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Abstract

Human parechoviruses (HPeVs) are highly prevalent RNA viruses classified in the family . Several antigenically distinct types circulate in human populations worldwide, whilst recombination additionally contributes to the genetic heterogeneity of the virus. To investigate factors influencing the likelihood of recombination and to compare its dynamics among types, 154 variants collected from four widely geographically separated referral centres (UK, The Netherlands, Thailand and Brazil) were typed by VP3/VP1 amplification/sequencing with recombination groups assigned by analysis of 3Dpol sequences. HPeV1B and HPeV3 were the most frequently detected types in each referral region, but with marked geographical differences in the frequencies of different recombinant forms (RFs) of types 1B, 5 and 6. HPeV1B showed more frequent recombination than HPeV3, in terms both of evolutionary divergence and of temporal/geographical indicators of population separation. HPeV1 variants showing between 10 and 20 % divergence in VP3/VP1 almost invariably fell into different recombination groups, compared with only one-third of similarly divergent HPeV3 variants. Substitution rates calculated by in the VP3/VP1 region of HPeV1 and HPeV3 allowed half-lives of the RFs of 4 and 20 years, respectively, to be calculated, estimates fitting closely with their observed lifespans based on population sampling. The variability in recombination dynamics between HPeV1B and HPeV3 offers an intriguing link with their markedly different seasonal patterns of transmission, age distributions of infection and clinical outcomes. Future investigation of the epidemiological and biological opportunities and constraints on intertypic recombination will provide more information about its influence on the longer term evolution and pathogenicity of parechoviruses.

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2010-05-01
2019-11-21
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References

  1. Abed, Y. & Boivin, G. ( 2005; ). Molecular characterization of a Canadian human parechovirus (HPeV)-3 isolate and its relationship to other HPeVs. J Med Virol 77, 566–570.[CrossRef]
    [Google Scholar]
  2. Abed, Y. & Boivin, G. ( 2006; ). Human parechovirus types 1, 2 and 3 infections in Canada. Emerg Infect Dis 12, 969–975.[CrossRef]
    [Google Scholar]
  3. Al Sunaidi, M., Williams, C. H., Hughes, P. J., Schnurr, D. P. & Stanway, G. ( 2007; ). Analysis of a new human parechovirus allows the definition of parechovirus types and the identification of RNA structural domains. J Virol 81, 1013–1021.[CrossRef]
    [Google Scholar]
  4. Bailly, J. L., Mirand, A., Henquell, C., Archimbaud, C., Chambon, M., Charbonne, F., Traore, O. & Peigue-Lafeuille, H. ( 2009; ). Phylogeography of circulating populations of human echovirus 30 over 50 years: nucleotide polymorphism and signature of purifying selection in the VP1 capsid protein gene. Infect Genet Evol 9, 699–708.[CrossRef]
    [Google Scholar]
  5. Benschop, K. S., Schinkel, J., Luken, M. E., van den Broek, P. J., Beersma, M. F., Menelik, N., van Eijk, H. W., Zaaijer, H. L., VandenBroucke-Grauls, C. M. & other authors ( 2006a; ). Fourth human parechovirus serotype. Emerg Infect Dis 12, 1572–1575.[CrossRef]
    [Google Scholar]
  6. Benschop, K. S., Schinkel, J., Minnaar, R. P., Pajkrt, D., Spanjerberg, L., Kraakman, H. C., Berkhout, B., Zaaijer, H. L., Beld, M. G. & Wolthers, K. C. ( 2006b; ). Human parechovirus infections in Dutch children and the association between serotype and disease severity. Clin Infect Dis 42, 204–210.[CrossRef]
    [Google Scholar]
  7. Benschop, K. S., Thomas, X., Serpenti, C., Molenkamp, R. & Wolthers, K. ( 2008a; ). High prevalence of human parechovirus genotypes in the Amsterdam region and the identification of specific HPeV variants by direct genotyping of stool samples. J Clin Microbiol 46, 3965–3970.[CrossRef]
    [Google Scholar]
  8. Benschop, K. S., Williams, C. H., Wolthers, K. C., Stanway, G. & Simmonds, P. ( 2008b; ). Widespread recombination within human parechoviruses: analysis of temporal dynamics and constraints. J Gen Virol 89, 1030–1035.[CrossRef]
    [Google Scholar]
  9. Benschop, K. S., de Vries, M., Minaar, R., Stanway, G., van der Hoek, L., Wolthers, K. & Simmonds, P. ( 2009; ). Comprehensive full length sequence analyses of human parechoviruses: diversity and recombination. J Gen Virol 91, 145–154.
