WEST NILE VIRUS IN VULTURES FROM EUROPE – A SIGHT AMONG OTHER RAPTORS

Authors

  • Filipa Loureiro * Wildlife Rehabilitation Centre (CRAS), Veterinary Teaching Hospital (HVUTAD), University of Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real; Animal and Veterinary Research Centre (CECAV), Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), UTAD, Vila Real, Portugal, filipal@utad.pt
  • Luís Cardoso Animal and Veterinary Research Centre (CECAV), Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), UTAD, Vila Real; Department of Veterinary Sciences, School of Agrarian and Veterinary Sciences (ECAV), UTAD, 5000-801 Vila Real, Portugal
  • Ana Matos Research Centre for Natural Resources, Environment and Society (CERNAS), Polytechnic Institute of Castelo Branco; 6001-909 Castelo Branco; Quality of Life in the Rural World (Q-RURAL), Polytechnic Institute of Castelo Branco, 6001-909 Castelo Branco, Portugal
  • Manuela Matos Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), UTAD, 5000-801 Vila Real, Portugal
  • Ana Cláudia Coelho Animal and Veterinary Research Centre (CECAV), Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), UTAD, Vila Real; Department of Veterinary Sciences, School of Agrarian and Veterinary Sciences (ECAV), UTAD, 5000-801 Vila Real, Portugal

DOI:

https://doi.org/10.26873/SVR-1923-2024

Keywords:

epidemiology, Europe, scavengers, vultures, West Nile virus, zoonotic

Abstract

The West Nile virus (WNV) is an arbovirus mainly transmitted by Culex spp. and the causative agent of a zoonotic disease that is present worldwide. This pathogen is endemically maintained in a life cycle with birds acting as reservoirs, and humans and horses as accidental and dead-end hosts. Sporadic WNV outbreaks have been reported in Europe, and the potential impact of WNV infection on populations of threatened or endangered birds of prey is considerable. Surveillance programs are needed for early detection of this virus. All four species of vultures present in Europe are considered protected species. As scavengers, vultures are at the top of the food chain, and can be susceptible to, and negatively affected by, pathogens like WNV. In a conservation perspective, the impact of WNV in European vultures, alone or concomitantly with other factors, should be addressed. This review of documented cases can be considered a starting point.

Virus Zahodnega Nila pri jastrebih iz Evrope – opaznih med drugimi ujedami

Izvleček: Virus Zahodnega Nila (WNV) je arbovirus, ki ga prenašajo predvsem Culex spp., in je povzročitelj zoonoze, prisotne po vsem svetu. Ta patogen se endemično ohranja v življenjskem ciklu, v katerem so ptice rezervoarji, ljudje in konji pa so naključni in končni gostitelji. V Evropi so poročali o sporadičnih izbruhih WNV, potencialni vpliv okužbe z WNV na populacijo ogroženih ptic ujed pa je lahko zelo velik. Za zgodnje odkrivanje tega virusa so potrebni programi nadzora. Vse štiri vrste jastrebov, ki živijo v Evropi, so zavarovane vrste. Kot mrhovinarji so jastrebi zaradi zasedanja vrha prehranjevalne verige lahko dovzetni za patogene, kot je WNV. Z varstvenega vidika je treba obravnavati neodvisen ali z drugimi dejavniki povezan vpliv WNV na evropske jastrebe. Ta pregled dokumentiranih primerov se lahko šteje kot izhodišče za ta namen.

Ključne besede: epidemiologija; Evropa; mrhovinarji; jastrebi; virus Zahodnega Nila; zoonoza

 

References

1. Houston DC, Cooper JE. The digestive tract of the whiteback griffon vulture and its role in disease transmission among wild ungulates. J Wildl Dis 1975; 11: 306–13.

