Ovine babesiosis

Abstract

Background/Aim: Babesia ovis, the main causative agent of ovine babesiosis is a tick-borne hemoprotozoan parasite and causes significant economic losses in small ruminant livestock in tropical and subtropical regions. Although the disease occurs between April and September depending on the tick activities, the pick occurrence is observed in June and July. Babesiosis may cause up to 30-50% mortality among susceptible sheep breeds. As there is no vaccine available against the disease, the main methods for the control of the disease are the eradication of ticks through the use of acaricides and treatment of the animals showing the sings of the disease. Conclusion: Although babesiosis causing significant economical losses in sensitive animals occurs in almost every region of Turkey, the disease remains to be rather neglected. There is an urgent need to conduct experiments aimed to increase our understanding of the pathogenesis and epidemiology of the disease that will in turn facilitate the development of diagnostic methods and effective vaccines as preventive measures against babesiosis.

Keywords

• Babesia ovis,Sheep,Babesiosis.

Koyun Babesiosisi

Abstract

Özbilgi/Amaç: Ovine babesiosisine neden olan Babesia ovis, kenelerle bulaşan bir kan protozoonu olup, oluşturduğu hastalık tropik ve subtropik bölgelerdeki küçükbaş hayvan yetiştiriciliğinde önemli ekonomik kayıplara neden olmaktadır. Kene aktivitesine bağlı olarak Haziran ve Temmuz aylarında pik yapan hastalık genellikle Nisan-Eylül arası görülmekte ve duyarlı koyun ırklarında %30-50 oranında mortaliteye neden olmaktadır. Hastalığa karşı herhangi bir aşı bulunmadığı için hastalıkla mücadele akut vakaların ilaç ile tedavisi ve akarasitlerle kene mücadelesi şeklinde yapılmaktadır. Sonuç: Türkiye’nin hemen her bölgesinde görülen ve duyarlı hayvanlarda önemli ekonomik kayıplara neden olan bir hastalık olmasına rağmen B. ovis enfeksiyonları genellikle göz ardı edilmektedir. Hastalığın patogenezini ve epidemiyolojisini daha iyi anlamak ve bu kayıpların önüne geçebilmek için araştırmaların yapılması gerekmektedir. Bu araştırmalar aynı zamanda tanı metotlarının ve korunmada önemli yer tutan aşıların geliştirilmesine katkı sağlayacaktır.

Keywords

• Babesia ovis,Koyun,Babesiosis.

References

1. Aiello SE (2008). The Merck Veterinary Manual. 8th ed. Whitehouse Station: Merck and Co. Inc., pp. 537-9.
2. Aktaş M, Düzgün A, Cahit B (2001). Malatya Yöresinde Koyunlarda B. ovis ‘in Seroprevalansı. Türk J. Vet. Anim. Sci., 25, 241-243.
3. Aktas M, Altay K, Dumanlı N (2005). Development of polymerase chain reaction method for diagnosis of Babesia ovis infection in sheep and goats. Vet. Parasitol., 133, 277-281.
4. Aktas M, Altay K, Dumanlı 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.
5. Altay K, Dumanli N, Aktas M (2007). Molecular identification, genetic diversity and distribution of Theileria and Babesia species infecting small ruminants, Veterinary Parasitology 147: 161–165.
6. Altay K, Aktas M, Dumanli N, (2008). Detection of Babesia ovis by PCR in Rhipicephalus bursa collected from naturally infested sheep and goats. Res. Vet. Sci., 85, 116–119.
7. Aydin L, Bakirci S (2007). Geographical distribution of ticks in Turkey. Parasitol. Res., 101 (2), 163–166.
8. Bilal T (2005). Koyun ve keçilerin iç hastalıkları ve beslenmesi. İstanbul Üniversitesi Vet Fak, İstanbul, 108-110.

9. Biu AA, Ibrahim AI, Kumshe HA, Ahmed TB (2012). Prevalence of Babesia ovis in maiduguri metropolis, nigeria, Journal of Science and Multidisciplinary Research, 2277-0135.
10. Bock R, Jackson L, De Vos A, Ve Jorgensen W (2004). Babesiosis of cattle. Cambridge University PressPrinted in the United Kingdom, Parasitology 129, 247–269.
