1887

Abstract

In order to obtain a better understanding of tick-borne encephalitis virus (TBEV) strain movements in central Europe the E gene sequences of 102 TBEV strains collected from 1953 to 2011 at 38 sites in the Czech Republic, Slovakia, Austria and Germany were determined. Bayesian analysis suggests a 350-year history of evolution and spread in central Europe of two main lineages, A and B. In contrast to the east to west spread at the Eurasian continent level, local central European spreading patterns suggest historic west to east spread followed by more recent east to west spread. The phylogenetic and network analyses indicate TBEV ingressions from the Czech Republic and Slovakia into Germany via landscape features (Danube river system), biogenic factors (birds, red deer) and anthropogenic factors. The identification of endemic foci showing local genetic diversity is of paramount importance to the field as these will be a prerequisite for in-depth analysis of focal TBEV maintenance and long-distance TBEV spread.

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2013-09-01
2024-11-02
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References

  1. Aberle J. H., Aberle S. W., Allison S. L., Stiasny K., Ecker M., Mandl C. W., Berger R., Heinz F. X. 1999; A DNA immunization model study with constructs expressing the tick-borne encephalitis virus envelope protein E in different physical forms. J Immunol 163:6756–6761[PubMed]
    [Google Scholar]
  2. Achazi K., Růžek D., Donoso-Mantke O., Schlegel M., Ali H. S., Wenk M., Schmidt-Chanasit J., Ohlmeyer L., Rühe F. other authors 2011; Rodents as sentinels for the prevalence of tick-borne encephalitis virus. Borne Zoonotic Dis 11:641–647 [View Article][PubMed]
    [Google Scholar]
  3. Bielejec F., Rambaut A., Suchard M. A., Lemey P. 2011; SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics 27:2910–2912 [View Article][PubMed]
    [Google Scholar]
  4. Bolzoni L., Rosà R., Cagnacci F., Rizzoli A. 2012; Effect of deer density on tick infestation of rodents and the hazard of tick-borne encephalitis. II: population and infection models. Int J Parasitol 42:373–381 [View Article][PubMed]
    [Google Scholar]
  5. Cagnacci F., Bolzoni L., Rosà R., Carpi G., Hauffe H. C., Valent M., Tagliapietra V., Kazimirova M., Koci J. other authors 2012; Effects of deer density on tick infestation of rodents and the hazard of tick-borne encephalitis. I: empirical assessment. Int J Parasitol 42:365–372 [View Article][PubMed]
    [Google Scholar]
  6. Carpi G., Cagnacci F., Neteler M., Rizzoli A. 2008; Tick infestation on roe deer in relation to geographic and remotely sensed climatic variables in a tick-borne encephalitis endemic area. Epidemiol Infect 136:1416–1424 [View Article][PubMed]
    [Google Scholar]
  7. Carrel M. A., Emch M., Jobe R. T., Moody A., Wan X. F. 2010; Spatiotemporal structure of molecular evolution of H5N1 highly pathogenic avian influenza viruses in Vietnam. PLoS ONE 5:e8631 [View Article][PubMed]
    [Google Scholar]
  8. Chambers T. J., Hahn C. S., Galler R., Rice C. M. 1990; Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44:649–688 [View Article][PubMed]
    [Google Scholar]
  9. Daniel M., Danielová V., Kriz B., Kott I. 2004; An attempt to elucidate the increased incidence of tick-borne encephalitis and its spread to higher altitudes in the Czech Republic. Int J Med Microbiol 293:Suppl 3755–62[PubMed]
    [Google Scholar]
  10. Daniel M., Benes C., Danielová V., Kríz B. 2011; Sixty years of research of tick-borne encephalitis a basis of the current knowledge of the epidemiological situation in Central Europe. Epidemiol Mikrobiol Imunol 60:135–155[PubMed]
    [Google Scholar]
