshida H., Yan W., Lin L., Tsuji T., Shimizu H., Miyamura T. 2008; Molecular typing and epidemiology of non-polio enteroviruses isolated from Yunnan Province, the People’s Republic of China. J Med Virol 80:670–679 [View Article][PubMed]
     [Google Scholar]
  10. Blinkova O., Kapoor A., Victoria J., Jones M., Wolfe N., Naeem A., Shaukat S., Sharif S., Alam M. M.& other authors ( 2009; Cardioviruses are genetically diverse and cause common enteric infections in South Asian children. J Virol 83:4631–4641 [View Article][PubMed]
     [Google Scholar]
  11. Blomqvist S., Bruu A.-L., Stenvik M., Hovi T. 2003; Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol 84:573–580 [View Article][PubMed]
     [Google Scholar]
  12. Blomqvist S., Savolainen-Kopra C., Paananen A., El Bassioni L., El Maamoon Nasr E. M., Firstova L., Zamiatina N., Kutateladze T., Roivainen M. 2010; Recurrent isolation of poliovirus 3 strains with chimeric capsid protein Vp1 suggests a recombination hot-spot site in Vp1. Virus Res 151:246–251 [View Article][PubMed]
     [Google Scholar]
  13. Chiu C. Y., Greninger A. L., Kanada K., Kwok T., Fischer K. F., Runckel C., Louie J. K., Glaser C. A., Yagi S.& other authors ( 2008; Identification of cardioviruses related to Theiler’s murine encephalomyelitis virus in human infections. Proc Natl Acad Sci U S A 105:14124–14129 [View Article][PubMed]
     [Google Scholar]
  14. Czechowicz J., Huaman J. L., Forshey B. M., Morrison A. C., Castillo R., Huaman A., Caceda R., Eza D., Rocha C.& other authors ( 2011; Prevalence and risk factors for encephalomyocarditis virus infection in Peru. Vector Borne Zoonotic Dis 11:367–374 [View Article][PubMed]
     [Google Scholar]
  15. Drexler J. F., Luna L. K., Stöcker A., Almeida P. S., Ribeiro T. C., Petersen N., Herzog P., Pedroso C., Huppertz H. I.& other authors ( 2008; Circulation of 3 lineages of a novel Saffold cardiovirus in humans. Emerg Infect Dis 14:1398–1405 [View Article][PubMed]
     [Google Scholar]
  16. Drexler J. F., Baumgarte S., Eschbach-Bludau M., Simon A., Kemen C., Bode U., Eis-Hübinger A.-M., Madea B., Drosten C. 2011; Human cardioviruses, meningitis, and sudden infant death syndrome in children. Emerg Infect Dis 17:2313–2315 [View Article][PubMed]
     [Google Scholar]
  17. Greninger A. L., Runckel C., Chiu C. Y., Haggerty T., Parsonnet J., Ganem D., DeRisi J. L. 2009; The complete genome of klassevirus – a novel picornavirus in pediatric stool. Virol J 6:82 [View Article][PubMed]
     [Google Scholar]
  18. Harvala H., Wolthers K. C., Simmonds P. 2010; Parechoviruses in children: understanding a new infection. Curr Opin Infect Dis 23:224–230 [View Article][PubMed]
     [Google Scholar]
  19. Holtz L. R., Finkbeiner S. R., Kirkwood C. D., Wang D. 2008; Identification of a novel picornavirus related to cosaviruses in a child with acute diarrhea. Virol J 5:159 [View Article][PubMed]
     [Google Scholar]
  20. Itagaki T., Abiko C., Ikeda T., Aoki Y., Seto J., Mizuta K., Ahiko T., Tsukagoshi H., Nagano M.& other authors ( 2010; Sequence and phylogenetic analyses of Saffold cardiovirus from children with exudative tonsillitis in Yamagata, Japan. Scand J Infect Dis 42:950–952 [View Article][PubMed]
     [Google Scholar]
  21. Jones D. T., Taylor W. R., Thornton J. M. 1992; The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282[PubMed]
     [Google Scholar]