    [Google Scholar]
  10. Boivin, G., Abed, Y. & Boucher, F. D. ( 2005; ). Human parechovirus 3 and neonatal infections. Emerg Infect Dis 11, 103–105.[CrossRef]
    [Google Scholar]
  11. Brown, B. A., Oberste, M. S., Alexander, J. P., Jr, Kennett, M. L. & Pallansch, M. A. ( 1999; ). Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73, 9969–9975.
    [Google Scholar]
  12. Cottam, E. M., Haydon, D. T., Paton, D. J., Gloster, J., Wilesmith, J. W., Ferris, N. P., Hutchings, G. H. & King, D. P. ( 2006; ). Molecular epidemiology of the foot-and-mouth disease virus outbreak in the United Kingdom in 2001. J Virol 80, 11274–11282.[CrossRef]
    [Google Scholar]
  13. Drexler, J. F., Grywna, K., Stocker, A., Almeida, P. S., Medrado-Ribeiro, T. C., Eschbach-Bludau, M., Petersen, N., da Costa-Ribeiro, Jr, H. & Drosten, C. ( 2009; ). Novel human parechovirus from Brazil. Emerg Infect Dis 15, 310–313.[CrossRef]
    [Google Scholar]
  14. Drummond, A. J. & Rambaut, A. ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214 [CrossRef]
    [Google Scholar]
  15. Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. ( 2006; ). Relaxed phylogenetics and dating with confidence. PLoS Biol 4, e88 [CrossRef]
    [Google Scholar]
  16. Faria, N. R., de Vries, M., van Hemert, F. J., Benschop, K. & van der Hoek, H. L. ( 2009; ). Rooting human parechovirus evolution in time. BMC Evol Biol 9, 164 [CrossRef]
    [Google Scholar]
  17. Figueroa, J. P., Ashley, D., King, D. & Hull, B. ( 1989; ). An outbreak of acute flaccid paralysis in Jamaica associated with echovirus type 22. J Med Virol 29, 315–319.[CrossRef]
    [Google Scholar]
  18. Harvala, H., Robertson, I., McWilliam Leitch, E. C., Benschop, K., Wolthers, K. C., Templeton, K. & Simmonds, P. ( 2008; ). Epidemiology and clinical associations of human parechovirus respiratory infections. J Clin Microbiol 46, 3446–3453.[CrossRef]
    [Google Scholar]
  19. Harvala, H., Robertson, I., McWilliam Leitch, C., Chieochansin, T., Templeton, K. & Simmonds, P. ( 2009; ). Aetiological role of human parechovirus type 3 in neonatal sepsis identified by direct typing assay on cerebrospinal fluid. J Infect Dis 199, 1753–1760.[CrossRef]
    [Google Scholar]
  20. Heath, L., van der Walt, E., Varsani, A. & Martin, D. P. ( 2006; ). Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80, 11827–11832.[CrossRef]
    [Google Scholar]
  21. Hyypia, T., Horsnell, C., Maaronen, M., Khan, M., Kalkkinen, N., Auvinen, P., Kinnunen, L. & Stanway, G. ( 1992; ). A distinct picornavirus group identified by sequence analysis. Proc Natl Acad Sci U S A 89, 8847–8851.[CrossRef]
    [Google Scholar]
  22. Ito, M., Yamashita, T., Tsuzuki, H., Takeda, N. & Sakae, K. ( 2004; ). Isolation and identification of a novel human parechovirus. J Gen Virol 85, 391–398.[CrossRef]
    [Google Scholar]
  23. Joki-Korpela, P. & Hyypia, T. ( 2001; ). Parechoviruses, a novel group of human picornaviruses. Ann Med 33, 466–471.[CrossRef]
    [Google Scholar]
  24. Kew, O., Mulders, M. N., Lipskaya, G. Y., da Silva, E. E. & Pallansch, M. A. ( 1995; ). Molecular epidemiology of polioviruses. Semin Virol 6, 401–414.[CrossRef]
    [Google Scholar]
  25. Koskiniemi, M., Paetau, R. & Linnavuori, K. ( 1989; ). Severe encephalitis associated with disseminated echovirus 22 infection. Scand J Infect Dis 21, 463–466.[CrossRef]
    [Google Scholar]
  26. Li, L., Victoria, J., Kapoor, A., Naeem, A., Shaukat, S., Sharif, S., Alam, M. M., Angez, M., Zaidi, S. Z. & Delwart, E. ( 2009; ). Genomic characterization of novel human parechovirus type. Emerg Infect Dis 15, 288–291.[CrossRef]
