1887

Abstract

Coxsackieviruses (CV) A1, CV-A19 and CV-A22 have historically comprised a distinct phylogenetic clade within (EV) . Several novel serotypes that are genetically similar to these three viruses have been recently discovered and characterized. Here, we report the coding sequence analysis of two genotypes of a previously uncharacterized serotype EV-C113 from Bangladesh and demonstrate that it is most similar to CV-A22 and EV-C116 within the capsid region. We sequenced novel genotypes of CV-A1, CV-A19 and CV-A22 from Bangladesh and observed a high rate of recombination within this group. We also report genomic analysis of the rarely reported EV-C104 circulating in the Gambia in 2009. All available EV-C104 sequences displayed a high degree of similarity within the structural genes but formed two clusters within the non-structural genes. One cluster included the recently reported EV-C117, suggesting an ancestral recombination between these two serotypes. Phylogenetic analysis of all available complete genome sequences indicated the existence of two subgroups within this distinct clade: one has been exclusively recovered from gastrointestinal samples, while the other cluster has been implicated in respiratory disease.

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2013-09-01
2024-12-10
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References

  1. 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]
  2. Benschop K., Minnaar R., Koen G., van Eijk H., Dijkman K., Westerhuis B., Molenkamp R., Wolthers K. 2010; Detection of human enterovirus and human parechovirus (HPeV) genotypes from clinical stool samples: polymerase chain reaction and direct molecular typing, culture characteristics, and serotyping. Diagn Microbiol Infect Dis 68:166–173 [View Article][PubMed]
    [Google Scholar]
  3. Bessaud M., Joffret M. L., Holmblat B., Razafindratsimandresy R., Delpeyroux F. 2011; Genetic relationship between cocirculating Human enteroviruses species C. PLoS ONE 6:e24823 [View Article][PubMed]
    [Google Scholar]
  4. Briese T., Palacios G., Kokoris M., Jabado O., Liu Z., Renwick N., Kapoor V., Casas I., Pozo F.& other authors ( 2005; Diagnostic system for rapid and sensitive differential detection of pathogens. Emerg Infect Dis 11:310–313 [View Article][PubMed]
    [Google Scholar]
  5. Brown B., Oberste M. S., Maher K., Pallansch M. A. 2003; Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 77:8973–8984 [View Article][PubMed]
    [Google Scholar]
  6. Brown B. A., Maher K., Flemister M. R., Naraghi-Arani P., Uddin M., Oberste M. S., Pallansch M. A. 2009; Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. J Gen Virol 90:1713–1723 [View Article][PubMed]
    [Google Scholar]
  7. Chitambar S., Gopalkrishna V., Chhabra P., Patil P., Verma H., Lahon A., Arora R., Tatte V., Ranshing S.& other authors ( 2012; Diversity in the enteric viruses detected in outbreaks of gastroenteritis from Mumbai, Western India. Int J Environ Res Public Health 9:895–915 [View Article][PubMed]
    [Google Scholar]
  8. Combelas N., Holmblat B., Joffret M. L., Colbère-Garapin F., Delpeyroux F. 2011; Recombination between poliovirus and coxsackie A viruses of species C: a model of viral genetic plasticity and emergence. Viruses 3:1460–1484 [View Article][PubMed]
    [Google Scholar]
  9. Daleno C., Piralla A., Scala A., Baldanti F., Usonis V., Principi N., Esposito S. 2012; Complete genome sequence of a novel human enterovirus C (HEV-C117) identified in a child with community-acquired pneumonia. J Virol 86:10888–10889 [View Article][PubMed]
    [Google Scholar]
  10. Daleno C., Greenberg D., Piralla A., Scala A., Baldanti F., Principi N., Esposito S. 2013; A novel human enterovirus C (EV-C118) identified in two children hospitalised because of acute otitis media and community-acquired pneumonia in Israel. J Clin Virol 56:159–162 [View Article][PubMed]
