Folia Parasitologica 68:024 (2021) | DOI: 10.14411/fp.2021.024

Detection of tick-borne pathogens in wild birds and their ticks in Western Siberia and high level of their mismatch

Igor G. Korobitsyn ORCID...1, Nina S. Moskvitina1, Oleg Yu. Tyutenkov1, Sergey I. Gashkov1, Yulia V. Kononova2, Sergey S. Moskvitin1, Vladimir N. Romanenko1, Tamara P. Mikryukova2, Elena V. Protopopova2, Mikhail Yu. Kartashov2, Eugene V. Chausov2, Svetlana N. Konovalova2, Natalia L. Tupota2, Alexandra O. Sementsova2, Vladimir A. Ternovoi2, Valery B. Loktev2
1 Tomsk State University, Tomsk, Russia;
2 State Research Centre of Virology and Biotechnology 'Vector', World-Class Genomic Research Center for Biological Safety and Technological Independence, Koltsovo, Novosibirsk Region, Russia

The Tomsk region located in the south of Western Siberia is one of the most high-risk areas for tick-borne diseases due to elevated incidence of tick-borne encephalitis and Lyme disease in humans. Wild birds may be considered as one of the reservoirs for tick-borne pathogens and hosts for infected ticks. A high mobility of wild birds leads to unpredictable possibilities for the dissemination of tick-borne pathogens into new geographical regions. The primary goal of this study was to evaluate the prevalence of tick-borne pathogens in wild birds and ticks that feed on them as well as to determine the role of different species of birds in maintaining the tick-borne infectious foci. We analysed the samples of 443 wild birds (60 species) and 378 ticks belonging to the genus Ixodes Latraille, 1795 collected from the wild birds, for detecting occurrence of eight tick-borne pathogens, the namely tick-borne encephalitis virus (TBEV), West Nile virus (WNV), and species of Borrelia, Rickettsia, Ehrlichia, Anaplasma, Bartonella and Babesia Starcovici, 1893, using RT-PCR/or PCR and enzyme immunoassay. One or more tick-borne infection markers were detected in 43 species of birds. All markers were detected in samples collected from fieldfare Turdus pilaris Linnaeus, Blyth's reed warbler Acrocephalus dumetorum Blyth, common redstart Phoenicurus phoenicurus (Linnaeus), and common chaffinch Fringilla coelebs Linnaeus. Although all pathogens have been identified in birds and ticks, we found that in the majority of cases (75.5 %), there were mismatches of pathogens in birds and ticks collected from them. Wild birds and their ticks may play an extremely important role in the dissemination of tick-borne pathogens into different geographical regions.

Keywords: birds, Ixodes, WNV, TBEV, Borrelia spp., Rickettsia spp., Anaplasma spp., Bartonella spp., Ehrlichia spp., Babesia spp.

Received: October 28, 2020; Revised: June 18, 2021; Accepted: July 18, 2021; Published online: November 16, 2021  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Korobitsyn, I.G., Moskvitina, N.S., Tyutenkov, O.Y., Gashkov, S.I., Kononova, Y.V., Moskvitin, S.S., ... Loktev, V.B. (2021). Detection of tick-borne pathogens in wild birds and their ticks in Western Siberia and high level of their mismatch. Folia Parasitologica68, Article 2021.024. https://doi.org/10.14411/fp.2021.024
Download citation

References

  1. Alekseev A.N., Dubinina E.V. 2007: [Tick-borne encephalitis virus in the internal environment of the tick-vector: ecological aspects]. Bull. Sib. Branch Russian Acad. ScI. 4: 100-104. (In Russian.)
  2. Alekseev A.N., Dubinina H.V., Semenov A.V., Bolshakov C.V. 2001: Evidence of ehrlichiosis agents found in ticks (Acari: Ixodidae) collected from migratory birds. J. Med. Entomol. 38: 471-474. Go to original source... Go to PubMed...
