Europe-Wide Meta-Analysis of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, metaanalýza, práce podpořená grantem
PubMed
28550059
PubMed Central
PMC5514677
DOI
10.1128/aem.00609-17
PII: AEM.00609-17
Knihovny.cz E-zdroje
- Klíčová slova
- Borrelia burgdorferi sensu lato, Ixodes ricinus, Lyme borreliosis, Lyme disease, genospecies, meta-analysis, tick,
- MeSH
- arachnida jako vektory mikrobiologie MeSH
- Borrelia burgdorferi klasifikace genetika izolace a purifikace MeSH
- klíště mikrobiologie MeSH
- lidé MeSH
- lymeská nemoc mikrobiologie přenos MeSH
- nymfa mikrobiologie MeSH
- prevalence MeSH
- zoonózy mikrobiologie přenos MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- metaanalýza MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
Lyme borreliosis is the most common zoonotic disease transmitted by ticks in Europe and North America. Despite having multiple tick vectors, the causative agent, Borrelia burgdorferisensu lato, is vectored mainly by Ixodes ricinus in Europe. In the present study, we aimed to review and summarize the existing data published from 2010 to 2016 concerning the prevalence of B. burgdorferi sensu lato spirochetes in questing I. ricinus ticks. The primary focus was to evaluate the infection rate of these bacteria in ticks, accounting for tick stage, adult tick gender, region, and detection method, as well as to investigate any changes in prevalence over time. The data obtained were compared to the findings of a previous metastudy. The literature search identified data from 23 countries, with 115,028 ticks, in total, inspected for infection with B. burgdorferi sensu lato We showed that the infection rate was significantly higher in adults than in nymphs and in females than in males. We found significant differences between European regions, with the highest infection rates in Central Europe. The most common genospecies were B. afzelii and B. garinii, despite a negative correlation of their prevalence rates. No statistically significant differences were found among the prevalence rates determined by conventional PCR, nested PCR, and real-time PCR.IMPORTANCEBorrelia burgdorferisensu lato is a pathogenic bacterium whose clinical manifestations are associated with Lyme borreliosis. This vector-borne disease is a major public health concern in Europe and North America and may lead to severe arthritic, cardiovascular, and neurological complications if left untreated. Although pathogen prevalence is considered an important predictor of infection risk, solitary isolated data have only limited value. Here we provide summarized information about the prevalence of B. burgdorferi sensu lato spirochetes among host-seeking Ixodes ricinus ticks, the principal tick vector of borreliae in Europe. We compare the new results with previously published data in order to evaluate any changing trends in tick infection.
Department of Virology Veterinary Research Institute Brno Czech Republic
Faculty of Science University of South Bohemia in České Budějovice České Budějovice Czech Republic
Zobrazit více v PubMed
Stanek G, Wormser GP, Gray J, Strle F. 2012. Lyme borreliosis. Lancet 379:461–473. doi:10.1016/S0140-6736(11)60103-7. PubMed DOI
Margos G, Vollmer SA, Cornet M, Garnier M, Fingerle V, Wilske B, Bormane A, Vitorino L, Collares-Pereira M, Drancourt M, Kurtenbach K. 2009. A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl Environ Microbiol 75:5410–5416. doi:10.1128/AEM.00116-09. PubMed DOI PMC
Strle F, Picken RN, Cheng Y, Cimperman J, Maraspin V, Lotric-Furlan S, Ruzic-Sabljic E, Picken MM. 1997. Clinical findings for patients with Lyme borreliosis caused by Borrelia burgdorferi sensu lato with genotypic and phenotypic similarities to strain 25015. Clin Infect Dis 25:273–280. doi:10.1086/514551. PubMed DOI
Rudenko N, Golovchenko M, Růzek D, Piskunova N, Mallátová N, Grubhoffer L. 2009. Molecular detection of Borrelia bissettii DNA in serum samples from patients in the Czech Republic with suspected borreliosis. FEMS Microbiol Lett 292:274–281. doi:10.1111/j.1574-6968.2009.01498.x. PubMed DOI
Collares-Pereira M, Couceiro S, Franca I, Kurtenbach K, Schäfer SM, Vitorino L, Gonçalves L, Baptista S, Vieira ML, Cunha C. 2004. First isolation of Borrelia lusitaniae from a human patient. J Clin Microbiol 42:1316–1318. doi:10.1128/JCM.42.3.1316-1318.2004. PubMed DOI PMC
