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Licensed Unlicensed Requires Authentication Published by De Gruyter December 28, 2016

Prevalence and molecular characterization of Theileria equi and Babesia caballi in jereed horses in Erzurum, Turkey

  • Esin Guven EMAIL logo , Hamza Avcioglu , Ahmet Deniz , İbrahim Balkaya , Ugur Abay , Şevki Yavuz and Muzaffer Akyüz
From the journal Acta Parasitologica

Abstract

Equine piroplasmosis (EP) is a hemoprotozoan tick-borne disease with worldwide distribution that is caused by Theileria equi and Babesia caballi. There are studies reporting the presence of equine piroplasmosis in Turkey but the situation in Erzurum is unknown. The aim of the current study was to determine the situation of equine piroplasmosis in jeered horses in Erzurum. Between April and August 2015, a total of 125 Arabian horse were examined and blood samples were collected. At the time of sampling, animals were also examined for tick infestations and clinical signs. Besides microscopic examination of Giemsastained blood smears, multiplex PCR performed with species specific primers partially amplifying the 18S rRNA gene of B. caballi and T. equi. During the microscopic examination of blood smears, T. equi piroplasms were found in 6 (4.8%) samples. In total, 11 (8.8%) T. equi DNA were detected with multiplex PCR. B. caballi piroplasms or DNA were not obtained. BLAST analysis of the sequenced T. equi samples (GenBank: KU921661-KU921667) indicated 98.8–100% identity to each other, and 100% similarity to T. equi isolates in South Africa, Iran, China, Sudan, India, Mongolia, Trinidad, Kenya, Spain, Serbia, Bosnia and Herzegovina and Turkey (Bursa). The results of our study indicate that T. equi occurs more frequently than B. caballi in the study area. To the authors’ knowledge, this is the first report of the molecular detection of equine piroplasmosis in jeered horses in Erzurum, Turkey.

  1. Conflict of interest statement:None of the authors of this paper has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper.

Acknowledgements

Thanks to all horse owners that made their horses available.

References

Abedi V., Razmi G., Seifi H., Naghibi A. 2014. Molecular and serological detection of Theileria equi and Babesia caballi infection in horses and ixodid ticks in Iran. Ticks and Tick-borne Diseases, 5, 239–244. 10.1016/j.ttbdis.2013.11.008Search in Google Scholar

Acici M., Umur S., Guvenc T., Arslan H.H., Kurt M. 2008. Seroprevalence of Equine babesiosis in the Black Sea region of Turkey. Parasitology Internatinal, 57, 198–200. 10.1016/ j.parint.2007.12.009Search in Google Scholar

Alhassan A., Pumidonming W., Okamura M., Hirata H., Battsetseg B., Fujisaki K., et al. 2005. Development of a single round and multiplex PCR method for the simultaneous detection of Babesia caballi and Babesia equi in horse blood. Veterinary Parasitology, 129, 43–49. 10.1016/j.vetpar.2004. 12.018Search in Google Scholar

Allsopp M.T., Allsopp B.A. 2006. Molecular sequence evidence for the reclassification of some Babesia species. Annals of the New York Academy of Sciences, 1081, 509–517. 10.1196/ annals.1373.076Search in Google Scholar

Asgarali Z., Coombs D.K., Mohammed F., Campbell M.D., Caesar E. 2007. A serological study of Babesia caballi and Theileria equi in thoroughbreds in Trinidad. Veterinary Parasitology, 144, 167–171. 10.1016/j.vetpar.2006.09.015Search in Google Scholar

Aydin L., Bakirci S. 2007. Geographical distribution of ticks in Turkey. Parasitology Research, 101, 163–166. 10.1007/ s00436-007-0694-5Search in Google Scholar

Bartolomé Del Pino L.E., Roberto N., Vincenzo V., Francesca I., Antonella C., Luca A.G., et al. 2016. Babesia caballi and Theileria equi infections in horses in Central-Southern Italy: Sero-molecular survey and associated risk factors. Ticks and Tick-borne Diseases, 7, 462–469. 10.1016/j.ttbdis.2016. 01.011Search in Google Scholar

