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Abstract

Human rhinoviruses (HRVs) frequently cause mild upper respiratory tract infections and more severe disease manifestations such as bronchiolitis and asthma exacerbations. HRV is classified into three species within the genus of the family . HRV species A and B contain 75 and 25 serotypes identified by cross-neutralization assays, although the use of such assays for routine HRV typing is hampered by the large number of serotypes, replacement of virus isolation by molecular methods in HRV diagnosis and the poor or absent replication of HRV species C in cell culture. To address these problems, we propose an alternative, genotypic classification of HRV-based genetic relatedness analogous to that used for enteroviruses. Nucleotide distances between 384 complete VP1 sequences of currently assigned HRV (sero)types identified divergence thresholds of 13, 12 and 13 % for species A, B and C, respectively, that divided inter- and intra-type comparisons. These were paralleled by 10, 9.5 and 10 % thresholds in the larger dataset of >3800 VP4 region sequences. Assignments based on VP1 sequences led to minor revisions of existing type designations (such as the reclassification of serotype pairs, e.g. A8/A95 and A29/A44, as single serotypes) and the designation of new HRV types A101–106, B101–103 and C34–C51. A protocol for assignment and numbering of new HRV types using VP1 sequences and the restriction of VP4 sequence comparisons to type identification and provisional type assignments is proposed. Genotypic assignment and identification of HRV types will be of considerable value in the future investigation of type-associated differences in disease outcomes, transmission and epidemiology.

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2013-08-01
2022-07-01
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References

  1. Arden K. E., McErlean P., Nissen M. D., Sloots T. P., Mackay I. M. 2006; Frequent detection of human rhinoviruses, paramyxoviruses, coronaviruses, and bocavirus during acute respiratory tract infections. J Med Virol 78:1232–1240 [View Article][PubMed]
    [Google Scholar]
  2. Blomqvist S., Savolainen-Kopra C., Paananen A., Hovi T., Roivainen M. 2009; Molecular characterization of human rhinovirus field strains isolated during surveillance of enteroviruses. J Gen Virol 90:1371–1381 [View Article][PubMed]
    [Google Scholar]
  3. Bochkov Y. A., Palmenberg A. C., Lee W.-M., Rathe J. A., Amineva S. P., Sun X., Pasic T. R., Jarjour N. N., Liggett S. B., Gern J. E. 2011; Molecular modeling, organ culture and reverse genetics for a newly identified human rhinovirus C. Nat Med 17:627–632 [View Article][PubMed]
    [Google Scholar]
  4. 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]
  5. Cooney M. K., Fox J. P., Kenny G. E. 1982; Antigenic groupings of 90 rhinovirus serotypes. Infect Immun 37:642–647[PubMed]
    [Google Scholar]
  6. de Vries M., Pyrc K., Berkhout R., Vermeulen-Oost W., Dijkman R., Jebbink M. F., Bruisten S., Berkhout B., van der Hoek L. 2008; Human parechovirus type 1, 3, 4, 5, and 6 detection in picornavirus cultures. J Clin Microbiol 46:759–762 [View Article][PubMed]
    [Google Scholar]
  7. Gaunt E. R., Harvala H., McIntyre C., Templeton K. E., Simmonds P. 2011; Disease burden of the most commonly detected respiratory viruses in hospitalized patients calculated using the disability adjusted life year (DALY) model. J Clin Virol 52:215–221 [View Article][PubMed]
    [Google Scholar]
  8. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2000; Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582 [View Article][PubMed]
    [Google Scholar]
  9. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  10. Gutman J. A., Peck A. J., Kuypers J., Boeckh M. 2007; Rhinovirus as a cause of fatal lower respiratory tract infection in adult stem cell transplantation patients: a report of two cases. Bone Marrow Transplant 40:809–811 [View Article][PubMed]
    [Google Scholar]
  11. Hamparian V. V., Colonno R. J., Cooney M. K., Dick E. C., Gwaltney J. M. Jr, Hughes J. H., Jordan W. S. Jr, Kapikian A. Z., Mogabgab W. J.& other authors ( 1987; A collaborative report: rhinoviruses–extension of the numbering system from 89 to 100. Virology 159:191–192 [View Article][PubMed]
    [Google Scholar]
  12. Han T. H., Chung J. Y., Hwang E. S., Koo J. W. 2009; Detection of human rhinovirus C in children with acute lower respiratory tract infections in South Korea. Arch Virol 154:987–991 [View Article][PubMed]
