Serological evidence of co-circulation of West Nile and Usutu viruses in equids from western Spain.
Abstract: West Nile virus (WNV) is a mosquito-borne emerging virus in Europe with capacity to cause neurological complications such as encephalitis or meningoencephalitis in humans, birds or equids. In Spain, WNV is actively circulating in mosquitoes, birds and horses in different regions, but never has been deeply studied in Extremadura. Therefore, the aim of this study was to evaluate the seroprevalence of WNV in equids of those areas and to analyse the risk factors associated with exposure to the virus. A total of 199 out of 725 equids presented antibodies against WNV by competition ELISA (27.45%), while 22 were doubtful (3.03%). Anti-WNV IgM antibodies were detected in 16 equids (2.21%), and 3 animals were doubtful (0.41%). All ELISA-reactive positive/doubtful sera (N = 226) were further tested by micro-virus neutralization test (VNT), and a total of 143 horses were confirmed as positive for WNV, obtaining a seroprevalence of 19.72% in equids of western Spain. In addition, specific antibodies against USUV were confirmed in 11 equids. In 24 equids, a specific flavivirus species (detected by ELISA test) could not be determined. The generalized linear mixed-effects models showed that the significant risk factors associated with individual WNV infection in equids were the age (adults) and hair coat colour (light), whereas in USUV infections, it was the breed (pure). Data demonstrated that WNV and USUV are circulating in regions of western Spain. Given the high WNV seroprevalence found in equids from the studied areas, it is important to improve the surveillance programmes of public health to detect undiagnosed human cases and to establish a vaccination programme in equid herds in these regions.
© 2020 Wiley-VCH GmbH.
Publication Date: 2020-09-05 PubMed ID: 32853452DOI: 10.1111/tbed.13810Google Scholar: Lookup
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Summary
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This study reveals the prevalence of West Nile and Usutu viruses in horses in western Spain and identifies the associated risk factors. The research suggests the need for improved public health surveillance and a potential vaccination program for equids in the area.
Objective and Methodology
- This study set out to determine the prevalence (seroprevalence) of West Nile virus (WNV) in equids (horses, donkeys, and mules) in western Spain’s Extremadura region, where the virus hadn’t been deeply studied. The researchers also sought to identify the risk factors linked to exposure to the virus.
- The researchers conducted a competition Enzyme-Linked Immunosorbent Assay (ELISA) which is a common laboratory technique used to measure the concentration of antibodies in the blood. This was used on 725 equids, 199 of which were found to have antibodies against the WNV.
- The ELISA-reactive positive/doubtful sera (a component of blood separated during coagulation) were further tested by a micro-virus neutralization test (VNT), which confirmed 143 horses were positive for WNV.
Findings
- The study found that 27.45% of the tested equids carried antibodies against WNV, and a total of 19.72% were confirmed as WNV positive via a secondary test. This suggests a significant presence of the virus in the equid population of western Spain.
- An additional virus, the Usutu virus (USUV), was also found in 11 equids, suggesting both these viruses are actively circulating in the area.
- The study also identified risk factors linked to these viral infections. It showed the significant risk factors associated with individual WNV infection in equids were the age (adults) and hair coat color (light). In contrast, for USUV infections, breed (pure) was highlighted as a risk factor.
Implication
- Given the high WNV seroprevalence in equids from the area studied, the researchers recommend improving public health surveillance strategies to detect undiagnosed human cases.
- Additionally, they suggest establishing a vaccination programme for equid herds in these regions to control the spread of the virus.
Cite This Article
APA
Guerrero-Carvajal F, Bravo-Barriga D, Martín-Cuervo M, Aguilera-Sepúlveda P, Ferraguti M, Jiménez-Clavero MÁ, Llorente F, Alonso JM, Frontera E.
(2020).
Serological evidence of co-circulation of West Nile and Usutu viruses in equids from western Spain.
