Babesia spp. in ticks and wildlife in different habitat types of Slovakia
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27207099
PubMed Central
PMC4874003
DOI
10.1186/s13071-016-1560-z
PII: 10.1186/s13071-016-1560-z
Knihovny.cz E-zdroje
- Klíčová slova
- Babesia spp., Birds, Haemaphysalis concinna, Ixodes ricinus, Piroplasmida, Rodents, Slovakia,
- MeSH
- Babesia izolace a purifikace MeSH
- divoká zvířata mikrobiologie MeSH
- hlodavci mikrobiologie parazitologie MeSH
- klíšťata mikrobiologie MeSH
- klíště mikrobiologie MeSH
- prevalence MeSH
- ptáci 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 MeSH
BACKGROUND: Babesiosis is an emerging and potentially zoonotic disease caused by tick-borne piroplasmids of the Babesia genus. New genetic variants of piroplasmids with unknown associations to vectors and hosts are recognized. Data on the occurrence of Babesia spp. in ticks and wildlife widen the knowledge on the geographical distribution and circulation of piroplasmids in natural foci. Questing and rodent-attached ticks, rodents, and birds were screened for the presence of Babesia-specific DNA using molecular methods. Spatial and temporal differences of Babesia spp. prevalence in ticks and rodents from two contrasting habitats of Slovakia with sympatric occurrence of Ixodes ricinus and Haemaphysalis concinna ticks and co-infections of Candidatus N. mikurensis and Anaplasma phagocytophilum were investigated. RESULTS: Babesia spp. were detected in 1.5 % and 6.6 % of questing I. ricinus and H. concinna, respectively. Prevalence of Babesia-infected I. ricinus was higher in a natural than an urban/suburban habitat. Phylogenetic analysis showed that Babesia spp. from I. ricinus clustered with Babesia microti, Babesia venatorum, Babesia canis, Babesia capreoli/Babesia divergens, and Babesia odocoilei. Babesia spp. amplified from H. concinna segregated into two monophyletic clades, designated Babesia sp. 1 (Eurasia) and Babesia sp. 2 (Eurasia), each of which represents a yet undescribed novel species. The prevalence of infection in rodents (with Apodemus flavicollis and Myodes glareolus prevailing) with B. microti was 1.3 % in an urban/suburban and 4.2 % in a natural habitat. The majority of infected rodents (81.3 %) were positive for spleen and blood and the remaining for lungs and/or skin. Rodent-attached I. ricinus (accounting for 96.3 %) and H. concinna were infected with B. microti, B. venatorum, B. capreoli/B. divergens, Babesia sp. 1 (Eurasia), and Babesia sp. 2 (Eurasia). All B. microti and B. venatorum isolates were identical to known zoonotic strains from Europe. Less than 1.0 % of Babesia-positive ticks and rodents carried Candidatus N. mikurensis or A. phagocytophilum. CONCLUSION: Our findings suggest that I. ricinus and rodents play important roles in the epidemiology of zoonotic Babesia spp. in south-western Slovakia. Associations with vertebrate hosts and the pathogenicity of Babesia spp. infecting H. concinna ticks need to be further explored.
CONICET C1033AAJ Buenos Aires Argentina
Institute of Zoology Slovak Academy of Sciences Dúbravská cesta 9 845 06 Bratislava Slovakia
Instituto de Patobiología CICVyA INTA Castelar 1686 Hurlingham Prov de Buenos Aires Argentina
Zobrazit více v PubMed
Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison D. Babesia: A world emerging. Infect Genet Evol. 2012;12:1788–1809. doi: 10.1016/j.meegid.2012.07.004. PubMed DOI
Yabsley MJ, Shock BC. Natural history of zoonotic Babesia: Role of wildlife reservoirs. Int J Parasitol Parasites Wildl. 2013;2:18–31. doi: 10.1016/j.ijppaw.2012.11.003. PubMed DOI PMC
Skrabalo Z, Deanovic Z. Piroplasmosis in man: report on a case. Doc Med Geogr Trop. 1957;9:11–16. PubMed
Hildebrandt A, Gray JS, Hunfeld KP. Human babesiosis in Europe: what clinicians need to know. Infection. 2013;41:1057–1072. doi: 10.1007/s15010-013-0526-8. PubMed DOI
Mørch K, Holmaas G, Frolander PS, Kristoffersen EK. Severe human Babesia divergens infection in Norway. Int J Infect Dis. 2014;33:37–38. doi: 10.1016/j.ijid.2014.12.034. PubMed DOI
Public Health Authority of the Slovak Republic (http://www.uvzsr.sk/en/). Accessed 4 dec 2015.