    [Google Scholar]
  11. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. 1989; The major human rhinovirus receptor is ICAM-1. Cell 56:839–847 [View Article][PubMed]
    [Google Scholar]
  12. Harvala H., McIntyre C. L., McLeish N. J., Kondracka J., Palmer J., Molyneaux P., Gunson R., Bennett S., Templeton K., Simmonds P. 2012; High detection frequency and viral loads of human rhinovirus species A to C in fecal samples; diagnostic and clinical implications. J Med Virol 84:536–542 http://www.picornaviridae.com [View Article][PubMed]
    [Google Scholar]
  13. Kaida A., Kubo H., Sekiguchi J., Hase A., Iritani N. 2012; Enterovirus 104 infection in adult, Japan, 2011. Emerg Infect Dis 18:882–883 [View Article][PubMed]
    [Google Scholar]
  14. Kapusinszky B., Szomor K. N., Farkas A., Takács M., Berencsi G. 2010; Detection of non-polio enteroviruses in Hungary 2000-2008 and molecular epidemiology of enterovirus 71, coxsackievirus A16, and echovirus 30. Virus Genes 40:163–173 [View Article][PubMed]
    [Google Scholar]
  15. Khetsuriani N., Lamonte-Fowlkes A., Oberst S., Pallansch M. A.Centers for Disease Control and Prevention 2006; Enterovirus surveillance – United States, 1970-2005. MMWR Surveill Summ 55:1–20[PubMed]
    [Google Scholar]
  16. Knowles N. J., Hovi T., Hyypia T., King A. M. Q., Lindberg A. M., Pallansch M. A., Palmenberg A. C., Simmonds P. et al. 2012; Picornaviridae. In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Edited by King A. M. J. et al. San Diego, CA: Elsevier Academic Press;
    [Google Scholar]
  17. Lipson S. M., Walderman R., Costello P., Szabo K. 1988; Sensitivity of rhabdomyosarcoma and guinea pig embryo cell cultures to field isolates of difficult-to-cultivate group A coxsackieviruses. J Clin Microbiol 26:1298–1303[PubMed]
    [Google Scholar]
  18. Lukashev A. N. 2005; Role of recombination in evolution of enteroviruses. Rev Med Virol 15:157–167 [View Article][PubMed]
    [Google Scholar]
  19. Lukashev A. N., Drexler J. F., Kotova V. O., Amjaga E. N., Reznik V. I., Gmyl A. P., Grard G., Taty Taty R., Trotsenko O. E.& other authors ( 2012; Novel serotypes 105 and 116 are members of distinct subgroups of human enterovirus C. J Gen Virol 93:2357–2362 [View Article][PubMed]
    [Google Scholar]
  20. Mirkovic R. R., Kono R., Yin-Murphy M., Sohier R., Schmidt N. J., Melnick J. L. 1973; Enterovirus type 70: the etiologic agent of pandemic acute haemorrhagic conjunctivitis. Bull World Health Organ 49:341–346[PubMed]
    [Google Scholar]
  21. Oberste M. S., Maher K., Kilpatrick D. R., Pallansch M. A. 1999a; Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948[PubMed]
    [Google Scholar]
  22. Oberste M. S., Maher K., Kilpatrick D. R., Flemister M. R., Brown B. A., Pallansch M. A. 1999b; Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 37:1288–1293[PubMed]
    [Google Scholar]
  23. Oberste M. S., Maher K., Pallansch M. A. 2004a; Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78:855–867 [View Article][PubMed]
    [Google Scholar]
  24. Oberste M. S., Peñaranda S., Maher K., Pallansch M. A. 2004b; Complete genome sequences of all members of the species Human enterovirus A. J Gen Virol 85:1597–1607 [View Article][PubMed]
    [Google Scholar]
  25. 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]
  26. Piralla A., Lilleri D., Sarasini A., Marchi A., Zecca M., Stronati M., Baldanti F., Gerna G. 2012; Human rhinovirus and human respiratory enterovirus (EV68 and EV104) infections in hospitalized patients in Italy, 2008-2009. Diagn Microbiol Infect Dis 73:162–167 [View Article][PubMed]
    [Google Scholar]
  27. Santti J., Hyypiä T., Kinnunen L., Salminen M. 1999; Evidence of recombination among enteroviruses. J Virol 73:8741–8749[PubMed]
    [Google Scholar]
