Risk of introducing African horse sickness virus into the Netherlands by international equine movements

Preventive Veterinary Medicine

Volumn 106, Issue 2, 2012, Pages 108-122

  de Vos, C J ^a   Hoek, C A ^a   Nodelijk, G ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

African horse sickness; Equine movements; Import risk assessment; Quantitative risk model

Indexed keywords

AFRICAN HORSE SICKNESS; AFRICAN HORSE SICKNESS VIRUS; ANIMAL; ANIMAL DISEASE; ARTICLE; BIOLOGICAL MODEL; CERATOPOGONIDAE; DISEASE CARRIER; DISEASE TRANSMISSION; EPIDEMIC; FEEDING BEHAVIOR; HORSE; INCIDENCE; NETHERLANDS; PHYSIOLOGY; PREVALENCE; RISK; SEASON; SENSITIVITY AND SPECIFICITY; SPECIES DIFFERENCE; TRAFFIC AND TRANSPORT; VIROLOGY;

AFRICAN HORSE SICKNESS; AFRICAN HORSE SICKNESS VIRUS; ANIMALS; CERATOPOGONIDAE; DISEASE OUTBREAKS; EQUIDAE; FEEDING BEHAVIOR; HORSES; INCIDENCE; INSECT VECTORS; MODELS, BIOLOGICAL; NETHERLANDS; PREVALENCE; RISK; SEASONS; SENSITIVITY AND SPECIFICITY; SPECIES SPECIFICITY; TRANSPORTATION;

AFRICAN HORSESICKNESS VIRUS; CULICOIDES IMICOLA; EQUIDAE; EQUUS ASINUS;

EID: 84865344498     PISSN: 01675877     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.prevetmed.2012.01.019     Document Type: Article

References (58)

