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
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
23171708
PubMed Central
PMC3523962
DOI
10.1186/1756-3305-5-268
PII: 1756-3305-5-268
Knihovny.cz E-resources
- MeSH
- Borrelia burgdorferi Group classification genetics isolation & purification MeSH
- Time Factors MeSH
- DNA, Bacterial genetics MeSH
- Population Density MeSH
- Ixodes growth & development microbiology MeSH
- Polymerase Chain Reaction MeSH
- Prevalence MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Germany MeSH
- Names of Substances
- DNA, Bacterial MeSH
BACKGROUND: During the last decades, population densities of Ixodes ricinus and prevalences of Borrelia burgdorferi s.l. have increased in different regions in Europe. In the present study, we determined tick abundance and the prevalence of different Borrelia genospecies in ticks from three sites in the Siebengebirge, Germany, which were already examined in the years 1987, 1989, 2001 and 2003. Data from all investigations were compared. METHODS: In 2007 and 2008, host-seeking I. ricinus were collected by monthly blanket dragging at three distinct vegetation sites in the Siebengebirge, a nature reserve and a well visited local recreation area near Bonn, Germany. In both years, 702 ticks were tested for B. burgdorferi s.l. DNA by nested PCR, and 249 tick samples positive for Borrelia were further genotyped by reverse line blotting. RESULTS: A total of 1046 and 1591 I. ricinus were collected in 2007 and 2008, respectively. In comparison to previous studies at these sites, the densities at all sites increased from 1987/89 and/or from 2003 until 2008. Tick densities and Borrelia prevalences in 2007 and 2008, respectively, were not correlated for all sites and both years. Overall, Borrelia prevalence of all ticks decreased significantly from 2007 (19.5%) to 2008 (16.5%), thus reaching the same level as in 2001 two times higher than in 1987/89 (7.6%). Since 2001, single infections with a Borrelia genospecies predominated in all collections, but the number of multiple infections increased, and in 2007, for the first time, triple Borrelia infections occurred. Prevalences of Borrelia genospecies differed considerably between the three sites, but B. garinii or B. afzelii were always the most dominant genospecies. B. lusitaniae was detected for the first time in the Siebengebirge, also in co-infections with B. garinii or B. valaisiana. CONCLUSIONS: Over the last two centuries tick densities have changed in the Siebengebirge at sites that remained unchanged by human activity since they belong to a nature reserve. Abiotic and biotic conditions most likely favored the host-seeking activity of I. ricinus and the increase of multiple Borrelia infections in ticks. These changes have led to a potential higher risk of humans and animals to be infected with Lyme borreliosis.
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de Castro JJ. Sustainable tick and tickborne disease control in livestock improvement in developing countries. Vet Parasitol. 1997;71:77–97. doi: 10.1016/S0304-4017(97)00033-2. PubMed DOI
Alciati S, Belligni E, Del Colle S, Pugliese A. Human infections tick-transmitted. Panminerva Med. 2001;43:295–304. PubMed
Pérez-Eid C, Rodhain F. Biologie d’Ixodes ricinus L., 1758. I. Ecologie, cycle évolutif. Bull Soc Pathol Exot Filiales. 1977;70:187–192. PubMed
Lindgren E, Tälleklint L, Polfeldt T. Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect. 2000;108:119–123. doi: 10.1289/ehp.00108119. PubMed DOI PMC