da Franca I, Santos L, Mesquita T, Collares-Pereira M, Baptista S, Vieira L, Viana I, Vale E, Prates C. 2005. Lyme borreliosis in Portugal caused by Borrelia lusitaniae? Clinical report on the first patient with a positive skin isolate. Wien Klin Wochenschr 117:429–432. PubMed
Fingerle V, Schulte-Spechtel UC, Ruzic-Sabljic E, Leonhard S, Hofmann H, Weber K, Pfister K, Strle F, Wilske B. 2008. Epidemiological aspects and molecular characterization of Borrelia burgdorferi s.l. from southern Germany with special respect to the new species Borrelia spielmanii sp. nov. Int J Med Microbiol 298:279–290. doi:10.1016/j.ijmm.2007.05.002. PubMed DOI
Diza E, Papa A, Vezyri E, Tsounis S, Milonas I, Antoniadis A. 2004. Borrelia valaisiana in cerebrospinal fluid. Emerg Infect Dis 10:1692–1693. doi:10.3201/eid1009.030439. PubMed DOI PMC
Stanek G, Reiter M. 2011. The expanding Lyme Borrelia complex—clinical significance of genomic species? Clin Microbiol Infect 17:487–493. doi:10.1111/j.1469-0691.2011.03492.x. PubMed DOI
Lommano E, Bertaiola L, Dupasquier C, Gern L. 2012. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Appl Environ Microbiol 78:4606–4612. doi:10.1128/AEM.07961-11. PubMed DOI PMC
Cotté V, Bonnet S, Cote M, Vayssier-Taussat M. 2010. Prevalence of five pathogenic agents in questing Ixodes ricinus ticks from western France. Vector Borne Zoonotic Dis 10:723–730. doi:10.1089/vbz.2009.0066. PubMed DOI
Ornstein K, Berglund J, Nilsson I, Norrby R, Bergström S. 2001. Characterization of Lyme borreliosis isolates from patients with erythema migrans and neuroborreliosis in southern Sweden. J Clin Microbiol 39:1294–1298. doi:10.1128/JCM.39.4.1294-1298.2001. PubMed DOI PMC
Schorn S, Pfister K, Reulen H, Mahling M, Silaghi C. 2011. Occurrence of Babesia spp., Rickettsia spp. and Bartonella spp. in Ixodes ricinus in Bavarian public parks, Germany. Parasit Vectors 4:135. doi:10.1186/1756-3305-4-135. PubMed DOI PMC
Schwarz A, Hönig V, Vavrušková Z, Grubhoffer L, Balczun C, Albring A, Schaub GA. 2012. Abundance of Ixodes ricinus and prevalence of Borrelia burgdorferi s.l. in the nature reserve Siebengebirge, Germany, in comparison to three former studies from 1978 onwards. Parasit Vectors 5:268. doi:10.1186/1756-3305-5-268. PubMed DOI PMC
Scharlemann JPW, Johnson PJ, Smith AA, Macdonald DW, Randolph SE. 2008. Trends in ixodid tick abundance and distribution in Great Britain. Med Vet Entomol 22:238–247. doi:10.1111/j.1365-2915.2008.00734.x. PubMed DOI
Jaenson TGT, Eisen L, Comstedt P, Mejlon HA, Lindgren E, Bergström S, Olsen B. 2009. Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden. Med Vet Entomol 23:226–237. doi:10.1111/j.1365-2915.2009.00813.x. PubMed DOI
Lindgren E, Tälleklint L, Polfeldt T. 2000. Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect 108:119–123. doi:10.1289/ehp.00108119. PubMed DOI PMC
Materna J, Daniel M, Danielová V. 2005. Altitudinal distribution limit of the tick Ixodes ricinus shifted considerably towards higher altitudes in central Europe: results of three years monitoring in the Krkonose Mts. (Czech Republic). Cent Eur J Public Health 13:24–28. PubMed
Morán Cadenas F, Rais O, Jouda F, Douet V, Humair P-F, Moret J, Gern L. 2007. Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along a north- and south-facing altitudinal gradient on Chaumont Mountain, Switzerland. J Med Entomol 44:683–693. doi:10.1093/jmedent/44.4.683. PubMed DOI
Jouda F, Perret J-L, Gern L. 2004. Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. J Med Entomol 41:162–169. doi:10.1603/0022-2585-41.2.162. PubMed DOI
Rauter C, Hartung T. 2005. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl Environ Microbiol 71:7203–7216. doi:10.1128/AEM.71.11.7203-7216.2005. PubMed DOI PMC
Nazzi F, Martinelli E, Del Fabbro S, Bernardinelli I, Milani N, Iob A, Pischiutti P, Campello C, D'Agaro P. 2010. Ticks and Lyme borreliosis in an alpine area in northeast Italy. Med Vet Entomol 24:220–226. doi:10.1111/j.1365-2915.2010.00877.x. PubMed DOI
Tappe J, Jordan D, Janecek E, Fingerle V, Strube C. 2014. Revisited: Borrelia burgdorferi sensu lato infections in hard ticks (Ixodes ricinus) in the city of Hanover (Germany). Parasit Vectors 7:441. doi:10.1186/1756-3305-7-441. PubMed DOI PMC
Kalmár Z, Mihalca AD, Dumitrache MO, Gherman CM, Magdaş C, Mircean V, Oltean M, Domşa C, Matei IA, Mărcuţan DI, Sándor AD, D'Amico G, Paştiu A, Györke A, Gavrea R, Marosi B, Ionică A, Burkhardt E, Toriay H, Cozma V. 2013. Geographical distribution and prevalence of Borrelia burgdorferi genospecies in questing Ixodes ricinus from Romania: a countrywide study. Ticks Tick-Borne Dis 4:403–408. doi:10.1016/j.ttbdis.2013.04.007. PubMed DOI