1. Backer J.A., Nodelijk G. Transmission and control of African horse sickness in The Netherlands: a model analysis. PLoS ONE 2011, 6(8):e23066.
2. Barnard B.J. Circulation of African horsesickness virus in zebra (Equus burchelli) in the Kruger National Park, South Africa, as measured by the prevalence of type specific antibodies. Onderstepoort J. Vet. Res. 1993, 60:111-117.
3. Barnard B.J., Bengis R., Keet D., Dekker E.H. Epidemiology of African horsesickness: duration of viraemia in zebra (Equus burchelli). Onderstepoort J. Vet. Res. 1994, 61:391-393.
4. Baylis M., O'Connell L., Mellor P.S. Rates of bluetongue virus transmission between Culicoides sonorensis and sheep. Med. Vet. Entomol. 2008, 22:228-237.
5. Carpenter S., Lunt H.L., Arav D., Venter G.J., Mellor P.S. Oral susceptibility to bluetongue virus of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom. J. Med. Entomol. 2006, 43:73-78.
6. CBS, 2010. CBS STATLINE. Available at: (accessed 30.11.10, in Dutch). http://statline.cbs.nl/StatWeb/default.aspx.
7. CEC (Commission of the European Communities), 1990. Council Directive 90/426/EEC of 26 June 1990 on animal health conditions governing the movement and import from third countries of equidae. Off. J. Eur. Union L 224, 42-54.
8. CEC (Commission of the European Communities), 1992. Council Directive 92/36/EEC of 29 April 1992 amending, with regard to African horse sickness, Directive 90/426/EEC on animal health conditions governing the movement and import from third countries of equidae. Off. J. Eur. Union L 157, 28-29.
9. Coetzer J.A.W., Erasmus B.J. African horsesickness. Infectious Diseases of Livestock with Special Reference to Southern Africa 1994, 460-475. Oxford University Press, Oxford, UK. J.A.W. Coetzer, G.R. Thomson, R.C. Tustin (Eds.).
10. Coetzer J.A.W., Guthrie A.J. African horse sickness. Infectious Diseases of Livestock 2004, 1231-1246. Oxford University Press Southern Africa, Cape Town, South Africa. 2nd edition. J.A.W. Coetzer, R.C. Tustin (Eds.).
11. Ducheyne E., De Deken R., Bécu S., Codina B., Nomikou K., Mangana O., Georgiev G., Purse B.V., Hendrickx G. Quantifying the wind dispersal of Culicoides species in Greece and Bulgaria. Geospatial Health 2007, 1:177-189.
12. EFSA Risk of bluetongue transmission in animal transit, scientific opinion of the panel on animal health and welfare (question no. EFSA-Q-2008-436). Adopted on 11 September 2008. EFSA J. 2008, 795:1-56.
13. Elbers A.R.W., Backx A., Meroc E., Gerbier G., Staubach C., Hendrickx G., van der Spek A., Mintiens K. Field observations during the bluetongue serotype 8 epidemic in 2006. I. Detection of first outbreaks and clinical signs in sheep and cattle in Belgium, France and the Netherlands. Prev. Vet. Med. 2008, 87:21-30.
14. European Commission, 2010. Bluetongue. Restricted zones as of 10 November 2010. Available at: (accessed 2.12.10). http://ec.europa.eu/food/animal/diseases/controlmeasures/bt_restrictedzones-map.jpg.
15. Eurostat, 2010. Eurostat Statistics, External Trade, Traditional external trade database access (ComExt). Available at: (accessed 22.03.10). http://epp.eurostat.ec.europa.eu/newxtweb/.
16. FAO, 2009. Global Livestock Production and Health Atlas (GLiPHA). Available at: (accessed 9.12.09). http://kids.fao.org/glipha/.
17. Fassi-Fihri O., El Harrak M., Fassi-Fehri M.M. Clinical, virological and immune responses of normal and immunosuppressed donkeys (Equus asinus africanus) after inoculation with African horse sickness virus. Arch. Virol. Suppl. 1998, 14:49-56.
18. FEI, 2010. Fédération Equestre Internationale. Search centre. Available at: (accessed 30.07.10). http://search.fei.org/Search_Centre/Calendar/Pages/Search.aspx.
19. Gerry A.C., Sarto I., Monteys V., Moreno Vidal J.-O., Francino O., Mullens B.A. Biting rates of Culicoides midges (Diptera: Ceratopogonidae) on sheep in Northeastern Spain in relation to midge capture using UV light and carbon dioxide-baited traps. J. Med. Entomol. 2009, 46:615-624.
20. Gubbins S., Carpenter S., Baylis M., Wood J.L.N., Mellor P.S. Assessing the risk of bluetongue to UK livestock: uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number. J. R. Soc. Interface 2008, 5:363-371.
21. Hendrickx G., Gilbert M., Staubach C., Elbers A., Mintiens K., Gerbier G., Ducheyne E. A wind density model to quantify the airborne spread of Culicoides species during north-western Europe bluetongue epidemic, 2006. Prev. Vet. Med. 2008, 87:162-181.
22. House C., Mikiciuk P.E., Beminger M.L. Laboratory diagnosis of African horse sickness: comparison of serological techniques and evaluation of storage methods of samples for virus isolation. J. Vet. Diagn. Invest. 1990, 2:44-50.
23. House C., House J.A., Mebus C.A. A review of African horse sickness with emphasis on selected vaccines. Ann. N. Y. Acad. Sci. 1992, 653:228-232.
24. KNHS, 2010. Koninklijke Nederlandse Hippische Sportfederatie. Wedstrijdlijsten, Internationale deelnemers. Available at: (accessed 13.04.10, in Dutch). http://www.knhs.nl/istarts.asp.
25. KNMI, 2009. Klimatologie. Daggegevens van het weer in Nederland. Available at: (accessed 16.11.09, in Dutch). http://www.knmi.nl/klimatologie/daggegevens/selectie.cgi.
26. Laegreid W.W. Diagnosis of African horsesickness. Comp. Immun. Microbiol. Infect. Dis. 1994, 17:297-303.
27. LNV, 2007. Concept beleidsdraaiboek Afrikaanse Paardenpest. Versie 1.0, December 2007 (in Dutch).
