Widespread Circulation of Flaviviruses in Horses and Birds in Northeastern Spain (Catalonia) between 2010 and 2019.
Abstract: The surveillance for West Nile virus (WNV) in Catalonia (northeastern Spain) has consistently detected flaviviruses not identified as WNV. With the aim of characterizing the flaviviruses circulating in Catalonia, serum samples from birds and horses collected between 2010 and 2019 and positive by panflavivirus competition ELISA (cELISA) were analyzed by microneutralization test (MNT) against different flaviviruses. A third of the samples tested were inconclusive by MNT, highlighting the limitations of current diagnostic techniques. Our results evidenced the widespread circulation of flaviviruses, in particular WNV, but also Usutu virus (USUV), and suggest that chicken and horses could serve as sentinels for both viruses. In several regions, WNV and USUV overlapped, but no significant geographical aggregation was observed. Bagaza virus (BAGV) was not detected in birds, while positivity to tick-borne encephalitis virus (TBEV) was sporadically detected in horses although no endemic foci were observed. So far, no human infections by WNV, USUV, or TBEV have been reported in Catalonia. However, these zoonotic flaviviruses need to be kept under surveillance, ideally within a One Health framework.
Publication Date: 2021-11-30 PubMed ID: 34960673PubMed Central: PMC8708358DOI: 10.3390/v13122404Google 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
- Research Support
- Non-U.S. Gov't
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 focuses on the detection and characterization of flaviviruses, particularly West Nile virus (WNV) and Usutu virus (USUV), in birds and horses in Catalonia, Spain, from 2010 to 2019. The findings highlight the limitations of current diagnostic methods, but also the value of birds and horses as sentinel species. The absence of reported human infections does not lessen the importance of continued monitoring within a One Health framework.
Flavivirus Detection and Analysis
- The study was conducted in Catalonia, a region in northeastern Spain, over a period of nearly a decade (2010 to 2019).
- The aim of the research was to characterize the range of flaviviruses found in this region, primarily through the testing of serum samples from birds and horses.
- These animals were selected because previous surveillance for the West Nile virus (WNV) had routinely identified flaviviruses other than WNV.
Diagnostic Techniques and Limitations
- The researchers used a panflavivirus competition ELISA (cELISA) as a diagnostic test, followed by a microneutralization test (MNT) against various flaviviruses.
- However, one-third of the samples produced inconclusive results in the MNT, which points to the limitations of the current diagnostic methods.
Findings and Implications
- The research provides evidence of the widespread presence of flaviviruses, particularly WNV and Usutu virus (USUV), in the region’s bird and horse populations.
- Yet, no significant geographical aggregation of these diseases was observed throughout the region, and the prevalence of Bagaza virus (BAGV) in birds and tick-borne encephalitis virus (TBEV) in horses was relatively low.
- No human infections by WNV, USUV, or TBEV were reported during the study period. However, given the zoonotic nature of these viruses, the researchers urged that monitoring should remain robust.
- The authors recommend using birds and horses as sentinel species. Sentinel species are organisms used to detect risks to humans by providing advance warning of a particular disease.
One Health Framework
- Given the interconnectedness of human and animal health, the authors recommend that surveillance efforts should ideally happen within a One Health framework.
- One Health is a collaborative, multisectoral, and transdisciplinary approach that works locally, regionally, nationally, and globally to achieve optimal health outcomes, recognizing the interconnections between people, animals, plants, and their shared environment.
Cite This Article
APA
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 MÁ, Busquets N.
(2021).
Widespread Circulation of Flaviviruses in Horses and Birds in Northeastern Spain (Catalonia) between 2010 and 2019.
Viruses, 13(12), 2404.
https://doi.org/10.3390/v13122404 Publication
Researcher Affiliations
- IRTA, Animal Health Research Centre (CReSA IRTA-UAB), 08193 Bellaterra, Spain.
- Centro de Investigación en Sanidad Animal (CISA), Instituto de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), 28130 Valdeolmos, Spain.
- UMR 1161 Virology, ANSES, INRAE, ENVA, ANSES Animal Health Laboratory, EURL for Equine Diseases, 94704 Maisons-Alfort, France.
- Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain.
- Servei Medicina Interna Equina, Fundació Hospital Clínic Veterinari (UAB), 08193 Bellaterra, Spain.
- Servei de Prevenció en Salut Animal, Departament d'Acció Climàtica, Alimentació i Agenda Rural (DACC), 08007 Barcelona, Spain.
- IRTA, Animal Health Research Centre (CReSA IRTA-UAB), 08193 Bellaterra, Spain.
- UMR 1161 Virology, ANSES, INRAE, ENVA, ANSES Animal Health Laboratory, EURL for Equine Diseases, 94704 Maisons-Alfort, France.
- Centro de Investigación en Sanidad Animal (CISA), Instituto de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), 28130 Valdeolmos, Spain.
- Centre de Fauna dels Aiguamolls de l'Empordà, Àrea de Gestió Ambiental Servei de Fauna i Flora, Forestal Catalana, 17486 Castelló d'Empúries, Spain.
- Centre de Fauna de Torreferrussa, Àrea de Gestió Ambiental Servei de Fauna i Flora, Forestal Catalana, 08130 Santa Perpètua de Mogoda, Spain.
- Centre de Fauna de Torreferrussa, Àrea de Gestió Ambiental Servei de Fauna i Flora, Forestal Catalana, 08130 Santa Perpètua de Mogoda, Spain.
- Centre de Fauna de Vallcalent, Àrea de Gestió Ambiental Servei de Fauna i Flora, Forestal Catalana, 25199 Lleida, Spain.
- Parc Natural de l'Alt Pirineu, Àrea de Gestió Ambiental Servei de Fauna i Flora, Forestal Catalana, 25595 Llavorsí, Spain.
- UMR 1161 Virology, ANSES, INRAE, ENVA, ANSES Animal Health Laboratory, EURL for Equine Diseases, 94704 Maisons-Alfort, France.
- Centro de Investigación en Sanidad Animal (CISA), Instituto de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), 28130 Valdeolmos, Spain.
- CIBER of Epidemiology and Public Health (CIBERESP), 28029 Madrid, Spain.
- IRTA, Animal Health Research Centre (CReSA IRTA-UAB), 08193 Bellaterra, Spain.
MeSH Terms
- Animals
- Antibodies, Viral / blood
- Bird Diseases / blood
- Bird Diseases / epidemiology
- Bird Diseases / virology
- Birds
- Enzyme-Linked Immunosorbent Assay / veterinary
- Flavivirus / genetics
- Flavivirus / immunology
- Flavivirus / isolation & purification
- Flavivirus / physiology
- Flavivirus Infections / blood
- Flavivirus Infections / epidemiology
- Flavivirus Infections / veterinary
- Flavivirus Infections / virology
- Horse Diseases / blood
- Horse Diseases / epidemiology
- Horse Diseases / virology
- Horses
- Seroepidemiologic Studies
- Spain / epidemiology
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 55 references
- Barzon L. Ongoing and emerging arbovirus threats in Europe.. J Clin Virol 2018 Oct;107:38-47.
- Beck C, Jimenez-Clavero MA, 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 Nov 12;10(11):6049-83.
- Weaver SC, Reisen WK. Present and future arboviral threats.. Antiviral Res 2010 Feb;85(2):328-45.
- Bakonyi T, Ivanics E, Erdélyi K, Ursu K, Ferenczi E, Weissenböck H, Nowotny N. Lineage 1 and 2 strains of encephalitic West Nile virus, central Europe.. Emerg Infect Dis 2006 Apr;12(4):618-23.
- Platonov AE, Karan' LS, Shopenskaia TA, Fedorova MV, Koliasnikova NM, Rusakova NM, Shishkina LV, Arshba TE, Zhuravlev VI, Govorukhina MV, Valentseva AA, Shipulin GA. [Genotyping of West Nile fever virus strains circulating in southern Russia as an epidemiological investigation method: principles and results].. Zh Mikrobiol Epidemiol Immunobiol 2011 Mar-Apr;(2):29-37.
- 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.
