Hedgehogs, Squirrels, and Blackbirds as Sentinel Hosts for Active Surveillance of Borrelia miyamotoi and Borrelia burgdorferi Complex in Urban and Rural Environments

. 2020 Nov 30 ; 8 (12) : . [epub] 20201130

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33266311

Grantová podpora
17-16009S Grantová Agentura České Republiky
CZ.02.1.01/16_019/0000759 Ministerstvo Školství, Mládeže a Tělovýchovy
QK1920258 Ministerstvo Zemědělství
IGA 20205007 Česká Zemědělská Univerzita v Praze
CIGA 20185006 Česká Zemědělská Univerzita v Praze

Odkazy

PubMed 33266311
PubMed Central PMC7760222
DOI 10.3390/microorganisms8121908
PII: microorganisms8121908
Knihovny.cz E-zdroje

Lyme borreliosis (LB), caused by spirochetes of the Borrelia burgdorferi sensu lato (s.l.) complex, is one of the most common vector-borne zoonotic diseases in Europe. Knowledge about the enzootic circulation of Borrelia pathogens between ticks and their vertebrate hosts is epidemiologically important and enables assessment of the health risk for the human population. In our project, we focused on the following vertebrate species: European hedgehog (Erinaceus europaeus), Northern white-breasted hedgehog (E. roumanicus), Eurasian red squirrel (Sciurus vulgaris), and Common blackbird (Turdus merula). The cadavers of accidentally killed animals used in this study constitute an available source of biological material, and we have confirmed its potential for wide monitoring of B. burgdorferi s.l. presence and genospecies diversity in the urban environment. High infection rates (90% for E. erinaceus, 73% for E. roumanicus, 91% for S. vulgaris, and 68% for T. merula) were observed in all four target host species; mixed infections by several genospecies were detected on the level of individuals, as well as in particular tissue samples. These findings show the usefulness of multiple tissue sampling as tool for revealing the occurrence of several genospecies within one animal and the risk of missing particular B. burgdorferi s.l. genospecies when looking in one organ alone.

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Lindgren E., Jaenson T. Lyme Borreliosis in Europe: Influences of Climate and Climate Change, Epidemiology, Ecology and Adaptation Measures. WHO Regional Office for Europe; Copenhagen, Denmark: 2006.

Hubálek Z. Epidemiology of lyme borreliosis. Curr. Probl. Dermatol. 2009;37:31–50. PubMed

Sykes R.A., Makiello P. An estimate of Lyme borreliosis incidence in Western Europe. J. Public Health. 2016;39:74–81. doi: 10.1093/pubmed/fdw017. PubMed DOI

Petrulioniené A., Radzišauskienè D., Ambrozaitis A., Čaplinskas S., Paulauskas A., Venalis A. Epidemiology of Lyme Disease in a highly endemic European zone. Medicina. 2020;56:115. doi: 10.3390/medicina56030115. PubMed DOI PMC

Stanek G., Strle F. Lyme borreliosis–from tick bite to diagnosis and treatment. FEMS Microbiol. Rev. 2018;42:233–258. doi: 10.1093/femsre/fux047. PubMed DOI

Canica M.M., Nato F., du Merle L., Mazie J.C., Baranton G., Postic D. Monoclonal antibodies for identification of Borrelia afzelii sp. nov. associated with late cutaneous manifestations of Lyme borreliosis. Scand. J. Infect. Dis. 1993;25:441–448. doi: 10.3109/00365549309008525. PubMed DOI

Margos G., Vollmer S.A., Cornet M., Garnier M., Fingerle V., Wilske B., Bormane A., Vitorino L., Collares-Pereira M., Drancourt M., et al. A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl. Environ. Microbiol. 2009;75:5410–5416. doi: 10.1128/AEM.00116-09. PubMed DOI PMC

Postic D., Ras N.M., Lane R.S., Hendson M., Baranton G. Expanded diversity among Californian Borrelia isolates and description of Borrelia bissettii sp. nov. (formerly Borrelia group DN127) J. Clin. Microbiol. 1998;36:3497–3504. doi: 10.1128/JCM.36.12.3497-3504.1998. PubMed DOI PMC

