Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in South-Western Slovakia
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25980768
PubMed Central
PMC4435654
DOI
10.1186/s13071-015-0880-8
PII: 10.1186/s13071-015-0880-8
Knihovny.cz E-zdroje
- MeSH
- Anaplasma phagocytophilum izolace a purifikace MeSH
- časové faktory MeSH
- ehrlichióza epidemiologie přenos MeSH
- ekosystém MeSH
- hlodavci MeSH
- klíště mikrobiologie MeSH
- kvantitativní polymerázová řetězová reakce MeSH
- nemoci hlodavců epidemiologie mikrobiologie přenos MeSH
- nymfa mikrobiologie MeSH
- rozšíření zvířat MeSH
- velkoměsta MeSH
- zdroje nemoci * mikrobiologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Slovenská republika epidemiologie MeSH
- velkoměsta MeSH
BACKGROUND: Ixodes ricinus is the principal vector of Anaplasma phagocytophilum, the ethiological agent of granulocytic anaplasmosis in Europe. Anaplasmosis is an emerging zoonotic disease with a natural enzootic cycle. The reservoir competence of rodents is unclear. Monitoring of A. phagocytophilum prevalence in I. ricinus and rodents in various habitat types of Slovakia may contribute to the knowledge about the epidemiology of anaplasmosis in Central Europe. METHODS: Over 4400 questing ixodid ticks, 1000 rodent-attached ticks and tissue samples of 606 rodents were screened for A. phagocytophilum DNA by real-time PCR targeting the msp2 gene. Ticks and rodents were captured along six transects in an urban/suburban and natural habitat in south-western Slovakia during 2011-2014. Estimates of wildlife (roe deer, red deer, fallow deer, mouflon, wild boar) densities in the study area were taken from hunter's yearly reports. Spatial and temporal differences in A. phagocytophilum prevalence in questing I. ricinus and relationships with relative abundance of ticks and wildlife were analysed. RESULTS: Overall prevalence of A. phagocytophilum in questing I. ricinus was significantly higher in the urban/suburban habitat (7.2%; 95% CI: 6.1-8.3%) compared to the natural habitat (3.1%; 95% CI: 2.5-3.9%) (χ(2) = 37.451; P < 0.001). Significant local differences in prevalence of infected questing ticks were found among transects within each habitat as well as among years and between seasons. The trapped rodents belonged to six species. Apodemus flavicollis and Myodes glareolus prevailed in both habitats, Microtus arvalis was present only in the natural habitat. I. ricinus comprised 96.3% of the rodent-attached ticks, the rest were Haemaphysalis concinna, Ixodes trianguliceps and Dermacentor reticulatus. Only 0.5% of rodent skin and 0.6% of rodent-attached ticks (only I. ricinus) were infected with A. phagocytophilum. Prevalence of A. phagocytophilum in questing I. ricinus did not correlate significantly with relative abundance of ticks or with abundance of wildlife in the area. CONCLUSION: The study confirms that urban I. ricinus populations are infected with A. phagocytophilum at a higher rate than in a natural habitat of south-western Slovakia and suggests that rodents are not the main reservoirs of the bacterium in the investigated area.
