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Diversity of SAT2 foot-and-mouth disease virus in Sudan: implication for diagnosis and control

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Abstract

Like other East African countries, Sudan experienced circulation of more than one topotype of SAT2 foot-and-mouth disease virus (FMDV). In Sudan, topotype XIII of SAT2 virus was recorded in 1977 and 2008 and topotype VII in 2007, 2010, 2013, 2014 and 2017. This work evaluated the impact of such diversity on diagnosis and control. After one or three doses of a vaccine derived from a Sudanese SAT2 virus of topotype VII originated in 2010, heterologous neutralizing antibody titres with Sudanese SAT2 viruses in 2008 were ≤ 1.2 log 10, not consistent with likely protection. Simultaneously, homologous titres were 1.65 (after one dose) or 1.95 and 2.55 log10 (after 3 doses). When r1 values between the vaccine virus and the SAT2 viruses isolated in 2008, whilst topotype XIII was circulating, were derived, values (≈ 0.00) suggested similarly poor antigenic relationship and unlikely cross protection. Concurrently, SAT2 positive field sera from Sudan in 2016 were not unvaryingly identified by virus neutralization tests (VNT) employing SAT2 viruses from 2010 and 2008. Proportions of positive sera by SAT2 virus from 2010 were always higher than those by viruses from 2008; consistent with the more frequent and recent circulation of topotype VII prior to 2016. Proportions by SAT2 virus from 2010 were 0.68 (± 0.1) in one location (n = 72), 0.39 (± 0.1) in another one (n = 94) and 0.52 (± 0.1) in the whole test group (n = 166). Corresponding values by viruses of 2008 were 0.53 (± 0.1), 0.27 (± 0.1) and 0.38 (± 0.1). In the whole test group, differences were statistically significant (p = .02339). Like post-vaccination sera, field sera (natural immunity) showed no considerable cross neutralization between topotype VII and presumably XIII; almost 45% (43/96) of SAT2 positive field sera were positive to one topotype but not to the other. Experimental and surveillance findings emphasized the implication of SAT2 diversity in Sudan. It is concluded that it is difficult to control SAT2 infection in Sudan using a monovalent vaccine. Beside a prophylactic vaccine from topotype VII, stockpiling of antigens from topotype XIII and enhanced virological surveillance with rapid genotyping and matching studies are necessary approaches. When more frequent circulation of more than one SAT2 topotype occurs, retrospective diagnosis by serological surveys could be problematic or imprecise.

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References

  • Acharya A, Fry E, Stuart D, Fox G, Rowlands D, Brown F (1990) The structure of foot-and-mouth disease virus: implications for its physical and biological properties. Vet Microbiol 23:21–34

    Article  CAS  Google Scholar 

  • Ahmed HA, Salem SA, Habashi AR, Arafa AA, Aggour MG, Salem GH, Gaber AS, Selem O, Abdelkader SH, Knowles NJ, Madi M, Valdazo-González B, Wadsworth J, Hutchings GH, Mioulet V, Hammond JM, King DP (2012) Emergence of foot-and-mouth disease virus SAT 2 in Egypt during 2012. Transbound Emerg Dis 59(6):476–481. https://doi.org/10.1111/tbed.12015 (Epub 2012 Oct 1 PMID: 23025522)

    Article  CAS  PubMed  Google Scholar 

  • Alfouz W, Raouf YA, Ahmed NH, Hamid AE, Osman NA (2021) Sero-epidemiology of foot-and-mouth disease in Darfur area, Western Sudan. Vet Res Commun. doi: https://doi.org/10.1007/s11259-021-09815-1. Epub ahead of print. PMID: 34476716.

  • Anon (2012) World Reference Laboratory for Foot-and-Mouth Disease. Foot-and-Mouth Disease vaccine matching strain differentiation report.

  • Anon (2016) Annual report of the Central Veterinary Research Laboratory. Khartoum, Sudan.

  • Anon (2018) Annual report OIE/FAO FMD Reference Laboratory Network. Ed. by Donald King, Antonello Di Nardo and Mark Henstock The Pirbright Institute UK.

  • Ayelet G, Mahapatra M, Gelaye E, Egziabher BG, Rufeal T, Sahle M, Ferris NP et al (2009) Genetic Characterization of Foot-and-Mouth Disease Viruses, Ethiopia, 1981–2007. Emerg Infect Dis 15(9):1409–1417

    Article  CAS  Google Scholar 

  • Bahnemann HG (1990) Inactivation of viral antigens for vaccine preparation with particular reference to the application of binary ethylenimine. Vaccine 8:299–303

    Article  CAS  Google Scholar 

  • Barteling SJ (2002) Method of preparing aluminium hydroxide gel. Document No. “WO/2002/094316” November (2002). http:// www.sumobrain.com/patents/WO2002094316. html

