Parasitology Research

, Volume 103, Supplement 1, pp 69–77 | Cite as

Bluetongue in Europe: vectors, epidemiology and climate change

  • Anthony WilsonEmail author
  • Philip Mellor
Biting midges


Bluetongue (BT) is an economically important disease of ruminants resulting from infection with bluetongue virus (BTV). Historically, BT outbreaks in Europe were rare and short-lived. However, during the last 10 years, BTV has become firmly established in southern Europe and, since 2006, has begun to occur in northern Europe. There is a substantial body of evidence linking this emergence to climate change. In this paper, we summarise the recent emergence of BTV in Europe, review the known links between climate and BTV transmission, and discuss gaps in our knowledge of the epidemiology of BT and how they might be filled by current and future research.


Blood Meal Vector Species Bluetongue Virus Export Restriction Extrinsic Incubation Period 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors would like to thank John Kennedy at the Met Office Hadley Centre for providing information on seasonal temperature anomalies for the European region from the CRUTEM3 dataset, and Peter Mertens, Simon Gubbins and Karin Darpel at IAH Pirbright for comments on this article. The funding sources of this study are BBSRC (ref: BBS/0/00603) and Defra (ref: SE4104).


  1. Barzilai E (1982) BT antibodies in camel’s sera in Israel. Refuah Veterinarith 39:90–93Google Scholar
  2. Barzilai E, Tadmor A (1971) Multiplication of bluetongue virus in goats following experimental infection. Refuah Veterinarith 28(1):11–20Google Scholar
  3. Baylis M (2002) The re-emergence of bluetongue. Vet J 164(1):5–6PubMedCrossRefGoogle Scholar
  4. Bonneau KR, DeMaula CD, Mullens BA, MacLachlan NJ (2002) Duration of viraemia infectious to Culicoides sonorensis in bluetongue virus-infected cattle and sheep. Vet Microbiol 88:115–125PubMedCrossRefGoogle Scholar
  5. Breard E, Sailleau C, Nomikou K, Hamblin C, Mertens PPC, Mellor PS, El Harrak M, Zientara S (2007) Molecular epidemiology of bluetongue virus serotype 4 isolated in the Mediterranean Basin between 1979 and 2004. Virus Res 125(2):191–197PubMedCrossRefGoogle Scholar
  6. Breeland SG, Smith JP (1962) Observations on the importance of flight range in the control of culicoides in the Panama Canal Zone. Mosq News 22:147–154Google Scholar
  7. Callis J (1985) Bluetongue in the United States. Bluetongue and related orbiviruses: proceedings of an international symposium. Alan R Liss, Monterey, CAGoogle Scholar
  8. Caracappa S, Torina A, Guercio A, Vitale F, Calabrò A, Purpari G, Ferrantelli V, Vitale M, Mellor PS (2003) Identification of a novel bluetongue virus vector species of Culicoides in Sicily. Vet Rec 153(3):71–74PubMedGoogle Scholar
  9. Carpenter S, Lunt HL, Arav D, Venter GJ, Mellor PS (2006) Oral susceptibility to bluetongue virus of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom. J Med Entomol 43(1):73–78PubMedCrossRefGoogle Scholar
  10. Conte A, Goffredo M, Ippoliti C, Meiswinkel R (2007) Influence of biotic and abiotic factors on the distribution and abundance of Culicoides imicola and the Obsoletus complex in Italy. Vet Parasitol 150(4):333–344PubMedCrossRefGoogle Scholar
  11. Darpel KE, Batten CA, Veronesi E, Shaw AE, Anthony S, Bachanek-Bankowska K, Kgosana L, bin-Tarif A, Carpenter S, Müller-Doblies U, Takamatsu H, Mellor PS, Mertens PPC, Oura CAL (2007) Clinical signs and pathology shown by British sheep and cattle infected with bluetongue virus serotype 8 derived from the 2006 outbreak in northern Europe. Vet Rec 161(8):253–261PubMedGoogle Scholar