Hunfeld KP, Hildebrandt A, Gray JS. Babesiosis: recent insights into an ancient disease. Int J Parasitol. 2008;38:1219–1237. doi: 10.1016/j.ijpara.2008.03.001. PubMed DOI
Baneth G, Florin Christensen M, Cardoso L, Schnittger L. Reclassification of Theileria annae as Babesia vulpes sp. nov. Parasit Vectors. 2015;8:207. doi: 10.1186/s13071-015-0830-5. PubMed DOI PMC
Hildebrandt A, Hunfeld KP, Baier M, Krumbholz A, Sachse S, Lorenzen T, et al. First confirmed autochthonous case of human Babesia microti infection in Europe. Eur J Clin Microbiol Infect Dis. 2007;26:595–601. doi: 10.1007/s10096-007-0333-1. PubMed DOI
Gray J, Zintl A, Hildebrandt A, Hunfeld KP, Weiss L. Zoonotic babesiosis: overview of the disease and novel aspects of pathogen identity. Ticks Tick Borne Dis. 2010;1:3–10. doi: 10.1016/j.ttbdis.2009.11.003. PubMed DOI
Kazimírová M, Hamšíková Z, Kocianová E, Marini G, Mojšová M, Mahríková L, et al. Relative density of host-seeking ticks in different habitat types of south-western Slovakia. Exp Appl Acarol. 2016;69:205–24. doi:10.1007/s10493-016-0025-6. PubMed
Blaňarová L, Stanko M, Miklisová D, Víchová B, Mošanský L, Kraljik J, et al. Presence of Candidatus Neoehrlichia mikurensis and Babesia microti in rodents and two tick species (Ixodes ricinus and Ixodes trianguliceps) in Slovakia. Ticks Tick Borne Dis. 2016;7:319–326. doi: 10.1016/j.ttbdis.2015.11.008. PubMed DOI
Švehlová A, Berthová L, Sallay B, Boldiš V, Sparagano OAE, Špitalská E. Sympatric occurrence of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks and Rickettsia and Babesia species in Slovakia. Ticks Tick Borne Dis. 2014;5:600–605. doi: 10.1016/j.ttbdis.2014.04.010. PubMed DOI
Nosek J. The ecology, bionomics and behaviour of Haemaphysalis (Haemaphysalis) concinna tick. Z Parasitenkd. 1971;36:233–241. PubMed
Hornok S, Kováts D, Csörgő T, Meli ML, Gönczi E, Hadnagy Z, et al. Birds as potential reservoirs of tick-borne pathogens: first evidence of bacteraemia with Rickettsia helvetica. Parasit Vectors. 2014;7:128. doi: 10.1186/1756-3305-7-128. PubMed DOI PMC
Homer MJ, Aguilar-Delfin I, Telford SR, III, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13:451–469. doi: 10.1128/CMR.13.3.451-469.2000. PubMed DOI PMC
Silaghi C, Woll D, Hamel D, Pfister K, Mahling M, Pfeffer M. Babesia spp. and Anaplasma phagocytophilum in questing ticks, ticks parasiting rodents and the parasitized rodents – analyzing the host-pathogen vector interface in metropolitan area. Parasit Vectors. 2012;5:191. doi: 10.1186/1756-3305-5-191. PubMed DOI PMC
Hasle G. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect Microbiol. 2013;3:48. doi: 10.3389/fcimb.2013.00048. PubMed DOI PMC
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. 45–47.
