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Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia

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Abstract

To evaluate the prevalence rate of tick-borne bacterial pathogens, unfed adult Ixodes ricinus ticks were collected from vegetation in 2001, 2003, and 2004 at 18 localities throughout Serbia. A total of 287 ticks were examined by PCR technique for the presence of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, and Francisella tularensis. The highest prevalence rate was that for B. burgdorferi sensu lato (42.5%), followed by A. phagocytophilum (13.9%) and F. tularensis (3.8%). The presence of five B. burgdorferi sensu lato genospecies, namely, B. burgdorferi sensu stricto, B. afzelii, B. garinii, B. lusitaniae, and B. valaisiana was identified by restriction fragment length polymorphism (RFLP) analysis. The most frequent B. burgdorferi sensu lato genospecies was B. lusitaniae, followed by B. burgdorferi sensu stricto. Co-infection by B. burgdorferi sensu stricto and B. lusitaniae was frequently observed. Co-infection by B. burgdorferi sensu lato and A. phagocytophilum and co-infection by B. burgdorferi sensu lato and F. tularensis appeared in 24 ticks. Sequencing of p44/msp2 paralogs of Serbian A. phagocytophilum showed that they were unique and distinct from those of A. phagocytophilum in US and UK. This is the first report of B. garinii, B. lusitaniae, B. valaisiana, as well as A. phagocytophilum and F. tularensis infected ticks in Serbia. These findings indicate a public health threat in Serbia of tick-borne diseases caused by B. burgdorferi sensu lato, A. phagocytophilum and F. tularensis.

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References

  • Casey ANJ, Birtles RJ, Radford AD et al (2004) Groupings of highly similar major surface protein (p44)-encoding paralogues: a potential index of genetic diversity amongst isolates of Anaplasma phagocytophilum. Microbiology 150:727–734

    Article  PubMed  CAS  Google Scholar 

  • Chen SM, Dumler JS, Bakken JS et al (1994) Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human diseases. J Clin Microbiol 32:589–595

    PubMed  CAS  Google Scholar 

  • Christova I, Schouls L, Van De Poul I et al (2001) High prevalence of granulocytic ehrlichiae and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from Bulgaria. J Clin Microbiol 39:4172–4174

    Article  PubMed  CAS  Google Scholar 

  • Collares-Pereira M, Couceiro S, Franca I et al (2004) First isolation of Borrelia lusitaniae from a human patient. J Clin Microbiol 42:1316–1318

    Article  PubMed  CAS  Google Scholar 

  • Derdáková M, Lenčáková D (2005) Association of genetic variability within the Borrelia burgdorferi sensu lato with the ecology, epidemiology of Lyme borreliosis in Europe. Ann Agric Environ Med 12:165–172

    PubMed  Google Scholar 

  • Dsouli N, Younsi-Kabachii H, Postic D et al (2006) Reservoir role of lizard Psammodromus algirus in transmission cycle of Borrelia burgdorferi sensu lato (Spirochaetaceae) in Tunisia. J Med Entomol 43:737–742

    Article  PubMed  Google Scholar 

  • Đokić M, Ćurčić P, Nožić D et al (2006) Human ehrlichiosis. Vojnosanit Pregl 63:403–408 (in Serbian)

    PubMed  Google Scholar 

  • Földvári G, Farkas R, Lakos A (2005) Borrelia spielmani erythema migrans, Hungary. Emerg Infect Dis 11:1794

    PubMed  Google Scholar 

  • Fukunaga M, Yabuki M, Hamase A et al (2000) Molecular phylogenetic analysis of ixodid ticks based on the ribosomal DNA spacer, internal transcribed spacer 2, sequences. J Parasitol 86:38–43

    PubMed  CAS  Google Scholar 

  • Grzeszczuk A, Stańczak J (2006) High prevalence of Anaplasma phagocytophilum infection in ticks removed from human skin in north-eastern Poland. Ann Agric Environ Med 13:45–48

    PubMed  Google Scholar 

  • Güner ES, Hashimoto N, Takada N et al (2003) First isolation and characterization of Borrelia burgdorferi sensu lato strains from Ixodes ricinus ticks in Turkey. J Med Microbiol 52:807–813

    Article  PubMed  CAS  Google Scholar 

  • Halos L, Vourc’h G, Cotte V et al (2006) Prevalence of Anaplasma phagocytophilum, Rickettsia sp and Borrelia burgdorferi sensu lato DNA in questing Ixodes ricinus ticks from France. Ann N Y Acad Sci 1078:316–319

