Skip to main content
SpringerLink
Log in

Prevalence of Theileria/Babesia Species in Ruminants in Burdur Province of Turkey

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

Theileriosis and babesiosis, two tick-borne haemoparasitic diseases (TBHDs) of ruminants, are caused by protozoan parasites of the genus Theileria and Babesia, respectively. Among them, some species are considered to be highly pathogenic causing serious economic losses to livestock holders especially in tropic and subtropic regions. Local and/or general control measures are needed to be applied to reduce economic impact of TBHDs. Prevalence studies are essential for the implementation and/or design of effective prevention and control measures based on true epidemiological data. Therefore, this study aimed to investigate the presence, prevalence and possible cross infections of Theileria/Babesia species between sheep, goat and cattle herds in Burdur province in Turkey.

Methods

A total of 964 blood samples were collected from sheep (n = 330), goat (n = 300) and cattle (n = 334) from five different districts of Burdur province. The samples were investigated for ovine and bovine Theileria/Babesia species using reverse line blot (RLB) hybridization assay.

Results

In small ruminants, T. ovis was the most abundant Theileria species detected in sheep with a rate of 79.69%. Among Babesia species, B. ovis and B. crassa were detected only in blood of goats (0.66%) and sheep (1.12%) as single and mixed infections, respectively. In cattle, T. annulata, B. bovis, Babesia spp. were detected in rates of 0.59%, 3.29%, 3.59%, respectively.

Conclusion

Obtained results clearly indicated that no cross infections with Theileria/Babesia species occurred in small ruminant and cattle herds that use the same grazing area.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Preston PM (2001) Theileriosis. In: Service MW (ed) The encyclopedia of arthropod-transmitted infections of man and domesticated animals. CABI Publishing, Wallingford, Oxon, UK; New York,USA, pp 487–502

    Google Scholar 

  2. Uilenberg G (2001) Babesiosis. In: Service MW (ed) The encyclopedia of arthropod-transmitted infections of man and domesticated animals. CABI Publishing, Wallingford, Oxon, UK; New York,USA, pp 53–60

    Google Scholar 

  3. Uilenberg G (2006) Babesia. A historical overview. Vet Parasitol 138(1–2):3–10. https://doi.org/10.1016/j.vetpar.2006.01.035

    Article  PubMed  Google Scholar 

  4. Mehlhorn H (2008) Babesiosis, Animals. Encyclopedia of parasitiology, vol 1, 3rd edn. Springer-Verlag, Berlin Heidelberg New York, pp 153–154

    Chapter  Google Scholar 

  5. Johnsson NN, Bock RE, Jorgensen WK (2008) Productivity and health effects of anaplasmosis and babesiosis on Bos indicus cattle and their crosses, and the effects of differing intensity of tick control in Australia. Vet Parasitol 155(1–2):1–9. https://doi.org/10.1016/j.vetpar.2008.03.022

    Article  Google Scholar 

  6. Gubbels JM, de Vos AP, van der Weide M, Viseras J, Schouls LM, de Vries E, Jongejan F (1999) Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J Clin Microbiol 37(6):1782–1789. https://doi.org/10.1128/JCM.37.6.1782-1789.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Zwart D (1985) Haemoparasitic diseases of bovines. Rev Sci Tech 4(3):447–458. https://doi.org/10.20506/rst.4.3.208 (PMID: 32736453)

    Article  CAS  PubMed  Google Scholar 

  8. Bai Q, Liu GY, Yin H, Qizu Z, Dekao L, Jiaxin R, Xin L (2002) Theileria sinensis sp nov: a new species of Bovine Theileria-classical taxonomic studies. Acta Veterinaria et Zootechnica Sinica 33:73–77

    Google Scholar 

  9. Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA (2012) Babesia: a world emerging. Infect Genet Evol 12(8):1788–1809. https://doi.org/10.1016/j.meegid.2012.07.004

    Article  PubMed  Google Scholar 

  10. Ray HN, Raghavachari K (1941) Observations on Babesia foliata n. sp. from a sheep. IJVSBT 11:239–242

    Google Scholar 

  11. Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ahmed JS (2004) Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting. Parasitol Res 92(3):189–196. https://doi.org/10.1007/s00436-003-0980-9

