1921
Volume 81, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

The Lyme borreliosis agent and the relapsing fever group species co-occur in the United States. We used species-specific, quantitative polymerase chain reaction to study both species in the blood and skin of mice and host-seeking nymphs at a Connecticut site. Bacteremias with or were most prevalent during periods of greatest activity for nymphs or larvae, respectively. Whereas was 30-fold more frequent than in skin biopsies and mice had higher densities of densities in the skin than in the blood, densities were higher in blood than skin. In a survey of host-seeking nymphs in 11 northern states, infection prevalences for and averaged ~0.20 and ~0.02, respectively. Co-infections of or with both and were neither more nor less common than random expectations.

Loading

Article metrics loading...

The graphs shown below represent data from March 2017
/content/journals/10.4269/ajtmh.2009.09-0208
2009-12-01
2019-12-16
Loading full text...

Full text loading...

/deliver/fulltext/14761645/81/6/0811120.html?itemId=/content/journals/10.4269/ajtmh.2009.09-0208&mimeType=html&fmt=ahah

References

  1. Barbour AG, 2001. Borrelia: a diverse and ubiquitous genus of tick-borne pathogens. Scheld WM, Craig WA, Hughes JM, eds. Emerging Infections 5. Washington, DC: American Society for Microbiology Press, 153–174.
  2. Barbour AG, 2005. Relapsing fever. Goodman JL, Dennis D, Sonenshine DE, eds. Tick-Borne Diseases of Humans. Washington, DC: ASM Press, 268–291.
  3. Steere AC, Coburn J, Glickstein L, 2005. Lyme borreliosis. Goodman JL, Dennis D, Sonenshine DE, eds. Tick-Borne Diseases of Humans. Washington, DC: ASM Press, 176–206.
  4. Rich SM, Armstrong PM, Smith RD, Telford SR 3rd, 2001. Lone star tick-infecting borreliae are most closely related to the agent of bovine borreliosis. J Clin Microbiol 39: 494–497. [Google Scholar]
  5. Barbour AG, Maupin GO, Teltow GJ, Carter CJ, Piesman J, 1996. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 173: 403–409. [Google Scholar]
  6. Armstrong PM, Rich SM, Smith RD, Hartl DL, Spielman A, Telford SR 3rd, 1996. A new Borrelia infecting Lone Star ticks. Lancet 347: 67–68. [Google Scholar]
  7. Varela-Stokes AS, 2007. Transmission of bacterial agents from lone star ticks to white-tailed deer. J Med Entomol 44: 478–483. [Google Scholar]
  8. Bunikis J, Tsao J, Garpmo U, Berglund J, Fish D, Barbour AG, 2004. Typing of Borrelia relapsing fever group strains. Emerg Infect Dis 10: 1661–1664. [Google Scholar]
  9. Fraenkel CJ, Garpmo U, Berglund J, 2002. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J Clin Microbiol 40: 3308–3312. [Google Scholar]
  10. Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, Nakao M, 1995. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol 45: 804–810. [Google Scholar]
  11. Mun J, Eisen RJ, Eisen L, Lane RS, 2006. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J Med Entomol 43: 120–123. [Google Scholar]
  12. Scoles GA, Papero M, Beati L, Fish D, 2001. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1: 21–34. [Google Scholar]
  13. Varela AS, Luttrell MP, Howerth EW, Moore VA, Davidson WR, Stallknecht DE, Little SE, 2004. First culture isolation of Borrelia lonestari, putative agent of southern tick-associated rash illness. J Clin Microbiol 42: 1163–1169. [Google Scholar]
  14. Bunikis J, Barbour AG, 2005. Third Borrelia species in white-footed mice. Emerg Infect Dis 11: 1150–1151. [Google Scholar]
  15. Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, Barbour AG, 2004. An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc Natl Acad Sci USA 101: 18159–18164. [Google Scholar]
  16. Gatewood AG, Liebman KA, Vourc’h G, Bunikis J, Hamer SA, Cortinas R, Melton F, Cislo P, Kitron U, Tsao J, Barbour AG, Fish D, Diuk-Wasser MA, 2009. Climate and tick seasonality predict Borrelia burgdorferi genotype distribution. Appl Environ Microbiol 75: 2476–2483. [Google Scholar]
  17. Zhioua E, Aeschlimann A, Gern L, 1994. Infection of field-collected Ixodes ricinus (Acari: Ixodidae) larvae with Borrelia burgdorferi in Switzerland. J Med Entomol 31: 763–766. [Google Scholar]
  18. Patrican LA, 1997. Absence of Lyme disease spirochetes in larval progeny of naturally infected Ixodes scapularis (Acari:Ixodidae) fed on dogs. J Med Entomol 34: 52–55. [Google Scholar]
  19. Nefedova VV, Korenberg EI, Gorelova NB, Kovalevskii YV, 2004. Studies on the transovarial transmission of Borrelia burgdorferi sensu lato in the taiga tick Ixodes persulcatus. Folia Parasitol (Praha) 51: 67–71. [Google Scholar]
