1887

Abstract

The current measures to control foot-and-mouth disease (FMD) include vaccination, movement control and slaughter of infected or susceptible animals. One of the difficulties in controlling FMD by vaccination arises due to the substantial diversity found among the seven serotypes of FMD virus (FMDV) and the strains within these serotypes. Therefore, vaccination using a single vaccine strain may not fully cross-protect against all strains within that serotype, and therefore selection of appropriate vaccines requires serological comparison of the field virus and potential vaccine viruses using relationship coefficients ( values). Limitations of this approach are that antigenic relationships among field viruses are not addressed, as comparisons are only with potential vaccine virus. Furthermore, inherent variation among vaccine sera may impair reproducibility of one-way relationship scores. Here, we used antigenic cartography to quantify and visualize the antigenic relationships among FMD serotype A viruses, aiming to improve the understanding of FMDV antigenic evolution and the scope and reliability of vaccine matching. Our results suggest that predicting antigenic difference using genetic sequence alone or by geographical location is not currently reliable. We found co-circulating lineages in one region that were genetically similar but antigenically distinct. Nevertheless, by comparing antigenic distances measured from the antigenic maps with the full capsid (P1) sequence, we identified a specific amino acid substitution associated with an antigenic mismatch among field viruses and a commonly used prototype vaccine strain, A/IRQ/24/64.

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2014-02-01
2019-09-21
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References

  1. Abdul-Hamid N. F., Hussein N. M., Wadsworth J., Radford A. D., Knowles N. J., King D. P.. ( 2011; ). Phylogeography of foot-and-mouth disease virus types O and A in Malaysia and surrounding countries. . Infect Genet Evol 11:, 320–328. [CrossRef] [PubMed]
    [Google Scholar]
  2. Armstrong R. M., Samuel A. R., Carpenter W. C., Kant R., Knowles N. J.. ( 1994; ). A comparative study of serological and biochemical methods for strain differentiation of foot-and-mouth disease type A viruses. . Vet Microbiol 39:, 285–298. [CrossRef] [PubMed]
    [Google Scholar]
  3. Ayelet G., Mahapatra M., Gelaye E., Egziabher B. G., Rufeal T., Sahle M., Ferris N. P., Wadsworth J., Hutchings G. H., Knowles N. J.. ( 2009; ). Genetic characterization of foot-and-mouth disease viruses, Ethiopia, 1981–2007. . Emerg Infect Dis 15:, 1409–1417. [CrossRef] [PubMed]
    [Google Scholar]
  4. Baxt B., Vakharia V., Moore D. M., Franke A. J., Morgan D. O.. ( 1989; ). Analysis of neutralizing antigenic sites on the surface of type A12 foot-and-mouth disease virus. . J Virol 63:, 2143–2151.[PubMed]
    [Google Scholar]
  5. Bolwell C., Clarke B. E., Parry N. R., Ouldridge E. J., Brown F., Rowlands D. J.. ( 1989; ). Epitope mapping of foot-and-mouth disease virus with neutralizing monoclonal antibodies. . J Gen Virol 70:, 59–68. [CrossRef] [PubMed]
    [Google Scholar]
  6. Booth J. C., Rweyemamu M. M., Pay T. W.. ( 1978; ). Dose–response relationships in a microneutralization test for foot-and-mouth disease viruses. . J Hyg (Lond) 80:, 31–42. [CrossRef] [PubMed]
    [Google Scholar]
  7. Borley D. W., Mahapatra M., Paton D. J., Esnouf R. M., Stuart D. I., Fry E. E.. ( 2013; ). Evaluation and use of in-silico structure-based epitope prediction with foot-and-mouth disease virus. . PLoS ONE 8:, e61122. [CrossRef] [PubMed]
    [Google Scholar]
  8. Carrillo C., Tulman E. R., Delhon G., Lu Z., Carreno A., Vagnozzi A., Kutish G. F., Rock D. L.. ( 2005; ). Comparative genomics of foot-and-mouth disease virus. . J Virol 79:, 6487–6504. [CrossRef] [PubMed]
    [Google Scholar]
  9. Crowther J. R., Farias S., Carpenter W. C., Samuel A. R.. ( 1993; ). Identification of a fifth neutralizable site on type O foot-and-mouth disease virus following characterization of single and quintuple monoclonal antibody escape mutants. . J Gen Virol 74:, 1547–1553. [CrossRef] [PubMed]
    [Google Scholar]
  10. de Jong J. C., Smith D. J., Lapedes A. S., Donatelli I., Campitelli L., Barigazzi G., Van Reeth K., Jones T. C., Rimmelzwaan G. F.. & other authors ( 2007; ). Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe. . J Virol 81:, 4315–4322. [CrossRef] [PubMed]
    [Google Scholar]
  11. Doel T. R.. ( 2003; ). FMD vaccines. . Virus Res 91:, 81–99. [CrossRef] [PubMed]
    [Google Scholar]
  12. Flannery B., Teukolsky S., Vetterling W.. ( 1988; ). Numerical Recipes in C. Cambridge:: Cambridge University Press;.