Transbound Emerg Dis, 68(3), 1432-1444.
https://doi.org/10.1111/tbed.13810 Publication
Researcher Affiliations
- Animal Health Department, Veterinary Faculty, University of Extremadura (UEx), Cáceres, Spain.
- Animal Health Department, Veterinary Faculty, University of Extremadura (UEx), Cáceres, Spain.
- Animal Medicine Department, Veterinary Faculty, University of Extremadura (UEx), Cáceres, Spain.
- Animal Health Research Centre, National Institute for Agricultural and Food Research and Technology (INIA-CISA), Valdeolmos, Madrid, Spain.
- Anatomy, Cellular Biology and Zoology Department, Science Faculty, University of Extremadura (UEx), Badajoz, Spain.
- Animal Health Research Centre, National Institute for Agricultural and Food Research and Technology (INIA-CISA), Valdeolmos, Madrid, Spain.
- Centro de Investigación Biomédica en Red de Epidemiologia y Salud Pública (CIBERESP), Madrid, Spain.
- Animal Health Research Centre, National Institute for Agricultural and Food Research and Technology (INIA-CISA), Valdeolmos, Madrid, Spain.
- Animal Health Department, Veterinary Faculty, University of Extremadura (UEx), Cáceres, Spain.
- Animal Health Department, Veterinary Faculty, University of Extremadura (UEx), Cáceres, Spain.
MeSH Terms
- Animals
- Coinfection / epidemiology
- Coinfection / veterinary
- Coinfection / virology
- Female
- Flavivirus / isolation & purification
- Flavivirus Infections / epidemiology
- Flavivirus Infections / veterinary
- Flavivirus Infections / virology
- Horse Diseases / epidemiology
- Horse Diseases / virology
- Horses
- Male
- Prevalence
- Risk Factors
- Seroepidemiologic Studies
- Spain / epidemiology
- West Nile Fever / epidemiology
- West Nile Fever / veterinary
- West Nile Fever / virology
- West Nile virus / isolation & purification
Grant Funding
- E-RTA2015-00002-C02-00 / Instituto Nacional de Investigaciu00f3n y Tecnologu00eda Agraria y Alimentaria
- IB16135 / Regional Ministry of Economy and Infrastructure, Extremadura Government and the European Regional Development Fund 'A way to make Europe'
References
This article includes 82 references
- Abad-Cobo A, Llorente F, Barbero M D C, Cruz-López F, Forés P, Jiménez-Clavero M Á. Serosurvey reveals exposure to West Nile virus in asymptomatic horse populations in central Spain prior to recent disease foci. Transboundary and Emerging Diseases 64(5), 1387-1392.
- Aberle S W, Kolodziejek J, Jungbauer C, Stiasny K, Aberle J H, Zoufaly A, Nowotny N. Increase in human West Nile and Usutu virus infections, Austria, 2018. Euro Surveillance 23(43), 1800545.
- Aharonson-Raz K, Lichter-Peled A, Tal S, Gelman B, Cohen D, Klement E, Steinman A. Spatial and temporal distribution of West Nile virus in horses in Israel (1997-2013)-from endemic to epidemics. PLoS One 9(11), 113149.
- Ahmadnejad F, Otarod V, Fallah M H, Lowenski S, Sedighi-moghaddam R, Zavareh A, Sabatier P. Spread of West Nile virus in Iran: A cross-sectional serosurvey in equines, 2008-2009. Epidemiology and Infection 139(10), 1587-1593.
- Allan S A, Day J F, Edman J D. Visual ecology of biting flies. Annual Review of Entomology 32(1), 297-314.
- Angenvoort J, Brault A C, Bowen R A, Groschup M H. West Nile viral infection of equids. Veterinary Microbiology 167(1-2), 168-180.
- Azmi K, Tirosh-Levy S, Manasrah M, Mizrahi R, Nasereddin A, Al-Jawabreh A, Steinman A. West Nile Virus: Seroprevalence in animals in Palestine and Israel. Vector-Borne and Zoonotic Diseases 17(8), 558-566.
