Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds

Journal of Applied Microbiology

Volumn 112, Issue 2, 2012, Pages 246-257

  Gale, P ^a   Stephenson, B ^a   Brouwer, A ^a   Martinez, M ^b   de la Torre, A ^b   Bosch, J ^b   Foley Fisher, M ^a   Bonilauri, P ^c   Lindstrom A ^d   Ulrich, R G ^e   de Vos, C J ^f   Scremin, M ^g   Liu, Z ^h   Kelly, L ^a   Munoz M J ^b  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

^b Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria   (Spain)

^c ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^d NATIONAL VETERINARY INSTITUTE   (Sweden)

^e FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^f WAGENINGEN UNIVERSITY   (Netherlands)

^g ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLE VENEZIE   (Italy)

^h Lanzhou Veterinary Research Institute   (China)

Author keywords

Climate change; Crimean Congo haemorrhagic fever; Europe; Geographical risk assessment; Migratory birds

Indexed keywords

AGRICULTURE; BIRDS; CLIMATE CHANGE; CLIMATE MODELS; MAPS; RISK PERCEPTION; VIRUSES;

'CURRENT; CLIMATE CHANGE SCENARIOS; CONDITION; CRIMEAN CONGO HEMORRHAGIC FEVER; EUROPE; FEVER VIRUS; GEOGRAPHICAL RISK ASSESSMENT; GRID CELLS; MIGRATORY BIRDS; RISKS ASSESSMENTS;

RISK ASSESSMENT;

ABUNDANCE; CLIMATE CHANGE; ENVIRONMENTAL IMPACT; GAMEBIRD; GEOGRAPHICAL DISTRIBUTION; HOME RANGE; LIVESTOCK; MIGRATORY SPECIES; MOLT; RISK ASSESSMENT; SONGBIRD; SPATIAL ANALYSIS; TICK; VIRAL DISEASE; VIRUS;

AFRICA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHUS TRIVIALIS; ARTICLE; CLIMATE CHANGE; COTURNIX COTURNIX; CRIMEAN CONGO HEMORRHAGIC FEVER; EUROPE; FEMALE; HYALOMMA MARGINATUM; INFECTION RISK; LIVESTOCK; MALE; MIGRANT BIRD; MOLTING; NONHUMAN; OENANTHE OENANTHE; PHYLLOSCOPUS TROCHILUS; SPRING; TEMPERATURE; TICK;

NORTHERN EUROPE; SUB-SAHARAN AFRICA;

ANTHUS TRIVIALIS; AVES; COTURNIX COTURNIX; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; HYALOMMA MARGINATUM; IXODIDA; OENANTHE OENANTHE; PHYLLOSCOPUS; PHYLLOSCOPUS TROCHILUS;

EID: 84855908613     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.05203.x     Document Type: Article

References (30)

