Mini Review
Tick-borne encephalitis 2010: Epidemiology, risk areas, and virus strains in Europe and Asia—An overview

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Abstract

Over the past decades, tick-borne encephalitis (TBE) has become a growing public health concern in Europe and Asia and is the most important viral tick-borne disease in Europe. It is also important in the Far East and in other parts of Asia. Vaccination can effectively prevent TBE. It is indicated for persons inhabiting or visiting a TBE endemic area who are likely to be exposed to tick bites. For this purpose, it is necessary to know where TBE virus (TBEV) occurs, where vectors are a potential hazard, and where as a consequence autochthonous TBE cases have been registered. Natural changes in the known TBE foci and the detection of new foci necessitate a summarizing data update to optimize the protection of inhabitants and visitors to TBE endemic areas. The present review includes an overview of the epidemiological data on TBE in Europe and Asia gathered between 1990 and 2009 and describes old and especially new TBE risk areas in Europe and Asia.

Introduction

Over the past decades, tick-borne encephalitis (TBE) has become a growing public health concern in Europe and Asia and is the most important viral tick-borne disease in Europe. It is also important in the Far East and in other parts of Asia. Vaccination can effectively prevent TBE. Protective vaccination is indicated for persons inhabiting or visiting TBE areas who have an increased risk of tick bites. For this purpose, it is necessary to know where TBE virus occurs, where vectors are a potential hazard, and where as a consequence autochthonous TBE cases have been registered. Unlike Lyme borreliosis endemic regions, TBE risk areas are distributed in a patchwork pattern, sometimes the situation remains stable, sometimes changes occur due to altered climatic conditions or other factors. This review is an update of an earlier one on the same topic (Süss, 2003).

The principal vectors of TBE virus (TBEV) are the hard ticks Ixodes ricinus and I. persulcatus. I. ricinus has the primary role as a vector of TBEV-Eu and I. persulcatus of TBEV-Fe and TBEV-Sib which represent different subtypes of TBEV. In some areas of Siberia and the Far East, where I. persulcatus is not the predominant species, other hard ticks, Dermacentor reticulatus, D. silvarum, and Haemaphysalis concinna, have been associated with local TBE outbreaks (Nuttall and Labuda, 2005). In China, TBEV has been isolated from H. concinna and I. ovatus.

Zoonotic tick-borne diseases are an increasing health burden in Europe, and there is speculation that this is partly due to climate changes affecting vector biology and pathogen transmission (Gray et al., 2009). Currently, individual aspects of tick activity (Gray, 2008) and distribution (Danielová et al., 2008) as well as the distribution of risk areas (Danielová et al., 2010) suggest an influence of the climate. The remarkably high host seeking activity of I. ricinus in Berlin, Germany, in the winter 2006/07 was probably due to a very mild winter (Dautel et al., 2008), and a retrospective study suggests that hotter summers might change the dynamics and pattern of seasonal activity, resulting in the bulk of the tick population becoming active in the later part of the year (Gray, 2008). However, the nature and significance of climate change effects on the components of TBEV ecology have not yet been fully determined.

It has been reported that ticks (I. ricinus) and TBEV reach higher altitudes in the mountains, higher than in former years between 1970 and 1980 (Danielová et al., 2006, Materna et al., 2008, Daniel et al., 2008a, Holzmann et al., 2009), and spread north in Sweden (Lindgren et al., 2000, Lindgren and Jaenson, 2006, Eisen, 2008), Norway (Skarpaas et al., 2006), Finland (Jääskeläinen et al., 2006), Germany (Hemmer et al., 2005, Süss et al., 2008a) and west in Austria (Holzmann et al., 2009). Nearly all these data were collected along the fringes of tick distribution and do not apply to the core areas.

However, there are authors who dispute the influence of climate change on TBE risk areas based on the current state of knowledge (Korenberg, 2009) or hold other factors (political and sociological changes and human behaviour which influenced the tick bite exposure of humans, vaccination acceptance) responsible for the increase (or decrease) in TBE incidence (and/or distribution) (Randolph, 2008, Šumilo et al., 2007, Šumilo et al., 2008a, Šumilo et al., 2008b, Süss et al., 2008b). Randolph and Rogers (2000) predicted that the expected summer rise in temperature and decrease in moisture might progressively drive the distribution of TBEV (Ixodes ticks) into higher latitude and higher-altitude regions through the 2020s, 2050s, and 2080s.

When previously undescribed risk areas are detected, it is often hard to decide whether these areas had already existed previously and remained undetected due to the absence of humans or whether they have developed recently. Risk areas can be very large, but they can also be extremely small and contain special TBEV variants (Kupča et al., 2010).

The epidemiological knowledge of TBE should be updated from time to time to provide a solid basis for recommendations with regard to protective vaccination.

For an understanding of the eco-epidemiology of TBEV, some basic facts about the biology and ecology of the virus are first presented.

