Blackbirds (Turdus merula) and song thrushes (Turdus philomelos) were found to carry 95% of all spirocheteinfected tick larvae among 40 bird species captured in Central Europe. More than 90% of the infections were typed as Borrelia garinii and Borrelia valaisiana. We conclude that thrushes are key players in the maintenance of these spirochete species in this region of Central Europe.Lyme borreliosis is a tick-transmitted zoonosis caused by spirochete bacteria from the genus Borrelia. This genus comprises 13 named species, and at least 4 of these cause disease in humans, namely, Borrelia burgdorferi, Borrelia spielmanii, Borrelia afzelii, and Borrelia garinii (1,14). All known strains of Lyme borreliosis spirochetes are maintained in nature by vertebrate hosts and ixodid ticks, with humans being ecological dead-end hosts.For Europe, pheasants (Phasianus colchicus), a few seabird species, and some passerine bird species have been shown to be reservoir competent for B. garinii and B. valaisiana but not for B. afzelii, a rodent specialist (4,5,6,7,13). However, little is known about the roles of the numerous European woodland bird species in the ecology of Lyme borreliosis spirochetes (2, 13). Therefore, we captured birds of a wide range of species, many of which are migratory, and determined their importance as hosts to ticks and as reservoirs for Lyme borreliosis spirochetes in selected sites of Central Europe.Ticks were collected from birds captured in four woodlands in Slovakia (16) during 2001 and 2002 and, in 2003, at one woodland in the southeastern Czech Republic. Questing adult and nymphal Ixodes ricinus ticks were collected from Slovak sites. Extracted DNA (3) was subjected to nested PCR targeting the 5S-23S intergenic spacer and also, in some cases, the flaB gene of Lyme borreliosis spirochetes (8, 15). Spirochete infections determined in ticks were assigned to species by the reverse line blot assay (5,8,15) or by DNA sequencing.Risk factors for tick infestation and infection with B. burgdorferi genospecies were investigated in negative binomial and logistic regression models, respectively. Explanatory variables were month, year, site, and bird species. Data from the Czech Republic were excluded because of differences in collection year and bird species range. The level of significance was set at a P value of Ͻ0.05. Because of the poor fit of Poisson regression models, the negative binomial models were used. For detailed statistical methods and results, see the supplemental material.Tick infestations of birds. Of 529 birds captured (345 and 184 at sites in Slovakia and the Czech Republic, respectively, comprising 40 species of 17 families), 187 (145 in Slovakia and 42 in the Czech Republic) carried I. ricinus (463 and 157 larvae and 375 and 495 nymphs in Slovakia and the Czech Republic, respectively) (Table 1). In Slovakia, blackbirds (Turdus merula), song thrushes (Turdus philomelos), and European robins (Erithacus rubecula) carried 55.6% of all collected I. ricinus ticks. In the Czech Republic, Europea...
