What we know and still do not know about tick-borne encephalitis?
Authors:
M. F. Kříha 1,2; A. Chrdle 1,3,4; D. Růžek 2,5,6; V. Chmelík 1,2
Authors‘ workplace:
Infekční oddělení, Nemocnice České Budějovice, a. s., České Budějovice
1; Katedra medicínské biologie, Přírodovědecká fakulta, Jihočeská univerzita v Českých Budějovicích, České Budějovice
2; Tropical and Infectious Diseases Unit, Royal Liverpool University Hospital, Liverpool UK
3; Zdravotně sociální fakulta, Jihočeská univerzita v Českých Budějovicích, České Budějovice
4; Laboratoř arbovirologie, Parazitologický ústav, Biologické centrum Akademie věd České republiky, České Budějovice
5; Oddělení infekčních chorob a preventivní medicíny, Výzkumný ústav veterinárního lékařství v Brně, Brno
6
Published in:
Epidemiol. Mikrobiol. Imunol. 70, 2021, č. 3, s. 189-198
Category:
Review Article
Overview
Tick-borne encephalitis (TBE) is a febrile illness caused by tick-borne encephalitis virus (TBEV), frequently manifesting as inflammation of the central nervous system. TBEV is a typical arbovirus, i.e., belongs to a group of viruses transmitted by blood-sucking arthropods. Taxonomically, TBEV is a member of the genus Flavivirus, family Flaviviridae. The disease is endemic in North Eurasia, from western Europe to East Asia. The virus occurs in natural foci of the disease all over Czechia, where it is transmitted predominantly by the castor bean tick (Ixodes ricinus). This infection has a potential to cause significant long-term disability affecting the quality of the patient’s life. Vaccine is available; however, vaccination coverage in Czechia is still low (around 30% of the total population). Lately, attention has been focused on new possibilities for early diagnosis and specific treatment, which so far has only been symptomatic or empirical.
Keywords:
Tick-borne encephalitis – tick-borne encephalitis virus – Pathogenesis – diagnostics – therapy – vaccination
Sources
1. Růžek D. Virus klíšťové encefalitidy – obecná charakteristika. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 19–39.
2. Státní zdravotní ústav. Klíšťová encefalitida – základní informace [online]. [cit. 2020-07-30]. Dostupné na www: http://www.szu. cz/uploads/Epidemiologie/Infekce_zakladni_informace/Klistova_ encefalitida.pd.
3. Heinz FX, Allison SL. Flavivirus structure and membrane fusion. Adv Virus Res, 2003;59: 63–97.
4. Mansfield KL, Johnson N, Phipps LP, et al. Tick-borne encephalitis virus – a review of an emerging zoonosis. J Gen Virol., 2009;90(Pt 8):1781–1794.
5. Danielová V, Daniel M. Ekologie viru klíšťové encefalitidy. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 55–72.
6. Danielová V, Holubová J. Transovarial transmission rates of tick- -borne encephalitis virus in Ixodes ricinus ticks. In: Dusbabek F, Bukva V, eds. Modern acarology. Vol 2, Prague, Czech Republic: SPB Academic Publishing; 1991: 7–10.
7. Labuda M, Nuttall P, Kožuch O, et al. Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia, 1993;49:802–805.
8. Kožuch O, Labuda M, Lysý J, et al. Longitudinal study of natural foci of central European encephalitis virus in west Slovakia. Acta Virol, 1990; 34: 537–44.
9. Süss J. Epidemiology and ecology of TBE relevant to the production of effective vaccines. Vaccine, 2003;21:S19–35.
10. Nosek J, Kožuch O, Lichard M. Persistence of tick-borne encephalitis virus in, and its transmission by Haemaphysalis spinigera and H. turturis ticks. Acta Virol., 1967;11(5):479.
11. Hubálek, Z, Halouzka J. Arthropod-borne viruses of vertebrates in Europe. Acta Sc Nat, Brno: Institute of Landscape Ecology, 1996;30(4-5):1–95.