Duh D, Slovák M, Saksida A, Strašek K, Petrovec M, Avsic Zupanc T. Molecular detection of Babesia canis in Dermacentor reticulatus ticks collected in Slovakia. Biologia (Bratisl) 2006;61:231–233. doi: 10.2478/s11756-006-0035-7. DOI
Chandoga P, Goldová M, Baranová D, Kozák M. First cases of canine babesiosis in the Slovak Republic. Vet Rec. 2002;150:82–84. doi: 10.1136/vr.150.3.82. PubMed DOI
Fuehrer HP, Biro N, Harl J, Worliczek HL, Beiglböck C, Farkas R, et al. Molecular detection of Theileria sp. ZS TO4 in red deer (Cervus elaphus) and questing Haemaphysalis concinna ticks in Eastern Austria. Vet Parasitol. 2013;197:653–657. doi: 10.1016/j.vetpar.2013.07.005. PubMed DOI
Hornok S, Takács N, Kontschán J, György Z, Micsutka A, Iceton S, et al. Diversity of Haemaphysalis-associated piroplasms of ruminants in Central-Eastern Europe, Hungary. Parasit Vectors. 2015;8:627. doi: 10.1186/s13071-015-1236-0. PubMed DOI PMC
Shock BC, Moncayo A, Cohen S, Michell EA, Williamson PC, Lopez G, et al. Diversity of piroplasms detected in blood-fed and questing ticks from several states in the United States. Ticks Tick Borne Dis. 2014;14:373–380. doi: 10.1016/j.ttbdis.2014.01.003. PubMed DOI
Paulauskas A, Radzijevskaja J, Mardosaitė-Busaitienė D, Aleksandravičienė A, Galdikas M, Krikštolaitis R. New localities of Dermacentor reticulatus ticks in the Baltic countries. Ticks Tick Borne Dis. 2015;6:630–635. doi: 10.1016/j.ttbdis.2015.05.007. PubMed DOI
Svitálková Z, Haruštiaková D, Mahríková L, Berthová L, Slovák M, Kocianová E, et al. Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in South-Western Slovakia. Parasit Vectors. 2015;8:276. doi: 10.1186/s13071-015-0880-8. PubMed DOI PMC
Berthová L, Slobodník V, Slobodník R, Olekšák M, Sekeyová Z, Svitálková Z, et al. The natural infection of birds and ticks feeding on birds with Rickettsia spp. and Coxiella burnetii in Slovakia. Exp Appl Acarol. 2016;68:299–314. doi: 10.1007/s10493-015-9975-3. PubMed DOI
Casati S, Sager H, Gern L, Piffaretti JC. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med. 2006;13:65–70. PubMed
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111–120. doi: 10.1007/BF01731581. PubMed DOI
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC
Hamšíková Svitálková Z, Haruštiaková D, Mahríková L, Mojšová M, Berthová L, Slovák M, et al. Candidatus Neoehrlichia mikurensis in ticks and rodents from urban and natural habitats of South-Western Slovakia. Parasit Vectors. 2016;9:2. doi: 10.1186/s13071-015-1287-2. PubMed DOI PMC
Corp IBM. IBM SPSS Statistics for windows, version 22.0. Armonk, NY: IBM Corp; 2013.