1. BirdLife International (2004) Birds in the European Union: A Status Assessment. Wageningen, The Netherlands: BirdLife International. Available at:.
2. EBCC (1997) European Bird Census Council. Atlas of European Breeding Birds. London: T & AD Poyser.
3. Ergonul, O. and Whitehouse, C.A. (2007) Introduction. In Crimean-Congo Hemorrhagic Fever - A Global Perspective ed. Ergonul, O. and Whitehouse, C.A. pp. 3-11 Dordrecht, Netherlands: Springer.
4. Estrada-Peña, A., Martínez Avilés, M. and Muñoz Reoyo, M.J. (2011) A population model to describe the distribution and seasonal dynamics of the tick Hyalomma marginatum in the Mediterranean basin. Transbound Emerg Dis 58, 213-223.
5. FAO (2007) Gridded livestock of the world 2007 (ed. Wint, G.R.W. and Robinson, T.P.) Rome. Available at: (accessed 21 April 2009).
6. Finlayson, C. (1992) Birds of the Strait of Gibraltar. London, UK: T. & A.D. Poyser.
7. Gale, P., Estrada-Pena, A., Martinez, M., Ulrich, R.G., Wilson, A., Capelli, G., Phipps, P., de la Torre, A. et al. (2010) The feasibility of developing a risk assessment for the impact of climate change on the emergence of Crimean-Congo haemorrhagic fever in livestock in Europe: a review. J Appl Microbiol 108, 1859-1870.
8. Gonzalez, J.P., Camicas, J.L., Cornet, J.P., Faye, O. and Wilson, M.L. (1992) Sexual and transovarian transmission of Crimean-Congo haemorrhagic fever virus in Hyalomma truncatum ticks. Res Virol 143, 23-28.
9. Gordon, S.W., Linthicum, K.J. and Moulton, J.R. (1993) Transmission of Crimean-Congo hemorrhagic fever virus in two species of Hyalomma ticks from infected adults to cofeeding immature forms. Am J Trop Med Hyg 48, 576-580.
10. 0 for tick-borne infections. Am Nat 171, 743-754.
11. Hasle, G., Bjune., G., Edvardsen, E., Jakobsen, C., Linnehol, B., Roer, J.E., Mehl, R., Roed, K.H. et al. (2009) Transport of ticks by migratory passerine birds to Norway. J Parasitol 95, 1342-1351.
12. Hillyard, P. (1996) Ticks of North-West Europe. In Synopses of the British Fauna ed. Barnes, R.S.K. and Crothers, J.H. pp. 124-125. London: The Natural History Museum.
13. Hoogstraal, H. (1972) Birds as tick hosts and as reservoirs and disseminators of tickborne infectious agents. Wia Parazytol 18, 703-706, NR 4-5-6.
14. Hoogstraal, H., Traylor, M.A., Gaber, S., Malakatis, G., Guindy, E. and Helmy, I. (1964) Ticks (Ixodoidea) on migrating birds in Egypt, Spring and Fall 1962. Bull World Health Organ 30, 355-367.
15. Huntley, B., Green, R.E., Collingham, Y.C. and Willis, S.G. (2007) A Climatic Atlas of European Breeding Birds. Durham: Durham University, RSPB and Lynx Edicions.
16. Kaiser, M.N., Hoogstraal, H. and Watson, G.E. (1974) Ticks (Ixodoidea) on migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. Bull Entomol Res 64, 97-110.
17. Kaltenrieder, M. (1990) Scototaxis and target perception in the camel tick Hyalomma dromedarii. Exp Appl Acarol 9, 267-278.
18. Lee, V.H. and Kemp, G.E. (1970) Congo virus: experimental infection of Hyalomma rufipes and transmission to a calf. Bull Entomol Soc Niger 2, 133-135.
19. Logan, T.M., Linthicum, K.J., Bailey, C., Watts, D.M. and Moulton, J.R. (1989) Experimental transmission of Crimean-Congo hemorrhagic fever virus by Hyalomma truncatum Koch. Am J Trop Med Hyg 40, 207-212.
20. Maltezou, H.C. and Papa, A. (2010) Crimean-Congo hemorrhagic fever: risk for emergence of new endemic foci in Europe? Travel Med Infect Dis 8, 139-143.
21. Martyn, K.P. (1988) Provisional Atlas of the Ticks (Ixodoidea) of the British Isles. Swindon: Biological Records Centre, Natural Environment Research Council.
22. Met Office and Hadley Centre (2008) HadRM3-PPE-UK Model Data, NCAS British Atmospheric Data Centre. Available at: (accessed 18 November 2010).
23. Mild, M., Simon, M., Albert, J. and Mirazimi, A. (2010) Towards an understanding of the migration of Crimean-Congo hemorrhagic fever virus. J Gen Virol 91, 199-207.
24. Molin, Y., Lindeborg, M., Nystrom, F., Madder, M., Hjelm, E., Olsen, B., Jaenson, T.G.T. and Ehrenborg, C. (2011) Migratory birds, ticks, and Bartonella. Infect Ecol Epidemiol 1, 5997, doi:.
25. Nijhof, A.M., Bodaan, C., Postigo, M., Nieuwenhuijs, H., Opsteegh, M., Franssen, L., Jebbink, F. and Jongejan, F. (2007) Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector Borne Zoonotic Dis 7, 585-595.
26. Randolph, S. and Ergonul, O. (2008) Crimean-Congo haemorrhagic fever: exceptional epidemic of viral haemorrhagic fever in Turkey. Future Virol 3, 303-306.
27. Sang, R., Lutomiah, J., Koka, H., Makio, A., Chepkorir, E., Ochieng, C., Yalwala, S., Mutisya, J. et al. (2011) Crimean-Congo hemorrhagic fever virus in Hyalommid ticks, Northeastern Kenya. Emerg Infect Dis 17, 1502-1505.
28. Tahmasebi, F., Ghiasi, S.M., Mostafavi, E., Moradi, M., Piazak, N., Mozafari, A., Haeri, A., Fooks, A.R. et al. (2010) Molecular epidemiology of Crimean-Congo hemorrhagic fever virus genome isolated from ticks of Hamadan province of Iran. J Vector Borne Dis 47, 211-216.
29. WHO (2011) World Health Organisation Crimean-Congo haemorrhagic fever (CCHF). Available at: (accessed 6 June 2011).
30. Wilson, M.L., Gonzalez, J.P., LeGuenno, B., Cornet, J.P., Guillaud, M., Calvo, M.A., Digoutte, J.P. and Camicas, J.L. (1990) Epidemiology of Crimean-Congo hemorrhagic fever in Senegal: temporal and spatial patterns. Arch Virol Suppl 1, 323-340.