12. Lichard M, Kožuch O. Persistence of tick-borne encephalitis virus in nymphs and adults of Ixodes arboricola and its transmission to white mice. Acta virol., 1967, 11:480.
13. Kříž B, Beneš Č, Daniel M. Alimentary transmission of tick-borne encephalitis in the Czech Republic (1997–2008). Epidemiol Mikrobiol Imunol., 2009;58(2):98–103.
14. Avsic-Zupanc T, Poljak M, Maticic M, et al. Laboratory acquired tick-borne meningoencephalitis: characterisation of virus strains. Clin Diagn Virol, 1995;4:51–59.
15. Pazdiora P. Epidemiologie klíšťové encefalitidy. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 73–93.
16. World Health Organization. Vaccines against tick-borne encephalitis: WHO position paper [online]. [cit. 2020-07-30]. Dostupné na www: https://www.who.int/publications/i/item/vaccines- against-tick-borne-encephalitis-who-position-paper.
17. ECDC. Tick-borne encephalitis – Annual Epidemiological Report for 2018 [online]. [cit. 2020-07-30]. Dostupné na www: https:// www.ecdc.europa.eu/en/publications-data/tick-borne-encephalitis- annual-epidemiological-report-2018.
18. Daniel M, Danielová V, Kříž B, et al. Shift of the tick Ixodes ricinus and tick-borne encephalitis to higher altitudes in central Europe. Eur J Clin Microbiol Infect Dis, 2003;22: 327–328.
19. Lindgren E, Gustafson R. Tick-borne encephalitis in Sweden and climate change. Lancet, 2001;358:16–18.
20. RIVM. First patient infected by tick-borne encephalitis virus [online]. [cit. 2020-07-30]. Dostupné na www: https://www.rivm.nl/ en/news/first-patient-infected-by-tick-borne-encephalitis-virus.
21. Kreusch TM, Holding M, Hewson R, et al. A probable case of tick- -borne encephalitis (TBE) acquired in England, July 2019. Euro Surveill., 2019;24(47):1900679.
22. Dobler G, Erber W, Schmitt H-J. TBE by country. In: Dobler G, Erber W, Bröker M, Schmitt H-J, editors. The TBE Book. 2nd ed. Singapore: Global Health Press Pte Ltd; 2019. p. 234–426.
23. Kunz C. TBE vaccination and the Austrian experience. Vaccine, 2003;21:S50–55.
24. Státní zdravotní ústav. Klíšťová encefalitida v České republice v roce 2019 – zpráva o epidemiologické situaci v kontextu předcházejících let [online]. [cit. 2020-02-28]. Dostupné na www: http://www.szu.cz/uploads/KE/CEM_5_2020_klistata_Zprava_ za_2019.pdf.
25. Danielová V, Rudenko N, Daniel M, et al. Extension of Ixodes ricinus ticks and agents of tick-borne diseases to mountain areas in the Czech Republic. Int J Med Microbiol., 2006;296(Suppl 40):48–53.
26. Chmelík V, Trnovcová R, Bouzková M, et al. Clinical picture of TBE; a retrospective study of 493 cases. Zentralblatt für Bakteriologie, 289.5-7. 1999:583–584.
27. Amicizia D, Domnich A, Panatto D, et al. Epidemiology of tick- -borne encephalitis (TBE) in Europe and its prevention by available vaccines. Hum Vaccin Immunother., 2013;9(5):1163–1171.
28. Mickiene A, Laiskonis A, Günther G, et al. Tick-borne encephalitis in an area of high endemicity in lithuania: disease severity and long-term prognosis. Clin Infect Dis., 2002;35(6):650–658.
29. Krausler J. 23 years of TBE in the district of Neunkirchen (Austria). In: Kunz C, ed. Tick-borne encephalitis. Wien: Facultas; 1981. pp. 6–12.
