-
One Health surveillance of West Nile and Usutu viruses: a repeated cross-sectional study exploring seroprevalence and endemicity in Southern France, 2016 to 2020
- Orianne Constant1,* , Patricia Gil2,* , Jonathan Barthelemy1 , Karine Bolloré1 , Vincent Foulongne1 , Caroline Desmetz3 , Agnès Leblond4 , Isabelle Desjardins5 , Sophie Pradier6 , Aurélien Joulié7 , Alain Sandoz8 , Rayane Amaral9 , Michel Boisseau2 , Ignace Rakotoarivony2 , Thierry Baldet2 , Albane Marie10 , Benoît Frances10 , Florence Reboul Salze11 , Bachirou Tinto1 , Philippe Van de Perre1 , Sara Salinas1 , Cécile Beck9 , Sylvie Lecollinet9,12 , Serafin Gutierrez2,** , Yannick Simonin1,2,**
-
View Affiliations Hide AffiliationsAffiliations: 1 Pathogenesis and Control of Chronic and Emerging Infections, Montpellier University, INSERM, EFS (etablissement français du sang), Montpellier, France 2 ASTRE research unit, CIRAD, INRAe, Montpellier University, Montpellier, France 3 BioCommunication en CardioMétabolique (BC2M), Montpellier University, Montpellier, France 4 EPIA, UMR 0346, Epidemiologie des maladies animales et zoonotiques, INRAE, VetAgro Sup, Marcy l’Etoile, France 5 University of Lyon, VetAgro Sup, GREMERES-ICE Lyon Equine Research Center, Marcy l’Etoile, France 6 Jolimont veterinary clinics, Toulouse, France 7 National veterinary school of Toulouse, Université de Toulouse, Toulouse, France 8 Aix Marseille Université – CNRS, UMR 7376, Laboratoire Chimie de l’Environnement, Marseille, France 9 UMR 1161 Virology, ANSES, INRAE, ENVA, ANSES Animal Health Laboratory, EURL for equine diseases, Maisons-Alfort, France 10 EID Méditérranée, Montpellier, France 11 Veterinary Clinic des étangs, Perols, France 12 CIRAD, UMR ASTRE, CRVC, Petit Bourg, France* These authors contributed equally to this manuscript and share first authorship.** These authors contributed equally to this manuscript and share last authorship.Correspondence:Yannick Simoninyannick.simonin umontpellier.frand Serafin Gutierrezserafin.gutierrez cirad.fr
-
View Citation Hide Citation
Citation style for this article: Constant Orianne, Gil Patricia, Barthelemy Jonathan, Bolloré Karine, Foulongne Vincent, Desmetz Caroline, Leblond Agnès, Desjardins Isabelle, Pradier Sophie, Joulié Aurélien, Sandoz Alain, Amaral Rayane, Boisseau Michel, Rakotoarivony Ignace, Baldet Thierry, Marie Albane, Frances Benoît, Reboul Salze Florence, Tinto Bachirou, Van de Perre Philippe, Salinas Sara, Beck Cécile, Lecollinet Sylvie, Gutierrez Serafin, Simonin Yannick. One Health surveillance of West Nile and Usutu viruses: a repeated cross-sectional study exploring seroprevalence and endemicity in Southern France, 2016 to 2020. Euro Surveill. 2022;27(25):pii=2200068. https://doi.org/10.2807/1560-7917.ES.2022.27.25.2200068 Received: 19 Jan 2022; Accepted: 22 Apr 2022
- Previous Article
- Table of Contents
- Next Article
Abstract
West Nile virus (WNV) and Usutu virus (USUV), two closely related flaviviruses, mainly follow an enzootic cycle involving mosquitoes and birds, but also infect humans and other mammals. Since 2010, their epidemiological situation may have shifted from irregular epidemics to endemicity in several European regions; this requires confirmation, as it could have implications for risk assessment and surveillance strategies.
To explore the seroprevalence in animals and humans and potential endemicity of WNV and USUV in Southern France, given a long history of WNV outbreaks and the only severe human USUV case in France in this region.
We evaluated the prevalence of WNV and USUV in a repeated cross-sectional study by serological and molecular analyses of human, dog, horse, bird and mosquito samples in the Camargue area, including the city of Montpellier, between 2016 and 2020.
