Clinical Characteristics of Patients with Tick-Borne Encephalitis (TBE): A European Multicentre Study from 2010 to 2017
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
Land Steiermark (Office of the regional government of Styria, department of health, care and science, unit science and research, Austria)
NV19-05-00457
Czech Ministry of Health
P3-0296
Slovenian Research Agency
PubMed
34209373
PubMed Central
PMC8306415
DOI
10.3390/microorganisms9071420
PII: microorganisms9071420
Knihovny.cz E-zdroje
- Klíčová slova
- central paresis, meningomyelitis, peripheral paresis, tick-borne encephalitis, vaccine-preventable disease,
- Publikační typ
- časopisecké články MeSH
Tick-borne encephalitis (TBE) virus is a major cause of central nervous system infections in endemic countries. Here, we present clinical and laboratory characteristics of a large international cohort of patients with confirmed TBE using a uniform clinical protocol. Patients were recruited in eight centers from six European countries between 2010 and 2017. A detailed description of clinical signs and symptoms was recorded. The obtained information enabled a reliable classification in 553 of 555 patients: 207 (37.3%) had meningitis, 273 (49.2%) meningoencephalitis, 15 (2.7%) meningomyelitis, and 58 (10.5%) meningoencephalomyelitis; 41 (7.4%) patients had a peripheral paresis of extremities, 13 (2.3%) a central paresis of extremities, and 25 (4.5%) had single or multiple cranial nerve palsies. Five (0.9%) patients died during acute illness. Outcome at discharge was recorded in 298 patients. Of 176 (59.1%) patients with incomplete recovery, 80 (27%) displayed persisting symptoms or signs without recovery expectation. This study provides further evidence that TBE is a severe disease with a large proportion of patients with incomplete recovery. We suggest monitoring TBE in endemic European countries using a uniform protocol to record the full clinical spectrum of the disease.
Department of General Paediatrics Medical University of Graz 8036 Graz Austria
Department of Infectious Diseases Hospital Ceske Budejovice 370 01 Ceske Budejovice Czech Republic
Department of Infectious Diseases Lithuanian University of Health Sciences 44307 Kaunas Lithuania
Department of Infectious Diseases University Medical Centre Ljubljana 1000 Ljubljana Slovenia
Department of Neurology Medical University of Graz 8036 Graz Austria
Deptartment of Infectious Diseases University Hospital Brno 625 00 Brno Czech Republic
Zobrazit více v PubMed
The European Comission . Commission Implementing Decision (EU) 2018/945 of 22 June 2018 on the Communicable Diseases and Related Special Health Issues to Be Covered by Epidemiological Surveillance as Well as Relevant Case Definitions. The Publications Office of the European Union; Luxembourg: 2018. pp. 1–74.
Süss J. Tick-borne encephalitis 2010: Epidemiology, risk areas, and virus strains in Europe and Asia-an overview. Ticks Tick. Borne. Dis. 2011;2:2–15. doi: 10.1016/j.ttbdis.2010.10.007. PubMed DOI
Bogovič P., Lotrič-Furlan S., Avšič-Županc T., Lusa L., Strle F. Factors associated with severity of tick-borne encephalitis: A prospective observational study. Travel Med. Infect. Dis. 2018;26:25–31. doi: 10.1016/j.tmaid.2018.10.003. PubMed DOI
