Skip to main content

Advertisement

SpringerLink
Log in

Diversity and prevalence of Bartonella species in small mammals from Slovakia, Central Europe

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Wild-living rodents are important hosts for zoonotic pathogens. Bartonella infections are widespread in rodents; however, in Slovakia, knowledge on the prevalence of these bacteria in small mammals is limited. We investigated the prevalence and diversity of Bartonella species in the spleens of 640 rodents of six species (Apodemus flavicollis, Apodemus sylvaticus, Myodes glareolus, Microtus arvalis, Microtus subterraneus, and Micromys minutus) and in the European mole (Talpa europaea) from three different habitat types in south-western and central Slovakia. Overall, the prevalence of Bartonella spp. in rodents was 64.8%; a rate of 73.8% was found in natural habitat (deciduous forest), 56.0% in suburban forest park and 64.9% in rural habitat. Bartonella spp. were detected in 63.0% of A. flavicollis, 69% of My. glareolus and 61.1% of M. arvalis and in T. europaea. However, Bartonella were not found in the other examined rodents. Molecular analyses of the 16S–23S rRNA intergenic spacer region revealed the presence of four different Bartonella spp. clusters. We identified B. taylorii, B. rochalimae, B. elizabethae, B. grahamii and Bartonella sp. wbs11 in A. flavicollis and My. glareolus. Bartonella genotypes ascribed to B. taylorii and B. rochalimae were found in M. arvalis. B. taylorii was identified in T. europaea. Questing Ixodes ricinus ticks that were collected at the study sites were not infected with Bartonella. This study improves our understanding of the ecoepidemiology of Bartonella spp. in Europe and underlines the necessity for further research on Bartonella-host-vector associations and their consequences on animal and human health in Slovakia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bai Y, Calisher CH, Kosoy MY, Root JJ, Doty JB (2011) Persistent infection or successive reinfection of deer mice with Bartonella vinsonii subsp. arupensis. Appl Environ Microbiol 77:1728–1731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajer A, Pawełczyk A, Behnke J, Gilbert F, Siński E (2001) Factors affecting the component community structure of haemoparasites in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 122:43–54

    Article  PubMed  Google Scholar 

  • Baker JR (1974) Protozoan parasites of the blood of British wild birds and mammals. J Zool London 172:169–190

    Article  Google Scholar 

  • Berthová L, Slobodník V, Slobodník R, Olekšák M, Sekeyová Z, Svitálková Z, Kazimírová M, Špitalská E (2016) The natural infection of birds and ticks feeding on birds with Rickettsia spp. and Coxiella burnetii in Slovakia. Exp Appl Acarol 68:299–314

    Article  PubMed  Google Scholar 

  • Billeter SA, Levy MG, Chomel BB, Breitschwerdt EB (2008) Vector transmission of Bartonella species with emphasis on potential for tick transmission. Med Vet Entomol 22:1–15

    Article  CAS  PubMed  Google Scholar 

  • Billeter SA, Sangmaneedet S, Kosakewich RC, Kosoy MY (2012) Bartonella species in dogs and their ectoparasites from Khon Kaen Province, Thailand. Southeast Asian J Trop Med Public Health 43:1186–1192

    PubMed  Google Scholar 

  • Birtles RJ, Harrison TG, Molyneux DH (1994) Grahamella in small woodland mammals in the U.K.: isolation, prevalence and host specificity. Ann Trop Med Parasitol 88:317–327

    Article  CAS  PubMed  Google Scholar 

  • Birtles RJ, Harrison TG, Saunders NA MDH (1995) Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella taplae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. Int J Syst Bacteriol 45:1–8

  • Birtles RJ, Hazel S, Bown K, Raoult D, Begon M, Bennett M (2000) Subtyping of uncultured bartonellae using sequence comparison of 16S/ 23S rRNA intergenic spacer regions amplified directly from infected blood. Mol Cell Probes 14:79–87

    Article  CAS  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 7:319–326. https://doi.org/10.1016/j.ttbdis.2015.11.008

    Article  PubMed  Google Scholar 

  • Bown KJ, Bennett M, Begon M (2004) Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerg Infect Dis 10(4):684e7

