Skip to main content

Advertisement

Log in

Bartonella, Rodents, Fleas and Ticks: a Molecular Field Study on Host-Vector-Pathogen Associations in Saxony, Eastern Germany

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Bartonellae cause zoonotic diseases and are transmitted by arthropods. Rodents are reservoirs for most Bartonella spp. As the knowledge about Bartonella in rodents and their parasitizing ectoparasites is scarce in Germany, this study’s objectives were to investigate Bartonella spp. in small mammals and in their ectoparasites. A total of 79 small mammals (seven species) were captured and their ectoparasites collected at seven sites around Leipzig, Saxony, Germany, in 2010 and 2011. Altogether, 79 spleen samples, 135 fleas (five species) and 365 ticks (three species) were investigated for Bartonella spp. by PCR targeting the ITS 16S–23S rRNA region. In total, 52 (65.8 %) small mammals, 73 (54.1 %) fleas and 51 (16.3 %) ticks were positive for Bartonella spp. Most small mammals were positive for uncultured Bartonella sp. (n = 29) followed by Bartonella grahamii (n = 12), Bartonella taylorii (n = 8) and Bartonella sp. N40 (n = 3). Likewise, most fleas were positive for uncultured Bartonella sp. (n = 45) followed by B. grahamii (n = 14), B. taylorii (n = 8), B. sp. N40 (n = 5) and Bartonella elizabethae (n = 2). Most ticks were positive for B. sp. (n = 19) followed by B. grahamii (n = 10), Bartonella chomelii (n = 3), B. taylorii (n = 2) and B. sp. N40 (n = 1). This study’s results suggest that rodents and fleas may be reservoirs and vectors, respectively. Zoonotic B. grahamii and B. elizabethae were found in rodents and their fleas. Therefore, humans may contract Bartonella infection by contact to wild rodents. Ticks seem of minor importance in transmitting Bartonella spp. found in fleas and rodents. However, ticks might be vectors of B. chomelii.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Antequera-Gómez ML, Lozano-Almendral L, Barandika JF, González-Martín-Niño RM, Rodríguez-Moreno I, García-Pérez AL, Gil H (2015) Bartonella chomelii is the most frequent species infecting cattle grazing in communal mountain pastures in Spain. Appl Environ Microbiol 81(2):623–629

    Article  PubMed  Google Scholar 

  2. Bajer A, Pawelczyk A, Behnke JM, Gilbert FS, Sinski 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 

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

    Article  CAS  PubMed  Google Scholar 

  4. Birtles RJ, Hazel SM, Bennett M, Bown K, Raoult D, Begon M (2001) Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol Infect 126(2):323–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bown KJ, Bennet M, Begon M (2004) Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerg Infect Dis 10(4):684–687

    Article  PubMed  PubMed Central  Google Scholar 

  6. Brenner DJ, O’Connor SP, Winkler HH, Steigerwalt AG (1993) Proposals to unify the genera Bartonella and Rochalimaea, with descriptions of Bartonella quintana comb. nov., Bartonella vinsonii comb. nov., Bartonella henselae comb. nov., and Bartonella elizabethae comb. nov., and to remove the family Bartonellaceae from the order Rickettsiales. Int J Syst Bacteriol 43(4):777–786

    Article  CAS  PubMed  Google Scholar 

  7. 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. ISME J 4(7):955–958

    Article  PubMed  Google Scholar 

  8. 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(6):583–589

    Article  PubMed  Google Scholar 

  9. Dehio C, Lanz C, Pohl R, Behrens P, Bermond D, Piémont Y, Pelz K, Sander A (2001) Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. Int J Syst Evol Microbiol 51:1557–1565

    Article  CAS  PubMed  Google Scholar 

  10. Dietrich F, Schmidgen T, Maggi RG, Richter D, Matuschka FR, Vonthein R, Breitschwerdt EB, Kempf VA (2010) Prevalence of Bartonella henselae and Borrelia burgdorferi sensu lato DNA in Ixodes ricinus ticks in Europe. Appl Environ Microbiol 76(5):1395–1398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ebani VV, Bertelloni F, Turchi B, Filogari D, Cerri D (2015) Molecular survey of tick-borne pathogens in ixodid ticks collected from hunted wild animals in Tuscany, Italy. Asian Pac J Trop Med 8(9):714–717

    Article  CAS  PubMed  Google Scholar 

  12. Gerrikagoitia X, Gil H, García-Esteban C, Anda P, Juste RA, Barral M (2012) Presence of Bartonella species in wild carnivores of Northern Spain. Appl Environ Microbiol 78(3):885–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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 

  14. 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 

  15. Halos L, Jamal T, Maillard R, Beugnet F, Le Menach A, Boulouis HJ, Vayssier-Taussat M (2005) Evidence of Bartonella sp. in questing adult and nymphal Ixodes ricinus ticks from France and co-infection with Borrelia burgdorferi sensu lato and Babesia sp. Vet Res 36(1):79–87