- Bakonyi T, Busquets N, Nowotny N. Comparison of complete genome sequences of Usutu virus strains detected in Spain, Central Europe and Africa. Vector-Borne and Zoonotic Diseases 14(5), 324-329.
- Bakonyi T, Ivanics É, Erdélyi K, Ursu K, Ferenczi E, Weissenböck H, Nowotny N. Lineage 1 and 2 strains of encephalitic West Nile virus, Central Europe. Emerging Infectious Diseases 12(4), 618-623.
- Bakonyi T, Jungbauer C, Aberle S W, Kolodziejek J, Dimmel K, Stiasny K, Nowotny N. Usutu virus infections among blood donors, Austria, July and August 2017 - Raising awareness for diagnostic challenges. Euro Surveillance 22(41), 17-00644.
- Barbić L, Listeš E, Katić S, Stevanović V, Madić J, Starešina V, Savini G. Spreading of West Nile virus infection in Croatia. Veterinary Microbiology 159(3-4), 504-508.
- Barbic L, Vilibic-Cavlek T, Listes E, Stevanovic V, Gjenero-Margan I, Ljubin-Sternak S, Savini G. Demonstration of Usutu Virus antibodies in horses. Croatia. Vector Borne and Zoonotic Diseases 13(10), 772-774.
- Barros S C, Ramos F, Fagulha T, Duarte M, Henriques M, Luís T, Fevereiro M. Serological evidence of West Nile virus circulation in Portugal. Veterinary Microbiology 152(3-4), 407-410.
- Bażanów B, Jansen van Vuren P, Szymański P, Stygar D, Frącka A, Twardoń J, Pawęska J. A survey on West Nile and Usutu viruses in horses and birds in Poland. Viruses 10(2), 87.
- Beck C, Jimenez-Clavero M, Leblond A, Durand B, Nowotny N, Leparc-Goffart I, Lecollinet S. Flaviviruses in Europe: Complex circulation patterns and their consequences for the diagnosis and control of West Nile disease. International Journal of Environmental Research and Public Health 10(11), 6049-6083.
- Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A. Mosquitoes and their control (2nd ed.). .
- Ben Hassine T, De Massis F, Calistri P, Savini G, BelHaj Mohamed B, Ranen A, Hammami S. First detection of co-circulation of West Nile and Usutu viruses in equids in the south-west of Tunisia. Transboundary and Emerging Diseases 61(5), 385-389.
- Benjelloun A, El Harrak M, Calistri P, Loutfi C, Kabbaj H, Conte A, Belkadi B. Seroprevalence of West Nile virus in horses in different Moroccan regions. Veterinary Medicine and Science 3(4), 198-207.
- Bigham A W, Buckingham K J, Husain S, Emond M J, Bofferding K M, Gildersleeve H, Bamshad M. Host genetic risk factors for West Nile virus infection and disease progression. PLoS One 6(9), e24745.
- Browne S M, Bennett G F. Response of mosquitoes to visual stimuli. Journal of Medical Entomology 18(6), 505-521.
- Bunning M L, Bowen R A, Cropp B C, Sullivan K G, Davis B S, Komar N, Mitchell C J. Experimental infection of horses with West Nile virus. Emerging Infectious Diseases 8(4), 380-386.
- Busquets N, Alba A, Allepuz A, Aranda C, Núñez J I. Usutu virus sequences in Culex pipiens (Diptera: Culicidae), Spain. Emerging Infectious Diseases 14(5), 861-863.
- Busquets N, Laranjo-González M, Soler M, Nicolás O, Rivas R, Talavera S, Napp S. Detection of West Nile virus lineage 2 in North-Eastern Spain (Catalonia). Transboundary and Emerging Diseases 66(2), 617-621.
