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Circulation of Rickettsia species and rickettsial endosymbionts among small mammals and their ectoparasites in Eastern Slovakia

  • Arthropods and Medical Entomology - Original Paper
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Abstract

Bacteria belonging to the genus Rickettsia are known as causative agents of vector-borne zoonotic diseases, such as spotted fevers, epidemic typhus and endemic typhus. Different species of ticks, mites and fleas could act as reservoirs and arthropod vectors of different pathogenic Rickettsia species. The aim of this work was to establish active surveillance of Rickettsia spp. in mites, ticks and fleas collected from small mammals (rodents and shrews) in Eastern Slovakia. A total of 964 animal ear biopsies, 871 mites, 667 ticks and 743 fleas were collected from small mammals in the Košice region, Eastern Slovakia. All specimens were identified using specialized taxonomic keys, and were conserved in ethanol until DNA extraction was performed. After DNA extraction, identification of Rickettsia species was performed by PCR-based methods. The total prevalence of rickettsiae from ear biopsies was 4.6% (95% CI, 3.2–5.9), in tested mites 9.3% (95% CI, 7.4–11.2), 17.2% (95% CI, 14.3–20.1) in I. ricinus ticks and 3.5% (95% CI, 2.2–4.8) in fleas. Sequence analysis of the partial gltA gene and Rickettsia helvetica-, Rickettsia slovaca-, Rickettsia raoultii- species specific real-time PCR tests revealed the presence of R. helvetica, R. slovaca, unidentified Rickettsia and rickettsial endosymbionts. These pathogenic and symbiotic species were confirmed in the following ectoparasite species—Laelaps jettmari, Haemogamasus nidi, Laelaps agilis and Eulaelaps stabularis mites, Ixodes ricinus ticks, Ctenophthalmus solutus, C. assimilis and Megabothris turbidus fleas infesting host—Apodemus agrarius, A. flavicollis, Microtus arvalis and Myodes glareolus small mammals. These results confirm the circulation of R. helvetica, R. slovaca, unidentified Rickettsia and rickettsial endosymbionts in mites, ticks and fleas collected on small mammals in the Košice region, Eastern Slovakia.

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References

  • Antolová D, Reiterová K, Miterpáková M, Stanko M, Dubinský P (2004) Circulation of Toxocara spp. in suburban and rural ecosystems in the Slovak Republic. Vet Parasitol 126(3):317–324

    PubMed  Google Scholar 

  • Azad AF, Beard CB (1998) Rickettsial pathogens and their arthropods vectors. Emerg Infect Dis 4:179–186

    PubMed  PubMed Central  CAS  Google Scholar 

  • Badiertakis EG, Fantinou AA, Emmanouel NG (2014) A qualitative and quantitative study of mite in similar alfalfa fields in Greece. Exp Appl Acarol 62:195–214

    Google Scholar 

  • Blair PJ, Jiang J, Schoeler GB, Moron C, Anaya E, Cespedes M, Cruz C, Felices V, Guevara C, Mendoza L, Villaseca P, Sumner JW, Richards AL, Olson JG (2004) Characterization of spotted fever group Rickettsiae in flea and tick specimens from North Peru. J Clin Microbiol 42:4961–4967

    PubMed  PubMed Central  CAS  Google Scholar 

  • Blaňarová L, Stanko M, Carpi G, Miklisová D, Víchová B, Mošanský L, Bona M, Derdáková M (2014) Distinct Anaplasma phagocytophilum genotypes associated with Ixodes trianguliceps ticks and rodents in Central Europe. Ticks Tick-Borne Dis 5(6):928–938

    PubMed  Google Scholar 

  • Blaňarová L, Stanko M, Miklisová D, Víchová B, Mošanský L, Kraljik J, Bona M, Derdáková M (2016) Presence of Candidatus Neoehrlichia mikurensis and Babesia microti in rodents and two tick species (Ixodes ricinus and Ixodes trianguliceps) in Slovakia. Ticks Tick-Borne Dis 7(2):319–326