28. Maan S., Maan N.S., van Rijn P.A., van Gennip R.G.P., Sanders A., Wright I.M., Batten C., Hoffmann B., Eschbaumer M., Oura C.A.L., Potgieter S.C., Nomikou K., Mertens P.P.C. Full genome characterization of bluetongue virus serotype 6 from the Netherlands 2008 and comparison to other field and vaccine strains. PLoS ONE 2010, 5(4):e10323.
29. MacLachlan N.J., Guthrie A.J. Re-emergence of bluetongue, African horse sickness, and other orbivirus diseases. Vet. Res. 2010, 41:35.
30. Mattioli R.C., Zinsstag J., Pfister K. African horse sickness and equine infectious anaemia serology in The Gambia. Trop. Anim. Health Prod. 1992, 24:207-208.
31. Meiswinkel R., Venter G.J., Nevill E.M. Vectors: Culicoides spp. Infectious diseases of livestock 2004, 93-136. Oxford University Press Southern Africa, Cape Town, South Africa. 2nd edition. J.A.W. Coetzer, R.C. Tustin (Eds.).
32. Meiswinkel R., Baldet T., De Deken R., Takken W., Delécolle J.-C., Mellor P.S. The 2006 outbreak of bluetongue in northern Europe - the entomological perspective. Prev. Vet. Med. 2008, 87:55-63.
33. Mellor P.S. African horse sickness: transmission and epidemiology. Vet. Res. 1993, 24:199-212.
34. Mellor P.S., Hamblin C. African horse sickness. Vet. Res. 2004, 35:445-466.
35. Mellor P.S., Boned J., Hamblin C., Graham S. Isolations of African horse sickness virus from vector insects made during the 1988 epizootic in Spain. Epidemiol. Infect. 1990, 105:447-454.
36. Mourits, M.C.M., Saatkamp, H.W., 2010. Kostenberekening van een uitbraak met Afrikaanse paardenpest in Nederland. Rapportage BO-08-010-021. Bedrijfseconomie, Wageningen Universiteit, Wageningen, Nederland (in Dutch).
37. OIE, 2009. World Animal Health Information Database (WAHID). Available at: (accessed 9.12.09). http://www.oie.int/wahis/public.php%3Fpage=disease_status_detail.
38. OIE, 2010a. Terrestrial Animal Health Code 2010. Available at: (accessed 30.11.10). http://www.oie.int/eng/normes/mcode/en_sommaire.htm.
39. OIE, 2010b. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2010. Available at: (accessed 30.11.10). http://www.oie.int/eng/normes/mmanual/A_summry.htm.
40. Paardensport.nu, 2010. Paardensport.nu, Evenementen, Internationale uitslagen. Available at: (accessed 13.04.10, in Dutch). http://www.paardensport.nu/internationale-uitslagen.html.
41. Palisade Corporation, 2004. Guide to using @Risk. Risk Analysis and Simulation Add-In for Microsoft Excel, Version 4.5. Palisade Corporation, Newfield, NY, USA.
42. Paweska J.T., Prinsloo S., Venter J. Oral susceptibility of South African Culicoides species to live-attenuated serotype-specific vaccine strains of African horse sickness virus (AHSV). Med. Vet. Entomol. 2003, 17:436-447.
43. Purse B.V., Mellor P.S., Rogers D.J., Samuel A.R., Mertens P.P.C., Baylis M. Climate change and the recent emergence of bluetongue in Europe. Nat. Rev. Microbiol. 2005, 3:171-181.
44. Rodriguez M., Hooghuis H., Castaňo Ma. African horse sickness in Spain. Vet. Microbiol. 1992, 33:129-142.
45. Sabirovic, M., López, M., Patel, K., Kingston, A., Hall, S., 2008. African horse sickness: potential risk factors and the likelihood for the introduction of the disease to the United Kingdom. Working document. DEFRA. Available at: (accessed 08.06.11). http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/monitoring/documents/ahs_uk081106.pdf.
46. Sloet van Oldruitenborgh-Oosterbaan, M.M., 2009. Inventarisatie van het voorkomen van Culicoides species (knutten) bij paarden in Nederland. Departement Gezondheidszorg Paard, Universiteit Utrecht, Nederland (in Dutch).
47. Takamatsu H., Mellor P.S., Mertens P.P.C., Kirkham P.A., Burroughs J.N., Parkhouse R.M.E. A possible overwintering mechanism for bluetongue virus in the absence of the insect vector. J. Gen. Virol. 2003, 84:227-235.
48. Townley P., Baker K.P., Quinn P.J. Preferential landing and engorging sites of Culicoides species landing on a horse in Ireland. Equine Vet. J. 1984, 16:117-120.
49. Van der Rijt R., Van den Boom R., Jongema Y., Sloet van Oldruitenborgh-Oosterbaan M.M. Culicoides species attracted to horses with and without insect hypersensitivity. Vet. J. 2008, 178:91-97.
50. Venter G.J., Paweska J.T. Virus recovery rates for wild-type and live-attenuated vaccine strains of African horse sickness virus serotype 7 in orally infected South African Culicoides species. Med. Vet. Entomol. 2007, 21:377-383.
51. Verwoerd D.W., Erasmus B.J. Bluetongue. Infectious diseases of livestock 2004, 1201-1220. Oxford University Press Southern Africa, Cape Town, South Africa. 2nd edition. J.A.W. Coetzer, R.C. Tustin (Eds.).
52. Vose D.J. Risk analysis in relation to the importation and exportation of animal products. Rev. Sci Tech. Off. Int. Epiz. 1997, 16:17-29.
53. Vose D. Risk Analysis. A Quantitative Guide 2008, John Wiley & Sons, Ltd., Chichester, England. third edition.
54. Wilson A., Mellor P.S. Bluetongue in Europe: vectors, epidemiology and climate change. Parasitol. Res. 2008, 103:S69-S77.
55. Wilson A., Mellor P.S. Bluetongue in Europe: past, present and future. Philos. Trans. R. Soc. B 2009, 364:2669-2681.
56. Wilson A., Mellor P.S., Szmaragd C., Mertens P.P.C. Adaptive strategies of African horse sickness virus to facilitate vector transmission. Vet. Res. 2009, 40:16.
57. Wittmann E.J., Mellor P.S., Baylis M. Using climate data to map the potential distribution of Culicoides imicola (Diptera: Ceratopogonidae) in Europe. Rev. Sci. Tech. Off. Int. Epiz. 2001, 20:731-740.
58. Wittmann E.J., Mellor P.S., Baylis M. Effect of temperature on the transmission of orbiviruses by the biting midge, Culicoides sonorensis. Med. Vet. Entomol. 2002, 16:147-156.