Abstract
Hemoprotozoal diseases are significant health concerns in small ruminants. The present study was conducted to identify and characterize the species of Theileria and Anaplasma in sheep and goats located in different districts of North Gujarat, India. A total of 226 (Banaskantha = 175, Patan = 26, and Bhuj = 25) blood samples were collected from sheep (n = 78) and goats (n = 148), and 46 ticks were collected and identified from sheep and goats. PCR assays were carried out using genus and species-specific primers for Theileria targeting 18S rRNA locus and for Anaplasma targeting the msp5 gene. Overall, 37.2% sheep (29/78) and 10.8% of goats (16/148) were positive for Theileria by PCR, whereas 15.4% of sheep (12/78) and 25.7% goats (38/148) were positive for Anaplasma infection. Moreover, mixed infection was found in 4.4% (10/226) of sheep and goats by PCR. Sanger sequencing of Theileria and Anaplasma positives revealed a high similarity to T. ovis and A. ovis using NCBI blast, respectively. Phylogenetic analyses revealed that the Anaplasma spp. DNA sequences belonged to the A. ovis group and closely associated with the A. ovis nucleotide sequence strain Haibei isolated in China from sheep (GQ483471). The phylogenetic analysis based on the SSU rRNA locus revealed that the Theileria ovis DNA sequences belonged to the T. ovis group and closely related to MW440586 isolated in Kerala, India, from a goat. The majority of ticks (91.3%) were identified as Hyalomma. In conclusion, Theileria ovis and Anaplasma ovis were commonly identified species in sheep and goats and transmitted mainly by Hyalomma ticks in North Gujarat, India, which is important baseline data for future research and control strategies. This is the first report on Theileria and Anaplasma co-infections in sheep and goats from North Gujarat, India.
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All supporting data was included within this article and its additional files. The data produced during the study are available from the corresponding author for further request. Data and materials will be made available on demand.
Abbreviations
- 18S rRNA :
-
18S ribosomal ribonucleic acid
- DNA :
-
Deoxyribonucleic acid
- EDTA :
-
Ethylenediamine tetraacetic acid
- mL :
-
Milliliter
- MSP :
-
Major surface protein
- PCR :
-
Polymerase chain reaction
References
Alessandra T, Annalisa A, Valeria B, Angelina A, Rosalia D, Santo C, Anna MF, Marino VD (2012) Development and validation of two PCR tests for the detection of and differentiation between Anaplasma ovis and Anaplasma marginale. Ticks Tick-Borne Dis 3(5–6):283–287. https://doi.org/10.1016/j.ttbdis.2012.10.033
Altay K, Dumanli N, Holman PJ, Aktas M (2005) Detection of Theileria ovis in naturally infected sheep by nested PCR. Vet Parasitol 127(2):99–104. https://doi.org/10.1016/j.vetpar.2004.09.012
Altay K, Aktas M, Dumanli N (2007) Theileria infections in small ruminants in the East and Southeast Anatolia. Turkiye Parazitol Derg 31:268–271
Aravind MS, Gowrishankar C, Soundararajan, Latha BR (2020) Molecular detection of Anaplasma ovis in apparently healthy sheep and goats in Tamil Nadu. Int J Curr Microbiol Appl Sci 9(05):3589–3593. https://doi.org/10.20546/ijcmas.2020.905.426
Barbosa IC, Andre MR, Amaral R, Valente J, Vasconcelos PC, Oliveira C, Jusi M, Machado RZ, Vieira T, Ueti MW, Vieira R (2021) Anaplasma marginale in goats from a multispecies grazing system in northeastern Brazil. Ticks Tick-borne Dis 12(1):101592. https://doi.org/10.1016/j.ttbdis.2020.101592
Benjamin MM (2005) Outline of veterinary clinical pathology. III. Kalyani Publishers, New Delhi
Cao S, Zhang S, Jia L, Xue S, Yu L, Kamyingkird K, Moumouni PF, Moussa AA, Zhou M, Zhang Y, Terkawi MA, Masatani T, Nishikawa Y, Xuan X (2013) Molecular detection of Theileria species in sheep from northern China. J Vet Med Sci 75(9):1227–1230. https://doi.org/10.1292/jvms.13-0028
