Small Ruminant Piroplasmosis: High Prevalence of Babesia aktasi n. sp. in Goats in Türkiye

Small ruminant piroplasmosis is the hemoparasitic infection of sheep and goats caused by Babesia and Theileria species responsible for clinical infections with high mortality outcomes. The disease is transmitted by ixodid ticks and prevalent in the tropical and subtropical regions of the world, including Türkiye. A prevalence survey, using molecular methods, is conducted in this study to determine the frequency of newly defined Babesia aktasi n. sp. and other tick-borne piroplasm species in small ruminants in Turkiye. A total of 640 blood samples from sheep (n = 137) and goats (n = 503) were analyzed by nested PCR-based reverse line blot (RLB) hybridization. The results show that 32.3% (207/640) of apparently healthy, small ruminants are infected with three Theileria and two Babesia species. Babesia aktasi n. sp. was the most prevalent species in goats, with 22.5% of samples being positive, followed by B. ovis (4%), T. ovis (2.8%), T. annulata (2.6%), and Theileria sp. (0.6%). None of the sheep samples were positive for Babesia aktasi n. sp.; however, 51.8% were infected with T. ovis. In conclusion, the findings reveal that B. aktasi n. sp. is highly prevalent in goats, but absent in sheep. In future studies, experimental infections will determine whether B. aktasi n. sp. is infectious to sheep, as well as its pathogenicity in small ruminants.

[1]  M. Aktas,et al.  Discovery of a Novel Species Infecting Goats: Morphological and Molecular Characterization of Babesia aktasi n. sp. , 2023, Pathogens.

[2]  B. Kumar,et al.  Molecular identification of Theileria species in naturally infected sheep using nested PCR–RFLP , 2022, Parasitology Research.

[3]  X. Xuan,et al.  Primary Tick-Borne Protozoan and Rickettsial Infections of Animals in Turkey , 2021, Pathogens.

[4]  C. Suárez,et al.  Bovine Babesiosis in Turkey: Impact, Current Gaps, and Opportunities for Intervention , 2020, Pathogens.

[5]  S. Stuen.  Haemoparasites—Challenging and Wasting Infections in Small Ruminants: A Review , 2020, Animals : an open access journal from MDPI.

[6]  K. Kundu,et al.  Investigations on First Confirmed Outbreak of Ovine Theileriosis (Theileria luwenshuni) from Maharashtra State, India , 2020, Indian Journal of Animal Research.

[7]  Xin He,et al.  Rapid detection of Babesia motasi responsible for human babesiosis by cross-priming amplification combined with a vertical flow , 2020, Parasites & Vectors.

[8]  F. Sevinc,et al.  Endemic instability of ovine babesiosis in Turkey: A country-wide sero-epidemiological study. , 2020, Veterinary parasitology.

[9]  W. Weir,et al.  Sheep as Host Species for Zoonotic Babesia venatorum, United Kingdom , 2019, Emerging infectious diseases.

[10]  M. F. Aydın,et al.  Tick-borne Pathogens in Small Ruminants in Turkey: A Systematic Review , 2019 .

[11]  Jia-Fu Jiang,et al.  Human Babesiosis Caused by a Babesia crassa–Like Pathogen: A Case Series , 2018, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[12]  Sudhir Kumar,et al.  MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. , 2018, Molecular biology and evolution.

[13]  M. Koyuncu,et al.  Goat production systems of Turkey: Nomadic to industrial , 2017, Small Ruminant Research.

[14]  W. Weir,et al.  Prevalence of tick-borne haemoparasites in small ruminants in Turkey and diagnostic sensitivity of single-PCR and RLB , 2017, Parasites & Vectors.

[15]  M. Aktas,et al.  Molecular evidence of a new Babesia sp. in goats. , 2017, Veterinary parasitology.

[16]  Pasi K. Korhonen,et al.  Genomic resources for a unique, low-virulence Babesia taxon from China , 2016, Parasites & Vectors.

[17]  M. Aktas,et al.  Molecular and Parasitological Survey of Ovine Piroplasmosis, Including the First Report of Theileria annulata (Apicomplexa: Theileridae) in Sheep and Goats from Turkey , 2016, Journal of Medical Entomology.

[18]  Jian-xun Luo,et al.  Genetic diversity and molecular characterization of Babesia motasi-like in small ruminants and ixodid ticks from China. , 2016, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[19]  N. Johnson,et al.  Detection of Theileria luwenshuni in sheep from Great Britain , 2016, Parasites & Vectors.

[20]  M. Aktas,et al.  Molecular and Parasitological Survey of Bovine Piroplasms in the Black Sea Region, Including the First Report of Babesiosis Associated with Babesia divergens in Turkey , 2015, Journal of medical entomology.

[21]  F. Jongejan,et al.  Theileria sp. OT3 and other tick-borne pathogens in sheep and ticks in Italy: molecular characterization and phylogeny. , 2015, Ticks and tick-borne diseases.

[22]  B. Penzhorn,et al.  Occurrence of tick-transmitted pathogens in dogs in Jos, Plateau State, Nigeria , 2014, Parasites & Vectors.

[23]  S. P. Yasini,et al.  Molecular Detection and Identification of Theileria Species by PCR-RFLP Method in Sheep from Ahvaz, Southern Iran , 2014, Iranian journal of parasitology.