    [Google Scholar]
  13. Fry E. E., Newman J. W., Curry S., Najjam S., Jackson T., Blakemore W., Lea S. M., Miller L., Burman A.. & other authors ( 2005; ). Structure of Foot-and-mouth disease virus serotype A1061 alone and complexed with oligosaccharide receptor: receptor conservation in the face of antigenic variation. . J Gen Virol 86:, 1909–1920. [CrossRef] [PubMed]
    [Google Scholar]
  14. Guindon S., Gascuel O.. ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52:, 696–704. [CrossRef] [PubMed]
    [Google Scholar]
  15. Habiela M., Ferris N. P., Hutchings G. H., Wadsworth J., Reid S. M., Madi M., Ebert K., Sumption K. J., Knowles N. J.. & other authors ( 2010; ). Molecular characterization of foot-and-mouth disease viruses collected from Sudan. . Transbound Emerg Dis 57:, 305–314. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hall T.. ( 1999; ). BioEdit: a user friendly biolgoical sequence alignment editor and analysis program for Windows 95/98/NT. . Nucleic Acids Symp Ser 41:, 95–98.
    [Google Scholar]
  17. Hamblin C., Barnett I. T., Crowther J. R.. ( 1986; ). A new enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies against foot-and-mouth disease virus. II. Application. . J Immunol Methods 93:, 123–129. [CrossRef] [PubMed]
    [Google Scholar]
  18. Haydon D. T., Samuel A. R., Knowles N. J.. ( 2001; ). The generation and persistence of genetic variation in foot-and-mouth disease virus. . Prev Vet Med 51:, 111–124. [CrossRef] [PubMed]
    [Google Scholar]
  19. Horton D. L., McElhinney L. M., Marston D. A., Wood J. L., Russell C. A., Lewis N., Kuzmin I. V., Fouchier R. A., Osterhaus A. D.. & other authors ( 2010; ). Quantifying antigenic relationships among the lyssaviruses. . J Virol 84:, 11841–11848. [CrossRef] [PubMed]
    [Google Scholar]
  20. Huang S. W., Hsu Y. W., Smith D. J., Kiang D., Tsai H. P., Lin K. H., Wang S. M., Liu C. C., Su I. J., Wang J. R.. ( 2009; ). Reemergence of enterovirus 71 in 2008 in Taiwan: dynamics of genetic and antigenic evolution from 1998 to 2008. . J Clin Microbiol 47:, 3653–3662. [CrossRef] [PubMed]
    [Google Scholar]
  21. Jackson T., King A. M., Stuart D. I., Fry E.. ( 2003; ). Structure and receptor binding. . Virus Res 91:, 33–46. [CrossRef] [PubMed]
    [Google Scholar]
  22. Jackson T., Clark S., Berryman S., Burman A., Cambier S., Mu D., Nishimura S., King A. M.. ( 2004; ). Integrin αvβ8 functions as a receptor for foot-and-mouth disease virus: role of the β-chain cytodomain in integrin-mediated infection. . J Virol 78:, 4533–4540. [CrossRef] [PubMed]
    [Google Scholar]
  23. Kitching R. P., Hutber A. M., Thrusfield M. V.. ( 2005; ). A review of foot-and-mouth disease with special consideration for the clinical and epidemiological factors relevant to predictive modelling of the disease. . Vet J 169:, 197–209. [CrossRef] [PubMed]
    [Google Scholar]
  24. Klein J., Hussain M., Ahmad M., Normann P., Afzal M., Alexandersen S.. ( 2007; ). Genetic characterisation of the recent foot-and-mouth disease virus subtype A/IRN/2005. . Virol J 4:, 122. [CrossRef] [PubMed]
