Transboundary movements of foot-and-mouth disease from India to Sri Lanka: A common pattern is shared by serotypes O and C

Autoři: L. T. Ranaweera aff001;  W. W. M. U. K. Wijesundara aff001;  H. S. M. Jayarathne aff001;  N. J. Knowles aff002;  J. Wadsworth aff002;  A. Gray aff002;  A. M. J. B. Adikari aff003;  C. K. Weebadde aff004;  S. D. S. S. Sooriyapathirana aff001
Působiště autorů: Department of Molecular Biology and Biotechnology, Faculty of Science, University of Peradeniya, Peradeniya, Sri Lanka aff001;  The Pirbright Institute, Pirbright, Woking, Surrey, United Kingdom aff002;  Department of Animal and Food Sciences, Faculty of Agriculture, Rajarata University of Sri Lanka, Puliyankulama, Anuradhapura, Sri Lanka aff003;  Department of Plant, Soil and Microbial Sciences, College of Agriculture and Natural Resources, Michigan State University, East Lansing, MI, United States of America aff004;  Postgraduate Institute of Science, University of Peradeniya, Peradeniya, Sri Lanka aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


Foot-and-mouth disease (FMD) affects the livestock industry in a transboundary manner. It is essential to understand the FMD phylodynamics to assist in the disease-eradication. FMD critically affects the Sri Lankan cattle industry causing substantial economic losses. Even though many studies have covered the serotyping and genotyping of FMD virus (FMDV) in Sri Lanka, there is a significant knowledge gap exists in understanding the FMDV phylodynamics in the country. In the present study, the VP1 genomic region of FMD viral isolates belonging to serotype C from Sri Lanka and other South Asian countries were sequenced. All the published VPI sequences of serotype C and most of the published VP1 sequences for lineage ME-SA/Ind-2001d of serotype O from Sri Lanka, India, and other South Asian countries were retrieved. The datasets of serotype C and serotype O were separately analyzed using Bayesian, maximum likelihood, and phylogenetic networking methods to infer the transboundary movements and evolutionary aspects of the FMDV incursions in Sri Lanka. A model-based approach was used to detect any possible recombination events of FMDV incursions. Our results revealed that the invasions of the topotype ASIA of serotype C and the lineage ME-SA/Ind-2001d have a similar pattern of transboundary movement and evolution. The haplotype networks and phylogenies developed in the present study confirmed that FMDV incursions in Sri Lanka mainly originate from the Indian subcontinent, remain quiet after migration, and then cause outbreaks in a subsequent year. Since there are no recombination events detected among the different viral strains across serotypes and topotypes, we can assume that the incursions tend to show the independent evolution compared to the ancestral viral populations. Thus, we highlight the need for thorough surveillance of cattle/ruminants and associated product-movement into Sri Lanka from other regions to prevent the transboundary movement of FMDV.

Klíčová slova:

Asia – Foot and mouth disease – Haplogroups – Haplotypes – India – Phylogenetic analysis – Sri Lanka – Viral evolution


1. Brito BP, Rodriguez LL, Hammond JM, Pinto J, Perez AM. Review of the Global Distribution of Foot‐and‐Mouth Disease Virus from 2007 to 2014. Transbound Emerg Dis. 2017;64(2): 316–332. doi: 10.1111/tbed.12373 25996568.

2. Samuel AR, Knowles NJ. Foot-and-mouth disease type O viruses exhibit genetically and geographically distinct evolutionary lineages (topotypes). J Gen Virol. 2001;82(3): 609–21. doi: 10.1099/0022-1317-82-3-609 11172103.

3. Jinding C, Mingqiu Z, Hui KH, Leung FC. Molecular characterization of foot-and-mouth disease virus in Hong Kong during 2001–2002. Virus Genes. 2006;32(2): 139–43. doi: 10.1007/s11262-005-6869-1 16604445.

4. Qian F, Chen X, Ma O, Liu Y, Ding M, Collins RA, et al. Serotype and VP1 gene sequence of a foot-and-mouth disease virus from Hong Kong. Biochem Biophys Res Commun. 2002;30: 715–721. doi: 10.1016/S0006-291X(03)00250-X 12646228.

5. Zhang Q, Liu X, Fang Y, Pan L, Lv J, Zhang Z, et al. Evolutionary analysis of structural protein gene VP1 of foot-and-mouth disease virus serotype Asia 1. Scientific World Journal. 2015;2015. doi: 10.1155/2015/734253 25793223.

6. Martinez MA, Dopazo J, Hernandez J, Mateu MG, Sobrino F, Domingo E, et al. Evolution of the capsid protein genes of foot-and-mouth disease virus: antigenic variation without accumulation of amino acid substitutions over six decades.  J Virol. 1992;66(6): 3557–65. 1316467.

