Diversity and Pathways of Baltic Group Tick-Borne Encephalitis Virus

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Tick-borne encephalitis virus (TBEV) is the causative agent of a serious disease that involves the central nervous system. Recently, we have sequenced the TBEV genome fragments isolated from Ixodes ticks, collected in Karelia in 2008–2018. In one village, the genetic diversity of viruses of the Baltic TBEV group turned out to be comparable to their diversity over a vast territory from Finland in the west to Chelyabinsk Oblast in the east. Moreover, the diversity of viruses is equitable in every region. In other words, active virus mixing took place and, possibly, still occurs over a vast territory. The most plausible explanation is the involvement of flying animals (birds) in the TBEV distribution.

About the authors

A. A Deviatkin

Sechenov First Moscow State Medical University, Ministry of Health of the Russian Federation; Lomonosov Moscow State University

Email: andreideviatkin@gmail.com
Moscow, Russia; Moscow, Russia

S. V Bugmyrin

Institute of Biology of the Karelian Research Centre, RAS

Email: sbugmyr@mail.ru
Petrozavodsk, Russia

Y. A Vakulenko

Sechenov First Moscow State Medical University, Ministry of Health of the Russian Federation; Lomonosov Moscow State University

Email: vjulia94@gmail.com
Moscow, Russia; Moscow, Russia

A. N Lukashev

Sechenov First Moscow State Medical University, Ministry of Health of the Russian Federation

Email: alexander_lukashev@hotmail.com
Moscow, Russia

G. G Karganova

Sechenov First Moscow State Medical University, Ministry of Health of the Russian Federation; Lomonosov Moscow State University; Chumakov Federal Scientific Center for Research and Development of Immune-and-Biological Products, RAS