Jaenson TGT, Jaenson DGE, Eisen L, Petersson E, Lindgren E. 2012. Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasit Vectors 5:8. doi:10.1186/1756-3305-5-8. PubMed DOI PMC
Kjelland V, Rollum R, Korslund L, Slettan A, Tveitnes D. 2015. Borrelia miyamotoi is widespread in Ixodes ricinus ticks in southern Norway. Ticks Tick-Borne Dis 6:516–521. doi:10.1016/j.ttbdis.2015.04.004. PubMed DOI
Hubálek Z, Halouzka J. 1998. Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitol Res 84:167–172. doi:10.1007/s004360050378. PubMed DOI
Rollend L, Fish D, Childs JE. 2013. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick-Borne Dis 4:46–51. doi:10.1016/j.ttbdis.2012.06.008. PubMed DOI
Wang H, Henbest PJ, Nuttall PA. 1999. Successful interrupted feeding of adult Rhipicephalus appendiculatus (Ixodidae) is accompanied by reprogramming of salivary gland protein expression. Parasitology 119(Part 2):143–149. doi:10.1017/S0031182099004540. PubMed DOI
van Duijvendijk G, Coipan C, Wagemakers A, Fonville M, Ersöz J, Oei A, Földvári G, Hovius J, Takken W, Sprong H. 2016. Larvae of Ixodes ricinus transmit Borrelia afzelii and B. miyamotoi to vertebrate hosts. Parasit Vectors 9:97. doi:10.1186/s13071-016-1389-5. PubMed DOI PMC
Wilhelmsson P, Lindblom P, Fryland L, Ernerudh J, Forsberg P, Lindgren P-E. 2013. Prevalence, diversity, and load of Borrelia species in ticks that have fed on humans in regions of Sweden and Åland Islands, Finland with different Lyme borreliosis incidences. PLoS One 8:e81433. doi:10.1371/journal.pone.0081433. PubMed DOI PMC
Wang G, Liveris D, Brei B, Wu H, Falco RC, Fish D, Schwartz I. 2003. Real-time PCR for simultaneous detection and quantification of Borrelia burgdorferi in field-collected Ixodes scapularis ticks from the northeastern United States. Appl Environ Microbiol 69:4561–4565. doi:10.1128/AEM.69.8.4561-4565.2003. PubMed DOI PMC
Gooskens J, Templeton KE, Claas EC, van Dam AP. 2006. Evaluation of an internally controlled real-time PCR targeting the ospA gene for detection of Borrelia burgdorferi sensu lato DNA in cerebrospinal fluid. Clin Microbiol Infect 12:894–900. doi:10.1111/j.1469-0691.2006.01509.x. PubMed DOI
Kjelland V, Ytrehus B, Stuen S, Skarpaas T, Slettan A. 2011. Prevalence of Borrelia burgdorferi in Ixodes ricinus ticks collected from moose (Alces alces) and roe deer (Capreolus capreolus) in southern Norway. Ticks Tick-Borne Dis 2:99–103. doi:10.1016/j.ttbdis.2010.12.002. PubMed DOI
Tälleklint L, Jaenson TG. 1994. Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. J Med Entomol 31:880–886. doi:10.1093/jmedent/31.6.880. PubMed DOI
Kiffner C, Lödige C, Alings M, Vor T, Rühe F. 2010. Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Exp Appl Acarol 52:73–84. doi:10.1007/s10493-010-9341-4. PubMed DOI PMC
Vor T, Kiffner C, Hagedorn P, Niedrig M, Rühe F. 2010. Tick burden on European roe deer (Capreolus capreolus). Exp Appl Acarol 51:405–417. doi:10.1007/s10493-010-9337-0. PubMed DOI PMC
Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George J-C, Golovljova I, Jaenson TGT, Jensen J-K, Jensen PM, Kazimirova M, Oteo JA, Papa A, Pfister K, Plantard O, Randolph SE, Rizzoli A, Santos-Silva MM, Sprong H, Vial L, Hendrickx G, Zeller H, Van Bortel W. 2013. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors 6:1. doi:10.1186/1756-3305-6-1. PubMed DOI PMC
Hu R, Rowley WA. 2000. Relationship between weights of the engorged nymphal stage and resultant sexes in Ixodes scapularis and Dermacentor variabilis (Acari: Ixodidae) ticks. J Med Entomol 37:198–200. doi:10.1603/0022-2585-37.1.198. PubMed DOI
Hovius JWR, Li X, Ramamoorthi N, van Dam AP, Barthold SW, van der Poll T, Speelman P, Fikrig E. 2007. Coinfection with Borrelia burgdorferi sensu stricto and Borrelia garinii alters the course of murine Lyme borreliosis. FEMS Immunol Med Microbiol 49:224–234. doi:10.1111/j.1574-695X.2006.00177.x. PubMed DOI
Kurtenbach K, De Michelis S, Etti S, Schäfer SM, Sewell H-S, Brade V, Kraiczy P. 2002. Host association of Borrelia burgdorferi sensu lato—the key role of host complement. Trends Microbiol 10:74–79. doi:10.1016/S0966-842X(01)02298-3. PubMed DOI
Semenza JC, Menne B. 2009. Climate change and infectious diseases in Europe. Lancet Infect Dis 9:365–375. doi:10.1016/S1473-3099(09)70104-5. PubMed DOI
