Infection of ixodes ticks and wild small mammals with pathogens of natural focal infections in the territory of the Kurortny district of St. Petersburg

The purpose of this study was to identify the genetic markers of Borrelia burgdorferi sensu lato, Rickettsia spp. SFG, Anaplasma phagocytophilum, Ehrlichia caffeensis/E. muris, Coxiella burnetii, and tick-borne encephalitis virus (TBE) in ixodes ticks and organs of wild small mammals collected and captured in 2020-2023 in the Kurortny district of St. Petersburg.
Materials and methods. Samples of ixodes ticks and organs of wild small mammals were examined by real-time PCR for the presence of genetic material of the causative agents of tick-borne infections. Ixodes ticks were collected and wild small mammals were captured in the Kurortny district of St.Petersburg in the period 2020-2023. The study was conducted using commercial test systems.
Results. The overall infection rates of ixodes ticks and wild small mammals in relation to B. burgdorferi s.l. were 23.7% and 5.2%, respectively; Rickettsia spp. SFG – 11.5% and 0.9%; E. chaffensis/ E. muris – 4.0% and 0.0%; A. phagocytophilum – 1.6% and 0.6%; C. burnetii – 3.3% and 5.2%; tick–borne encephalitis virus – 0.2% and 0.0%. The total infection rate of ticks with two or more pathogens was 6.6%, the most common combinations of mixed infections were: B. burgdorferi s.l. + Rickettsia spp. SFG, B. burgdorferi s.l. + C. burnetii and B. burgdorferi s.l. + E. chaffensis/ E. muris.
Conclusion. The results obtained indicate the existence of active natural foci of tick-borne infections in the Kurortny district of St. Petersburg and substantiate the expediency of continuous entomological and zoological monitoring and improvement of preventive measures against tick-borne infections.

1. Provorova V.V., Krasnova E.I., Khokhlova N.I., Savel’eva M.A., Filimonova E.S., Kuznetsova V.G. Tissue infections in Russia // Infektsionnye bolezni: novosti, mneniya, obuchenie, 2019, vol. 8, no. 2, pp. 102-112. DOI: 10.24411/2305-3496-2019-12013

2. O’Neill X., White A., Gortüzar C., Ruiz-Fons F. The Impact of Host Abundance on the Epidemiology of Tick-Borne Infection. Bulletin of Mathematical Biology, 2023, vol. 85, no.4, pp. 30. DOI: 10.1007/s11538-023-01133-8.

3. Nuttall P. A. Climate change impacts on ticks and tickborne infections. Biologia, 2022, vol. 77, no.6, pp.1503-1512. DOI: 10.1146/annurev-ento-052720-094533.

4. Hofmeester T.R., Jansen P.A., Wijnen H.J., Coipan E.C., Fonville M., Prins H.H.T., Sprong H., van Wieren S.E. Cascading effects of predator activity on tick-borne disease risk. Proceedings of the Royal Society B: Biological Sciences, 2017, vol. 284, no.1859, pp.20170453. DOI: 10.1098/rspb.2017.0453.

5. Sprong H., Matthysen E. Recreational hazard: Vegetation and host habitat use correlate with changes in tick- borne disease hazard at infrastructure within forest stands. Science of The Total Environment, 2024, vol. 919. DOI: 10.1016/j.scitotenv.2024.170749.

6. Wang Y.X.G., Matson K.D., Prins H.H.T., Xu Y., Huang Z.Y.X., de Boer W.F. Risk factors for Lyme disease: A scale-dependent effect of host species diversity and a consistent negative effect of host phylogenetic diversity. Ticks and Tick-borne Diseases, 2023, vol. 14, no. 1. DOI: 10.1016/j.ttbdis.2022.102073.

7. Krawczyk A.I., van Duijvendijk G.L., Swart A., Heylen D., Jaarsma R.I., Jacobs F.H., Fonville M., Sprong H., Takken W. Effect of rodent density on tick and tick-borne pathogen populations: consequences for infectious disease risk. Parasites & vectors, 2020, vol.13, no. 1, pp.34. DOI: 10.1186/s13071-020-3902-0.

8. Kim K., Hwang J., Kim K., Yoon K., Oh D., Park Y. Habitat Type-Based Assemblage and Distribution Prediction of Small Mammals and Chigger Mites (Acari: Trombiculidae) in Chuncheon City, Republic of Korea. Animals (Basel), 2024, vol.14, no.23. DOI: 10.3390/ani14233433.

9. Siuziumova E.A., Telnova N.V., Shapar A.O., Aslanov B.I., Stoyanova N.A., Tokarevich N.K. Ecological and epidemiological characteristics of tick-borne encephalitis in St. Petersburg // Russian Journal of Infection and Immunity, 2020, vol. 10, no. 3, pp. 533–542. DOI: 10.15789/10.15789/2220-7619-EAE-924

10. Panferova Yu.A., Vaganova A.N., Freylikhman O.A., Tretyakov K.A., Medvedev S.G., Shapar’ A.O., Tokarevich N.K. Prevalence of Borrelia burgdorferi sensu lato genetic markers in blood-sucking ticks in suburban park zones in Saint Petersburg // Russian Journal of Infection and Immunity, 2020, vol. 10, no. 1, pp. 175-179. DOI: 10.15789/2220-7619-P0B-806

11. Pirozhkova A. S., Vedenina E. Y. Statistical analysis of the data on the treatment of patients affected by tick bite in St. Petersburg in the period from 2015 to 2019// Materials of the AllRussian scientific forum of students with international participation “Student Science 2020”,2020, vol. 3, no. S, pp. 299-300.