    Article  PubMed  Google Scholar 

  12. Yin H, Schnittger L, Luo J, Seitzer U, Ahmed JS (2007) Ovine theileriosis in China: a new look at an old story. Parasitol Res 101(2):191–195. https://doi.org/10.1007/s00436-007-0689-2

    Article  Google Scholar 

  13. Altay K, Aktas M, Dumanli N, Aydin MF (2008) Evaluation of a PCR and comparison with RLB for detection and differentiation of Theileria sp. MK and other Theileria and Babesia species of small ruminants. Parasitol Res 103(2):319–323. https://doi.org/10.1007/s00436-008-0973-9

    Article  PubMed  Google Scholar 

  14. Guan GQ, Ma ML, Moreau E, Liu J, Lu B, Bai Q, Luo J, Jorgensen W, Chauvin A, Yin H (2009) A new ovine Babesia species transmitted by Hyalomma anatolicum anatolicum. Exp Parasitol 122(4):261–267. https://doi.org/10.1016/j.exppara.2009.05.001

    Article  PubMed  Google Scholar 

  15. Aktas M, 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. J Med Entomol 52(6):1344–1350. https://doi.org/10.1093/jme/tjv126

    Article  CAS  PubMed  Google Scholar 

  16. Elsify A, Sivakumar T, Nayel M, Salama A, Elkhtam A, Rizk M, Mosaab O, Sultan K, Elsayed S, Igarashi I, Yokoyama N (2015) An epidemiological survey of bovine Babesia and Theileria parasites in cattle, buffaloes, and sheep in Egypt. Parasitol Int 64(1):79–85. https://doi.org/10.1016/j.parint.2014.10.002

    Article  PubMed  Google Scholar 

  17. Altay K, Atas AD, Ozkan E (2017) Molecular survey of Theileria and Babesia species in small ruminants and ticks from Sivas Region of Turkey. Manas J Agr Vet Life Sci 7(1):30–39

    Google Scholar 

  18. Criado-Fornelio A, Martinez-Marcos A, Buling-Saraña A, Barba-Carretero JC (2003) Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part I Epizootiological aspects. Vet Parasitol 13:189–201. https://doi.org/10.1016/s0304-4017(03)00078-5

    Article  Google Scholar 

  19. Criado-Fornelio A, Martinez-Marcos A, Buling-Saraña A, Barba-Carretero JC (2003) Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part II. Phylogenetic analysis and evolutionary history. Veterinary Parasitol 114:173–194. https://doi.org/10.1016/s0304-4017(03)00141-9

    Article  CAS  Google Scholar 

  20. Sivakumar T, Lan DT, Long PT, Yoshinari T, Tattiyapong M, Guswanto A, Okubo K, Igarashi I, Inoue N, Xuan X, Yokoyama N (2013) PCR detection and genetic diversity of bovine hemoprotozoan parasites in Vietnam. J Vet Med Sci 75:1455–1462. https://doi.org/10.1292/jvms.13-0221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gholami S, Laktarashi B, Shiadeh MM, Spotin A (2016) Genetic variability, phylogenetic evaluation and first global report of Theileria luwenshuni, T. buffeli, and T. ovis in sheepdogs in Iran. Parasitol Res 115(5):2125–2130. https://doi.org/10.1007/s00436-016-5005-6

    Article  PubMed  Google Scholar 

  22. Neitz WO (1957) Theileriosis, gonderioses and cyauxzoonoses: a review 2 Theileria annulata infection. Onderstepoort J Vet Res 27(3):319–346

    Google Scholar 

  23. Callow LL (1984) Protozoan and rickettsial diseases. Australian Bureau of animal health, animal health in Australia, vol 5. Australian Government Publishing Service, Canberra, pp 121–216

    Google Scholar 

  24. Bilgic HB, Karagenc T, Shiels B, Tait A, Eren H, Weir W (2010) Evaluation of cytochrome b as a sensitive target for PCR-based detection of T. annulata carrier animals. Vet Parasitol 174(3–4):341–347. https://doi.org/10.1016/j.vetpar.2010.08.025

    Article  CAS  PubMed  Google Scholar 

  25. Ndao M (2009) Diagnosis of parasitic diseases: old and new approaches (review article). Interdiscip Perspect Infect Dis. https://doi.org/10.1155/2009/278246