    PubMed  Google Scholar 

  • Boretti FS, Perreten A, Meli MM, Cattori V, Willi B, Wengi N et al (2009) Molecular investigation of Rickettsia helvetica infection in dogs, foxes, humans, and Ixodes ticks. Appl Environ Microbiol 75:3230–3237

    PubMed  PubMed Central  CAS  Google Scholar 

  • Brinkerhoff RJ, Kabeya H, Inoue K, Bai Y, Maruyama S (2010) Detection of multiple Bartonella species in digestive and reproductive tissues of fleas collected from sympatric mammals. Multidisciplinary J Microbial Ecol 4(7):955–958

    Google Scholar 

  • Bullová E, Lukáň M, Stanko M, Peťko B (2009) Spatial distribution of Dermacentor reticulatus tick in Slovakia in the beginning of the 21st century. Vet Parasitol 165:357–360

    PubMed  Google Scholar 

  • Burri C, Schumann O, Schumann C, Gern L (2014) Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, “Candidatus Neoehrlichia mikurensis”, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick Borne Dis 5:245–251

    PubMed  CAS  Google Scholar 

  • Caspi-Fluger A, Inbar M, Steinberg S, Friedmann Y, Freund M, Mozes-Daube N, Zchori-Fein E (2014) Characterization of the symbiont Rickettsia in the mirid bug Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae). Bull Entomol Res 104:681–688

    PubMed  CAS  Google Scholar 

  • Choi YJ, Jang WJ, Ryu JS, Lee SH, Park KH, Paik HS, Koh YS, Choi MS, Kim IS (2005) Spotted fever group and typhus group rickettsioses in humans, South Korea. Emerg Infect Dis 11(2):237–244

    PubMed  PubMed Central  CAS  Google Scholar 

  • Choi YJ, Lee EM, Park JM, Lee KM, Han SH, Kim JK, Lee SH, Song HJ, Choi MS, Kim IS, Park KH, Jang WJ (2007) Molecular detection of various rickettsiae in mites (Acari: Trombiculidae) in southern Jeolla province, Korea. Microbiol Immunol 51:307–312

    PubMed  CAS  Google Scholar 

  • Čisláková L, Stanko M, Fričová J, Mošanský L, Trávniček M, Halánová M, Mardzinová S, Štefančíková A (2004) Small mammals (Insectivora, Rodentia) as a potential source of chlamydial infection in East Slovakia. Ann Agricult Environ Med 11:139–143

    Google Scholar 

  • Čondlová Š, Horčičková M, Sak B, Květonová D, Hlásková L, Konečný R, Stanko M, McEvoy J, Kváč M (2018) Cryptosporidium apodemi sp. n. and Cryptosporidium ditrichi sp. n. (Apicomplexa: Cryptosporidiidae) in Apodemus spp. Eur J Protistol 63:1–12

    PubMed  Google Scholar 

  • Cyprich D, Rolníková T, Krumpál M (2002) Výskyt cicavčích druhov bĺch (Siphonaptera) na vtákoch a v ich hniezdach. Folia Faunistica Slovaca 7:61–68

    Google Scholar 

  • Danišová O, Valenčáková A, Stanko M, Luptáková L, Hatalová E, Čanády A (2017) Rodents as a reservoir of infection caused by multiple zoonotic species/genotypes of C. parvum, C. hominis, C. suis, C. scrofarum, and the first evidence of C. muskrat genotypes I and II of rodents in Europe. Acta Trop 172:29–35

    PubMed  Google Scholar 

  • Dudich A (1993) The knowledge of small mammals and their ectoparasites in Ponitie region. 3. Fleas (Siphonaptera) of mammals (Mammalia) living in Nitra district. Rosalia (Nitra) 9:241–227

    Google Scholar 

  • Faccini-Martínez ÁA, García-Álvarez L, Hidalgo M, Oteo JA (2014) Syndromic classification of rickettsioses: an approach for clinical practice. Int J Infect Dis 28:126–139