  11. Danielová V., Rudenko N., Daniel M., Holubová J., Materna J., Golovchenko M., Schwarzová L. 2006; Extension of Ixodes ricinus ticks and agents of tick-borne diseases to mountain areas in the Czech Republic. Int J Med Microbiol 296:Suppl 4048–53 [View Article][PubMed]
    [Google Scholar]
  12. Donoso Mantke O., Escadafal C., Niedrig M., Pfeffer M. Working Group For Tick-Borne Encephalitis Virus C. 2011; Tick-borne encephalitis in Europe, 2007 to 2009. Euro Surveill 16:pii: 19976[PubMed]
    [Google Scholar]
  13. Drummond A. J., Rambaut A. 2007; BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [View Article][PubMed]
    [Google Scholar]
  14. Durmiši E., Knap N., Saksida A., Trilar T., Duh D., Avšič-Županc T. 2011; Prevalence and molecular characterization of tick-borne encephalitis virus in Ixodes ricinus ticks collected in Slovenia. Vector Borne Zoonotic Dis 11:659–664 [View Article][PubMed]
    [Google Scholar]
  15. Fajs L., Durmiši E., Knap N., Strle F., Avšič-Županc T. 2012; Phylogeographic characterization of tick-borne encephalitis virus from patients, rodents and ticks in Slovenia. PLoS ONE 7:e48420 [View Article][PubMed]
    [Google Scholar]
  16. Felsenstein J. 2004 Inferring Phylogenies Sunderland: Sinauer Associates Inc;
    [Google Scholar]
  17. Fickel J., Bubliy O. A., Stache A., Noventa T., Jirsa A., Heurich M. 2012; Crossing the border? Structure of the red deer (Cervus elaphus) population from the Bavarian–Bohemian forest ecosystem. Mamm Biol 77:211–220
    [Google Scholar]
  18. Fourment M., Gibbs M. J. 2006; PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol Biol 6:1 [View Article][PubMed]
    [Google Scholar]
  19. Frey S., Mossbrugger I., Altantuul D., Battsetseg J., Davaadorj R., Tserennorov D., Buyanjargal T., Otgonbaatar D., Zöller L. other authors 2012; Isolation, preliminary characterization, and full-genome analyses of tick-borne encephalitis virus from Mongolia. Virus Genes 45:413–425 (Epub ahead of print) [View Article][PubMed]
    [Google Scholar]
  20. Heinze D. M., Gould E. A., Forrester N. L. 2012; Revisiting the clinal concept of evolution and dispersal for the tick-borne flaviviruses by using phylogenetic and biogeographic analyses. J Virol 86:8663–8671 [View Article][PubMed]
    [Google Scholar]
  21. Hillyard P. D. 1996 Ticks of North-West Europe Dorset Press; Dorchester:
    [Google Scholar]
  22. Hoogstraal H., Kaiser M. N., Traylor M. A., Guindy E., Gaber S. 1963; Ticks (Ixodidae) on birds migrating from Europe and Asia to Africa 1959–61. Bull World Health Organ 28:235–262[PubMed]
    [Google Scholar]
  23. Huson D. H., Richter D. C., Rausch C., Dezulian T., Franz M., Rupp R. 2007; Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460 [View Article][PubMed]
    [Google Scholar]
  24. Klaus C., Hoffmann B., Hering U., Mielke B., Sachse K., Beer M., Süss J. 2010; Tick-borne encephalitis (TBE) virus prevalence and virus genome characterization in field-collected ticks (Ixodes ricinus) from risk, non-risk and former risk areas of TBE, and in ticks removed from humans in Germany. Clin Microbiol Infect 16:238–244 [View Article][PubMed]
    [Google Scholar]
  25. Knap N., Korva M., Dolinšek V., Sekirnik M., Trilar T., Avšič-Županc T. 2012; Patterns of tick-borne encephalitis virus infection in rodents in Slovenia. Vector Borne Zoonotic Dis 12:236–242 [View Article][PubMed]
    [Google Scholar]
  26. Kovalev S. Y., Chernykh D. N., Kokorev V. S., Snitkovskaya T. E., Romanenko V. V. 2009; 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 90:2884–2892 [View Article][PubMed]
    [Google Scholar]
  27. Krejčí J. 1949; [Outbreak of encephalitis virus in the region of Vyškov.]. Lék Listy (Brno) 473–75, , 112–116, 132–134
    [Google Scholar]
  28. Kriz B., Maly M., Benes C., Daniel M. 2012; Epidemiology of tick-borne encephalitis in the Czech Republic 1970–2008. Vector Borne Zoonotic Dis 12:994–999 [View Article][PubMed]
