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Environmental determinants of Ixodes ricinus ticks and the incidence of Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in Scotland

Published online by Cambridge University Press:  24 September 2012

M. C. JAMES ,
A. S. BOWMAN ,
K. J. FORBES ,
F. LEWIS ,
J. E. MCLEOD  and
L. GILBERT
M. C. JAMES
Affiliation:
Institute of Biological and Environmental Sciences, Zoology Building, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK Section of Immunology and Infection, Medical School, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, UK James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen, AB15 8QH, UK
A. S. BOWMAN
Affiliation:
Institute of Biological and Environmental Sciences, Zoology Building, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
K. J. FORBES
Affiliation:
Section of Immunology and Infection, Medical School, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, UK
F. LEWIS
Affiliation:
Section of Epidemiology, Vetsuisse, University of Zürich, 8057 Zürich, Switzerland
J. E. MCLEOD
Affiliation:
James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen, AB15 8QH, UK
L. GILBERT*
Affiliation:
James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen, AB15 8QH, UK
*
*Corresponding author:James Hutton Institute, Macaulay Drive, Craigiebuckler, Aberdeen AB15 8QH, UK. Tel: +44 (0)1224 395187. Fax: +44 (0) 844 928 5429. E-mail: Lucy.Gilbert@hutton.ac.uk
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Summary

Lyme borreliosis (LB) is the most common arthropod-borne disease of humans in the Northern hemisphere. In Europe, the causative agent, Borrelia burgdorferi sensu lato complex, is principally vectored by Ixodes ricinus ticks. The aim of this study was to identify environmental factors influencing questing I. ricinus nymph abundance and B. burgdorferi s.l. infection in questing nymphs using a large-scale survey across Scotland. Ticks, host dung and vegetation were surveyed at 25 woodland sites, and climatic variables from a Geographical Information System (GIS) were extracted for each site. A total of 2397 10 m2 transect surveys were conducted and 13 250 I. ricinus nymphs counted. Questing nymphs were assayed for B. burgdorferi s.l. and the average infection prevalence was 5·6% (range 0·8–13·9%). More questing nymphs and higher incidence of B. burgdorferi s.l. infection were found in areas with higher deer abundance and in mixed/deciduous compared to coniferous forests, as well as weaker correlations with season, altitude, rainfall and ground vegetation. No correlation was found between nymph abundance and infection prevalence within the ranges encountered. An understanding of the environmental conditions associated with tick abundance and pathogen prevalence may be used to reduce risk of exposure and to predict future pathogen prevalence and distributions under environmental changes.

Keywords

woodlandnymphshostsPCRGISnegative binomial hurdle modeldisease
Type
Research Article
Information
Parasitology , Volume 140 , Issue 2 , February 2013 , pp. 237 - 246
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Altobelli, A., Boemo, B., Mignozzi, K., Bandi, M., Floris, R., Menardi, G. and Cinco, M. (2008). Spatial Lyme borreliosis risk assessment in north-eastern Italy. International Journal of Medical Microbiology 298, (Suppl. 1), 125–128.CrossRefGoogle Scholar
Beyer, H. L. (2004). Hawth's Analysis Tools for ArcGIS. Available at www.spatialecology.com/htools. Last accessed November 2009.Google Scholar
Bolzoni, L., Rosà, R., Cagnacci, F. and Rizzoli, A. (2012). Effect of deer density on tick infestation of rodents and the hazard of tick-borne encephalitis. Part II: population and infection models. International Journal for Parasitology 42, 373–381.CrossRefGoogle Scholar
