Landscape epidemiology of neglected tick-borne pathogens in central Europe
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
AZV no. 16-33934A
Agentura pro zdravotnický výzkum České republiky
IGA_PrF_2020_020
Palacky University Olomouc
PubMed
32966705
DOI
10.1111/tbed.13845
Knihovny.cz E-zdroje
- Klíčová slova
- Anaplasma, Babesia, Rickettsia, Candidatus Neoehrlichia mikurensis, Czech Republic,
- MeSH
- Anaplasmataceae izolace a purifikace MeSH
- Babesia izolace a purifikace MeSH
- Ixodidae mikrobiologie parazitologie MeSH
- Rickettsia izolace a purifikace MeSH
- životní prostředí MeSH
- zoonózy * mikrobiologie parazitologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Česká republika MeSH
Studies of tick-borne diseases (TBDs) in Europe focus on pathogens with principal medical importance (e.g. Lyme disease and tick-borne encephalitis), but we have limited epidemiological information on the neglected pathogens, such as the members of the genera Anaplasma, Rickettsia, Babesia and Candidatus Neoehrlichia mikurensis. Here, we integrated an extensive field sampling, laboratory analysis and GIS models to provide first publicly available information on pathogen diversity, prevalence and infection risk for four overlooked zoonotic TBDs in the Czech Republic. In addition, we assessed the effect of landscape variables on the abundance of questing ticks at different spatial scales and examined whether pathogen prevalence increased with tick density. Our data from 13,340 ticks collected in 142 municipalities showed that A. phagocytophilum (MIR = 3.5%) and Ca. Neoehrlichia mikurensis (MIR = 4.0%) pose geographically uneven risks with localized hotspots, while Rickettsia (MIR = 4.9%) and Babesia (MIR = 1.1%) had relatively homogeneous spatial distribution. Landscape variables had significant effect on tick abundance up to the scale of 1 km around the sampling sites. Questing ticks responded positively to landscape diversity and configuration, especially to forest patch density that strongly correlates with the amount of woodland-grassland ecotones. For all four pathogens, we found higher prevalence in places with higher densities of ticks, confirming the hypothesis that tick abundance amplifies the risk of TB infection. Our findings highlight the importance of landscape parameters for tick vectors, likely due to their effect on small vertebrates as reservoir hosts. Future studies should explicitly investigate the combined effect of landscape parameters and the composition and population dynamics of hosts on the host-vector-pathogen system.
Zobrazit více v PubMed
Allan, B.F., Keesing, F., & Ostfeld, R.S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology, 17(1), 267-272. https://doi.org/10.1046/j.1523-1739.2003.01260.x
Asghar, N., Petersson, M., Johansson, M., & Dinnetz, P. (2016). Local landscape effects on population dynamics of Ixodes ricinus. Geospatial Health, 11(487), 283-289. https://doi.org/10.4081/gh.2016.487
Balážová, A., Baláž, V., Ondruš, J., & Široký, P. (2020). Duplex qPCR assay for detection and quantification of Anaplasma phagocytophilum and Rickettsia spp. Ticks and Tick-Borne Diseases, 11(5), 101462. https://doi.org/10.1016/j.ttbdis.2020.101462
Brownstein, J.S., Skelly, D.K., Holford, T.R., & Fish, D. (2005). Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia, 146(3), 469-475. https://doi.org/10.1007/s00442-005-0251-9
Cowling, D.W., Gardner, I.A., & Johnson, W.O. (1999). Comparison of methods for estimation of individual-level prevalence based on pooled samples. Preventive Veterinary Medicine, 39(3), 211-225. https://doi.org/10.1016/S0167-5877(98)00131-7
Derdáková, M., Václav, R., Pangrácova-Blaňárová, L., Selyemová, D., Koči, J., Walder, G., & Špitalská, E. (2014). Candidatus Neoehrlichia mikurensis and its co-circulation with Anaplasma phagocytophilum in Ixodes ricinus ticks across ecologically different habitats of Central Europe. Parasites & Vectors, 7(1), 160. https://doi.org/10.1186/1756-3305-7-160
Dormann, C.F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., Marquéz, J.R.G., Gruber, B., Lafourcade, B., Leitão, P.J., Münkemüller, T., McClean, C., Osborne, P.E., Reineking, B., Schröder, B., Skidmore, A.K., Zurell, D., & Lautenbach, S. (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36(1), 27-46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Dumler, J.S., Choi, K.-S., Garcia-Garcia, J.C., Barat, N.S., Scorpio, D.G., Garyu, J.W., & Bakken, J.S. (2005). Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerging Infectious Diseases, 11(12), 1828.
