Analyze Diet
Veterinary sciences2024; 11(6); 259; doi: 10.3390/vetsci11060259

West Nile Virus Seroprevalence in Wild Birds and Equines in Madrid Province, Spain.

Abstract: West Nile virus (WNV) is a re-emerging flavivirus, primarily circulating among avian hosts and mosquito vectors, causing periodic outbreaks in humans and horses, often leading to neuroinvasive disease and mortality. Spain has reported several outbreaks, most notably in 2020 with seventy-seven human cases and eight fatalities. WNV has been serologically detected in horses in the Community of Madrid, but to our knowledge, it has never been reported from wild birds in this region. To estimate the seroprevalence of WNV in wild birds and horses in the Community of Madrid, 159 wild birds at a wildlife rescue center and 25 privately owned equines were sampled. Serum from thirteen birds (8.2%) and one equine (4.0%) tested positive with a WNV competitive enzyme-linked immunosorbent assay (cELISA) designed for WNV antibody detection but sensitive to cross-reacting antibodies to other flaviviruses. Virus-neutralization test (VNT) confirmed WNV antibodies in four bird samples (2.5%), and antibodies to undetermined flavivirus in four additional samples. One equine sample (4.0%) tested positive for WNV by VNT, although this horse previously resided in a WN-endemic area. ELISA-positive birds included both migratory and resident species, juveniles and adults. Two seropositive juvenile birds suggest local flavivirus transmission within the Community of Madrid, while WNV seropositive adult birds may have been infected outside Madrid. The potential circulation of flaviviruses, including WNV, in birds in the Madrid Community raises concerns, although further surveillance of mosquitoes, wild birds, and horses in Madrid is necessary to establish the extent of transmission and the principal species involved.
Publication Date: 2024-06-07 PubMed ID: 38922006PubMed Central: PMC11209238DOI: 10.3390/vetsci11060259Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

Overview

  • This study investigated the presence of West Nile Virus (WNV) antibodies in wild birds and horses in the Madrid region of Spain to understand the prevalence and potential local transmission of WNV and related flaviviruses.

Background

  • West Nile Virus (WNV) is a flavivirus primarily transmitted between birds and mosquitoes.
  • It can cause serious infections in humans and horses, including neuroinvasive disease and death.
  • Spain experienced a notable WNV outbreak in 2020, with 77 human cases and 8 deaths.
  • Previous evidence showed WNV presence in horses in Madrid, but no data existed on wild birds in this region.

Objective

  • To estimate the seroprevalence of WNV in both wild birds and horses within the Community of Madrid.
  • To explore whether local transmission of WNV or similar flaviviruses occurs in Madrid.

Methods

  • Sampled 159 wild birds housed at a wildlife rescue center in Madrid, including both resident and migratory species, juveniles and adults.
  • Collected blood samples from 25 privately owned horses in the same region.
  • Tested serum samples using WNV competitive ELISA (cELISA) for WNV antibodies; this test is sensitive to cross-reacting antibodies from other flaviviruses.
  • Confirmed positive ELISA results using virus-neutralization tests (VNT) to specifically identify WNV antibodies or antibodies to other flaviviruses.

Results

  • Thirteen birds (8.2%) and one horse (4%) tested ELISA-positive for WNV antibodies.
  • VNT confirmed four bird samples (2.5%) had specific WNV antibodies, while four other birds had antibodies to flaviviruses that could not be precisely identified.
  • One horse sample (4%) was VNT-positive for WNV; however, that horse had a history of living in an area known to be endemic for WNV, not necessarily Madrid.
  • Both migratory and resident birds showed seropositivity, including two juvenile birds, which implies local flavivirus transmission within Madrid.
  • Adult birds with WNV antibodies could either have been infected locally or in other regions during migration.

Significance and Interpretation

  • The detection of WNV antibodies in juvenile birds supports the likelihood of active flavivirus circulation in Madrid.
  • Presence in both residents and migrators indicates potential overlap of local and external virus transmission sources.
  • The low detection rate in horses may reflect limited local spread or prior exposures outside Madrid.
  • Serological cross-reactivity with other flaviviruses suggests the need to consider other circulating viruses in the region.

Conclusions and Recommendations

  • Flaviviruses, including WNV, appear to be circulating among wild birds in the Community of Madrid.
  • Further surveillance of mosquito vectors, wild birds, and horses is critical for clarifying the extent of transmission and identifying major host species involved locally.
  • Understanding local transmission dynamics will enhance public health preparedness and control strategies to mitigate the risk of future outbreaks.