11. Braskara RAO P, Surendran NS, Ramachandra RAO PV (1989). Study on outbreaks of babesiosis in sheep in Andhra Pradesh. İndian Vet J., 66, 348-351.
12. Çiçek H, Düzgün A, Emre Z, Karaer Z (2004). Seroprevalance of Babesia ovis in Around Afyon. Turk. J. Vet. Amin. Sci., 28, 683-686.
13. De Waal DT, Combrink MP (2006). Live vaccines against bovine babesiosis. Vet. Parasitol., 138, (1–2), 88–96.
14. Dumanlı N, Köroğlu E, Düzgün A, Angın M ve Küçükerdem N (1997). Elazığ Yöresinde Koyunlarda B. ovis’ in Seroprevalansı. Türk Journal of Veterinary and Animal Sciences, 21, 183-186.
15. Ekici OD, Sevinc F, Isik N (2012). Instability of ovine babesiosis in anendemic area in Turkey. Vet. Parasitol., 188, (3-4), 372–375.
16. Emre Z, Duzgun A, Iriadam M, Sert H (2001). Seroprevalence of Babesia ovis in Awassi sheep in Urfa, Turkey. Turk. J. Vet. Anim. Sci., 25, 759–762.
17. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S (2012a). Investigation of hematological and biochemical parameters in small ruminants nat- urally infected with Babesia ovis. Vet. Res. Forum. 3, (1), 31–36.
18. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh (2012b). Evaluation of antioksidant status and oxsidative stress in sheep naturally infected with Babesia ovis, Veterinary Parasitology 185:124-130.
19. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir- Naghadeh B, Mardani K, Jalilzadeh-Amin G, Golabi M, Arjmand J (2014). PCR- Based Detection of Babesia ovis in Rhipicephalus bursa and Small Ruminants. Hindawi Publishing Corporation Journal of Parasitology, Research Article ID 294704, 6 p.
20. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Malekinejad H, Jalilzadeh-Amin G, Arjmand J, Golabi M, Hajipour N (2014b). Evaluation of antioxidant status, oxidative stress and serum trace mineral levels associated with Babesia ovis parasitemia in sheep, Veterinary Parasitology 205:38-45).
21. Fakhar, M, Hajihasani A, Maroufi S, Alizadeh H, Shirzad H, Piri F, Pagheh AS (2012). An epidemiological survey on bovine and ovinebabesiosis in Kurdistan Province, western Iran. Trop. Anim. HealthProd., 44, (2), 319–322.
22. Ferrer D, CastellaÁ J, GutieÂrrez JF (1998). Seroprevalence of Babesia ovis in sheep in Catalonia, northeastern Spain, Veterinary Parasitology, 79:275-281.
23. Friedhoff KT (1988). Transmission of Babesia, In: Babesiosis of domestic animals and man Ristic M. (Ed), Florida, Boca Raton, pp. 23–52.
24. Friedhoff KT (1997). Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parasitologia, 39, 99– 109.
25. Gaffar FR, Yatsuda AP, Franssen FFJ, Vries E (2004). Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infection and immunity, 72, (5), 2947–2955.
26. Geleta AR (2005). Antibody response to Babesia bigemina and Babesia bovis by vaccinated and unvaccinated cattle in an endemic area of South Africa. Master thesis, University of Retoria.
27. Georges K, Loria GR, Riili S, Greco A, Caracappa S, Jongejan F, Sparagano O (2001). Detection of haemoparasites in cattle by reverseline blot hybridisation with a note on the distribution of ticks in Sicily. Vet. Parasitol., 99, 273–286.
28. Göksu K. (1976). Yerli koyunlarımızda Babesidae ve Theileridae’lerin epizootiyolojik durumlarıyla biyolojilerine dair araştırmalar. AÜ. Vet. Fak. Yay., 205.
29. 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.
30. Habela M, Reina D, Nieto C, Navarrete I (1990). Antibody response and duration of latent infection in sheep following experimental infection with Babesia ovis, Veterinary Parasitology 35:1-10.
31. Habela MA, Reina D, Navarrete I, Redondo E, Hernandez S (1991). Histopathological changes in sheep experimentally infected with Babesia ovis. Vet. Parasitology, 38:1-12.
