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Peri-domestic entomological surveillance using private traps allows detection of dengue virus in Aedes albopictus during an autochthonous transmission event in mainland France, late summer 2023
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Barbara Viginier1
, Raphaëlle Klitting2,3
, Clémence Galon4
, Violaine Bonnefoux5 , Christophe Bellet5 , Albin Fontaine3,6
, Élise Brottet7
, Marie-Claire Paty8 , Armelle Mercurol9 , Nathalie Ragozin9 , Sara Moutailler4
, Gilda Grard2,3
, Xavier de Lamballerie2,3 , Frédérick Arnaud1
, Maxime Ratinier1
, Vincent Raquin1
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View Affiliations Hide AffiliationsAffiliations: 1 EPHE, Université PSL, INRAE, Universite Claude Bernard Lyon1, IVPC UMR754, F-69007, Lyon, France 2 National Reference Center for Arboviruses, Inserm-IRBA, Marseille, France 3 Unité des Virus Émergents (UVE: Aix-Marseille Univ, Università di Corsica, IRD 190, Inserm 1207, IRBA), Marseille, France 4 Anses, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, France 5 Entente Interdépartementale Rhône-Alpes pour la démoustication (French public mosquito control organisation), Chindrieux, France 6 Institut de Recherches Biomédicales des Armées (IRBA), Unité de virologie, Marseille, France 7 Santé publique France (French National Public Health Agency), Lyon, France 8 Santé publique France (French National Public Health Agency), Saint-Maurice, France 9 Agence Régionale de Santé Auvergne-Rhône-Alpes (French Regional Health Agency), Lyon FranceVincent Raquinvincent.raquin ephe.psl.eu
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View Citation Hide Citation
Citation style for this article: Viginier Barbara, Klitting Raphaëlle, Galon Clémence, Bonnefoux Violaine, Bellet Christophe, Fontaine Albin, Brottet Élise, Paty Marie-Claire, Mercurol Armelle, Ragozin Nathalie, Moutailler Sara, Grard Gilda, de Lamballerie Xavier, Arnaud Frédérick, Ratinier Maxime, Raquin Vincent. Peri-domestic entomological surveillance using private traps allows detection of dengue virus in Aedes albopictus during an autochthonous transmission event in mainland France, late summer 2023. Euro Surveill. 2024;29(36):pii=2400195. https://doi.org/10.2807/1560-7917.ES.2024.29.36.2400195 Received: 28 Mar 2024; Accepted: 02 Jul 2024
Abstract
While locally-acquired dengue virus (DENV) human infections occur in mainland France since 2010, data to identify the mosquito species involved and to trace the virus are frequently lacking. Supported by a local network gathering public health agencies and research laboratories, we analysed, in late summer 2023, mosquitoes from privately-owned traps within a French urban neighbourhood affected by a dengue cluster. The cluster, in Auvergne-Rhône-Alpes, comprised three cases, including two autochthonous ones. Upon return from a recent visit to the French Caribbean Islands, the third case had consulted healthcare because of dengue-compatible symptoms, but dengue had not been recognised. For the two autochthonous cases, DENV-specific antibodies in serum or a positive quantitative PCR for DENV confirmed DENV infection. The third case had anti-flavivirus IgMs. No DENV genetic sequences were obtained from affected individuals but Aedes albopictus mosquitoes trapped less than 200 m from the autochthonous cases’ residence contained DENV. Genetic data from the mosquito-derived DENV linked the cluster to the 2023–2024 dengue outbreak in the French Caribbean Islands. This study highlights the importance of raising mosquito-borne disease awareness among healthcare professionals. It demonstrates Ae. albopictus as a DENV vector in mainland France and the value of private mosquito traps for entomo−virological surveillance.