    Article  Google Scholar 

  • Breitschwerdt EB, Kordick DL (2000) Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clin Microbiol Rev 13:428–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buffet JP, Marsot M, Vaumourin E, Gasqui P, Masséglia S, Marcheteau E, Huet D, Chapuis JL, Pisanu B, Ferquel E, Halos L, Vourc’h G, Vayssier-Taussat M (2012) Co-infection of Borrelia afzelii and Bartonella spp. in bank voles from a suburban forest. Comp Immunol Microbiol Infect Dis 35:583–589

    Article  PubMed  Google Scholar 

  • Cotté V, Bonnet S, Le Rhun D, Le Naour E, Chauvin A, Boulouis HJ, Lecuelle B, Lilin T, Vayssier-Taussat M (2008) Transmission of Bartonella henselae by Ixodes ricinus. Emerg Infect Dis 14:1074–1080

    Article  PubMed  PubMed Central  Google Scholar 

  • Daly JS, Worthington MG, Brenner DJ, Moss CW, Hollis DG, Weyant RS, Steigerwalt AG, Weaver RE, Daneshvar MI, O’Connor SP (1993) Rochalimaea elizabethae sp. nov. isolated from a patient with endocarditis. J Clin Microbiol 31:872–881

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engbaek K, Lawson PA (2004) Identification of Bartonella species in rodents, shrews and cats in Denmark: detection of two Bartonella henselae variants, one in cats and the other in the long-tailed field mouse. APMIS 112:336–341

    Article  PubMed  Google Scholar 

  • Engel P, Salzburger W, Liesch M, Chang CC, Maruyama S, Lanz C, Calteau A, Lajus A, Médigue C, Schuster SC, Dehio C (2011) Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella. PLoS Genet 7:e1001296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eremeeva ME, Gerns HL, Lydy SL et al (2007) Bacteremia, fever, and splenomegaly caused by a newly recognized Bartonella species. N Engl J Med 356:2381e7

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Gil H, García-Esteban C, Barandika JF, Peig J, Toledo A, Escudero R, Jado I, Rodríguez-Vargas M, García-Amil C, Lobo B, Roales P, Rodríguez-Moreno I, Olmeda AS, García-Pérez AL, Anda P (2010) Variability of Bartonella genotypes among small mammals in Spain. Appl Environ Microbiol 76(24):8062–8070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gundi VA, Davoust B, Khamis A, Boni M, Raoult D, La Scola B (2004) Isolation of Bartonella rattimassiliensis sp. nov. and Bartonella phoceensis sp. nov. from European Rattus norvegicus. J Clin Microbiol 42:3816–3818

    Article  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez R, Krasnov B, Morick D, Gottlieb Y, Khokhlova IS, Harrus S (2015) Bartonella infection in rodents and their flea ectoparasites: an overview. Vector Borne Zoonotic Dis 15(1):27–39

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamšíková Svitálková Z, Haruštiaková D, Mahríková L, Mojšová M, Berthová L, Slovák M, Kocianová E, Vayssier-Taussat M, Kazimírová M (2016) Candidatus Neoehrlichia mikurensis in ticks and rodents from urban and natural habitats of South-Western Slovakia. Parasit Vectors 9:2

    Article  Google Scholar 

  • Hamšíková Z, Kazimírová M, Haruštiaková D, Mahríková L, Slovák M, Berthová L, Kocianová E, Schnittger L (2016) Babesia spp. in ticks and wildlife in different habitat types of Slovakia. Parasit Vectors 9:292

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamšíková Z, Coipan C, Mahríková L, Minichová L, Sprong H, Kazimírová M (2017) Borrelia miyamotoi and co-infection with Borrelia afzelii in Ixodes ricinus ticks and rodents from Slovakia. Microb Ecol 73:1000–1008

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Harrison A, Bown KJ, Montgomery WI, Birtles RJ (2012) Ixodes ricinus is not an epidemiologically relevant vector of Bartonella species in the wood mouse (Apodemus sylvaticus). Vector Borne Zoonotic Dis 12(5):366–371

