Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin

Journal of Medical Entomology

Volumn 45, Issue 2, 2008, Pages 289-297

  Steiner, Fresia E ^a   Pinger, Robert R ^a   Vann, Carolyn N ^a   Grindle, Nate ^b   Civitello, David ^b   Clay, Keith ^b   Fuqua, Clay ^b  

^a BALL STATE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Ixodes scapularis; Microbial pathogens; Polymerase chain reaction

Indexed keywords

ANAPLASMA PHAGOCYTOPHILUM; ANIMAL; ARTICLE; BABESIA; BORRELIA BURGDORFERI; CLASSIFICATION; DISEASE TRANSMISSION; FEMALE; GENETICS; ISOLATION AND PURIFICATION; IXODES; MALE; MICROBIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RICKETTSIA; SYMBIOSIS; TICK BORNE DISEASE; UNITED STATES;

ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; BABESIA; BORRELIA BURGDORFERI; FEMALE; GREAT LAKES REGION; IXODES; MAINE; MALE; POLYMERASE CHAIN REACTION; RICKETTSIA; SYMBIOSIS; TICK-BORNE DISEASES;

ACARI; ANAPLASMA PHAGOCYTOPHILUM; BABESIA; BABESIA MICROTI; BABESIA ODOCOILEI; BORRELIA BURGDORFERI; CERVIDAE; IXODES; IXODES SCAPULARIS; IXODES SCAPULARIS ENDOSYMBIONT; IXODIDA; IXODIDAE;

EID: 41049096592     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/0022-2585(2008)45[289:IACROA]2.0.CO;2     Document Type: Article

References (47)