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References
-
Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013;496(7446):504-7. https://doi.org/10.1038/nature12060 PMID: 23563266
-
World Health Organization (WHO). Disease Outbreak News. Dengue - Global situation. Geneva: WHO. [Accessed 13 Mar 2024]. Available from: https://www.who.int/emergencies/disease-outbreak-news/item/2023-DON498
-
European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious diseases. Stockholm: ECDC. [Accessed 29 Aug 2024]. Available from: https://atlas.ecdc.europa.eu/public/index.aspx
-
European Centre for Disease Prevention and Control (ECDC). Worsening spread of mosquito-borne disease outbreaks in EU/EEA, according to latest ECDC figures. Stockholm: ECDC; 2024. Available from: https://www.ecdc.europa.eu/en/news-events/worsening-spread-mosquito-borne-disease-outbreaks-eueea-according-latest-ecdc-figures
-
De Santis O, Bouscaren N, Flahault A. Asymptomatic dengue infection rate: A systematic literature review. Heliyon. 2023;9(9):e20069. https://doi.org/10.1016/j.heliyon.2023.e20069 PMID: 37809992
-
La Ruche G, Souarès Y, Armengaud A, Peloux-Petiot F, Delaunay P, Desprès P, et al. First two autochthonous dengue virus infections in metropolitan France, September 2010. Euro Surveill. 2010;15(39):19676. https://doi.org/10.2807/ese.15.39.19676-en PMID: 20929659
-
Gjenero-Margan I, Aleraj B, Krajcar D, Lesnikar V, Klobučar A, Pem-Novosel I, et al. Autochthonous dengue fever in Croatia, August-September 2010. Euro Surveill. 2011;16(9):19805. https://doi.org/10.2807/ese.16.09.19805-en PMID: 21392489
-
European Centre for Diseases Prevention and Control (ECDC). Autochthonous transmission of dengue virus in Europe. Stockholm: ECDC. [Accessed 13 Mar 2024]. Available from: https://www.ecdc.europa.eu/en/all-topics-z/dengue/surveillance-and-disease-data/autochthonous-transmission-dengue-virus-eueea
-
Franke F, Giron S, Cochet A, Jeannin C, Leparc-Goffart I, de Valk H, et al. Autochthonous chikungunya and dengue fever outbreak in Mainland France, 2010-2018. Eur J Public Health. 2019;29(Supplement_4) Supplement_4;ckz186.628. https://doi.org/10.1093/eurpub/ckz186.628
-
Fournet N, Voiry N, Rozenberg J, Bassi C, Cassonnet C, Karch A, et al. , investigation team. A cluster of autochthonous dengue transmission in the Paris region - detection, epidemiology and control measures, France, October 2023. Euro Surveill. 2023;28(49):2300641. https://doi.org/10.2807/1560-7917.ES.2023.28.49.2300641 PMID: 38062947
-
Agence Régionale de Santé Auvergne-Rhône-Alpes. Surveillance épidémiologique régionale. [Accessed 13 Mar 2024]. Available from: https://www.santepubliquefrance.fr/regions/auvergne-rhone-alpes/documents/bulletin-regional/2020/bilan-de-la-surveillance-epidemiologique-des-arboviroses-en-2019-en-region-auvergne-rhone-alpes
-
Ministère du travail, de la santé et des solidarités. Cartes de présence du moustique tigre (Aedes albopictus) en France métropolitaine. Available from: https://sante.gouv.fr/sante-et-environnement/risques-microbiologiques-physiques-et-chimiques/especes-nuisibles-et-parasites/article/cartes-de-presence-du-moustique-tigre-aedes-albopictus-en-france-metropolitaine.
