Dissemination of Spotted Fever Rickettsia Agents in Europe by Migrating Birds

Karin Elfving,Sven Bergström,Åke Lundkvist,Hans Mejlon,Björn Olsen,Kenneth Nilsson,Jonas Waldenström,Anders Sjöstedt,Mike B Gravenor

doi:10.1371/journal.pone.0008572

Abstract

Migratory birds are known to play a role as long-distance vectors for many microorganisms. To investigate whether this is true of rickettsial agents as well, we characterized tick infestation and gathered ticks from 13,260 migratory passerine birds in Sweden. A total of 1127 Ixodes spp. ticks were removed from these birds and the extracted DNA from 957 of them was available for analyses. The DNA was assayed for detection of Rickettsia spp. using real-time PCR, followed by DNA sequencing for species identification. Rickettsia spp. organisms were detected in 108 (11.3%) of the ticks. Rickettsia helvetica, a spotted fever rickettsia associated with human infections, was predominant among the PCR-positive samples. In 9 (0.8%) of the ticks, the partial sequences of 17kDa and ompB genes showed the greatest similarity to Rickettsia monacensis, an etiologic agent of Mediterranean spotted fever-like illness, previously described in southern Europe as well as to the Rickettsia sp.IrITA3 strain. For 15 (1.4%) of the ticks, the 17kDa, ompB, gltA and ompA genes showed the greatest similarity to Rickettsia sp. strain Davousti, Rickettsia japonica and Rickettsia heilongjiangensis, all closely phylogenetically related, the former previously found in Amblyomma tholloni ticks in Africa and previously not detected in Ixodes spp. ticks. The infestation prevalence of ticks infected with rickettsial organisms was four times higher among ground foraging birds than among other bird species, but the two groups were equally competent in transmitting Rickettsia species. The birds did not seem to serve as reservoir hosts for Rickettsia spp., but in one case it seems likely that the bird was rickettsiemic and that the ticks had acquired the bacteria from the blood of the bird. In conclusion, migratory passerine birds host epidemiologically important vector ticks and Rickettsia species and contribute to the geographic distribution of spotted fever rickettsial agents and their diseases.

Highlights

The spotted fever group (SFG) rickettsiae are obligate intracellular bacteria transmitted by various arthropods species, which are either vectors and/or reservoirs for the organisms [1]
Because the tick samples had been used for different analyses, extracted DNA from 957 of these ticks representing 529 larvae, 409 nymphs and 19 undetermined or adults collected from 407 birds was available for analyses of Rickettsia spp. (Table S1)
This is the first study to show that migratory passerine birds are an important factor explaining the distribution and expansion of Rickettsia spp., including species associated with spotted fever rickettsioses in humans

Summary

Introduction

The spotted fever group (SFG) rickettsiae are obligate intracellular bacteria transmitted by various arthropods species, which are either vectors and/or reservoirs for the organisms [1]. The members of SFG, which have a worldwide distribution, are mainly associated with ticks, and with fleas and mites [2], and the distribution of the rickettsioses will be identical to that of its competent arthropod vector when the tick serves as a reservoir. Rickettsial species are principally associated with arthropods, they are capable of infecting vertebrates, including humans, in most cases as accidental hosts when bitten by ticks. Rickettsia helvetica is the only spotted fever rickettsia (SFR) reported from Sweden, and documented patients have presented a mild, self-limited disease associated with fever, headaches and myalgias, but an acute febrile clinical picture has been described [4,5]. There is a documented association with perimyocarditis and sudden death [6]

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