Tick abundance and infection with three zoonotic bacteria are heterogeneous in a Belgian peri-urban forest.
Borrelia burgdorferi s.l.
Ixodes ricinus
Forest
Tick-borne disease risk
Tick-borne pathogens
Journal
Experimental & applied acarology
ISSN: 1572-9702
Titre abrégé: Exp Appl Acarol
Pays: Netherlands
ID NLM: 8507436
Informations de publication
Date de publication:
13 Jun 2024
13 Jun 2024
Historique:
received:
17
10
2023
accepted:
29
04
2024
medline:
13
6
2024
pubmed:
13
6
2024
entrez:
13
6
2024
Statut:
aheadofprint
Résumé
Ixodes ricinus is a vector of several pathogens of public health interest. While forests are the primary habitat for I. ricinus, its abundance and infection prevalence are expected to vary within forest stands. This study assesses the spatio-temporal variations in tick abundance and infection prevalence with three pathogens in and around a peri-urban forest where human exposure is high. Ticks were sampled multiple times in 2016 and 2018 in multiple locations with a diversity of undergrowth, using the consecutive drags method. Three zoonotic pathogens were screened for, Borrelia burgdorferi s.l., Coxiella burnetii, and Francisella tularensis. The influence of season, type of site and micro-environmental factors on tick abundance were assessed with negative binomial generalized linear mixed-effects models. We collected 1642 nymphs and 181 adult ticks. Ticks were most abundant in the spring, in warmer temperatures, and where undergrowth was higher. Sites with vegetation unaffected by human presence had higher abundance of ticks. Forest undergrowth type and height were significant predictors of the level of tick abundance in a forest. The consecutive drags method is expected to provide more precise estimates of tick abundance, presumably through more varied contacts with foliage. Borrelia burgdorferi s.l. prevalence was estimated from pooled ticks at 5.33%, C. burnetii was detected in six pools and F. tularensis was not detected. Borrelia afzelii was the dominant B. burgdorferi genospecies. Tick abundance and B. burgdorferi s.l. infection prevalence were lower than other estimates in Belgian forests.
Identifiants
pubmed: 38869724
doi: 10.1007/s10493-024-00919-2
pii: 10.1007/s10493-024-00919-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme Disease risk. Conserv Biol 17:267–272. https://doi.org/10.1046/j.1523-1739.2003.01260.x
doi: 10.1046/j.1523-1739.2003.01260.x
Anderson A, Bijlmer H, Fournier P-E, Graves S, Hartzell J, Kersh GJ, Limonard G, Marrie TJ, Massung RF, McQuiston JH, Nicholson WL, Paddock CD, Sexton DJ (2013) Diagnosis and management of Q fever—United States, 2013: recommendations from CDC and the Q fever Working Group. Recommendations and Reports, Morbidity and Mortality Weekly Report
Bakdash JZ, Marusich LR (2017) Repeated measures correlation. Front Psychol 8:1–13. https://doi.org/10.3389/fpsyg.2017.00456
doi: 10.3389/fpsyg.2017.00456
Bakdash JZ, Marusich LR (2023) rmcorr: Repeated Measures Correlation
Boehnke D, Gebhardt R, Petney T, Norra S (2017) On the complexity of measuring forests microclimate and interpreting its relevance in habitat ecology: the example of Ixodes ricinus ticks. Parasites Vectors 10:1–14. https://doi.org/10.1186/s13071-017-2498-5
doi: 10.1186/s13071-017-2498-5
Bord S, Druilhet P, Gasqui P, Abrial D, Vourc’h G (2014) Bayesian estimation of abundance based on removal sampling under weak assumption of closed population with catchability depending on environmental conditions. Application to tick abundance. Ecol Modell 274:72–79. https://doi.org/10.1016/j.ecolmodel.2013.12.004
doi: 10.1016/j.ecolmodel.2013.12.004