  • Bastos ADS, Haydon DT, Sangare´ O, Boshoff CI, Edrich JL, Thomson GR, (2003) The implications of virus diversity within the SAT 2 serotype for control of foot-and-mouth disease in sub-Saharan Africa. J Gen Virol 84:1595–1606

    Article  CAS  Google Scholar 

  • Blignaut B, van Heerden J, Reininghaus B, Fosgate GT, Heath L (2020) Characterization of SAT2 foot-and-mouth disease 2013/2014 outbreak viruses at the wildlife-livestock interface in South Africa. Transbound Emerg Dis 67(4):1595–1606. https://doi.org/10.1111/tbed.13493 (Epub 2020 Feb 12 PMID: 31984622)

    Article  CAS  PubMed  Google Scholar 

  • Borrego B, Camarero JA, Mateu MG, Domingo E (1995) A highly divergent antigenic site of foot-and-mouth disease virus retains its immunodominance. Viral Immunol 8:11–18

    Article  CAS  Google Scholar 

  • Browning CFJ, Di Nardo A, Henry L, Pollard T, Hendry L, Romey A, Relmy A, Eble P, EmilianaBrocchi E, Grazioli S, King DP, Ludi AB (2020) Inter-laboratory comparison of 2 ELISA kits used for foot-and-mouth disease virus nonstructural protein serology. J Vet Diagn Invest 32(6):933–937

    Article  CAS  Google Scholar 

  • Chamberlain K, Fowler VL, Barnett PV, Gold S, Wadsworth J, Knowles NJ, Jakson T (2015) Identification of a novel cell culture adaptation site on the capsid of foot-and-mouth disease virus. J Gen Virol 96:2684–2692

    Article  CAS  Google Scholar 

  • Crowther JR, Rowe CA, Butcher R (1993) Characterization of monoclonal antibodies against a type SAT-2 foot-and-mouth disease virus. Epidemiol Infect 111:391–406

    Article  CAS  Google Scholar 

  • Dill V, Hoffmann B, Zimmer A, Beer M, Eschbaumer M (2018) Influence of cell type and cell culture media on propagation of foot-and-mouth disease virus with regard to vaccine quality. Virol J 15:46–57

    Article  Google Scholar 

  • Doel TR (2005) Natural and vaccine induced immunity to FMD. Curr Top Microbiol Immunol 288:103–131. https://doi.org/10.1007/3-540-27109-0_5 (PMID: 15648176)

    Article  CAS  PubMed  Google Scholar 

  • Domenech J, Lubroth J, Eddi C, Martin V, Roger F (2006) Regional and international approaches on prevention and control of animal transboundary and emerging diseases. Ann. N.Y. Acad Sci 1081:90–107. https://doi.org/10.1196/annals.1373.010

    Article  CAS  Google Scholar 

  • Fletcher RH, Fletcher SW (2005) Clinical Epidemiology: The Essentials, 4th edn. Lippincott Williams & Wilkins, Philadelphia, Pennsylvania, USA

    Google Scholar 

  • Grazioli S, Ferris NP, Dho G, Pezzoni G, Morris AS, Mioulet V, Brocchi E (2020) Development and Validation of a Simplified Serotyping ELISA Based on Monoclonal Antibodies for the Diagnosis of Foot-and-Mouth Disease Virus Serotypes O, A, C and Asia 1. Transbound Emerg Dis 67:3005–3015

    Article  CAS  Google Scholar 

  • Grubman MJ, Baxt B (2004) Foot-and-mouth disease. Clin Microbiol Rev 17(2):465–493

    Article  CAS  Google Scholar 

  • Habiela M, Ferris NP, Hutching GH, Wadsworth J, Reid SM, Madi M et al (2010) Molecular characterization of foot-and-mouth disease Viruses collected from Sudan. Transbound Emerg Dis 57(5):305–314

    Article  CAS  Google Scholar 

  • Habiela M, Seago J, Perez-Martin E, Waters R, Windsor M, Salguero FJ, Wood J et al (2014) Laboratory animal models to study foot-and-mouth disease: a review with emphasis on natural and vaccine-induced immunity. J Gen Virol 2014(95):2329–2345

    Article  Google Scholar 

  • Hall MD, Knowles NJ, Wadsworth J, Rambaut A, Woolhouse MEJ (2013) Reconstructing geographical movements and host species transitions of foot-and-mouth disease virus serotype SAT 2. mBio 4(5):e00591–13. doi:https://doi.org/10.1128/mBio.00591-13.

  • Hamblin C, Barnett ITR, Crowther JR (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

    Article  CAS  Google Scholar 

  • Hedger RS, Barnett ITR, D.V. Gradwell DV, Dias PT (1982) Serological tests for foot-and-mouth disease in bovine serum samples. Problems of interpretation Rev. sci. tech. Off. int. Epiz., 1 (2), 387–393.

