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Article

Incidence of Tick-Borne Encephalitis during the COVID-19 Pandemic in Selected European Countries

by
Zbigniew Zając
*,
Katarzyna Bartosik
,
Joanna Kulisz
and
Aneta Woźniak
Department of Biology and Parasitology, Faculty of Health Sciences, Medical University of Lublin, Radziwiłłowska 11 Street, 20-080 Lublin, Poland
*
Author to whom correspondence should be addressed.
J. Clin. Med. 2022, 11(3), 803; https://doi.org/10.3390/jcm11030803
Submission received: 13 December 2021 / Revised: 27 January 2022 / Accepted: 1 February 2022 / Published: 2 February 2022
(This article belongs to the Special Issue Current Scientific Advances in the Prevention, Diagnosis and Treatment of Parasitic Diseases)
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Abstract

:
Ixodes ricinus ticks are one of the most important vectors and reservoirs of infectious diseases in Europe, and tick-borne encephalitis (TBE) is one of the most dangerous human diseases transmitted by these vectors. The aim of the present study was to investigate the TBE incidence in some European countries during the COVID-19 pandemic. To this end, we analyzed the data published by the European Center for Disease Prevention and Control (ECDC) and Eurostat on the number of reported TBE and COVID-19 cases in 2020 and TBE cases in 2015–2019 (reference period). Significant differences in the TBE incidence were found between the analyzed countries. The highest TBE incidence was found in Lithuania (25.45/100,000 inhabitants). A high TBE incidence was also observed in Central European countries. In 12 of the 23 analyzed countries, there was significant increase in TBE incidence during the COVID-19 pandemic during 2020 compared to 2015–2019. There was no correlation between the incidence of COVID-19 and TBE and between the availability of medical personnel and TBE incidence in the studied countries. In conclusion, Central Europe and the Baltic countries are areas with a high risk of TBE infection. Despite the COVID-19 pandemic and imposed restrictions, the incidence of TBE is increasing in more than half of the analyzed countries.

1. Introduction

Ticks (Acari: Ixodida) are one of the most important vectors and reservoirs of infectious and parasitic diseases in Europe [1]. Ixodes ricinus ticks, i.e., representatives of a group of more than 40 species of arthropods in the ixodid tick fauna occurring on the European continent, have great medical and epidemiological importance [2,3]. This is mainly related to the host preferences [4,5] and wide occurrence range of this species [2,6], as well as the spectrum of transmitted pathogens, e.g., Borrelia burgdorferi s.l. spirochetes causing Lyme borreliosis (LB); tick-borne encephalitis virus (TBEV), i.e., a causative agent of tick-borne encephalitis (TBE); and other less frequent tick-borne pathogens infecting humans, e.g., Rickettsia spp. (tick-borne Rickettsial Spotted Fever Group; RSFG), Anaplasma phagocytophilum (human granulocytic anaplasmosis; HGA), or Francisiella tularensis (tularemia), where infection via a tick bite is only one of the possible transmission routes [1,7,8,9,10]. An important role in the circulation and maintenance of tick-borne pathogens in the environment that are potentially dangerous to human health is played by other tick species occurring in Europe [1]. Dermacentor reticulatus ticks are capable of transmitting TBEV [11]. In turn, the presence of the genetic material of this virus in D. marginatus has been confirmed, but the role of this species as a competent TBEV vector has not been elucidated [12].
Next to LB, TBE is one of the most commonly diagnosed tick-borne diseases in Europe [13,14]. In recent years, a systematic increase in the incidence of this disease has been reported in many countries. Austria, the Czech Republic, Germany, Lithuania, Latvia, Estonia, southern Scandinavia, northeastern Poland, and the European part of Russia, where I. persulcatus is another TBEV vector, should be considered as high TBE risk areas [15,16,17].
Based on molecular studies, three main genetic types of TBEV have been distinguished, including European, Siberian and Far Eastern types. Additionally, detailed studies showed the existence of other subtypes, e.g., 886 strand group, reported form southern Siberia [18]. TBEV Far Eastern type, common in eastern Russia, South Korea, and China is associated with complications in 60% of patients and mortality up to 20%, whereas the Siberian type reported from central and western Russia and Eastern Europe mortality rate is estimated at 6–8%. Therefore, the European TBEV subtype seems to be less virulent, with a mortality rate of 1–2% and symptoms developing in 1/3 of infected subjects [19,20,21].
The European type of TBE is most often characterized by a biphasic course. The viremic period, which lasts for several days, is associated with flu-like symptoms followed by a period of apparent improvement. The second phase develops after the entry of the virus into the central nervous system in approximately 30% of patients. It is manifested by recurrent high fever, headaches, dizziness, and vomiting. Depending on the infected area in the nervous system, further symptoms may appear. Patients with meningitis (the most common form of TBE) develop photosensitivity and neck stiffness without consciousness impairment, which is characteristic of the less common encephalomyelitis and/or spinal cord inflammation. Additionally, patients present with ataxia, agitation, hyperkinesia of limb and facial muscles, convulsions, and speech disorders; mental disorders are also possible. The elderly are especially vulnerable to the severe course of TBE. Children often develop asymptomatic infections. Post-inflammatory complications develop in up to 60% of patients [14,20,22,23,24]. The TBE prophylaxis methods include the use of repellents and avoidance of tick habitats. The most effective method is vaccination, which provides protection at the level of 98% after the full cycle [20,25,26].
Both, TBE and COVID-19 are seasonal viral diseases. In the case of TBE, cyclic variations are determined by the rhythms of seasonal activity, abundance and population size of the main vector (depending on the region I. ricinus or I. persulcatus or both), whereas in the case of COVID-19, the current course of the pandemic suggests that periodic increases in the incidence of this disease in Europe are observed in the autumn–winter period, i.e., similar to other seasonal viral diseases affecting the respiratory system [27,28,29].
The global COVID-19 pandemic, which developed towards the end of 2019 in China, and in Europe in March 2020, has resulted in limitations in the access to primary and specialized medical care in many countries [30,31]. This may increase the incidence of various diseases in the future (due to late diagnosis), including tick-borne diseases [32,33]. The aim of the present study was to investigate the TBE incidence in some European countries during the COVID-19 pandemic in 2020.