1. Adelson, M. E., R. V. Rao, R. C. Tilton, K. Cabets, E. Eskow, L. Fein, J. L. Occi, and E. Mordechai. 2004. Prevalence of Borrelia burgdorferi, Bartonella spp., Babesia microti, and Anaplasma phagocytophila in Ixodes scapularis ticks collected in northern New Jersey. J. Clin. Microbiol, 42: 2799-2801.
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. Armstrong, P. M., P. Katavolos, D. A. Caporale, R. P. Smith, A. Spielman, and S. R. Telford, III. 1998. Diversity of Babesia infecting deer ticks (Ixodes dammini). Am. J. Trop. Med. Hyg. 58: 739-742.
4. Benson, M. J., J. D. Gawronski, D. E. Eveleigh, and D. R. Benson. 2004. Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl. Environ. Microbiol. 70: 616-620.
5. Burgdorfer, W.S.F. Hayes, and A. J. Mavros. 1981. Non-pathogenic rickettsiae in Dermacentor andersoni: a limiting factor for the distribution of Rickettsia rickettsii, pp. 585-594. In W. Burgdorfer and R. L. Anacker [eds.], Rickettsiae and rickettsial diseases. Academic, New York.
6. Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, and J. P. Davis. 1982. Lyme disease - a tick-borne spirochetosis? Science (Wash., D.C.) 216: 1317-1319.
7. Caporale, D. A., C. M. Johnson, and B. J. Millard. 2005. Presence of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) in Southern Kettle Moraine State Forest Wisconsin, and characteristization of strain (W97F51). J. Med. Entomol. 42: 457-472.
8. [CDC] Center for Disease Control and Prevention. 2004. Lyme Disease - United States, 2001-2002. Morb. Mort. Wkly. Rep. 53: 365-369.
9. Chen, S. M., J. S. Dumler, J. S. Bakken, and D. W. Walker. 1994. Identification of a granulocytic Ehrlichia species as the etiologic agent of human disease. J. Clin. Microbiol. 32: 589-595.
10. Courtney, J. W., R. L. Dryden, J. Montgomery, B. S. Schneider, G. Smith, and R. F. Massung. 2003. Molecular characterization of Anaplasma phagocytophilum and Borrelia burgdorferi in Ixodes scapularis ticks from Pennsylvania. J. Clin. Microbiol. 41: 1569-1573.
11. Dennis, 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.
12. Dugan, V. G., M. J. Yabsley, C. M. Tate, D. G. Mead, U. G. Munderloh, M. J. Herren, D. E. Stallknecht, S. E. Little, and W. R. Davidson. 2006. Evualation of white-tailed deer (Odocoileus virginianus) as natural sentinels for Anaplasma phagocytophilum. Vector Borne Zoonotic Dis. 6: 192-207.
13. Dumler, J. S., A. F. Barbet, C.P.J. Bekker, G. A. Dasch, G. H. Palmer, S. C. Ray, Y. Rikihisa, and F. R. Rurangirwa. 2001. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia, and Ehrlichia with Neorickettsia, descriptions of six new species new species combinations and designation of Ehrlichia equi and "HGE agent" as subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 51: 2145-2165.
14. Emerson, H. R., and W. T. Wright. 1968. The isolation of a Babesia in white-tailed deer. Bull. Wildl. Dis. Assoc. 4: 142-143.
15. Emerson, H. R., and W. T. Wright. 1970. Correction. J. Wildl. Dis. 6: 519.
16. Gotelli, N. J. 2000. Null model analysis of species co-occurrence patterns. Ecology 81: 2606-2621.
17. Gotelli, N.J., and G.L. Entsminger. 2003. EcoSim: null models software for ecology, version 7. (http://homepages.together.net/∼gentsmin/ ecosim.htm).
18. Guerra, M., E. Walker, C. Jones, S. Paskewitz, M. R. Cortinas, A. Stancil, L. Beck, M. Bobo, and U. Kitron. 2002. Predicting the risk of Lyme disease: habitat suitability for Ixodes scapularis in the North Central United States. Emerg. Infect. Dis. 8: 289-297.
19. Herwaldt, B. L., F. E. Springs, P. P. Roberts, M. L. Eberhard, K. Case, and D. H. Persing, and W. A. Agger. 1995. Babesiosis in Wisconsin: apotentially fatal disease. Am. J. Trop. Med. Hyg. 53: 146-151.
20. Holman, M. S., D. A. Caporale, J. Goldberg, E. Lacombe, C. H. Lubelczyk, P. W. Rand, and R. P. Smith. 2004. Anaplasma phagocytophilum, Babesia microti, and Borrelia burgdorferi, in Ixodes scapularis, southern Coastal Maine. Emerg. Infect. Dis. 10: 744-746.
21. Holman, P. J., J. Madeley, T. M. Craig, B. A. Allsopp, M. T. Allsopp, K. R. Petrini, S. D. Waghela, and G. G. Wagner. 2000. Antigenic, phenotypic and molecular characterization confirms Babesia odocoilei isolated from three cervids. J. Wildl. Dis. 36: 581-530.
22. Homer, M. J., and D. H. Persing. 2005. Human babesiosis, pp. 343-360. In J. L. Goodman, D. T. Dennis, and D. E. Sonenshine [eds.], Tick-borne diseases of humans. ASM Press, Washington, DC.
23. Jackson, C. A., S. D. Lovrich, W. A. Agger, and S. M. Callister. 2002. Reassessment of a midwestern Lyme disease focus for Borrelia burgdorferi and the human granulocytic ehrlichiosis agent. J. Clin. Microbiol. 40: 2070-2073.
