Rate of evolution and molecular epidemiology of tick-borne encephalitis virus in Europe, including two isolations from the same focus 44 years apart

Journal of General Virology

Volumn 93, Issue 4, 2012, Pages 786-796

  Uzcátegui, Nathalie Y ^a   Sironen, Tarja ^a   Golovljova, Irina ^b,c   Jääskeläinen, Anu E ^a   Välimaa, Hannamari ^a,d   Lundkvist, Åke ^b   Plyusnin, Alexander ^a   Vaheri, Antti ^a,d   Vapalahti, Olli ^a,d,e  

^a UNIVERSITY OF HELSINKI   (Finland)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c NATIONAL INSTITUTE FOR HEALTH DEVELOPMENT   (Estonia)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4A;

ARTICLE; EUROPE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VIRUS ISOLATION; VIRUS RECOMBINATION; VIRUS STRAIN;

ANIMALS; BASE SEQUENCE; ENCEPHALITIS VIRUSES, TICK-BORNE; ENCEPHALITIS, TICK-BORNE; ESTONIA; EUROPE; EVOLUTION, MOLECULAR; FEMALE; FINLAND; GENETIC VARIATION; HUMANS; IXODES; MALE; MICE; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; PHYLOGENY;

FLAVIVIRIDAE; IXODES; IXODIDA; MAMMALIA; RODENTIA; TICK-BORNE ENCEPHALITIS VIRUS;

EID: 84858260920     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.035766-0     Document Type: Article

References (72)