    [Google Scholar]
  13. 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 [View Article][PubMed]
    [Google Scholar]
  14. Henquell C., Mirand A., Deusebis A.-L., Regagnon C., Archimbaud C., Chambon M., Bailly J.-L., Gourdon F., Hermet E.& other authors ( 2012; Prospective genotyping of human rhinoviruses in children and adults during the winter of 2009–2010. J Clin Virol 53:280–284 [View Article][PubMed]
    [Google Scholar]
  15. Hofer F., Gruenberger M., Kowalski H., Machat H., Huettinger M., Kuechler E., Blaas D. 1994; Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Sci U S A 91:1839–1842 [View Article][PubMed]
    [Google Scholar]
  16. Ison M. G., Hayden F. G., Kaiser L., Corey L., Boeckh M. 2003; Rhinovirus infections in hematopoietic stem cell transplant recipients with pneumonia. Clin Infect Dis 36:1139–1143 [View Article][PubMed]
    [Google Scholar]
  17. Kaida A., Kubo H., Takakura K., Togawa M., Shiomi M., Kohdera U., Iritani N. 2011; Molecular epidemiology of human rhinovirus C in patients with acute respiratory tract infections in Osaka City, Japan. Jpn J Infect Dis 64:488–492[PubMed]
    [Google Scholar]
  18. Kaiser L., Aubert J.-D., Pache J.-C., Deffernez C., Rochat T., Garbino J., Wunderli W., Meylan P., Yerly S.& other authors ( 2006; Chronic rhinoviral infection in lung transplant recipients. Am J Respir Crit Care Med 174:1392–1399 [View Article][PubMed]
    [Google Scholar]
  19. Kapikian A., Conant R., Hamparian V. 1967; Rhinoviruses: a numbering system. Nature 213:761–763 [View Article][PubMed]
    [Google Scholar]
  20. Kapikian A., Conant R., Hamparian V., Chanock R., Dick E., Gwaltney J. Jr, Hamre D., Jordan W. Jr, Kenny G.& other authors ( 1971; A collaborative report: rhinoviruses – extension of the numbering system. Virology 43:524–526 [View Article][PubMed]
    [Google Scholar]
  21. Khetsuriani N., Lu X., Teague W. G., Kazerouni N., Anderson L. J., Erdman D. D. 2008; Novel human rhinoviruses and exacerbation of asthma in children. Emerg Infect Dis 14:1793–1796 [View Article][PubMed]
    [Google Scholar]
  22. Kiang D., Newbower E. C., Yeh E., Wold L., Chen L., Schnurr D. P. 2009; An algorithm for the typing of enteroviruses and correlation to serotyping by viral neutralization. J Clin Virol 45:334–340 [View Article][PubMed]
    [Google Scholar]
  23. Kilpatrick D. R., Nottay B., Yang C. F., Yang S. J., Da Silva E., Peñaranda S., Pallansch M., Kew O. 1998; Serotype-specific identification of polioviruses by PCR using primers containing mixed-base or deoxyinosine residues at positions of codon degeneracy. J Clin Microbiol 36:352–357[PubMed]
    [Google Scholar]
  24. Kistler A., Avila P. C., Rouskin S., Wang D., Ward T., Yagi S., Schnurr D., Ganem D., DeRisi J. L., Boushey H. A. 2007a; Pan-viral screening of respiratory tract infections in adults with and without asthma reveals unexpected human coronavirus and human rhinovirus diversity. J Infect Dis 196:817–825 [View Article][PubMed]
    [Google Scholar]
  25. Kistler A. L., Webster D. R., Rouskin S., Magrini V., Credle J. J., Schnurr D. P., Boushey H. A., Mardis E. R., Li H., DeRisi J. L. 2007b; Genome-wide diversity and selective pressure in the human rhinovirus. Virol J 4:40 [View Article][PubMed]
    [Google Scholar]
  26. Knowles N. J., Hovi T., Hyypiä T., King A. M. Q., Lindberg A. M., Pallansch M. A., Palmenberg A. C., Simmonds P., Skern T.& 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]
  27. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D. W. 2006; gard: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098 [View Article][PubMed]
    [Google Scholar]
  28. Lamson D., Renwick N., Kapoor V., Liu Z., Palacios G., Ju J., Dean A., St George K., Briese T., Lipkin W. I. 2006; MassTag polymerase-chain-reaction detection of respiratory pathogens, including a new rhinovirus genotype, that caused influenza-like illness in New York State during 2004–2005. J Infect Dis 194:1398–1402 [View Article][PubMed]
    [Google Scholar]
  29. Lau S. K. P., Yip C. C. Y., Tsoi H.-W., Lee R. A., So L. Y., Lau Y. L., Chan K. H., Woo P. C., Yuen K. Y. 2007; Clinical features and complete genome characterization of a distinct human rhinovirus (HRV) genetic cluster, probably representing a previously undetected HRV species, HRV-C, associated with acute respiratory illness in children. J Clin Microbiol 45:3655–3664 [View Article][PubMed]
    [Google Scholar]