    Article  PubMed  Google Scholar 

  • Healing TD (1981) Infections with blood parasites in the small British rodents Apodemus sylvaticus, Clethrionomys glareolus and Microtus agrestis. Parasitology 83:179–189

    Article  CAS  PubMed  Google Scholar 

  • Holmberg M, Mills JN, McGill S, Benjamin G, Ellis (2003) Bartonella infection in sylvatic small mammals of central Sweden. Epidemiol Infect 130:149–157

  • Jiyipong T, Jittapalapong S, Morand S, Rolain JM (2014) Bartonella species in small mammals and their potential vectors in Asia. Asian Pac J Trop Biomed 4(10):757e67

    Article  Google Scholar 

  • Karbowiak G, Rychlik L, Nowakowski W, Wita I (2005) Natural infections of small mammals with blood parasites on the borderland of boreal and temperate forest zones. Acta Theriol 50:31–42

    Article  Google Scholar 

  • Karbowiak G, Stanko M, Fričová J, Wita I, Hapunik J, Peťko B (2009) Blood parasites of the striped field mouse Apodemus agrarius and their morphological characteristics. Biologia 64:1219–1224

    Article  Google Scholar 

  • Kazimírová M, Hamšíková Z, Kocianová E, Marini G, Mojšová M, Mahríková L, Berthová L, Slovák M, Rosá R (2016) Relative density of host-seeking ticks in different habitat types of south-western Slovakia. Exp Appl Acarol 69:205–224

  • Kerkhoff FT, Bergmans AM, van Der Zee A, Rothova A (1999) Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis. J Clin Microbiol 37:4034–4038

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knap N, Duh D, Birtles R, Trilar T, Petrovec M, Avšič-Županc T (2007) Molecular detection of Bartonella species infecting rodents in Slovenia. FEMS Immunol Med Microbiol 50(1):45–50

    Article  CAS  PubMed  Google Scholar 

  • Kosoy M, Murray M, Gilmore RD Jr, Bai Y, Gage KL (2003) Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol 41:645–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosoy M, Bai Y, Sheff K, Morway C, Baggett H, Maloney SA, Boonmar S, Bhengsri S, Dowell SF, Sitdhirasdr A, Lerdthusnee K, Richardson J, Peruski LF (2010) Identification of Bartonella infections in febrile human patients from Thailand and their potential animal reservoirs. Am J Trop Med Hyg 82:1140–1145

    Article  PubMed  PubMed Central  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

    Article  PubMed  Google Scholar 

  • Lin JW, Chen CY, Chen WC, Chomel BB, Chang CC (2008) Isolation of Bartonella species from rodents in Taiwan including a strain closely related to ‘Bartonella rochalimae’ from Rattus norvegicus. J Med Microbiol 57:1496e501

    Google Scholar 

  • Lipatova I, Paulauskas A, Puraite I, Radzijevskaja J, Balciauskas L, Gedminas V (2015) Bartonella infection in small mammals and their ectoparasites in Lithuania. Microbes Infect 17:884–888

    Article  CAS  PubMed  Google Scholar 

  • Maggi RG, Diniz PP, Cadenas MB, Breitschwerdt EB (2006) The use of molecular diagnostic techniques to detect Anaplasma, Bartonella and Ehrlichia species in arthropods or patients. The International Canine Vector-Borne Disease Symposium; April 18-20th 2006 Billesley, Alcester, UK: 9–14

  • Maggi RG, Kosoy M, Mintzer M, Breitschwerdt EB (2009) Isolation of Candidatus Bartonella melophagi from human blood. Emerg Infect Dis 15:66–68

    Article  PubMed  PubMed Central  Google Scholar 

  • Malania L, Bai Y, Osikowicz LM, Tsertsvadze N, Katsitadze G, Imnadze P, Kosoy M (2016) Prevalence and diversity of Bartonella species in rodents from Georgia (Caucasus). Am J Trop Med Hyg 95:466–471

    Article  PubMed  PubMed Central  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. https://doi.org/10.1186/s13071-017-2094-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Mogollon-Pasapera E, Otvos L, Giordano A, Cassone M (2009) Bartonella: Emerging pathogen or emerging awareness? Int J Infect Dis 13:3–8

    Article  PubMed  Google Scholar 

  • Morozova OV, Chernousova N, Morozov IV (2005) Detection of the Bartonella DNA by the method of nested PCR in patients after tick bites in Novosibirsk region. Mol Gen Mikrobiol Virusol 4:14–17

    Google Scholar 

  • Mosepele M, Mazo D, Cohn J (2012) Bartonella infection in immunocompromised hosts: immunology of vascular infectionand vasoproliferation. Clin Dev Immunol 2012:612809

    Article  PubMed  Google Scholar 

  • Mullins KE, Hang J, Clifford RJ, Onmus-Leone F, Yang Y, Jiang J, Leguia M, Kasper MR, Maguina C, Lesho EP, Jarman RG, Richards A, Blazes D (2017) Whole-genome analysis of Bartonella ancashensis, a novel pathogen causing verruga peruana, rural Ancash region, Peru. Emerg Infect Dis 23:430–438

    Article  PubMed  PubMed Central  Google Scholar 

  • Oksi J, Rantala S, Kilpinen S, Silvennoinen R, Vornanen M, Veikkolainen V et al (2013) Cat scratch disease caused by Bartonella grahamii in an immunocompromised patient. J Clin Microbiol 51(8):2781e4

    Article  Google Scholar 

  • Pawełczyk A, Bajer A, Behnke JM, Gilbert FS, Siński E (2004) Factors affecting the component community structure of haemoparasites in common voles (Microtus arvalis) from the Mazury Lake District region of Poland. Parasitol Res 92:270–284

    Article  PubMed  Google Scholar 

  • Potkonjak A, Gutiérrez R, Savić S, Vračar V, Nachum-Biala Y, Jurišić A, Kleinerman G, Rojas A, Petrović A, Baneth G, Harrus S (2016) Molecular detection of emerging tick-borne pathogens in Vojvodina, Serbia. Ticks Tick Borne Dis 7:199–203

    Article  PubMed  Google Scholar 

  • Regier Y, O’Rourke F, Kempf VAJ (2016) Bartonella spp.—a chance to establish One Health concepts in veterinary and human medicine. Parasit Vectors 9:261

  • Regier Y, Ballhorn W, Kempf VAJ (2017) Molecular detection of Bartonella henselae in 11 Ixodes ricinus ticks extracted from a single cat. Parasit Vectors 10:105

    Article  PubMed  PubMed Central  Google Scholar 

  • Reis C, Cote M, Le Rhun D, Lecuelle B, Levin ML, Vayssier-Taussat M, Bonnet SI (2011) Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii. PLoS Negl Trop Dis 5:e1186

    Article  PubMed  PubMed Central  Google Scholar 

  • Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G, Plantard O, Vayssier-Taussat M, Bonnet S, Špitalská E, Kazimírová M (2014) Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health 2:251

  • Rudolf I, Betášová L, Bischof V, Venclíková K, Blažejová H, Mendel J, Hubálek Z, Kosoy M (2016) Molecular survey of arthropod-borne pathogens in sheep keds (Melophagus ovinus), Central Europe. Parasitol Res 115:3679

  • Saitou N, Nie M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schmidt S, Essbauer SS, Mayer-Scholl A, Poppert S, Schmidt-Chanasit J, Klempa B, Henning K, Schares G, Groschup MH, Spitzenberger F, Richter D, Heckel G, Ulrich RG (2014) Multiple infections of rodents with zoonotic pathogens in Austria. Vector Borne Zoonot Dis 14(7):467–475

    Article  Google Scholar 

  • Schorn S, Pfister K, Reulen H, Mahling M, Silaghi C (2011) Occurrence of Babesia spp., Rickettsia spp. and Bartonella spp. in Ixodes ricinus in Bavarian public parks, Germany. Parasit Vectors 4:135

    Article  PubMed  PubMed Central  Google Scholar 

  • Šebek Z (1960) Některé nové poznatky o krevních parasitech našich hmyzožravců a myšovitých. Vlastivědný Sborník Vysočiny, Oddíl Věd Přirodních, 75–80

  • Šebek Z (1975) Blutparasiten der wildlebenden Kleinsäuger in der Tschechoslowakei. Folia Parasitol (Praha) 22:11–20