34. StatSoft, Inc. STATISTICA (data analysis software system), version 12. 2013. www.statsoft.com. Accessed 2 Feb 2016
Reye AL, Hübschen JM, Sausy A, Müller CP. Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol. 2010;76:2923–2931. doi: 10.1128/AEM.03061-09. PubMed DOI PMC
Schorn S, Pfister K, Reulen H, Mahling M, Silaghi C. Occurrence of Babesia spp., Rickettsia spp. and Bartonella spp. in Ixodes ricinus in Bavarian public parks, Germany. Parasit Vectors. 2011;4:135. doi: 10.1186/1756-3305-4-135. PubMed DOI PMC
Katargina O, Geller J, Vasilenko V, Kuznetsova T, Järvekülg L, Vene S, et al. Detection and characterization of Babesia species in Ixodes ticks in Estonia. Vector Borne Zoonot Dis. 2011;11:923–928. doi: 10.1089/vbz.2010.0199. PubMed DOI
Egyed L, Elő P, Sréter-Lancz Z, Széll Z, Balogh Z, Sréter T. Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick Borne Dis. 2012;3:90–94. doi: 10.1016/j.ttbdis.2012.01.002. PubMed DOI
Øines Ø, Radzijevskaja J, Paulauskas A, Rosef O. Prevalence and diversity of Babesia spp. in questing Ixodes ricinus ticks from Norway. Parasit Vectors. 2012;5:156. doi: 10.1186/1756-3305-5-156. PubMed DOI PMC
Overzier E, Pfister K, Thiel C, Herb I, Mahling M, Silaghi C. Diversity of Babesia and Rickettsia species in questing Ixodes ricinus: a longitudinal study in urban, pasture and natural habitats. Vector Borne Zoonot Dis. 2013;13:559–564. doi: 10.1089/vbz.2012.1278. PubMed DOI PMC
Bonnet S, Michelet L, Moutailler S, Cheval J, Hébert C, Vayssier-Taussat M, et al. Identification of parasitic communities within European ticks using next-generation sequencing. PLoS Negl Trop Dis. 2014;8:e2753. doi: 10.1371/journal.pntd.0002753. PubMed DOI PMC
Venclikova K, Mendel J, Betasova L, Hubalek Z, Rudolf I. First evidence of Babesia venatorum and Babesia capreoli in questing Ixodes ricinus ticks in the Czech Republic. Ann Agric Environ Med. 2015;22:212–214. doi: 10.5604/12321966.1152067. PubMed DOI
Capligina V, Berzina I, Bormane A, Salmane I, Vilks K, Kazarina A, et al. Prevalence and phylogenetic analysis of Babesia spp. in Ixodes ricinus and Ixodes persulcatus ticks in Latvia. Exp Appl Acarol. 2016;68:325–336. doi: 10.1007/s10493-015-9978-0. PubMed DOI
Duh D, Petrovec M, Avsic-Zupanc T. Diversity of Babesia infecting European sheep ticks (Ixodes ricinus) J Clin Microbiol. 2001;39:3395–3397. doi: 10.1128/JCM.39.9.3395-3397.2001. PubMed DOI PMC
Duh D, Petrovec M, Trilar T, Avsic-Zupanc T. The molecular evidence of Babesia microti infection in small mammals collected in Slovenia. Parasitology. 2003;126:113–117. doi: 10.1017/S0031182002002743. PubMed DOI
Karbowiak G. Zoonotic reservoir of Babesia microti in Poland. Pol J Microbiol. 2004;53:61–65. doi: 10.1099/jmm.0.05250-0. PubMed DOI
Siński E, Bajer A, Welc R, Pawełczyk A, Ogrzewalska M, Behnke JM. Babesia microti: prevalence in wild rodents and Ixodes ricinus ticks from the Mazury Lakes District of North-Eastern Poland. Int J Med Microbiol. 2006;296:137–143. doi: 10.1016/j.ijmm.2006.01.015. 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;74:7118–7125. doi: 10.1128/AEM.00625-08. PubMed DOI PMC
Beck R, Vojta L, Curković S, Mrljak V, Margaletić J, Habrun B. Molecular survey of Babesia microti in wild rodents in central Croatia. Vector Borne Zoonot Dis. 2011;11:81–83. doi: 10.1089/vbz.2009.0260. PubMed DOI
Bajer A, Welc-Falęciak R, Bednarska M, Alsarraf M, Behnke-Borowczyk J, Siński E, et al. Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of bank voles (Myodes glareolus) in NE Poland. Microb Ecol. 2014;68:196–211. doi: 10.1007/s00248-014-0390-9. PubMed DOI PMC
Obiegala A, Pfeffer M, Pfister K, Karnath C, Silaghi C. Molecular examinations of Babesia microti in rodents and rodent-attached ticks from urban and sylvatic habitats in Germany. Ticks Tick Borne Dis. 2015;6:445–449. doi: 10.1016/j.ttbdis.2015.03.005. PubMed DOI
Šebek Z. Blutparasiten der wildlebenden Kleinsäuger in der Tschechoslowakei. Folia Parasit. 1975;22:11–20. PubMed
Šebek Z, Sixl W, Stünzner D, Valová M, Hubálek Z, Troger H. Zur Kenntnis der Blutparasiten wildlebender Kleinsäuger in der Steiermark und im Burgenland. Folia Parasit. 1980;27:295–301. PubMed
Herwaldt BL, Cacciò S, Gherlinzoni F, Aspöck H, Slemenda SB, Piccaluga P, et al. Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis. 2003;9:943–948. PubMed PMC
Svitálková Z, Mydlová L, Derdáková M, Tarageľová V, Selyemová D, Kocianová E, et al. Prevalencia kliešťami prenášaných mikroorganizmov v Ixodes ricinus v urbánnej a sylvatickej oblasti na juhozápadnom Slovensku. In: Hodová I, Přikrylová I, et al., editors. X. České a slovenské parazitologické dny. Program a sborník abstraktů. Brno: Masaryk University; 2012. p. 113.