Section snippets

TBE virus classification

Taxonomically, TBE viruses belong to the tick-borne viruses within the genus Flavivirus in the family Flaviviridae (Fauquet et al., 2005). Most members of this virus genus are arthropod-borne. The mosquito-borne virus group of the genus Flavivirus includes medically important viruses such as Yellow fever virus, the 4 serotypes of Dengue virus, West Nile virus, and Japanese encephalitis virus. The group of tick-borne flaviviruses currently comprises 12 virus species divided into 2 groups,

Biology of TBE virus transmission

TBEV circulates within a ‘parasitic triangle’ of interactions between virus, vector ticks, and tick hosts and is able to persist in a given habitat over long periods of time (Nuttall, 1999).

The occurrence of vector ticks and suitable vertebrates on which ticks can become infected are crucial for virus existence in a given area. The following mechanisms of virus transmission between ticks occur: (i) feeding/cofeeding (Labuda et al., 1993a, Labuda et al., 1993b), (ii) transovarial transmission,

Changes in TBE epidemiology since 1990

Over the past decades, TBE has become a growing public health concern in Europe and other parts of the world (Süss, 2003, Süss, 2008, Kunze and ISW-TBE, 2007, Kunze and ISW-TBE, 2008a, Kunze and ISW-TBE, 2008b, Kunze and ISW-TBE, 2010).

TBEV is endemic in areas extending from central and Eastern Europe to Siberia and parts of Asia. More and more TBEV endemic areas are being detected, especially in Asia, and therefore a large number of new data must be expected.

TBEV occurs in central Europe, the

Key epidemiological concepts

Unfortunately, country data are not fully comparable because, even though many countries with mandatory notification use a case definition based on clinical and laboratory data, these definitions vary between countries. Other endemic countries such as Switzerland, Russia, Latvia, Lithuania, Slovakia, and Norway do not have a formal case definition at all. Epidemiological data would be comparable more directly if, at least at the European level, endemic countries were to use a common TBE case

Endemic area definition

An area endemic for TBEV is defined as an area with proven TBEV circulation between ticks and vertebrate hosts as determined by the detection of TBEV or the confirmation of autochthonous infections in animals or humans in the past 20 years. The development of a natural TBE focus depends on a variety of factors, including the population dynamics of vector ticks and there hosts and the presence of susceptible host species.

However, the reason for the patchy distribution of TBE is not quite clear.

TBE case definition

According to Nuttall and Labuda (2005) the incidence of clinically expressed forms of human TBE is dependent on 4 main factors:

  • (i)

    degree of exposure to infected ticks,

  • (ii)

    infection prevalence in ticks, which varies in different years and in different regions, ranging from <0.1 to 5% in Europe and from 4 to 39% in Asia,

  • (iii)

    concentration of infectious virus in ticks; most people receive bites from ticks carrying low doses of virus, and only about 15% are bitten by highly infected ticks,

  • (iv)

    virulence of the

Descriptive country-by-country TBE epidemiology

TBE is endemic in 27 European countries as well as in Asia, notably in China, Japan, Kazakhstan, Mongolia, Kyrgyzstan and South Korea.

Asia

In recent years, reliable data from Asia have become available, showing that TBEV is also endemic in a number of non-European countries, such as Mongolia, Kazakhstan, Kyrgyzstan, China, Japan, and South Korea. However, because notification of TBE cases has not been mandatory, diagnostic tools have been underused, and awareness of the disease is low, the epidemiological picture is still patchy.

Conclusion

All the data presented here clearly demonstrate the importance of TBE for the individual as well as for the health care systems of these countries. Therefore, we have to continue tackling the problem of TBE with all our available capacity.

Acknowledgements

I thank the anonymous referees and the Associate Editor whose helpful suggestions have improved the review substantially.

Sincere thanks to all colleagues who generously provided their data for this review.

All data have been checked thoroughly. Should you notice any mistakes, please let the author know.

References (158)

  • E.A. Gould et al.

    Pathogenic flaviviruses

    Lancet

    (2008)
  • G. Grard et al.

    Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy

    Virology

    (2007)
  • J.S. Gray

    Ixodes ricinus seasonal activity: implications of global warming indicated by revisiting tick and weather data

    Int. J. Med. Microbiol.

    (2008)
  • M. Haglund et al.

    Tick-borne encephalitis – pathogenesis, clinical course and long-term follow-up

    Vaccine

    (2003)
  • X. Han et al.

    Studies on TBE epidemiology in Finland (and Lithuania)

    Int. J. Med. Microbiol.

    (2002)
  • D. Hayasaka et al.

    Evaluation of European tick-borne encephalitis virus vaccine against recent Siberian and Far-eastern subtype strains

    Vaccine

    (2001)
  • H. Holzmann et al.

    Molecular epidemiology of tick-borne encephalitis virus: cross-protection between European and Far Eastern subtypes

    Vaccine

    (1992)
  • E.I. Korenberg

    Problems in the study and prophylaxis of mixed infections transmitted by ixodid ticks

    Int. J. Med. Microbiol.