Estrada-Peña, A. (2003). The relationships between habitat topology, critical scales of connectivity and tick abundance Ixodes ricinus in a heterogeneous landscape in northern Spain. Ecography, 26(5), 661-671.
Estrada-Peña, A. (2005). Effects of habitat suitability and landscape patterns on tick (Acarina) metapopulation processes. Landscape Ecology, 20(5), 529-541. https://doi.org/10.1007/s10980-004-3318-9
Estrada-Peña, A. (2008). Climate, niche, ticks, and models: What they are and how we should interpret them. Parasitology Research, 103(1), 87-95. https://doi.org/10.1007/s00436-008-1056-7
Estrada-Peña, A., Venzal, J.M., & Sánchez Acedo, C. (2006). The tick Ixodes ricinus: Distribution and climate preferences in the western Palaearctic. Medical and Veterinary Entomology, 20(2), 189-197. https://doi.org/10.1111/j.1365-2915.2006.00622.x
Estrada-Peña, A.(2001). Forecasting habitat suitability for ticks and prevention of tick-borne diseases. Veterinary Parasitology, 98(1-3), 111-132. https://doi.org/10.1016/S0304-4017(01)00426-5
Ferrell, A.M., & Brinkerhoff, R.J. (2018). Using landscape analysis to test hypotheses about drivers of tick abundance and infection prevalence with Borrelia burgdorferi. International Journal of Environmental Research and Public Health, 15(4), 737. https://doi.org/10.3390/ijerph15040737
Fick, S.E., & Hijmans, R.J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302-4315. https://doi.org/10.1002/joc.5086
Gassner, F., vanVliet, A.J.H., Burgers, S.L.G.E., Jacobs, F., Verbaarschot, P., Hovius, E.K.E., & Takken, W. (2011). Geographic and temporal variations in population dynamics of Ixodes ricinus and associated Borrelia infections in The Netherlands. Vector-Borne and Zoonotic Diseases, 11(5), 523-532.
Gray, J.S., Kahl, O., Janetzki, C., & Stein, J. (1992). Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology, 29(6), 915-920. https://doi.org/10.1093/jmedent/29.6.915
Hartelt, K., Oehme, R., Frank, H., Brockmann, S.O., Hassler, D., & Kimmig, P. (2004). Pathogens and symbionts in ticks: Prevalence of Anaplasma phagocytophilum (Ehrlichia sp.), Wolbachia sp., Rickettsia sp., and Babesia sp. in Southern Germany. International Journal of Medical Microbiology Supplements, 293, 86-92.
Herwaldt, B.L., Cacciò, S., Gherlinzoni, F., Aspöck, H., Slemenda, S.B., Piccaluga, P., & Poletti, G. (2003). Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerging Infectious Diseases, 9(8), 943.
Hönig, V., Švec, P., Marek, L., Mrkvička, T., Dana, Z., Wittmann, M., Masař, O., Szturcová, D., Růžek, D., Pfister, K., & Grubhoffer, L. (2019). Model of risk of exposure to Lyme borreliosis and tick-borne encephalitis virus-infected ticks in the border area of the Czech Republic (South Bohemia) and Germany (Lower Bavaria and Upper Palatinate). International Journal of Environmental Research and Public Health, 16(7), 1173. https://doi.org/10.3390/ijerph16071173
Hrazdilová, K., Rybářová, M., Široký, P., Votýpka, J., Zintl, A., Burgess, H., & Modrý, D. (2020). Diversity of Babesia spp. in cervid ungulates based on the 18S rDNA and cytochrome c oxidase subunit I phylogenies. Infection, Genetics and Evolution, 77, 104060.