  3. Azarova I.A., Mishaeva N.P. 2002: [Consistent patterns of circulation of the West Nile virus in the tick-vertebrate parasitic system and the factors affecting the pathogen reproduction and dissemination.] In: N.N. Maksimiuk, A.K. Yuzbekov, V.G. Fedorova (Eds.), Ecology, Biodiversity and Role of Blood Sucking Insects and Ticks in the Ecosystems of Russia. Proc. II Resp. ScI. Conf. V. Novgorod, 27-29 May 2002, pp. 128-133. (In Russian.)
  4. Balança G., Gaidet N., Savini G., Vollot B., Foucart A. Reiter P., Boutonnier A., Lelli R., Monicat F. 2009: Low West Nile virus circulation in wild birds in an area of recurring outbreaks in southern France. Vector Borne Zoonotic Dis. 9: 737-741. Go to original source... Go to PubMed...
  5. Capligina V., Salmane I., Keiąs O., Vilks K., Japina K., Baumanisa V., Ranka R. 2014: Prevalence of tick-borne pathogens in ticks collected from migratory birds in Latvia. Ticks Tick Borne Dis. 5: 75-81. Go to original source... Go to PubMed...
  6. Cazorla C., Socolovschi C., Jensenius M., Parola P. 2008: Tick-borne diseases: tick-borne spotted fever rickettsioses in Africa. Infect. Dis. Clin. N. Am. 22: 531-544. Go to original source... Go to PubMed...
  7. Chausov E.V., Protopopova E.V., Konovalova S.N., Kononova Yu.V., Pershikova N. L., Moskvitina N.S., Romanenko V.N., Ivanova N.V., Bolshakova N.P., Moskvitin S.S., Korobitsyn I.G., Gashkov S.I., Tiutenkov O.Yu., Kuranova V.N., Kravchenko L.B., Suchkova N.G., Agulova L.P., Loktev V.B. 2010: Genetic diversity of tick-borne pathogenes in Tomsk and environs. Entomol. Rev. 90: 240-250. Go to original source...
  8. Ciota A.T., Payne A.F., Kramer L.D. 2015: West Nile virus adaptation to ixodid tick cells is associated with phenotypic trade-offs in primary hosts. Virology 482: 128-132. Go to original source... Go to PubMed...
  9. Comstedt P., Bergström S., Olsen B., Garpmo U., Marjavaara L., Mejlon H., Barbour A.G., Bunikis J. 2006: Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg. Infect. Dis. 12: 1087-1095. Go to original source... Go to PubMed...
  10. Czank T., Bhide K., Bencúrová E., Dolinská S., Drzewniková P., Major P., Korytár L., Bocková E., Bhide M., Pistl J. 2016: Detection of West Nile virus and tick-borne encephalitis virus in birds in Slovakia, using a universal primer set. Arch. Virol. 161: 1679-1683. Go to original source... Go to PubMed...
  11. Diakou A., Norte A.C., Lopes de Carvalho I., Núncio S., Nováková M., Kautman M., Alivizatos H., Kazantzidis S., Sychra O., Literák I. 2016: Ticks and tick-borne pathogens in wild birds in Greece. Parasitol. Res. 115: 2011-2016. Go to original source... Go to PubMed...
  12. Dubska L., Literak I., Kocianova E., Taragelova V., Sverakova V., Sychra O., Hromadko M. 2011: Synanthropic birds influence the distribution of Borrelia species: analysis of Ixodes ricinus ticks feeding on passerine birds. Appl. Environ. Microbiol. 77: 1115-1117. Go to original source... Go to PubMed...
  13. Dubska L., Literak I., Kocianova E., Taragelova V., Sychra O. 2009: Differential role of passerine birds in distribution of Borrelia spirochetes, based on data from ticks collected from birds during the postbreeding migration period in Central Europe. Appl. Environ. Microbiol. 75: 596-602. Go to original source... Go to PubMed...
  14. Dubska L., Literak I., Kverek P., Roubalova E., Kocianova E., Taragelova V. 2012: Tick-borne zoonotic pathogens in ticks feeding on the common nightingale including a novel strain of Rickettsia sp. Ticks Tick Borne Dis. 3: 265-268. Go to original source... Go to PubMed...