    Article  PubMed  PubMed Central  Google Scholar 

  26. Mans BJ, Pienaar R, Latif AA (2015) A review of Theileria diagnostics and epidemiology. Int J Parasitol Parasites Wildl 4(1):104–118. https://doi.org/10.1016/j.ijppaw.2014.12.006

    Article  PubMed  PubMed Central  Google Scholar 

  27. Niu Q, Luo J, Guan G, Ma M, Liu Z, Liu A, Dang Z, Gao J, Ren Q, Li Y, Liu J, Yin H (2009) Detection and differentiation of ovine Theileria and Babesia by reverse line blotting in China. Parasitol Res 104(6):1417–1423. https://doi.org/10.1007/s00436-009-1344-x

    Article  PubMed  Google Scholar 

  28. Inci A, Ica A, Yildirim A, Duzlu O (2010) Identification of Babesia and Theileria species in small ruminants in Central Anatolia (Turkey) via reverse line blotting. Turk J Vet Anim Sci 34(2):205–210. https://doi.org/10.3906/vet-0902-15

    Article  CAS  Google Scholar 

  29. Bilgic HB, Bakirci S, Kose O, Unlu AH, Hacilarlioglu S, Eren H, Weir W, Karagenc T (2017) Prevalence of tick-borne haemoparasites in small ruminants in Turkey and diagnostic sensitivity of single-PCR and RLB. Parasit Vectors 10(1):211. https://doi.org/10.1186/s13071-017-2151-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Altay K, Atas AD, Ograk YZ, Ozkan E (2020) Survey of Theileria, Babesia and Anaplasma infections of cattle and ticks from Sivas province of Turkey. Erciyes Üniv Vet Fak Derg 17(1):32–38

    Google Scholar 

  31. Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ (2012) Current advances in detection and treatment of babesiosis. Curr Med Chem 19(10):1504–1518. https://doi.org/10.2174/092986712799828355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Nagore D, Garcia-Sanmartin J, Garcia-Perez AL, Juste RA, Hurtado A (2004) Identification, genetic diversity and prevalence of Theileria and Babesia species in a sheep population from Northern Spain. Int J Parasitol 34(9):1059–1067. https://doi.org/10.1016/j.ijpara.2004.05.008

    Article  CAS  PubMed  Google Scholar 

  33. Altay K, Dumanli N, Aktas M (2012) A study on ovine tick-borne hemoprotozoan parasites (Theileria and Babesia) in the East Black Sea Region of Turkey. Parasitol Res 111(1):149–153. https://doi.org/10.1007/s00436-011-2811-8

    Article  PubMed  Google Scholar 

  34. Karatepe B, Ozubek S, Karatepe M, Aktas M (2019) Detection of Theileria and Babesia species in sheep and goats by microscopy and molecular methods in Niğde province, Turkey. Rev Med Vet 170(7–9):136–143

    CAS  Google Scholar 

  35. Sarayli H, Inci A, Ica A, Yildirim A, Duzlu O (2006) Investigation of the Babesia agents in sheep and goats by the reverse line blotting hybridization method around Yeşilhisar. Erciyes Univ J Health Sci 15(3):181–188

    Google Scholar 

  36. Altay K, Dumanli N, Aktas M (2007) Molecular identification, genetic diversity and distribution of Theileria and Babesia species infecting small ruminants. Vet Parasitol 147(1–2):161–165. https://doi.org/10.1016/j.vetpar.2007.04.001

    Article  CAS  PubMed  Google Scholar 

  37. Ica A, Inci A, Yildirim A (2007) Parasitological and molecular prevalence of bovine Theileria and Babesia species in the vicinity of Kayseri. Turk J Vet Anim Sci 31(1):33–38

    Google Scholar 

  38. Altay K, Aktas M, Dumanli N (2007) Survey of T. annulata and T. buffeli/orientalis in cattle in the region of Erzincan Using reverse line blotting. Turkiye Parazitol Derg 31(2):94–97

    PubMed  Google Scholar 

  39. Altay K, Aydin MF, Dumanli N, Aktas M (2008) Molecular detection of Theileria and Babesia infections in cattle. Vet Parasitol 158:295–301. https://doi.org/10.1016/j.vetpar.2008.09.025b