-
Delatte H, Desvars A, Bouétard A, Bord S, Gimonneau G, Vourc’h G, et al. Blood-feeding behavior of Aedes albopictus, a vector of Chikungunya on La Réunion. Vector Borne Zoonotic Dis. 2010;10(3):249-58. https://doi.org/10.1089/vbz.2009.0026 PMID: 19589060
-
Vega-Rua A, Zouache K, Caro V, Diancourt L, Delaunay P, Grandadam M, et al. High efficiency of temperate Aedes albopictus to transmit chikungunya and dengue viruses in the Southeast of France. PLoS One. 2013;8(3):e59716. https://doi.org/10.1371/journal.pone.0059716 PMID: 23527259
-
Yoon IK, Getis A, Aldstadt J, Rothman AL, Tannitisupawong D, Koenraadt CJM, et al. Fine scale spatiotemporal clustering of dengue virus transmission in children and Aedes aegypti in rural Thai villages. PLoS Negl Trop Dis. 2012;6(7):e1730. https://doi.org/10.1371/journal.pntd.0001730 PMID: 22816001
-
Aranda C, Martínez MJ, Montalvo T, Eritja R, Navero-Castillejos J, Herreros E, et al. Arbovirus surveillance: first dengue virus detection in local Aedes albopictus mosquitoes in Europe, Catalonia, Spain, 2015. Euro Surveill. 2018;23(47):1700837. https://doi.org/10.2807/1560-7917.ES.2018.23.47.1700837 PMID: 30482266
-
De Carli G, Carletti F, Spaziante M, Gruber CEM, Rueca M, Spezia PG, et al. , Lazio Dengue Outbreak Group, Lazio dengue Outbreak Group. Outbreaks of autochthonous Dengue in Lazio region, Italy, August to September 2023: preliminary investigation. Euro Surveill. 2023;28(44):2300552. https://doi.org/10.2807/1560-7917.ES.2023.28.44.2300552 PMID: 37917030
-
Marini F, Caputo B, Pombi M, Tarsitani G, della Torre A. Study of Aedes albopictus dispersal in Rome, Italy, using sticky traps in mark-release-recapture experiments. Med Vet Entomol. 2010;24(4):361-8. https://doi.org/10.1111/j.1365-2915.2010.00898.x PMID: 20666995
-
Luciani L, Combe P, Touret F, Gazin C, Klitting R, Pezzi L, et al. Broad-spectrum dengue virus detection using the commercial RealStar dengue RT-PCR kit 3.0 (Altona) and an in-house combined real-time RT-PCR assay. Heliyon. 2024;10(10):e31252. https://doi.org/10.1016/j.heliyon.2024.e31252 PMID: 38803933
-
Moutailler S, Yousfi L, Mousson L, Devillers E, Vazeille M, Vega-Rúa A, et al. A New High-Throughput Tool to Screen Mosquito-Borne Viruses in Zika Virus Endemic/Epidemic Areas. Viruses. 2019;11(10):904. https://doi.org/10.3390/v11100904 PMID: 31569736
-
Klitting R, Piorkowski G, Rousset D, Cabié A, Frumence E, Lagrave A, et al. , arbovirus genomics diagnostic laboratories working group, Arbovirus genomics diagnostic laboratories working group members. Molecular epidemiology identifies the expansion of the DENV2 epidemic lineage from the French Caribbean Islands to French Guiana and mainland France, 2023 to 2024. Euro Surveill. 2024;29(13):2400123. https://doi.org/10.2807/1560-7917.ES.2024.29.13.2400123 PMID: 38551097
-
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol Biol Evol. 2020;37(5):1530-4. https://doi.org/10.1093/molbev/msaa015 PMID: 32011700
-
Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30(5):1188-95. https://doi.org/10.1093/molbev/mst024 PMID: 23418397
-
Cochet A, Calba C, Jourdain F, Grard G, Durand GA, Guinard A, et al. , Investigation team. Autochthonous dengue in mainland France, 2022: geographical extension and incidence increase. Euro Surveill. 2022;27(44):2200818. https://doi.org/10.2807/1560-7917.ES.2022.27.44.2200818 PMID: 36330819
-
Schaffner A, Geoffroy H. The Mosquitoes of Europe. An identification and training programme. IRD Editions & EID Méditerranée; 2001. [Accessed 14 Mar 2024]. Available from: https://mivegec.fr/fr/identiciels
-
Nguyet MN, Duong TH, Trung VT, Nguyen TH, Tran CN, Long VT, et al. Host and viral features of human dengue cases shape the population of infected and infectious Aedes aegypti mosquitoes. Proc Natl Acad Sci USA. 2013;110(22):9072-7. https://doi.org/10.1073/pnas.1303395110 PMID: 23674683
-
Yang D, He Y, Ni W, Lai Q, Yang Y, Xie J, et al. Semi-field life-table studies of Aedes albopictus (Diptera: Culicidae) in Guangzhou, China. PLoS One. 2020;15(3):e0229829. https://doi.org/10.1371/journal.pone.0229829 PMID: 32187227