2. Moleón M, Sánchez-Zapata JA, Margalida A, Carrete M, Owen-Smith N, Donázar JA. Humans and scavengers: the evolution of interactions and ecosystem services, BioScience 2014; 64(5): 394–403. doi: 10.1093/biosci/biu034

3. Arbulu S, Jiménez JJ, Gútiez L, et al. Evaluation of bacteriocinogenic activity, safety traits and biotechnological potential of fecal lactic acid bacteria (LAB), isolated from Griffon Vultures (Gyps fulvus subsp. fulvus). BMC Microbiol 2016; 16(1): 228. doi: 10.1186/s12866-016-0840-2

4. Blumstein DT, Rangchi TN, Briggs T, De Andrade FS, Natterson-Horowitz B. A systematic review of carrion eaters' adaptations to avoid sickness. J Wildl Dis 2017; 53(3): 577–81. doi: 10.7589/2016-07-162

5. Plaza P, Blanco G, Lambertucci S. Implications of bacterial, viral and mycotic microorganisms in vultures for wildlife conservation, ecosystem services and public health. Ibis 2020; 162(4): 1109-–24. doi: 10.1111/ibi.12865

6. BirdLife International and Handbook of the Birds of the World 2021. The IUCN Red List of Threatened Species, Version 2022–2. https://www.iucnredlist.org/ (27. 9. 2023).

7. Hiraldo F, Delibes M . El quebrantahuesos Gypaetus barbatus (L.). sistemática, taxonomía, biología, distribución y protección. Madrid: Instituto para la Conservación de la Naturaleza, 1979.

8. Donázar JA, Palacios CJ, Gangoso L, Ceballos O, González MJ, Hiraldo F. Conservation status and limiting factors in the endangered population of Egyptian vulture (Neophron percnopterus) in the Canary Islands. Biol Conserv 2002; 107; 89–97. doi: 10.1016/S0006-3207(02)00049-6

9. Thiollay J-M. The decline of raptors in West Africa: long-term assessment and the role of protected areas. Ibis 2006; 148(2): 240–54. doi: 10.1111/j.1474-919X.2006.00531.x

10. Angelov I, Hashim I, Oppel S. Persistent electrocution mortality of Egyptian Vultures Neophron percnopterus over 28 years in East Africa. Bird Conserv Int 2013; 23(1): 1–6. doi: 10.1017/S0959270912000123

11. Cortés-Avizanda A, Jovani R, Carrete M, Donázar JA. Resource unpredictability promotes species diversity and coexistence in an avian scavenger guild: a field experiment. Ecology 2012; 93(12): 2570–9. doi: 10.1890/12-0221.1

12. Pirastru M, Mereu P, Manca L, Bebbere D, Naitana S, Leoni GG. Anthropogenic drivers leading to population decline and genetic preservation of the Eurasian griffon vulture (Gyps fulvus). Life (Basel) 2021; 11(10): 1038. doi: 10.3390/life11101038

13. Virani MZ, Kendall C, Njoroge P, Thomsett S. Major declines in the abundance of vultures and other scavenging raptors in and around the Masai Mara ecosystem, Kenya. Biol Conserv 2011; 144(2): 746–52. doi: 10.1016/j.biocon.2010.10.024

14. Cabral MJ, Almeida J, Almeida PR, et al. Livro Vermelho dos Vertebrados de Portugal. Lisboa: Instituto da Conservação da Natureza, 2005: 215–6.

15. Ives AM, Brenn-White M, Buckley JY, Kendall CJ, Wilton S, Deem SL. A global review of causes of morbidity and mortality in free-living vultures. EcoHealth 2022; 19(1): 40–54. doi: 10.1007/s10393-021-01573-5

16. Garcês A, Pires I, Sargo R, Sousa L, Prada J, Silva F. Admission causes, morbidity, and outcomes in scavenger birds in the North of Portugal (2005–2022). Animals (Basel) 2023; 13(13): 2093. doi: 10.3390/ani13132093

17. Hugh-Jones ME, De Vos V. Anthrax and wildlife. Rev Sci Tech 2002; 21(2): 359–83. doi: 10.20506/rst.21.2.1336

18. Ohishi I, Sakaguchi G, Riemann H, Behymer D, Hurvell B. Antibodies to Clostridium botulinum toxins in free-living birds and mammals. J Wildl Dis 1979; 15(1): 3–9. doi: 10.7589/0090-3558-15.1.3

