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Acta Parasitologica

, Volume 64, Issue 1, pp 19–30 | Cite as

Simultaneous Occurrence of Borrelia miyamotoi, Borrelia burgdorferi Sensu Lato, Anaplasma phagocytophilum and Rickettsia helvetica in Ixodes ricinus Ticks in Urban Foci in Bratislava, Slovakia

  • Tatiana VaculováEmail author
  • Markéta Derdáková
  • Eva Špitalská
  • Radovan Václav
  • Michal Chvostáč
  • Veronika Rusňáková Tarageľová
Original Paper
  • 33 Downloads

Abstract

Background

Questing Ixodes ricinus ticks were collected in two urban parks (Železná studienka and Horský park) of the capital city of Slovakia, Bratislava, during two consecutive years in 2011 and 2012. A total of 932 ticks were analyzed for the presence of tick-borne agents: B. miyamotoi, B. burgdorferi s.l., A. phagocytophilum and R. helvetica.

Results

PCR analysis confirmed the presence of all pathogens at both localities. The overall infection prevalence of B. miyamotoi, B. burgdorferi s.l., A. phagocytophilum and R. helvetica was 0.75, 13.2, 5.6 and 8.9%, respectively. B. burgdorferi s.l. positive samples were represented by six genospecies. The most frequent one was B. afzelii followed by B. garinii and B. valaisiana.

Conclusion

Our study confirms the presence of I. ricinus ticks and at least nine tick-borne bacterial agents in city forest parks, which are used for recreational purposes. Ordination analysis revealed significant differences in the composition of pathogens with respect to study site location, time of season and ambient temperature, despite the fact that both sites are located relatively close to one another within the city.

Keywords

Ixodes ricinus Borrelia miyamotoi Borrelia burgdorferi sensu lato Anaplasma phagocytophilum Rickettsia helvetica Urban foci 

Notes

Acknowledgements

This study was financially supported from the Scientific Grant Agency of Ministry of Education and Slovak Academy of Sciences—mainly by the project VEGA Nos. 2/0119/17 (70%) and partially by VEGA 2/0068/17 and the Slovak Research and Development Agency under contract No. APVV-14-0274, No. APVV-16-0518 and No. APVV-14-0556.

