Tick-borne encephalitis (TBE) is a serious acute neuroinfection of humans caused by a tick-borne flavivirus. The disease is typically seasonal, linked to the host-seeking activity of Ixodes ricinus (predominantly nymphs), the principal European tick vector species. To address the need for accurate risk predictions of contracting TBE, data on 4,044 TBE cases reported in the Czech Republic during 2001-2006 were compared with questing activity of I. ricinus nymphs monitored weekly at a defined location for the same 6-year period. A time shift of 21 days between infected tick bite and recorded disease onset provided the optimal model for comparing the number of cases of TBE with numbers of questing nymphs. Mean annual distribution of TBE cases and tick counts showed a similar bimodal distribution. Significantly, the ratio of TBE cases to questing nymphs was highest in the summer-autumn period even though the number of questing nymphs peaked in the spring-summer period. However, this pattern changed during a period of extreme meteorological events of flooding and abnormally high temperatures, indicating that changes in climate affect the incidence of TBE. Previous studies failed to link human behavior with changes in incidence of TBE but showed extrinsic temperature impacts arbovirus replication. Hence, we hypothesize the apparent discrepancy between peak nymphal tick activity and greatest risk of contracting TBE is due to the effect of temperature on virus replication in the tick vector. Relative proportions of questing nymphs and the numbers of weeks in which they were found were greater in summer-autumn compared with spring-summer at near-ground temperatures >5°C and at standard day and weekly average temperatures of >15°C. Thus, during the summer-autumn period, the virus dose in infected tick bites is likely greater owing to increased virus replication at higher microclimatic temperatures, consequently increasing the relative risk of contracting TBE per summer-autumn tick bite. The data support the use of weather-based forecasts of tick attack risk (based on daytime ambient temperature) supplemented with weekly average temperature (as a proxy for virus replication) to provide much-needed real-time forecasts of TBE risk.

3rd Medical Faculty Charles University Prague Czechia

Centre for Ecology and Hydrology Wallingford United Kingdom

Centre for Epidemiology and Microbiology National Institute of Public Health Prague Czechia

Department of Biostatistics National Institute of Public Health Prague Czechia

Department of Zoology University of Oxford Oxford United Kingdom

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Amato-Gauci A., Zeller H. (2012). Tick-borne encephalitis joins the diseases under surveillance in the European Union. Euro. Surveill. 17:20299. 10.2807/ese.17.42.20299-en PubMed DOI

Bedjanič M., Rus S., Kmet J., Vesenjak-Zmijanac J. (1955). Virus meningo-encephalitis in Slovenia. Bull. World Health Organ. 12, 503–512. PubMed PMC

Brabec M., Daniel M., Malý M., Danielová V., Kříž B., Kott I., et al. (2017). Analysis of meterological effects on the incidence of tick-borne encephalitis in the Czech Republic over a thirty-year period. Virol. Res. Rev. 1, 2–8. 10.15761/VRR.1000103 DOI

Carpenter S., Wilson A., Barber J., Veronesi E., Mellor P., Venter G., et al. . (2011). Temperature dependence of the extrinsic incubation period of orbiviruses in Culicoides biting midges. PLoS ONE 6:e27987. 10.1371/journal.pone.0027987 PubMed DOI PMC

Daniel M., Beneš Č., Danielová V., Kříž 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. Immunol. 60, 135–155. PubMed

Daniel M., Danielová V., Kříž B., Ružek D., Fialová A., Malý M., et al. . (2016). The occurrence of Ixodes ricinus tick and important tick-borne pathogens in areas with high tick-borne encephalitis prevalence in different altitudinal levels of the Czech Republic. Part, I. Ixodes ricinus ticks and tick-borne encephalitis virus. Epidemiol. Microbiol. Immunol. 65, 118–128. PubMed

Daniel M., Dusbábek F. (1994). Micrometeorological and microhabitat factors affecting maintenance and dissemination of tick-borne diseases in the environment, in Ecological Dynamics of Tick-Borne Zoonoses, eds Sonenshine D. E., Mather T. N. (Oxford: Oxford University Press; ), 91–138.