Víchová B, Haklová B, Pangrácová L, Stanko M, Bona M, Mošanský L, et al. Occurrence of ticks (Ixodida) and tick-borne pathogens in urban areas of Košice city, eastern Slovakia. In: Program and Abstracts. XII International Jena Symposium on Tick Borne Diseases. 2013;p.143. http://www.tbd-symposium.com/media/public/abs_ijstd_xii/P81_Vichova_et_al_edx.pdf. Accessed 15 Feb 2016.
Bonnet S, Jouglin M, L’Hostis M, Chauvin A. Babesia sp. EU1 from roe deer and transmission within Ixodes ricinus. Emerg Infect Dis. 2007;13:1208–1210. doi: 10.3201/eid1308.061560. PubMed DOI PMC
Bonnet S, Brisseau N, Hermouet A, Jouglin M, Chauvin A. Experimental in vitro transmission of Babesia sp. (EU1) by Ixodes ricinus. Vet Res. 2009;40:21. doi: 10.1051/vetres/2009004. PubMed DOI PMC
Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Rev Microbiol. 2003;16:622–636. doi: 10.1128/CMR.16.4.622-636.2003. PubMed DOI PMC
Duh D, Petrovec M, Bidovec A, Avsic-Zupanc T. Cervids as Babesiae hosts, Slovenia. Emerg Infect Dis. 2005;11:1121–1123. doi: 10.3201/eid1107.040724. PubMed DOI PMC
Malandrin L, Jouglin M, Sun Y, Brisseau N, Chauvin A. Redescription of Babesia capreoli (Enigk and Friedhoff, 1962) from roe deer (Capreolus capreolus): isolation, cultivation, host specificity, molecular characterisation and differentiation from Babesia divergens. Int J Parasitol. 2010;40:277–284. doi: 10.1016/j.ijpara.2009.08.008. PubMed DOI
Zintl A, Finnerty EJ, Murphy TM, de Waal T, Gray JS. Babesias of red deer (Cervus elaphus) in Ireland. Vet Res. 2011;42:7. doi: 10.1186/1297-9716-42-7. PubMed DOI PMC
Malandrin L, Jouglin M, Moreau E, Chauvin A. Individual heterogeneity in erythrocyte susceptibility to Babesia divergens is a critical factor for the outcome of experimental spleen-intact sheep infections. Vet Res. 2009;40:25. doi: 10.1051/vetres/2009008. PubMed DOI PMC
Bartlett SL, Abou-Madi N, Messick JB, Birkenheuer A, Kollias GV. Diagnosis and treatment of Babesia odocoilei in captive reindeer (Rangifer tarandus tarandus) and recognition of three novel host species. J Zoo Wildl Med. 2009;40:152–159. doi: 10.1638/2008-0011.1. PubMed DOI
Silaghi C, Hamel D, Pfister K, Rehbein S. Babesia species and coinfection with Anaplasma phagocytophilum in free-ranging ungulates from Tyrol (Austria) Tierärztl Mschr Vet Med Austria. 2011;98:268–274.