Hrkľová, G., Nováková, M., Chytra, M., Kostova, C., & Petko, B. (2008). Monitoring the distribution and abundance of Ixodes ricinus ticks in relevance of climate change and prevalence of Borrelia burgdorferi sensu lato in Northern Slovakia (Liptovska valley). Folia Veterinaria, 52(2), 62-63.
Jahfari, S., Coipan, E., Fonville, M., vanLeeuwen, A., Hengeveld, P., Heylen, D., Heyman, P., vanMaanen, C., Butler, C.M., Földvári, G., Szekeres, S., vanDuijvendijk, G., Tack, W., Rijks, J.M., van derGiessen, J., Takken, W., vanWieren, S.E., Takumi, K., & Sprong, H. (2014). Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasites & Vectors, 7(1), 365. https://doi.org/10.1186/1756-3305-7-365
Jones, E.O., Webb, S.D., Ruiz-Fons, F.J., Albon, S., & Gilbert, L. (2011). The effect of landscape heterogeneity and host movement on a tick-borne pathogen. Theoretical Ecology, 4(4), 435-448. https://doi.org/10.1007/s12080-010-0087-8
Keesing, F., Holt, R.D., & Ostfeld, R.S. (2006). Effects of species diversity on disease risk. Ecology Letters, 9(4), 485-498. https://doi.org/10.1111/j.1461-0248.2006.00885.x
Kitron, U. (2000). Risk maps: Transmission and burden of vector-borne diseases. Parasitology Today, 16(8), 324-325. https://doi.org/10.1016/S0169-4758(00)01708-7
Kříž, B., Daniel, M., Beneš, Č., & Malý, M. (2014). The role of game (wild boar and roe deer) in the spread of tick-borne encephalitis in the Czech Republic. Vector-Borne and Zoonotic Diseases, 14(11), 801-807. https://doi.org/10.1089/vbz.2013.1569
Labuda, M., Jones, L.D., Williams, T., Danielova, V., & Nuttall, P.A. (1993). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. Journal of Medical Entomology, 30(1), 295-299. https://doi.org/10.1093/jmedent/30.1.295
Lindström, A., & Jaenson, T.G.T. (2003). Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. Journal of Medical Entomology, 40(4), 375-378.
Marino, P.C., & Landis, D.A. (1996). Effect of landscape structure on parasitoid diversity and parasitism in agroecosystems. Ecological Applications, 6(1), 276-284. https://doi.org/10.2307/2269571
McGarigal, K. (2002). Landscape pattern metrics. In A. H.El-Shaarawi & W. W.Piegorsch (Eds.), Encyclopedia of environmetrics (Vol. 2, pp. 1135-1142). Sussex, England: John Wiley & Sons.
McGarigal, K., Cushman, S.A., & Ene, E. (2012). FRAGSTATS v4: Spatial pattern analysis program for categorical and continuous maps. Computer Software Program Produced by the Authors at the University of Massachusetts, Amherst. Available at the Following Web Site: Http://Www.Umass.Edu/landeco/research/fragstats/fragstats.Html
Medlock, J.M., Hansford, K.M., Bormane, A., Derdakova, M., Estrada-Peña, A., George, J.-C., Golovljova, I., Jaenson, T.G.T., Jensen, J.-K., Jensen, P.M., Kazimirova, M., Oteo, J.A., Papa, A., Pfister, K., Plantard, O., Randolph, S.E., Rizzoli, A., Santos-Silva, M.M., Sprong, H., … Van Bortel, W. (2013). Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites & Vectors, 6(1), 1. https://doi.org/10.1186/1756-3305-6-1
Meentemeyer, R.K., Haas, S.E., & Václavík, T. (2012). Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems. Annual Review of Phytopathology, 50(1), 379-402. https://doi.org/10.1146/annurev-phyto-081211-172938
Michel, N., Burel, F., & Butet, A. (2006). How does landscape use influence small mammal diversity, abundance and biomass in hedgerow networks of farming landscapes?Acta Oecologica, 30(1), 11-20.