Bashiruddin J.B., Cammá C., Rebêlo E. 1999. Molecular detection of Babesia equi and Babesia caballi in horse blood by PCR amplification of part of the 16s rRNA gene. Veterinary Parasitology, 84, 75–8310.1016/S0304-4017(99)00049-7Search in Google Scholar

Bhagwan J., Kumar A., Kumar R., Goyal L., Goel P., Kumar S. 2015. Molecular evidence of Theileria equi infection in Hyalomma anatolicum ticks infested on sero-positive Indian horses. Acta Parasitologica, 60, 322–329. 10.1515/ap-2015-0045Search in Google Scholar PubMed

Bhoora R., Quan M., Matjila P.T., Zweygarth E., Guthrie A.J., Collins N.E. 2010. Sequence heterogeneity in the equi merozoite anti-gen gene (ema-1) of Theileria equi and development of an ema-1-specific TaqMan MGBTM assay for the detection of T. equi. Veterinary Parasitology, 172, 33–45. 10.1016/ j.vetpar.2010.04.025Search in Google Scholar

Brüning A. 1996. Equine piroplasmosis an update on diagnosis, treatment and prevention. British Veterinary Journal, 152, 139–15110.1016/S0007-1935(96)80070-4Search in Google Scholar

Chauvin A., Moreau E., Bonnet S., Plantard O., Malandrin L. 2009. Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Veterinary Research, 40, 37. 10.1051/vetres/2009020Search in Google Scholar

Davitkov D., Vucicevic M., Stevanovic J., Krstic V., Slijepcevic D., Glavinic U., Stanimirovic Z. 2016. Molecular detection and prevalence of Theileria equi and Babesia caballi in horses of central Balkan. Acta Parasitologica, 61, 337–342. 10.1515/ap-2016-0044Search in Google Scholar

Deniz A., Karaer Z., Çakmak A., Pişkin Ç., Balkaya İ., Vatansever Z., Nalbantoğlu S. 2007. Türkiye’de atlarda Babesia etkenlerinin saptanmasinda PCR tekniğinin uygulanmasi (TAGEM 2007, Project number: HS/01/02/06/05/103)10.2118/0102-05-TTSearch in Google Scholar

De Waal T. 1992. Equine piroplasmosis: A review. British Veterinary Journal, 148, 6–14. 10.1016/0007-1935(92)90061-5Search in Google Scholar

Duzlu O. 2013. Atlarin vektör kaynakli protozoon hastaliklari. 17th National Parasitology Congress Proceedings, Denizli, Turkey, pp. 51–54Search in Google Scholar

Farkas R., Tánczos B., Gyurkovszky M., Földvári G., Solymosi N., Edelhofer R., Hornok S. 2013. Serological and molecular detection of Theileria equi infection in horses in Hungary. Veterinary Parasitology, 192, 143–148. 10.1016/j.vetpar.2012.09.035Search in Google Scholar

Gallusová M., Qablan M.A., D’Amico G., Oborník M., Petrzelková K.J., Mihalca A.D, Modry’ D. 2014. Piroplasms in feral and domestic equines in rural areas of the Danube Delta, Romania, with survey of dogs as a possible reservoir. Veterinary Parasitology, 206, 287–292. 10.1016/j.vetpar.2014. 10.018Search in Google Scholar

Garcia-Bocanegra I., Arenas-Montes A., Hernández E., Adaszek L., Carbonero A., Almeria S., et al. 2013. Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infection in equids. Veterinary Journal, 195, 172–178. 10.1016/j.tvjl.2012.06.012Search in Google Scholar

Guidi E., Pradier S., Lebert I., Leblond A. 2015. Piroplasmosis in an endemic area: analysis of the risk factors and their implications in the control of Theileriosis and Babesiosis in horses. Parasitology Researche, 114, 71–83. 10.1007/s00436-014-4161-9Search in Google Scholar

Güçjü H.Z., Karaer K.Z. 2007. Ankara Yöiesinde Sportif ve Gösteri Amaçli Yetiştirilen Atlarda Babesia caballi (Nuttall, 1910) ve Theileria equi (Syn. Babesia equi, Laveran, 1901)’nin Yayilişmm Polimeraz Zincir Reaksiyonu ile Araştmlmasi. Türkiye Parazitoloji Dergisi, 31, 89–93. (In Turkish)Search in Google Scholar