Perret JL, Guigoz E, Rais O, Gern L. Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland) Parasitol Res. 2000;86:554–557. doi: 10.1007/s004360000209. PubMed DOI
Hubálek Z, Halouzka J, Juricová Z. Host-seeking activity of ixodid ticks in relation to weather variables. J Vector Ecol. 2003;28:159–165. PubMed
Lindström A, Jaenson TG. Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. J Med Entomol. 2003;40:375–378. doi: 10.1603/0022-2585-40.4.375. PubMed DOI
Schwarz A, Maier WA, Kistemann T, Kampen H. Analysis of the distribution of the tick Ixodes ricinus L. (Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information Systems. Int J Hyg Environ Health. 2009;212:87–96. doi: 10.1016/j.ijheh.2007.12.001. PubMed DOI
Materna J, Daniel M, Danielová V. 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. 2005;13:24–28. PubMed
Stanek G. Büchse der Pandora: Krankheitserreger in Ixodes ricinus-Zecken in Mitteleuropa. Wien Klin Wochenschr. 2009;121:673–683. doi: 10.1007/s00508-009-1281-9. PubMed DOI
Mejlon HA, Jaenson TGT. Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae) Exp Appl Acarol. 1997;21:747–754. doi: 10.1023/A:1018421105231. DOI
Randolph SE. Evidence that climate change has caused 'emergence' of tick-borne diseases in Europe? Int J Med Microbiol. 2004;293(Suppl 37):5–15. PubMed
Humair P, Gern L. The wild hidden face of Lyme borreliosis in Europe. Microbes Infect. 2000;2:915–922. doi: 10.1016/S1286-4579(00)00393-2. PubMed DOI
Hubálek Z, Halouzka J. Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitol Res. 1998;84:167–172. PubMed
Kampen H, Rötzel DC, Kurtenbach K, Maier WA, Seitz HM. Substantial rise in the prevalence of Lyme borreliosis spirochetes in a region of western Germany over a 10-year period. Appl Environ Microbiol. 2004;70:1576–1582. doi: 10.1128/AEM.70.3.1576-1582.2004. PubMed DOI PMC
Jensen PM, Jespersen JB. Five decades of tick-man interaction in Denmark-an analysis. Exp Appl Acarol. 2005;35:131–146. doi: 10.1007/s10493-004-1991-7. PubMed DOI
Gern L, Estrada-Peña A, Frandsen F, Gray JS, Jaenson TG, Jongejan F, Kahl O, Korenberg E, Mehl R, Nuttall PA. European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralbl Bakteriol. 1998;287:196–204. doi: 10.1016/S0934-8840(98)80121-7. PubMed DOI
Hubálek Z, Halouzka J. Distribution of Borrelia burgdorferi sensu lato genomic groups in Europe, a review. Eur J Epidemiol. 1997;13:951–957. doi: 10.1023/A:1007426304900. PubMed DOI
Richter D, Postic D, Sertour N, Livey I, Matuschka FR, 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
Margos G, Vollmer SA, Cornet M, Garnier M, Fingerle V, Wilske B, Bormane A, Vitorino L, Collares-Pereira M, Drancourt M, Kurtenbach K. 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
Wilske B, Preac-Mursic V, Gobel UB, Graf B, Jauris S, Soutschek E, Schwab E, Zumstein G. An OspA serotyping system for Borrelia burgdorferi based on reactivity with monoclonal antibodies and OspA sequence analysis. J Clin Microbiol. 1993;31:340–350. PubMed PMC
van Dam AP, Kuiper H, Vos K, Widjojokusumo A, de Jongh BM, Spanjaard L, Ramselaar AC, Kramer MD, Dankert J. Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin Infect Dis. 1993;17:708–717. doi: 10.1093/clinids/17.4.708. PubMed DOI
Rijpkema SG, Tazelaar DJ, Molkenboer MJ, Noordhoek GT, Plantinga G, Schouls LM, Schellekens JF. Detection of Borrelia afzelii, Borrelia burgdorferi sensu stricto, Borrelia garinii and group VS116 by PCR in skin biopsies of patients with erythema migrans and acrodermatitis chronica atrophicans. Clin Microbiol Infect. 1997;3:109–116. doi: 10.1111/j.1469-0691.1997.tb00259.x. PubMed DOI