  • http://www.wrlfmd.org/. World Reference Laboratory for Foot-and-Mouth Disease Molecular epidemiology reports.

  • Kärber G (1931) Beitrag zur Kollek tiven Behandlung phormakologischer Reihenversuche. Arch Exp Path Pharmak 162:480–487

    Article  Google Scholar 

  • Knezevic A (2008) StatNews # 73: Cornell University Statistical Consulting Unit, Overlapping Confidence Intervals and Statistical Significance, available from http://www.cscu.cornell.edu/news/statnews/stenews

  • Knight-Jones TJ, Rushton J (2013) The economic impacts of foot and mouth disease—what are they, how big are they and where do they occur? Prev Vet Med 112:161–173. https://doi.org/10.1016/j.prevetmed.2013.07.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knowles NJ, Samuel AR (2003) Molecular epidemiology of foot-and-mouth disease virus. Virus Res 91:65–80

    Article  CAS  Google Scholar 

  • Lycett S, Tanya VN, Hall M, King DP, Mazeri S, Mioulet V, Knowles NJ et al (2019) The evolution and phylodynamics of serotype A and SAT2 foot-and-mouth disease viruses in endemic regions of Africa. Sci Rep 9:5614

    Article  CAS  Google Scholar 

  • Maree FF, Blignaut B, Esterhuysen JJ, de Beer TAP, Theron J, O’Neill HG, 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(Pt 10):2297–2309. https://doi.org/10.1099/vir.0.032839-0 (Epub 2011 Jun 22 PMID: 21697350)

    Article  CAS  PubMed  Google Scholar 

  • Mateu MG, Camarero JA, Giralt E, Andreu D, Domingo E (1995) Direct evaluation of the immunodominance of a major antigenic site of foot-and-mouth disease virus in a natural host. Virology 206:298–306

    Article  CAS  Google Scholar 

  • Mattion N, Goris N, Willems T, Robiolo B, Maradei E, Beascoechea CP, Perez A et al (2009) Some guidelines for determining foot-and-mouth disease vaccine strain matching by serology. Vaccine 27:741–747

    Article  Google Scholar 

  • McCullough KC, Bruckner L, Schaffner R, Fraefel W, Müller HK, Kihm U (1992) Relationship between the anti-FMD virus antibody reaction as measured by different assays, and protection in vivo against challenge infection. Vet Microbiol 30(2–3):99–112

    Article  CAS  Google Scholar 

  • Mohapatra JK, Pandey LK, Rai DK, Das B, Rodriguez LL, Rout M, Subramaniam S, Sanyal A, Rieder E, Pattnaik B (2015) Cell culture adaptation mutations in foot-and-mouth disease virus serotype A capsid proteins: implications for receptor interactions. J Gen Virol 96:553–564

    Article  CAS  Google Scholar 

  • OIE (2018). Manual of Standard Diagnostic Tests and Vaccine for Terrestrial Animals. Foot-and-mouth disease,. PP.1–32.

  • Paton DJ, Di Nardo A, Knowles NJ, Wadsworth J, Pituco EM, Cosivi O, Rivera AM, Kassimi LB, Brocchi E, de Clercq K, Carrillo C, Maree FF, Singh RK, Vosloo W, Park M, Sumption KJ, Ludi AB, King DP (2021) The history of foot-and-mouth disease virus serotype C: the first known extinct serotype? Virus Evolution, Volume 7, Issue 1, January 2021, veab009, https://doi.org/10.1093/ve/veab009

  • Paton DJ, Valarcher JF, Bergemann I, Matlho OG, Zakharov VM, Palma EL, Thomson GR (2005) Selection of foot and mouth disease vaccine strains – a review. Rev Sci Tech off Int Epiz 24(3):981–993

    Article  CAS  Google Scholar 

  • Pay TWF, Hingley PJ (1987) Correlation of 140S antigen dose with the serum neutralizing antibody response and the level of protection induced in cattle by foot and mouth disease vaccines. Vaccine 5:60–64

    Article  CAS  Google Scholar 

  • Pay TWF, Hingley PJ (1992) Foot and mouth disease vaccine potency tests in cattle: the interrelationship of antigen dose, serum neutralizing antibody response and protection from challenge. Vaccine 10:699–706

    Article  CAS  Google Scholar 

  • Periera HG (1978) Antigenic variation in relation to epidemiology and control of foot and mouth. Br Vet J 134:58–62

    Article  Google Scholar 

  • Raouf YA, Ali BH, El Amin MA, Al shallali AM, Hiba Hashim, Habiela M, (2010) Laboratory investigation of three outbreaks of foot-and-mouth disease at central Sudan and the disease type situation. Bull Anim Hlth Prod Afr 58(4):308–314