    [Google Scholar]
  25. Knowles N. J., Samuel A. R.. ( 2003; ). Molecular epidemiology of foot-and-mouth disease virus. . Virus Res 91:, 65–80. [CrossRef] [PubMed]
    [Google Scholar]
  26. Knowles N. J., Wadsworth J., Reid S. M., Swabey K. G., El-Kholy A. A., El-Rahman A. O. A., Soliman H. M., Ebert K., Ferris N. P.. & other authors ( 2007; ). Foot-and-mouth disease virus serotype A in Egypt. . Emerg Infect Dis 13:, 1593–1596. [CrossRef] [PubMed]
    [Google Scholar]
  27. Knowles N. J., Nazem Shirazi M. H., Wadsworth J., Swabey K. G., Stirling J. M., Statham R. J., Li Y., Hutchings G. H., Ferris N. P.. & other authors ( 2009; ). Recent spread of a new strain (A-Iran-05) of foot-and-mouth disease virus type A in the Middle East. . Transbound Emerg Dis 56:, 157–169. [CrossRef] [PubMed]
    [Google Scholar]
  28. Knowles N. J., He J., Shang Y., Wadsworth J., Valdazo-González B., Onosato H., Fukai K., Morioka K., Yoshida K.. & other authors ( 2012; ). Southeast Asian foot-and-mouth disease viruses in Eastern Asia. . Emerg Infect Dis 18:, 499–501. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lewis N., Daly J., Russell C., Horton D., Skepner E., Bryant N., Burke D., Rash A., Wood J.. & other authors ( 2011; ). The antigenic and genetic evolutionof equine influenza A (H3N8) virus from 1968 to 2007. . J Virol Methods 85:, 12742–12749. [CrossRef]
    [Google Scholar]
  30. Logan D., Abu-Ghazaleh R., Blakemore W., Curry S., Jackson T., King A., Lea S., Lewis R., Newman J.. & other authors ( 1993; ). Structure of a major immunogenic site on foot-and-mouth disease virus. . Nature 362:, 566–568. [CrossRef] [PubMed]
    [Google Scholar]
  31. Lorusso A., Vincent A. L., Harland M. L., Alt D., Bayles D. O., Swenson S. L., Gramer M. R., Russell C. A., Smith D. J.. & other authors ( 2011; ). Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. . J Gen Virol 92:, 919–930. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mahapatra M., Seki C., Upadhyaya S., Barnett P. V., La Torre J., Paton D. J.. ( 2011; ). Characterisation and epitope mapping of neutralising monoclonal antibodies to A24 Cruzeiro strain of FMDV. . Vet Microbiol 149:, 242–247. [CrossRef] [PubMed]
    [Google Scholar]
  33. Maree F. F., Blignaut B., Esterhuysen J. J., de Beer T. A., Theron J., O’Neill H. G., Rieder E.. ( 2011; ). Predicting antigenic sites on the foot-and-mouth disease virus capsid of the South African Territories types using virus neutralization data. . J Gen Virol 92:, 2297–2309. [CrossRef] [PubMed]
    [Google Scholar]
  34. Mattion N., Goris N., Willems T., Robiolo B., Maradei E., Beascoechea C. P., Perez A., Smitsaart E., Fondevila N.. & other authors ( 2009; ). Some guidelines for determining foot-and-mouth disease vaccine strain matching by serology. . Vaccine 27:, 741–747. [CrossRef] [PubMed]
    [Google Scholar]
  35. OIE. ( 2008; ). Foot and mouth disease. . In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, , 6th edn., pp. 190–217. Paris:: Office International Des Epizooties;.