Diza E, Papa A, Vezyri E, Tsounis S, Milonas I, Antoniadis A. Borrelia valaisiana in cerebrospinal fluid. Emerg Infect Dis. 2004;10:1692–1693. doi: 10.3201/eid1009.030439. PubMed DOI PMC
Strle F, Picken RN, Cheng Y, Cimperman J, Maraspin V, Lotric-Furlan S, Ruzic-Sabljic E, Picken MM. Clinical findings for patients with Lyme borreliosis caused by Borrelia burgdorferi sensu lato with genotypic and phenotypic similarities to strain 25015. Clin Infect Dis. 1997;25:273–280. doi: 10.1086/514551. PubMed DOI
Rudenko N, Golovchenko M, Mokrácek A, Piskunová N, Ruzek 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
Fingerle V, Schulte-Spechtel UC, Ruzic-Sabljic E, Leonhard S, Hofmann H, Weber K, Pfister K, Strle F, Wilske B. 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. 2008;298:279–290. doi: 10.1016/j.ijmm.2007.05.002. PubMed DOI
Collares-Pereira M, Couceiro S, Franca I, Kurtenbach K, Schäfer SM, Vitorino L, Gonçalves L, Baptista S, Vieira ML, Cunha C. First isolation of Borrelia lusitaniae from a human patient. J Clin Microbiol. 2004;42:1316–1318. doi: 10.1128/JCM.42.3.1316-1318.2004. PubMed DOI PMC
Kurtenbach K, De Michelis S, Sewell HS, Etti S, Schäfer SM, Hails R, Collares-Pereira M, Santos-Reis M, Hanincová K, Labuda M. et al.Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol. 2001;67:4926–4929. doi: 10.1128/AEM.67.10.4926-4929.2001. PubMed DOI PMC
Richter D, Klug B, Spielman A, Matuschka FR. Adaptation of diverse lyme disease spirochetes in a natural rodent reservoir host. Infect Immun. 2004;72:2442–2444. doi: 10.1128/IAI.72.4.2442-2444.2004. PubMed DOI PMC
Kurtenbach K, De Michelis S, Sewell HS, Etti S, Schäfer SM, Holmes E, Hails R, Collares-Pereira M, Santos-Reis M, Hanincová K. et al.The key roles of selection and migration in the ecology of Lyme borreliosis. Int J Med Microbiol. 2002;291:152–154. PubMed
Hanincová K, Kurtenbach K, Diuk-Wasser M, Brei B, Fish D. Epidemic spread of Lyme borreliosis, northeastern United States. Emerg Infect Dis. 2006;12:604–611. doi: 10.3201/eid1204.051016. PubMed DOI PMC
Margos G, Hojgaard A, Lane RS, Cornet M, Fingerle V, Rudenko N, Ogden N, Aanensen DM, 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
Richter D, Schlee DB, Allgöwer R, Matuschka FR. Relationships of a novel Lyme disease spirochete, Borrelia spielmanii sp. nov., with its hosts in Central Europe. Appl Environ Microbiol. 2004;70:6414–6419. doi: 10.1128/AEM.70.11.6414-6419.2004. PubMed DOI PMC
Wodecka B, Skotarczak B. First isolation of Borrelia lusitaniae DNA from Ixodes ricinus ticks in Poland. Scand J Infect Dis. 2005;37:27–34. doi: 10.1080/00365540410026059. PubMed DOI
Richter D, Matuschka FR. Perpetuation of the Lyme disease spirochete Borrelia lusitaniae by lizards. Appl Environ Microbiol. 2006;72:4627–4632. doi: 10.1128/AEM.00285-06. PubMed DOI PMC
Kurtenbach K, Kampen H, Dizij A, Arndt S, Seitz HM, Schaible UE, Simon MM. Infestation of rodents with larval Ixodes ricinus (Acari: Ixodidae) is an important factor in the transmission cycle of Borrelia burgdorferi s.l. in German woodlands. J Med Entomol. 1995;32:807–817. PubMed
Kurtenbach K. Epidemiologische und immunologische Untersuchungen zur Rolle von Zecken (Ixodoidea, Ixodidae) und Wildnagern (Rodentia) im Infektionskreislauf von Borrelia burgdorferi (Spirochaetaceae) PhD thesis: University of Bonn, Faculty of Mathematics and Natural Sciences; 1992.
Hillyard PD. In: Synopses of the British Fauna (New Series). No. 52. Barnes RSK, Crothers JH, editor. Shrewsbury: Field Studies Council; 1996. Ticks of north-west Europe: keys and notes for identification of species; p. 178.
