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Rickettsia Spp. in Bats of Romania: High Prevalence of Rickettsia Monacensis in Two Insectivorous Bat Species Ioana A

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Rickettsia Spp. in Bats of Romania: High Prevalence of Rickettsia Monacensis in Two Insectivorous Bat Species Ioana A Matei et al. Parasites Vectors (2021) 14:107 https://doi.org/10.1186/s13071-021-04592-x Parasites & Vectors RESEARCH Open Access Rickettsia spp. in bats of Romania: high prevalence of Rickettsia monacensis in two insectivorous bat species Ioana A. Matei1*† , Alexandra Corduneanu2†, Attila D. Sándor2,3, Angela Monica Ionica2,4, Luciana Panait2, Zsuzsa Kalmár2, Talida Ivan5, Ionel Papuc5, Cosmina Bouari1, Nicodim Fit1 and Andrei Daniel Mihalca2 Abstract Background: Spotted fever group rickettsiae represent one of the most diverse groups of vector-borne bacteria, with several human pathogenic species showing an emerging trend worldwide. Most species are vectored by ticks (Ixodidae), with many zoonotic reservoir species among most terrestrial vertebrate groups. While the reservoir compe- tence of many diferent vertebrate species is well known (e.g. birds, rodents and dogs), studies on insectivorous bats have been rarely performed despite their high species diversity, ubiquitous urban presence and importance in har- boring zoonotic disease agents. Romania has a high diversity and ubiquity of bats. Moreover, seven out of eight SFG rickettsiae species with zoonotic potential were previously reported in Romania. Based on this, the aim of this study was to detect Rickettsia species in tissue samples in bats. Methods: Here we report a large-scale study (322 bats belonging to 20 species) on the presence of Rickettsia spp. in Romanian bat species. Tissue samples from insectivorous bats were tested for the presence of Rickettsia DNA using PCR detection amplifying a 381 bp fragment of the gltA gene. Positive results were sequenced to confrm the results. The obtained results were statistically analyzed by chi-squared independence test. *Correspondence: [email protected] †Ioana A. Matei and Alexandra Corduneanu contributed equally to this work 1 Department of Microbiology, Immunology and Epidemiology, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, Cluj-Napoca, Romania Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Matei et al. Parasites Vectors (2021) 14:107 Page 2 of 9 Results: Positive results were obtained in 14.6% of bat samples. Sequence analysis confrmed the presence of R. monacensis in two bat species (Nyctalus noctula and Pipistrellus pipistrellus) in two locations. Conclusion: This study provides the frst evidence of a possible involvement of these bat species in the epidemiol- ogy of Rickettsia spp., highlighting the importance of bats in natural cycles of these vector-borne pathogens. Keywords: Chiroptera, Insectivorous bats, SFG rickettsiae, Vector-borne diseases, Zoonotic reservoir Background Candidatus Rickettsia species and strains of unknown Among tick-borne diseases, rickettsioses are considered pathogenicity were also described [1]. Seven of the eight to be the oldest known afecting humanity. Tick-borne human pathogenic species were previously reported in rickettsioses are caused by obligate intracellular bacteria Romania (Table 1) [5–15]. Despite the common detec- belonging to the spotted fever group (SFG) of the genus tion of tick-borne rickettsiae in ticks collected from Rickettsia, one of the most diverse groups among Rick- diverse hosts, to the best of our knowledge, they have ettsiales, comprising a large number of zoonotic agents been reported only in humans and birds in Romania. [1]. Te frst clinical description of the prototypical Romania has a remarkable biodiversity, having in its tick-borne rickettsiosis (Rocky Mountain spotted fever, territory 21 ecoregions in 5 biogeographical regions [16]. RMSF) was made in 1899 by Edward E. Maxey [2]. Its Tis unique situation is associated with a wide range of agent, Rickettsia rickettsii, was demonstrated to have habitats and is mirrored by a very rich fauna including vectorial transmission in 1906 by Howard T. Ricketts [3], 32 species of insectivorous bats [17], more than 82% of which was later confrmed by S. Burt Wolbach [4]. all continental European bat species [18]. Romania is not Tis complex of diseases is still intensively studied, only