References

  1. 1.
    Barbour A. G., Bunikis J., Travinsky B., Hoen A. G., Diuk-Wasser M. A., Fish D. et al. 2009. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. American Journal of Tropical Medicine and Hygiene, 81, 1120-1131.  https://doi.org/10.4269/ajtmh.2009.09-0208 CrossRefGoogle Scholar
  2. 2.
    Barbour A. G. and Fish D. 1993. The biological and social phenomenon of Lyme disease. Science, 260, 1610-1616.  https://doi.org/10.1126/science.8503006 CrossRefGoogle Scholar
  3. 3.
    Black W. C. and Roehrdanz R. L. 1998. Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Molecular Biology and Evolution, 15, 1772-1785.  https://doi.org/10.1093/oxfordjournals.molbev.a025903 CrossRefGoogle Scholar
  4. 4.
    Boretti F. S., Perreten A., Meli M. L., Cattori V., Willi B., Wengi N. et al. 2009. Molecular Investigations of Rickettsia helvetica infection in dogs, foxes, humans, and Ixodes ticks. Applied and Environmental Microbiology, 75, 3230-3237.  https://doi.org/10.1128/aem.00220-09 CrossRefGoogle Scholar
  5. 5.
    Bown K. J., Begon M., Bennett M., Birtles R. J., Burthe S., Lambin X. et al. 2006. Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector-Borne and Zoonotic Diseases, 6, 404-410.  https://doi.org/10.1089/vbz.2006.6.404 CrossRefGoogle Scholar
  6. 6.
    Bown K. J., Lambin X., Telford G. R., Ogden N. H., Telfer S., Woldehiwet Z. et al. 2008. Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Applied and Environmental Microbiology, 74, 7118-7125.  https://doi.org/10.1128/aem.00625-08 CrossRefGoogle Scholar
  7. 7.
    Brownstein J. S., Skelly D. K., Holford T. R. and Fish D. 2005. Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia, 146, 469-475.  https://doi.org/10.1007/s00442-005-0251-9 CrossRefGoogle Scholar
  8. 8.
    Burri C., Schumann O., Schumann C. and 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 and Tick-borne Diseases, 5, 245-251.  https://doi.org/10.1016/j.ttbdis.2013.11.007 CrossRefGoogle Scholar
  9. 9.
    Casjens S. R., Fraser-Liggett C. M., Mongodin E. F., Qiu W. G., Dunn J. J., Luft B. J. et al. 2011. Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. Journal of Bacteriology, 193, 1489-1490.  https://doi.org/10.1128/jb.01521-10 CrossRefGoogle Scholar
  10. 10.
    Cosson J. F., Michelet L., Chotte J., Le Naour E., Cote M., Devillers E. et al. 2014. Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France. Parasites and Vectors, 7, 233.  https://doi.org/10.1186/1756-3305-7-233 CrossRefGoogle Scholar
  11. 11.
    Courtney J. W., Kostelnik L. M., Zeidner N. S. and Massung R. F. 2004. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. Journal of Clinical Microbiology, 42, 3164-3168.  https://doi.org/10.1128/jcm.42.7.3164-3168.2004 CrossRefGoogle Scholar
  12. 12.
    Dautel H. and Kahl O. 1999. Ticks (Acari: Ixodoidea) and their medical importance in the urban environment. In: Proceedings of the 3rd international conference on urban pests, Prague, pp.73-82Google Scholar
  13. 13.
    de La Fuente J., Naranjo V., Ruiz-Fons F., Hofle U., Fernandez De Mera I. G., Villanua D. et al. 2005. Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector-Borne and Zoonotic Diseases, 5, 390-401.  https://doi.org/10.1089/vbz.2005.5.390 CrossRefGoogle Scholar
  14. 14.
    Derdáková M., Beati L., Pet’ko B., Stanko M. and Fish D. 2003a. Genetic variability within Borrelia burgdorferi sensu lato genospecies established by PCR-single-strand conformation polymorphism analysis of the rrfA-rrlB intergenic spacer in ixodes ricinus ticks from the Czech Republic. Applied and Environmental Microbiology, 69, 509-516.  https://doi.org/10.1128/aem.69.1.509-516.2003 CrossRefGoogle Scholar