Hailat N.Q., Lafi S.Q., Al-Darraji A.M., Al-Ani F.K. 1997. Equine babesiosis associated with strenuous exercise: clinical and pathological studies in Jordan. Veterinary Parasitology, 69, 1–8. 10.1016/S0304-4017(96)01100-4Search in Google Scholar

Heim A., Passos L.M.F., Ribeiro M.F.B., Costa-Junior L.M., Bastos C.V., CabralD.D., et al. 2007. Detection and molecular characterization of Babesia caballi and Theileria equi isolates from endemic areas of Brazil. Parasitology Research, 102, 63–68. 10.1007/s00436-007-0726-1Search in Google Scholar PubMed

Hussain M.H., Saqib M., Fahad Raza Muhammad G., Asi M.N., Mansoor M.K., Saleem M., Jabbar A. 2014. Seroprevalence of Babesia caballi and Theileria equi in five draught equine populated metropolises of Punjab, Pakistan. Veterinary Parasitology, 202, 248–256. 10.1016/j.vetpar.2014.01.026Search in Google Scholar PubMed

Jaffer O., Abdishakur F., Hakimuddin F., Riya A., Wernery U., Schuster R.K., 2010. A comparative study of serological tests and PCR for the diagnosis of equine piroplasmosis. Parasitology Research, 106, 709–713. 10.1007/s00436-009-1669-5Search in Google Scholar PubMed

Kizilarslan F., Yildirim A., Duzlu O., Inci A., Onder Z., Ciloglu A. 2015. Molecular Detection and Characterization of Theileria equi and Babesia caballi in Horses (Equus ferus caballus) in Turkey. Journal of Equine Veterinary Science, 35, 830–835. 10.1016/j.jevs.2015.08.002Search in Google Scholar

Krause P.K. 2003. Babesiosis Diagnosis and Treatment. Vector Borne and Zoonotic Diseases, 3, 45–51. 10.1089/15303660 3765627451Search in Google Scholar

Mahmoud M.S., Abu El-Ezz N.T., Abdel-Shafy S., Nassar S.A., El Namaky A.H., Khalil W.K.B., et al. 2016. Assessment of Theileria equi and Babesia caballi infections in equine populations in Egypt by molecular, serological and hematological approaches. Parasites and Vectors, 9, 260. 10.1186/ s13071-016-1539-9Search in Google Scholar

Mehlhorn H., Schein E. 1998. Redescription of Babesia equi Laveran, 1901 as Theileria equi Mehlhorn, Schein 1998. Parasitology Research, 84, 467–47510.1007/s004360050431Search in Google Scholar PubMed

Moretti A., Mangili V., Salvatori R., Maresca C., Scoccia E., Torina A., et al. 2010. Prevalence and diagnosis of Babesia and Theileria infections in horses in Italy: A preliminary study. Veterinary Journal, 184, 346–350. 10.1016/j.tvjl.2009. 03.021Search in Google Scholar

Mujicaa F.F., Perrone T., Forlano M., Coronado A., Meléndez R.D., Barrios N., et al. 2011. Serological prevalence of Babesia caballi and Theileria equi in horses of Lara State, Venezuela. Veterinary Parasitology, 178, 180–183. 10.1016/j.vetpar.2010.12.036Search in Google Scholar PubMed

Munkhjargal T., Sivakumar T., Battsetseg B., Nyamjargal T., Aboulaila M., Purevtseren B., et al. 2013. Prevalence and genetic diversity of equine piroplasms in Tov province, Mongolia. Infection, Genetics and Evolution, 16, 178–185. 10.1016/j.meegid.2013.02.005Search in Google Scholar PubMed

OIE Terrestrial Manual 2014. Equine Piroplasmosis. NB: Version adopted by the World Assembly of Delegates of the OIE in May 2014 CHAPTER 2.5.8Search in Google Scholar

