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Molecular evidence of tick-borne pathogens in Hyalomma anatolicum ticks infesting cattle in Xinjiang Uygur Autonomous Region, Northwestern China

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Abstract

Although tick-borne pathogens have been widely reported in ticks in China, there is little information available on the prevalence of information in Hyalomma ticks from cattle. This study aims to determine the occurrence of pathogens in Hyalomma anatolicum collected from cattle in Xinjiang Uygur Autonomous Region, China, by PCR, sequencing and phylogenetic analysis. Borrelia burgdorferi s.s., Rickettsia massiliae and Anaplasma bovis were identified, whereas DNA of Ehrlichia species and an Anaplasma platys-like pathogen were also detected. Our findings highlight the risk of infection of animals and humans with these pathogens in north-western China.

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References

  • Abdallah M, Niu Q, Yang J, Hassan M, Yu P, Guan G, Chen Z, Liu G, Luo J, Yin H (2017) Identification of 12 piroplasms infecting ten tick species in China using reverse line blot hybridization. J Parasitol. doi:10.1645/16-161

    PubMed  Google Scholar 

  • Ai C, Wen Y, Zhang Y, Wang S, Qiu G, Shi Z, Cheng Z, Li D, Liu X (1987) Epidemiological study on Lyme disease in Hailin of Heilongjiang. Chin Public Health 6:82–85

    Google Scholar 

  • Aktas M, Özübek S, Altay K, Ipek NDS, Balkaya İ, Utuk AE, Kırbas A, Şimsek S, Dumanlı N (2015) Molecular detection of tick-borne rickettsial and protozoan pathogens in domestic dogs from Turkey. Parasite Vector 1:1–6

    Google Scholar 

  • Barlough J, Madigan J, DeRock E, Bigornia L (1996) Nested polymerase chain reaction for detection of Ehrlichia equi genomic DNA in horses and ticks (Ixodes pacificus). Vet Parasitol 63:319–329

    Article  CAS  PubMed  Google Scholar 

  • Beata W, Agata L, Bogumila S (2010) A comparative analysis of molecular markers for the detection and identification of Borrelia spirochaetes in Ixodes ricinus. J Med Microbiol 59:309–314

    Article  Google Scholar 

  • Beati L, Raoult D (1993) Rickettsia massiliae sp. nov., a new spotted fever group rickettsia. Int J Syst Bacteriol 43:839–840

    Article  CAS  PubMed  Google Scholar 

  • Bhagwan J, Kumar A, Kumar R, Goyal L, Goel P, Kumar S (2015) Molecular evidence of Theileria equi infection in Hyalomma anatolicum ticks infested on sero-positive Indian horses. Acta Parasitologica 60:322–329

    Article  CAS  PubMed  Google Scholar 

  • Biesiada G, Czepiel J, Lesniak MR, Garlicki A, Mach T (2012) Lyme disease: review. Arch Med Sci 8:978–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Zhang X, Ma J, Zhang Y, Qian J, Wei G (1988) Borrelia burgdorferi isolated from Ixodes persulatus in Xinjiang. Endem Dis Bull 4:004

    Google Scholar 

  • Chen Z, Yang X, Bu F, Yang X, Yang X, Liu J (2010) Ticks (acari: ixodoidea: argasidae, ixodidae) of China. Exp Appl Acarol 51:393–404

    Article  PubMed  Google Scholar 

  • Chu CY, Liu W, Jiang BG, Wang DM, Jiang WJ, Zhao QM, Zhang PH, Wang ZX, Tang GP, Yang H (2008) Novel genospecies of Borrelia burgdorferi sensu lato from rodents and ticks in southwestern China. J Clin Microbiol 46:3130–3133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de la Fuente J, Torina A, Naranjo V, Nicosia S, Alongi A, La Mantia F, Kocan KM (2006) Molecular characterization of Anaplasma platys strains from dogs in Sicily, Italy. BMC Vet Res 2:1–5

    Article  Google Scholar 

  • Dong X, Chen XP, Liu N, Dumler SJ, Zhang YZ (2014) Co-circulation of multiple species of Rickettsiales bacteria in one single species of hard ticks in Shenyang, China. Ticks Tick Borne Dis 5:727–733

    Article  PubMed  Google Scholar 

  • Dumler JS, Bakken JS (1995) Ehrlichial diseases of humans: emerging tick-borne infections. Clin Infect Dis 20:1102–1110