  15. 15.
    Derdáková M., Halánová M., Stanko M., Štefančíková A., Čisláková L. and Pet’ko B. 2003b. Molecular evidence for Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from eastern Slovakia. Annals of Agricultural and Environmental Medicine, 10, 269-271.Google Scholar
  16. 16.
    Derdáková M., Štefančíková A., Špitalská E., Tarageľová V., Košťálová T., Hrklová G. et al. 2011. Emergence and genetic variability of Anaplasma species in small ruminants and ticks from Central Europe. Veterinary Microbiology, 153, 293-298.  https://doi.org/10.1016/j.vetmic.2011.05.044 CrossRefGoogle Scholar
  17. 17.
    Derdáková M., Václav R., Pangracová-Blaňárová L., Selyemová D., Koči J., Walder G. et al. 2014. Candidatus Neoehrlichia mikurensis and its co-circulation with Anaplasma phagocytophilum in Ixodes ricinus ticks across ecologically different habitats of Central Europe. Parasites and Vectors, 7, 160.  https://doi.org/10.1186/1756-3305-7-160 CrossRefGoogle Scholar
  18. 18.
    Dister S. W., Fish D., Bros S. M., Frank D. H. and Wood B. L. 1997. Landscape characterization of peridomestic risk for Lyme disease using satellite imagery. The American Journal of Tropical Medicine and Hygiene, 57, 687-692.CrossRefGoogle Scholar
  19. 19.
    Drgonová M. and Řeháček J. 1995. Prevalence of Lyme borrelia in ticks in Bratislava, Slovak Republic. Central European Journal of Public Health, 3, 134-137.Google Scholar
  20. 20.
    Eisen R. J., Piesman J., Zielinski-Gutierrez E. and Eisen L. 2012. What do we need to know about disease ecology to prevent Lyme disease in the northeastern United States? Journal of Medical Entomology, 49, 11-22.  https://doi.org/10.1603/me11138 CrossRefGoogle Scholar
  21. 21.
    Foggie A. 1951. Studies on the infectious agent of tick-borne fever in sheep. Journal of Pathology and Bacteriology, 63, 1-15.  https://doi.org/10.1002/path.1700630103 CrossRefGoogle Scholar
  22. 22.
    Földvári G., Jahfari S., Rigó K., Jablonszky M., Szekeres S., Majoros G. et al. 2014. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in urban hedgehogs. Emerging Infectious Diseases Journal, 20, 496-498.  https://doi.org/10.3201/eid2003.130935 CrossRefGoogle Scholar
  23. 23.
    Földvári G., Rigó K., Jablonszky M., Biró N., Majoros G., Molnár V. et al. 2011. Ticks and the city: ectoparasites of the Northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks and Tick-borne Diseases, 2, 231-234.  https://doi.org/10.1016/j.ttbdis.2011.09.001 CrossRefGoogle Scholar
  24. 24.
    Fukunaga M., Takahashi Y., Tsuruta Y., Matsushita O., Ralph D., McClelland M. et al. 1995. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. International Journal of Systematic Bacteriology, 45, 804-810.  https://doi.org/10.1099/00207713-45-4-804 CrossRefGoogle Scholar
  25. 25.
    Gabriel K. R. 2002. Goodness of fit of biplots and correspondence analysis Biometrica, 89, 423-436.Google Scholar
  26. 26.
    Glatz M., Müllegger R. R., Maurer F., Fingerle V., Achermann Y., Wilske B. et al. 2014. Detection of Candidatus Neoehrlichia mikurensis, Borrelia burgdorferi sensu lato genospecies and Anaplasma phagocytophilum in a tick population from Austria. Ticks and Tick-borne Diseases, 5, 139-144.  https://doi.org/10.1016/j.ttbdis.2013.10.006 CrossRefGoogle Scholar
  27. 27.
