Seasonal patterns and spatial variation of Borrelia burgdorferi (sensu lato) infections in Ixodes ricinus in the Netherlands.
Acarological risk
Lyme borreliosis
Prevalence
Seasonality
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
24 Feb 2021
24 Feb 2021
Historique:
received:
29
10
2020
accepted:
23
01
2021
entrez:
25
2
2021
pubmed:
26
2
2021
medline:
4
9
2021
Statut:
epublish
Résumé
The incidence of Lyme borreliosis varies over time and space through as yet incompletely understood mechanisms. In Europe, Lyme borreliosis is caused by infection with a Borrelia burgdorferi (s.l.) genospecies, which is primarily transmitted by a bite of Ixodes ricinus nymphs. The aim of this study was to investigate the spatial and temporal variation in nymphal infection prevalence of B. burgdorferi (s.l.) (NIP), density of questing nymphs (DON) and the resulting density of infected nymphs (DIN). We investigated the infection rates in I. ricinus nymphs that were collected monthly between 2009 and 2016 in 12 locations in the Netherlands. Using generalized linear mixed models, we explored how the NIP, DON and DIN varied during the seasons, between years and between locations. We also determined the genospecies of the Borrelia infections and investigated whether the genospecies composition differed between locations. The overall NIP was 14.7%. A seasonal pattern in infection prevalence was observed, with higher estimated prevalences in the summer than in the spring and autumn. This, combined with higher nymphal densities in summer, resulted in a pronounced summer peak in the estimated DIN. Over the 7.5-year study period, a significant decrease in infection prevalence was found, as well as a significant increase in nymphal density. These two effects appear to cancel each other out; the density of infected nymphs, which is the product of NIP × DON, showed no significant trend over years. Mean infection prevalence (NIP, averaged over all years and all months) varied considerably between locations, ranging from 5 to 26%. Borrelia genospecies composition differed between locations: in some locations almost all infections consisted of B. afzelii, whereas other locations had more diverse genospecies compositions. In the Netherlands, the summer peak in DIN is a result of peaks in both NIP and DON. No significant trend in DIN was observed over the years of the study, and variations in DIN between locations were mostly a result of the variation in DON. There were considerable differences in acarological risk between areas in terms of infection prevalence and densities of ticks as well as in Borrelia genospecies composition.
Sections du résumé
BACKGROUND
BACKGROUND
The incidence of Lyme borreliosis varies over time and space through as yet incompletely understood mechanisms. In Europe, Lyme borreliosis is caused by infection with a Borrelia burgdorferi (s.l.) genospecies, which is primarily transmitted by a bite of Ixodes ricinus nymphs. The aim of this study was to investigate the spatial and temporal variation in nymphal infection prevalence of B. burgdorferi (s.l.) (NIP), density of questing nymphs (DON) and the resulting density of infected nymphs (DIN).
METHODS
METHODS
We investigated the infection rates in I. ricinus nymphs that were collected monthly between 2009 and 2016 in 12 locations in the Netherlands. Using generalized linear mixed models, we explored how the NIP, DON and DIN varied during the seasons, between years and between locations. We also determined the genospecies of the Borrelia infections and investigated whether the genospecies composition differed between locations.
RESULTS
RESULTS
The overall NIP was 14.7%. A seasonal pattern in infection prevalence was observed, with higher estimated prevalences in the summer than in the spring and autumn. This, combined with higher nymphal densities in summer, resulted in a pronounced summer peak in the estimated DIN. Over the 7.5-year study period, a significant decrease in infection prevalence was found, as well as a significant increase in nymphal density. These two effects appear to cancel each other out; the density of infected nymphs, which is the product of NIP × DON, showed no significant trend over years. Mean infection prevalence (NIP, averaged over all years and all months) varied considerably between locations, ranging from 5 to 26%. Borrelia genospecies composition differed between locations: in some locations almost all infections consisted of B. afzelii, whereas other locations had more diverse genospecies compositions.
CONCLUSION
CONCLUSIONS
In the Netherlands, the summer peak in DIN is a result of peaks in both NIP and DON. No significant trend in DIN was observed over the years of the study, and variations in DIN between locations were mostly a result of the variation in DON. There were considerable differences in acarological risk between areas in terms of infection prevalence and densities of ticks as well as in Borrelia genospecies composition.