    [Google Scholar]
  29. Kupča A. M., Essbauer S., Zoeller G., de Mendonça P. G., Brey R., Rinder M., Pfister K., Spiegel M., Doerrbecker B. other authors 2010; Isolation and molecular characterization of a tick-borne encephalitis virus strain from a new tick-borne encephalitis focus with severe cases in Bavaria, Germany. Ticks Tick-borne Dis 1:44–51 [View Article][PubMed]
    [Google Scholar]
  30. Labuda M., Nuttall P. A. 2004; Tick-borne viruses. Parasitology 129:Suppl S1S221–S245 [View Article][PubMed]
    [Google Scholar]
  31. Labuda M., Randolph S. E. 1999; Survival strategy of tick-borne encephalitis virus: cellular basis and environmental determinants. Zentralbl Bakteriol 289:513–524 [View Article][PubMed]
    [Google Scholar]
  32. Labuda M., Elecková E., Licková M., Sabó A. 2002; Tick-borne encephalitis virus foci in Slovakia. Int J Med Microbiol 291:Suppl 3343–47 [View Article][PubMed]
    [Google Scholar]
  33. Lemey P., Rambaut A., Drummond A. J., Suchard M. A. 2009; Bayesian phylogeography finds its roots. PLOS Comput Biol 5:e1000520 [View Article][PubMed]
    [Google Scholar]
  34. Lemey P., Rambaut A., Welch J. J., Suchard M. A. 2010; Phylogeography takes a relaxed random walk in continuous space and time. Mol Biol Evol 27:1877–1885 [View Article][PubMed]
    [Google Scholar]
  35. Licoppe A., Lievens J. 2011 Seasonal home ranges of red deer (Cervus elaphus) and its impact on the scale of culling management. In Abstracts XXXth International Union of Game Biologists Congress 5–9 September 2011, Barcelona, Spain, p. 319 Available at http://www.alospaincongress.com/contenido/Llibre_Abstrats%20retocat%20iugb.pdf
    [Google Scholar]
  36. Lommano E., Burri C., Maeder G., Guerne M., Bastic V., Patalas E., Gern L. 2012; Prevalence and genotyping of tick-borne encephalitis virus in questing Ixodes ricinus ticks in a new endemic area in western Switzerland. J Med Entomol 49:156–164 [View Article][PubMed]
    [Google Scholar]
  37. Moshkin M. P., Novikov E. A., Tkachev S. E., Vlasov V. V. 2009; Epidemiology of a tick-borne viral infection: theoretical insights and practical implications for public health. Bioessays 31:620–628 [View Article][PubMed]
    [Google Scholar]
  38. Nicolaisen L. E., Desai M. M. 2012; Distortions in genealogies due to purifying selection. Mol Biol Evol 29:3589–3600 [View Article][PubMed]
    [Google Scholar]
  39. Oksanen J., Blanchet F., Kindt R., Legendre P., Minchin P. R., O’Hara R. B., Simpson G. L. 2012; Vegan: Community Ecology Package. R package version 2.0–5. http://cran.r-project.org/package/vegan/index.html
  40. Paradis E., Claude J., Strimmer K. 2004; APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290 [View Article][PubMed]
    [Google Scholar]
  41. Pond S. L. K., Frost S. D. W., Muse S. V. 2005; HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679 [View Article][PubMed]
    [Google Scholar]
  42. Posada D. 2008; jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256 [View Article][PubMed]
    [Google Scholar]
  43. Randolph S. E., Storey K. 1999; Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. J Med Entomol 36:741–748[PubMed] [CrossRef]
    [Google Scholar]
  44. Randolph S. E., Miklisová D., Lysy J., Rogers D. J., Labuda M. 1999; Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118:177–186 [View Article][PubMed]
    [Google Scholar]
  45. Randolph S. E., Green R. M., Peacey M. F., Rogers D. J. 2000; Seasonal synchrony: the key to tick-borne encephalitis foci identified by satellite data. Parasitology 121:15–23 [View Article][PubMed]
    [Google Scholar]