- Cahill M E, Conley S, DeWan A T, Montgomery R R. Identification of genetic variants associated with dengue or West Nile virus disease: A systematic review and meta-analysis. BMC Infectious Diseases 18(1), 282.
- 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. Journal of General Virology 70(1), 37-43.
- Cardinale E, Bernard C, Lecollinet S, Rakotoharinome V M, Ravaomanana J, Roger M, Cêtre-Sossah C. West Nile virus infection in horses, Indian Ocean. Comparative Immunology, Microbiology and Infectious Diseases 53, 45-49.
- 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. Transboundary and Emerging Diseases 58(3), 206-212.
- Christova I, Papa A, Trifonova I, Panayotova E, Pappa S, Mikov O. West Nile virus lineage 2 in humans and mosquitoes in Bulgaria, 2018-2019. Journal of Clinical Virology 127, 104365.
- Clé M, Beck C, Salinas S, Lecollinet S, Gutierrez S, Van de Perre P, Simonin Y. Usutu virus: A new threat?. Epidemiology and Infection 147, e232.
- Csank T, Drzewnioková P, Korytár L, Major P, Gyuranecz M, Pistl J, Bakonyi T. A serosurvey of flavivirus infection in horses and birds in Slovakia. Vector-Borne and Zoonotic Diseases 18(4), 206-213.
- Del Amo J, Sotelo E, Fernández-Pinero J, Gallardo C, Llorente F, Agüero M, Jiménez-Clavero M A. A novel quantitative multiplex real-time RT-PCR for the simultaneous detection and differentiation of West Nile virus lineages 1 and 2, and of Usutu virus. Journal of Virological Methods 189(2), 321-327.
- Durand B, Chevalier V, Pouillot R, Labie J, Marendat I, Murgue B, Zientara S. West Nile virus outbreak in horses, Southern France, 2000: Results of a serosurvey. Emerging Infectious Diseases 8(8), 777-782.
- Engel D, Jöst H, Wink M, Börstler J, Bosch S, Garigliany M-M, Schmidt-Chanasit J. Reconstruction of the evolutionary history and dispersal of Usutu virus, a neglected emerging arbovirus in Europe and Africa. MBio 7(1), e01938-e2015.
- Epp T, Waldner C, West K, Townsend H. Factors associated with West Nile virus disease fatalities in horses. Canadian Veterinary Journal 48(11), 1137-1145.
- European Centre for Disease Prevention and Control (ECDC). West Nile virus infection. In ECDC. Annual epidemiological report for 2018. Stockholm, Sweden.
- Ferraguti M, De la Puente J M, Soriguer R, Llorente F, Jiménez-Clavero M A, Figuerola J. West Nile virus-neutralizing antibodies in wild birds from southern Spain. Epidemiology and Infection 144(9), 1907-1911.
- 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. Emerging Infectious Diseases 13(12), 1915-1917.
- Gangoso L, Aragonés D, Martínez-de la Puente J, Lucientes J, Delacour-Estrella S, Estrada Peña R, Figuerola J. Determinants of the current and future distribution of the West Nile virus mosquito vector Culex pipiens in Spain. Environmental Research 188, 109837.
- García-Bocanegra I, Belkhiria J, Napp S, Cano-Terriza D, Jiménez-Ruiz S, Martínez-López B. Epidemiology and spatio-temporal analysis of West Nile virus in horses in Spain between 2010 and 2016. Transboundary and Emerging Diseases 65(2), 567-577.
- García-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 and Zoonotic Diseases 11(8), 1107-1113.
- García-Bocanegra I, Jaén-Téllez J A, Napp S, Arenas-Montes A, Fernández-Morente M, Fernández-Molera V, Arenas A. Monitoring of the West Nile virus epidemic in Spain between 2010 and 2011. Transboundary and Emerging Diseases 59(5), 448-455.