30. Haditsch M, Kunze U. Tick-borne encephalitis: a disease neglected by travel medicine. Travel Med Infect Dis., 2013;11(5):295–300.
31. Nuttall PA, Labuda M. Saliva-assisted transmission of tick-borne pathogens. In: Bowman AS, Nuttall PA, eds. Ticks: Biology, Disease and Control. Cambridge: Cambridge University Press; 2008:205–219.
32. Cook MJ. Lyme borreliosis: a review of data on transmission time after tick attachment. Int J Gen Med., 2014;8:1–8.
33. Pospíšilová T, Urbanová V, Hes O, et al. Tracking of Borrelia afzelii Transmission from Infected Ixodes ricinus Nymphs to Mice. Infect Immun., 2019;87(6):e00896–18.
34. Kaiser R. The clinical and epidemiological profile of tick-borne encephalitis in southern Germany 1994–98: a prospective study of 656 patients. Brain, 1999;122:2067–2078.
35. Růžek, D. Patogeneze klíšťové encefalitidy. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 41–54.
36. Chmelík V. Klinický obraz klíšťové encefalitidy. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 105–126.
37. Bogovic P, Strle F. Tick-borne encephalitis: A review of epidemiology, clinical characteristics, and management. World J Clin Cases., 2015;3(5):430–441.
38. Kaiser R. Tick-borne encephalitis: Clinical findings and prognosis in adults. Wien Med Wochenschr., 2012;162(11–12):239–243.
39. Lindquist L, Vapalahti O. Tick-borne encephalitis. Lancet, 2008;371(9627):1861–1871.
40. Taba P, Schmutzhard E, Forsberg P, et al. EAN consensus review on prevention, diagnosis and management of tick-borne encephalitis. Eur J Neurol., 2017;24(10):1214–e61.
41. Růžek D, Avšič Županc T, Borde J, et al. Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. Antiviral Res., 2019;164:23–51.
42. Luňáčková J, Chmelík V, Šípová I, et al. Epidemiologic monitoring of tick-borne encephalitis in Rimov in Southern Bohemia. Epidemiol Mikrobiol Imunol., 2003;52(2):51–58.
43. Fauser S, Stich O, Rauer S. Unusual case of tick borne encephalitis with isolated myeloradiculitis. J Neurol Neurosurg Psychiatry, 2007;78(8):909–910.
44. Chmelík V, Bouzková M, Slámová I, et al. Quality of Life after Tick Borne Encephalitis. ECCMID Praha 1.– 4.5.2004 P1418 Abstract in Clinical Microbiology and Infection, 2004;10: 397.
45. Šmit R, Postma MJ. The Burden of Tick-Borne Encephalitis in Disability-Adjusted Life Years (DALYs) for Slovenia. PLoS One, 2015;10(12):e0144988.
46. Holzmann H. Diagnosis of tick-borne encephalitis. Vaccine, 2003;21(Suppl 1):S36–S40.
47. Česká vakcinologická společnost ČLS JEP. Doporučený postup České vakcinologické společnosti pro prevenci a očkování proti klíšťové encefalitidě [online]. [cit. 2020-02-28]. Dostupné na www: https://www.vakcinace.eu/doporuceni-a-stanoviska.
48. Schwarz B. Health economics of early summer meningoencephalitis in Austria. Effects of a vaccination campaign 1981 to 1990. Wiener Medizinische Wochenschrift (1946), 1993;143(21):551–555.
49. ECDC. Epidemiological situation of tick-borne encephalitis in the European Union and European Free Trade Association countries [online]. [cit. 2020-08-05]. Dostupné na www: https://www. ecdc.europa.eu/en/publications-data/epidemiological-situation- tick-borne-encephalitis-european-union-and-european.
50. Štruncová V, Sedláček D. Klíšťová encefalitida u dětí. Pediatrie pro praxi, 2009;10(2): 70–71.
51. 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(4):449–458.
