Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in northern Europe with particular reference to Southern Sweden

Particle and Fibre Toxicology

Thomas GT Jaenson²  Sirkka Vene¹  Irina Golovljova³  John H-O Pettersson² 

[1] Public Health Agency of Sweden, Solna, Sweden;Medical Entomology Unit, Subdepartment of Systematic Biology, Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18d, SE-752 36, Uppsala, Sweden;Department of Virology, National Institute for Health Development, Tallinn, Estonia

关键词: Virus prevalence;    Tick-borne encephalitis virus;    TBE;    Finland;    Denmark;    Norway;    Sweden;    Real-time PCR;    Minimum infection rate;    Ixodes ricinus;   

Others  :  810593
DOI  :  10.1186/1756-3305-7-102

 received in 2014-01-02, accepted in 2014-02-16,  发布年份 2014

【 摘 要 】

Background

In northern Europe, the tick-borne encephalitis virus (TBEV) of the European subtype is usually transmitted to humans by the common tick Ixodes ricinus. The aims of the present study are (i) to obtain up-to-date information on the TBEV prevalence in host-seeking I. ricinus in southern and central Sweden; (ii) to compile and review all relevant published records on the prevalence of TBEV in ticks in northern Europe; and (iii) to analyse and try to explain how the TBE virus can be maintained in natural foci despite an apparently low TBEV infection prevalence in the vector population.

Methods

To estimate the mean minimum infection rate (MIR) of TBEV in I. ricinus in northern Europe (i.e. Denmark, Norway, Sweden and Finland) we reviewed all published TBEV prevalence data for host-seeking I. ricinus collected during 1958–2011. Moreover, we collected 2,074 nymphs and 906 adults of I. ricinus from 29 localities in Sweden during 2008. These ticks were screened for TBEV by RT-PCR.

Results

The MIR for TBEV in nymphal and adult I. ricinus was 0.28% for northern Europe and 0.23% for southern Sweden. The infection prevalence of TBEV was significantly lower in nymphs (0.10%) than in adult ticks (0.55%). At a well-known TBEV-endemic locality, Torö island south-east of Stockholm, the TBEV prevalence (MIR) was 0.51% in nymphs and 4.48% in adults of I. ricinus.

Conclusions

If the ratio of nymphs to adult ticks in the TBEV-analysed sample differs from that in the I. ricinus population in the field, the MIR obtained will not necessarily reflect the TBEV prevalence in the field. The relatively low TBEV prevalence in the potential vector population recorded in most studies may partly be due to: (i) inclusion of uninfected ticks from the ‘uninfected areas’ surrounding the TBEV endemic foci; (ii) inclusion of an unrepresentative, too large proportion of immature ticks, compared to adult ticks, in the analysed tick pools; and (iii) shortcomings in the laboratory techniques used to detect the virus that may be present in a very low concentration or undetectable state in ticks which have not recently fed.

