Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T08:11:55.816Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic diversity of Babesia in Ixodes persulcatus and small mammals from North Ural and West Siberia, Russia

Published online by Cambridge University Press:  27 August 2010

V. A. RAR ,
T. I. EPIKHINA ,
N. N. LIVANOVA  and
V. V. PANOV
V. A. RAR*
Affiliation:
Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, pr. Lavrent'eva 8, Novosibirsk, 630090 Russian Federation
T. I. EPIKHINA
Affiliation:
Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, pr. Lavrent'eva 8, Novosibirsk, 630090 Russian Federation
N. N. LIVANOVA
Affiliation:
Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, pr. Lavrent'eva 8, Novosibirsk, 630090 Russian Federation Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, ul. Frunze 11, Novosibirsk, 630091 Russian Federation
V. V. PANOV
Affiliation:
Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, pr. Lavrent'eva 8, Novosibirsk, 630090 Russian Federation Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, ul. Frunze 11, Novosibirsk, 630091 Russian Federation
*
*Corresponding author: Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, pr. Lavrent'eva 8, Novosibirsk, 630090 Russian Federation. Tel: +7 383 3635177. Fax: +7 383 3635164. E-mail: rarv@niboch.nsc.ru
Get access Rights & Permissions [Opens in a new window]

Summary

Objective. The aim of this work was to study the prevalence and genetic diversity of Babesia in Ixodes persulcatus ticks and small mammals from Ural and Siberia in Russia. Methods. In total, 481 small mammals and 922 questing adult I. persulcatus from North Ural (Sverdlovsk region) and West Siberia (Novosibirsk region) were examined for the presence of Babesia by nested PCR based on the 18S rRNA gene. Results. Babesia microti of the ‘Munich’-type was found in 36·2% of blood samples of the small mammals from the Sverdlovsk region and B. microti of the ‘US’-type in 5·3% of the animals from the Novosibirsk region. Babesia DNA was not detected in 133 analysed I. persulcatus from the Sverdlovsk region; however, it was found in 24 of 789 ticks from the Novosibirsk region. Three distinct Babesia species were detected in I. persulcatus. B. microti ‘US’-type was identified in 10 ticks, Babesia closely related to B. divergens/B. capreoli in 2 ticks, and Babesia closely related to B. venatorum (EU1) in 12 ticks. Conclusion. To our knowledge, this is the first detection of Babesia sensu stricto in I. persulcatus ticks and of B. microti in I. persulcatus in the Asian part of Russia.