diverse in species, but also hosts large bat popula- and newly associated clinical conditions are continu- tions, including two of the largest hibernating colonies of ously described. Its importance and recognition have bats from Europe (> 100,000 individuals) [19]. increased considerably over the last 3 decades [1]. More Bats are well-known reservoir hosts for important than 24 Rickettsia species and subspecies are associ- zoonotic viruses such as Lyssavirus and Ebola virus, ated with human infections, while for many others the probable reservoirs for Hendra and Nipah henipaviruses, public health relevance is still unknown [1]. In Europe, MERS and SARS coronaviruses, probably including eight tick-borne rickettsiae with known pathogenic- SARS-CoV-2, and other emerging viruses [20, 21]. Along- ity to humans were reported in European patients: side viruses, in the last few years, bacterial and protozoan R. aeschlimannii, R. conorii subsp. conorii, R. helvet- pathogens from bats have been intensively studied to ica, R. massiliae, R. monacensis, R. raoultii, R. sibirica clarify their zoonotic potential. As a result, several path- subsp. mongolitimonae, and R. slovaca. Additionally, 15 ogens have been identifed in diferent samples (blood, Matei et al. Parasites Vectors (2021) 14:107 Page 3 of 9 Table 1 Review of SFG Rickettsia detected in Romania Rickettsia species Organism Ticks origin References R. aeschlimannii Hyalomma marginatum Cattle [5] R. conorii humans - [6, 7] Rhipicephalus sanguineus Dog [8] R. helvetica Ixodes ricinus Questing [9] I. ricinus Dogs, cattle, horses [8, 10, 11] I. ricinus Humans [12] I. ricinus Erithacus rubecula, Panurus biarmicus, Turdus [13] merula I. arboricola Birds* [13] I. redikorzevi I. ricinus Dogs, foxes, sheep, cats [5]** I. crenulatus Dermacentor reticulatus R. sanguineus R. massiliae humans - [14] I. ricinus T. philomelos [13] I. arboricola D. reticulatus Dogs, foxes [5] R. monacensis I. ricinus Questing [9] I. ricinus E. rubecula, T. merula [13] I. ricinus Dogs, cattle, horses [8, 10] I. ricinus Humans [12] Haemaphysalis concinna Birds* [13] I. ricinus Dogs, foxes, cats [5]** D. reticulatus R. sanguineus R. raoultii humans - [14] D. reticulatus Questing [5, 9] D. reticulatus Dogs [8] D. marginatus Cattle [10] D. reticulatus Dogs, sheep, goats [5]** D. marginatus R. sanguineus R. slovaca humans - [14] D. marginatus Cattle, sheep [10] D. reticulatus Dogs [8] I. ricinus T. merula [13] I. ricinus Dogs, foxes, sheep, goats [5]** D. marginatus R. sanguineus *The bird species is not specifed **Which tick species was collected from which host is not clearly specifed tissues, ectoparasites, guano) such as Babesia spp. [22, tick (Argas vespertilionis and A. transgariepinus) are 23], diferent strains of Bartonella spp. [24, 25], including considered specifc to bats [17]. However, other gener- species with zoonotic potential [26], Borrelia spp., some alist tick species have been occasionally found on bats, with a possible zoonotic potential [27, 28], and Rickettsia including SFG-rickettsiae-vector ticks, such as I. rici- spp. [29, 30]. nus and Haemaphysalis concinna [1, 17, 29], suggesting Bats are hosts for their specifc ectoparasites such as the possibility of harboring these pathogens. bat bugs, fies, feas, mites and ticks (hard and soft). In Motivated by the high diversity and ubiquity of bats in Europe, three species of hard ticks (Ixodes ariadnae, Romania and their potential to harbor SFG rickettsiae, I. simplex and I. vespertilionis) and two species of soft Matei et al. Parasites Vectors (2021) 14:107 Page 4 of 9 the aim of this study was to detect Rickettsia species in confrmed by sequencing (accession no. KR906075). Te tissue samples in bats. negative control consisted of reaction mix without DNA. Te PCR was carried out using a T100TM Termal Cycler Methods (Bio-Rad). PCR products were visualized by electropho- Tissue collection resis in a 1.5% agarose gel stained with SYBR ® Safe DNA Te samples were collected from carcasses of bats acci- gel stain (Invitrogen). dentally killed, mainly by collisions (n = 165), or which DNA sequencing died of natural causes (n = 157). Te collection of car- casses was performed during all-year periods between All positive PCR products were purifed using Isolate 2011-2019. Te majority of naturally caused deaths were II
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