We observed the active transmission of both viruses and higher USUV prevalence in humans, dogs, birds and mosquitoes, while WNV prevalence was higher in horses. In 500 human samples, 15 were positive for USUV and 6 for WNV. Genetic data showed that the same lineages, WNV lineage 1a and USUV lineage Africa 3, were found in mosquitoes in 2015, 2018 and 2020.
These findings support existing literature suggesting endemisation in the study region and contribute to a better understanding of USUV and WNV circulation in Southern France. Our study underlines the importance of a One Health approach for the surveillance of these viruses.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Article metrics loading...
Full text loading...
References
-
Calisher CH, Gould EA. Taxonomy of the virus family Flaviviridae. Adv Virus Res. 2003;59:1-19. https://doi.org/10.1016/S0065-3527(03)59001-7 PMID: 14696325
-
Zannoli S, Sambri V. West Nile virus and Usutu virus co-circulation in Europe: Epidemiology and implications. Microorganisms. 2019;7(7):E184. https://doi.org/10.3390/microorganisms7070184 PMID: 31248051
-
European Centre for Disease Prevention and Control (ECDC). Expert consultation on risk assessment and outbreak mapping tools for West Nile virus infection in Europe. Stockholm: ECDC; 29 May 2012. Available from: https://www.ecdc.europa.eu/en/publications-data/expert-consultation-risk-assessment-and-outbreak-mapping-tools-west-nile-virus
-
Kramer LD, Li J, Shi PY. West Nile virus. Lancet Neurol. 2007;6(2):171-81. https://doi.org/10.1016/S1474-4422(07)70030-3 PMID: 17239804
-
Clé M, Beck C, Salinas S, Lecollinet S, Gutierrez S, Van de Perre P, et al. Usutu virus: A new threat? Epidemiol Infect. 2019;147:e232. https://doi.org/10.1017/S0950268819001213 PMID: 31364580
-
Weissenböck H, Kolodziejek J, Fragner K, Kuhn R, Pfeffer M, Nowotny N. Usutu virus activity in Austria, 2001-2002. Microbes Infect. 2003;5(12):1132-6. https://doi.org/10.1016/S1286-4579(03)00204-1 PMID: 14554255
-
Seino KK, Long MT, Gibbs EPJ, Bowen RA, Beachboard SE, Humphrey PP, et al. Comparative efficacies of three commercially available vaccines against West Nile Virus (WNV) in a short-duration challenge trial involving an equine WNV encephalitis model. Clin Vaccine Immunol. 2007;14(11):1465-71. https://doi.org/10.1128/CVI.00249-07 PMID: 17687109
-
Zeller H, Marrama L, Sudre B, Van Bortel W, Warns-Petit E. Mosquito-borne disease surveillance by the European Centre for Disease Prevention and Control. Clin Microbiol Infect. 2013;19(8):693-8. https://doi.org/10.1111/1469-0691.12230 PMID: 23607415
-
Constant O, Bollore K, Clé M, Barthelemy J, Foulongne V, Chenet B, et al. Evidence of exposure to USUV and WNV in zoo animals in France. Pathogens. 2020;9(12):100-5. https://doi.org/10.3390/pathogens9121005 PMID: 33266071
-
Beck C, Leparc Goffart I, Franke F, Gonzalez G, Dumarest M, Lowenski S, et al. Contrasted epidemiological patterns of West Nile virus lineages 1 and 2 infections in France from 2015 to 2019. Pathogens. 2020;9(11):908. https://doi.org/10.3390/pathogens9110908 PMID: 33143300
-
García San Miguel Rodríguez-Alarcón L, Fernández-Martínez B, Sierra Moros MJ, Vázquez A, Julián Pachés P, García Villacieros E, et al. Unprecedented increase of West Nile virus neuroinvasive disease, Spain, summer 2020. Euro Surveill. 2021;26(19). https://doi.org/10.2807/1560-7917.ES.2021.26.19.2002010 PMID: 33988123
-