Cite This Article

APA
Williams RAJ, Criollo Valencia HA, López Márquez I, González González F, Llorente F, Jiménez-Clavero MÁ, Busquets N, Mateo Barrientos M, Ortiz-Díez G, Ayllón Santiago T. (2024). West Nile Virus Seroprevalence in Wild Birds and Equines in Madrid Province, Spain. Vet Sci, 11(6), 259. https://doi.org/10.3390/vetsci11060259

Publication

ISSN: 2306-7381
NlmUniqueID: 101680127
Country: Switzerland
Language: English
Volume: 11
Issue: 6
PII: 259

Researcher Affiliations

Williams, Richard A J
  • Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University of Madrid, José Antonio Nováis, 28040 Madrid, Spain.
Criollo Valencia, Hillary A
  • Faculty of Health Sciences, Alfonso X El Sabio University, 28691 Madrid, Spain.
López Márquez, Irene
  • Group for the Rehabilitation of Native Fauna and their Habitat-GREFA, 28220 Madrid, Spain.
González González, Fernando
  • Group for the Rehabilitation of Native Fauna and their Habitat-GREFA, 28220 Madrid, Spain.
  • Department of Pharmacology and Toxicology, Faculty of Veterinary Medicine, Complutense University of Madrid, 28040 Madrid, Spain.
Llorente, Francisco
  • Animal Health Research Center (CISA-INIA), CSIC, 28130 Valdeolmos, Spain.
Jiménez-Clavero, Miguel Ángel
  • Animal Health Research Center (CISA-INIA), CSIC, 28130 Valdeolmos, Spain.
Busquets, Núria
  • IRTA, Animal Health Program, Animal Health Research Center (CReSA), Campus of the Autonomous University of Barcelona (UAB), 08193 Cerdanyola del Vallès, Spain.
  • Mixed Research Unit IRTA-UAB in Animal Health, Animal Health Research Center (CReSA), Campus of the Autonomous University of Barcelona (UAB), 08193 Cerdanyola del Vallès, Spain.
Mateo Barrientos, Marta
  • Department of Microbiology and Parasitology, Faculty of Pharmacy, Complutense University of Madrid, 28040 Madrid, Spain.
Ortiz-Díez, Gustavo
  • Department of Animal Medicine and Surgery, Faculty of Veterinary Medicine, Complutense University of Madrid, 28040 Madrid, Spain.
Ayllón Santiago, Tania
  • Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University of Madrid, José Antonio Nováis, 28040 Madrid, Spain.
  • Faculty of Health Sciences, Alfonso X El Sabio University, 28691 Madrid, Spain.

Grant Funding

  • Project code: 1.012.017 / XII call for Research Projects Santander-UAX
  • PID2020-116768RR-C21 / Partially funded by AEI project

Conflict of Interest Statement

The authors declare no conflicts of interest.

References

This article includes 75 references
  1. Brinton MA. Replication cycle and molecular biology of the West Nile virus.. Viruses 2014;6:13–53.
    doi: 10.3390/v6010013pmc: PMC3917430pubmed: 24378320google scholar: lookup
  2. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M. Experimental infection of North American birds with the New York 1999 strain of West Nile virus.. Emerg. Infect. Dis. 2003;9:311–322.
    doi: 10.3201/eid0903.020628pmc: PMC2958552pubmed: 12643825google scholar: lookup
  3. Malkinson M, Banet C, Weisman Y, Pokamunski S, King R, Drouet MT, Deubel V. Introduction of West Nile virus in the Middle East by migrating white storks.. Emerg. Infect. Dis. 2002;8:392–397.
    doi: 10.3201/eid0804.010217pmc: PMC2730252pubmed: 11971773google scholar: lookup
  4. Scherret JH, Poidinger M, Mackenzie JS, Broom AK, Deubel V, Lipkin WI, Briese T, Gould EA, Hall RA. The relationships between West Nile and Kunjin viruses.. Emerg. Infect. Dis. 2001;7:697–705.
    doi: 10.3201/eid0704.017418pmc: PMC2631745pubmed: 11585535google scholar: lookup
  5. Fall G, Di Paola N, Faye M, Dia M, Freire CCDM, Loucoubar C, Zanotto PMDA, Faye O, Sall AA. Biological and phylogenetic characteristics of West African lineages of West Nile virus.. PLoS Negl. Trop. Dis. 2017;11:e0006078.
  6. Smithburn K, Hughes T, Burke A, Paul J. A neurotropic virus isolated from the blood of a native of Uganda.. Am. J. Trop. Med. 1940;20:471–472.
  7. Joubert L, Oudar J, Hannoun C, Beytout D, Corniou B, Guillon J, Panthier R. Epidémiologie du virus West Nile: Étude d’un foyer en Camargue. IV. La méningo-encéphalomyélite du cheval.. Ann. Inst. Pasteur. 1970;118:239–247.
    pubmed: 5461277
  8. Filipe AR, Deandrade HR. Arboviruses in the Iberian peninsula.. Acta Virol. 1990;34:582–591.
    pubmed: 1983187
  9. El Harrack M, Le Guenno B, Gounon P. Isolement du virus West Nile au Maroc.. Virologie 1997;1:248–249.
  10. Kaptoul D, Viladrich PF, Domingo C, Niubó J, Martínez-Yélamos S, De Ory F, Tenorio A. West Nile virus in Spain: Report of the first diagnosed case (in Spain) in a human with aseptic meningitis.. Scand. J. Infect. Dis. 2007;39:70–71.
    doi: 10.1080/00365540600740553pubmed: 17366016google scholar: lookup
  11. Figuerola J, Soriguer R, Rojo G, Tejedor CG, Jimenez-Clavero MA. Seroconversion in wild birds and local circulation of West Nile virus, Spain.. Emerg. Inf. Dis. 2007;13:1915–1917.
    doi: 10.3201/eid1312.070343pmc: PMC2876749pubmed: 18258046google scholar: lookup
  12. European Centre for Disease Prevention and Control (ECDC) West Nile Virus-Infections among Humans and Outbreaks among Equids and/or Birds, 13 December 2023. [(accessed on 22 January 2024)]. Available online: https://www.ecdc.europa.eu/en/west-nile-fever/surveillance-and-disease-data/disease-data-ecdc.
  13. Magallanes S, Llorente F, Ruiz-López MJ, Martínez-de la Puente J, Soriguer R, Calderon J, Jímenez-Clavero MÁ, Aguilera-Sepúlveda P, Figuerola J. Long-term serological surveillance for West Nile and Usutu virus in horses in south-west Spain.. One Health 2023;17:100578.
  14. Abad-Cobo A, Llorente F, Barbero MDC, Cruz-López F, Forés P, Jiménez-Clavero MÁ. Serosurvey reveals exposure to West Nile Virus in asymptomatic horse populations in central Spain prior to recent disease foci.. Transbound. Emerg. Dis. 2017;64:1387–1392.
    doi: 10.1111/tbed.12510pubmed: 27156847google scholar: lookup
  15. Williams RAJ, Sánchez-Llatas CJ, Doménech A, Madrid R, Fandiño S, Cea-Callejo P, Gomez-Lucia E, Benítez L. Emerging and novel viruses in passerine birds.. Microorganisms 2023;11:2355.
  16. Jimenez-Clavero M.A., Sotelo E., Fernandez-Pinero J., Llorente F., Blanco J.M., Rodriguez-Ramos J., Perez-Ramirez E., Hofle U.. West Nile virus in golden eagles, Spain, 2007. Emerg. Infect. Dis. 2008;14:1489–1491.
    doi: 10.3201/eid1409.080190pmc: PMC2603101pubmed: 18760030google scholar: lookup
  17. Marzal A., Ferraguti M., Muriel J., Magallanes S., Ortiz J.A., Garcia-Longoria L., Bravo-Barriga D., Guerrero-Carvajal F., Aguilera-Sepulveda P., Llorente F.. Circulation of zoonotic flaviviruses in wild passerine birds in Western Spain. Vet. Microbiol. 2022;268:5.
    doi: 10.1016/j.vetmic.2022.109399pubmed: 35344925google scholar: lookup
  18. Lopez G., Jimenez-Clavero M.A., Vazquez A., Soriguer R., Gomez-Tejedor C., Tenorio A., Figuerola J.. Incidence of West Nile virus in birds arriving in wildlife rehabilitation centers in southern Spain. Vector-Borne Zoonotic Dis. 2011;11:285–290.
    doi: 10.1089/vbz.2009.0232pubmed: 20645867google scholar: lookup
  19. Llorente F., Pérez-Ramírez E., Fernández-Pinero J., Soriguer R., Figuerola J., Jiménez-Clavero M.A.. Flaviviruses in game birds, southern Spain, 2011–2012. Emerg. Infect. Dis. 2013;19:1023–1025.
    doi: 10.3201/eid1906.130122pmc: PMC3713840pubmed: 23735195google scholar: lookup
  20. Zehender G., Veo C., Ebranati E., Carta V., Rovida F., Percivalle E., Moreno A., Lelli D., Calzolari M., Lavazza A.. Reconstructing the recent West Nile virus lineage 2 epidemic in Europe and Italy using discrete and continuous phylogeography. PLoS ONE 2017;12:e0179679.
  21. Lu L., Zhang F., Oude Munnink B.B., Munger E., Sikkema R.S., Pappa S., Tsioka K., Sinigaglia A., Dal Molin E., Shih B.B.. West Nile virus spread in Europe: Phylogeographic pattern analysis and key drivers. PLoS Pathog. 2024;20:e1011880.
  22. Sotelo E., Fernández-Pinero J., Llorente F., Vázquez A., Moreno A., Agüero M., Cordioli P., Tenorio A., Jiménez-Clavero M.Á.. Phylogenetic relationships of Western Mediterranean West Nile virus strains (1996–2010) using full-length genome sequences: Single or multiple introductions?. J. Gen. Virol. 2011;92:2512–2522.
    doi: 10.1099/vir.0.033829-0pubmed: 21775579google scholar: lookup
  23. García San Miguel Rodríguez-Alarcón L., Fernández-Martínez B., Sierra Moros M.J., Vázquez A., Julián Pachés P., García Villacieros E., Gómez Martín M.B., Figuerola Borras J., Lorusso N., Ramos Aceitero J.M.. Unprecedented increase of West Nile virus neuroinvasive disease, Spain, summer 2020. Eurosurveillance 2021;26:2002010.
  24. Ruiz-López M.J., Aguilera-Sepúlveda P., Cebrián-Camisón S., Figuerola J., Magallanes S., Varona S., Cuesta I., Cano-Gómez C., Sánchez-Mora P., Camacho J.. Re-emergence of a West Nile virus (WNV) variant in South Spain with rapid spread capacity. Viruses 2023;15:2372.
    doi: 10.3390/v15122372pmc: PMC10747266pubmed: 38140614google scholar: lookup
  25. Busquets N., Laranjo-González M., Soler M., Nicolás O., Rivas R., Talavera S., Villalba R., San Miguel E., Torner N., Aranda C.. Detection of West Nile virus lineage 2 in North-Eastern Spain (Catalonia). Transbound. Emerg. Dis. 2019;66:617–621.
    doi: 10.1111/tbed.13086pmc: PMC7380044pubmed: 30506625google scholar: lookup
  26. Aguilera-Sepulveda P., Napp S., Llorente F., Solano-Manrique C., Molina-Lopez R., Obon E., Sole A., Jimenez-Clavero M.A., Fernandez-Pinero J., Busquets N.. West Nile virus lineage 2 spreads westwards in Europe and overwinters in North-Eastern Spain (2017–2020). Viruses 2022;14:569.
    doi: 10.3390/v14030569pmc: PMC8951896pubmed: 35336976google scholar: lookup
  27. Ministerio de Sanidad Dirección General de Salud Pública. Centro de Coordinación de Alertas y Emergencias Sanitarias. Meningoencefalitis Por el Virus Del Nilo Occidental en España 2021. [(accessed on 5 April 2024)]. Available online: https://www.sanidad.gob.es/profesionales/saludPublica/ccayes/alertasActual/docs/20210902_ERR_Nilo_Occidental.pdf.
  28. European Centre for Disease Prevention and Control (ECDC) Historical Data by Year-West Nile Virus Seasonal Surveillance. 2023. [(accessed on 22 January 2024)]. Available online: https://www.ecdc.europa.eu/en/west-nile-fever/surveillance-and-disease-data/historical.
  29. Llorente F., García-Irazábal A., Pérez-Ramírez E., Cano-Gómez C., Sarasa M., Vázquez A., Jiménez-Clavero M.Á.. Influence of flavivirus co-circulation in serological diagnostics and surveillance: A model of study using West Nile, Usutu and Bagaza viruses. Transbound. Emerg. Dis. 2019;66:2100–2106.
    doi: 10.1111/tbed.13262pubmed: 31150146google scholar: lookup
  30. Jurado-Tarifa E., Napp S., Lecollinet S., Arenas A., Beck C., Cerda-Cuellar M., Fernandez-Morente M., Garcia-Bocanegra I.. Monitoring of West Nile virus, Usutu virus and Meaban virus in waterfowl used as decoys and wild raptors in southern Spain. Comp. Immunol. Microbiol. 2016;49:58–64.
    doi: 10.1016/j.cimid.2016.10.001pubmed: 27865265google scholar: lookup
  31. Höfle U., Gamino V., de Mera I.G.F., Mangold A.J., Ortiz J.A., de la Fuente J.. Usutu virus in migratory song thrushes, Spain. Emerg. Infect. Dis. 2013;19:1173–1175.
    doi: 10.3201/eid1907.130199pmc: PMC3713991pubmed: 23764143google scholar: lookup
  32. Napp S., Llorente F., Beck C., Jose-Cunilleras E., Soler M., Pailler-Garcia L., Amaral R., Aguilera-Sepulveda P., Pifarre M., Molina-Lopez R.. Widespread circulation of Flaviviruses in horses and birds in northeastern Spain (Catalonia) between 2010 and 2019. Viruses 2021;13:2404.
    doi: 10.3390/v13122404pmc: PMC8708358pubmed: 34960673google scholar: lookup
  33. Agüero M., Fernandez-Pinero J., Buitrago D., Sanchez A., Elizalde M., Miguel E.S., Villalba R., Llorente F., Jimenez-Clavero M.A.. Bagaza virus in partridges and pheasants, Spain, 2010. Emerg. Infect. Dis. 2011;17:1498–1501.
    doi: 10.3201/eid1708.110077pmc: PMC3381565pubmed: 21801633google scholar: lookup
  34. Arnal A., Gómez-Díaz E., Cerdà-Cuéllar M., Lecollinet S., Pearce-Duvet J., Busquets N., García-Bocanegra I., Pagès N., Vittecoq M., Hammouda A.. Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the western Mediterranean basin. PLoS ONE 2014;9:e89601.
  35. Mansfield K.L., Morales A.B., Johnson N., Ayllón N., Höfle U., Alberdi P., Fernández de Mera I.G., Marín J.F.G., Gortázar C., de la Fuente J.. Identification and characterization of a novel tick-borne flavivirus subtype in goats (Capra hircus) in Spain. J. Gen. Virol. 2015;96:1676–1681.
    doi: 10.1099/vir.0.000096pubmed: 25701823google scholar: lookup
  36. López-Albors O., Gil F., Vázquez J.M., Latorre R., Ramíre-Zarzosa G., Orenes M., Moreno F.. Revisión: Nomenclatura e iconografía de las partes de la pluma y sus diferentes tipos. An. Vet. Murcia 1999;15:3–16.
  37. Svensson L., Mullarney K. Guía de Aves de España y Europa. Ediciones Omega; Barcelona, Spain: 2023.
  38. Gómez-Catasús J., Carrascal L.M., Moraleda V., Colsa J., Garcés F., Schuster C.. Factors affecting differential underestimates of bird collision fatalities at electric lines: A case study in the Canary Islands. Ardeola 2020;68:71–94.
  39. Bravo-Barriga D., Aguilera-Sepulveda P., Guerrero-Carvajal F., Llorente F., Reina D., Perez-Martin J.E., Jimenez-Clavero M.A., Frontera E.. 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.2021.109020pubmed: 33677369google scholar: lookup
  40. Pallari C.T., Efstathiou A., Moysi M., Papanikolas N., Christodoulou V., Mazeris A., Koliou M., Kirschel A.N.. Evidence of West Nile virus seropositivity in wild birds on the island of Cyprus. Comp. Immunol. Microbiol. Infect. Dis. 2021;74:101592.
    doi: 10.1016/j.cimid.2020.101592pubmed: 33276289google scholar: lookup
  41. Chevalier V., Reynaud P., Lefrançois T., Durand B., Baillon F., Balança G., Gaidet N., Mondet B., Lancelot R.. Predicting West Nile virus seroprevalence in wild birds in Senegal. Vector-Borne Zoonotic Dis. 2009;9:589–596.
    doi: 10.1089/vbz.2008.0130pubmed: 19196131google scholar: lookup
  42. Beveroth T.A., Ward M.P., Lampman R.L., Ringia A.M., Novak R.J.. Changes in seroprevalence of West Nile virus across Illinois in free-ranging birds from 2001 through 2004. Am. J. Trop. Med. Hyg. 2006;74:174–179.
    doi: 10.4269/ajtmh.2006.74.174pubmed: 16407365google scholar: lookup
  43. Islam A., Islam S., Hossain M.E., Ferdous J., Abedin J., Ziaur Rahman M., Rahman M.K., Hoque M.A., Hassan M.M.. Serological evidence of West Nile virus in wild birds in Bangladesh. Vet. Sci. 2020;7:164.
    doi: 10.3390/vetsci7040164pmc: PMC7712446pubmed: 33126740google scholar: lookup
  44. Niczyporuk J.S., Samorek-Salamonowicz E., Lecollinet S., Pancewicz S.A., Kozdruń W., Czekaj H.. Occurrence of West Nile virus antibodies in wild birds, horses, and humans in Poland. BioMed Res. Int. 2015;2015:234181.
    doi: 10.1155/2015/234181pmc: PMC4383358pubmed: 25866767google scholar: lookup