32. Hildebrandt PK (1981). The organ and vascular pathology of babesiosis. In: Babesiosis. Ristic M, Kreier JP (Eds). New York, Academic Press, 459-473.
33. Horta S, Barreto MC, Pepe A, Campos J, Oliva A (2014). Highly sensitive method for diagnosis of subclinical B. ovis infection. Ticks and Tick- borne Diseases, 5, 902-906.
34. Iça A (2003). Sığırlarda Bazı Babesia Türlerinin Reverse Line Blotting ve Indirect Floresan Antikor Testi ile Karşılaştırmalı Tanısı Üzerine Araştırmalar. Doktora Tezi, Ankara Üniversitesi, Sağlık Bilimleri Enstitüsü, Ankara.
35. Ijaz M, Rehman A, Ali MM, Umai M, Khalid S, Mehmood K, Hanif A (2013). Clinico-epidemiology and therapeutıcal trials on babesiosis in sheep and goats in Lahore, Pakistan. The Journal of Animal & Plant Sciences, 23, (2), 666-669.
36. Inci A, Yukarı BA, Sayın F (1998). Çankırı yöresinde bazı koyun ve keçi sürülerinde babesiosis ve theileriosis etkenlerinin mikroskobik kan muayenesiyle araştırılması, Ankara Üniv. Vet. Fak. Derg., 45: 105- 113.
37. Inci A, Karaer Z, İça A (2002). Kayseri Yöresinde Koyun ve Keçilerde Babesiosis. Fırat Ünivetsitesi Sağlık Bilimleri Dergisi, 16,(1), 79-83.
38. Inci A, Ica A, Yıldırım A, Duzlu O (2010a). Identification of Babesia and Theileria species in small ruminants in Central Anatolia (Turkey) via reverse line blotting Turk. J. Vet. Anim. Sci., 34: 205–210.
39. Inci A, Düzlü Ö, İça A (2010b). Babesiidae. In: Veteriner Protozooloji, Dumanli N, Karaer Z (Eds), Ankara: Medisan Yayınevi: 183-206.
40. Karaer Z, Nalbantoğlu S (2005). Protozoon Hastalıklarında Tedavi. In: Veteriner Hekimliğinde Parazit Hastalıklarında Tedavi. Burgu A, Karaer Z (Ed). İzmir, 15-16.
41. Karatepe M ve Karatepe B (2013). Koyun ve keçilerde Babesiosis. In: Veteriner Hekimliğinde parazit hastalıkları, Yukarı BA (Ed), cilt 2, Türkiye Parazitoloji Derneği Yayını no:24.
42. Kreier JP, Baker JR (1987). Parasitic Protozoa. Boston: Allen and Unwin Inc. pp 241.
43. Kuttler KL (1988). Worldwide impact of babesiosis. In: Babesiosis of Domestic Animals and Man. Ristic M (Ed), CRC Press, Boca Raton, Florida, pp.1-22.
44. Levine ND (1985). Phylum II. Apicomplexa Levine, 1970. In: An Illustrated Guide to the Protozoa Society of Protozoologists. Lee JJ, Hutner SH, Bovee EC (Eds). Kansas, Lawrence, pp. 322-374.
45. Mahoney DF. (1977). Babesia of domestic animals. In: Parasitic Protozoa, Kreier JP (Ed). Newyork: Academic Press: 1-52.
46. Mehlhorn H, Schein E (1984). The piroplasms: life cycle and sexual stages. Adv. Parasitol, 23, 37–103.
47. Mehlborn H (2005). Cellular Organisation of Parasite Protozoa. In: Microbiology and Microbial Infections. Parasitology. Stephen H, Gillespie and Dickson D Topley and Wilson (Eds). Despommier, ASM Press.
48. Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ (2012). Current advances in detection and treatment of babesiosis. Curr. Med. Chem., 19,1504–1518.
49. Papadopoulos B (1990). Ticks and piroplasms of domestic animals. Revue Suisse de Zoologie 97:782.
50. Pipano E (1995). Live vaccines against hemoparasitic diseases in livestock. Vet. Parasitol., 57, (1-3), 213–231.
51. Purnell RE (1981). Babesiosis in Various Hosts. In: Babesiosis. Ristic M, Kreier JP (Eds) New York, Academic Press. pp 25-63.