Tälleklint L, Jaenson TG. 1998. Increasing geographical distribution and density of Ixodes ricinus (Acari: Ixodidae) in central and northern Sweden. J Med Entomol 35:521–526. doi:10.1093/jmedent/35.4.521. PubMed DOI
Danielová V, Rudenko N, Daniel M, Holubová J, Materna J, Golovchenko M, Schwarzová L. 2006. Extension of Ixodes ricinus ticks and agents of tick-borne diseases to mountain areas in the Czech Republic. Int J Med Microbiol 296(Suppl 40):S48–S53. PubMed
Mechai S, Margos G, Feil EJ, Barairo N, Lindsay LR, Michel P, Ogden NH. 2016. Evidence for host-genotype associations of Borrelia burgdorferi sensu stricto. PLoS One 11:e0149345. doi:10.1371/journal.pone.0149345. PubMed DOI PMC
Sonnleitner ST, Margos G, Wex F, Simeoni J, Zelger R, Schmutzhard E, Lass-Flörl C, Walder G. 2015. Human seroprevalence against Borrelia burgdorferi sensu lato in two comparable regions of the eastern Alps is not correlated to vector infection rates. Ticks Tick-Borne Dis 6:221–227. doi:10.1016/j.ttbdis.2014.12.006. PubMed DOI
Glatz M, Müllegger RR, Maurer F, Fingerle V, Achermann Y, Wilske B, Bloemberg GV. 2014. Detection of Candidatus Neoehrlichia mikurensis, Borrelia burgdorferi sensu lato genospecies and Anaplasma phagocytophilum in a tick population from Austria. Ticks Tick-Borne Dis 5:139–144. doi:10.1016/j.ttbdis.2013.10.006. PubMed DOI
Glatz M, Muellegger RR, Hizo-Teufel C, Fingerle V. 2014. Low prevalence of Borrelia bavariensis in Ixodes ricinus ticks in southeastern Austria. Ticks Tick-Borne Dis 5:649–650. doi:10.1016/j.ttbdis.2014.04.014. PubMed DOI
Reye AL, Hübschen JM, Sausy A, Muller CP. 2010. Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol 76:2923–2931. doi:10.1128/AEM.03061-09. PubMed DOI PMC
Reye AL, Stegniy V, Mishaeva NP, Velhin S, Hübschen JM, Ignatyev G, Muller CP. 2013. Prevalence of tick-borne pathogens in Ixodes ricinus and Dermacentor reticulatus ticks from different geographical locations in Belarus. PLoS One 8:e54476. doi:10.1371/journal.pone.0054476. PubMed DOI PMC
Michelet L, Delannoy S, Devillers E, Umhang G, Aspan A, Juremalm M, Chirico J, van der Wal FJ, Sprong H, Boye Pihl TP, Klitgaard K, Bødker R, Fach P, Moutailler S. 2014. High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol 4:103. doi:10.3389/fcimb.2014.00103. PubMed DOI PMC
Pacilly FCA, Benning ME, Jacobs F, Leidekker J, Sprong H, Van Wieren SE, Takken W. 2014. Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus. Ticks Tick-Borne Dis 5:810–817. doi:10.1016/j.ttbdis.2014.06.004. PubMed DOI
Coipan EC, Jahfari S, Fonville M, Maassen CB, van der Giessen J, Takken W, Takumi K, Sprong H. 2013. Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus. Front Cell Infect Microbiol 3:36. doi:10.3389/fcimb.2013.00036. PubMed DOI PMC
Gassner F, Takken W, Plas CL, Kastelein P, Hoetmer AJ, Holdinga M, van Overbeek LS. 2013. Rodent species as natural reservoirs of Borrelia burgdorferi sensu lato in different habitats of Ixodes ricinus in The Netherlands. Ticks Tick-Borne Dis 4:452–458. doi:10.1016/j.ttbdis.2012.11.017. PubMed DOI
Kesteman T, Rossi C, Bastien P, Brouillard J, Avesani V, Olive N, Martin P, Delmée M. 2010. Prevalence and genetic heterogeneity of Borrelia burgdorferi sensu lato in Ixodes ticks in Belgium. Acta Clin Belg 65:319–322. doi:10.1179/acb.2010.069. PubMed DOI
Tveten A-K. 2013. Prevalence of Borrelia burgdorferi sensu stricto, Borrelia afzelii, Borrelia garinii, and Borrelia valaisiana in Ixodes ricinus ticks from the northwest of Norway. Scand J Infect Dis 45:681–687. doi:10.3109/00365548.2013.799288. PubMed DOI
Mysterud A, Easterday WR, Qviller L, Viljugrein H, Ytrehus B. 2013. Spatial and seasonal variation in the prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in questing Ixodes ricinus ticks in Norway. Parasit Vectors 6:187. doi:10.1186/1756-3305-6-187. PubMed DOI PMC
Soleng A, Kjelland V. 2013. Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in Ixodes ricinus ticks in Brønnøysund in northern Norway. Ticks Tick-Borne Dis 4:218–221. doi:10.1016/j.ttbdis.2012.11.006. PubMed DOI
Kjelland V, Stuen S, Skarpaas T, Slettan A. 2010. Prevalence and genotypes of Borrelia burgdorferi sensu lato infection in Ixodes ricinus ticks in southern Norway. Scand J Infect Dis 42:579–585. doi:10.3109/00365541003716526. PubMed DOI
Hvidsten D, Stordal F, Lager M, Rognerud B, Kristiansen B-E, Matussek A, Gray J, Stuen S. 2015. Borrelia burgdorferi sensu lato-infected Ixodes ricinus collected from vegetation near the Arctic Circle. Ticks Tick-Borne Dis 6:768–773. doi:10.1016/j.ttbdis.2015.07.002. PubMed DOI
