{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,3]],"date-time":"2026-03-03T02:24:17Z","timestamp":1772504657753,"version":"3.50.1"},"reference-count":38,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2019,11,15]],"date-time":"2019-11-15T00:00:00Z","timestamp":1573776000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Tick-borne encephalitis exhibits profound inter-annual fluctuations in incidence. Previous studies showed that three-fifths of the variation can be explained in terms of four superimposed oscillations: a quasi-biennial, triennial, pentennial, and a decadal cycle. This study was conducted to determine how these cycles could be influenced by climate change. Epidemiological data, spanning from the 1970s to the present, and originating from six regions\/countries bridging Scandinavia and the Mediterranean, represented a temporal\/latitudinal gradient. Spectral analysis of time series was used to determine variation in the cycles\u2019 length\/amplitude with respect to these gradients. The analysis showed that\u2014whereas the lengths of the shorter cycles do not vary substantially\u2014cycles in the decadal band tend to be longer southwards. When comparing the disease\u2019s oscillations before- and after the mid-1990s, a shift towards longer oscillations was detected in the pentennial\u2013decadal band, but not in the biennial\u2013 triennial band. Simultaneously, oscillations in the latter band increased in intensity whereas the decadal oscillations weakened. In summary, the rhythm of the cycles has been altered by climate change. Lengthened cycles may be explained by prolonged survival of some animal hosts, and consequently greater inertia in herd immunity changes, slowing down a feedback loop between the herd immunity and amount of virus circulating in nature.<\/jats:p>","DOI":"10.3390\/ijerph16224532","type":"journal-article","created":{"date-parts":[[2019,11,15]],"date-time":"2019-11-15T11:24:32Z","timestamp":1573817072000},"page":"4532","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Prolongation of Tick-Borne Encephalitis Cycles in Warmer Climatic Conditions"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3516-7690","authenticated-orcid":false,"given":"Petr","family":"Zeman","sequence":"first","affiliation":[{"name":"Medical Laboratories, Konevova 205, 130 00 Prague, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,11,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/j.idc.2008.03.013","article-title":"Tick-borne encephalitis","volume":"22","author":"Kaiser","year":"2008","journal-title":"Infect. Dis. Clin. N. Am."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Beaut\u00e9, J., Spiteri, G., Warns-Petit, E., and Zeller, H. (2018). Tick-borne encephalitis in Europe, 2012 to 2016. Euro Surveill., 23.","DOI":"10.2807\/1560-7917.ES.2018.23.45.1800201"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S0166-3542(02)00206-1","article-title":"Tick-borne encephalitis","volume":"57","author":"Gritsun","year":"2003","journal-title":"Antivir. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"S19","DOI":"10.1016\/S0264-410X(02)00812-5","article-title":"Epidemiology and ecology of TBE relevant to the production of effective vaccines","volume":"21","author":"Suess","year":"2003","journal-title":"Vaccine"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"430","DOI":"10.12998\/wjcc.v3.i5.430","article-title":"Tick-borne encephalitis: A review of epidemiology, clinical characteristics, and management","volume":"3","author":"Bogovic","year":"2015","journal-title":"J. Clin. Cases"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.antiviral.2019.01.014","article-title":"Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines","volume":"164","author":"Ruzek","year":"2019","journal-title":"Antivir. Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"366","DOI":"10.3109\/00365548.2011.552072","article-title":"Forecasting risk of tick-borne encephalitis (TBE): Using data from wildlife and climate to predict next year\u2019s number of human victims","volume":"43","author":"Haemig","year":"2011","journal-title":"Scand. J. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1089\/vbz.2013.1386","article-title":"Tick-borne encephalitis transmission risk: Its dependence on host population dynamics and climate effects","volume":"14","author":"Palo","year":"2014","journal-title":"Vector Borne Zoon. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1007\/s10493-018-0267-6","article-title":"Forecasting next season\u2019s Ixodes ricinus nymphal density: The example of southern Germany 2018","volume":"75","author":"Brugger","year":"2018","journal-title":"Exp. Appl. Acarol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1017\/S0950268816002223","article-title":"Cyclic patterns in the central European tick-borne encephalitis incidence series","volume":"145","author":"Zeman","year":"2017","journal-title":"Epidemiol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2781","DOI":"10.1017\/S0950268817001662","article-title":"Predictability of tick-borne encephalitis fluctuations","volume":"145","author":"Zeman","year":"2017","journal-title":"Epidemiol. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Cazelles, B., Chavez, M., McMichael, A.J., and Hales, S. (2005). Nonstationary influence of El Ni\u00f1o on the synchronous dengue epidemics in Thailand. PLoS Med., 2.","DOI":"10.1371\/journal.pmed.0020106"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Kreppel, K.S., Caminade, C., Telfer, S., Rajerison, M., Rahalison, L., Morse, A., and Baylis, M. (2014). A Non-Stationary Relationship between Global Climate Phenomena and Human Plague Incidence in Madagascar. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0003155"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"8041","DOI":"10.1073\/pnas.1701777114","article-title":"Interannual cycles of Hantaan virus outbreaks at the human\u2013animal interface in Central China are controlled by temperature and rainfall","volume":"114","author":"Tian","year":"2017","journal-title":"PNAS"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.tree.2007.10.010","article-title":"Collapsing population cycles","volume":"23","author":"Ims","year":"2007","journal-title":"Trends Ecol. Evol."