2. Materials and Methods

The study covered the countries of the European Union and the European Economic Area, which in 2015–2020 reported on the number of infected patients and TBE incidence to the European Center for Disease Prevention and Control (ECDC). In total, 23 countries were analyzed: Austria, Belgium, Bulgaria, Croatia, Czech Republic, Estonia, Finland, France, Germany, Greece, Hungary, Ireland, Italy, Latvia, Lithuania, Luxembourg, Norway, Poland, Romania, Slovakia, Slovenia, Spain, and Sweden.

2.1. COVID-19 Incidence

Data on the number of COVID-19 cases in 2020 and the number of inhabitants in the studied countries were obtained from the statistical office of the European Union (Eurostat) [34,35]. The data were used to calculate the incidence of COVID-19 per 100,000 inhabitants in each country according to the formula:
I = k p × 100 , 000
where:
  • I—incidence per 100,000 inhabitants;
  • k—number of recorded cases,
  • p—total number of inhabitants.

2.2. TBE Incidence

The data on the number of TBE cases were obtained from ECDC [36]. Two periods were analyzed: the pre-pandemic period (2015–2019) and the COVID-19 pandemic year (2020). The incidence rate per 100,000 inhabitants was calculated as above (Section 2.1). Additionally, based on the data from 2015–2019, the projected TBE incidence in 2020 was calculated.
Moreover, Eurostat data on the number of medical personnel in the countries were analyzed [37].

2.3. Statistical Analysis

The measurable variables of TBE incidence in the analyzed countries were described using the median due to their right-skewed distribution.
The distribution of the data was verified using the Shapiro–Wilk test. The statistical significance of differences in the TBE incidence between the studied countries over the years was verified by the Friedman ANOVA test with the post hoc Dunn test. The differences between the projected and reported TBE incidence rates were tested using the pairwise Wilcoxon test. The Spearman rank correlation coefficient was used to test the relationships between the number of healthcare staff per 100,000 inhabitants in the analyzed countries and the TBE incidence, and between the incidence of COVID-19 and TBE. The significance of the differences in the TBE incidence between 2015–2019 and the pandemic year (2020) was verified by a one-sample t-test.
The value of p < 0.05 was considered statistically significant. Statistical calculations were performed using the STATISTICA 13 PL statistical package (StatSoft, TIBCO Software Inc., Palo Alto, CA, USA).

3. Results

3.1. TBE Incidence in 2015–2019

In 2015–2019, the TBE incidence in the analyzed countries ranged from 0.00 to 25.45/100,000 inhabitants and were statistically, significantly different between the countries (χ2 = 13.25, p = 0.0101). A growing trend was noted between the subsequent years (Table 1). The highest incidence was recorded in the Baltic republics and Central European countries. The highest five-year incidence median was reported in Lithuania (16.64/100,000 inhabitants) and in the Czech Republic (6.40/100,000 inhabitants). The median incidence exceeding 5.00/100,000 inhabitants was also noted in Estonia and Latvia. The lowest incidence rates were recorded in Western Europe. The median incidence was 0.02/100,000 inhabitants in France and 0.05/100,000 inhabitants in Italy. In the group of countries reporting tick-borne diseases to ECDC, no TBE infection was confirmed in Greece, Spain, and Ireland in 2015–2019 (Figure 1).

3.2. TBE Incidence in the Pandemic Year 2020

The projected TBE incidence in 2020 in the studied countries ranged from 0.00/100,000 inhabitants in Luxembourg to 31.04/100,000 inhabitants in Lithuania. In turn, the reported incidence reached 24.3/100,000 inhabitants in Lithuania. There was no significant difference between the predicted and reported values (Z = 0.15, p = 0.8789) (Figure 2).
As in 2015–2019, the analyzed countries were characterized by a similar distribution of the incidence values (Table 1, Figure 1). In the case of Austria, Belgium, Bulgaria, Finland, France, Germany, Italy, Norway, and Slovenia, there was a statistically significant increase in the TBE incidence in 2020 versus the incidence in 2015–2019 (Table 2). In comparison with the reference period, the increase in the TBE incidence in these countries ranged from 32.0% (Finland) to 250.0% (France) (Figure 3). In turn, a significantly lower incidence rate in 2020 than in the reference period 2015–2019 was observed in Poland (−42.3%) and Estonia (−17.4%) (Figure 3, Table 2). Nevertheless, in all the countries, there was no significant difference in the TBE incidence between 2020 and 2015–2019 (Z = 1.93, p = 0.0534).
In the analyzed countries, there was no correlation between the availability of medical personnel and TBE incidence (rs = 0.151, p = 0.6403), or between the incidence of COVID-19 regarded as a factor reducing access to healthcare and TBE incidence (rs = 0.129, p = 0.5572).