Baranton G., Postic D., Saint Girons I., Boerlin P., Piffaretti J.C., Assous M., Grimont P.A. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int. J. Syst. Bacteriol. 1992;42:378–383. doi: 10.1099/00207713-42-3-378. PubMed DOI

Margos G., Hojgaard A., Lane R.S., Cornet M., Fingerle V., Rudenko N., Ogden N., Aanensen D.M., Fish D., Piesman J. Multilocus sequence analysis of Borrelia bissettii strains from North America reveals a new Borrelia species, Borrelia kurtenbachii. Ticks Tick Borne Dis. 2010;1:151–158. doi: 10.1016/j.ttbdis.2010.09.002. PubMed DOI PMC

Le Fleche A., Postic D., Girardet K., Peter O., Baranton G. Characterization of Borrelia lusitaniae sp. nov. by 16S ribosomal DNA sequence analysis. Int. J. Syst. Bacteriol. 1997;47:921–925. doi: 10.1099/00207713-47-4-921. PubMed DOI

Pritt B.S., Respicio-Kingry L.B., Sloan L.M., Schriefer M.E., Replogle A.J., Bjork J., Liu G., Kingry L.C., Mead P.S., Neitzel D.F., et al. Borrelia mayonii sp. nov., a member of the Borrelia burgdorferi sensu lato complex, detected in patients and ticks in the upper midwestern United States. Int. J. Syst. Evol. Microbiol. 2016;66:4878–4880. doi: 10.1099/ijsem.0.001445. PubMed DOI PMC

Richter D., Postic D., Sertour N., Livey I., Matuschka F.R., Baranton G. Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. Int. J. Syst. Evol. Microbiol. 2006;56:873–881. doi: 10.1099/ijs.0.64050-0. PubMed DOI

Wang G., van Dam A.P., Le Fleche A., Postic D., Peter O., Baranton G., de Boer R., Spanjaard L., Dankert J. Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19) Int. J. Syst. Bacteriol. 1997;47:926–932. doi: 10.1099/00207713-47-4-926. PubMed DOI

Rudenko N., Golovchenko M., Lin T., Gao L., Grubhoffer L., Oliver J.H., Jr Delineation of a new species of the Borrelia burgdorferi Sensu Lato Complex, Borrelia americana sp. nov. J. Clin. Microbiol. 2009;47:3875–3880. doi: 10.1128/JCM.01050-09. PubMed DOI PMC

Marconi R.T., Liveris D., Schwartz I. Identification of novel insertion elements, restriction fragment length polymorphism patterns, and discontinuous 23S rRNA in Lyme disease spirochetes: Phylogenetic analyses of rRNA genes and their intergenic spacers in Borrelia japonica sp. nov. and genomic group 21038 (Borrelia andersonii sp. nov.) isolates. J. Clin. Microbiol. 1995;33:2427–2434. PubMed PMC

Postic D., Garnier M., Baranton G. Multilocus sequence analysis of atypical Borrelia burgdorferi sensu lato isolates--description of Borrelia californiensis sp. nov., and genomospecies 1 and 2. Int. J. Med. Microbiol. 2007;297:263–271. doi: 10.1016/j.ijmm.2007.01.006. PubMed DOI

Rudenko N., Golovchenko M., Grubhoffer L., Oliver J.H., Jr. Borrelia carolinensis sp. nov., a new (14th) member of the Borrelia burgdorferi Sensu Lato complex from the southeastern region of the United States. J Clin. Microbiol. 2009;47:134–141. doi: 10.1128/JCM.01183-08. PubMed DOI PMC

Ivanova L.B., Tomova A., González-Acuña D., Murúa R., Moreno C.X., Hernández C., Cabello J., Cabello C., Daniels T.J., Godfrey H.P., et al. Borrelia chilensis, a new member of the Borrelia burgdorferi sensu lato complex that extends the range of this genospecies in the Southern Hemisphere. Environ Microbiol. 2014;16:1069–1080. doi: 10.1111/1462-2920.12310. PubMed DOI PMC

Casjens S.R., Fraser-Liggett C.M., Mongodin E.F., Qiu W.G., Dunn J.J., Luft B.J., Schutzer S.E. Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J/ Bacteriol. 2011;193:1489–1490. doi: 10.1128/JB.01521-10. PubMed DOI PMC

