A longitudinal investigation on tick populations and their Borrelia infections in the Netherlands was undertaken between 2006 and 2011 with the aim to assess spatial and temporal patterns of the acarological risk in forested sites across the country and to assess variations in Borrelia genospecies diversity. Ticks were collected monthly in 11 sites and nymphs were examined for Borrelia infections. Tick populations expressed strong seasonal variations, with consistent and significant differences in mean tick densities between sites. Borrelia infections were present in all study sites, with a site-specific mean prevalence per month ranging from 7% to 26%. Prevalence was location-dependent and was not associated with tick densities. Mean Borrelia prevalence was lowest in January (4%), gradually increasing to reach a maximum (24%) in August. Borrelia afzelii represented 70% of all infections, with Borrelia burgdorferi sensu stricto, Borrelia garinii, and Borrelia valaisiana represented with 4%, 8%, and 10%, respectively. The density of infected nymphs and the proportional distribution of the four Borrelia genospecies, were significantly different between sites. The results show a consistent and significant spatial and temporal difference in acarological risk across the Netherlands.
Get full access to this article
View all access options for this article.
References
1.
Braun-BlanquetJ. Pflanzensoziologie: Grundzüge der Vegetationskunde. Berlin, Germany: Springer Verlag, 1964.
2.
CernyV, DanielM, RosickyB. Some features of the developmental cycle of the tick Ixodes ricinus (L.) (Acarina: Ixodidae). Folia Parasitol, 1974; 21:85–87.
3.
CoipanEC, FonvilleM, Tijsse-KlasenE, van der GiessenJWB, et al.Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S-23S rDNA spacer region. Infect Genet Evol, 2013a; 17:216–222.
4.
CoipanEC, JahfariS, FonvilleM, MaassenCB, et al.Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus. Front Cell Infect Microbiol, 2013b; 3:36.
5.
DanielM, MalýM, DanielováV, KřížB, et al.Abiotic predictors and annual seasonal dynamics of Ixodes ricinus, the major disease vector of Central Europe. Parasit Vectors, 2015; 8:478.
6.
DanielsTJ, FalcoRC, FishD. Estimating population size and drag sampling efficiency for the blacklegged tick (Acari: Ixodidae). J Med Entomol, 2000; 37:357–363.
7.
DuijvendijkGv, SprongH, TakkenW. Multi-trophic interactions driving the transmission cycle of Borrelia afzelii between Ixodes ricinus and rodents: A review. Parasit Vectors, 2015; 8:643.
8.
EisenRJ, EisenL, GirardYA, FedorovaN, et al.A spatially-explicit model of acarological risk of exposure to Borrelia burgdorferi-infected Ixodes pacificus nymphs in northwestern California based on woodland type, temperature, and water vapor. Ticks Tick Borne Dis, 2010; 1:35–43.
9.
Estrada-PenaA, OrtegaC, SanchezN, DeSimoneL, et al.Correlation of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks with specific abiotic traits in the western Palearctic. Appl Environ Microbiol, 2011; 77:3838–3845.
10.
FerdinJ, CerarT, StrleF, Ružić-Sabljić E. Evaluation of real-time PCR targeting hbb gene for Borrelia species identification. J Microbiol Methods, 2010; 82:115–119.
11.
GassnerF, TakkenW, Lombaers-van der PlasC, KasteleinP, et al.Rodent species as natural reservoirs of Borrelia burgdorferi sensu lato in different habitats of Ixodes ricinus in The Netherlands. Ticks Tick Borne Dis, 2013; 4:452–458.
12.
GassnerF, Van VlietAJH, BurgersSLGE, JacobsF, et al.Geographic and temporal variations in population dynamics of Ixodes ricinus and associated Borrelia infections in the Netherlands. Vector Borne Zoonotic Dis, 2011; 11:523–532.
13.
GassnerF, VerbaarschotP, SmallegangeRC, SpitzenJ, et al.Variations in Ixodes ricinus density and Borrelia infections associated with cattle introduced into a woodland in The Netherlands. Appl Environ Microbiol, 2008; 74:7138–7144.
14.