1. Anderson, J. F. & Magnarelli, L. A. (2008). Biology of ticks. Infect Dis Clin North Am 22, 195-215.
2. Asikainen, K., Hänninen, T., Henttonen, H., Niemimaa, J., Laakkonen, J., Andersen, H. K., Bille, N., Leirs, H., Vaheri, A. & Plyusnin, A. (2000). Molecular evolution of Puumala hantavirus in Fennoscandia: phylogenetic analysis of strains from two recolonization routes, Karelia and Denmark. J Gen Virol 81, 2833-2841.
3. Bakhvalova, V. N., Potapova, O. F., Panov, V. V. & Morozova, O. V. (2009). Vertical transmission of tick-borne encephalitis virus between generations of adapted reservoir small rodents. Virus Res 140, 172-178.
4. Bourhy, H., Kissi, B., Audry, L., Smreczak, M., Sadkowska-Todys, M., Kulonen, K., Tordo, N., Zmudzinski, J. F. & Holmes, E. C. (1999). Ecology and evolution of rabies virus in Europe. J Gen Virol 80, 2545-2557.
5. Brummer-Korvenkontio, M., Saikku, P., Korhonen, P. & Oker-Blom, N. (1973). Arboviruses in Finland. I. Isolation of tick-borne encephalitis (TBE) virus from arthropods, vertebrates, and patients. Am J Trop Med Hyg 22, 382-389.
6. Charrel, R. N., Attoui, H., Butenko, A. M., Clegg, J. C., Deubel, V., Frolova, T. V., Gould, E. A., Gritsun, T. S., Heinz, F. X. & other authors (2004). Tick-borne virus diseases of human interest in Europe. Clin Microbiol Infect 10, 1040-1055.
7. Cook, S. & Holmes, E. C. (2006). A multigene analysis of the phylogenetic relationships among the flaviviruses (family: Flaviviridae) and the evolution of vector transmission. Arch Virol 151, 309-325.
8. Danielová, V. & Holubová, J. (1991). Transovarial transmission rate of tick-borne encephalitis virus in Ixodes ricinus ticks. In Modern Acarology, pp. 7-10. Edited by F. Dusbabek & V. Bukva. The Hague: Academia, Prague and SPB Academic Publishing.
9. Danielová, V., Kliegrová, S., Daniel, M. & Benes, C. (2008). Influence of climate warming on tickborne encephalitis expansion to higher altitudes over the last decade (1997-2006) in the Highland Region (Czech Republic). Cent Eur J Public Health 16, 4-11.
10. Drummond, A. J. & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214.
11. Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.
12. Estrada-Peña, A. &Jongejan, F. (1999). Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23, 685-715.
13. Felsenstein, J. (1989). PHYLIP-phylogeny inference package (version 3.2). Cladistics 5, 164-166.
14. Gaunt, M. W., Sall, A. A., de Lamballerie, X., Falconar, A. K., Dzhivanian, T. I. & Gould, E. A. (2001). Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol 82, 1867-1876.
15. Golovljova, I., Vene, S., Sjölander, K. B., Vasilenko, V., Plyusnin, A. & Lundkvist, A. (2004). Characterization of tick-borne encephalitis virus from Estonia. J Med Virol 74, 580-588.
16. Golovljova, I., Katargina, O., Geller, J., Tallo, T., Mittzenkov, V., Vene, S., Nemirov, K., Kutsenko, A., Kilosanidze, G. & other authors (2008).Unique signature amino acid substitution in Baltic tick-borne encephalitis virus (TBEV) strains within the Siberian TBEV subtype. Int J Med Microbiol 298 (Suppl. 1), 108-120.
17. Gould, E. A., de Lamballerie, X., Zanotto, P. M. & Holmes, E. C. (2001). Evolution, epidemiology, and dispersal of flaviviruses revealed by molecular phylogenies. Adv Virus Res 57, 71-103.
18. Grard, G., Moureau, G., Charrel, R. N., Lemasson, J. J., Gonzalez, J. P., Gallian, P., Gritsun, T. S., Holmes, E. C., Gould, E. A. & de Lamballerie, X. (2007). Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology 361, 80-92.
19. Gritsun, T. S., Frolova, T. V., Zhankov, A. I., Armesto, M., Turner, S. L., Frolova, M. P., Pogodina, V. V., Lashkevich, V. A. & Gould, E. A. (2003). Characterization of a siberian virus isolated from a patient with progressive chronic tick-borne encephalitis. J Virol 77, 25-36.
20. Haglund, M., Forsgren, M., Lindh, G. & Lindquist, L. (1996). A 10-year follow-up study of tick-borne encephalitis in the Stockholm area and a review of the literature: need for a vaccination strategy. Scand J Infect Dis 28, 217-224.
21. Han, X., Aho, M., Vene, S., Peltomaa, M., Vaheri, A. & Vapalahti, O. (2001). Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in Finland. J Med Virol 64, 21-28.
22. Hasegawa, M., Kishino, H. & Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22, 160-174.