Boyard C, Barnouin J, Gasqui P, Vourc’h G (2007) Local environmental factors characterizing Ixodes ricinus nymph abundance in grazed permanent pastures for cattle. Parasitology 134:987–994. https://doi.org/10.1017/S0031182007002351
doi: 10.1017/S0031182007002351
pubmed: 17291383
Boyard C, Barnouin J, Bord S, Gasqui P, Vourc’h G (2011) Reproducibility of local environmental factors for the abundance of questing Ixodes ricinus nymphs on pastures. Ticks Tick Borne Dis 2:104–110. https://doi.org/10.1016/j.ttbdis.2011.02.001
doi: 10.1016/j.ttbdis.2011.02.001
pubmed: 21771544
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized Linear mixed modeling. R J 9:378–400
doi: 10.32614/RJ-2017-066
Brownstein JS, Skelly DK, Holford TR, Fish D (2005) Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146:469–475. https://doi.org/10.1007/s00442-005-0251-9
doi: 10.1007/s00442-005-0251-9
pubmed: 16187106
Carvalho CL, Lopes de Carvalho I, Zé-Zé L, Núncio MS, Duarte EL (2014) Tularaemia: a challenging zoonosis. Comp Immunol Microbiol Infect Dis 37:85–96. https://doi.org/10.1016/j.cimid.2014.01.002
doi: 10.1016/j.cimid.2014.01.002
pubmed: 24480622
pmcid: 7124367
Cochez C, Heyman P, Heylen D, Fonville M, Hengeveld P, Takken W, Simons L, Sprong H (2015) The presence of Borrelia miyamotoi, a relapsing fever spirochaete, in questing Ixodes ricinus in Belgium and in the Netherlands. Zoonoses Public Health 62:331–333. https://doi.org/10.1111/zph.12154
doi: 10.1111/zph.12154
pubmed: 25212814
Comstedt P, Bergström S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, Barbour AG, Bunikis J (2006) Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg Infect Dis 12:1307
doi: 10.3201/eid1207.060127
Core Team R (2022) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing
Cutler SJ, Bouzid M, Cutler RR (2007) Q Fever J Infect 54:313–318. https://doi.org/10.1016/j.jinf.2006.10.048
doi: 10.1016/j.jinf.2006.10.048
pubmed: 17147957
Dantas-Torres F, Chomel BB, Otranto D (2012) Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol 28:437–446. https://doi.org/10.1016/j.pt.2012.07.003
doi: 10.1016/j.pt.2012.07.003
pubmed: 22902521
de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946. https://doi.org/10.2741/3200
doi: 10.2741/3200
pubmed: 18508706
Diuk-Wasser MA, Vourc G, Cislo P, Hoen AG, Melton F, Hamer SA, Rowland M, Cortinas R, Hickling GJ, Tsao JI, Barbour AG, Kitron U, Piesman J, Fish D (2010) Field and climate-based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne disease agents in the eastern United States. Glob Ecol Biogeogr 19:504–514. https://doi.org/10.1111/j.1466-8238.2010.00526.x
doi: 10.1111/j.1466-8238.2010.00526.x
Dobson ADM (2013) Ticks in the wrong boxes: assessing error in blanket-drag studies due to occasional sampling. Parasites Vectors 6:344. https://doi.org/10.1186/1756-3305-6-344
doi: 10.1186/1756-3305-6-344
pubmed: 24321224
pmcid: 4029458
Dobson ADM, Taylor JL, Randolph SE (2011) Tick (Ixodes ricinus) abundance and seasonality at recreational sites in the UK: hazards in relation to fine-scale habitat types revealed by complementary sampling methods. Ticks Tick Borne Dis 2:67–74. https://doi.org/10.1016/j.ttbdis.2011.03.002
doi: 10.1016/j.ttbdis.2011.03.002
pubmed: 21771540
Duron O, Sidi-Boumedine K, Rousset E, Moutailler S, Jourdain E (2015) The importance of ticks in Q fever transmission: what has (and has not) been demonstrated? Trends Parasitol 31:536–552. https://doi.org/10.1016/j.pt.2015.06.014
doi: 10.1016/j.pt.2015.06.014
pubmed: 26458781
ECDC (2017) Tularaemia factsheet [WWW Document]. URL https://www.ecdc.europa.eu/en/tularaemia/facts