    PubMed  Google Scholar 

  • Filippova NA (1977) Ixodid ticks of the subfamily Ixodinae. Fauna of the USSR, Nauka, Leningrad

    Google Scholar 

  • Guo XG, Speakman JR, Dong WG, Men XY, Qian TJ, Wu D, Qin F, Song WY (2013) Ectoparasitic insects and mites on Yunnan redbacked voles (Eothenomys miletus) from a localized area in southwest China. Parasitol Res 112:3543–3549

    PubMed  Google Scholar 

  • Hajduskova E, Literak I, Papousek I, Costa FB, Novakova M, Labruna MB, Zdrazilova-Dubska L (2016) ‘Candidatus Rickettsia mendelii’, a novel basal group rickettsia detected in Ixodes ricinus ticks in the Czech Republic. Ticks Tick-Borne Dis 7:482–486

    PubMed  Google Scholar 

  • Hanincová K, Schäfer SM, Etti S, Sewell HS, Tarageľová V, Žiak D, Labuda M, Kurtenbach K (2003) Association of Borrelia afzelii with rodents in Europe. Parasitology 126(Pt 1):11–20

    PubMed  Google Scholar 

  • Heglasová I, Vichova B, Kraljik J, Mosansky L, Miklisova D, Stanko M (2018) Molecular evidence and diversity of the spotted-fever group Rickettsia spp. in small mammals from natural, suburban and urban areas of Eastern Slovakia. Ticks Tick Borne Dis 9:1400–1406

    PubMed  Google Scholar 

  • Hornok S, Kovács R, Meli ML, Kontschán J, Gyuranecz M, Dán Á, Molnár V (2012) First detection of bartonellae in a broad range of bat ectoparasites. Vet Microbiol 159:541–543

    PubMed  CAS  Google Scholar 

  • Hornok S, Foldvári G, Rigó K, Meli ML, Tóth M, Molnár V, Gonczi E, Farkas R, Hofmann-Lehmann R (2014) Vector-borne agents detected in fleas of the northern white-breasted hedgehog. Vector Borne Zoonot Dis 14:1–3

    Google Scholar 

  • Huegli D, Hu CM, Humair PF, Wilske B, Gern L (2002) Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. J Clin Microbiol 40:4735–4737

    PubMed  PubMed Central  CAS  Google Scholar 

  • Humair PF, Rais O, Gern L (1999) Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 118:33–42

    PubMed  Google Scholar 

  • Jiang J, You BJ, Liu E, Apte A, Yarina TR, Myers TE, Lee JS, Francesconi SC, O’Guinn ML, Tsertsvadze N, Vephkhvadze N, Babuadze G, Sidamonidze K, Kokhreidze M, Donduashvili M, Onashvili T, Ismayilov A, Agayev N, Aliyev M, Muttalibov N, Richards AL (2012) Development of three quantitative real-time PCR assays for the detection of Rickettsia raoultii, Rickettsia slovaca, and Rickettsia aeschlimannii and their validation with ticks from the country of Georgia and the Republic of Azerbaijan. Ticks Tick Borne Dis 3:327–331

    PubMed  Google Scholar 

  • Karg W (1971) Die freilebenden Gamasina (Gamasides), Raubmilben. In: Die Tierwelt Deutschlands und angrenzende Meeresteile, Teil 59, Fischer Verlag, Jena

  • Karg W (1993) Acari (Acarina), Milben Parasitiformes (Anactinochaeta) Cohors Gamasina Leach Raubmilben. In: Die Tierwelt Deutschlands, Teil 59, Gustav Fischer Verlag, Jena, Stuttgart, New York

  • Khrouf F, M’ Ghirbi Y, Znazen A, Jemaa MB, Hammami A, Bouttour A (2014) Detection of Rickettsia in Rhipicephalus sanguineus ticks and Ctenophalides felis fleas from Southeastern Tunisia by reverse line blot assays. J Clin Microbiol 52:268–274