Kawabata H., Masuzawa T., Yanagihara Y. Genomic analysis of Borrelia japonica sp. nov. isolated from Ixodes ovatus in Japan. Microbiol/ Immunol. 1993;37:843–848. doi: 10.1111/j.1348-0421.1993.tb01714.x. PubMed DOI

Margos G., Fedorova N., Kleinjan J.E., Hartberger C., Schwan T.G., Sing A., Fingerle V. Borrelia lanei sp. nov. extends the diversity of Borrelia species in California. Int. J. Syst. Evol. Microbiol. 2017;67:3872–3876. doi: 10.1099/ijsem.0.002214. PubMed DOI PMC

Fukunaga M., Hamase A., Okada K., Nakao M. Borrelia tanukii sp. nov. and Borrelia turdae sp. nov. found from ixodid ticks in Japan: Rapid species identification by 16S rRNA gene-targeted PCR analysis. Microbiol Immunol. 1996;40:877–881. doi: 10.1111/j.1348-0421.1996.tb01154.x. PubMed DOI

Masuzawa T., Takada N., Kudeken M., Fukui T., Yano Y., Ishiguro F., Kawamura Y., Imai Y., Ezaki T. Borrelia sinica sp. nov., a lyme disease-related Borrelia species isolated in China. Int. J. Syst. Evol. Microbiol. 2001;51:1817–1824. doi: 10.1099/00207713-51-5-1817. PubMed DOI

Chu C.Y., Liu W., Jiang B.G., Wang D.M., Jiang W.J., Zhao Q.M., Zhang P.H., Wang Z.X., Tang G.P., Yang H., et al. Novel genospecies of Borrelia burgdorferi sensu lato from rodents and ticks in southwestern China. J. Clin. Microbiol. 2008;46:3130–3133. doi: 10.1128/JCM.01195-08. PubMed DOI PMC

Rudenko N., Golovchenko M., Mokráček A., Piskunová N., Růžek D., Mallatová N., Grubhoffer L. Detection of Borrelia bissettii in cardiac valve tissue of a patient with endocarditis and aortic valve stenosis in the Czech Republic. J. Clin. Microbiol. 2008;46:3540–3543. doi: 10.1128/JCM.01032-08. PubMed DOI PMC

Rudenko N., Golovchenko M., Grubhoffer L., Oliver J.H., Jr Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks Tick Borne Dis. 2011;2:123–128. doi: 10.1016/j.ttbdis.2011.04.002. PubMed DOI PMC

Rudenko N., Golovchenko M., Vancová M., Clark K., Grubhoffer L., Oliver J.H., Jr Isolation of live Borrelia burgdorferi sensu lato spirochaetes from patients with undefined disorders and symptoms not typical for Lyme borreliosis. Clin. Microbiol. Infect. 2016;22:267.e9–267.e15. doi: 10.1016/j.cmi.2015.11.009. PubMed DOI

Stanek G., Reiter M. The expanding Lyme Borrelia complex--clinical significance of genomic species? Clin. Microbiol. Infect. 2011;17:487–493. doi: 10.1111/j.1469-0691.2011.03492.x. PubMed DOI

Gern L. Borrelia burgdorferi sensu lato, the agent of lyme borreliosis: Life in the wilds. Parasite. 2008;15:244–247. doi: 10.1051/parasite/2008153244. PubMed DOI

Estrada- Peña A., Jongejan F. Ticks feeding on humans: A review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp. Appl. Acarol. 1999;23:685–715. doi: 10.1023/A:1006241108739. PubMed DOI

Gern L., Rouvinez E., Toutoungi L.N., and Godfroid E. Transmission cycles of Borrelia burgdorferi sensu lato involving Ixodes ricinus and/or I. hexagonus ticks and the European hedgehog, Erinaceus europaeus, in suburban and urban areas in Switzerland. Folia Parasitol. 1997;44:309–314. PubMed

Kybicová K., Baštová K., Malý M. Detection of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing ticks Ixodes ricinus from the Czech Republic. Ticks Tick Borne Dis. 2017;8:483–487. doi: 10.1016/j.ttbdis.2017.02.007. PubMed DOI

Rizzoli A., Silaghi C., Obiegala A., Rudolf I., Hubálek Z., Földvári G., Plantard O., Vayssier-Taussat M., Bonnet S., Špitalská E., 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

Gassner F., Hansford K.M., Medlock J.M. Greener cities, a wild card for ticks? In: Braks M.A.H., van Wieren S.E., Takken W., Sprong H., editors. Ecology and Prevention of Lyme Borreliosis. Ecology and Control of Vector-Borne Diseases Volume 4. Wageningen Academic Publishers; Wageningen, The Netherlands: 2016. pp. 187–203.