4. Discussion

Tick-borne diseases are one of the most significant infectious diseases in Europe [13,38]. The results of the present study show that TBE is an especially important and growing problem in the Baltic, Central European, and Scandinavian countries, as the incidence of this disease in the analyzed period reached as high as 24.3/100.00 inhabitants in Lithuania (Figure 1). In many European countries, TBE is the second-most common human tick-borne disease after LB in terms of the number of diagnosed cases [39,40,41,42]. Microclimatic conditions are the main factors that support the activity of ticks and, in an indirect way, the transmission of tick-borne pathogens [43]. Nevertheless, an important role in formation and stability of TBE natural foci plays coincidence of several ecological factors such as air temperature and air relative humidity, soil humidity, vegetation, type of the biotope, population density and the dynamics of seasonal activity of ticks and their hosts. Significant factors influencing TBEV circulation in the zoonotic cycle are hosts’ immunological statuses, their susceptibility to TBEV infection and the prevalence of this virus in reservoir animals [44,45,46,47,48]. The shorter winter period accelerates and extends the period of tick activity, thus contributing to a higher survival rate of ticks [49] and their potential hosts [50]. Such conditions have recently been observed in Central Europe [51], i.e., the region with the highest TBE incidence on the continent. The significant differences in the incidence of TBE between the analyzed European countries shown in the present study may primarily be caused by the location of these countries in different climatic zones. The lowest TBE incidence is reported in Southern European countries with a dry climate (Figure 1, Table 1). Such conditions may exert an adverse effect on the number of potential hosts and reduce the level of infestation with juvenile tick stages [49]. With sufficient reserve materials, I. ricinus larvae and nymphs, which are sensitive to water loss, avoid unfavorable conditions. This shortens the host questing time and reduces the probability of TBEV transmission in the rodent (reservoir)–tick (vector) system [49,52]. Another possible route of TBEV infection is the consumption of unpasteurized dairy products [53]. Nevertheless, in our opinion, based on current sanitary restrictions on the sale of unpasteurized milk, this route of infection accounts for a negligible percentage of all TBE cases.
The countries analyzed in the present study were characterized by an uneven distribution of TBE incidence between the sub-regions [15]. This phenomenon was particularly evident in the case of Sweden, Norway (most TBE cases were reported from southern regions), Germany (Bavaria), and Poland, where the northeastern part of the country is the endemic TBE region. These regions are characterized by a large proportion of forest cover [54,55,56]. Our earlier study conducted in eastern Poland showed a significant positive correlation between TBE and LB prevalence rates and the surface area of forests [42]. Regional differences in TBE prevalence have also been reported in the Czech Republic, Austria, and Slovakia [57,58,59].
The present results indicate the highest TBE incidence in the Baltic republics, both in the reference period and in the pandemic year (2020; Table 1, Figure 1). This situation has been noted for many years. During the period 1990–2000, Latvia reported the highest TBE incidence in the world (up to 53/100,000 inhabitants) [60]. Very high TBE incidence (up to 40.3/100,000 inhabitants) and death rates were also reported in Lithuania [61,62]. The very high TBE incidence in these countries is most probably associated with specific microhabitat conditions and the presence of I. persulcatus ticks [63,64]. In this region, approx. 26.6% of I. ricinus ticks and 37.3% of I. persulcatus ticks collected from the vegetation were infected with TBEV. In turn, TBEV was detected in nearly 30% of ticks removed from humans [64]. Notably, these countries have the highest TBE vaccination rates, i.e., 53% of the population in Latvia [64], compared to 3% in Germany [65] and approx. 10% in Slovakia (based on self-report surveys) [66].
The results of the present study show that the reported TBE incidence in the analyzed countries in 2020 did not differ significantly from the projected incidence values (Figure 2). Moreover, the TBE incidence increased in more than half of the analyzed countries in 2020 (of which a statistically significant increase was observed in 12 countries (Table 2)), compared to the reference period, with the largest increase in France and Bulgaria (250% and 200%, respectively) (Table 2, Figure 3). The very high increase in the TBE incidence in these countries is, however, related to the very low baseline value in the reference period (Table 2). Nevertheless, the increase in the number of TBE cases was noted across the continent despite the COVID-19 pandemic and government-imposed lockdowns.
A decrease in TBE incidence in 2020 compared to the reference period was recorded in only three countries, i.e., Poland (−42.3%), Sweden (−25.3%), and Estonia (−17.4%) (Figure 3). The decrease was statistically significant in the case of Poland and Estonia (Table 2). We believe that this may be associated with the change in the seasonal dynamics of ticks and/or the restrictions on movement. For instance, the so-called hard lockdown imposed in Poland from March to April 2020, with a ban on access to forests and parks, reduced the risk of exposure to tick bites. In our opinion, given the course of symptomatic TBE [64,67], the limitation of access to primary and specialist healthcare may have had minor importance, although other authors emphasize this factor [32,68,69]. Our opinion is confirmed by the results of the analyses showing no correlations between the availability of medical personnel and TBE incidence, or between the COVID-19 and TBE incidence rates in the analyzed countries. Symptomatic patients infected with TBEV require medical care and, most often, hospitalization [26,70]. Due to the course of the disease, a “substantial delay” in the diagnosis and treatment of TBE should be ruled out. However, the incomplete reporting due to the large bureaucratic burden posed on the health service by the pandemic may have influenced the official number of TBE cases in government reports.

5. Conclusions

Based on the long-term period (2015–2019), Central Europe and the Baltic Sea countries are areas of high TBEV infection risk. Despite the COVID-19 pandemic in 2020 and the resulting restrictions, an increase in the TBE incidence rate was observed in more than half of the analyzed countries. In the pandemic year (2020), the highest increase in TBE incidence rate was observed in countries with different climatic zones, including France, Bulgaria, Norway, Austria and Italy. We highly recommend future research that focus on TBE incidence in the context of the COVID-19 pandemic.

