Synanthropic Birds Associated with High Prevalence of Tick-Borne Rickettsiae and with the First Detection ofRickettsia aeschlimanniiin Hungary

Abstract

The aim of this study was to analyze synanthropic birds as risk factors for introducing ticks and tick-borne pathogens into human settlements, with an emphasis on rickettsiae. Altogether 184 subadult ticks were found on 5846 birds. Tick infestation was most prevalent during the spring. In this sample group the majority of ticks were molecularly identified as Ixodes ricinus, and three individuals collected from the European robin as Hyalomma marginatum marginatum. The latter is the first molecularly confirmed occurrence of this species in Hungary. Rickettsia aeschlimannii was detected in H. marginatum, also for the first time in Hungary, and in ticks from an urbanized bird species north of the Mediterranean countries. The overall prevalence range of rickettsiae (including R. helvetica and R. monacensis) in ticks of synanthropic birds was 29-40%, exceeding that in questing ticks of relevant species reported earlier. Additionally, in specimens of I. ricinus, the presence of Borrelia burgdorferi sensu lato (s.l.), Anaplasma phagocytophilum, and a new Francisella-like genotype was also verified. Thus, it can be concluded that birds with urban or periurban habitats pose a high risk as tick carriers and reservoirs of zoonotic agents, especially of rickettsiae. The aim of this study was to analyze synanthropic birds as risk factors for introducing ticks and tick-borne pathogens into human settlements, with an emphasis on rickettsiae. Altogether 184 subadult ticks were found on 5846 birds. Tick infestation was most prevalent during the spring. In this sample group the majority of ticks were molecularly identified as Ixodes ricinus, and three individuals collected from the European robin as Hyalomma marginatum marginatum. The latter is the first molecularly confirmed occurrence of this species in Hungary. Rickettsia aeschlimannii was detected in H. marginatum, also for the first time in Hungary, and in ticks from an urbanized bird species north of the Mediterranean countries. The overall prevalence range of rickettsiae (including R. helvetica and R. monacensis) in ticks of synanthropic birds was 29-40%, exceeding that in questing ticks of relevant species reported earlier. Additionally, in specimens of I. ricinus, the presence of Borrelia burgdorferi sensu lato (s.l.), Anaplasma phagocytophilum, and a new Francisella-like genotype was also verified. Thus, it can be concluded that birds with urban or periurban habitats pose a high risk as tick carriers and reservoirs of zoonotic agents, especially of rickettsiae.

Anaplasma phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies

“…Studies from Europe indicate that migrating birds may be important in the dispersal of A. phagocytophilum infected I. ricinus (Alekseev et al, 2001b; Bjöersdorff et al, 2001). However, A. phagocytophium DNA has sometimes been detected in ticks collected from birds at low prevalence, and it was questioned by some authors whether birds may really be involved in the spreading of the pathogen whereas other authors discussed their possible involvement (Daniels et al, 2002; Ogden et al, 2008; Franke et al, 2010; Hildebrandt et al, 2010a; Dubska et al, 2012; Palomar et al, 2012; Hornok et al, 2013; Kang et al, 2013). The involvement of birds and their ticks in the life cycle of A. phagocytophilum has also been tested in a transmission study in the US.…”

Birds as disseminators of ixodid ticks and tick-borne pathogens: note on the relevance to migratory routes

“…In all three specimens of these ticks Rickettsia aeschlimannii was identifi ed, also for the fi rst time in Hungary (Hornok et al 2013). This bacterial pathogen is responsible for spotted fever in humans and is endemic to the Mediterranean countries.…”

“…Additionally, from an I. ricinus larva also obtained from a Robin the sequence of a novel Francisella-like genotype was identifi ed (Hornok et al 2013). This endosymbiont is taxonomically close to the causative agent of tularemia in mammals.…”

“…However, in most (if not all) of the reports concerned about the import of exotic tick species and tick-borne pathogens by birds into regions formerly exempt of them focus on epidemiological implications. Therefore in this note the authors would like to highlight that some fi ndings in the fi rst molecular study on ticks and tick-borne pathogens associa ted with migratory birds in Hungary (Hornok et al 2013) show that tracking the possible geographical origin of DNA sequences from ticks or tick-borne pathogens carried by birds may be relevant to their migratory routes (and vica versa).…”

“…From 1.786 birds caught in the spring 108 subadult ticks were collected (Hornok et al 2013). The majority (96.3%) of them was Ixodes ricinus, but three Hyalomma immatures (two moulting larvae and one nymph) were also collected from a Robin (Erithacus rubecula).…”