Dhaim YA, A’aiz NN (2014) Prevalence of theileriosis in sheep in Wasit province ALQadisiya. J Vet Med Sci 13:14–18
Estrada-Pena A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean Region. A guide of identification of species. Zaragoza: University of Zaragoza Press. p 131
Ghosh S, Nagar G (2014) Problem of ticks and tick-borne diseases in India with special emphasis on progress in tick control research: a review. J Vector Borne Dis 51:259–270
Grau HE, Cunha Filho NA, Pappen FG, Farias NA (2013) Transplacental transmission of Anaplasma marginale in beef cattle chronically infected in southern Brazil. Rev Bras Parasitol Vet 22(2):189–193. https://doi.org/10.1590/S1984-29612013000200038
Habibi G, Sepahvand-Mohammadi E, Afshari A, Bozorgi S (2020) Molecular detection of Theileria spp and Babesia ovis Infection in Sheep in Baneh, Iran. Archives of Razi Institute 75(2):289–296. https://doi.org/10.22092/ari.2019.125136.1297
Heid- arpourBami M, Khazraiinia P, Haddadzadeh HR, Kazemi B (2010) Identification of Theileria species in sheep in the eastern half of Iran using nested PCR-RFLP and microscopic techniques. Iran J Vet Res 11:262–266
Hornok S, Fuente DL, Biro J, Fernandez N, Meli IG, Elek ML, Gonczi V, Meili E, Tanczos T, Farkas B, Lutz H, Hofmann-Lehmann R (2011) First molecular evidence of Anaplasma ovis and Rickettsia spp. in keds (Diptera: Hippoboscidae) of sheep and wild ruminants. Vector Borne Zoonotic Dis 11(10):1319–1321. https://doi.org/10.1089/vbz.2011.0649
Inci A, Nalbantoğlu S, Cam Y, Atasever A, Karaer Z, Cakmak A, Sayin F, Yukari BA, Ica A, Deniz A (2003) Theileriosis and tick infestations in sheep and goats around Kayseri. Turkish J Vet Anim Sci 27:57–60
Jalali SM, Khaki Z, Kazemi B, Rahbari S, Shayan P, Bandehpour M, Yasini SP (2014) Molecular detection and identification of Theileria species by PCR-RFLP method in sheep from Ahvaz, Southern. Iran Iran J Parasitol 9(1):99–106
Jayalakshmi K, Selvaraj P, Veeraselvam M, Ravikumar R, Saravanan M, Venkatesan M, Ramkumar PK, Yogeshpriya S (2022) Prevalence of haemoparasites in sheep and goats in tropical climate of Tamil Nadu. Indian J Anim Sci 92(4):440–442
Kirvar E, Ilhan T, Katzer F, Wilkie G, Hooshmand-Rad P, Brown D (1998) Detection of Theileria lestoquardi (hirci) in ticks, sheep, and goats using the polymerase chain reaction. Ann N Y Acad Sci 849:52–62. https://doi.org/10.1111/j.1749-6632.1998.tb11033.x
Kumar B, Maharana BR, Thakre B, Brahmbhatt NN, Joseph JP (2022) 18S rRNA gene-based piroplasmid PCR: an assay for rapid and precise molecular screening of Theileria and Babesia species in animals. Acta Parasitol 67(4):1697–1707. https://doi.org/10.1007/s11686-022-00625
Kuttler KL (1984) Anaplasma infections in wild and domestic ruminants: a review. J Wildl Dis 20(1):12–20. https://doi.org/10.7589/0090-3558-20.1.12
Lalljee S, Soundararajan C, Singh Y, Sargison N (2019) The potential of small ruminant farming as a means of poverty alleviation in rural southern India. Trop Anim Health Prod 51(2):303–311. https://doi.org/10.1007/s11250-018-1686-4
Nagaraj HV, Lakshmanan B, Lonappan GV, Shameem H, Jose J, Sabu L (2019) Molecular identification of caprine carriers of theileriosis in South India. Vet Arh 89(3):367–378. https://doi.org/10.24099/vet.arhiv.0227
Nangru A, Maharana BR, Vohra S, Kumar B (2022) Molecular identification of Theileria species in naturally infected sheep using nested PCR-RFLP. Parasitol Res 121(5):1487–1497. https://doi.org/10.1007/s00436-022-07489-5
Niaz S, Ur Rahman Z, Ali I, Cossío-Bayúgar R, Amaro-Estrada I, Alanazi AD, Khattak I, Zeb J, Nasreen N, Khan A (2021) Molecular prevalence, characterization and associated risk factors of Anaplasma spp. and Theileria spp in small ruminants in Northern Pakistan. Parasite 28:3. https://doi.org/10.1051/parasite/2020075