Institute of Virology Slovak Academy of Sciences Dúbravská cesta 9 845 05 Bratislava Slovakia
Institute of Zoology Slovak Academy of Sciences Dúbravská cesta 9 845 06 Bratislava Slovakia
Zobrazit více v PubMed
Rikihisa Y. The tribe Ehrlichieae and ehrlichial diseases. Clin Microbiol Rev. 1991;4:286–308. PubMed PMC
Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC, et al. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol. 2001;51:2145–65. doi: 10.1099/00207713-51-6-2145. PubMed DOI
Stuen S, Granquist EG, Silaghi C. Anaplasma phagocytophilum - a widespread multihost pathogen with highly adaptive strategies. Front Cell Infect Microbiol. 2013;3:31. doi: 10.3389/fcimb.2013.00031. PubMed DOI PMC
Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G, et al. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health. 2014;2:251. doi: 10.3389/fpubh.2014.00251. PubMed DOI PMC
Nováková M, Víchová B, Majláthová V, Lesňáková A, Pochybová M, Peťko B. First case of human granulocytic anaplasmosis from Slovakia. Ann Agric Environ Med. 2010;17:173–5. PubMed
Ogden NH, Bown K, Horrocks BK, Woldehiwet Z, Bennett M. Granulocytic Ehrlichia infection in ixodid ticks and mammals in woodlands and uplands of the UK. Med Vet Entomol. 1998;12:423–9. doi: 10.1046/j.1365-2915.1998.00133.x. PubMed DOI
Liz JS, Anderes L, Sumner JW, Massung RF, Gern L, Rutti B, et al. PCR detection of granulocytic ehrlichiae in Ixodes ricinus ticks and wild small mammals in western Switzerland. J Clin Microbiol. 2000;38:1002–7. PubMed PMC
Petrovec M, Sixl W, Schweiger R, Mikulasek S, Elke L, Wüst G, et al. Infections of wild animals with Anaplasma phagocytophila in Austria and the Czech Republic. Ann N Y Acad Sci. 2003;990:103–6. doi: 10.1111/j.1749-6632.2003.tb07345.x. PubMed DOI
Bown KJ, Begon M, Bennett M, Birtles RJ, Burthe S, Lambin X, et al. Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom. Vector Borne Zoonotic Dis. 2006;6:404–10. doi: 10.1089/vbz.2006.6.404. PubMed DOI
Bown KJ, Lambin X, Telford GR, Ogden NH, Telfer S, Woldehiwet Z, et al. Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Appl Environ Microbiol. 2008;74:7118–25. doi: 10.1128/AEM.00625-08. PubMed DOI PMC
Štefančíková A, Derdáková M, Lenčáková D, Ivanová R, Stanko M, Čisláková L, et al. Serological and molecular detection of Borrelia burgdorferi sensu lato and Anaplasmataceae in rodents. Folia Microbiol. 2008;53:493–9. doi: 10.1007/s12223-008-0077-z. PubMed DOI
Overzier E, Pfister K, Herb I, Mahling M, Böck G, Jr, Silaghi C. Detection of tick-borne pathogens in roe deer (Capreolus capreolus), questing ticks (Ixodes ricinus) and ticks infesting roe deer in southern Germany. Ticks Tick Borne Dis. 2013;4:320–8. doi: 10.1016/j.ttbdis.2013.01.004. PubMed DOI
Blaňarová L, Stanko M, Carpi G, Miklisová D, Víchová B, Mošanský L, et al. Distinct Anaplasma phagocytophilum genotypes associated with Ixodes trianguliceps ticks and rodents in Central Europe. Ticks Tick Borne Dis. 2014;5:928–38. doi: 10.1016/j.ttbdis.2014.07.012. PubMed DOI
Obiegala A, Pfeffer M, Pfister K, Tiedemann T, Thiel C, Balling A, et al. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum: prevalences and investigations on a new transmission path in small mammals and ixodid ticks. Parasit Vectors. 2014;7:563. PubMed PMC
Víchová B, Majláthová V, Nováková M, Stanko M, Hviščová I, Pangrácová L, et al. Anaplasma infections in ticks and reservoir host in Slovakia. Infect Genet Evol. 2014;22:265–72. doi: 10.1016/j.meegid.2013.06.003. PubMed DOI
Strle F. Human granulocytic ehrlichiosis in Europe. Int J Med Microbiol. 2004;293:27–35. PubMed
Woldehiwet Z. The natural history of Anaplasma phagocytophilum. Vet Parasitol. 2010;167:108–22. doi: 10.1016/j.vetpar.2009.09.013. PubMed DOI
Overzier E, Pfister K, Thiel C, Herb I, Mahling M, Silaghi C. Anaplasma phagocytophilum in questing Ixodes ricinus ticks: Comparison of prevalences and partial 16S rRNA gene variants in urban, pasture, and natural habitats. Appl Environ Microbiol. 2013;79:1730–4. doi: 10.1128/AEM.03300-12. PubMed DOI PMC
Silaghi C, Gilles J, Höhle M, Fingerle V, Just FT, Pfister K. Anaplasma phagocytophilum infection in Ixodes ricinus, Bavaria, Germany. Emerg Infect Dis. 2008;14:972–4. doi: 10.3201/eid1406.071095. PubMed DOI PMC
Venclikova K, Rudolf I, Mendel J, Betasova L, Hubalek Z. Rickettsiae in questing Ixodes ricinus ticks in the Czech Republic. Ticks Tick Borne Dis. 2014;5:135–8. doi: 10.1016/j.ttbdis.2013.09.008. PubMed DOI
Massung RF, Lee K, Mauel M, Gusa A. Characterization of the rRNA genes of Ehrlichia chaffeensis and Anaplasma phagocytophila. DNA Cell Biol. 2002;21:587–96. doi: 10.1089/104454902320308960. PubMed DOI
Massung RF, Priestley RA, Levin ML. Route of transmission alters the infectivity of Anaplasma phagocytophila in mice. Ann N Y Acad Sci. 2003;990:494–5. doi: 10.1111/j.1749-6632.2003.tb07416.x. PubMed DOI
Silaghi C, Woll D, Hamel D, Pfister K, Mahling M, Pfeffer M. Babesia spp. and Anaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents – Analyzing the host pathogen-vector interface in a metropolitan area. Parasit Vectors. 2012;5:191. doi: 10.1186/1756-3305-5-191. PubMed DOI PMC
Bown KJ, Lambin X, Ogden NH, Begon M, Telford G, Woldehiwet Z, et al. Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerg Infect Dis. 2009;15:1948–54. doi: 10.3201/eid1512.090178. PubMed DOI PMC
Baráková I, Derdáková M, Carpi G, Rosso F, Collini M, Tagliapietra V, et al. Genetic and ecologic variability among Anaplasma phagocytophilum strains in Northern Italy. Emerg Infect Dis. 2014;20:1082–4. doi: 10.3201/eid2006.131023. PubMed DOI PMC
de la Fuente J, Massung RF, Wong SJ, Chu FK, Lutz H, Meli M, et al. Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. J Clin Microbiol. 2005;43:1309–17. doi: 10.1128/JCM.43.3.1309-1317.2005. PubMed DOI PMC
Derdáková M, Štefančíková A, Špitálska E, Tarageľová V, Košťálová T, Hrkľová G, et al. Emergence and genetic variability of Anaplasma species in small ruminants and ticks from Central Europe. Vet Microbiol. 2011;153:293–8. doi: 10.1016/j.vetmic.2011.05.044. PubMed DOI
Scharf W, Schauer S, Freyburger F, Petrovec M, Schaarschmidt-Kiener D, Liebisch G, et al. Distinct host species correlate with Anaplasma phagocytophilum ankA gene clusters. J Clin Microbiol. 2011;49:790–6. doi: 10.1128/JCM.02051-10. PubMed DOI PMC
Jahfari S, Coipan C, Fonville M, van Leeuwen AD, Hengeveld P, Heylen D, et al. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors. 2014;7:365. doi: 10.1186/1756-3305-7-365. PubMed DOI PMC
Siuda K. Kleszcze Polski (Acari: Ixodida). Systematyka i rozmieszczenie. Polskie Towarzystwo Parazytologiczne: Warszawa; 1993.
Stanko M. Small mammal communities of windbreaks and adjacent fields in the eastern Slovakian lowlands. Folia Zool. 1994;43:135–43.
Courtney JW, Kostelnik LM, Zeidner NS, Massung RF. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol. 2004;42:3164–8. doi: 10.1128/JCM.42.7.3164-3168.2004. PubMed DOI PMC
Derdáková M, Václav R, Pangrácova-Blaňarová L, Selyemová D, Koči J, Walder G, et al. Candidatus Neoehrlichia mikurensis and its co-circulation with Anaplasma phagocytophilum in Ixodes ricinus ticks across ecologically different habitats of Central Europe. Parasit Vectors. 2014;7:160. doi: 10.1186/1756-3305-7-160. PubMed DOI PMC
Špitalská E, Kocianová E. Agents of Ehrlichia phagocytophila group and other microorganisms co-infecting ticks in southwestern Slovakia. Acta Virol. 2002;46:49–50. PubMed
Derdáková M, Halánová M, Stanko M, Štefančíková A, Čisláková L, Peťko B. Molecular evidence for Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from eastern Slovakia. Ann Agric Environ Med. 2003;10:269–71. PubMed
Smetanová K, Schwarzová K, Kocianová E. Detection of Anaplasma phagocytophilum, Coxiella burnetii, Rickettsia spp. and Borrelia burgdorferi s. l. in ticks, and wild-living animals in western and middle Slovakia. Ann N Y Acad Sci. 2006;1078:312–5. doi: 10.1196/annals.1374.058. PubMed DOI
Špitalská E, Boldiš V, Košťanová Z, Kocianová E, Štefanidesová K. Incidence of various tick-borne microorganisms in rodents and ticks of central Slovakia. Acta Virol. 2008;52:175–9. PubMed
Koči J, Tarageľová V, Derdáková M, Selyemová D, Cíglerová I, Lenčáková D, et al. Tick seasonal dynamics and prevalence of tick-borne pathogens in Slovakia. In: Špitalská E, Kazimírová M, Kocianová E, Šustek Z, et al., editors. Zborník z Konferencie “Labudove dni”. Bratislava: Virologický ústav SAV; 2009. pp. 45–7.
