The importance of the aggregation of ticks on small mammal hosts for the establishment and persistence of tick-borne pathogens: An investigation using the R 0 model

Parasitology

Volumn 139, Issue 12, 2012, Pages 1605-1613

  Harrison, Alan ^a   Bennett, Nigel C ^a,b  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

aggregation; Borrelia burgdorferi s.l.; epidemiology; Ixodes ricinus; transmission; vector borne diseases

Indexed keywords

ARTICLE; BACTERIAL TRANSMISSION; BASIC REPRODUCTION NUMBER; BORRELIA BURGDORFERI; FEMALE; HOST PARASITE INTERACTION; INFECTION RISK; MALE; MAMMAL; MOUSE; NONHUMAN; PARASITE PHENOMENA AND FUNCTIONS; POPULATION DISTRIBUTION; POPULATION MODEL; PRIORITY JOURNAL; TICK; TICK AGGREGATION; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VIRUS TRANSMISSION;

ANIMALS; ARACHNID VECTORS; BORRELIA BURGDORFERI; DISEASE RESERVOIRS; ENCEPHALITIS VIRUSES, TICK-BORNE; ENCEPHALITIS, TICK-BORNE; HOST-PARASITE INTERACTIONS; IXODES; LYME DISEASE; MAMMALS; TICK INFESTATIONS;

EID: 84867765219     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012000893     Document Type: Article

References (50)

1. Anderson, R. M. and May,R.M. (1990). Modern vaccines: Immunisation and herd immunity. Lancet 335, 641-645.
2. Bouchard, C., Beauchamp, G., Trudel, L., Milford, F., Lindsay, L. R., Belanger, D. and Ogden, N. H. (2011). Associations between Ixodes scapularis ticks and small mammal hosts in a newly endemic zone in southeastern Canada: Implications for Borrelia burgdorferi transmission. Ticks and Tick-borne Diseases 2, 183-190.
3. Boyer, N., Réale, D., Marmet, J., Pisanu, B. and Chapuis, J. L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. Journal of Animal Ecology 79, 538-547.
4. Caraco, T., Glavankov, S., Chen, G., Flaherty, J. E., Ohsumi, T. K. and Szymanksi, B. K. (2002). Stage-structured infection transmission and a spatial epidemic: A model for Lyme disease. American Naturalist 160, 348-359.
5. Crofton, H. (1971). A quantitative approach to parasitism. Parasitology 62, 179-193.
6. Daniels, T. J. and Fish, D. (1990). Spatial distribution and dispersal of unfed larval Ixodes dammini (Acari: Ixodidae) in southern New York. Environmental Entomology 19, 1029-1033.
7. Diekmann, O., Heesterbeek, J. A. P. and Metz, J. A. J. (1990). On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. Journal of Mathematical Biology 28, 365-382.
8. Dobson, A. P. and Merenlender, A. (1991). Coevolution of macroparasites and their hosts. In Parasite-host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), pp. 83-101. Oxford University Press, Oxford, UK
9. Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88-94.
10. Gallivan, G. and Horak, I. (1997). Body size and habitat as determinants of tick infestations of wild ungulates in South Africa. South African Journal of Wildlife Research 27, 63-70.
11. Gatewood, A. G., Liebman, K. A., Vourc'h, G., Bunikis, J., Hamer, S. A., Cortinas, R., Melton, F., Cislo, P., Kitron, U. and Tsao, J. (2009). Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Applied and Environmental Microbiology 75, 2476-2483.
12. Gern, L. and Rais, O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189-192.
13. Ghosh, M. and Pugliese, A. (2004). Seasonal population dynamics of ticks, and its influence on infection transmission: A semi-discrete approach. Bulletin of Mathematical Biology 66, 1659-1684.
14. Goodman, J. L., Dennis, D. T. and Sonenshine, D. E. (2005). Tick-borne diseases of humans. 1st Edn. American Society for Microbiology, Washington
15. Gray, J. S. (2002). Biology of Ixodes species ticks in relation to tick-borne zoonoses. Wiener klinische Wochenschrift 114, 473-478.
16. Harrison, A., Montgomery, W. I. and Bown, K. J. (2011). Investigating the persistence of tick-borne pathogens via the R0 model. Parasitology 138, 896-905.
17. Harrison, A., Scantlebury, M. and Montgomery, W. I. (2010). Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 9999.
18. Hartemink, N. A., Randolph, S. E., Davis, S. A. and Heesterbeek, J. A. P. (2008). The basic reproduction number for complex disease systems: Defining R0 for tick-borne infections. The American Naturalist 171, 743-754.
19. Hubálek, Z. and Halouzka, J. (1998). Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167-172.
20. Hudson, P. J., Norman, R., Laurenson, M. K., Newborn, D., Gaunt, M., Jones, L., Reid, H., Gould, E., Bowers, R., and Dobson, A. (1995). Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations. Parasitology 111, S49-S58.
21. Hughes, V. L. and Randolph, S. E. (2001). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: A force for aggregated distributions of parasites. Journal of Parasitology 87, 49-54.
22. 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.
23. Jongejan, F. and Uilenberg, G. (2004). The global importance of ticks. Parasitology 129, 3-14.
24. Koch, R. (1999). 80/20 Principle: The Secret to Success by Achieving More with Less. 1st Edn. Currency, New York, USA
25. 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.
26. Kurtenbach, K., Dizij, A., Seitz, H. M., Margos, G., Moter, S. E., Kramer, 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.
27. Labuda, M., Jones, L. D., Williams, T., Danielova, V. and Nuttall, P. A. (1993). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. Journal of Medical Entomology 30, 295-299.
28. Labuda, M., Kozuch, O. and Lys, J. (1997). Tickborne encephalitis virus natural foci in Slovakia: Ticks, rodents, and. . . goats. In 4th International Potsdam Symposium on Tick-borne Diseases: Tick-borne Encephalitis and Lyme borreliosis (ed. Suss, J. and Kahl, O.), pp. 21-22. Pabst Science Publishers, Lengerich, Germany
29. Mannelli, A., Bertolotti, L., Gern, L. and Gray, J. (2012). Ecology of Borrelia burgdorferi sensu lato in Europe: Transmission dynamics in multihost systems, influence of molecular processes and effects of climate change. FEMS Microbiology Reviews (in the Press
30. Norman, R., Bowers, R. G., Begon, M. and Hudson, P. J. (1999). Persistence of tick-borne virus in the presence of multiple host species: Tick reservoirs and parasite mediated competition. Journal of Theoretical Biology 200, 111-118.
31. Norman, R., Ross, D., Laurenson, M. K., and Hudson, P. J. (2004). The role of non-viraemic transmission on the persistence and dynamics of a tick borne virus-Louping ill in red grouse (Lagopus Lagopus scoticus) and mountain hares (Lepus timidus). Journal of Mathematical Biology 48, 119-134.
32. Ostfeld, R. S. and Keesing, F. (2000). Biodiversity and disease risk: The case of Lyme disease. Conservation Biology 14, 722-728.
33. Pal, U., De Silva, A. M., Montgomery, R. R., Fish, D., Anguita, J., Anderson, J. F., Lobet, Y. and Fikrig, E. (2000). Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. Journal of Clinical Investigation 106, 561-569.
34. Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909-917.
35. Randolph, S. E. (1977). Changing spatial relationships in a population of Apodemus sylvaticus with the onset of breeding. The Journal of Animal Ecology 46, 653-676.
36. Randolph, S. (1998). Ticks are not insects: Consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186-192.
37. Randolph, S. E. (2004). Tick ecology: Processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, 37-65.
38. Randolph, S. E. and Craine, N. G. (1995). General framework for comparative quantitative studies on transmission of tick-borne diseases using Lyme borreliosis in Europe as an example. Journal of Medical Entomology 32, 765-777.
39. Randolph, S. E., Gern, L. and Nuttall, P. A. (1996). Co-feeding ticks: Epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472-479.
40. Randolph, S. E., Miklisova, D., Lysy, J., Rogers, D. J. and Labuda, M. (1999). Incidence from coincidence: Patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177-186.
41. Randolph, S. E. and Rogers, D. J. (2000). Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. Proceedings of the Royal Society of London, B 267, 1741-1744.
42. Randolph, S. E. and Steele, G. M. (1985). An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari: Ixodidae). II. The dynamics of the tick-host interaction. Bulletin of Entomological Research 75, 501-518.
43. Rosá, R. and Pugliese, R. (2007). Effects of tick population dynamics and host densities on the persistence of tick-borne infections. Mathematical Biosciences 208, 216-240.
44. Rosá, R., Pugliese, R., Norman, R. and Hudson, P. J. (2003). Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. Journal of Theoretical Biology 224, 359-376.
45. Schmidt, K. A. and Ostfeld, R. S. (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82, 609-619.
46. Shaw, D. and Dobson, A. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: A quantitative review. Parasitology 111, 111-133.
47. Telford III, S. R., Cunningham, J. A., Waltari, E. and Hu, L. (2011). Nest box-deployed bait for delivering oral vaccines to white-footed mice. Ticks and Tick-borne Diseases 2, 151-155.
48. Tsao, J. I., Wootton, J. T., Bunikis, J., Luna, M. G., Fish, D. and Barbour, A. G. (2004). An ecological approach to preventing human infection: Vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences, USA 101, 18159- 18164.
49. Wilson, K., Bjørnstad, O., Dobson, A., Merler, S., Poglayen, G., Randolph, S., Read, A., Skorping, A., Hudson, P. and Rizzoli, A. (2002). Heterogeneities in macroparasite infections: Patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6-44. Oxford University Press, Oxford, UK.
50. Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J., Garnett, G., Hagan, P., Hii, J., Ndhlovu, P. and Quinnell, R. (1997). Heterogeneities in the transmission of infectious agents: Implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338-342.