    Gray J. S., Kahl O., Janetzki-Mittman C., Stein J. and Guy E. 1994. Acquisition of Borrelia burgdorferi by Ixodes ricinus ticks fed on the European hedgehog, Erinaceus europaeus. Experimental and Applied Acarology, 18, 485-491.CrossRefGoogle Scholar
  28. 28.
    Guy E. C. and Stanek G. 1991. Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. Journal of Clinical Pathology, 44, 610-611.CrossRefGoogle Scholar
  29. 29.
    Hamšíková Z., Coipan C., Mahríková L., Minichová L., Sprong H. and Kazimírová M. 2017. Borrelia miyamotoi and co-Infection with Borrelia afzelii in Ixodes ricinus ticks and rodents from Slovakia. Microbial Ecology, 73, 1000-1008.  https://doi.org/10.1007/s00248-016-0918-2 CrossRefGoogle Scholar
  30. 30.
    Han S., Hickling G. J. and Tsao J. I. 2016. High Prevalence of Borrelia miyamotoi among adult blacklegged ticks from white-tailed deer. Emerging Infectious Diseases Journal, 22, 316-318.  https://doi.org/10.3201/eid2202.151218 CrossRefGoogle Scholar
  31. 31.
    Hanincová K., Tarageľová V., Koči J., Schäfer S. M., Hails R., Ullmann A. J. et al. 2003. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Applied and Environmental Microbiology, 69, 2825-2830.  https://doi.org/10.1128/aem.69.5.2825-2830.2003 CrossRefGoogle Scholar
  32. 32.
    Hansford K. M., Fonville M., Gillingham E. L., Coipan E. C., Pietzsch M. E., Krawczyk A. I. et al. 2017. Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England. Ticks and Tick-borne Diseases, 8, 353-361.  https://doi.org/10.1016/j.ttbdis.2016.12.009 CrossRefGoogle Scholar
  33. 33.
    Hornok S., Meli M. L., Gönczi E., Halász E., Takács N., Farkas R. et al. 2014. Occurrence of ticks and prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi s.l. in three types of urban biotopes: forests, parks and cemeteries. Ticks and Tick-borne Diseases, 5, 785-789.  https://doi.org/10.1016/j.ttbdis.2014.05.010 CrossRefGoogle Scholar
  34. 34.
    Hubálek Z. and Halouzka J. 1998. Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research, 84, 167-172.CrossRefGoogle Scholar
  35. 35.
    Hubálek Z. and Rudolf I. 2007. Microbial Zoonoses and Sapronoses Springer, Dordrecht, 176 pp.Google Scholar
  36. 36.
    Hulínská D., Langrová K., Pejcoch M. and Pavlásek I. 2004. Detection of Anaplasma phagocytophilum in animals by real-time polymerase chain reaction. Acta Pathologica, Microbiologica et Immunologica Scandinavica, 112, 239-247.  https://doi.org/10.1111/j.1600-0463.2004.apm11204-0503.x CrossRefGoogle Scholar
  37. 37.
    Ivanova L. B., Tomova A., González-Acuña D., Murúa R., Moreno C. X., Hernández C. et al. 2014. Borrelia chilensis, a new member of the Borrelia burgdorferi sensu lato complex that extends the range of this genospecies in the Southern Hemisphere. Environmental Microbiology, 16, 1069-1080.  https://doi.org/10.1111/1462-2920.12310 CrossRefGoogle Scholar
  38. 38.
    Korenberg E., Černý V. and Daniel M. 1984. Occurrence of ixodid ticks-the main vectors of tick-borne encephalitis virus in urbanized territory. Folia Parasitologica, 31, 365-370.Google Scholar
  39. 39.
    Kurtenbach K., De Michelis S., Etti S., Schäfer S. M., Sewell H. S., Brade V. et al. 2002. Host association of Borrelia burgdorferi sensu lato-the key role of host complement. Trends in Microbiology, 10, 74-79.  https://doi.org/10.1016/s0966-842x(01)02298-3 CrossRefGoogle Scholar
  40. 40.
    Legendre P. and Legendre L. F. 2012. Numerical Ecology Elsevier, pp. 1006Google Scholar
  41. 41.
    Liz J. S., Anderes L., Sumner J. W., Massung R. F., Gern L., Rutti B. et al. 2000. PCR detection of granulocytic ehrlichiae in Ixodes ricinus ticks and wild small mammals in western Switzerland. Journal of Clinical Microbiology, 38, 1002-1007.Google Scholar