[24]  S. Renneker,et al.  Coinfection of sheep with Anaplasma, Theileria and Babesia species in the Kurdistan Region, Iraq. , 2013, Transboundary and emerging diseases.

[25]  G. Razmi,et al.  Molecular surveillance of Theileria ovis, Theileria lestoquardi and Theileria annulata infection in sheep and ixodid ticks in Iran. , 2013, The Onderstepoort journal of veterinary research.

[26]  M. Aktas,et al.  Molecular identification of Theileria and Babesia in sheep and goats in the Black Sea Region in Turkey , 2013, Parasitology Research.

[27]  A. Rashidi,et al.  Molecular Detection of Theileria Spp. and Babesia Spp. in Sheep and Ixodid Ticks from the Northeast of Iran , 2013, The Journal of parasitology.

[28]  R. Yildiz,et al.  Babesia ovis infections: detailed clinical and laboratory observations in the pre- and post-treatment periods of 97 field cases. , 2013, Veterinary parasitology.

[29]  D. Salih,et al.  Naturally occurring infections of cattle with Theileria lestoquardi and sheep with Theileria annulata in the Sudan. , 2013, Veterinary parasitology.

[30]  D. Morrison,et al.  Babesia: a world emerging. , 2012, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[31]  A. Paparini,et al.  Identification of novel Babesia and Theileria genotypes in the endangered marsupials, the woylie (Bettongia penicillata ogilbyi) and boodie (Bettongia lesueur). , 2012, Experimental parasitology.

[32]  B. Kazemi,et al.  Identification of different Theileria species (Theileria lestoquardi, Theileria ovis, and Theileria annulata) in naturally infected sheep using nested PCR–RFLP , 2011, Parasitology Research.

[33]  F. Iqbal,et al.  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) , 2011, Parasite.

[34]  R. Pienaar,et al.  Diversity in the 18S SSU rRNA V4 hyper-variable region of Theileria spp. in Cape buffalo (Syncerus caffer) and cattle from southern Africa , 2011, Parasitology.

[35]  Jian-xun Luo,et al.  A new ovine Babesia species transmitted by Hyalomma anatolicum anatolicum. , 2009, Experimental parasitology.

[36]  D. M. Sherman,et al.  Goat Medicine: Smith/Goat Medicine , 2009 .

[37]  M. Bandehpour,et al.  Molecular identification of ovine Theileria species by a new PCR-RFLP method. , 2009, Veterinary parasitology.

[38]  M. Aktas,et al.  Detection of Babesia ovis by PCR in Rhipicephalus bursa collected from naturally infested sheep and goats. , 2008, Research in veterinary science.

[39]  M. Oosthuizen,et al.  Identification of a Novel Babesia sp. from a Sable Antelope (Hippotragus niger Harris, 1838) , 2008, Journal of Clinical Microbiology.

[40]  M. Aktas,et al.  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 , 2008, Parasitology Research.

[41]  J. Ahmed,et al.  At least two genetically distinct large Babesia species infective to sheep and goats in China. , 2007, Veterinary parasitology.

[42]  M. Aktas,et al.  Molecular identification, genetic diversity and distribution of Theileria and Babesia species infecting small ruminants. , 2007, Veterinary parasitology.

[43]  G. Uilenberg.  Babesia--a historical overview. , 2006, Veterinary parasitology.

[44]  A. García-Pérez,et al.  Identification, genetic diversity and prevalence of Theileria and Babesia species in a sheep population from Northern Spain. , 2004, International journal for parasitology.

[45]  S. Niemann,et al.  Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting , 2004, Parasitology Research.

[46]  Shuzhen Guo,et al.  Epidemiology of ovine theileriosis in Ganan region, Gansu Province, China , 2002, Parasitology Research.

[47]  S. Caracappa,et al.  Detection of haemoparasites in cattle by reverse line blot hybridisation with a note on the distribution of ticks in Sicily. , 2001, Veterinary parasitology.

[48]  L. Schouls,et al.  Simultaneous Detection of BovineTheileria and Babesia Species by Reverse Line Blot Hybridization , 1999, Journal of Clinical Microbiology.

[49]  D. Brown,et al.  Infectivity and cross-immunity studies of Theileria lestoquardi and Theileria annulata in sheep and cattle: I. In vivo responses. , 1999, Veterinary parasitology.

[50]  Jian-xun Luo,et al.  Theileriosis of sheep and goats in China , 1997, Tropical Animal Health and Production.

[51]  R. Hashemi-Fesharki.  Tick-borne diseases of sheep and goats and their related vectors in Iran. , 1997, Parassitologia.

[52]  K T Friedhoff,et al.  Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. , 1997, Parassitologia.

[53]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[54]  M. Hussien,et al.  Cross-infectivity of Theileria annulata and Theileria lestoquardi between cattle and sheep in the field in Sudan , 2022, Veterinary Research Notes.

[55]  H. Mehlhorn.  Progress in Parasitology , 2011 .

[56]  H. Mehlhorn,et al.  Small Ruminant Theileriosis , 2011 .

[57]  U. Kapil.  Iodine deficiency. , 1986, Indian pediatrics.