Brown, R. N., Peot, M. A. and Lane, R. S. (2006). Sylvatic maintenance of Borrelia burgdorferi (Spirochaetales) in northern California: Untangling the web of transmission. Journal of Medical Entomology 43, 743–751.CrossRefGoogle ScholarPubMed
Burri, C., Cadenas, F. M., Douet, V., Moret, J. and Gern, L. (2007). Ixodes ricinus density and infection prevalence of Borrelia burdorferi sensu lato along a north-facing altitudinal gradient in the Rhone valley (Switzerland). Vector-Borne and Zoonotic Diseases 7, 50–58.CrossRefGoogle Scholar
Cadenas, F. M., Rais, O., Jouda, F., Douet, V., Humair, P.-F., Moret, J. and Gern, L. (2007). Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along and north- and south-facing altitudinal gradient on Chaumont mountain, Switzerland. Journal of Medical Entomology 44, 683–693.CrossRefGoogle Scholar
Cagnacci, F., Bolzoni, L., Rosà, R., Carpi, G., Hauffe, H. C., Valent, M., Tagliapietra, V., Kazimirova, M., Koci, J., Stanko, M., Lukan, M., Henttonen, H. and Rizzoli, A. (2012). Effect of deer density on tick infestation of rodents and the hazard of tick-borne encephalitis. Part I: Empirical assessment. International Journal for Parasitology 42, 365–372.CrossRefGoogle Scholar
Eisen, L., Eisen, R. J. and Lane, R. S. (2002). Seasonal activity patterns of Ixodes pacificus nymphs in relation to climatic conditions. Medical and Veterinary Entomology 16, 235–244.CrossRefGoogle ScholarPubMed
Eisen, R. J., Eisen, L., Girard, Y. A., Fedorova, N., Mun, J., Slikas, B., Leonhard, S., Kitron, U. and Lane, R. S. (2010). 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 and Tick-Borne Diseases 1, 35–43.CrossRefGoogle ScholarPubMed
ESRI (2008). ArcMap v9.3. Environmental Systems Research Institute, Redlands, CA, USA.Google Scholar
Estrada-Peña, A. (2001). Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in northern Spain. Journal of Medical Entomology 38, 361–370.CrossRefGoogle ScholarPubMed
Falco, R. C., McKenna, D. F., Daniels, T. J., Nadelman, R. B., Nowakowski, J., Fish, D. and Wormser, G. P. (1999). Temporal relation between Ixodes scapularis abundance and risk for Lyme disease associated with erythema migrans. American Journal of Epidemiology 149, 771–776.CrossRefGoogle ScholarPubMed
Flowerdew, J. R. (1993). Mice and Voles. British Natural History Series. Whittet Books Ltd, London, UK.Google Scholar
Gilbert, L. (2010). Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? Oecologia 162, 217–225.CrossRefGoogle ScholarPubMed
Gilbert, L., Norman, R., Laurenson, K. M., Reid, H. W. and Hudson, P. J. (2001). Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale wild populations. Journal of Animal Ecology 70, 1053–1061.CrossRefGoogle Scholar
Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249–258.CrossRefGoogle Scholar
Gray, J. S. and Lohan, G. (1982). The development of a sampling method for the tick Ixodes ricinus and its use in a redwater fever area. Annals of Applied Biology 101, 421–427.CrossRefGoogle Scholar
Guerra, M., Walker, E., Jones, C., Paskewitz, S., Roberto Cortinas, M., Ashley Stancil, L. B., Bobo, M. and Kitron, U. (2002). Predicting the risk of Lyme disease: Habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8, 289–297.CrossRefGoogle ScholarPubMed
Guy, E. C. and Stanek, G. (1991). Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. Journal of Clinical Pathology 44, 610–611.CrossRefGoogle ScholarPubMed
Hanincová, K., Schäfer, S. M., Etti, S., Sewell, H., Taragelová, V., Ziak, D., Labuda, M. and Kurtenbach, K., (2003 b). Association of Borrelia afzelii with rodents in Europe. Parasitology 126, 11–20.CrossRefGoogle ScholarPubMed
Hanincová, K., Taragelová, V., Koci, J., Schäfer, S. M., Hails, R., Ullmann, A. J., Piesman, J., Labuda, M. and Kurtenbach, K. (2003 a). Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Applied Environmental Microbiology 69, 2825–2830.CrossRefGoogle Scholar