Author Contributions

Conceptualization, Z.Z.; methodology, Z.Z.; data analysis Z.Z., K.B., J.K. and A.W.; writing—original draft preparation, Z.Z.; writing—review and editing, K.B., J.K. and A.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data are available from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Jongejan, F.; Uilenberg, G. The global importance of ticks. Parasitology 2004, 129, S3–S14. [Google Scholar] [CrossRef] [PubMed]
  2. Estrada-Peña, A.; Mihalca, A.D.; Petney, T. Ticks of Europe and North Africa: A Guide to Species Identification; Springer: Cham, Germany, 2018; ISBN 9783319637594. [Google Scholar]
  3. Wilhelmsson, P.; Lindblom, P.; Fryland, L.; Nyman, D.; Jaenson, T.G.; Forsberg, P.; Lindgren, P.-E. Ixodes ricinus ticks removed from humans in Northern Europe: Seasonal pattern of infestation, attachment sites and duration of feeding. Parasites Vectors 2013, 6, 362. [Google Scholar] [CrossRef] [PubMed]
  4. Opalińska, P.; Wierzbicka, A.; Asman, M.; Rączka, G.; Dyderski, M.K.; Nowak-Chmura, M. Fivefold higher abundance of ticks (Acari: Ixodida) on the European roe deer (Capreolus capreolus L.) forest than field ecotypes. Sci. Rep. 2021, 11, 10649. [Google Scholar] [CrossRef] [PubMed]
  5. Mihalca, A.D.; Sándor, A.D. The role of rodents in the ecology of Ixodes ricinus and associated pathogens in Central and Eastern Europe. Front. Cell. Infect. Microbiol. 2013, 3, 56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Gray, J.; Kahl, O.; Zintl, A. What do we still need to know about Ixodes ricinus? Ticks Tick-Borne Dis. 2021, 12, 101682. [Google Scholar] [CrossRef]
  7. Pettersson, J.H.-O.; Golovljova, I.; Vene, S.; Jaenson, T.G. Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in northern Europe with particular reference to Southern Sweden. Parasites Vectors 2014, 7, 102. [Google Scholar] [CrossRef] [Green Version]
  8. Rosef, O.; Paulauskas, A.; Radzijevskaja, J. Prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing Ixodes ricinus ticks in relation to the density of wild cervids. Acta Veter. Scand. 2009, 51, 47. [Google Scholar] [CrossRef] [Green Version]
  9. Kirczuk, L.; Piotrowski, M.; Rymaszewska, A. Detection of tick-borne pathogens of the genera Rickettsia, Anaplasma and Francisella in Ixodes ricinus ticks in Pomerania (Poland). Pathogens 2021, 10, 901. [Google Scholar] [CrossRef]
  10. Grochowska, A.; Milewski, R.; Pancewicz, S.; Dunaj, J.; Czupryna, P.; Milewska, A.J.; Róg-Makal, M.; Grygorczuk, S.; Moniuszko-Malinowska, A. Comparison of tick-borne pathogen prevalence in Ixodes ricinus ticks collected in urban areas of Europe. Sci. Rep. 2020, 10, 6975. [Google Scholar] [CrossRef]
  11. Ličková, M.; Fumačová Havlíková, S.; Sláviková, M.; Slovák, M.; Drexler, J.F.; Klempa, B. Dermacentor reticulatus is a vector of tick-borne encephalitis virus. Ticks Tick-borne Dis. 2020, 11, 101414. [Google Scholar] [CrossRef]
  12. Nosek, J. The ecology, bionomics, behaviour and public healh importance of Dermacentor marginatus and D. reticulatus ticks. Wiad. Parazytol. 1972, 18, 721–725. [Google Scholar] [PubMed]
  13. Heyman, P.; Cochez, C.; Hofhuis, A.; Van der Giessen, J.; Sprong, H.; Porter, S.R.; Losson, B.; Saegerman, C.; Donoso-Mantke, O.; Niedrig, M.; et al. A clear and present danger: Tick-borne diseases in Europe. Expert Rev. Anti-Infect. Ther. 2010, 8, 33–50. [Google Scholar] [CrossRef] [PubMed]
  14. Ruzek, D.; Avšič Županc, T.; Borde, J.; Chrdle, A.; Eyer, L.; Karganova, G.; Kholodilov, I.; Knap, N.; Kozlovskaya, L.; Matveev, A.; et al. Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. Antivir. Res. 2019, 164, 23–51. [Google Scholar] [CrossRef]
  15. Beauté, J.; Spiteri, G.; Warns-Petit, E.; Zeller, H. Tick-borne encephalitis in Europe, 2012 to 2016. Eurosurveillance 2018, 23, 1800201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. 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. 2018, 9, 369–378. [Google Scholar] [CrossRef] [PubMed]
  17. Tokarevich, N.K.; Tronin, A.A.; Blinova, O.V.; Buzinov, R.V.; Boltenkov, V.P.; Yurasova, E.D.; Nurse, J. The impact of climate change on the expansion of Ixodes persulcatus habitat and the incidence of tick-borne encephalitis in the north of European Russia. Glob. Health Action 2011, 4, 8448. [Google Scholar] [CrossRef]