  42. 42.
    Majláthová V., Majláth I., Derdáková M., Víchová B. and Pet’ko B. 2006. Borrelia lusitaniae and green lizards (Lacerta viridis), Karst Region, Slovakia. Emerging Infectious Diseases Journal, 12, 1895-1901.  https://doi.org/10.3201/eid1212.060784 CrossRefGoogle Scholar
  43. 43.
    Margos G., Hojgaard A., Lane R. S., Cornet M., Fingerle V., Rudenko N. et al. 2010. Multilocus sequence analysis of Borrelia bissettii strains from North America reveals a new Borrelia species, Borrelia kurtenbachii. Ticks and Tick-borne Diseases, 1, 151-158.  https://doi.org/10.1016/j.ttbdis.2010.09.002 CrossRefGoogle Scholar
  44. 44.
    Margos G., Vollmer S. A., Cornet M., Garnier M., Fingerle V., Wilske B. et al. 2009. A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Applied and Environmental Microbiology, 75, 5410-5416.  https://doi.org/10.1128/aem.00116-09 CrossRefGoogle Scholar
  45. 45.
    Massung R. F., Levin M. L., Munderloh U. G., Silverman D. J., Lynch M. J., Gaywee J. K. et al. 2007. Isolation and propagation of the Ap-Variant 1 strain of Anaplasma phagocytophilum in a tick cell line. Journal of Clinical Microbiology, 45, 2138-2143.  https://doi.org/10.1128/jcm.00478-07 CrossRefGoogle Scholar
  46. 46.
    Matuschka F. R., Endepols S., Richter D. and Spielman A. 1997. Competence of urban rats as reservoir hosts for Lyme disease spirochetes. Journal of Medical Entomology, 34, 489-493.CrossRefGoogle Scholar
  47. 47.
    Maupin G. O., Fish D., Zultowsky J., Campos E. G. and Piesman J. 1991. Landscape ecology of Lyme disease in a residential area of Westchester County, New York. American Journal of Epidemiology, 133, 1105-1113.CrossRefGoogle Scholar
  48. 48.
    May K. and Strube C. 2014. Prevalence of Rickettsiales (Anaplasma phagocytophilum and Rickettsia spp.) in hard ticks (Ixodes ricinus) in the city of Hamburg, Germany. Parasitology Research, 113, 2169-2175.  https://doi.org/10.1007/s00436-014-3869-x CrossRefGoogle Scholar
  49. 49.
    McKinney M. L. 2006. Urbanization as a major cause of biotic homogenization. Biological Conservation, 127, 247-260.  https://doi.org/10.1016/j.biocon.2005.09.005 CrossRefGoogle Scholar
  50. 50.
    Medlock J. M., Hansford K. M., Bormane A., Derdáková M., Estrada-Peña A., George J. C. et al. 2013. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites and Vectors, 6, 1.  https://doi.org/10.1186/1756-3305-6-1 CrossRefGoogle Scholar
  51. 51.
    Menardi G., Floris R., Mignozzi K., Boemo B., Altobelli A. and Cinco M. 2008. Detection and genotyping of Borrelia burgdorferi in the trans-border area between Italy and Slovenia and evaluation of co-infection with Anaplasma phagocytophilum in ticks. International Journal of Medical Microbiology, 298, 121-124.  https://doi.org/10.1016/j.ijmm.2008.01.007 CrossRefGoogle Scholar
  52. 52.
    Munderloh U. G., Madigan J. E., Dumler J. S., Goodman J. L., Hayes S. F., Barlough J. E. et al. 1996. Isolation of the equine granulocytic ehrlichiosis agent, Ehrlichia equi, in tick cell culture. Journal of Clinical Microbiology, 34, 664-670.Google Scholar
  53. 53.
    Nosek J. and Sixl W. 1972. Central-European ticks (Ixodoidea). Key for determination. Mitteilungen der Abteilung für Zoologie am Landesmuseum Joanneum, 1, 61-92.Google Scholar
  54. 54.
    Oksanen J., Blanchet F. G., Friendly M., Kindt R., Legendre P., Mcglinn D. et al. (2011) Vegan: community ecology package. Version 2.4-1.Google Scholar