  22. Jones M. S., Lukashov V. V., Ganac R. D., Schnurr D. P. 2007; Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J Clin Microbiol 45:2144–2150 [View Article][PubMed]
     [Google Scholar]
  23. Junttila N., Lévêque N., Kabue J. P., Cartet G., Mushiya F., Muyembe-Tamfum J. J., Trompette A., Lina B., Magnius L. O.& other authors ( 2007; New enteroviruses, EV-93 and EV-94, associated with acute flaccid paralysis in the Democratic Republic of the Congo. J Med Virol 79:393–400 [View Article][PubMed]
     [Google Scholar]
  24. Kapoor A., Ayyagari A., Dhole T. N. 2001; Non-polio enteroviruses in acute flaccid paralysis. Indian J Pediatr 68:927–929 [View Article][PubMed]
     [Google Scholar]
  25. Kapoor A., Victoria J., Simmonds P., Slikas E., Chieochansin T., Naeem A., Shaukat S., Sharif S., Alam M. M.& other authors ( 2008; A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc Natl Acad Sci U S A 105:20482–20487 [View Article][PubMed]
     [Google Scholar]
  26. Kilpatrick D. R., Yang C.-F., Ching K., Vincent A., Iber J., Campagnoli R., Mandelbaum M., De L., Yang S.-J.& other authors ( 2009; Rapid group-, serotype-, and vaccine strain-specific identification of poliovirus isolates by real-time reverse transcription-PCR using degenerate primers and probes containing deoxyinosine residues. J Clin Microbiol 47:1939–1941 [View Article][PubMed]
     [Google Scholar]
  27. Knowles N. J., Hovi T., Hyypiä T., King A. M. Q., Lindberg A. M., Pallansch M. A., Palmenberg A. C., Skern T., Stanway G.& other authors ( 2012; Picornaviridae. In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses pp. 855–880 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. San Diego: Elsevier;
     [Google Scholar]
  28. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; mega2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245 [View Article][PubMed]
     [Google Scholar]
  29. Martínez H. R., Bermudez M. V., Rangel-Guerra R. A., de Leon Flores L. 1998; Clinical diagnosis in Karwinskia humboldtiana polyneuropathy. J Neurol Sci 154:49–54 [View Article][PubMed]
     [Google Scholar]
  30. Maurice H., Nielen M., Brocchi E., Nowotny N., Bakkali, Kassimi L., Billinis C., Loukaides P., O’Hara R. S., Koenen F. 2005; The occurrence of encephalomyocarditis virus (EMCV) in European pigs from 1990 to 2001. Epidemiol Infect 133:547–557 [View Article][PubMed]
     [Google Scholar]
  31. Ng T. F., Marine R., Wang C., Simmonds P., Kapusinszky B., Bodhidatta L., Oderinde B. S., Wommack K. E., Delwart E. 2012; High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J Virol 86:12161–12175 [View Article][PubMed]
     [Google Scholar]
  32. Nielsen A. C., Böttiger B., Banner J., Hoffmann T., Nielsen L. P. 2012; Serious invasive Saffold virus infections in children, 2009. Emerg Infect Dis 18:7–12 doi:10.3201/eid1801.110725[PubMed]
     [Google Scholar]
  33. Nix W. A., Oberste M. S., Pallansch M. A. 2006; Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 44:2698–2704 [View Article][PubMed]
     [Google Scholar]
  34. Nix W. A., Maher K., Johansson E. S., Niklasson B., Lindberg A. M., Pallansch M. A., Oberste M. S. 2008; Detection of all known parechoviruses by real-time PCR. J Clin Microbiol 46:2519–2524 [View Article][PubMed]
     [Google Scholar]
  35. Nix W. A., Maher K., Pallansch M. A., Oberste M. S. 2010; Parechovirus typing in clinical specimens by nested or semi-nested PCR coupled with sequencing. J Clin Virol 48:202–207 [View Article][PubMed]
     [Google Scholar]