    Article  CAS  PubMed  Google Scholar 

  40. Yukari BA, Umur S (2002) The prevalence of tick species (Ixodoidea) in cattle, sheep and goats in the Burdur Region, Turkey. Turk J Vet Anim Sci 26(6):1263–1270

    Google Scholar 

  41. Ozubek S, Bastos RG, Alzan HF, Inci A, Aktas M, Suarez CE (2020) Bovine Babesiosis in Turkey: impact, current gaps, and opportunities for intervention. Pathogens 9(12):1041. https://doi.org/10.3390/pathogens9121041

    Article  CAS  PubMed Central  Google Scholar 

  42. Georges K, Loria GR, Riili S, Greco A, Caracappa S, Jongejan F, Sparagano O (2001) Detection of haemoparasites in cattle by reverse line blot hybridisation with a note on the distribution of ticks in Sicily. Vet Parasitol 99(4):273–286. https://doi.org/10.1016/S0304-4017(01)00488-5

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The present study is an extension of a PhD thesis and was presented at 20. National Parasitology Congress, 25–29 September 2017, Osman Gazi University, Eskisehir, TURKEY by the PhD student; Onur KOSE.

Funding

The present study was financially supported by Aydın Adnan Menderes University, Scientific Research Projects Unit (Project no: VTF-15038).

Author information

Authors and Affiliations

  1. Department of Parasitology, Faculty of Veterinary Medicine, Burdur Mehmet Akif Ersoy University, 15030, Burdur, Turkey

    Onur Kose, Ramazan Adanir & Bayram Ali Yukari

  2. Department of Parasitology, Faculty of Veterinary Medicine, Aydin Adnan Menderes University, Aydin, Turkey

    Huseyin Bilgin Bilgic, Serkan Bakirci, Tulin Karagenc & Hasan Eren

Authors
  1. Onur Kose
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huseyin Bilgin Bilgic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Serkan Bakirci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tulin Karagenc
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ramazan Adanir
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bayram Ali Yukari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hasan Eren
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

OK, TK, BAY and HE participated in the design of study. OK and RA conducted sample collection. OK, HBB and SB participated in molecular analysis of collected samples and statistical analysis of results. OK wrote the article and drafted the final manuscript. OK, HBB and TK participated in the critical reading and revision of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Onur Kose.

Ethics declarations

Conflict of Interest

The authors declare there are no conflicts of interest.

Ethical Approval

The present study was approved by Adnan Menderes University Animal Experiments Local Ethics Committee (Date: 12.11.2014, Number: 64583101/2014/183).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

11686_2021_515_MOESM1_ESM.jpg

RLB reaction of the various positive controls and examined samples-1. Reverse line blot (RLB) hybridization signals of PCR products generated by amplification of genomic DNA of infected field samples and various positive controls. Oligonucleotide probes were loaded in columns, PCR products in rows. Various positive controls and detected samples infected with single or mixed Theileria and/or Babesia species as follows: lane 1, 10 and 25 are mixed positive controls for T. annulata, T. ovis, T. lestoquardi, and B. crassa., 11, 13, 16, 23, 24, 27, 28, 29, 31, 33 are samples infected with T. ovis + Babesia spp., 26 is sample infected with T. ovis + BcI (B. crassa Iran) (JPG 776 KB)

11686_2021_515_MOESM2_ESM.jpg

RLB reaction of the various positive controls and examined samples-2 Reverse line blot (RLB) hybridization signals of PCR products generated by amplification of genomic DNA of infected field samples and various positive controls. Oligonucleotide probes were loaded in columns, PCR products in rows. Various positive controls and detected samples infected with single or mixed Theileria and/or Babesia species as follows: lane 10, 20 and 35 are mixed positive controls for T. annulata, T. buffeli, T. hirci, T. ovis, T. lestoquardi, T. sp. OT1, T. sp. MK, B. ovis, BcG (B. crassa group), 1–5, 9, 11, 13–19, 21–34, 36–39 are samples infected with T. ovis + Babesia spp (JPG 870 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kose, O., Bilgic, H.B., Bakirci, S. et al. Prevalence of Theileria/Babesia Species in Ruminants in Burdur Province of Turkey. Acta Parasit. 67, 723–731 (2022). https://doi.org/10.1007/s11686-021-00515-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-021-00515-z

Keywords

Search

Navigation