- García-Bocanegra I, Paniagua J, Gutiérrez-Guzmán A V, Lecollinet S, Boadella M, Arenas-Montes A, Höfle U. Spatio-temporal trends and risk factors affecting West Nile virus and related flavivirus exposure in spanish wild ruminants. BMC Veterinary Research 12(1), 249.
- Hawkes F, Gibson G. Seeing is believing: The nocturnal malarial mosquito Anopheles coluzzii responds to visual host-cues when odour indicates a host is nearby. Parasites and Vectors 9(1), 320.
- Hernández-Triana L M, Jeffries C L, Mansfield K L, Carnell G, Fooks A R, Johnson N. Emergence of West Nile virus lineage 2 in Europe: A review on the introduction and spread of a mosquito-borne disease. Frontiers in Public Health 2, 271.
- Heus P, Kolodziejek J, Camp J V, Dimmel K, Bagó Z, Hubálek Z, Nowotny N. Emergence of West Nile virus lineage 2 in Europe: Characteristics of the first seven cases of West Nile neuroinvasive disease in horses in Austria. Transboundary and Emerging Diseases 67(3), 1189-1197.
- Höfle U, Gamino V, de Mera I G F, Mangold A J, Ortíz J-A, de la Fuente J. Usutu virus in migratory song thrushes, Spain. Emerging Infectious Diseases 19(7), 1173-1175.
- Jiménez-Clavero M A, Llorente F, Sotelo E, Soriguer R, Gómez-Tejedor C, Figuerola J. West Nile virus serosurveillance in horses in Doñana, Spain, 2005 to 2008. Veterinary Record 167(10), 379-380.
- Jiménez-Clavero M A, Tejedor C G, Rojo G, Soriguer R, Figuerola J. Serosurvey of West Nile virus in equids and bovids in Spain. Veterinary Record 161(6), 212.
- Jurado-Tarifa E, Napp S, Lecollinet S, Arenas A, Beck C, Cerdà-Cuéllar M, García-Bocanegra I. Monitoring of West Nile virus, Usutu virus and Meaban virus in waterfowl used as decoys and wild raptors in southern Spain. Comparative Immunology, Microbiology and Infectious Diseases 49, 58-64.
- Kaptoul D, Viladrich P F, 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. Scandinavian Journal of Infectious Diseases 39(1), 70-71.
- Lafri I, Prat C M, Bitam I, Gravier P, Besbaci M, Zeroual F, Leparc-Goffart I. Seroprevalence of West Nile virus antibodies in equids in the North-East of Algeria and detection of virus circulation in 2014. Comparative Immunology, Microbiology and Infectious Diseases 50, 8-12.
- Lehane M J. Biology blood sucking insects. (2nd ed.). In Entomology. Cambridge, UK: Cambridge University Press.
- 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. Transboundary and Emerging Diseases 66(5), 2100-2106.
- Llorente F, Pérez-Ramírez E, Fernández-Pinero J, Soriguer R C, Figuerola J, Jiménez-Clavero M Á. Flaviviruses in game birds. Emerging Infectios Diseases 19(6), 1023-1025.
- Martinet J P, Ferté H, Failloux A B, Schaffner F, Depaquit J. Mosquitoes of north-western Europe as potential vectors of arboviruses: A review. Viruses 11(11), 1059.
- Mashimo T, Lucas M, Simon-Chazottes D, Frenkiel M-P, Montagutelli X, Ceccaldi P-E, Despres P. A nonsense mutation in the gene encoding 2′-5′-oligoadenylate synthetase/L1 isoform is associated with West Nile virus susceptibility in laboratory mice. Proceedings of the National Academy of Sciences of the United States of America 99(17), 11311-11316.
- Ministerio de Agricultura, P. y A.. El sector equino en cifras. Principales indicadores económicos. Ministerio de Agricultura, Pesca y Alimentación.
- Mixão V, Bravo Barriga D, Parreira R, Novo M T, Sousa C A, Frontera E, Almeida A P G. Comparative morphological and molecular analysis confirms the presence of the West Nile virus mosquito vector, Culex univittatus, in the Iberian Peninsula. Parasites and Vectors 9(1), 601.
- Moreno J, Tenorio A, Figuerola J, Sánchez-Seco M P, Ruiz S, Vázquez A, Herrero L. West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009. American Journal of Tropical Medicine and Hygiene 85(1), 178-181.
- Ng T, Hathaway D, Jennings N, Champ D, Chiang Y W, Chu H J. Equine vaccine for West Nile virus. Journal of Developmental Biology 114, 221-227.
- Ostlund E N, Crom R L, Pedersen D D, Johnson D J, Williams W O, Schmitt B J. Equine West Nile encephalitis, United States. Emerging Infectious Diseases 7(4), 665-669.
- Pérez-Ramírez E, Llorente F, del Amo J, Fall G, Sall A A, Lubisi A, Jiménez-Clavero M Á. Pathogenicity evaluation of twelve West Nile virus strains belonging to four lineages from five continents in a mouse model: Discrimination between three pathogenicity categories. Journal of General Virology 98(4), 662-670.
- Petersen L R, Brault A C, Nasci R S. West Nile virus: Review of the literature. Journal of the American Medical Association 310(3), 308-315.
- Ravagnan S, Montarsi F, Cazzin S, Porcellato E, Russo F, Palei M, Capelli G. First report outside Eastern Europe of West Nile virus lineage 2 related to the Volgograd 2007 strain, northeastern Italy, 2014. Parasites and Vectors 8(1), 418.
- Rios J J, Fleming J A G W, Bryant U K, Carter C N, Huber J C, Long M T, Adelson D L. OAS1 polymorphisms are associated with susceptibility to West Nile encephalitis in horses. PLoS One 5(5), e10537.
- Rios L M V, Sheu J-J, Day J F, Maruniak J E, Seino K, Zaretsky H, Long M T. Environmental risk factors associated with West Nile virus clinical disease in Florida horses. Medical and Veterinary Entomology 23(4), 357-366.
- Rizzoli A, Jiménez-Clavero M, Barzon L, Cordioli P, Figuerola J, Koraka P, Tenorio A. The challenge of West Nile virus in Europe: Knowledge gaps and research priorities. Euro Surveillance 20(20), 21135.
- Rodríguez G. Models for over-dispersed count data Generalized Linear Models. Princeton University.
- 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 16(4), 734-742.
- Sánchez-Gómez A, Amela C, Fernández-Carrión E, Martínez-Avilés M, Sánchez-Vizcaíno J M, Sierra-Moros M J. Risk mapping of West Nile virus circulation in Spain, 2015. Acta Tropica 169, 163-169.
- Savini G, Capelli G, Monaco F, Polci A, Russo F, Di Gennaro A, Lelli R. Evidence of West Nile virus lineage 2 circulation in Northern Italy. Veterinary Microbiology 158(3-4), 267-273.
- Savini G, Monaco F, Terregino C, Di Gennaro A, Bano L, Pinoni C, Lelli R. Usutu virus in Italy: An emergence or a silent infection?. Veterinary Microbiology 151(3-4), 264-274.
- Sotelo E, Fernández-Pinero J, Jiménez-Clavero M Á. La fiebre/encefalitis por virus West Nile: Reemergencia en Europa y situación en España. Enfermedades Infecciosas Y Microbiologia Clinica 30(2), 75-83.
- Stejskalova K, Cvanova M, Oppelt J, Janova E, Horecky C, Horecka E, Horin P. Genetic susceptibility to West Nile virus infection in Camargue horses. Research in Veterinary Science 124, 284-292.
- Tber A A. West Nile fever in horses in Morocco. Bulletin De L'office International Des Epizooties 11, 867-869.