  18. Kozlova, I.; Verkhozina, M.; Demina, T.; Dzhioev, Y.; Tkachev, S.; Karan, L.; Doroshchenko, E.; Lisak, O.; Suntsova, O.; Paramonov, A.; et al. Genetic and biological properties of original TBEV strains group circulating in Eastern Siberia. Encephalitis 2013, 283, 95–112. [Google Scholar]
  19. 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. [Google Scholar] [CrossRef]
  20. Garlicki, A. Choroby Infekcyjne Ośrodkowego Układu Nerwowego. In Choroby Zakaźne i Pasożytnicze; Boroń-Kaczmarska, A., Wiercińska-Drapało, A., Eds.; PZWL: Warszawa, Poland, 2017. [Google Scholar]
  21. Bogovic, P. Tick-borne encephalitis: A review of epidemiology, clinical characteristics, and management. World J. Clin. Cases 2015, 3, 430–441. [Google Scholar] [CrossRef]
  22. Kohlmaier, B.; Schweintzger, N.A.; Sagmeister, M.G.; Švendová, V.; Kohlfürst, D.S.; Sonnleitner, A.; Leitner, M.; Berghold, A.; Schmiedberger, E.; Fazekas, F.; et al. Clinical characteristics of patients with tick-borne encephalitis (TBE): A European Multicentre Study from 2010 to 2017. Microorganisms 2021, 9, 1420. [Google Scholar] [CrossRef]
  23. 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. 2010, 18, 673–679. [Google Scholar] [CrossRef] [PubMed]
  24. Radzišauskienė, D.; Urbonienė, J.; Kaubrys, G.; Andruškevičius, S.; Jatužis, D.; Matulytė, E.; Žvirblytė-Skrebutienė, K. The epidemiology, clinical presentation, and predictors of severe tick-borne encephalitis in Lithuania, a highly endemic country: A retrospective study of 1040 patients. PLoS ONE 2020, 15, e0241587. [Google Scholar] [CrossRef]
  25. Amicizia, D.; Domnich, A.; Panatto, D.; Lai, P.L.; Cristina, M.L.; Avio, U.; Gasparini, R. Epidemiology of tick-borne encephalitis (TBE) in Europe and its prevention by available vaccines. Hum. Vaccines Immunother. 2013, 9, 1163–1171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Kuchar, E.; Zajkowska, J.; Flisiak, R.; Mastalerz-Migas, A.; Rosińska, M.; Szenborn, L.; Wdówik, P.; Walusiak-Skorupa, J. Epidemiology, diagnosis, and prevention of tick-borne encephalitis in Poland and selected european countries—A position statement of the polish group of experts. Med. Pr. 2021, 72, 193–210. [Google Scholar] [CrossRef] [PubMed]
  27. Altizer, S.; Dobson, A.; Hosseini, P.; Hudson, P.; Pascual, M.; Rohani, P. Seasonality and the dynamics of infectious diseases. Ecol. Lett. 2006, 9, 467–484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Borde, J.P.; Kaier, K.; Hehn, P.; Böhmer, M.M.; Kreusch, T.M.; Dobler, G. Tick-borne encephalitis virus infections in Germany. Seasonality and in-year patterns. A retrospective analysis from 2001-2018. PLoS ONE 2019, 14, e0224044. [Google Scholar] [CrossRef] [PubMed]
  29. Audi, A.; Al Ibrahim, M.; Kaddoura, M.; Hijazi, G.; Yassine, H.M.; Zaraket, H. Seasonality of Respiratory Viral Infections: Will COVID-19 Follow Suit? Front. Public Health 2020, 8, 567184. [Google Scholar] [CrossRef] [PubMed]
  30. Wosik, J.; Clowse, M.E.B.; Overton, R.; Adagarla, B.; Economou-Zavlanos, N.; Cavalier, J.; Henao, R.; Piccini, J.P.; Thomas, L.; Pencina, M.J.; et al. Impact of the COVID-19 pandemic on patterns of outpatient cardiovascular care. Am. Heart J. 2021, 231, 1–5. [Google Scholar] [CrossRef]
  31. Piątkowska, K.; Zimmermann, A.; Pilarska, A. Limitation of patients’ rights during the COVID-19 pandemics in Poland. Eur. J. Transl. Clin. Med. 2021, 4, 79–85. [Google Scholar] [CrossRef]
  32. Wormser, G.P.; Jacobson, E.; Shanker, E.M. Negative impact of the COVID-19 pandemic on the timely diagnosis of tick-borne infections. Diagn. Microbiol. Infec. Dis. 2020, 99, 115226. [Google Scholar] [CrossRef]
  33. Novak, C.B.; Scheeler, V.M.; Aucott, J.N. Lyme disease in the era of COVID-19: A delayed diagnosis and risk for complications. Case Rep. Infect. Dis. 2021, 2021, 6699536. [Google Scholar] [CrossRef] [PubMed]
  34. Eurostat. Data—COVID-19. Available online: https://ec.europa.eu/eurostat/web/covid-19/data (accessed on 4 November 2021).
  35. Eurostat. Database—Population and Demography. Available online: https://ec.europa.eu/eurostat/web/population-demography/demography-population-stock-balance/database (accessed on 4 November 2021).
  36. European Centre for Disease Prevention and Control. Surveillance Atlas of Infectious Diseases. Available online: https://atlas.ecdc.europa.eu/public/index.aspx (accessed on 4 November 2021).
  37. Eurostat. Health Personnel, Nursing and Caring Professionals. Available online: https://ec.europa.eu/eurostat/databrowser/view/HLTH_RS_PRSNS__custom_88217/bookmark/table?lang=en&bookmarkId=f209f632-69ec-4656-829e-f6e562c9888a (accessed on 4 November 2021).