  46. Silaghi C., Woll D., Mahling M., Pfister K., Pfeffer M. 2012; Candidatus Neoehrlichia mikurensis in rodents in an area with sympatric existence of the hard ticks Ixodes ricinus and Dermacentor reticulatus, Germany. Parasit Vectors 5:285 [View Article][PubMed]
    [Google Scholar]
  47. Široký P., Kubelová M., Bednář M., Modrý D., Hubálek Z., Tkadlec E. 2011; The distribution and spreading pattern of Der macentor reticulatus over its threshold area in the Czech Republic –how much is range of this vector expanding?. Vet Parasitol 183:130–135 [View Article][PubMed]
    [Google Scholar]
  48. Suchard M. A., Weiss R. E., Sinsheimer J. S. 2001; Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 18:1001–1013 [View Article][PubMed]
    [Google Scholar]
  49. SurvStat 2012 See http://www3.rki.de/SurvStat/QueryForm.aspx Robert Koch Institute
  50. Tonteri E., Jääskeläinen A. E., Tikkakoski T., Voutilainen L., Niemimaa J., Henttonen H., Vaheri A., Vapalahti O. 2011; Tick-borne encephalitis virus in wild rodents in winter, Finland, 2008–2009. Emerg Infect Dis 17:72–75 [View Article][PubMed]
    [Google Scholar]
  51. Twiddy S. S., Holmes E. C., Rambaut A. 2003; Inferring the rate and time-scale of dengue virus evolution. Mol Biol Evol 20:122–129 [View Article][PubMed]
    [Google Scholar]
  52. Uzcátegui N. Y., Sironen T., Golovljova I., Jääskeläinen A. E., Välimaa H., Lundkvist A., Plyusnin A., Vaheri A., Vapalahti O. 2012; Rate of evolution and molecular epidemiology of tick-borne encephalitis virus in Europe, including two isolations from the same focus 44 years apart. J Gen Virol 93:786–796 [View Article][PubMed]
    [Google Scholar]
  53. Vor T., Kiffner C., Hagedorn P., Niedrig M., Rühe F. 2010; Tick burden on European roe deer (Capreolus capreolus). Exp Appl Acarol 51:405–417 [View Article][PubMed]
    [Google Scholar]
  54. Walczak A. M., Nicolaisen L. E., Plotkin J. B., Desai M. M. 2012; The structure of genealogies in the presence of purifying selection: a fitness-class coalescent. Genetics 190:753–779 [View Article][PubMed]
    [Google Scholar]
  55. Waldenström J., Lundkvist A., Falk K. I., Garpmo U., Bergström S., Lindegren G., Sjöstedt A., Mejlon H., Fransson T. other authors 2007; Migrating birds and tickborne encephalitis virus. Emerg Infect Dis 13:1215–1218 [View Article][PubMed]
    [Google Scholar]
  56. Weidmann M., Ruzek D., Krivanec K., Zöller G., Essbauer S., Pfeffer M., Zanotto P. M., Hufert F. T., Dobler G. 2011; Relation of genetic phylogeny and geographical distance of tick-borne encephalitis virus in central Europe. J Gen Virol 92:1906–1916 [View Article][PubMed]
    [Google Scholar]
  57. Wertheim J. O., Kosakovsky Pond S. L. 2011; Purifying selection can obscure the ancient age of viral lineages. Mol Biol Evol 28:3355–3365 [View Article][PubMed]
    [Google Scholar]
  58. Woolley S. M., Posada D., Crandall K. A. 2008; A comparison of phylogenetic network methods using computer simulation. PLoS ONE 3:e1913 [View Article][PubMed]
    [Google Scholar]
  59. Zanotto P. M. de A., Gao G. F., Gritsun T., Marin M. S., Jiang W. R., Venugopal K., Reid H. W., Gould E. A. 1995; An arbovirus cline across the northern hemisphere. Virology 210:152–159 [View Article][PubMed]
    [Google Scholar]
  60. Zanotto P. M., Gould E. A., Gao G. F., Harvey P. H., Holmes E. C. 1996; Population dynamics of flaviviruses revealed by molecular phylogenies. Proc Natl Acad Sci U S A 93:548–553 [View Article][PubMed]
    [Google Scholar]
  61. Zwickl D. J. 2006 Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion Austin: University of Texas;
    [Google Scholar]
  62. Zygner W., Górski P., Wedrychowicz H. 2009; New localities of Dermacentor reticulatus tick (vector of Babesia canis canis) in central and eastern Poland. Pol J Vet Sci 12:549–555[PubMed]
    [Google Scholar]
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