  12. De Clerq K, Vandenbussche F, Vandemeulebroucke E, Vanbinst T, De Leeuw I, Verheyden B, Goris N, Mintiens K, Meroc E, Herr C, Hooybergs J, Houdart P, Sustronck B, De Deken R, Maquet G, Bughin J, Saulmont M, Lebrun M, Bertels G, Miry C (2008) Transplacental bluetongue infection in cattle. Vet Rec 162(17):564.Google Scholar
  13. Elbers ARW, Mintiens K, Staubach C, Gerbier G, Meiswinkel R, Hendrickx G, Backx A, Conraths FJ, Meroc E, Ducheyne E, Gethmann J, Heesterbeek JAP, De Clerq K, Unger F, Stegeman JA (2007) Bluetongue virus serotype 8 epidemic in north-western Europe in 2006: preliminary findings. Society for Veterinary Epidemiology and Preventive Medicine, Dipoli, Espoo, FinlandGoogle Scholar
  14. European Commission (2000) Council directive 2000/75/EC of 20 November 2000 laying down specific provisions for the control and eradication of bluetongue. 2000/75/ECGoogle Scholar
  15. Eurostat (2007) Number of sheep. Key indicators on EU policy. Accessed October 10, 2007
  16. Federal Agency for the Safety of the Food Chain (2007) Bluetongue situation in Belgium. Standing Committee on the Food Chain and Animal Health, European Commission, BrusselsGoogle Scholar
  17. Gambles R (1949) Bluetongue of sheep in Cyprus. J Comp Pathol 59:176–190Google Scholar
  18. Gerry AC, Mullens BA (2000) Seasonal abundance and survivorship of Culicoides sonorensis (Diptera: Ceratopogonidae) at a Southern California Dairy, with reference to potential bluetongue virus transmission and persistence. J Med Entomol 37(5):675–688PubMedCrossRefGoogle Scholar
  19. Gibbs EPJ, Lawman MJP, Herniman KAJ (1979) Preliminary observations on transplacental infection of bluetongue virus in sheep—a possible overwintering mechanism. Res Vet Sci 27:118–120PubMedGoogle Scholar
  20. Gloster J, Mellor PS, Burgin L, Sanders C, Carpenter S (2007a) Will bluetongue come on the wind to the United Kingdom in 2007? Vet Rec 160(13):422–426PubMedGoogle Scholar
  21. Gloster J, Mellor PS, Manning AJ, Webster HN, Hort MC (2007b) Assessing the risk of windborne spread of bluetongue in the 2006 outbreak of disease in northern Europe. Vet Rec 160(2):54–56PubMedGoogle Scholar
  22. Gubbins S, Carpenter S, Baylis M, Wood JLN, Mellor PS (2008) Assessing the risk of bluetongue to UK livestock: uncertainty and sensitivity analysis of a temperature-dependent model for the basic reproductive number. J R Soc Interface 5(20):363–371PubMedCrossRefGoogle Scholar
  23. Henrich M, Reinacher M, Hamann H (2007) Lethal bluetongue virus infection in an alpaca. Vet Rec 161(22):764PubMedGoogle Scholar
  24. Hoogendam K (2007) International study on the economic consequences of outbreaks of bluetongue serotype 8 in north-western Europe. Van Hall Institute, LeeuwardenGoogle Scholar
  25. Howell PG (1963) Bluetongue. Emerging diseases of animals. FAO, Rome, pp 109–153Google Scholar
  26. Howell PG, Verwoerd DW (1971) Chapter VI. Interactions with mammalian hosts. In: Gard, S, Hallauer, C, Meyer, K (eds) Virology monographs 9: bluetongue virus. Springer-Verlag, New York, pp 56–71Google Scholar
  27. Hunt GJ, Tabachnick WJ, McKinnon CN (1989) Environmental factors affecting mortality of adult Culicoides variipennis (Diptera: Ceratopogonidae) in the laboratory. J Am Mosq Control Assoc 5(3):387–391PubMedGoogle Scholar
  28. International Society for Infectious Diseases (2006a) Bluetongue—Netherlands, Belgium, Germany (06): BTV-8. ProMED-mail 2006; 28 August: 20060828.2448. Accessed August 29, 2006
  29. International Society for Infectious Diseases (2006b) Bluetongue, ovine—Netherlands: confirmed. ProMED-mail 2006; 18 August: 20060818.2311. Accessed February 4, 2008
  30. International Society for Infectious Diseases (2007a) African horse sickness—Nigeria: serotype 2. ProMED-mail 2007; 30 Jan: 20070131.0399. Accessed February 12, 2008