【 授权许可】

   
2014 Pettersson et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Granström M: Tick-borne zoonoses in Europe. Clin Microbiol Infect 1997, 3:156-169.
• [2]Charrel RN, Attoui H, Butenko AM, Clegg JC, Deubel V, Frolova TV, Gould EA, Gritsun TS, Heinz FX, Labuda M, Lashkevich VA, Loktev V, Lundkvist A, Lvov DV, Mandl CW, Niedrig M, Papa A, Petrov VS, Plyusnin A, Randolph S, Süss J, Zlobin VI, de Lamballerie X: Tick-borne virus diseases of human interest in Europe. Clin Microbiol Infect 2004, 10:1040-1055.
• [3]Gritsun TS, Nuttall PA, Gould EA: Tick-borne flaviviruses. Adv Virus Res 2003, 61:317-371.
• [4]International Committee on Taxonomy of Viruses: Virus Taxonomy. 2012. Release. Available: http://ictvonline.org/virusTaxonomy.asp?version=2012 webcite Accessed on: 2013-04-22
• [5]Gritsun TS, Lashkevich VA, Gould EA: Tick-borne encephalitis. Antiviral Res 2003, 57:129-146.
• [6]European Centre for Disease Prevention and Control: Epidemiological situation of tick-borne encephalitis in the European Union and European Free Trade Association countries. ECDC 2012. doi: 10.2900/62311. Available: http://ecdc.europa.eu/en//publications/publications/tbe-in-eu-efta.pdf webcite
• [7]Süss J: Tick-borne encephalitis, epidemiology, risk areas, and virus strains in Europe and Asia-an overview. Ticks Tick Borne Dis 2010, 2011(2):2-15.
• [8]Wu X-B, Na RH, Wei S-S, Zhu J-S, Peng H-J: Distribution of tick-borne diseases in China. Parasit Vectors 2013, 6:119. BioMed Central Full Text
• [9]Ecker M, Allison SL, Meixner T, Heinz FX: Sequence analysis and genetic classification of tick-borne encephalitis viruses from Europe and Asia. J Gen Virol 1999, 80(Pt 1):179-185.
• [10]Katargina O, Russakova S, Geller J, Kondrusik M, Zajkowska J, Zygutiene M, Bormane A, Trofimova J, Golovljova I: Detection and characterization of tick-borne encephalitis virus in Baltic countries and eastern Poland. PLoS ONE 2013, 8:e61374.
• [11]Kovalev SY, Kokorev VS, Belyaeva IV: Distribution of Far-Eastern tick-borne encephalitis virus subtype strains in the former Soviet Union. J Gen Virol 2010, 91:2941-2946.
• [12]Kovalev SY, Chernykh DN, Kokorev VS, Snitkovskaya TE, Romanenko VV: Origin and distribution of tick-borne encephalitis virus strains of the Siberian subtype in the Middle Urals, the north-west of Russia and the Baltic countries. J Gen Virol 2009, 90(Pt 12):2884-2892.
• [13]Jääskeläinen AE, Tikkakoski T, Uzcategui NY, Alekseev AN, Vaheri A, Vapalahti O: Siberian subtype tick-borne encephalitis virus, Finland. Emerg Infect Dis 2006, 12:1568-1571.
• [14]Lundkvist Å, Vene S, Golovljova I, Mavtchoutko V, Forsgren M, Kalnina V, Plyusnin A: Characterization of tick-borne encephalitis virus from Latvia: evidence for co-circulation of three distinct subtypes. J Med Virol 2001, 65:730-735.
• [15]Golovljova I, Vene S, Sjölander KB, Vasilenko V, Plyusnin A, Lundkvist Å: Characterization of tick-borne encephalitis virus from Estonia. J Med Virol 2004, 74:580-588.
• [16]Haglund M, Vene S, Forsgren M, Günther G, Johansson B, Niedrig M, Plyusnin A, Lindquist L, Lundkvist A: Characterisation of human tick-borne encephalitis virus from Sweden. J Med Virol 2003, 71:610-621.
• [17]Melik W, Nilsson AS, Johansson M: Detection strategies of tick-borne encephalitis virus in Swedish Ixodes ricinus reveal evolutionary characteristics of emerging tick-borne flaviviruses. Arch Virol 2007, 152:1027-1034.
• [18]Norberg P, Roth A, Bergström T: Genetic recombination of tick-borne flaviviruses among wild-type strains. Virology 2013, 440:105-116.
• [19]Skarpaas T, Golovljova I, Vene S, Ljøstad U, Sjursen H, Plyusnin A, Lundkvist A: Tickborne encephalitis virus, Norway and Denmark. Emerging Infect Dis 2006, 12:1136-1138.
• [20]Fomsgaard A, Fertner ME, Essbauer S, Nielsen AY, Frey S, Lindblom P, Lindgren P-E, Bødker R, Weidmann M, Dobler G: Tick-borne encephalitis virus, Zealand, Denmark, 2011. Emerging Infect Dis 2013, 19:1171-1173.
