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High prevalence of Babesia microti ‘Munich’ type in small mammals from an Ixodes persulcatus/Ixodes trianguliceps sympatric area in the Omsk region, Russia

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Abstract

Babesia microti is a genetically diverse group of protozoan parasites whose life cycle is associated with both small mammals and Ixodes spp. ticks. In this study, the prevalence of different B. microti genetic groups in ticks and small rodents in an area with Ixodes persulcatus and Ixodes trianguliceps occurring in sympatry was examined. A total of 541 small mammals were captured during eight sampling periods between 2013 and 2015 at a site in the Omsk region of Russia and tested for the presence of B. microti using nested PCR with subsequent sequencing of positive samples. B. microti DNA was found in 31.6 % of examined samples, and prevalence rates ranged from 5.3 to 61.6 % in different sampling periods. The sequenced B. microti samples belonged to two genetic groups: enzootic B. microti ‘Munich’ type and zoonotic B. microti ‘US’ type. B. microti ‘Munich’ type was more common across all sampling periods, with greater than 80 % prevalence in infected animals. Despite the high B. microti ‘Munich’-type prevalence in voles, B. microti was not found in any of 394 adult I. persulcatus ticks collected by flagging or in the 84 I. persulcatus or 20 I. trianguliceps ticks taken from voles and molted under laboratory conditions. It was demonstrated that B. microti ‘Munich’-type DNA can be detected in the blood of naturally infected voles for at least 20 weeks after capture. Thus, the high prevalence of B. microti ‘Munich’ type in small mammals may be explained by the prolonged persistence of B. microti in the blood of wild voles.

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References

  • Bajer A, Welc-Falęciak R, Bednarska M, Alsarraf M, Behnke-Borowczyk J, Siński E, Behnke JM (2014) Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of bank voles (Myodes glareolus) in NE Poland. Microb Ecol 68:196–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Beck R, Vojta L, Curković S, Mrljak V, Margaletić J, Habrun B (2011) Molecular survey of Babesia microti in wild rodents in central Croatia. Vector Borne Zoonotic Dis 11:81–83

    Article  PubMed  Google Scholar 

  • Bednarska M, Bajer A, Drozdowska A, Mierzejewska EJ, Tolkacz K, Welc-Falęciak R (2015) Vertical transmission of Babesia microti in BALB/c mice: preliminary report. PLoS One 10(9):e0137731

    Article  PubMed  PubMed Central  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

    Article  PubMed  Google Scholar 

  • Bown KJ, Lambin X, Telford GR, Ogden N, Telfer S, Woldehiwet Z, Birtles R (2008) Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Appl Environ Microbiol 74:7118–7125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canty A, Ripley B (2014) Boot: bootstrap R (S-Plus) functions. R package version 1.3-11

  • Capligina V, Berzina I, Bormane A, Salmane I, Vilks K, Kazarina A, Bandere D, Baumanis V, Ranka R (2016) Prevalence and phylogenetic analysis of Babesia spp. in Ixodes ricinus and Ixodes persulcatus ticks in Latvia. Exp Appl Acarol 68:325–336

    Article  PubMed  Google Scholar 

  • Duh D, Petrovec M, Trilar T, Avsic-Zupanc T (2003) The molecular evidence of Babesia microti infection in small mammals collected in Slovenia. Parasitology 126(Pt 2):113–117

    Article  CAS  PubMed  Google Scholar 

  • Filippova NA (1977) Ixodid ticks of the subfamily Ixodinae. Fauna of the USSR. Arachnida. Vol. 4 (4). Publishing House Nauka, Leningrad, 396 pp. (in Russian)

  • Gray J, von Stedingk LV, Gürtelschmid M, Granström M (2002) Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. J Clin Microbiol 40:1259–1263

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray J, Zintl A, Hildebrandt A, Hunfeld K, Weiss L (2010) Zoonotic babesiosis: overview of the disease and novel aspects of pathogen identity. Ticks Tick Borne Dis 1:3–10

