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Molecular identification of Theileria and Babesia in ticks collected from sheep and goats in the Black Sea region of Turkey

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Abstract

A molecular survey was undertaken in the Black Sea region of Turkey to determine the presence of Theileria and Babesia species of medical and veterinary importance. The ticks were removed from sheep and goats, pooled according to species and locations, and analyzed by PCR-based reverse line blot (RLB) and sequencing. A total of 2241 ixodid ticks belonging to 5 genus and 12 species were collected and divided into 310 pools. Infection rates were calculated as the maximum likelihood estimation (MLE) with 95 % confidence intervals (CI). Of the 310 pools tested, 46 (14.83 %) were found to be infected with Theileria or Babesia species, and the overall MLE of the infection rate was calculated as 2.27 % (CI 1.67–2.99). The MLE of the infection rates were calculated as 0.691 % (CI 0.171–1.78) in Haemaphysalis parva, 1.47 % (CI 0.081–6.37) in Rhipicephalus sanguineus, 1.84 % (CI 0.101–7.87) in Ixodes ricinus, 2.86 % (CI 1.68–4.48) in Rhipicephalus turanicus, 5.57 % (CI 0.941–16.3) in Hyalomma marginatum, and 6.2 % (CI 4.02–9.02) in Rhipicephalus bursa. Pathogens identified in ticks included Theileria ovis, Babesia ovis, Babesia bigemina, and Babesia microti. Most tick pools were infected with a single pathogen. However, five pools displayed mixed infections with T. ovis and B. ovis. This study provides the first molecular evidence for the presence of B. microti in ticks in Turkey.

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References

  • Aktas M (2014) A survey of ixodid tick species and molecular identification of tick-borne pathogens. Vet Parasitol 200(3–4):276–283

    Article  CAS  PubMed  Google Scholar 

  • Aktas M, Dumanli N, Angin M (2004) Cattle infestation by Hyalomma ticks and prevalence of Theileria in Hyalomma species in the east of Turkey. Vet Parasitol 119:1–8

    Article  CAS  PubMed  Google Scholar 

  • Aktas M, Altay K, Dumanli N (2006) PCR-based detection of Theileria ovis in Rhipicephalus bursa adult ticks. Vet Parasitol 140:259–263

    Article  CAS  PubMed  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 100:797–802

    Article  PubMed  Google Scholar 

  • Aktas M, Altay K, Dumanli N, Kalkan A (2009) Molecular detection and identification of Ehrlichia and Anaplasma species in ixodid ticks. Parasitol Res 104(5):1243–1248

    Article  PubMed  Google Scholar 

  • Aktas M, Vatansever Z, Altay K, Aydin MF, Dumanli N (2010) Molecular evidence for Anaplasma phagocytophilum in Ixodes ricinus from Turkey. Trans R Soc Trop Med Hyg 104:10–15

    Article  CAS  PubMed  Google Scholar 

  • Aktas M, Altay K, Ozubek S, Dumanli N (2012) A survey of ixodid ticks feeding on cattle and prevalence of tick-borne pathogens in the Black Sea region of Turkey. Vet Parasitol 187(3–4):567–571

    Article  PubMed  Google Scholar 

  • Aktas M, Ozübek S, Ipek DN (2013) Molecular investigations of Hepatozoon species in dogs and developmental stages of Rhipicephalus sanguineus. Parasitol Res 112:2381–2385

    Article  PubMed  Google Scholar 

  • Altay K, Aktas M, Dumanli N (2008a) Detection of Babesia ovis by PCR in Rhipicephalus bursa collected from naturally infested sheep and goats. Res Vet Sci 85(1):116–119

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Altay K, Aktas M, Dumanli N, Aydin MF (2008c) 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 103:319–323

    Article  PubMed  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 

  • Aydin MF, Aktas M, Dumanli N (2012) Tick infestations on sheep and goats in the Black Sea region. Kafkas Univ Vet Fak Derg 18(Suppl-A):A17–A22

    Google Scholar 

  • Aydin MF, Aktas M, Dumanli N (2013) Molecular identification of Theileria and Babesia in sheep and goats in the Black Sea region in Turkey. Parasitol Res 112(8):2817–2824

    Article  PubMed  Google Scholar 

  • Berggoetz M, Schmid M, Ston D, Wyss V, Chevillon C, Pretorius AM, Gern L (2014) Protozoan and bacterial pathogens in tick salivary glands in wild and domestic animal environments in South Africa. Ticks Tick Borne Dis 5(2):176–185

    Article  CAS  PubMed  Google Scholar 

  • Çiçek H, Karatepe M, Çakır M, Eser M (2009) Blood parasites detected from Anatolian squirrel, Spermophilus xanthophrymnus (Rodentia: Sciuridae) in Nigde province, Turkey. Ankara Univ Vet Fak Derg 56:147–148

    Google Scholar 

  • de La Fuente J, Estrada-Peña A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946

    Article  PubMed  Google Scholar 

  • de Vos AJ, Potgieter FT (1994) Bovine babesiosis. In: Coetzer JAW, Thomson GR, Tustin RC (eds) Infectious diseases of livestock, 2nd edn. Oxford University Press, Cape Town, pp 277–294

    Google Scholar 

  • Ekici OD, Sevinc F, Isik N (2012) Instability of ovine babesiosis in an endemic area in Turkey. Vet Parasitol 188(3–4):372–375