Keywords

Ixodes persulcatusBabesia spp.prevalencegenetic diversityNorth UralWest Siberia
Type
Research Article
Information
Parasitology , Volume 138 , Issue 2 , February 2011 , pp. 175 - 182
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alekseev, A. N., Semenov, A. V. and Dubinina, H. V. (2003). Evidence of Babesia microti infection in multi-infected Ixodes persulcatus ticks in Russia. Experimental and Applied Acarology 29, 345–353. doi: 10.1023/A.1025841901909.CrossRefGoogle ScholarPubMed
Armstrong, P. M., Katavolos, P., Caporale, D. A., Smith, R. P., Spielman, A. and Telford, S. R. III (1998). Diversity of Babesia infecting deer ticks (Ixodes dammini). American Journal of Tropical Medicine and Hygiene 58, 739–742.CrossRefGoogle ScholarPubMed
Becker, C. A., Bouju-Albert, A., Jouglin, M., Chauvin, A. and Malandrin, L. (2009). Natural transmission of zoonotic Babesia spp. by Ixodes ricinus ticks. Emerging Infectious Diseases 15, 320–322. doi: 10.3201/eid1502.081247.CrossRefGoogle ScholarPubMed
Bonnet, S., Brisseau, N., Hermouet, A., Jouglin, M. and Chauvin, A. (2009). Experimental in vitro transmission of Babesia sp. (EU1) by Ixodes ricinus.Veterinary Research 40, 21. doi: 10.1051/vetres/2009004.CrossRefGoogle ScholarPubMed
Boom, R., Sol, C. J., Salimans, M. M., Jansen, C. L., Wertheim-van Dillen, P. M. and van der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology 28, 495–503.CrossRefGoogle ScholarPubMed
Bown, K. J., Lambin, X., Telford, G. R., Ogden, N. H., Telfer, S., Woldehiwet, Z. and Birtles, R. J. (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. doi: 10.1128/AEM.00625-08.CrossRefGoogle ScholarPubMed
Criado-Fornelio, A., Martinez-Marcos, A., Buling-Saraña, A. and Barba-Carretero, J. C. (2003). Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part I. Epizootiological aspects. Veterinary Parasitology 113, 189–201. doi:10.1016/S0304–4017(03)00078-5.CrossRefGoogle ScholarPubMed
Duh, D., Petrovec, M., Bidovec, A. and Avsic-Zupanc, T. (2005). Cervids as Babesiae hosts, Slovenia. Emerging Infectious Diseases 11, 1121–1123.CrossRefGoogle ScholarPubMed
Foppa, I. M., Krause, P. J., Spielman, A., Goethert, H., Gern, L., Brand, B. and Telford, S. R. III (2002). Entomologic and serologic evidence of zoonotic transmission of Babesia microti, eastern Switzerland. Emerging Infectious Diseases 8, 722–726.CrossRefGoogle ScholarPubMed
Goethert, H. K. and Telford, S. R. III (2003). What is Babesia microti? Parasitology 127, 301–309. doi: 10.1017/S0031182003003822.CrossRefGoogle ScholarPubMed
Gray, J., von Stedingk, L. V., Gürtelschmid, M. and Granström, M. (2002). Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. Journal of Clinical Microbiology 40, 1259–1263. doi: 10.1128/JCM.40.4.1259-1263.2002.CrossRefGoogle ScholarPubMed
Gray, J., Zintl, A., Hildebrandt, A., Hunfeld, K. P. and Weiss, L. (2010). Zoonotic babesiosis: Overview of the disease and novel aspects of pathogen identity. Ticks and Tick-borne Diseases 1, 3–10. doi: 10.1016/j.ttbdis.2009.11.003.CrossRefGoogle ScholarPubMed
Häselbarth, K., Tenter, A. M., Brade, V., Krieger, G. and Hunfeld, K. P. (2007). First case of human babesiosis in Germany – Clinical presentation and molecular characterisation of the pathogen. International Journal of Medical Microbiology 297, 197–204. doi: 10.1016/j.ijmm.2007.01.002.CrossRefGoogle ScholarPubMed
Herwaldt, B. L., Cacciò, S., Gherlinzoni, F., Aspöck, H., Slemenda, S. B., Piccaluga, P., Martinelli, G., Edelhofer, R., Hollenstein, U., Poletti, G., Pampiglione, S., Löschenberger, K., Tura, S. and Pieniazek, N. J. (2003). Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerging Infectious Diseases 9, 942–948.CrossRefGoogle ScholarPubMed
Herwaldt, B. L., de Bruyn, G., Pieniazek, N. J., Homer, M., Lofy, K. H., Slemenda, S. B., Fritsche, T. R., Persing, D. H. and Limaye, A. P. (2004). Babesia divergens-like infection, Washington State. Emerging Infectious Diseases 10, 622–629.CrossRefGoogle ScholarPubMed
Hildebrandt, A., Hunfeld, K. P., Baier, M., Krumbholz, A., Sachse, S., Lorenzen, T., Kiehntopf, M., Fricke, H. J. and Straube, E. (2007). First confirmed autochthonous case of human Babesia microti infection in Europe. European Journal of Clinical Microbiology and Infectious Diseases 6, 595–601. doi: 10.1007/s10096-007-0333-1.CrossRefGoogle Scholar
Hunfeld, K. P., Hildebrandt, A. and Gray, J. S. (2008). Babesiosis: recent insights into an ancient disease. International Journal for Parasitology 38, 1219–1237. doi: 10.1016/j.ijpara.2008.03.001.CrossRefGoogle ScholarPubMed
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163. doi: 10.1093/bib/5.2.150.CrossRefGoogle ScholarPubMed