52. 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(4):363–366.
53. Brauchli YB, Gittermann M, Michot M, et al. A fatal tick bite occurring during the course of tick-borne encephalitis vaccination. Pediatr Infect Dis J, 2008;27:363–365.
54. Kaiser R, Holzmann H. Laboratory findings in tick-borne encephalitis – correlation with clinical outcome. Infection, 2000;28(2):78–84.
55. Dobler G, Kaier K, Hehn P, Böhmer MM, Kreusch TM, Borde JP. Tick-borne encephalitis virus vaccination breakthrough infections in Germany: a retrospective analysis from 2001 to 2018. Clin Microbiol Infect., 2020;26(8):1090.e7–1090.e13.
56. Mansfield KL, Horton DL, Johnson N, et al. Flavivirus-induced antibody cross-reactivity. J Gen Virol., 2011;92(Pt 12):2821–2829.
57. Ergunay K, Tkachev S, Kozlova I, Růžek D. A Review of Methods for Detecting Tick-Borne Encephalitis Virus Infection in Tick, Animal, and Human Specimens. Vector Borne Zoonotic Dis., 2016;16(1):4–12.
58. Yoshii K, Ikawa A, Chiba Y, et al. Establishment of a neutralization test involving reporter gene-expressing virus-like particles of tick-borne encephalitis virus. Journal of Virological Methods, 2009;161(1):173–176.
59. Gassmann C, Bauer G. Avidity determination of IgG directed against tick-borne encephalitis virus improves detection of current infections. J Med Virol., 1997;51(3):242–251.
60. Veje M, Studahl M, Norberg P, et al. Detection of tick-borne encephalitis virus RNA in urine. J Clin Microbiol., 2014;52(11):4111– 4112.
61. Lorenzl S, Pfister H, Padovan C, et al. MRI abnormalities in tick-borne encephalitis. Lancet, 1996;347:698–699.
62. Marjelund S, Tikkakoski T, Tuieku S, et al. Magnetic resonance imaging findings and outcome in severe tick-borne encephalitis. Report of four cases and review of the literature. Acta Radiol, 2004;45:88–94.
63. Bröker M. Following a tick bite: double infections by tick-borne encephalitis virus and the spirochete Borrelia and other potential multiple infections. Zoonoses and Public Health, 2012;59(3):176– 180.
64. Logina I, Krumina A, Karelis G, et al. Clinical features of double infection with tick-borne encephalitis and Lyme borreliosis transmitted by tick bite. J Neurol Neurosurg Psychiatry, 2006;77(12):1350–1353.
65. Chrdle A, Chmelík V, Růžek D. Tick-borne encephalitis: What travelers should know when visiting an endemic country. Hum Vaccin Immunother., 2016;12(10):2694–2699.
66. Penievskaya NA. Etiotropic preparations for post-exposure tick-borne encephalitis prevention: perspective development and problems of epidemiological effectiveness evaluation. Epidemiologiya I Vaktsinoprofilaktika, 2010;(1):39–45.
67. Waldvogel K, Bossart W, Huisman T, et al. Severe tick-borne encephalitis following passive immunization. European Journal of Pediatrics, 1996;155(9):775–779.
68. Phillpotts RJ, Stephenson JR, Porterfield JS. Antibody-dependent enhancement of tick-borne encephalitis virus infectivity. J Gen Virol., 1985;66(Pt 8):1831–1837.
69. Barrett PN, Schober-Bendixen S, Ehrlich HJ. History of TBE vaccines. Vaccine, 2003;21(Suppl 1):S41–S49.
70. Domnich A, Panatto D, Arbuzova EK, et al. Immunogenicity against Far Eastern and Siberian subtypes of tick-borne encephalitis (TBE) virus elicited by the currently available vaccines based on the European subtype: systematic review and meta- analysis. Hum Vaccin Immunother., 2014;10(10):2819–2833.