EEA (2020) European Environment Agency - Site BE31006C0: Vallée de la Dyle à Ottignies [WWW Document]. Nat. 2000, Stand. Data Form./ URL https://natura2000.eea.europa.eu/Natura2000/SDF.aspx?site=BE31006C0
Estrada-Pena A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean Region: a guide to identification of species. Zaragoza
Estrada-Peña A, de la Fuente J (2014) The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Res 108:104–128. https://doi.org/10.1016/j.antiviral.2014.05.016
doi: 10.1016/j.antiviral.2014.05.016
pubmed: 24925264
Fracasso G, Grillini M, Grassi L, Gradoni F, da Rold G, Bertola M (2023) Effective methods of estimation of pathogen prevalence in pooled ticks. Pathogens 45:1–9. https://doi.org/10.3390/pathogens12040557
doi: 10.3390/pathogens12040557
Geebelen L, Van Cauteren D, Devleesschauwer B, Moreels S, Tersago K, Van Oyen H, Speybroeck N, Lernout T (2019) Combining primary care surveillance and a meta-analysis to estimate the incidence of the clinical manifestations of Lyme borreliosis in Belgium, 2015–2017. Ticks Tick Borne Dis 10:598–605. https://doi.org/10.1016/j.ttbdis.2018.12.007
doi: 10.1016/j.ttbdis.2018.12.007
pubmed: 30772196
Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873. https://doi.org/10.1002/sim
doi: 10.1002/sim
pubmed: 17960576
Gray JS (1998) The ecology of ticks transmitting Lyme borreliosis. Exp Appl Acarol 22:249–258. https://doi.org/10.1023/A:1006070416135
doi: 10.1023/A:1006070416135
Guerra M, Walker E, Jones C, Paskewitz S, Cortinas MR, Stancil A, Beck L, Bobo M, Kitron U (2002) Predicting the risk of Lyme Disease: Habitat Suitability for Ixodes scapularis in the North Central United States. Emerg Infect Dis 8:289–297. https://doi.org/10.3201/eid0803.010166
doi: 10.3201/eid0803.010166
pubmed: 11927027
pmcid: 2732460
Hanincova K, Schäfer SM, Etti S, Sewell HS, Taragelová V, Ziak D, Labuda M, Kurtenbach K (2003) Association of Borrelia afzelii with rodents in Europe. Parasitology 126:11–20. https://doi.org/10.1017/S0031182002002548
doi: 10.1017/S0031182002002548
pubmed: 12613759
Hansford KM, Fonville M, Gillingham EL, Coipan EC, Pietzsch ME, Krawczyk AI, Vaux AGC, Cull B, Sprong H, Medlock JM (2017) Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England. Ticks Tick Borne Dis 8:353–361. https://doi.org/10.1016/j.ttbdis.2016.12.009
doi: 10.1016/j.ttbdis.2016.12.009
pubmed: 28089123
Hartemink N, van Vliet AJH, Gort G, Gassner F, Jacobs F, Fonville M, Takken W, Sprong H (2021) Seasonal patterns and spatial variation of Borrelia burgdorferi (Sensu Lato) infections in Ixodes ricinus in the Netherlands. Parasites Vectors 14:1–16. https://doi.org/10.1186/s13071-021-04607-7
doi: 10.1186/s13071-021-04607-7
Hartig F (2022) DHARMa: residual Diagnostics for Hierarchical. Multi-Level / Mixed) Regression Models
Heylen D, De Coninck E, Jansen F, Madder M (2014a) Differential diagnosis of three common Ixodes spp. ticks infesting songbirds of Western Europe: Ixodes arboricola, I. frontalis and I. ricinus. Ticks Tick. Borne. Dis. 5, 693–700. https://doi.org/10.1016/j.ttbdis.2014.05.006
Heylen D, Matthysen E, Fonville M, Sprong H (2014b) Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes Rinicus ticks. Environ Microbiol 16:2859–2868. https://doi.org/10.1111/1462-2920.12304
doi: 10.1111/1462-2920.12304
pubmed: 24118930
Heylen D, Lasters R, Adriaensen F, Fonville M, Sprong H, Matthysen E (2019) Ticks and tick-borne diseases in the city: role of landscape connectivity and green space characteristics in a metropolitan area. Sci Total Environ 670:941–949. https://doi.org/10.1016/j.scitotenv.2019.03.235
doi: 10.1016/j.scitotenv.2019.03.235
pubmed: 30921726
