Abstract
We determined whether the infectivity of the Lyme disease spirochete (Borrelia burgdorferi) to vector ticks varies with the duration of infection in laboratory mice. Thus, noninfected nymphal deer ticks were permitted to feed on two strains of early (2 months after infection) and late (8 months after infection) spirochete-infected mice. The attached ticks were removed from their hosts at specified time intervals and were thereafter examined for spirochetes by direct immunofluorescence microscopy. Spirochetes can be acquired by nymphal ticks as fast as 8 h after attachment. More than 80% of the attached ticks acquired spirochetal infection within 48 h after feeding on early spirochete-infected mice. In contrast, spirochetal infectivity to ticks was less than 50% after feeding on late spirochete-infected mice. The overall infectivity of spirochete-infected mice to ticks correlated with the duration of tick attachment. In addition, there was no adverse effect on the spirochetal infectivity to ticks by high levels of host antibody against spirochetes, and no obvious differences in infectivity to ticks was observed by the site of tick feeding. We conclude that the span of spirochetal infectivity to ticks varies with the duration of infection in mice and suggest that spirochetes may persist and may be evenly distributed in the skin of infected hosts, regardless of prominent host immunity.
Full Text
The Full Text of this article is available as a PDF (180.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson J. F. Epizootiology of Borrelia in Ixodes tick vectors and reservoir hosts. Rev Infect Dis. 1989 Sep-Oct;11 (Suppl 6):S1451–S1459. doi: 10.1093/clinids/11.supplement_6.s1451. [DOI] [PubMed] [Google Scholar]
- Anderson J. F., Johnson R. C., Magnarelli L. A., Hyde F. W. Identification of endemic foci of Lyme disease: isolation of Borrelia burgdorferi from feral rodents and ticks (Dermacentor variabilis). J Clin Microbiol. 1985 Jul;22(1):36–38. doi: 10.1128/jcm.22.1.36-38.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anderson J. F., Magnarelli L. A., Burgdorfer W., Barbour A. G. Spirochetes in Ixodes dammini and mammals from Connecticut. Am J Trop Med Hyg. 1983 Jul;32(4):818–824. doi: 10.4269/ajtmh.1983.32.818. [DOI] [PubMed] [Google Scholar]
- Appel M. J., Allan S., Jacobson R. H., Lauderdale T. L., Chang Y. F., Shin S. J., Thomford J. W., Todhunter R. J., Summers B. A. Experimental Lyme disease in dogs produces arthritis and persistent infection. J Infect Dis. 1993 Mar;167(3):651–664. doi: 10.1093/infdis/167.3.651. [DOI] [PubMed] [Google Scholar]
- Asbrink E., Hovmark A. Successful cultivation of spirochetes from skin lesions of patients with erythema chronicum migrans Afzelius and acrodermatitis chronica atrophicans. Acta Pathol Microbiol Immunol Scand B. 1985 Apr;93(2):161–163. doi: 10.1111/j.1699-0463.1985.tb02870.x. [DOI] [PubMed] [Google Scholar]
- Barbour A. G., Tessier S. L., Todd W. J. Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect Immun. 1983 Aug;41(2):795–804. doi: 10.1128/iai.41.2.795-804.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barthold S. W., de Souza M. S., Janotka J. L., Smith A. L., Persing D. H. Chronic Lyme borreliosis in the laboratory mouse. Am J Pathol. 1993 Sep;143(3):959–971. [PMC free article] [PubMed] [Google Scholar]
- Benach J. L., Coleman J. L., Garcia-Monco J. C., Deponte P. C. Biological activity of Borrelia burgdorferi antigens. Ann N Y Acad Sci. 1988;539:115–125. doi: 10.1111/j.1749-6632.1988.tb31845.x. [DOI] [PubMed] [Google Scholar]
- Bosler E. M., Ormiston B. G., Coleman J. L., Hanrahan J. P., Benach J. L. Prevalence of the Lyme disease spirochete in populations of white-tailed deer and white-footed mice. Yale J Biol Med. 1984 Jul-Aug;57(4):651–659. [PMC free article] [PubMed] [Google Scholar]
- Brossard M., Fivaz V. Ixodes ricinus L.: mast cells, basophils and eosinophils in the sequence of cellular events in the skin of infested or re-infested rabbits. Parasitology. 1982 Dec;85(Pt 3):583–592. doi: 10.1017/s0031182000056365. [DOI] [PubMed] [Google Scholar]
