An investigation on the presence of apicomplexan parasites of the genus Babesia in ticks collected from wild mammals in Türkiye

Year 2025, Volume: 7 Issue: 2, 118 - 124, 31.07.2025

Muhsin Kişi , Ayşe Sarı , Ahmet Yesari Selçuk , Adem Keskin

https://doi.org/10.47121/acarolstud.1698839

Abstract

Members of the genus Babesia, belonging to the group Apicomplexa, are protozoan parasites transmitted by ticks to humans and animals, infecting the red blood cells of mammals. In the present study, a total of 112 ticks collected from 80 different hosts belonging to 23 mammalian species from 16 provinces in Türkiye were screened for the presence of Babesia using PCR with primers targeting the 411-452 base pair region of the 18S rRNA gene. As a result of molecular analyses, Babesia positivity was detected in 7 ticks (6.25%). Phylogenetic analysis revealed the presence of Babesia microti in Ixodes acuminatus ticks collected from Edirne, Balıkesir, and Tokat provinces and Babesia caballi in a Hyalomma species tick collected from Kars province. These findings highlight the presence of Babesia pathogens in ticks collected from wild mammals in Türkiye, underscoring the ecological and epidemiological significance of these species. The study provides valuable data for understanding the spread of tick-borne diseases and for developing control strategies.

Keywords

Acari, Babesia, diseases, ectoparasites, Mammalia, ticks, zoonoses

Ethical Statement

Not applicable.

Supporting Institution

The Scientific and Technological Research Council of Türkiye (TÜBİTAK)