Email: arganova@bk.ru
Moscow, Russia; Moscow, Russia; Moscow, Russia

References

  1. Ruzek D., Zupanc T.A., Borde J. et. al. Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. Antiviral Research. 2019; 164: 23–51. doi: 10.1016/j.antiviral.2019.01.014.
  2. Beauté J., Spiteri G., Warns-Petit E. et. al. Tick-borne encephalitis in Europe, 2012 to 2016. Euro Surveill. 2018; 23(45): pii=1800201. doi: 10.2807/1560-7917.ES.2018.23.45.1800201.
  3. Kriz B., Hubalek Z., Marek M. et al. Results of the screening of tick-borne encephalitis virus antibodies in human sera from eight districts collected two decades apart. Vector-Borne and Zoonotic Diseases. 2015; 15(8): 489–493. doi: 10.1089/vbz.2014.1747.
  4. Stjernberg L., Holmkvist K., Berglund J. A newly detected tick-borne encephalitis (TBE) focus in south-east Sweden: A follow-up study of TBE virus (TBEV) seroprevalence. Scandinavian Journal of Infectious Diseases. 2008; 40: 4–10. doi: 10.1080/00365540701522934.
  5. Maikova G.B., Chernokhaeva L.L., Rogova Yu.V. et al. Ability of inactivated vaccines based on far-eastern tick-borne encephalitis virus strains to induce humoral immune response in originally seropositive and seronegative recipients. J. Med. Virol. 2019; 91: 190–200. doi: 10.1002/jmv.25316.
  6. Makenov M., Karan L., Shashina N. et. al. First detection of tick-borne encephalitis virus in Ixodes ricinus ticks and their rodent hosts in Moscow, Russia. Ticks Tick Borne Dis. 2019; 10(6): 101265. doi: 10.1016/j.ttbdis.2019.101265.
  7. Holding M., Dowall S.D., Medlock J.M. et. al. Tick-borne encephalitis virus, United Kingdom. Emerg. Infect. Dis. 2020; 26(1): 90–96. doi: 10.3201/eid2601.191085.
  8. Agergaard Ch.N, Rosenstierne M.W., Bødker R. et. al. New tick-borne encephalitis virus hot spot in Northern Zealand, Denmark, October 2019. Euro Surveill. 2019; 24(43): pii=1900639. doi: 10.2807/1560-7917.ES.2019.24.43.1900639.
  9. Tkachev S.E., Babkin I.V., Chicherina G.S. et. al. Genetic diversity and geographical distribution of the Siberian subtype of the tick-borne encephalitis virus. Ticks Tick Borne Dis. 2020; 11(2): 101327. doi: 10.1016/j.ttbdis.2019.101327.
  10. Dekker M., Laverman G.D., de Vries A. et al. Emergence of tick-borne encephalitis (TBE) in the Netherlands. Ticks Tick Borne Dis. 2019; 10(1): 176–179. doi: 10.1016/j.ttbdis.2018.10.008.
  11. Heinz F.X., Stiasny K., Holzmann H. et. al. Emergence of tick-borne encephalitis in new endemic areas in Austria: 42 years of surveillance. Euro Surveill. 2015; 20(13): pii=21077. doi: 10.2807/1560-7917.ES2015.20.13.21077.
  12. Ponomareva E.P., Mikryukova T.P., Gori A.V. et al. Detection of Far-Eastern subtype of tick-borne encephalitis viral RNA in ticks collected in the Republic of Moldova. J. Vector Borne Dis. 2015; 52(4): 334–336.
  13. Deviatkin A.A., Kholodilov I.S., Belova O.A. et. al. Baltic group tick-borne encephalitis virus phylogeography: systemic inconsistency pattern between genetic and geographic distances. Microorganisms. 2020; 8(10): 1589. doi: 10.3390/microorganisms8101589.
  14. Ecker M., Allison S.L., Meixner T. et al. Sequence analysis and genetic classification of tick-borne encephalitis viruses from Europe and Asia. J. Gen. Virol. 1999; 80(1): 179–185. doi: 10.1099/0022-1317-80-1-179.
  15. Deviatkin A.A., Kholodilov I.S., Vakulenko Yu.A. et al. Tick-Borne Encephalitis Virus: An Emerging Ancient Zoonosis? Viruses. 2020; 12(2): 247. doi: 10.3390/v12020247.
  16. Yoshii K., Song J.Y., Park S.B. et al. Tick-borne encephalitis in Japan, Republic of Korea and China. Emerg. Microbes Infect. 2017; 6(9): e82. doi: 10.1038/emi.2017.69.
  17. Jaaskelainen A.E., Sironen T., Murueva G.B. et. al. Tick-borne encephalitis virus in ticks in Finland, Russian Karelia and Buryatia. J. Gen. Virol. 2010; 91(11): 2706–2712. doi: 10.1099/vir.0.023663-0.
  18. Golovljova I., Vene S., Sjцlander K.B. et. al. Characterization of tick-borne encephalitis virus from Estonia. J. Med. Virol. 2004; 74(4): 580–588. doi: 10.1002/jmv.20224.
  19. Tkachev S.E., Babkin I.V., Chicherina G.S. et. al. Genetic diversity and geographical distribution of the Siberian subtype of the tick-borne encephalitis virus. Ticks Tick Borne Dis. 2020; 11(2): 101327. doi: 10.1016/j.ttbdis.2019.101327.