23. Hasle, G., Bjune, G., Edvardsen, E., Jakobsen, C., Linnehol, B., Røer, J. E., Mehl, R., Røed, K. H., Pedersen, J. & Leinaas, H. P. (2009). Transport of ticks by migratory passerine birds to Norway. J Parasitol 95, 1342-1351.
24. Hayasaka, D., Suzuki, Y., Kariwa, H., Ivanov, L., Volkov, V., Demenev, V., Mizutani, T., Gojobori, T. & Takashima, I. (1999). Phylogenetic and virulence analysis of tick-borne encephalitis viruses from Japan and far- Eastern Russia. J Gen Virol 80, 3127-3135.
25. Heinz, F. X., Holzmann, H., Essl, A. & Kundi, M. (2007). Field effectiveness of vaccination against tick-borne encephalitis. Vaccine 25, 7559-7567.
26. Holzmann, H., Aberle, S. W., Stiasny, K., Werner, P., Mischak, A., Zainer, B., Netzer, M., Koppi, S., Bechter, E. & Heinz, F. X. (2009). Tick-borne encephalitis from eating goat cheese in a mountain region of Austria. Emerg Infect Dis 15, 1671-1673.
27. Jääskeläinen, A. E., Tikkakoski, T., Uzcá tegui, N. Y., Alekseev, A. N., Vaheri, A. &Vapalahti, O. (2006). Siberian subtype tickborne encephalitis virus, Finland. Emerg Infect Dis 12, 1568-1571.
28. Jääskeläinen, A. E., Sironen, T., Murueva, G. B., Subbotina, N., Alekseev, A. N., Castrén, J., Alitalo, I., Vaheri, A. & Vapalahti, O. (2010). Tick-borne encephalitis virus in ticks in Finland, Russian Karelia and Buryatia. J Gen Virol 91, 2706-2712.
29. Jääskeläinen, A. E., Tonteri, E., Sironen, T., Pakarinen, L., Vaheri, A. & Vapalahti, O. (2011). European subtype tick-borne encephalitis virus in Ixodes persulcatus ticks. Emerg Infect Dis 17, 323-325.
30. Juceviciene, A., Vapalahti, O., Laiskonis, A., Ceplikiene, J. & Leinikki, P. (2002). Prevalence of tick-borne-encephalitis virus antibodies in Lithuania. J Clin Virol 25, 23-27.
31. Kerbo, N., Donchenko, I., Kutsar, K. & Vasilenko, V. (2005). Tickborne encephalitis outbreak in Estonia linked to raw goat milk, May-June 2005. Euro Surveill 10, E050623.2.
32. Kim, S. Y., Yun, S. M., Han, M. G., Lee, I. Y., Lee, N. Y., Jeong, Y. E., Lee, B. C. & Ju, Y. R. (2008). Isolation of tick-borne encephalitis viruses from wild rodents, South Korea. Vector Borne Zoonotic Dis 8, 7-14.
33. Kim, S. Y., Jeong, Y. E., Yun, S. M., Lee, I. Y., Han, M. G. & Ju, Y. R. (2009). Molecular evidence for tick-borne encephalitis virus in ticks in South Korea. Med Vet Entomol 23, 15-20.
34. 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 theMiddle Urals, the north-west of Russia and the Baltic countries. J GenVirol 90, 2884-2892.
35. Kovalev, S. Y., Kokorev, V. S. & Belyaeva, I. V. (2010). Distribution of Far-Eastern tick-borne encephalitis virus subtype strains in the former Soviet Union. J Gen Virol 91, 2941-2946.
36. Labuda, M., Nuttall, P. A., Kozuch, O., Elecková, E., Williams, T., Zuffová, E. & Sabó, A. (1993). Non-viraemic transmission of tickborne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49, 802-805.
37. Labuda, M., Kozuch, O., Zuffová, E., Elecková, E., Hails, R. S. & Nuttall, P. A. (1997). Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235, 138-143.
38. Lindquist, L. & Vapalahti, O. (2008). Tick-borne encephalitis. Lancet 371, 1861-1871.
39. Lindström, A. and Jaenson, T. G. (2003). Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. J Med Entomol 40, 375-378.
40. Lukan, M., Bullova, E. & Petko, B. (2010). Climate warming and tickborne encephalitis, Slovakia. Emerg Infect Dis 16, 524-526.
41. Lundkvist, Å., Vene, S., Golovljova, I., Mavtchoutko, V., Forsgren, M., Kalnina, V. & Plyusnin, A. (2001). Characterization of tick-borne encephalitis virus from Latvia: evidence for co-circulation of three distinct subtypes. J Med Virol 65, 730-735.
42. Luterbacher, J., Dietrich, D., Xoplaki, E., Grosjean, M. & Wanner, H. (2004). European seasonal and annual temperature variability, trends, and extremes since 1500. Science 303, 1499-1503.
43. Mansfield, K. L., Johnson, N., Phipps, L. P., Stephenson, J. R., Fooks, A. R. & Solomon, T. (2009). Tick-borne encephalitis virus -a review of an emerging zoonosis. J Gen Virol 90, 1781-1794.
44. Martin, D. & Rybicki, E. (2000). RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562-563.
45. Mavtchoutko, V., Vene, S., Haglund, M., Forsgren, M., Duks, A., Kalnina, V., Hö rling, J. & Lundkvist, A. (2000). Characterization of tick-borne encephalitis virus from Latvia. J Med Virol 60, 216-222.
