Multiple factors affecting Ixodes ricinus ticks and associated pathogens in European temperate ecosystems (northeastern France).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 Apr 2024
24 Apr 2024
Historique:
received:
23
05
2023
accepted:
16
04
2024
medline:
25
4
2024
pubmed:
25
4
2024
entrez:
24
4
2024
Statut:
epublish
Résumé
In Europe, the main vector of tick-borne zoonoses is Ixodes ricinus, which has three life stages. During their development cycle, ticks take three separate blood meals from a wide variety of vertebrate hosts, during which they can acquire and transmit human pathogens such as Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis. In this study conducted in Northeastern France, we studied the importance of soil type, land use, forest stand type, and temporal dynamics on the abundance of ticks and their associated pathogens. Negative binomial regression modeling of the results indicated that limestone-based soils were more favorable to ticks than sandstone-based soils. The highest tick abundance was observed in forests, particularly among coniferous and mixed stands. We identified an effect of habitat time dynamics in forests and in wetlands: recent forests and current wetlands supported more ticks than stable forests and former wetlands, respectively. We observed a close association between tick abundance and the abundance of Cervidae, Leporidae, and birds. The tick-borne pathogens responsible for Lyme borreliosis, anaplasmosis, and hard tick relapsing fever showed specific habitat preferences and associations with specific animal families. Machine learning algorithms identified soil related variables as the best predictors of tick and pathogen abundance.
Identifiants
pubmed: 38658696
doi: 10.1038/s41598-024-59867-x
pii: 10.1038/s41598-024-59867-x
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9391Subventions
Organisme : LabEx DRIIHM Investissement d'avenir
ID : ANR-11-LABX-0010
Informations de copyright
© 2024. The Author(s).
Références
Dantas-Torres, F., Chomel, B. B. & Otranto, D. Ticks and tick-borne diseases: A One Health perspective. Trends Parasitol. 28, 437–446 (2012).
pubmed: 22902521
doi: 10.1016/j.pt.2012.07.003
Rochlin, I. & Toledo, A. Emerging tick-borne pathogens of public health importance: A mini-review. J. Med. Microb. 69, 781–791 (2020).
doi: 10.1099/jmm.0.001206
Kilpatrick, A. & Randolph, S. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380, 1946–1955 (2012).
pubmed: 23200503
pmcid: 3739480
doi: 10.1016/S0140-6736(12)61151-9
Gray, J. S., Dautel, H., Estrada-Peña, A., Kahl, O. & Lindgren, E. Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscip. Perspect. Infect. Dis. 2009, 593232 (2009).
pubmed: 19277106
pmcid: 2648658
doi: 10.1155/2009/593232
Ogden, N. H., Ben Beard, C., Ginsberg, H. S. & Tsao, J. I. Possible effects of climate change on ixodid ticks and the pathogens they transmit: Predictions and observations. J. Med. Entomol. 58, 1536–1545 (2021).
Silaghi, C., Beck, R., Oteo, J., Pfeffer, M. & Sprong, H. Neoehrlichiosis: an emerging tick-borne zoonosis caused by Candidatus Neoehrlichia mikurensis. Exp. Appl. Acarol. 68, 279–297 (2016).
pubmed: 26081117
doi: 10.1007/s10493-015-9935-y
Baneth, G. Tick-borne infections of animals and humans: A common ground. Int. J. Parasitol. 44, 591–596 (2014).
pubmed: 24846527
doi: 10.1016/j.ijpara.2014.03.011
Pfäffle, M., Littwin, N., Muders, S. V. & Petney, T. N. The ecology of tick-borne diseases. Int. J. Parasitol. 43, 1059–1077 (2013).
pubmed: 23911308
doi: 10.1016/j.ijpara.2013.06.009
Wikel, S. Ticks and tick-borne infections: Complex ecology, agents, and host interactions. Vet Sci. 5, E60 (2018).
Lindquist, L. & Vapalahti, O. Tick-borne encephalitis. Lancet 371, 1861–1871 (2008).
pubmed: 18514730
doi: 10.1016/S0140-6736(08)60800-4
Lindgren, E., Tälleklint, L. & Polfeldt, T. Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ. Health Perspect. 108, 119–123 (2000).
pubmed: 10656851
pmcid: 1637900
doi: 10.1289/ehp.00108119
Voyiatzaki, C. et al. Climate Changes Exacerbate the Spread of Ixodes ricinus and the Occurrence of Lyme Borreliosis and Tick-Borne Encephalitis in Europe-How Climate Models Are Used as a Risk Assessment Approach for Tick-Borne Diseases. https://doi.org/10.3390/ijerph19116516 (2022).
doi: 10.3390/ijerph19116516
Sprong, H. et al. Control of Lyme borreliosis and other Ixodes ricinus-borne diseases. Parasit Vectors. 11, 145 (2018).
pubmed: 29510749
pmcid: 5840726
doi: 10.1186/s13071-018-2744-5
Gern, L. & Humair, P. Ecology of Borrelia burgdorferi sensu lato in Europe. In Lyme borreliosis: biology, epidemiology and control. (ed. Gray J., Kahl O., Lane R.S., Stanek, G.) 347 (CABI publishing, 2002).