Daniel M., Kříž B., Danielová V., Valter J., Kott I. (2008). Correlation between meteorological factors and tick-borne encephalitis in the Czech Republic. Parasitol. Res. 103(Suppl. 1), S97–S107. 10.1007/s00436-008-1061-x PubMed DOI

Daniel M., Malý M., Danielová V., Kříž B., Nuttall P. A. (2015). Abiotic predictors and annual seasonal dynamics of Ixodes ricinus, the major disease vector of Central Europe. Parasit. Vectors 8:478. 10.1186/s13071-015-1092-y PubMed DOI PMC

Daniel M., Vráblík T., Valter J., Kříž B., Danielová V. (2010). The TICKPRO computer program for predicting Ixodes ricinus host-seeking activity and the warning system published on websites. Cent. Eur. J. Pub. Health 18, 230–236. PubMed

Daniel M., Zitek K., Danielová V., Kříž B., Valter J., Kott I. (2006). Risk assessment and prediction of Ixodes ricinus tick questing activity and human tick-borne encephalitis infection in space and time in the Czech Republic. Int. J. Med. Microbiol. 296(Suppl. 40), 41–47. 10.1016/j.ijmm.2006.02.008 PubMed DOI

Danielová V. (1975). Growth of Tahyna virus at low temperatures. Acta Virol. 19, 327–332. PubMed

Danielová V. (1990). Experimental infection of ticks Ixodes ricinus with tick-borne encephalitis virus under different microclimatic conditions. Folia Parasit. 37, 279–282. PubMed

Danielová V., Daniel M., Holubová J., Hájková Z., Albrecht V. (1983). Influence of microclimatic factors on the development and virus infection rate of ticks Ixodes ricinus L. under experimental conditions. Folia Parasit. 30, 153–161.

Dohm D. J., O'Guinn M. L., Turell M. (2002). Effect of environmental temperature on the ability of Culex pipiens (Diptera: Culicidae) to transit West Nile virus. J. Med. Entomol. 39, 221–225. 10.1603/0022-2585-39.1.221 PubMed DOI

Draganescu N. (1959). Inframicrobial meningoencephalitis belonging to the group transmitted by arthropods. Identification of the pathogenic agent and study of the nerve lesions induced in white mice [In Romanian]. Stud. Tercet. Inframicrobiol. 10, 363–369. PubMed

Duniewiecz M. (1999). Central European Tick-borne encephalitis, in Neuroinfection, eds Duniewiecz M., Adam P. (Prague: Maxdorf; ), 119–127.

European Centre for Disease Prevention Control (2016). Annual Epidemiological Report 2016 – Tick-borne Encephalitis. Stockholm: ECDC; Available online at: https://ecdc.europa.eu/en/tick-borne-encephalitis/surveillance-and-disease-data/annual-epidemiological-report (Accessed March 14, 2018).

Fomsgaard A., Christiansen C., Bodker R. (2009). First identification of tick-borne encephalitis in Denmark outside of Bornholm, August 2009. Euro. Surveill. 14:19325. 10.2807/ese.14.36.19325-en PubMed DOI

Fornosi F., Molnár E. (1952). Meningoencephalitis in Hungary [In Hungarian]. Orv. Hetil. 93, 993–996. PubMed

Gallia F., Rampas J., Hollender L. (1949). Laboratory infection with encephalitis virus [In Czech]. Cas. Lék. Ces. 88, 224–229.

Heinz F. X., Stiasny K., Holzmann H., Grgic-Vitek M., Kříž B., Essl A., et al. . (2013). Vaccination and tick-borne encephalitis, Central Europe. Emerg. Infect. Dis. 19, 69–76. 10.3201/eid1901.120458 PubMed DOI PMC

Hladný J., Krátká M., Kašpárek L. (eds.). (2004). August 2002 Catastrophic Flood in the Czech Republic. Prague: Ministry of Environment of the Czech Republic; ), 1–48. ISBN 80-7212-343-2.

Johan F., Åsa L., Rolf A., Barbro C., Ingvar E., Mats H., et al. . (2006). Tick-borne encephalitis (TBE) in Skåne, southern Sweden: a new TBE endemic region? Scand. J. Infect. Dis. 38, 800–804. 10.1080/00365540600664068 PubMed DOI

Kaäriainen L. E., Hirvonen E., Oker-Blom N. (1961). Geographical distribution of biphasic tick-borne encephalitis in Finland. Ann. Med. Exp. Fenn. 39, 316–328.

Korenberg E. I. (2000). Seasonal population dynamics of Ixodes ticks and tick-borne encephalitis virus. Exp. Appl. Acarol. 24, 665–681. 10.1023/A:1010798518261 PubMed DOI

Korenberg E. I., Kovalevskii Yu. V. (1994). Variation in parameters affecting risk of human disease due to TBE virus. Folia Parasit. 42, 307–312. PubMed

Korenberg E. I., Kovalevskii Y. V. (1999). Main features of tick-borne encephalitis eco-epidemiology in Russia. Zent. Bakteriol. 289, 525–539. 10.1016/S0934-8840(99)80006-1 PubMed DOI

Krejčí J. (1949). Isolement d'un virus nouveau en course d'une épidemie de meningoencephalitides dans le région de Vyškov (Moravie) [In French]. Presse méd. 74:1084. PubMed

Kříž B., Benes C., Daniel M. (2009). Alimentary transmission of tick-borne encephalitis in the Czech Republic (1997-2008). Epidemiol. Mikrobiol. Imunol. 58, 98–103. PubMed

