Analyze Diet
One health (Amsterdam, Netherlands)2023; 17; 100578; doi: 10.1016/j.onehlt.2023.100578

Long-term serological surveillance for West Nile and Usutu virus in horses in south-West Spain.

Abstract: West Nile virus (WNV) is a re-emerging zoonotic pathogen with increasing incidence in Europe, producing a recent outbreak in 2020 in Spain with 77 human cases and eight fatalities. However, the factors explaining the observed changes in the incidence of WNV in Europe are not completely understood. Longitudinal monitoring of WNV in wild animals across Europe is a useful approach to understand the eco-epidemiology of WNV in the wild and the risk of spillover into humans. However, such studies are very scarce up to now. Here, we analysed the occurrence of WNV and Usutu virus (USUV) antibodies in 2102 samples collected between 2005 and 2020 from a population of feral horses in Doñana National Park. The prevalence of WNV antibodies varied between years, with a mean seroprevalence of 8.1% (range 0%-25%) and seasonally. Climate conditions including mean minimum annual temperatures and mean rainy days per year were positively correlated with WNV seroprevalence, while the annual rainfall was negatively. We also detected the highest incidence of seroconversions in 2020 coinciding with the human outbreak in southern Spain. Usutu virus-specific antibodies were detected in the horse population since 2011. The WNV outbreak in humans was preceded by a long period of increasing circulation of WNV among horses with a very high exposure in the year of the outbreak. These results highlight the utility of One Health approaches to better understand the transmission dynamics of zoonotics pathogens.
Publication Date: 2023-06-12 PubMed ID: 38024263PubMed Central: PMC10665154DOI: 10.1016/j.onehlt.2023.100578Google 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.

The research investigates the occurrence of West Nile virus (WNV) and Usutu virus (USUV) antibodies in horses in southwest Spain, revealing that climate conditions and increasing WNV activity among horses anticipated a 2020 human outbreak.

Overview and Objectives of the Research

  • The aim of this study was to explore the factors contributing to changes in the incidence of West Nile Virus (WNV) in Europe, specifically through a longitudinal analysis of WNV and Usutu virus (USUV) in a horse population in Doñana National Park, Spain.
  • These findings stem from a need to better understand re-emerging zoonotic pathogens like WNV, whose prevalence has been increasing in Europe, resulting in a significant outbreak in Spain in 2020.
  • The researchers addressed the lack of previous studies monitoring WNV in wild animals across Europe, aiming to clarify the eco-epidemiology of WNV and the potential risk of viral transmission to humans.

Methodology and Results

  • The researchers analyzed 2102 samples taken from feral horses between 2005 and 2020 for the occurrence of WNV and USUV antibodies.
  • The level of WNV antibodies varied annually, with an average seroprevalence of 8.1%, and also demonstrated seasonal fluctuations.
  • Climate factors such as mean minimum annual temperatures and average rainy days per year were found to be positively correlated with WNV seroprevalence, whereas overall annual rainfall was negatively correlated.
  • Interestingly, the highest incidence of seroconversions were detected in 2020, coinciding with the human outbreak in Southern Spain.
  • For the first time, USUV-specific antibodies were detected in the horse population in 2011.

Conclusions and Implications

  • The most revealing result showed that a long-term increase in WNV circulation among horses preceded the human outbreak, with the exposed level peaking in the outbreak year.
  • This provides valuable insight into the transmission dynamics of zoonotic pathogens and underscores the potential for a One Health approach — integrating human, animal and environmental health — in predicting and managing such outbreaks.
  • These findings serve as an alert system for future WNV outbreaks in human populations, suggesting that monitoring seroprevalence in certain animal populations could serve as a warning for potential spillover into humans.

Cite This Article

APA
Magallanes S, Llorente F, Ruiz-López MJ, Martínez-de la Puente J, Soriguer R, Calderon J, Jímenez-Clavero MÁ, Aguilera-Sepúlveda P, Figuerola J. (2023). Long-term serological surveillance for West Nile and Usutu virus in horses in south-West Spain. One Health, 17, 100578. https://doi.org/10.1016/j.onehlt.2023.100578

Publication

ISSN: 2352-7714
NlmUniqueID: 101660501
Country: Netherlands
Language: English
Volume: 17
Pages: 100578
PII: 100578

