Lyme Borreliosis in Horses

Yıl 2024, Cilt: 3 Sayı: 2, 48 - 65, 31.12.2024

Barış Tolga Candan , Ilgın Kekeç , Büşra Gülay Celil Özaslan , Barış Halaç

Öz

Lyme disease is a zoonotic disease caused by Borrelia burgdorferi, a spiral-shaped bacterium, transmitted especially by tick species of the Ixodes genus, and has a wide host range. The fact that vector ticks spread widely around the world and can travel long distances with wild animals and migratory birds is an important risk factor. Lyme disease was named as a result of studies carried out relatively recently in 1975, due to an epidemic that caused arthritis-like symptoms in children and adults in the Lyme Town of Connecticut, USA, and the causative agent Borrelia burgdorferi was isolated and named by Willy Burgdorfer in 1982. It has non-pathognomonic findings such as chronic wasting, behavioral changes, abortion, mild fever, and causes nervous symptoms, namely neuroborrelliosis, in horses. Lyme is a disease that poses a risk to public health due to the zoonotic character of Borrelia burgdorferi, and the fact that animals that have extensive contact with humans, such as cats, dogs and horses, cause serious cases in humans as well. It is known that the seroprevalence of Lyme disease, for which serological tests play a key role in diagnosis as it is very difficult to reproduce in culture, is high and is increasing day by day, as international animal movements are becoming easier and the spread of vector ticks is changing with global warming.
In this review, it is aimed to provide general information about Lyme disease and its causative agent, which is an animal disease that is not yet mandatory to be notified in Turkey, its diagnosis and treatment, as well as information about the seroprevalence obtained from studies conducted with horses in Turkey and around the world.

Anahtar Kelimeler

Horse, Borreliosis, Borrelia burgdorferi, Lyme Disease, Turkiye

Atlarda Lyme Borreliozis

Öz

Lyme hastalığı, spiral şekilli bir bakteri olan Borrelia burgdorferi tarafından oluşturulan, özellikle Ixodes cinsi kene türleri ile bulaşan ve geniş bir konakçı yelpazesi bulunan zoonoz bir hastalıktır. Vektör kenelerin dünya genelinde geniş bir yayılım göstermesi, yaban hayvanları ve göçmen kuşlarla uzun mesafelere ulaşabilmesi önemli bir risk faktörüdür. Lyme hastalığı, 1975 yılında nispeten yakın sayılabilecek bir tarihte, ABD’nin Connecticut Eyaletinin Lyme Kasabasında çocuklar ve yetişkinlerde ortaya çıkan artrit benzeri semptomlar veren salgın nedeniyle yapılan çalışmalar sonucu adlandırılmış, etken Borrelia burgdorferi ise 1982 yılında Willy Burgdorfer tarafından izole edilerek adlandırılmıştır. Kronik zayıflama, davranış değişiklikleri, abort, hafif ateş gibi patognomik olmayan bulgulara sahiptir ve atlarda sinirsel semptomlara yani nöroborrelliozise neden olmaktadır. Lyme hastalığı etkeni Borrelia burgdorferi’nin zoonoz karakteri ve kedi, köpek, at gibi insanlarla yoğun teması olan hayvanların da konakçı olması nedeniyle insanlarda da ciddi vakalara neden olması sebebiyle toplum sağlığı açısından risk oluşturan bir hastalıktır. Kültür ortamında üremesi oldukça güç olduğundan, tanısında serolojik testlerin kilit rol oynadığı Lyme hastalığının seroprevalansının yüksek olduğu ve uluslararası hayvan hareketlerinin kolaylaştığı, vektör kenelerin küresel ısınma ile yayılımının değişim gösterdiği günümüzde, gün geçtikçe arttığı bilinmektedir.
Bu derlemede, Türkiye’de henüz ihbarı zorunlu olmayan bir hayvan hastalığı olan, Lyme hastalığı ve etkeni hakkında genel bilgi, tanı ve tedavisi ile birlikte Türkiye’de ve dünyada atlar ile yapılmış çalışmalarda elde edilen seroprevalansa dair bilgi verilmesi amaçlanmıştır.