19. Duriez O, Sassi Y, Le Gall-Ladevèze C, et al. Highly pathogenic avian influenza affects vultures' movements and breeding output. Curr Biol 2023; 33(17): 3766–74.e3. doi: 10.1016/j.cub.2023.07.061

20. Movalli P, Krone O, Osborn D, Pain D. Monitoring contaminants, emerging infectious diseases and environmental change with raptors, and links to human health. Bird Study 2018; 65(10): 1–10. doi: 10.1080/00063657.2018.1506735

21. European Food Safety Authority (EFSA). The European Union One health 2022 zoonoses report. EFSA J 2023; 21: e8442. doi: 10.2903/j.efsa.2023.8442

22. May FJ, Davis CT, Tesh RB, Barrett AD. Phylogeography of West Nile virus: from the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J Virol 2011; 85(6): 2964–74.

23. Hernández-Triana LM, Jeffries CL, Mansfield KL, Carnell G, Fooks AR, Johnson N. Emergence of West Nile virus lineage 2 in Europe: a review on the introduction and spread of a mosquito-borne disease. Front Public Health 2014; 2: 271. doi: 10.3389/fpubh.2014.00271

24. Habarugira G, Suen WW, Hobson-Peters J, Hall RA, Bielefeldt-Ohmann, H. West Nile virus: an update on pathobiology, epidemiology, diagnostics, control and “One Health” implications. Pathogens 2020; 9(7): 589. doi: 10.3390/pathogens9070589

25. García-Carrasco JM, Muñoz AR, Olivero J, Segura M, Real R. Mapping the risk for West Nile virus transmission, Africa. Emerg Infect Dis 2022; 28(4): 777–85. doi: 10.3201/eid2804.211103

26. Watts MJ, Monteys VSI, Mortyn PG, Kotsila P. The rise of West Nile virus in Southern and Southeastern Europe: a spatial-temporal analysis investigating the combined effects of climate, land use and economic changes. One Health 2021; 13: 100315. doi: 10.1016/j.onehlt.2021.100315

27. Young JJ, Haussig JM, Aberle SW, et al. Epidemiology of human West Nile virus infections in the European Union and European Union enlargement countries, 2010 to 2018. Euro Surveill 2021; 26(19): 2001095. doi: 10.2807/1560-7917.ES.2021.26.19.2001095

28. Lanciotti RS, Ebel GD, Deubel V, et al. Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology. 2002; 298(1): 96–105. doi: 10.1006/viro.2002.1449

29. Pachler K, Lebl K, Berer D, Rudolf I, Hubalek Z, Nowotny N. Putative new West Nile virus lineage in Uranotaenia unguiculata mosquitoes, Austria, 2013. Emerg Infect Dis 2014; 20(12): 2119–22. doi: 10.3201/eid2012.140921

30. Valiakos G, Touloudi A, Iacovakis C, et al. Molecular detection and phylogenetic analysis of West Nile virus lineage 2 in sedentary wild birds (Eurasian magpie), Greece, 2010. Euro Surveill 2011; 16(18): 19862.

31. Savini G, Capelli G, Monaco F, et al. Evidence of West Nile virus lineage 2 circulation in Northern Italy. Vet Microbiol 2012; 158(3/4): 267–73. doi: 10.1016/j.vetmic.2012.02.018

32. Gamino V, Höfle, U. Pathology and tissue tropism of natural West Nile virus infection in birds: a review. Vet Res 2013; 44(1): 39. doi: 10.1186/1297-9716-44-39

33. Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ. West Nile virus. Lancet Infect Dis 2002; 2(9): 519–29. doi: 10.1016/s1473-3099(02)00368-7

34. Samuel MA, Diamond MS. Pathogenesis of West Nile Virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J Virol 2006; 80(19): 9349–60. doi: 10.1128/JVI.01122-06

35. Sejvar JJ. Clinical manifestations and outcomes of West Nile virus infection. Viruses 2014; 6(2): 606–23. doi: 10.3390/v6020606.