    Article  CAS  PubMed  Google Scholar 

  • Dumler JS, Barbet AF, Bekker C, Dasch GA, Palmer GH, Ray SC, Rikihisa Y, Rurangirwa FR (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. Int J Syst Evol Microbiol 51:2145–2165

    Article  CAS  PubMed  Google Scholar 

  • Fang LQ, Liu K, Li XL, Liang S, Yang Y, Yao HW, Sun RX, Sun Y, Chen WJ, Zuo SQ (2015) Emerging tick-borne infections in mainland China: an increasing public health threat. Lancet Infect Dis 15:1467–1479

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernández de Mera I, Zivkovic Z, Bolaños M, Carranza C, Pérez-Arellano J, Gutiérrez C (2009) Rickettsia massiliae in the Canary Islands. Emerg Infect Dis 15:1869–1870

    Article  PubMed  PubMed Central  Google Scholar 

  • Guan G, Ma M, Moreau E, Liu J, Lu B, Bai Q, Luo J, Jorgensen W, Chauvin A, Yin H (2009) A new ovine Babesia species transmitted by Hyalomma anatolicum anatolicum. Exp Parasitol 122:261–267

    Article  PubMed  Google Scholar 

  • Hao Q, Hou X, Geng Z, Wan K (2011) Distribution of Borrelia burgdorferi sensu lato in China. J Clin Microbiol 49:647–650

    Article  PubMed  PubMed Central  Google Scholar 

  • Haque M, Singh N, Rath S (2010) Prevalence of Theileria annulata infection in Hyalomma anatolicum anatolicum in Punjab state, India. J Parasit Dis 34:48–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey JW, Simpson CF, Gaskin JM (1978) Cyclic thrombocytopenia induced by a Rickettsia-like agent in dogs. J Infect Dis 137:182–188

    Article  CAS  PubMed  Google Scholar 

  • Kang YJ, Diao XN, Zhao GY, Chen MH, Xiong Y, Shi M, Fu WM, Guo YJ, Pan B, Chen XP (2014) Extensive diversity of Rickettsiales bacteria in two species of ticks from China and the evolution of the Rickettsiales. BMC Evol Biol 14:167

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawahara M, Rikihisa Y, Lin Q, Isogai E, Tahara K, Itagaki A, Hiramitsu Y, 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. Appl Environ Microb 72:1102–1109

    Article  CAS  Google Scholar 

  • Lane R, Piesman J, Burgdorfer W (1991) Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Ann Rev Entomol 36:587–609

    Article  CAS  Google Scholar 

  • Li Y, Chen Z, Liu Z, Liu J, Yang J, Li Q, Li Y, Luo J, Yin H (2015) Molecular survey of Anaplasma and Ehrlichia of red deer and sika deer in Gansu, China in 2013. Transbound Emerg Dis 63:e228–e236

    Article  PubMed  Google Scholar 

  • Liu Z, Ma M, Wang Z, Wang J, Peng Y, Li Y, Guan G, Luo J, Yin H (2012) Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Appl Environ Microbiol 78:464–470

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu H, Li Q, Zhang X, Li Z, Wang Z, Song M, Wei F, Wang S, Liu Q (2016) Characterization of rickettsiae in ticks in northeastern China. Parasite Vector 1:1–9

    Google Scholar 

  • Luo J, Chen F, Lu W, Guan G, Ma M, Yin H (2003) Experimental transmission of an unnamed bovine Babesia by Hyalomma spp., Haemaphysalis longicornis and Boophilus microplus. Vet Parasitol 116:115–124

    Article  PubMed  Google Scholar 

  • Margos G, Wilske B, Sing A, Hizoteufel C, Cao WC, Chu C, Scholz H, Straubinger RK, Fingerle V (2013) Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia. Int J Syst Evol Microbiol 63:4284–4288

    Article  PubMed  Google Scholar 

  • Margos G, Chu CY, Takano A, Jiang BG, Liu W, Kurtenbach K, Masuzawa T, Fingerle V, Cao WC, Kawabata H (2015) Borrelia yangtzensis sp. nov., a rodent-associated species in Asia, is related to Borrelia valaisiana. Int J Syst Evol Microbiol 65:3836–3840

    Article  CAS  PubMed  Google Scholar 

  • Masuzawa T, Takada N, Kudeken M, Fukui T, Yano Y, Ishiguro F, Kawamura Y, Imai Y, Ezaki T (2001) Borrelia sinica sp. nov., a Lyme disease-related Borrelia species isolated in China. Int J Syst Evol Microbiol 51:1817–1824