Hildebrandt A, Straube E, Neubauer H, Schmoock G (2011) Coxiella burnetii and coinfections in Ixodes ricinus ticks in Central Germany. Vector-Borne Zoonotic Dis 11:1205–1207. https://doi.org/10.1089/vbz.2010.0180
doi: 10.1089/vbz.2010.0180
pubmed: 21142964
Hillyard PD (1996) Ticks of North-West Europe, The Natura. ed. London
Horobik V, Keesing F, Ostfeld RS (2006) Abundance and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks along forest-field edges. EcoHealth 3:262–268. https://doi.org/10.1007/s10393-006-0065-1
doi: 10.1007/s10393-006-0065-1
Hubálek Z, Halouzka J, Juřicová Z, Šikutová S, Rudolf I (2006) 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. https://doi.org/10.1111/j.1365-2915.2006.00615.x
doi: 10.1111/j.1365-2915.2006.00615.x
pubmed: 16796612
Jackman S, {pscl} (2020) Classes and Methods for {R} Developed in the Political Science Computational Laboratory
James MC, Bowman AS, Forbes KJ, Lewis F, McLeod JE, Gilbert L (2013) Environmental determinants of Ixodes ricinus ticks and the incidence of Borrelia burgdorferi Sensu Lato, the agent of Lyme borreliosis. Scotl Parasitol 140:237–246. https://doi.org/10.1017/S003118201200145X
doi: 10.1017/S003118201200145X
Jost L (2006) Entropy Divers Oikos 113:363–375
doi: 10.1111/j.2006.0030-1299.14714.x
Jouda F, Perret J-L, Gern L (2004) Density of questing Ixodes ricinus nymphs and adults infected by Borrelia burgdorferi Sensu Lato in Switzerland: Spatio-temporal pattern at a regional scale. Vector Borne Zoonotic Dis 4:23–32
doi: 10.1089/153036604773082960
pubmed: 15018770
Kesteman T, Rossi C, Bastien P, Brouillard J, Avesani V, Olive N, Martin P, Delmée M (2010) Prevalence and genetic heterogeneity of Borrelia burgdorferi sensu lato in Ixodes ticks in Belgium. Acta Clin Belg 65:319–322. https://doi.org/10.1179/acb.2010.069
doi: 10.1179/acb.2010.069
pubmed: 21128558
Kiewra D, Kryza M, Szymanowski M (2014) Influence of selected meteorological variables on the questing activity of Ixodes ricinus ticks in Lower Silesia. SW Pol J Vector Ecol 39:138–145. https://doi.org/10.1111/j.1948-7134.2014.12080.x
doi: 10.1111/j.1948-7134.2014.12080.x
Körner S, Makert GR, Ulbert S, Pfeffer M (2021) The prevalence of Coxiella burnetii in hard ticks in Europe and their role in Q fever transmission revisited - a systematic review. Front Vet Sci 8:1–16. https://doi.org/10.3389/fvets.2021.655715
doi: 10.3389/fvets.2021.655715
Kurtenbach K, De Michelis S, Etti S, Schäfer SM, Sewell HS, Brade V, Kraiczy P (2002) Host association of Borrelia burgdorferi sensu lato - the key role of host complement. Trends Microbiol 10:74–79. https://doi.org/10.1016/S0966-842X(01)02298-3
doi: 10.1016/S0966-842X(01)02298-3
pubmed: 11827808
Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V (2010) Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts. Int J Health Geogr 9:54. https://doi.org/10.1186/1476-072X-9-54
doi: 10.1186/1476-072X-9-54
pubmed: 20979609
pmcid: 2984574
Lernout T, De Regge N, Tersago K, Fonville M, Suin V, Sprong H (2019) Prevalence of pathogens in ticks collected from humans through citizen science in Belgium. Parasites Vectors 12:1–11. https://doi.org/10.1186/s13071-019-3806-z
doi: 10.1186/s13071-019-3806-z
Li S, Heyman P, Cochez C, Simons L, Vanwambeke SO (2012) A multi-level analysis of the relationship between environmental factors and questing Ixodes ricinus dynamics in Belgium. Parasit Vectors 5:1–11. https://doi.org/10.1186/1756-3305-5-149
doi: 10.1186/1756-3305-5-149
Litzroth AA, Mori M (2021) Surveillance épidémiologique de la tularémie. Francisella tularensis– 2021. Sciensano report
Litzroth AA, Stefani G, Esbroeck M, Van, Mori M (2021) Surveillance épidémiologique de la fièvre Q. Coxiella burnetii– 2021