• [21]Jääskeläinen AE, Sironen T, Murueva GB, Subbotina N, Alekseev AN, Castrén J, Alitalo I, Vaheri A, Vapalahti O: Tick-borne encephalitis virus in ticks in Finland, Russian Karelia and Buryatia. J Gen Virol 2010, 91(Pt 11):2706-2712.
• [22]Jääskeläinen AE, Tonteri E, Sironen T, Pakarinen L, Vaheri A, Vapalahti O: European subtype tick-borne encephalitis virus in Ixodes persulcatus ticks. Emerging Infect Dis 2011, 17:323-325.
• [23]Kaiser R: Tick-borne encephalitis. Infect Dis Clin North Am 2008, 22:561-575.
• [24]Lindquist L, Vapalahti O: Tick-borne encephalitis. Lancet 2008, 371:1861-1871.
• [25]Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR, Solomon T: Tick-borne encephalitis virus–a review of an emerging zoonosis. J Gen Virol 2009, 90(Pt 8):1781-1794.
• [26]Holmgren EB, Forsgren M: Epidemiology of tick-borne encephalitis in Sweden 1956-1989: a study of 1116 cases. Scand J Infect Dis 1990, 22:287-295.
• [27]Jaenson TGT, Hjertqvist M, Bergström T, Lundkvist A: Why is tick-borne encephalitis increasing? A review of the key factors causing the increasing incidence of human TBE in Sweden. Parasit Vectors 2012, 5:184. BioMed Central Full Text
• [28]Jaenson TGT, Jaenson DGE, Eisen L, Petersson E, Lindgren E: Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasit Vectors 2012, 5:8. BioMed Central Full Text
• [29]Brinkley C, Nolskog P, Golovljova I, Lundkvist Å, Bergström T: Tick-borne encephalitis virus natural foci emerge in western Sweden. Int J Med Microbiol 2008, 298, Supplement 1:73-80.
• [30]Blaskovic D, Nosek J: The ecological approach to the study of tick-borne encephalitis. Prog Med Virol 1972, 14:275-320.
• [31]Nosek J, Kožuch O, Mayer V: Spatial distribution and stability of natural foci of tick-borne encephalitis virus in Central Europe. In Beiträge zur Geoökologie der Zentraleuropäischen Zecken-Encephalitis. Edited by Jusatz HJ. Berlin, Heidelberg: Springer Berlin Heidelberg; 1978:60-74.
• [32]Kupča AM, Essbauer S, Zoeller G, de Mendonça PG, Brey R, Rinder M, Pfister K, Spiegel M, Doerrbecker B, Pfeffer M, Dobler G: 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, 1:44-51.
• [33]Dobler G, Hufert F, Pfeffer M, Essbauer S: Tick-borne encephalitis: From microfocus to human disease. In Progress in Parasitology. Edited by Mehlhorn H. Berlin, Heidelberg: Springer Berlin Heidelberg; 2011:323-331.
• [34]Skarphédinsson S, Lyholm BF, Ljungberg M, Søgaard P, Kolmos HJ, Nielsen LP: Detection and identification of Anaplasma phagocytophilum, Borrelia burgdorferi, and Rickettsia helvetica in Danish Ixodes ricinus ticks. APMIS 2007, 115:225-230.
• [35]Stuen S, Granquist EG, Silaghi C: Anaplasma phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies. Front Cell Infect Microbiol 2013, 3:31. doi:10.3389/fcimb.2013.0031
• [36]Hubálek Z, Halouzka J: Distribution of Borrelia burgdorferi sensu lato genomic groups in Europe, a review. Eur J Epidemiol 1997, 13:951-957.
• [37]Blaschitz M, Narodoslavsky-Gföller M, Kanzler M, Walochnik J, Stanek G: Borrelia burgdorferi sensu lato genospecies in questing Ixodes ricinus ticks in Austria. Int J Med Microbiol 2008, 298:168-176.
• [38]Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier P-E, Raoult D: Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 2013, 26:657-702.
• [39]Wallménius K, Pettersson JH-O, Jaenson TGT, Nilsson K: Prevalence of Rickettsia spp., Anaplasma phagocytophilum, and Coxiella burnetii in adult Ixodes ricinus ticks from 29 study areas in central and southern Sweden. Ticks Tick Borne Dis 2012, 3:100-106.
• [40]Mejlon HA, Jaenson TGT: Seasonal prevalence of Borrelia burgdorferi in Ixodes ricinus in different vegetation types in Sweden. Scand J Infect Dis 1993, 25:449-456.
• [41]Arthur DR: British Ticks. London: Butterworths; 1963.
• [42]Filippova NA: Fauna of the SSSR, Paukoobraznye: Arachnidea. Ixodid ticks of subfamily Ixodinae. Volume 4(4). Russian: Leningrad: Nauka; 1977.
• [43]Von Zeipel G: Isolation of viruses of the Russian spring summer encephalitis-louping ill group from Swedish ticks and from a human case of meningoencephalitis. Arch Gesamte Virusforsch 1959, 9:460-469.