Radzišauskienė D., Žagminas K., Ašoklienė L., Jasionis A., Mameniškienė R., Ambrozaitis A., Jančorienė L., Jatužis D., Petraitytė I., Mockienė E. Epidemiological patterns of tick-borne encephalitis in Lithuania and clinical features in adults in the light of the high incidence in recent years: A retrospective study. Eur. J. Neurol. 2018;25:268–274. doi: 10.1111/ene.13486. PubMed DOI PMC
Czupryna P., Grygorczuk S., Krawczuk K., Pancewicz S., Zajkowska J., Dunaj J., Matosek A., Kondrusik M., Moniuszko-Malinowska A. Sequelae of tick-borne encephalitis in retrospective analysis of 1072 patients. Epidemiol. Infect. 2018;146:1663–1670. doi: 10.1017/S0950268818002005. PubMed DOI PMC
Haglund M., Forsgren M., Lindh G., Lindquist L. 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. 1996;28:217–224. doi: 10.3109/00365549609027160. PubMed DOI
Kaiser R. The clinical and epidemiological profile of tick-borne encephalitis in southern Germany A prospective study of 656 patients. Brain. 1999;122:2067–2078. doi: 10.1093/brain/122.11.2067. PubMed DOI
Haglund M., Günther G. Tick-borne encephalitis—Pathogenesis, clinical course and long-term follow-up. Vaccine. 2003;21:S11–S18. doi: 10.1016/S0264-410X(02)00811-3. PubMed DOI
Kaiser R. Tick-borne encephalitis: Clinical findings and prognosis in adults. Wien. Med. Wochenschr. 2012;162:239–243. doi: 10.1007/s10354-012-0105-0. PubMed DOI
Karelis G., Bormane A., Logina I., Lucenko I., Suna N., Krumina A., Donaghy M. Tick-borne encephalitis in Latvia 1973–2009: Epidemiology, clinical features and sequelae. Eur. J. Neurol. 2012;19:62–68. doi: 10.1111/j.1468-1331.2011.03434.x. PubMed DOI
Rezza G., Farchi F., Pezzotti P., Ruscio M., Lo Presti A., Ciccozzi M., Mondardini V., Paternoster C., Bassetti M., Merelli M., et al. Tick-borne encephalitis in north-east Italy: A 14-year retrospective study, January 2000 to December 2013. Eurosurveillance. 2015;20:30034. doi: 10.2807/1560-7917.ES.2015.20.40.30034. PubMed DOI
Kunze U., Kunze M. The Austrian vacccination paradox:Tick-borne encaphilitis vaccination versus influenza vaccination. Cent. Eur. J. Public Health. 2015;23:223–226. doi: 10.21101/cejph.a4169. PubMed DOI
Nah K., Bede-Fazekas Á., Trájer A.J., Wu J. The potential impact of climate change on the transmission risk of tick-borne encephalitis in Hungary. BMC Infect. Dis. 2020;20:34. doi: 10.1186/s12879-019-4734-4. PubMed DOI PMC
Heinz F.X., Stiasny K., Holzmann H., Grgic-Vitek M., Kriz B., Essl A., Kundi M. Vaccination and tick-borne encephalitis, central Europe. Emerg. Infect. Dis. 2013;19:69–76. doi: 10.3201/eid1901.120458. PubMed DOI PMC
Lenhard T., Ott D., Jakob N.J., Martinez-Torres F., Grond-Ginsbach C., Meyding-Lamadé U. Clinical outcome and cerebrospinal fluid profiles in patients with tick-borne encephalitis and prior vaccination history. Ticks Tick-Borne Dis. 2018;9:882–888. doi: 10.1016/j.ttbdis.2018.02.021. PubMed DOI
Günther G., Haglund M., Lindquist L., Forsgren M., Sköldenberg B. Tick-borne encephalitis in Sweden in relation to aseptic meningo-encephalitis of other etiology: A prospective study of clinical course and outcome. J. Neurol. 1997;244:230–238. doi: 10.1007/s004150050077. PubMed DOI