  15. Ebani V.V., Bertelloni F., Mani P. 2016: Molecular survey on zoonotic tick-borne bacteria and chlamydiae in feral pigeons (Columba livia domestica). Asian Pac. J. Trop. Med. 9: 324-327. Go to original source... Go to PubMed...
  16. Eidson M., Komar N., Sorhage F., Nelson R., Talbot T., Mostashari F., McLean R., Stone W., Anand M., Fine A., Jeffery N., Huang A., Falco C., Kopian S., Bradley C., Schmit K., Willsey A., Hagiwara Y., White D., Wallace B., Smith P., Chang H.-G., Bresnitz E., Campbell C., Roscoe D., Andreadis T., Anderson J., Vossbrinck C., Hadler J., Van Kruiningen H., Garmendia A., French R., Dickson J., Sileo L., Kerst A., Lanciotti R., Panella N.A. 2001: Dead crow densities and human cases of West Nile virus, New York State, 2000. Emerg. Infect. Dis. 7: 662-664.
  17. Filippova N.A. 1977: [Ixodid Ticks (Ixodinae)]. Nauka Publ. House, Leningrad, 396 pp. (In Russian.)
  18. Franke J., Moldenhauer A., Hildebrandt A., Dorn W. 2010: Are birds reservoir hosts for Borrelia afzelii? Ticks Tick Borne Dis. 1: 109-112. Go to original source... Go to PubMed...
  19. de la Fuente J., Naranjo V., Ruiz-Fons F., Höfle U., Fernández de Mera I.G., Villanúa D., Almazán C., Torina A., Caracappa S., Kocan K.M., Gortázar C. 2005: Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Dis. 5: 390-401. Go to original source... Go to PubMed...
  20. Geller J., Nazarova L., Katargina O., Leivits A., Järvekülg L., Golovljova I. 2013: Tick-borne pathogens in ticks feeding on migratory passerines in western part of Estonia. Vector Borne Zoonotic Dis. 13: 443-448. Go to original source... Go to PubMed...
  21. Ghosh S., Nagar G. 2014: Problem of ticks and tick-borne diseases in India with special emphasis on progress in tick control research: a review. J. Vector Borne Dis. 51: 259-270. Go to PubMed...
  22. Hagman K., Barboutis C., Ehrenborg C., Fransson T., Jaenson T., Lindgren P-E., Lundkvist Å., Nyström F., Waldenström J., Salaneck E. 2014: On the potential roles of ticks and migrating birds in the ecology of West Nile virus. Inf. Ecol. Epidemiol. 4: 20943. Go to original source... Go to PubMed...
  23. Hamer S.A., Lehrer E., Magle S.B. 2012: Wild birds as sentinels for multiple zoonotic pathogens along an urban to ruralgradient in Greater Chicago, Illinois. Zoonoses Publ. Hlth. 59: 355-364. Go to original source... Go to PubMed...
  24. Hasle G. 2013: Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front. Cell. Infect. Microbiol. 3: 48. Go to original source... Go to PubMed...
  25. Heylen D.J.A., Madder M., Matthysen E. 2010: Lack of resistance against the tick Ixodes ricinus in two related passerine bird species. Int. J. Parasitol. 40: 183-191. Go to original source... Go to PubMed...
  26. Heylen D., Tijsse E., Fonville M., Matthysen E., Sprong H. 2013: Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ. Microbiol. 15: 663-673 Go to original source... Go to PubMed...
  27. Hildebrandt A., Franke J., Meier F., Sachse S., Dorn W., Straube E. 2010: The potential role of migratory birds in transmission cycles of Babesia spp., Anaplasma phagocytophilum, and Rickettsia spp. Ticks Tick Borne Dis. 1: 105-107. Go to original source... Go to PubMed...