Subramanian G, Sekeyova Z, Raoult D, Mediannikov O. Multiple tick-associated bacteria in Ixodes ricinus from Slovakia. Ticks Tick Borne Dis. 2012;3:406–10. doi: 10.1016/j.ttbdis.2012.10.001. PubMed DOI
Pangrácová L, Derdáková M, Pekárik L, Hviščová I, Víchová B, Stanko M, et al. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors. 2013;6:238. doi: 10.1186/1756-3305-6-238. PubMed DOI PMC
Egyed L, Elo P, Sreter-Lancz Z, Szell Z, Balogh Z, Sreter T. Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick Borne Dis. 2012;3:90–4. doi: 10.1016/j.ttbdis.2012.01.002. PubMed DOI
Strašek Smrdel K, Serdt M, Duh D, Knap N, Avšič ŽT. Anaplasma phagocytophilum in ticks in Slovenia. Parasit Vectors. 2010;3:102. doi: 10.1186/1756-3305-3-102. PubMed DOI PMC
Coipan EC, Jahfari S, Fonville M, Maassen CB, Giessen J, Takken W, et al. Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus. Front Cell Infect Microbiol. 2013;3:36. doi: 10.3389/fcimb.2013.00036. PubMed DOI PMC
Lommano E, Bertaiola L, Dupasquier C, Gern L. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in western Switzerland. Appl Environ Microbiol. 2012;78:4606–12. doi: 10.1128/AEM.07961-11. PubMed DOI PMC
Reye AL, Hübschen JM, Sausy A, Muller CP. Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol. 2010;76:2923–31. doi: 10.1128/AEM.03061-09. PubMed DOI PMC
Movila A, Rolain JM, Podavalenko A, Toderas I, Tkachenco L, Naglov V, et al. Detection of spotted fever group rickettsiae and family Anaplasmataceae in Ixodes ricinus ticks from Republic of Moldova and Eastern Ukraine. Clin Microbiol Infect. 2009;15:32–3. doi: 10.1111/j.1469-0691.2008.02152.x. PubMed DOI
Sytykiewicz H, Karbowiak G, Hapunik J, Szpechcinski A, Supergan-Marwicz M, Golawska S, et al. Molecular evidence of Anaplasma phagocytophilum and Babesia microti co-infections in Ixodes ricinus ticks in central-eastern region of Poland. Ann Agri Environ Med. 2012;19:45–9. PubMed
Welc-Falęciak R, Kowalec M, Karbowiak G, Bajer A, Behnke JM, Siński E. Rickettsiaceae and Anaplasmataceae infections in Ixodes ricinus ticks from urban and natural forested areas of Poland. Parasit Vectors. 2014;7:121. doi: 10.1186/1756-3305-7-121. PubMed DOI PMC
Schorn S, Pfister K, Reulen H, Mahling M, Manitz J, Thiel C, et al. Prevalence of Anaplasma phagocytophilum in Ixodes ricinus in Bavarian public parks, Germany. Ticks Tick Borne Dis. 2011;2:196–203. doi: 10.1016/j.ttbdis.2011.09.009. PubMed DOI
Hornok S, Meli ML, Gönczi E, Halász E, Takács N, Farkas R, et al. Occurrence of ticks and prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi s.l. in three types of urban biotopes: forests, parks and cemeteries. Ticks Tick Borne Dis. 2014;5:785–9. doi: 10.1016/j.ttbdis.2014.05.010. PubMed DOI
Vaculová T, Tarageľová V. V. Seasonal dynamics of Ixodes ricinus ticks and prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in urban parks in Bratislava. In: Oros M, Vasilková Z, editors. V4 Parasitological Meeting. Parasites in the Heart of Europe. Book of Abstracts. Košice: Slovak Society for Parasitology at SAS. 2014. p. 129.