  31. International Society for Infectious Diseases (2007b) Bluetongue—Europe (14): BTV-8, Germany (Nordrhein-Westfalen), confirmed. ProMED-mail 2007; 13 June: 20070613.1928. Accessed June 14, 2007
  32. Jeggo MH, Corteyn AH, Taylor WP, Davidson WL, Gorman BM (1987) Virulence of bluetongue virus for British sheep. Res Vet Sci 42(1):24–28PubMedGoogle Scholar
  33. Jennings DM, Mellor PS (1988) The vector potential of British Culicoides species for bluetongue virus. Vet Microbiol 17(1):1–10PubMedCrossRefGoogle Scholar
  34. Koumbati M, Mangana O, Nomikou K, Mellor PS, Papadopoulos O (1999) Duration of bluetongue viraemia and serological responses in experimentally infected European breeds of sheep and goats. Vet Microbiol 64:277–285PubMedCrossRefGoogle Scholar
  35. Losson B, Mignon B, Paternostre J, Madder M, De Deken R, De Deken G, Deblauwe I, Fassotte C, Cors R, Defrance T, Delecolle J-C, Baldet T, Haubruge E, Frederic F, Bortels J, Simonon G (2007) Biting midges overwintering in Belgium. Vet Rec 160(13):451–452PubMedGoogle Scholar
  36. Luedke AJ, Jochim MM, Bowne JG (1965) Preliminary bluetongue transmission with the sheep ked Melophagus ovinus (L.). Can J Comp Med Vet Sci 29:229–231PubMedGoogle Scholar
  37. Lunt RA, Melville LF, Hunt NT, Davis S, Rootes CL, Newberry KM, Pritchard LI, Middleton D, Bingham J, Daniels PW, Eaton BT (2006) Cultured skin fibroblast cells derived from bluetongue virus-inoculated sheep and field-infected cattle are not a source of late and protracted recoverable virus. J Gen Virol 87(12):3661–3666PubMedCrossRefGoogle Scholar
  38. Lysyk TJ, Danyk T (2007) Effect of temperature on life history parameters of adult Culicoides sonorensis (Diptera: Ceratopogonidae) in relation to geographic origin and vectorial capacity for bluetongue virus. J Med Entomol 44(5):741–751PubMedCrossRefGoogle Scholar
  39. MacLachlan NJ (1994) The pathogenesis and immunology of bluetongue virus infection of ruminants. Comp Immunol Microbiol Infect Dis 17:197–206PubMedCrossRefGoogle Scholar
  40. MacLachlan NJ, Barratt-Boyes B, Brewer AW, Stott JL (1991) Bluetongue virus infection of cattle. In: Walton, TE, Osburn, BI (eds) Bluetongue, African horse sickness and related orbiviruses. CRC, FL, pp 725–736Google Scholar
  41. Manso-Ribeiro J, Rosa-Azevedo J, Noronha F, Braco-Forte-Junior M, Grave-Periera C, Vasco-Fernandes M (1957) Fievre catarrhale du mouton (blue-tongue). Bulletin de l’Office International des Epizooties 48:350–367Google Scholar
  42. Mathieu B, Perrin A, Baldet T, Delecolle J-C, Albina E, Cêtre-Sossah C (2007) Molecular identification of western European species of Obsoletus complex (Diptera: Ceratopogonidae) by an internal transcribed spacer-1 rDNA multiplex polymerase chain reaction assay. J Med Entomol 44(6):1019–1025PubMedCrossRefGoogle Scholar
  43. Meiswinkel R, van Rijn P, Leijs P, Goffredo M (2007) Potential new Culicoides vector of bluetongue virus in northern Europe. Vet Rec 161(16):564–565PubMedGoogle Scholar
  44. Mellor PS (1990) The replication of bluetongue virus in Culicoides vectors. Curr Top Microbiol Immunol 162:143–161PubMedGoogle Scholar
  45. Mellor PS (2000) Replication of arboviruses in insect vectors. J Comp Pathol 123:231–247PubMedCrossRefGoogle Scholar
  46. Mellor PS, Boorman J (1995) The transmission and geographical spread of African horse sickness and bluetongue viruses. Ann Trop Med Parasitol 89(1):1–15PubMedGoogle Scholar
  47. Mellor PS, Pitzolis G (1979) Observations on breeding sites and light-trap collections of Culicoides during an outbreak of bluetongue in Cyprus. Bull Entomol Res 69(2):229–234Google Scholar