    Google Scholar 

  • Reeve R, Borley DW, Maree FF, Upadhyaya S, Lukhwareni A, Esterhuysen JJ et al (2016) Tracking the Antigenic Evolution of Foot-and-Mouth Disease Virus. PLoS ONE 11(7):e0159360. https://doi.org/10.1371/journal.pone.0159360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roeder PL, Le Blanc Smith PM (1987) Detection and typing of foot-and-mouth disease virus by enzyme-linked immunosorbent assay: a sensitive, rapid and reliable technique for primary diagnosis. Res Vet Sci 43:225–232

    Article  CAS  Google Scholar 

  • Rweyemamu MM (1984) Antigenic variation in foot-and mouth disease: studies based on the virus neutralization reaction. J Biol Standard 12:323–337

    Article  CAS  Google Scholar 

  • Rweyemamu MM, Booth JC, Head M et al (1978) Microneutralization tests for serological typing and subtyping of foot-and-mouth disease virus strains. J Hyg (lond) 81:107–123

    Article  CAS  Google Scholar 

  • Sahle M, Dwarka RM, Venter EH, Vosloo W (2007) Study of the genetic heterogeneity of SAT-2 foot-and-mouth disease virus in sub-Saharan Africa with specific focus on East Africa. Onderstepoort J Vet Res 74(4):289–299. https://doi.org/10.4102/ojvr.v74i4.115 (PMID: 18453238)

    Article  CAS  PubMed  Google Scholar 

  • Samuel AR, Knowles NJ (2001) Foot-and-mouth disease type O viruses exhibit genetically and geographically distinct evolutionary lineages (topotypes). J Gen Virol 82:609–621

    Article  CAS  Google Scholar 

  • Sirdar MM, Fosgate GT, Blignaut B, Gummow B, Shileyi B, Lazarus DD, Mutowembwa P, van der Merwe D, Heath L (2019) A novel method for performing antigenic vaccine matching for foot-and-mouth disease in absence of the homologous virus. Vaccine. 14;37(35):5025–5034. doi: https://doi.org/10.1016/j.vaccine.2019.07.002. Epub 2019 Jul 8. PMID: 31296377.

  • Soltan MA, Dohreig RMA, Abbas H, Ellawa M, Yousif I, Aly AE, Wasfy M, El-Sayed MM (2019) Emergence of foot and mouth disease virus, Lib-12 lineage of topotype VII, serotype SAT2 in Egypt, 2018. Transbound Emerg Dis 66(3):1105–1106. https://doi.org/10.1111/tbed.13152 (Epub 2019 Mar 9 PMID: 30779326)

    Article  PubMed  Google Scholar 

  • Strohmaier K, Franz R, Adam KH (1982) Location and characterization of the antigenic portion of the foot and mouth disease virus immunizing protein. J Gen Virol 59:295–306

    Article  CAS  Google Scholar 

  • Tekleghiorghis T, Moormann RJ, Weerdmeester K, Dekker A (2014) Serological evidence indicates that foot-and-mouth disease virus serotype O, C and SAT1 are most dominant in Eritrea. Transbound Emerg Dis 61(6):e83-88. https://doi.org/10.1111/tbed.12065 (Epub 2013 Mar 11 PMID: 23480728)

    Article  CAS  PubMed  Google Scholar 

  • Thrusfield M (2007) Veterinary Epidemiology, 3rd edn. Blackwell Science Ltd., Oxford, UK

    Google Scholar 

  • www.sociostatistics.com (SPSS: Statistical Packages for Social Sciences).

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Acknowledgements

The Director CVRL, late Dr. Yousif Hussien, encouraged enthusiastically this work. Efforts of the technical staff at the Department of FMD-CVRL were indispensible.

Funding

This work was funded and supported by the Government of Sudan (GoS).

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  1. Department of Foot-and-Mouth Disease, Central Veterinary Research Laboratory (CVRL), Soba, P.O. Box 8067, Al Amarat, Khartoum, Sudan

    Yazeed A/Raouf & Inas Ibrahim

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  1. Yazeed A/Raouf
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  2. Inas Ibrahim
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Yazeed A/Raouf carried out some of the laboratory work, analyzed data and wrote most of the manuscript. Inas Ibrahim carried out part of the laboratory work and wrote parts of the materials and methods section.

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Correspondence to Yazeed A/Raouf.

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Animal species used were indicated for the type of the study. Minimum numbers required to maintain the scientific quality of the experiment were included. Throughout the experiment good animal welfare was provided and all experimental procedures were approved by the Ethics Scientific Committee of CVRL-Sudan (1/A/1/824).

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A/Raouf, Y., Ibrahim, I. Diversity of SAT2 foot-and-mouth disease virus in Sudan: implication for diagnosis and control. Vet Res Commun 46, 789–798 (2022). https://doi.org/10.1007/s11259-022-09899-3

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