Harvested white-tailed deer as sentinel hosts for early establishing ixodes scapularis populations and risk from vector-borne zoonoses in Southeastern Canada

Journal of Medical Entomology

Volumn 50, Issue 2, 2013, Pages 384-393

  Bouchard, C ^a   Leighton, P A ^a   Beauchamp, G ^a   Nguon, S ^b   Trudel, L ^b   Milord, F ^b   Lindsay, L R ^c   Belanger D ^a   Ogden, N H ^a,d  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b INSTITUT NATIONAL DE SANTÉ PUBLIQUE DU QUÉBEC   (Canada)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

Anaplasma phagocytophilum; Borrelia burgdorferi; environmental factor; Ixodes scapularis; white tailed deer

Indexed keywords

BACTERIAL RNA; MSP2 PROTEIN, ANAPLASMA PHAGOCYTOPHILUM; OUTER MEMBRANE PROTEIN; RNA 23S;

AGE; ANAPLASMA PHAGOCYTOPHILUM; ANIMAL; ANIMAL DISEASE; ARTICLE; BABESIA MICROTI; BORRELIA BURGDORFERI; CANADA; CLIMATE; DEER; DISEASE TRANSMISSION; DNA SEQUENCE; ECOSYSTEM; EVALUATION; FEMALE; HEALTH SURVEY; HUMAN; ISOLATION AND PURIFICATION; IXODES; MALE; METHODOLOGY; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; SENTINEL SURVEILLANCE; SEX DIFFERENCE; TICK INFESTATION; ZOONOSIS;

AGE FACTORS; ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; BABESIA MICROTI; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; CLIMATE; DEER; ECOSYSTEM; FEMALE; HUMANS; IXODES; MALE; POLYMERASE CHAIN REACTION; POPULATION SURVEILLANCE; QUEBEC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, RIBOSOMAL, 23S; SENTINEL SURVEILLANCE; SEQUENCE ANALYSIS, DNA; SEX FACTORS; TICK INFESTATIONS; ZOONOSES;

EID: 84874868761     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12093     Document Type: Article

References (49)

1. Anderson, D. R., and K. P. Burnham. 2002. Avoiding pitfalls when using information-theoretic methods. J. Wildl. Manage. 66: 912-918.
2. Bouchard, C., G. Beauchamp, S. Nguon, L. Trudel, F. Milord, L. R. Lindsay, D. Belanger, and N. H. Ogden. 2011. Associations between Ixodes scapularis ticks and small mammal hosts in a newly endemic zone in southeastern Canada: Implications for Borrelia burgdorferi transmission. Ticks Tick Borne Dis. 2: 183-190.
3. Cortinas, M. 2007. Investigations of white-tailed deer infestation by Ixodes scapularis on the Illinois River, USA. University of Illinois, Champaign-Urbana, IL.
4. Courtney, J. W., L. M. Kostelnik, N. S. Zeidner, and R. F. Massung. 2004. Multiplex real-timePCRfor detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J. Clin. Microbiol. 42: 3164-3168.
5. De la Fuente, J., R. F. Massung, S. J. Wong, F. K. Chu, H. Lutz, M. Meli, F. D. von Loewenich, A. Grzeszczuk, A. Torina, S. Caracappa, et al. 2005. Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. J. Clin. Microbiol. 43: 1309-1317.
6. Dohoo, I., W. Martin, and H. Stryhn. 2003. Veterinary epidemiologic research. AVC Inc., Charlottetown, PEI, Canada.
7. Dormann, C. F., J. M. McPherson, M. B. Araujo, R. Bivand, J. Bolliger, G. Carl, R. G. Davies, A. Hirzel, W. Jetz, W. D. Kissling, et al. 2007. Methods to account for spatial autocorrelation in the analysis of species distributional data: A review. Ecography 30: 609-628.
8. Dugan, V. G., M. J. Yabsley, C. M. Tate, D. G. Mead, U. G. Munderloh, M. J. Herron, D. E. Stallknecht, S. E. Little, and W. R. Davidson. 2006. Evaluation of white-tailed deer (Odocoileus virginianus) as natural sentinels for Anaplasma phagocytophilum. Vector Borne Zoonotic Dis. 6: 192-207.
9. Estrada-Pena, A. 2001. Forecasting habitat suitability for ticks and prevention of tick-borne diseases. Vet. Parasitol. 98: 111-132.
10. Ginsberg, H. S., and E. Zhioua. 1999. Influence of deer abundance on the abundance of questing adult Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 36: 376-381.
11. Hamer, S. A., J. I. Tsao, E. D. Walker, and G. J. Hickling. 2010. Invasion of the Lyme disease vector Ixodes scapularis: Implications for Borrelia burgdorferi endemicity. Ecohealth 7: 47-63.
12. Katavolos, P., P. M. Armstrong, J. E. Dawson, and S. R. Telford. 1998. Duration of tick attachment required for transmission of granulocytic ehrlichiosis. J. Infect. Dis. 177: 1422-1425.
13. Keefe, L. M., M. H. Moro, J. Vinasco, C. Hill, C. C. Wu, and E. A. Raizman. 2009. The use of harvested white-tailed deer (Odocoileus virginianus) and geographic information system (GIS) Methods to characterize distribution and locate spatial clusters of Borrelia burgdorferi and its vector Ixodes scapularis in Indiana. Vector Borne Zoonotic Dis. 9: 671-680.
14. Kitron, U., C. J. Jones, J. K. Bouseman, J. A. Nelson, and D. L. Baumgartner. 1992. Spatial analysis of the distribution of Ixodes dammini (Acari, Ixodidae) on white-tailed deer in Ogle County, Illinois. J. Med. Entomol. 29: 259-266.
15. Koffi, J. K., P. A. Leighton, Y. Pelcat, L. Trudel, L. R. Lindsay, F. Milord, and N. H. Ogden. 2012. Passive surveillance for I. scapularis ticks: Enhanced analysis for early detection of emerging Lyme disease risk. J. Med. Entomol. 49: 400-409.
16. Lacombe, E., P. W. Rand, and R. P. Smith. 1993. Disparity of Borrelia burgdorferi infection rates of adult Ixodes dammini on deer and vegetation. J. Infect. Dis. 167: 1236-1238.
17. Legendre, L., and P. Legendre. 1983. Numerical ecology. Elsevier Scientific Publ. Co., New York.
18. Leighton, P. A., J. K. Koffi, Y. Pelcat, L. R. Lindsay and N. H. Ogden. 2012. Predicting the speed of tick invasion: An empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J. Appl. Ecol. 49: 457-464.
19. Lesage, L., M. Crete, J. Huot, A. Dumont, and J. P. Ouellet. 2000. Seasonal home range size and philopatry in two northern white-tailed deer populations. Can. J. Zool. 78: 1930-1940.
20. Lindsay, L. R., S. W. Mathison, I. K. Barker, S. A. Mcewen, T. J. Gillespie, and G. A. Surgeoner. 1999. Microclimate and habitat in relation to Ixodes scapularis (Acari: Ixodidae) populations on Long Point, Ontario, Canada. J. Med. Entomol. 36: 255-262.
21. Loken, K. I., C. C. Wu, R. C. Johnson, and R. F. Bey. 1985. Isolation of the Lyme disease spirochete from mammals in Minnesota. Proc. Soc. Exp. Biol. Med. 179: 300-302.
22. Magnarelli, L. A., J. F. Anderson, and M. L. Cartter. 1993. Geographic distribution of white-tailed deer with ticks and antibodies to Borrelia burgdorferi in Connecticut. Yale J. Biol. Med. 66: 19-26.
23. Magnarelli, L. A., A. Denicola, K. C. Stafford, and J. F. Anderson. 1995. Borrelia burgdorferi in an urban environment-white-tailed deer with infected ticks and antibodies. J. Clin. Microbiol. 33: 541-544.
24. Massung, R. F., J. W. Courtney, S. L. Hiratzka, V. E. Pitzer, G. Smith, and R. L. Dryden. 2005. Anaplasma phagocytophilum in white-tailed deer. Emerg. Infect. Dis. 11: 1604-1606.
25. Massung, R. F., K. Lee, M. Mauel, and A. Gusa. 2002. Characterization of the rRNA genes of Ehrlichia chaffeensis and Anaplasma phagocytophila. DNA Cell Biol. 21: 587-596.
26. Massung, R. F., M. J. Mauel, J. H. Owens, N. Allan, J. W. Courtney, K. C. Stafford, and T. N. Mather. 2002. Genetic variants of Ehrlichia phagocytophila, Rhode Island and Connecticut. Emerg. Infect. Dis. 8: 467-472.
27. Nakajima, R., M. Tsuji, K. Oda, A. Zamoto-Niikura, Q. Wei, T. Kawabuchi-Kurata, A. Nishida, and C. Ishihara. 2009. Babesia microti-group parasites compared phylogenetically by complete sequencing of the CCT eta gene in 36 isolates. J. Vet. Med. Sci. 71: 55-68.
28. Nelson, M. E. and L. D. Mech. 1981. Deer social organization and wolf predation in northeastern Minnesota. Wildl. Monogr. 77: 1-53.
29. Nelson, M. E., and L. D. Mech. 1984. Home range formation and dispersal of deer in northeastern Minnesota. J. Mammal. 65: 567-575.
30. Ogden, N. H., I. K. Barker, G. Beauchamp, S. Brazeau, D. F. Charron, A. Maarouf, M. G. Morshed, C. J. O'Callaghan, R. A. Thompson, D. Waltner-Toews, et al. 2006. Investigation of ground level and remote-sensed data for habitat classification and prediction of survival of Ixodes scapularis in habitats of southeastern Canada. J. of Medical Entomology. 43: 403-414.
31. Ogden, N. H., M. Bigras-Poulin, C. J. O'Callaghan, I. K. Barker, L. R. Lindsay, A. Maarouf, K. E. Smoyer-Tomic, D. Waltner-Toews, and D. Charron. 2005. A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. Int. J. Parasitol. 35: 375-389.
32. Ogden, N. H., C. Bouchard, K. Kurtenbach, G. Margos, L. R. Lindsay, L. Trudel, S. Nguon, and F. Milord. 2010. Active and passive surveillance and phylogenetic analysis of Borrelia burgdorferi elucidate the process of Lyme disease risk emergence in Canada. Environ. Health Perspect. 118: 909-914.
33. Ogden, N. H., L. R. Lindsay, M. Morshed, P. N. Sockett, and H. Artsob. 2009. The emergence of Lyme disease in Canada. Can. Med. Assoc. J. 180: 1221-1224.
34. Ogden, N. H., R. L. Lindsay, K. Hanincova, I. K. Barker, M. Bigras-Poulin, D. F. Charron, A. Heagy, C. A. Francis, C. J. O'Callaghan, I. Schwartz, and R. A. Thompson. 2008. Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl. Environ. Microbiol. 74: 1780-1790.
35. Ogden, N. H., L. Trudel, H. Artsob, I. K. Barker, G. Beauchamp, D. F. Charron, M. A. Drebot, T. D. Galloway, R. O'Handley, R. A. Thompson, et al. 2006. Ixodes scapularis ticks collected by passive surveillance in Canada: Analysis of geographic distribution and infection with Lyme Borreliosis agent Borrelia burgdorferi. J. Med. Entomol. 43: 600-609.
36. Piesman, J., and A. Spielman. 1979. Host associations and seasonal abundance of immature Ixodes dammini (Acarina, Ixodidae) in southeastern Massachusetts. Ann. Entomol. Soc. Am. 72: 829-832.
37. Piesman, J., A. Spielman, P. Etkind, T. K. Ruebush, and D. D. Juranek. 1979. Role of deer in the epizootiology of Babesia microti in Massachusetts, USA. J. Med. Entomol. 15: 537-540.
38. Quinn, G. P., and M. J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, United Kingdom.
39. Rand, P. W., C. Lubelczyk, G. R. Lavigne, S. Elias, M. S. Holman, E. H. Lacombe, and R. P. Smith. 2003. Deer density and the abundance of Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 40: 179-184.
40. Randolph, S. E. 2004. Tick ecology: Processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129: S37-S65.
41. Steiner, F. E., R. R. Pinger, C. N. Vann, M. J. Abley, B. Sullivan, N. Grindle, K. Clay, and C. Fuqua. 2006. Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari: Ixodidae) collected in Indiana. J. Med. Entomol. 43: 437-442.
42. Tate, C. M., D. G. Mead, M. P. Luttrell, E. W. Howerth, V. G. Dugan, U. G. Munderloh, and W. R. Davidson. 2005. Experimental infection of white-tailed deer with Anaplasma phagocytophilum, etiologic agent of human granulocytic anaplasmosis. J. Clin. Microbiol. 43: 3595-3601.
43. Telford, S. R., T. N. Mather, S. I. Moore, M. L. Wilson, and A. Spielman. 1988. Incompetence of deer as reservoirs of the Lyme disease spirochete. Am. J. Trop. Med. Hyg. 39: 105-109.
44. Thompson, C., A. Spielman, and P. J. Krause. 2001. Coinfecting deer-associated zoonoses: Lyme disease, babesiosis, and ehrlichiosis. Clin. Infect. Dis. 33: 676-685.
45. Tsao, J. I. 2009. Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Vet. Res. 40: 36.
46. Watson, T. G., and R. C. Anderson. 1976. Ixodes scapularis Say on white-tailed deer (Odocoileus virginianus) from Long Point, Ontario. J. Wildl. Dis. 12: 66-71.
47. Wilson, M. L., A. M. Ducey, T. S. Litwin, T. A. Gavin, and A. Spielman. 1990. Microgeographic distribution of immature Ixodes dammini ticks correlated with that of deer. Med. Vet. Entomol. 4: 151-159.
48. Wilson, M. L., S. R. Telford, III, J. Piesman, and A. Spielman. 1988. Reduced abundance of immature Ixodes dammini (Acari: Ixodidae) following elimination of deer. J. Med. Entomol. 25: 224-228.
49. Zuur, A. F. 2009. Mixed effects models and extensions in ecology with R. Springer, New York.