{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T12:16:09Z","timestamp":1787314569329,"version":"build-2736575974"},"reference-count":91,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2021,11,23]],"date-time":"2021-11-23T00:00:00Z","timestamp":1637625600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Ticks are widely distributed across the globe, serving as hosts for numerous pathogens that make them major contributors to zoonotic parasitosis. Borrelia burgdorferi is a bacterial species that causes an emerging zoonotic tick-borne disease known as Lyme borreliosis. The role of ticks in the transmission of this pathogen was explored in this study. According to this systematic review, undertaken according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, 19 tick species are known to carry Borrelia burgdorferi, with more than half of the recorded cases in the last two decades related to Ixodes ricinus and Ixodes scapularis ticks. Forty-six studies from four continents, Europe, North America, Asia, and Africa, reported this pathogen in ticks collected from vegetation, animals, and humans. This study highlights an increasing distribution of tick-associated Borrelia burgdorferi, likely driven by accelerated tick population increases in response to climate change coupled with tick dispersal via migratory birds. This updated catalogue helps in compiling all tick species responsible for the transmission of B. burgdorferi across the globe. Gaps in research exist on Borrelia burgdorferi in continents such as Asia and Africa, and in considering environmentally friendly vector control strategies in Europe and North America.<\/jats:p>","DOI":"10.3390\/microorganisms9122412","type":"journal-article","created":{"date-parts":[[2021,11,30]],"date-time":"2021-11-30T05:42:10Z","timestamp":1638250930000},"page":"2412","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["The Role of Ticks in the Emergence of Borrelia burgdorferi as a Zoonotic Pathogen and Its Vector Control: A Global Systemic Review"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8573-1907","authenticated-orcid":false,"given":"Sabir","family":"Hussain","sequence":"first","affiliation":[{"name":"Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0335-3103","authenticated-orcid":false,"given":"Abrar","family":"Hussain","sequence":"additional","affiliation":[{"name":"Department of Epidemiology and Public Health, University of Veterinary and Animal Sciences, Lahore 54600, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0075-713X","authenticated-orcid":false,"given":"Umair","family":"Aziz","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7834-8064","authenticated-orcid":false,"given":"Baolin","family":"Song","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5565-9935","authenticated-orcid":false,"given":"Jehan","family":"Zeb","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"George","sequence":"additional","affiliation":[{"name":"School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne NE1 7RU, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7218-429X","authenticated-orcid":false,"given":"Jun","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3141-310X","authenticated-orcid":false,"given":"Olivier","family":"Sparagano","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1186\/s13071-015-1154-1","article-title":"Flying ticks: Anciently evolved associations that constitute a risk of infectious disease spread","volume":"8","author":"Brey","year":"2015","journal-title":"Parasites Vectors"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"5719081","DOI":"10.1155\/2018\/5719081","article-title":"\u201cTicking bomb\u201d: The impact of climate change on the incidence of Lyme disease","volume":"2018","author":"Dumic","year":"2018","journal-title":"Can. J. Infect. Dis. Med. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"67","DOI":"10.4269\/ajtmh.2009.81.67","article-title":"Tick-borne zoonotic bacteria in ticks collected from central Spain","volume":"81","author":"Toledo","year":"2009","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1111\/eve.12070","article-title":"Equine piroplasmosis: An updated review","volume":"25","author":"Tamzali","year":"2013","journal-title":"Equine Vet. Educ."