Gray, J. & Kahl, O. Tick ecology and the eco-epidemiology of Borrelia burgdorferi sensu lato. in Lyme borreliosis (ed. Editors, H. K. and G. J.) 31–45 (Springer, Switzerland., 2022).
Kahl, O. & Gray, J. S. The biology of Ixodes ricinus with emphasis on its ecology. Ticks Tick. Borne. Dis. 14, 102114 (2023).
pubmed: 36603231
doi: 10.1016/j.ttbdis.2022.102114
Boulanger, N., Boyer, P. & Talagrand-Reboul, E., & Hansmann, Y. Ticks and tick-borne diseases. Med Mal Infect. (2019).
Gassner, F., Hansford, K. & Medlock, J. Greener cities, a wild card for ticks ? in Ecology and Prevention of Lyme borreliosis. (ed. Braks MAH, Van Wieren SE, Takken W, S. H.) 187–203 (Wageningen Academic Publishers, 2016).
Rizzoli, A. et al. Ixodes ricinus and its transmitted pathogens in urban and Peri-Urban Areas in Europe: New hazards and relevance for public health. Front. Public Heal. 2, 251 (2014).
Boyer, P. H. et al. Impact of Different Anthropogenic Environments on Ticks and Tick-Associated Pathogens in Alsace, a French Region Highly Endemic for Tick-Borne Diseases. Microorganisms 10, (2022).
Medlock, J. M. et al. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit. Vectors 6, 1 (2013).
pubmed: 23281838
pmcid: 3549795
doi: 10.1186/1756-3305-6-1
Eisen, R. & Eisen, L. The Blacklegged Tick, Ixodes scapularis: An increasing public health concern. Trends Parasitol. 34, 295–309 (2018).
pubmed: 29336985
pmcid: 5879012
doi: 10.1016/j.pt.2017.12.006
Boulanger, N. et al. Surveillance du vecteur de la borréliose de Lyme, Ixodes ricinus, en Alsace de 2013 à 2016. Bull. Epidemiol. Hebd. 19–20, 400–405 (2018).
Goldstein, V. et al. Factors responsible for Ixodes ricinus nymph abundance: Are soil features indicators of tick abundance in a French region where Lyme borreliosis is endemic?. Ticks Tick. Borne. Dis. 9, 938–944 (2018).
pubmed: 29606622
doi: 10.1016/j.ttbdis.2018.03.013
Gray, J., Kahl, O. & Zintl, A. What do we still need to know about Ixodes ricinus? Ticks Tick-borne Dis. 12, (2021).
Tveten, A. K. Prevalence of Borrelia burgdorferi sensu stricto, Borrelia afzelii, Borrelia garinii, and Borrelia valaisiana in Ixodes ricinus ticks from the northwest of Norway. Scand. J. Infect. Dis. 45, 681–687. https://doi.org/10.3109/00365548.2013.799288 (2013).
doi: 10.3109/00365548.2013.799288
pubmed: 23808719
Takumi, K., Sprong, H. & Hofmeester, T. R. Impact of vertebrate communities on Ixodes ricinus-borne disease risk in forest areas. Parasites Vect. 12, 434 (2019).
doi: 10.1186/s13071-019-3700-8
Coipan, E. C. et al. Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus. Front. Cell. Infect. Microbiol. 3, 36 (2013).
pubmed: 23908971
pmcid: 3726834
doi: 10.3389/fcimb.2013.00036
Hauser, G. et al. Influence of climatic factors on Ixodes ricinus nymph abundance and phenology over a long-term monthly observation in Switzerland (2000–2014). Parasit Vectors. 11, 289 (2018).
pubmed: 29739424
pmcid: 5941567
doi: 10.1186/s13071-018-2876-7
Stanek, G., Wormser, G., Gray, J. & Strle, F. Lyme borreliosis. Lancet 379, 461–473 (2012).
pubmed: 21903253
doi: 10.1016/S0140-6736(11)60103-7
Destoumieux-Garzón, D. et al. The one health concept: 10 years old and a long road ahead. Front. Vet. Sci. 5, 14 (2018).
pubmed: 29484301
pmcid: 5816263
doi: 10.3389/fvets.2018.00014
Gilbert, L. How landscapes shape Lyme borreliosis risk. in Ecology and prevention of Lyme borreliosis (ed. Braks MAH, van Wieren SE, Takken W., S. H.) pp462 (Wageningen Academic Publishers, 2016).