46. McGuire, K., Holmes, E. C., Gao, G. F., Reid, H. W. & Gould, E. A. (1998). Tracing the origins of louping ill virus by molecular phylogenetic analysis. J Gen Virol 79, 981-988.
47. Myat Thu, H., Lowry, K., Jiang, L., Hlaing, T., Holmes, E. C. & Aaskov, J. (2005). Lineage extinction and replacement in dengue type 1 virus populations are due to stochastic events rather than to natural selection. Virology 336, 163-172.
48. Posada, D. & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818.
49. Randolph, S. E. (2000). Ticks and tick-borne disease systems in space and from space. Adv Parasitol 47, 217-243.
50. Randolph, S. E. (2010). To what extent has climate change contributed to the recent epidemiology of tick-borne diseases? Vet Parasitol 167, 92-94.
51. Randolph, S. E. & Rogers, D. J. (2000). Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. Proc Biol Sci 267, 1741-1744.
52. 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.
53. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002). TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504.
54. Shapiro, B., Rambaut, A. & Drummond, A. J. (2006). Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23, 7-9.
55. Silber, L. A. & Soloviev, V. D. (1946). Far Eastern tick-borne spring-summer (spring) encephalitis. Am Rev Sov Med (Spec. Suppl.), 1-80.
56. Sumilo, D., Bormane, A., Asokliene, L., Lucenko, I., Vasilenko, V. & Randolph, S. (2006). Tick-borne encephalitis in the Baltic States: identifying risk factors in space and time. Int J Med Microbiol 296 (Suppl. 40), 76-79.
57. Sumilo, D., Asokliene, L., Bormane, A., Vasilenko, V., Golovljova, I. & Randolph, S. E. (2007). Climate change cannot explain the upsurge of tick-borne encephalitis in the Baltics. PLoS One 2, e500.
58. Sumilo, D., Bormane, A., Asokliene, L., Vasilenko, V., Golovljova, I., Avsic-Zupanc, T., Hubalek, Z. & Randolph, S. E. (2008a). Socioeconomic factors in the differential upsurge of tick-borne encephalitis in Central and Eastern Europe. Rev Med Virol 18, 81-95.
59. Sumilo, D., Asokliene, L., Avsic-Zupanc, T., Bormane, A., Vasilenko, V., Lucenko, I., Golovljova, I. & Randolph, S. E. (2008b). Behavioural responses to perceived risk of tick-borne encephalitis: vaccination and avoidance in the Baltics and Slovenia. Vaccine 26, 2580-2588.
60. Sü ss, J. (2008). Tick-borne encephalitis in Europe and beyond -the epidemiological situation as of 2007. Euro Surveill 13, 18916.
61. Suzuki, Y. (2007). Multiple transmissions of tick-borne encephalitis virus between Japan and Russia. Genes Genet Syst 82, 187-195.
62. Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
63. Thiel, H. J., Collett, M. S., Gould, E. A., Heinz, F. X., Houghton, M., Meyers, G., Purcell, R. H. & Rice, C. M. (2005). Family Flaviviridae. In Virus Taxonomy: Classification and Nomenclature. Eighth Report of the International Committee on the Taxonomy of Viruses, pp. 981-998. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego, CA: Elsevier Academic Press.
64. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
65. Tonteri, E., Jääskeläinen, A. E., Tikkakoski, T., Voutilainen, L., Niemimaa, J., Henttonen, H., Vaheri, A. & Vapalahti, O. (2011). Tickborne encephalitis virus in wild rodents in winter, Finland, 2008-2009. Emerg Infect Dis 17, 72-75.
66. Twiddy, S. S. & Holmes, E. C. (2003). The extent of homologous recombination in members of the genus Flavivirus. J Gen Virol 84, 429-440.
67. Waldenström, J., Lundkvist, Å., Falk, K. I., Garpmo, U., Bergströ m, S., Lindegren, G., Sjö stedt, A., Mejlon, H., Fransson, T. & other authors (2007). Migrating birds and tickborne encephalitis virus. Emerg Infect Dis 13, 1215-1218.
68. Whitby, J. E., Jennings, A. D. & Barrett, A. D. (1993). Nucleotide sequence of the envelope protein gene of the tick-borne flavivirus, Kumlinge A52. Virus Genes 7, 145-149.
69. Xia, X. & Xie, Z. (2001). DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92, 371-373.
70. Zanotto, P. M., 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.
71. 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.
72. Zeman, P. & Bene, C. (2004). A tick-borne encephalitis ceiling in Central Europe has moved upwards during the last 30 years: possible impact of global warming? Int J Med Microbiol 293 (Suppl. 37), 48-54.