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1128\/CMR.00032-13","article-title":"Update on tick-borne rickettsioses around the world: A geographic approach","volume":"26","author":"Parola","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"19906","DOI":"10.2807\/ese.16.27.19906-en","article-title":"Lyme borreliosis in Europe","volume":"16","author":"Rizzoli","year":"2011","journal-title":"Eurosurveillance"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.ttbdis.2011.04.002","article-title":"Updates on Borrelia burgdorferi sensu lato complex with respect to public health","volume":"2","author":"Rudenko","year":"2011","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3872","DOI":"10.1099\/ijsem.0.002214","article-title":"Borrelia lanei sp. nov. extends the diversity of Borrelia species in California","volume":"67","author":"Margos","year":"2017","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e00479","DOI":"10.1016\/j.idcr.2018.e00479","article-title":"Acute transverse myelitis\u2013A rare clinical manifestation of Lyme neuroborreliosis","volume":"15","author":"Dumic","year":"2019","journal-title":"IDCases"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"496","DOI":"10.15585\/mmwr.mm6717e1","article-title":"Vital signs: Trends in reported vectorborne disease cases\u2014United States and Territories, 2004\u20132016","volume":"67","author":"Rosenberg","year":"2018","journal-title":"Morb. Mortal. Wkly. Rep."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"499","DOI":"10.3201\/eid2702.202728","article-title":"Use of commercial claims data for evaluating trends in Lyme disease diagnoses, United States, 2010\u20132018","volume":"27","author":"Schwartz","year":"2021","journal-title":"Emerg. Infect. Dis."},{"key":"ref_12","first-page":"74","article-title":"An estimate of Lyme borreliosis incidence in Western Europe","volume":"39","author":"Sykes","year":"2017","journal-title":"J. Public Health"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Slatculescu, A.M., Clow, K.M., McKay, R., Talbot, B., Logan, J.J., Thickstun, C.R., Jardine, C.M., Ogden, N.H., Knudbury, A.J., and Kulkarni, M.A. (2020). Species distribution models for the eastern blacklegged tick, Ixodes scapularis, and the Lyme disease pathogen, Borrelia burgdorferi, in Ontario, Canada. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0238126"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/s41579-020-0400-5","article-title":"Interactions between Borrelia burgdorferi and ticks","volume":"18","author":"Kurokawa","year":"2020","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"616","DOI":"10.3201\/eid2702.202731","article-title":"Estimating the frequency of Lyme disease diagnoses, United States, 2010\u20132018","volume":"27","author":"Kugeler","year":"2021","journal-title":"Emerg. Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1080\/14787210.2018.1417836","article-title":"Diagnosis and management of Lyme neuroborreliosis","volume":"16","author":"Halperin","year":"2018","journal-title":"Expert Rev. Anti-Infect. Ther."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Shah, A., O\u2019Horo, J.C., Wilson, J.W., Granger, D., and Theel, E.S. (2018). An Unusual Cluster of Neuroinvasive Lyme Disease Cases Presenting with Bannwarth Syndrome in the Midwest United States (U.S). Open Forum Infectious Diseases, Oxford University Press.","DOI":"10.1093\/ofid\/ofx276"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"401","DOI":"10.3389\/fevo.2019.00401","article-title":"Borrelia bavariensis: Vector switch, niche invasion, and geographical spread of a tick-borne bacterial parasite","volume":"7","author":"Margos","year":"2019","journal-title":"Front. Ecol. Evol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"101359","DOI":"10.1016\/j.ttbdis.2019.101359","article-title":"Vector competence studies with hard ticks and Borrelia burgdorferi sensu lato spirochetes: A review","volume":"11","author":"Eisen","year":"2020","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_20","first-page":"73","article-title":"Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British","volume":"42","author":"Craine","year":"1995","journal-title":"Folia Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1186\/s13071-018-2744-5","article-title":"W Control of Lyme borreliosis and other Ixodes ricinus-borne diseases","volume":"11","author":"Sprong","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"768","DOI":"10.1016\/j.ttbdis.2016.03.010","article-title":"Biological control of Ixodes ricinus larvae and nymphs with Metarhizium anisopliae blastospores","volume":"7","author":"Wassermann","year":"2016","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.ijsu.2010.02.007","article-title":"Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement","volume":"8","author":"Moher","year":"2010","journal-title":"Int. J. Surg."