Pervanidou D, Vakali A, Georgakopoulou T, Panagiotopoulos T, Patsoula E, Koliopoulos G, et al. West Nile virus in humans, Greece, 2018: the largest seasonal number of cases, 9 years after its emergence in the country. Euro Surveill. 2020;25(32). https://doi.org/10.2807/1560-7917.ES.2020.25.32.1900543 PMID: 32794446
-
Carletti F, Colavita F, Rovida F, Percivalle E, Baldanti F, Ricci I, et al. Expanding Usutu virus circulation in Italy: detection in the Lazio region, central Italy, 2017 to 2018. Euro Surveill. 2019;24(3). https://doi.org/10.2807/1560-7917.ES.2019.24.3.1800649 PMID: 30670139
-
Nagy A, Mezei E, Nagy O, Bakonyi T, Csonka N, Kaposi M, et al. Extraordinary increase in West Nile virus cases and first confirmed human Usutu virus infection in Hungary, 2018. Euro Surveill. 2019;24(28). https://doi.org/10.2807/1560-7917.ES.2019.24.28.1900038 PMID: 31311619
-
Čabanová V, Šikutová S, Straková P, Šebesta O, Vichová B, Zubríková D, et al. Co-Circulation of West Nile and Usutu Flaviviruses in Mosquitoes in Slovakia, 2018. Viruses. 2019;11(7):639. https://doi.org/10.3390/v11070639 PMID: 31336825
-
Martin MF, Simonin Y. Progression historique du virus du Nil occidental en Europe. [West Nile virus historical progression in Europe]. Virologie (Montrouge). 2019;23(5):265-70. French. https://doi.org/10.1684/vir.2019.0787 PMID: 31826847
-
European Centre for Disease Prevention and Control (ECDC). West Nile fever in Europe in 2018 - human cases compared to previous seasons, updated 23 November. Stockholm: ECDC; 2019. Available from: https://ecdc.europa.eu/en/publications-data/west-nile-fever-europe-2018-human-cases-compared-previous-seasons-updated-23
-
Michel F, Sieg M, Fischer D, Keller M, Eiden M, Reuschel M, et al. Evidence for West Nile virus and Usutu Virus infections in wild and resident birds in Germany, 2017 and 2018. Viruses. 2019;11(7):674. https://doi.org/10.3390/v11070674 PMID: 31340516
-
Veo C, Della Ventura C, Moreno A, Rovida F, Percivalle E, Canziani S, et al. Evolutionary Dynamics of the Lineage 2 West Nile Virus That Caused the Largest European Epidemic: Italy 2011-2018. Viruses. 2019;11(9):814. https://doi.org/10.3390/v11090814 PMID: 31484295
-
Chaintoutis SC, Papa A, Pervanidou D, Dovas CI. Evolutionary dynamics of lineage 2 West Nile virus in Europe, 2004-2018: Phylogeny, selection pressure and phylogeography. Mol Phylogenet Evol. 2019;141:106617. https://doi.org/10.1016/j.ympev.2019.106617 PMID: 31521822
-
Srihi H, Chatti N, Ben Mhadheb M, Gharbi J, Abid N. Phylodynamic and phylogeographic analysis of the complete genome of the West Nile virus lineage 2 (WNV-2) in the Mediterranean basin. BMC Ecol Evol. 2021;21(1):183. https://doi.org/10.1186/s12862-021-01902-w PMID: 34579648
-
Johnson N, Fernández de Marco M, Giovannini A, Ippoliti C, Danzetta ML, Svartz G, et al. Emerging mosquito-borne threats and the response from European and Eastern Mediterranean countries. Int J Environ Res Public Health. 2018;15(12):2775. https://doi.org/10.3390/ijerph15122775 PMID: 30544521
-
Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF. Present and future Köppen-Geiger climate classification maps at 1-km resolution. Sci Data. 2018;5(1):180214. https://doi.org/10.1038/sdata.2018.214 PMID: 30375988
-
Pradier S, Sandoz A, Paul MC, Lefebvre G, Tran A, Maingault J, et al. Importance of wetlands management for West Nile Virus circulation risk, Camargue, Southern France. Int J Environ Res Public Health. 2014;11(8):7740-54. https://doi.org/10.3390/ijerph110807740 PMID: 25093652
-