Livanova, N. N. and Livanov, S. G. (2010). Zoological presupposition of human tick-borne infections in the Northern Urals. Zoological Journal 89, 1–8 (in Russian).Google Scholar
Malandrin, L., Jouglin, M., Sun, Y., Brisseau, N. and Chauvin, A. (2010). Redescription of Babesia capreoli (Enigk and Friedhoff, 1962) from roe deer (Capreolus capreolus): isolation, cultivation, host specificity, molecular characterisation and differentiation from Babesia divergens. International Journal for Parasitology 40, 277–284.CrossRefGoogle ScholarPubMed
Morozov, A. V., Kovalevsky, U. V., Korenberg, E. I., Gorelova, N. V. and Podlesniy, L. A. (2006). Preliminary results of Babesia microti DNA detection in small mammals inhabiting natural foci in Middle Ural. Bulletin ESSC SB RAMS 5, 136–138 (in Russian).Google Scholar
Nakajima, R., Tsuji, M., Oda, K., Zamoto-Niikura, A., Wei, Q., Kawabuchi-Kurata, T., Nishida, A. and Ishihara, C. (2009). Babesia microti-group parasites compared phylogenetically by complete sequencing of the CCTeta gene in 36 isolates. Journal of Veterinary Medical Science 71, 55–68. doi: 10.1292/jvms.71.55.CrossRefGoogle ScholarPubMed
Pieniazek, N., Sawczuk, M. and Skotarczak, B. (2006). Molecular identification of Babesia parasites isolated from Ixodes ricinus ticks collected in northwestern Poland. Journal of Parasitology 92, 32–35.CrossRefGoogle ScholarPubMed
Piesman, J., Karakashian, S. J., Lewengrub, S., Rudzinska, M. A. and Spielmank, A. (1986). Development of Babesia microti sporozoites in adult Ixodes dammini. International Journal for Parasitology 16, 381–385. doi: 10.1016/0020-7519(86)90118-9.CrossRefGoogle ScholarPubMed
Rabinovich, S. A., Voronina, Z. K., Stepanova, N. I., Maruashvili, G. M., Bakradze, T. L., Odisharija, M. S. and Gvasalija, N. I. (1978). The first detection of human babesiosis in USSR and the short analysis of cases described in literature. Medical Parazitology 3, 97–107 (in Russian).Google Scholar
Rar, V. A., Maksimova, T. G., Zakharenko, L. P., Bolykhina, S. A., Dobrotvorsky, A. K. and Morozova, O. V. (2005). Babesia DNA detection in canine blood and Dermacentor reticulatus ticks in southwestern Siberia, Russia. Vector-Borne and Zoonotic Diseases 5, 285–287. doi: 10.1089/vbz.2005.5.285.CrossRefGoogle ScholarPubMed
Siński, E., Bajer, A., Welc, R., Pawełczyk, A., Ogrzewalska, M. and Behnke, J. M. (2006). Babesia microti: prevalence in wild rodents and Ixodes ricinus ticks from the Mazury Lakes District of North-Eastern Poland. International Journal of Medical Microbiology 296 (Suppl. 40), 137–143. doi: 10.1016/j.ijmm.2006.01.015.CrossRefGoogle ScholarPubMed
Spencer, A. M., Goethert, H. K., Telford, S. R. III and Holman, P. J. (2006). In vitro host erythrocyte specificity and differential morphology of Babesia divergens and a zoonotic Babesia sp. from eastern cottontail rabbits (Sylvilagus floridanus). Journal of Parasitology 92, 333–340. doi: 10.1645/GE-662R.1.CrossRefGoogle Scholar
Sun, Y., Liu, G., Yang, L., Xu, R. and Cao, W. (2008). Babesia microti-like rodent parasites isolated from Ixodes persulcatus (Acari: Ixodidae) in Heilongjiang Province, China. Veterinary Parasitology 156, 333–339. doi: 10.1016/j.vetpar.2008.05.026.CrossRefGoogle ScholarPubMed
Telford, S. R. III, Korenberg, E. I., Goethert, H. K., Kovalevskii, U. V., Gorelova, N. B. and Spielman, A. (2002). Detection of natural foci of babesiosis and granulocytic ehrlichioses in Russia. Zhurnal Mikrobiologii, Epidemiologii IImmunobiologii 6, 21–25 (in Russian).Google Scholar
Tsuji, M., Wei, Q., Zamoto, A., Morita, C., Arai, S., Shiota, T., Fujimagari, M., Itagaki, A., Fujita, H. and Ishihara, C. (2001). Human babesiosis in Japan: epizootiologic survey of rodent reservoir and isolation of new type of Babesia microti-like parasite. Journal of Clinical Microbiology 39, 4316–4322. doi: 10.1128/JCM.39.12.4316-4322.2001.CrossRefGoogle ScholarPubMed
Zamoto, A., Tsuji, M., Kawabuchi, T., Wei, Q., Asakawa, M. and Ishihara, C. (2004 a). U.S.-type Babesia microti isolated from small wild mammals in Eastern Hokkaido, Japan. Journal of Veterinary Medical Science 66, 919–926. doi: 10.1292/jvms.66.919.CrossRefGoogle ScholarPubMed
Zamoto, A., Tsuji, M., Wei, Q., Cho, S. H., Shin, E. H., Kim, T. S., Leonova, G. N., Hagiwara, K., Asakawa, M., Kariwa, H., Takashima, I. and Ishihara, C. (2004 b). Epizootiologic survey for Babesia microti among small wild mammals in northeastern Eurasia and a geographic diversity in the beta-tubulin gene sequences. Journal of Veterinary Medical Science 66, 785–792. doi: 10.1292/jvms.66.785.CrossRefGoogle Scholar
Zintl, A., Mulcahy, G., Skerrett, H. E., Taylor, S. M. and Gray, J. S. (2003). Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clinical Microbiology Reviews 16, 622–636. doi: 10.1128/CMR.16.4.622-636.2003.CrossRefGoogle ScholarPubMed