  38. Madison-Antenucci, S.; Kramer, L.D.; Gebhardt, L.L.; Kauffman, E. Emerging tick-borne diseases. Clin. Microbiol. Rev. 2020, 33, e0008318. [Google Scholar] [CrossRef] [PubMed]
  39. Stefanoff, P.; Orlíková, H.; Príkazský, V.; Beneš, Č.; Rosińska, M. Cross-border surveillance differences: Tick-borne encephalitis and Lyme borreliosis in the Czech Republic and Poland, 1999-2008. Central Eur. J. Public Health 2014, 22, 54–59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Kotrbova, K.; Lunackova, J. Seroprevalence of tick-borne encephalitis and Lyme borreliosis in a defined Czech population. Int. J. Infect. Dis. 2019, 79, 135. [Google Scholar] [CrossRef] [Green Version]
  41. Kiffner, C.; Zucchini, W.; Schomaker, P.; Vor, T.; Hagedorn, P.; Niedrig, M.; Rühe, F. Determinants of tick-borne encephalitis in counties of southern Germany, 2001–2008. Int. J. Health Geogr. 2010, 9, 42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Zając, Z.; Kulisz, J.; Bartosik, K.; Woźniak, A.; Dzierżak, M.; Khan, A. Environmental determinants of the occurrence and activity of Ixodes ricinus ticks and the prevalence of tick-borne diseases in eastern Poland. Sci. Rep. 2021, 11, 15472. [Google Scholar] [CrossRef] [PubMed]
  43. Pfäffle, M.; Littwin, N.; Muders, S.V.; Petney, T.N. The ecology of tick-borne diseases. Int. J. Parasitol. 2013, 43, 1059–1077. [Google Scholar] [CrossRef]
  44. Hofmann, H.; Kunz, C. Early serological diagnosis of virus infections. Wien. Klin. Wochenschr. 1973, 85, 490–493. [Google Scholar]
  45. Korotkov, Y.S.; Nikitin, A.Y.; Antonova, A.M. Role of climatic factors in long-term dynamics of tick-borne encephalitis morbidity in the city of Irkutsk. Byull. Vostochno-Sibirskogo Nauchnogo Tsentr. Sibirsk. Otdel. Ross. Akad. Med. Nauk. 2007, 3, 121–125. [Google Scholar]
  46. Lindgren, E. Climate and tickborne encephalitis. Conserv. Ecol. 1998, 2, 5. [Google Scholar] [CrossRef] [Green Version]
  47. Dörrbecker, B.; Dobler, G.; Spiegel, M.; Hufert, F.T. Tick-borne encephalitis virus and the immune response of the mammalian host. Travel Med. Infect. Dis. 2010, 8, 213–222. [Google Scholar] [CrossRef] [PubMed]
  48. Labuda, M.; Kozuch, O.; Zuffová, E.; Elecková, E.; Hails, R.S.; Nuttall, P.A. Tick-Borne Encephalitis Virus Transmission between Ticks Cofeeding on Specific Immune Natural Rodent Hosts. Virology 1997, 235, 138–143. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Burri, C.; Bastic, V.; Maeder, G.; Patalas, E.; Gern, L. Microclimate and the zoonotic cycle of tick-borne encephalitis virus in Switzerland. J. Med. Entomol. 2011, 48, 615–627. [Google Scholar] [CrossRef] [PubMed]
  50. Ostfeld, R.S.; Canham, C.D.; Oggenfuss, K.; Winchcombe, R.J.; Keesing, F. Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biol. 2006, 4, 40145. [Google Scholar] [CrossRef]
  51. Tutiempo Network, S.L. Weather in Europe. Available online: https://en.tutiempo.net/europe.html (accessed on 5 November 2021).
  52. Steele, G.M.; Randolph, S.E. An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari: Ixodidae). I. A unimodal seasonal activity pattern. Bull. Entomol. Res. 1985, 75, 489–500. [Google Scholar] [CrossRef]
  53. Dorko, E.; Hockicko, J.; Rimárová, K.; Bušová, A.; Popaďák, P.; Popaďáková, J.; Schréter, I. Milk outbreaks of tick-borne encephalitis in Slovakia, 2012–2016. Cent. Eur. J. Public Health 2018, 26, S47–S50. [Google Scholar] [CrossRef] [Green Version]
  54. Alix-Garcia, J.; Munteanu, C.; Zhao, N.; Potapov, P.V.; Prishchepov, A.V.; Radeloff, V.C.; Krylov, A.; Bragina, E. Drivers of forest cover change in Eastern Europe and European Russia, 1985–2012. Land Use Policy 2016, 59, 284–297. [Google Scholar] [CrossRef]
  55. Eurostat. Database—Forestry. Available online: https://ec.europa.eu/eurostat/web/forestry/data/database (accessed on 5 November 2021).
  56. Hellenbrand, W.; Kreusch, T.; Böhmer, M.; Wagner-Wiening, C.; Dobler, G.; Wichmann, O.; Altmann, D. Epidemiology of tick-borne encephalitis (TBE) in Germany, 2001–2018. Pathogens 2019, 8, 42. [Google Scholar] [CrossRef] [Green Version]
  57. Kříž, B.; Fialová, A.; Šebestová, H.; Daniel, M.; Malý, M. Comparison of the epidemiological patterns of Lyme borreliosis and tick-borne encephalitis in the Czech Republic in 2007–2016. Epidemiol. Mikrobiol. Imunol. Cas. Spol. Pro Epidemiol. Mikrobiol. Ces. Lek. Spol. JE Purkyne 2018, 67, 134–140. [Google Scholar]