Anahtar Kelimeler

At, Borreliozis, Borrelia burgdorferi, Lyme hastalığı, Türkiye

Kaynakça

• Alruhaili M.H., Marzok M., Gattan H.S., Salem M., Abd El-Lateef H.M. & Selim A. (2024) Seroprevalence and Assessment of Risk Factors Associated to Borrelia burgdorferi Infection in Egyptian Horses. Kafkas Univ Vet Fak Derg., 30(3): 349-354.
• Amusategui I., Tesouro M.A., Kakoma I. & Sainz A. (2008). Serological reactivity to Ehrlichia canis, Anaplasma phagocytophilum, Neorickettsia risticii, Borrelia burgdorferi and Rickettsia conorii in dogs from northwestern Spain. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 8(6): 797–803. https://doi.org/10.1089/vbz.2007.0277
• Basile R.C., Rivera G.G., Del Rio L.A., de Bonis T.C., do Amaral G.P., Giangrecco E., Ferraz G., Yoshinari N.H., Canola P.A. & Queiroz Neto A. (2015). Anaphylactoid reaction caused by sodium ceftriaxone in two horses experimentally infected by Borrelia burgdorferi. BMC Veterinary Research, 11: 197. https://doi.org/10.1186/s12917-015-0478-6
• Bhide M., Yilmaz Z., Golcu E., Torun S. & Mikula I. (2008). Seroprevalence of anti-Borrelia burgdorferi antibodies in dogs and horses in Turkey. Annals of agricultural and environmental medicine: AAEM, 15(1): 85–90.
• Brodziński S. & Nasierowski T. (2019). Psychosis in Borrelia burgdorferi infection - part I: epidemiology, pathogenesis, diagnosis and treatment of neuroborreliosis. Zaburzenia psychotyczne w przebiegu zakażenia Borrelia burgdorferi – część I: epidemiologia, patogeneza, diagnostyka i leczenie neuroboreliozy. Psychiatria Polska, 53(3): 629–640. https://doi.org/10.12740/PP/97336
• Butler C.M., Houwers D.J., Jongejan F. & van der Kolk J.H. (2005). Borrelia burgdorferi infections with special reference to horses. A review. The Veterinary Quarterly, 27(4): 146–156.
• Burgess B. (1988). British Columbia. Lyme Disease in horses. The Canadian Veterinary Journal, 29(4): 393–394.
• Cabello F.C., Godfrey H.P. & Newman S.A. (2007). Hidden in plain sight: Borrelia burgdorferi and the extracellular matrix. Trends in Microbiology, 15(8): 350–354. https://doi.org/10.1016/j.tim.2007.06.003
• Caol S., Divers T., Crisman M. & Chang Y.F. (2017). In vitro susceptibility of Borrelia burgdorferi isolates to three antibiotics commonly used for treating equine Lyme disease. BMC Veterinary Research, 13(1): 293. https://doi.org/10.1186/s12917-017-1212-3
• Chang Y.F., Ku Y. W., Chang C.F., Chang C.D., McDonough S.P., Divers T., Pough M. & Torres A. (2005). Antibiotic treatment of experimentally Borrelia burgdorferi-infected ponies. Veterinary Microbiology, 107(3-4): 285–294. https://doi.org/10.1016/j.vetmic.2005.02.006
• Chang Y.F., Novosol V., McDonough S.P., Chang C.F., Jacobson R.H., Divers T., Quimby F.W., Shin S. & Lein D.H. (2000). Experimental infection of ponies with Borrelia burgdorferi by exposure to Ixodid ticks. Veterinary Pathology, 37(1): 68–76. https://doi.org/10.1354/vp.37-1-68
• Clark K.L., Leydet B. & Hartman S. (2013). Lyme borreliosis in human patients in Florida and Georgia, USA. International Journal of Medical Sciences, 10(7): 915–931. https://doi.org/10.7150/ijms.6273
• Couto C.G., Lorentzen L., Beall M.J., Shields J., Bertolone N., Couto J.I., Couto K. M., Nash S., Slack J., Kvitko H., Westendorf N., Marin L., Iazbik M.C., Vicario F.C., Sanz P. & Ruano R. (2010). Serological study of selected vector-borne diseases in shelter dogs in central Spain using point-of-care assays. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 10(9): 885–888. https://doi.org/10.1089/vbz.2009.0063
