Characterization of Borrelia burgdorferi isolated from different organs of Ixodes ricinus Ticks collected in nature

Leuba-Garcia, S.; Kramer, Michael D.; Wallich, R; Gern, Lise

doi:10.1016/s0934-8840(11)80506-2

Cited by 37 publications

(31 citation statements)

References 13 publications

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“…In contrast, a study by Kahl et al (13) with B. burgdorferi sensu lato-infected I. ricinus revealed that infection of Mongolian gerbils occurred as early as 16.7 h after the start of a tick blood meal. Further evidence that early transmission may occur in Europe is given by the high salivary gland infection rates found in unfed I. ricinus: 36% in adult ticks and up to 22% in nymphal ticks collected in different parts of Switzerland (14,15). Borreliae already present in the salivary glands might be transmitted much earlier to a host than those residing in the midgut.…”

Section: Discussionmentioning

confidence: 99%

Dynamics of Dissemination and Outer Surface Protein Expression of Different European Borrelia burgdorferi Sensu Lato Strains in Artificially Infected Ixodes ricinus Nymphs

et al. 2002

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Unfed Ixodes ricinus nymphs were infected with eight different strains and clones of Borrelia afzelii and B. garinii by capillary feeding. Except one B. afzelii clone, all expressed OspC in culture. Tick midguts and salivary glands were investigated at different time intervals for the presence of borreliae and for OspA and OspC phenotypes by immunofluorescence with simultaneous staining of OspA and OspC with monoclonal antibodies. Both species were transmittable to I. ricinus. All OspC-expressing strains and clones were able to disseminate into the salivary glands. In contrast, the OspC-negative B. afzelii clone was not detectable in the salivary glands, an indication that OspC plays an important role in dissemination. OspA-positive borreliae prevailed in the midgut. OspC positives were more frequent in the salivary glands than in the midgut. Notably, simultaneously OspA-and OspC-negative borreliae were detected in both organs. Kinetics of dissemination varied with the strains. The OspC-positive B. afzelii clone and all B. garinii OspA type 4 strains were detectable in the salivary glands right after feeding, while one B. garinii OspA type 6 strain invaded the salivary glands with a delay of 24 h. These findings support the hypothesis that OspA is abundantly expressed in unfed ticks while upregulation of OspC is also a prerequisite for dissemination in the vector for the Eurasian species B. afzelii and B. garinii. However, we found strain-specific dynamics of Osp expression and strain-specific kinetics of systemic infection in the vector tick and it appears that additional factors are involved in the initiation and regulation of the dissemination process.The Borrelia burgdorferi sensu lato complex comprises at least three human-pathogenic species, all of which are present in Europe: B. burgdorferi sensu stricto, the only species causing Lyme borreliosis in the United States; B. afzelii; and B. garinii (1, 3). These spirochetes alternate in nature between endothermic hosts (mammals) and poikilothermic vectors (hard ticks within the genus Ixodes). In the vector, the spirochetes restart replication during the feeding process, migrate through the gut wall, and invade various tissues, including the salivary glands, wherefrom they are transmitted to the host via saliva (2,7,11,25,27,36). The borreliae are confronted with abrupt environmental changes during this cycling, such as differences in temperature, pH, the immune system, or osmotic pressure. To cope with these rapid changes, effective regulatory mechanisms for adaptation are required. Alteration of the outer surface protein (Osp) expression pattern-especially that of OspA and OspC-seems to be crucial for this adaptation process; expression of these two proteins varies even under routine culture conditions and seems to be inversely correlated (5,29,30,31). Elevated temperature and cocultivation with tick cells have been shown to induce OspC expression (10,20,26,28). OspA is abundantly expressed in unfed ticks, possibly mediating adherence to midgut cells and thu...