  58. Rubel, F.; Brugger, K. Operational TBE incidence forecasts for Austria, Germany, and Switzerland 2019–2021. Ticks Tick-Borne Dis. 2021, 12, 101579. [Google Scholar] [CrossRef]
  59. Kerlik, J.; Avdičová, M.; Štefkovičová, M.; Tarkovská, V.; Pántiková Valachová, M.; Molčányi, T.; Mezencev, R. Slovakia reports highest occurrence of alimentary tick-borne encephalitis in Europe: Analysis of tick-borne encephalitis outbreaks in Slovakia during 2007–2016. Travel Med. Infect. Dis 2018, 26, 37–42. [Google Scholar] [CrossRef] [PubMed]
  60. Zavadska, D.; Odzelevica, Z. TBE in Latvia. In The TBE Book; Dobler, G., Erber, W., Bröker, M., Schmitt, H.-J., Eds.; Global Health Press Pte Ltd.: Singapore, 2020; 248p. [Google Scholar]
  61. Mickiene, A. TBE in Lithuania. In The TBE Book; Dobler, G., Erber, W., Bröker, M., Schmitt, H.-J., Eds.; Global Health Press Pte Ltd.: Singapore, 2020; 256p. [Google Scholar]
  62. 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Capligina, V.; Seleznova, M.; Akopjana, S.; Freimane, L.; Lazovska, M.; Krumins, R.; Kivrane, A.; Namina, A.; Aleinikova, D.; Kimsis, J.; et al. Large-scale countrywide screening for tick-borne pathogens in field-collected ticks in Latvia during 2017–2019. Parasites Vectors 2020, 13, 351. [Google Scholar] [CrossRef] [PubMed]
  64. Zavadska, D.; Odzelevica, Z.; Karelis, G.; Liepina, L.; Litauniece, Z.A.; Bormane, A.; Lucenko, I.; Perevoscikovs, J.; Bridina, L.; Veide, L.; et al. Tick-borne encephalitis: A 43-year summary of epidemiological and clinical data from Latvia (1973 to 2016). PLoS ONE 2018, 13, e0204844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Schley, K.; Malerczyk, C.; Beier, D.; Schiffner-Rohe, J.; Von Eiff, C.; Häckl, D.; Süß, J. Vaccination rate and adherence of tick-borne encephalitis vaccination in Germany. Vaccine 2021, 39, 830–838. [Google Scholar] [CrossRef]
  66. Erber, W.; Schmitt, H.-J. Self-reported tick-borne encephalitis (TBE) vaccination coverage in Europe: Results from a cross-sectional study. Ticks Tick-Borne Dis. 2018, 9, 768–777. [Google Scholar] [CrossRef]
  67. Bogovic, P.; Lotric-Furlan, S.; Strle, F. What tick-borne encephalitis may look like: Clinical signs and symptoms. Travel Med. Infect. Dis. 2010, 8, 246–250. [Google Scholar] [CrossRef]
  68. Moniuszko-Malinowska, A.; Pancewicz, S.; Czupryna, P. Has COVID-19 influenced on tick-borne epidemiology? Prz. Epidemiol. 2020, 74, 740–741. [Google Scholar] [CrossRef]
  69. Pańczuk, A. Lyme borreliosis in the Lublin province during the COVID-19 pandemic. Health Probl. Civiliz. 2021, 15, 291–297. [Google Scholar] [CrossRef]
  70. 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. NeuroVirology 2020, 26, 565–571. [Google Scholar] [CrossRef]
Jcm 11 00803 g001 550
Figure 1. Median TBE incidence in some European countries in 2015–2019 and TBE incidence in the pandemic year 2020. Abbreviations: E—Spain, FR—France, I—Italy, IRD—Ireland, BE—Belgium, D—Germany, A—Austria, SLO—Slovenia, HR—Croatia, H—Hungary, RO—Romania, BG—Bulgaria, GR—Greece, SK—Slovakia, CZ—Czech Republic, PL—Poland, LT—Lithuania, LV—Latvia, EST—Estonia, FIN—Finland, SE—Sweden, NO—Norway.
Figure 1. Median TBE incidence in some European countries in 2015–2019 and TBE incidence in the pandemic year 2020. Abbreviations: E—Spain, FR—France, I—Italy, IRD—Ireland, BE—Belgium, D—Germany, A—Austria, SLO—Slovenia, HR—Croatia, H—Hungary, RO—Romania, BG—Bulgaria, GR—Greece, SK—Slovakia, CZ—Czech Republic, PL—Poland, LT—Lithuania, LV—Latvia, EST—Estonia, FIN—Finland, SE—Sweden, NO—Norway.
Jcm 11 00803 g001
Jcm 11 00803 g002 550
Figure 2. Projected and reported TBE incidence in the analyzed countries. The graph presents countries reporting TBE cases.
Figure 2. Projected and reported TBE incidence in the analyzed countries. The graph presents countries reporting TBE cases.
Jcm 11 00803 g002
Jcm 11 00803 g003 550
Figure 3. Percentage change in the TBE incidence per 100,000 inhabitants in 2020 compared to the 2015–2019 median in the analyzed countries. Abbreviations: E—Spain, FR—France, I—Italy, IRD—Ireland, BE—Belgium, D—Germany, A—Austria, SLO—Slovenia, HR—Croatia, H—Hungary, RO—Romania, BG—Bulgaria, GR- Greece, SK—Slovakia, CZ—Czech Republic, PL—Poland, LT—Lithuania, LV—Latvia, EST—Estonia, FIN—Finland, SE—Sweden, NO—Norway.