  55. 55.
    Platonov A. E., Karan L. S., Kolyasnikova N. M., Makhneva N. A., Toporkova M. G., Maleev V. V. et al. 2011. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerging Infectious Diseases Journal, 17, 1816-1823.  https://doi.org/10.3201/eid1710.101474 CrossRefGoogle Scholar
  56. 56.
    Postic D., Garnier M. and Baranton G. 2007. Multilocus sequence analysis of atypical Borrelia burgdorferi sensu lato isolates–description of Borrelia californiensis sp. nov., and genomospecies 1 and 2. International Journal of Medical Microbiology, 297, 263-271.  https://doi.org/10.1016/j.ijmm.2007.01.006 CrossRefGoogle Scholar
  57. 57.
    Pritt B. S., Mead P. S., Johnson D. K. H., Neitzel D. F., Respicio-Kingry L. B., Davis J. P. et al. 2016. Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study. The Lancet Infectious Diseases, 16, 556-564.  https://doi.org/10.1016/s1473-3099(15)00464-8 CrossRefGoogle Scholar
  58. 58.
    Rauter C. and Hartung T. 2005. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Applied and Environmental Microbiology, 71, 7203-7216.  https://doi.org/10.1128/aem.71.11.7203-7216.2005 CrossRefGoogle Scholar
  59. 59.
    Regnery R. L., Spruill C. L. and Plikaytis B. D. 1991. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. Journal of Bacteriology, 173, 1576-1589.  https://doi.org/10.1128/jb.173.5.1576-1589.1991 CrossRefGoogle Scholar
  60. 60.
    Reis C., Cote M., Paul R. E. and Bonnet S. 2011. Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector-Borne and Zoonotic Diseases, 11, 907-916.  https://doi.org/10.1089/vbz.2010.0103 CrossRefGoogle Scholar
  61. 61.
    Richter D. and Matuschka F. R. 2010. Elimination of lyme disease spirochetes from ticks feeding on domestic ruminants. Applied and Environmental Microbiology, 76, 7650-7652.  https://doi.org/10.1128/aem.01649-10 CrossRefGoogle Scholar
  62. 62.
    Richter D., Postic D., Sertour N., Livey I., Matuschka F. R. and Baranton G. 2006. Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. International Journal of Systematic and Evolutionary Microbiology, 56, 873-881.  https://doi.org/10.1099/ijs.0.64050-0 CrossRefGoogle Scholar
  63. 63.
    Richter D., Schlee D. B. and Matuschka F. R. 2003. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerging Infectious Diseases Journal, 9, 697-701.  https://doi.org/10.3201/eid0906.020459 CrossRefGoogle Scholar
  64. 64.
    Richter D., Schlee D. B. and Matuschka F. R. 2011. Reservoir competence of various rodents for the lyme disease Spirochete Borrelia spielmanii. Applied and Environmental Microbiology, 77, 3565-3570.  https://doi.org/10.1128/aem.00022-11 CrossRefGoogle Scholar
  65. 65.
    Rizzoli A., Silaghi C., Obiegala A., Rudolf I., Hubálek Z., Földvári G. et al. 2014. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Frontiers in Public Health, 2, 251.  https://doi.org/10.3389/fpubh.2014.00251 CrossRefGoogle Scholar
  66. 66.
    Rudenko N., Golovchenko M., Grubhoffer L. and Oliver J. H., Jr. 2009a. Borrelia carolinensis sp. nov., a new (14th) member of the Borrelia burgdorferi sensu lato complex from the southeastern region of the United States. Journal of Clinical Microbiology, 47, 134-141.  https://doi.org/10.1128/jcm.01183-08 CrossRefGoogle Scholar
  67. 67.
    Rudenko N., Golovchenko M., Lin T., Gao L., Grubhoffer L. and Oliver J. H., Jr. 2009b. Delineation of a new species of the Borrelia burgdorferi Sensu Lato Complex, Borrelia americana sp. nov. Journal of Clinical Microbiology, 47, 3875-3880.  https://doi.org/10.1128/jcm.01050-09 CrossRefGoogle Scholar
