Wild Birds as Sentinels for Multiple Zoonotic Pathogens Along an Urban to Rural Gradient in Greater Chicago, Illinois

Zoonoses and Public Health

Volumn 59, Issue 5, 2012, Pages 355-364

  Hamer, S A ^a   Lehrer, E ^b   Magle, S B ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Urban Wildlife Institute   (United States)

Author keywords

Borrelia burgdorferi; Salmonella; Urbanization; West nile virus; Wild birds; Zoonoses

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIRD; BLOOD ANALYSIS; BLOOD SAMPLING; BORRELIA; CONTROLLED STUDY; DIAGNOSTIC TEST; ECTOPARASITE; FECES ANALYSIS; IXODES SCAPULARIS; NONHUMAN; PARASITE EXAMINATION; PRIORITY JOURNAL; RISK FACTOR; RURAL AREA; SALMONELLA ENTERICA; TICK BORNE FLAVIVIRUS; UNITED STATES; URBAN AREA; WEST NILE FLAVIVIRUS; WILD BIRD; ZOONOSIS;

ANIMALS; ANIMALS, WILD; BIRD DISEASES; BIRDS; CHICAGO; DISEASE RESERVOIRS; HUMANS; IXODES; LYME DISEASE; RISK FACTORS; SALMONELLA INFECTIONS, ANIMAL; SENTINEL SURVEILLANCE; URBANIZATION; WEST NILE FEVER; WEST NILE VIRUS; ZOONOSES;

AVES; BORRELIA BURGDORFERI; IXODES SCAPULARIS; IXODIDA; SALMONELLA; SALMONELLA ENTERICA; WEST NILE VIRUS;

EID: 84864050906     PISSN: 18631959     EISSN: 18632378     Source Type: Journal    
DOI: 10.1111/j.1863-2378.2012.01462.x     Document Type: Article

References (56)