-
Lambrechts L, Scott TW. Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. Proc Biol Sci. 2009;276(1660):1369-78. https://doi.org/10.1098/rspb.2008.1709 PMID: 19141420
-
Bellone R, Lequime S, Jupille H, Göertz GP, Aubry F, Mousson L, et al. Experimental adaptation of dengue virus 1 to Aedes albopictus mosquitoes by in vivo selection. Sci Rep. 2020;10(1):18404. https://doi.org/10.1038/s41598-020-75042-4 PMID: 33110109
-
Fortuna C, Severini F, Marsili G, Toma L, Amendola A, Venturi G, et al. Assessing the Risk of Dengue Virus Local Transmission: Study on Vector Competence of Italian Aedes albopictus. Viruses. 2024;16(2):176. https://doi.org/10.3390/v16020176 PMID: 38399952
-
Brustolin M, Santamaria C, Napp S, Verdún M, Rivas R, Pujol N, et al. Experimental study of the susceptibility of a European Aedes albopictus strain to dengue virus under a simulated Mediterranean temperature regime. Med Vet Entomol. 2018;32(4):393-8. https://doi.org/10.1111/mve.12325 PMID: 30051490
-
Viglietta M, Bellone R, Blisnick AA, Failloux AB. Vector Specificity of Arbovirus Transmission. Front Microbiol. 2021;12:773211. https://doi.org/10.3389/fmicb.2021.773211 PMID: 34956136
-
Lequime S, Dehecq JS, Matheus S, de Laval F, Almeras L, Briolant S, et al. Modeling intra-mosquito dynamics of Zika virus and its dose-dependence confirms the low epidemic potential of Aedes albopictus. PLoS Pathog. 2020;16(12):e1009068. https://doi.org/10.1371/journal.ppat.1009068 PMID: 33382858
-
Viginier B, Cappuccio L, Garnier C, Martin E, Maisse C, Valiente Moro C, et al. Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential. Peer Community J. 2023;3:e96. https://doi.org/10.24072/pcjournal.326
-
Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8(4):e1002588. https://doi.org/10.1371/journal.ppat.1002588 PMID: 22496640
-
Gossner CM, Fournet N, Frank C, Fernández-Martínez B, Del Manso M, Gomes Dias J, et al. Dengue virus infections among European travellers, 2015 to 2019. Euro Surveill. 2022;27(2):2001937. https://doi.org/10.2807/1560-7917.ES.2022.27.2.2001937 PMID: 35027102
-
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
-
L’Ambert G, Gendrot M, Briolant S, Nguyen A, Pages S, Bosio L, et al. Analysis of trapped mosquito excreta as a noninvasive method to reveal biodiversity and arbovirus circulation. Mol Ecol Resour. 2023;23(2):410-23. https://doi.org/10.1111/1755-0998.13716 PMID: 36161270
-
Kai I, Kobayashi D, Itokawa K, Sanjoba C, Itoyama K, Isawa H. Evaluation of long-term preservation methods for viral RNA in mosquitoes at room temperature. J Virol Methods. 2024;325:114887. https://doi.org/10.1016/j.jviromet.2024.114887 PMID: 38237867
-
Fontaine A, Mignotte A, Lacour G, Nguyen A, Gomez N, Chanaud L, et al. Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in Southern France. bioRxiv. 2023;2023.08.05.552101. doi: https://doi.org/10.1101/2023.08.05.552101
-
Baldacchino F, Caputo B, Chandre F, Drago A, della Torre A, Montarsi F, et al. Control methods against invasive Aedes mosquitoes in Europe: a review. Pest Manag Sci. 2015;71(11):1471-85. https://doi.org/10.1002/ps.4044 PMID: 26037532
-
Pernat N, Kampen H, Jeschke JM, Werner D. Citizen science versus professional data collection: Comparison of approaches to mosquito monitoring in Germany. J Appl Ecol. 2021;58(2):214-23. https://doi.org/10.1111/1365-2664.13767
-
Kampen H, Medlock JM, Vaux AG, Koenraadt CJ, van Vliet AJ, Bartumeus F, et al. Approaches to passive mosquito surveillance in the EU. Parasit Vectors. 2015;8(1):9. https://doi.org/10.1186/s13071-014-0604-5 PMID: 25567671
-
Simonin Y. Circulation of West Nile Virus and Usutu Virus in Europe: Overview and Challenges. Viruses. 2024;16(4):599. https://doi.org/10.3390/v16040599 PMID: 38675940
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Supplementary data
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Supplementary Table 1
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