Abstract
The prevalence of Lyme disease Borrelia-infected ticks on migrating birds was studied in Scandinavia. A total of 22,998 birds were caught at eight different bird observatories and examined for ticks. Five different species of ticks were found infesting the birds. The dominant species, Ixodesricinus, constituted 98.3% of the ticks collected. The presence of spirochetes was determined by an immunofluorescence assay of tick larvae and DNA amplification by PCR on all ticks. To determine which Borrelia burgdorferi sensu lato species were present, a species classification was performed by DNA amplification with species-specific 16S rDNA primers and by DNA sequencing (rDNA is DNA coding for rRNA). Flagellin gene sequences of all species of B. burgdorferi sensu lato previously recorded in Europe were observed. Borrelia garinii was the most prevalent Lyme disease Borrelia species in ticks collected from birds arriving from the South or Southeast in the spring, whereas the distribution was more heterogeneous in ticks from birds migrating from the Southwest. These data support the notion that birds are partly responsible for the heterogeneous distribution of Lyme disease Borrelia spirochetes in Europe.
Full Text
The Full Text of this article is available as a PDF (265.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ackermann R., Kabatzki J., Boisten H. P., Steere A. C., Grodzicki R. L., Hartung S., Runne U. Ixodes ricinus spirochete and European erythema chronicum migrans disease. Yale J Biol Med. 1984 Jul-Aug;57(4):573–580. [PMC free article] [PubMed] [Google Scholar]
- Aeschlimann A., Chamot E., Gigon F., Jeanneret J. P., Kesseler D., Walther C. B. burgdorferi in Switzerland. Zentralbl Bakteriol Mikrobiol Hyg A. 1987 Feb;263(3):450–458. doi: 10.1016/s0176-6724(87)80107-4. [DOI] [PubMed] [Google Scholar]
- Anderson J. F., Johnson R. C., Magnarelli L. A., Hyde F. W. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infect Immun. 1986 Feb;51(2):394–396. doi: 10.1128/iai.51.2.394-396.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anderson J. F., Magnarelli L. A., Stafford K. C., 3rd Bird-feeding ticks transstadially transmit Borrelia burgdorferi that infect Syrian hamsters. J Wildl Dis. 1990 Jan;26(1):1–10. doi: 10.7589/0090-3558-26.1.1. [DOI] [PubMed] [Google Scholar]
- Asbrink E., Hederstedt B., Hovmark A. The spirochetal etiology of erythema chronicum migrans Afzelius. Acta Derm Venereol. 1984;64(4):291–295. [PubMed] [Google Scholar]
- Asbrink E., Hovmark A., Hederstedt B. The spirochetal etiology of acrodermatitis chronica atrophicans Herxheimer. Acta Derm Venereol. 1984;64(6):506–512. [PubMed] [Google Scholar]
- Baranton G., Postic D., Saint Girons I., Boerlin P., Piffaretti J. C., Assous M., Grimont P. A. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int J Syst Bacteriol. 1992 Jul;42(3):378–383. doi: 10.1099/00207713-42-3-378. [DOI] [PubMed] [Google Scholar]
- Bergström S., Olsén B., Burman N., Gothefors L., Jaenson T. G., Jonsson M., Mejlon H. A. Molecular characterization of Borrelia burgdorferi isolated from Ixodes ricinus in northern Sweden. Scand J Infect Dis. 1992;24(2):181–188. doi: 10.3109/00365549209052610. [DOI] [PubMed] [Google Scholar]
- Canica M. M., Nato F., du Merle L., Mazie J. C., Baranton G., Postic D. Monoclonal antibodies for identification of Borrelia afzelii sp. nov. associated with late cutaneous manifestations of Lyme borreliosis. Scand J Infect Dis. 1993;25(4):441–448. doi: 10.3109/00365549309008525. [DOI] [PubMed] [Google Scholar]
- Gern L., Toutoungi L. N., Hu C. M., Aeschlimann A. Ixodes (Pholeoixodes) hexagonus, an efficient vector of Borrelia burgdorferi in the laboratory. Med Vet Entomol. 1991 Oct;5(4):431–435. doi: 10.1111/j.1365-2915.1991.tb00571.x. [DOI] [PubMed] [Google Scholar]
- HOOGSTRAAL H., KAISER M. N., TRAYLOR M. A., GABER S., GUINDY E. Ticks (Ixodoidea) on birds migrating from Africa to Europe and Asia. Bull World Health Organ. 1961;24:197–212. [PMC free article] [PubMed] [Google Scholar]
- HOOGSTRAAL H., KAISER M. N., TRAYLOR M. A., GUINDY E., GABER S. Ticks (Ixodidae) on birds migrating from Europe and Asia to Africa 1959-61. Bull World Health Organ. 1963;28(2):235–262. [PMC free article] [PubMed] [Google Scholar]
- HOOGSTRAAL H., KAISER M. N. Ticks from European-Asiatic birds migrating through Egypt into Africa. Science. 1961 Jan 27;133(3448):277–278. doi: 10.1126/science.133.3448.277. [DOI] [PubMed] [Google Scholar]
- Humair P. F., Turrian N., Aeschilimann A., Gern L. Borrelia burgdorferi in a focus of Lyme borreliosis: epizootiologic contribution of small mammals. Folia Parasitol (Praha) 1993;40(1):65–70. [PubMed] [Google Scholar]