    Article  PubMed  Google Scholar 

  • Kallio ER, Begon M, Birtles RJ, Bown KJ, Koskela E, Mappes T, Watts PC (2014) First report of Anaplasma phagocytophilum and Babesia microti in rodents in Finland. Vector Borne Zoonotic Dis 14:389–933

    Article  PubMed  PubMed Central  Google Scholar 

  • Katargina O, Geller J, Vasilenko V, Kuznetsova T, Järvekülg L, Vene S, Lundkvist Å, Golovljova I (2011) Detection and characterization of Babesia species in Ixodes ticks in Estonia. Vector Borne Zoonotic Dis 11:923–928

    Article  PubMed  Google Scholar 

  • Korenberg EI, Lebedeva NN (1969) Distribution and some general features of the ecology of Ixodes trianguliceps Bir. in the Soviet Union. Folia Parasitol 16:143–152

    Google Scholar 

  • Nakajima R, Tsuji M, Oda K, Zamoto-Niikura A, Wei Q, Kawabuchi-Kurata T, Nishida A, Ishihara C (2009) Babesia microti-group parasites compared phylogenetically by complete sequencing of the CCTeta gene in 36 isolates. J Vet Med Sci 71:55–68

    Article  CAS  PubMed  Google Scholar 

  • Nefedova VV, Korenberg EI, Kovalevsky YV, Samokhvalov MV, Gorelova NB (2012) The role of Ixodes trianguliceps tick larvae in circulation of Babesia microti in the Middle Urals. Zool J 9(91):1034–1042 (in Russian)

    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

    Article  PubMed  Google Scholar 

  • Pieniazek N, Sawczuk M, Skotarczak B (2006) Molecular identification of Babesia parasites isolated from Ixodes ricinus ticks collected in northwestern Poland. J Parasitol 92:32–35

    Article  CAS  PubMed  Google Scholar 

  • Randolph SE (1995) Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys glareolus). Parasitology 110:287–295

    Article  PubMed  Google Scholar 

  • Rar VA, Epikhina TI, Livanova NN, Panov VV, Pukhovskaia NM, Vysochina NP, Ivanov LI (2010) Detection of Babesia spp. DNA in small mammals and ixodic ticks on the territory of North Ural, West Siberia and Far East of Russia. Mol Gen Mikrobiol Virusol 3:26–30 (in Russian)

    PubMed  Google Scholar 

  • Rar VA, Epikhina TI, Livanova NN, Panov VV (2011) Genetic diversity of Babesia in Ixodes persulcatus and small mammals from North Ural and West Siberia, Russia. Parasitology 138:175–182

    Article  CAS  PubMed  Google Scholar 

  • Rar VA, Epikhina TI, Suntsova OV, Kozlova IV, Lisak OV, Pukhovskaya NM, Vysochina NP, Ivanov LI, Tikunova NV (2014a) Genetic variability of Babesia parasites in Haemaphysalis spp. and Ixodes persulcatus ticks in the Baikal region and Far East of Russia. Infect Genet Evol 28:270–275

    Article  CAS  PubMed  Google Scholar 

  • Rar VA, Epikhina TI, Tikunova NV, Bondarenko EI, Ivanov MK, Iakimenko VV, Mal’kova MG, Tantsev AK (2014b) DNA detection of pathogens transmitted by Ixodid ticks in blood of small mammals inhabiting the forest biotopes in Middle Irtysh Area (Omsk Region, West Siberia). Parazitologiia 48:37–53 (in Russian)

    CAS  PubMed  Google Scholar 

  • Rar VA, Fedulina OO, Suntsova OV, Tikunov AJu, Panov VV, Lisak OV, Kozlova IV, Tikunova NV (2016) Detection of Babesia and Anaplasmataceae bacteria in small mammals from Irkutsk and Novosibirsk regions. Byulleten VSNC SO RAMN 3, in press (in Russian)