- García-Bocanegra I, Jaén-Téllez JA, Napp S, Arenas-Montes A, Fernández-Morente M, Fernández-Molera V, Arenas A. West Nile fever outbreak in horses and humans, Spain, 2010.. Emerg Infect Dis 2011 Dec;17(12):2397-9.
- Busquets N, Laranjo-González M, Soler M, Nicolás O, Rivas R, Talavera S, Villalba R, San Miguel E, Torner N, Aranda C, Napp S. Detection of West Nile virus lineage 2 in North-Eastern Spain (Catalonia).. Transbound Emerg Dis 2019 Mar;66(2):617-621.
- Camp JV, 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 Feb;18(2):145-154.
- Bakonyi T, Haussig JM. West Nile virus keeps on moving up in Europe.. Euro Surveill 2020 Nov;25(46).
- García San Miguel Rodríguez-Alarcón L, Fernández-Martínez B, Sierra Moros MJ, Vázquez A, Julián Pachés P, García Villacieros E, Gómez Martín MB, Figuerola Borras J, Lorusso N, Ramos Aceitero JM, Moro E, de Celis A, Oyonarte S, Mahillo B, Romero González LJ, Sánchez-Seco MP, Suárez Rodríguez B, Ameyugo Catalán U, Ruiz Contreras S, Pérez-Olmeda M, Simón Soria F. Unprecedented increase of West Nile virus neuroinvasive disease, Spain, summer 2020.. Euro Surveill 2021 May;26(19).
- 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.. Emerg Infect Dis 2002 Jul;8(7):652-6.
- Weissenböck H, Bakonyi T, Rossi G, Mani P, Nowotny N. Usutu virus, Italy, 1996.. Emerg Infect Dis 2013 Feb;19(2):274-7.
- Busquets N, Alba A, Allepuz A, Aranda C, Ignacio Nuñez J. Usutu virus sequences in Culex pipiens (Diptera: Culicidae), Spain.. Emerg Infect Dis 2008 May;14(5):861-3.
- Bakonyi T, Busquets N, Nowotny N. Comparison of complete genome sequences of Usutu virus strains detected in Spain, Central Europe, and Africa.. Vector Borne Zoonotic Dis 2014 May;14(5):324-9.
- Vázquez A, Ruiz S, Herrero L, Moreno J, Molero F, Magallanes A, Sánchez-Seco MP, Figuerola J, Tenorio A. West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009.. Am J Trop Med Hyg 2011 Jul;85(1):178-81.
- 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 Jan;147:e232.
- Höfle U, Gamino V, de Mera IG, Mangold AJ, Ortíz JA, de la Fuente J. Usutu virus in migratory song thrushes, Spain.. Emerg Infect Dis 2013 Jul;19(7):1173-5.
- Agüero M, Fernández-Pinero J, Buitrago D, Sánchez A, Elizalde M, San Miguel E, Villalba R, Llorente F, Jiménez-Clavero MA. Bagaza virus in partridges and pheasants, Spain, 2010.. Emerg Infect Dis 2011 Aug;17(8):1498-501.
- Llorente F, Pérez-Ramírez E, Fernández-Pinero J, Soriguer R, Figuerola J, Jiménez-Clavero MA. Flaviviruses in game birds, southern Spain, 2011-2012.. Emerg Infect Dis 2013 Jun;19(6):1023-5.
- Napp S, Montalvo T, Piñol-Baena C, Gómez-Martín MB, Nicolás-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 Aug 5;11(8).
- Estrada-Peña A, de la Fuente J. The ecology of ticks and epidemiology of tick-borne viral diseases.. Antiviral Res 2014 Aug;108:104-28.
- Beauté J, Spiteri G, Warns-Petit E, Zeller H. Tick-borne encephalitis in Europe, 2012 to 2016.. Euro Surveill 2018 Nov;23(45).
- European Centre for Disease Prevention and Control. Annual Epidemiological Report for 2017. ECDC 2021.