Quarsten H, Skarpaas T, Fajs L, Noraas S, Kjelland V. 2015. Tick-borne bacteria in Ixodes ricinus collected in southern Norway evaluated by a commercial kit and established real-time PCR protocols. Ticks Tick-Borne Dis 6:538–544. doi:10.1016/j.ttbdis.2015.04.008. PubMed DOI
Hodžić A, Fuehrer H-P, Duscher GG. 22 January 2016 First molecular evidence of zoonotic bacteria in ticks in Bosnia and Herzegovina. Transbound Emerg Dis doi:10.1111/tbed.12473. PubMed DOI
Skotarczak B, Wodecka B, Rymaszewska A, Adamska M. 2016. Molecular evidence for bacterial pathogens in Ixodes ricinus ticks infesting Shetland ponies. Exp Appl Acarol 69:179–189. doi:10.1007/s10493-016-0027-4. PubMed DOI PMC
Wójcik-Fatla A, Zając V, Sawczyn A, Sroka J, Cisak E, Dutkiewicz J. 2016. Infections and mixed infections with the selected species of Borrelia burgdorferi sensu lato complex in Ixodes ricinus ticks collected in eastern Poland: a significant increase in the course of 5 years. Exp Appl Acarol 68:197–212. doi:10.1007/s10493-015-9990-4. PubMed DOI PMC
Król N, Kiewra D, Szymanowski M, Lonc E. 2015. The role of domestic dogs and cats in the zoonotic cycles of ticks and pathogens. Preliminary studies in the Wrocław Agglomeration (SW Poland). Vet Parasitol 214:208–212. doi:10.1016/j.vetpar.2015.09.028. PubMed DOI
Strzelczyk JK, Gaździcka J, Cuber P, Asman M, Trapp G, Gołąbek K, Zalewska-Ziob M, Nowak-Chmura M, Siuda K, Wiczkowski A, Solarz K. 2015. Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland. Acta Parasitol 60:666–674. doi:10.1515/ap-2015-0095. PubMed DOI
Sytykiewicz H, Karbowiak G, Chorostowska-Wynimko J, Szpechciński A, Supergan-Marwicz M, Horbowicz M, Szwed M, Czerniewicz P, Sprawka I. 2015. Coexistence of Borrelia burgdorferi s.l. genospecies within Ixodes ricinus ticks from central and eastern Poland. Acta Parasitol 60:654–661. doi:10.1515/ap-2015-0093. PubMed DOI
Kiewra D, Stańczak J, Richter M. 2014. Ixodes ricinus ticks (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in Lower Silesia, Poland—preliminary study. Ticks Tick-Borne Dis 5:892–897. doi:10.1016/j.ttbdis.2014.07.004. PubMed DOI
Dunaj J, Zajkowska JM, Kondrusik M, Gern L, Rais O, Moniuszko A, Pancewicz S, Świerzbińska R. 2014. Borrelia burgdorferi genospecies detection by RLB hybridization in Ixodes ricinus ticks from different sites of North-Eastern Poland. Ann Agric Environ Med 21:239–243. doi:10.5604/1232-1966.1108583. PubMed DOI
Cisak E, Wójcik-Fatla A, Zając V, Dutkiewicz J. 2014. Prevalence of tick-borne pathogens at various workplaces in forest exploitation environment. Med Pr 65:575–581. PubMed
Asman M, Nowak M, Cuber P, Strzelczyk J, Szilman E, Szilman P, Trapp G, Siuda K, Solarz K, Wiczkowski A. 2013. The risk of exposure to Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Babesia sp. and co-infections in Ixodes ricinus ticks on the territory of Niepołomice forest (southern Poland). Ann Parasitol 59:13–19. PubMed
Wójcik-Fatla A, Zając V, Cisak E, Sroka J, Sawczyn A, Dutkiewicz J. 2012. Leptospirosis as a tick-borne disease? Detection of Leptospira spp. in Ixodes ricinus ticks in eastern Poland. Ann Agric Environ Med 19:656–659. PubMed
Cisak E, Wójcik-Fatla A, Zając V, Sroka J, Dutkiewicz J. 2012. Risk of Lyme disease at various sites and workplaces of forestry workers in eastern Poland. Ann Agric Environ Med 19:465–468. PubMed
Sytykiewicz H, Karbowiak G, Werszko J, Czerniewicz P, Sprawka I, Mitrus J. 2012. Molecular screening for Bartonella henselae and Borrelia burgdorferi sensu lato co-existence within Ixodes ricinus populations in central and eastern parts of Poland. Ann Agric Environ Med 19:451–456. PubMed
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. J Clin Microbiol 50:943–947. doi:10.1128/JCM.05802-11. PubMed DOI PMC
Hönig V, Svec P, Halas P, Vavruskova Z, Tykalova H, Kilian P, Vetiskova V, Dornakova V, Sterbova J, Simonova Z, Erhart J, Sterba J, Golovchenko M, Rudenko N, Grubhoffer L. 2015. Ticks and tick-borne pathogens in South Bohemia (Czech Republic)—spatial variability in Ixodes ricinus abundance, Borrelia burgdorferi and tick-borne encephalitis virus prevalence. Ticks Tick-Borne Dis 6:559–567. doi:10.1016/j.ttbdis.2015.04.010. PubMed DOI
