Abstract
Theileria species, with a broad geographic distribution, infect a wide range of both domestic and wild animals and are transmitted by ixodid ticks. Currently, there is no comprehensive report regarding the distribution of Theileria spp. in the eastern Tibetan Plateau, especially in Ganze Tibetan autonomous prefecture (153,700 km2) and Ngawa Tibetan and Qiang autonomous prefecture (84,242 km2) of Sichuan province, China. In this study, we collected blood samples from yaks (n = 144) (Bos grunniens), Tibetan sheep (n = 92), and Tibet horses (n = 142) in Ganze and Ngawa.
Theileria sinensis, T. luwenshuni, and T. equi were the dominant Theileria species detected in yaks, Tibetan sheep, and horses with the total infection rates of 25.7% (37/144), 75.0% (69/92), and 51.4% (73/142), respectively. For ectoparasites, T. luwenshuni was the only Theileria species detected in sheep keds (Melophagus ovinus) with an infection rate of 30.8% (8/26). The total infection rates of T. sinensis in Haemaphysalis qinghaiensis, Dermacentor everestianus, and Rhipicephalus microplus were 34.6% (36/104), 34.0% (17/50), and 51.3% (58/113), respectively. Theileria spp., belonging to T. sergenti/buffeli/orientalis group, were only detected in R. microplus collected in Danba county of Ganze with a total infection rate of 39.9% (19/48). Our results provide important data of the epidemiology of Theileria spp. in livestock and ectoparasites and will assist with the implementation of measures to control theileriosis transmission in eastern Tibetan Plateau, China.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
Apanaskevich DA, Duan W, Apanaskevich MA, Filippova NA, Chen J (2014) Redescription of Dermacentor everestianus Hirst (Acari: Ixodidae), a parasite of mammals in mountains of China and Nepal with synonymization of D. abaensis Teng and D. birulai Olenev. J Parasitol 100(3):268–278. https://doi.org/10.1645/13-369.1
Bai Q, Liu GY, Yin H, Zhao QZ, Liu DK, Ren JX, Li X (2002) Theileria sinensis sp nov: a new species of bovine Theileria -molecular taxonomic studies. Acta Veterinaria et Zootechnica Sinica 33(2):185–190
Barre N, Uilenberg G (2010) Spread of parasites transported with their hosts: case study of two species of cattle tick. Rev Sci Tech 29(1):149–160 135-47
Bawm S, Kakisaka K, Thu MJ, Chel HM, Oo YMN, Soe NC, Win SY, Htun LL, Win MM, Suzuki H, Nakao R, Katakura K (2018) First molecular detection of Theileria luwenshuni from goats in Myanmar. Parasitol Res 117(10):3361–3364. https://doi.org/10.1007/s00436-018-6073-6
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Rapp BA, Wheeler DL (2002) GenBank. Nucleic Acids Res 30(1):17–20. https://doi.org/10.1093/nar/30.1.17
Bishop R, Musoke A, Morzaria S, Gardner M, Nene V (2004) Theileria: intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks. Parasitology 129(Suppl):S271–S283. https://doi.org/10.1017/s0031182003004748
Black WC, Piesman J (1994) Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci U S A 91(21):10034–10038. https://doi.org/10.1073/pnas.91.21.10034
Chen Z, Liu Q, Jiao FC, Xu BL, Zhou XN (2014) Detection of piroplasms infection in sheep, dogs and hedgehogs in Central China. Infect Dis Poverty 3:18. https://doi.org/10.1186/2049-9957-3-18
Chu CY, Jiang BG, Qiu EC, Zhang F, Zuo SQ, Yang H, Liu W, Cao WC (2011) Borrelia burgdorferi sensu lato in sheep keds (Melophagus ovinus), Tibet, China. Vet Microbiol 149(3–4):526–529. https://doi.org/10.1016/j.vetmic.2010.11.031