12. Eremeeva M.E., Oliveira A., Moriarity J., Robinson J.B., Tokarevich N.K., Antyukova L.P., Pyanyh V.A., Emeljanova O.N., Ignatjeva V.N., Buzinov R., Pyankova V., Dasch G.A. Detection and identification of bacterial agents in Ixodes persulcatus Schulze ticks from the north western region of Russia. Vector-borne and zoonotic diseases, 2007, vol.7, no. 3, pp. 426-436. DOI: 10.1089/vbz.2007.0112

13. Filippova N.A. Ixodid Ticks Subfamily Ixodinae. Arachnida. IV. Fauna of the USSR.4 ed. Leningrad: Nauka Press Publ.; 1977.

14. Grigorieva L. A., Miteva O. A., Samoilova E. P. The parasitic system of Ixodes persulcatus (Ixodinae) — Borrelia garinii — small mammals in northwestern Russia // Proceedings of the Zoological Institute of the Russian Academy of Sciences, 2024, vol. 328, no. 2, pp. 308-322. DOI: 10.31610/trudyzin/2024.328.2.308

15. Steinbrink A., Brugger K., Margos G., Kraiczy P., Klimpel S. The evolving story of Borrelia burgdorferi sensu lato transmission in Europe. Parasitology Research, 2022, vol.121, no. 3, pp. 781-803. DOI: 10.1007/s00436-022-07445-3.

16. Prislegina D.A., Dubyanskiy V.M., Platonov A.E., Maletskaya O.V. Effect of the natural and climatic factors on epidemiological situation related to natural focal infections // Russian Journal of Infection and Immunity = Infektsiya i immunitet, 2021, vol. 11, no. 5, pp. 820–836. DOI: 10.15789/2220-7619-EOT-1631

17. Krawczyk A.I., Röttjers S., Coimbra-Dores M.J., Heylen D., Fonville M., Takken W., Faust K., Sprong H. Tick microbial associations at the crossroad of horizontal and vertical transmission pathways. Parasit Vectors, 2022, vol.15, no. 1, pp. 380. DOI: 10.1186/s13071-022-05519-w.

18. Freilikhman O. A., Panferova Yu. A., Saines T. V., Shapar A. O., Tokarevich N. K. Infection of ticks with pathogens of infectious tick-borne borreliosis and ku fever in St. Petersburg // Russian Journal of Infection and Immunity, 2016, vol. 6, no. 3, pp. 118.

19. Sharova A. A., Tokarevich N. K., Baimova R. R., Freylikhman O. A., Karmokov I. A., Riabiko E. G., Lunina G. A., Buzinov R. V., Sokolova O. V., Buts L. V., Bespyatova L. A., Bubnova L. A., Safonova O. S., Kalinina E. L., Stankevich A. I., Vikse R., Andreassen A. K., Gladkikh A. S., Forghani M., Gritseva A. S., Popova M. R., Ramsay E. S., Dedkov V.G. Prevalence and genetic diversity of tick-borne encephalitis virus in ixodid ticks from specific regions of northwestern Russia. PLoS One, 2025, vol. 20, no. 1. DOI: 10.1371/journal.pone.0314385.

20. Kaufman W. R. Gluttony and sex in female ixodid ticks: how do they compare to other blood-sucking arthropods? Journal of insect physiology, 2007, vol. 53, no. 3, pp. 264-273. DOI: 10.1016/j.jinsphys.2006.10.004.

21. Nasirian H., Zahirnia A. Detailed Infestation Spectrums About Biological Stages of Hard Ticks (Acari: Ixodida: Ixodidae) in Humans: A Systematic Review and Meta-Analysis. Acta Parasitologica, 2021, vol. 66, no. 3, pp. 770-796. DOI: 10.1007/s11686-021-00362-y.

22. Pakanen V.M., Sormunen J.J., Sippola E., Blomqvist D., Kallio E.R. Questing abundance of adult taiga ticks Ixodes persulcatus and their Borrelia prevalence at the north- western part of their distribution. Parasites & Vectors, 2020, vol. 13, no. 1, pp. 384. DOI: 10.1186/s13071-020-04259-z.

23. Korenberg E.I., Sirotkin M.B., Kovalevskii Yu.V. A general scheme of the circulation of ixodid tick-borne borrelioses pathogens in natural foci of Eurasia // Zoologicheskiy zhurnal, 2016, vol. 95, no. 3, pp.283-299. DOI:10.7868/S0044513416030090

24. Shkarin V.V., Blagonravova A.S., Chumakov E.M. Epidemiological Features of Combined Natural-Focal Infections // Epidemiology and Vaccinal Prevention, 2017, vol. 16, no. 5, pp. 43-52. DOI: 10.31631/2073-3046-2017-16-5-43-52

25. Freilichman O.A., Panferova Yu.A., Tokarevich H.K. Test results of new primers for the detection of Coxiella burnetii in wild small mammals// 5th International conference “Pasteur’s ideas in the fight against infections”, 2008, pp. 104

26. Rudakova S. A. Reservoir role of small mammals in combined natural foci of bacterial infections in Western Siberia // Zoological Journal, 2010, vol. 89, no. 1, pp. 88-92.