What is the risk for exposure to vector-borne pathogens in United States national parks?

Journal of Medical Entomology

Volumn 50, Issue 2, 2013, Pages 221-230

  Eisen, Lars ^a   Wong, David ^b   Shelus, Victoria ^b,c   Eisen, Rebecca J ^d  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b NATIONAL PARK SERVICE   (United States)

^c DUKE UNIVERSITY   (United States)

^d NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

flea; mosquito; national park; tick; vector borne disease

Indexed keywords

ANIMAL; BACTERIAL INFECTION; DISEASE CARRIER; DISEASE TRANSMISSION; HEALTH SURVEY; HUMAN; METHODOLOGY; MICROBIOLOGY; PARASITE VECTOR; PARASITOLOGY; PARASITOSIS; PHYSIOLOGY; REVIEW; RISK ASSESSMENT; UNITED STATES; VIROLOGY; VIRUS INFECTION;

ANIMALS; ARACHNID VECTORS; BACTERIAL INFECTIONS; HUMANS; INSECT VECTORS; PARASITIC DISEASES; POPULATION SURVEILLANCE; RISK ASSESSMENT; UNITED STATES; VIRUS DISEASES;

EID: 84874873530     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12228     Document Type: Review

References (86)

1. Adjemian, J., I. B. Weber, J. McQuiston, K. S. Griffith, P. S. Mead, W. Nicholson, A. Roche, M. Schriefer, M. Fischer, O. Kosoy, et al. 2012. Zoonotic infections among employees from Great Smoky Mountains and Rocky Mountain National Parks, 2008-2009. Vector-Borne Zoon. Dis. 12: 922-931.
2. Aguirre, A. A., D. E. Hansen, E. E. Starkey, and R. G. McLean. 1995. Serologic survey of wild cervids for potential disease agents in selected national parks in the United States. Prev. Vet. Med. 21: 313-322.
3. Aruch, S., C. T. Atkinson, A. F. Savage, and D. A. LaPointe. 2007. Prevalence and distribution of pox-like lesions, avian malaria, and mosquito vectors in Kipahulu Valley, Haleakala National Park, HawaiÕi, USA. J. Wildl. Dis. 43: 567-575.
4. Barbour, A. G. 2005. Relapsing fever, pp. 268-291. In J. L. Goodman, D. T. Dennis, and D. E. Sonenshine (eds.), Tick-Borne Diseases of Humans.ASMPress, Washington, DC.
5. Barnard, D. R., U. R. Bernier, K. H. Posey, and R. D. Xue. 2002. Repellency of IR3535, KBR3023, para-menthane-3,8-diol, and DEET to black salt marsh mosquitoes (Diptera: Culicidae) in the Everglades National Park. J. Med. Entomol. 39: 895-899.
6. Barnes, A. M. 1982. Surveillance and control of bubonic plague in the United States. Symp. Zool. Soc. Lond. 50: 237-270.
7. Beck, D. E. 1966. Siphonaptera (fleas) of Mesa Verde National Park, Montezuma, Colorado. Great Basin Nat. 26: 76-78.
8. Biek, R., T. K. Ruth, K. M. Murphy, C. R. Anderson, M. Johnson, R. DeSimone, R. Gray, M. G. Hornocker, C. M. Gillin, and M. Poss. 2006. Factors associated with pathogen seroprevalence and infection in Rocky Mountain cougars. J. Wildl. Dis. 42: 606-615.
9. Bowen, G. S., R. G. McLean, R. B. Shriner, D. B. Francy, K. S. Pokorny, J. M. Trimble, R. A. Bolin, A. M. Barnes, C. H. Calisher, and D. J. Muth. 1981. The ecology of Colorado tick fever in Rocky Mountain National Park in 1974. II. Infection in small mammals. Am. J. Trop. Med. Hyg. 30: 490-496.
10. Boyer, K. M., R. S. Munford, G. O. Maupin, C. P. Pattison, M. D. Fox, A. M. Barnes, W. L. Jones, and J. E. Maynard. 1977. Tick-borne relapsing fever: An interstate outbreak originating at Grand Canyon National Park. Am. J. Epidemiol. 105: 469-479.
11. Brown, R. T., R. S. Lane, and D. T. Dennis. 2005. Geographic distributions of tick-borne diseases and their vectors, pp. 363-391. In J. L. Goodman, D. T. Dennis, and D. E. Sonenshine (eds.), Tick-Borne Diseases of Humans. ASM Press, Washington, DC.
12. Carey, A. B., R. G. McLean, and G. O. Maupin. 1980. The structure of a Colorado tick fever ecosystem. Ecol. Monogr. 50: 131-151.