  20. Muto M., Bazartseren B., Tsevel B. et. al. Isolation and characterization of tick-borne encephalitis virus from Ixodes persulfates in Mongolia in 2012. Ticks Tick Borne Dis. 2015; 6(5): 623–629. doi: 10.1016/j.ttbdis.2015.05.006.
  21. Briggs B.J., Atkinson B., Czechowski D.M. et. al. Tick-borne encephalitis virus, Kyrgyzstan. Emerg. Infect. Dis. 2011; (5): 876–879. doi: 10.3201/eid1705.101183.
  22. Пуховская Н.М., Морозова О.В., Белозерова Н.Б. и др. Сравнительный анализ геномов штаммов вируса клещевого энцефалита, выделенных от комаров и клещей. Вопросы вирусологии. 2017; 62(1): 30–35. doi: 10.18821/0507-4088-2017-62-1-30-35.
  23. Jaaskelainen A., Tikkakoski T., Uzcategui N. et. al. Siberian subtype tick-borne encephalitis virus, Finland. Emerg. Infect. Dis. 2006; 12(10): 1568–1571. doi: 10.3201/eid1210.060320.
  24. Golovljova I., Katargina O., Geller J. et. al. Unique signature amino acid substitution in Baltic tick-borne encephalitis virus (TBEV) strains within the Siberian TBEV subtype. Int. J. Med. Microbiol. 2008; 298: 108–120. doi: 10.1016/j.ijmm.2007.12.004.
  25. Lundkvist A., Vene S., Golovljova I. et. al. Characterization of tick-borne encephalitis virus from latvia: Evidence for co-circulation of three distinct subtypes. J. Med. Virol. 2001; 65(4): 730–735. doi: 10.1002/jmv.2097.
  26. Khasnatinov M.A., Ustanikova K., Frolova T.V. et. al. Non-Hemagglutinating Flaviviruses: Molecular Mechanisms for the Emergence of New Strains via Adaptation to European Ticks. PLoS ONE. 2009; 4: e7295. doi: 10.1371/journal.pone.0007295.
  27. Kovalev S.Yu., Chernykh D.N., Kokorev V.S. et al. Origin and distribution of tick-borne encephalitis virus strains of the Siberian subtype in the Middle Urals, the north-west of Russia and the Baltic countries. J. Gen. Virol. 2009; 90(12): 2884–2892. doi: 10.1099/vir.0.012419-0.
  28. Погодина В.В., Карань Л.С., Колясникова Н.М. и др. Эволюция клещевого энцефалита и проблема эволюции возбудителя. Вопросы вирусологии. 2007; 52(5): 16–21.
  29. Labuda M., Nuttall P.A. Tick-borne viruses. Parasitology. 2004; 129(51): S221–S245. doi: 10.1017/S0031182004005220.
  30. Kovalenko A.I., Rubis L.V., Ekimova O.V. et al. Natural foci infections in Republic of Karelia. EpiNorth. 2003; 4: 3–4.
  31. Bugmyrin S.V., Bespyatova L.A., Korotkov Yu.S. Long-term dynamics of Ixodes persulcatus (Acari: Ixodidae) abundance in the north–west of its range (Karelia, Russia). Exp Appl Acarol. 2019; 77: 229–240. doi: 10.1007/s10493-019-00342-y.
  32. Bugmyrin S.V., Bespyatova L.A., Korotkov Yu.S. et. al. Distribution of Ixodes ricinus and I.persulcatus ticks in southern Karelia (Russia). Ticks Tick Borne Dis. 2013; 4, 57-62. doi: 10.1016/j.ttbdis.2012.07.004.
  33. Laaksonen M., Sajanti E., Sormunen J.J. et. al. Crowdsourcing-based nationwide tick collection reveals the distribution of Ixodes ricinus and I.persulcatus and associated pathogens in Finland. Emerg. Microbes Infect. 2017; 6(1): 1–7. doi: 10.1038/emi.2017.17.
  34. Sormunen J.J., Andersson T., Aspi J. et. al. Monitoring of ticks and tick-borne pathogens through a nationwide research station network in Finland. Ticks Tick Borne Dis. 2020; 11(5): 101449. doi: 10.1016/j.ttbdis.2020.101449.
  35. Jaenson T.G.T., Värv K., Fröjdman I. et. al. First evidence of established populations of the taiga tick Ixodes persulcatus (Acari: Ixodidae) in Sweden. Parasites Vectors. 2016; 9: 377. doi: 10.1186/s13071-016-1658-3.
  36. Tkachev S.E., Chicherina G.S., Golovljova I. et. al. New genetic lineage within the Siberian subtype of tick-borne encephalitis virus found in Western Siberia, Russia. Infection, Genetics and Evolution. 2017; 56: 36–43. doi: 10.1016/j.meegid.2017.10.020.
  37. Бессолицына Е.А., Волков С.А., Столбова Ф.С. Динамика зараженности бактериями рода Borrelia и вирусом клещевого энцефалита клещей, собранных в Кировской области. Инфекция и иммунитет. 2017; 7(2):171–180. doi: 10.15789/2220-7619-2017-2-171-180.
  38. Margos G., Fingerle V., Reynolds S. Borrelia bavariensis: vector switch, niche invasion, and geographical spread of a tick-borne bacterial parasite. Front. Ecol. Evol. 2019; 7: 401. doi: 10.3389/fevo.2019.00401.