Millins, C., Dickinson, E.R., Isakovic, P., Gilbert, L., Wojciechowska, A., Paterson, V., Tao, F., Jahn, M., Kilbride, E., Birtles, R., Johnson, P., & Biek, R. (2018). Landscape structure affects the prevalence and distribution of a tick-borne zoonotic pathogen. Parasites & Vectors, 11(1), 1-11. https://doi.org/10.1186/s13071-018-3200-2
Ondruš, J., Balážová, A., Baláž, V., Zechmeisterová, K., Novobilský, A., & Široký, P. (2020). Candidatus Neoehrlichia mikurensis is widespread in questing Ixodes ricinus ticks in the Czech Republic. Ticks and Tick-Borne Diseases, 11(3), 101371. https://doi.org/10.1016/j.ttbdis.2020.101371
Ostfeld, R.S., Schauber, E.M., Canham, C.D., Keesing, F., Jones, C.G., & Wolff, J.O. (2001). Effects of acorn production and mouse abundance on abundance and Borrelia burgdorferi infection prevalence of nymphal Ixodes scapularis ticks. Vector Borne and Zoonotic Diseases, 1(1), 55-63.
Oteo, J.A., & Portillo, A. (2012). Tick-borne rickettsioses in Europe. Ticks and Tick-Borne Diseases, 3(5-6), 271-278. https://doi.org/10.1016/j.ttbdis.2012.10.035
Parola, P., Paddock, C.D., Socolovschi, C., Labruna, M.B., Mediannikov, O., Kernif, T., Abdad, M.Y., Stenos, J., Bitam, I., Fournier, P.-E., & Raoult, D. (2013). Update on tick-borne rickettsioses around the world: A geographic approach. Clinical Microbiology Reviews, 26(4), 657-702. https://doi.org/10.1128/CMR.00032-13
Perez, G., Bastian, S., Agoulon, A., Bouju, A., Durand, A., Faille, F., Lebert, I., Rantier, Y., Plantard, O., & Butet, A. (2016). Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts. Parasites & Vectors, 9(1), 20. https://doi.org/10.1186/s13071-016-1296-9
Perlman, S.J., Hunter, M.S., & Zchori-Fein, E. (2006). The emerging diversity of Rickettsia. Proceedings of the Royal Society B: Biological Sciences, 273(1598), 2097-2106.
Pfäffle, M., Littwin, N., Muders, S.V., & Petney, T.N. (2013). The ecology of tick-borne diseases. International Journal for Parasitology, 43(12-13), 1059-1077. https://doi.org/10.1016/j.ijpara.2013.06.009
R Core Team (2014). R: A language and environment for statistical computing, Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/
Randolph, S.E., & Storey, K. (1999). Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): Implications for parasite transmission. Journal of Medical Entomology, 36(6), 741-748. https://doi.org/10.1093/jmedent/36.6.741
Richter, D., & Matuschka, F.-R. (2012). “Candidatus Neoehrlichia mikurensis”, Anaplasma phagocytophilum, and Lyme disease spirochetes in questing European vector ticks and in feeding ticks removed from people. Journal of Clinical Microbiology, 50(3), 943-947. https://doi.org/10.1128/JCM.05802-11
Rudolf, I., Golovchenko, M., Sikutova, S., Rudenko, N., Grubhoffer, L., & Hubalek, Z. (2005). Babesia microti (Piroplasmida: Babesiidae) in nymphal Ixodes ricinus (Acari: Ixodidae) in the Czech Republic. Folia Parasitologica, 52(3), 274. https://doi.org/10.14411/fp.2005.036
Rybářová, M., Honsová, M., Papoušek, I., & Široký, P. (2017). Variability of species of Babesia Starcovici, 1893 in three sympatric ticks (Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna) at the edge of Pannonia in the Czech Republic and Slovakia. Folia Parasitologica, 64, 28.
