Document Type : Original Article


Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran


A total number of 450 blood samples were collected from 45 different randomly selected cattle herds. Light microscopic examination of blood smears revealed Babesia spp. infection in 4.2%, while 8.9% of blood samples were positive using PCR. Upon multiplex-PCR (mPCR), B. bigemina and B. bovis infections were detected in 37/40 (92.5%) and 3/40 (7.5%) samples, respectively. 530 ticks of 10 Ixodid species were collected from the same cattle. Hyalomma anatolicum was the most prevalent tick species (19.9%). An expected 520 bp fragment of Babesia spp. was generated in 22 (48.8%) of Rhpicephalus annulatus, 18 (40.0%) of R. bursa and 12 (30.0%) R. sanguineus sensu lato. The mPCR findings revealed that all infected ticks including R. annulatus, R. bursa and R. sanguineus were totally infected with B. bigemina. The DNA amplification of B. bovis and B. bigemina in egg samples showed that only B. bigemina was detected in two specimens of R. annulatus. It could be concluded that B. bigemina was the dominant causative agent in this region but the evidence of B. bovis infection of cattle in a few cases was noted, as well. The results suggested that B. bigemina and B. bovis could be detected in the DNA extracted from R. annulatus, R. bursa and R. sanguineus sensu lato confirming previous reports. Since B. bigemina is transmitted transovarially by R. annulatus, it might act as an important vector for B. bigemina.


Main Subjects

  1. Terkawi MA, Alhasan H, Huyen NX, et al. Molecular and serological prevalence of Babesia bovis and Babesia bigemina in cattle from central region of Syria. Vet Parasitol 2012; 187: 307-311.
  2. Bilgiç HB, Karagenç T, Simuunza M, et al. Development of a multiplex PCR assay for simultaneous detection of Theileria annulata, Babesia bovis and Anaplasma marginale in cattle. Exp Parasitol 2013; 133: 222-229.
  3. Liu J, Guan G, Liu A, et al. A PCR method targeting internal transcribed spacers: the simultaneous detection of Babesia bigemina and Babesia bovis in cattle. Acta Parasitol 2014; 59: 132-138.
  4. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, et al. Determination of prevalence and risk factors of infection with Babesia ovis in small ruminants from West Azerbaijan province, Iran by polymerase chain reaction. Iran J Arthropod Borne Dis 2015; 9: 246-252.
  5. Estrada-Pena A, Bouattaur A, Camicas JL, et al. Ticks of domestic animals in the Mediterranean region: A Guide to Identification of Species. Zaragoza, Spain: University of Zaragoza 2004; 43-131.
  6. Oliveira-Sequeira TCG, Oliveira MCS, Araujo JP, et al. PCR-based detection of Babesia bovis and Babesia bigemina in their natural host Boophilus microplus and cattle. Int J Parasitol 2005; 35: 105-111.
  7. Georges K, Loria GR, Riili S, et al. Detection of haemoparasites in cattle by reverse line blot hybridization with a note on the distribution of ticks in Sicily. Vet Parasitol 2001; 99: 273-286.
  8. Fakhar M, Hajihasani A, Maroufi S, et al. An epidemiological survey on bovine and ovine babesiosis in Kurdistan province, western Iran. Trop Anim Health Prod 2012; 44:319-322.
  9. Noaman V. A molecular study on Theileria and Babesia in cattle from Isfahan province, central Iran. J Parasit Dis 2013; 37: 208-210.
  10. Ekici, OD, Sevinc F. Comparison of cELISA and IFA tests in the serodiagnosis of anaplasmosis in cattle. Afr J Microbiol Res 2011; 5: 1188-1191.
  11. Ziapour SP, Esfandiari B, Youssefi MR. Study of the prevalence of babesiosis in domesticated animals with suspected signs in Mazandaran province, north of Iran, during 2008. Asian J Anim Vet Adv 2011; 10: 712-714.
  12. Khamesipour F, Doosti A, Koohi A, et al. Determination of the presence of babesia DNA in blood samples of cattle, camel and sheep in Iran by PCR. Arch Biol Sci 2015; 67:83-90.