24. Jasinskas, A., J. M. Zhong, and A. G. Barbour. 2007. Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl. Environ. Microbiol. 73:334-336.
25. Johnson, R. C., G. P. Schmidt, F. W. Hyde, A. G. Steigerwalt, and D. J. Brenner. 1984. Borrelia burgdorferi sp. nov.: etiologic agent of Lyme disease. J. Syst. Biol. 34: 496-497.
26. Klyachko O., B. Stein, N. Grindle, K. Clay, and C. Fuqua. 2007. Localization and visualization of a Coxiella-type symbiont within the lone star tick Amblyomma americanum. Appl. Environ. Microbiol. 73: 6584-6594.
27. Macaluso, K. R., D. E. Sonenshine, S. M. Ceraul, and A. F. Azad. 2002. Rickettsial infection in Dermocentor variabilis (Acari: Ixodidae) inhibits transovarial transmission of a second Rickettsia. J. Med. Entomol. 39: 809-813.
28. Massung, R. F., J. W. Courtney, S. L. Hiratzka, V. E. Pitzer, G. Smith, and R. L. Dryden. 2005. Anaplasma phagocytaphilum in white-tailed deer. Emerg. Infect. Dis. 11: 1604-1606.
29. Messung, R. F., M. J. Mauel, J. H. Owens, N. Allan, J. W. Courtney, K. C. Stafford, III, and T. N. Mather. 2002. Genetic variants of Ehrlichia phagocytophila, Rhode Island and Connecticut. Emerg. Infect. Dis. 8: 467-472.
30. Massung, R. F., K. Slater, J. H. Owens, W. L. Nicholson, T. N. Mather, V. B. Solberg, and J. G. Olson. 1998. Nested PCR assay for detection of granulocytic Ehrlichiae. J. Clin. Microbiol. 36: 1090-1095.
31. Michalski, M., C. Rosenfield, M. Erickson, R. Selle, K. Bates, D. Essar, and H. Massung. 2006. Anaplasma phagocytophilum in central and western Wisconsin: a molecular survey. Parasitol. Res. 99: 694-699.
32. Moreno, C. X., F. Moy, T. J. Daniels, H. P. Godfrey, and F. Cabello. 2006. Molecular analysis of microbial communities identified in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess counties, New York. Environ. Microbiol. 8: 761-772.
33. Niebylski, M. L., M. G. Peacock, E. R. Fischer, S. F. Porcella, and T. G. Schwan. 1997. Characterization of an endosymbiont infecting wood ticks, Dermacentor andersoni, as a member of the genus Francisella. Appl. Environ. Microbiol. 63: 3393-3940.
34. Noda, H., U. G. Munderloh, and T. J. Kurtti. 1997. Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of human and animals. Appl. Environ. Microbiol. 63: 3926-3932.
35. Paskewitz, S. M., M. Vandermause, E. A. Belongiu, and J. Kazmierczak. 2001. Ixodes scapularis (Acari: Ixodidae): abundance and rate of infection with Borrelia burgdorferi in four state parks in Wisconsin. J. Med. Entomol. 38: 33-38.
36. Perlman S.J.M.S. Hunter, and E. Zchori-Fein. 2006. The emerging diversity of Rickettsia. Proc. R. Soc. B Biol. Sci. 273: 2097-2106.
37. Piesman, J., T. C. Hicks, R. J. Sinsky, and G. Obiri. 1987. Simultaneous transmission of Borrelia burgdorferi and Babesia microti by individual nymphal Ixodes dammini ticks. J. Clin. Microbiol. 25: 2010-2013.
38. Finger, R. R., L. Timmons, and K. Karris. 1996. Spread of Ixodes scapularis (Acari: Ixodidae) in Indiana: collection of adults in 1991-1994 and description of Borrelia burgdorferi-infected population. J. Med. Entomol. 28: 745-749.
39. Regnery, R. L., C. L. Spruill, and B. D. Plikaytis. 1991. Genotypic identification of Rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J. Bacteriol. 173: 1576-1589.
40. Schabereiter-Gurtner, C., W. Lubitz, and S. Rolleke. 2003. Application of broad-range 16S rRNA PCR amplification and DGGE fingerprinting for detection of tick-infecting bacteria. J. Microbiol. Methods 52: 251-260.
41. Schmidt, B., R. R. Muellegger, C. Stockenhuber, H. P. Soyer, S. Hoedl, A. Luger, and H. Kerl. 1996. Detection of Borrelia burgdorferi- specific DNA in urine specimens from patients with erythema migrans before and after antibiotic therapy. J. Clin. Microbiol. 34: 1359-1363.
42. Spielman, A., C. M. Clifford, J. Piesman, and M. D. Corwin. 1979. Human babesiosis on Nantucket Island, USA: description of the vector, Ixodes (Ixodes) dammini, n. sp. (Acarina: Ixodidae). J. Med. Entomol. 15: 218-234.
43. Spielman, A., M. L. Wilson, J. F. Levine, and J. Piesman. 1985. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annu. Rev. Entomol. 30: 439-460.
44. 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.
45. Swanson, S. J., D. Neitzel, K. D. Reed, and E. A. Belongia. 2006. Coinfections acquired from Ixodes ticks. Clin. Microbiol. Rev. 19: 703-727.
46. Varde, S., J. Beckley, and I. Schwartz. 1998. Prevalence of tick-borne pathogens in Ixodes scapularis in a rural New Jersey county. Emerg. Infect. Dis. 4: 97-99.
47. Waldrup, K. A., A. A. Kocan, R. W. Barker, and G. G. Wagner. 1990. Transmission of Babesia odocoilei in white-tailed deer (Odocoileus virginianus) by Ixodes scapularis. (Acari: Ixodidae). J. Wildl. Dis. 26: 390-391.