- Botelho-Nevers E, Gagneux-Brunon A, Velay A, Guerbois-Galla M, Grard G, Bretagne C, Mailles A, Verhoeven PO, Pozzetto B, Gonzalo S, Fafi-Kremer S, Leparc-Goffart I, Pillet S. Tick-Borne Encephalitis in Auvergne-Rhône-Alpes Region, France, 2017-2018.. Emerg Infect Dis 2019 Oct;25(10):1944-1948.
- Waldenström J, Lundkvist A, Falk KI, Garpmo U, Bergström S, Lindegren G, Sjöstedt A, Mejlon H, Fransson T, Haemig PD, Olsen B. Migrating birds and tickborne encephalitis virus.. Emerg Infect Dis 2007 Aug;13(8):1215-8.
- Beck C, Lowenski S, Durand B, Bahuon C, Zientara S, Lecollinet S. Improved reliability of serological tools for the diagnosis of West Nile fever in horses within Europe.. PLoS Negl Trop Dis 2017 Sep;11(9):e0005936.
- Nikolay B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap?. Trans R Soc Trop Med Hyg 2015 Oct;109(10):609-18.
- Santos PD, Michel F, Wylezich C, Höper D, Keller M, Holicki CM, Szentiks CA, Eiden M, Muluneh A, Neubauer-Juric A, Thalheim S, Globig A, Beer M, Groschup MH, Ziegler U. Co-infections: Simultaneous detections of West Nile virus and Usutu virus in birds from Germany.. Transbound Emerg Dis 2022 Mar;69(2):776-792.
- Alba A, Allepuz A, Napp S, Soler M, Selga I, Aranda C, Casal J, Pages N, Hayes EB, Busquets N. Ecological surveillance for West Nile in Catalonia (Spain), learning from a five-year period of follow-up.. Zoonoses Public Health 2014 May;61(3):181-91.
- Llorente F, García-Irazábal A, Pérez-Ramírez E, Cano-Gómez C, Sarasa M, Vázquez A, Jiménez-Clavero MÁ. 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 Sep;66(5):2100-2106.
- Beck C, Desprès P, Paulous S, Vanhomwegen J, Lowenski S, Nowotny N, Durand B, Garnier A, Blaise-Boisseau S, Guitton E, Yamanaka T, Zientara S, Lecollinet S. A High-Performance Multiplex Immunoassay for Serodiagnosis of Flavivirus-Associated Neurological Diseases in Horses.. Biomed Res Int 2015;2015:678084.
- Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference.. Stat Med 1995 Apr 30;14(8):799-810.
- Bravo-Barriga D, Aguilera-Sepúlveda P, Guerrero-Carvajal F, Llorente F, Reina D, Pérez-Martín JE, Jiménez-Clavero MÁ, Frontera E. West Nile and Usutu virus infections in wild birds admitted to rehabilitation centres in Extremadura, western Spain, 2017-2019.. Vet Microbiol 2021 Apr;255:109020.
- Engel D, Jöst H, Wink M, Börstler J, Bosch S, Garigliany MM, Jöst A, Czajka C, Lühken R, Ziegler U, Groschup MH, Pfeffer M, Becker N, Cadar D, Schmidt-Chanasit J. Reconstruction of the Evolutionary History and Dispersal of Usutu Virus, a Neglected Emerging Arbovirus in Europe and Africa.. mBio 2016 Feb 2;7(1):e01938-15.
- Jurado-Tarifa E, Napp S, Lecollinet S, Arenas A, Beck C, Cerdà-Cuéllar M, Fernández-Morente 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.. Comp Immunol Microbiol Infect Dis 2016 Dec;49:58-64.
- Saiz JC, Blazquez AB. Usutu virus: Current knowledge and future perspectives. Virus Adapt Treat 2017;9:27–40.
- Chvala S, Bakonyi T, Hackl R, Hess M, Nowotny N, Weissenböck H. Limited pathogenicity of Usutu virus for the domestic chicken (Gallus domesticus).. Avian Pathol 2005 Oct;34(5):392-5.
- Chaintoutis SC, Chaskopoulou A, Chassalevris T, Koehler PG, Papanastassopoulou M, Dovas CI. West Nile virus lineage 2 strain in Greece, 2012.. Emerg Infect Dis 2013 May;19(5):827-9.
- 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 Dec;16(4):734-742.