  20. Schwan TG, Battisti JM, Porcella SF, Raffel SJ, Schrumpf ME, Fischer ER, Carroll JA, Stewart PE, Rosa P, Somerville GA, 2003. Glycerol-3-phosphate acquisition in spirochetes: distribution and biological activity of glycerophosphodiester phosphodiesterase (GlpQ) among Borrelia species. J Bacteriol 185: 1346–1356. [Google Scholar]
  21. Ramakrishnan U, 2001. Methods of controlling white-tailed deer. Front Plant Sci 53: 7. [Google Scholar]
  22. Tsao J, Barbour AG, Luke CJ, Fikrig E, Fish D, 2001. OspA immunization decreases transmission of Borrelia burgdorferi spirochetes from infected Peromyscus leucopus mice to larval Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1: 65–74. [Google Scholar]
  23. Sinsky RJ, Piesman J, 1989. Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. J Clin Microbiol 27: 1723–1727. [Google Scholar]
  24. Pennington PM, Allred CD, West CS, Alvarez R, Barbour AG, 1997. Arthritis severity and spirochete burden are determined by serotype in the Borrelia turicatae-mouse model of Lyme disease. Infect Immun 65: 285–292. [Google Scholar]
  25. Falco RC, Fish D, 1992. A comparison of methods for sampling the deer tick, Ixodes dammini, in a Lyme disease endemic area. Exp Appl Acarol 14: 165–173. [Google Scholar]
  26. Diuk-Wasser MA, GatewoodAG, Cortinas MR,Yaremych-Hamer S, Tsao J, Kitron U, Hickling G, Brownstein JS, Walker E, Piesman J, Fish D, 2006. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J Med Entomol 43: 166–176. [Google Scholar]
  27. Bunikis J, Tsao J, Luke CJ, Luna MG, Fish D, Barbour AG, 2004. Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: a longitudinal study in an area where Lyme borreliosis is highly endemic. J Infect Dis 189: 1515–1523. [Google Scholar]
  28. Beati L, Keirans JE, 2001. Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. J Parasitol 87: 32–48. [Google Scholar]
  29. Hanincova K, Kurtenbach K, Diuk-Wasser M, Brei B, Fish D, 2006. Epidemic spread of Lyme borreliosis, northeastern United States. Emerg Infect Dis 12: 604–611. [Google Scholar]
  30. Comstedt P, Bergstrom S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, Barbour AG, Bunikis J, 2006. Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg Infect Dis 12: 1087–1095. [Google Scholar]
  31. Barbour AG, 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521–525. [Google Scholar]
  32. Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG, 2004. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150: 1741–1755. [Google Scholar]
  33. Hutchinson G, 1959. Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93: 145–159. [Google Scholar]
  34. Anderson JF, Flavell RA, Magnarelli LA, Barthold SW, Kantor FS, Wallich R, Persing DH, Mathiesen D, Fikrig E, 1996. Novel Borrelia burgdorferi isolates from Ixodes scapularis and Ixodes dentatus ticks feeding on humans. J Clin Microbiol 34: 524–529. [Google Scholar]
  35. Goethert HK, Telford SR 3rd, 2003. Enzootic transmission of Babesia divergens among cottontail rabbits on Nantucket Island, Massachusetts. Am J Trop Med Hyg 69: 455–460. [Google Scholar]
  36. Schneider BS, Zeidner NS, Burkot TR, Maupin GO, Piesman J, 2000. Borrelia isolates in Northern Colorado identified as Borrelia bissettii. J Clin Microbiol 38: 3103–3105. [Google Scholar]
  37. Rijpkema S, Golubic D, Molkenboer M, Verbeek-De Kruif N, Schellekens J, 1996. Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp Appl Acarol 20: 23–30. [Google Scholar]
  38. Kurtenbach K, De Michelis S, Sewell HS, Etti S, Schafer SM, Hails R, Collares-Pereira M, Santos-Reis M, Hanincova K, Labuda M, Bormane A, Donaghy M, 2001. Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol 67: 4926–4929. [Google Scholar]
  39. Vennestrom J, Egholm H, Jensen PM, 2008. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitol Int 57: 32–37. [Google Scholar]
  40. Kurtenbach K, Hanincova K, Tsao JI, Margos G, Fish D, Ogden NH, 2006. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat Rev Microbiol 4: 660–669. [Google Scholar]
  41. Donahue JG, Piesman J, Spielman A, 1987. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am J Trop Med Hyg 36: 92–96. [Google Scholar]
  42. Richter D, Klug B, Spielman A, Matuschka FR, 2004. Adaptation of diverse lyme disease spirochetes in a natural rodent reservoir host. Infect Immun 72: 2442–2444. [Google Scholar]
  43. Hanincova K, Ogden NH, Diuk-Wasser M, Pappas CJ, Iyer R, Fish D, Schwartz I, Kurtenbach K, 2008. Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Appl Environ Microbiol 74: 153–157. [Google Scholar]