Project Number

2209A-1919B012323597

References

• Aktas, M., Altay, K. and Dumanli, N. 2007. Determination of prevalence and risk factors for infection with Babesia ovis in small ruminants from Turkey by polymerase chain reaction. Parasitology Research, 100 (4): 797-802. doi: 10.1007/s00436-006-0345-2
• Aktas, M., Altay, K., Ozubek, S. and Dumanli, N. 2012. A survey of ixodid ticks feeding on cattle and prevalence of tick-borne pathogens in the Black Sea region of Turkey. Veterinary Parasitology, 187 (3-4): 567-571. doi: 10.1016/j.vetpar.2012.01.035
• Aktas, M. and Ozubek, S. 2015. Molecular and parasitological survey of bovine piroplasms in the Black Sea Region, including the first report of babesiosis associated with Babesia divergens in Turkey. Journal of Medical Entomology, 52 (6): 1344-1350. doi: 10.1093/jme/tjv126
• Altay, K., Atas, A.D., Ograk, Y.Z. and Ozkan, E. 2020. Survey of Theileria, Babesia and Anaplasma infections of cattle and ticks from Sivas region of Turkey. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 17 (1): 32-38. doi: 10.32707/ercivet.690618
• Altuğ, N., Muz, M.N., Muz, D. and Yipel, F.A. 2022. The molecular prevalence of Borrelia burgdorferi, Babesia spp., and Anaplasma spp. in shelter dogs of the Thrace Region in Turkey. Turkish Journal of Veterinary and Animal Sciences, 46 (3): 483-493. doi: 10.55730/1300-0128.4219
• Aslantaş, Ö., Çelebi, B. and Usluca, S. 2020. Investigation of vector-borne diseases in dogs. Harran Üniversitesi Veteriner Fakültesi Dergisi, 9 (2): 154-160. doi: 10.31196/huvfd.792147
• Aydın, N., Vatansever, Z. and Arslan, M.Ö. 2022. Molecular epidemiology of Babesia and Theileria species in sheep in Kars region of Turkey. Turkish Journal of Parasitology, 46 (1): 20-27. doi: 10.4274/tpd.galenos.2021.09709
• Babes, V. 1888. Sur l’hemoglobinurie bacterienne du boeuf. Comptes rendus de l'Académie des Sciences, 107: 692-694. [In French]
• Bakirci, S., Sarali, H., Aydin, L., Eren, H. and Karagenc, T. 2012. Distribution and seasonal activity of tick species on cattle in the West Aegean region of Turkey. Experimental and Applied Acarology, 56 (2): 165-178. doi: 10.1007/s10493-011-9502-0
• Bursali, A., Keskin, A. and Tekin, S. 2012. A review of the ticks (Acari: Ixodida) of Turkey: Species diversity, hosts and geographical distribution. Experimental and Applied Acarology, 57 (1): 91-104. doi: 10.1007/s10493-012-9530-4
• Bursali, A., Keskin, A. and Tekin, S. 2013. Ticks (Acari: Ixodida) infesting humans in the provinces of Kelkit Valley, a Crimean-Congo hemorrhagic fever endemic region in Turkey. Experimental and Applied Acarology, 59 (4): 507-515. doi: 10.1007/s10493-012-9608-z
• Bursalı, A., Tekin, Ş. and Keskin, A. 2020. A contribution to the tick (Acari: Ixodidae) fauna of Turkey: The first record of Ixodes inopinatus Estrada-Peña, Nava and Petney. Acarological Studies, 2 (2): 126-130. doi: 10.47121/acarolstud.706768
• Casati, S., Sager, H., Gern, L. and Piffaretti, J.C. 2006. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Annals of Agricultural and Environmental Medicine, 13 (1): 65-70.
• Chitimia-Dobler, L., Mans, B.J., Handschuh, S. and Dunlop, J.A. 2022. A remarkable assemblage of ticks from mid-Cretaceous Burmese amber. Parasitology, 149 (6): 820-830. doi: 10.1017/S0031182022000269
• Chitimia-Dobler, L., Handschuh, S., Dunlop, J.A., Pienaar, R. and Mans, B.J. 2024. Nuttalliellidae in Burmese amber: implications for tick evolution. Parasitology, 151 (9): 891-907. doi: 10.1017/S0031182024000477
• Dantas-Torres, F. 2018. Species concepts: What about ticks? Trends in Parasitology, 34 (12): 1017-1026. doi: 10.1016/j.pt.2018.09.009
• Estrada-Peña, A., Mihalca, A.D. and Petney, T.N. 2017. Ticks of Europe and North Africa: A guide to species identification. Springer, The Netherlands, 404 pp. doi: 10.1007/978-3-319-63760-0
• Filippova, N.A. 1997. Fauna of Russia and neighbouring countries. Ixodid ticks of subfamily Amblyomminae. 4 (5). Nauka Publishing House, St Petersburg, Russia, 436 pp. [In Russian]
• Filippova, N.A. 1977. Ixodid ticks (Ixodinae). Fauna USSR New Ser. 4 (4). Nauka, Moscow, Leningrad, Russia, 316 pp. [In Russian]