  48. Mellor PS, Wittmann EJ (2002) Bluetongue virus in the Mediterranean Basin 1998–2001. Vet J 164(1):20–37PubMedCrossRefGoogle Scholar
  49. Mellor PS, Boorman J, Baylis M (2000) Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol 45:307–340PubMedCrossRefGoogle Scholar
  50. Mertens PPC, Maan NS, Prasad G, Samuel AR, Shaw AE, Potgieter AC, Anthony SJ, Maan S (2007) Design of primers and use of RT-PCR assays for typing European bluetongue virus isolates: differentiation of field and vaccine strains. J Gen Virol 88:2811–2823PubMedCrossRefGoogle Scholar
  51. Mullens BA, Holbrook FR (1991) Temperature effects on the gonotrophic cycle of Culicoides variipennis (Diptera: Ceratopogonidae). Arch Gesamte Virusforsch 46:105–110Google Scholar
  52. Mullens BA, Tabachnick WJ, Holbrook FR, Thompson LH (1995) Effects of temperature on virogenesis of bluetongue virus serotype 11 in Culicoides variipennis sonorensis. Med Vet Entomol 9(1):71–76PubMedCrossRefGoogle Scholar
  53. Nolan DV, Carpenter S, Barber J, Mellor PS, Dallas JF, Mordue JA, Piertney SB (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Vet Microbiol 124(1–2):82–94PubMedCrossRefGoogle Scholar
  54. O’Connell L (2002) Entomological aspects of orbiviruses by Culicoides biting midges. PhD thesis, University of BristolGoogle Scholar
  55. Osburn BI (1994) The impact of bluetongue virus on reproduction. Comp Immunol Microbiol Infect Dis 17(3–4):189–196PubMedCrossRefGoogle Scholar
  56. Osmani A, Murati B, Kabashi Q, Goga I, Berisha B, Wilsmore AJ, Hamblin C (2006) Evidence for the presence of bluetongue virus in Kosovo between 2001 and 2004. Vet Rec 158(12):393–396PubMedGoogle Scholar
  57. Pagès N, Sarto I Monteys V (2005) Differentiation of Culicoides obsoletus and Culicoides scoticus (Diptera: Ceratopogonidae) based on mitochondrial cytochrome oxidase subunit I. J Med Entomol 42(6):1026–1034PubMedCrossRefGoogle Scholar
  58. Parsonson IM (1990) Pathology and pathogenesis of BT infections. Curr Top Microbiol Immunol 162:119–141PubMedGoogle Scholar
  59. Paweska JT, Venter GJ, Mellor PS (2002) Vector competence of South African Culicoides species for bluetongue virus serotype 1 (BTV-1) with special reference to the effect of temperature on the rate of virus replication in C. imicola and C. bolitinos. Med Vet Entomol 16:10–21PubMedCrossRefGoogle Scholar
  60. Purse BV, Baylis M, Tatem AJ, Rogers DJ, Mellor PS, Van Ham M, Chizov-Ginzberg A, Braverman Y (2004a) Predicting the risk of bluetongue through time: climate models of temporal patterns of outbreaks in Israel. Rev Sci Tech Off Int Epizoot 23(3):761–775Google Scholar
  61. Purse BV, Tatem AJ, Caracappa S, Rogers DJ, Mellor PS, Baylis M, Torina A (2004b) Modelling the distributions of Culicoides bluetongue virus vectors in Sicily in relation to satellite-derived climate variables. Med Vet Entomol 18(2):90–101PubMedCrossRefGoogle Scholar
  62. Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PPC, Baylis M (2005) Climate change and the recent emergence of bluetongue in Europe. Nat Rev Microbiol 3(2):171–181PubMedCrossRefGoogle Scholar
  63. Purse BV, McCormick BJJ, Mellor PS, Baylis M, Boorman JPT, Borras D, Burgu I, Capela R, Caracappa S, Collantes F, De Liberato C, Delgado JA, Denison E, Georgiev G, El Harak M, De La Rocque S, Lhor Y, Lucientes J, Mangana O, Miranda MA, Nedelchev N, Nomikou K, Ozkul A, Patakakis M, Pena I, Scaramozzino P, Torina A, Rogers DJ (2007) Incriminating bluetongue virus vectors with climate envelope models. J Appl Ecol 44(6):1231–1242CrossRefGoogle Scholar
  64. Sellers RF, Taylor WP (1980) Epidemiology of bluetongue and the import and export of livestock, semen and embryos. Bulletin de l’Office International des Epizooties 92:587–592Google Scholar