  28. Hornok S., Csörgő T., de la Fuente J., Gyuranecz M., Privigyei C., Meli M.L., Kreizinger Z., Gönczi E., Fernández de Mera I.G., Hofmann-Lehmann R. 2013: Synanthropic birds associated with high prevalence of tick-borne Rickettsiae and with the first detection of Rickettsia aeschlimannii in Hungary. Vector Borne Zoonotic Dis. 13: 77-83. Go to original source... Go to PubMed...
  29. Hornok S., Kováts D., Csörgő T., Meli M.L., Gönczi E., Hadnagy Z., Takács N., Farkas R., Hofmann-Lehmann R. 2014: Birds as potential reservoirs of tick-borne pathogens: first evidence of bacteraemia with Rickettsia helvetica. Parasit. Vectors 7: 128. Go to original source... Go to PubMed...
  30. Hubálek Z. 2004: An annotated checklist of pathogenic microorganisms associated with migratory birds. J. Wildl. Dis. 40: 639-659. Go to original source... Go to PubMed...
  31. Ioannou I., Chochlakis D., Kasinis N., Anayiotos P., Lyssandrou A., Papadopoulos B., Tselentis Y., Psaroulaki A. 2009: Carriage of Rickettsia spp., Coxiella burnetii and Anaplasma spp. by endemic and migratory wild birds and their ectoparasites in Cyprus. Clin. Microbiol. Infect. 15: 158-160. Go to original source... Go to PubMed...
  32. Jourdain E., Olsen B., Lundkvist A., Hubálek Z., ©ikutová S., Waldenström J., Karlsson M., Wahlström M., Jozan M., Falk K.I. 2011: Surveillance for West Nile virus in wild birds from northern Europe. Vector Borne Zoonotic Dis. 11: 77-79. Go to original source... Go to PubMed...
  33. Kang J.-G., Kim H.-C., Choi C.-Y., Nam H.-Y., Chae H.-Y., Chong S.-T., Klein T.A., Ko S., Chae J.-S. 2013: Molecular detection of Anaplasma, Bartonella, and Borrelia species in ticks collected from migratory birds from Hong-do Island, Republic of Korea. Vector Borne Zoonotic Dis. 4: 215-225. Go to original source... Go to PubMed...
  34. Kartashov M.Y., Kononova Y.V., Petrova I.D., Tupota N.L., Mikryukova T.P., Ternovoi V.A., Tishkova F.H., Loktev V.B. 2020: Detection of Ehrlichia spp. and Theileria spp. in Hyalomma anatolicum ticks collected in Tajikistan. Vavilovskii Zh. Genet. Selektsii 24: 55-59. Go to original source... Go to PubMed...
  35. Kartashov M.Y., Mikryukova T.P., Moskvitina N.S., Krivosheina E.I., Kuznetsov A.I., Romanenko V.N., Bol'shakova N.P., Ternovoi V.A., Loktev V.B. 2019: [Detection and genotyping of Anaplasma phagocytophilum in I. persulcatus and D. reticulatus ticks collected in Tomsk (Western Siberia) in 2015-2016.] Bull. Siberian Med. 18: 89-98. (In Russian.) Go to original source...
  36. Kislenko G.S., Korotkov Y.S. 1998: [On existence of functional relationship between the index of larva and nymph abundance in a virus carrier and the quantity immunity to infectious stimulus in small rodents from natural locus of tick-borne encephalitis]. Zool. Zh. 77: 504-506. (In Russian.)
  37. Klaus C., Gethmann J., Hoffmann B., Ziegler U., Heller M., Beer M. 2016: Tick infestation in birds and prevalence of pathogens in ticks collected from different places in Germany. Parasitol. Res. 115: 2729-2740. Go to original source... Go to PubMed...
  38. Kuo C.-C., Lin Y.-F., Yao C.-T., Shih H.-C., Chung L.-H., Liao H.-C., Hsu Y.-C., Wang H.-C. 2017: Tick-borne pathogens in ticks collected from birds in Taiwan. Parasit. Vectors 10: 587. Go to original source... Go to PubMed...
  39. Kurtenbach K., Peacey M., Rijpkema S.G.T., Hoodless A.N., Nuttall P.A., Randolph S.E. 1998: Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl. Environ. Microbiol. 64: 1169-1174. Go to original source... Go to PubMed...