    PubMed  PubMed Central  CAS  Google Scholar 

  • Klempa B, Stanko M, Labuda M, Ulrich R, Meisel H, Kruger DH (2005) Central European Dobrava hantavirus isolate from a striped field mouse (Apodemus agrarius). J Clin Microbiol 43:2756–2763

    PubMed  PubMed Central  Google Scholar 

  • Kocianová E (1980) Akarofauna drobných zemných cicavcov Západných Tatier – Roháčov. I Biológia (Bratislava) 35:97–108

    Google Scholar 

  • Kocianová E (1989) Gnezdovye ektoparasity (gamazovye kleshchi) kak perenoschiky rikketsij v eksperimente. Rikketsiozy. Sbornik Nauchnykh Trudov, Leningrad 66:89–94

    Google Scholar 

  • Kocianová E, Kožuch O, Bakoss P, Řeháček J, Kováčová E (1993) The prevalence of small terrestrial mammals infected with tick- borne encephalitis virus and leptospirae in the foothills of the southern Bavarian forest, Germany. Appl Parasitol 34:283–290

    PubMed  Google Scholar 

  • Kraljik J, Paziewska-Harris A, Miklisová D, Blaňarová L, Mošanský L, Bona M, Stanko M (2016) Genetic diversity of Bartonella genotypes found in the striped field mouse (Apodemus agrarius) in Central Europe. Parasitology 143(11):1437–1442

    PubMed  Google Scholar 

  • Krasnov BR, Stanko M, Miklisová D, Morand S (2006) Habitat variation in species composition of flea assemblages on small mammals in Central Europe. Ecol Res 21:460–469

    Google Scholar 

  • Krasnov BR, Stanko M, Morand S (2007) Host community structure and infestation by ixodid ticks: repeability, dilution effect and ecological specialization. Oecologia 154:185–194

    PubMed  Google Scholar 

  • Krasnov B, Stanko M, Morand S (2010) Competition, facilitation or mediation via host? Patterns of infestation of small European mammals by two taxa of hematophagous arthropods. Ecologic Entomol 35:37–44

    Google Scholar 

  • Labuda M, Lysý J, Krippel E (1989) Ixodes ricinus, Haemaphysalis concinna and Dermacentor reticulatus ticks (Acarina, Ixodidae) on terrestrial micromammals in selected localities in western Slovakia. Biológia (Bratislava) 44(10):897–909

  • Liu D, Wang YZ, Zhang H, Liu ZQ, Wureli H, Wang SW, Tu CC, Chen CF (2016) First report of Rickettsia raoultii and R. slovaca in Melophagus ovinus, the sheep ked. Parasite vector 9:600

    Google Scholar 

  • Lukáň M, Bullová E, Peťko B (2010) Climate warming and tick-borne encephalitis, Slovakia. Emerg Infect Dis 16(3):524–526

    PubMed  PubMed Central  Google Scholar 

  • Mácová A, Hoblíková A, Hypša V, Stanko M, Martinů J, Kvičerová J (2018) Mysteries of host switching: diversification and host specificity in rodent-coccidia associations. Mol Phylogenet Evol 127:179–189

    PubMed  Google Scholar 

  • Marie JL, Fournier PE, Rolain JM, Briolant S, Davoust B, Raoult D (2006) Molecular detection of Bartonella quintana, B. elizabethae, B. koehlerae, B. doshiae, B. taylorii, and Rickettsia felis in rodent fleas collected in Kabul, Afghanistan. Am J Trop Med Hyg 74(3):436–439

    PubMed  CAS  Google Scholar 

  • Martin OY, Puniamoorthy N, Gubler A, Wimmer C, Bernasconi MV (2013) Infections with Wolbachia, Spiroplasma, and Rickettsia in the Dolichopodidae and other Empidoidea. Infect Genet Evol 13:317–330

