Bartonella washoensis infection in red squirrels (Sciurus vulgaris) and their ectoparasites in Lithuania

https://doi.org/10.1016/j.cimid.2019.101391Get rights and content

Highlights

  • Bartonella washoensis was detected in red squirrels and their ectoparasites.

  • Ceratophyllus sciurorum fleas were more infected with B. washoensis than Ixodes ricinus ticks.

  • Infection of B. washoensis varied in different internal organs of squirrels.

  • It is a first report of B. washoensis detection in Europe.

Abstract

This is the first study to investigate the presence of Bartonella infections in different internal organs of red squirrels and their ectoparasites in Lithuania. A total of 39 roadkill red squirrels were collected. Squirrels were infested with Ixodes ricinus ticks (191) and Ceratophyllus sciurorum fleas (36). The presence of Bartonella spp. was screened using 16 S–23 S rRNA internal transcribed spacer region and bacteria were detected in 38.5 % (15/39) samples of squirrels, 1.0 % (2/191) samples of ticks and 55.5 % (20/36) samples of fleas. The infection rate of different internal organs of squirrels varied from 11.1%–47.4%. The 16 S–23 S rRNA ITS region sequences showed that Bartonella washoensis were detected in squirrels and their ectoparasites. The results from this study support the hypothesis that S. vulgaris and their fleas, C.sciurorum, serve as a major reservoir and a vector, respectively, of zoonotic B. washoensis in Lithuania.

Introduction

Bartonella are facultative intracellular, Gram-negative bacteria that are transmitted by bloodsucking arthropod vectors. Bartonella species has been described in a wide range of wild and domestic mammals [1,2]. Over the last 10 years new Bartonella species have been described. Currently, the genus Bartonella contains 46 species, of which at least 15 species are known to cause diseases for human [[3], [4], [5]].

Rodents are natural reservoirs of about 20 Bartonella species. Various Bartonella species have been detected almost from 100 rodent species worldwide [2]. Fleas (Siphonaptera) plays an important role in the transmission of Bartonella pathogen among rodents [6]. The number of rodent-associated Bartonella species is growing [5]. Some Bartonella species have low specificity for host, while others infect a single host species [3]. Therefore, investigations of diversity of Bartonella spp. in different hosts and detection of potential reservoirs are necessary.

In Europe, the presence of Bartonella infection in squirrels has been detected only in the United Kingdom and Georgia [7,8]. The Eurasian red squirrel (Sciurus vulgaris Linnaeus, 1758) has a large distribution range in the Palearctic region. It is widespread in Europe, but in some areas the population is decreasing and listed as Near Threatened [9]. Red squirrels and other rodents are found in parks, gardens and urban areas which may pose a risk to people, because small mammals have close contact with humans and can transmit pathogens via ectoparasites [[10], [11], [12], [13], [14]].

In Lithuania, Bartonella grahamii, B. tailorii and B. rochalimae were detected in several species of small rodents [15]. Also some clinical cases of bartonellosis in human were documented [16,17]. However, not all cases were reported and Bartonella-vector-host interaction in transmission of disease is not clear in Lithuania. There are limited information about pathogens in squirrels and their ectoparasites in Europe [7,8,10,18]. In the present study, we aimed to investigate the presence of Bartonella infections in red squirrels and their ectoparasites in Lithuania using molecular tools. The presence of Bartonella was examined in different internal organs of red squirrel as well as in their ectoparasites.

Section snippets

Sample collecting

Roadkill red squirrels were collected during 2001–2016 in Lithuania from 17 different locations (Fig. 1). All squirrels were stored in individual plastic bags, labelled as to date and location. In the laboratory, animals were examined for ectoparasites and necropsied. Ectoparasites were placed into 1.5 ml tubes with 70 % ethanol and kept at 4 °C until investigation. Fleas and ticks species were identified based on morphological criteria [19,20]. Also different internal organs (spleen, lungs,

Results

A total of 39 roadkill red squirrels were collected of which 10 (25.6 %) were infested with ectoparasites. A total of 227 ectoparasites of 2 different species were collected. The number of parasite per host ranged between 1 and 68. Altogether, 191 Ixodes ricinus ticks (1 male, 2 females, 159 nymphs, 29 larvae) were collected from 9 (23.1 %) squirrels; 36 fleas of Ceratophyllus (Monopsyllus) sciurorum species (16 males and 20 females) were collected from 8 (20.5 %) squirrels.

Six dead squirrels

Discussion

Studies of Bartonella infection in rodents and their ectoparasites have suggested that they play important role in the transmission of Bartonella spp. [2,3,15,25,26]. A same rodent can be infected with more than one Bartonella spp. or genetic variants. Also a same Bartonella spp. can be presented in more than one rodent species [2,15,26]. In the present study, 8 B. washoensis strains in red squirrels and their ectoparasites were detected based on 16S–23S rRNA ITS region sequence analysis. This

Conclusion

The results from this study suppose that S. vulgaris and their fleas, C.sciurorum, serve as a reservoir and a vector, respectively, of zoonotic B. washoensis in Lithuania. Furthermore, we detected that I. ricinus does not play an important role in the transmission of B. washoensis in red squirrels. The data presented in this paper extend the knowledge on the distribution of B. washoensis. Till now B. washoensis has never been detected in Lithuania. This is the first report of B. washoensis in

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest

The authors declare that there are no conflicts of interest.

Acknowledgments

The authors thank Ieva Jankauskaitė for technical assistance.

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