Deng GF, Jiang ZJ (1991) Economic insect fauna of China. Ixodes [M]. Beijing: science press
Fischer T, Myalkhaa M, Krücken J, Battsetseg G, Batsukh Z, Baumann MPO, Clausen PH, Nijhof AM (2019) Molecular detection of tick-borne pathogens in bovine blood and ticks from Khentii, Mongolia. Transbound Emerg Dis. https://doi.org/10.1111/tbed.13315
Friedhoff KT, Tenter AM, Muller I (1990) Haemoparasites of equines: impact on international trade of horses. Rev Sci Tech 9(4):1187–1194
Gibson W, Pilkington JG, Pemberton JM (2010) Trypanosoma melophagium from the sheep ked Melophagus ovinus on the island of St Kilda. Parasitology 137(12):1799–1804. https://doi.org/10.1017/S0031182010000752
He L, Feng H.H., Zhang W.J., Zhang Q.L., Fang R., Wang L.X., Tu P., Zhou Y.Q., Zhao J.L., Oosthuizen M.C.et al. (2012) Occurrence of Theileria and Babesia species in water buffalo (Bubalus babalis, Linnaeus, 1758) in the Hubei province, South China. Vet Parasitol 186(3–4):490–496 https://doi.org/10.1016/j.vetpar.2011.11.021
Jonsson NN, Piper EK, Constantinoiu CC (2014) Host resistance in cattle to infestation with the cattle tick Rhipicephalus microplus. Parasite Immunol 36(11):553–559. https://doi.org/10.1111/pim.12140
Kakati P et al (2015) Emergence of oriental theileriosis in cattle and its transmission through Rhipicephalus (Boophilus) microplus in Assam, India. Vet World 8(9):1099–1104. https://doi.org/10.14202/vetworld.2015.1099-1104
Kim SJ, Tsuji M, Kubota S, Wei Q, Lee JM, Ishihara C, Onuma M (1998) Sequence analysis of the major piroplasm surface protein gene of benign bovine Theileria parasites in East Asia. Int J Parasitol 28(8):1219–1227. https://doi.org/10.1016/s0020-7519(98)00095-2
Kundave VR, Ram H, Shahzad M, Garg R, Banerjee PS, Nehra AK, Rafiqi SI, Ravikumar G, Tiwari AK (2019) Genetic characterization of Theileria species infecting bovines in India. Infect Genet Evol 75:103962. https://doi.org/10.1016/j.meegid.2019.103962
Lee SH et al (2016) Novel detection of Coxiella spp., Theileria luwenshuni, and T. ovis Endosymbionts in deer keds (Lipoptena fortisetosa). PLoS one 11(5):e0156727. https://doi.org/10.1371/journal.pone.0156727
Li Y, Luo J, Liu Z, Guan G, Gao J, Ma M, Dang Z, Liu A, Ren Q, Lu B, Liu J, Zhao H, Li J, Liu G, Bai Q, Yin H (2007) Experimental transmission of Theileria sp. (China 1) infective for small ruminants by Haemaphysalis longicornis and Haemaphysalis qinghaiensis. Parasitol Res 101(3):533–538. https://doi.org/10.1007/s00436-007-0509-8
Li Y, Li X, Liu J, Wang J, Jia D, Liu A, He Z, Guan G, Liu Z, Liu G, Luo J, Yin H (2019) First report of Theileria infection of Bactrian camels (Camelus bactrianus) in Xinjiang, China. Acta Parasitol 64(4):923–926. https://doi.org/10.2478/s11686-019-00086-0
Liu Q, Zhou YQ, He GS, Oosthuizen MC, Zhou DN, Zhao JL (2010) Molecular phylogenetic studies on Theileria spp. isolates (China) based on small subunit ribosomal RNA gene sequences. Trop Anim Health Prod 42(1):109–114. https://doi.org/10.1007/s11250-009-9392-x
Luo J, Yin H (1997) Theileriosis of sheep and goats in China. Trop Anim Health Prod 29(4 Suppl):8S–10S. https://doi.org/10.1007/bf02632907
Mamatha GS (2017) Molecular epidemiology and phylogenetic characterization of Theileria luwenshuni in India: a first report. Small Rumin Res 154(17):52–57. https://doi.org/10.1016/j.smallrumres.2017.07.003
Moorhouse DE, Tatchell RJ (1966) The feeding processes of the cattle-tick Boophilus microplus (Canestrini): a study in host-parasite relations. I Attachment to the host. Parasitology 56(4):623–632. https://doi.org/10.1017/s003118200007164x