},{"key":"ref_16","unstructured":"ISW-TBE (2002, April 15). International Scientific Working Group on TBE. Available online: http:\/\/www.tbe-info.com."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Lundkvist, A., Wallensten, A., Vene, S., and Hjertqvist, M. (2011). Tick-borne encephalitis increasing in Sweden, 2011. Euro Surveill., 16.","DOI":"10.2807\/ese.16.39.19981-en"},{"key":"ref_18","first-page":"69","article-title":"Tick-borne encephalitis (TBE) in Germany\u2014Epidemiological data, development of risk areas and virus prevalence in field-collected ticks and in ticks removed from humans","volume":"293","author":"Suess","year":"2004","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_19","unstructured":"PFIZER (2018, March 11). FSME Erkrankungsf\u00e4lle in \u00d6sterreich. Available online: https:\/\/www.pfizer.at\/fileadmin\/content\/Content\/04_Presse\/04.3_Pressemappen\/FSME_in_Oesterreich\/FSME_Situationsbericht_2017_Endversion.pdf."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Rezza, G., Farchi, F., Pezzott, P., Ruscio, M., Lo Presti, A., Ciccozzi, M., Mondardini, V., Paternoster, C., Bassetti, M., and Merelli, M. (2015). Tick-borne encephalitis in north-east Italy: A 14-year retrospective study, January 2000 to December 2013. Euro Surveill., 20.","DOI":"10.2807\/1560-7917.ES.2015.20.40.30034"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1098\/rspa.1998.0193","article-title":"The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis","volume":"454","author":"Huang","year":"1998","journal-title":"Proc. R. Soc. Lond. Ser. A"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1175\/1520-0477(1998)079<0061:APGTWA>2.0.CO;2","article-title":"A practical guide to wavelet analysis","volume":"79","author":"Torrence","year":"1998","journal-title":"Bull. Am. Meteorol. Soc."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"40","DOI":"10.32614\/RJ-2009-002","article-title":"EMD: A package for empirical mode decomposition and Hilbert spectrum","volume":"1","author":"Donghoh","year":"2009","journal-title":"R J."},{"key":"ref_24","unstructured":"Roesch, A., and Schmidbauer, H. (2018, March 18). WaveletComp 1.1: A guided tour through the R package. Available online: http:\/\/www.hs-stat.com\/projects\/WaveletComp\/WaveletComp_guided_tour.pdf."},{"key":"ref_25","unstructured":"EDJNet (2019, August 23). Europe one degree warmer. Available online: https:\/\/www.onedegreewarmer.eu."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"24","DOI":"10.2807\/ese.15.27.19606-en","article-title":"Human activities predominate in determining changing incidence of tick-borne encephalitis in Europe","volume":"15","author":"Randolph","year":"2010","journal-title":"Euro Surveill."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1186\/s13071-018-3057-4","article-title":"The importance of wildlife in the ecology and epidemiology of the TBE virus in Sweden: Incidence of human TBE correlates with abundance of deer and hares","volume":"11","author":"Jaenson","year":"2018","journal-title":"Parasit. Vectors"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s10654-004-6518-3","article-title":"North Atlantic weather oscillation and human infectious diseases in the Czech Republic, 1951-2003","volume":"20","author":"Hubalek","year":"2005","journal-title":"Eur. J. Epidemiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1111\/j.1365-3024.1995.tb00887.x","article-title":"Clethrionomys glareolus, but not Apodemus flavicollis, acquires resistance to lxodes ricinus L, the main European vector of Borrelia burgdorferi","volume":"17","author":"Dizij","year":"1995","journal-title":"Parasit. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1006\/jtbi.1995.0158","article-title":"Trends and oscillations in tick population dynamics","volume":"175","author":"Awerbuch","year":"1995","journal-title":"J. Theor. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1007\/s00285-014-0845-0","article-title":"Delay differential systems for tick population dynamics","volume":"71","author":"Fan","year":"2015","journal-title":"J. Math. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41426-018-0149-3","article-title":"Seroprevalence of TBEV in bank voles from Poland\u2014A long-term approach","volume":"7","author":"Grzybek","year":"2018","journal-title":"Emerg. Microb. Infect."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1017\/S0950268800058477","article-title":"Roe deer as sentinels for endemicity of tick-borne encephalitis virus","volume":"115","author":"Gerth","year":"1995","journal-title":"Epidemiol. Infect."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1016\/j.ttbdis.2014.07.021","article-title":"Range expansion of Ixodes ricinus to higher altitude, and co-infestation of small rodents with Dermacentor marginatus in the Northern Apennines, Italy","volume":"5","author":"Martello","year":"2014","journal-title":"Ticks Tick Borne Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/1756-3305-5-8","article-title":"Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden","volume":"5","author":"Jaenson","year":"2012","journal-title":"Parasit. Vectors"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1002\/ecm.1250","article-title":"Migration in geographic and ecological space by a large herbivore","volume":"87","author":"Peters","year":"2017","journal-title":"Ecol. Monogr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1002\/jwmg.1029","article-title":"Beyond climate envelope projections: Roe deer survival and environmental change","volume":"80","author":"Davis","year":"2016","journal-title":"J. Wildl. Manag."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1111\/ele.12059","article-title":"How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer","volume":"16","author":"Gaillard","year":"2013","journal-title":"Ecol. Lett."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/16\/22\/4532\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:34:56Z","timestamp":1760189696000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/16\/22\/4532"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,15]]},"references-count":38,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2019,11]]}},"alternative-id":["ijerph16224532"],"URL":"https:\/\/doi.org\/10.3390\/ijerph16224532","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,15]]}}}