GrayJS. The development and seasonal activity of the tick Ixodes ricinus: A vector of lyme borreliosis. Rev Med Vet Entomol, 1991; 79:323–333.
15.
GrayJS. Review: The ecology of ticks transmitting Lyme borreliosis. Exp Appl Acarol, 1998; 22:249–258.
16.
HalosL, BordS, CottéV, GasquiP, et al.Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol, 2010; 76:4413–4420.
17.
HancockPA, BrackleyR, PalmerSCF. Modelling the effect of temperature variation on the seasonal dynamics of Ixodes ricinus tick populations. Int J Parasitol, 2011; 41:513–522.
18.
HanincovaK, SchaferSM, EttiS, SewellHS, et al.Association of Borrelia afzelii with rodents in Europe. Parasitology, 2003; 126:11–20.
19.
HeylenD, MatthysenE, FonvilleM, SprongH. Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes rinicus ticks. Environ Microbiol, 2014; 16:2859–2868.
20.
HeylenD, TijsseE, FonvilleM, MatthysenE, et al.Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol, 2013; 15:663–673.
21.
HofhuisA, HarmsM, van den WijngaardC, SprongH, et al.Continuing increase of tick bites and Lyme disease between 1994 and 2009. Ticks Tick Borne Dis, 2015; 6:69–74.
22.
HofmeesterT, CoipanE, WierenS, PrinsH, et al.Few vertebrate species dominate the Borrelia burgdorferi s.l. life cycle. Environ Res Lett, 2016; 11:043001.
23.
HouwerzylJ, RootJJ, Hoogkamp-KorstanjeJAA. A case of Lyme disease with cardiac involvement in The Netherlands. Infection, 1984; 12:358.
24.
HumairPF, RaisO, GernL. Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: Differential transmission pattern and overwintering maintenance. Parasitology, 1999; 118 (Pt 1):33–42.
25.
JaensonTGT, EisenL, ComstedtP, MejlonHA, et al.Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden. Med Vet Entomol, 2009; 23:226–237.
26.
JoudaF, PerretJL, GernL. Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. J Med Entomol, 2004; 41:162–169.
27.
KurtenbachK, De MichelisS, SewellHS, EttiS, et al.Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol, 2001; 67:4926–4929.
28.
KurtenbachK, De MichelisS, SewellHS, EttiS, et al.The key roles of selection and migration in the ecology of Lyme borreliosis. Int J Med Microbiol, 2002; 291Suppl 33:152–154.
29.
KurtenbachK, KampenH, DizijA, ArndtS, et al.Infestation of rodents with larval Ixodes ricinus (Acari: Ixodidae) is an important factor in the transmission cycle of Borrelia burgdorferi s.l. in German woodlands. J Med Entomol, 1995; 32:807–817.
30.
MannelliA, BertolottiL, GernL, GrayJ. Ecology of Borrelia burgdorferi sensu lato in Europe: Transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol Rev, 2012; 36:837–861.
31.
MannelliA, BoggiattoG, GregoE, CincoM, et al.Acarological risk of exposure to agents of tick-borne zoonoses in the first recognized Italian focus of Lyme borreliosis. Epidemiol Infect, 2003; 131:1139–1147.
32.
MannelliA, NebbiaP, TramutaC, GregoE, et al.Borrelia burgdorferi sensu lato infection in larval Ixodes ricinus (Acari: Ixodidae) feeding on blackbirds in northwestern Italy. J Med Entomol, 2005; 42:168–175.
33.
MargosG, VollmerSA, OgdenNH, FishD. Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato. Infect Genetic Evol, 2011; 11:1545–1563.
34.
MedlockJM, HansfordKM, BormaneA, DerdakovaM, et al.Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors, 2013; 6.
35.
MilneA. The ecology of the sheep tick, Ixodes ricinus L—The seasonal activity in Britain with particular reference to northern England. Parasitology, 1945; 36:142–152.
36.
MysterudA, EasterdayWR, StigumVM, AAs AB, et al.Contrasting emergence of Lyme disease across ecosystems. Nat Commun, 2016; 7:e1182.
37.
NorteAC, RamosJA, GernL, NuncioMS, et al.Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: Circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environ Microbiol, 2013; 15:386–397.