- Brown S. J., Askenase P. W. Rejection of ticks from guinea pigs by anti-hapten-antibody-mediated degranulation of basophils at cutaneous basophil hypersensitivity sites: role of mediators other than histamine. J Immunol. 1985 Feb;134(2):1160–1165. [PubMed] [Google Scholar]
- Donahue J. G., Piesman J., Spielman A. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am J Trop Med Hyg. 1987 Jan;36(1):92–96. doi: 10.4269/ajtmh.1987.36.92. [DOI] [PubMed] [Google Scholar]
- Gern L., Schaible U. E., Simon M. M. Mode of inoculation of the Lyme disease agent Borrelia burgdorferi influences infection and immune responses in inbred strains of mice. J Infect Dis. 1993 Apr;167(4):971–975. doi: 10.1093/infdis/167.4.971. [DOI] [PubMed] [Google Scholar]
- Golde W. T., Burkot T. R., Sviat S., Keen M. G., Mayer L. W., Johnson B. J., Piesman J. The major histocompatibility complex-restricted response of recombinant inbred strains of mice to natural tick transmission of Borrelia burgdorferi. J Exp Med. 1993 Jan 1;177(1):9–17. doi: 10.1084/jem.177.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levine J. F., Wilson M. L., Spielman A. Mice as reservoirs of the Lyme disease spirochete. Am J Trop Med Hyg. 1985 Mar;34(2):355–360. doi: 10.4269/ajtmh.1985.34.355. [DOI] [PubMed] [Google Scholar]
- Magnarelli L. A., Anderson J. F., Burgdorfer W., Chappell W. A. Parasitism by Ixodes dammini (Acari: Ixodidae) and antibodies to spirochetes in mammals at Lyme disease foci in Connecticut, USA. J Med Entomol. 1984 Jan 26;21(1):52–57. doi: 10.1093/jmedent/21.1.52. [DOI] [PubMed] [Google Scholar]
- Main A. J., Carey A. B., Carey M. G., Goodwin R. H. Immature Ixodes dammini (acari: Ixodidae) on small animals in Connecticut, USA. J Med Entomol. 1982 Nov 30;19(6):655–664. doi: 10.1093/jmedent/19.6.655. [DOI] [PubMed] [Google Scholar]
- Mather T. N., Telford S. R., 3rd, Moore S. I., Spielman A. Borrelia burgdorferi and Babesia microti: efficiency of transmission from reservoirs to vector ticks (Ixodes dammini). Exp Parasitol. 1990 Jan;70(1):55–61. doi: 10.1016/0014-4894(90)90085-q. [DOI] [PubMed] [Google Scholar]
- Mather T. N., Wilson M. L., Moore S. I., Ribeiro J. M., Spielman A. Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). Am J Epidemiol. 1989 Jul;130(1):143–150. doi: 10.1093/oxfordjournals.aje.a115306. [DOI] [PubMed] [Google Scholar]
- Moody K. D., Barthold S. W., Terwilliger G. A., Beck D. S., Hansen G. M., Jacoby R. O. Experimental chronic Lyme borreliosis in Lewis rats. Am J Trop Med Hyg. 1990 Feb;42(2):165–174. doi: 10.4269/ajtmh.1990.42.165. [DOI] [PubMed] [Google Scholar]
- Nadelman R. B., Pavia C. S., Magnarelli L. A., Wormser G. P. Isolation of Borrelia burgdorferi from the blood of seven patients with Lyme disease. Am J Med. 1990 Jan;88(1):21–26. doi: 10.1016/0002-9343(90)90122-t. [DOI] [PubMed] [Google Scholar]
- Nakayama Y., Spielman A. Ingestion of Lyme disease spirochetes by ticks feeding on infected hosts. J Infect Dis. 1989 Jul;160(1):166–167. doi: 10.1093/infdis/160.1.166. [DOI] [PubMed] [Google Scholar]
- Nocton J. J., Dressler F., Rutledge B. J., Rys P. N., Persing D. H., Steere A. C. Detection of Borrelia burgdorferi DNA by polymerase chain reaction in synovial fluid from patients with Lyme arthritis. N Engl J Med. 1994 Jan 27;330(4):229–234. doi: 10.1056/NEJM199401273300401. [DOI] [PubMed] [Google Scholar]
- Piesman J. Experimental acquisition of the Lyme disease spirochete, Borrelia burgdorferi, by larval Ixodes dammini (Acari: Ixodidae) during partial blood meals. J Med Entomol. 1991 Mar;28(2):259–262. doi: 10.1093/jmedent/28.2.259. [DOI] [PubMed] [Google Scholar]
- Piesman J., Mather T. N., Dammin G. J., Telford S. R., 3rd, Lastavica C. C., Spielman A. Seasonal variation of transmission risk of Lyme disease and human babesiosis. Am J Epidemiol. 1987 Dec;126(6):1187–1189. doi: 10.1093/oxfordjournals.aje.a114757. [DOI] [PubMed] [Google Scholar]
- Piesman J., Mather T. N., Donahue J. G., Levine J., Campbell J. D., Karakashian S. J., Spielman A. Comparative prevalence of Babesia microti and Borrelia burgdorferi in four populations of Ixodes dammini in eastern Massachusetts. Acta Trop. 1986 Sep;43(3):263–270. [PubMed] [Google Scholar]
