Transhemispheric exchange of Lyme disease spirochetes by seabirds

Infection and Immunity, 2002

The abilities of the most common European genospecies of Borrelia burgdorferi sensu lato to survive blood meals taken by ticks feeding on birds were analyzed. A pattern of differential survival of the spirochetes in feeding ticks was observed. The result is consistent with the concept of selective transmission of Lyme borreliosis spirochetes.

Journal of Medical Entomology, 2016

The genus Borrelia includes species responsible for severe human diseases such as Lyme disease. Birds are involved in their epidemiology as dispersers of infected ticks (Ixodida: Ixodidae) and as reservoirs or amplifiers of the bacterium. Herein, the presence of Borrelia burgdorferi sensu lato (s.l.) Johnson, Schmid, Hyde, Steigerwalt & Brenner in 336 ticks collected from birds in the north of Spain from 2009 to 2011 was investigated. Nucleic acid extracts from 174 Ixodes frontalis (Panzer), 108 Haemaphysalis punctata Canestrini & Fanzango, 34 Hyalomma marginatum Koch, 17 Ixodes ricinus (L.), and 3 Ixodes spp. were screened for the presence of B. burgdorferi s.l. by PCR. Borrelia turdi was detected in 22 I. frontalis, 2 H. punctata, and 2 I. ricinus. Additionally, 1 I. frontalis and 1 H. punctata were found to be infected with the human pathogen Borrelia valaisiana. Moreover, 3 I. frontalis showed coinfection with both Borrelia species. This study corroborates the presence of B. turdi and B. valaisiana in ticks from birds in the north of Spain. The presence of these bacteria in larval specimens could suggest the role of birds as their reservoirs, or the occurrence of the cofeeding phenomenon. In addition, the detection of B. turdi and B. valaisiana in H. punctata and I. frontalis ticks, respectively, is reported for the first time.

Applied and Environmental Microbiology, 2009

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.

Applied and Environmental Microbiology, 2010

The importance of established and emerging tick-borne pathogens in Central and Northern Europe is steadily increasing. In 2007, we collected Ixodes ricinus ticks feeding on birds (n ‫؍‬ 211) and rodents (n ‫؍‬ 273), as well as host-seeking stages (n ‫؍‬ 196), in a habitat in central Germany. In order to find out more about their natural transmission cycles, the ticks were tested for the presence of Lyme disease borreliae, Anaplasma phagocytophilum, spotted fever group (SFG) rickettsiae, Francisella tularensis, and babesiae. Altogether, 20.1% of the 680 ticks examined carried at least one pathogen. Bird-feeding ticks were more frequently infected with Borrelia spp. (15.2%) and A. phagocytophilum (3.2%) than rodent-feeding ticks (2.6%; 1.1%) or questing ticks (5.1%; 0%). Babesia spp. showed higher prevalence rates in ticks parasitizing birds (13.2%) and host-seeking ticks (10.7%), whereas ticks from small mammals were less frequently infected (6.6%). SFG rickettsiae and F. tularensis were also found in ticks collected off birds (2.1%; 1.2%), rodents (1.8%; 1.5%), and vegetation (4.1%; 1.6%). Various combinations of coinfections occurred in 10.9% of all positive ticks, indicating interaction of transmission cycles. Our results suggest that birds not only are important reservoirs for several pathogens but also act as vehicles for infected ticks and might therefore play a key role in the dispersal of tick-borne diseases.

Acta Veterinaria Scandinavica, 2010

Background: Borrelia burgdorferi sensu lato (s.l.) are the causative agent for Lyme borreliosis (LB), the most common tick-borne disease in the northern hemisphere. Birds are considered important in the global dispersal of ticks and tick-borne pathogens through their migration. The present study is the first description of B. burgdorferi prevalence and genotypes in Ixodes ricinus ticks feeding on birds during spring and autumn migration in Norway. Methods: 6538 migratory birds were captured and examined for ticks at Lista Bird Observatory during the spring and the autumn migration in 2008. 822 immature I. ricinus ticks were collected from 215 infested birds. Ticks were investigated for infection with B. burgdorferi s.l. by real-time PCR amplification of the 16S rRNA gene, and B. burgdorferi s.l. were thereafter genotyped by melting curve analysis after real-time PCR amplification of the hbb gene, or by direct sequencing of the PCR amplicon generated from the rrs (16S)-rrl (23S) intergenetic spacer.