- Vanhomwegen J, Beck C, Desprès P, Figuerola A, García R, Lecollinet S, Serra-Cobo J. Circulation of zoonotic arboviruses in equine populations of Mallorca Island (Spain). Vector-Borne and Zoonotic Diseases 17(5), 340-346.
- Vázquez A, Sánchez-Seco M P, Ruiz S, Molero F, Hernández L, Moreno J, Tenorio A. Putative new lineage of West Nile virus, Spain. Emerging Infectious Diseases 16(3), 549-552.
- Vilibic-Cavlek T, Savic V, Petrovic T, Toplak I, Barbic L, Petric D, Savini G. Emerging trends in the epidemiology of West Nile and Usutu Virus infections in southern Europe. Frontiers in Veterinary Science 6, 437.
- Weissenböck H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N. Emergence of Usutu virus, an African mosquito-borne Flavivirus of the Japanese encephalitis virus group, central Europe. Emerging Infectious Diseases 8(7), 652-656.
- Yan J, Gangoso L, Martínez-de la Puente J, Soriguer R, Figuerola J. Avian phenotypic traits related to feeding preferences in two Culex mosquitoes. Science of Nature 104(9-10), 76.
- Zeller H G, Schuffenecker I. West Nile virus: An overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. European Journal of Clinical Microbiology and Infectious Diseases 23(3), 147-156.
- Zuur A F, Ieno E N, Elphick C S. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1(1), 3-14.
Citations
This article has been cited 19 times.- Angeloni G, Bertola M, Lazzaro E, Morini M, Masi G, Sinigaglia A, Trevisan M, Gossner CM, Haussig JM, Bakonyi T, Capelli G, Barzon L. Epidemiology, surveillance and diagnosis of Usutu virus infection in the EU/EEA, 2012 to 2021. Euro Surveill 2023 Aug;28(33).
- Llorente F, Gutiérrez-López R, Pérez-Ramirez E, Sánchez-Seco MP, Herrero L, Jiménez-Clavero MÁ, Vázquez A. Experimental infections in red-legged partridges reveal differences in host competence between West Nile and Usutu virus strains from Southern Spain. Front Cell Infect Microbiol 2023;13:1163467.
- Gothe LMR, Ganzenberg S, Ziegler U, Obiegala A, Lohmann KL, Sieg M, Vahlenkamp TW, Groschup MH, Hörügel U, Pfeffer M. Horses as Sentinels for the Circulation of Flaviviruses in Eastern-Central Germany. Viruses 2023 Apr 30;15(5).
- Casades-Martí L, Holgado-Martín R, Aguilera-Sepúlveda P, Llorente F, Pérez-Ramírez E, Jiménez-Clavero MÁ, Ruiz-Fons F. Risk Factors for Exposure of Wild Birds to West Nile Virus in A Gradient of Wildlife-Livestock Interaction. Pathogens 2023 Jan 3;12(1).
- García-Bocanegra I, Franco JJ, León CI, Barbero-Moyano J, García-Miña MV, Fernández-Molera V, Gómez MB, Cano-Terriza D, Gonzálvez 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 Nov;69(6):3624-3636.
- Figuerola J, Jiménez-Clavero MÁ, Ruíz-López MJ, Llorente F, Ruiz S, Hoefer A, Aguilera-Sepúlveda P, Jiménez-Peñuela J, García-Ruiz O, Herrero L, Soriguer RC, Fernández Delgado R, Sánchez-Seco MP, Martínez-de la Puente J, Vázquez A. A One Health view of the West Nile virus outbreak in Andalusia (Spain) in 2020. Emerg Microbes Infect 2022 Dec;11(1):2570-2578.
- Constant O, Bollore K, Clé M, Barthelemy J, Foulongne V, Chenet B, Gomis D, Virolle L, Gutierrez S, Desmetz C, Moares RA, Beck C, Lecollinet S, Salinas S, Simonin Y. Evidence of Exposure to USUV and WNV in Zoo Animals in France. Pathogens 2020 Nov 30;9(12).