Uspensky I. Tick pests and vectors (Acari: Ixodoidea) in European towns: Introduction, persistence and management. Ticks Tick Borne Dis. 2014;5:41–47. doi: 10.1016/j.ttbdis.2013.07.011. PubMed DOI

Földvári G., Rigó K., Jablonszky M., Biró N., Majoros G., Molnár V., Tóth M. Ticks and the city: Ectoparasites of the Northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks Tick Borne Dis. 2011;2:231–234. doi: 10.1016/j.ttbdis.2011.09.001. PubMed DOI

Heylen D., Lasters R., Adriaensen F., Fonville M., Sprong H., Matthysen E. Ticks and tick-borne diseases in the city: Role of landscape connectivity and green space characteristics in a metropolitan area. Sci. Total Environ. 2019;670:941–949. doi: 10.1016/j.scitotenv.2019.03.235. PubMed DOI

Hornok S., Meli M.L., Gönczi E., Halász E., Takács N., Farkas R., Hofmann-Lehmann R. 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;5:785–789. doi: 10.1016/j.ttbdis.2014.05.010. PubMed DOI

Kubiak K., Sielawa H., Dziekońska-Rynko J., Kubiak D., Rydzewska M., Dzika E. Dermacentor reticulatus ticks (Acari: Ixodidae) distribution in north-eastern Poland: An endemic area of tick-borne diseases. Exp. Appl. Acarol. 2018;75:289–298. doi: 10.1007/s10493-018-0274-7. PubMed DOI PMC

Kubiak K., Dziekońska-Rynko J., Szymańska H., Kubiak D., Dmitryjuk M., Dzika E. Questing Ixodes ricinus ticks (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in an urban area of north-eastern Poland. Exp. Appl. Acarol. 2019;78:113–126. doi: 10.1007/s10493-019-00379-z. PubMed DOI

Maetzel D., Maier W.A., Kampen H. Borrelia burgdorferi infection prevalences in questing Ixodes ricinus ticks (Acari: Ixodidae) in urban and suburban Bonn, western Germany. Parasitol. Res. 2005;95:5–12. doi: 10.1007/s00436-004-1240-3. PubMed DOI

Mancini F., Di Luca M., Toma L., Vescio F., Bianchi R., Khoury C., Marini L., Rezza G., and Ciervo A. Prevalence of tick-borne pathogens in an urban park in Rome, Italy. Ann. Agric. Environ. Med. 2014;21:723–727. doi: 10.5604/12321966.1129922. PubMed DOI

Szekeres S., van Leeuwen A.D., Tóth E., Majoros G., Sprong H., Földvári G. Road-killed mammals provide insight into tick-borne bacterial pathogen communities within urban habitats. Transbound. Emerg. Dis. 2019;66:277–286. doi: 10.1111/tbed.13019. PubMed DOI

Venclíková K., Betášová L., Sikutová S., Jedličková P., Hubálek Z., Rudolf I. Human pathogenic borreliae in Ixodes ricinus ticks in natural and urban ecosystem (Czech Republic) Acta Parasitol. 2014;59:717–720. doi: 10.2478/s11686-014-0296-1. PubMed DOI

Evans K.L., Gaston K.J., Frantz A.C., Dimon M.T., Sharp S.P., McGowan A., Dawson D.A., Walasz K., Partecke J., Burke T., et al. Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc. Biol. Sci. 2009;276:2403–2410. doi: 10.1098/rspb.2008.1712. PubMed DOI PMC