Mackenzie DI, Kendall WL, Ecology S, Sep N (2002) How should detection probability be incorporated into estimates of relative abundance? Ecology 83:2387–2393
doi: 10.1890/0012-9658(2002)083[2387:HSDPBI]2.0.CO;2
McLure A, O’Neill B, Mayfield H, Lau C, McPherson B (2021) PoolTestR: an R package for estimating prevalence and regression modelling for molecular xenomonitoring and other applications with pooled samples. Environ Model Softw 145:105158. https://doi.org/10.1016/j.envsoft.2021.105158
doi: 10.1016/j.envsoft.2021.105158
Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George J-C, Golovljova I, Jaenson TGT, Jensen J-K, Jensen PM, Kazimirova M, Oteo Ja, Papa A, Pfister K, Plantard O, Randolph SE, Rizzoli A, Santos-Silva MM, Sprong H, Vial L, Hendrickx G, Zeller H, Van Bortel W (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors 6:1–11. https://doi.org/10.1186/1756-3305-6-1
doi: 10.1186/1756-3305-6-1
pubmed: 23281838
pmcid: 3549795
Michelet L, Delannoy S, Devillers E, Umhang G, Aspan A, Juremalm M, Chirico J, van der Wal FJ, Sprong H, Pihl B, Klitgaard TP, Bødker K, Fach R, Moutailler P, S (2014) High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol 4:1–13. https://doi.org/10.3389/fcimb.2014.00103
doi: 10.3389/fcimb.2014.00103
Mori M, Boarbi S, Michel P, Bakinahe R, Rits K, Wattiau P, Fretin D (2013) In vitro and in vivo infectious potential of Coxiella burnetii: a study on Belgian livestock isolates. PLoS ONE 8:1–9. https://doi.org/10.1371/journal.pone.0067622
doi: 10.1371/journal.pone.0067622
Mori M, Mertens K, Cutler SJ, Santos AS (2017) Critical aspects for detection of Coxiella burnetii, in: Vector-Borne and Zoonotic Diseases. Mary Ann Liebert, Inc. 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA, pp. 33–41
Mysterud A, Easterday WR, Qviller L, Viljugrein H, Ytrehus B (2013) Spatial and seasonal variation in the prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi Sensu Lato in questing Ixodes ricinus ticks in Norway. Parasites Vectors 6:1–8. https://doi.org/10.1186/1756-3305-6-187
doi: 10.1186/1756-3305-6-187
Nyrhilä S, Sormunen JJ, Mäkelä S, Sippola E, Vesterinen EJ, Klemola T (2020) One out of ten: low sampling efficiency of cloth dragging challenges abundance estimates of questing ticks. Exp Appl Acarol. https://doi.org/10.1007/s10493-020-00564-5
doi: 10.1007/s10493-020-00564-5
pubmed: 33128644
pmcid: 7686165
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) vegan: Community Ecology Package
Paul REL, Cote M, Le Naour E, Bonnet SI (2016) Environmental factors influencing tick densities over seven years in a French suburban forest. Parasit Vectors 9:309. https://doi.org/10.1186/s13071-016-1591-5
doi: 10.1186/s13071-016-1591-5
pubmed: 27234215
pmcid: 4884405
Pedersen BN, Jenkins A, Kjelland V (2020) Tick-borne pathogens in Ixodes ricinus ticks collected from migratory birds in southern Norway. PLoS ONE 15:1–13. https://doi.org/10.1371/journal.pone.0230579
doi: 10.1371/journal.pone.0230579
Pérez D, Kneubühler Y, Rais O, Gern L (2012) 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 12:633–644. https://doi.org/10.1089/vbz.2011.0763
doi: 10.1089/vbz.2011.0763
pubmed: 22607074
pmcid: 3413890
Perret J-L, Guigoz E, Rais O, Gern L (2000) Infuence of saturation deficit and temperature on Ixodes ricinus tick. Parasitol Res 86:554–557. https://doi.org/10.1007/s004360000209
doi: 10.1007/s004360000209
pubmed: 10935905
Pilloux L, Baumgartner A, Jaton K, Lienhard R, Ackermann-Gäumann R, Beuret C, Greub G (2019) Prevalence of Anaplasma phagocytophilum and Coxiella burnetii in Ixodes ricinus ticks in Switzerland: an underestimated epidemiologic risk. New Microbes New Infect 27:22–26. https://doi.org/10.1016/j.nmni.2018.08.017