Glatz M, Müllegger RR, Maurer F, Fingerle V, Achermann Y, Wilske B, et al. Detection of Candidatus Neoehrlichia mikurensis, Borrelia burgdorferi sensu lato genospecies and Anaplasma phagocytophilum in a tick population from Austria. Ticks Tick Borne Dis. 2014;5:139–44. doi: 10.1016/j.ttbdis.2013.10.006. PubMed DOI
Hartelt K, Oehme R, Frank H, Brockmann SO, Hassler D, Kimmig P. Pathogens and symbionts in ticks: prevalence of Anaplasma phagocytophilum (Ehrlichia sp.), Wolbachia sp., Rickettsia sp., and Babesia sp. in Southern Germany. Int J Med Microbiol. 2004;293(37):86–92. PubMed
Hildebrandt A, Franke J, Meier F, Sachse S, Dorn W, Straube E. The potential role of migratory birds in transmission cycles of Babesia spp., Anaplasma phagocytophilum, and Rickettsia spp. Ticks Tick Borne Dis. 2010;1:105–7. doi: 10.1016/j.ttbdis.2009.12.003. PubMed DOI
Oehme R, Hartelt K, Backe H, Brockmann S, Kimmig P. Foci of tick-borne diseases in southwest Germany. Int J Med Microbiol. 2002;291(Suppl 33):22–9. doi: 10.1016/S1438-4221(02)80005-4. PubMed DOI
Tappe J, Strube C. Anaplasma phagocytophilum and Rickettsia spp. infections in hard ticks (Ixodes ricinus) in the city of Hanover (Germany): Revisited. Ticks Tick Borne Dis. 2013;4:432–8. doi: 10.1016/j.ttbdis.2013.04.009. PubMed DOI
Liz JS, Sumner JW, Pfister K, Brossard M. PCR detection and serological evidence of granulocytic ehrlichial infection in roe deer (Capreolus capreolus) and chamois (Rupicapra rupicapra) J Clin Microbiol. 2002;40:892–7. doi: 10.1128/JCM.40.3.892-897.2002. PubMed DOI PMC
Oporto B, Gil H, Barral M, Hurtado A, Juste RA, García-Pérez AL. A survey on Anaplasma phagocytophila in wild small mammals and roe deer (Capreolus capreolus) in Northern Spain. Ann N Y Acad Sci. 2003;990:98–102. doi: 10.1111/j.1749-6632.2003.tb07344.x. PubMed DOI
Polin H, Hufnagl P, Haunschmid R, Gruber F, Ladurner G. Molecular evidence of Anaplasma phagocytophilum in Ixodes ricinus ticks and wild animals in Austria. J Clin Microbiol. 2004;42:2285–6. doi: 10.1128/JCM.42.5.2285-2286.2004. PubMed DOI PMC
Skarphedinsson S, Jensen PM, Kristiansen K. Survey of tick borne infections in Denmark. Emerg Infect Dis. 2005;11:1055–61. doi: 10.3201/eid1107.041265. PubMed DOI PMC
Štefanidesová K, Kocianová E, Boldiš V, Košťanová Z, Kanka P, Némethová D, et al. Evidence of Anaplasma phagocytophilum and Rickettsia helvetica infection in free-ranging ungulates in central Slovakia. Eur J Wildl Res. 2008;54:519–24. doi: 10.1007/s10344-007-0161-8. DOI
Silaghi C, Hamel D, Pfister K, Rehbein S. Babesia species and co-infection with Anaplasma phagocytophilum in free-ranging ungulates from Tyrol (Austria) Tierärztliche Mschr Vet Med Austria. 2011;98:268–74.
Chvostáč M, Berthová L, Derdáková M. Influence of local biodiversity on the ecology of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum. In: Oros M, Vasilková Z, editors. V4 Parasitological Meeting. Parasites in the Heart of Europe. Book of Abstracts. Košice: Slovak Society for Parasitology at SAS. 2014. p. 79.