  13. Ibrahim O, Taha Z, Jassim S. Prevalence of Babesia bovis in cattle in Tikreet city and its surroundings with hematological study. Tikrit J Pure Sci 2012; 17: 32-34.
  14. Altay K, Aydin MF, Dumanli N, et al. Molecular detection of Theileria and Babesia infections in cattle. Vet Parasitol 2008; 158: 295-301.
  15. Acici M, Bölükbaş CS, Pekmezci GZ, et al. Sero-epidemiological survey of bovine tick-borne infections in the Black Sea region of Turkey. Turk J Vet Anim Sci 2016; 40: 170-174.
  16. Aktas M, Ozubek S. 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 2015; 52: 1344-1350.
  17. Saleh MA. Erythrocytic oxidative damage in crossbred cattle naturally infected with Babesia bigemina. Res Vet Sci 2009; 86: 43-48.
  18. Yavuz A, İnci A, Düzlü Ö, et al. Molecular characterization of Babesia bovis msa-2c gene. Turk Parazitol Derg 2011; 35: 140-144.
  19. Rodriguez AE, Florin-Christensen M, Flores DA, et al. The glycosylphosphatidylinositol-anchored protein repertoire of Babesia bovis and its significance for erythrocyte invasion. Ticks Tick Borne Dis 2014; 5: 343-348.
  20. Ozlem DE, Sevinc F. Seroepidemiology study of B. bigemina in cattle in the Konya province, Turkey. Bull Vet Inst Pulawy 2009; 53: 645-649.
  21. Sevgili M, Cakmak A, Gokcen A, et al. Prevalence of Theileria annulata and Babesia bigemina in cattle in the vicinity of Sanliurfa. Asian J Anim Vet Adv 2010; 9: 292-296.
  22. Ameen KAH, Abdullah BA, Abdul-Razaq RA. Sero-prevalence of Babesia bigemina and Anaplasma marginale in domestic animals in Erbil, Iraq. Iraq J Vet Sci 2012; 26: 109-114.
  23. Calder JA, Reddy GR, Chieves L, et al. Monitoring Babesia bovis infections in cattle by using PCR-based tests. J Clin Microbiol 1996; 34: 2748-2755.
  24. Bell-Sakyi L, Koney EBM, Dogbey O, et al. Incidence and prevalence of tick-borne haemoparasites in domestic ruminants in Ghana. Vet Parasitol 2004; 124: 25-42.
  25. Oliveira MC, Oliveira-Sequeira TC, Araujo JP Jr, et al. Babesia spp. infection in Boophilus microplus engorged females and eggs in Sao Paulo state, Brazil. Vet Parasitol 2005; 130: 61-67.
  26. Terkawi MA, Huyen NX, Shinuo C, et al. Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Vet Parasitol 2011; 178: 201-207.
  27. Zintl A, Gray JS, Skerrett HE, et al. Possible mechanisms underlying age‐related resistance to bovine babesiosis. Parasite immunol 2005; 27: 115-120.
  28. Sappenfield E, Jamieson DJ, Kourtis AP. Pregnancy and susceptibility to infectious diseases. Infect Dis Obstetrics Gynecology 2013; 213: 1-9.
  29. Theodoropoulos G, Gazouli M, Ikonomopoulos JA, et al. Determination of prevalence and risk factors of infection with Babesia in small ruminants from Greece by polymerase chain reaction amplification. Vet Parasitol 2006; 135: 99-104.
  30. Ibrahim HM, Adjou Moumouni PF, Mohammed-Geba K, et al. Molecular and serological prevalence of Babesia bigemina and Babesia bovis in cattle and water buffalos under small-scale dairy farming in Beheira and Faiyum provinces, Egypt. Vet Parasitol 2013; 198: 187-192.
  31. Laha R, Mondal B, Biswas SK, et al. Detection of Babesia bigemina infection in cattle from north-eastern India by polymerase chain reaction and its genetic relatedness with other isolates. Trop Anim Health Prod 2015; 47: 633-636.