Researcher Affiliations

Magallanes, Sergio
  • Department of Wetland Ecology (EBD-CSIC), Estación Biológica de Doñana, Avda. Américo Vespucio 26, E-41092 Sevilla, Spain.
Llorente, Francisco
  • Centro de Investigación en Sanidad Animal (CISA-INIA), CSIC, 28130, Valdeolmos, Madrid, Spain.
Ruiz-López, María José
  • Department of Wetland Ecology (EBD-CSIC), Estación Biológica de Doñana, Avda. Américo Vespucio 26, E-41092 Sevilla, Spain.
  • CIBER of Epidemiology and Public Health (CIBERESP), Spain.
Martínez-de la Puente, Josué
  • Department of Parasitology, University of Granada, Granada E-18071, Spain.
  • CIBER of Epidemiology and Public Health (CIBERESP), Spain.
Soriguer, Ramon
  • Department of Wetland Ecology (EBD-CSIC), Estación Biológica de Doñana, Avda. Américo Vespucio 26, E-41092 Sevilla, Spain.
  • CIBER of Epidemiology and Public Health (CIBERESP), Spain.
Calderon, Juan
  • Department of Wetland Ecology (EBD-CSIC), Estación Biológica de Doñana, Avda. Américo Vespucio 26, E-41092 Sevilla, Spain.
Jímenez-Clavero, Miguel Ángel
  • Centro de Investigación en Sanidad Animal (CISA-INIA), CSIC, 28130, Valdeolmos, Madrid, Spain.
  • CIBER of Epidemiology and Public Health (CIBERESP), Spain.
Aguilera-Sepúlveda, Pilar
  • Centro de Investigación en Sanidad Animal (CISA-INIA), CSIC, 28130, Valdeolmos, Madrid, Spain.
Figuerola, Jordi
  • Department of Wetland Ecology (EBD-CSIC), Estación Biológica de Doñana, Avda. Américo Vespucio 26, E-41092 Sevilla, Spain.
  • CIBER of Epidemiology and Public Health (CIBERESP), Spain.