71. Pöllabauer EM, Pavlova BG, Löw-Baselli A, et al. Comparison of immunogenicity and safety between two paediatric TBE vaccines. Vaccine, 2010;28(29):4680–4685.
72. SÚKL. Souhrn údajů o přípravku FSME-IMMUN 0,5 ml [online]. [cit. 2020-08-07]. Dostupné na www: http://www.sukl.cz/modules/ medication/download.php?file=SPC158465.pdf&type=spc& as=fsme-immun-spc.
73. SÚKL. Souhrn údajů o přípravku Encepur pro dospělé [online]. [cit. 2020-08-07]. Dostupné na www: http://www.sukl.cz/modules/ medication/download.php?file=SPC71652.pdf&type=spc& as=encepur-pro-dospele-spc.
74. Schöndorf I, Beran J, Cizkova D, et al. Tick-borne encephalitis (TBE) vaccination: applying the most suitable vaccination schedule. Vaccine, 2007;25(8):1470–1475.
75. Löw-Baselli A, Pöllabauer EM, Pavlova BG, et al. Prevention of tick- -borne encephalitis by FSME-IMMUN vaccines: review of a clinical development programme. Vaccine, 2011;29(43):7307–7319.
76. Girgsdies OE, Rosenkranz G. Tick-borne encephalitis: development of a paediatric vaccine. A controlled, randomized, double- blind and multicentre study. Vaccine, 1996;14(15):1421–1428.
77. Kollaritsch H, Chmelík V, Dontsenko I, et al. The current perspective on tick-borne encephalitis awareness and prevention in six Central and Eastern European countries: report from a meeting of experts convened to discuss TBE in their region. Vaccine, 2011;29(28):4556–4564.
78. Prymula R. Možnosti prevence a očkování proti klíšťové encefalitidě. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 155–172.
79. Studahl M, Lindquist L, Eriksson BM, et al. Acute viral infections of the central nervous system in immunocompetent adults: diagnosis and management. Drugs, 2013;73(2):131–158.
80. Czupryna P, Moniuszko A, Garkowski A, et al. Evaluation of hyponatraemia in patients with tick-borne encephalitis – a preliminary study. Ticks Tick Borne Dis., 2014;5(3):284–286.
81. Chrdle, A. Terapie klíšťové encefalitidy. In: Růžek D. a kolektiv. Klíšťová encefalitida. Praha: Grada Publishing; 2015. s. 141–154.
82. Cantu RC, Ojemann RG. Corticosteroids in aseptic meningitis. Lancet, 1967;2(7530):1360–1361.
83. Duniewicz M., et al. Corticoids in the Therapy of TBE and Other Viral Encephalitides. Cas Lek Cesk, 1974;9,113(32):984–987.
84. Wengse C, Ericsson J, Hallberg S, et al. Rapid improvement of tick-borne encephalitis after treatment with corticosteroids. Lakartidningen, 2017;114:ELAI. Swedish.
85. ČLK. Standardy délky trvání dočasné pracovní neschopnosti u vybraných diagnóz [online]. [cit. 2020-08-09]. Dostupné na www: https://www.lkcr.cz/doc/cms_library/standardy-delky-trvani- dpn-100848.pdf.
86. Bröker M, Kollaritsch H. After a tick bite in a tick-borne encephalitis virus endemic area: current positions about post-exposure treatment. Vaccine, 2008;26(7):863–868.
87. Růžek D, Dobler G, Niller HH. May early intervention with high dose intravenous immunoglobulin pose a potentially successful treatment for severe cases of tick-borne encephalitis? BMC Infect Dis., 2013;13:306.
88. Elsterová J, Palus M, Širmarová J, et al. Tick-borne encephalitis virus neutralization by high dose intravenous immunoglobulin. Ticks Tick Borne Dis., 2017;8(2):253–258.
89. Baykov IK, Matveev AL, Stronin OV, et al. A protective chimeric antibody to tick-borne encephalitis virus. Vaccine, 2014;32(29):3589–3594.