Desjardins I, Joulié A, Pradier S, Lecollinet S, Beck C, Vial L, et al. Seroprevalence of horses to Coxiella burnetii in an Q fever endemic area. Vet Microbiol. 2018;215:49-56. PMID: 29426406
-
Eiden M, Gil P, Ziegler U, Rakotoarivony I, Marie A, Frances B, et al. Emergence of two Usutu virus lineages in Culex pipiens mosquitoes in the Camargue, France, 2015. Infect Genet Evol. 2018;61:151-4. https://doi.org/10.1016/j.meegid.2018.03.020 PMID: 29592838
-
Chevalier V, Marsot M, Molia S, Rasamoelina H, Rakotondravao R, Pedrono M, et al. Serological evidence of west nile and usutu viruses circulation in domestic and wild birds in wetlands of mali and madagascar in 2008. Int J Environ Res Public Health. 2020;17(6):1998. https://doi.org/10.3390/ijerph17061998 PMID: 32197367
-
Beck C, Desprès P, Paulous S, Vanhomwegen J, Lowenski S, Nowotny N, et al. A High-Performance Multiplex Immunoassay for Serodiagnosis of Flavivirus-Associated Neurological Diseases in Horses. Biomed Res Int. 2015;2015:678084. https://doi.org/10.1155/2015/678084 PMID: 26457301
-
Nikolay B, Weidmann M, Dupressoir A, Faye O, Boye CS, Diallo M, et al. Development of a Usutu virus specific real-time reverse transcription PCR assay based on sequenced strains from Africa and Europe. J Virol Methods. 2014;197:51-4. https://doi.org/10.1016/j.jviromet.2013.08.039 PMID: 24036076
-
Garcia M, Alout H, Diop F, Damour A, Bengue M, Weill M, et al. Innate Immune response of primary human keratinocytes to West Nile Virus infection and its modulation by mosquito saliva. Front Cell Infect Microbiol. 2018;8:387. https://doi.org/10.3389/fcimb.2018.00387 PMID: 30450338
-
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;8(7):652-6. https://doi.org/10.3201/eid0807.020094 PMID: 12095429
-
Bahuon C, Marcillaud-Pitel C, Bournez L, Leblond A, Beck C, Hars J, et al. West Nile virus epizootics in the Camargue (France) in 2015 and reinforcement of surveillance and control networks. Rev Sci Tech. 2016;35(3):811-24. https://doi.org/10.20506/rst.35.3.2571 PMID: 28332648
-
Vittecoq M, Lecollinet S, Jourdain E, Thomas F, Blanchon T, Arnal A, et al. Recent circulation of West Nile virus and potentially other closely related flaviviruses in Southern France. Vector Borne Zoonotic Dis. 2013;13(8):610-3. https://doi.org/10.1089/vbz.2012.1166 PMID: 23930977
-
Durand B, Chevalier V, Pouillot R, Labie J, Marendat I, Murgue B, et al. West Nile virus outbreak in horses, southern France, 2000: results of a serosurvey. Emerg Infect Dis. 2002;8(8):777-82. https://doi.org/10.3201/eid0808.010486 PMID: 12141961
-
Pradier S, Sandoz A, Paul MC, Lefebvre G, Tran A, Maingault J, et al. Importance of wetlands management for West Nile Virus circulation risk, Camargue, Southern France. Int J Environ Res Public Health. 2014;11(8):7740-54. https://doi.org/10.3390/ijerph110807740 PMID: 25093652
-
Bahuon C, Marcillaud-Pitel C, Bournez L, Leblond A, Beck C, Hars J, et al. West Nile virus epizootics in the Camargue (France) in 2015 and reinforcement of surveillance and control networks. Rev Sci Tech. 2016;35(3):811-24. https://doi.org/10.20506/rst.35.3.2571 PMID: 28332648
-
Young JJ, Coulombier D, Domanović D, Zeller H, Gossner CM, European Union West Nile Fever Working Group. One Health approach for West Nile virus surveillance in the European Union: relevance of equine data for blood safety. Euro Surveill. 2019;24(16):1. https://doi.org/10.2807/1560-7917.ES.2019.24.16.1800349 PMID: 31014416
-