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt A, Schmidt KH, Wilske B et al (2003) Prevalence of four species of Borrelia burgdorferi sensu lato and coinfection with Anaplasma phagocytophila in Ixodes ricinus ticks in central Germany. Eur J Clin Microbiol Infect Dis 22:364–367

    Article  PubMed  CAS  Google Scholar 

  • Hotopp JCD, Lin M, Madupu R (2006) Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2:208–223

    Article  CAS  Google Scholar 

  • Hubálek Z, Halouzka J (1997) Mosquitoes (Diptera: Culicidae), in contrast to ticks (Acari: Ixodidae), do not carry Francisella tularensis in a natural focus of tularemia in the Czech Republic. J Med Entomol 34:660–663

    PubMed  Google Scholar 

  • Hubálek Z, Treml F, Halouzka J et al (1996) Frequent isolation of Francisella tularensis from Dermacentor reticulatus ticks in an enzootic focus of tularaemia. Med Vet Entomol 10:241–246

    Article  PubMed  Google Scholar 

  • Kantardijev T, Ivanov I, Velinov T et al (2006) Tularemia outbreak, Bulgaria, 1997–2005. Emerg Infect Dis 12:678–680

    Google Scholar 

  • Kurtenbach K, De Michelis S, Sewell H-S (2001) Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol 67:4926–4929

    Article  PubMed  CAS  Google Scholar 

  • Kurtenbach K, De Michelis S, Etti S et al (2002) Host association of Borrelia burgdorferi sensu lato—the key role of host complement. Trends Microbiol 10:74–79

    Article  PubMed  CAS  Google Scholar 

  • Lako B, Ristanović E, Spasić M et al (2001) The first epidemy of tularemia in FR Yugoslavia. ASA Newslett 5:19–20

    Google Scholar 

  • Majláthová V, Majláth I, Derdáková M et al (2006) Borrelia lusitaniae and green lizards (Lacerta viridis), Karst Region, Slovakia. Emerg Infect Dis 12:1895–1901

    PubMed  Google Scholar 

  • Mannelli A, Cerri D, Buffrini L et al (1999) Low risk of Lyme borreliosis in a protected area on the Tyrrhenian coast, in central Italy. Eur J Epidemiol 15:371–377

    Article  PubMed  CAS  Google Scholar 

  • Mantelli B, Pecchioli E, Hauffe HC et al (2006) Prevalence of Borrelia burgdorferi s.l. and Anaplasma phagocytophilum in the wood tick Ixodes ricinus in the Province of Trento, Italy. Eur J Clin Microbiol Infect Dis 25:737–739

    Article  PubMed  CAS  Google Scholar 

  • Masuzawa T, Komikado T, Iwaki A et al (1996) Characterization of Borrelia sp. isolated from Ixodes tanuki, I. turdus, and I. columnae in Japan by restriction fragment length polymorphism of rrf (5S)–rrl (23S) intergenic spacer amplicons. FEMS Microbiol Lett 142:77–83

    Article  PubMed  CAS  Google Scholar 

  • Milutinović M (1992) Ecological investigations of ticks (Acarina, Ixodoidea, Ixodidae) of Serbia. Dissertation, University of Belgrade (in Serbian)

  • Milutinović M, Radulović Ž (2002) Ecological notes on ticks (Acari: Ixodidae) in Serbia (central regions). Acta Vet 52:49–58

    Article  Google Scholar 

  • Milutinović M, Radulović Ž, Tomanović S et al (2006) Seasonal distribution of borreliae in Ixodes ricinus ticks in the Belgrade region, Serbia. Arch Biol Sci 58:183–186

    Google Scholar 

  • Ogden NH, Woldehiwet Z, Hart CA (1998) Granulocytic ehrlichiosis: an emerging or rediscovered tick-borne disease? J Med Microbiol 47:475–482

    PubMed  CAS  Google Scholar 

  • Ohashi N, Inayoshi M, Kitamura K et al (2005) Anaplasma phagocytophilum-infected ticks, Japan. Emerg Infect Dis 11:1780–1783

    PubMed  Google Scholar 

  • Petrovec M, Lotrič-Furlan S, Avšič-Županc T et al (1997) Human disease in Europe caused by a granulocytic Ehrlichia species. J Clin Microbiol 35:1556–1559

    PubMed  CAS  Google Scholar 

  • Postic D, Assous MV, Grimont PAD (1994) Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)–rrl (23S) intergenic spacer amplicons. Int J Syst Bacteriol 44:743–752