Duniewicz M., Mertenová J., Moravcová E., Jelinková E., Holý M., Kulková H., Doutlik S. Central european tick-borne encephalitis from 1969 to 1972 in central bohemia (author’s transl.) Infection. 1975;3:223–228. doi: 10.1007/BF01642770. PubMed DOI
Ackermann R., Rehse-Küpper B. Central European encephalitis in the Federal Republic of Germany (author’s transl.) Fortschr. Neurol. Psychiatr. Grenzgeb. 1979;47:103–122. PubMed
Kaiser R. Tick-borne encephalitis in southwestern Germany. Infection. 1996;24:398–399. doi: 10.1007/BF01716094. PubMed DOI
Kaiser R. Tick-borne encephalitis (TBE) in Germany and clinical course of the disease. Int. J. Med. Microbiol. 2002;291:58–61. doi: 10.1016/S1438-4221(02)80012-1. PubMed DOI
Grygorczuk S., Mierzynska D., Zdrodowska A., Zajkowska J., Pancewicz S., Kondrusik M., Swierzbinska R., Pryszmont J., Hermanowska-Szpakowicz T. Tick-borne Encephalitis in North-eastern Poland in 1997–2001: A Retrospective Study. Scand. J. Infect. Dis. 2002;34:904–909. doi: 10.1080/0036554021000026979. PubMed DOI
Zimmermann H., Koch D. Epidemiologie der frühsommer-meningoenzephalitis (FSME) in der Schweiz 1984 bis 2004. Ther. Umschau. 2005;62:719–725. doi: 10.1024/0040-5930.62.11.719. PubMed DOI
Hansmann Y., Gut J.P., Remy V., Martinot M., Allard Witz M., Christmann D. Tick-borne encephalitis in eastern France. Scand. J. Infect. Dis. 2006;38:520–526. doi: 10.1080/00365540600585073. PubMed DOI
Logar M., Bogovič P., Cerar D., Avšič-Zǔpanc T., Strle F. Tick-borne encephalitis in Slovenia from 2000 to 2004: Comparison of the course in adult and elderly patients. Wien. Klin. Wochenschr. 2006;118:702–707. doi: 10.1007/s00508-006-0699-6. PubMed DOI
Czupryna P., Moniuszko A., Pancewicz S.A., Grygorczuk S., Kondrusik M., Zajkowska J. Tick-borne encephalitis in Poland in years 1993–2008—Epidemiology and clinical presentation. A retrospective study of 687 patients. Eur. J. Neurol. 2011;18:673–679. doi: 10.1111/j.1468-1331.2010.03278.x. PubMed DOI
Hellenbrand W., Kreusch T., Böhmer M.M., Wagner-Wiening C., Dobler G., Wichmann O., Altmann D. Epidemiology of Tick-Borne Encephalitis (TBE) in Germany, 2001–2018. Pathogens. 2019;8:42. doi: 10.3390/pathogens8020042. PubMed DOI PMC
Krawczuk K., Czupryna P., Pancewicz S., Ołdak E., Moniuszko-Malinowska A. Comparison of tick-borne encephalitis between children and adults—Analysis of 669 patients. J. Neurovirol. 2020;26:565–571. doi: 10.1007/s13365-020-00856-x. PubMed DOI PMC
Lesnicar G., Poljak M., Seme K., Lesnicar J. Pediatric tick-borne encephalitis in 371 cases from an endemic region in Slovenia, 1959 to 2000. Pediatr. Infect. Dis. J. 2003;22:612–617. doi: 10.1097/00006454-200307000-00009. PubMed DOI
Fritsch P., Gruber-Sedlmayr U., Pansi H., Zöhrer B., Mutz I., Spork D., Zenz W. Tick-borne encephalitis in Styrian children from 1981 to 2005: A retrospective study and a review of the literature. Acta Paediatr. 2008;97:535–538. doi: 10.1111/j.1651-2227.2008.00763.x. PubMed DOI
Stähelin-Massik J., Zimmermann H., Gnehm H.E. Tick-Borne Encephalitis in Swiss Children 2000–2004. Pediatr. Infect. Dis. J. 2008;27:555–557. doi: 10.1097/INF.0b013e318165c195. PubMed DOI