Calistri P, Giovannini A, Hubalek Z, Ionescu A, Monaco F, Savini G, et al. Epidemiology of west nile in europe and in the mediterranean basin. Open Virol J. 2010;4(1):29-37. https://doi.org/10.2174/1874357901004010029 PMID: 20517490
-
Simonin Y, Sillam O, Carles MJ, Gutierrez S, Gil P, Constant O, et al. Human Usutu virus infection with atypical neurologic presentation, Montpellier, France, 2016. Emerg Infect Dis. 2018;24(5):875-8. https://doi.org/10.3201/eid2405.171122 PMID: 29664365
-
Durand B, Haskouri H, Lowenski S, Vachiery N, Beck C, Lecollinet S. Seroprevalence of West Nile and Usutu viruses in military working horses and dogs, Morocco, 2012: dog as an alternative WNV sentinel species? Epidemiol Infect. 2016;144(9):1857-64. https://doi.org/10.1017/S095026881600011X PMID: 26838515
-
L’Ambert G, Gendrot M, Briolant S, Nguyen A, Pages S, Bosio L, et al. Mosquito excreta reveals circulation of West Nile virus and its underlying ecosystem. bioRxiv2021, 2021.12.05.471258, doi:. https://doi.org/10.1101/2021.12.05.471258
-
Lustig Y, Sofer D, Bucris ED, Mendelson E. Surveillance and diagnosis of west nile virus in the face of flavivirus cross-reactivity. Front Microbiol. 2018;9:2421. https://doi.org/10.3389/fmicb.2018.02421 PMID: 30369916
-
Percivalle E, Cassaniti I, Sarasini A, Rovida F, Adzasehoun KMG, Colombini I, et al. West nile or usutu virus? A three-year follow-up of humoral and cellular response in a group of asymptomatic blood donors. Viruses. 2020;12(2):157. https://doi.org/10.3390/v12020157 PMID: 32013152
-
Grottola A, Marcacci M, Tagliazucchi S, Gennari W, Di Gennaro A, Orsini M, et al. Usutu virus infections in humans: a retrospective analysis in the municipality of Modena, Italy. Clin Microbiol Infect. 2017;23(1):33-7. https://doi.org/10.1016/j.cmi.2016.09.019 PMID: 27677699
-
Clé M, Constant O, Barthelemy J, Desmetz C, Martin MF, Lapeyre L, et al. Differential neurovirulence of Usutu virus lineages in mice and neuronal cells. J Neuroinflammation. 2021;18(1):11. https://doi.org/10.1186/s12974-020-02060-4 PMID: 33407600
-
Angelini P, Tamba M, Finarelli AC, Bellini R, Albieri A, Bonilauri P, et al. West Nile virus circulation in Emilia-Romagna, Italy: the integrated surveillance system 2009. Euro Surveill. 2010;15(16):11-5. https://doi.org/10.2807/ese.15.16.19547-en PMID: 20430000
-
Paternoster G, Babo Martins S, Mattivi A, Cagarelli R, Angelini P, Bellini R, et al. Economics of One Health: Costs and benefits of integrated West Nile virus surveillance in Emilia-Romagna. PLoS One. 2017;12(11):e0188156. https://doi.org/10.1371/journal.pone.0188156 PMID: 29176851
-
Scaramozzino P, Carvelli A, Bruni G, Cappiello G, Censi F, Magliano A, et al. West Nile and Usutu viruses co-circulation in central Italy: outcomes of the 2018 integrated surveillance. Parasit Vectors. 2021;14(1):243. https://doi.org/10.1186/s13071-021-04736-z PMID: 33962673
-
Calzolari M, Bonilauri P, Bellini R, Albieri A, Defilippo F, Maioli G, et al. Evidence of simultaneous circulation of West Nile and Usutu viruses in mosquitoes sampled in Emilia-Romagna region (Italy) in 2009. PLoS One. 2010;5(12):e14324. https://doi.org/10.1371/journal.pone.0014324 PMID: 21179462
-
Lauriano A, Rossi A, Galletti G, Casadei G, Santi A, Rubini S, et al. West nile and usutu viruses’ surveillance in birds of the Province of Ferrara, Italy, from 2015 to 2019. Viruses. 2021;13(7):13. https://doi.org/10.3390/v13071367 PMID: 34372573
Data & Media loading...
Supplementary data
-
-
Supplement
-