  45. Amin M., Zaim M., Edalat H., Basseri H.R., Yaghoobi-Ershadi M.R., Rezaei F., Azizi K., Salehi-Vaziri M., Ghane M., Yousefi S.. Seroprevalence study on West Nile virus (WNV) infection, a hidden viral disease in Fars province, southern Iran. J. Arthropod-Borne Dis. 2020;14:173–184.
    doi: 10.18502/jad.v14i2.3735pmc: PMC7738928pubmed: 33365345google scholar: lookup
  46. Paştiu A.I., Pap P.L., Vágási C.I., Niculae M., Páll E., Domşa C., Brudaşcă F.G., Spînu M.. Wild birds in Romania are more exposed to West Nile virus than to Newcastle disease virus. Vector Borne Zoonotic Dis. 2016;16:176–180.
    doi: 10.1089/vbz.2015.1805pubmed: 26824796google scholar: lookup
  47. Ferraguti M., Martinez-De la Puente J., Soriguer R., Llorente F., Jimenez-Clavero M.A., Figuerola J.. West Nile virus-neutralizing antibodies in wild birds from southern Spain. Epidemiol. Infect. 2016;144:1907–1911.
    doi: 10.1017/S0950268816000133pmc: PMC9150652pubmed: 26846720google scholar: lookup
  48. Zakhia R., Dupuis A.P., Khodr F., Fadel M., Kramer L.D., Haddad N.. Evidence of West Nile virus circulation in Lebanon. Viruses 2021;13:994.
    doi: 10.3390/v13060994pmc: PMC8227205pubmed: 34073485google scholar: lookup
  49. Benjelloun A., El Harrak M., Calistri P., Loutfi C., Kabbaj H., Conte A., Ippoliti C., Danzetta M.L., Belkadi B.. Seroprevalence of West Nile virus in horses in different Moroccan regions. Vet. Med. Sci. 2017;3:198–207.
    doi: 10.1002/vms3.71pmc: PMC5677775pubmed: 29152314google scholar: lookup
  50. Sule W.F., Oluwayelu D.O., Adedokun R.A.M., Rufai N., McCracken F., Mansfield K.L., Johnson N.. High seroprevelance of West Nile virus antibodies observed in horses from southwestern Nigeria. Vector-Borne Zoonotic Dis. 2015;15:218–220.
    doi: 10.1089/vbz.2014.1706pmc: PMC4369928pubmed: 25793479google scholar: lookup
  51. Aquila a-Life. Informe Anual de Seguimiento de Aves Liberadas en Madrid 2022. [(accessed on 10 November 2023)]. Available online: https://aquila-a-life.org/index.php/es/avances/acciones/monitorizacion/62-acciones-d/476-accion-d1-informe-anual-de-seguimiento-de-aves-liberadas-en-madrid-2022.
  52. Instituto Nacional de Estadística List of Place Name: Population of the Continuous Municipal Register by Population Unit: Alcobendas. 2024. [(accessed on 25 January 2024)]. Available online: https://www.ine.es/en/index.htm.
  53. Baitchman E.J., Tlusty M.F., Murphy H.W.. Passive transfer of maternal antibodies to West Nile virus in flamingo chicks (Phoenicopterus chilensis and Phoenicopterus ruber ruber). J. Zoo Wildl. Med. 2007;38:337–340.
  54. Nemeth N.M., Hahn D.C., Gould D.H., Bowen R.A.. Experimental West Nile virus infection in Eastern screech owls (Megascops asio). Avian Dis. 2006;50:252–258.
    doi: 10.1637/7466-110105R1.1pubmed: 16863076google scholar: lookup
  55. Millins C., Reid A., Curry P., Drebot M.A., Andonova M., Buck P., Leighton F.A.. Evaluating the use of house sparrow nestlings as sentinels for West Nile virus in Saskatchewan. Vector Borne Zoonotic Dis. 2011;11:53–58.
    doi: 10.1089/vbz.2009.0235pubmed: 20518643google scholar: lookup
  56. Nemeth N.M., Bowen R.A.. Dynamics of passive immunity to West Nile virus in domestic chickens (Gallus gallus domesticus). Am. J. Trop. Med. Hyg. 2007;76:310–317.
    doi: 10.4269/ajtmh.2007.76.310pubmed: 17297041google scholar: lookup
  57. Xirouchakis S.M.. Breeding biology and reproductive performance of Griffon Vultures Gyps fulvus on the island of Crete (Greece). Bird Study 2010;57:213–225.
    doi: 10.1080/00063650903505754google scholar: lookup
  58. BirdLife International IUCN Red List for Birds. 2023. [(accessed on 27 October 2023)]. Available online: http://datazone.birdlife.org.
  59. SEO/Birdlife La Guía de Aves de España. 2023. [(accessed on 15 November 2023)]. Available online: https://seo.org/guia-de-aves/
  60. Figuerola J., Jiménez-Clavero M.A., López G., Rubio C., Soriguer R., Gómez-Tejedor C., Tenorio A.. Size matters: West Nile virus neutralizing antibodies in resident and migratory birds in Spain. Vet. Microbiol. 2008;132:39–46.
    doi: 10.1016/j.vetmic.2008.04.023pubmed: 18514437google scholar: lookup
  61. Vidaña B., Busquets N., Napp S., Pérez-Ramírez E., Jiménez-Clavero M.A., Johnson N.. The role of birds of prey in West Nile virus epidemiology. Vaccines 2020;8:550.