  65. Sellers RF, Pedgeley DE, Tucker MR (1977) Possible spread of African horse sickness on the wind. J Hyg 79(2):279–298Google Scholar
  66. Sellers RF, Pedgeley DE, Tucker MR (1978) Possible windborne spread of bluetongue to Portugal, June–July 1956. J Hyg 81(2):189–196Google Scholar
  67. Sellers RF, Gibbs EPJ, Herniman KAJ, Pedgeley DE, Tucker MR (1979) Possible origin of the bluetongue epidemic in Cyprus, August 1977. J Hyg 83(3):547–555Google Scholar
  68. Stott JL, Osburn BI, Barber TL (1982) Recovery of dual serotypes of bluetongue virus from infected sheep and cattle. Vet Microbiol 7:197–207PubMedCrossRefGoogle Scholar
  69. Stott JL, Osburn BI, Alexander L (1985) Ornithodorus coriaceus (Pajaroello tick) as a vector of bluetongue virus. Am J Vet Res 46:1197–1199PubMedGoogle Scholar
  70. Takamatsu H, Mellor PS, Mertens PPC, Kirkham PA, Burroughs JN, Parkhouse RME (2003) A possible overwintering mechanism for bluetongue virus in the absence of the insect vector. J Gen Virol 84:227–235PubMedCrossRefGoogle Scholar
  71. Tatem AJ, Baylis M, Mellor PS, Purse BV, Capela R, Pena I, Rogers DJ (2003) Prediction of bluetongue vector distribution in Europe and north Africa using satellite imagery. Vet Microbiol 97(1–2):13–29PubMedCrossRefGoogle Scholar
  72. Taylor WP, Mellor PS (1994) Distribution of bluetongue virus in Turkey, 1978–81. Epidemiol Infect 112(3):623–633PubMedGoogle Scholar
  73. Trenberth KE, Jones P, Ambenje P, Bojariu R, Easterling D, Klein Tank A, Parker D, Rahimzadeh F, Renwick JA, Rusticucci M, Soden B, Zhai P (2007) Observations: surface and atmospheric climate change. In: Solomon, S, Qin, D, Manning, M et al (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UKGoogle Scholar
  74. Vasalos M (1980) Cas de Fievre Catarrhale du mouton dan l’ ile Lesbos (Greece). Bulletin de l’Office International des Epizooties 92:547Google Scholar
  75. Vosdingh RA, Trainer DO, Easterday BC (1968) Experimental bluetongue disease in white-tailed deer. Can J Comp Med Vet Sci 31(1):382–387Google Scholar
  76. Wellby MP, Baylis M, Mellor PS (1996) Effect of temperature on survival and rate of virogenesis of African horse sickness virus in Culicoides variipennis sonorensis (Diptera: Ceratopogonidae) and its significance in relation to the epidemiology of the disease. Bull Entomol Res 86:715–720CrossRefGoogle Scholar
  77. White DM, Wilson WC, Blair CD, Beaty BJ (2005) Studies on overwintering of bluetongue viruses in insects. J Gen Virol 86(2):453–462PubMedCrossRefGoogle Scholar
  78. Williams RW (1962) Observations on the bionomics of Culicoides furens (Poey) on St John, U.S. Virgin Islands (Diptera, Ceratopogonidae). Mosq News 22:155–157Google Scholar
  79. Wilson A, Carpenter S, Gloster J, Mellor PS (2007) Re-emergence of BTV-8 in northern Europe in 2007. Vet Rec 161(14):487–489PubMedGoogle Scholar
  80. Wittmann EJ, Mellor PS, Baylis M (2002) Effect of temperature on the transmission of orbiviruses by the biting midge, Culicoides sonorensis. Med Vet Entomol 16(2):147–156PubMedCrossRefGoogle Scholar
  81. World Organisation for Animal Health (2006) Bluetongue detected for first time in Northern Europe.
  82. Yadin H, Brenner J, Bumbrov V, Oved Z, Stram Y, Klement E, Perl S, Anthony S, Maan S, Batten C, Mertens PPC (2008) Epizootic haemorrhagic disease virus type 7 infection in cattle in Israel. Vet Rec 162(2):53–56PubMedGoogle Scholar
  83. Yonguc AD, Taylor WP, Csontos L, Worrall E (1982) Bluetongue in western Turkey. Vet Rec 111(7):144–146PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Epidemiology DivisionInstitute for Animal HealthPirbrightUK

Personalised recommendations