36. Van der Meulen KM, Pensaert MB, Nauwynck HJ. West Nile virus in the vertebrate world. Arch Virol 2005; 150(4): 637–57. doi: 10.1007/s00705-004-0463-z

37. Nemeth NM, Kratz GE, Bates R, Scherpelz JA, Bowen RA, Komar N. Clinical evaluation and outcomes of naturally acquired West Nile virus infection in raptors. J Zoo Wildl Med 2009; 40(1): 51–63. doi: 10.1638/2007-0109.1

38. Vidaña B, Busquets N, Napp S, Pérez-Ramírez E, Jiménez-Clavero MÁ, Johnson N. The role of birds of prey in West Nile virus epidemiology. Vaccines (Basel) 2020; 8(3): 550. doi: 10.3390/vaccines8030550

39. Kritzik KL, Kratz G, Panella NA, Burkhalter K, Clark RJ, Biggerstaff BJ, Komar N. Determining raptor species and tissue sensitivity for improved West Nile virus surveillance. J Wildl Dis 2018; 54(3): 528–33. doi: 10.7589/2017-12-292

40. Komar N, Langevin S, Hinten S, et al. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 2003; 9(3): 311–22. doi: 10.3201/eid0903.020628

41. Hull J, Hull A, Reisen W, Fang Y, Ernst H. Variation of West Nile virus antibody prevalence in migrating and wintering hawks in central California. Condor 2006; 108: 435–9.

42. Jiménez-Clavero MÁ. Animal viral diseases and global change: bluetongue and West Nile fever as paradigms. Front Genet 2012; 3: 105. doi: 10.3389/fgene.2012.00105

43. Nemeth NM, Gould DH, Bowen RA, Komar N. Natural and experimental West Nile virus infection in five raptor species. J Wildl Dis 2006; 42: 1–13. doi: 10.7589/0090-3558-42.1.1.

44. Ziegler U, Angenvoort J, Fischer D, et al. Pathogenesis of West Nile virus lineage 1 and 2 in experimentally infected large falcons. Vet Microbiol 2013; 161(3/4): 263–73. doi: 10.1016/j.vetmic.2012.07.041

45. Bergmann F, Fischer D, Fischer L, et al. Vaccination of zoo birds against West Nile Virus – a field study. Vaccines (Basel) 2023; 11(3): 652. doi: 10.3390/vaccines11030652

46. Steele KE, Linn MJ, Schoepp RJ, et al. Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York. Vet Pathol 2000; 37(3): 208–24. doi: 10.1354/vp.37-3-208

47. D'Agostino JJ, Isaza R. Clinical signs and results of specific diagnostic testing among captive birds housed at zoological institutions and infected with West Nile virus. J Am Vet Med Assoc 2004; 224(19): 1640–3. doi: 10.2460/javma.2004.224.1640

48. Jiménez de Oya N, Escribano-Romero E, Blázquez AB, Martín-Acebes MA, Saiz JC. Current progress of avian vaccines against West Nile virus. Vaccines (Basel) 2019; 7(4): 126. doi: 10.3390/vaccines7040126

49. Joyner PH, Kelly S, Shreve AA, Snead SE, Sleeman JM, Pettit DA. West Nile virus in raptors from Virginia during 2003: clinical, diagnostic, and epidemiologic findings. J Wildl Dis 2006; 42(2): 335–44. doi: 10.7589/0090-3558-42.2.335

50. Saggese MD. West Nile virus in Neotropical raptors: should we be concerned? In: Neotropical Raptors. Texas: College of Veterinary medicine and biomedical sciences, 2007: 149–73.