    Article  PubMed  Google Scholar 

  • Foppa IM, Krause PJ, Spielman A, Goethert H, Gern L, Brand B, Telford SR 3rd (2002) Entomologic and serologic evidence of zoonotic transmission of Babesia microti, Eastern Switzerland. Emerg Infect Dis 8(7):722–726

    Article  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Gachohi JM, Ngumi PN, Kitala PM, Skilton RA (2010) Estimating seroprevalence and variation to four tick-borne infections and determination of associated risk factors in cattle under traditional mixed farming system in Mbeere District, Kenya. Prev Vet Med 95(3–4):208–223

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Gray J, von Stedingk LV, Gürtelschmid M, Granström M (2002) Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. J Clin Microbiol 40(4):1259–1263

    Article  PubMed Central  PubMed  Google Scholar 

  • Gu W, Lampman R, Novak RJ (2003) Problems in estimating mosquito infection rates using MIR. J Med Entomol 40:595–596

    Article  PubMed  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 

  • 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  CAS  PubMed  Google Scholar 

  • Hunfeld KP, Lambert A, Kampen H, Albert S, Epe C, Brade V, Tenter AM (2002) Seroprevalence of Babesia infections in humans exposed to ticks in midwestern Germany. J Clin Microbiol 40(7):2431–2436

    Article  PubMed Central  PubMed  Google Scholar 

  • Ica A, Vatansever Z, Yildirim A, Duzlu O, Inci A (2007) Detection of Theileria and Babesia species in ticks collected from cattle. Vet Parasitol 148:156–160

    Article  CAS  PubMed  Google Scholar 

  • Iqbal F, Fatima M, Shahnawaz S, Naeem M, Shaikh R, Ali M, Shaikh A, Aktas M, Ali M (2011) A study on the determination of risk factors associated with babesiosis and prevalence of Babesia sp., by PCR amplification, in small ruminants from Southern Punjab (Pakistan). Parasite 18(3):229–234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Ozdarendeli A, Aydin K, Tonbak S, Aktas M, Altay K, Koksal I, Bolat Y, Dumanli N, Kalkan A (2008) Genetic analysis of the M segment of Crimean-Congo hemorrhagic fever virus strain in Turkey. Arch Virol 153(1):37–44

    Article  CAS  PubMed  Google Scholar 

  • Ozdarendeli A, Canakoglu N, Berber E, Aydın K, Tonbak S, Ertek M, Buzgan T, Bolat Y, Aktas M, Kalkan A (2010) The complete genome analysis of Crimean-Congo hemorrhagic fever virus isolated in Turkey. Virus Res 147:288–293

    Article  PubMed  Google Scholar 

  • Parviz S, Hooshmand E, Rahbari S, Nabian S (2008) Determination of Rhipicephalus spp. as vectors for Babesia ovis in Iran. Parasitol Res 101:1029–1033

    Google Scholar 

  • Poyraz O, Güneş T (2010) Seroprevalence of Babesia microti in humans living in rural areas of the Sinop region. Türk Parazitol Derg 34(2):81–85

    Google Scholar 

  • Ravindran R, Rao JR, Mishra AK (2006) Detection of Babesia bigemina DNA in ticks by DNA hybridization using a nonradioactive probe generated by arbitrary PCR. Vet Parasitol 141:181–185

    Article  CAS  PubMed  Google Scholar 

  • Razmi G, Yaghfoori S (2013) Molecular surveillance of Theileria ovis, Theileria lestoquardi and Theileria annulata infection in sheep and ixodid ticks in Iran. Onderstepoort J Vet 80(1):635

    Article  Google Scholar 

  • Tavassoli M, Tabatabaei M, Mohammadi M, Esmaeilnejad B, Mohamadpour H (2013) PCR-based detection of Babesia spp. infection in collected ticks from cattle in west and north-west of Iran. J Arthropod Borne Dis 7(2):132–138

    PubMed Central  PubMed  Google Scholar 

  • Tonbak S, Aktas M, Altay K, Azkur AK, Kalkan A, Bolat Y, Dumanli N, Ozdarendeli A (2006) Crimean-Congo hemorrhagic fever virus: genetic analysis and tick survey in Turkey. J Clin Microbiol 44(11):4120–4124

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uilenberg G (1995) International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Vet Parasitol 57(1–3):19–41

    Article  CAS  PubMed  Google Scholar 

  • Vannier E, Krause PJ (2012) Human babesiosis. N Engl J Med 366:2397–2407

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported financially by grants (109 O 766) from the Scientific and Technical Research Council of Turkey (TUBITAK) and (45-M-12) Commission of Scientific Research Projects, Karamanoğlu Mehmetbey University. We thank all veterinarians, technicians, and also animal breeders in the region for their kind help during sample collection. We are also grateful to Weidong Gu (Health Statistician, PhD, Centers for Disease Control and Prevention, Atlanta, GA, USA) for MLE-IR program used for estimating infection rates of pooled samples.

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Correspondence to Mehmet Fatih Aydin.

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Nucleotide sequence data reported in this paper are available in GenBank, EMBL 21, and DDBJ databases under accession numbers from KF737169 to KF737171.

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Aydin, M.F., Aktas, M. & Dumanli, N. Molecular identification of Theileria and Babesia in ticks collected from sheep and goats in the Black Sea region of Turkey. Parasitol Res 114, 65–69 (2015). https://doi.org/10.1007/s00436-014-4160-x

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