  44. Piesman J, Gern L, 2004. Lyme borreliosis in Europe and North America. Parasitology 129 (Suppl): S191–S220. [Google Scholar]
  45. Woolhouse ME, Taylor LH, Haydon DT, 2001. Population biology of multihost pathogens. Science 292: 1109–1112. [Google Scholar]
  46. Krampitz HE, 1986. In vivo isolation and maintenance of some wild strains of European hard tick spirochetes in mammalian and arthropod hosts. A parasitologist’s view. Zentralbl Bakteriol Mikrobiol Hyg [A] 263: 21–28. [Google Scholar]
  47. Stanek G, Burger I, Hirschl A, Wewalka G, Radda A, 1986. Borrelia transfer by ticks during their life cycle. Studies on laboratory animals. Zentralbl Bakteriol Mikrobiol Hyg [A] 263: 29–33. [Google Scholar]
  48. Richter D, Matuschka FR, 2006. Modulatory effect of cattle on risk for Lyme disease. Emerg Infect Dis 12: 1919–1923. [Google Scholar]
  49. Wodecka B, 2007. [Significance of red deer (Cervus elaphus) in the ecology of Borrelia burgdorferi sensu lato]. Wiad Parazytol 53: 231–237. [Google Scholar]
  50. Burgdorfer W, Gage KL, 1987. Susceptibility of the hispid cotton rat (Sigmodon hispidus) to the Lyme disease spirochete (Borrelia burgdorferi). Am J Trop Med Hyg 37: 624–628. [Google Scholar]
  51. Ullmann AJ, Gabitzsch ES, Schulze TL, Zeidner NS, Piesman J, 2005. Three multiplex assays for detection of Borrelia burgdorferi sensu lato and Borrelia miyamotoi sensu lato in field-collected Ixodes nymphs in North America. J Med Entomol 42: 1057–1062. [Google Scholar]
  52. Richter D, Schlee DB, Matuschka FR, 2003. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg Infect Dis 9: 697–701. [Google Scholar]
  53. Hulinska D, Votypka J, Kriz B, Holinkova N, Novakova J, Hulinsky V, 2007. Phenotypic and genotypic analysis of Borrelia spp. isolated from Ixodes ricinus ticks by using electrophoretic chips and real-time polymerase chain reaction. Folia Microbiol (Praha) 52: 315–324. [Google Scholar]
  54. Anderson JF, Magnarelli LA, Burgdorfer W, Barbour AG, 1983. Spirochetes in Ixodes dammini and mammals from Connecticut. Am J Trop Med Hyg 32: 818–824. [Google Scholar]
  55. Walker ED, Smith TW, DeWitt J, Beaudo DC, McLean RG, 1994. Prevalence of Borrelia burgdorferi in host-seeking ticks (Acari: Ixodidae) from a Lyme disease endemic area in northern Michigan. J Med Entomol 31: 524–528. [Google Scholar]
  56. Wang G, Liveris D, Brei B, Wu H, Falco RC, Fish D, Schwartz I, 2003. Real-time PCR for simultaneous detection and quantification of Borrelia burgdorferi in field-collected Ixodes scapularis ticks from the Northeastern United States. Appl Environ Microbiol 69: 4561–4565. [Google Scholar]
  57. Ornstein K, Barbour AG, 2006. A reverse transcriptase-polymerase chain reaction assay of Borrelia burgdorferi 16S rRNA for highly sensitive quantification of pathogen load in a vector. Vector Borne Zoonotic Dis 6: 103–112. [Google Scholar]
  58. Brunet LR, Spielman A, Telford SR 3rd, 1995. Short report: density of Lyme disease spirochetes within deer ticks collected from zoonotic sites. Am J Trop Med Hyg 53: 300–302. [Google Scholar]
  59. Burkot TR, Patrican L, Piesman J, 1994. Field trial of an outer surface protein A (OspA) antigen-capture enzyme-linked immunosorbent assay (ELISA) to detect Borrelia burgdorferi in Ixodes scapularis. Am J Trop Med Hyg 50: 354–358. [Google Scholar]
  60. Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP, 1982. Lyme disease—a tick-borne spirochetosis? Science 216: 1317–1319. [Google Scholar]
  61. De Silva AM, Fikrig E, 1995. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am J Trop Med Hyg 53: 397–404. [Google Scholar]
  62. Lane RS, Burgdorfer W, 1987. Transovarial and transstadial passage of Borrelia burgdorferi in the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Am J Trop Med Hyg 37: 188–192. [Google Scholar]
  63. Burgdorfer W, Lane RS, Barbour AG, Gresbrink RA, Anderson JR, 1985. The western black-legged tick, Ixodes pacificus: a vector of Borrelia burgdorferi. Am J Trop Med Hyg 34: 925–930. [Google Scholar]
  64. Fine PE, 1975. Vectors and vertical transmission: an epidemiologic perspective. Ann N Y Acad Sci 266: 173–194. [Google Scholar]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2009.09-0208
Loading
/content/journals/10.4269/ajtmh.2009.09-0208
Loading

Data & Media loading...

Supplementary table 1

  • Received : 22 Apr 2009
  • Accepted : 03 Aug 2009

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error