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2825","DOI":"10.1128\/AEM.69.5.2825-2830.2003","article-title":"Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia","volume":"69","author":"Koci","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1051\/parasite\/2010174357","article-title":"Borrelia burgdorferi in ticks and dogs in the province of Vojvodina, Serbia","volume":"17","author":"Lako","year":"2010","journal-title":"Parasite"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2923","DOI":"10.1128\/AEM.03061-09","article-title":"Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg","volume":"76","author":"Reye","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"4606","DOI":"10.1128\/AEM.07961-11","article-title":"Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland","volume":"78","author":"Lommano","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1111\/j.1420-9101.2012.02515.x","article-title":"Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii","volume":"25","year":"2012","journal-title":"J. Evol. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Reye, A.L., Stegniy, V., Mishaeva, N.P., Velhin, S., H\u00fcbschen, J.M., Ignatyev, G., and Muller, C.P. (2013). Prevalence of tick-borne pathogens in Ixodes ricinus and Dermacentor reticulatus ticks from different geographical locations in Belarus. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0054476"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1017\/S0950268803001328","article-title":"Acarological risk of exposure to agents of tick-borne zoonoses in the first recognized Italian focus of Lyme borreliosis","volume":"131","author":"Mannelli","year":"2003","journal-title":"Epidemiol. Infect."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1186\/s13071-015-0843-0","article-title":"Babesia spp. and other pathogens in ticks recovered from domestic dogs in Denmark","volume":"8","author":"Stensvold","year":"2015","journal-title":"Parasites Vectors"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"459","DOI":"10.5604\/12321966.1167714","article-title":"P Abundance of questing ticks and molecular evidence for pathogens in ticks in three parks of Emilia-Romagnaregion of Northern Italy","volume":"22","author":"Aureli","year":"2015","journal-title":"Ann. Agric. Environ. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1111\/zph.12156","article-title":"Detection of invasive Borrelia burgdorferi strains in north-eastern Piedmont, Italy","volume":"62","author":"Pintore","year":"2015","journal-title":"Zoonoses Public Health"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"4236","DOI":"10.1128\/AEM.00109-15","article-title":"An invasive mammal (the gray squirrel, Sciurus carolinensis) commonly hosts diverse and atypical genotypes of the zoonotic pathogen Borrelia burgdorferi sensu lato","volume":"81","author":"Millins","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1007\/s10493-015-9899-y","article-title":"Molecular detection of Rickettsia, Borrelia, and Babesia species in Ixodes ricinus sampled in northeastern, central, and insular areas of Italy","volume":"66","author":"Castro","year":"2015","journal-title":"Exp. Appl. Acarol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1016\/j.apjtm.2015.07.033","article-title":"Molecular survey of tick-borne pathogens in Ixodid ticks collected from hunted wild animals in Tuscany, Italy","volume":"8","author":"Ebani","year":"2015","journal-title":"Asian Pac. J. Trop. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1186\/s13071-015-0814-5","article-title":"Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas","volume":"8","author":"Krawczyk","year":"2015","journal-title":"Parasites Vectors"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"335","DOI":"10.21836\/PEM20160406","article-title":"Borrelia burgdorferi and Anaplasma phagocytophilum in ticks and their equine hosts: A prospective clinical and diagnostic study of 47 horses following removal of a feeding tick","volume":"32","author":"Butler","year":"2016","journal-title":"Pferdeheilkunde"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"817","DOI":"10.2298\/VSP150115069K","article-title":"Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and assessment of entomological risk index at localities in Belgrade","volume":"73","year":"2016","journal-title":"Vojnosanit. Pregl."