52. Rahbari S, Nabian S, Shayan P (2007). Primary report on distribution of tick fauna in Iran, Parasitology Research, 101:175-177.
53. Rahbari S, Nabian S, Khaki Z, Alidadi N, Ashrafihelan J (2008). Clinical, haematologic and patholojic aspects of experimental ovine babesiosis in Iran, Iranian Journal of Veterinary research, Shiraz University, 9:1:22.
54. Ranjbar-Bahadori S, Eckert B, Omidian Z, Shirazi NS, Shayan P (2011). Babesia ovis as the main causative agent of sheep babesiosis in Iran. Parasitol. Res., 110, 1531–1536.
55. Rashid A, Khan JA, Khan MS, Rasheed K, Maqbool A, Iqbal J (2010). Prevalence and chemotherapy of babesiosis among Lohi sheep in the Livestock Experiment Station, Qadirabad, Pakistan and environs. The Journal of Venomous Animals and Toxins including Tropical Diseases, 16, (4), 587-591.
56. Ray HN, Raghavachari K (1941). Observations on Babesia foliata n. sp. from a sheep. Indian J Vet Sci., 11:239–242.
57. Razmi GR, Naghibi A, Aslani MR, Fathivand M, Dastjerdi K (2002).An epidemiological study on ovine babesiosis in the Mashhad suburb area, province of Khorasan, Iran, Veterinary Parasitology, 108: 109- 115.
58. Rjeibi MR, , Mhadhbi M, Mabrouk W, Ayari B, Nasfi I, Jedidi M, Sassi L, Rekik M, Darghouth MA (2014). Prevalence of piroplasms in small ruminants in North-West Tunisia and the first genetic characterisation of Babesia ovis in Africa. Parasite, 21:23.
59. Saraylı H, Inci A, Ica A, Yıldırım A ve Düzlü Ö (2006). Yeşilhisar yöresindeki koyun ve keçilerde Babesia etkenlerinin reverse line blotting (RLB) yöntemiyle araştırılması. Sağlık Bilimleri Dergisi ( Journal of Health Sciences), 15, (3), 181-188.
60. Sarwar SM (1935). A hitherto undescribed piroplasm of goats (Piroplasma taylori). Indian Jour Vet Sci and Anim Husb., 5:171–176.
61. Sayin F, Dincer S, Karaer Z, Cakmak A, Yukarı BA, Eren H, Değer S, Nalbantoglu S (1997). Status of tick-borne diseases in sheep and goats in Turkey. Parasitologia, 39, 153–156.
62. Schetters TP, Kleuskens JA,Van De Crommert J (2009). Systematic inflamatory response in dogs experimentally infected with babasia canis, a hematological study, Vet Parasitol., 162:7-15.
63. Sevinc F, Dik B (1996). Konya yöresindeki koyunlarda Babesia ovis’in ELISA ile teşhisi, Vet. Bil. Derg., 12, 2 : 73- 79. Mardani K, Jalilzadeh-Amin G, Golabi M, Arjmand J (2014). PCR- Based Detection of Babesia ovis in Rhipicephalus bursa and Small Ruminants. Hindawi Publishing Corporation Journal of Parasitology, Research Article ID 294704, 6 p.
64. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Malekinejad H, Jalilzadeh-Amin G, Arjmand J, Golabi M, Hajipour N (2014b). Evaluation of antioxidant status, oxidative stress and serum trace mineral levels associated with Babesia ovis parasitemia in sheep, Veterinary Parasitology 205:38-45).
65. Fakhar, M, Hajihasani A, Maroufi S, Alizadeh H, Shirzad H, Piri F, Pagheh AS (2012). An epidemiological survey on bovine and ovinebabesiosis in Kurdistan Province, western Iran. Trop. Anim. HealthProd., 44, (2), 319–322.
66. Ferrer D, CastellaÁ J, GutieÂrrez JF (1998). Seroprevalence of Babesia ovis in sheep in Catalonia, northeastern Spain, Veterinary Parasitology, 79:275-281.
67. Friedhoff KT (1988). Transmission of Babesia, In: Babesiosis of domestic animals and man Ristic M. (Ed), Florida, Boca Raton, pp. 23–52.