Conflict of Interest Statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

This article includes 50 references
  1. Beck C, Jimenez-Clavero M.A., Leblond A, Durand B, Nowotny N, Leparc-Goffart I, Zientara S, Jourdain E, Lecollinet S. Flaviviruses in europe: complex circulation patterns and their consequences for the diagnosis and control of west nile disease.. Int. J. Environ. Res. Public Health 2013;10:6049–6083.
    doi: 10.3390/ijerph10116049pmc: PMC3863887pubmed: 24225644google scholar: lookup
  2. Reisen W.K., Fang Y, Martinez V.M.. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission.. J. Med. Entomol. 2005;42:367–375.
    doi: 10.1093/jmedent/42.3.367pubmed: 15962789google scholar: lookup
  3. Root J.J., Bosco-Lauth A.M.. West Nile Virus Associations in Wild Mammals: an update.. Viruses 2019;11.
    doi: 10.3390/V11050459pmc: PMC6563505pubmed: 31117189google scholar: lookup
  4. Petersen L.R., Marfin A.A.. West Nile virus: a primer for the clinician.. Ann. Intern. Med. 2002;137:173–179.
  5. Venter M., Pretorius M., Fuller J.A., Botha E., Rakgotho M., Stivaktas V., Weyer C., Romito M., Williams J.. West Nile virus lineage 2 in horses and other animals with neurologic disease, South Africa, 2008-2015.. Emerg. Infect. Dis. 2017;23:2060–2064.
    doi: 10.3201/EID2312.162078pmc: PMC5708237pubmed: 29148375google scholar: lookup
  6. Bertram F.M., Thompson P.N., Venter M.. Epidemiology and clinical presentation of west nile virus infection in Horses in South Africa, 2016–2017.. Pathog. 2021;10(2020):20.
    doi: 10.3390/PATHOGENS10010020pmc: PMC7823741pubmed: 33396935google scholar: lookup
  7. Vilibic-Cavlek T., Savic V., Petrovic T., Toplak I., Barbic L., Petric D., Tabain I., Hrnjakovic-Cvjetkovic I., Bogdanic M., Klobucar A., Mrzljak A., Stevanovic V., Dinjar-Kujundzic P., Radmanic L., Monaco F., Listes E., Savini G. Emerging trends in the epidemiology of West Nile and Usutu virus infections in Southern Europe.. Front. Vet. Sci. 2019;6:437.
  8. Figuerola J., Soriguer R., Rojo G., Tejedor C.G., Jimenez-Clavero M.A.. Seroconversion in wild birds and local circulation of West Nile Virus, Spain.. Emerg. Infect. Dis. 2007;13:1915.
    doi: 10.3201/EID1312.070343pmc: PMC2876749pubmed: 18258046google scholar: lookup
  9. 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
  10. Jiménez-Clavero M.A., Llorente F., Sotelo E., Soriguer R., Gómez-Tejedor C., Figuerola J., et al. Vet. Rec. 2010;167:379–380. doi: 10.1136/VR.C3155.
    doi: 10.1136/VR.C3155pubmed: 20817900google scholar: lookup
  11. Jiménez-Clavero M.A., Sotelo E., Fernandez-Pinero J., Llorente F., Blanco J.M., Rodriguez-Ramos J., Perez-Ramirez E., Höfle 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
  12. Vázquez A., Sánchez-Seco M.P., Ruiz S., Molero F., Hernández L., Moreno J., Magallanes A., Tejedor C.G., Tenorio A.. Putative new lineage of West Nile Virus, Spain.. Emerg. Infect. Dis. 2010;16:549.
    doi: 10.3201/EID1603.091033pmc: PMC3322021pubmed: 20202444google scholar: lookup
  13. Rodríguez-Alarcón L.G.S.M., Fernández-Martínez B., Moros M.J.S., Vázquez A., Pachés P.J., Villacieros E.G., Martín M.B.G., Borras J.F., Lorusso N., Aceitero J.M.R., Moro E., de Celis A., Oyonarte S., Mahillo B., González L.J.R., Sánchez-Seco M.P., Rodríguez B.S., Catalán U.A., Contreras S.R., Pérez-Olmeda M., Soria F.S.. Unprecedented increase of West Nile virus neuroinvasive disease, Spain, summer 2020.. Eurosurveillance 2021;26:2002010.
  14. Figuerola J., Jiménez-Clavero M.Á., Ruíz-López M.J., Llorente F., Ruiz S., Hoefer A., Aguilera-Sepúlveda P., Jiménez-Peñuela J., García-Ruiz O., Herrero L., Soriguer R.C., Delgado R. Fernández, Sánchez-Seco M.P., la Puente J. Martínez-de, Vázquez A.. A One Health view of the West Nile virus outbreak in Andalusia (Spain) in 2020.. Emerg. Microbes Infect. 2022;11:2570–2578.
  15. Brugueras S., Fernández-Martínez B., Martínez-de la Puente J., Figuerola J., Porro T.M., Rius C., Larrauri A., Gómez-Barroso D.. Environmental drivers, climate change and emergent diseases transmitted by mosquitoes and their vectors in southern Europe: A systematic review.. Environ. Res. 2020;191.
    doi: 10.1016/J.ENVRES.2020.110038pubmed: 32810503google scholar: lookup