    [Google Scholar]
  36. Posada D.. ( 2008; ). jModelTest: phylogenetic model averaging. . Mol Biol Evol 25:, 1253–1256. [CrossRef] [PubMed]
    [Google Scholar]
  37. Reeve R., Blignaut B., Esterhuysen J. J., Opperman P., Matthews L., Fry E. E., de Beer T. A., Theron J., Rieder E.. & other authors ( 2010; ). Sequence-based prediction for vaccine strain selection and identification of antigenic variability in foot-and-mouth disease virus. . PLOS Comput Biol 6:, e1001027. [CrossRef] [PubMed]
    [Google Scholar]
  38. Rweyemamu M. M., Pay T. W., Parker M. J.. ( 1976; ). Serological differentiation of foot-and-mouth disease virus strains in relation to selection of suitable vaccine viruses. . Dev Biol Stand 35:, 205–4.[PubMed]
    [Google Scholar]
  39. Schumann K. R., Knowles N. J., Davies P. R., Midgley R. J., Valarcher J. F., Raoufi A. Q., McKenna T. S., Hurtle W., Burans J. P.. & other authors ( 2008; ). Genetic characterization and molecular epidemiology of foot-and-mouth disease viruses isolated from Afghanistan in 2003–2005. . Virus Genes 36:, 401–413. [CrossRef] [PubMed]
    [Google Scholar]
  40. Smith D. J., Lapedes A. S., de Jong J. C., Bestebroer T. M., Rimmelzwaan G. F., Osterhaus A. D., Fouchier R. A.. ( 2004a; ). Mapping the antigenic and genetic evolution of influenza virus. . Science 305:, 371–376. [CrossRef] [PubMed]
    [Google Scholar]
  41. Smith D. J., Lapedes A. S., de Jong J. C., Bestebroer T. M., Rimmelzwaan G. F., Osterhaus A. D., Fouchier R. A.. ( 2004b; ). Mapping the antigenic and genetic evolution of influenza virus. . Science 305:, 371–376. [CrossRef] [PubMed]
    [Google Scholar]
  42. 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. [CrossRef] [PubMed]
    [Google Scholar]
  43. Thomas A. A., Woortmeijer R. J., Puijk W., Barteling S. J.. ( 1988; ). Antigenic sites on foot-and-mouth disease virus type A10. . J Virol 62:, 2782–2789.[PubMed]
    [Google Scholar]
  44. Thompson D., Muriel P., Russell D., Osborne P., Bromley A., Rowland M., Creigh-Tyte S., Brown C.. ( 2002; ). Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001. . Rev Sci Tech 21:, 675–687.[PubMed]
    [Google Scholar]
  45. Thompson J. D., Higgins D. G., Gibson T. J.. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. . Nucleic Acids Res 22:, 4673–4680. [CrossRef] [PubMed]
    [Google Scholar]
  46. Upadhyaya S., Ayelet G., Paul G., King D. P., Paton D. J., Mahapatra M.. ( 2013; ). Genetic basis of antigenic variation in foot-and-mouth disease serotype A viruses from the Middle East. . Vaccine 2013:, pii: S0264-410X(13)01214-0. doi: 10.1016/j.vaccine.2013.08.102
    [Google Scholar]
  47. Valarcher J. F., Leforban Y., Rweyemamu M., Roeder P. L., Gerbier G., Mackay D. K., Sumption K. J., Paton D. J., Knowles N. J.. ( 2008; ). Incursions of foot-and-mouth disease virus into Europe between 1985 and 2006. . Transbound Emerg Dis 55:, 14–34. [CrossRef] [PubMed]
    [Google Scholar]
  48. Waheed U., Parida S., Khan Q., Hussain M., Ebert K., Wadsworth J., Reid S., Hutchings G., Mahapatra M.. & other authors ( 2011; ). Molecular characterisation of foot-and-mouth diseae virus from Pakistan 2005–2008. . Transbound Emerg Dis 58:, 166–172. [CrossRef]
    [Google Scholar]
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