68. Friedhoff KT (1997). Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parasitologia, 39, 99– 109.
69. Gaffar FR, Yatsuda AP, Franssen FFJ, Vries E (2004). Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infection and immunity, 72, (5), 2947–2955.
70. Geleta AR (2005). Antibody response to Babesia bigemina and Babesia bovis by vaccinated and unvaccinated cattle in an endemic area of South Africa. Master thesis, University of Retoria.
71. Georges K, Loria GR, Riili S, Greco A, Caracappa S, Jongejan F, Sparagano O (2001). Detection of haemoparasites in cattle by reverseline blot hybridisation with a note on the distribution of ticks in Sicily. Vet. Parasitol., 99, 273–286.
72. Göksu K. (1976). Yerli koyunlarımızda Babesidae ve Theileridae’lerin epizootiyolojik durumlarıyla biyolojilerine dair araştırmalar. AÜ. Vet. Fak. Yay., 205.
73. 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.
74. Habela M, Reina D, Nieto C, Navarrete I (1990). Antibody response and duration of latent infection in sheep following experimental infection with Babesia ovis, Veterinary Parasitology 35:1-10.
75. Habela MA, Reina D, Navarrete I, Redondo E, Hernandez S (1991). Histopathological changes in sheep experimentally infected with Babesia ovis. Vet. Parasitology, 38:1-12.
76. Hildebrandt PK (1981). The organ and vascular pathology of babesiosis. In: Babesiosis. Ristic M, Kreier JP (Eds). New York, Academic Press, 459-473.
77. Horta S, Barreto MC, Pepe A, Campos J, Oliva A (2014). Highly sensitive method for diagnosis of subclinical B. ovis infection. Ticks and Tick- borne Diseases, 5, 902-906.
78. Iça A (2003). Sığırlarda Bazı Babesia Türlerinin Reverse Line Blotting ve Indirect Floresan Antikor Testi ile Karşılaştırmalı Tanısı Üzerine Araştırmalar. Doktora Tezi, Ankara Üniversitesi, Sağlık Bilimleri Enstitüsü, Ankara.
79. Ijaz M, Rehman A, Ali MM, Umai M, Khalid S, Mehmood K, Hanif A (2013). Clinico-epidemiology and therapeutıcal trials on babesiosis in sheep and goats in Lahore, Pakistan. The Journal of Animal & Plant Sciences, 23, (2), 666-669.
80. Inci A, Yukarı BA, Sayın F (1998). Çankırı yöresinde bazı koyun ve keçi sürülerinde babesiosis ve theileriosis etkenlerinin mikroskobik kan muayenesiyle araştırılması, Ankara Üniv. Vet. Fak. Derg., 45: 105- 113.
81. Inci A, Karaer Z, İça A (2002). Kayseri Yöresinde Koyun ve Keçilerde Babesiosis. Fırat Ünivetsitesi Sağlık Bilimleri Dergisi, 16,(1), 79-83.
82. Inci A, Ica A, Yıldırım A, Duzlu O (2010a). Identification of Babesia and Theileria species in small ruminants in Central Anatolia (Turkey) via reverse line blotting Turk. J. Vet. Anim. Sci., 34: 205–210.
83. Inci A, Düzlü Ö, İça A (2010b). Babesiidae. In: Veteriner Protozooloji, Dumanli N, Karaer Z (Eds), Ankara: Medisan Yayınevi: 183-206.
84. Karaer Z, Nalbantoğlu S (2005). Protozoon Hastalıklarında Tedavi. In: Veteriner Hekimliğinde Parazit Hastalıklarında Tedavi. Burgu A, Karaer Z (Ed). İzmir, 15-16.
85. Karatepe M ve Karatepe B (2013). Koyun ve keçilerde Babesiosis. In: Veteriner Hekimliğinde parazit hastalıkları, Yukarı BA (Ed), cilt 2, Türkiye Parazitoloji Derneği Yayını no:24.
86. Kreier JP, Baker JR (1987). Parasitic Protozoa. Boston: Allen and Unwin Inc. pp 241.
87. Kuttler KL (1988). Worldwide impact of babesiosis. In: Babesiosis of Domestic Animals and Man. Ristic M (Ed), CRC Press, Boca Raton, Florida, pp.1-22.