    (2004)
  • E.I. Korenberg

    Recent epidemiology of tick-borne encephalitis: an effect of climate change?

    Adv. Virus Res.

    (2009)
  • T. Krech

    TBE foci in Switzerland

    Int. J. Med. Microbiol.

    (2002)
  • C. Kunz

    Vaccination against TBE in Austria: the success story continues

    Int. J. Med. Microbiol.

    (2002)
  • U. Kunze et al.

    Conference report of the 9th meeting of the International Scientific Working Group of Tick-borne Encephalitis (ISW-TBE). Tick-borne Encephalitis: from epidemiology to current vaccination recommendations

    Vaccine

    (2007)
  • U. Kunze et al.

    Conference report of the 10th meeting of the International Scientific Working Group on Tick-borne Encephalitis (ISW-TBE): combating tick-borne encephalitis: vaccination rates on the rise

    Vaccine

    (2008)
  • U. Kunze et al.

    Tick-borne encephalitis: from childhood to golden age does increased mobility mean increased risk? Conference report of the 11th meeting of the International Scientific Working Group on Tick-borne Encephalitis (ISW-TBE)

    Vaccine

    (2010)
  • A.M. Kupča et al.

    Isolation and molecular characterization of a tick-borne encephalitis virus strain from a new tick-borne encephalitis focus with severe cases in Bavaria, Germany

    Ticks Tick-borne Dis.

    (2010)
  • M. Labuda et al.

    Importance of localized skin infection in tick-borne encephalitis virus transmission

    Virology

    (1996)
  • M. Labuda et al.

    Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts

    Virology

    (1997)
  • M. Labuda et al.

    Tick-borne encephalitis virus foci in Slovakia

    Int. J. Med. Microbiol.

    (2002)
  • Anonymous, 2004–2008. Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten des Robert-Koch-Instituts für...
  • Anonymous, 2007. Epi. Bull. 15, 129-135, Robert Koch Institute...
  • Anonymous, 2010. Epid. Bull. 18, 165-172, Robert Koch Institute...
  • Asokliene, L., 2004. Tick-borne encephalitis in Lithuania. Eurosurveillance Weekly 8(26).040624....
  • Atkinson, B., 2010. Of mice and men: Epidemiological surveillance of TBE in Kyrgyzstan. Vienna, Conference report of...
  • Z. Balogh et al.

    Tick-borne encephalitis outbreak in Hungary due to consumption of raw goat milk

    J. Virol. Methods

    (2009)
  • Balogh, Z., Egyed, L., Ferenczi, E., Bán, E., Szomor, K.N., Takács, M., Berencsi, G., 2011. Experimental infection of...
  • Č. Beneš

    National Reference Centre for Analysis of Epidemiological Data

    (2006)
  • Beran, J., 2004. Tick-borne encephalitis in the Czech Republic. Eurosurveillance Weekly 8....
  • D. Blaškovič

    The epidemic of encephalitis in the Roznava natural focus of infection

    Slov. Acad. Sci.

    (1954)
  • D. Blaškovič et al.

    The ecological approach to the study of tick-borne encephalitis

    Prog. Med. Virol.

    (1972)
  • H. Blystad et al.

    Tick-borne encephalitis in Norway

    EpiNorth

    (2009)
  • M. Bröker

    Tick-borne encephalitis virus within and outside Japan: a cause for concern?

    Jpn. J. Infect. Dis.

    (2002)
  • Bundesamt für Gesundheit, Bern, Switzerland, 2007....
  • E. Burenhult et al.

    Several cases of tick-borne encephalitis in Skane. Should high-risk groups be vaccinated?

    Lakartidningen

    (2002)
  • A. Cristofolini et al.

    Zoonoses transmitted by ticks in forest workers (tick-borne encephalitis and Lyme borreliosis): preliminary results

    Med. Lav.

    (1993)
  • P.A. Csango et al.

    Tick-borne encephalitis in southern Norway

    Emerg. Infect. Dis.

    (2004)
  • P. D’Ágaro et al.

    Prevalence of tick-borne encephalitis virus in Ixodes ricinus from a novel endemic area of North Eastern Italy

    J. Med. Virol.

    (2009)
  • V. Danielová et al.

    Integration of a tick-borne encephalitis virus and Borrelia burgdorferi sensu lato into mountain ecosystems, following a shift in the altitudinal limit of distribution of their vector, Ixodes ricinus (Krkonoše mountains, Czech Republic)

    Vector Borne Zoonotic Dis.

    (2010)
  • Deryabin, P., 2010. TBE in Kazakhstan. Vienna, Conference report of the 12th meeting of the International Scientific...
  • U. Dumpis et al.

    Tick-borne encephalitis

    Clin. Infect. Dis.

    (1999)
  • M. Ecker et al.

    Sequence analysis and genetic classification of tick-borne encephalitis viruses from Europe and Asia

    J. Gen. Virol.

    (1999)
  • Cited by (316)

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