13. CDC) United States Centers for Disease Control and Prevention. 1973. Relapsing fever -Georgia, Arizona. Morb. Mort. Wkly. Rep. 22: 242,247.
14. CDC) United States Centers for Disease Control and Prevention. 1991. Outbreak of relapsing fever -Grand Canyon National Park, Arizona, 1990. Morb. Mort. Wkly. Rep. 40: 296-297,303.
15. Childs, J. E., and C. D. Paddock. 2003. The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu. Rev. Entomol. 48: 307-337.
16. Clover, J. R., and R. S. Lane. 1995. Evidence implicating nymphal Ixodes pacificus (Acari: Ixodidae) in the epidemiology of Lyme disease in California. Am. J. Trop. Med. Hyg. 53: 237-240.
17. Conrad, P. A., A. M. Kjemtrup, R. A. Carreno, J. Thomford, K. Wainwright, M. Eberhard, R. Quick, S. R. Telford, and B. L. Herwaldt. 2006. Description of Babesia duncani n.sp. (Apicomplexa: Babesiidae) from humans and its differentiation from other piroplasms. Int. J. Parasitol. 36: 779-789.
18. Darsie, Jr., R F., and R. A. Ward. 2005. Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico. University Press of Florida, Gainesville, FL.
19. Dennis, D. T., T. S. Nekomoto, J. C. Victor, W. S. Paul, and J. Piesman. 1998. Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the United States. J. Med. Entomol. 35: 629-638.
20. Dworkin, M. S., P. C. Shoemaker, and D. E. Anderson. 1999. Tick paralysis: 33humancases in Washington State, 1946-1996. Clin. Infect. Dis. 29: 1435-1439.
21. Dworkin, M. S., P. C. Shoemaker, C. L. Fritz, M. E. Dowell, and D. E. Anderson. 2002. The epidemiology of tickborne relapsing fever in the United States. Am. J. Trop. Med. Hyg. 66: 753-758.
22. Eads, R. B., and E. G. Campos. 1983. Deer mouse, Peromyscus maniculatus, and associated rodent fleas (Siphonaptera) in the arctic-alpine life zone of Rocky Mountain National Park, Colorado. Great Basin Nat. 43: 168-174.
23. Ebel, G. D. 2010. Update on Powassan virus: Emergence of a North American tick-borne flavivirus. Annu. Rev. Entomol. 55: 95-110.
24. Eisen, L. 2007. A call for renewed research on tick-borne Francisella tularensis in the Arkansas-Missouri primary national focus of tularemia in humans. J. Med. Entomol. 44: 389-397.
25. Eisen, L., and R. J. Eisen. 2007. Need for improved methods to collect and present spatial epidemiologic data for vectorborne diseases. Emerg. Infect. Dis. 13: 1816-1820.
26. Eisen, L., and R. J. Eisen. 2011. Using geographic information systems and decision support systems for the pre-diction, prevention, and control of vector-borne diseases. Annu. Rev. Entomol. 56: 41-61.
27. Eisen, L., L. A. Ibarra-Juarez, R. J. Eisen, and J. Piesman. 2008. Indicators for elevated risk of human exposure to host-seeking adults of the Rocky Mountain wood tick (Dermacentor andersoni) in Colorado. J. Vector Ecol. 33: 117-128.
28. Eisen, R. J., and L. Eisen. 2008. Spatial modeling of human risk of exposure to vector-borne pathogens based on epidemiological versus arthropod vector data. J. Med. Entomol. 45: 181-192.
29. Eisen, R. J., S. W. Bearden, A. P. Wilder, J. A. Montenieri, M. F. Antolin, and K. L. Gage. 2006. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc. Natl. Acad. Sci. U.S.A. 103: 15380-15385.
30. Eisen, R. J., L. Eisen, and K. L. Gage. 2009. Studies of vector competency and efficiency of North American fleas for Yersinia pestis: State of the field and future research needs. J. Med. Entomol. 46: 737-744.
31. Eisen, R. J., J. Piesman, E. Zielinski-Gutierrez, and L. Eisen. 2012. What do we need to know about disease ecology to prevent Lyme disease in the Northeastern United States? J. Med. Entomol. 49: 11-22.
32. Eskey, C. R., and V. H. Haas. 1940. Plague in the western part of the United States. Public Health Bull. 254: 1-83.