  39. Lv J., Fernбndez de Marco M.d.M., Goharriz H. et. al. Detection of tick-borne bacteria and babesia with zoonotic potential in Argas (Carios) vespertilionis (Latreille, 1802) ticks from British bats. Sci. Rep. 2018; 8. doi: 10.1038/s41598-018-20138-1.
  40. Sándor A.D., Corduneanu A., Péter Á. et. al. Bats and ticks: host selection and seasonality of bat-specialist ticks in eastern Europe. Parasites Vectors. 2019; 12. doi: 10.1186/s13071-019-3861-5.
  41. Jaunbauere G., Salmane I., Spungis V. Occurrence of bat ectoparasites in Latvia. Latv. Entomol. 2008; 45: 38–42.
  42. Klaus Ch., Gethmann J., Hoffmann B. et. al. Tick infestation in birds and prevalence of pathogens in ticks collected from different places in Germany. Parasitol Res. 2016; 115: 2729–2740. doi: 10.1007/s00436-016-5022-5.
  43. Lommano E., Dvorák Ch., Vallotton L. et. al. Tick-borne pathogens in ticks collected from breeding and migratory birds in Switzerland. Ticks Tick Borne Dis. 2014; 5(6): 871–882. doi: 10.1016/j.ttbdis.2014.07.001.
  44. Mikryukova T.P., Moskvitina N.S., Kononova Y.V. et. al. Surveillance of tick-borne encephalitis virus in wild birds and ticks in Tomsk city and its suburbs (Western Siberia). Ticks Tick Borne Dis. 2014; 5(2): 145–151. doi: 10.1016/j.ttbdis.2013.10.004.
  45. Hasle G. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front. Cell. Infect. Microbiol. 2013; 3. doi: 10.3389/fcimb.2013.00048.
  46. Michelitsch A., Wernike K., Klaus C. et. al. Exploring the reservoir hosts of tick-borne encephalitis virus. Viruses. 2019; 11(7): 669. doi: 10.3390/v11070669.
  47. Waldenstrцm J., Lundkvist A., Falk K.I. et. al. Migrating birds and tickborne encephalitis virus. Emerg. Infect. Dis. 2007; 13(8): 1215–1218. doi: 10.3201/eid1308.061416.
  48. Fleming T.H. Bat Migration. Encyclopedia of Animal Behavior. Coral Gables (USA), 2019; 605–610. doi: 10.1016/B978-0-12-809633-8.20764-4.
  49. Russell A.L., Pinzari C.A., Vonhof M.J. et. al. Two tickets to paradise: multiple dispersal events in the founding of hoary bat populations in Hawaii. PLoS ONE. 2015; 10(6): e0127912; doi: 10.1371/journal.pone.0127912.
  50. Roberts B.J., Catterall C.P., Eby P. et. al. Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PLoS ONE. 2012; 7(8): e42532; doi: 10.1371/journal.pone.0042532.
  51. Cryan P.M. Seasonal distribution of migratory tree bats (Lasiurus and Lasionycteris) in North America. Journal of Mammalogy. 2003; 84(2): 579–593. doi: 10.1644/1545-1542(2003)084<0579:SDOMTB>2.0.CO;2.
  52. Havlik O., Kolman J. The demonstration of antibodies against the virus of the tick-borne encephalitis in certain bats. J. Hyg. Epidemiol. Microbiol. Immunol. 1957; 1(2): 231–233.
  53. Дробищенко Н.И., Львов Д.К., Укбаева Т.Д. и др. Экспериментальное подтверждение персистенции вируса клещевого энцефалита у летучих мышей в зимний период. Медицинская паразитология. 1978; 47: 81–82.
  54. Nosek J., Gresikova M., Rehacek J. Persistence of tick-borne encephalitis virus in hibernating bats. Acta Virol. 1961; 5: 112–116.
  55. Fagre A.C., Kading R.C. Can bats serve as reservoirs for arboviruses? Viruses. 2019; 11(3): 215. doi: 10.3390/v11030215.
  56. Geller J., Nazarova L., Katargina O. et. al. Tick-borne pathogens in ticks feeding on migratory passerines in Western Part of Estonia. Vector-Borne and Zoonotic Diseases. 2013; 13(7): 443–448. doi: 10.1089/vbz.2012.1054.
  57. Kazarina A., Japiтa K., Keišs O. et. al. Detection of tick-borne encephalitis virus in I.ricinus ticks collected from autumn migratory birds in Latvia. Ticks Tick Borne Dis. 2015; 6(2): 178–180. doi: 10.1016/j.ttbdis.2014.11.011.
  58. Csank T., Korytár ј., Pošiváková T. et al. Surveillance on antibodies against West Nile virus, Usutu virus, tick-borne encephalitis virus and Tribec virus in wild birds in Drienovská wetland, Slovakia. Biologia. 2019; 74: 813–820. doi: 10.2478/s11756-019.
  59. Alcaide M., Scordato E.S.C., Price T.D. et al. Genomic divergence in a ring species complex. Nature. 2014; 511: 83–85. doi: 10.1038/nature13285.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Издательство «Наука»

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies