1887

Abstract

Tick-borne encephalitis (TBE) is a severe disease that has been endemic in north-east Italy since 1992. Over the past two decades, there has been an increase in the number of human cases reported in many European countries, including Italy. To assess the current TBE infection risk, questing ticks were collected from known TBE foci, as well as from a site in northern Italy where no human infections have been reported previously. A total of 1739 (1485 nymphs and 254 adults) was collected and analysed for TBEV prevalence by a real-time RT-PCR targeting the 3′ untranslated region. Phylogenetic analyses of the partial envelope gene were conducted on two newly sequenced TBE virus (TBEV) strains and 28 previously published sequences to investigate the genealogical relationships of the circulating TBEV strains. These phylogenetic analyses confirmed a previous report that the European TBEV subtype is the only subtype circulating within the TBE foci in north-east Italy. Interestingly, nucleotide sequence analysis revealed a high degree of divergence (mean 2.54 %) between the TBEV strains recovered in the Italian province of Trento, despite the circulation of a single TBEV subtype. This elevated genetic variability within a single TBE focus may reflect local differences in the long-standing evolutionary dynamics of TBEV at this site relative to previously characterized sites, or more recent and continuous reintroduction of various TBEV strains.

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2009-12-01
2019-11-19
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References

  1. Akaike, H. ( 1973; ). Information theory and an extension of the maximum likelihood principle. In 2nd International Symposium on Information Theory, pp. 267–281. Budapest: Akadémiai Kiadó.
  2. Beltrame, A., Ruscio, M., Cruciatti, B., Londero, A., Di Piazza, V., Copetti, R., Moretti, V., Rossi, P., Gigli, G. L. & other authors ( 2006; ). Tickborne encephalitis virus, northeastern Italy. Emerg Infect Dis 12, 1617–1619.[CrossRef]
    [Google Scholar]
  3. Cowling, D. W., Gardner, I. A. & Johnson, W. O. ( 1999; ). Comparison of methods for estimation of individual-level prevalence based on pooled samples. Prev Vet Med 39, 211–225.[CrossRef]
    [Google Scholar]
  4. Cruciatti, B., Beltrame, A., Ruscio, M., Viale, P. & Gigli, G. L. ( 2006; ). Neurological manifestation of tick-borne encephalitis in North-Eastern Italy. Neurol Sci 27, 122–124.[CrossRef]
    [Google Scholar]
  5. D'Agaro, P., Martinelli, E., Burgnich, P., Nazzi, F., Del Fabbro, S., Iob, A., Ruscio, M., Pischiutti, P. & Campello, C. ( 2009; ). Prevalence of tick-borne encephalitis virus in Ixodes ricinus from a novel endemic area of North Eastern Italy. J Med Virol 81, 309–316.[CrossRef]
    [Google Scholar]
  6. Danielová, V., Holubová, J., Pejcoch, M. & Daniel, M. ( 2002; ). Potential significance of transovarial transmission in the circulation of tick-borne encephalitis virus. Folia Parasitol (Praha) 49, 323–325.[CrossRef]
    [Google Scholar]
  7. Floris, R., Altobelli, A., Boemo, B., Mignozzi, K. & Cinco, M. ( 2006; ). First detection of TBE virus sequences in Ixodes ricinus from Friuli Venezia Giulia (Italy). New Microbiol 29, 147–150.
    [Google Scholar]
  8. 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.[CrossRef]
    [Google Scholar]
  9. Golovljova, I., Katargina, O., Geller, J., Tallo, T., Mittženkov, 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.[CrossRef]
    [Google Scholar]
  10. Gould, E. A. & Solomon, T. ( 2008; ). Pathogenic flaviviruses. Lancet 371, 500–509.[CrossRef]
    [Google Scholar]
  11. Gould, E. A., de Lamballerie, X., Zanotto, P. M. & Holmes, E. C. ( 2003; ). Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59, 277–314.
    [Google Scholar]
  12. Gritsun, T. S. & Gould, E. A. ( 1995; ). Infectious transcripts of tick-borne encephalitis virus, generated in days by RT-PCR. Virology 214, 611–618.[CrossRef]
    [Google Scholar]
  13. Gritsun, T. S., Lashkevich, V. A. & Gould, E. A. ( 2003; ). Tick-borne encephalitis. Antiviral Res 57, 129–146.[CrossRef]
    [Google Scholar]
  14. Günther, G., Haglund, M., Lindquist, L., Skoldenberg, B. & Forsgren, M. ( 1997; ). Intrathecal IgM, IgA and IgG antibody response in tick-borne encephalitis. Long-term follow-up related to clinical course and outcome. Clin Diagn Virol 8, 17–29.[CrossRef]
    [Google Scholar]
  15. Haglund, M., Vene, S., Forsgren, M., Günther, G., Johansson, B., Niedrig, M., Plyusnin, A., Lindquist, L. & Lundkvist, A. ( 2003; ). Characterisation of human tick-borne encephalitis virus from Sweden. J Med Virol 71, 610–621.[CrossRef]
    [Google Scholar]
  16. 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.[CrossRef]
    [Google Scholar]
  17. Hanada, K., Suzuki, Y. & Gojobori, T. ( 2004; ). A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Biol Evol 21, 1074–1080.[CrossRef]
    [Google Scholar]
  18. 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.
    [Google Scholar]
  19. Hudson, P. J., Rizzoli, A., Rosà, R., Chemini, C., Jones, L. D. & Gould, E. A. ( 2001; ). Tick-borne encephalitis virus in northern Italy: molecular analysis, relationships with density and seasonal dynamics of Ixodes ricinus. Med Vet Entomol 15, 304–313.[CrossRef]
    [Google Scholar]
  20. Huelsenbeck, J. P., Ronquist, F., Nielsen, R. & Bollback, J. P. ( 2001; ). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.[CrossRef]
    [Google Scholar]
  21. Labuda, M., Nuttall, P. A., Kozuch, O., Elecková, E., Williams, T., Zuffová, E. & Sabó, A. ( 1993; ). Non-viremic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49, 802–805.[CrossRef]
    [Google Scholar]
  22. 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.[CrossRef]
    [Google Scholar]
  23. Lundkvist, A., 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.[CrossRef]
    [Google Scholar]
  24. Manilla, G. ( 1998; ). Fauna d'Italia, Acari Ixodida, vol. XXXVI. Bologna, Italy: Edizioni Calderini.
  25. Marin, M. S., Zanotto, P. M., Gritsun, T. S. & Gould, E. A. ( 1995; ). Phylogeny of TYU, SRE, and CFA virus: different evolutionary rates in the genus Flavivirus. Virology 206, 1133–1139.[CrossRef]
    [Google Scholar]
  26. Melik, W., Nilsson, S. A. & Johansson, M. ( 2007; ). Detection strategies of tick-borne encephalitis virus in Swedish Ixodes ricinus reveal evolutionary characteristics of emerging tick-borne flaviviruses. Arch Virol 152, 1027–1034.[CrossRef]
    [Google Scholar]
  27. Nei, M. ( 1987; ). Molecular Evolutionary Genetics. New York: Columbia University Press.
  28. Pedrini, P., Rossi, F., Rizzolli, F. & Spina, F. ( 2008; ). Le Alpi italiane quale barriera ecologica nel corso della migrazione post-riproduttiva attraverso l'Europa. Risultati generali della prima fase del Progetto Alpi (1997–2002). Biol Cons Fauna 116, 183–184 (in Italian).