33. Fleer, K. A., P. Foley, L. Calder, and J. E. Foley. 2011. Arthropod vectors and vector-borne bacterial pathogens in Yosemite National Park. J. Med. Entomol. 48: 101-110.
34. Foley, J. E., J. E. Barlough, R. B. Kimsey, J. E. Madigan, E. DeRock, and A. Poland. 1998. Ehrlichia spp. in cervids from California. J. Wildl. Dis. 34: 731-737.
35. Foley, J. E., P. Foley, R. N. Brown, R. S. Lane, J. S. Dumler, and J. E. Madigan. 2004. Ecology of Anaplasma phagocytophilum and Borrelia burgdorferi in the western United States. J. Vector Ecol. 29: 41-50.
36. Gage, K. L. 1999. Plague surveillance, pp. 135-165. In Plague Manual: Epidemiology, Distribution, Surveillance, and Control. World Health Organization, Geneva, Switzerland.
37. Gage, K L., J. A. Montenieri, and R. E. Thomas. 1994. The role of predators in the ecology, epidemiology, and surveillance of plague in the United States, pp. 200-206.
38. Gese, E. M., R. D. Schultz, M. R. Johnson, E. S. Williams, R. L. Crabtree, and R. L. Raff. 1997. Serological survey for diseases in free-ranging coyotes (Canis latrans) in Yellowstone National Park, Wyoming. J. Wildl. Dis. 33: 47-56.
39. Ginsberg, H. W. 2005. Vector-borne diseases on Fire Island, New York (Fire Island National Seashore Science Synthesis Paper). Technical Report NPS/NER/NRTR-2005/018. United States Department of the Interior-National Park Service, Northeast Region, Boston, MA.
40. Gresbrink, R. A., and D. D. Hopkins. 1982. Siphonaptera: host records from Crater Lake National Park, Oregon. Northwest Sci. 56: 176-179.
41. Hakim, J. A., and A. Bitto. 2005. Public education and Lyme Disease prevention in Monroe County: A multi-faceted program of personal protection strategies, tick identification/risk assessment, bi-directional referrals, and vector control. Calif. J. Health Promotion 3: 137-145.
42. Holmquist, J. G., J. R. Jones, J. Schmidt-Gengenbach, L. F. Pierotti, and J. P. Love. 2011. Terrestrial and aquatic macroinvertebrate assemblages as a function of wetland type across a mountain landscape. Arct. Antarct. Alp. Res. 43: 568-584.
43. James, A. M., J. E. Freier, J. E. Keirans, L. A. Durden, J. W. Mertins, and J. L. Schlater. 2006. Distribution, seasonality, and hosts of the Rocky Mountain wood tick in the United States. J. Med. Entomol. 43: 17-24.
44. Kline, D. L., J. R. Wood, and J. A. Cornell. 1991. Interactive effects of 1-octen-3-ol and carbon dioxide on mosquito (Diptera: Culicidae) surveillance and control. J. Med. Entomol. 28: 254-258.
45. Kramer, L. D., L. M. Styer, and G. D. Ebel. 2008. A global perspective on the epidemiology of West Nile virus. Annu. Rev. Entomol. 53: 61-81.
46. Lane, R. S., D. B. Steinlein, and J. Mun. 2004. Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. J. Med. Entomol. 41: 239-248.
47. Leong, K. M. 2010. Everglades National Park mosquito risk assessment pilot: results of focus groups and interviews. Natural Resource Report NPS/BRMD/NRR-2010/189. National Park Service, Fort Collins, CO.
48. Levy, C. E., and K. L. Gage. 1999. Plague in the United States, 1995-1997. Infect. Med. 16: 54-64.
49. Lowell, J. L., R. J. Eisen, A. M. Schotthoefer, X. C. Liang, J. A. Montenieri, D. Tanda, J. Pape, M. E. Schriefer, M. F. Antolin, and K. L. Gage. 2009. Colorado animal-based plague surveillance systems: relationships between targeted animal species and prediction efficacy of areas at risk for humans. J. Vector Ecol. 34: 22-31.
50. McCue, C. M., J. B. Stone, and L. E. Sutton. 1948. Tick paralysis-3 cases of tick (Dermacentor variabilis Say) paralysis in Virginia-with a summary of all the cases reported in the eastern United States. Pediatrics 1: 174-180.