  • Sasaki M, Fujii Y, Iwamoto M, Ikadai H (2013) Effect of sex steroids on Babesia microti infection in mice. Am J Trop Med Hyg 88:367–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scherer R (2014) PropCIs: various confidence interval methods for proportions. R package version. 0.2-5. http://CRAN.R-project.org/package=PropCIs. Accessed 16 April 2014

  • 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 

  • Siński E, Bajer A, Welc R, Pawełczyk A, Ogrzewalska M, Behnke JM (2006) Babesia microti: prevalence in wild rodents and Ixodes ricinus ticks from the Mazury Lakes District of North-Eastern Poland. Int J Med Microbiol 296(Suppl 40):137–143

    PubMed  Google Scholar 

  • Telford SR 3rd, Korenberg EI, Goethert HK, Kovalevskii UV, Gorelova NB, Spielman A (2002) Detection of natural foci of babesiosis and granulocytic ehrlichiosis in Russia. Zh Mikrobiol Epidemiol Immunobiol 6:21–25 (in Russian)

    PubMed  Google Scholar 

  • Tsuji M, Wei Q, Zamoto A, Morita C, Arai S, Shiota T, Fujimagari M, Itagaki A, Fujita H, Ishihara C (2001) Human babesiosis in Japan: epizootiologic survey of rodent reservoir and isolation of new type of Babesia microti-like parasite. J Clin Microbiol 39:4316–4322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vannier E, Borggraefe I, Telford SR 3rd, Menon S, Brauns T, Spielman A, Gelfand JA, Wortis HH (2004) Age-associated decline in resistance to Babesia microti is genetically determined. J Infect Dis 189:1721–1728

    Article  PubMed  Google Scholar 

  • Welc-Faleciak R, Bajer A, Bednarska M, Paziewska A, Siński E (2007) Long term monitoring of Babesia microti infection in BALB/c mice using nested PCR. Ann Agric Environ Med 14:287–290

    CAS  PubMed  Google Scholar 

  • Welc-Falęciak R, Bajer A, Paziewska-Harris A, Baumann-Popczyk A, Siński E (2012) Diversity of Babesia in Ixodes ricinus ticks in Poland. Adv Med Sci 57:364–369

    Article  PubMed  Google Scholar 

  • Yabsley MJ, Shock BC (2013) Natural history of Zoonotic Babesia: role of wildlife reservoirs. Int J Parasitol Parasites Wildl 2:18–31

    Article  PubMed  Google Scholar 

  • Zamoto A, Tsuji M, Wei Q, Cho SH, Shin EH, Kim TS, Leonova GN, Hagiwara K, Asakawa M, Kariwa H, Takashima I, Ishihara C (2004) Epizootiologic survey for Babesia microti among small wild mammals in northeastern Eurasia and a geographic diversity in the beta-tubulin gene sequences. J Vet Med Sci 66:785–792

    Article  CAS  PubMed  Google Scholar 

  • Zamoto-Niikura A, Tsuji M, Qiang W, Nakao M, Hirata H, Ishihara C (2012) Detection of two zoonotic Babesia microti lineages, the Hobetsu and U.S. lineages, in two sympatric tick species, Ixodes ovatus and Ixodes persulcatus, respectively, in Japan. Appl Environ Microbiol 78:3424–3430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Russian Foundation for Basic Research (project no. 14-04-00567a) and the Russian Ministry of Education and Science (project VI.55.1.1).

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Correspondence to Vera Rar.

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Rar, V., Yakimenko, V., Makenov, M. et al. High prevalence of Babesia microti ‘Munich’ type in small mammals from an Ixodes persulcatus/Ixodes trianguliceps sympatric area in the Omsk region, Russia. Parasitol Res 115, 3619–3629 (2016). https://doi.org/10.1007/s00436-016-5128-9

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