Health Protection Scotland (2011). www.documents.hps.scot.nhs.uk/giz/10-year-tables/lyme.pdf (last accessed October 2011).Google Scholar
Hillyard, P. (1996). Ticks of North West Europe. Field Studies Council, Shrewsbury, UK.Google Scholar
Hubálek, Z. and Halouzka, J. (1998). Prevalence rates of Borrelia burgdorferi sensu in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167–172.Google ScholarPubMed
Humair, P. F., Rais, O. and Gern, L. (1999). Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: Differential transmission pattern and overwintering maintenance. Parasitology 118, 33–42.CrossRefGoogle ScholarPubMed
Jaenson, T. G. T., Eisen, L., Comstedt, P., Mejlon, H. A., Lindgren, E., Bergström, S. and Olsen, B. (2009). Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden. Medical and Veterinary Entomology 23, 226–237.CrossRefGoogle ScholarPubMed
Jaenson, T. G. and Tälleklint, L. (1992). Incompetence of roe deer as reservoirs of the Lyme borreliosis spirochete. Journal of Medical Entomology 29, 813–817.CrossRefGoogle ScholarPubMed
James, M. C. (2010). The ecology, genetic diversity and epidemiology of Lyme Borreliosis in Scotland. Ph.D. thesis. University of Aberdeen, Aberdeen, Scotland.Google Scholar
James, M. C., Furness, R. W., Bowman, A. S., Forbes, K. J. and Gilbert, L. (2011). The importance of passerine birds as tick hosts and in the transmission of Borrelia burgdorferi, the agent of Lyme disease. A case study from Scotland. Ibis 153, 293–302.CrossRefGoogle Scholar
Jensen, P. M., Hansen, H. and Frandsen, F. (2000). Spatial risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 32, 545–550.Google ScholarPubMed
Jouda, F., Perret, J. and 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 Diseases 4, 23–32.CrossRefGoogle Scholar
Kalsbeek, V. and Frandsen, F. (1996). The seasonal activity of Ixodes ricinus ticks in Denmark. Anzeiger für Schädlingskunde 69, 160–161.CrossRefGoogle Scholar
Kiffner, C., Lödige, C., Alings, , Vor, T. and Rühe, F. (2010). Abundance estimate of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Experimental and Applied Acarology 52, 73–84.CrossRefGoogle ScholarPubMed
Killilea, M. E., Swei, A., Lane, R. S., Briggs, C. J. and Ostfeld, R. S. (2008). Spatial dynamics of Lyme disease: A review. EcoHealth 5, 167–195.CrossRefGoogle ScholarPubMed
Kirby, A. D., Smith, A. A., Benton, T. G. and Hudson, P. J. (2004). Rising burden of immature sheep ticks (Ixodes ricinus) on red grouse (Lagopus lagopus scoticus) chicks in the Scottish uplands. Medical and Veterinary Entomology 18, 67–70.CrossRefGoogle ScholarPubMed
Kurtenbach, K., Dizij, A., Seitz, H. M., Margos, G., Moter, S. E., Kramers, M. D., Wallich, R., Schaible, U. E. and Simon, M. M. (1994). Differential immune responses to Borrelia burgdorferi in European wild rodent species influence spirochete transmission to Ixodes ricinus L. (Acari: Ixodidae). Infection and Immunity 62, 5344–5352.CrossRefGoogle ScholarPubMed
Kurtenbach, K, Hanincová, K., Tsao, J. I., Margos, G., Fish, D. and Ogden, N. H. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660–669.CrossRefGoogle ScholarPubMed
Kurtenbach, K., Peacey, M., Rijpkema, S. G., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998). Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied Environmental Microbiology 64, 1169–1174.CrossRefGoogle ScholarPubMed
Lindström, A. and Jaenson, T. G. T. (2003). Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. Journal of Medical Entomology 40, 375–378.CrossRefGoogle ScholarPubMed
Ling, C. L., Joss, A. W. L., Davidson, M. M. and Ho-Yen, D. O. (2000). Identification of different Borrelia burgdorferi genomic groups from Scottish ticks Molecular Pathology 53, 94–98.CrossRefGoogle ScholarPubMed
Maetzel, D., Maier, W. A. and Kampen, H. (2005). Borrelia burgdorferi infection prevalences in questing Ixodes ricinus ticks (Acari: Ixodidae) in urban and suburban Bonn, western Germany. Parasitology Research 95, 5–12.CrossRefGoogle Scholar