51. Ferraguti M, De La Puente JM, Soriguer R, Llorente F, Jiménez-Clavero, MÁ, Figuerola J. West Nile virus-neutralizing antibodies in wild birds from southern Spain. Epidemiol Infect 2016; 144(9): 1907–11. doi: 10.1017/S0950268816000133

52. Hahn DC, Nemeth NM, Edwards E, Bright PR, Komar N. Passive West Nile virus antibody transfer from maternal Eastern screech-owls (Megascops asio) to progeny. Avian Dis 2006; 50(3): 454–5. doi: 10.1637/7509-012606R1.1

53. Nemeth NM, Kratz GE, Bates R, Scherpelz JA, Bowen RA, Komar N. Naturally induced humoral immunity to West Nile virus infection in raptors. Ecohealth 2008; 5(3): 298–304. doi: 10.1007/s10393-008-0183-z

54. Marra PP, Griffing S, Caffrey C, et al. West Nile virus and wildlife. BioScience 2004; 54(5): 393–402. doi: 10.1641/0006-3568(2004)054[0393:WNVAW]2.0.CO;2

55. Wünschmann A, Shivers J, Bender J, et al. Pathologic and immunohistochemical findings in Goshawks (Accipiter gentilis) and Great Horned Owls (Bubo virginianus) naturally infected with West Nile virus. Avian Dis 2005; 49(2): 252–9.. doi: 10.1637/7297-103104R

56. Palmieri C, Franca M, Uzal F, et al. Pathology and immunohistochemical findings of West Nile virus infection in Psittaciformes. Vet Pathol 2011; 48(5): 975–84. doi: 10.1177/0300985810391112

57. Phalen DN, Dahlhausen B. West Nile virus. Semin. Avian Exot. Pet Med. 2004; 13: 67–78.

58. Jones MP. Selected infectious diseases of birds of prey. J Exot Pet Med 2006; 15(1): 5–17. doi:10.1053/j.jepm.2005.11.008

59. Wodak E, Richter S, Bagó Z, et al. Detection and molecular analysis of West Nile virus infections in birds of prey in the eastern part of Austria in 2008 and 2009. Vet Microbiol 2011; 149(3/4): 358–66. doi: 10.1016/j.vetmic.2010.12.012

60. Bakonyi T, Ferenczi E, Erdelyi K, et al. Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009. Vet Microbiol 2013; 165(1/): 61–70. doi: 10.1016/j.vetmic.2013.03.005

61. García-Bocanegra I, Busquets N, Napp S, et al. Serosurvey of West Nile virus and other flaviviruses of the Japanese encephalitis antigenic complex in birds from Andalusia, southern Spain. Vector Borne Zoonotic Dis 2011; 11(8): 1107–13. doi: 10.1089/vbz.2009.0237

62. Busquets N, Laranjo-González M, Soler M, et al. Detection of West Nile virus lineage 2 in North-Eastern Spain (Catalonia). Transbound Emerg Dis 2019; 66(2): 617–21. doi: 10.1111/tbed.13086

63. Bakhshi H, Beck C, Lecollinet S, et al. Serological evidence of West Nile virus infection among birds and horses in some geographical locations of Iran. Vet Med Sci 2021; 7(1): 204–9. doi: 10.1002/vms3.342

64. García‐Ripollés C, López‐López P, Urios V. First description of migration and wintering of adult Egyptian Vultures Neophron percnopterus tracked by GPS satellite telemetry. Bird study 2010; 57(2): 261–5. 10.1080/00063650903505762

65. Phipps WL, López-López P, Buechley ER. Spatial and temporal variability in migration of a soaring raptor across three continents. Front Ecol Evol 2019; 7: 1–14. 10.3389/fevo.2019.00323

66. Bravo-Barriga D, Aguilera-Sepúlveda P, Guerrero-Carvajal F, et al. West Nile and Usutu virus infections in wild birds admitted to rehabilitation centres in Extremadura, western Spain, 2017–2019. Vet Microbiol 2021; 255: 109020. doi: 10.1016/j.vetmic.2021.109020

67. Marinković D, Nešić V, Davitkov D, Aničić M. Causes of morbidity and mortality in European griffon vulture (Gyps fulvus) population in Serbia in the period of 2018–2022 – post-mortem findings. J Comp Pathol 2023; 203: 52. doi: 10.1016/j.jcpa.2023.03.042

68. Nash D, Mostashari F, Fine A, et al. The outbreak of West Nile virus infection in the New York City area in 1999. N Engl J Med 2001; 344(4): 1807–14. doi: 10.1056/NEJM200106143442401