    PubMed  Google Scholar 

  • Mašán P, Fenďa P (2010) A review of the laelapid mites associated with terrestrial mammals in Slovakia, with a key to the European species (Acari: Mesostigmata: Dermanyssoidea). Slovak Academy of Sciences, NOI Press, Bratislava, Institue of Zoology 187 pp

    Google Scholar 

  • Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270

    PubMed  Google Scholar 

  • Minichová L, Hamšíková Z, Mahríková L, Slovák M, Kocianová E, Kazimírová M, Škultéty Ľ, Štefanidesová K, Špitalská E (2017) Molecular evidence of Rickettsia spp. in ixodid ticks and rodents in suburban, natural and rural habitats in Slovakia. Parasit Vectors 10:158

    PubMed  PubMed Central  Google Scholar 

  • Miťková K, Berthová L, Kalúz S, Kazimírová M, Burdová L, Kocianová E (2015) First detections of Rickettsia helvetica and R. monacensis in ectoparasitic mites (Laelapidae and Trombiculidae) infesting rodents in south-western Slovakia. Parasitol Res 114:2465–2472

    PubMed  Google Scholar 

  • Mori E, Pisanu B, Zozzoli R, Solano E, Olivieri E, Sassera D, Montagna M (2018) Arthropods and associated pathogens from native and introduced rodents in Northeastern Italy. Parasitol Res 117:3237–3243

    PubMed  Google Scholar 

  • Morick D, Baneth G, Avidor B, Kosoy MY, Mumcuoglu KY, Mintz D, Eyal O, Goethe R, Mietze A, Shpigel N, Harrus S (2009) Detection of Bartonella spp. in wild rodents in Israel using HRM real-time PCR. Vet Microbiol 139(3–4):293–297

    PubMed  CAS  Google Scholar 

  • Morick D, Krasnov BR, Khokhlova IS, Shenbrot GI, Kosoy MY, Harrus S (2010) Bartonella genotypes in fleas (Insecta: Siphonaptera) collected from rodents in the Negev desert, Israel. Appl Environ Microbiol 76(20):6864–6869

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nosek J, Sixl W, Kvíčala P, Waltinger H (1972) Central Europaean ticks (Ixodoidea), keys for determination. Mitteilungen der Abteilung fűr Zoologie am Landesmuseum, Joanneum in Graz 1:61–92

    Google Scholar 

  • Obiegala A, Pfeffer M, Pfister K, Karnath C, Silaghi C (2015) Molecular examinations of Babesia microti in rodents and rodent-attached ticks from urban and sylvatic habitats in Germany. Ticks Tick Borne Dis 6:445–449

    PubMed  Google Scholar 

  • Obiegala A, Oltersdorf C, Silaghi C, Kiefer D, Kiefer M, Woll D, Pfeffera M (2016) Rickettsia spp. in small mammals and their parasitizing ectoparasites from Saxony, Germany. Vet Parasitol 5:19–24

    Google Scholar 

  • Oteo JA, Portillo A (2012) Tick-borne rickettsioses in Europe. Ticks Tick Borne Dis 3:271–278

    PubMed  Google Scholar 

  • Radzijevskaja J, Paulauskas A, Aleksandraviciene A, Jonauskaite I, Stanko M, Karbowiak G, Peťko B (2015) New records of spotted fever group rickettsiae in Baltic region. Microbes Infect 17:874–878

    PubMed  Google Scholar 

  • Radzijevskaja J, Kaminskiene E, Lipatova I, Mardosaite-Busaitiene D, Balčiauskas L, Stanko M, Paulauskas A (2018) Prevalence and diversity of Rickettsia species in ectoparasites collected from small rodents in Lithuania. Parasite Vector 11:375

    Google Scholar 

  • Randolph SE, Miklisová D, Lysy J, Rogers DJ, Labuda M (1999) Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118:177–186

    PubMed  Google Scholar 

  • Raoult D, Parola P (2007) Rickettsial diseases. CRC Press

  • Raoult D, Roux V (1997) Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev 10:694–719