Figure 3. Percentage change in the TBE incidence per 100,000 inhabitants in 2020 compared to the 2015–2019 median in the analyzed countries. Abbreviations: E—Spain, FR—France, I—Italy, IRD—Ireland, BE—Belgium, D—Germany, A—Austria, SLO—Slovenia, HR—Croatia, H—Hungary, RO—Romania, BG—Bulgaria, GR- Greece, SK—Slovakia, CZ—Czech Republic, PL—Poland, LT—Lithuania, LV—Latvia, EST—Estonia, FIN—Finland, SE—Sweden, NO—Norway.
Jcm 11 00803 g003
Table
Table 1. Healthcare personnel, COVID-19 incidence in 2020, and TBE incidence in 2015–2020 in the analyzed countries.
Table 1. Healthcare personnel, COVID-19 incidence in 2020, and TBE incidence in 2015–2020 in the analyzed countries.
CountryHealth Care Personnel per 100,000Incidence of COVID-19 per 100,000 in 2020Number of Cases and Incidence of TBE per 100,000 Inhabitants
201520162017201820192020
NInc.NInc.NInc.NInc.NInc.NInc.
Austria1612.144040.5790.92961.101231.401701.931061.202502.81
Belgium1296.335587.710.0110.0130.0330.0340.0370.06
Bulgariand.2922.920.0300.0010.0100.0010.0120.03
Croatiand.5218.7260.6260.14100.24220.54130.32140.34
Czech Republic1400.436716.53493.315655.356776.407126.717737.268497.94
Estonia994.672104.51158.75806.08846.38856.44826.19705.27
Finlandnd.652.9681.24611.11821.49791.43691.25911.65
France1754.853880.3100.02150.0220.01 *250.0440.01460.07
Germany1262.442117.02210.273530.434860.595830.704440.537050.85
Greecend.1300.110.0100.0000.0020.0200.0000.00
Hungary1002.613314.6220.22140.14140.14300.31170.17180.18
Ireland1258.121831.900.0000.0000.0000.0010.0200.00
Italynd.3555.850.01480.08240.04390.06370.05550.09
Latviand.2164.21417.10914.621789.131005.171186.151497.81
Lithuania1628.415069.833611.563321.9147416.6438413.6771125.4567924.3
Luxembourgnd.7367.510.1800.0000.0000.0000.0000.00
Norway1906.19919.690.17120.23160.30260.49350.66410.76
Polandnd.3422.01150.302110.561960.521480.391970.521140.3
Romania946.673294.800.0000.0010.0140.0200.0000.00
Slovakia793.443288.3801.481693.11751.381562.871612.951853.39
Sloveniand.5789.2623.01834.021024.941537.401115.331878.92
Spainnd.4068.900.0000.0000.0000.0010.01 *00.00
Swedennd.4213.72682.752382.423653.653593.553553.472672.59
nd.—no data, N—number of reported cases of TBE, Inc.—incidence of TBE per 100,000 inhabitants, * incidence < 0.01.
Table
Table 2. Comparisons and the level of the statistical significance of differences in the TBE incidence in 2015–2019 and in 2020 in the analyzed countries.
Table 2. Comparisons and the level of the statistical significance of differences in the TBE incidence in 2015–2019 and in 2020 in the analyzed countries.
CountryIncidence of TBE per 100,000 InhabitantsStatistical Analysis
2015–20192020t (df = 4)p
Austria1.312.81−8.650.0010
Belgium0.020.06−7.760.0015
Bulgaria0.010.03−3.650.0217
Croatia0.370.340.350.7414
Czech Republic5.817.94−3.060.0376
Estonia6.775.273.000.0400
Finland1.301.65−5.020.0074
France0.020.07−7.840.0014
Germany0.500.85−4.740.0091
Greece0.010.001.500.2080
Hungary0.200.180.500.6436
Ireland0.000.001.000.3739
Italy0.050.09−3.630.0222
Latvia6.437.81−1.730.1590
Lithuania17.8324.30−2.500.0666
Luxembourg0.040.001.000.3739
Norway0.370.76−4.320.0124
Poland0.460.303.240.0318
Romania0.010.001.500.2080
Slovakia2.363.39−2.710.0537
Slovenia4.948.92−5.420.0056
Spain0.000.00--
Sweden3.172.592.360.0780
t—result of the statistical test, p—probability, df—degrees of freedom.
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Zając, Z.; Bartosik, K.; Kulisz, J.; Woźniak, A. Incidence of Tick-Borne Encephalitis during the COVID-19 Pandemic in Selected European Countries. J. Clin. Med. 2022, 11, 803. https://doi.org/10.3390/jcm11030803

AMA Style

Zając Z, Bartosik K, Kulisz J, Woźniak A. Incidence of Tick-Borne Encephalitis during the COVID-19 Pandemic in Selected European Countries. Journal of Clinical Medicine. 2022; 11(3):803. https://doi.org/10.3390/jcm11030803

Chicago/Turabian Style

Zając, Zbigniew, Katarzyna Bartosik, Joanna Kulisz, and Aneta Woźniak. 2022. "Incidence of Tick-Borne Encephalitis during the COVID-19 Pandemic in Selected European Countries" Journal of Clinical Medicine 11, no. 3: 803. https://doi.org/10.3390/jcm11030803

APA Style

Zając, Z., Bartosik, K., Kulisz, J., & Woźniak, A. (2022). Incidence of Tick-Borne Encephalitis during the COVID-19 Pandemic in Selected European Countries. Journal of Clinical Medicine, 11(3), 803. https://doi.org/10.3390/jcm11030803

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