88. Levine ND (1985). Phylum II. Apicomplexa Levine, 1970. In: An Illustrated Guide to the Protozoa Society of Protozoologists. Lee JJ, Hutner SH, Bovee EC (Eds). Kansas, Lawrence, pp. 322-374.
89. Mahoney DF. (1977). Babesia of domestic animals. In: Parasitic Protozoa, Kreier JP (Ed). Newyork: Academic Press: 1-52.
90. Mehlhorn H, Schein E (1984). The piroplasms: life cycle and sexual stages. Adv. Parasitol, 23, 37–103.
91. Mehlborn H (2005). Cellular Organisation of Parasite Protozoa. In: Microbiology and Microbial Infections. Parasitology. Stephen H, Gillespie and Dickson D Topley and Wilson (Eds). Despommier, ASM Press.
92. Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ (2012). Current advances in detection and treatment of babesiosis. Curr. Med. Chem., 19,1504–1518.
93. Papadopoulos B (1990). Ticks and piroplasms of domestic animals. Revue Suisse de Zoologie 97:782.
94. Pipano E (1995). Live vaccines against hemoparasitic diseases in livestock. Vet. Parasitol., 57, (1-3), 213–231.
95. Purnell RE (1981). Babesiosis in Various Hosts. In: Babesiosis. Ristic M, Kreier JP (Eds) New York, Academic Press. pp 25-63.
96. Rahbari S, Nabian S, Shayan P (2007). Primary report on distribution of tick fauna in Iran, Parasitology Research, 101:175-177.
97. Rahbari S, Nabian S, Khaki Z, Alidadi N, Ashrafihelan J (2008). Clinical, haematologic and patholojic aspects of experimental ovine babesiosis in Iran, Iranian Journal of Veterinary research, Shiraz University, 9:1:22.
98. Ranjbar-Bahadori S, Eckert B, Omidian Z, Shirazi NS, Shayan P (2011). Babesia ovis as the main causative agent of sheep babesiosis in Iran. Parasitol. Res., 110, 1531–1536.
99. Rashid A, Khan JA, Khan MS, Rasheed K, Maqbool A, Iqbal J (2010). Prevalence and chemotherapy of babesiosis among Lohi sheep in the Livestock Experiment Station, Qadirabad, Pakistan and environs. The Journal of Venomous Animals and Toxins including Tropical Diseases, 16, (4), 587-591.
100. Ray HN, Raghavachari K (1941). Observations on Babesia foliata n. sp. from a sheep. Indian J Vet Sci., 11:239–242.
101. Razmi GR, Naghibi A, Aslani MR, Fathivand M, Dastjerdi K (2002).An epidemiological study on ovine babesiosis in the Mashhad suburb area, province of Khorasan, Iran, Veterinary Parasitology, 108: 109- 115.
102. Rjeibi MR, , Mhadhbi M, Mabrouk W, Ayari B, Nasfi I, Jedidi M, Sassi L, Rekik M, Darghouth MA (2014). Prevalence of piroplasms in small ruminants in North-West Tunisia and the first genetic characterisation of Babesia ovis in Africa. Parasite, 21:23.
103. Saraylı H, Inci A, Ica A, Yıldırım A ve Düzlü Ö (2006). Yeşilhisar yöresindeki koyun ve keçilerde Babesia etkenlerinin reverse line blotting (RLB) yöntemiyle araştırılması. Sağlık Bilimleri Dergisi ( Journal of Health Sciences), 15, (3), 181-188.
104. Sarwar SM (1935). A hitherto undescribed piroplasm of goats (Piroplasma taylori). Indian Jour Vet Sci and Anim Husb., 5:171–176.
105. Sayin F, Dincer S, Karaer Z, Cakmak A, Yukarı BA, Eren H, Değer S, Nalbantoglu S (1997). Status of tick-borne diseases in sheep and goats in Turkey. Parasitologia, 39, 153–156.
106. Schetters TP, Kleuskens JA,Van De Crommert J (2009). Systematic inflamatory response in dogs experimentally infected with babasia canis, a hematological study, Vet Parasitol., 162:7-15.
107. Sevinc F, Dik B (1996). Konya yöresindeki koyunlarda Babesia ovis’in ELISA ile teşhisi, Vet. Bil. Derg., 12, 2 : 73- 79.