    Article  PubMed  Google Scholar 

  16. 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 

  17. Hillyard PD (1996) Ticks of North-West Europe synopses of the British Fauna No. 52. The Linnean Society of London

  18. Hsu MH, Wu WJ (2001) Off-host observations of mating and postmating behaviors in the cat flea (Siphonaptera: Pulicidae). J Med Entomol 38:352–360

    Article  CAS  PubMed  Google Scholar 

  19. Inoue K, Maruyama S, Kabeya H, Kawanami K, Yanai K, Jitchum S, Jittaparapong S (2009) Prevalence of Bartonella infection in cats and dogs in a metropolitan area, Thailand. Epidemiol Infect 137(11):1568–1573

    Article  CAS  PubMed  Google Scholar 

  20. Janecek E, Mietze A, Goethe R, Schnieder T, Strube C (2012) Bartonella spp. infection rate and B. grahamii in ticks. Emerg Infect Dis 18(10):1689–1690

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  22. Kosoy MY, Regnery RL, Tzianabos T, Marston EL, Jones DC, Green D, Maupin GO, Olson JG, Childs JE (1997) Distribution, diversity, and host specificity of Bartonella in rodents from the Southeastern United States. Am J Trop Med Hyg 57(5):578–588

    CAS  PubMed  Google Scholar 

  23. Kosoy MY, Regnery RL, Kosaya OI, Jones DC, Marston EL, Childs JE (1998) Isolation of Bartonella spp. from embryos and neonates of naturally infected rodents. J Wildl Dis 34(2):305–309

    Article  CAS  PubMed  Google Scholar 

  24. Krasnov BR, Shenbrot GI, Khokhlova IS, Poulin R (2004) Relationships between parasite abundance and the taxonomic distance among a parasite’s host species: an example with fleas parasitic on small mammals. Int J Parasitol 34(11):1289–1297

    Article  CAS  PubMed  Google Scholar 

  25. 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. In: The International Canine Vector-Borne Disease Symposium; April 18th-20th, Billesley, Alcester, UK, vol 2006., pp 9–14

    Google Scholar 

  26. Maguiña C, Gotuzzo E (2000) Bartonellosis. New and old. Infect Dis Clin N Am 14(1):1–22, vii

    Article  Google Scholar 

  27. Mascarelli PE, Maggi RG, Hopkins S, Mozayeni BR, Trull CL, Bradley JM, Hegarty BC, Breitschwerdt EB (2013) Bartonella henselae infection in a family experiencing neurological and neurocognitive abnormalities after woodlouse hunter spider bites. Parasit Vectors 6:98

    Article  PubMed  PubMed Central  Google Scholar 

  28. Matsumoto K, Cook JA, Goethert HK, Telford SR 3rd (2010) Bartonella sp. infection of voles trapped from an interior Alaskan site where ticks are absent. J Wildl Dis 46(1):173–178

    Article  CAS  PubMed  Google Scholar 

  29. Meheretu Y, Leirs H, Welegerima K, Breno M, Tomas Z, Kidane D, Girmay K, de Bellocq JG (2013) Bartonella prevalence and genetic diversity in small mammals from Ethiopia. Vector Borne Zoonotic Dis 13(3):164–175

    Article  PubMed  Google Scholar 

  30. Obiegala A, Pfeffer M, Pfister K, Tiedemann T, Thiel C, Balling A, Karnath C, Woll D, Silaghi C (2014) Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum: prevalences and investigations on a new transmission path in small mammals and ixodid ticks. Parasit Vectors 7:563

    PubMed  PubMed Central  Google Scholar 

  31. Oksi J, Rantala S, Kilpinen S, Silvennoinen R, Vornanen M, Veikkolainen V, Eerola E, Pulliainen AT (2013) Cat scratch disease caused by Bartonella grahamii in an immunocompromised patient. J Clin Microbiol 51(8):2781–2784

    Article  PubMed  PubMed Central  Google Scholar 

  32. Overzier E (2013) Habitatabhängige Prävalenzunterschiede zeckenübertragener Erreger in Ixodes ricinus und das Reservoirpotential von Rehwild. Dissertation, LMU München: Tierärztliche Fakultät

  33. Parola P, Sanogo OY, Lerdthusnee K, Zeaiter Z, Chauvancy G, Gonzalez JP, Miller RS, Telford SR 3rd, Wongsrichanalai C, Raoult D (2003) Identification of Rickettsia spp. and Bartonella spp. in fleas from the Thai-Myanmar border. Ann N Y Acad Sci 990:173–181

    Article  CAS  PubMed  Google Scholar 

  34. Parson W, Pegoraro K, Niederstätter H, Föger M, Steinlechner M (2000) Species identification by means of the cytochrome b gene. Int J Legal Med 114(1-2):23–28

    Article  CAS  PubMed  Google Scholar 

  35. Paziewska A, Harris PD, Zwolińska L, Bajer A, Siński E (2012) Differences in the ecology of Bartonella infections of Apodemus flavicollis and Myodes glareolus in a boreal forest. Parasitology 139(7):881–893

    Article  CAS  PubMed  Google Scholar 

  36. Peus F (1970) Zur Kenntnis der Flöhe Deutschlands. III. Faunistik und Ökologie der Säugetierflöhe. Insectivora, Lagomorpha, Rodentia. – Zoologische Jahrbücher für Systematik, Jena

  37. Peus F (1972) Zur Kenntnis Flöhe Deutschlands. – IV. Faunistik und Ökologie der Säugetierflöhe. Schluß. – Zoologische Jahrbücher für Systematik, Jena

  38. Podsiadly E, Chmielewski T, Sochon E, Tylewska- Wierzbanowska S (2007) Bartonella henselae in Ixodes ricinus ticks removed from dogs. Vector Borne Zoonotic Dis 7:189–192

    Article  PubMed  Google Scholar 

  39. Prutsky G, Domecq JP, Mori L, Bebko S, Matzumura M, Sabouni A, Shahrour A, Erwin PJ, Boyce TG, Montori VM, Malaga G, Murad MH (2013) Treatment outcomes of human bartonellosis: a systematic review and meta-analysis. Int J Infect Dis 17(10):e811–e819

    Article  PubMed  Google Scholar 

  40. Relman DA, Falkow S, LeBoit PE, Perkocha LA, Min KW, Welch DF, Slater LN (1991) The organism causing bacillary angiomatosis, peliosis hepatis, and fever and bacteremia in immunocompromised patients. N Engl J Med 324(21):1514

    CAS  PubMed  Google Scholar 

  41. Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G, Plantard O, Vayssier-Taussat M, Bonnet S, Spitalská 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

    Article  PubMed  PubMed Central  Google Scholar 

  42. Sanogo YO, Zeaiter Z, Caruso G, Merola F, Shpynov S, Brouqui P, Raoult D (2003) Bartonella henselae in Ixodes ricinus ticks (Acari: Ixodida) removed from humans, Belluno Province, Italy. Emerg Infect Dis 9(3):329–332

    Article  PubMed  PubMed Central  Google Scholar 

  43. 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 

  44. Schouls LM, Van De Pol I, Rijpkema SG, Schot CS (1999) Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J Clin Microbiol 37(7):2215–2222

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Silaghi C, Woll D, Hamel D, Pfister K, Mahling M, Pfeffer M (2012) Babesia spp. and Anaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents-analyzing the host-pathogen-vector interface in a metropolitan area. Parasit Vectors 5:191

    Article  PubMed  PubMed Central  Google Scholar 

  46. Silaghi C, Knaus M, Rapti D, Shukullari E, Pfister K, Rehbein S (2012) Rickettsia felis and Bartonella spp. in fleas from cats in Albania. Vector Borne Zoonotic Dis 12(1):76–77

    Article  PubMed  Google Scholar 

  47. Siuda K (1991) Kleszcze (Acari: Ixodida) Polski: Zagadnienia ogólne Teil 1 von Kleszcze (Icari: Ixodida) Polski. Monografie parazytologiczne

  48. Stresemann E (1989) Exkursionsfauna von Deutschland, Wirbeltiere. Volume 3. Spektrum Akademischer Verlag, Gustav Fischer, Heidelberg

  49. Telfer S, Clough HE, Birtles LR, Bennett M, Carslake D, Helyar S, Begon M (2007) Ecological differences and coexistence in a guild of microparasites: Bartonella in wild rodents. Ecology 88(7):1841–1849

    Article  PubMed  Google Scholar 

  50. Telford SR, Wormser GP (2010) Bartonella spp. transmission by ticks not established. Emerg Infect Dis 16(3):379–384

    Article  PubMed  PubMed Central  Google Scholar 

  51. Tsai YL, Chuang ST, Chang CC, Kass PH, Chomel BB (2010) Bartonella species in small mammals and their ectoparasites in Taiwan. Am J Trop Med Hyg 83(4):917–923

    Article  PubMed  PubMed Central  Google Scholar 

  52. Tsai YL, Chang CC, Chuang ST, Chomel BB (2011) Bartonella species and their ectoparasites: selective host adaptation or strain selection between the vector and the mammalian host? Comp Immunol Microbiol Infect Dis 34(4):299–314

    Article  PubMed  Google Scholar 

  53. Vayssier-Taussat M, Le Rhun D, Bonnet S, Cotté V (2009) Insights in Bartonella host specificity. Ann N Y Acad Sci 1166:127–132

    Article  PubMed  Google Scholar 

  54. Welc-Faleciak R, Bajer A, Behnke JM, Siński E (2010) The ecology of Bartonella spp. infections in two rodent communities in the Mazury Lake District region of Poland. Parasitology 137(7):1069–1077

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Claudia Thiel for the excellent technical assistance and Dr. Carolin Karnath and Dietlinde Woll for their help in rodent trapping. The Federal Environment Agency of Germany (FKZ 371148) funded part of this project. The work of AO, MP and CS was done under the frame of EurNegVec COST Action TD1303.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Obiegala.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silaghi, C., Pfeffer, M., Kiefer, D. et al. Bartonella, Rodents, Fleas and Ticks: a Molecular Field Study on Host-Vector-Pathogen Associations in Saxony, Eastern Germany. Microb Ecol 72, 965–974 (2016). https://doi.org/10.1007/s00248-016-0787-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0787-8

Keywords

Navigation