  30. Ledford R. M., Patel N. R., Demenczuk T. M., Watanyar A., Herbertz T., Collett M. S., Pevear D. C. 2004; VP1 sequencing of all human rhinovirus serotypes: insights into genus phylogeny and susceptibility to antiviral capsid-binding compounds. J Virol 78:3663–3674 [View Article][PubMed]
    [Google Scholar]
  31. Lee W. M., Kiesner C., Pappas T., Lee I., Grindle K., Jartti T., Jakiela B., Lemanske R. F. Jr, Shult P. A., Gern J. E. 2007; A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS ONE 2:e966 [View Article][PubMed]
    [Google Scholar]
  32. Linsuwanon P., Payungporn S., Suwannakarn K., Chieochansin T., Theamboonlers A., Poovorawan Y. 2011; Complete coding sequence characterization and comparative analysis of the putative novel human rhinovirus (HRV) species C and B. Virol J 8:5 (BioMed Central Ltd.) [View Article][PubMed]
    [Google Scholar]
  33. Martin D., Rybicki E. 2000; rdp: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [View Article][PubMed]
    [Google Scholar]
  34. Martin D. P., Posada D., Crandall K. A., Williamson C. 2005; A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21:98–102 [View Article][PubMed]
    [Google Scholar]
  35. Martin D. P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. 2010; rdp3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463 [View Article][PubMed]
    [Google Scholar]
  36. McErlean P., Shackelton L. A., Lambert S. B., Nissen M. D., Sloots T. P., Mackay I. M. 2007; Characterisation of a newly identified human rhinovirus, HRV-QPM, discovered in infants with bronchiolitis. J Clin Virol 39:67–75 [View Article][PubMed]
    [Google Scholar]
  37. McIntyre C. L., McWilliam Leitch E. C., Savolainen-Kopra C., Hovi T., Simmonds P. 2010; Analysis of genetic diversity and sites of recombination in human rhinovirus species C. J Virol 84:10297–10310 [View Article][PubMed]
    [Google Scholar]
  38. McIntyre, C., Savolainen-Kopra, C., Hovi, T. & Simmonds, P. (2013). Recombination in the evolution of human rhinovirus genomes. Arch Virol [Epub ahead of print]
  39. McWilliam Leitch E. C., Harvala H., Robertson I., Ubillos I., Templeton K., Simmonds P. 2009; Direct identification of human enterovirus serotypes in cerebrospinal fluid by amplification and sequencing of the VP1 region. J Clin Microbiol 44:119–124
    [Google Scholar]
  40. Miller E. K., Lu X., Erdman D. D., Poehling K. A., Zhu Y., Griffin M. R., Hartert T. V., Anderson L. J., Weinberg G. A.& other authors ( 2007; Rhinovirus-associated hospitalizations in young children. J Infect Dis 195:773–781 [View Article][PubMed]
    [Google Scholar]
  41. Miller E. K., Edwards K. M., Weinberg G. A., Iwane M. K., Griffin M. R., Hall C. B., Zhu Y., Szilagyi P. G., Morin L. L.& other authors ( 2009; A novel group of rhinoviruses is associated with asthma hospitalizations. J Allergy Clin Immunol 123:98–104, e1 [View Article][PubMed]
    [Google Scholar]
  42. Mirand A., Rouveyrol F., Chambon M., Archimbaud C., Regagnon C., Bailly J.-L., Peigue-Lafeuille H., Henquell C. 2009; Enterovirus genotyping directly from original clinical specimens: prospective application to a severe neonatal infection. J Clin Virol 44:177–178 [View Article][PubMed]
    [Google Scholar]
  43. Mizuta K., Hirata A., Suto A., Aoki Y., Ahiko T., Itagaki T., Tsukagoshi H., Morita Y., Obuchi M.& other authors ( 2010; Phylogenetic and cluster analysis of human rhinovirus species A (HRV-A) isolated from children with acute respiratory infections in Yamagata, Japan. Virus Res 147:265–274 [View Article][PubMed]
    [Google Scholar]
  44. Monto A. S. 2002; The seasonality of rhinovirus infections and its implications for clinical recognition. Clin Ther 24:1987–1997 [View Article][PubMed]
    [Google Scholar]
  45. 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]
  46. Norder H., Bjerregaard L., Magnius L., Lina B., Aymard M., Chomel J. J. 2003; Sequencing of ‘untypable’ enteroviruses reveals two new types, EV-77 and EV-78, within human enterovirus type B and substitutions in the BC loop of the VP1 protein for known types. J Gen Virol 84:827–836 [View Article][PubMed]
    [Google Scholar]
  47. 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]
  48. 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]
  49. Oberste M. S., Maher K., Pallansch M. A. 2002; Molecular phylogeny and proposed classification of the simian picornaviruses. J Virol 76:1244–1251 [View Article][PubMed]
    [Google Scholar]