Rauter C, Oehme R, Diterich I, Engele M, Hartung T. Distribution of clinically relevant Borrelia genospecies in ticks assessed by a novel, single-run, real-time PCR. J Clin Microbiol. 2002;40:36–43. doi: 10.1128/JCM.40.1.36-43.2002. PubMed DOI PMC
Walsh PS, Metzger DA, Higuchi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques. 1991;10:506–513. PubMed
Guy EC, Stanek G. Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. J Clin Pathol. 1991;44:610–611. doi: 10.1136/jcp.44.7.610. PubMed DOI PMC
Barbour AG. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984;57:521–525. PubMed PMC
Rijpkema SG, Molkenboer MJ, Schouls LM, Jongejan F, Schellekens JF. Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. J Clin Microbiol. 1995;33:3091–3095. PubMed PMC
Liebisch G, Sohns B, Bautsch W. Detection and typing of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks attached to human skin by PCR. J Clin Microbiol. 1998;36:3355–3358. PubMed PMC
Schwartz I, Wormser GP, Schwartz JJ, Cooper D, Weissensee P, Gazumyan A, Zimmermann E, Goldberg NS, Bittker S, Campbell GL, Pavia CS. Diagnosis of early Lyme disease by polymerase chain reaction amplification and culture of skin biopsies from erythema migrans lesions. J Clin Microbiol. 1992;30:3082–3088. PubMed PMC
Gern L, Douet V, Lopez Z, Rais O, Cadenas FM. 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. 2010;1:23–29. doi: 10.1016/j.ttbdis.2009.11.001. PubMed DOI
Alekseev AN, Dubinina HV, Van De Pol I, Schouls LM. Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. J Clin Microbiol. 2001;39:2237–2242. doi: 10.1128/JCM.39.6.2237-2242.2001. PubMed DOI PMC
Burri C, Moran Cadenas F, Douet V, Moret J, Gern L. Ixodes ricinus density and infection prevalence of Borrelia burgdorferi sensu lato along a North-facing altitudinal gradient in the Rhone Valley (Switzerland) Vector Borne Zoonotic Dis. 2007;7:50–58. doi: 10.1089/vbz.2006.0569. PubMed DOI
Priem S, Rittig MG, Kamradt T, Burmester GR, Krause A. An optimized PCR leads to rapid and highly sensitive detection of Borrelia burgdorferi in patients with Lyme borreliosis. J Clin Microbiol. 1997;35:685–690. PubMed PMC
Bouillon B, Felinks B, Hand R, Krause S, Röhlinger-Nord B, Schuhmacher W. Floristisch-vegetationskundliche Bestandsaufnahme und Bewertung des NSG Siebengebirge: Mit Empfehlungen zur Entwicklung und Pflege. Siegburg: Untere Landschaftsbehörde des Rhein-Sieg-Kreises; 1994.
Schwarz A. GIS-gestützte Untersuchung zur Risikoabschätzung der Verbreitung von Ixodes ricinus L. (Acari: Ixodidae) im Naturpark Siebengebirge bei Bonn. Diploma thesis: University of Bonn, Faculty of Mathematics and Natural Sciences; 2004.
Gray JS. The development and seasonal activity of the tick Ixodes ricinus: a vector of Lyme borreliosis. Rev Med Vet Entomol. 1991;79:323–333.
Randolph SE. Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology. 2004;129:37–65. doi: 10.1017/S0031182004004925. PubMed DOI
Scharlemann JPW, Johnson PJ, Smith AA, Macdonald DW, Randolph SE. Trends in ixodid tick abundance and distribution in Great Britain. Med Vet Entomol. 2008;22:238–247. doi: 10.1111/j.1365-2915.2008.00734.x. PubMed DOI
Knap N, Durmisi E, Saksida A, Korva M, Petrovec M, Avsic-Zupanc T. Influence of climatic factors on dynamics of questing Ixodes ricinus ticks in Slovenia. Vet Parasitol. 2009;164:275–281. doi: 10.1016/j.vetpar.2009.06.001. PubMed DOI
Tagliapietra V, Rosa R, Arnoldi D, Cagnacci F, Capelli G, Montarsi F, Hauffe HC, Rizzoli A. Saturation deficit and deer density affect questing activity and local abundance of Ixodes ricinus (Acari, Ixodidae) in Italy. Vet Parasitol. 2011;183:114–124. doi: 10.1016/j.vetpar.2011.07.022. PubMed DOI
Tälleklint L, Jaenson TG. Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. J Med Entomol. 1996;33:805–811. PubMed
Güneş T, Kaya S, Poyraz O, Engin A. The prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks in the Sinop Region of Turkey. Turk J Vet Anim Sci. 2007;31:153–158.
Arneberg P, Skorping A, Grenfell B, Read AF. Host densities as determinants of abundance in parasite communities. Proc R Soc Lond B. 1998;265:1283–1289. doi: 10.1098/rspb.1998.0431. DOI
LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci U S A. 2003;100:567–571. doi: 10.1073/pnas.0233733100. PubMed DOI PMC
Krasnov BR, Khokhlova IS, Burdelova NV, Mirzoyan NS, Degen AA. Fitness consequences of density-dependent host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. J Anim Ecol. 2004;73:815–820. doi: 10.1111/j.0021-8790.2004.00860.x. DOI
Peréz-Eid C. Report of WHO Workshop on Lyme Borreliosis Diagnosis and Surveillance. Warsaw: WHO; 1995. Epidemiology of Lyme borreliosis in the commuter belt of Paris; pp. 80–83.