Krbková L., Štroblová H., Bednářová J. Clinical course and sequelae for tick-borne encephalitis among children in South Moravia (Czech Republic) Eur. J. Pediatr. 2015;174:449–458. doi: 10.1007/s00431-014-2401-8. PubMed DOI
Wahlberg P., Saikku P., Brummer-Korvenkontio M. Tick-borne viral encephalitis in Finland. The clinical features of Kumlinge disease during 1959–1987. J. Intern. Med. 1989;225:173–177. doi: 10.1111/j.1365-2796.1989.tb00059.x. PubMed DOI
Holmgren E.B., Forsgren M. Epidemiology of tick-borne encephalitis in Sweden 1956–1989: A study of 1116 cases. Scand. J. Infect. Dis. 1990;22:287–295. doi: 10.3109/00365549009027050. PubMed DOI
Mickienė A., Laiškonis A., Günther G., Vene S., Lundkvist Å., Lindquist L. Tickborne Encephalitis in an Area of High Endemicity in Lithuania: Disease Severity and Long-Term Prognosis. Clin. Infect. Dis. 2002;35:650–658. doi: 10.1086/342059. PubMed DOI
Hansson M.E.A., Orvell C., Engman M.-L., Wide K., Lindquist L., Lidefelt K.-J., Sundin M. Tick-borne encephalitis in childhood: Rare or missed? Pediatr. Infect. Dis. J. 2011;30:355–357. doi: 10.1097/INF.0b013e3181fe3b5a. PubMed DOI
Wahlberg P., Carlsson S.A., Granlund H., Jansson C., Lindén M., Nyberg C., Nyman D. TBE in Åland Islands 1959–2005: Kumlinge disease. Scand. J. Infect. Dis. 2006;38:1057–1062. doi: 10.1080/00365540600868297. PubMed DOI
Köck T., Stünzner D., Freidl W., Pierer K. Clinical aspects of early summer meningoencephalitis in Styria. Nervenarzt. 1992;63:205–208. PubMed
Kaiser R., Vollmer H., Schmidtke K., Rauer S., Berger W., Gores D. Verlauf und Prognose der FSME. Nervenarzt. 1997;68:324–330. doi: 10.1007/s001150050130. PubMed DOI
Bogovic P., Logar M., Avsic-Zupanc T., Strle F., Lotric-Furlan S. Quantitative evaluation of the severity of acute illness in adult patients with tick-borne encephalitis. BioMed Res. Int. 2014;2014:841027. doi: 10.1155/2014/841027. PubMed DOI PMC
Kriz B., Maly M., Benes C., Daniel M. Epidemiology of Tick-Borne Encephalitis in the Czech Republic 1970–2008. Vector-Borne Zoonotic Dis. 2012;12:994–999. doi: 10.1089/vbz.2011.0900. PubMed DOI PMC
Schuler M., Zimmermann H., Altpeter E., Heininger U. Epidemiology of tick-borne encephalitis in Switzerland, 2005 to 2011. Eurosurveillance. 2014;19:20756. doi: 10.2807/1560-7917.ES2014.19.13.20756. PubMed DOI
Fafangel M., Cassini A., Colzani E., Klavs I., Grgič Vitek M., Učakar V., Muehlen M., Vudrag M., Kraigher A. Estimating the annual burden of tick-borne encephalitis to inform vaccination policy, Slovenia, 2009 to 2013. Eurosurveillance. 2017;22:30509. doi: 10.2807/1560-7917.ES.2017.22.16.30509. PubMed DOI PMC
Barp N., Trentini A., Di Nuzzo M., Mondardini V., Francavilla E., Contini C. Clinical and laboratory findings in tick-borne encephalitis virus infection. Parasite Epidemiol. Control. 2020;10:e00160. doi: 10.1016/j.parepi.2020.e00160. PubMed DOI PMC
Cizman M., Rakar R., Zakotnik B., Pokorn M., Arnez M. Severe forms of tick-borne encephalitis in children. Wien. Klin. Wochenschr. 1999;111:484–487. PubMed
Zenz W., Pansi H., Zoehrer B., Mutz I. Tick-Borne Encephalitis in Children in Styria and Slovenia Between 1980 and 2003. Pediatr. Infect. Dis. J. 2005;24:892–896. doi: 10.1097/01.inf.0000180506.76201.43. PubMed DOI