  50. Oberste M. S., Michele S. M., Maher K., Schnurr D., Cisterna D., Junttila N., Uddin M., Chomel J.-J., Lau C.-S.& other authors ( 2004; Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. J Gen Virol 85:3205–3212 [View Article][PubMed]
    [Google Scholar]
  51. Oberste M. S., Maher K., Nix W. A., Michele S. M., Uddin M., Schnurr D., al-Busaidy S., Akoua-Koffi C., Pallansch M. A. 2007; Molecular identification of 13 new enterovirus types, EV79–88, EV97, and EV100–101, members of the species Human Enterovirus B . Virus Res 128:34–42 [View Article][PubMed]
    [Google Scholar]
  52. Olenec J. P., Kim W. K., Lee W.-M., Vang F., Pappas T. E., Salazar L. E. P., Evans M. D., Bork J., Roberg K.& other authors ( 2010; Weekly monitoring of children with asthma for infections and illness during common cold seasons. J Allergy Clin Immunol 125:1001–1006, e1 [View Article][PubMed]
    [Google Scholar]
  53. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [View Article][PubMed]
    [Google Scholar]
  54. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [View Article][PubMed]
    [Google Scholar]
  55. Rathe J. A., Liu X., Tallon L. J., Gern J. E., Liggett S. B. 2010; Full-genome sequence and analysis of a novel human rhinovirus strain within a divergent HRV-A clade. Arch Virol 155:83–87 [View Article][PubMed]
    [Google Scholar]
  56. Renwick N., Schweiger B., Kapoor V., Liu Z., Villari J., Bullmann R., Miething R., Briese T., Lipkin W. I. 2007; A recently identified rhinovirus genotype is associated with severe respiratory-tract infection in children in Germany. J Infect Dis 196:1754–1760 [View Article][PubMed]
    [Google Scholar]
  57. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  58. Savolainen-Kopra C., Blomqvist S., Kilpi T., Roivainen M., Hovi T. 2009; Novel species of human rhinoviruses in acute otitis media. Pediatr Infect Dis J 28:59–61 [View Article][PubMed]
    [Google Scholar]
  59. Silva P. A., Diedrich S., de Paula Cardoso D., Schreier E. 2008; Identification of enterovirus serotypes by pyrosequencing using multiple sequencing primers. J Virol Methods 148:260–264 [View Article][PubMed]
    [Google Scholar]
  60. Simmonds P. 2012; sse: a nucleotide and amino acid sequence analysis platform. BMC Res Notes 5:50 [View Article][PubMed]
    [Google Scholar]
  61. Simmonds P., McIntyre C., Savolainen-Kopra C., Tapparel C., Mackay I. M., Hovi T. 2010; Proposals for the classification of human rhinovirus species C into genotypically assigned types. J Gen Virol 91:2409–2419 [View Article][PubMed]
    [Google Scholar]
  62. Smith J. M. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129 [View Article][PubMed]
    [Google Scholar]
  63. Smura T., Blomqvist S., Paananen A., Vuorinen T., Sobotová Z., Bubovica V., Ivanova O., Hovi T., Roivainen M. 2007a; 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]
  64. Smura T. P., Junttila N., Blomqvist S., Norder H., Kaijalainen S., Paananen A., Magnius L. O., Hovi T., Roivainen M. 2007b; Enterovirus 94, a proposed new serotype in human enterovirus species D. J Gen Virol 88:849–858 [View Article][PubMed]
    [Google Scholar]
  65. 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 Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  66. 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]
  67. Uncapher C. R., DeWitt C. M., Colonno R. J. 1991; The major and minor group receptor families contain all but one human rhinovirus serotype. Virology 180:814–817 [View Article][PubMed]
    [Google Scholar]
  68. Vesa S., Kleemola M., Blomqvist S., Takala A., Kilpi T., Hovi T. 2001; Epidemiology of documented viral respiratory infections and acute otitis media in a cohort of children followed from two to twenty-four months of age. Pediatr Infect Dis J 20:574–581 [View Article][PubMed]
    [Google Scholar]
  69. Wisdom A., Leitch E. C., Gaunt E., Harvala H., Simmonds P. 2009a; Screening respiratory samples for detection of human rhinoviruses (HRVs) and enteroviruses: comprehensive VP4-VP2 typing reveals high incidence and genetic diversity of HRV species C. J Clin Microbiol 47:3958–3967 [View Article][PubMed]
    [Google Scholar]
  70. Wisdom A., Kutkowska A. E., McWilliam Leitch E. C., Gaunt E., Templeton K., Harvala H., Simmonds P. 2009b; Genetics, recombination and clinical features of human rhinovirus species C (HRV-C) infections; interactions of HRV-C with other respiratory viruses. PLoS ONE 4:e8518 [View Article][PubMed]
    [Google Scholar]
  71. 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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