7. Di Nardo A, Knowles NJ, Paton DJ. Combining livestock trade patterns with phylogenetics to help understand the spread of foot and mouth disease in sub-Saharan Africa, the Middle East and Southeast Asia. Rev Sci Tech Off Int Epiz. 2011;30(1): 63–85. doi: 10.20506/rst.30.1.2022 21809754.

8. Reid SM, Grierson SS, Ferris NP, Hutchings GH, Alexandersen S. Evaluation of automated RT-PCR to accelerate the laboratory diagnosis of foot-and-mouth disease virus. J Virol Methods. 2003;107(2): 129–39. doi: 10.1016/s0166-0934(02)00210-0 12505626.

9. Knowles NJ, Wadsworth J, Bachanek-Bankowska K, King DP. VP1 sequencing protocol for foot and mouth disease virus molecular epidemiology. Rev Sci Tech Off Int Epiz. 2016;35(3): 741–55. doi: 10.20506/rst.35.3.2565 28332654.

10. James AD, Rushton J. The economics of foot and mouth disease. Rev Sci Tech Off Int Epiz. 2002;21(3): 637–41.

11. Forman S, Le Gall F, Belton D, Evans B, François JL, Murray G, et al. Moving towards the global control of foot and mouth disease: an opportunity for donors. Rev Sci Tech Off Int Epiz. 2009;28(3): 883. doi: 10.20506/rst.28.3.1935 20462147.

12. Gurumurthy CB, Sanyal A, Venkataramanan R, Tosh C, George M, Hemadri D. Genetic diversity in the VP1 gene of foot-and-mouth disease virus serotype Asia 1. Arch Virol. 2002;147(1): 85–102. doi: 10.1007/s705-002-8304-y 11855637.

13. Lavine JS, Poss M, Grenfell BT. Directly transmitted viral diseases: modeling the dynamics of transmission. Trends Microbiol. 2008;16(4):165–72. doi: 10.1016/j.tim.2008.01.007 18356058.

14. Fox G, Parry NR, Barnett PV, McGinn B, Rowlands DJ, Brown F. The cell attachment site on foot-and-mouth disease virus includes the amino acid sequence RGD (arginine-glycine-aspartic acid). J Gen Virol. 1989;70(3):625–37. doi: 10.1099/0022-1317-70-3-625 2543752.

15. Tosh C, Sanyal A, Hemadri D, Venkataramanan R. Phylogenetic analysis of serotype A foot-and-mouth disease virus isolated in India between 1977 and 2000. Arch Virol. 2002;147(3): 493–513. doi: 10.1007/s007050200002 11958451

16. Jackson T, Sharma A, Ghazaleh RA, Blakemore WE, Ellard FM, Simmons DL, et al. Arginine-glycine-aspartic acid-specific binding by foot-and-mouth disease viruses to the purified integrin alpha (v) beta3 in vitro. J Virol. 1997;71(11): 8357–61. 9343190.

17. Knowles NJ, Samuel AR. Molecular epidemiology of foot-and-mouth disease virus. Virus Res. 2003;91(1): 65–80. doi: 10.1016/s0168-1702(02)00260-5 12527438.

18. Knowles NJ, Samuel AR, Davies PR, Midgley RJ, Valarcher JF. Pandemic strain of foot-and-mouth disease virus serotype O. Emerg Infect Dis. 2005;11(12):1887. doi: 10.3201/eid1112.050908 16485475.

19. Beck E, Strohmaier K. Subtyping of European foot-and-mouth disease virus strains by nucleotide sequence determination. J Virol. 1987;61(5): 1621–9. 3033288

20. Tosh C, Hemadri D, Sanyal A, Bandyopadhyay SK. Genetic and antigenic analysis of two recently circulating genotypes of type A foot-and-mouth disease virus in India: evidence for positive selection in the capsid-coding genes. Arch Virol. 2003;148(5): 853–69. doi: 10.1007/s00705-002-0968-2 12721795.

21. Rweyemamu M, Roeder P, Mackay D, Sumption K, Brownlie J, Leforban Y, et al. Epidemiological patterns of foot‐and‐mouth disease worldwide. Transbound Emerg Dis. 2008;55(1): 57–72. doi: 10.1111/j.1865-1682.2007.01013.x 18397509.

22. Abdul-Hamid NF, Hussein NM, Wadsworth J, Radford AD, Knowles NJ, King DP. Phylogeography of foot-and-mouth disease virus types O and A in Malaysia and surrounding countries. Infect Genet Evol. 2011;11(2): 320–8. doi: 10.1016/j.meegid.2010.11.003 21093614.