    PubMed  PubMed Central  CAS  Google Scholar 

  • Reeves WK, Dowling APG, Dasch AGA (2006) Rickettsial agents from parasitic Dermanyssoidea (Acari: Mesostigmata). Exp Appl Acarol 38:181–188

    PubMed  Google Scholar 

  • Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol 173:1576–1589

    PubMed  PubMed Central  CAS  Google Scholar 

  • Reiterová K, Antolová D, Zaleśny G, Stanko M, Špilovská S, Mošanský L (2013) Small rodents –permanent reservoirs of toxocarosis in different habitats of Slovakia. Helminthologia 50(1):20–26

    Google Scholar 

  • Rijpkema S, Golubić D, Molkenboer M, Verbeek-De Kruif N, Schellekens J (1996) Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp Appl Acarol 20:23–30

    PubMed  CAS  Google Scholar 

  • Rosický B (1957) Blechy – Aphaniptera. Fauna ČSR 10, NČSAV, Praha

  • Rynkiewicz EC, Hawlena H, Durden LA, Hastriter MW, Demas GE, Clay K (2013) Associations between innate immune function and ectoparasites in wild rodent hosts. Parasitol Res 112:1763–1770

    PubMed  Google Scholar 

  • Sekeyová Z, Mediannikov O, Roux V, Subramanian G, Špitalská E, Kristofík J, Darolová A, Raoult D (2012) Identification of Rickettsia africae and Wolbachia sp. in Ceratophyllus garei fleas from Passerine birds migrated from Africa. Vector Borne Zoonot Dis 12(7):539-543

  • Schőtta AM, Wijnveld M, Stockinger H, Stanek G (2017) Approaches for reverse line blot-based detection of microbial pathogens in Ixodes ricinus ticks collected in Austria and impact of the chosen method. Appl Environ Microbiol 83:e00489–e00417

    PubMed  PubMed Central  Google Scholar 

  • Segura F, Pons I, Miret J, Pla J, Ortuno A, Nogueras MM (2014) The role of cats in the eco-epidemiology of spotted fever group diseases. Parasite Vector 7:353

    Google Scholar 

  • Slovák M (2010) Pictorial key to the adults of ticks (Acari: Ixodida) of the Slovakia fauna. Entomofauna carpathica 22:8–13

    Google Scholar 

  • Song S, Chen C, Yang M, Zhao S, Wang B, Hornok S, Makhatov B, Rizabek K, Wang Y (2018) Diversity of Rickettsia species in border regions of northwestern China. Parasite Vector 11:634

    CAS  Google Scholar 

  • Špitalská E, Štefanidesová K, Kocianová E, Boldiš V (2012) Rickettsia slovaca and Rickettsia raoultii in Dermacentor marginatus and Dermacentor reticulatus ticks from Slovak Republic. Exp Appl Acarol 57:189–197

    PubMed  Google Scholar 

  • Špitalská E, Boldiš V, Derdáková M, Selyemová D, Rusňáková Tarageľová V (2014) Rickettsial infection in Ixodes ricinus ticks in urban and natural habitats of Slovakia. Ticks Tick Borne Dis 5(2):161–165

    PubMed  Google Scholar 

  • Špitalská E, Boldiš V, Mošanský L, Sparagano O, Stanko M (2015) Rickettsia species in fleas collected from small mammals in Slovakia. Parasitol Res 114:4333–4339

    PubMed  Google Scholar 

  • Špitalská E, Stanko M, Mošanský L, Kraljik J, Miklisová D, Mahriková L, Bona M, Kazimírová M (2016) Seasonal analysis of Rickettsia species in ticks in an agricultural site of Slovakia. Exp Appl Acarol 68:315–324

    PubMed  Google Scholar 

  • Špitalská E, Minichová L, Kocianová E, Škultéty Ľ, Mahríková L, Hamšíková Z, Slovák M, Kazimírová M (2017) Diversity and prevalence of Bartonella species in small mammals from Slovakia, Central Slovakia. Parasitol Res 116:3087–3095