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1186\/s13071-016-1449-x","article-title":"Tick-borne bacterial pathogens in southwestern Finland","volume":"9","author":"Sormunen","year":"2016","journal-title":"Parasites Vectors"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/s10493-016-0027-4","article-title":"Molecular evidence for bacterial pathogens in Ixodes ricinus ticks infesting Shetland ponies","volume":"69","author":"Skotarczak","year":"2016","journal-title":"Exp. Appl. Acarol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"36","DOI":"10.3389\/fcimb.2017.00036","article-title":"Borrelia diversity and co-infection with other tick borne pathogens in ticks","volume":"7","author":"Raileanu","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.vetpar.2017.07.033","article-title":"Prevalence of ticks and tick-borne pathogens: Babesia and Borrelia species in ticks infesting cats of Great Britain","volume":"244","author":"Davies","year":"2017","journal-title":"Vet. Parasitol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1186\/s13071-017-2053-4","article-title":"The enzootic life-cycle of Borrelia burgdorferi (sensu lato) and tick-borne rickettsiae: An epidemiological study on wild-living small mammals and their ticks from Saxony, Germany","volume":"10","author":"Obiegala","year":"2017","journal-title":"Parasites Vectors"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Chvost\u00e1\u010d, M., \u0160pitalsk\u00e1, E., V\u00e1clav, R., Vaculov\u00e1, T., Minichov\u00e1, L., and Derd\u00e1kov\u00e1, M. (2018). Seasonal patterns in the prevalence and diversity of tick-borne Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Rickettsia spp. in an urban temperate forest in south western Slovakia. Int. J. Environ. Res. Public Health, 15.","DOI":"10.3390\/ijerph15050994"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1186\/s13071-018-2726-7","article-title":"Ticks are more suitable than red foxes for monitoring zoonotic tick-borne pathogens in northeastern Italy","volume":"11","author":"Ravagnan","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1186\/s13071-018-3200-2","article-title":"Landscape structure affects the prevalence and distribution of a tick-borne zoonotic pathogen","volume":"11","author":"Millins","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Namina, A., Capligina, V., Seleznova, M., Krumins, R., Aleinikova, D., Kivrane, A., Akopjana, S., Lazovska, M., Berzina, I., and Ranka, R. (2019). Tick-borne pathogens in ticks collected from dogs, Latvia, 2011\u20132016. BMC Vet. Res., 15.","DOI":"10.1186\/s12917-019-2149-5"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Millet, I., Ragionieri, M., Tomassone, L., Trentin, C., and Mannelli, A. (2019). Assessment of the exposure of people to questing ticks carrying agents of zoonoses in Aosta Valley, Italy. Vet. Sci., 6.","DOI":"10.3390\/vetsci6010028"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1186\/s13071-020-04219-7","article-title":"Large-scale countrywide screening for tick-borne pathogens in field-collected ticks in Latvia during 2017\u20132019","volume":"13","author":"Capligina","year":"2020","journal-title":"Parasites Vectors"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Zanet, S., Battisti, E., Pepe, P., Ciuca, L., Colombo, L., Trisciuoglio, A., Ferroglio, E., Cringoli, G., Rinaldi, L., and Maurelli, M.P. (2020). Tick-borne pathogens in Ixodidae ticks collected from privately-owned dogs in Italy: A country-wide molecular survey. BMC Vet. Res., 16.","DOI":"10.1186\/s12917-020-2263-4"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1186\/s13071-020-04259-z","article-title":"Questing abundance of adult taiga ticks Ixodes persulcatus and their Borrelia prevalence at the north-western part of their distribution","volume":"13","author":"Pakanen","year":"2020","journal-title":"Parasites Vectors"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1111\/mec.15336","article-title":"Host dispersal shapes the population structure of a tick-borne bacterial pathogen","volume":"29","author":"Norte","year":"2020","journal-title":"Mol. Ecol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"101586","DOI":"10.1016\/j.ttbdis.2020.101586","article-title":"Detection of pathogens in ixodid ticks collected from animals and vegetation in five regions of Ukraine","volume":"12","author":"Levytska","year":"2021","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1089\/vbz.2021.0006","article-title":"The Prevalence and Genetic Characterization of Strains of Borrelia Isolated from Ixodes Tick Vectors in Belarus (2012\u20132019)","volume":"21","author":"Kniazeva","year":"2021","journal-title":"Vector-Borne Zoonotic Dis."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"645002","DOI":"10.3389\/fmicb.2021.645002","article-title":"High Diversity, Prevalence, and Co-infection Rates of Tick-Borne Pathogens in Ticks and Wildlife Hosts in an Urban Area in Romania","volume":"12","author":"Galon","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1089\/vbz.2020.2716","article-title":"Prevalence of Borrelia burgdorferi and Anaplasma phagocytophilum in Ixodid Ticks from Southeastern Ukraine","volume":"21","author":"Kovryha","year":"2021","journal-title":"Vector-Borne Zoonotic Dis."