Margos, G., Gatewood, A. G., Aanensen, D. M., Hanincová, K., Terekhova, D., Vollmer, S. A., Cornet, M., Piesman, J., Donaghy, M., Bormane, A., Hurn, M. A., Feil, E. J., Fish, D., Casjens, S., Wormser, G. P., Schwartz, I. and Kurtenbach, K. (2008). MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proceedings of the National Academy of Sciences, USA 105, 8730–8735.CrossRefGoogle ScholarPubMed
Met Office (2009). www.metoffice.gov.uk/climate/uk/2007/summer/averages.html. Last accessed March 2010.Google Scholar
Ostfeld, R. S. and Keesing, F. (2000). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 1–7.CrossRefGoogle Scholar
Perry, M. and Hollis, D. (2005). The development of a new set of long-term climate averages for the UK. International Journal of Climatology 25, 1023–1039.CrossRefGoogle Scholar
Piesman, J. and Gern, L. (2004). Lyme borreliosis in Europe and North America. Parasitology 129, S191–S220.CrossRefGoogle ScholarPubMed
Prusinski, M. A., Chen, H., Drobnack, J. M., Kogut, S. J., Means, R. G., Howard, J. J., Oliver, J., Lukacik, G., Backenson, P. B. and White, D. J. (2006). Habitat structure associated with Borrelia burgdorferi prevalence in small mammals in New York State. Environmental Entomology 35, 308–319.CrossRefGoogle Scholar
R Development Core Team (2010). R: A Language and Environment for Statistical Computing. www.R-project.org. Vienna, Austria.Google Scholar
Randolph, S.E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, S1–S29.CrossRefGoogle ScholarPubMed
Randolph, S.E., Green, R. M., Peacey, M. F. and Rogers, D. J. (2000). Seasonal synchrony: The key to tick-borne encephalitis foci identified by satellite data. Parasitology 121, 15–23.CrossRefGoogle ScholarPubMed
Rijpkema, S. G. T., Molkenboer, M. J. C. H., Schouls, L. M., Jongejan, F. and Schellekens, J. F. P. (1995). Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. Journal of Clinical Microbiology 33, 3091–3095.CrossRefGoogle ScholarPubMed
Robertson, J. N., Gray, J. S. and Stewart, P. (2000). Tick bite and Lyme borreliosis risk at a recreational site in England. European Journal of Epidemiology 16, 647–652.CrossRefGoogle Scholar
Ruiz-Fons, F. and Gilbert, L. (2010). The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. International Journal for Parasitology 40, 1013–1020.CrossRefGoogle ScholarPubMed
Sergeant, G. and Morris, P. (2003). How to Find and Identify Mammals. 2nd Edn. The Mammal Society, London, UK.Google Scholar
Tälleklint, L. and Jaenson, T. G. (1996). Seasonal variations in density of questing Ixodes ricinus (Acari: Ixodidae) nymphs and prevalence of infection of B. burgdorferi s.l. in south central Sweden. Journal of Medical Entomology 33, 592–597.CrossRefGoogle ScholarPubMed
Telford, S. R. III, Mather, T. N., Moore, S. I., Wilson, M. L. and Spielman, A. (1988). Incompetence of deer as reservoirs of the Lyme disease spirochete. American Journal of Tropical Medicine and Hygiene 39, 105–109.CrossRefGoogle ScholarPubMed
Vollmer, S. A., Bormane, A., Dinnis, R. E., Seelig, F., Dobson, A. D. M., Aanensen, D. M., James, M. C., Donaghy, M., Randolph, S. E., Feil, E. J., Kurtenbach, K. and Margos, G. (2011). Host migration impacts on the phylogeography of Lyme borreliosis spirochaete species in Europe. Environmental Microbiology 13, 184–192.CrossRefGoogle ScholarPubMed
Vor, T., Kiffner, C., Hagedorn, P., Niedrig, M. and Rühe, F. (2010). Tick burden on European roe deer (Capreolus capreolus). Experimental and Applied Acarology 51, 405–417.CrossRefGoogle ScholarPubMed
Walker, A. R., Alberdi, M. P., Urquhart, K. A. and Rose, H. (2001). Risk factors in habitats of the tick Ixodes ricinus influencing human exposure to Ehrlichia phagocytophila bacteria. Medical and Veterinary Entomology 15, 40–49.CrossRefGoogle ScholarPubMed
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