Gray J.S., Kahl O., Janetzki-Mittman C., Stein J., Guy E. Acquisition of Borrelia burgdorferi by Ixodes ricinus ticks fed on the European hedgehog, Erinaceus europaeus L. Exp. Appl. Acarol. 1994;18:485–491. doi: 10.1007/BF00051470. PubMed DOI

Hubert P., Julliard R., Biagianti S., Poulle M.L. Ecological factors driving the higher hedgehog (Erinaceus europeaus) density in an urban area compared to the adjacent rural area. Landsc. Urban Plan. 2011;103:34–43. doi: 10.1016/j.landurbplan.2011.05.010. DOI

Humair P.F., Gern L.E. Relationship between Borrelia burgdorferi sensu lato species, Eurasian red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Trop. 1998;69:213–227. doi: 10.1016/S0001-706X(97)00126-5. PubMed DOI

Humair P.F., Postic D., Wallich R., Gern L. An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralbl. Bakteriol. 1998;287:521–538. doi: 10.1016/S0934-8840(98)80194-1. PubMed DOI

Skuballa J., Oehme R., Hartelt K., Petney T., Bücher T., Kimmig P., Taraschewski H. European hedgehogs as hosts for Borrelia spp., Germany. Emerg. Infect Dis. 2007;13:952–953. doi: 10.3201/eid1306.070224. PubMed DOI PMC

Skuballa J., Petney T., Pfäffle M., Oehme R., Hartelt K., Fingerle V., Kimmig P., Taraschewski H. Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis, and B. spielmanii in hedgehogs (Erinaceus spp.) in Europe. Ticks Tick Borne Dis. 2012;3:8–13. doi: 10.1016/j.ttbdis.2011.09.008. PubMed DOI

Taragel’ová V., Koči J., Hanincová K., Kurtenbach K., Derdáková M., Ogden N.H., Literák I., Kocianová E., Labuda M. Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of borreliosis in Central Europe. Appl. Environ. Microbiol. 2008;74:1289–1293. doi: 10.1128/AEM.01060-07. PubMed DOI PMC

Hudec K., Šťastný K. Fauna ČR Ptáci III/I (pěvci) 2nd ed. Academia; Prague, Czech Republic: 2011. pp. 278–289.

Wilson D.E., Lacher T.E., Mittermeier R.A. Handbook of the Mammals of the World. Volume 6: Lagomorphs and Rodents I. Lynx Edicions and IUCN; Barcelona, Spain: 2016. p. 987.

Wilson D.E., Mittermeier R.A. Handbook of the Mammals of the World. Volume 8: Insectivores, Sloths and Colugos. Lynx Edicions and IUCN; Barcelona, Spain: 2018. p. 710.

Bolfíková B., Hulva P. Microevolution of sympatry: Landscape genetics of hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe. Heredity (Edinb) 2012;108:248–255. doi: 10.1038/hdy.2011.67. PubMed DOI PMC

Černá Bolfíková B., Eliášová K., Loudová M., Kryštufek B., Lymberakis P., Sándor A.D., Hulva P. Glacial allopatry vs. postglacial parapatry and peripatry: The case of hedgehogs. PeerJ. 2017;5:e3163. doi: 10.7717/peerj.3163. PubMed DOI PMC

Hönig V., Palus M., Kašpar T., Zemanová M., Majerová K., Hofmannová L., Papežík P., Šikutová S., Rettich F., Hubálek Z., et al. Multiple Lineages of Usutu Virus (Flaviviridae, Flavivirus) in Blackbirds (Turdus merula) and Mosquitoes (Culex pipiens, Cx. modestus) in the Czech Republic (2016–2019). Microorganisms. 2019;7:568. PubMed PMC

Kasahara T., Miyazaki T., Nitta H., Ono A., Miyagishima T., Nagao T., Urushidani T. Evaluation of methods for duration of preservation of RNA quality in rat liver used for transcriptome analysis. J. Toxicol. Sci. 2006;31:509–519. doi: 10.2131/jts.31.509. PubMed DOI

Heylen D.J.A., Tijsse E., Fonville M., Matthysen E., Sprong H. Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ. Microbiol. 2013;15:663–673. doi: 10.1111/1462-2920.12059. PubMed DOI

Demaerschalck I., Ben Messaoud A., De Kesel M., Hoyois B., Lobet Y., Hoet P., Bigaignon G., Bollen A., Godfroid E. Simultaneous presence of different Borrelia burgdorferi genospecies in biological fluids of Lyme disease patients. J. Clin. Microbiol. 1995;33:602–608. doi: 10.1128/JCM.33.3.602-608.1995. PubMed DOI PMC

Agresti A. Categorical Data Analysis. 2nd ed. John Wiley & Sons; Hoboken, NJ, USA: 2002.