Kilpatrick, A. et al. Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control. Philos. Trans. R Soc. L. B Biol. Sci. 372, 1722 (2017).
Eisen, L. Control of ixodid ticks and prevention of tick-borne diseases in the United States: The prospect of a new Lyme disease vaccine and the continuing problem with tick exposure on residential properties. Ticks Tick. Borne. Dis. 12, (2021).
Septfons, A. 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. Eurosurveillance 24, (2019).
http://invs.santepubliquefrance.fr/Dossiers-hematiques/Maladies-infectieuses/Maladies-a-transmission-vectorielle/Borreliose-de-lyme/Donnees-epidemiologiques , S. publique F. D. épidémiologiques B. de L. [Data and surveillance. L. B. P. S. publique F. [Accessed: 2 M. 2019]. F. A. from: No Title.
Morán Cadenas, F. et al. Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along a north- and south-facing altitudinal gradient on Chaumont Mountain, Switzerland. J. Med. Entomol. 44, 683–693 (2007).
Gray, J. et al. Lyme borreliosis habitat assessment. Zentralbl Bakteriol. 287, 211–228 (1998).
pubmed: 9580424
doi: 10.1016/S0934-8840(98)80123-0
Ferquel, E. et al. Prevalence of Borrelia burgdorferi Sensu Lato and Anaplasmataceae Members in Ixodes ricinus Ticks in Alsace, a Focus of Lyme Borreliosis Endemicity in France Prevalence of Borrelia burgdorferi Sensu Lato and Anaplasmataceae Members in Ixodes ricinus Tick. Appl. Environ. Microbiol. 72, 3074–3078 (2006).
pubmed: 16598024
pmcid: 1449083
doi: 10.1128/AEM.72.4.3074-3078.2006
Jensen, P. M. Host seeking activity of Ixodes ricinus ticks based on daily consecutive flagging samples. Exp. Appl. Acarol. 24, 695–708 (2000).
pubmed: 11227827
doi: 10.1023/A:1010640219816
Guerra, M. et al. Predicting the Risk of Lyme Disease: Habitat Suitability for Ixodes scapularis in the North Central United States. Emerging Infectious Diseases 8, (2002).
Morgan, J. M., Scott, T. W., Amerasinghe, F. P. & Glass, G. E. Predicting Ixodes scapularis abundance on white-tailed deer using geographic information systems. Am. J. Trop. Med. Hyg. 51, 538–544 (1994).
pubmed: 7985745
doi: 10.4269/ajtmh.1994.51.538
Swart, A. et al. Predicting tick presence by environmental risk mapping. Front. Public Heal. 2, 238 (2014).
Bourdin, A. et al. Forest diversity reduces the prevalence of pathogens transmitted by the Tick Ixodes ricinus. Front. Ecol. Evol. 10, (2022).
Ehrmann, S. et al. Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments. Parasit. Vectors 11, 23 (2018).
Hubálek, Z., Halouzka, J., Juricová, Z., Sikutová, S. & Rudolf, I. Effect of forest clearing on the abundance of Ixodes ricinus ticks and the prevalence of Borrelia burgdorferi s.l. Med. Vet. Entomol. 20, 166–172 (2006).
Sytykiewicz, H. et al. Molecular screening for Bartonella henselae and Borrelia burgdorferi sensu lato co-existence within Ixodes ricinus populations in central and eastern parts of Poland. Ann. Agric. Environ. Med. 19, 451–456 (2012).
pubmed: 23020038
Ruiz-Fons, F., Fernández-de-Mera, I. G., Acevedo, P., Gortázar, C. & de la Fuente, J. Factors driving the abundance of ixodes ricinus ticks and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Appl. Environ. Microbiol. 78, 2669–76 (2012).
Vourc’h, G. et al. Mapping human risk of infection with Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. Ticks Tick. Borne. Dis. 7, 644–652 (2016).