doi: 10.1016/j.nmni.2018.08.017
pubmed: 30534383
Randolph SE (2001) The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lond B Biol Sci 356:1045–1056
doi: 10.1098/rstb.2001.0893
pubmed: 11516382
pmcid: 1088499
Rousseau R, Vanwambeke SO, Boland C, Mori M (2021) The isolation of culturable bacteria in Ixodes ricinus ticks of a Belgian peri-urban forest uncovers opportunistic bacteria potentially important for public health. Int J Environ Res Public Health 18:1–14
doi: 10.3390/ijerph182212134
Royal Meteorological, Institute (2023) Le climat dans votre commune [WWW Document]. Clim. la Belgique. URL https://www.meteo.be/fr/climat/climat-de-la-belgique/climat-dans-votre-commune
Ruiz-Fons F, Gilbert L (2010) The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. Int J Parasitol 40:1013–1020. https://doi.org/10.1016/j.ijpara.2010.02.006
doi: 10.1016/j.ijpara.2010.02.006
pubmed: 20211625
Ruiz-Fons F, Fernández-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J (2012) Factors driving the abundance of Ixodes ricinus ticks and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol 78:2669–2676. https://doi.org/10.1128/AEM.06564-11
doi: 10.1128/AEM.06564-11
pubmed: 22286986
pmcid: 3318823
Ruyts SC, Ampoorter E, Coipan EC, Baeten L, Heylen D, Sprong H, Matthysen E, Verheyen K (2016) Diversifying forest communities may change Lyme disease risk: Extra dimension to the dilution effect in Europe. Parasitology 143:1310–1319. https://doi.org/10.1017/S0031182016000688
doi: 10.1017/S0031182016000688
pubmed: 27173094
Ruyts SC, Tack W, Ampoorter E, Coipan EC, Matthysen E, Heylen D, Sprong H, Verheyen K (2017) Year-to-year variation in the density of Ixodes ricinus ticks and the prevalence of the rodent-associated human pathogens Borrelia afzelii and B. Miyamotoi in different forest types. Ticks Tick Borne Dis 9:141–145. https://doi.org/10.1016/j.ttbdis.2017.08.008
doi: 10.1016/j.ttbdis.2017.08.008
pubmed: 28869190
Ruyts SC, Landuyt D, Ampoorter E, Heylen D, Ehrmann S, Coipan EC, Matthysen E, Sprong H, Verheyen K (2018) Low probability of a dilution effect for Lyme borreliosis in Belgian forests. Ticks Tick Borne Dis 9:1143–1152. https://doi.org/10.1016/j.ttbdis.2018.04.016
doi: 10.1016/j.ttbdis.2018.04.016
pubmed: 29716838
Salomon J, Hamer SA, Swei A (2020) A beginner’s guide to collecting questing hard ticks (acari: ixodidae): a standardized tick dragging protocol. J Insect Sci 20:1–8. https://doi.org/10.1093/jisesa/ieaa073
doi: 10.1093/jisesa/ieaa073
Schwarz A, Maier Wa, Kistemann T, Kampen H (2009) Analysis of the distribution of the tick Ixodes ricinus L. (Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information systems. Int J Hyg Environ Health 212:87–96. https://doi.org/10.1016/j.ijheh.2007.12.001
doi: 10.1016/j.ijheh.2007.12.001
pubmed: 18262840
Sprong H, Tijsse-Klasen E, Langelaar M, De Bruin A, Fonville M, Gassner F, Takken W, Van Wieren S, Nijhof A, Jongejan F, Maassen CBM, Scholte EJ, Hovius JW, Emil Hovius K, Špitalská E, Van Duynhoven YT (2012) Prevalence of Coxiella burnetii in ticks after a large outbreak of Q fever. Zoonoses Public Health 59:69–75. https://doi.org/10.1111/j.1863-2378.2011.01421.x
doi: 10.1111/j.1863-2378.2011.01421.x
pubmed: 21824373
SPW (2005) Services Publics de Wallonie - Carte des Principaux Types de Sols de Wallonie– 1/250000 [WWW Document]. Serv. Publics Wallonie. URL https://geoportail.wallonie.be/catalogue/64bbc088-367c-485c-bd7c-d2d08baedf9d.html (accessed 5.29.21)
Stanek G, Reiter M (2011) The expanding Lyme Borrelia complex-clinical significance of genomic species? Clin. Microbiol Infect 17:487–493. https://doi.org/10.1111/j.1469-0691.2011.03492.x