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"744","DOI":"10.3201\/eid1004.030566","article-title":"Anaplasma phagocytophilum, Babesia microti, and Borrelia burgdorferi in Ixodes scapularis, southern coastal Maine","volume":"10","author":"Holman","year":"2004","journal-title":"Emerg. Infect. Dis."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1603\/0022-2585-41.2.239","article-title":"Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest","volume":"41","author":"Lane","year":"2004","journal-title":"J. Med. Entomol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1999","DOI":"10.1128\/AEM.02479-10","article-title":"Diverse Borrelia burgdorferi strains in a bird-tick cryptic cycle","volume":"77","author":"Hamer","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1589","DOI":"10.3201\/eid1810.120511","article-title":"Wild birds and urban ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005\u20132010","volume":"18","author":"Hamer","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1089\/vbz.2013.1475","article-title":"The prevalence of zoonotic tick-borne pathogens in Ixodes scapularis collected in the Hudson Valley, New York State","volume":"14","author":"Aliota","year":"2014","journal-title":"Vector-Borne Zoonotic Dis."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1186\/s13071-018-2623-0","article-title":"Multiflora rose invasion amplifies prevalence of Lyme disease pathogen, but not necessarily Lyme disease risk","volume":"11","author":"Adalsteinsson","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1111\/zph.12749","article-title":"Active surveillance of pathogens from ticks collected in New York State suburban parks and schoolyards","volume":"67","author":"Yuan","year":"2020","journal-title":"Zoonoses Public Health"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"e00319-21","DOI":"10.1128\/AEM.00319-21","article-title":"Examining prevalence and diversity of tick-borne pathogens in questing Ixodes pacificus ticks in California","volume":"87","author":"Salkeld","year":"2021","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1186\/s13071-021-04750-1","article-title":"Monitoring the patterns of submission and presence of tick-borne pathogens in Ixodes scapularis collected from humans and companion animals in Ontario, Canada (2011\u20132017)","volume":"14","author":"Nelder","year":"2021","journal-title":"Parasites Vectors"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Kim, S.Y., Kim, T.-K., Kim, T.Y., and Lee, H.I. (2020). Geographical Distribution of Borrelia burgdorferi sensu lato in Ticks Collected from Wild Rodents in the Republic of Korea. Pathogens, 9.","DOI":"10.3390\/pathogens9110866"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"547","DOI":"10.4269\/ajtmh.2003.68.547","article-title":"Prevalence of Anaplasma phagocytophila and Borrelia burgdorferi in Ixodes persulcatus ticks from northeastern China","volume":"68","author":"Cao","year":"2003","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Elhelw, R., Elhariri, M., Hamza, D., Abuowarda, M., Ismael, E., and Farag, H. (2021). Evidence of the presence of Borrelia burgdorferi in dogs and associated ticks in Egypt. BMC Vet. Res., 17.","DOI":"10.1186\/s12917-020-02733-5"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-3305-6-1","article-title":"Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe","volume":"6","author":"Medlock","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.ttbdis.2012.07.004","article-title":"Distribution of Ixodes ricinus and I. persulcatus ticks in southern Karelia (Russia)","volume":"4","author":"Bugmyrin","year":"2013","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1111\/j.1365-2915.2009.00813.x","article-title":"Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden","volume":"23","author":"Jaenson","year":"2009","journal-title":"Med. Vet. Entomol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1111\/zph.12369","article-title":"Pet ownership increases human risk of encountering ticks","volume":"65","author":"Jones","year":"2018","journal-title":"Zoonoses Public Health"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"815","DOI":"10.3201\/eid1905.120796","article-title":"Atypical erythema migrans in patients with PCR-positive Lyme disease","volume":"19","author":"Schutzer","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"ref_75","first-page":"5","article-title":"The establishment of a blacklegged tick population by migratory songbirds in Ontario, Canada","volume":"2","author":"Scott","year":"2014","journal-title":"J. Vet. Sci. Med."