51. McLean, R. G., D. B. Francy, G. S. Bowen, R. E. Bailey, C. H. Calisher, and A. M. Barnes. 1981. The ecology of Colorado tick fever in Rocky Mountain National Park in 1974. I. Objectives, study design, and summary of principal findings. Am. J. Trop. Med. Hyg. 30: 483-489.
52. McLean, R. G., R. B. Shriner, K. S. Pokorny, and G. S. Bowen. 1989. The ecology of Colorado tick fever in Rocky Mountain National Park in 1974. III. Habitats supporting the virus. Am. J. Trop. Med. Hyg. 40: 86-93.
53. McLean, R. G., A. B. Carey, L. J. Kirk, and D. B. Francy. 1993a. Ecology of porcupines (Erethizon dorsatum) and Colorado tick fever virus in Rocky Mountain National Park, 1975-1977. J. Med. Entomol. 30: 236-238.
54. McLean, R. G., S. R. Ubico, C.A.N. Hughes, S. M. Engstrom, and R. C. Johnson. 1993. Isolation and characterization of Borrelia burgdorferi from blood of a bird captured in the Saint Croix River Valley. J. Clin. Microbiol. 31: 2038-2043.
55. Mixson, T. R., S. R. Campbell, J. S. Gill, H. S. Ginsberg, M. V. Reichard, T. L. Schulze, and G. A. Dasch. 2006. Prevalence of Ehrlichia, Borrelia, and rickettsial agents in Amblyomma americanum (Acari: Ixodidae) collected from nine states. J. Med. Entomol. 43: 1261-1268.
56. Moore, C. G., R. G. McLean, C. J. Mitchell, R. S. Nasci, T. F. Tsai, C. H. Calisher, A. A. Marfin, P. S. Moore, and D. J. Gubler. 1993. Guidelines for arbovirus surveillance programs in the United States. United States Department of Health and Human Services-Centers for Disease Control and Prevention, Fort Collins, CO.
57. Moore, J. P. 2001. Mosquitoes of Grand Teton National Park, Teton County, Wyoming, USA. J. Am. Mosq. Control Assoc. 17: 249-253.
58. National Park Service. 2006. Management Policies 2006. United States Government Printing Office, Washington, DC.
59. National Park Service and California Department of Public Health. 2011. Preventing vector-borne diseases in na-tional parks in California. California Department of Public Health, Sacramento, CA.
60. Nelson, B. C. 1980. Plague studies in California: The roles of various species of sylvatic rodents in plague ecology of California, pp. 89-96. Proceedings of the 9th Vertebrate Pest Conference, Fresno, CA.
61. Nelson, B. C., and C. R. Smith. 1976. Ecological effects of a plague epizootic on the activities of rodents inhabiting caves at Lava Beds National Monument, California. J. Med. Entomol. 13: 51-61.
62. Nielsen, L. T. 2009. The mosquitoes of Glacier National Park, Montana. J. Am. Mosq. Control Assoc. 25: 246-247.
63. Nielsen, L. T. 2012. The mosquitoes and chaoborids of Glacier and Yellowstone National Parks with new records and Ochlerotatus nevadensis, a new state record for Montana. J. Am. Mosq. Control Assoc. 28: 6-8.
64. Nielsen, L. T., and M. S. Blackmore. 1996. The mosquitoes of Yellowstone National Park (Diptera: Culicidae). J. Am. Mosq. Control Assoc. 12: 695-700.
65. Oliver, J., and J. J. Howard. 1998. Occurrence of Ixodes scapularis (Acari: Ixodidae) on a selected segment of the Appalachian Trail. J. Med. Entomol. 35: 54-58.
66. Oliver, J. H., L. A. Magnarelli, H. J. Hutcheson, and J. F. Anderson. 1999. Ticks and antibodies to Borrelia burgdorferi from mammals at Cape Hatteras, NC and Assateague Island, MD and VA. J. Med. Entomol. 36: 578-587.
67. Pape, W. J., K. Gershman, and W. M. Bamberg. 2006. Cluster of tick paralysis cases: Colorado, 2006. J. Am. Med. Assoc. 296: 1721-1722.
68. Parker, W. T., R. R. Gerhardt, L. I. Muller, N. D. Caldwell, S. B. Castleberry, and W. M. Ford. 2009. External parasites of Neotoma magister Baird (Allegheny woodrat) in the Cumberland Mountains and Plateau, Tennessee. Southeast. Nat. 8: 167-174.