69. Rideout BA, Stalis I, Papendick R, et al. Patterns of mortality in free-ranging California Condors (Gymnogyps californianus). J Wildl Dis 2012; 48(1): 95–112. doi: 10.7589/0090-3558-48.1.95

70. Straub MH, Kelly TR, Rideout BA, et al. Seroepidemiologic survey of potential pathogens in obligate and facultative scavenging avian species in California. PLoS One 2015; 10: e0143018. doi: 10.1371/journal.pone.0143018

71. Terraube J, Andevski J, Loercher F, Tavares J. Population estimates for the five European vulture species. Arnhem: The Vulture Conservation Foundation, 2022.

72. Schönenberger AC, Wagner S, Tuten HC, et al. Host preferences in host-seeking and blood-fed mosquitoes in Switzerland. Med Vet Entomol 2016; 30(1): 39–52. doi: 10.1111/mve.12155

73. Nemeth NM, Hahn DC, Gould DH, Bowen RA. Experimental West Nile virus infection in Eastern Screech Owls (Megascops asio). Avian Dis 2006; 50(2): 252–8. doi: 10.1637/7466-110105R1.1.

74. Ip HS, Van Wettere AJ, McFarlane L, et al. West Nile virus transmission in winter: the 2013 Great Salt Lake bald eagle and eared grebes mortality event. PLoS Curr. 2014; 6. doi: 10.1371/currents.outbreaks.b0f031fc8db2a827d9da0f30f0766871

75. Komar N, Lanciotti R, Bowen R, Langevin S, Bunning M. Detection of West Nile virus in oral and cloacal swabs collected from bird carcasses. Emerg Infect Dis 2002; 8(7): 741–2. doi: 10.3201/eid0807.020157

76. Heinz-Taheny KM, Andrews JJ, Kinsel MJ, et al. West Nile virus infection in free-ranging squirrels in Illinois. J Vet Diagn Invest 2004; 16(3): 186–90. doi: 10.1177/104063870401600302.

77. Bosè M, Duriez O, Sarrazin F. Intra-specific competition in foraging griffon vultures Gyps fulvus: 1. Dynamics of group feeding. Bird Study 2012; 59: 182–92. doi:10.1080/00063657.2012.658639

78. Donázar JA. Los buitres ibéricos: biología y conservación. Madrid: J. M. Reyero, 1993.

79. Donázar JA, Cortés-Avizanda A, Carrete M. Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation. Eur J Wildl Res. 2010; 56(4): 613–21. doi: 10.1007/s10344-009-0358-0

80. Houston DC, Meeb A, McGradyc M. Why do condors and vultures eat junk?: the implications for conservation. J Raptor Res 2007; 41: 235–8. doi: 10.3356/0892-1016(2007)41[235:WDCAVE]2.0.CO;2

81. Benmazouz I, Jokimäki J, Lengyel S, et al. Corvids in urban environments: a systematic global literature review. Animals. 2021; 11: 3226.

82. McLean RG, Ubico SR, Docherty DE, Hansen WR, Sileo L, McNamara TS. West Nile virus transmission and ecology in birds. Ann N Y Acad Sci 2001; 951: 54–7. doi: 10.1111/j.1749-6632.2001.tb02684.x

83. Ward MR, Stallknecht DE, Willis J, Conroy MJ, Davidson WR. Wild bird mortality and West Nile virus surveillance: biases associated with detection, reporting, and carcass persistence. J Wildl Dis 2006; 42(1): 92–106. doi: 10.7589/0090-3558-42.1.92

84. Jones KE, Patel NG, Levy MA, et al. Global trends in emerging infectious diseases. Nature 2008; 451(7181): 990–3. doi: 10.1038/nature06536

85. Smithburn KC, Hughes TP, Burke AW, Paul JH. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg 1940; s1-20: 471–92. doi: 10.4269/AJTMH.1940.S1-20.471

86. Taylor RM, Work TH, Hurlbut HS, Rizk F. A study of the ecology of West Nile virus in Egypt. Am J Trop Med Hyg 1956; 5(4): 579–20. doi: 10.4269/ajtmh.1956.5.579

87. Mencattelli G, Ndione MHD, Rosà R, et al. Epidemiology of West Nile virus in Africa: an underestimated threat. PLoS Negl Trop Dis 2022; 16(1): e0010075. doi: 10.1371/journal.pntd.0010075

88. Joubert L, Oudar J, Hannoun C, Beytout D, Corniou B, Guillon JC, Panthier R. [Epidemiology of the West Nile virus: study of a focus in Camargue. IV. Meningo-encephalomyelitis of the horse]. Ann Inst Pasteur (Paris) 1970; 118(2): 239–47.