Pazdiora P., Štruncová V., Švecová M. Tick-borne encephalitis in children and adolescents in the Czech Republic between 1960 and 2007. World J. Pediatr. 2012;8:363–366. doi: 10.1007/s12519-012-0383-z. PubMed DOI
Günther G., Haglund M., Lindquist L., Sköldenberg B., Forsgren M. Intrathecal IgM, IgA and IgG antibody response in tick-borne encephalitis. Long-term follow-up related to clinical course and outcome. Clin. Diagn. Virol. 1997;8:17–29. doi: 10.1016/S0928-0197(97)00273-0. PubMed DOI
Kaiser R., Holzmann H. Laboratory findings in tick-borne encephalitis–correlation with clinical outcome. Infection. 2000;28:78–84. doi: 10.1007/s150100050051. PubMed DOI
Taba P., Schmutzhard E., Forsberg P., Lutsar I., Ljøstad U., Mygland A., Levchenko I., Strle F., Steiner I. EAN consensus review on prevention, diagnosis and management of tick-borne encephalitis. Eur. J. Neurol. 2017;24:1214.e61. doi: 10.1111/ene.13356. PubMed DOI
Ponfick M., Hacker S., Gdynia H.J., Linden R., Gränz M., Nowak D.A. Meningoencephaloradiculomyelitis after tick-borne encephalitis virus infection: A case series. Eur. J. Neurol. 2012;19:776–782. doi: 10.1111/j.1468-1331.2011.03651.x. PubMed DOI
Misić Majerus L., Daković Rode O., Ruzić Sabljić E. Post-encephalitic syndrome in patients with tick-borne encephalitis. Acta Med. Croat. 2009;63:269–278. PubMed
Bogovič P., Stupica D., Rojko T., Lotrič-Furlan S., Avšič-Županc T., Kastrin A., Lusa L., Strle F. The long-term outcome of tick-borne encephalitis in Central Europe. Ticks Tick-Borne Dis. 2017;9:369–378. doi: 10.1016/j.ttbdis.2017.12.001. PubMed DOI
Šmit R., Postma M.J. The burden of tick-borne encephalitis in disability-adjusted life years (DALYs) for Slovenia. PLoS ONE. 2015;10:e0144988. doi: 10.1371/journal.pone.0144988. PubMed DOI PMC
Veje M., Nolskog P., Petzold M., Bergström T., Lindén T., Peker Y., Studahl M. Tick-Borne Encephalitis sequelae at long-term follow-up: A self-reported case–control study. Acta Neurol. Scand. 2016;134:434–441. doi: 10.1111/ane.12561. PubMed DOI
Andersson C.R., Vene S., Insulander M., Lindquist L., Lundkvist A., Günther G., Lundkvist Å., Günther G. Vaccine failures after active immunisation against tick-borne encephalitis. Vaccine. 2010;28:2827–2831. doi: 10.1016/j.vaccine.2010.02.001. PubMed DOI
Hansson K., Rosdahl A., Insulander M., Vene S., Lindquist L., Gredmark-Russ S. Tick-borne encephalitis (TBE) vaccine failures: A ten-year retrospective study supporting the rationale for adding an extra priming dose in individuals from the age of 50 years. Clin. Infect. Dis. 2019;70:245–251. doi: 10.1093/cid/ciz176. PubMed DOI PMC
Lotrič-Furlan S., Bogovič P., Avšič-Županc T., Jelovšek M., Lusa L., Strle F. Tick-borne encephalitis in patients vaccinated against this disease. J. Intern. Med. 2017;282:142–155. doi: 10.1111/joim.12625. PubMed DOI
Dobler G., Kaier K., Hehn P., Böhmer M.M., Kreusch T.M., Borde J.P. Tick-borne encephalitis virus vaccination breakthrough infections in Germany: A retrospective analysis from 2001 to 2018. Clin. Microbiol. Infect. 2019;26:1090.e7–1090.e13. doi: 10.1016/j.cmi.2019.12.001. PubMed DOI
Editorial for the Special Issue: "Tick-Borne Encephalitis"