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

Parasitology

Volumn 140, Issue 2, 2013, Pages 237-246

  James, M C ^a,b,d   Bowman, A S ^a   Forbes, K J ^b   Lewis, F ^c   McLeod, J E ^d   Gilbert, L ^d  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

disease; GIS; hosts; negative binomial hurdle model; nymphs; PCR; woodland

Indexed keywords

RAIN;

ALTITUDE; ARTICLE; BORRELIA BURGDORFERI; ENVIRONMENTAL FACTOR; FOREST; HUMAN; INCIDENCE; IXODES RICINUS; LYME DISEASE; PREVALENCE; PRIORITY JOURNAL; SEASONAL VARIATION; UNITED KINGDOM; VEGETATION;

ALTITUDE; ANIMALS; BORRELIA BURGDORFERI; DEER; ENVIRONMENT; INCIDENCE; IXODES; LYME DISEASE; NYMPH; POPULATION DENSITY; PREVALENCE; RAIN; RISK FACTORS; SCOTLAND; SEASONS; TREES;

EID: 84873334763     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S003118201200145X     Document Type: Article

References (59)

1. 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.
2. Beyer, H. L. (2004). Hawth's Analysis Tools for ArcGIS. Available at www. spatialecology.com/htools. Last accessed November 2009.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. ESRI (2008). ArcMap v9.3. Environmental Systems Research Institute, Redlands, CA, USA.
11. Estrada-Peña, A. (2001). Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in northern Spain. Journal of Medical Entomology 38, 361-370.
12. 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.
13. Flowerdew, J. R. (1993). Mice and Voles. British Natural History Series. Whittet Books Ltd, London, UK.
14. 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.
15. 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.
16. Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249-258.
17. 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.
18. 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.
19. 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.
20. Hanincová, K., Schäfer, S. M., Etti, S., Sewell, H., Taragelová, V., Ziak, D., Labuda, M. and Kurtenbach, K., (2003b). Association of Borrelia afzelii with rodents in Europe. Parasitology 126, 11-20.
21. Hanincová, K., Taragelová, V., Koci, J., Schäfer, S. M., Hails, R., Ullmann, A. J., Piesman, J., Labuda, M. and Kurtenbach, K. (2003a). Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Applied Environmental Microbiology 69, 2825-2830.
22. Health Protection Scotland (2011). www.documents.hps.scot.nhs.uk/giz/10- year-tables/lyme.pdf (last accessed October 2011)
23. Hillyard, P. (1996). Ticks of North West Europe. Field Studies Council, Shrewsbury, UK.
24. 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.
25. 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.
26. 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.
27. 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.
28. James, M. C. (2010). The ecology, genetic diversity and epidemiology of Lyme Borreliosis in Scotland. Ph.D. thesis. University of Aberdeen, Aberdeen, Scotland.
29. 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.
30. 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.
31. 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.
32. Kalsbeek, V. and Frandsen, F. (1996). The seasonal activity of Ixodes ricinus ticks in Denmark. Anzeiger für Schädlingskunde 69, 160-161.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Met Office (2009). www.metoffice.gov.uk/climate/uk/2007/summer/averages. html. Last accessed March 2010.
44. Ostfeld, R. S. and Keesing, F. (2000). Biodiversity and disease risk: The case of Lyme disease. Conservation Biology 14, 1-7.
45. Perry, M. and Hollis, D. (2005). The development of a new set of longterm climate averages for the UK. International Journal of Climatology 25, 1023-1039.
46. Piesman, J. and Gern, L. (2004). Lyme borreliosis in Europe and North America. Parasitology 129, S191-S220.
47. 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.
48. R Development Core Team (2010). R: A Language and Environment for Statistical Computing. www.R-project.org. Vienna, Austria.
49. Randolph, S.E. (2004). Tick ecology: Processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, S1-S29.
50. 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.
51. 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.
52. 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.
53. 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.
54. Sergeant, G. and Morris, P. (2003). How to Find and Identify Mammals. 2nd Edn. The Mammal Society, London, UK.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.