International Journal for Parasitology, 2012

Wild birds are important hosts for vector-borne pathogens, especially those borne by ticks. However, few studies have been conducted on the role of different bird species within a community as hosts of vectorborne pathogens. This study addressed individual and species factors that could explain the burden of Ixodes ricinus on forest birds during the reproductive periods of both vectors and hosts. The goal was to identify which bird species contribute the most to the tick population at the community level. Birds were mist-netted on four plots in 2008 and on seven plots in 2009 in two forests (Sénart and Notre Dame, near Paris, France). The dependence of the tick load per bird upon environmental conditions (questing nymph density, year and plot) and on host species traits (species, age, sex, body size, vertical space use, level of innate and acquired immunity) was analysed. Finally, the relative contribution of each bird species to the local dynamics of ticks was estimated, while accounting for their respective abundance. Tick burden differed markedly between bird species and varied according to questing nymph density. Bird species with a high body mass, those that forage low in the vegetation, and those that had a high innate immune response and a high spleen mass were more likely to have a high tick burden. Four species (the Common Blackbird, Turdus merula, the European Robin, Erithacus rubecula, the Song Thrush, Turdus philomelos, and the Winter Wren, Troglodytes troglodytes) hosted more than 90% of the ticks in the local bird community. These species, and particularly T. merula which was host to a high proportion of the nymphs, are likely to contribute significantly to the circulation of pathogens for which they are competent, such as the agent of Lyme borreliosis.

Environmental Microbiology, 2014

Our study tested whether two European birdspecialized ticks, Ixodes arboricola and I. frontalis, can act as vectors in the transmission cycles of Borrelia burgdorferi s.l. The ticks have contrasting ecologies but share songbird hosts (such as the great tit, Parus major) with the generalist I. ricinus which may therefore act as a bridging vector. In the first phase of the experiment, we obtained Borreliainfected ornithophilic nymphs by exposing larvae to great tits that had previously been exposed to I. ricinus nymphs carrying a community of genospecies (Borrelia garinii, valaisiana, afzelii, burgdorferi s.s., spielmanii). Skin samples showed that birds selectively amplified B. garinii and B. valaisiana. The spirochetes were transmitted to the ornithophilic ticks and survived moulting, leading to infection rates of 16% and 27% in nymphs of I. arboricola and I. frontalis respectively. In the second phase, pathogen-free great tits were exposed to the Borreliainfected ornithophilic nymphs. None of these ticks were able to infect the birds, as indicated by the tissue samples. Analysis of xenodiagnostic I. ricinus larvae found no evidence for co-feeding or systemic transmission of B. burgdorferi s.l. These outcomes do not support the occurrence of enzootic cycles of Borrelia burgdorferi s.l. involving songbirds and their specialized ornithophilic ticks.

Biologija, 2011

Wild birds are increasingly considered to be important in the global dispersal of tickborne pathogens as they are capable of transporting infected ticks over large distances. To define the role of migrating birds as hosts and disseminators of infected ticks in Lithuania we analysed immature stage of ticks feeding on different passerine bird species. During autumn 2009 and 2010 we screened 3 959 migrating birds at Ventės Ragas ornithological station and found 7.2% birds infested with ticks. The most infested bird species were Erithacus rubecula and Prunela modularis. We used PCR and sequence analyses for detection and identifying of pathogens in ticks collected from migrating birds. Forty eight tick pools (consisting of 487 Ixodes ricinus ticks) were screened for tick-borne pathogens. Borrelia spp. were detected in 9 tick pools, Babesia spp. in 6 tick pools and Anaplasma phagocytophilum in one tick pool. Three Borrelia species were identified: B. garinii, B. afzelii and B. miyamotoi. The results of the present study showed the pathway of introduction of B. miyamotoi in Lithuania and confirmed the impact of birds on spreading of non-native invasive pathogens in new areas. The present study is the first report of Babesia microti in Lithuania. We did not find tick-borne encephalitis virus (TBEV) in ticks collected from migrating birds. The bird species that carried the highest number of infected ticks were Parus major and Erithacus rubecula.

The spirochete Borrelia garinii, one of three genospecies of B. burgdorferi sensu lato (B. burdorferi s.l.) that can cause Lyme disease in humans, has recently been isolated from seabirds from a colony in Newfoundland, Canada. Previous records of B. garinii in seabirds suggest that it has been endemic in seabird colonies in the greater North Atlantic since at least the early 1990s. We determined the prevalence of B. garinii in different seabird hosts from colonies in the northwest Atlantic. We recorded B. garinii from Gannet Islands, Labrador, and Gull Island, Newfoundland, Canada, in Atlantic Puffins (Fratercula arctica), Herring Gulls (Larus argentatus), Common Murres (Uria aalge), and Razorbills (Alca torda). Prevalence of infections varied between years and within and among species. Ticks from Atlantic Puffins had a prevalence ranging from 10.3 to 36.4%, although the highest prevalence was noted in Herring Gulls (37.5%) in 2005. Earlier studies from the same localities failed to find evidence of B. garinii, suggesting a recent arrival of the spirochete into the northwest Atlantic. B. garinii is closely related to European strains of the spirochete, and its likely source is from areas of endemicity in the Bothnian Gulf and the northeast Atlantic seabird colonies where seabirds, songbirds, and two different tick species come in close proximity. Phylogenetic studies suggest a gradual movement of the European strains into seabird colonies in the northeast Atlantic with subsequent spread into the North and northwest Atlantic colonies. Atlantic Puffins seem to be suitable reservoirs, although other abundant species such as Common Murres and Thick-billed Murres (Uria lomvia) may be involved in B. garinii dynamics. Further work is urgently needed to help document the ecology and spread of this spirochete of importance to human health.

Journal of Vector …, 2011