Skip to main content
Log in

Molecular identification of Theileria and Babesia in sheep and goats in the Black Sea Region in Turkey

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

This study was carried out to investigate presence and distribution of Theileria and Babesia species via microscopic examination and reverse line blotting (RLB) techniques in sheep and goats in the Black Sea region of Turkey. For this purpose, 1,128 blood samples (869 sheep and 259 goats) were collected by active surveillance from sheep and goats in different provinces of various cities in the region in the years 2010 and 2011. Smears were prepared from the blood samples, stained with Giemsa, and examined under the light microscope for Theileria and Babesia piroplasms. The genomic DNAs were extracted from blood samples. The length of 360–430-bp fragment in the variable V4 region of 18S SSU rRNA gene of Theileria and Babesia species was amplified using the gDNAs. The polymerase chain reaction products were hybridized to the membrane-connected species-specific probes. A total of 38 animals (3.37 %) including 34 sheep (3.91 %) and 4 goats (1.54 %) were found to be positive for Theileria spp. piroplasms in microscopic examination of smears while Babesia spp. piroplasm could not detected. Infection rates were 34.64 % in sheep, 10.04 % in goats, and totally 28.99 % for Theileria ovis while 0.58 % in sheep and totally 0.44 % for Babesia ovis. However, Theileria sp. OT3 was detected in 2.65 % of sheep and 2.04 % of all animals; besides Theileria sp., MK had 0.58 % prevalence in sheep and 0.77 % in goats, with a total 0.62 % with RLB. Although T. ovis and Theileria sp. MK were determined in both sheep and goats, B. ovis and Theileria sp. OT3 were observed only in the sheep. These results provide the first detailed molecular data for sheep and goat theileriosis and babesiosis in the region.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmed JS, Luo J, Schnittger L, Seitzer U, Jongejan F, Yin H (2006) Phylogenetic position of small ruminant infecting piroplasms. Ann NY Acad Sci 1081:498–504

    Article  PubMed  CAS  Google Scholar 

  • Aktas M, Altay K, Dumanli N (2005a) Survey of Theileria parasites of sheep in eastern Turkey using polymerase chain reaction. Small Rum Res 60:289–293

    Article  Google Scholar 

  • Aktas M, Altay K, Dumanli N (2005b) Development of a polymerase chain reaction method for diagnosis of Babesia ovis infection in sheep and goats. Vet Parasitol 133:277–281

    Article  PubMed  CAS  Google Scholar 

  • Aktas M, Altay K, Dumanli N (2007) Determination of prevalence and risk factors for infection with Babesia ovis in small ruminants from Turkey by polymerase chain reaction. Parasitol Res 100(4):797–802

    Article  PubMed  Google Scholar 

  • Alani AJ, Herbert IV (1988) The morphometrics of Babesia motasi (Wales) and its transmission by Haemaphysalis punctata (Canestrni and Fanzago, 1877) to sheep. Vet Parasitol 30:87–95

    Article  PubMed  CAS  Google Scholar 

  • Altay K, Aktas M, Dumanli N (2007a) Theileria infections in small ruminants in the east and southeast Anatolia. Turkiye Parazitol Derg 31(4):268–271

    PubMed  Google Scholar 

  • Altay K, Dumanli N, Aktas M (2007b) Molecular identification, genetic diversity and distribution of Theileria and Babesia species infecting small ruminants. Vet Parasitol 147:161–165

    Article  PubMed  CAS  Google Scholar 

  • Altay K, Aktas M, Dumanli N, Aydin MF (2008a) 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

    Article  PubMed  Google Scholar 

  • Altay K, Aydin MF, Dumanli N, Aktas M (2008b) Molecular detection of Theileria and Babesia infections in cattle. Vet Parasitol 158:295–301

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Anonymous (2011) Livestock statistics data base. Turkey Statistical Institute Web. http://www.tuik.gov.tr/hayvancilikapp/hayvancilik.zul 2008. Accessed 10 December 2011

  • Brown CG (1990) Control of tropical theileriosis (Theileria annulata infection) of cattle. Parassitologia 32(1):23–31

    Google Scholar 

  • Burridge MJ, Brown CG, Kimber CD (1974) Theileria annulata: cross-reactions between a cell culture schizont antigen and antigens of East African species in the indirect fluorescent antibody test. Exp Parasitol 35(3):374–380

    Google Scholar 

  • Friedhoff KT (1997) Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parassitologia 39:99–109

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Guan GQ, Ma ML, Moreau E, Liu JL, Lu BY, Bai Q (2009) A new ovine Babesia species transmitted by Hyalomma anatolicum anatolicum. Exp Parasitol 122:261–267

    Article  PubMed  Google Scholar 

  • Guan G, Moreau E, Liu J, Hao X, Ma M, Luo J, Chauvin A, Yin H (2010) Babesia sp. BQ1 (Lintan): molecular evidence of experimental transmission to sheep by Haemaphysalis qinghaiensis and Haemaphysalis longicornis. Parasitol Int 59(2):265–267