• [44]Brummer-Korvenkontio M, Saikku P, Korhonen P, Oker-Blom N: Arboviruses in Finland: I: isolation of tick-borne encephalitis (TBE) virus from arthropods, vertebrates, and patients. Am J Trop Med Hyg 1973, 22:382-389.
• [45]Han X, Aho M, Vene S, Peltomaa M, Vaheri A, Vapalahti O: Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in Finland. J Med Virol 2001, 64:21-28.
• [46]Andreassen A, Jore S, Cuber P, Dudman S, Tengs T, Isaksen K, Hygen HO, Viljugrein H, Anestad G, Ottesen P, Vainio K: Prevalence of tick borne encephalitis virus in tick nymphs in relation to climatic factors on the southern coast of Norway. Parasit Vectors 2012, 5:177. BioMed Central Full Text
• [47]Jensen PM: Tætheder af skovflåten (Ixodes ricinus) og koeksistens af Louping ill-virus og tick borne encephalitis-virus på Bornholm. Ugeskr Laeger 2004, 166:2563-2565.
• [48]Fomsgaard A, Christiansen C, Bodker R: First identification of tick-borne encephalitis in Denmark outside of Bornholm, August 2009. Euro Surveill 2009, 14:36. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19325 webcite
• [49]Schwaiger M, Cassinotti P: Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol 2003, 27:136-145.
• [50]Geller J, Nazarova L, Katargina O, Leivits A, Järvekülg L, Golovljova I: Tick-borne pathogens in ticks feeding on migratory passerines in western part of Estonia. Vector Borne Zoonotic Dis 2013, 13:443-448.
• [51]Cowling DW, Gardner IA, Johnson WO: Comparison of methods for estimation of individual-level prevalence based on pooled samples. Prev Vet Med 1999, 39:211-225.
• [52]Speybroeck N, Williams CJ, Lafia KB, Devleesschauwer B, Berkvens D: Estimating the prevalence of infections in vector populations using pools of samples. Med Vet Entomol 2012, 26:361-371.
• [53]Ebert TA, Brlansky R, Rogers M: Reexamining the pooled sampling approach for estimating prevalence of infected insect vectors. Ann Entomol Soc Am 2010, 103:827-837.
• [54]Randolph SE, Green RM, Hoodless AN, Peacey MF: An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol 2002, 32:979-989.
• [55]Tälleklint L, Jaenson TG: Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden. Exp Appl Acarol 1997, 21:755-771.
• [56]Dobson ADM, Finnie TJR, Randolph SE: A modified matrix model to describe the seasonal population ecology of the European tick Ixodes ricinus: Ixodes ricinus population model. J Appl Ecol 2011, 48:1017-1028.
• [57]Süss J, Schrader C, Abel U, Voigt WP, Schosser R: Annual and seasonal variation of tick-borne encephalitis virus (TBEV) prevalence in ticks in selected hot spot areas in Germany using a nRT-PCR: results from 1997 and 1998. Zentralbl Bakteriol 1999, 289:564-578.
• [58]Milne A: The ecology of the sheep tick, Ixodes ricinus L. Parasitology 1950, 40:35-45.
• [59]Needham GR, Teel PD: Off-host physiological ecology of ixodid ticks. Annu Rev Entomol 1991, 36:659-681.
• [60]Fraenkel C-J, Garpmo U, Berglund J: Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J Clin Microbiol 2002, 40:3308-3312.
• [61]Severinsson K, Jaenson TG, Pettersson J, Falk K, Nilsson K: Detection and prevalence of Anaplasma phagocytophilum and Rickettsia helvetica in Ixodes ricinus ticks in seven study areas in Sweden. Parasit Vectors 2010, 3:66. BioMed Central Full Text
• [62]Labuda M, Jones LD, Williams T, Danielova V, Nuttall PA: Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. J Med Entomol 1993, 30:295-299.
• [63]Labuda M, Kozuch O, Zuffová E, Elecková E, Hails RS, Nuttall PA: Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 1997, 235:138-143.
• [64]Gould EA, de Lamballerie X, Zanotto PM, Holmes EC: Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 2003, 59:277-314.
• [65]Nuttall PA, Labuda M: Dynamics of infection in tick vectors and at the tick-host interface. Adv Virus Res 2003, 60:233-272.
• [66]Randolph SE: Population regulation in ticks: the role of acquired resistance in natural and unnatural hosts. Parasitology 1979, 79:141-156.