  40. Lommano E., Dvořák C., Vallotton L., Jenni L., Gern L. 2014: Tick-borne pathogens in ticks collected from breeding and migratory birds in Switzerland. Ticks Tick Borne Dis. 5: 871-882. Go to original source... Go to PubMed...
  41. López G., Jiménez-Clavero M.Á., Vázquez A., Soriguer R., Gómez-Tejedor C., Tenorio A., Figuerola J. 2011: Incidence of West Nile virus in birds arriving in wildlife rehabilitation centers in southern Spain. Vector Borne Zoonotic Dis. 11: 285-290. Go to original source... Go to PubMed...
  42. Lvov D.K., Il'ichev V.D. 1979: [Migration of Birds and Transmission of Pathogens of Infections. Ecological and Geographical Relations of Birds with Pathogens of Infections]. Nauka, Moscow, 271 pp. (In Russian.)
  43. Lvov D.K., Kovtunov A.I., Yashkulov K.В., Gromashevsky V.L., Djarkenov A.F., Shchelkanov M.Yu., Kulikova L.N., Savidge G., Chimidova N.M., Mikhalyayeva L.В., Vasilyev A.V., Galkina I.V., Prilipov A.G., Kinni R., Samokhvalov E.I., Bushkiyeva B. Ts., Gubler D., Alkhovsky S.V., Aristova V.A., Deryabin P.G., Butenko A.M., Moskvina T.M., Lvov D.N., Zlobina L.V., Lyapina O.V., Sadykova G.K., Shatalov A.G., Usachyov V.Е., Voronina A.G., Lunyova L.I. 2004: [The specificity of circulation of West Nile Virus (Flaviviridae, Flavivirus) and of some other arboviruses in the ecosystems of Volga delta, Volga-Akhtuba flood-lands and adjoining arid regions (2000-2002)]. Vopr. Virusol. 49: 45-52. (In Russian.)
  44. Michelet L., Joncour G., Devillers E. Torina A., Vayssier-Taussat M., Bonnet S.I., Moutailler S. 2016: Tick species, tick-borne pathogens and symbionts in an insular environment off the coast of Western France. Ticks Tick Borne Dis. 7: 1109-1115. Go to original source... Go to PubMed...
  45. Mikryukova T.P., Moskvitina N.S., Kononova Yu.V., Korobitsyn I.G., Kartashov M.Y., Tyuten'kov O.Y., Protopopova E.V., Romanenko V.N., Chausov E.V., Gashkov S.I., Konovalova S.N., Moskvitin S.S., Tupota N.L., Sementsova A.O., Ternovoi V.A., Loktev V.B. 2014: Surveillance of tick-borne encephalitis virus in wild birds and ticks in Tomsk City and its suburbs (Western Siberia). Ticks Tick Borne Dis. 5: 145-151. Go to original source... Go to PubMed...
  46. Molin Y., Lindeborg M., Nyström F., Madder M., Hjelm E., Olsen B., Jaenson T.G.T., Ehrenborg C. 2011: Migratory birds, ticks, and Bartonella. Inf. Ecol. Epidemiol. 1: 5997. Go to original source... Go to PubMed...
  47. Moskvitin S.S. 1992: [Wintering of birds of the Tomsk region and the issue of managing their populations]. In: V.P. Parnachov (Ed.), Problems of Ecology of the Tomsk Region. Vol. I. Tomsk State University, Tomsk, pp. 104-106. (In Russian.)
  48. Moskvitin S.S., Dubovik A.D. 1969: [About the migration of birds of Tomsk region according to the banding]. In: V.P. Parnachov (Ed.), Migratory Birds and Their Role in Spreading Arboviruses. Nauka, Novosibirsk, pp. 50-55. (In Russian.)
  49. Moskvitin S.S., Dubovik A.D. 1977: [About the migration of birds of Tomsk region according to the banding data (message 2)]. In: V.A. Pegel (Ed.), Proceedings of Research of the Institute of Biology and Biophysics, Tomsk State University. Publishing House of Tomsk State University, Tomsk, pp. 6-10. (In Russian.)