  32. Ica A, Inci A, Yildirim A. Parasitological and molecular prevalence of bovine Theileria and Babesia species in the vicinity of Kayseri. Turk J Vet Anim Sci 2007; 31: 33-38.
  33. Inci A, YazarS, Tuncbilek AS, et al. Vectors and vector-borne diseases in Turkey. Ankara Univ Vet Fak 2013; 60: 281-296.
  34. Yıldırım A, Düzlü Ö, Inci A, et al. Comparative diagnosis of Babesia bovis and Babesia bigemina in cattle by reverse line blotting, nested PCR and real-time PCR techniques. Kafkas Univ Vet Fak Derg 2013; 19: 895-902.
  35. Nabian S, Rahbari S. Occurrence of soft and hard ticks on ruminants in Zagros mountainous areas of Iran. Iran J Arthropod Borne Dis, 2008; 2: 16-20.
  36. Tavassoli M, Tabatabaei M, Mohammadi M, et al. PCR-based detection of Babesia spp. infection in collected ticks from cattle in west and north-west of Iran. Iran J Arthropod Borne Dis 2013; 7: 132-138.
  37. Sohrabi S, Yakhchali M, Ghashghai O. Hard ticks (Acarina: Ixodidae) diversity in the natural habitat of Iranian domestic ruminants: A provincial study in Kermanshah. J Vet Res 2013; 68: 39-46.
  38. Abdigoudarzi M. Detection of naturally infected vector ticks (Acari: Ixodidae) by different species of Babesia and Theileria agents from three different enzootic parts of Iran. Iran J Arthropod Borne Dis 2013; 7: 164-172.
  39. Omer LT, Kadir MAA, Seitzer U, et al. A survey of ticks (Acari: Ixodidae) on cattle, sheep and goats in the Dohuk Governorate, Iraq. Parasitol Res 2007; 101: 179-181.
  40. Dumanli N, Aktas M, Cetinkaya B, et al. Prevalence and distribution of tropical theileriosis in eastern Turkey. Vet Parasitol 2005; 127: 9-15.
  41. Aktas M, Altay K, Ozubek S, et al. A Survey of ixodid ticks feeding on cattle and prevalence of tickborne pathogens in the Black Sea region of Turkey. Vet Parasitol 2012; 187(3-4): 567-571.
  42. Riabi H, Atarodi A. Faunistic study of hard ticks (Ixodidae) of domestic ruminants in the Southern Khorasan-e-Razavi in comparing with other regions of the province in 2012 Iran. J Vet Adv 2014; 4: 508-515.
  43. Gharekhani J, Gerami-Sadeghian A, Sadeghi-Dehkordi Z, et al. Determination of hard tick species (Acarina: Ixodidae) on sheep and cattle in Hamedan province, Iran. J Coast Life Med 2015; 3: 612-615.
  44. Aydin MF, 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 2015; 114: 65-69.
  45. Hunfeld KP, Hildebrandt A, Gray JS. Babesiosis: recent insights into an ancient disease. Int J Parasitol 2008; 38: 1219-1237.
  46. Yeruham I, Hadani A, Galker F. Some epizootiological and clinical aspects of ovine babesiosis caused by Babesia ovis-a review. Vet Parasitol 1998; 74: 153-163.
  47. Yakhchali M, Rostami A, Esmaelzadeh M. Diversity and seasonal distribution of ixodid ticks in the natural habitat of domestic ruminants in north and south of Iran. Rev Med Vet 2011; 162: 229-235.
  48. Bakirci S, Sarali H, Aydin L, et al. Distribution and seasonal activity of tick species on cattle in the West Aegean region of Turkey. Exp Appl Acarol 2012; 56: 165-178.
  49. Howell JM, Ueti MW, Palmer GH, et al. Transovarial transmission efficiency of Babesia bovis tick stages acquired by Rhipicephalus (Boophilus) microplus during acute infection. J Clin Microbiol 2007; 45: 426-431.
  50. Chauvin A, Moreau E, Bonnet S, et al. Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Vet Res 2009; 40: 1-18.