38.
PacillyFCA, BenningME, JacobsF, LeidekkerJ, et al.Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus. Ticks Tick Borne Dis, 2014; 5:810–817.
39.
PangracovaL, DerdakovaM, PekarikL, HviscovaI, et al.Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors, 2013; 6.
40.
PerezD, KneubuhlerY, RaisO, GernL. 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; 12:633–644.
41.
RagagliC, BertolottiL, GiacobiniM, MannelliA, et al.Transmission dynamics of Borrelia lusitaniae and Borrelia afzelii among Ixodes ricinus, lizards, and mice in Tuscany, Central Italy. Vect Borne Zoonotic Dis, 2011; 11:21–28.
42.
RandolphSE, GreenRM, HoodlessAN, PeaceyMF. An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol, 2002; 32:979–989.
43.
RichterD, SchroderB, HartmannNK, MatuschkaFR. Spatial stratification of various Lyme disease spirochetes in a Central European site. FEMS Microbiol Ecol, 2013; 83:738–744.
44.
SchmidtKA, OstfeldRS. Biodiversity and the dilution effect in disease ecology. Ecology, 2001; 82:609–619.
45.
SchoulsL, PolIvd, RijpkemaS, SchotCS. Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato and Bartonella species in Dutch Ixodes ricinus ticks. J Clin Microbiol, 1999; 37:2215–2222.
46.
SchulzM, MahlingM, PfisterK. Abundance and seasonal activity of questing Ixodes ricinus ticks in their natural habitats in southern Germany in 2011. J Vector Ecol, 2014; 39:56–65.
47.
SchwarzA, HonigV, VavruskovaZ, GrubhofferL, et al.Abundance of Ixodes ricinus and prevalence of Borrelia burgdorferi s.l. in the nature reserve Siebengebirge, Germany, in comparison to three former studies from 1978 onwards. Parasit Vectors, 2012; 5:268.
48.
SinskiE, PawelczykA, BajerA, BehnkeJ. Abundance of wild rodents, ticks and environmental risk of Lyme borreliosis: A longitudinal study in an area of Mazury Lakes district of Poland. Ann Agric Environ Med, 2006; 13:295–300.
49.
SprongH, HofhuisA, GassnerF, TakkenW, et al.Circumstantial evidence for an increase in the total number and activity of Borrelia-infected Ixodes ricinus in the Netherlands. Parasit Vectors, 2012; 5.
50.
TackW, MadderM, BaetenL, De FrenneP, et al.The abundance of Ixodes ricinus ticks depends on tree species composition and shrub cover. Parasitology, 2012; 139:1273–1281.
51.
TälleklintL, JaensonTG. Seasonal variations in density of questing Ixodes ricinus (Acari: Ixodidae) nymphs and prevalence of infection with B. burgdorferi s.l. in south central Sweden. J Med Entomol, 1996; 33:592–597.
52.
Tijsse-KlasenE, PandakN, HengeveldP, TakumiK, et al.Ability to cause erythema migrans differs between Borrelia burgdorferi sensu lato isolates. Parasit Vectors, 2013; 6:23.
53.
TvetenAK. 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, 2013; 45:681–687.
54.
van OverbeekL, GassnerF, van der PlasCL, KasteleinP, et al.Diversity of Ixodes ricinus tick-associated bacterial communities from different forests. FEMS Microbiol Ecol, 2008; 66:72.
55.
WeedaEJ, SchaminéeJHJ, Van DuurenL. Atlas van Plantengemeenschappen in Nederland. Utrecht: KNNV Uitgeverij (gezamenlijk met Centraal Bureau voor de Statistiek, Alterra, VEWIN, Ministerie van Landbouw, Natuurbeheer en Voedselkwaliteit, Rijkswaterstaat en KIWA), 2005.
56.
WielingaPR, GaasenbeekC, FonvilleM, de BoerA, et al.Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Appl Environ Microbiol, 2006; 72:7594–7601.
57.
WilsonWL, MontgomeryWI, ElwoodRW. Population regulation in the wood mouse Apodemus sylvaticus (L.). Mamm Rev, 1993; 23:73–92.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