  28. Schieble J. H., Fox V. L., Lennette E. H. 1967; A probable new human picornavirus associated with respiratory diseases. Am J Epidemiol 85:297–310[PubMed]
    [Google Scholar]
  29. Schmidt N. J., Ho H. H., Lennette E. H. 1975; Propagation and isolation of group A coxsackieviruses in RD cells. J Clin Microbiol 2:183–185[PubMed]
    [Google Scholar]
  30. Simmonds P., Welch J. 2006; Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80:483–493 [View Article][PubMed]
    [Google Scholar]
  31. Smura T., Blomqvist S., Paananen A., Vuorinen T., Sobotová Z., Bubovica V., Ivanova O., Hovi T., Roivainen M. 2007; Enterovirus surveillance reveals proposed new serotypes and provides new insight into enterovirus 5′-untranslated region evolution. J Gen Virol 88:2520–2526 [View Article][PubMed]
    [Google Scholar]
  32. Sun Q., Zhang Y., Zhu S., Cui H., Tian H., Yan D., Huang G., Zhu Z., Wang D.& other authors ( 2012; Complete genome sequence of two coxsackievirus A1 strains that were cytotoxic to human rhabdomyosarcoma cells. J Virol 86:10228–10229 [View Article][PubMed]
    [Google Scholar]
  33. Tamura K., Dudley J., Nei M., Kumar S. 2007; MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  34. Tapparel C., Junier T., Gerlach D., Van-Belle S., Turin L., Cordey S., Mühlemann K., Regamey N., Aubert J. D.& other authors ( 2009; New respiratory enterovirus and recombinant rhinoviruses among circulating picornaviruses. Emerg Infect Dis 15:719–726 [View Article][PubMed]
    [Google Scholar]
  35. Tapparel C., Siegrist F., Petty T. J., Kaiser L. 2013; Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 14:282–293 [View Article][PubMed]
    [Google Scholar]
  36. Tokarz R., Kapoor V., Wu W., Lurio J., Jain K., Mostashari F., Briese T., Lipkin W. I. 2011; Longitudinal molecular microbial analysis of influenza-like illness in New York City, May 2009 through May 2010. Virol J 8:288 [View Article][PubMed]
    [Google Scholar]
  37. Tokarz R., Firth C., Madhi S. A., Howie S. R., Wu W. Y., Sall A. A., Haq S., Briese T., Lipkin W. I. 2012; Worldwide emergence of multiple clades of enterovirus 68. J Gen Virol 93:1952–1958 [View Article][PubMed]
    [Google Scholar]
  38. Tokarz R., Hirschberg D. L., Sameroff S., Haq S., Luna G., Bennett A. J., Silva M., Leguia M., Kasper M.& other authors ( 2013; Genomic analysis of two novel human enterovirus C genotypes found in respiratory samples from Peru. J Gen Virol 94:120–127 [View Article][PubMed]
    [Google Scholar]
  39. Witsø E., Palacios G., Cinek O., Stene L. C., Grinde B., Janowitz D., Lipkin W. I., Rønningen K. S. 2006; High prevalence of human enterovirus a infections in natural circulation of human enteroviruses. J Clin Microbiol 44:4095–4100 [View Article][PubMed]
    [Google Scholar]
  40. Xiang Z., Gonzalez R., Wang Z., Ren L., Xiao Y., Li J., Li Y., Vernet G., Paranhos-Baccalà G.& other authors ( 2012; Coxsackievirus A21, enterovirus 68, and acute respiratory tract infection, China. Emerg Infect Dis 18:821–824 [View Article][PubMed]
    [Google Scholar]
  41. Xiao C., Bator C. M., Bowman V. D., Rieder E., He Y., Hébert B., Bella J., Baker T. S., Wimmer E.& other authors ( 2001; Interaction of coxsackievirus A21 with its cellular receptor, ICAM-1. J Virol 75:2444–2451 [View Article][PubMed]
    [Google Scholar]
  42. Yip C. C., Lau S. K., Woo P. C., Chan K. H., Yuen K. Y. 2011; Complete genome sequence of a coxsackievirus A22 strain in Hong Kong reveals a natural intratypic recombination event. J Virol 85:12098–12099 [View Article][PubMed]
    [Google Scholar]
  43. Yozwiak N. L., Skewes-Cox P., Gordon A., Saborio S., Kuan G., Balmaseda A., Ganem D., Harris E., DeRisi J. L. 2010; Human enterovirus 109: a novel interspecies recombinant enterovirus isolated from a case of acute pediatric respiratory illness in Nicaragua. J Virol 84:9047–9058 [View Article][PubMed]
    [Google Scholar]
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