108. Sevinc F, Turgut K, Sevinc M, Ekici OD, Coskun A, Koc Y, Erol M, Ica A (2007). Therapeutic and Prophylactic efficacy of imidocard dipropionate on experimental Babesia ovis infection of lambs. Veterinary Parasitology, 149, 65-71.
109. Sevinc F, Sevinc M, Ekici OD, Yildiz R, Isik N, Aydogdu U (2013a). Babesia ovis infections:Detailed clinical and laboratory observationsin the pre- and post-treatment periods of 97 field cases. Vet. Parasitol.,191, (1-2), 35–43.
110. Sevinc F, Guler L, Sevinc M, Ekici OD, Isik N (2013b). Determination of immunoreactive proteins of Babesia ovis. Veterinary Parasitology, 198, 391-395.
111. Sevinc F, Sevinc M, Koc Y, Alkan F, Ekici OD, Yıldız R, Isık N ve Aydogdu U (2014). The effect of 12 successive blood passage on virulence of Babesia ovis in splenectomized lambs:A preliminary study. Small ruminant research, 116, 66-70.
112. Sevinc F, Cao S, Xuan X, Sevinc M, Ceylan O (2015). The identification and expression of a secreted protein 1 of Babesia ovis and an evaluation of its diagnostic potential in an enzyme-linked immunosorbent assay, J Clin Microbiol., JCM.03219-14.
113. Sivakumar T, Okubo K, Igarashi I, Silva WK, Kothalawala H, Silva SSP, Vimalakumar SC, Meewewa AS, Yokoyama N (2013). Genetic diversity of merozoite surface antigens in Babesia bovis detected from Sri Lankan cattle. Infection Genetics and Evolution, 19, 134- 140.
114. Soulsby EJL (1986). Helmints, Arthropods and Protozoa of Domestic Animals. 7th Ed Bailliere, Tindall, London, UK.
115. Starcovici, C (1893). Bemerkungen über den durch Babes entdeckten Blutparasiten und die durch denselben hervorgebrachten Krankheiten, die seuchenhafte Hämoglobinurie des Rindes (Babes), das Texasfieber (Th. Smith) und der Carceag der Schafe (Babes). Centralblatt für Bakteriologie und Parasitenkunde, 14: 1-8.
116. Sulaiman EG, Arslan SH, Al-Obaidi QT, Daham E (2010). Clinical, haematological and biochemical studies of babesiosis in native goats in Mosul, Iraqi Journal of Veterinary Sciences, 24:1, 31-35.
117. Sun Y, Moreau E, Chauvin A, Malandrin L (2011). The invasion process of bovine erythrocyte by Babesia divergens: knowledge from an in vitro assay. Veterinary Research, 42:62.
118. Systema naturale (2000). http://taxonomicon.taxonomy.nl/TaxonTree. aspx?id=154462&src=0.
119. Theodoropoulos G, Gazouli M, Ikonomopoulos JA, Kantzoura V, Kominakis A (2006). Determination of prevalence and risk factors of infection with Babesia in small ruminants from Greece by polymerase chain reaction amplification. Veterinary Parasitology, 135, 99–104.
120. Tufan E, Aslan Ö (2009). Doğal akut babesiosisli koyunlarda bazı kan parametrelerinin belirlenmesi. Sağlık Bilimleri Dergisi (Journal of Health Sciences), 18, (1), 33-37.
121. Tuik (2014). http://www.tuik.gov.tr/PreHaberBultenleri.do?id=16184.
122. 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.
123. Uilenberg G (2006). Babesia – a historical overview., Vet. Parasitol., 138, 3–10.
124. Wright IG, Goodger BV (1988). Pathogenesis of babesiosis. In: Babesiosis of domestic animals and man. Ristic M (Ed). Boca Raton, Florida, CRC Press, 99-118.
125. Yeruham I, Hadani A, Galker F, Rosen S (1995). A study of an enzootic focus of sheep babesiosis. Vet Parasitol, 60, 349-354.
126. Yeruham I, Hadani A, Galker F (1998). Some epizootiological and clinical aspects of ovine babesiosis caused by Babesia ovis, Veterinary Parasitology, 74: 153-163.
127. Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS (2003). Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin. Microbiol. Rev., 16, 622–636.