23. Casey MB, Lembo T, Knowles NJ, Fyumagwa R, Kivaria F, Maliti H, et al. Patterns of Foot-and-Mouth Disease Virus Distribution in Africa: The Role of Livestock and Wildlife in Virus Emergence. In The Role of Animals in Emerging Viral Diseases 2014; pp. 21–38. doi: 10.1016/B978-0-12-405191-1.00002–8

24. Sumption K, Rweyemamu M, Wint W. Incidence and distribution of foot‐and‐mouth disease in Asia, Africa and South America; combining expert opinion, official disease information and livestock populations to assist risk assessment. Transbound Emerg Dis. 2008;55(1): 5–13. doi: 10.1111/j.1865-1682.2007.01017.x 18397505.

25. Cottam EM, Haydon DT, Paton DJ, Gloster J, Wilesmith JW, Ferris NP, et al. Molecular epidemiology of the foot-and-mouth disease virus outbreak in the United Kingdom in 2001.  J Virol. 2006;80(22): 11274–82. doi: 10.1128/JVI.01236-06 16971422.

26. Valarcher JF, Knowles NJ, Ferris NP, Paton DJ, Zakharov V, Sherbakov A, et al. Recent spread of FMD virus serotype Asia 1. Vet Rec. 2005;157(1):30. doi: 10.1136/vr.157.1.30 15995241

27. Donaldson AI. Foot-and-mouth disease in Taiwan. Vet Rec. 1997;140(15):407. 9141228.

28. Gleeson LJ. A review of the status of foot and mouth disease in South-East Asia and approaches to control and eradication. Rev Sci Tech Off Int Epiz. 2002;21(3): 465–72. doi: 10.20506/rst.21.3.1346 12530354.

29. Sakamoto K, Yoshida K. Recent outbreaks of foot and mouth disease in countries of east Asia. Rev Sci Tech Off Int Epiz. 2002;21(3): 459–61.

30. Chhetri BK, Perez AM, Thurmond MC. Factors associated with spatial clustering of foot-and-mouth disease in Nepal. Trop Anim Health Prod. 2010;42(7): 1441–9. doi: 10.1007/s11250-010-9573-7 20603723.

31. Loth L, Osmani MG, Kalam MA, Chakraborty RK, Wadsworth J, Knowles NJ, et al. Molecular characterization of foot‐and‐mouth disease virus: implications for disease control in Bangladesh. Transbound Emerg Dis. 2011;58(3): 240–6. doi: 10.1111/j.1865-1682.2011.01206.x 21320294.

32. Subramaniam S, Pattnaik B, Sanyal A, Mohapatra JK, Pawar SS, Sharma GK, et al. Status of Foot‐and‐mouth Disease in India. Transbound Emerg Dis. 2013;60(3): 197–203. doi: 10.1111/j.1865-1682.2012.01332.x 22551096.

33. Vosloo W, Bastos AD, Sangare O, Hargreaves SK, Thomson GR. Review of the status and control of foot and mouth disease in sub-Saharan Africa. Rev Sci Tech Off Int Epiz. 2002;21(3): 437–45. doi: 10.20506/rst.21.3.1349 12523685.

34. Vosloo W, Dwarka RM, Bastos AD, Esterhuysen JJ, Sahle M, Sangare O. Molecular epidemiological studies of foot-and-mouth disease virus in sub-Saharan Africa indicate the presence of large numbers of topotypes: implications for local and international control. Report of the standing technical committee of the European Commission for the Control of Foot-and-Mouth Disease. 2004:12–5.

35. Tekleghiorghis T, Moormann RJ, Weerdmeester K, Dekker A. Foot‐and‐mouth disease transmission in Africa: implications for control, a review. Transbound Emerg Dis. 2016;63(2): 136–51. doi: 10.1111/tbed.12248 25052411.

36. Balinda SN, Sangula AK, Heller R, Muwanika VB, Belsham GJ, Masembe C, et al. Diversity and transboundary mobility of serotype O foot-and-mouth disease virus in East Africa: implications for vaccination policies. Infect Genet Evol. 2010;10(7): 1058–65. doi: 10.1016/j.meegid.2010.06.017 20619358.

37. Lin YL, Jong MH, Huang CC, Shieh HK, Chang PC. Genetic and antigenic characterization of foot-and-mouth disease viruses isolated in Taiwan between 1998 and 2009. Vet Microbiol. 2010;145(1–2): 34–40. doi: 10.1016/j.vetmic.2010.03.003 20362404.