69. Paul,W.S., G. Maupin, A. O. Scott-Wright, R. B. Craven, and D. T. Dennis. 2002. Outbreak of tick-borne relapsing fever at the North Rim of the Grand Canyon: Evidence for effectiveness of preventive measures. Am. J. Trop. Med. Hyg. 66: 71-75.
70. Piesman, J., and L. Eisen. 2008. Prevention of tick-borne diseases. Annu. Rev. Entomol. 53: 323-343.
71. Ransmeier, J. C. 1949. Tick paralysis in the eastern United States: A summary, with report of 4 new cases from Georgia. J. Pediatr. 34: 299-308.
72. Reeves, W. K., P. H. Adler, W. L. Grogan, and P. E. Super. 2004. Hematophagous and parasitic Diptera (Insecta) in the Great Smoky Mountains National Park, USA. Zootaxa 483: 1-44.
73. Reeves, W. K., L. A. Durden, C. M. Ritzi, K. R. Beckham, P. E. Super, and B. M. Oconnor. 2007. Ectoparasites and other ectosymbiotic arthropods of vertebrates in the Great Smoky Mountains National Park, USA. Zootaxa 1392: 31-68.
74. Reiter, M. E., and D. A. LaPointe. 2009. Larval habitat for the avian malaria vector Culex quinquefasciatus (Diptera: Culicidae) in altered mid-elevation mesic-dry forests in HawaiÕi. J. Vector Ecol. 34: 208-216.
75. Schwan, T. G., M. E. Schrumpf, R. H. Karstens, J. R. Clover, J. Wong, M. Daugherty, M. Struthers, and P. A. Rosa. 1993. Distribution and molecular analysis of Lyme disease spirochetes, Borrelia burgdorferi, isolated from ticks throughout California. J. Clin. Microbiol. 31: 3096-3108.
76. Shapiro, M. R., C. L. Fritz, K. Tait, C. D. Paddock, W. L. Nicholson, K. F. Abramowicz, S. E. Karpathy, G. A. Dasch, J. W. Sumner, P. V. Adem, et al. 2010. Rickettsia 364D: A newly recognized cause of eschar-associated illness in California. Clin. Infect. Dis. 50: 541-548.
77. Smith, C. R., J. R. Tucker, B. A. Wilson, and J. R. Clover. 2010. Plague studies in California: A review of long-term disease activity, flea-host relationships and plague ecology in the coniferous forests of the Southern Cascades and northern Sierra Nevada mountains. J. Vector Ecol. 35: 1-12.
78. Sonenshine, D. E. 1993. Biology of ticks, vol. 2. Oxford University Press, New York, NY.
79. Stark, H. E., and A. R. Kinney. 1969. Abundance of rodents and fleas as related to plague in Lava Beds National Monument, California. J. Med. Entomol. 6: 287-294.
80. Vail, S. G., and G. Smith. 1997. Density-dependent seasonal dynamics of blacklegged tick (Acari: Ixodidae) nymphs. J. Med. Entomol. 34: 301-306.
81. Vail, S. G., and G. Smith. 1998. Air temperature and relative humidity effects on behavioral activity of blacklegged tick (Acari: Ixodidae) nymphs in New Jersey. J. Med. Entomol. 35: 1025-1028.
82. Watkins, R. A., S. E. Moshier, W. D. Odell, and A. J. Pinter. 1991. Splenomegally and reticulocystosis caused by Babesia microti infections in natural populations of the montane vole, Microtus montanus. J. Protozool. 38: 573-576.
83. Watkins, R. A., S. E. Moshier, and A. J. Pinter. 2006. The flea, Megabothris abantis: An invertebrate host of Hepatozoon sp. and a likely definitive host in Hepatozoon infections of the montane vole, Microtus montanus. J. Wildl. Dis. 42: 386-390.
84. Wong, D., M. A. Wild, M. A. Walburger, C. L. Higgins, M. Callahan, L. A. Czarnecki, E. W. Lawaczeck, C. E. Levy, J. G. Patterson, R. Sunenshine, et al. 2009. Primary pneumonic plague contracted from a mountain lion carcass. Clin. Infect. Dis. 49: E33-E38.
85. Wood, C. L., and K. D. Lafferty. 2013. Biodiversity and disease: A synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol. Evol. (http://dx.doi.org/10.1016/j.tree.2012.10.011
86. WHO) World Health Organization. 1991. Relapsing fever. Outbreak at the Grand Canyon National Park. Wkly. Epic. Rec. 66: 261-262.