    Article  PubMed  CAS  Google Scholar 

  • Poupon MA, Lommano E, Humair PF et al (2006) Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl Environ Microbiol 72:976–979

    Article  CAS  Google Scholar 

  • Rauter C, Hartung T (2005) Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl Environ Microbiol 71:7203–7216

    Article  PubMed  CAS  Google Scholar 

  • Reintjes R, Dedushaj I, Gjini A (2002) Tularemia outbreak investigation in Kosovo: case control and environmental studies. Emerg Infect Dis 8:69–73

    PubMed  Google Scholar 

  • Richter D, Postic D, Sertour N et al (2006) Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. Int J Syst Evol Microbiol 56:873–881

    Article  PubMed  CAS  Google Scholar 

  • Rijpkema S, Golubić D, Molkenboer M et al (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

    Article  PubMed  CAS  Google Scholar 

  • Ristanović ES, Kitamura K, Masuzawa T et al (2007) Molecular characterization of Borrelia burgdorferi sensu lato strains isolated in the area of Belgrade, Serbia. Braz J Microbiol 38:14–16

    Google Scholar 

  • Ružić-Sabljić E, Strle F, Cimperman J (2000) Characterisation of Borrelia burgdorferi sensu lato strains isolated from patient with skin manifestations of Lyme borreliosis residing in Slovenia. J Med Microbiol 49:47–53

    PubMed  Google Scholar 

  • Sanogo YO, Parola P, Shpynov S et al (2004) Genetic diversity of bacterial agents detected in ticks removed from asymptomatic patients in northeastern Italy. Ann N Y Acad Sci 990:182–190

    Article  Google Scholar 

  • Sjöstedt A, Kuoppa K, Johansson T et al (1992) The 17 kDa lipoprotein and encoding gene of Francisella tularensis LSV are conserved in strains of Francisella tularensis. Microb Pathog 13:243–249

    Article  PubMed  Google Scholar 

  • Sjöstedt A, Eriksson U, Berglund L et al (1997) Detection of Francisella tularensis in ulcers of patients with tularemia by PCR. J Clin Microbiol 35:1045–1048

    PubMed  Google Scholar 

  • Stanczak J, Kubica-Biernat B, Racewicz M (2000) Detection of three genospecies of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in different regions of Poland. Int J Med Microbiol 290:559–566

    PubMed  CAS  Google Scholar 

  • Strle F (1999) Lyme borreliosis in Slovenia. Zentralbl Bakteriol 289:643–652

    PubMed  CAS  Google Scholar 

  • Van Dam AP, Kuiper H, Vos K et al (1993) Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin Infect Dis 17:708–717

    PubMed  Google Scholar 

  • Wodecka B, Skotarczak B (2005) First isolation of Borrelia lusitaniae DNA from Ixodes ricinus ticks in Poland. Scand J Infect Dis 37:27–34

    Article  PubMed  CAS  Google Scholar 

  • Zhi N, Ohashi N, Tajima T et al (2002) Transcript heterogeneity of the p44 multigene family in a human granulocytic ehrlichiosis agent transmitted by ticks. Infect Immun 70:1175–1184

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Ministry of Science and Environmental Protection of the Republic of Serbia (Project No. 1726 and 145002) and by Chiba Institute Science (CIS) research grants.

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Authors and Affiliations

  1. Laboratory for Medical Arachnoentomology, Centre for Parasitic Zoonoses, Institute for Medical Research, University of Belgrade, P.O. Box 102, Dr. Subotića 4, 11129, Belgrade, Serbia

    Marija Milutinović, Snežana Tomanović & Željko Radulović

  2. Laboratory of Microbiology & Immunology, Faculty of Pharmaceutical Sciences, Chiba Institute of Science (CIS), Shiomi-3, Choshi, Chiba, 288-0025, Japan

    Toshiyuki Masuzawa, Takashi Fukui & Yoshihiro Okamoto

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  1. Marija Milutinović
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  2. Toshiyuki Masuzawa
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  3. Snežana Tomanović
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  4. Željko Radulović
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  5. Takashi Fukui
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  6. Yoshihiro Okamoto
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Correspondence to Marija Milutinović.

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Milutinović, M., Masuzawa, T., Tomanović, S. et al. Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol 45, 171–183 (2008). https://doi.org/10.1007/s10493-008-9166-6

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  • DOI: https://doi.org/10.1007/s10493-008-9166-6

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