Hothorn T., Hornik K., van de Wiel M.A., Zeileis A. Implementing a class of permutation tests: The coin package. J. Stat. Softw. 2008;28:1–23. doi: 10.18637/jss.v028.i08. PubMed DOI

Cutler S., Vayssier-Taussat M., Estrada-Peña A., Potkonjak A., Mihalca A.D., Zeller H. A new Borrelia on the block: Borrelia miyamotoi—A human health risk? Euro Surveill. 2019;24:1800170. doi: 10.2807/1560-7917.ES.2019.24.18.1800170. PubMed DOI PMC

Crowder C.D., Carolan H.E., Rounds M.A., Hönig V., Mothes B., Haag H., Nolte O., Luft B.J., Grubhoffer L., Ecker D.J., et al. Prevalence of Borrelia miyamotoi in Ixodes Ticks in Europe and the United States. Emerg. Infect. Dis. 2014;20:1678–1682. doi: 10.3201/eid2010.131583. PubMed DOI PMC

Page S., Daschkin C., Anniko S., Krey V., Nicolaus C., Maxeiner H.G. First report of Borrelia miyamotoi in an Ixodes ricinus tick in Augsburg, Germany. Exp. Appl. Acarol. 2018;74:191–199. doi: 10.1007/s10493-018-0220-8. PubMed DOI

Răileanu C., Tauchmann O., Vasić A., Wöhnke E., Silaghi C. Borrelia miyamotoi and Borrelia burgdorferi (sensu lato) identification and survey of tick-borne encephalitis virus in ticks from north-eastern Germany. Parasit. Vectors. 2020;13:106. doi: 10.1186/s13071-020-3969-7. PubMed DOI PMC

Morán Cadenas F., Rais O., Humair P.F., Douet V., Moret J., Gern L. Identification of host bloodmeal source and Borrelia burgdorferi sensu lato in field-collected Ixodes ricinus ticks in Chaumont (Switzerland) J. Med. Entomol. 2007;44:1109–1117. doi: 10.1093/jmedent/44.6.1109. PubMed DOI

Pisanu B., Chapuis J.L., Dozières A., Basset F., Poux V., Vourc´h G. High prevalence of Borrelia burgdorferi s. l. in the European res squirrel in France. Ticks Tick Borne Dis. 2014;5:1–6. doi: 10.1016/j.ttbdis.2013.07.007. PubMed DOI

Ruyts S.C., Frazer-Mendelewska E., Van Den Berge K., Verheyen K., Sprong H. Molecular detection of tick-borne pathogens Borrelia afzelii, Borrelia miyamotoi and Anaplasma phagocytophilum in Eurasian red squirrels (Sciurus vulgaris) Eur. J. Wildl. Res. 2017;63:43. doi: 10.1007/s10344-017-1104-7. DOI

Mysterud A., Stigum V.M., Jaarsma R.I., Sprong H. Genospecies of Borrelia burgdorferi s. l. detected in 16 mammal species and questing ticks from northern Europe. Sci. Rep. 2019;9:5088. doi: 10.1038/s41598-019-41686-0. PubMed DOI PMC

Krawczyk A.I., van Leeuwen A.D., Jacobs-Reitsma W., Wijnands L.M., Bouw E., Jahfari S., van Hoek A.H., van der Giessen J.W., Roelfsema J.H., Kroes M., et al. Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas. Parasit. Vectors. 2015;8:210. doi: 10.1186/s13071-015-0814-5. PubMed DOI PMC

Szekeres S., Majláthová V., Majláth I., Földvári G. Neglected hosts: The role of lacertid lizards and medium-sized mammals in the eco-epidemiology of Lyme borreliosis. In: Braks M.A.H., van Wieren S.E., Takken W., Sprong H., editors. Ecology and Prevention of Lyme Borreliosis. Ecology and Control of Vector-Borne Diseases Volume 4. Wageningen Academic Publishers; Wageningen, The Netherlands: 2016. pp. 103–126.