- Mas-Coma S, Artigas P, Cuervo PF, De Elías-Escribano A, Fantozzi MC, Colangeli G, Córdoba A, Marquez-Guzman DJ, Mas-Bargues C, Borrás C, Pérez-Pérez P, Bethencourt-Estrella CJ, Rodríguez-Expósito RL, Peña-Prunell MD, Chao-Pellicer J, García-Pérez O, Domínguez de Barros AT, García-Ramos A, Sirvent-Blanco C, Gajeta-Arenas M, Córdoba-Lanús AE, Piñero JE, Valero MA, Lorenzo-Morales J, Bargues MD. Infectious disease risk after the October 2024 flash flood in Valencia, Spain: Disaster evolution, strategic scenario analysis, and extrapolative baseline for a One Health assessment. One Health 2025 Dec;21:101093.
- Bravo-Barriga D, Ferraguti M, Magallanes S, Aguilera-Sepúlveda P, Llorente F, Pérez-Ramírez E, Vázquez A, Guerrero-Carvajal F, Sánchez-Seco MP, Jiménez-Clavero MÁ, 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;2023:6893677.
- Körsten C, Al-Hosary AA, Holicki CM, Schäfer M, Tews BA, Vasić A, Ziegler U, Groschup MH, Silaghi C. Simultaneous Coinfections with West Nile Virus and Usutu Virus in Culex pipiens and Aedes vexans Mosquitoes. Transbound Emerg Dis 2023;2023:6305484.
- Chevalier N, Migné CV, Mariteragi-Helle T, Dumarest M, De Mas M, Chevrier M, Queré E, Marcillaud-Pitel C, Lupo C, Bigeard C, Touzet T, Leblond A, Durand B, Depecker M, Gonzalez G. Seroprevalence of West Nile, Usutu and tick-borne encephalitis viruses in equids from south-western France in 2023. Vet Res 2025 Apr 24;56(1):91.
- 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).
- Castro-Scholten S, Caballero-Gómez J, Bravo-Barriga D, Llorente F, Cano-Terriza D, Jiménez-Clavero MÁ, Jiménez-Martín D, Camacho-Sillero L, García-Bocanegra I. Exposure to West Nile Virus in Wild Lagomorphs in Spanish Mediterranean Ecosystems. Zoonoses Public Health 2025 Mar;72(2):207-214.
- Varga Z, Bueno-Marí R, Risueño Iranzo J, Kurucz K, Tóth GE, Zana B, Zeghbib S, Görföl T, Jakab F, Kemenesi G. Accelerating targeted mosquito control efforts through mobile West Nile virus detection. Parasit Vectors 2024 Mar 18;17(1):140.
- 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 Dec;17:100578.
- Ferraguti M, Dimas Martins A, Artzy-Randrup Y. Quantifying the invasion risk of West Nile virus: Insights from a multi-vector and multi-host SEIR model. One Health 2023 Dec;17:100638.
- Macias A, Martín P, Pérez-Olmeda M, Fernández-Martínez B, Gómez-Barroso D, Fernández E, Ramos JM, Herrero L, Rodríguez S, Delgado E, Sánchez-Seco MP, Galán M, Corbacho AJ, Jimenez M, Montero-Peña C, Valle A, Vázquez A. West Nile virus emergence in humans in Extremadura, Spain 2020. Front Cell Infect Microbiol 2023;13:1155867.
- Schwarz ER, Long MT. Comparison of West Nile Virus Disease in Humans and Horses: Exploiting Similarities for Enhancing Syndromic Surveillance. Viruses 2023 May 24;15(6).
- Casades-Martí L, Cuadrado-Matías R, Peralbo-Moreno A, Baz-Flores S, Fierro Y, Ruiz-Fons F. Insights into the spatiotemporal dynamics of West Nile virus transmission in emerging scenarios. One Health 2023 Jun;16:100557.
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