    Google Scholar 

  • Silaghi C, Pfeffer M, Kiefer D, Kiefer M, Obiegala A (2016) Bartonella, rodents, fleas and ticks: a molecular field study on host-vector-pathogen associations in Saxony, Eastern Germany. Microb Ecol 72(4):965–974

    Article  PubMed  Google Scholar 

  • Sormunen JJ, Penttinen R, Klemola T, Hanninen J, Vuorinen I, Laaksonen M et al (2016) Tick-borne bacterial pathogens in southwestern Finland. Parasit Vectors 9:168

    Article  PubMed  PubMed Central  Google Scholar 

  • Špitalská E, Boldiš V, Košťanová Z, Kocianová E, Štefanidesová K (2008) Incidence of various tick-borne microorganisms in rodents and ticks of central Slovakia. Acta Virol 52:175–179

    PubMed  Google Scholar 

  • Svitálková Z, Haruštiaková D, Mahríková L, Berthová L, Slovák M, Kocianová E, Kazimírová M (2015) Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in South-Western Slovakia. Parasit Vectors 8:276

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tea A, Alexiou-Daniel S, Papoutsi A, Papa A, Antoniadis A (2004) Bartonella species isolated from rodents, Greece. Emerg Infect Dis 10:963–964

    Article  PubMed  PubMed Central  Google Scholar 

  • Welc-Falęciak R, Paziewska A, Bajer A, Behnke JM, Siński E (2008) Bartonella spp. infection in rodents from different habitats in the Mazury Lake District, Northeast Poland. Vector Borne Zoonotic Dis 8:467–474

    Article  PubMed  Google Scholar 

  • Welch DF, Carroll KC, Hofmeister EK, Persing DH, Robison DA, Steigerwalt AG, Brenner DJ (1999) Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. J Clin Microbiol 37:2598–2601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wiger R (1979) Seasonal and annual variations in the prevalence of blood parasites in cyclic species of small rodents in Norway with special reference to Clethrionomys glareolus. Holarct Ecol 2:169–175

    Google Scholar 

  • Ying B, Kosoy MY, Maupin GO, Tsuchiya KR, Gage KL (2002) Genetic and ecologic characteristics of Bartonella communities in rodents in southern China. Am J Trop Med Hyg 66:622–627

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Cornelia Silaghi, LMU, Munich, Germany for providing Bartonella-positive DNA from rodents.

Funding

This study was financially supported by the Scientific Grant Agency of Ministry of Education, Science, Research and Sport of the Slovak Republic and Slovak Academy of Sciences (project Vega 2/0068/17), EU grant FP7-261504 EDENext, and the Slovak Research and Development Agency (projects no. 0280–12 and DO7RP–0014–11). This contribution is also the result of using infrastructure acquired by the project implementation (code ITMS: 26240220044), supported by the Research & Development Operational Programme funded by the ERDF.

Author information

Authors and Affiliations

  1. Institute of Virology, Biomedical Research Center, Slovak Academy of Sciences, Dúbravská cesta 9, 845 05, Bratislava, Slovakia

    Eva Špitalská, Lenka Minichová, Elena Kocianová & Ľudovít Škultéty

  2. Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, 845 06, Bratislava, Slovakia

    Lenka Mahríková, Zuzana Hamšíková, Mirko Slovák & Mária Kazimírová

Authors
  1. Eva Špitalská
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lenka Minichová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elena Kocianová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ľudovít Škultéty
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lenka Mahríková
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zuzana Hamšíková
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mirko Slovák
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mária Kazimírová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eva Špitalská.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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.

Work with small mammals was approved by the Ministry of Environment of the Slovak Republic, Regional Environmental Office in Bratislava (licence ZPO-594/2012-SAB).

This article does not contain any studies with human participants performed by any of the authors.

Electronic supplementary material

Table S1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Špitalská, E., Minichová, L., Kocianová, E. et al. Diversity and prevalence of Bartonella species in small mammals from Slovakia, Central Europe. Parasitol Res 116, 3087–3095 (2017). https://doi.org/10.1007/s00436-017-5620-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-017-5620-x

Keywords

Search

Navigation