Skip to main content Accessibility help

First molecular survey and identification of Anaplasma spp. in white yaks (Bos grunniens) in China



Anaplasmosis is caused by a group of obligate intracellular bacteria in the genus Anaplasma, which are transmitted by ticks and infect humans, domestic animals and wildlife. This study was conducted to determine the prevalence and molecular characterization of Anaplasma spp. in semi-wild white yaks sampled in Tianzhu Tibetan Autonomous County, northwest China. Out of 332 samples tested, 35 (10·9%) were positive for Anaplasma spp. The positive rates were 6·2% (20/322) and 5·3% (17/322) for Anaplasma bovis and Anaplasma phagocytophilum in white yaks, respectively. None of the sample was positive for Anaplasma marginale. Two (0·6%) samples were simultaneously positive to A. bovis and A. phagocytophilum. Sequence analysis of the 16S rRNA gene revealed two genotypes (ApG1 and ApG2) of A. phagocytophilum and two sequence types (ST1 and ST2) of A. bovis in white yaks. This study is the first to document the presence of Anaplasma in white yaks. Our findings extend the host range for Anaplasma species and provide more valuable information for the control and management of anaplasmosis in white yaks.


Corresponding author

*Corresponding authors: Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu, 730046, People's Republic of China. E-mail: and


Hide All
Aktas, M. and Ozubek, S. (2015). Bovine anaplasmosis in Turkey: first laboratory confirmed clinical cases caused by Anaplasma phagocytophilum . Veterinary Microbiology 178, 246251.
Aktas, M., Vatansever, Z., Altay, K., Aydin, M. F. and Dumanli, N. (2010). Molecular evidence for Anaplasma phagocytophilum in Ixodes ricinus from Turkey. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 1015.
Aktas, M., Altay, K. and Dumanli, N. (2011). Molecular detection and identification of Anaplasma and Ehrlichia species in cattle from Turkey. Ticks and Tick-borne Diseases 2, 6265.
Aktas, M., Altay, K., Ozubek, S. and Dumanli, N. (2012). A survey of ixodid ticks feeding on cattle and prevalence of tick-borne pathogens in the Black Sea region of Turkey. Veterinary Parasitology 187, 567571.
Altay, K., Dumanlı, N., Aktaş, M. and Özübek, S. (2014). Survey of anaplasma infections in small ruminants from East Part of Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi 20, 14.
Bai, Q., Chen, Z., Ying, S., Liu, G. and Zhou, J. (1987). Study on isolation and preservation of single species of haematocytozoon in bovine: separation of bovine A. marginale single isolate. Chinese Journal of Veterinary Science and Technology 3, 1215.
Baldridge, G. D., Scoles, G. A., Burkhardt, N. Y., Schloeder, B., Kurtti, T. J. and Munderloh, U. G. (2009). Transovarial transmission of Francisella-like endosymbionts and Anaplasma phagocytophilum variants in Dermacentor albipictus (Acari: Ixodidae). Journal of Medical Entomology 46, 625632.
Ben Said, M., Belkahia, H., Karaoud, M., Bousrih, M., Yahiaoui, M., Daaloul-Jedidi, M. and Messadi, L. (2015). First molecular survey of Anaplasma bovis in small ruminants from Tunisia. Veterinary Microbiology 179, 322326.
Bown, K. J., Lambin, X., Telford, G. R., Ogden, N. H., Telfer, S., Woldehiwet, Z. and Birtles, R. J. (2008). Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Applied and Environmental Microbiology 74, 71187125.
Brown, W. C. and Barbet, A. F. (2016). Persistent infections and immunity in ruminants to arthropod-borne bacteria in the family Anaplasmataceae. Annual Review of Animal Biosciences 4, 177197.
Cao, W. C., Zhao, Q. M., Zhang, P. H., Yang, H., Wu, X. M., Wen, B. H., Zhang, X. T. and Habbema, J. D. (2003). Prevalence of Anaplasma phagocytophila and Borrelia burgdorferi in Ixodes persulcatus ticks from northeastern China. American Journal of Tropical Medicine and Hygiene 68, 547550.
Ceci, L., Iarussi, F., Greco, B., Lacinio, R., Fornelli, S. and Carelli, G. (2014). Retrospective study of hemoparasites in cattle in southern Italy by reverse line blot hybridization. Journal of Veterinary Medical Science 76, 869875.
Chen, S. M., Dumler, J. S., Bakken, J. S. and Walker, D. H. (1994). Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. Journal of Clinical Microbiology 32, 589595.
de la Fuente, J., Van Den Bussche, R. A. and Kocan, K. M. (2001). Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Veterinary Parasitology 97, 6576.
Dumler, J. S., Barbet, A. F., Bekker, C. P., Dasch, G. A., Palmer, G. H., Ray, S. C., Rikihisa, Y. and Rurangirwa, F. R. (2001). Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila . International Journal of Systematic and Evolutionary Microbiology 51, 21452165.