Identifiants
pubmed: 33627166
doi: 10.1186/s13071-021-04607-7
pii: 10.1186/s13071-021-04607-7
pmc: PMC7905678
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
121Références
Arthur DR. British ticks. London: Butterworths; 1963.
Brooks ME, Kristensen K, Benthem KJ van, Magnusson A, Berg CW, Nielsen A, et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 2017;9(2):378–400. https://doi.org/10.32614/RJ-2017-066 .
Burri C, Cadenas FM, 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;7:50–8. https://doi.org/10.1089/vbz.2006.0569 .
doi: 10.1089/vbz.2006.0569
pubmed: 17417957
Chvostáč M, Špitalská E, Václav R, Vaculová T, Minichová L, Derdáková M. 2018. Seasonal patterns in the prevalence and diversity of tick-borne Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Rickettsia spp. in an urban temperate forest in south western Slovakia. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15050994
Coipan EC, Fonville M, Tijsse-Klasen E, van der Giessen JWB, Takken W, Sprong H, et al. Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S–23S rDNA spacer region. Infect Genet Evol. 2013;17:216–22. https://doi.org/10.1016/j.meegid.2013.04.009 .
doi: 10.1016/j.meegid.2013.04.009
pubmed: 23602839
Coipan EC, Jahfari S, Fonville M, Maassen C, van der Giessen J, Takken W, et al . Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus. Front Cell Infect Microbiol. 2013. https://doi.org/10.3389/fcimb.2013.00036 .
doi: 10.3389/fcimb.2013.00036
pubmed: 23908971
pmcid: 3726834
Coipan EC, Jahfari S, Fonville M, Oei GA, Spanjaard L, Takumi K, et al.. Imbalanced presence of Borrelia burgdorferi s.l. multilocus sequence types in clinical manifestations of Lyme borreliosis. Infect Genet Evol. 2016;42:66–76. https://doi.org/10.1016/j.meegid.2016.04.019 .
doi: 10.1016/j.meegid.2016.04.019
pubmed: 27125686
Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M, et al. Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States. Am J Trop Med Hyg. 2012;86:320–7. https://doi.org/10.4269/ajtmh.2012.11-0395 .
doi: 10.4269/ajtmh.2012.11-0395
pubmed: 22302869
pmcid: 3269287
Egyed L, Élő P, Sréter-Lancz Z, Széll Z, Balogh Z, Sréter T. Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick-Borne Dis. 2012;3:90–4. https://doi.org/10.1016/j.ttbdis.2012.01.002 .
doi: 10.1016/j.ttbdis.2012.01.002
pubmed: 22445929
Eisen RJ, Eisen L, Girard YA, Fedorova N, Mun J, Slikas B, 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. https://doi.org/10.1016/j.ttbdis.2009.12.002 .
doi: 10.1016/j.ttbdis.2009.12.002
pubmed: 20532183
pmcid: 2880809
Fingerle V, Bergmeister H, Liegl G, Vanek E, Wilske B. Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus in Southern Germany. J Spiroch Tick Dis. 1994;1:41–5.
Gassner F. Tick tactics. Interactions between habitat characteristics, hosts and microorganisms in relation to the biology of the sheep tick Ixodes ricinus. PhD thesis. Wageningen: Wageningen University. 2010.
Gassner F, van Vliet AJH, Burgers SLGE, Jacobs F, Verbaarschot P, Hovius EKE, et al. Geographic and temporal variations in population dynamics of Ixodes ricinus and associated Borrelia infections in the Netherlands. Vector Borne Zoonotic Dis. 2011;11:523–32. https://doi.org/10.1089/vbz.2010.0026 .
doi: 10.1089/vbz.2010.0026
pubmed: 21083369
Guy EC, Stanek G. Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. J Clin Pathol. 1991;44:610–1. https://doi.org/10.1136/jcp.44.7.610 .
doi: 10.1136/jcp.44.7.610
pubmed: 1856296
pmcid: 496808
Hartemink N, van Vliet A, Sprong H, Jacobs F, Garcia-Martí I, Zurita-Milla R, et al. Temporal-spatial variation in questing tick activity in the Netherlands: the effect of climatic and habitat factors. Vector Borne Zoonotic Dis. 2019;9(7):494–505. https://doi.org/10.1089/vbz.2018.2369
Heylen D, Tijsse E, Fonville M, Matthysen E, Sprong H. Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol. 2013;15:663–73. https://doi.org/10.1111/1462-2920.12059 .
doi: 10.1111/1462-2920.12059
pubmed: 23279105
Hillyard P. Ticks of north-west Europe: keys and notes for identification of the species. Synopses of the British fauna. Shrewsbury: Field Studies Council; 1996.
Hofhuis A, Bennema S, Harms M, van Vliet AJH, Takken W, van den Wijngaard CC, et al. Decrease in tick bite consultations and stabilization of early Lyme borreliosis in the Netherlands in 2014 after 15 years of continuous increase. BMC Public Health. 2016;16:425. https://doi.org/10.1186/s12889-016-3105-y .
doi: 10.1186/s12889-016-3105-y
pubmed: 27216719
pmcid: 4877959
Hofhuis A, Harms M, van den Wijngaard C, Sprong H, van Pelt W. Continuing increase of tick bites and Lyme disease between 1994 and 2009. Ticks Tick-Borne Dis. 2015;6:69–74. https://doi.org/10.1016/j.ttbdis.2014.09.006 .
doi: 10.1016/j.ttbdis.2014.09.006
pubmed: 25448421
Kesteman T, Rossi C, Bastien P, Brouillard J, Avesani V, Olive N, et al. Prevalence and genetic heterogeneity of Borrelia burgdorferi sensu lato in Ixodes ticks in Belgium. Acta Clin Belg. 2010;65:319–22.
doi: 10.1179/acb.2010.069
Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V. Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts. Int J Health Geogr. 2010;9:54.
doi: 10.1186/1476-072X-9-54
Lenth R. emmeans: estimated marginal means, aka least-squares means. R package version 1.4.6. 2020. https://CRAN.R-project.org/package=emmeans .
Lin Y-P, Diuk-Wasser MA, Stevenson B, Kraiczy P. Complement evasion contributes to Lyme Borreliae–host associations. Trends Parasitol. 2020;36:634–45. https://doi.org/10.1016/j.pt.2020.04.011 .
doi: 10.1016/j.pt.2020.04.011
pubmed: 32456964
pmcid: 7292789
Mather TN, Nicholson MC, Donnelly EF, Matyas BT. Entomologic index for human risk of Lyme disease. Am J Epidemiol. 1996;144:1066–9. https://doi.org/10.1093/oxfordjournals.aje.a008879 .
doi: 10.1093/oxfordjournals.aje.a008879
pubmed: 8942438
Mysterud A, Easterday W, Qviller L, Viljugrein H, Ytrehus B. Spatial and seasonal variation in the prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in questing Ixodes ricinus ticks in Norway. Parasites Vectors. 2013;6:187. https://doi.org/10.1186/1756-3305-6-187 .
doi: 10.1186/1756-3305-6-187
pubmed: 23786850
pmcid: 3691722
Okeyo M, Hepner S, Rollins RE, Hartberger C, Straubinger RK, Marosevic D, et al. Longitudinal study of prevalence and spatio-temporal distribution of Borrelia burgdorferi sensu lato in ticks from three defined habitats in Latvia, 1999–2010. Environ Microbiol. 2020. https://doi.org/10.1111/1462-2920.15100 .
doi: 10.1111/1462-2920.15100
Pepin KM, Eisen RJ, Mead PS, Piesman J, Fish D, Hoen AG, et al. Geographic variation in the relationship between human Lyme disease incidence and density of infected host-seeking Ixodes scapularis nymphs in the eastern United States. Am J Trop Med Hyg. 2012;86:1062–71. https://doi.org/10.4269/ajtmh.2012.11-0630 .
doi: 10.4269/ajtmh.2012.11-0630
pubmed: 22665620
pmcid: 3366524
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;12:633–44. https://doi.org/10.1089/vbz.2011.0763 .
doi: 10.1089/vbz.2011.0763
pubmed: 22607074
pmcid: 3413890
Pichon B, Mousson L, Figureau C, Rodhain F, Perez-Eid C. Density of deer in relation to the prevalence of Borrelia burgdorferi s.1. in Ixodes ricinus nymphs in Rambouillet forest. France Exp Appl Acarol. 1999;23:267–75. https://doi.org/10.1023/A:1006023115617 .
doi: 10.1023/A:1006023115617
pubmed: 10356769
R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2016.
Rauter C, Hartung T. Prevalence of Borrelia burgdorferi Sensu Lato Genospecies in Ixodes ricinus Ticks in Europe: a Metaanalysis. Appl Env Microbiol. 2005;71:7203–16.
doi: 10.1128/AEM.71.11.7203-7216.2005
Reye AL, Hübschen JM, Sausy A, Muller CP. Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol. 2010;76:2923–31. https://doi.org/10.1128/AEM.03061-09 .
doi: 10.1128/AEM.03061-09
pubmed: 20228110
pmcid: 2863427
Rosef O, Paulauskas A, Radzijevskaja J. Prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing Ixodes ricinus ticks in relation to the density of wild cervids. Acta Vet Scand. 2009;51:47. https://doi.org/10.1186/1751-0147-51-47 .
doi: 10.1186/1751-0147-51-47
pubmed: 19943915
pmcid: 2788566
Ruyts SC, Landuyt D, Ampoorter E, Heylen D, Ehrmann S, Coipan EC, et al. Low probability of a dilution effect for Lyme borreliosis in Belgian forests. Ticks Tick-Borne Dis. 2018;9:1143–52. https://doi.org/10.1016/j.ttbdis.2018.04.016 .
doi: 10.1016/j.ttbdis.2018.04.016
pubmed: 29716838
Ruyts SC, Tack W, Ampoorter E, Coipan EC, Matthysen E, Heylen D, et al. 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. 2018;9:141–5. https://doi.org/10.1016/j.ttbdis.2017.08.008 .
doi: 10.1016/j.ttbdis.2017.08.008
pubmed: 28869190
Sormunen JJ, Klemola T, Vesterinen EJ, Vuorinen I, Hytönen J, Hänninen J, et al. Assessing the abundance, seasonal questing activity, and Borrelia and tick-borne encephalitis virus (TBEV) prevalence of Ixodes ricinus ticks in a Lyme borreliosis endemic area in Southwest Finland. Ticks Tick Borne Dis. 2016;7:208–15. https://doi.org/10.1016/j.ttbdis.2015.10.011 .
doi: 10.1016/j.ttbdis.2015.10.011
pubmed: 26548608
Sprong H, Hofhuis A, Gassner F, Takken W, Jacobs F, van Vliet AJ, et al. Circumstantial evidence for an increase in the total number and activity of Borrelia-infected Ixodes ricinus in the Netherlands. Parasites Vectors. 2012;5:294. https://doi.org/10.1186/1756-3305-5-294 .
doi: 10.1186/1756-3305-5-294
pubmed: 23244453
pmcid: 3562265
Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012;379:461–73. https://doi.org/10.1016/S0140-6736(11)60103-7 .
doi: 10.1016/S0140-6736(11)60103-7
pubmed: 21903253
Strnad M, Hönig V, Růžek D, Grubhoffer L, Rego ROM. Europe-wide meta-analysis of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks. Appl Environ Microbiol. 2017;83:e00609–17. https://doi.org/10.1128/AEM.00609-17 .
doi: 10.1128/AEM.00609-17
pubmed: 28550059
pmcid: 5514677
Takken W, van Vliet AJH, Verhulst NO, Jacobs FHH, Gassner F, Hartemink N, et al. Acarological risk of Borrelia burgdorferi sensu lato infections across space and time in The Netherlands. Vector Borne Zoonotic Dis. 2017;17:99–107. https://doi.org/10.1089/vbz.2015.1933 .
doi: 10.1089/vbz.2015.1933
Tälleklint L, Jaenson TGT. 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;33:592–7. https://doi.org/10.1093/jmedent/33.4.592 .
doi: 10.1093/jmedent/33.4.592
pubmed: 8699453
Tekenradar. 2020. https://www.tekenradar.nl/ziekte-van-lyme/lyme-in-nederland . Accessed 23 Sept 2020.
Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W, 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;72:7594–601. https://doi.org/10.1128/AEM.01851-06 .
doi: 10.1128/AEM.01851-06
pubmed: 17028227
pmcid: 1694262
Zeimes CB, Olsson GE, Hjertqvist M, Vanwambeke SO. Shaping zoonosis risk: landscape ecology vs. landscape attractiveness for people, the case of tick-borne encephalitis in Sweden. Parasites Vectors. 2014;7:370. https://doi.org/10.1186/1756-3305-7-370 .
doi: 10.1186/1756-3305-7-370
pubmed: 25128197
pmcid: 4143547