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 Vet Scand. 2009;51:47. doi: 10.1186/1751-0147-51-47. PubMed DOI PMC
Mysterud A, Easterday WR, Qviller L, Viljugrein H, Ytrehus B. Spatial and seasonal variation in the prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in questing Ixodes ricinus ticks in Norway. Parasit Vectors. 2013;6:187. doi: 10.1186/1756-3305-6-187. PubMed DOI PMC
Michalik J, Stańczak J, Cieniuch S, Racewicz M, Sikora B, Dabert M. Wild boars as hosts of human-pathogenic Anaplasma phagocytophilum variants. Emerg Infect Dis. 2012;18:2094–5. doi: 10.3201/eid1806.110997. PubMed DOI PMC
Galindo RC, Ayllón N, Strašek Smrdel K, Boadella M, Beltrán-Beck B, Mazariegos M, et al. Gene expression profile suggests that pigs (Sus scrofa) are susceptible to Anaplasma phagocytophilum but control infection. Parasit Vectors. 2012;5:181. doi: 10.1186/1756-3305-5-181. PubMed DOI PMC
Keesing F, Belden LK, Daszak P, Dobson AP, Harvell CD, Holt RD, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468:647–52. doi: 10.1038/nature09575. PubMed DOI PMC
Carrade DD, Foley JE, Borjesson DL, Sykes JE. Canine granulocytic anaplasmosis: a review. J Vet Intern Med. 2009;23:1129–41. doi: 10.1111/j.1939-1676.2009.0384.x. PubMed DOI
Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W, et al. Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in the Netherlands. Appl Environ Microbiol. 2006;72:7594–601. doi: 10.1128/AEM.01851-06. PubMed DOI PMC
Hildebrandt A, Schmidt KH, Fingerle V, Wilske B, Straube E. Prevalence of granulocytic Ehrlichiae in Ixodes ricinus ticks in Middle Germany (Thuringia) detected by PCR and sequencing of a16S ribosomal DNA fragment. FEMS Microbiol Lett. 2002;211:225–30. doi: 10.1111/j.1574-6968.2002.tb11229.x. PubMed DOI
Tomanovic S, Chochlakis D, Radulovic Z, Milutinovic M, Cakic S, Mihaljica D, et al. Analysis of pathogen co-occurrence in host-seeking adult hard ticks from Serbia. Exp Appl Acarol. 2013;59:367–76. doi: 10.1007/s10493-012-9597-y. PubMed DOI
Rigó K, Gyuranecz M, Tóth AG, Földvári G. Detection of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in small mammals and ectoparasites in Hungary. Vector Borne Zoonotic Dis. 2011;11:1499–501. doi: 10.1089/vbz.2011.0608. PubMed DOI
Szekeres S, Coipan EC, Rigó K, Majorosa G, Jahfari S, Sprong H, et al. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in natural rodent and tick communities in Southern Hungary. Ticks Tick Borne Dis. 2014;6:111–6. doi: 10.1016/j.ttbdis.2014.10.004. PubMed DOI
Hartelt K, Pluta S, Oehme R, Kimmig P. Spread of ticks and tick-borne diseases in Germany due to global warming. Parasitol Res. 2008;103(Suppl 1):109–16. doi: 10.1007/s00436-008-1059-4. PubMed DOI
Špitalská E, Kocianová E. Tick-Borne microorganisms in southwestern Slovakia. Ann N Y Acad Sci. 2003;990:196–200. doi: 10.1111/j.1749-6632.2003.tb07362.x. PubMed DOI
Burri C, Schumann O, Schumann C, Gern L. Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick Borne Dis. 2014;5:245–51. doi: 10.1016/j.ttbdis.2013.11.007. PubMed DOI
Burri C, Dupasquier C, Bastic V, Gern L. Pathogens of emerging tick-borne diseases, Anaplasma phagocytophilum, Rickettsia spp., and Babesia spp., in Ixodes ticks collected from rodents at four sites in Switzerland (Canton of Bern) Vector Borne Zoonotic Dis. 2011;11:939–44. doi: 10.1089/vbz.2010.0215. PubMed DOI
Bown KJ, Negon M, Bennett M, Woldehiwet Z, Odgen NH. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (I. trianguliceps) system, United Kingdom. Emerg Infect Dis. 2003;9:63–70. doi: 10.3201/eid0901.020169. PubMed DOI PMC
Wild Small Mammals and Ticks in Zoos-Reservoir of Agents with Zoonotic Potential?
Effect of Climate and Land Use on the Spatio-Temporal Variability of Tick-Borne Bacteria in Europe
Babesia spp. in ticks and wildlife in different habitat types of Slovakia