Goethert, H. K. and Telford, S. R. III (2003). Enzootic transmission of the agent of human granulocytic ehrlichiosis among cottontail rabbits. American Journal of Tropical Medicine and Hygiene 68, 633637.
Jahfari, S., Coipan, E. C., Fonville, M., van Leeuwen, A. D., Hengeveld, P., Heylen, D., Heyman, P., van Maanen, C., Butler, C. M., Foldvari, G., Szekeres, S., van Duijvendijk, G., Tack, W., Rijks, J. M., van der Giessen, J., Takken, W., van Wieren, S. E., Takumi, K. and Sprong, H. (2014). Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasites and Vectors 7, 365.
Kawahara, M., Rikihisa, Y., Lin, Q., Isogai, E., Tahara, K., Itagaki, A., Hiramitsu, Y. and Tajima, T. (2006). Novel genetic variants of Anaplasma phagocytophilum, Anaplasma bovis, Anaplasma centrale, and a novel Ehrlichia sp. in wild deer and ticks on two major islands in Japan. Applied and Environmental Microbiology 72, 11021109.
Li, Y., Chen, Z., Liu, Z., Liu, J., Yang, J., Li, Q., Luo, J. and Yin, H. (2015). Molecular Survey of Anaplasma and Ehrlichia of Red Deer and Sika Deer in Gansu, China in 2013. Transboundary and Emerging Diseases, in press.
Liu, Z., Ma, M., Wang, Z., Wang, J., Peng, Y., Li, Y., Guan, G., Luo, J. and Yin, H. (2012). Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Applied and Environmental Microbiology 78, 464470.
Ooshiro, M., Zakimi, S., Matsukawa, Y., Katagiri, Y. and Inokuma, H. (2008). Detection of Anaplasma bovis and Anaplasma phagocytophilum from cattle on Yonaguni Island, Okinawa, Japan. Veterinary Parasitology 154, 360364.
Qin, S. Y., Huang, S. Y., Yin, M. Y., Tan, Q. D., Liu, G. X., Zhou, D. H., Zhu, X. Q., Zhou, J. Z. and Qian, A. D. (2015 a). Seroprevalence and risk factors of Chlamydia abortus infection in free-ranging white yaks in China. BMC Veterinary Research 11, 8.
Qin, S. Y., Wang, J. L., Ning, H. R., Tan, Q. D., Yin, M. Y., Zhang, X. X., Zhou, D. H. and Zhu, X. Q. (2015 b). First report of Babesia bigemina infection in white yaks in China. Acta Tropica 145, 5254.
Rar, V. and Golovljova, I. (2011). Anaplasma, Ehrlichia, and “Candidatus Neoehrlichia” bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infection, Genetics and Evolution 11, 18421861.
Rejmanek, D., Bradburd, G. and Foley, J. (2012). Molecular characterization reveals distinct genospecies of Anaplasma phagocytophilum from diverse North American hosts. Journal of Medical Microbiology 61, 204212.
Sakamoto, L., Ichikawa, Y., Sakata, Y., Matsumoto, K. and Inokuma, H. (2010). Detection of Anaplasma bovis DNA in the peripheral blood of domestic dogs in Japan. Japanese Journal of Infectious Diseases 63, 349352.
Stuen, S. (2007). Anaplasma phagocytophilum – the most widespread tick-borne infection in animals in Europe. Veterinary Research Communications 31, 7984.
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.
Tateno, M., Nishio, T., Sakuma, M., Nakanishi, N., Izawa, M., Asari, Y., Okamura, M., Maruyama, S., Miyama, T. S., Setoguchi, A. and Endo, Y. (2013). Molecular epidemiologic survey of Bartonella, Ehrlichia, and Anaplasma infections in Japanese Iriomote and Tsushima leopard cats. Journal of Wildlife Diseases 49, 646652.
Teglas, M. B. and Foley, J. (2006). Differences in the transmissibility of two Anaplasma phagocytophilum strains by the North American tick vector species, Ixodes pacificus and Ixodes scapularis (Acari: Ixodidae). Experimental and Applied Acarology 38, 4758.
Yang, J., Liu, Z., Guan, G., Liu, Q., Li, Y., Chen, Z., Ma, M., Liu, A., Ren, Q., Luo, J. and Yin, H. (2013). Prevalence of Anaplasma phagocytophilum in ruminants, rodents and ticks in Gansu, north-western China. Journal of Medical Microbiology 62, 254258.
Yang, J., Li, Y., Liu, Z., Guan, G., Chen, Z., Luo, J., Wang, X. and Yin, H. (2014). Molecular evidence for Anaplasma bovis infection in wild Reeves’ muntjac (Muntiacus reevesi), southwest China. Journal of Wildlife Diseases 50, 982985.
Yang, J., Li, Y., Liu, Z., Liu, J., Niu, Q., Ren, Q., Chen, Z., Guan, G., Luo, J. and Yin, H. (2015). Molecular detection and characterization of Anaplasma spp. in sheep and cattle from Xinjiang, northwest China. Parasites and Vectors 8, 108.
Zhang, L., Wang, Y., Cai, D., He, G., Cheng, Z., Liu, J., Meng, K., Yang, D. and Wang, S. (2013). Detection of Anaplasma marginale in Hyalomma asiaticum ticks by PCR assay. Parasitology Research 112, 26972702.
Zhou, Y., Hou, X. and Piao, F. Z. (2007). Detection of dairy cattle anaplasmosis and its application by PCR. Chinese Journal of Preventive Veterinary Medicine 29, 718722.



Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed