Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area

Abstract

BackgroundA few billion birds migrate annually between their breeding grounds in Europe and their wintering grounds in Africa. Many bird species are tick-infested, and as a result of their innate migratory behavior, they contribute significantly to the geographic distribution of pathogens, including spotted fever rickettsiae. The aim of the present study was to characterize, in samples from two consecutive years, the potential role of migrant birds captured in Europe as disseminators of Rickettsia-infected ticks.MethodsTicks were collected from a total of 14,789 birds during their seasonal migration northwards in spring 2009 and 2010 at bird observatories on two Mediterranean islands: Capri and Antikythira. All ticks were subjected to RNA extraction followed by cDNA synthesis and individually assayed with a real-time PCR targeting the citrate synthase (gltA) gene. For species identification of Rickettsia, multiple genes were sequenced.ResultsThree hundred and ninety-eight (2.7%) of all captured birds were tick-infested; some birds carried more than one tick. A total number of 734 ticks were analysed of which 353 ± 1 (48%) were Rickettsia-positive; 96% were infected with Rickettsia aeschlimannii and 4% with Rickettsia africae or unidentified Rickettsia species. The predominant tick taxon, Hyalomma marginatum sensu lato constituted 90% (n = 658) of the ticks collected. The remaining ticks were Ixodes frontalis, Amblyomma sp., Haemaphysalis sp., Rhipicephalus sp. and unidentified ixodids. Most ticks were nymphs (66%) followed by larvae (27%) and adult female ticks (0.5%). The majority (65%) of ticks was engorged and nearly all ticks contained visible blood.ConclusionsMigratory birds appear to have a great impact on the dissemination of Rickettsia-infected ticks, some of which may originate from distant locations. The potential ecological, medical and veterinary implications of such Rickettsia infections need further examination.

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

“…While no virus was detected, as was the case in similar surveys (27,44,46), Rickettsia was prevalent in H. rufipes and H. marginatum complex ticks from birds (34.6% and 81.3%, respectively). The sequenced SFGR samples were identified as R. aeschlimannii, a prevalent tick-borne SFGR in the African continent, previously detected in ticks from migratory birds arriving to Europe (49,50). Rickettsia aeschlimannii is more common in northern Africa, and its high prevalence might point to the wintering location of the tick-infested birds (49).…”

“…The sequenced SFGR samples were identified as R. aeschlimannii, a prevalent tick-borne SFGR in the African continent, previously detected in ticks from migratory birds arriving to Europe (49,50). Rickettsia aeschlimannii is more common in northern Africa, and its high prevalence might point to the wintering location of the tick-infested birds (49). The most commonly tickinfested bird species in this study, Sylvia atricapilla, may occasionally winter in the area (45), suggesting that the majority of the ticks inspected originated from northern Africa.…”

Serological evidence of exposure to zoonotic tick-borne bacteria in pheasants (Phasianus colchicus)

“…Previous surveys carried out in Europe have found DNA of SFG rickettsiae in ticks collected from birds, underling the role of migratory birds in the dispersal of tick-borne agents. In particular, recent molecular studies have detected Rickettsia spp., mainly R. aeschlimannii and R. africae, in ticks collected from migratory birds in European Mediterranean areas [5,28]. However, the competence of birds to function as Rickettsia reservoir capable of transmitting and infecting ticks with rickettsiae is not yet completely understood [29].…”

Rickettsia species in human-parasitizing ticks in Greece

“…However, it has to be mentioned that R. africae has been detected in the spring of 2010 in H. marginatum larva and nymphs on migratory birds (common redstart, song thrush, and Eurasian siskin) which landed on a Greek island (Antikythira). 21 Hyalomma ticks which attach as unfed larvae to migrating birds can remain up to 4 weeks on the same bird and may be transported long distances, e.g., from sub-Saharan Africa to northern Europe. 21 R. africae is known to be transmitted by Amblyomma ticks in sub-Saharan Africa and the French West Indies causing African tick bite fever characterized by fever and multiple eschars.…”

“…21 Hyalomma ticks which attach as unfed larvae to migrating birds can remain up to 4 weeks on the same bird and may be transported long distances, e.g., from sub-Saharan Africa to northern Europe. 21 R. africae is known to be transmitted by Amblyomma ticks in sub-Saharan Africa and the French West Indies causing African tick bite fever characterized by fever and multiple eschars. 22 The detection of R. africae in 4.5% (6/132) of the Rh.…”