Molecular epidemiology, risk factors and hematological evaluation of asymptomatic Theileria annulata infected cattle in Odisha, India

Document Type : Full paper (Original article)


1 Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt

2 Department of Clinical Medicine, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture and Technology, Bhubaneshwar 751003, Odisha, India

3 Department of Animal Breeding and Genetics, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture and Technology, Bhubaneshwar 751003, Odisha, India

4 Department of Veterinary Parasitology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture and Technology, Bhubaneshwar 751003, Odisha, India

5 Department of Veterinary Pathology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture and Technology, Bhubaneshwar 751003, Odisha, India


Background: Theileria annulata is a tick-borne apicomplexan parasite that affects bovine and causes severe economic losses. Aims: Our study aimed to determine the molecular prevalence of T. annulata infection in asymptomatic carrier cattle in Odisha, India, to study the association of potential risk factors with theileriosis, and to investigate the effect of the parasite infection on hematological parameters in naturally affected animals. Methods: A total of 226 cattle blood samples were collected from seven districts of Odisha, India. Molecular diagnoses of tropical theileriosis by polymerase chain reaction (PCR), cloning, sequencing, and phylogenetic analysis of isolated parasites were performed. Potential risk factors were investigated by univariable and multivariable logistic regression statistical analysis. Hematological parameters were compared between positive and negative animals. Results: All animals included in our study were clinically normal, however, 54.86% (124/226) of examined animals were positive by PCR for T. annulata. The multivariable logistic regression showed that contact with other cattle from different herds during grazing (P<0.0001; OR: 12.75; 95% CI: 5.21-31.21), previous history of clinical signs (P=0.002; OR: 3.31; 95% CI: 1.53-6.31), and frequency of a ectoparasiticides application pre year (P<0.0001; OR: 9.22; 95% CI: 3.03-28.09) were the potential risk factors for the occurrence of tropical theileriosis. Nucleotide sequence identity data demonstrated that T. annulata strain (MN818858) Odisha shared homology of 99.6%, 99.49%, and 99.36% with Uttar Pradesh, India (MF346035), Bahrain (AF214797), and Hyderabad, India (MK034702), respectively. Conclusion: This is the first study to gain insight into the molecular epidemiology, risk factors, phylogeny, and hematological analysis of asymptomatic T. annulata infected cattle from India.