• Demaerschalck I., Ben Messaoud A., De Kesel M., Hoyois B., Lobet Y., Hoet P., Bigaignon G., Bollen A. & Godfroid, E. (1995). Simultaneous presence of different Borrelia burgdorferi genospecies in biological fluids of Lyme disease patients. Journal of Clinical Microbiology, 33(3): 602–608. https://doi.org/10.1128/jcm.33.3.602-608.1995
• Demir Ö. & Keskin, O. (2019). Şanlıurfa’da Safkan Arap Atlarında Borrelia burgdorferi Seropozitifliğinin Belirlenmesi. Harran Üniv Vet Fak Derg. 8(2): 221-224
• Divers T.J., Chang Y.F., Jacobson R.H. & McDonough S.P. (2001) Lyme disease in horses. Comp Cont Educ Prac Vet. 23: 375-380.
• Divers T.J., Gardner R.B., Madigan J.E., Witonsky S.G., Bertone J.J., Swinebroad E.L., Schutzer S.E. & Johnson A.L. (2018). Borrelia burgdorferi Infection and Lyme Disease in North American Horses: A Consensus Statement. Journal of Veterinary Internal Medicine, 32(2): 617–632. https://doi.org/10.1111/jvim.15042
• Divers T.J. (2013) Equine lyme disease. J. Equine Vet. Sci..:33(7):488-492.
• Dressler F., Whalen J.A., Reinhardt B.N. & Steere A.C. (1993). Western blotting in the serodiagnosis of Lyme disease. The Journal of Infectious Diseases, 167(2): 392–400. https://doi.org/10.1093/infdis/167.2.392
• Durrani A.Z., Goyal S. M. & Kamal N. (2011). Retrospective Study on Seroprevalence of Borrelia burgdorferi Antibodies in Horses in Minnesota. Journal of Equine Veterinary Science, 31(8): 427–429. https://doi.org/10.1016/j.jevs.2011.03.007
• El Hamzaoui B., Laroche M., Bechah Y., Bérenger J.M. & Parola P. (2019). Testing the Competence of Cimex lectularius Bed Bugs for the Transmission of Borrelia recurrentis, the Agent of Relapsing Fever. The American Journal of Tropical Medicine and hygiene, 100(6): 1407–1412. https://doi.org/10.4269/ajtmh.18-0804
• Fikrig E. & Narasimhan S. (2006). Borrelia burgdorferi--traveling incognito?. Microbes and Infection, 8(5): 1390–1399. https://doi.org/10.1016/j.micinf.2005.12.022
• Funk R.A., Pleasant R.S., Witonsky S.G., Reeder D.S., Werre S.R. & Hodgson D.R. (2016). Seroprevalence of Borrelia burgdorferi in Horses Presented for Coggins Testing in Southwest Virginia and Change in Positive Test Results Approximately 1 Year Later. Journal of Veterinary Internal Medicine, 30(4): 1300–1304. https://doi.org/10.1111/jvim.13973
• Gern L., Estrada-Peña A., Frandsen F., Gray J. S., Jaenson T. G., Jongejan F., Kahl O., Korenberg E., Mehl R. & Nuttall P. A. (1998). European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblatt fur Bakteriologie: International Journal of Medical Microbiology, 287(3):196–204. https://doi.org/10.1016/s0934-8840(98)80121-7
• Hansen M.G., Christoffersen M., Thuesen L.R., Petersen M.R. & Bojesen A.M. (2010). Seroprevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in Danish horses. Acta Veterinaria Scandinavica, 52(1): 3. https://doi.org/10.1186/1751-0147-52-3
• Hayes S. & Burgdorfer W. (1993). Ultrastructure of Borrelia burgdorferi. In Springer eBooks (pp. 29–43). https://doi.org/10.1007/978-3-642-77614-4_3
• Hızel K. (1997). Lyme hastalığı. Klimik Derg,10 (1): 7-11.
• Humair P. & Gern L. (2000). The wild hidden face of Lyme borreliosis in Europe. Microbes and Infection, 2(8): 915–922. https://doi.org/10.1016/s1286-4579(00)00393-2