Lambin, E. F., Tran, A., Vanwambeke, S. O., Linard, C. & Soti, V. Pathogenic landscapes: Interactions between land, people, disease vectors, and their animal hosts. Int. J. Health Geogr. 9, 54 (2010).
pubmed: 20979609
pmcid: 2984574
doi: 10.1186/1476-072X-9-54
Tälleklint, L. & Jaenson, T. G. T. Maintenance by Hares of European Borrelia burgdorferi in ecosystems without rodents. J. Med. Entomol. 30, 273–276 (1993).
pubmed: 8433337
doi: 10.1093/jmedent/30.1.273
Kazimírová, M. et al. Diverse tick-borne microorganisms identified in free-living ungulates in Slovakia. Parasit Vectors 11, 1–18 (2018).
doi: 10.1186/s13071-018-3068-1
Kurtenbach, K., Sewell, H., Ogden, N., Randolph, S. & Nuttall, P. Serum complement sensitivity as a key factor in Lyme disease ecology. Infect. Immun. 66, 1248–1251 (1998).
pubmed: 9488421
pmcid: 108041
doi: 10.1128/IAI.66.3.1248-1251.1998
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. & Keesing, F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc. Natl. Acad. Sci. U. S. A. 100, 567–71 (2003).
Humair, P. & Gern, L. The wild hidden face of Lyme borreliosis in Europe. Microbes Infect. 2, 915–922 (2000).
pubmed: 10962275
doi: 10.1016/S1286-4579(00)00393-2
Hrazdilová, K. et al. Wild boar as a potential reservoir of zoonotic tick-borne pathogens. Ticks Tick. Borne. Dis. 12, (2021).
Fabri, N. D. et al. Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens. Parasites Vectors 14, 360 (2021).
pubmed: 34246293
pmcid: 8272276
doi: 10.1186/s13071-021-04860-w
Randolph, S. & Dobson, A. Pangloss revisited: A critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology. 139, 847–863 (2012).
pubmed: 22336330
doi: 10.1017/S0031182012000200
Ogden, N. H. & Tsao, J. I. Biodiversity and Lyme disease: Dilution or amplification?. Epidemics 1, 196–206 (2009).
pubmed: 21352766
doi: 10.1016/j.epidem.2009.06.002
Wood, C. L. & Lafferty, K. D. Biodiversity and disease: A synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol. Evol. 28, 239–247 (2013).
pubmed: 23182683
doi: 10.1016/j.tree.2012.10.011
Lin, Y.-P., Diuk-Wasser, M. A., Stevenson, B. & Kraiczy, P. Complement evasion contributes to lyme borreliae-host associations HHS Public Access. Trends Parasitol. 36, 634–645 (2020).
pubmed: 32456964
pmcid: 7292789
doi: 10.1016/j.pt.2020.04.011
Steinbrink, A., Brugger, K., Margos, G., Kraiczy, Peter & Klimpel, S. Arthropods and medical entomology-review. The evolving story of Borrelia burgdorferi sensu lato transmission in Europe. 1, 3
Baize, D. A sound reference base for soils: The “Référentiel Pédologique”. (1998).
Boyer, P. H. et al. Impact of different anthropogenic environments on ticks and tick-associated pathogens in Alsace, a French region highly endemic for tick-borne diseases. Microorganisms 10, 245 (2022).
pubmed: 35208700
pmcid: 8877010
doi: 10.3390/microorganisms10020245
Koebel, C. et al. Human granulocytic anaplasmosis in eastern France: Clinical presentation and laboratory diagnosis. Diagn. Microbiol. Infect. Dis. 72, 214–218 (2012).
pubmed: 22321996
doi: 10.1016/j.diagmicrobio.2011.12.005
Hovius, J. W. R. et al. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 382, 658 (2013).
pubmed: 23953389
pmcid: 3987849
doi: 10.1016/S0140-6736(13)61644-X
Dupouey, J., Thimonier, A. & Behr, P. Variations de la densité des sols de hêtraies du Nord-Est de la France en relation avec leus caractéristiques physico-chimiques. Etude Gest. des sols 4, 43–52 (1997).
AFNOR. Norme expérimentale X31–001, Q. des sols. Analyse granulométrique par sédimentation. Méthode la pipette. 2, 57–71 (1999).
Campbell, C., Chapman, S., Cameron, C., Davidson, M. & Potts, J. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl. Environ. Microbiol. 69, 3593–3599 (2003).
pubmed: 12788767
pmcid: 161481
doi: 10.1128/AEM.69.6.3593-3599.2003
Lundberg, S. M. & Lee, S.-I. A Unified Approach to Interpreting Model Predictions. in Advances in Neural Information Processing Systems (eds. Guyon, I. et al.) 30, (Curran Associates, Inc., 2017).