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Section: Discussionmentioning

confidence: 99%

Dynamics of Dissemination and Outer Surface Protein Expression of Different European Borrelia burgdorferi Sensu Lato Strains in Artificially Infected Ixodes ricinus Nymphs

et al. 2002

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“…Isolation of B. burgdorferi sensu lato Organs were cultured in 4 ml of BSK (Barbour-Stoener-Kelly) II medium prepared as previously described (7), supplemented with 6% of rabbit serum (BSK-RS) (Sigma-Aldrich Quimica S.A., Alcobendas, Madrid, Spain), 50 g of rifampin/ml, 50 g of phosphomycin/ml, and 2.5 g of amphotericin B/ml (52,76). Before the preparation of the BSK medium, five batches of bovine serum albumin (Sigma) were tested to judge the medium's performance with low-passage autochthonous strains; the best was used to make 12-liter batches of medium.…”

Section: Methodsmentioning

confidence: 99%

Identification of a New Borrelia Species among Small Mammals in Areas of Northern Spain Where Lyme Disease Is Endemic

Gil

Barral

Escudero

et al. 2005

Appl Environ Microbiol

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The role of small mammals as reservoir hosts for Borrelia burgdorferi was investigated in several areas where Lyme disease is endemic in northern Spain. A low rate of infestation by Ixodes ricinus nymphs was found in the small mammal populations studied that correlated with the near-absence of B. burgdorferi sensu lato in 184 animals tested and with the lack of transmission of B. burgdorferi sensu lato to I. ricinus larvae that fed on them. In contrast, questing ticks collected at the same time and in the same areas were found to carry a highly variable B. burgdorferi sensu lato repertoire (B. burgdorferi sensu stricto, Borrelia garinii, Borrelia valaisiana, and Borrelia afzelii). Interestingly, the only isolate obtained from small mammals (R57, isolated from a bank vole) grouped by phylogenetic analyses with other Borrelia species but in a separate clade from the Lyme disease and relapsing fever organisms, suggesting that it is a new species. This new agent was widely distributed among small mammals, with infection rates of 8.5 to 12% by PCR. Moreover, a high seroprevalence to B. burgdorferi sensu lato was found in the animal sera, suggesting cross-reactivity between B. burgdorferi sensu lato and R57. Although small mammals do not seem to play an important role as reservoirs for B. burgdorferi sensu lato in the study area, they seem to be implicated in the maintenance of spirochetes similar to R57.

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“…During the tick feeding period, borreliae residing in the tick's midgut are induced to migrate through the tick hemolymph to the salivary glands and subsequently are injected into the host (1,5,15). Although there may be borreliae present in the salivary glands of unfed ticks, these organisms do not appear to be infectious (8,18). Borreliae capable of infection do not regularly reach the salivary glands until approximately 60 to 72 h postattachment (12).…”

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confidence: 99%

Inhibition of Borrelia burgdorferi Migration from the Midgut to the Salivary Glands following Feeding by Ticks on OspC-Immunized Mice

Gilmore

Piesman

2000

Infect Immun

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Borrelia burgdorferi-infected ticks were fed on either OspC-immunized mice or normal, nonimmunized mice. After 72 h, the ticks were detached, followed by dissection and subsequent culturing in Barbour-StoennerKelley II medium of the salivary glands from each tick to determine the presence of borreliae. Forty percent (10 of 25) of salivary glands from ticks that had fed on nonimmunized mice were culture positive, while only 7.4% (2 of 27) of salivary glands from ticks that had fed on OspC-immunized mice were culture positive, thus indicating a much reduced borrelial migration from the midgut when the bloodmeal contained anti-OspC antibodies. Fluorescent antibody staining of the corresponding midguts from ticks that had fed on the OspC-immunized mice showed that borreliae were present but did not produce OspC. In contrast, borreliae in midguts from ticks that had fed on normal mice demonstrated substantial ospC expression. This study provides evidence that, during tick feeding on an OspC-immunized host, transmission of borreliae from the tick is prevented; it also suggests that OspC functions in a tick-to-host transmission mechanism.

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Characterization of Borrelia burgdorferi isolated from different organs of Ixodes ricinus Ticks collected in nature

Cited by 37 publications

References 13 publications

Dynamics of Dissemination and Outer Surface Protein Expression of Different European Borrelia burgdorferi Sensu Lato Strains in Artificially Infected Ixodes ricinus Nymphs

Dynamics of Dissemination and Outer Surface Protein Expression of Different European Borrelia burgdorferi Sensu Lato Strains in Artificially Infected Ixodes ricinus Nymphs

Identification of a New Borrelia Species among Small Mammals in Areas of Northern Spain Where Lyme Disease Is Endemic

Inhibition of Borrelia burgdorferi Migration from the Midgut to the Salivary Glands following Feeding by Ticks on OspC-Immunized Mice

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