Osterkamp J, Wahl U, Schmalfuss G, Haas W (1999) Host-odour recognition in two tick species is coded in a blend of vertebrate volatiles. J Comp Physiol A 185(1):59–67. https://doi.org/10.1007/s003590050366
Phipps LP, Hernandez-Triana LM, Goharriz H, Welchman D, Johnson N (2016) Detection of Theileria luwenshuni in sheep from Great Britain. Parasit Vectors 9:203. https://doi.org/10.1186/s13071-016-1486-5
Qin G, Li Y, Liu J, Liu Z, Yang J, Zhang L, Liu G, Guan G, Luo J, Yin H (2016) Molecular detection and characterization of Theileria infection in cattle and yaks from Tibet plateau region, China. Parasitol Res 115(7):2647–2652. https://doi.org/10.1007/s00436-016-5011-8
Shimizu S, Nojiri K, Matsunaga N, Yamane I, Minami T (2000) Reduction in tick numbers (Haemaphysalis longicornis), mortality and incidence of Theileria sergenti infection in field-grazed calves treated with flumethrin pour-on. Vet Parasitol 92(2):129–138. https://doi.org/10.1016/s0304-4017(00)00278-8
Shiono H, Yagi Y, Thongnoon P, Kurabayashi N, Chikayama Y, Miyazaki S, Nakamura I (2001) Acquired methemoglobinemia in anemic cattle infected with Theileria sergenti. Vet Parasitol 102(1–2):45–51. https://doi.org/10.1016/s0304-4017(01)00520-9
Uilenberg G (2006) Babesia--a historical overview. Vet Parasitol 138(1–2):3–10. https://doi.org/10.1016/j.vetpar.2006.01.035
Wang J, Zhang J, Zhu Z, Zhou X, Li B (2018) Molecular phylogenetic studies on clinical bovine piroplasmosis caused by benign Theileria in Shaanxi Province, China. J Vet Sci 19(6):846–849. https://doi.org/10.4142/jvs.2018.19.6.846
Wang J, Liu J, Yang J, Wang X, Li Z, Jianlin X, Li X, Xiang Q, Li Y, Liu Z, Luo J, Guan G, Yin H (2019) The first molecular detection and genetic diversity of Babesia caballi and Theileria equi in horses of Gansu province, China. Ticks Tick Borne Dis 10(3):528–532. https://doi.org/10.1016/j.ttbdis.2019.01.003
Wise LN, Kappmeyer LS, Mealey RH, Knowles DP (2013) Review of equine piroplasmosis. J Vet Intern Med 27(6):1334–1346. https://doi.org/10.1111/jvim.12168
Yin H, Schnittger L, Luo J, Seitzer U, Ahmed JS (2007) Ovine theileriosis in China: a new look at an old story. Parasitol Res 101(Suppl 2):S191–S195. https://doi.org/10.1007/s00436-007-0689-2
Yin H, Liu Z, Guan G, Liu A, Ma M, Ren Q, Luo J (2008) Detection and differentiation of Theileria luwenshuni and T. uilenbergi infection in small ruminants by PCR. Transbound Emerg Dis 55(5–6):233–237. https://doi.org/10.1111/j.1865-1682.2008.01031.x
Acknowledgments
We thank colleagues (Center for Animal Disease Control and Prevention in Sichuan Province, Chengdu, China) for their kind assistance during the sample collection. We are grateful to the reviewers for their invaluable comments that contributed to improving this manuscript.
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This work was supported by funding from the National Key Research and Development Program of China (2017YFD0500400).
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This study was approved by the Animal Ethics Committee of Southwest Minzhu University (approval no. AECSWU2019-14).
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Hao, L., Yuan, D., Li, S. et al. Detection of Theileria spp. in ticks, sheep keds (Melophagus ovinus), and livestock in the eastern Tibetan Plateau, China. Parasitol Res 119, 2641–2648 (2020). https://doi.org/10.1007/s00436-020-06757-6
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DOI: https://doi.org/10.1007/s00436-020-06757-6