89. Tsai TF, Popovici F, Cernescu C, Campbell GL, Nedelcu NI. West Nile encephalitis epidemic in Southeastern Romania. Lancet 1998; 352(9130): 767–71. doi: 10.1016/s0140-6736(98)03538-7

90. García-Carrasco JM, Muñoz AR, Olivero J, Figuerola J, Fa JE, Real R. Gone (and spread) with the birds: can chorotype analysis highlight the spread of West Nile virus within the Afro-Palaearctic flyway? One Health 2023; 17: 100585. doi: 10.1016/j.onehlt.2023.100585

91. Rappole JH, Derrickson SR, Hubálek Z. Migratory birds and spread of West Nile virus in the Western Hemisphere. Emerg Infect Dis 2000; 6(4): 319–28. doi: 10.3201/eid0604.000401

92. Nir Y, Goldwasser R, Lasowski Y, Avivi A. Isolation of arboviruses from wild birds in Israel. Am J Epidemiol 1967; 86(2): 372–8. doi: 10.1093/oxfordjournals.aje.a120747

93. Hubálek Z, Halouzka J. West Nile fever – a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 1999; 5(5): 643–50. doi: 10.3201/eid0505.990505

94. Jupp PG. The ecology of West Nile virus in South Africa and the occurrence of outbreaks in humans. Ann N Y Acad Sci 2001; 951: 143–2. doi: 10.1111/j.1749-6632.2001.tb02692.x.

95. López G, Jiménez-Clavero MA, Tejedor CG, Soriguer R, Figuerola J. Prevalence of West Nile virus neutralizing antibodies in Spain is related to the behavior of migratory birds. Vector Borne Zoonotic Dis 2008; 8(5): 615–21. doi: 10.1089/vbz.2007.0200.

96. Lord RD, Calisher CH. Further evidence of southward transport of arboviruses by migratory birds. Am J Epidemiol 1970; 92(1): 73–8. doi: 10.1093/oxfordjournals.aje.a121181

97. Malkinson M, Banet C, Weisman Y, et al. Introduction of West Nile vi-rus in the Middle East by migrating white storks. Emerg Infect Dis 2002; 8(4): 392–7. doi: 10.3201/eid0804.010217

98. Smith KA, Campbell GD, Pearl DL, Jardine CM, Salgado-Bierman F, Nemeth NM. A retrospective summary of raptor mortality in Ontario, Canada (1991-2014), including the effects of West Nile virus. J Wildl Dis 2018; 54(2): 261–71. doi: 10.7589/2017-07-157

99. Giesen C, Herrador Z, Fernandez-Martinez B, et al. A systematic review of environmental factors related to WNV circulation in European and Mediterranean countries. One Health 2023; 16: 100478. doi: 10.1016/j.onehlt.2022.100478

100. Fluhr J, Benhamou S, Peyrusque D, Duriez O. Space use and time budget in two populations of griffon vultures in contrasting landscapes. J. Raptor Res 2021; 55(3): 425–37. doi: 10.3356/JRR-20-14

101. Höfle U, Blanco JM, Crespo E, et al. West Nile virus in the endangered Spanish imperial eagle. Vet Microbiol 2008; 129(1/2): 171–8. doi: 10.1016/j.vetmic.2007.11.006

102. Brugueras S, Fernández-Martínez B, Martínez-de la Puente J, et al. Environmental drivers, climate change and emergent diseases transmitted by mosquitoes and their vectors in southern Europe: a systematic review. Environ Res 2020; 191: 110038. doi: 10.1016/j.envres.2020.110038