- 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 Sep 21;8(3).
- García-Bocanegra I, Arenas-Montes A, Napp S, Jaén-Téllez JA, Fernández-Morente M, Fernández-Molera V, Arenas A. Seroprevalence and risk factors associated to West Nile virus in horses from Andalusia, Southern Spain.. Vet Microbiol 2012 Dec 7;160(3-4):341-6.
- ICO. SIOC: Servidor d’informació Ornitològica de Catalunya. ICO 2021.
- Bournez L, Umhang G, Moinet M, Boucher JM, Demerson JM, Caillot C, Legras L, Devillers E, Hansmann Y, Velay A, Richomme C, Moutailler S, Boué F. Disappearance of TBEV Circulation among Rodents in a Natural Focus in Alsace, Eastern France.. Pathogens 2020 Nov 10;9(11).
- European Centre for Disease Prevention and Control. Ixodes ricinus—Current Known Distribution. European Centre for Disease Prevention and Control 2020.
- Espunyes J, Cabezón O, Pailler-García L, Dias-Alves A, Lobato-Bailón L, Marco I, Ribas MP, Encinosa-Guzmán PE, Valldeperes M, Napp S. Hotspot of Crimean-Congo Hemorrhagic Fever Virus Seropositivity in Wildlife, Northeastern Spain.. Emerg Infect Dis 2021 Sep;27(9):2480-2484.
- García-Bocanegra I, Jurado-Tarifa E, Cano-Terriza D, Martínez R, Pérez-Marín JE, Lecollinet S. Exposure to West Nile virus and tick-borne encephalitis virus in dogs in Spain.. Transbound Emerg Dis 2018 Jun;65(3):765-772.
- Vanhomwegen J, Beck C, Desprès P, Figuerola A, García R, Lecollinet S, López-Roig M, Manuguerra JC, Serra-Cobo J. Circulation of Zoonotic Arboviruses in Equine Populations of Mallorca Island (Spain).. Vector Borne Zoonotic Dis 2017 May;17(5):340-346.
- Camino E, Schmid S, Weber F, Pozo P, de Juan L, König M, Cruz-Lopez F. Detection of antibodies against tick-borne encephalitis flaviviruses in breeding and sport horses from Spain.. Ticks Tick Borne Dis 2020 Sep;11(5):101487.
- Rushton JO, Lecollinet S, Hubálek Z, Svobodová P, Lussy H, Nowotny N. Tick-borne encephalitis virus in horses, Austria, 2011.. Emerg Infect Dis 2013 Apr;19(4):635-7.
- Weingartl HM, Drebot MA, Hubálek Z, Halouzka J, Andonova M, Dibernardo A, Cottam-Birt C, Larence J, Marszal P. Comparison of assays for the detection of West Nile virus antibodies in chicken serum.. Can J Vet Res 2003 May;67(2):128-32.
- Arnal A, Gómez-Díaz E, Cerdà-Cuéllar M, Lecollinet S, Pearce-Duvet J, Busquets N, García-Bocanegra I, Pagès N, Vittecoq M, Hammouda A, Samraoui B, Garnier R, Ramos R, Selmi S, González-Solís J, Jourdain E, Boulinier T. Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the western Mediterranean basin.. PLoS One 2014;9(3):e89601.
- Balseiro A, Royo LJ, Martínez CP, Fernández de Mera IG, Höfle Ú, Polledo L, Marreros N, Casais R, Marín JF. Louping ill in goats, Spain, 2011.. Emerg Infect Dis 2012 Jun;18(6):976-8.
- Roesch F, Fajardo A, Moratorio G, Vignuzzi M. Usutu Virus: An Arbovirus on the Rise.. Viruses 2019 Jul 12;11(7).
- Fros JJ, Miesen P, Vogels CB, Gaibani P, Sambri V, Martina BE, Koenraadt CJ, van Rij RP, Vlak JM, Takken W, Pijlman GP. Comparative Usutu and West Nile virus transmission potential by local Culex pipiens mosquitoes in north-western Europe.. One Health 2015 Dec;1:31-36.
Citations
This article has been cited 0 times.Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists