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Abstract

Background

Lyme borreliosis (LB) is the most widespread hard tick-borne zoonosis in the northern hemisphere. Existing studies in Europe have focused mainly on acarological risk assessment, with few investigations exploring human LB occurrence.

Aim

We explored the determinants of spatial and seasonal LB variations in France from 2016 to 2021 by integrating environmental, animal, meteorological and anthropogenic factors, and then mapped seasonal LB risk predictions.

Methods

We fitted 2016–19 LB national surveillance data to a two-part spatio-temporal statistical model. Spatial and temporal random effects were specified using a Besag-York-Mollie model and a seasonal model, respectively. Coefficients were estimated in a Bayesian framework using integrated nested Laplace approximation. Data from 2020–21 were used for model validation.

Results

A high vegetation index (≥ 0.6) was positively associated with seasonal LB presence, while the index of deer presence (> 60%), mild soil temperature (15–22 °C), moderate air saturation deficit (1.5–5 mmHg) and higher tick bite frequency were associated with increased incidence. Prediction maps show a higher risk of LB in spring and summer (April–September), with higher incidence in parts of eastern, midwestern and south-western France.

Conclusion

We present a national level spatial assessment of seasonal LB occurrence in Europe, disentangling factors associated with the presence and increased incidence of LB. Our findings yield quantitative evidence for national public health agencies to plan targeted prevention campaigns to reduce LB burden, enhance surveillance and identify further data needs. This approach can be tested in other LB endemic areas.

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This work is licensed under a Creative Commons Attribution 4.0 International License.
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/content/10.2807/1560-7917.ES.2023.28.14.2200581
2023-04-06
2024-12-21
/content/10.2807/1560-7917.ES.2023.28.14.2200581
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References

  1. Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012;379(9814):461-73.  https://doi.org/10.1016/S0140-6736(11)60103-7  PMID: 21903253 
  2. Sykes RA, Makiello P. An estimate of Lyme borreliosis incidence in Western Europe. J Public Health (Oxf). 2017;39(1):74-81. https://doi.org/10.1093/pubmed/fdw017  PMID: 26966194 
  3. Steinbrink A, Brugger K, Margos G, Kraiczy P, Klimpel S. The evolving story of Borrelia burgdorferi sensu lato transmission in Europe. Parasitol Res. 2022;121(3):781-803.  https://doi.org/10.1007/s00436-022-07445-3  PMID: 35122516 
  4. Gilot B, Pautou G, Moncada E, Ain G. Première contribution à l’étude écologique d’Ixodes ricinus (Linné, 1758) (Acarina, Ixodoidea) dans le Sud-Est de la France. [Ecological study of Ixodes ricinus (Linné, 1758) (Acarina, Ixodoides) in southeastern France.]. Acta Trop. 1975;32(3):232-58. PMID: 1985 
  5. Gilot B, Pautou G, Moncada E. L’analyse de la végétation appliquée á la détection des populations de tiques exophiles dans le sud-est de la France: l’exemple d’lxodes ricinus (Linné 1758) (acarina, Ixodoidea). [Vegetation analysis used for the detection of exophile tick populations in the south-east of France: the example Ixodes ricinus (Linne 1758) (acarina, ixodoidea)]. Acta Trop. 1975;32(4):340-7. PMID: 7119 
  6. Ceballos LA, Pintore MD, Tomassone L, Pautasso A, Bisanzio D, Mignone W, et al. Habitat and occurrence of ixodid ticks in the Liguria region, northwest Italy. Exp Appl Acarol. 2014;64(1):121-35.  https://doi.org/10.1007/s10493-014-9794-y  PMID: 24682615 
  7. Qviller L, Grøva L, Viljugrein H, Klingen I, Mysterud A. Temporal pattern of questing tick Ixodes ricinus density at differing elevations in the coastal region of western Norway. Parasit Vectors. 2014;7(1):179.  https://doi.org/10.1186/1756-3305-7-179  PMID: 24725997 
  8. Burri C, Moran Cadenas F, Douet V, Moret J, Gern L. Ixodes ricinus density and infection prevalence of Borrelia burgdorferi sensu lato along a North-facing altitudinal gradient in the Rhône Valley (Switzerland). Vector Borne Zoonotic Dis. 2007;7(1):50-8.  https://doi.org/10.1089/vbz.2006.0569  PMID: 17417957 
  9. Gethmann J, Hoffmann B, Kasbohm E, Süss J, Habedank B, Conraths FJ, et al. Research paper on abiotic factors and their influence on Ixodes ricinus activity-observations over a two-year period at several tick collection sites in Germany. Parasitol Res. 2020;119(5):1455-66.  https://doi.org/10.1007/s00436-020-06666-8  PMID: 32219549 
  10. Tagliapietra V, Rosà R, Arnoldi D, Cagnacci F, Capelli G, Montarsi F, et al. Saturation deficit and deer density affect questing activity and local abundance of Ixodes ricinus (Acari, Ixodidae) in Italy. Vet Parasitol. 2011;183(1-2):114-24.  https://doi.org/10.1016/j.vetpar.2011.07.022  PMID: 21820245 
  11. Rosà R, Andreo V, Tagliapietra V, Baráková I, Arnoldi D, Hauffe HC, et al. Effect of climate and land use on the spatio-temporal variability of tick-borne bacteria in Europe. Int J Environ Res Public Health. 2018;15(4):732.  https://doi.org/10.3390/ijerph15040732  PMID: 29649132 
  12. Pérez D, Kneubühler Y, Rais O, Gern L. Seasonality of Ixodes ricinus ticks on vegetation and on rodents and Borrelia burgdorferi sensu lato genospecies diversity in two Lyme borreliosis-endemic areas in Switzerland. Vector Borne Zoonotic Dis. 2012;12(8):633-44.  https://doi.org/10.1089/vbz.2011.0763  PMID: 22607074 
  13. Porter WT, Motyka PJ, Wachara J, Barrand ZA, Hmood Z, McLaughlin M, et al. Citizen science informs human-tick exposure in the Northeastern United States. Int J Health Geogr. 2019;18(1):9.  https://doi.org/10.1186/s12942-019-0173-0  PMID: 31064416 
  14. Joly D, Brossard T, Cardot H, Cavailhès J, Hilal M, Joly D, et al. Les types de climats en France, une construction spatiale. [The types of climate in France, a spatial construction]. European Journal of Geography.2010;501:1-23. French. Available: https://hal.inrae.fr/hal-02660374/document
  15. Institut national de l’information géographique et forestière (IGN). L’enquête Statistique Inventaire Forestier National. Mémento 2022. [The National Forest Inventory Statistical Survey]. Saint-Mandé: IGN; 2022. French. Available from: https://inventaire-forestier.ign.fr/IMG/pdf/memento_2022.pdf
  16. Réseau Sentinelles. Bilan d’activité 2020. Veille sanitaire et recherche en soins primaires, pp. 89-90. [Activity report 2020. Health surveillance and primary care research.]. Paris: Réseau Sentinelles; 2020. French. Available from: https://www.sentiweb.fr/document/5361
  17. Ministère des Solidarités et de la santé. Plan national de lutte contre la maladie de Lyme et les maladies transmissibles par les tiques. [National plan for the control of Lyme disease and tick-borne diseases]. Paris: Ministère des Solidarités et de la santé; 2016. French. Available from: https://solidarites-sante.gouv.fr/IMG/pdf/plan_lyme_180117.pdf
  18. Septfons A, Goronflot T, Jaulhac B, Roussel V, De Martino S, Guerreiro S, et al. Epidemiology of Lyme borreliosis through two surveillance systems: the national Sentinelles GP network and the national hospital discharge database, France, 2005 to 2016. Euro Surveill. 2019;24(11):1800134.  https://doi.org/10.2807/1560-7917.ES.2019.24.11.1800134  PMID: 30892181 
  19. Réseau Sentinelles. Estimation des incidences à partir des données de médecine de ville du réseau Sentinelles. [Incidence estimate based on GP data in the Sentinelles network]. Paris: Réseau Sentinelles; 2010. French. Available from: http://www.sentiweb.fr/1384.pdf
  20. Souty C, Turbelin C, Blanchon T, Hanslik T, Le Strat Y, Boëlle PY. Improving disease incidence estimates in primary care surveillance systems. Popul Health Metr. 2014;12(1):19.  https://doi.org/10.1186/s12963-014-0019-8  PMID: 25435814 
  21. Stanek G, Fingerle V, Hunfeld KP, Jaulhac B, Kaiser R, Krause A, et al. Lyme borreliosis: clinical case definitions for diagnosis and management in Europe. Clin Microbiol Infect. 2011;17(1):69-79.  https://doi.org/10.1111/j.1469-0691.2010.03175.x  PMID: 20132258 
  22. Kleijnen JPC. Kriging: Methods and Applications. CentER Discussion paper series. Tilburg: Center for Economic Research; 2017.  https://doi.org/10.2139/ssrn.3075151 
  23. Rue H, Martino S, Chopin N. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J R Stat Soc Series B Stat Methodol. 2009;71(2):319-92.  https://doi.org/10.1111/j.1467-9868.2008.00700.x 
  24. Martins TG, Simpson D, Lindgren F, Rue H. Bayesian computing with INLA: New features. Comput Stat Data Anal. 2013;67:68-83.  https://doi.org/10.1016/j.csda.2013.04.014 
  25. Watanabe S. Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. J Mach Learn Res. 2010;11:3571-94.
  26. Dawid P. Statistical theory: the prequential approach. J R Stat Soc [Ser A]. 1984;147(2):278-92.  https://doi.org/10.2307/2981683 
  27. Réseau Sentinelles. Maladie de Lyme. [Lyme disease]. Paris: Réseau Sentinelles. [Accessed: 01 Jan 2023]. French. Available from: https://www.sentiweb.fr/france/fr/?page=maladies&mal=18
  28. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2022. Available from: https://www.R-project.org
  29. Office fédéral de la santé publique. Maladies transmises par les tiques – Situation en Suisse. [Tick-borne diseases - Situation in Switzerland]. Berne: Office fédéral de la santé publique. [Accessed: 30 Dec 2022]. French. Available from: https://www.bag.admin.ch/bag/fr/home/krankheiten/ausbrueche-epidemien-pandemien/aktuelle-ausbrueche-epidemien/zeckenuebertragene-krankheiten.html
  30. Leroy M, Dupont Y, Tersago K. Epistat, surveillance of human tick bites. Brussels: Sciensano. [Accessed: 28 Nov 2022]. Available from: https://epistat.wiv-isp.be/ticks
  31. Ministère des solidarités et de la santé. Décrets, arrêtés, circulaires: textes généraux. [Decrees, orders, circulars: general texts]. Paris: Journal officiel de la république française. [Accessed: 16 Mar 2023]. French. Available from: https://www.legifrance.gouv.fr/download/pdf?id=YTXQyL3I14RgMkscchJ4EWWUgvYvfJ3GciREwkWtl3E=
  32. Di Domenico L, Sabbatini CE, Boëlle PY, Poletto C, Crépey P, Paireau J, et al. Adherence and sustainability of interventions informing optimal control against the COVID-19 pandemic. Commun Med (Lond). 2021;1(57).
  33. Fu W, Bonnet C, Figoni J, Septfons A, Métras R. Exploratory space-time analyses of reported Lyme borreliosis cases in France, 2016-2019. Pathogens. 2021;10(4):444.  https://doi.org/10.3390/pathogens10040444  PMID: 33917723 
  34. Rosà R, Pugliese A. Effects of tick population dynamics and host densities on the persistence of tick-borne infections. Math Biosci. 2007;208(1):216-40.  https://doi.org/10.1016/j.mbs.2006.10.002  PMID: 17125804 
  35. Mysterud A, Easterday WR, Stigum VM, Aas AB, Meisingset EL, Viljugrein H. Contrasting emergence of Lyme disease across ecosystems. Nat Commun. 2016;7(1):11882.  https://doi.org/10.1038/ncomms11882  PMID: 27306947 
  36. Pacilly FCA, Benning ME, Jacobs F, Leidekker J, Sprong H, Van Wieren SE, et al. Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus. Ticks Tick Borne Dis. 2014;5(6):810-7.  https://doi.org/10.1016/j.ttbdis.2014.06.004  PMID: 25113977 
  37. Gandy S, Kilbride E, Biek R, Millins C, Gilbert L. Experimental evidence for opposing effects of high deer density on tick-borne pathogen prevalence and hazard. Parasit Vectors. 2021;14(1):509.  https://doi.org/10.1186/s13071-021-05000-0  PMID: 34593023 
  38. Septfons A, Figoni J, Gautier A, Soullier N, de Valk H, Desenclos JC. Increased awareness and knowledge of Lyme Borreliosis and tick bite prevention among the general population in France: 2016 and 2019 health barometer survey. BMC Public Health. 2021;21(1):1808.  https://doi.org/10.1186/s12889-021-11850-1  PMID: 34620144 
  39. Bregnard C, Rais O, Voordouw MJ. Climate and tree seed production predict the abundance of the European Lyme disease vector over a 15-year period. Parasit Vectors. 2020;13(1):408.  https://doi.org/10.1186/s13071-020-04291-z  PMID: 32778177 
  40. Muñoz Sabater J. ERA5-Land hourly data from 1950 to present. Copernicus Climate Change Service (C3S) Climate Data Store (CDS). 2019. [Accessed: 1 Dec 2022]. Available from: https://cds.climate.copernicus.eu https://doi.org/10.24381/cds.e2161bac 
  41. Hersbach H, Bell B, Berrisford P, Biavati G, Horányi A, Muñoz Sabater J, et al. ERA5 hourly data on pressure levels from 1940 to present. Copernicus Climate Change Service (C3S) Climate Data Store (CDS).  https://doi.org/10.24381/cds.bd0915c6 . [Accessed: 1 March 2023]. Available from: https://cds.climate.copernicus.eu/cdsapp#!/dataset/10.24381/cds.bd0915c6?tab=overview https://doi.org/10.24381/cds.bd0915c6 
  42. Copernicus. Copernicus Global Land NDVI (Normalized Difference Vegetation Index). Paris: European Space Agency (ESA). [Accessed: 3 Apr 2023]. Available from: https://land.copernicus.eu/global/products/ndvi
  43. Wint W, Morley D, Alexander N. Four rodent and vole biodiversity models for Europe. Open Health Data. 2013;1(1):e3.  https://doi.org/10.5334/jophd.ac 
  44. Alexander NS, Morley D, Medlock J, Searle K, Wint W. A first attempt at modelling roe deer (Capreolus capreolus) distributions over Europe. Open Health Data. 2014;2(1):e2.  https://doi.org/10.5334/ohd.ah 
  45. Wint W, Morley D, Medlock J, Alexander NS. A first attempt at modelling red deer (Cervus elaphus) distributions over Europe. Open Health Data. 2014;2(1):e1.  https://doi.org/10.5334/ohd.ag 
  46. Chan CB, Ryan DA. Assessing the effects of weather conditions on physical activity participation using objective measures. Int J Environ Res Public Health. 2009;6(10):2639-54.  https://doi.org/10.3390/ijerph6102639  PMID: 20054460 
  47. Hofhuis A, van de Kassteele J, Sprong H, van den Wijngaard CC, Harms MG, Fonville M, et al. Predicting the risk of Lyme borreliosis after a tick bite, using a structural equation model. PLoS One. 2017;12(7):e0181807.  https://doi.org/10.1371/journal.pone.0181807  PMID: 28742149 
  48. National Research Institute for Agriculture, Food and the Environment (INRAE). CiTIQUE. Un programme de recherche participative où les citoyens peuvent aider la recherche sur les tiques et les maladies qu’elles transmettent. [CiTIQUE. A participatory research program where citizens can help research on ticks and the diseases they transmit]. Nancy: Programme CiTIQUE. [Accessed: 3 Jan 2023]. French. Available from: https://www.citique.fr
Spatial and seasonal determinants of Lyme borreliosis incidence in France, 2016 to 2021
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Wen+Fu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fu Wen</a>, <a href="/search?value1=Camille+Bonnet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bonnet Camille</a>, <a href="/search?value1=Alexandra+Septfons&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Septfons Alexandra</a>, <a href="/search?value1=Julie+Figoni&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Figoni Julie</a>, <a href="/search?value1=Jonas+Durand&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Durand Jonas</a>, <a href="/search?value1=Pascale+Frey-Klett&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Frey-Klett Pascale</a>, <a href="/search?value1=Denis+Rustand&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rustand Denis</a>, <a href="/search?value1=Beno%C3%AEt+Jaulhac&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jaulhac Benoît</a>, <a href="/search?value1=Rapha%C3%ABlle+M%C3%A9tras&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Métras Raphaëlle</a></span>. Spatial and seasonal determinants of Lyme borreliosis incidence in France, 2016 to 2021. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(14):pii=2200581. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.14.2200581" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.14.2200581</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 15 Jul 2022;&nbsp;&nbsp; <span class="generated">Accepted</span>: 12 Jan 2023 </span> </p>
/content/10.2807/1560-7917.ES.2023.28.14.2200581
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