38. Abeyratne SA, Amarasekera SS, Ranaweera LT, Salpadoru TB, Thilakarathne SM, Knowles NJ, et al. The phylogenetic analysis of VP1 genomic region in foot-and-mouth disease virus serotype O isolates in Sri Lanka reveals the existence of'Srl-97', a newly named endemic lineage. PloS one. 2018;13(3): e0194077. doi: 10.1371/journal.pone.0194077 29570746

39. Wijewardana BD, Fernando WW. The position of foot-and-mouth disease in Sri Lanka during 1977–1981 [serotype O, cattle]. Revue Scientifique et Technique de l'OIE. 1983.

40. Fernando WW. Foot-and-mouth disease in Ceylon. I. History, epizootiology and the economic losses. Ceylon Vet J. 1969.

41. Fernando WW. Foot-and-mouth disease in Ceylon. II. Serological types of the virus present in Ceylon. Ceylon Vet J. 1969.

42. Gunarathne A, Kubota S, Kumarawadu P, Karunagoda K, Kon H. Is hiding foot and mouth disease sensitive behavior for farmers? A survey study in Sri Lanka. Asian-Australasian Journal of Animal Sciences. 2016;29(2): 280. doi: 10.5713/ajas.15.0241 26732453

43. Bachanek-Bankowska K, Di Nardo A, Wadsworth J, Mioulet V, Pezzoni G, Grazioli S, et al. Reconstructing the evolutionary history of pandemic foot-and-mouth disease viruses: the impact of recombination within the emerging O/ME-SA/Ind-2001 lineage. Sci Rep. 2018; 8(1):14693. doi: 10.1038/s41598-018-32693-8 30279570.

44. Fernando W.W.H.S. and Mettananda I. The introduction and spread of foot and mouth disease virus type C in Sri Lanka. Ceylon Vet J. 1980; 28: 51–54.

45. Ibrahim MN, Staal SJ, Daniel SL, Thorpe W. Appraisal of the Sri Lanka Dairy Sector volume 2: Main report.

46. Kitching RP, Donaldson AI. Collection and transportation of specimens for vesicular virus investigation. Rev Sci Tech Off Int Epiz. 1987;6(1):263–72.

47. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33(7): 1870–1874. doi: 10.1093/molbev/msw054 27004904.

48. Akaike H. A new look at the statistical model identification. IEEE Trans Automat Contr. 1974; 19(6): 716–723.

49. Cavanaugh JE. Unifying the derivations for the Akaike and corrected Akaike information criteria. Statistics & Probability Letters. 1997;33(2): 201–8.

50. Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media; 2003 Dec 4.

51. Minin V, Abdo Z, Joyce P, Sullivan J. Performance-based selection of likelihood models for phylogeny estimation. Systematic Biology. 2003;52(5): 674–83. doi: 10.1080/10635150390235494 14530134.

52. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol. 25: 1253–1256. doi: 10.1093/molbev/msn083 18397919.

53. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE), 2010. 2010; 1–8. Available from:

54. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006; 22(21): 2688–2690. doi: 10.1093/bioinformatics/btl446 16928733.

55. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 2008;57(5): 758–71. doi: 10.1080/10635150802429642 18853362.

56. Rodriguez FJ, Oliver JL, Marin A, Medina JR. The general stochastic model of nucleotide substitution. J Theor Biol. 1990;142(4): 485–501. doi: 10.1016/s0022-5193(05)80104-3 2338834.

57. Huelsenbeck JP, Ronquist F, MrBayes: Bayesian inference of phylogeny. Bioinformatics 2001;17: 754–755. doi: 10.1093/bioinformatics/17.8.754 11524383.

58. Rambaut A, Drummond AJ. Tracer ver. 1.4. See

59. Rambaut, A. (2014) FigTree, a graphical viewer of aphylogenetic trees. Available from: (Date of access: 20.08.2017).

60. Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1): 37–48. doi: 10.1093/oxfordjournals.molbev.a026036 10331250.

61. Clement M, Snell Q, Walker P, Posada D, Crandall K. TCS: estimating gene genealogies. In ipdps; 2002. p. 0184. IEEE. doi: 10.1109/IPDPS.2002.1016585

62. French N, Yu S, Biggs P, Holland B, Fearnhead P, Binney B, et al. Evolution of Campylobacter species in New Zealand. Campylobacter ecology and evolution, Caister Academic Press, Swansea University, Swansea, UK; 2014. Pp. 221–240.

63. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 2006;23(10): 1891–901. doi: 10.1093/molbev/msl051 16818476.

64. Pond SL, Frost SD. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005;21(10): 2531–3. doi: 10.1093/bioinformatics/bti320 15713735.

65. Sáiz JC, Sobrino F, Dopazo J. Molecular epidemiology of foot-and-mouth disease virus type O. J Gen Virol. 1993;74(10):2281–5. doi: 10.1099/0022-1317-74-10-2281 8409952.

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