• Imai D. M., Barr B. C., Daft B., Bertone J. J., Feng S., Hodzic E., Johnston J.M., Olsen, K.J. & Barthold S.W. (2011). Lyme neuroborreliosis in 2 horses. Veterinary Pathology, 48(6): 1151–1157. https://doi.org/10.1177/0300985811398246
• İnci A. & Düzlü Ö. (2009). Vektörler ve Vektörlerle Bulaşan Hastalıklar [Vectors and Vector-Borne Diseases]. Erciyes Üniv Vet Fak Derg, 6(1):53-63.
• İzgür M. (1997). Sığır Kan Serumlarında Borrelıa Burgdorferı Antikorlarının Flüoresan Antikor Tekniği İle Türkiye'de İlk Kez Saptanması. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 44(01): 57-62.
• Johnson A.L., Divers T.J. & Chang Y.F. (2008). Validation of an in-clinic enzyme-linked immunosorbent assay kit for diagnosis of Borrelia burgdorferi infection in horses. Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc, 20(3): 321–324. https://doi.org/10.1177/104063870802000309
• Johnstone L.K., Engiles J.B., Aceto H., Buechner-Maxwell V., Divers T., Gardner R., Levine R., Scherrer N., Tewari D., Tomlinson J. & Johnson A.L. (2016). Retrospective Evaluation of Horses Diagnosed with Neuroborreliosis on Postmortem Examination: 16 Cases (2004-2015). Journal of Veterinary Internal Medicine, 30(4): 1305 –1312. https://doi.org/10.1111/jvim.14369
• Käsbohrer A. & Schönberg A. (1990). Serologische Untersuchungen zum Vorkommen von Borrelia burgdorferi bei Haustieren in Berlin (West) [Serologic studies of the occurrence of Borrelia burgdorferi in domestic animals in Berlin (West)]. Berliner und Munchener Tierarztliche Wochenschrift, 103(11): 374–378.
• Liang F.T., Brown E.L., Wang T., Iozzo R.V. & Fikrig E. (2004). Protective niche for Borrelia burgdorferi to evade humoral immunity. The American Journal of Pathology, 165(3): 977–985. https://doi.org/10.1016/S0002-9440(10)63359-7
• Lindgren E. & Jaenson TGT. (2016) WHO Lyme borreliosis in Europe: influences of climate and climate change, epidemiology, ecology and adaptation measures, http://www.euro.who.int/ data/assets/pdf_file/0006/96819/E8952 2.pdf
• Magnarelli L.A. & Anderson J.F. (1988). Ticks and biting insects infected with the etiologic agent of Lyme disease, Borrelia burgdorferi. Journal of Clinical Microbiology, 26(8): 1482–1486. https://doi.org/10.1128/jcm.26.8.1482-1486.1988
• Magnarelli L.A., Ijdo J.W., Van Andel A.E., Wu C., Padula S.J. & Fikrig E. (2000). Serologic confirmation of Ehrlichia equi and Borrelia burgdorferi infections in horses from the northeastern United States. Journal of the American Veterinary Medical Association, 217(7): 1045–1050. https://doi.org/10.2460/javma.2000.217.1045
• Margos G., Fingerle V. & Reynolds S.E. (2019). Borrelia bavariensis: Vector Switch, Niche Invasion, and Geographical Spread of a Tick-Borne Bacterial Parasite. Front. Ecol. Evol. 7. 1-21 https://doi.org/10.3389/fevo.2019.00401
• Margos G., Tsao, J. I., Castillo-Ramírez S., Girard Y.A., Hamer S. A., Hoen A.G., Lane R.S., Raper, S.L. & Ogden N.H. (2012). Two boundaries separate Borrelia burgdorferi populations in North America. Applied and Environmental Microbiology, 78(17): 6059–6067. https://doi.org/10.1128/AEM.00231-12
• Masuzawa T. (2004). Terrestrial distribution of the Lyme borreliosis agent Borrelia burgdorferi sensu lato in East Asia. Japanese Journal of Infectious Diseases, 57(6): 229–235.
• Maurizi L., Marié J.L., Aoun O., Courtin C., Gorsane S., Chal D. & Davoust B. (2010). Seroprevalence survey of equine Lyme borreliosis in France and in sub-Saharan Africa. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 10(5): 535–537. https://doi.org/10.1089/vbz.2009.0083