Niu Q, Luo J, Guan G, Ma M, Liu Z, Liu A, Dang Z, Gao J, Ren Q, Li Y, Liu J, Yin H (2009) Detection and differentiation of ovine Theileria and Babesia by reverse line blotting in China. Parasitol Res 104(6):1417–1423. https://doi.org/10.1007/s00436-009-1344-x
Noaman V (2014) Comparison of molecular and microscopic technique for detection of Theileria spp. in carrier cattle. J Parasit Dis 38(1):64–67. https://doi.org/10.1007/s12639-012-0196-y
Oza J, Bhatt D, Patel K, Trivedi J (2020) Study of prevalence of tick Hyalomma excavatum (Acari: Ixodidae) on Bubalus bubalis in Patan District, Gujarat state, India. J B S 3(2):69–78
Rabeya B, Talukdar SK, Sarmah PC, Bulbul KH, Kakati P, Tamuly S, Islam S (2019) Molecular and microscopic detection of Theileria luwenshuni infection in goats in and around Guwahati of Assam. Biol Rhythm Res, India. https://doi.org/10.1080/09291016.2019.1621066
Shruthi R, Thimmareddy PM, Mamatha GS, Chandranaik BM, Puttalakshmamma GC (2017) Studies on theileriosis in goats from Karnataka. South India J Parasit Dis 41(4):1082–1085. https://doi.org/10.1007/s12639-017-0937-z
Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals. 7. London: Bailliere Tindall. pp-463–466
Tabbasum R, Awais T, Sakhawat A, Khalil R, Sharif A, Yousaf A, Arshad MI, Sindhu SR, Habib F, Shaheen S, Bachaya A, Ramzan MA, Rahman K, Zahra G (2021) Prevalence and risk factors of theileriosis in goat and sheep in Lahore. J Vet Sci Res 6(2):00215. https://doi.org/10.23880/oajvs-16000215
Taha KM, Salih DA, Ahmed BM, Enan KA, Ali AM, ElHussein AM (2011) First confirmed report of outbreak of malignant ovine theileriosis among goats in Sudan. Parasitol Res 109:1525–1527
Uilenberg G (2001) Babesiosis. In: Service MW (ed) Encyclopedia of arthropod-transmitted infections of man and domesticated animals. CABI, Wallingford, pp 53–60
Wang H, Yang J, Mukhtar MU, Zhijje L, Minghai Z, Xiaolong W (2019) Molecular detection and identification of tick-borne bacteria and protozoans in goats and wild Siberian roe deer (Capreolus pygargus) from Heilongjiang Province, northeastern China. Parasit Vectors 12:296. https://doi.org/10.1186/s13071-019-3553-1
Zakkyeh T, Mohammad Ali O, Nasibeh HV, Mohammad Reza YE, Farhang B, Fatemeh M (2012) First molecular detection of Theileria ovis in Rhipicephalus sanguineus tick in Iran. Asian Pac J Trop Med 5(1):29–32. https://doi.org/10.1016/S1995-7645(11)60240-X
Acknowledgements
The authors acknowledge the Department of Veterinary Public Health and the Department of Microbiology for providing the necessary facilities for the study. The author also acknowledges the Principal Veterinary College, Sardarkrushinagar, for giving the required funds for the study.
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This study was supported by the Plan scheme of Veterinary College, Sardarkrushinagar (B. H. 0108070018). This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Conceptualization, methodology, formal analysis, and investigation: Ankit Prajapati, Bhavesh Prajapati, and Arun Patel. Writing—original draft preparation: Ankit Prajapati. Writing—review and editing: Ankit Prajapati, Tarun Sutaria, and Ravjibhai K. Chaudhari. Resources: Arun Patel, Bhavesh Prajapati, Prakash Chauhan, Abhinav Suthar, Tarun Sutaria, Pankaj Patel, Vandip Chauhan, Samir Raval, and Bhupamani Das. Statistical analysis: Ravjibhai K Chaudhari. Supervision: Ramesh Patel.
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Prajapati, A., Prajapati, B., Patel, A. et al. Molecular identification and genetic characterization of Theileria and Anaplasma infection in sheep and goat of North Gujarat, India. Parasitol Res 122, 1427–1433 (2023). https://doi.org/10.1007/s00436-023-07848-w
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DOI: https://doi.org/10.1007/s00436-023-07848-w