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.pt.2017.12.006","article-title":"The blacklegged tick, Ixodes scapularis: An increasing public health concern","volume":"34","author":"Eisen","year":"2018","journal-title":"Trends Parasitol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1186\/s13071-017-2042-7","article-title":"Molecular detection of Bartonella henselae in 11 Ixodes ricinus ticks extracted from a single cat","volume":"10","author":"Regier","year":"2017","journal-title":"Parasites Vectors"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.3201\/eid1407.071110","article-title":"Transmission of Bartonella henselae by Ixodes ricinus","volume":"14","author":"Bonnet","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1051\/vetres\/2009019","article-title":"Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles","volume":"40","author":"Tsao","year":"2009","journal-title":"Vet. Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1093\/jmedent\/43.3.600","article-title":"Ixodes scapularis ticks collected by passive surveillance in Canada: Analysis of geographic distribution and infection with Lyme borreliosis agent Borrelia burgdorferi","volume":"43","author":"Ogden","year":"2006","journal-title":"J. Med. Entomol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1780","DOI":"10.1128\/AEM.01982-07","article-title":"Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada","volume":"74","author":"Ogden","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1128\/JCM.39.6.2237-2242.2001","article-title":"Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia","volume":"39","author":"Alekseev","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"4208","DOI":"10.1128\/JCM.38.11.4208-4210.2000","article-title":"Granulocytic Ehrlichiae in Ixodes persulcatus ticks from an area in China where Lyme disease is endemic","volume":"38","author":"Cao","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1046\/j.1469-0691.2001.00200.x","article-title":"Tick-borne bacterial diseases emerging in Europe","volume":"7","author":"Parola","year":"2001","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"\u010cern\u00fd, J., Lynn, G., Hrnkov\u00e1, J., Golovchenko, M., Rudenko, N., and Grubhoffer, L. (2020). Management options for Ixodes ricinus-associated pathogens: A review of prevention strategies. Int. J. Environ. Res. Public Health, 17.","DOI":"10.3390\/ijerph17061830"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Alkishe, A.A., Peterson, A.T., and Samy, A.M. (2017). Climate change influences on the potential geographic distribution of the disease vector tick Ixodes ricinus. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0189092"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1146\/annurev.en.30.010185.002255","article-title":"Ecology of Ixodes dammini-borne human babesiosis and Lyme disease","volume":"30","author":"Spielman","year":"1985","journal-title":"Annu. Rev. Entomol."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Deplazes, P., Eckert, J., Mathis, A., Samson-Himmelstjerna, G., and Zahner, H. (2016). Parasitology in Veterinary Medicine, Wageningen Academic Publishers.","DOI":"10.3920\/978-90-8686-274-0"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Braks, M.A., van Wieren, S.E., Takken, W., and Sprong, H. (2016). Ecology and Prevention of Lyme Borreliosis, Wageningen Academic Publishers.","DOI":"10.3920\/978-90-8686-838-4"},{"key":"ref_90","first-page":"40","article-title":"Ticks as the main target of human tick-borne disease control: Russian practical experience and its lessons","volume":"24","author":"Uspensky","year":"1999","journal-title":"J. Vector Ecol. J. Soc. Vector Ecol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1146\/annurev.ento.53.103106.093429","article-title":"Prevention of tick-borne diseases","volume":"53","author":"Piesman","year":"2008","journal-title":"Annu. Rev. Entomol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/12\/2412\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:34:28Z","timestamp":1760168068000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/12\/2412"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,23]]},"references-count":91,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["microorganisms9122412"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9122412","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,23]]}}}