• Motaleb M.A., Liu J. & Wooten R.M. (2015). Spirochetal motility and chemotaxis in the natural enzootic cycle and development of Lyme disease. Current Opinion in Microbiology, 28: 106–113. https://doi.org/10.1016/j.mib.2015.09.006
• Neely M., Arroyo L.G., Jardine C., Moore A., Hazlett M., Clow K., Archer H. & Weese J.S. (2021). Seroprevalence and evaluation of risk factors associated with seropositivity for Borrelia burgdorferi in Ontario horses. Equine Veterinary Journal, 53(2): 331–338. https://doi.org/10.1111/evj.13317
• Ogden N.H., Radojevic M., Wu X., Duvvuri V.R., Leighton P.A. & Wu J. (2014). Estimated effects of projected climate change on the basic reproductive number of the Lyme disease vector Ixodes scapularis. Environmental Health Perspectives, 122(6): 631–638. https://doi.org/10.1289/ehp.1307799
• Öncel S. (2018). Türkiye’de Lyme hastalığı. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi, 4(3), 103–106. https://doi.org/10.30934/kusbed.423490
• Özeren G.S., Kaya G. & Önlen Y. (2013). Seroprevalence of Tick-Borne lyme borreliosis in Hatay. Klimik Dergisi 25(2): 58–62. https://doi.org/10.5152/kd.2012.17
• Öztürk D.B. (2019). Türkiye’den Bildirilen Lyme Hastalığı Olgularının Havuz Analizi Yöntemiyle Değerlendirilmesi. FLORA, 24(1): 46-51.
• Pal U., Montgomery R.R., Lusitani D., Voet P., Weynants V., Malawista S.E., Lobet Y. & Fikrig E. (2001). Inhibition of Borrelia burgdorferi-tick interactions in vivo by outer surface protein A antibody. Journal of Immunology (Baltimore, Md. : 1950), 166(12): 7398–7403. https://doi.org/10.4049/jimmunol.166.12.7398.
• Pantchev N., Schnyder M., Vrhovec M. G., Schaper R. & Tsachev I. (2015). Current Surveys of the Seroprevalence of Borrelia burgdorferi, Ehrlichia canis, Anaplasma phagocytophilum, Leishmania infantum, Babesia canis, Angiostrongylus vasorum and Dirofilaria immitis in Dogs in Bulgaria. Parasitology Research, 114 Suppl 1: S117–S130. https://doi.org/10.1007/s00436-015-4518-8
• Ramamoorthi N., Narasimhan S., Pal U., Bao F., Yang X.F., Fish D., Anguita J., Norgard M.V., Kantor F.S., Anderson J. F., Koski R.A. & Fikrig E. (2005). The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature, 436(7050): 573–577. https://doi.org/10.1038/nature03812
• Ranka R., Bormane A., Salmina K. & Baumanis V. (2004). Identification of three clinically relevant Borrelia burgdorferi sensu lato genospecies by PCR-restriction fragment length polymorphism analysis of 16S-23S ribosomal DNA spacer amplicons. Journal of Clinical Microbiology, 42(4): 1444–1449. https://doi.org/10.1128/JCM.42.4.1444-1449.2004
• Re III, V.L., Occi J.L. & MacGregor R.R. (2004). Identifying the vector of Lyme disease. American Family Physician, 69(8): 1935–1937.
• Rudenko N., Golovchenko M., Grubhoffer L. & Oliver J.H., Jr (2011). Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks and Tick-Borne Diseases, 2(3): 123–128. https://doi.org/10.1016/j.ttbdis.2011.04.002
• Rupprecht T.A., Koedel U., Fingerle V. & Pfister H.W. (2008). The pathogenesis of lyme neuroborreliosis: from infection to inflammation. Molecular Medicine (Cambridge, Mass.), 14(3-4): 205–212. https://doi.org/10.2119/2007-00091.Rupprecht
• Scherrer N.M., Knickelbein K.E., Engiles J. B., Johnstone L.K., Tewari D. & Johnson A. L. (2020). Ocular disease in horses with confirmed ocular or central nervous system Borrelia infection: Case series and review of literature. Veterinary Ophthalmology, 23(6): 1014–1024. https://doi.org/10.1111/vop.12817
• Schwan T.G. & Piesman J. (2000). Temporal changes in outer surface proteins A and C of the lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. Journal of Clinical Microbiology, 38(1): 382–388. https://doi.org/10.1128/JCM.38.1.382-388.2000
• Sears K.P., Divers T.J., Neff R.T., Miller W.H. Jr & McDonough S. P. (2012). A case of Borrelia-associated cutaneous pseudolymphoma in a horse. Veterinary Dermatology, 23(2), 153–156. https://doi.org/10.1111/j.1365-3164.2011.01013.x
• Singh S. K. & Girschick H. J. (2004). Molecular survival strategies of the Lyme disease spirochete Borrelia burgdorferi. The Lancet. Infectious Diseases, 4(9): 575–583. https://doi.org/10.1016/S1473-3099(04)01132-6
• Solay, A.H. & Cezayir, D.Y. (2024). Fonksiyonel Tıbbın Lyme Hastalığı Tedavisindeki Yeri. Turkiye Klinikleri Infectious Diseases-Special Topics, 17(1): 82-85.
• Songer G.J. & Post K.W. (2004). Veterinary Microbiology, Bacterial and Fungal Agents of Animal Diseases, Elsevier Saunders, (9): 10-80.
• Sorensen K. (1990) Lyme disease antibodies in thoroughbred broodmares. correlation to early pregnancy failure. J. Equine Vet. Sci. (10): 166–168.
• Stanek G., Gray J., Strle F., Wormser G. (2004). Lyme borreliosis. The Lancet. Infectious Diseases, 4(4): 197–199. https://doi.org/10.1016/S1473-3099(04)00965-X
• Steere A. C., Strle F., Wormser G.P., Hu L.T., Branda J.A., Hovius J. ., Li X. & Mead P.S. (2016). Lyme borreliosis. Nature reviews. Disease Primers, 2: 16090. https://doi.org/10.1038/nrdp.2016.90
• Stefanciková A., Adaszek Ł., Pet'ko B., Winiarczyk S. & Dudinák V. (2008). Serological evidence of Borrelia burgdorferi sensu lato in horses and cattle from Poland and diagnostic problems of Lyme borreliosis. Annals of Agricultural and Environmental Medicine : AAEM, 15(1): 37–43.
• Stricker R.B., Lautin A. & Burrascano J. J. (2005). Lyme disease: point/counterpoint. Expert Review of Anti-infective Therapy, 3(2): 155–165. https://doi.org/10.1586/14787210.3.2.155
• Şen E. (2006) Lyme hastalığının epidemiyolojisi [Epidemiology of Lyme disease], Turk Mikrobiyol Cem Derg. 36 (1): 55-66.
• Tekbıyık S. & Eyigör M. (2006). İnsanlarda ve Sığırlarda Borrelia burgdorferii İnfeksiyonunun ELISA Yöntemiyle Tanısı, VII. Ulusal Veteriner Mikrobiyoloji Kongresi (Uluslararası katılımlı), Antalya, Turkey, pp.188-189
• Wagner B., Freer H., Rollins A., Erb H. N., Lu Z. & Gröhn Y. (2011). Development of a multiplex assay for the detection of antibodies to Borrelia burgdorferi in horses and its validation using Bayesian and conventional statistical methods. Veterinary Immunology and Immunopathology, 144(3-4): 374–381. https://doi.org/10.1016/j.vetimm.2011.08.005
• Wilske B. (2003). Diagnosis of lyme borreliosis in europe. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 3(4): 215–227. https://doi.org/10.1089/153036603322662200
• Wolcott K.A., Margos G., Fingerle V. & Becker N.S. (2021). Host association of Borrelia burgdorferi sensu lato: A review. Ticks and Tick-borne Diseases, 12(5): 101766. https://doi.org/10.1016/j.ttbdis.2021.101766
• Yener M. & İkiz S. (2022). Lyme hastalığı ve Türkiye’de köpeklerdeki durumu. İstanbul Rumeli Üniversitesi Sağlık Bilimleri Dergisi, 1(1): 49-65.
• Yücel A. & Çalışır B. (1997). Lyme hastalığı ve vektörleri. Parazitolojide Artropod Hastalıkları ve Vektörleri, [Lyme disease and its vectors. Arthropod Diseases and Vectors in Parasitology] Türkiye Parazitol. Der, 1(13): 435–457.