    Article  PubMed  CAS  Google Scholar 

  • 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 37:1782–1789

    PubMed  CAS  Google Scholar 

  • Guo S, Yuan Z, Wu G, Wang W, Ma D, Du H (2002) Epidemiology of ovine theileriosis in Ganan region, Gansu Province, China. Parasitol Res 88:36–37

    Google Scholar 

  • Hashemi-Fesharki R, Uilenburg G (1981) Babesia crassa n. sp. (Sporozoa, Babesiidae) of domestic sheep in Iran. Vet Quart 2:3–14

    Google Scholar 

  • Heidarpour Bami M, Haddadzadeh HR, Kazemi B, Khazraiinia P, Bandehpour M, Aktas M (2009) Molecular identification of ovine Theileria species by a new PCR-RFLP method. Vet Parasitol 161(3–4):171–177

    Article  PubMed  CAS  Google Scholar 

  • Hoosmand- Rad P, Hawa NY (1973) Malignant theileriosis of sheep and goats. Trop Anim Health Pro 5:97–102

    Article  Google Scholar 

  • Iça A, Yıldırım A, Inci A (2005) Investigation of blood protozoa in sheep by reverse line blotting method in Kayseri province. XIV National Congress of Parasitology, Dokuz Eylul University, İzmir p: 161

  • İnci A, Yukarı BA, Sayın F (1998) Study on babesiosis and theileriosis agents detected in some sheep and goat flocks using microscopic examination in Çankırı region. Ankara Üniv Vet Fak Derg 45:105–113

    Google Scholar 

  • İnci A, Karaer Z, İca A (2002) Babesiosis in sheep and goats around Kayseri. FÜ Sag Bil Derg 16(1):79–83

    Google Scholar 

  • İnci A, İca A, Yıldırım A, Düzlü Ö (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

    Google Scholar 

  • Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129(Suppl):3–14

    Google Scholar 

  • Levine ND (1985) Veterinary protozoology. Iowa State University Press, Ames, Iowa

    Google Scholar 

  • Liu AH, Yin H, Guan GQ, Schnittger L, Liu ZJ, Ma ML, Dang ZS, Liu JL, Ren QY, Bai Q, Ahmed JS, Luo JX (2007) At least two genetically distinct large Babesia species infective to sheep and goats in China. Vet Parasitol 147:246–251

    Article  PubMed  CAS  Google Scholar 

  • Luo J, Yin H (1997) Theileriosis of sheep and goats in China. Trop Anim Health Prod 29(4):8–10

    Article  Google Scholar 

  • Nagore D, García-Sanmartín J, García-Pérez 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 34:1059–1067

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ray HN, Raghavachari K (1941) Observations on Babesia foliata n. sp. from a sheep. Indian J Vet Sci 11:239–242

    Google Scholar 

  • Rijpkema SG, Molkenboer MJ, Schouls LM, Jongejan F, Schellekens JF (1995) 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 33:3091–3095

    Google Scholar 

  • 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 Sag Bil Derg 15(3):181–188

    Google Scholar 

  • Sarwar SM (1935) A hitherto undescribed piroplasm of goats (Piroplasma taylori). Indian Jour Vet Sci and Anim Husb 5:171–176

    Google Scholar 

  • Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ahmed JS (2004) Simultaneously detection and differentiation of Theileria and Babesia parasite infecting small ruminants by reverse line blotting. Parasitol Res 92:189–196

    Article  PubMed  Google Scholar 

  • Sevinc F, Dik B (1996) The diagnosis of Babesia ovis in sheep in Konya around by ELISA. Veteriner Bilim Derg 12(2):73–79

    Google Scholar 

  • Uilengberg G, Rombach MC, Perie NM, Zwart D (1980) Blood parasites of sheep in The Netherlands. II. Babesia motasi (Sporozoa, Babesiidae). Vet Quart 2:3–14

    Article  Google Scholar 

  • Yin H, Liu G, Luo J, Guan G, Ma M, Ahmed J, Bai Q (2003) Observation on the schizont stage of an unidentified Theileria sp. in experimentally infected sheep. Parasitol Res 91(1):34–39

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Yin H, Liu Z, Guan G, Liu A, Ma M, Ren Q, Luo J (2008) Detection and differentiation of Theileria luwenshuni and T. uilenbergi infection in small ruminants by PCR. Transbound Emerg Dis 55(5–6):233–237

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Yasin Baykalır, Sezayi Özübek, Çağrı Özçetin, and all veterinarians and technicians also animal breeders in the region for their kind help during sample collection. This study was financially supported by the Scientific and Technical Research Council of Turkey (TUBITAK) with a grant (TOVAG 109 O 766).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mehmet Fatih Aydin.

Additional information

Nucleotide sequence data reported in this paper are available in GenBank, EMBL 21, and DDBJ databases under accession numbers from JQ867384 to JQ867387.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aydin, M.F., Aktas, M. & Dumanli, N. Molecular identification of Theileria and Babesia in sheep and goats in the Black Sea Region in Turkey. Parasitol Res 112, 2817–2824 (2013). https://doi.org/10.1007/s00436-013-3452-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3452-x

Keywords

Navigation