    [Google Scholar]
  29. Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. & Hudson, P. J. ( 2003; ). Empirical evidence for key hosts in persistence of a tick-borne disease. Int J Parasitol 33, 909–917.[CrossRef]
    [Google Scholar]
  30. Posada, D. & Crandall, K. A. ( 1998; ). modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef]
    [Google Scholar]
  31. Posada, D. & Crandall, K. A. ( 2001; ). Selecting the best-fit model of nucleotide substitution. Syst Biol 50, 580–601.[CrossRef]
    [Google Scholar]
  32. Randolph, S. E. ( 2006; ). EDEN – emerging diseases in a changing European environment: tick-borne diseases. Int J Med Microbiol 296 (Suppl. 1), 84–86.[CrossRef]
    [Google Scholar]
  33. Randolph, S. E., Gern, L. & Nuttall, P. A. ( 1996; ). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol Today 12, 472–479.[CrossRef]
    [Google Scholar]
  34. 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.[CrossRef]
    [Google Scholar]
  35. Randolph, S. E., Asokliene, L., Avsic-Zupanc, T., Bormane, A., Burri, C., Gern, L., Golovljova, I., Hubalek, Z., Knap, N. & other authors ( 2008; ). Variable spikes in tick-borne encephalitis incidence in 2006 independent of variable tick abundance but related to weather. Parasit Vectors 1, 44 [CrossRef]
    [Google Scholar]
  36. Rizzoli, A., Hauffe, H. C., Tagliapietra, V., Neteler, M. & Rosà, R. ( 2009; ). Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE 4, e4336 [CrossRef]
    [Google Scholar]
  37. Ronquist, F. & Huelsenbeck, J. P. ( 2003; ). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.[CrossRef]
    [Google Scholar]
  38. Rosà, R., Pugliese, A., Ghosh, M., Perkins, S. E. & Rizzoli, A. ( 2007; ). Temporal variation of Ixodes ricinus intensity on the rodent host Apodemus flavicollis in relation to local climate and host dynamics. Vector Borne Zoonotic Dis 7, 285–295.[CrossRef]
    [Google Scholar]
  39. Schrader, C. & Süss, J. ( 1999; ). A nested RT-PCR for the detection of tick-borne encephalitis virus (TBEV) in ticks in natural foci. Zentralbl Bakteriol 289, 319–328.[CrossRef]
    [Google Scholar]
  40. Schwaiger, M. & Cassinotti, P. ( 2003; ). Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol 27, 136–145.[CrossRef]
    [Google Scholar]
  41. Skarpaas, T., Golovljova, I., Vene, S., Ljøstad, U., Sjursen, H., Plyusnin, A. & Lundkvist, A. ( 2006; ). Tickborne encephalitis virus, Norway and Denmark. Emerg Infect Dis 12, 1136–1138.[CrossRef]
    [Google Scholar]
  42. Süss, J. ( 2003; ). Epidemiology and ecology of TBE relevant to the production of effective vaccines. Vaccine 21 (Suppl. 1), S19–S35.[CrossRef]
    [Google Scholar]
  43. Süss, J., Klaus, C., Diller, R., Schrader, C., Wohanka, N. & Abel, U. ( 2006; ). TBE incidence versus virus prevalence and increased prevalence of the TBE virus in Ixodes ricinus removed from humans. Int J Med Microbiol 296 (Suppl. 40), 63–68.
    [Google Scholar]
  44. Suzuki, Y. ( 2007; ). Multiple transmissions of tick-borne encephalitis virus between Japan and Russia. Genes Genet Syst 82, 187–195.[CrossRef]
    [Google Scholar]
  45. Swofford, D. ( 2003; ). paup*. Phylogenetic analysis using parsimony (* and other methods). Sunderland, MA: Sinauer Associates.
  46. Thiel, H. J., Collett, M. S., Gould, E. A., Heinz, F. X., Houghton, M., Meyers, G., Purcell, R. H. & Rice, C. ( 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. London/San Diego, CA: Elsevier/Academic Press.
  47. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  48. 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 tick-borne encephalitis virus. Emerg Infect Dis 13, 1215–1218.[CrossRef]
    [Google Scholar]
  49. Weaver, S. C. ( 2006; ). Evolutionary influences in arboviral disease. Curr Top Microbiol Immunol 299, 285–314.
    [Google Scholar]
  50. Xu, G., Fang, Q. Q., Sun, Y., Keirans, J. E. & Durden, L. A. ( 2005; ). Hard tick calreticulin (CRT) gene coding regions have only one intron with conserved positions and variable sizes. J Parasitol 91, 1326–1331.[CrossRef]
    [Google Scholar]
  51. 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.[CrossRef]
    [Google Scholar]
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