1. Allan, B. F., F. Keesing, and R. S. Ostfeld, 2003: Effect of forest fragmentation on Lyme disease risk. Conserv. Biol. 17, 267-272.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, 1990: Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Anderson, J. R., E. E. Hardy, J. T. Roach, and R. E. Witmer. 1976: A land use and land cover classification system for use with remote sensor data. In Geological Survey Professional Paper 964. United States Government Printing Office, Washington, DC.
4. AOU (ed.), 2011: Check-list of North American Birds.
5. Benskin, C. M. H., K. Wilson, K. Jones, and I. R. Hartley, 2009: Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol. Rev. Camb. Philos. Soc. 84, 349-373.
6. Beran, G. W., 2008: Disease and destiny - mystery and mastery. Prev. Vet. Med. 86, 198-207.
7. Blitvich, B. J., N. L. Marlenee, R. A. Hall, C. H. Calisher, R. A. Bowen, J. T. Roehrig, N. Komar, S. A. Langevin, and B. J. Beaty, 2003: Epitope-blocking enzyme-linked immunosorbent assays for the detection of serum antibodies to west nile virus in multiple avian species. J. Clin. Microbiol. 41, 1041-1047.
8. Bowden, S. E., K. Magori, and J. M. Drake, 2011: Regional differences in the association between land cover and West Nile virus disease incidence in humans in the United States. Am. J. Trop. Med. Hyg. 84, 234-238.
9. Bradley, C. A., and S. Altizer, 2007: Urbanization and the ecology of wildlife diseases. Trends Ecol. Evol. 22, 95-102.
10. Bradley, C. A., S. E. Gibbs, and S. Altizer, 2008: Urban land use predicts West Nile virus exposure in songbirds. Ecol. Appl. 18, 1083-1092.
11. Brittingham, M. C., S. A. Temple, and R. M. Duncan, 1988: A survey of the prevalence of selected bacteria in wild birds. J. Wildl. Dis. 24, 299-307.
12. Campos, P. C., L. M. Barros, J. O. Campos, V. B. Braga, I. M. Cazorla, G. R. Albuquerque, and S. M. S. Carvalho, 2008: Zoonotic parasites in dog feces at public squares in the municipality of Itabuna, Bahia, Brazil. Rev. Bras. Parasitol. Vet. 17, 206-209.
13. Cízek, A., I. Literák, K. Hejlíćek, F. Treml, and J. Smola, 1994: Salmonella contamination of the environment and its incidence in wild birds. Journal of Veterinary Medicine, Series B. 41, 320-327.
14. Cooper, J. E., 1990: Birds and zoonoses. Ibis 132, 181-191.
15. Daniels, T. J., G. R. Battaly, D. Liveris, R. C. Falco, and I. Schwartz, 2002: Avian reservoirs of the agent of human granulocytic ehrlichiosis? Emerg. Infect. Dis. 8, 1524-1525.
16. Daoust, P. Y., and J. F. Prescott, 2007: Salmonellosis. In: Thomas, N. J., D. B. Hunter, and C. T. Atkinson (eds), Infectious diseases of wild birds, 270-288. Blackwell, Ames, Iowa.
17. Dobson, A., 2004: Population dynamics of pathogens with multiple host species. Amer. Nat. 164, S64-S78.
18. Durden, L. A., and J. E. Keirans, 1996: Nymphs of the Genus Ixodes (Acari: Ixodidae) of the United States: Taxonomy, Identification Key, Distribution, Hosts, and Medical/Veterinary Importance. Thomas Say Publications in Entomology, Entomological Society of America, Lanham, MD.
19. Estrada-Pena, A., P. Acevedo, F. Ruiz-Fons, C. Gortazar, and J. de la Fuente, 2008: Evidence of the importance of host habitat use in predicting the dilution effect of wild boar for deer exposure to Anaplasma spp. PLoS One 3, e2999.
20. Gaertner, J. P., D. Hahn, F. L. Rose, and M. R. Forstner, 2008: Detection of salmonellae in different turtle species within a headwater spring ecosystem. J. Wildl. Dis. 44, 519-526.
21. Geery, P. R., and R. E. Holub, 1989: Seasonal abundance and control of Culex spp. in catch basins in Illinois. J. Am. Mosq. Control Assoc. 5, 537-540.
22. Giardina, A. R., K. A. Schmidt, E. M. Schauber, and R. S. Ostfeld, 2000: Modeling the role of songbirds and rodents in the ecology of Lyme disease. Can. J. Zool. 78, 2184-2197.
23. Gomez, A., A. M. Kilpatrick, L. D. Kramer, A. P. Dupuis II, J. G. Maffei, S. J. Goetz, P. P. Marra, P. Daszak, and A. A. Aguirre, 2008: Land use and West Nile virus seroprevalence in wild mammals. Emerg. Infect. Dis. 14, 962-965.
24. Gyure, K. A., 2009: West Nile virus infections. J. Neuropathol. Exp. Neurol. 68, 1053-1060.
25. Hamer, G. L., E. D. Walker, J. D. Brawn, S. R. Loss, M. O. Ruiz, T. L. Goldberg, A. M. Schotthoefer, W. M. Brown, E. Wheeler, and U. D. Kitron, 2008: Rapid amplification of West Nile virus: the role of hatch-year birds. Vector Borne Zoonotic Dis. 8, 57-67.
26. 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.
27. Hamer, G. L., L. F. Chaves, T. K. Anderson, U. D. Kitron, J. D. Brawn, M. O. Ruiz, S. R. Loss, E. D. Walker, and T. L. Goldberg, 2011a: Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission. PLoS One 6, e23767.
28. Hamer, S. A., G. J. Hickling, J. L. Sidge, M. E. Rosen, E. D. Walker, and J. I. Tsao, 2011b: Diverse Borrelia burgdorferi strains in a bird-tick cryptic cycle. Appl. Environ. Microbiol. 77, 1999-2007.
29. Holden, K., J. T. Boothby, S. Anand, and R. F. Massung, 2003: Detection of Borrelia burgdorferi, Ehrlichia chaffeensis, and Anaplasma phagocytophilum in ticks (Acari: Ixodidae) from a coastal region of California. J. Med. Entomol. 40, 534-539.
30. IDPH, 2011: Reportable Communicable Disease Cases, 2000-2009. Illinois Department of Public Health, Springfield.
31. Jobe, D. A., S. D. Lovrich, J. A. Nelson, T. C. Velat, C. Anchor, T. Koeune, and S. A. Martin, 2006: Borrelia burgdorferi in Ixodes scapularis ticks, Chicago area. Emerg. Infect. Dis. 12, 1039-1041.
32. Jobe, D. A., J. A. Nelson, M. D. Adam, and S. A. Martin, 2007: Lyme disease in urban areas, Chicago. Emerg. Infect. Dis. 13, 1799-1800.
33. Jones, D. N., and S. James Reynolds, 2008: Feeding birds in our towns and cities: a global research opportunity. J. Avian Biol. 39, 265-271.
34. Lanciotti, R. S., A. J. Kerst, R. S. Nasci, M. S. Godsey, C. J. Mitchell, H. M. Savage, N. Komar, N. A. Panella, B. C. Allen, K. E. Volpe, B. S. Davis, and J. T. Roehrig, 2000: Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J. Clin. Microbiol. 38, 4066-4071.
35. LoGiudice, K., R. S. Ostfeld, K. A. Schmidt, and F. Keesing, 2003: The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc. Natl. Acad. Sci. U S A 100, 567-571.
36. Loss, S. R., G. L. Hamer, E. D. Walker, M. O. Ruiz, T. L. Goldberg, U. D. Kitron, and J. D. Brawn, 2009: Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecol. 159, 415-424.
37. Makita, K., E. M. Fèvre, C. Waiswa, W. Kaboyo, B. M. De Clare Bronsvoort, M. C. Eisler, and S. C. Welburn, 2008: Human brucellosis in urban and peri-urban areas of Kampala, Uganda. Ann. N. Y. Acad. Sci. 1149, 309-311.
38. McKinney, M. L., 2002: Urbanization, biodiversity, and conservation. Bioscience 52, 883-890.
39. Medley, K. E., M. J. McDonnell, and S. T. A. Pickett, 1995: Forest-landscape structure along an urban-to-rural gradient. Prof. Geogr. 47, 159-168.
40. Nasci, R. S., K. L. Gottfried, K. L. Burkhalter, V. L. Kulasekera, A. J. Lambert, R. S. Lanciotti, A. R. Hunt, and J. R. Ryan, 2002: Comparison of Vero cell plaque assay, TaqMan reverse transcriptase polymerase chain reaction RNA assay, and VecTest antigen assay for detection of West Nile virus in field-collected mosquitoes. J. Am. Mosq. Control Assoc. 18, 294-300.
41. Ogden, N. H., and J. I. Tsao, 2009: Biodiversity and Lyme disease: dilution or amplification? Epidemics 1, 196-206.
42. Ostfeld, R., and F. Keesing, 2000: The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can. J. Zool. 78, 2061-2078.
43. Rahn, K., S. A. De Grandis, R. C. Clarke, S. A. McEwen, J. E. Galan, C. Ginocchio, R. Curtiss III, and C. L. Gyles, 1992: Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Mol. Cell. Probes 6, 271-279.
44. Reed, K. D., J. K. Meece, J. S. Henkel, and S. K. Shukla, 2003: Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clin. Med. Res. 1, 5-12.
45. Ringia, A. M., B. J. Blitvich, H. Y. Koo, M. Van de Wyngaerde, J. D. Brawn, and R. J. Novak, 2004: Antibody prevalence of West Nile virus in birds, Illinois, 2002. Emerg. Infect. Dis. 10, 1120-1124.
46. Ruiz, M. O., L. F. Chaves, G. L. Hamer, T. Sun, W. M. Brown, E. D. Walker, L. Haramis, T. L. Goldberg, and U. D. Kitron, 2010: Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit. Vectors 3, 19.
47. Schmidt, K. A., and R. S. Ostfeld, 2001: Biodiversity and the dilution effect in disease ecology. Ecology 82, 609-619.
48. Simpson, J. E., P. J. Hurtado, J. Medlock, G. Molaei, T. G. Andreadis, A. P. Galvani, and M. A. Diuk-Wasser, 2012: Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system. Proc. Biol. Sci. 279, 925-933.
49. Skoracki, M., J. Michalik, B. Skotarczak, A. Rymaszewska, B. Sikora, T. Hofman, B. Wodecka, and M. Sawczuk, 2006: First detection of Anaplasma phagocytophilum in quill mites (Acari: Syringophilidae) parasitizing passerine birds. Microbes Infect. 8, 303-307.
50. Sonenshine, D. E., 1979: Ticks of Virginia, pp. 42. Virginia Polytechnic Institute and State University, College of Agriculture and Life Sciences, Blacksburg, VA.
51. Soriano, S. V., N. B. Pierangeli, I. Roccia, H. F. J. Bergagna, L. E. Lazzarini, A. Celescinco, M. S. Saiz, A. Kossman, P. A. Contreras, C. Arias, and J. A. Basualdo, 2010: A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquen, Patagonia, Argentina. Vet. Parasitol. 167, 81-85.
52. Swaddle, J. P., and S. E. Calos, 2008: Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS One 3, e2488.
53. Taylor, L. H., S. M. Latham, and M. E. Woolhouse, 2001: Risk factors for human disease emergence. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356, 983-989.
54. Tsao, J. I., J. T. Wootton, J. Bunikis, M. G. Luna, D. Fish, and A. G. Barbour, 2004: An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc. Natl. Acad. Sci. U S A 101, 18159-18164.
55. Weaver, S. C., and W. K. Reisen, 2010: Present and future arboviral threats. Antiviral Res. 85, 328-345.
56. Williams, M. C., 1957: Birds in relation to the arthropod-borne virus zoonoses. Ibis 99, 303-306.