Kříž B., Kott I., Daniel M., Vráblík T., Beneš C. (2015). Impact of climate changes on the incidence of tick-borne encephalitis in the Czech Republic in 1982-2011 [In Czech]. Epidemiol. Mikrobiol. Imunol. 64, 24–32. PubMed

Kříž B., Malý M., Beneš C., Daniel M. (2012). Epidemiology of tick-borne encephalitis in the Czech Republic 1970-2008. Vector Borne Zoon. Dis. 12, 994–999. 10.1089/vbz.2011.0900 PubMed DOI PMC

Lindblom P., Wilhelmsson P., Fryland L., Sjöwall J., Haglund M., Matussek A., et al. . (2013). Tick-borne encephalitis virus in ticks detached from humans and follow-up of serological and clinical response. Ticks Tick Borne Dis. 5, 21–28. 10.1016/j.ttbdis.2013.07.009 PubMed DOI

Luňáčková J., Chmelík V., Šípová L., Žampachová E., Bečvářová J. (2003). Epidemiologické sledování klíštové encefalitidy v jižních Čechách (Epidemiological survey of tick-borne encephalitis in Southern Bohemia) [In Czech]. Epidemiol. Mikrobiol. Imunol. 52, 51–58. PubMed

Mellor P. S., Leake C. J. (2000). Climatic and geographic influences on arboviral infections and vectors. Rev. Sci. Tech. Off. Int. Epiz. 19, 41–54. 10.20506/rst.19.1.1211 PubMed DOI

Menne B., Ebi K. L. eds. (2006). Climate Change and Adaptation Strategies for Human Health. Darmstadt: Steinkopff Verlag.

Oker-Blom N. (1956). Kumlinge disease; a meningo-encephalitis occurring in the Aaland Islands. Ann. Med. Exp. Biol. Fenn. 34, 309–318. PubMed

Pattyn S. R., Wyler R. (1955). Viral meningoencephalitis in Austria. IV. Virus in blood in experimental infection; attempted transmission by mosquitoes [In French]. Bull. World Health Organ. 12, 581–589. PubMed PMC

Penyevskaya N. A. (2008). Methodological approach to the estimation of efficacy of etiotropic immunoprophylaxis in tick-borne encephalitis [In Russian]. Clin. Microbiol. Chemother. 10, 70–84.

Prymula R. (2015). Prevention possibilities and vaccination against tick-borne encephalitis, in Klíšt'ová encefalitida (Tick-Borne Encephalitis), ed Ružek D. (Prague: Grada Publishing a.s.), 155–172.

Przesmycki F., Taytsch Z., Semkow R., Walentynowicz-Stanczyk R. (1954). Research on the tick-borne encephalitis; I. Biology of the tick-borne encephalitis viral strains isolated in Poland [In Polish]. Przegl. Epidemiol. 8, 205–214. PubMed

R Core Team (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, Available online at: http://www.R-project.org/

Rampas J., Gallia F. (1949). Isolation of an encephalitis virus from Ixodes ricinus ticks [In Czech]. Cas. Lék. Ces. 88, 1179–1180.

Raška K., Bárdoš V. (1954). Epidemiology of the Czechoslovak tick-borne encephalitis, in Československá klíšt'ová encefalitis (Czechoslovak Tick-Borne Encephalitis), ed Raška K. (Prague: Státní zdravotnické nakladatelství Publishing House; ), 65–77.

Rebetez M., Dupont O., Giroud M. (2009). An analysis of the July 2006 heatwave extent in Europe compared to the record year of 2003. Theor. Appl. Climatol. 95, 1–7. 10.1007/s00704-007-0370-9 DOI

Ružek D. ed. (2015). Klíšt’ová encefalitida (Tick-Borne Encephalitis). Prague: Grada Publishing a.s.

Sinnecker H. (1960). Zecken encephalitis in Deutschland [In German]. Zbl. Bact. Orig. 180, 12–18.

Skarpaas T., Ljøstad U., Sundøy A. (2004). First human cases of tickborne encephalitis, Norway. Emerg. Infect. Dis. 10, 2241–2243. 10.3201/eid1012.040598 PubMed DOI PMC

Vaptsarov I., Turpomanov A., Spasov Z., Nikov D., Dragiev M. (1954). Recurrent viral meningoencephalitis in southern Bulgaria [In Bulgarian]. Suvr. Med. (Sofia) 5, 86–103. PubMed

Watts D. M., Burke D. S., Harrison B. A., Whitmire R. E., Nisalak A. (1987). Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. Am. J. Trop. Med. Hyg. 36, 143–152. 10.4269/ajtmh.1987.36.143 PubMed DOI

Spatiotemporal spread of tick-borne encephalitis in the EU/EEA, 2012 to 2020

History of Arbovirus Research in the Czech Republic