Rybářová, M., & Široký, P. (2017). Occurrence of Anaplasma phagocytophilum in three sympatric tick species in the South Moravia, Czech Republic. Biologia, 72(4), 365-369. https://doi.org/10.1515/biolog-2017-0051
Saïd, S., & Servanty, S. (2005). The influence of landscape structure on female roe deer home-range size. Landscape Ecology, 20(8), 1003-1012. https://doi.org/10.1007/s10980-005-7518-8
Schlinkert, H., Ludwig, M., Batáry, P., Holzschuh, A., Kovács-Hostyánszki, A., Tscharntke, T., & Fischer, C. (2016). Forest specialist and generalist small mammals in forest edges and hedges. Wildlife Biology, 22(3), 86-94. https://doi.org/10.2981/wlb.00176
Silaghi, C., Beck, R., Oteo, J.A., Pfeffer, M., & Sprong, H. (2016). Neoehrlichiosis: An emerging tick-borne zoonosis caused by Candidatus Neoehrlichia mikurensis. Experimental and Applied Acarology, 68(3), 279-297. https://doi.org/10.1007/s10493-015-9935-y
Stafford, K.C., Cartter, M.L., Magnarelli, L.A., Ertel, S.-H., & Mshar, P.A. (1998). Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. Journal of Clinical Microbiology, 36(5), 1240-1244. https://doi.org/10.1128/JCM.36.5.1240-1244.1998
Süss, J., Klaus, C., Gerstengarbe, F., & Werner, P.C. (2008). What makes ticks tick? Climate change, ticks, and tick-borne diseases. Journal of Travel Medicine, 15(1), 39-45. https://doi.org/10.1111/j.1708-8305.2007.00176.x
Svoboda, V., Máca, P., Hanel, M., & Pech, P. (2015). Spatial correlation structure of monthly rainfall at a mesoscale region of north-eastern Bohemia. Theoretical and Applied Climatology, 121(1-2), 359-375. https://doi.org/10.1007/s00704-014-1241-9
Tarrés-Call, J., Salman, M., & Estrada-Peña, A. (2013). Ticks and tick-borne diseases: Geographical distribution and control strategies in the Euro-Asia region-mini review. CAB Reviews, 8(52), 1-3. https://doi.org/10.1079/PAVSNNR20138052
Tkadlec, E., Václavík, T., Kubelová, M., & Široký, P. (2018). Negative spatial covariation in abundance of two European ticks: Diverging niche preferences or biotic interaction?Ecological Entomology, 43(6), https://doi.org/10.1111/een.12668
Tufto, J., Andersen, R., & Linnell, J. (1996). Habitat use and ecological correlates of home range size in a small cervid: The roe deer. Journal of Animal Ecology, 715-724. https://doi.org/10.2307/5670
Uilenberg, G. (2006). Babesia-a historical overview. Veterinary Parasitology, 138(1-2), 3-10. https://doi.org/10.1016/j.vetpar.2006.01.035
Venclíková, K., Mendel, J., Betášová, L., Blažejová, H., Jedličková, P., Straková, P., Hubálek, Z., & Rudolf, I. (2016). Neglected tick-borne pathogens in the Czech Republic, 2011-2014. Ticks and Tick-Borne Diseases, 7(1), 107-112. https://doi.org/10.1016/j.ttbdis.2015.09.004
Venclikova, K., Rudolf, I., Mendel, J., Betasova, L., & Hubalek, Z. (2014). Rickettsiae in questing Ixodes ricinus ticks in the Czech Republic. Ticks and Tick-Borne Diseases, 5(2), 135-138. https://doi.org/10.1016/j.ttbdis.2013.09.008
Wackernagel, H. (2013). Multivariate geostatistics: An introduction with applications. Springer-Verlag Berlin Heidelberg.
Zeman, P. (1997). Objective assessment of risk maps of tick-borne encephalitis and Lyme borreliosis based on spatial patterns of located cases. International Journal of Epidemiology, 26(5), 1121-1129. https://doi.org/10.1093/ije/26.5.1121
Role of Zoo-Housed Animals in the Ecology of Ticks and Tick-Borne Pathogens-A Review