  16. Giesen C., Herrador Z., Fernandez-Martinez B., Figuerola J., Gangoso L., Vazquez A., Gómez-Barroso D.. A systematic review of environmental factors related to WNV circulation in European and Mediterranean countries.. One Heal. 2023;16.
  17. Hahn M.B., Monaghan A.J., Hayden M.H., Eisen R.J., Delorey M.J., Lindsey N.P., Nasci R.S., Fischer M.. Meteorological conditions associated with increased incidence of West Nile virus disease in the United States, 2004–2012.. Am. J. Trop. Med. Hyg. 2015;92:1013.
    doi: 10.4269/AJTMH.14-0737pmc: PMC4426558pubmed: 25802435google scholar: lookup
  18. Vilibic-Cavlek T., Petrovic T., Savic V., Barbic L., Tabain I., Stevanovic V., Klobucar A., Mrzljak A., Ilic M., Bogdanic M., Benvin I., Santini M., Capak K., Monaco F., Listes E., Savini G. Epidemiology of usutu virus: the European scenario.. Pathog. (Basel, Switzerland) 2020;9:1–19.
    doi: 10.3390/PATHOGENS9090699pmc: PMC7560012pubmed: 32858963google scholar: lookup
  19. Busquets N., Alba A., Allepuz A., Aranda C., Núñez J.I.. Usutu virus sequences in Culex pipiens (Diptera: Culicidae), Spain.. Emerg. Infect. Dis. 2008;14:861.
    doi: 10.3201/EID1405.071577pmc: PMC2600269pubmed: 18439389google scholar: lookup
  20. Vázquez A., Ruiz S., Herrero L., Moreno J., Molero F., Magallanes A., Sánchez-Seco M.P., Figuerola J., Tenorio A.. West Nile and Usutu viruses in Mosquitoes in Spain, 2008–2009.. Am. J. Trop. Med. Hyg. 2011;85:178.
    doi: 10.4269/AJTMH.2011.11-0042pmc: PMC3122364pubmed: 21734145google scholar: lookup
  21. Roiz D., Vázquez A., Ruiz S., Tenorio A., Soriguer R., Figuerola J.. Evidence that passerine birds act as amplifying hosts for usutu virus circulation.. Ecohealth 2019;16:734–742.
  22. Bravo-Barriga D., Ferraguti M., Magallanes S., Aguilera-Sepúlveda P., Llorente F., Pérez-Ramírez E., Vázquez A., Guerrero-Carvajal F., Sánchez-Seco M.P., Jiménez-Clavero M.Á., Mora-Rubio C., Marzal A., Frontera E., de Lope F.. Identification of Usutu Virus Africa 3 lineage in a survey of mosquitoes and birds from urban areas of Western Spain.. Transbound. Emerg. Dis. 2023;2023:1–10.
    doi: 10.1155/2023/6893677google scholar: lookup
  23. Epp T., Waldner C., West K., Townsend H.. Factors associated with West Nile virus disease fatalities in horses.. Can. Vet. J. 2007;48:1137.
    pmc: PMC2034420pubmed: 18050794
  24. Roiz D., Ruiz S., Soriguer R., Figuerola J.. Climatic effects on mosquito abundance in Mediterranean wetlands.. Parasit. Vectors. 2014;7:1–13.
  25. 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
  26. Calisher C.H., Karabatsos N., Dalrymple J.M., Shope R.E., Porterfield J.S., Westaway E.G., Brandt W.E.. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera.. J. Gen. Virol. 1989;70:37–43.
  27. Sotelo E., Llorente F., Rebollo B., Camuñas A., Venteo A., Gallardo C., Lubisi A., Rodríguez M.J., Sanz A.J., Figuerola J., Jiménez-Clavero M.Á.. Development and evaluation of a new epitope-blocking ELISA for universal detection of antibodies to West Nile virus.. J. Virol. Methods. 2011;174:35–41.
  28. Agüero M., Fernández-Pinero J., Buitrago D., Sánchez A., Elizalde M., Miguel E.S., Villalba R., Llorente F., Jiménez-Clavero M.Á.. Bagaza virus in partridges and pheasants, Spain, 2010.. Emerg. Infect. Dis. 2011;17:1498.
    doi: 10.3201/EID1708.110077pmc: PMC3381565pubmed: 21801633google scholar: lookup
  29. Meinshausen M., Smith S.J., Calvin K., Daniel J.S., Kainuma M.L.T., Lamarque J., Matsumoto K., Montzka S.A., Raper S.C.B., Riahi K., Thomson A., Velders G.J.M., van Vuuren D.P.P.. The RCP greenhouse gas concentrations and their extensions from 1765 to 2300.. Clim. Chang. 2011;109:213–241.
  30. Zuur A.F., Ieno E.N., Elphick C.S.. A protocol for data exploration to avoid common statistical problems.. Methods Ecol. Evol. 2010;1:3–14.
  31. Napp S., Llorente F., Beck C., Jose-cunilleras E., Soler M., Pailler-garcía L., Amaral R., Aguilera-sepúlveda P., Pifarré M., Molina-lópez R., Obón E., Nicolás O., Lecollinet S., Jiménez-clavero M.Á., Busquets N.. Widespread circulation of flaviviruses in horses and birds in northeastern spain (Catalonia) between 2010 and 2019.. Viruses 2021;13.
    doi: 10.3390/V13122404/S1pmc: PMC8708358pubmed: 34960673google scholar: lookup