Jahfari S., Ruyts S.C., Frazer-Mendelewska E., Jaarsma R., Verheyen K., Sprong H. Melting pot of tick-borne zoonoses: The European hedgehog contributes to the maintenance of various tick-borne diseases in natural cycles urban and suburban areas. Parasit. Vectors. 2017;10:134. doi: 10.1186/s13071-017-2065-0. PubMed DOI PMC

Dumitrache M.O., Paştiu A.I., Kalmár Z., Mircean V., Sándor A.D., Gherman C.M., Peştean C., Mihalca A.D., Cozma V. Northern white-breasted hedgehogs Erinaceus roumanicus as hosts for ticks infected with Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in Romania. Ticks Tick Borne Dis. 2013;4:214–217. doi: 10.1016/j.ttbdis.2012.11.010. PubMed DOI

Dziemian S., Sikora B., Pilacinska P., Michalik J., Zwolak R. Ectoparasite loads in sympatric urban populations of the Northern white-breasted and the European hedgehog. Parasitol. Res. 2015;114:2317–2323. doi: 10.1007/s00436-015-4427-x. PubMed DOI PMC

Heylen D.J.A. Ecological interactions between songbirds, ticks, and Borrelia burfdorferi s.l. In: Braks M.A.H., van Wieren S.E., Takken W., Sprong H., editors. Europe. In Ecology and Prevention of Lyme Borreliosis. Ecology and Control of Vector-Borne Diseases Volume 4. Wageningen Academic Publishers; Wageningen, The Netherlands: 2016. pp. 91–101.

Mtierová Z., Derdáková M., Chvostáč M., Didyk Y.M., Mangová B., Rusňáková Tarageľová V., Selyemová D., Šujanová A., Václav R. Local population structure and seasonal variability of Borrelia garinii genotypes in Ixodes ricinus ticks, Slovakia. Int. J. Environ. Res. Public Health. 2020;17:3607. doi: 10.3390/ijerph17103607. PubMed DOI PMC

Norte A.C., Margos G., Becker N.S., Ramos J.A., Núncio M.S., Fingerle V., Araújo P.M., Adamík P., Alivizatos H., Barba E., et al. Host dispersal shapes the population structure of a tick-borne bacterial pathogen. Mol. Ecol. 2020;29:485–501. doi: 10.1111/mec.15336. PubMed DOI

Margos G., Fingerle V., Reynolds S. Borrelia bavariensis: Vector switch, niche invasion, and geographical spread of a tick-borne bacterial parasite. Front. Ecol. Evol. 2019;7:401. doi: 10.3389/fevo.2019.00401. DOI

Heylen D.J.A., Sprong H., Krawczyk A., Van Houtte N., Genné D., Gomez-Chamorro A., van Oers K., Voordouw M.J. Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds. Sci. Rep. 2017;7:39596. doi: 10.1038/srep39596. PubMed DOI PMC

Franke J., Moldenhauer A., Hildebrandt A., Dorn W. Are birds reservoir hosts for Borrelia afzelii? Ticks Tick Borne Dis. 2010;1:109–112. doi: 10.1016/j.ttbdis.2010.03.001. PubMed DOI

Tichá L., Golovchenko M., Oliver J.H., Grubhoffer L., Rudenko N. Sensitivity of Lyme borreliosis spirochetes to serum complement of regular Zoo animals: Potential reservoir competence of some exotic vertebrates. Vector Borne Zoonotic Dis. 2016;16:13–19. doi: 10.1089/vbz.2015.1847. PubMed DOI

Norte A.C., de Carvalho I.L., Núncio M.S., Araújo P.M., Matthysen E., Ramos J.A., Sprong H., Heylen D. Getting under the bird´s skin-tissue tropism of Borrelia burgdorferi s.l. in naturally and experimentally infected avian hosts. Microb. Ecol. 2020;79:756–769. doi: 10.1007/s00248-019-01442-3. PubMed DOI

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