  68. 68.
    Scoles G. A., Papero M., Beati L. and Fish D. 2001. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector-Borne and Zoonotic Diseases, 1, 21-34.  https://doi.org/10.1089/153036601750137624 CrossRefGoogle Scholar
  69. 69.
    Scott M. C., Rosen M. E., Hamer S. A., Baker E., Edwards H., Crowder C. et al. 2010. High-prevalence Borrelia miyamotoi infection among wild turkeys (Meleagris gallopavo) in Tennessee. Journal of Medical Entomology, 47, 1238-1242.  https://doi.org/10.1603/me10075 CrossRefGoogle Scholar
  70. 70.
    Skarphédinsson S., Lyholm B. F., Ljungberg M., Sogaard P., Kolmos H. J. and Nielsen L. P. 2007. Detection and identification of Anaplasma phagocytophilum, Borrelia burgdorferi, and Rickettsia helvetica in Danish Ixodes ricinus ticks. Acta Pathologica, Microbiologica et Immunologica Scandinavica, 115, 225-230.  https://doi.org/10.1111/j.1600-0463.2007.apm_256.x CrossRefGoogle Scholar
  71. 71.
    Slovák M. 2010. Pictorial key to the adults of ticks (Acari: Ixodida) of the Slovakia fauna. Entomofauna carpathica, 22, 8-13.Google Scholar
  72. 72.
    Smetanová K., Schwarzová K. and Kocianová E. 2006. Detection of Anaplasma phagocytophilum, Coxiella burnetii, Rickettsia spp., and Borrelia burgdorferi s. l. in ticks, and wild-living animals in western and middle Slovakia. Annals of the New York Academy of Sciences, 1078, 312-315.  https://doi.org/10.1196/annals.1374.058 CrossRefGoogle Scholar
  73. 73.
    Stuen S., Scharf W., Schauer S., Freyburger F., Bergstrom K. and von Loewenich F. D. 2010. Experimental infection in lambs with a red deer (Cervus elaphus) isolate of Anaplasma phagocytophilum. Journal of Wildlife Diseases, 46, 803-809.  https://doi.org/10.7589/0090-3558-46.3.803 CrossRefGoogle Scholar
  74. 74.
    Subramanian G., Sekeyová Z., Raoult D. and Mediannikov O. 2012. Multiple tick-associated bacteria in Ixodes ricinus from Slovakia. Ticks and Tick-borne Diseases, 3, 406-410.  https://doi.org/10.1016/j.ttbdis.2012.10.001 CrossRefGoogle Scholar
  75. 75.
    Sytykiewicz H., Karbowiak G., Hapunik J., Szpechcinski A., Supergan-Marwicz M., Golawska S. et al. 2012. Molecular evidence of Anaplasma phagocytophilum and Babesia microti co-infections in Ixodes ricinus ticks in central-eastern region of Poland. Annals of Agricultural and Environmental Medicine, 19, 45-49.Google Scholar
  76. 76.
    Szekeres S., Coipan E. C., Rigó K., Majoros G., Jahfari S., Sprong H. et al. 2015. Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary. Parasites and Vectors, 8, 309.  https://doi.org/10.1186/s13071-015-0922-2 CrossRefGoogle Scholar
  77. 77.
    Špitalská E., Boldiš V., Derdáková M., Selyemová D. and Rusňáková Tarageľová V. 2014. Rickettsial infection in Ixodes ricinus ticks in urban and natural habitats of Slovakia. Ticks and Tick-borne Diseases, 5, 161-165.  https://doi.org/10.1016/j.ttbdis.2013.10.002 CrossRefGoogle Scholar
  78. 78.
    Špitalská E. and Kocianová E. 2002. Agents of Ehrlichia phagocytophila group and other microorganisms co-infecting ticks in southwestern Slovakia. Acta Virologica, 46, 49-50.Google Scholar
  79. 79.
    Špitalská E., Stanko M., Mošanský L., Kraljik J., Miklisová D., Mahríková L. et al. 2016. Seasonal analysis of Rickettsia species in ticks in an agricultural site of Slovakia. Experimental and Applied Acarology, 68, 315-324.  https://doi.org/10.1007/s10493-015-9941-0 CrossRefGoogle Scholar
  80. 80.
    Štefanidesová K., Kocianová E., Boldiš V., Košťanová Z., Kanka P., Nemethová D. et al. 2008. Evidence of Anaplasma phagocytophilum and Rickettsia helvetica infection in free-ranging ungulates in central Slovakia. European Journal of Wildlife Research, 54, 519-524.  https://doi.org/10.1007/s10344-007-0161-8 CrossRefGoogle Scholar
  81. 81.
    Švehlová A., Berthová L., Sallay B., Boldiš V., Sparagano O. A. and Špitalská E. 2014. Sympatric occurrence of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks and Rickettsia and Babesia species in Slovakia. Ticks and Tick-borne Diseases, 5, 600-605.  https://doi.org/10.1016/j.ttbdis.2014.04.010 CrossRefGoogle Scholar
  82. 82.
    Tarageľová V. R., Mahríková L., Selyemová D., Václav R. and Derdáková M. 2016. Natural foci of Borrelia lusitaniae in a mountain region of Central Europe. Ticks and Tick-borne Diseases, 7, 350-356.  https://doi.org/10.1016/j.ttbdis.2015.12.006 CrossRefGoogle Scholar
  83. 83.
    Team R. C. 2016. R: A language and environment for statistical computing. 15. AprilGoogle Scholar
  84. 84.
    Venczel R., Knoke L., Pavlovic M., Dzaferovic E., Vaculová T., Silaghi C. et al. 2016. A novel duplex real-time PCR permits simultaneous detection and differentiation of Borrelia miyamotoi and Borrelia burgdorferi sensu lato. Infection, 44, 47-55.  https://doi.org/10.1007/s15010-015-0820-8 CrossRefGoogle Scholar
  85. 85.
    Víchová B., Majláthová V., Nováková M., Stanko M., Hviščová I., Pangrácová L. et al. 2014. Anaplasma infections in ticks and reservoir host from Slovakia. Infection Genetics and Evolution, 22, 265-272.  https://doi.org/10.1016/j.meegid.2013.06.003 CrossRefGoogle Scholar
  86. 86.
    Wagemakers A., Staarink P. J., Sprong H. and Hovius J. W. 2015. Borrelia miyamotoi: a widespread tick-borne relapsing fever spirochete. Trends in Parasitology, 31, 260-269.  https://doi.org/10.1016/j.pt.2015.03.008 CrossRefGoogle Scholar
  87. 87.
    Wang G., van Dam A. P., Le Fleche A., Postic D., Peter O., Baranton G. et al. 1997. Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19). International Journal of Systematic Bacteriology, 47, 926-932.  https://doi.org/10.1099/00207713-47-4-926 CrossRefGoogle Scholar
  88. 88.
    Wilhelmsson P., Fryland L., Börjesson S., Nordgren J., Bergström S., Ernerudh J. et al. 2010. Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. Journal of Clinical Microbiology, 48, 4169-4176.  https://doi.org/10.1128/jcm.01061-10 CrossRefGoogle Scholar
  89. 89.
    Woldehiwet Z. 2010. The natural history of Anaplasma phagocytophilum. Veterinary Parasitology, 167, 108-122.  https://doi.org/10.1016/j.vetpar.2009.09.013 CrossRefGoogle Scholar
  90. 90.
    Wood C. L. and Lafferty K. D. 2013. Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution, 28, 239-247.  https://doi.org/10.1016/j.tree.2012.10.011 CrossRefGoogle Scholar
  91. 91.
    Zygner W., Gorski P. and Wedrychowicz H. 2009. Detection of the DNA of Borrelia afzelii, Anaplasma phagocytophilum and Babesia canis in blood samples from dogs in Warsaw. Veterinary Record, 164, 465-467.  https://doi.org/10.1136/vr.164.15.465 CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  • Tatiana Vaculová
    • 1
    Email author
  • Markéta Derdáková
    • 1
  • Eva Špitalská
    • 2
  • Radovan Václav
    • 1
  • Michal Chvostáč
    • 1
  • Veronika Rusňáková Tarageľová
    • 1
  1. 1.Institute of Zoology, Slovak Academy of SciencesBratislavaSlovak Republic
  2. 2.Institute of Virology, Biomedical Research CenterSlovak Academy of SciencesBratislavaSlovak Republic

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