  50. Moskvitin S.S., Strelkov V.E. 1977: [About the bird migration in Tomsk region according to the banding]. In: K.T. Yurlov (Ed.), Bird Migration in Asia. Nauka, Novosibirsk, pp. 101-107. (In Russian.)
  51. Moskvitina N.S., Korobitsyn I.G., Tutenkov O.Yu., Gashkov S.I., Kononova Yu.V., Moskvitin S.S., Romanenko V.N., Mikryukova T.P., Protopopova E.V., Kartashov M.Yu., Chausov E.V., Konovalova S.N., Tupota N.L., Sementsova A.O., Ternovoy V.A., Loktev V.B. 2014: The role of birds in the maintenance of tick borne infections in the Tomsk anthropourgic foci. Biol. Bull. 4: 387-393. Go to original source...
  52. Moskvitina N.S., Romanenko V.N., Ternovoi V.A., Ivanova N.V., Protopopova E.V., Kravchenko L.B., Kononova Iu.V., Kuranova V.N., Chausov E.V., Moskvitin S.S., Pershikova N.L., Gashkov S.I., Konovalova S.N., Bol'shakova N.P., Loktev V.B. 2008: [Detection of the West Nile virus and its genetic typing in ixodid ticks (Parasitiformes: Ixodidae) in Tomsk City and its suburbs]. Parazitologiya 42: 210-225. (In Russian.)
  53. Movila A., Alekseev A.N., Dubinina H.V. Toderas I. 2013: Detection of tick-borne pathogens in ticks from migratory birds in the Baltic region of Russia. Med. Vet. Entomol. 27: 113-117. Go to original source... Go to PubMed...
  54. Movila A., Dubinina H.V., Sitnicova N., Bespyatova L., Uspenskaia I., Efremova G., Toderas I., Alekseev A.N. 2014: Comparison of tick-borne microorganism communities in Ixodes spp. of the Ixodes ricinus species complex at distinct geographical regions. Exp. Appl. Acarol. 63: 65-76. Go to original source... Go to PubMed...
  55. Movila A., Reye A.L, Dubinina H.V., Tolstenkov O.O., Toderas I., Hubschen J.M., Muller C.P., Alekseev A.N. 2011: Detection of Babesia sp. EU1 and members of spotted fever group Rickettsiae in ticks collected from migratory birds at Curonian Spit, North-Western Russia. Vector Borne Zoonotic Dis. 11: 89-91. Go to original source... Go to PubMed...
  56. Mumcuoglu K.Y., Banet-Noach C., Malkinson M., Shalom U., Galun R. 2005: Argasid ticks as possible vectors of West Nile virus in Israel. Vector Borne Zoonotic Dis. 5: 65-71. Go to original source... Go to PubMed...
  57. Murata R., Hashiguchi K., Yoshii K., Kariwa H., Nakajima K., Ivanov L.I., Leonova G.N., Takashima, I. 2011: Seroprevalence of West Nile virus in wild birds in Far Eastern Russia using a focus reduction neutralization test. Am. J. Trop. Med. Hyg. 84: 461-465. Go to original source... Go to PubMed...
  58. Nekipelov N.V. 1978: [On possibility of introgression of arboviruses, brought by migratory birds from southern latitude.] In: A.I. Cherepanov (Ed.), Transcontinental Connections of Migratory Birds and Their Roles in the Dispersal of Arboviruses. Nauka, Novosibirsk, pp. 150-152. (In Russian.)
  59. Norte A.C., Ramos J. A., Gern L., Núncio M.S., Lopes de Carvalho I. 2013: Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environ. Microbiol. 15: 386-397. Go to original source... Go to PubMed...
  60. Olsén B., Jaenson T.G.T., Bergrström S. 1995: Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl. Environ. Microbiol. 61: 3082-3087. Go to original source... Go to PubMed...