Angelov L, Arnaudov D, Rakadjieva TT, Lichev D, Kostova E. Report of WHO Workshop on Lyme Borreliosis Diagnosis and Surveillance. Warsaw: WHO; 1995. Lyme borreliosis in Bulgaria (epidemiologic and epizootologic review) pp. 41–52.
Estrada-Peña A, Osacar JJ, Pichon B, Gray JS. Hosts and pathogen detection for immature stages of Ixodes ricinus (Acari: Ixodidae) in North-Central Spain. Exp Appl Acarol. 2005;37:257–268. doi: 10.1007/s10493-005-3271-6. PubMed DOI
Juřicová Z, Hubálek Z. Serologic survey of the wild boar (Sus scrofa) for Borrelia burgdorferi sensu lato. Vector Borne Zoonotic Dis. 2009;9:479–482. doi: 10.1089/vbz.2008.0125. PubMed DOI
Landesbetrieb Wald und Holz NRW. Wildschweinbestände mit Zukunft. Detmold: Hermann Bösmann Verlag; 2009.
Landesbetrieb Wald und Holz NRW. Fallwildbericht: Auswertung der im Jagdjahr 2008/09 durchgeführten Fallwilduntersuchungen im Land Nordrhein-Westfalen. Bonn: Leppelt Grafik & Druck GmbH; 2009.
Landesbetrieb Wald und Holz NRW. Fallwildbericht: Auswertung der im Jagdjahr 2009/10 durchgeführten Fallwilduntersuchungen im Land Nordrhein-Westfalen. Bonn: Carthaus GmbH & Co.KG; 2010.
Ruiz-Fons F, Gilbert L. The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. Int J Parasitol. 2010;40:1013–1020. doi: 10.1016/j.ijpara.2010.02.006. PubMed DOI
Matuschka FR, Heiler M, Eiffert H, Fischer P, Lotter H, Spielman A. Diversionary role of hoofed game in the transmission of Lyme disease spirochetes. AmJTrop Med Hyg. 1993;48:693–699. PubMed
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
Estrada-Peña A, Acevedo P, Ruiz-Fons F, Gortázar C, de la Fuente J. Evidence of the importance of host habitat use in predicting the dilution effect of wild boar for deer exposure to Anaplasma spp. PLoS One. 2008;3:e2999. doi: 10.1371/journal.pone.0002999. PubMed DOI PMC
Pérez D, Kneubühler Y, Rais O, Jouda F, Gern L. Borrelia afzelii ospC genotype diversity in Ixodes ricinus questing ticks and ticks from rodents in two Lyme borreliosis endemic areas: contribution of co-feeding ticks. Ticks Tick Borne Dis. 2011;2:137–142. doi: 10.1016/j.ttbdis.2011.06.003. PubMed DOI
Gern L, Hu CM, Kocianova E, Vyrostekova V, Rehacek J. Genetic diversity of Borrelia burgdorferi sensu lato isolates obtained from Ixodes ricinus ticks collected in Slovakia. Eur J Epidemiol. 1999;15:665–669. doi: 10.1023/A:1007660430664. PubMed DOI
Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl Environ Microbiol. 1998;64:1169–1174. PubMed PMC
Vennestrøm J, Egholm H, Jensen PM. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitol Int. 2008;57:32–37. doi: 10.1016/j.parint.2007.07.004. PubMed DOI
Pichon B, Rogers M, Egan D, Gray J. Blood-meal analysis for the identification of reservoir hosts of tick-borne pathogens in Ireland. Vector Borne Zoonotic Dis. 2005;5:172–180. doi: 10.1089/vbz.2005.5.172. PubMed DOI
Kurtenbach K, Sewell HS, Ogden NH, Randolph SE, Nuttall PA. Serum complement sensitivity as a key factor in Lyme disease ecology. Infect Immun. 1998;66:1248–1251. PubMed PMC
Humair PF, Postic D, Wallich R, Gern L. An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralbl Bakteriol. 1998;287:521–538. PubMed
Kurtenbach K, Carey D, Hoodless AN, Nuttall PA, Randolph SE. Competence of pheasants as reservoirs for Lyme disease spirochetes. J Med Entomol. 1998;35:77–81. PubMed
Richter D, Spielman A, Komar N, Matuschka FR. Competence of American robins as reservoir hosts for Lyme disease spirochetes. Emerg Infect Dis. 2000;6:133–138. doi: 10.3201/eid0602.000205. PubMed DOI PMC
Escudero R, Barral M, Perez A, Vitutia MM, García-Pérez AL, Jiménez S, Sellek RE, Anda P. Molecular and pathogenic characterization of Borrelia burgdorferi sensu lato isolates from Spain. J Clin Microbiol. 2000;38:4026–4033. PubMed PMC
Younsi H, Postic D, Baranton G, Bouattour A. High prevalence of Borrelia lusitaniae in Ixodes ricinus ticks in Tunisia. Eur J Epidemiol. 2001;17:53–56. doi: 10.1023/A:1010928731281. PubMed DOI
Zeidner NS, Núncio MS, Schneider BS, Gern L, Piesman J, Brandão O, Filipe AR. A portuguese isolate of Borrelia lusitaniae induces disease in C3H/HeN mice. J Med Microbiol. 2001;50:1055–1060. PubMed
Sarih M, Jouda F, Gern L, Postic D. First isolation of Borrelia burgdorferi sensu lato from Ixodes ricinus ticks in Morocco. Vector Borne Zoonotic Dis. 2003;3:133–139. doi: 10.1089/153036603768395834. PubMed DOI
Núncio MS, Péter O, Alves MJ, Bacellar F, Filipe AR. Isolemento e caracterização de borrélias de Ixodes ricinus L. em Portugal. Rev Portug Doenças Infec. 1993;16:175–179.
Postic D, Korenberg E, Gorelova N, Kovalevski YV, Bellenger E, Baranton G. Borrelia burgdorferi sensu lato in Russia and neighbouring countries: high incidence of mixed isolates. Res Microbiol. 1997;148:691–702. doi: 10.1016/S0923-2508(99)80068-0. PubMed DOI
Mizak B, Król J. Analysis of Polish isolates of Borrelia burgdorferi by amplification of rrf (5S)–rrl (23S) intergenic spacer. Bull Vet Inst Pulawy. 2000;44:147–154.
Richter D, Schlee DB, Matuschka FR. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg Infect Dis. 2003;9:697–701. doi: 10.3201/eid0906.020459. PubMed DOI PMC
Jouda F, Crippa M, Perret JL, Gern L. Distribution and prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks of canton Ticino (Switzerland) Eur J Epidemiol. 2003;18:907–912. doi: 10.1023/A:1025602600434. PubMed DOI
Wilhelmsson P, Fryland L, Börjesson S, Nordgren J, Bergström S, Ernerudh J, Forsberg P, Lindgren PE. Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. J Clin Microbiol. 2010;48:4169–4176. doi: 10.1128/JCM.01061-10. PubMed DOI PMC
Poupon MA, Lommano E, Humair PF, Douet V, Rais O, Schaad M, Jenni L, Gern L. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl Environ Microbiol. 2006;72:976–979. doi: 10.1128/AEM.72.1.976-979.2006. PubMed DOI PMC
Norte AC, Ramos JA, Gern L, Nuncio MS, Lopes-de-Carvalho I. Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environ Microbiol. 2012. in press. PubMed DOI
de Carvalho IL, Zeidner N, Ullmann A, Hojgaard A, Amaro F, Ze-Ze L, Alves MJ, de Sousa R, Piesman J, Nuncio MS. Molecular characterization of a new isolate of Borrelia lusitaniae derived from Apodemus sylvaticus in Portugal. Vector Borne Zoonotic Dis. 2010;10:531–534. doi: 10.1089/vbz.2008.0210. PubMed DOI
De Sousa R, Lopes de Carvalho I, Santos AS, Bernardes C, Milhano N, Jesus J, Menezes D, Nuncio MS. Role of the lizard Teira dugesii as a potential host for Ixodes ricinus tick-borne pathogens. Appl Environ Microbiol. 2012;78:3767–3769. doi: 10.1128/AEM.07945-11. PubMed DOI PMC
Majláthová V, Majláth I, Derdáková M, Vichová B, Pet'ko B. Borrelia lusitaniae and green lizards (Lacerta viridis), Karst Region, Slovakia. Emerg Infect Dis. 2006;12:1895–1901. doi: 10.3201/eid1212.060784. PubMed DOI PMC
Amore G, Tomassone L, Grego E, Ragagli C, Bertolotti L, Nebbia P, Rosati S, Mannelli A. Borrelia lusitaniae in immature Ixodes ricinus (Acari: Ixodidae) feeding on common wall lizards in Tuscany, central Italy. J Med Entomol. 2007;44:303–307. doi: 10.1603/0022-2585(2007)44[303:BLIIIR]2.0.CO;2. PubMed DOI