†Present address: Foreign Animal Disease Research Unit, US Department of Agriculture, Agricultural Research Service, Plum Island Animal Disease Centre, Greenport NY 11944, USA.
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 (r1 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, A22/IRQ/24/64.
Abdul-HamidN. F., HusseinN. M., WadsworthJ., RadfordA. D., KnowlesN. J., KingD. P.2011; Phylogeography of foot-and-mouth disease virus types O and A in Malaysia and surrounding countries. Infect Genet Evol 11:320–328 [View Article][PubMed]
ArmstrongR. M., SamuelA. R., CarpenterW. C., KantR., KnowlesN. 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 [View Article][PubMed]
BaxtB., VakhariaV., MooreD. M., FrankeA. J., MorganD. O.1989; Analysis of neutralizing antigenic sites on the surface of type A12 foot-and-mouth disease virus. J Virol 63:2143–2151[PubMed]
BoothJ. C., RweyemamuM. M., PayT. W.1978; Dose–response relationships in a microneutralization test for foot-and-mouth disease viruses. J Hyg (Lond) 80:31–42 [View Article][PubMed]
BorleyD. W., MahapatraM., PatonD. J., EsnoufR. M., StuartD. I., FryE. E.2013; Evaluation and use of in-silico structure-based epitope prediction with foot-and-mouth disease virus. PLoS ONE 8:e61122 [View Article][PubMed]
CrowtherJ. R., FariasS., CarpenterW. C., SamuelA. 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 [View Article][PubMed]
de JongJ. C., SmithD. J., LapedesA. S., DonatelliI., CampitelliL., BarigazziG., Van ReethK., JonesT. C., RimmelzwaanG. F.other authors2007; Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe. J Virol 81:4315–4322 [View Article][PubMed]
FryE. E., NewmanJ. W., CurryS., NajjamS., JacksonT., BlakemoreW., LeaS. M., MillerL., BurmanA.other authors2005; 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 [View Article][PubMed]
GuindonS., GascuelO.2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
HamblinC., BarnettI. T., CrowtherJ. 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 [View Article][PubMed]
HaydonD. T., SamuelA. R., KnowlesN. J.2001; The generation and persistence of genetic variation in foot-and-mouth disease virus. Prev Vet Med 51:111–124 [View Article][PubMed]
HortonD. L., McElhinneyL. M., MarstonD. A., WoodJ. L., RussellC. A., LewisN., KuzminI. V., FouchierR. A., OsterhausA. D.other authors2010; Quantifying antigenic relationships among the lyssaviruses. J Virol 84:11841–11848 [View Article][PubMed]
HuangS. W., HsuY. W., SmithD. J., KiangD., TsaiH. P., LinK. H., WangS. M., LiuC. C., SuI. J., WangJ. 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 [View Article][PubMed]
JacksonT., ClarkS., BerrymanS., BurmanA., CambierS., MuD., NishimuraS., KingA. 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 [View Article][PubMed]
KitchingR. P., HutberA. M., ThrusfieldM. 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 [View Article][PubMed]
KnowlesN. J., WadsworthJ., ReidS. M., SwabeyK. G., El-KholyA. A., El-RahmanA. O. A., SolimanH. M., EbertK., FerrisN. P.other authors2007; Foot-and-mouth disease virus serotype A in Egypt. Emerg Infect Dis 13:1593–1596 [View Article][PubMed]
KnowlesN. J., Nazem ShiraziM. H., WadsworthJ., SwabeyK. G., StirlingJ. M., StathamR. J., LiY., HutchingsG. H., FerrisN. P.other authors2009; 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 [View Article][PubMed]
LoganD., Abu-GhazalehR., BlakemoreW., CurryS., JacksonT., KingA., LeaS., LewisR., NewmanJ.other authors1993; Structure of a major immunogenic site on foot-and-mouth disease virus. Nature 362:566–568 [View Article][PubMed]
LorussoA., VincentA. L., HarlandM. L., AltD., BaylesD. O., SwensonS. L., GramerM. R., RussellC. A., SmithD. J.other authors2011; Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. J Gen Virol 92:919–930 [View Article][PubMed]
MahapatraM., SekiC., UpadhyayaS., BarnettP. V., La TorreJ., PatonD. J.2011; Characterisation and epitope mapping of neutralising monoclonal antibodies to A24 Cruzeiro strain of FMDV. Vet Microbiol 149:242–247 [View Article][PubMed]
MareeF. F., BlignautB., EsterhuysenJ. J., de BeerT. A., TheronJ., O’NeillH. G., RiederE.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 [View Article][PubMed]
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;
ReeveR., BlignautB., EsterhuysenJ. J., OppermanP., MatthewsL., FryE. E., de BeerT. A., TheronJ., RiederE.other authors2010; Sequence-based prediction for vaccine strain selection and identification of antigenic variability in foot-and-mouth disease virus. PLOS Comput Biol 6:e1001027 [View Article][PubMed]
RweyemamuM. M., PayT. W., ParkerM. 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]
SmithD. J., LapedesA. S., de JongJ. C., BestebroerT. M., RimmelzwaanG. F., OsterhausA. D., FouchierR. A.2004a; Mapping the antigenic and genetic evolution of influenza virus. Science 305:371–376 [View Article][PubMed]
SmithD. J., LapedesA. S., de JongJ. C., BestebroerT. M., RimmelzwaanG. F., OsterhausA. D., FouchierR. A.2004b; Mapping the antigenic and genetic evolution of influenza virus. Science 305:371–376 [View Article][PubMed]
ThompsonD., MurielP., RussellD., OsborneP., BromleyA., RowlandM., Creigh-TyteS., BrownC.2002; Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001. Rev Sci Tech 21:675–687[PubMed]
ThompsonJ. D., HigginsD. G., GibsonT. J.1994; clustalw: 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 [View Article][PubMed]