    doi: 10.3390/vaccines8030550pmc: PMC7564710pubmed: 32967268google scholar: lookup
  62. Castillo-Olivares J., Mansfield K.L., Phipps L.P., Johnson N., Tearle J., Fooks A.R.. Antibody response in horses following experimental infection with West Nile virus lineages 1 and 2. Transbound. Emerg. Dis. 2011;58:206–212.
  63. Jimenez-Clavero M.A., Llorente F., Sotelo E., Soriguer R., Gomez-Tejedor C., Figuerola J.. West Nile virus serosurveillance in horses in Doñana, Spain, 2005 to 2008. Vet. Rec. 2010;167:379–380.
    doi: 10.1136/vr.c3155pubmed: 20817900google scholar: lookup
  64. European Centre for Disease Prevention and Control Culex Pipiens-Factsheet for Experts. 2020. [(accessed on 22 January 2024)]. Available online: https://www.ecdc.europa.eu/en/infectious-disease-topics/related-public-health-topics/disease-vectors/facts/mosquito-factsheets/culex-pipiens.
  65. Höfle U, Blanco J.M, Crespo E, Naranjo V, Jiménez-Clavero M.A, Sanchez A, de La Fuente J, Gortazar C. West Nile virus in the endangered Spanish imperial eagle. Vet. Microbiol. 2008;129:171–178.
    doi: 10.1016/j.vetmic.2007.11.006pubmed: 18155367google scholar: lookup
  66. Aguilera-Sepulveda P, Gomez-Martin B, Aguero M, Jimenez-Clavero M.A, Fernandez-Pinero J. A new cluster of West Nile virus lineage 1 isolated from a northern goshawk in Spain. Transbound. Emerg. Dis. 2022;69:3121–3127.
    doi: 10.1111/tbed.14399pubmed: 34812592google scholar: lookup
  67. Alba A, Allepuz A, Napp S, Soler M, Selga I, Aranda C, Casal J, Pages N, Hayes E.B, Busquets N. Ecological surveillance for West Nile in Catalonia (Spain), learning from a five-year period of follow-up. Zoonoses Public Health 2014;61:181–191.
    doi: 10.1111/zph.12048pubmed: 23590452google scholar: lookup
  68. Cano-Terriza D, Guerra R, Lecollinet S, Cerda-Cuellar M, Cabezon O, Almeria S, Garcia-Bocanegra I. Epidemiological survey of zoonotic pathogens in feral pigeons (Columba livia var. domestica) and sympatric zoo species in Southern Spain. Comp. Immunol. Microbiol. Infect. Dis. 2015;43:22–27.
    pubmed: 26616657
  69. Figuerola J, Angel Jiménez-Clavero M, Rojo G, Gómez-Tejedor C, Soriguer R. Prevalence of West Nile virus neutralizing antibodies in colonial aquatic birds in southern Spain. Avian Pathol. 2007;36:209–212.
    doi: 10.1080/03079450701332329pubmed: 17497333google scholar: lookup
  70. Gangoso L, Grande J.M, Llorente F, Jiménez-Clavero M.Á, Pérez J.M, Figuerola J. Prevalence of neutralizing antibodies to West Nile virus in Eleonora’s Falcons in the Canary Islands. J. Wildlife Dis. 2010;46:1321–1324.
    doi: 10.7589/0090-3558-46.4.1321pubmed: 20966288google scholar: lookup
  71. Garcia-Bocanegra I, Busquets N, Napp S, Alba A, Zorrilla I, Villalba R, Arenas A. 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;11:1107–1113.
    doi: 10.1089/vbz.2009.0237pubmed: 21142954google scholar: lookup
  72. Garcia-Bocanegra I, Franco J.J, Leon C.I, Barbero-Moyano J, Garcia-Mina M.V, Fernandez-Molera V, Gomez M.B, Cano-Terriza D, Gonzalvez M. High exposure of West Nile virus in equid and wild bird populations in Spain following the epidemic outbreak in 2020. Transbound. Emerg. Dis. 2022;69:3624–3636.
    doi: 10.1111/tbed.14733pmc: PMC10092718pubmed: 36222172google scholar: lookup
  73. Lopez G, Jimenez-Clavero A, Tejedor C.G, 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;8:615–621.
    doi: 10.1089/vbz.2007.0200pubmed: 18399777google scholar: lookup
  74. Martínez-de la Puente J, Ferraguti M, Ruiz S, Roiz D, Llorente F, Pérez-Ramírez E, Jiménez-Clavero M.Á, Soriguer R, Figuerola J. Mosquito community influences West Nile virus seroprevalence in wild birds: Implications for the risk of spillover into human populations. Sci. Rep. 2018;8:2599.
    doi: 10.1038/s41598-018-20825-zpmc: PMC5805708pubmed: 29422507google scholar: lookup
  75. Napp S, Montalvo T, Pinol-Baena C, Gomez-Martin M.B, Nicolas-Francisco O, Soler M, Busquets N. Usefulness of Eurasian magpies (Pica pica) for West Nile virus surveillance in non-endemic and endemic situations. Viruses 2019;11:2404.
    doi: 10.3390/v11080716pmc: PMC6722797pubmed: 31387316google scholar: lookup