Main Subjects

Abd Ellah, MR (2015). Studying the correlations among hematological and serum biochemical constituents in cattle theileriosis. J. Parasitic Dis., 39: 134-139.
Aparna, M; Vimalkumar, MB; Varghese, S; Senthilvel, K; Ajithkumar, KG; Raji, K; Syamala, K; Priya, MN and Deepa, CK (2013). Phylogenetic analysis of bovine Theileria spp. isolated in south India. Trop. Biomed., 30: 281-290.
Brown, CGD (1997). Dynamics and impact of tick borne diseases of cattle. Trop. Anim. Health Pro., 29: 15-35.
Chauhan, HC; Patel, BK; Bhagat, AG; Patel, MV; Patel, SI; Raval, SH; Panchasara, HH; Shrimali, MD; Patel, AC and Chandel, BS (2015). Comparison of molecular and microscopic technique for detection of Theileria annulata from the field cases of cattle. Vet. World. 8: 1370-1374.
Demeneghi, D; Stachurski, F and Adakal, H (2016). Experiences in tick control by acaricide in the traditional cattle sector in Zambia and Burkina Faso: possible environmental and public health implications. Front Public Health. 4: 239.
Dobbelaere, DAE and McKeever, DJ (2002). World class parasites. Vol. 3, Theileria. Boston, Kluwer Academic Publishers. PP: 1-22.
d’Oliveira, C; Van Der Weide, M and Habela, P (1995). Detection of Theileria orientalis in blood samples of carrier cattle by PCR. J. Clin. Microbiol., 13: 2665-2669.
Eamens, GJ; Bailey, G; Gonsalves, JR and Jenkins, C (2013). Distribution and temporal prevalence of Theileria orientalis major piroplasm surface protein types in eastern Australian cattle herds. Aust. Vet. J., 91: 332-340.
Gangly, A; Bhanot, V and Bisla, RS (2015). Hemato-biochemical alterations and direct blood polymerase chain reaction detection of Theileria annulata in naturally infected crossbred cows. Vet. World. 8: 24-28.
Ghaemi, P; Hoghooghi-Rad, N and Shayan, P (2012). Detection of Theileria orientalis in Iran by semi-nested PCR. Parasitol. Res., 110: 527-531.
Gharbi, M and Darghouth, MA (2014). A review of Hyalomma scupense (Acari, Ixodidae) in the Maghreb region: from biology to control. Parasite. 21: 12-18.
Gharbi, M; Sassi, L and Dorchies, P (2006). Infection of calves with Theileria annulata in Tunisia: economic analysis and evaluation of the potential benefit of vaccination. Vet. Parasitol., 137: 231-241.
Jabbar, A; Abbas, T; Saddiqi, HA; Qamar, MF and Gasser, RB (2015). Tick borne diseases of bovines in Pakistan: major scope for future research and improved control. Parasit Vectors. 8: 283. doi: 10.1186/s13071-015-0894-2.
Kala, SK; Deo, BG and Kumari, N (2018). Epidemiological aspects of theileriosis in cattle in and around Patna, Bihar, India. Int. J. Curr. Microbiol. Appl. Sci., 7: 1183-1191.
Kirvar, E; Ilhan, T; Katzer, F; Hooshmand-Rad, P; Zweygarth, E; Gerstenberg, C; Phipps, P and Brown, CGD (2000). Detection of Theileria annulata in cattle and vector ticks by PCR using the Tams 1 gene sequences. Parasitology. 120: 245-254.
Kohli, S; Atheya, UK and Thapliyal, A (2014). Assessment of optimum thermal humidity index for crossbred dairy cows in Dehradun district, Uttarakhand, India. Vet. World. 1: 7. doi: 10.14202/vetworld.2014.916-921.
Kundave, VR; Patel, AK; Patel, PV; Hasnani, JJ and Joshi, CG (2014). Qualitative and quantitative assessment of Theileria annulata in cattle and buffaloes polymerase chain reaction. Trop. Biomed., 31: 728-735.
Nazifi, S; Razavi, SM and Reiszadeh, M (2010). Evaluation of the resistance of indigenous Iranian cattle to Theileria annulata compared with Holstein cattle by measurement of acute phase proteins. Comp. Clin. Pathol., 19: 155-161.
Oryan, A; Namazi, F; Sharifiyazdi, H; Razavi, M and Shahriari, R (2013). Clinicopathological findings of a natural outbreak of Theileria annulata in cattle: an emerging disease in southern Iran. Parasitol. Res., 112: 123-127.
Ponnudurai, G; Larcombe, S and Velusamy, R (2017). Prevalence of tick-borne pathogens in co-grazed dairy bovines differs by region and host-type in Tamil Nadu; India. J. Adv. Dairy Res., 5: 177. 2329-888X.1000177.
Radostitis, OM; Blood, DC and Gay, CC (2006). A text book of veterinary medicine. 8th Edn., Baieller, Tindal and Cox. PP: 1206-1212.
Rizk, MA; Salama, A and El-Sayed, SA (2017). Animal level risk factors associated with Babesia and Theileria infections in cattle in Egypt. Acta Parasitol., 62: 796-803.
Sahoo, N; Behera, BK; Khuntia, HK and Dash, M (2017). Prevalence of carrier state theileriosis in lactating cows. Vet. world. 10: 1471. Fvetworld.2017.1471-1474.
Sharifiyazdi, H; Namazi, F; Oryan, A; Shahriari, R and Razavi, M (2012). Point mutations in the Theileria annulata cytochrome b gene are associated with buparvaquone treatment failure. Vet. Parasitol., 187: 431-435.
Sitotaw, TF; Regassa, F and Zeru, AG (2014). Epidemiological significance of major hemoparasites of ruminants in and around Debre-Zeit; Central Ethiopia. J. Parasitol. Vector Bio., 6: 16-22.
Sivakumar, T; Fujita, S; Tuvshintulga, B; Kothalawala, H; Silva, S and Yokoyama, N (2019). Discovery of a new Theileria sp. closely related to Theileria annulata in cattle from Sri Lanka. Sci. Rep., 9: 1-10.
Tamura, K; Stecher, G and Peterson, D (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 30: 2725-2729.
Thrusfield, M; Ortega, C; de Blas, I; Noordhuizen, JP and Frankena, K (2001). WIN EPISCOPE 2.0: improved epidemiological software for veterinary medicine. Vet. Record., 148: 567-572.
Watts, JG; Playford, MC and Hickey, KL (2016). Theileria orientalis: a review. N. Z. Vet. J., 64: 3-9.