    [Google Scholar]
  27. Lukashev, A. N. ( 2005; ). Role of recombination in evolution of enteroviruses. Rev Med Virol 15, 157–167.[CrossRef]
    [Google Scholar]
  28. McWilliam Leitch, E. C.., Bendig, J. W., Cabrerizo, M., Cardosa, J., Hyypia, T., Ivanova, O. E., Kelly, A., Kroes, A. C. M., Lukashev, A. N. & other authors ( 2009; ). Transmission networks and population turnover of echovirus 30. J Virol 83, 2109–2118.[CrossRef]
    [Google Scholar]
  29. Minor, P. D., John, A., Ferguson, M. & Icenogle, J. P. ( 1986; ). Antigenic and molecular evolution of the vaccine strain of type 3 poliovirus during the period of excretion by a primary vaccinee. J Gen Virol 67, 693–706.[CrossRef]
    [Google Scholar]
  30. Oberste, M. S., Maher, K. & Pallansch, M. A. ( 1998; ). Complete sequence of echovirus 23 and its relationship to echovirus 22 and other human enteroviruses. Virus Res 56, 217–223.[CrossRef]
    [Google Scholar]
  31. Santti, J., Hyypia, T., Kinnunen, L. & Salminen, M. ( 1999; ). Evidence of recombination among enteroviruses. J Virol 73, 8741–8749.
    [Google Scholar]
  32. Shapiro, B., Rambaut, A. & Drummond, A. J. ( 2006; ). Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23, 7–9.
    [Google Scholar]
  33. Simmonds, P. ( 2006; ). Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J Virol 80, 11124–11140.[CrossRef]
    [Google Scholar]
  34. Stanway, G., Kalkkinen, N., Roivainen, M., Ghazi, F., Khan, M., Smyth, M., Meurman, O. & Hyypia, T. ( 1994; ). Molecular and biological characteristics of echovirus 22, a representative of a new picornavirus group. J Virol 68, 8232–8238.
    [Google Scholar]
  35. Stanway, G., Joki-Korpela, P. & Hyypia, T. ( 2000; ). Human parechoviruses – biology and clinical significance. Rev Med Virol 10, 57–69.[CrossRef]
    [Google Scholar]
  36. Stanway, G., Brown, F., Christian, P., Hovi, T., Hyypia, T., King, A. M. Q., Knowles, N. J., Lemon, S. M., Minor, P. D. & other authors ( 2005; ). Family Picornaviridae. In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 757–778. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego: Elsevier/Academic Press.
  37. Takeda, N., Tanimura, M. & Miyamura, K. ( 1994; ). Molecular evolution of the major capsid protein VP1 of enterovirus 70. J Virol 68, 854–862.
    [Google Scholar]
  38. van der Sanden, S., de Bruin, E., Vennema, H., Swanink, C., Koopmans, M. & van der Avoort, H. ( 2008; ). Prevalence of human parechovirus in The Netherlands in 2000 to 2007. J Clin Microbiol 46, 2884–2889.[CrossRef]
    [Google Scholar]
  39. Watanabe, K., Oie, M., Higuchi, M., Nishikawa, M. & Fujii, M. ( 2007; ). Isolation and characterization of novel human parechovirus from clinical samples. Emerg Infect Dis 13, 889–895.[CrossRef]
    [Google Scholar]
  40. Wigand, R. & Sabin, A. B. ( 1961; ). Properties of ECHO types 22, 23 and 24 viruses. Arch Gesamte Virusforsch 11, 224–247.[CrossRef]
    [Google Scholar]
  41. Williams, C. H., Panayiotou, M., Girling, G. D., Peard, C. I., Oikarinen, S., Hyoty, H. & Stanway, G. ( 2009; ). Evolution and conservation in human parechovirus genomes. J Gen Virol 90, 1702–1712.[CrossRef]
    [Google Scholar]
  42. Zoll, J., Galama, J. M. & van Kuppeveld, F. J. ( 2009; ). Identification of potential recombination breakpoints in human parechoviruses. J Virol 83, 3379–3383.[CrossRef]
    [Google Scholar]
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vol. , part 5, pp. 1229 - 1238

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