Wiegmann L, Silaghi C, Obiegala A, Karnath C, Langer S, Ternes K, et al. Occurrence of Babesia species in captive reindeer (Rangifer tarandus) in Germany. Vet Parasitol. 2015;211:16–22. doi: 10.1016/j.vetpar.2015.04.026. PubMed DOI
Cieniuch S, Stańczak J, Ruczaj A. The first detection of Babesia EU1 and Babesia canis canis in Ixodes ricinus ticks (Acari, Ixodidae) collected in urban and rural areas in northern Poland. Pol J Microbiol. 2009;58:231–236. PubMed
Stańczak J, Cieniuch S, Lass A, Biernat B, Racewicz M. Detection and quantification of Anaplasma phagocytophilum and Babesia spp. in Ixodes ricinus ticks from urban and rural environment, northern Poland, by real-time polymerase chain reaction. Exp Appl Acarol. 2015;66:63–81. doi: 10.1007/s10493-015-9887-2. 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
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 Zoonot Dis. 2011;11:939–944. doi: 10.1089/vbz.2010.0215. PubMed DOI
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;1:105–107. doi: 10.1016/j.ttbdis.2009.12.003. PubMed DOI
Rar VA, Epikhina TI, Suntsova OV, Kozlova IV, Lisak OV, Pukhovskaya NM, et al. Genetic variability of Babesia parasites in Haemaphysalis spp. and Ixodes persulcatus ticks in the Baikal region and Far East of Russia. Infect Genet Evol. 2014;28:270–275. doi: 10.1016/j.meegid.2014.10.010. PubMed DOI
Galuppi R, Aureli S, Bonoli C, Caffara M, Tampieri MP. Detection and molecular characterization of Theileria sp. in fallow deer (Dama dama) and ticks from an Italian natural preserve. Res Vet Sci. 2011;91:110–115. doi: 10.1016/j.rvsc.2010.07.029. PubMed DOI
Hasle G, Leinaas HP, Røed KH, Øines Ø. Transport of Babesia venatorum-infected Ixodes ricinus to Norway by northward migrating passerine birds. Acta Vet Scand. 2011;53:41. doi: 10.1186/1751-0147-53-41. PubMed DOI PMC
Capligina V, Salmane I, Keišs O, Vilks K, Japina K, Baumanis V, et al. Prevalence of tick-borne pathogens in ticks collected from migratory birds in Latvia. Ticks Tick Borne Dis. 2014;5:75–81. doi: 10.1016/j.ttbdis.2013.08.007. PubMed DOI
Toma L, Mancini F, Di Luca M, Cecere JG, Bianchi R, Khoury C, et al. Detection of microbial agents in ticks collected from migratory birds in central Italy. Vector Borne Zoonot Dis. 2014;14:199–205. doi: 10.1089/vbz.2013.1458. PubMed DOI PMC
Sytykiewicz H, Karbowiak G, Hapunik J, Szpechciński A, Supergan-Marwicz M, Goławska S, et al. Molecular evidence of Anaplasma phagocytophilum and Babesia microti coinfections in Ixodes ricinus ticks in central-eastern region of Poland. Ann Agric Environ Med. 2012;19:45–49. PubMed
Silaghi C, Woll D, Mahling M, Pfister K, Pfeffer M. Candidatus Neoehrlichia mikurensis in rodents in an area with sympatric existence of the hard ticks Ixodes ricinus and Dermacentor reticulatus, Germany. Parasit Vectors. 2012;5:285. doi: 10.1186/1756-3305-5-285. PubMed DOI PMC
Coipan EC, Jahfari S, Fonville M, Maassen CB, van der 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
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;12:563. PubMed PMC
Diuk-Wasser MA, Vannier E, Krause PJ. Coinfection by Ixodes tick-borne pathogens: Ecological, epidemiological, and clinical consequences. Trends Parasitol. 2016;32:30–42. doi: 10.1016/j.pt.2015.09.008. PubMed DOI PMC
Circulation of Babesia Species and Their Exposure to Humans through Ixodes Ricinus