- Piesman J., Mather T. N., Telford S. R., 3rd, Spielman A. Concurrent Borrelia burgdorferi and Babesia microti infection in nymphal Ixodes dammini. J Clin Microbiol. 1986 Sep;24(3):446–447. doi: 10.1128/jcm.24.3.446-447.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piesman J. Standard system for infecting ticks (Acari: Ixodidae) with the Lyme disease spirochete, Borrelia burgdorferi. J Med Entomol. 1993 Jan;30(1):199–203. doi: 10.1093/jmedent/30.1.199. [DOI] [PubMed] [Google Scholar]
- Preac-Mursic V., Weber K., Pfister H. W., Wilske B., Gross B., Baumann A., Prokop J. Survival of Borrelia burgdorferi in antibiotically treated patients with Lyme borreliosis. Infection. 1989 Nov-Dec;17(6):355–359. doi: 10.1007/BF01645543. [DOI] [PubMed] [Google Scholar]
- Roehrig J. T., Piesman J., Hunt A. R., Keen M. G., Happ C. M., Johnson B. J. The hamster immune response to tick-transmitted Borrelia burgdorferi differs from the response to needle-inoculated, cultured organisms. J Immunol. 1992 Dec 1;149(11):3648–3653. [PubMed] [Google Scholar]
- Schmidli J., Hunziker T., Moesli P., Schaad U. B. Cultivation of Borrelia burgdorferi from joint fluid three months after treatment of facial palsy due to Lyme borreliosis. J Infect Dis. 1988 Oct;158(4):905–906. doi: 10.1093/infdis/158.4.905. [DOI] [PubMed] [Google Scholar]
- Schmitz J. L., Schell R. F., Lovrich S. D., Callister S. M., Coe J. E. Characterization of the protective antibody response to Borrelia burgdorferi in experimentally infected LSH hamsters. Infect Immun. 1991 Jun;59(6):1916–1921. doi: 10.1128/iai.59.6.1916-1921.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwan T. G., Karstens R. H., Schrumpf M. E., Simpson W. J. Changes in antigenic reactivity of Borrelia burgdorferi, the Lyme disease spirochete, during persistent infection in mice. Can J Microbiol. 1991 Jun;37(6):450–454. doi: 10.1139/m91-074. [DOI] [PubMed] [Google Scholar]
- Schwan T. G., Kime K. K., Schrumpf M. E., Coe J. E., Simpson W. J. Antibody response in white-footed mice (Peromyscus leucopus) experimentally infected with the Lyme disease spirochete (Borrelia burgdorferi). Infect Immun. 1989 Nov;57(11):3445–3451. doi: 10.1128/iai.57.11.3445-3451.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwan T. G., Simpson W. J., Schrumpf M. E., Karstens R. H. Identification of Borrelia burgdorferi and B. hermsii using DNA hybridization probes. J Clin Microbiol. 1989 Aug;27(8):1734–1738. doi: 10.1128/jcm.27.8.1734-1738.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shih C. M., Pollack R. J., Telford S. R., 3rd, Spielman A. Delayed dissemination of Lyme disease spirochetes from the site of deposition in the skin of mice. J Infect Dis. 1992 Oct;166(4):827–831. doi: 10.1093/infdis/166.4.827. [DOI] [PubMed] [Google Scholar]
- Shih C. M., Spielman A. Accelerated transmission of Lyme disease spirochetes by partially fed vector ticks. J Clin Microbiol. 1993 Nov;31(11):2878–2881. doi: 10.1128/jcm.31.11.2878-2881.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snydman D. R., Schenkein D. P., Berardi V. P., Lastavica C. C., Pariser K. M. Borrelia burgdorferi in joint fluid in chronic Lyme arthritis. Ann Intern Med. 1986 Jun;104(6):798–800. doi: 10.7326/0003-4819-104-6-798. [DOI] [PubMed] [Google Scholar]
- Spielman A., Levine J. F., Wilson M. L. Vectorial capacity of North American Ixodes ticks. Yale J Biol Med. 1984 Jul-Aug;57(4):507–513. [PMC free article] [PubMed] [Google Scholar]
- Spielman A., Wilson M. L., Levine J. F., Piesman J. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annu Rev Entomol. 1985;30:439–460. doi: 10.1146/annurev.en.30.010185.002255. [DOI] [PubMed] [Google Scholar]
- Steere A. C., Broderick T. F., Malawista S. E. Erythema chronicum migrans and Lyme arthritis: epidemiologic evidence for a tick vector. Am J Epidemiol. 1978 Oct;108(4):312–321. doi: 10.1093/oxfordjournals.aje.a112625. [DOI] [PubMed] [Google Scholar]
- Telford S. R., 3rd, Urioste S. S., Spielman A. Clustering of host-seeking nymphal deer ticks (Ixodes dammini) infected by Lyme disease spirochetes (Borrelia burgdorferi). Am J Trop Med Hyg. 1992 Jul;47(1):55–60. doi: 10.4269/ajtmh.1992.47.55. [DOI] [PubMed] [Google Scholar]