103. Casades-Martí L, Holgado-Martín R, Aguilera-Sepúlveda P. Risk factors for exposure of wild birds to West Nile virus in a gradient of wildlife-livestock interaction. Pathogens 2023; 12(1): 83. doi: 10.3390/pathogens12010083

104. Díaz M, Campos P, Pulido FJ. The Spanish dehesas: a diversity of land use and wildlife. In: Pain D, Pienkowski M, eds. Farming and birds in Europe: The Common Agricultural Policy and its implications for bird conservation. London: Academic Press, 1997: 178–209.

105. European Environment Agency (EUNIS). https://eunis.eea.europa.eu/habitats/393 (23. 10. 2023).

106. Delgado-González A, Cortés-Avizanda A, Serrano D, et al. Apex scavengers from different European populations converge at threatened savannah landscapes. Sci Rep 2022; 12: 2500. doi: 10.1038/s41598-022-06436-9

107. Guerrero-Carvajal F, Bravo-Barriga D, Martín-Cuervo M, et al. Serological evidence of co-circulation of West Nile and Usutu viruses in equids from western Spain. Transbound Emerg Dis 2021; 68(3): 1432–44. doi: 10.1111/tbed.13810

108. Morant J, Arrondo E, Sánchez-Zapata JA, et al. Large-scale movement patterns in a social vulture are influenced by seasonality, sex, and breeding region. Ecol Evol 2023; 13(2): e9817. doi: 10.1002/ece3.9817

109. Ramírez J, de Langarica FMZG, Molina MG. Spring migration of eurasian griffon vultures across the strait of Gi-braltar: number, timing and age composition. Ardeola 2019; 66(1): 113–8. doi: 10.13157/arla.66.1.2019.sc5

110. Adelman JS, Tokarz RE, Euken AE, Field EN, Russell MC, Smith RC. Relative influence of land use, mosquito abundance, and bird communities in defining West Nile virus infection rates in Culex mosquito populations. Insects 2022; 13(9): 758. doi:10.3390/insects13090758

111. Palomar AM, Veiga J, Portillo A, et al. Novel genotypes of nidicolous argas ticks and their associated microorganisms from Spain. Front Vet Sci 2021; 8: 637837. doi: 10.3389/fvets.2021.637837

112. Blahove MR, Carter JR. Flavivirus persistence in wildlife populations. Viruses 2021; 13(10): 2099. doi: 10.3390/v13102099

113. Moraga-Fernández A, Oliva-Vidal P, Sánchez-Sánchez M, et al. Health risks associated with argasid ticks, transmitted pathogens, and blood parasites in Pyrenean griffon vulture (Gyps fulvus) nestlings. Eur J Wildl Res 2023; 69: 112. 10.1007/s10344-023-01741-8

114. Cacho IM. Exposure and carriage of West Nile virus in feathered Iberian scavengers. Master’s thesis: Uppsala University, Uppsala. 2022.

115. Gangoso L, Cortés-Avizanda A, Sergiel A, et al. Avian scavengers living in anthropized landscapes have shorter telomeres and higher levels of glucocorticoid hormones. Sci Total Environ 2021; 782: 146920. doi: 10.1016/j.scitotenv.2021.146920

116. FAO & UNEP. The State of the World’s Forests 2020. Forests, Biodiversity and People. Rome: FAO & UNEP, 2020: 72–9.

117. Morand S, Lajaunie C. Outbreaks of vector-borne and zoonotic diseases are associated with changes in forest cover and oil palm expansion at global scale. Front Vet Sci 2021; 8: 661063. doi: 10.3389/fvets.2021.661063

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Published

2024-12-31

How to Cite

Loureiro, F., Cardoso, L., Matos, A., Matos, M., & Coelho, A. C. (2024). WEST NILE VIRUS IN VULTURES FROM EUROPE – A SIGHT AMONG OTHER RAPTORS. Slovenian Veterinary Research, 61(4), 233–44. https://doi.org/10.26873/SVR-1923-2024

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Review Article