• Dantas-Torres, F., Alves, L.C. and Uilenberg, G. 2017. Babesiosis. In: Arthropod borne diseases. Marcondes, C.B. (Ed.). Springer International Publishing, Switzerland, 347-354. doi: 10.1007/978-3-319-13884-8_21
• Gargili, A., Kar, S., Yilmazer, N., Ergönül, O. and Vatansever, Z. 2011. Different abundances of human-biting ticks in two neighboring provinces in Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi, 17 (Suppl. A): 93-97. doi: 10.9775/kvfd.2010.3545
• Gargili, A., Palomar, A.M., Midilli, K., Portillo, A., Kar, S. and Oteo, J.A. 2012. Rickettsia species in ticks removed from humans in Istanbul, Turkey. Vector-Borne and Zoonotic Diseases, 12 (11): 938-941. doi: 10.1089/vbz.2012.0996
• Guven, E., Akyuz, M., Kirman, R., Balkaya, I. and Avcioglu, H. 2022. Zoonotic Babesia microti infection in wild rodents in Erzurum province, northeastern Turkey. Zoonoses and Public Health, 69 (7): 875-883. doi: 10.1111/zph.12983
• Hildebrandt, A., Zintl, A., Montero, E., Hunfeld, K.P. and Gray, J. 2021. Human Babesiosis in Europe. Pathogens, 10 (9): 1165. doi: 10.3390/pathogens10091165
• İbiş, O., Koepfli, K. P., Özcan, S. and Tez, C. 2023. Whole mitogenomes of Turkish white-toothed shrews, genus Crocidura (Eulipotyphla: Soricidae), with new insights into the phylogenetic positions of Crocidura leucodon and the Crocidura suaveolens group. Organisms Diversity & Evolution, 23 (1): 221-241. doi: 10.1007/s13127-022-00579-3
• Jongejan, F. and Uilenberg, G. 2004. The global importance of ticks. Parasitology, 129 (S1): S3-S14. doi: 10.1017/S0031182004005967
• Kadir, K., Özçelik, S. and Malatyalı, E. 2010. The investigation of seroprevalence of human babesiosis in Sivas. Cumhuriyet Medical Journal, 32 (4): 280-376.
• Karasartova, D., Gureser, A.S., Gokce, T., Celebi, B., Yapar, D., Keskin, A., Celik, S., Ece, Y., Erenler, A.K., Usluca, S., Mumcuoglu, K.Y. and Taylan-Ozkan, A. 2018. Bacterial and protozoal pathogens found in ticks collected from humans in Corum province of Turkey. PLOS Neglected Tropical Diseases, 12 (4): e0006395. doi: 10.1371/journal.pntd.0006395
• Keskin, A., Bursali, A., Keskin, A. and Tekin, S. 2016. Molecular detection of spotted fever group rickettsiae in ticks removed from humans in Turkey. Ticks and Tick-Borne Diseases, 7 (5): 951-953. doi: 10.1016/j.ttbdis.2016.04.015
• Keskin, A., Koprulu, T.K., Bursali, A., Ozsemir, A.C., Yavuz, K.E. and Tekin, S. 2014. First record of Ixodes arboricola (Ixodida: Ixodidae) from Turkey with presence of Candidatus Rickettsia vini (Rickettsiales: Rickettsiaceae). Journal of Medical Entomology, 51 (4): 864-867. doi: 10.1603/ME13169
• Keskin, A. and Doi, K. 2025. Discovery of the potentially invasive Asian longhorned tick, Haemaphysalis longicornis Neumann (Acari: Ixodidae) in Türkiye: an unexpected finding through citizen science. Experimental and Applied Acarology, 94 (3): 47. doi: 10.1007/s10493-025-01015-9
• Kryštufek, B. and Vohralík, V. 2001. Mammals of Turkey and Cyprus. Introduction, checklist, Insectivora. Knjiznica Annales Majora, Koper, Slovenia, 140 pp.
• Kryštufek, B. and Vohralík, V. 2007. Distribution of field mice (Apodemus) (Mammalia: Rodentia) in Anatolia. Zoology in the Middle East, 42 (1): 25-36. doi: 10.1080/09397140.2007.10638243
• Kryštufek, B. and Vohralík, V. 2009. Mammals of Turkey and Cyprus: Rodentia II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromydae, Hystricidae, Castoridae. Knjiznica Annales Majora, Koper, Slovenia, 372 pp.
• Kryštufek, B. and Shenbrot, G. 2022. Voles and lemmings (Arvicolinae) of the Palaearctic region. University of Maribor, University Press, Maribor, Slovenia, 449 pp.
• Kumar, S., Stecher, G., Suleski, M., Sanderford, M., Sharma, S. and Tamura, K. 2024. MEGA12: Molecular evolutionary genetic analysis version 12 for adaptive and green computing. Molecular Biology and Evolution, 41: 1-9. doi: 10.1093/molbev/msae263
• Kurt, E.K., Kandemir, B., Handemir, E. and Bitirgen, M. 2021. A rare zoonotic infection in Konya; case report of babesiozis. Genel Tıp Dergisi, 31 (2): 182-184. [In Turkish] doi: 10.15321/GenelTipDer.2021.311
• Mahmoud, M.S., Kandil, O.M., Abu El-Ezz, N. T., Hendawy, S.H.M., Elsawy, B.S.M., Knowles, D.P., Bastos, R.G., Kappmeyer, L.S., Laughery, J.M., Alzan, H.F. and Suarez, C.E. 2020. Identification and antigenicity of the Babesia caballi spherical body protein 4 (SBP4). Parasites and Vectors, 13 (1): 369. doi: 10.1186/s13071-020-04241-9
• Mahmoudi, A., Golenishchev, F.N., Malikov, V.G., Arslan, A., Pavlova, S.V., Petrova, T.V. and Kryštufek, B. 2022. Taxonomic evaluation of the “irani–schidlovskii” species complex (Rodentia: Cricetidae) in the Middle East: A morphological and genetic combination. Zoologischer Anzeiger, 300: 1-11. doi:10.1016/j.jcz.2022.07.001
• Ochi, A., Kidaka, T., Hakimi, H., Asada, M. and Yamagishi, J. 2023. Chromosome-level genome assembly of Babesia caballi reveals diversity of multigene families among Babesia species. BMC Genomics, 24 (1): 483. doi: 10.1186/s12864-023-09540-w
• Orkun, Ö. and Emir, H. 2020. Identification of tick-borne pathogens in ticks collected from wild animals in Turkey. Parasitology Research, 119 (9): 3083-3091. doi: 10.1007/s00436-020-06812-2
• Orkun, Ö. and Karaer, Z. 2017. Molecular characterization of Babesia species in wild animals and their ticks in Turkey. Infection, Genetics and Evolution, 55: 8-13. doi: 10.1016/j.meegid.2017.08.026
• Orkun, Ö. and Karaer, Z. 2018. First record of the tick Ixodes (Pholeoixodes) kaiseri in Turkey. Experimental and Applied Acarology, 74 (2): 201-205. doi: 10.1007/s10493-018-0219-1
• Orkun, Ö., Karaer, Z., Çakmak, A. and Nalbantoğlu, S. 2014. Identification of tick-borne pathogens in ticks feeding on humans in Turkey. PLoS Neglected Tropical Diseases, 8 (8): e3067. doi: 10.1371/journal.pntd.0003067
• Orkun, Ö., Karaer, Z., Çakmak, A. and Nalbantoǧlu, S. 2014. Spotted fever group rickettsiae in ticks in Turkey. Ticks and Tick-Borne Diseases, 5 (2): 213-218. doi: 10.1016/j.ttbdis.2012.11.018
• Orkun, Ö. and Vatansever, Z. 2021. Rediscovery and first genetic description of some poorly known tick species: Haemaphysalis kopetdaghica Kerbabaev, 1962 and Dermacentor raskemensis Pomerantzev, 1946. Ticks and Tick-Borne Diseases, 12 (4): 101726. doi: 10.1016/j.ttbdis.2021.101726
• Ozubek, S., Bastos, R.G., Alzan, H.F., Inci, A., Aktas, M. and Suarez, C.E. 2020. Bovine babesiosis in Turkey: Impact, current gaps, and opportunities for intervention. Pathogens, 9 (12): 1041. doi: 10.3390/pathogens9121041
• Scholtens, R.G., Braff, E.H., Healy, G.R. and Gleason, N. 1968. A case of Babesiosis in man in the United States. The American Journal of Tropical Medicine and Hygiene, 17 (6): 810-813. doi: 10.4269/ajtmh.1968.17.810
• Skrabalo, Z. and Deanovic, Z. 1957. Piroplasmosis in man; report of a case. Documenta de Medicina Geographica et Tropica, 9 (1): 11-16.
• Smith, T. and Kilborne, F.L. 1893. Investigations into the nature, causation, and prevention of Texas or southern cattle fever (Issue 1). Government Printing Office, Washington, USA, 301 pp. doi: 10.5962/bhl.title.124068
• Usluca, S., Celebi, B., Karasartova, D., Gureser, A.S., Matur, F., Oktem, M.A., Sozen, M., Karatas, A., Babur, C., Mumcuoglu, K.Y. et al. 2019. Molecular survey of Babesia microti (Aconoidasida: Piroplasmida) in wild rodents in Turkey. Journal of Medical Entomology, 56 (6): 1605-1609. doi: 10.1093/jme/tjz084
• Vannier, E. and Krause, P.J. 2012. Human babesiosis. New England Journal of Medicine, 366 (25): 2397-2407. doi: 10.1056/NEJMra1202018
• Venter, A., Vorster, I., Nkosi, N.F., Sibeko-Matjila, K.P. and Bhoora, R.V. 2024. Molecular genotyping of Babesia caballi. Veterinary Parasitology, 329: 110214. doi: 10.1016/j.vetpar.2024.110214
• Wise, L.N., Pelzel-McCluskey, A.M., Mealey, R.H. and Knowles, D.P. 2014. Equine piroplasmosis. Veterinary Clinics of North America: Equine Practice, 30 (3): 677-693. doi: 10.1016/j.cveq.2014.08.008
• Yang, Y., Christie, J., Köster, L., Du, A. and Yao, C. 2021. Emerging human babesiosis with “Ground Zero” in North America. Microorganisms, 9 (2): 440. doi: 10.3390/microorganisms9020440