90. Agudelo, M., Palus, M., Keeffe, J, et al. Broad and Potent Neutralizing Human Antibodies to Tick-borne Flaviviruses Protect Mice from Disease. Journal of Experimental Medicine. 2021 (in press).
91. Kollaritsch H, Krasilnikov V, Holzmann H, et al. Background document on vaccines and vaccination against tick–borne encephalitis. Geneva, WHO Strategic Advisory Group of Experts on Immunization [online]. [cit. 2020-08-11]. Dostupné na www: https://www.who.int/immunization/sage/6_TBE_backgr_18_ Mar_net_apr_2011.pdf.
92. Pogodina VV, Frolova MP, Erman BA. Chronic tick-borne encephalitis. In: E. F. Bocharov (ed.). 1986. Nauka, Moscow, Russia.
93. Osolodkin DI, Kozlovskaya LI, Dueva EV, et al. Inhibitors of tick- -borne flavivirus reproduction from structure-based virtual screening. ACS Medicinal Chemistry Letters, 2013;4(9):869–874.
94. Sedenkova KN, Dueva EV, Averina EB, et al. Synthesis and assessment of 4-aminotetrahydroquinazoline derivatives as tick- -borne encephalitis virus reproduction inhibitors. Org. Biomol. Chem., 2015;13(11):3406–3415.
95. De Clercq E, Neyts J. Antiviral agents acting as DNA or RNA chain terminators. Handb Exp Pharmacol., 2009;(189):53–84.
96. Leyssen P, Balzarini J, De Clercq E, et al. The predominant mechanism by which ribavirin exerts its antiviral activity in vitro against flaviviruses and paramyxoviruses is mediated by inhibition of IMP dehydrogenase. J Virol., 2005;79(3):1943– 1947.
97. Eyer L, Kondo H, Zouharova D, et al. Escape of Tick-Borne Flavivirus from 2‘-C-Methylated Nucleoside Antivirals Is Mediated by a Single Conservative Mutation in NS5 That Has a Dramatic Effect on Viral Fitness. J Virol., 2017;91(21):e01028–17.
98. Lo MK, Shi PY, Chen YL, et al. In vitro antiviral activity of adenosine analog NITD008 against tick-borne flaviviruses. Antiviral Res., 2016;130:46–49.
99. Eyer L, Šmídková M, Nencka R, et al. Structure-activity relationships of nucleoside analogues for inhibition of tick-borne encephalitis virus. Antiviral Res., 2016;133:119–129.
100. Eyer L, Zouharová D, Širmarová J, et al. Antiviral activity of the adenosine analogue BCX4430 against West Nile virus and tick- -borne flaviviruses. Antiviral Res., 2017;142:63–67.
101. Delang L, Abdelnabi R, Neyts J. Favipiravir as a potential countermeasure against neglected and emerging RNA viruses. Antiviral Res., 2018;153:85–94.
102. Orlov AA, Drenichev MS, Oslovsky VE, et al. New tools in nucleoside toolbox of tick-borne encephalitis virus reproduction inhibitors. Bioorg Med Chem Lett., 2017;27(5):1267–1273.
103. Rogova YV, Kozlovskaya LI, Shevtsova AS, at al. Evaluation of virasole efficiency for prevention of tick-borne encephalitis in experiments in laboratory mice. Medical virology. Proceedings of Chumakov Institute of Poliomyelitis and Viral Encephalitides, 2008;25:115–118.
104. Krylova NV, Leonova GN, Popov AM, et al. Investigation of luromarin efficacy on mice with experimental tick-borne encephalitis. Antibiot Khimioter., 2011;56(7-8):13–15.
105. Krylova NV, Leonova GN, Maĭstrovskaia OS, et al. In vitro activity of luromarin against tick-borne encephalitis virus. Antibiot Khimioter., 2010;55(7-8):17–19.
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