  32. Ferraguti M., Martínez-de la Puente J., Jiménez-Clavero M.Á., Llorente F., Roiz D., Ruiz S., Soriguer R., Figuerola J.. A field test of the dilution effect hypothesis in four avian multi-host pathogens.. PLoS Pathog. 2021;17.
  33. Abad-Cobo A., Llorente F., Del Barbero M.C., Cruz-López F., Forés P., Jiménez-Clavero M.. 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
  34. Guerrero-Carvajal F., Bravo-Barriga D., Martín-Cuervo M., Aguilera-Sepúlveda P., Ferraguti M., Jiménez-Clavero M.Á., Llorente F., Alonso J.M., Frontera E.. Serological evidence of co-circulation of West Nile and Usutu viruses in equids from western Spain.. Transbound. Emerg. Dis. 2021;68:1432–1444.
    doi: 10.1111/TBED.13810pubmed: 32853452google scholar: lookup
  35. Selim A., Megahed A., Kandeel S., Alouffi A., Almutairi M.M.. West Nile virus seroprevalence and associated risk factors among horses in Egypt.. Sci. Report. 2021;2021 111. 11:1–9.
    doi: 10.1038/s41598-021-00449-6pmc: PMC8536702pubmed: 34686730google scholar: lookup
  36. Folstad I., Karter A.J.. Parasites, Bright males, and the immunocompetence handicap.. Am. Nat. 1992;139:603–622.
    doi: 10.1086/285346google scholar: lookup
  37. Turner J.L., Waggoner J.W., Rose S.S., Arns M.J., Hankins K.G., Tuttle J.. West Nile Virus antibody titers and total immunoglobulin G concentrations in foals from mares vaccinated in Late Gestation.. J. Equine Vet. Sci. 2008;28:17–21.
  38. Kilpatrick A.M., Meola M.A., Moudy R.M., Kramer L.D.. Temperature, viral genetics, and the transmission of west nile virus by culex pipiens mosquitoes.. PLoS Pathog. 2008;4.
  39. Paz S., Semenza J.C.. Environmental drivers of West Nile fever epidemiology in Europe and Western Asia—A Review.. Int. J. Environ. Res. Public Health 2013;10:3543–3562.
    doi: 10.3390/IJERPH10083543pmc: PMC3774453pubmed: 23939389google scholar: lookup
  40. Camp J.V., Nowotny N.. The knowns and unknowns of West Nile virus in Europe: what did we learn from the 2018 outbreak?. Expert Rev. Anti-Infect. Ther. 2020;18:145–154.
    doi: 10.1080/14787210.2020.1713751pubmed: 31914833google scholar: lookup
  41. Marini G., Manica M., Delucchi L., Pugliese A., Rosà R.. Spring temperature shapes West Nile virus transmission in Europe.. Acta Trop. 2021;215.
  42. Vandyk J.K., Rowley W.A.. Response of Iowa mosquito populations to unusual precipitation patterns as measured by New Jersey light trap collections.. J. Am. Mosq. Control Assoc. 1995;11:200–205.
    pubmed: 7595446
  43. Chase J.M., Knight T.M.. Drought-induced mosquito outbreaks in wetlands.. Ecol. Lett. 2003;6:1017–1024.
  44. Roiz D., Vazquez A., Rosà R., Muñoz J., Arnoldi D., Rosso F., Figuerola J., Tenorio A., Rizzoli A.. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy.. J. Vector Ecol. 2012;37:20–28.
  45. Muñoz J., Ruiz S., Soriguer R., Alcaide M., Viana D.S., Roiz D., Vázquez A., Figuerola J.. Feeding patterns of potential West Nile virus vectors in south-west Spain.. PLoS One. 2012;7(6).
  46. Roiz D., Ruiz S., Soriguer R., Figuerola J.. Landscape effects on the presence, abundance and diversity of mosquitoes in Mediterranean wetlands.. PLoS One. 2015;10(6).
  47. AEMet Agencia Estatal de Meteorología, Gobierno de España, El Tiempo. 2013. http://www.aemet.es/es/serviciosclimaticos/cambio_climat/result_graficos?opc4=0&opc6=0 (accessed June 20, 2022)
  48. Cabre O., Grandadam M., Lou Marié J., Gravier P., Prangé A., Santinelli Y., Rous V., Bourry O., Durand J.P., Tolou H., Davoust B.. West Nile Virus in horses, sub-Saharan Africa.. Emerg. Infect. Dis. 2006;12:1958–1960.
    doi: 10.3201/EID1212.060042pmc: PMC3291339pubmed: 17326952google scholar: lookup
  49. Clé M., Beck C., Salinas S., Lecollinet S., Gutierrez S., Van de Perre P., Baldet T., Foulongne V., Simonin Y.. Usutu virus: A new threat?. Epidemiol. Infect. 2019;147:1–11.
    doi: 10.1017/S0950268819001213pmc: PMC6625183pubmed: 31364580google scholar: lookup
  50. Salinas S., Constant O., Desmetz C., Barthelemy J., Lemaitre J.M., Milhavet O., Nagot N., Foulongne V., Perrin F.E., Saiz J.C., Lecollinet S., Van de Perre P., Simonin Y.. Deleterious effect of Usutu virus on human neural cells.. PLoS Negl. Trop. Dis. 2017;11.

Citations

This article has been cited 0 times.