Borrelia spirochetes in bird-feeding ticks were studied in the Czech Republic. During the postbreeding period (July to September 2005), 1,080 passerine birds infested by 2,240 Ixodes ricinus subadult ticks were examined. Borrelia garinii was detected in 22.2% of the ticks, Borrelia valaisiana was detected in 12.8% of the ticks, Borrelia afzelii was detected in 1.6% of the ticks, and Borrelia burgdorferi sensu stricto was detected in 0.3% of the ticks. After analysis of infections in which the blood meal volume and the stage of the ticks were considered, we concluded that Eurasian blackbirds (Turdus merula), song thrushes (Turdus philomelos), and great tits (Parus major) are capable of transmitting B. garinii; that juvenile blackbirds and song thrushes are prominent reservoirs for B. garinii spirochetes; that some other passerine birds investigated play minor roles in transmitting B. garinii; and that the presence B. afzelii in ticks results from infection in a former stage. Thus, while B. garinii transmission is associated with only a few passerine bird species, these birds have the potential to distribute millions of Lyme disease spirochetes between urban areas.Lyme borreliosis, the most frequent tick-borne human disease in the northern hemisphere, is a multisystemic disorder caused by spirochetes belonging to the genus Borrelia (12). At least seven Borrelia species have been obtained from the tick Ixodes ricinus (Acari: Ixodidae) in Europe: B. afzelii, B. bissettii, B. burgdorferi, B. garinii, B. lusitaniae, B. spielmanii, and B. valaisiana (30,33). Various reservoir hosts seem to harbor different Borrelia species, which is explained by differential properties of the hosts' complement systems (17). Generally, B. afzelii is a rodent specialist, B. garinii and B. valaisiana are associated with birds, and B. lusitaniae is associated with lizards (7,16,22,32). The clinical manifestations of Lyme borreliosis in humans differ depending on the Borrelia species; B. garinii is associated with neurological diseases, while B. burgdorferi and B. afzelii are more likely to cause arthritis and cutaneous symptoms, respectively (2, 4, 5, 36).Ixodid ticks may attach to a host for 24 to 48 h, which is sufficient time for some birds to travel hundreds of kilometers along migration routes before ticks complete their feeding and drop off (31). The role of migratory birds in distributing Lyme disease spirochetes to new areas has been established in North America (25,28,37).Recently, it has become clear that the bird host competency for maintaining and transmitting Borrelia spirochetes is different in different bird species. Pheasants in the United Kingdom (15, 16) and blackbirds and song thrushes in Central Europe (13, 35) have been shown to be important reservoirs of B. garinii and B. valaisiana. However, little is known about the other migrating passerine bird species with respect to their competence as Lyme disease reservoirs and transmission abilities.Here we characterized tick infestation in migratory passerine bird species ...
BackgroundFree-living ungulates are hosts of ixodid ticks and reservoirs of tick-borne microorganisms in central Europe and many regions around the world. Tissue samples and engorged ticks were obtained from roe deer, red deer, fallow deer, mouflon, and wild boar hunted in deciduous forests of south-western Slovakia. DNA isolated from these samples was screened for the presence of tick-borne microorganisms by PCR-based methods.ResultsTicks were found to infest all examined ungulate species. The principal infesting tick was Ixodes ricinus, identified on 90.4% of wildlife, and included all developmental stages. Larvae and nymphs of Haemaphysalis concinna were feeding on 9.6% of wildlife. Two specimens of Dermacentor reticulatus were also identified. Ungulates were positive for A. phagocytophilum and Theileria spp. Anaplasma phagocytophilum was found to infect 96.1% of cervids, 88.9% of mouflon, and 28.2% of wild boar, whereas Theileria spp. was detected only in cervids (94.6%). Importantly, a high rate of cervids (89%) showed mixed infections with both these microorganisms. In addition to A. phagocytophilum and Theileria spp., Rickettsia helvetica, R. monacensis, unidentified Rickettsia sp., Coxiella burnetii, “Candidatus Neoehrlichia mikurensis”, Borrelia burgdorferi (s.l.) and Babesia venatorum were identified in engorged I. ricinus. Furthermore, A. phagocytophilum, Babesia spp. and Theileria spp. were detected in engorged H. concinna. Analysis of 16S rRNA and groEL gene sequences revealed the presence of five and two A. phagocytophilum variants, respectively, among which sequences identified in wild boar showed identity to the sequence of the causative agent of human granulocytic anaplasmosis (HGA). Phylogenetic analysis of Theileria 18S rRNA gene sequences amplified from cervids and engorged I. ricinus ticks segregated jointly with sequences of T. capreoli isolates into a moderately supported monophyletic clade.ConclusionsThe findings indicate that free-living ungulates are reservoirs for A. phagocytophilum and Theileria spp. and engorged ixodid ticks attached to ungulates are good sentinels for the presence of agents of public and veterinary concern. Further analyses of the A. phagocytophilum genetic variants and Theileria species and their associations with vector ticks and free-living ungulates are required.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-3068-1) contains supplementary material, which is available to authorized users.
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