Citations

This article has been cited 4 times.
  1. Ayllón T, Martínez I, Ortiz-Díez G, Navarro A, Fuster F, Iriso A, Villaverde S, Lara J, García N. Long-Term Surveillance of Chlamydia psittaci and West Nile Virus in Wild Birds from Central Spain (2013-2022).. Microorganisms 2025 Dec 25;14(1).
  2. Nistor P, Stanga L, Chirila A, Iorgoni V, Gligor A, Ciresan A, Popa I, Florea B, Imre M, Cocioba V, Iancu I, Degi J, Herman V. Seroprevalence and Passive Clinical Surveillance of West Nile Virus in Horses from Ecological High-Risk Areas in Western Romania: Exploratory Findings from a Cross-Sectional Study.. Microorganisms 2025 Aug 16;13(8).
  3. Gobbo F, Chiarello G, Sgubin S, Toniolo F, Gradoni F, Danca LI, Carlin S, Capello K, De Conti G, Bortolami A, Varotto M, Favero L, Brichese M, Russo F, Mutinelli F, Vogiatzis S, Pacenti M, Barzon L, Montarsi F. Integrated One Health Surveillance of West Nile Virus and Usutu Virus in the Veneto Region, Northeastern Italy, from 2022 to 2023.. Pathogens 2025 Feb 25;14(3).
    doi: 10.3390/pathogens14030227pubmed: 40137712google scholar: lookup
  4. Carrasco L, Utrilla MJ, Fuentes-Romero B, Fernandez-Novo A, Martin-Maldonado B. West Nile Virus: An Update Focusing on Southern Europe.. Microorganisms 2024 Dec 18;12(12).