Daniel M, Rudenko N, Golovchenko M, Danielová V, Fialová A, Kříž B, Malý M. 2016. The occurrence of Ixodes ricinus ticks and important tick-borne pathogens in areas with high tick-borne encephalitis prevalence in different altitudinal levels of the Czech Republic. Part II. Ixodes ricinus ticks and genospecies of Borrelia burgdorferi sensu lato complex. Epidemiol Mikrobiol Imunol 65:182–192. PubMed
Venclíková K, Betášová L, Sikutová S, Jedličková P, Hubálek Z, Rudolf I. 2014. Human pathogenic borreliae in Ixodes ricinus ticks in natural and urban ecosystem (Czech Republic). Acta Parasitol 59:717–720. doi:10.2478/s11686-014-0296-1. PubMed DOI
Nunes M, Parreira R, Lopes N, Maia C, Carreira T, Sousa C, Faria S, Campino L, Vieira ML. 2015. Molecular identification of Borrelia miyamotoi in Ixodes ricinus from Portugal. Vector Borne Zoonotic Dis 15:515–517. doi:10.1089/vbz.2014.1765. PubMed DOI
Milhano N, de Carvalho IL, Alves AS, Arroube S, Soares J, Rodriguez P, Carolino M, Núncio MS, Piesman J, de Sousa R. 2010. Coinfections of Rickettsia slovaca and Rickettsia helvetica with Borrelia lusitaniae in ticks collected in a Safari Park, Portugal. Ticks Tick-Borne Dis 1:172–177. doi:10.1016/j.ttbdis.2010.09.003. PubMed DOI
Coipan EC, Vladimirescu AF. 2011. Ixodes ricinus ticks (Acari: Ixodidae): vectors for Lyme disease spirochetes in Romania. Exp Appl Acarol 54:293–300. doi:10.1007/s10493-011-9438-4. PubMed DOI
Coipan EC, Vladimirescu AF. 2010. First report of Lyme disease spirochetes in ticks from Romania (Sibiu County). Exp Appl Acarol 52:193–197. doi:10.1007/s10493-010-9353-0. PubMed DOI
Geller J, Nazarova L, Katargina O, Golovljova I. 2013. Borrelia burgdorferi sensu lato prevalence in tick populations in Estonia. Parasit Vectors 6:202. doi:10.1186/1756-3305-6-202. PubMed DOI PMC
Tomanović S, Radulović Z, Masuzawa T, Milutinović M. 2010. Coexistence of emerging bacterial pathogens in Ixodes ricinus ticks in Serbia. Parasite (Paris, Fr) 17:211–217. doi:10.1051/parasite/2010173211. PubMed DOI
Tomanović S, Chochlakis D, Radulović Z, Milutinović M, Cakić S, Mihaljica D, Tselentis Y, Psaroulaki A. 2013. Analysis of pathogen co-occurrence in host-seeking adult hard ticks from Serbia. Exp Appl Acarol 59:367–376. doi:10.1007/s10493-012-9597-y. PubMed DOI
Potkonjak A, Kleinerman G, Gutiérrez R, Savić S, Vračar V, Nachum-Biala Y, Jurišić A, Rojas A, Petrović A, Ivanović I, Harrus S, Baneth G. 2016. Occurrence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks with first identification of Borrelia miyamotoi in Vojvodina, Serbia. Vector Borne Zoonotic Dis 16:631–635. doi:10.1089/vbz.2016.2008. PubMed DOI
Sormunen JJ, Penttinen R, Klemola T, Hänninen J, Vuorinen I, Laaksonen M, Sääksjärvi IE, Ruohomäki K, Vesterinen EJ. 2016. Tick-borne bacterial pathogens in southwestern Finland. Parasit Vectors 9:168. doi:10.1186/s13071-016-1449-x. PubMed DOI PMC
Sormunen JJ, Klemola T, Vesterinen EJ, Vuorinen I, Hytönen J, Hänninen J, Ruohomäki K, Sääksjärvi IE, Tonteri E, Penttinen R. 2016. Assessing the abundance, seasonal questing activity, and Borrelia and tick-borne encephalitis virus (TBEV) prevalence of Ixodes ricinus ticks in a Lyme borreliosis endemic area in Southwest Finland. Ticks Tick-Borne Dis 7:208–215. doi:10.1016/j.ttbdis.2015.10.011. PubMed DOI
Pangrácová L, Derdáková M, Pekárik L, Hviščová I, Víchová B, Stanko M, Hlavatá H, Pet'ko B. 2013. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors 6:238. doi:10.1186/1756-3305-6-238. PubMed DOI PMC
Subramanian G, Sekeyova Z, Raoult D, Mediannikov O. 2012. Multiple tick-associated bacteria in Ixodes ricinus from Slovakia. Ticks Tick-Borne Dis 3:406–410. doi:10.1016/j.ttbdis.2012.10.001. PubMed DOI
Taragel'ová VR, Mahríková L, Selyemová D, Václav R, Derdáková M. 2016. Natural foci of Borrelia lusitaniae in a mountain region of Central Europe. Ticks Tick-Borne Dis 7:350–356. doi:10.1016/j.ttbdis.2015.12.006. PubMed DOI
Cosson J-F, Michelet L, Chotte J, Le Naour E, Cote M, Devillers E, Poulle M-L, Huet D, Galan M, Geller J, Moutailler S, Vayssier-Taussat M. 2014. Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France. Parasit Vectors 7:233. doi:10.1186/1756-3305-7-233. PubMed DOI PMC
Reis C, Cote M, Paul REL, Bonnet S. 2011. Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis 11:907–916. doi:10.1089/vbz.2010.0103. PubMed DOI
Halos L, Bord S, Cotté V, Gasqui P, Abrial D, Barnouin J, Boulouis H-J, Vayssier-Taussat M, Vourc'h G. 2010. Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol 76:4413–4420. doi:10.1128/AEM.00610-10. PubMed DOI PMC
Dietrich F, Schmidgen T, Maggi RG, Richter D, Matuschka F-R, Vonthein R, Breitschwerdt EB, Kempf VAJ. 2010. Prevalence of Bartonella henselae and Borrelia burgdorferi sensu lato DNA in ixodes ricinus ticks in Europe. Appl Environ Microbiol 76:1395–1398. doi:10.1128/AEM.02788-09. PubMed DOI PMC
Bonnet S, de la Fuente J, Nicollet P, Liu X, Madani N, Blanchard B, Maingourd C, Alongi A, Torina A, Fernández de Mera IG, Vicente J, George J-C, Vayssier-Taussat M, Joncour G. 2013. Prevalence of tick-borne pathogens in adult Dermacentor spp. ticks from nine collection sites in France. Vector Borne Zoonotic Dis 13:226–236. doi:10.1089/vbz.2011.0933. PubMed DOI
Moutailler S, Valiente Moro C, Vaumourin E, Michelet L, Tran FH, Devillers E, Cosson J-F, Gasqui P, Van VT, Mavingui P, Vourc'h G, Vayssier-Taussat M. 2016. Co-infection of ticks: the rule rather than the exception. PLoS Negl Trop Dis 10:e0004539. doi:10.1371/journal.pntd.0004539. PubMed DOI PMC
Vourc'h G, Abrial D, Bord S, Jacquot M, Masséglia S, Poux V, Pisanu B, Bailly X, Chapuis J-L. 2016. Mapping human risk of infection with Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. Ticks Tick-Borne Dis 7:644–652. doi:10.1016/j.ttbdis.2016.02.008. PubMed DOI
Ruiz-Fons F, Fernández-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J. 2012. Factors driving the abundance of Ixodes ricinus ticks and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol 78:2669–2676. doi:10.1128/AEM.06564-11. PubMed DOI PMC
May K, Jordan D, Fingerle V, Strube C. 2015. Borrelia burgdorferi sensu lato and co-infections with Anaplasma phagocytophilum and Rickettsia spp. in Ixodes ricinus in Hamburg, Germany. Med Vet Entomol 29:425–429. doi:10.1111/mve.12125. PubMed DOI
Bingsohn L, Beckert A, Zehner R, Kuch U, Oehme R, Kraiczy P, Amendt J. 2013. Prevalences of tick-borne encephalitis virus and Borrelia burgdorferi sensu lato in Ixodes ricinus populations of the Rhine-Main region, Germany. Ticks Tick-Borne Dis 4:207–213. doi:10.1016/j.ttbdis.2012.11.012. PubMed DOI
Richter D, Schröder B, Hartmann NK, Matuschka F-R. 2013. Spatial stratification of various Lyme disease spirochetes in a Central European site. FEMS Microbiol Ecol 83:738–744. doi:10.1111/1574-6941.12029. PubMed DOI
Richter D, Matuschka F-R. 2011. Differential risk for Lyme disease along hiking trail, Germany. Emerg Infect Dis 17:1704–1706. doi:10.3201/eid1709.101523. PubMed DOI PMC
Franke J, Hildebrandt A, Meier F, Straube E, Dorn W. 2011. Prevalence of Lyme disease agents and several emerging pathogens in questing ticks from the German Baltic coast. J Med Entomol 48:441–444. doi:10.1603/ME10182. PubMed DOI
Franke J, Fritzsch J, Tomaso H, Straube E, Dorn W, Hildebrandt A. 2010. Coexistence of pathogens in host-seeking and feeding ticks within a single natural habitat in Central Germany. Appl Environ Microbiol 76:6829–6836. doi:10.1128/AEM.01630-10. PubMed DOI PMC
Hildebrandt A, Pauliks K, Sachse S, Straube E. 2010. Coexistence of Borrelia spp. and Babesia spp. in Ixodes ricinus ticks in Middle Germany. Vector Borne Zoonotic Dis 10:831–837. doi:10.1089/vbz.2009.0202. PubMed DOI
Herrmann C, Gern L. 2012. Do the level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks? Parasitology 139:330–337. doi:10.1017/S0031182011002095. PubMed DOI
Herrmann C, Gern L. 2013. Survival of Ixodes ricinus (Acari: Ixodidae) nymphs under cold conditions is negatively influenced by frequent temperature variations. Ticks Tick-Borne Dis 4:445–451. doi:10.1016/j.ttbdis.2013.05.002. PubMed DOI
Pérez D, Kneubühler Y, Rais O, Gern L. 2012. Seasonality of Ixodes ricinus ticks on vegetation and on rodents and Borrelia burgdorferi sensu lato genospecies diversity in two Lyme borreliosis-endemic areas in Switzerland. Vector Borne Zoonotic Dis 12:633–644. doi:10.1089/vbz.2011.0763. PubMed DOI PMC
Gern L, Douet V, López Z, Rais O, Cadenas FM. 2010. Diversity of Borrelia genospecies in Ixodes ricinus ticks in a Lyme borreliosis endemic area in Switzerland identified by using new probes for reverse line blotting. Ticks Tick-Borne Dis 1:23–29. doi:10.1016/j.ttbdis.2009.11.001. PubMed DOI
Hornok S, Meli ML, Gönczi E, Halász E, Takács N, Farkas R, Hofmann-Lehmann R. 2014. 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 5:785–789. doi:10.1016/j.ttbdis.2014.05.010. PubMed DOI
Szekeres S, Coipan EC, Rigó K, Majoros G, Jahfari S, Sprong H, Földvári G. 2015. Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary. Parasit Vectors 8:309. doi:10.1186/s13071-015-0922-2. PubMed DOI PMC
Nelson C, Banks S, Jeffries CL, Walker T, Logan JG. 2015. Tick abundances in South London parks and the potential risk for Lyme borreliosis to the general public. Med Vet Entomol 29:448–452. doi:10.1111/mve.12137. PubMed DOI
Hansford KM, Fonville M, Jahfari S, Sprong H, Medlock JM. 2015. Borrelia miyamotoi in host-seeking Ixodes ricinus ticks in England. Epidemiol Infect 143:1079–1087. doi:10.1017/S0950268814001691. PubMed DOI PMC
Bettridge J, Renard M, Zhao F, Bown KJ, Birtles RJ. 2013. Distribution of Borrelia burgdorferi sensu lato in Ixodes ricinus populations across central Britain. Vector Borne Zoonotic Dis 13:139–146. doi:10.1089/vbz.2012.1075. PubMed DOI
Millins C, Gilbert L, Johnson P, James M, Kilbride E, Birtles R, Biek R. 2016. Heterogeneity in the abundance and distribution of Ixodes ricinus and Borrelia burgdorferi (sensu lato) in Scotland: implications for risk prediction. Parasit Vectors 9:595. doi:10.1186/s13071-016-1875-9. PubMed DOI PMC
James MC, Gilbert L, Bowman AS, Forbes KJ. 2014. The heterogeneity, distribution, and environmental associations of Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in Scotland. Front Public Health 2:129. doi:10.3389/fpubh.2014.00129. PubMed DOI PMC
James MC, Bowman AS, Forbes KJ, Lewis F, McLeod JE, Gilbert L. 2013. Environmental determinants of Ixodes ricinus ticks and the incidence of Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in Scotland. Parasitology 140:237–246. doi:10.1017/S003118201200145X. PubMed DOI
Ragagli C, Mannelli A, Ambrogi C, Bisanzio D, Ceballos LA, Grego E, Martello E, Selmi M, Tomassone L. 2016. Presence of host-seeking Ixodes ricinus and their infection with Borrelia burgdorferi sensu lato in the Northern Apennines, Italy. Exp Appl Acarol 69:167–178. doi:10.1007/s10493-016-0030-9. PubMed DOI
Aureli S, Galuppi R, Ostanello F, Foley JE, Bonoli C, Rejmanek D, Rocchi G, Orlandi E, Tampieri MP. 2015. Abundance of questing ticks and molecular evidence for pathogens in ticks in three parks of Emilia-Romagna region of Northern Italy. Ann Agric Environ Med 22:459–466. doi:10.5604/12321966.1167714. PubMed DOI
Mancini F, Di Luca M, Toma L, Vescio F, Bianchi R, Khoury C, Marini L, Rezza G, Ciervo A. 2014. Prevalence of tick-borne pathogens in an urban park in Rome, Italy. Ann Agric Environ Med 21:723–727. doi:10.5604/12321966.1129922. PubMed DOI
Pintore MD, Ceballos L, Iulini B, Tomassone L, Pautasso A, Corbellini D, Rizzo F, Mandola ML, Bardelli M, Peletto S, Acutis PL, Mannelli A, Casalone C. 2015. Detection of invasive Borrelia burgdorferi strains in north-eastern Piedmont, Italy. Zoonoses Public Health 62:365–374. doi:10.1111/zph.12156. PubMed DOI
Corrain R, Drigo M, Fenati M, Menandro ML, Mondin A, Pasotto D, Martini M. 2012. Study on ticks and tick-borne zoonoses in public parks in Italy. Zoonoses Public Health 59:468–476. doi:10.1111/j.1863-2378.2012.01490.x. PubMed DOI
Pistone D, Pajoro M, Fabbi M, Vicari N, Marone P, Genchi C, Novati S, Sassera D, Epis S, Bandi C. 2010. Lyme borreliosis, Po River Valley, Italy. Emerg Infect Dis 16:1289–1291. doi:10.3201/eid1608.100152. PubMed DOI PMC
Herrmann C, Voordouw MJ, Gern L. 2013. Ixodes ricinus ticks infected with the causative agent of Lyme disease, Borrelia burgdorferi sensu lato, have higher energy reserves. Int J Parasitol 43:477–483. doi:10.1016/j.ijpara.2012.12.010. PubMed DOI
Herrmann C, Gern L. 2010. Survival of Ixodes ricinus (Acari: Ixodidae) under challenging conditions of temperature and humidity is influenced by Borrelia burgdorferi sensu lato infection. J Med Entomol 47:1196–1204. doi:10.1603/ME10111. PubMed DOI
Tveten A-K. 2014. Exploring diversity among Norwegian Borrelia strains originating from Ixodes ricinus ticks. Int J Microbiol 2014:397143. doi:10.1155/2014/397143. PubMed DOI PMC
Granquist EG, Kristiansson M, Lindgren P-E, Matussek A, Nødtvedt A, Okstad W, Stuen S. 2014. Evaluation of microbial communities and symbionts in Ixodes ricinus and ungulate hosts (Cervus elaphus and Ovis aries) from shared habitats on the west coast of Norway. Ticks Tick Borne Dis 5:780–784. doi:10.1016/j.ttbdis.2014.05.005. PubMed DOI
Synovial fluid alpha-defensins in Lyme arthritis-a useful marker
Pathogenicity and virulence of Borrelia burgdorferi
Novel targets and strategies to combat borreliosis
Ticks and bacterial tick-borne pathogens in Piemonte region, Northwest Italy