• [67]Dizij A, Kurtenbach K: Clethrionomys glareolus, but not Apodemus flavicollis, acquires resistance to lxodes ricinus L, the main European vector of Borrelia burgdorferi. Parasite Immunol 1995, 17:177-183.
• [68]Randolph SE, Gern L, Nuttall PA: Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol Today (Regul Ed) 1996, 12:472-479.
• [69]Achazi K, Růžek D, Donoso-Mantke O, Schlegel M, Ali HS, Wenk M, Schmidt-Chanasit J, Ohlmeyer L, Rühe F, Vor T, Kiffner C, Kallies R, Ulrich RG, Niedrig M: Rodents as sentinels for the prevalence of tick-borne encephalitis virus. Vector Borne Zoonotic Dis 2011, 11:641-647.
• [70]Tonteri E, Jääskeläinen AE, Tikkakoski T, Voutilainen L, Niemimaa J, Henttonen H, Vaheri A, Vapalahti O: Tick-borne encephalitis virus in wild rodents in winter, Finland, 2008–2009. Emerg Infect Dis 2011, 17:72-75.
• [71]Bakhvalova VN, Dobrotvorsky AK, Panov VV, Matveeva VA, Tkachev SE, Morozova OV: Natural tick-borne encephalitis virus infection among wild small mammals in the southeastern part of western Siberia, Russia. Vector Borne Zoonotic Dis 2006, 6:32-41.
• [72]Danielová V, Holubová J: Transovarial transmission rates of tick-borne encephalitis virus in Ixodes ricinus ticks. In Modern Acarology. 2nd edition. Edited by Dusbabek F, Bukva V. Prague, Czech Republic: SPB Academic Publishing; 1991:7-10.
• [73]Alekseev AN: Ecology of tick-borne encephalitis virus: part of Ixodidae ticks males in its circulation. Ecol Parasitol 1992, 1:48-58.
• [74]Jones LD, Davies CR, Steele GM, Nuttall PA: A novel mode of arbovirus transmission involving a nonviremic host. Science 1987, 237:775-777.
• [75]Randolph SE, Miklisová D, Lysy J, Rogers DJ, Labuda M: Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 1999, 118(Pt 2):177-186.
• [76]Nonaka E, Ebel GD, Wearing HJ: Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes. PLoS ONE 2010, 5:e11745.
• [77]Labuda M, Elečková E, Ličková M, Sabó A: Tick-borne encephalitis virus foci in Slovakia. Int J Med Microbiol 2002, 291:43-47.
• [78]Skarphédinsson S, Jensen PM, Kristiansen K: Survey of tickborne infections in Denmark. Emerg Infect Dis 2005, 11:1055-1061.
• [79]Kiffner C, Lödige C, Alings M, Vor T, Rühe F: Attachment site selection of ticks on roe deer, Capreolus capreolus. Exp Appl Acarol 2010, 53:79-94.
• [80]Zeman P, Januška J: Epizootiologic background of dissimilar distribution of human cases of Lyme borreliosis and tick-borne encephalitis in a joint endemic area. Comp Immunol Microbiol Infect Dis 1999, 22:247-260.
• [81]Süss J, Schrader C, Falk U, Wohanka N: Tick-borne encephalitis (TBE) in Germany–epidemiological data, development of risk areas and virus prevalence in field-collected ticks and in ticks removed from humans. Int J Med Microbiol 2004, 293(Suppl 37):69-79.
• [82]Bormane A, Lucenko I, Duks A, Mavtchoutko V, Ranka R, Salmina K, Baumanis V: Vectors of tick-borne diseases and epidemiological situation in Latvia in 1993–2002. Int J Med Microbiol 2004, 293(Suppl 37):36-47.
• [83]Alekseev AN, Chunikhin SP: The experimental transmission of the tick-borne encephalitis virus by ixodid ticks (the mechanisms, time periods, species and sex differences). Parazitologia 1990, 24:177-185.
• [84]Belova OA, Burenkova LA, Karganova GG: Different tick-borne encephalitis virus (TBEV) prevalences in unfed versus partially engorged ixodid ticks—evidence of virus replication and changes in tick behavior. Ticks Tick Borne Dis 2012, 3:240-246.
• [85]Kuypers J, Wright N, Ferrenberg J, Huang M-L, Cent A, Corey L, Morrow R: Comparison of real-time PCR assays with fluorescent-antibody assays for diagnosis of respiratory virus infections in children. J Clin Microbiol 2006, 44:2382-2388.
• [86]Morozova OV, Dobrotvorsky AK, Livanova NN, Tkachev SE, Bakhvalova VN, Beklemishev AB, Cabello FC: PCR detection of Borrelia burgdorferi sensu lato, tick-borne encephalitis virus, and the human granulocytic ehrlichiosis agent in Ixodes persulcatus ticks from western Siberia, Russia. J Clin Microbiol 2002, 40:3802-3804.