  • Špitalská E, Sparagano O, Stanko M, Schwarzova K, Špitalský Z, Škultéty Ľ, Fumačová Havlíková S (2018) Diversity of Coxiella-like and Francisella-like endosymbionts, and Rickettsia spp., Coxiella burnetii as pathogens in the tick populations of Slovakia, Central Europe. Ticks Tick-borne Dis 9:1207–1211

  • Sprong H, Wielinga PR, Fonville M, Reusken C, Brandenburg AH, Borgsteede F, Gaasenbeek C, van der Giessen JWB (2009) Ixodes ricinus ticks are reservoir hosts for Rickettsia helvetica and potentially carry flea-borne Rickettsia species. Parasite Vector 2:41

    Google Scholar 

  • Stanko M (1989) Roztoče (Acarina, Mesostigmata) drobných cicavcov dvoch územných celkov Západných Karpát. Biológia (Bratislava) 44:449–512

    Google Scholar 

  • Stanko M (1994) Small mammal communities of windbreaks and adjacent fields in the Eastern Slovakian lowlands. Folia Zool 43:135–143

    Google Scholar 

  • Stanko M, Miklisova D (1995) Interactions of small mammal communities of wind-breaks and adjacent fields with respect to epidemiological aspects. Ekologia CSSR 14:3–16

    Google Scholar 

  • Stanko M, Prokopčaková H, Fričová J, Peťko B (1996) Occurrence of antibodies to leptospira in small mammals in Eastern Slovakia. Veterinární Medicína Czech 41:373–377

    CAS  Google Scholar 

  • Stanko M, Miklisová D, de Bellocq G, Morand S (2002) Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131:289–295

    PubMed  Google Scholar 

  • Stanko M, Fričová J, Miklisová D, Khokhlová IS, Krasnov BR (2015) Environment-related and host-related factors affecting the occurrence of lice on rodents in Central Europe. Parasitology 142:932–947

    Google Scholar 

  • Švehlová A, Berthová L, Sallay B, Boldiš V, Sparagano OAE, Špitalská E (2014) Sympatric occurrence of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks and Rickettsia and Babesia species in Slovakia. Ticks Tick Borne Dis 5:600–605

    PubMed  Google Scholar 

  • Svoboda P, Dobler G, Markotić A, Kurolt IC, Speck S, Habuš J, Vucelja M, Krajinović LC, Tadin A, Margaletić J, Essbauer S (2014) Survey for hantaviruses, tick-borne encephalitis virus, and Rickettsia spp. in small rodents in Croatia. Vector Borne Zoonotic Dis 14:523–530

    PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nie M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed  PubMed Central  CAS  Google Scholar 

  • Uchiyama T (2012) Tropism and pathogenicity of Rickettsiae. Front Microbiol 3:230

    PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We are grateful to Ladislav Mošanský and Monika Onderová for help in the field and laboratory work.

Funding

This study was financially supported by the VEGA No. 2/0068/17 and VEGA 1/0084/18 projects from the Scientific Grant Agency of Ministry of Education and Slovak Academy of Sciences.

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Correspondence to Eva Špitalská.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Small mammals were euthanized according to the laws of the Slovak Republic under the licences of the Ministry of Environment of the Slovak Republic No. 297/108/06–3.1 and No. 6743/2008–2.1.

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Phylogenetic tree inferred from comparison of the Rickettsia gltA partial sequences. The evolutionary history was inferred using the neighbour-joining method. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) is shown next to the branches. The evolutionary distances were computed using the number of different methods and are in the units of the number of base differences per sequence. GenBank accession numbers are included. (PNG 77 kb)

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Špitalská, E., Kraljik, J., Miklisová, D. et al. Circulation of Rickettsia species and rickettsial endosymbionts among small mammals and their ectoparasites in Eastern Slovakia. Parasitol Res 119, 2047–2057 (2020). https://doi.org/10.1007/s00436-020-06701-8

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