doi: 10.1111/j.1469-0691.2011.03492.x
Strle F, Stanek G (2009) Clinical manifestations and diagnosis of Lyme borreliosis. In: Lipsker, Dan, Jaulhac B (ed) Lyme Borreliosis- Biological and clinical aspects. Karger, Basel, pp 51–110
doi: 10.1159/000213070
Strnad M, Hönig V, Ružek D, Grubhoffer L, Rego ROM (2017) Europe-wide meta-analysis of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks. Appl Environ Microbiol 83:1–16. https://doi.org/10.1128/AEM.00609-17
doi: 10.1128/AEM.00609-17
Tack W, Madder M, de Frenne P, Vanhellemont M, Gruwez R, Verheyen K (2011) The effects of sampling method and vegetation type on the estimated abundance of Ixodes ricinus ticks in forests. Exp Appl Acarol 54:285–292. https://doi.org/10.1007/s10493-011-9444-6
doi: 10.1007/s10493-011-9444-6
pubmed: 21431925
Tack W, Madder M, Baeten L, Vanhellemont M, Gruwez R, Verheyen K (2012) Local habitat and landscape affect Ixodes ricinus tick abundances in forests on poor, sandy soils. Ecol Manage 265:30–36. https://doi.org/10.1016/j.foreco.2011.10.028
doi: 10.1016/j.foreco.2011.10.028
Tack W, Madder M, Baeten L, Vanhellemont M, Verheyen K (2013) Shrub clearing adversely affects the abundance of Ixodes ricinus ticks. Exp Appl Acarol 60:411–420. https://doi.org/10.1007/s10493-013-9655-0
doi: 10.1007/s10493-013-9655-0
pubmed: 23344639
Van Gestel M, Verheyen K, Matthysen E, Heylen D (2021) Danger on the track? Tick densities near recreation infrastructures in forests. Urban Urban Green 59:126994. https://doi.org/10.1016/j.ufug.2021.126994
doi: 10.1016/j.ufug.2021.126994
Van Overbeek L, Gassner F, Van Der Plas CL, Kastelein P, Nunes-Da Rocha U, Takken W (2008) Diversity of Ixodes ricinus tick-associated bacterial communities from different forests. FEMS Microbiol Ecol 66:72–84. https://doi.org/10.1111/j.1574-6941.2008.00468.x
doi: 10.1111/j.1574-6941.2008.00468.x
pubmed: 18355299
Vanwambeke SO, Sumilo D, Bormane A, Lambin EF, Randolph SE (2010) Landscape predictors of tick-borne encephalitis in Latvia: land cover, land use, and land ownership. Vector-borne Zoonotic Diseaes 10:497–506. https://doi.org/10.1089/vbz.2009.0116
doi: 10.1089/vbz.2009.0116
Versage JL, Severin DDM, Chu MC, Petersen JM (2003) Development of a Multitarget Real-Time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. J Clin Microbiol 41:5492–5499. https://doi.org/10.1128/JCM.41.12.5492-5499.2003
doi: 10.1128/JCM.41.12.5492-5499.2003
pubmed: 14662930
pmcid: 309004
Vourc’h G, Abrial D, Bord S, Jacquot M, Masséglia S, Poux V, Pisanu B, Bailly X, Chapuis JL (2016) 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. https://doi.org/10.1016/j.ttbdis.2016.02.008
doi: 10.1016/j.ttbdis.2016.02.008
pubmed: 26897396
Wallonie (2021) Site de Grand Intérêt Biologique (SGIB)– 219: Bois de Lauzelle. Site de Grand Intérêt Biologique (SGIB) [WWW Document]. La biodiversité en Wallonie. URL http://biodiversite.wallonie.be/fr/219-bois-de-lauzelle.html?IDD=251659334&IDC=1881 (accessed 4.30.21)
WHO (2007) World Health Organization guidelines on tularaemia: epidemic and pandemic alert and response [WWW Document]. URL http://www.who.int/csr/resources/publications/WHO_CDS_EPR_2007_7.pdf
Woldehiwet Z (2004) Q fever (coxiellosis): epidemiology and pathogenesis. Res Vet Sci 77:93–100. https://doi.org/10.1016/j.rvsc.2003.09.001
doi: 10.1016/j.rvsc.2003.09.001
pubmed: 15196898
Zeimes CB, Olsson GE, Hjertqvist M, Vanwambeke SO (2014) Shaping zoonosis risk: landscape ecology vs. landscape attractiveness for people, the case of tick-borne encephalitis in Sweden. Parasit Vectors 7:370. https://doi.org/10.1186/1756-3305-7-370
doi: 10.1186/1756-3305-7-370
pubmed: 25128197
pmcid: 4143547