  36. Oberste M. S., Maher K., Williams A. J., Dybdahl-Sissoko N., Brown B. A., Gookin M. S., Peñaranda S., Mishrik N., Uddin M., Pallansch M. A. 2006; Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. J Gen Virol 87:119–128 [View Article][PubMed]
     [Google Scholar]
  37. Oberste M. S., Gotuzzo E., Blair P. J., Nix W. A., Ksiazek T. G., Comer J. A., Rollin P., Goldsmith C. A., Olson J., Kochel T. J. 2009; Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerg Infect Dis 15:640–646 [View Article][PubMed]
     [Google Scholar]
  38. Oberste M. S., Feeroz M. M., Maher K., Nix W. A., Engel G. A., Hasan K. M., Begum S., Oh G., Chowdhury A. H.& other authors ( 2013; Characterizing the picornavirus landscape among synanthropic nonhuman primates in Bangladesh, 2007 to 2008. J Virol 87:558–571 [View Article][PubMed]
     [Google Scholar]
  39. Ocampo-Roosens L. V., Ontiveros-Nevares P. G., Fernández-Lucio O. 2007; Intoxication with buckthorn (Karwinskia humboldtiana): report of three siblings. Pediatr Dev Pathol 10:66–68 [View Article][PubMed]
     [Google Scholar]
  40. Saeed M., Zaidi S. Z., Naeem A., Masroor M., Sharif S., Shaukat S., Angez M., Khan A. 2007; Epidemiology and clinical findings associated with enteroviral acute flaccid paralysis in Pakistan. BMC Infect Dis 7:6 [View Article][PubMed]
     [Google Scholar]
  41. Santos A. P., Costa E. V., Oliveira S. S., Souza M. C., Da Silva E. E. 2002; RT-PCR based analysis of cell culture negative stools samples from poliomyelitis suspected cases. J Clin Virol 23:149–152 [View Article][PubMed]
     [Google Scholar]
  42. Serrano M., Terán J. 2000 Identificación de Especies Vegetales en Chuquisaca – Teoría, Práctica y Resultados Sucre, Bolivia: PLAFOR, Intercooperación, Fundación Ceibo;
     [Google Scholar]
  43. Shoja Z. O., Tabatabai H., Sarijloo M., Shahmahmoodi S., Azad T. M., Nategh R. 2007; Detection of enteroviruses by reverse-transcriptase polymerase chain reaction in cell culture negative stool specimens of patients with acute flaccid paralysis. J Virol Methods 142:95–97 [View Article][PubMed]
     [Google Scholar]
  44. Victoria J. G., Kapoor A., Li L., Blinkova O., Slikas B., Wang C., Naeem A., Zaidi S., Delwart E. 2009; Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83:4642–4651 [View Article][PubMed]
     [Google Scholar]
  45. World Organization for Animal Health 2012; World Animal Health Information Database. http://www.oie.int/wahis_2/public/wahid.php/Wahidhome/Home
  46. Zell R., Krumbholz A., Henke A., Birch-Hirschfeld E., Stelzner A., Doherty M., Hoey E., Dauber M., Prager D., Wurm R. 2000; Detection of porcine enteroviruses by nRT-PCR: differentiation of CPE groups I-III with specific primer sets. J Virol Methods 88:205–218 [View Article][PubMed]
     [Google Scholar]
  47. Zoll J., Erkens Hulshof S., Lanke K., Verduyn Lunel F., Melchers W. J. G., Schoondermark-van de Ven E., Roivainen M., Galama J. M. D., van Kuppeveld F. J. M. 2009; Saffold virus, a human Theiler’s-like cardiovirus, is ubiquitous and causes infection early in life. PLoS Pathog 5:e1000416 [View Article][PubMed]
     [Google Scholar]
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Diversity of picornaviruses in rural Bolivia
J. Gen. Virol. 94, 2017 (2013); https://doi.org/10.1099/vir.0.053827-0
/content/journal/jgv/10.1099/vir.0.053827-0
/content/journal/jgv/10.1099/vir.0.053827-0
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