- Humair P. F., Turrian N., Aeschlimann A., Gern L. Ixodes ricinus immatures on birds in a focus of Lyme borreliosis. Folia Parasitol (Praha) 1993;40(3):237–242. [PubMed] [Google Scholar]
- Ishizawa M., Kobayashi Y., Miyamura T., Matsuura S. Simple procedure of DNA isolation from human serum. Nucleic Acids Res. 1991 Oct 25;19(20):5792–5792. doi: 10.1093/nar/19.20.5792. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jaenson T. G., Tälleklint L., Lundqvist L., Olsen B., Chirico J., Mejlon H. Geographical distribution, host associations, and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden. J Med Entomol. 1994 Mar;31(2):240–256. doi: 10.1093/jmedent/31.2.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jonsson M., Noppa L., Barbour A. G., Bergström S. Heterogeneity of outer membrane proteins in Borrelia burgdorferi: comparison of osp operons of three isolates of different geographic origins. Infect Immun. 1992 May;60(5):1845–1853. doi: 10.1128/iai.60.5.1845-1853.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawabata H., Tashibu H., Yamada K., Masuzawa T., Yanagihara Y. Polymerase chain reaction analysis of Borrelia species isolated in Japan. Microbiol Immunol. 1994;38(8):591–598. doi: 10.1111/j.1348-0421.1994.tb01828.x. [DOI] [PubMed] [Google Scholar]
- Marconi R. T., Garon C. F. Development of polymerase chain reaction primer sets for diagnosis of Lyme disease and for species-specific identification of Lyme disease isolates by 16S rRNA signature nucleotide analysis. J Clin Microbiol. 1992 Nov;30(11):2830–2834. doi: 10.1128/jcm.30.11.2830-2834.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mather T. N., Telford S. R., 3rd, MacLachlan A. B., Spielman A. Incompetence of catbirds as reservoirs for the Lyme disease spirochete (Borrelia burgdorferi). J Parasitol. 1989 Feb;75(1):66–69. [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]
- Matuschka F. R., Fischer P., Heiler M., Blümcke S., Spielman A. Stage-associated risk of transmission of the Lyme disease spirochete by European Ixodes ticks. Parasitol Res. 1992;78(8):695–698. doi: 10.1007/BF00931523. [DOI] [PubMed] [Google Scholar]
- Matuschka F. R., Spielman A. Loss of Lyme disease spirochetes from Ixodes ricinus ticks feeding on European blackbirds. Exp Parasitol. 1992 Mar;74(2):151–158. doi: 10.1016/0014-4894(92)90042-9. [DOI] [PubMed] [Google Scholar]
- McLean R. G., Ubico S. R., Hughes C. A., Engstrom S. M., Johnson R. C. Isolation and characterization of Borrelia burgdorferi from blood of a bird captured in the Saint Croix River Valley. J Clin Microbiol. 1993 Aug;31(8):2038–2043. doi: 10.1128/jcm.31.8.2038-2043.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mejlon H. A., Jaenson T. G. Seasonal prevalence of Borrelia burgdorferi in Ixodes ricinus in different vegetation types in Sweden. Scand J Infect Dis. 1993;25(4):449–456. doi: 10.3109/00365549309008526. [DOI] [PubMed] [Google Scholar]
- NUORTEVA P., HOOGSTRAAL H. THE INCIDENCE OF TICKS (IXODOIDEA, IXODIDAE) ON MIGRATORY BIRDS ARRIVING IN FINLAND DURING THE SPRING OF 1962. Ann Med Exp Biol Fenn. 1963;41:457–468. [PubMed] [Google Scholar]
- Nohlmans L. M., de Boer R., van den Bogaard A. E., van Boven C. P. Genotypic and phenotypic analysis of Borrelia burgdorferi isolates from The Netherlands. J Clin Microbiol. 1995 Jan;33(1):119–125. doi: 10.1128/jcm.33.1.119-125.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noppa L., Burman N., Sadziene A., Barbour A. G., Bergström S. Expression of the flagellin gene in Borrelia is controlled by an alternative sigma factor. Microbiology. 1995 Jan;141(Pt 1):85–93. doi: 10.1099/00221287-141-1-85. [DOI] [PubMed] [Google Scholar]
- Olsén B., Jaenson T. G., Noppa L., Bunikis J., Bergström S. A Lyme borreliosis cycle in seabirds and Ixodes uriae ticks. Nature. 1993 Mar 25;362(6418):340–342. doi: 10.1038/362340a0. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tälleklint L., Jaenson T. G. Maintenance by hares of European Borrelia burgdorferi in ecosystems without rodents. J Med Entomol. 1993 Jan;30(1):273–276. doi: 10.1093/jmedent/30.1.273. [DOI] [PubMed] [Google Scholar]
- Tälleklint L., Jaenson T. G. Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. J Med Entomol. 1994 Nov;31(6):880–886. doi: 10.1093/jmedent/31.6.880. [DOI] [PubMed] [Google Scholar]
- Weisbrod A. R., Johnson R. C. Lyme disease and migrating birds in the Saint Croix River Valley. Appl Environ Microbiol. 1989 Aug;55(8):1921–1924. doi: 10.1128/aem.55.8.1921-1924.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhioua E., Aeschlimann A., Gern L. Infection of field-collected Ixodes ricinus (Acari: Ixodidae) larvae with Borrelia burgdorferi in Switzerland. J Med Entomol. 1994 Sep;31(5):763–766. doi: 10.1093/jmedent/31.5.763. [DOI] [PubMed] [Google Scholar]