1887
Surveillance Open Access
Like 0

Abstract

Background

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.

Aim

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.

Methods

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.

Results

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.

Conclusion

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.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2022.27.25.2200068
2022-06-23
2022-10-06
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.25.2200068
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/27/25/eurosurv-27-25-1.html?itemId=/content/10.2807/1560-7917.ES.2022.27.25.2200068&mimeType=html&fmt=ahah

References

  1. 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 
  2. 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 
  3. 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
  4. 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 
  5. 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 
  6. 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 
  7. 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 
  8. 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 
  9. 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 
  10. 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 
  11. 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 
  12. 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 
  13. 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 
  14. 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 
  15. 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 
  16. 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 
  17. 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
  18. 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 
  19. 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 
  20. 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 
  21. 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 
  22. 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 
  23. 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 
  24. 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 
  25. 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 
  26. 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 
  27. 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 
  28. 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 
  29. 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 
  30. 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 
  31. 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 
  32. 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 
  33. 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 
  34. 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 
  35. 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 
  36. 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 
  37. 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 
  38. 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 
  39. 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 
  40. 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 
  41. 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 
  42. 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 
  43. 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 
  44. 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 
  45. 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 
  46. 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 
  47. 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 
  48. 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 
  49. 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 
  50. 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 
/content/10.2807/1560-7917.ES.2022.27.25.2200068
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error