  61. Palomar A.M., Santibáñez P., Mazuelas D., Roncero L., Santibáñez S., Portillo A., Oteo J. 2012: Role of birds in dispersal of etiologic agents of tick-borne zoonoses, Spain, 2009. Emerg. Inf. Dis. 18: 1188-1191. Go to original source... Go to PubMed...
  62. Pankina T.M., Poltoratskaya N.V., Istratkina S.V., Poltoratskaya T.N., Shikhin A.V. 2015: [Modern epidemiology of infections transmitted by ticks (Parasitiformes, Ixodidae) in the Tomsk region.] In: V. Romanenko, Y. Maximova, R. Bagirov, E. Subbotina (Eds.), Conceptual and Applied Aspects of Scientific Research and Education in the Field of Invertebrate Zoology. Tomsk State University, Tomsk, pp. 200-205. (In Russian.)
  63. Platonov A.E. 2001: West Nile encephalitis in Russia 1999-2001: were we ready? Are we ready? Ann. N.Y. Acad. ScI. 951: 102-116. Go to original source... Go to PubMed...
  64. Ponomareva E.P., Ternovoi V.A., Mikryukova T.P., Protopopova E.V., Tupota N.L., Loktev V.B. 2021. Genetic variability of 5'-untraslated region of the tick-borne encephalitis virus genome in various regions of northern Eurasia. Mol. Biol. 55: 431-440. (In Russian.) Go to original source...
  65. Poupon M.-A., Lomanno E., Humair P.-F., Douet V., Rais O., Schaad M., Lukas J., Gern L. 2006: Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl. Environ. Microbiol. 72: 976-979. Go to original source... Go to PubMed...
  66. Rar V.A., Fomenko N.V., Dobrotvorsky A.K., Livanova N.N., Rudakova S.A., Fedorov E.G., Astanin V.B., Morozova O.V. 2005. Tick-borne pathogen detection in Western Siberia, Russia. Emerg. Infect. Dis. 11: 1708-1715. Go to original source... Go to PubMed...
  67. Reiter P. 2010: West Nile virus in Europe: understanding the present to gauge the future. Euro Surveill. 15: 19508. Go to original source... Go to PubMed...
  68. Romanenko V.N., Chekalkina N.B. 2004: [Species composition of ixodid ticks in the territory of Tomsk]. Vestnik Tomsk State Univ. 11: 132-135. (In Russian.)
  69. Ryabitsev V.K. 2001: [Birds of the Urals and Western Siberia: Identification Guides]. Ural State University, Ekaterinburg, 608 pp. (In Russian.)
  70. Ryabitsev V.K., Boyko G.V., Moskvitin S.S., Vasilchenko A.A., Gagina T.N., Gashev S.N., Zakharov V.D., Irisova N.L., Korovin V.A., Mitrofanov O.B., Petrov V.Yu.., Soloviev S.A., Strelnikov E.G., Tarasov V.V., Tsybulin S.M., Yakimenko V.V. 2001: [Fauna of birds of Western Siberia regions. Inventory, Monitoring and Protection of Important Ornithological Territories of Russia]. Vol. 3. Russian Bird Conservation Union, Moscow, pp. 140-168. (In Russian.)
  71. Sándor A.D., Kalmár Z., Matei I., Ionică A.M., Mărcuţan, I.-D. 2016: Urban breeding corvids as disseminators of ticks and emerging tick-borne pathogens. Vector Borne Zoonotic Dis. 17: 152-154. Go to original source... Go to PubMed...
  72. Sparagano O., George D., Giangaspero A., ©pitalská E. 2015: Arthropods and associated arthropod-borne diseases transmitted by migrating birds. The case of ticks and tick-borne pathogens. Vet. Parasitol. 213: 61-66. Go to original source... Go to PubMed...
  73. ©pitalská E., Literák I., Kocianová E., Taragel'ová V. 2011: The importance of Ixodes arboricola in transmission of Rickettsia spp., Anaplasma phagocytophilum, and Borrelia burgdorferi sensu lato in the Czech Republic, Central Europe. Vector Borne Zoonotic Dis. 9: 1235-1241. Go to original source... Go to PubMed...
  74. Stańczak J., Racewicz M., Michalik J., Cieniuch S., Sikora B., Skoracki M. 2009: Prevalence of infection with Rickettsia helvetica in feeding ticks and their hosts in western Poland. Clin. Microbiol. Infect. 15: 328-329. Go to original source... Go to PubMed...
  75. State Report on Sanitary and Epidemiological Situation in Tomsk District in 2017. http://70.rospotrebnadzor.ru. (In Russian.)
  76. Sumner J.W., Nicholson W.L., Massung R.F. 1997: PCR amplification and comparison of nucleotide sequences from the groESL heat shock operon of Ehrlichia species. J. Clin. Microbiol. 35: 2087-2092. Go to original source... Go to PubMed...
  77. Ternovoi V.A., Protopopova E.V., Chausov E.V., Novikov D.V., Leonova G.N., Netesov S.V., Loktev V.B. 2007: Novel variant of tickborne encephalitis virus, Russia. Emerg. Infect. Dis. 13: 1574-1578. Go to original source... Go to PubMed...
  78. Ternovoi V.A., Schelkanov M.Yu., Shestopalov A.M., Aristova V.A., Protopopova E.V., Gromashevskiy V.L., Druzyaka A.V., Slavskiy A.A., Zolotykh S.I., Loktev V.B., Lvov D.K. 2004: [Detection of West Nile virus in birds in the territory of Baraba and Kulunda lowland (West-Siberean migration flyway) in the summer-autumn period of 2002 year]. Vopr. Virol. 3: 52-56. (In Russian.)
  79. Toma L., Mancini F., Di Luca M., Cecere J.G., Bianchi R., Khoury C., Quarchioni E., Manzia F., Rezza G., Ciervo A. 2014: Detection of microbial agents in ticks collected from migratory birds in Central Italy. Vector Borne Zoonotic Dis. 3: 199-205. Go to original source... Go to PubMed...
  80. Tonetti N., Berggoetz M., Rühle C., Pretorius A. M., Gern L. 2009: Ticks and tick-borne pathogens from wildlife in the Free State Province, South Africa. J. Wildlife Dis. 45: 437-446. Go to original source... Go to PubMed...
  81. Tsiodras S., Kelesidis T., Kelesidis I., Bauchinger U., Falagas M.E. 2008: Human infections associated with wild birds. J. Infect. 56: 83-89. Go to original source... Go to PubMed...
  82. Ushakova G.V., Filippova N.A., Panova I.V. 1969: [On the types of groups of Ixodes persulcatus (Parasitiformes, Ixodidae). IV. New data on the ecology of Ixodes pavlovskyi Pom. in Eastern Kazakhstan]. Parazitologiya 5: 436-439. (In Russian.)
  83. Wakelin D. 1996: Immunity to Parasites. Cambridge University Press, Cambridge, 204 pp.
  84. Wheeler S.S., Vineyard M.P., Woods L.W., Reisen W.K. 2012: Dynamics of West Nile virus persistence in house sparrows (Passer domesticus). PLoS Negl. Trop. Dis. 6: e1860. Go to original source... Go to PubMed...
  85. Wikel S.K., Ramachandra R.N., Bergman D.K., Burkot T.R., Piesman J. 1997: Infestation with pathogen-free nymphs of the tick Ixodes scapularis induces host resistance to transmission of Borrelia burgdorferi by ticks. Infect. Immun. 65: 335-338. Go to original source... Go to PubMed...
  86. Yabsley M.J., Shock B.C. 2013: Natural history of zoonotic Babesia: role of wildlife reservoirs. Int. J. Parasitol. Parasites Wildl. 2: 18-31. Go to original source... Go to PubMed...
  87. Yang J., Liu Z., Niu Q., Tian Z., Liu J., Guan G., Liu G., Luo J., Wang X., Yin H. 2015: Tick-borne zoonotic pathogens in birds in Guangxi, Southwest China. Parasit. Vectors 8: 637. Go to original source... Go to PubMed...