Qablan M.A., Oborník M., Petrželková K.J., Sloboda M., Shudiefat M.F., Hořín P., et al. 2013. Infections by Babesia caballi and Theileria equi in Jordanian equids: epidemiology and genetic diversity. Parasitology, 140, 1096–1103. 10.1017/S003 1182013000486Search in Google Scholar

Rothschild C.M. 2013. Equine piroplasmosis. Journal of Equine Veterinary Science, 33, 497–508. 10.1016/j.jevs.2013.03.189Search in Google Scholar

Schnittger L., Rodriguez A.E., Florin-Christensen M., Morrison, D.A. 2012. Babesia: A world emerging. Infection, Genetics and Evolution, 12, 1788–1809. 10.1016/j.meegid.2012.07.004Search in Google Scholar PubMed

Sevinc F., Maden M., Kumas C., Sevinc M., Ekici O.D. 2008. A comparative study on the prevalence of Theileria equi and Babesia caballi infections in horse sub-populations in Turkey. Veterinary Parasitology, 156, 173–177. 10.1016/j.vetpar.2008.06.006Search in Google Scholar PubMed

Sgorbini M., Bonelli F., Nardoni S., Rocchigiani G., Corazza M., Mancianti F. 2015. Seroprevalence and Molecular Analysis of Babesia caballi and Theileria equi in Horses from Central Italy During a 10-Year Period Journal of Equine Veterinary Science, 35, 865–868. 10.1016/j.jevs.2015.08.011Search in Google Scholar

Sigg L., Gerber V., Gottstein B., Doherr M.G., Frey C.F. 2010. Seroprevalence of Babesia caballi and Theileria equi in the Swiss horse population. Parasitology International, 59, 313–317. 10.1016/j.parint.2010.02.005Search in Google Scholar PubMed

Slivinska K., Víchová B., Werszkoc J., Szewczyk T., Wróblewski Z., Petko B., et al. 2016. Molecular surveillance of Theileria equi and Anaplasma phagocytophilum infections in horses from Ukraine, Poland and Slovakia. Veterinary Parasitology, 215, 35–37. 10.1016/j.vetpar.2015.10.025Search in Google Scholar PubMed

Sloboda M., Jirkú M., Lukesova D., Qablan M.A., Batsukh Z., Fiala I., et al. 2011. A survey of piroplasmids in horses and Bactrian camels in North-Eastern Mongolia. Veterinary Parasitology,179, 246–249. 10.1016/j.vetpar.2011.01.064Search in Google Scholar PubMed

Yilmaz O., Ertugrul M., Boztepe S. 2012. Some Morphological Traits of Arabian Horses Used for Javelin Swarm (Cirit) Game in Erzurum. Journal of Animal Science Advances, 2, 659–663Search in Google Scholar

Yilmaz O., Wilson R.T. 2013. The Domestic Livestock Resources of Turkey: Occurrence and Control of Diseases of Horses, Donkeys and Mules. Journal of Equine Veterinary Science, 33, 1021–1030. 10.1016/j.jevs.2013.05.003Search in Google Scholar

Takeet M., Adeleye A., Adebayo O.O., Akande F. 2009. Haematology and serum biochemical alteration in stress induced equine theileriosis. A case report. The Scientific World Journal, 4, 19–2110.4314/swj.v4i2.51840Search in Google Scholar

Tamura K., Dudley J., Nei M., Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Molecular Biology and Evolution, 24, 1596–1599. 10.1093/molbev/msm092Search in Google Scholar PubMed

Tamzali Y. 2013. Equine piroplasmosis: An updated review. Equine Veterinary Education, 25, 590–598. 10.1111/eve.12070Search in Google Scholar

Wise L.N., Kappmeyer L.S., Mealey R.H., Knowles D.P. 2013. Review of Equine Piroplasmosis. Journal of Veterinary Internal Medicine, 27, 1334–1346. 10.1111/jvim.12168Search in Google Scholar PubMed

Received: 2016-8-28
Revised: 2016-11-8
Accepted: 2016-11-17
Published Online: 2016-12-28
Published in Print: 2017-3-1

© 2017 W. Stefański Institute of Parasitology, PAS

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