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto K, Ogawa M, Brouqui P, Raoult D, Parola P (2005) Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus. Med Vet Entomol 19:263–270

    Article  CAS  PubMed  Google Scholar 

  • Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702

    Article  PubMed  PubMed Central  Google Scholar 

  • Postic D, Assous MV, Grimont PAD, Baranton G (1994) Diversity of Borrelia burgdorfeii sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. Int J Syst Evol Microbiol 44:743–752

    CAS  Google Scholar 

  • Raoult D, Roux V (1997) Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev 10:694–719

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rar V, Golovljova I (2011) Anaplasma, Ehrlichia, and “Candidatus Neoehrlichia” bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect Genet Evol 11:1842–1861

    Article  CAS  PubMed  Google Scholar 

  • Regnery RL, Spruill CL, Plikaytis B (1991) Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol 173:1576–1589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rose J, Nachum-Biala Y, Mumcuoglu K, Alkhamis M, Ben-Nun A, Lensky I, Klement E, Nasereddin A, Abdeen Z, Harrus S (2017) Genetic characterization of spotted fever group rickettsiae in questing ixodid ticks collected in Israel and environmental risk factors for their infection. Parasitology. doi:10.1017/S0031182017000336

    PubMed  Google Scholar 

  • Schwartz J, Gazumyan A, Schwartz I (1992) rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi. J Bacteriol 174:3757–3765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sreekumar C, Anandan R, Balasundaram S, Rajavelu G (1996) Morphology and staining characteristics of Ehrlichia bovis. Comp Immunol Microbiol Infect Dis 19:79–83

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Xu R, Cao W (2003) Ixodes sinensis: competence as a vector to transmit the Lyme disease spirochete Borrelia garinii. Vector Borne Zoonotic Dis 3:39–44

    Article  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng K, Jiang Z (1991) Economic insect fauna of China Fasc 39 Acari: Ixodidae. Science, Beijing, pp 52–349

    Google Scholar 

  • Tian ZC, Liu GY, Shen H, Xie JR, Luo J, Tian MY (2012) First report on the occurrence of Rickettsia slovaca and Rickettsia raoultii in Dermacentor silvarum in China. Parasite Vector 5:1–4

    Article  Google Scholar 

  • Vitale G, Mansuelo S, Rolain JM, Raoult D (2006) Rickettsia massiliae human isolation. Emerg Infect Dis 12:174–175

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang YZ, Mu LM, Zhan K, Yang MH, Zhang L, Du JY, Liu ZQ, Li YX, Lu WH, Chen CF (2015) A broad-range survey of ticks from livestock in Northern Xinjiang: changes in tick distribution and the isolation of Borrelia burgdorferi sensu stricto. Parasite Vector 8:1–9

    Article  Google Scholar 

  • Wei QQ, Guo LP, Wang AD, Mu LM, Zhang K, Chen CF, Zhang WJ, Wang YZ (2015) The first detection of Rickettsia aeschlimannii and Rickettsia massiliae in Rhipicephalus turanicus ticks, in northwest China. Parasite Vector 8:1–4

    Article  CAS  Google Scholar 

  • Wen B, Cao W, Pan H (2003) Ehrlichiae and ehrlichial diseases in China. Ann NY Acad Sci 990:45–53

    Article  CAS  PubMed  Google Scholar 

  • Wodecka B (2006) Significance of red deer (Cervus elaphus) in the ecology of Borrelia burgdorferi sensu lato. Wiad Parazytol 53:231–237

    Google Scholar 

  • Wu Q (2014) Study on pathogenic characteristics and transmission vectors of Borrelia garinii SZ. Chinese Academy of Agricultural Sciences

  • Yang J, Li Y, Liu Z, Guan G, Chen Z, Luo J, Wang X, Yin H (2014) Molecular evidence for Anaplasma bovis infection in wild Reeves’ Muntjac (Muntiacus reevesi), southwest China. J Wildlife Dis 50:982–985

    Article  Google Scholar 

  • Yang J, Li Y, Liu Z, Liu J, Niu Q, Ren Q, Chen Z, Guan G, Luo J, Yin H (2015) Molecular detection and characterization of Anaplasma spp. in sheep and cattle from Xinjiang, northwest China. Parasite Vector 1:1–7

    CAS  Google Scholar 

  • Yu PF, Niu QL, Liu ZJ, Yang JF, Chen Z, Guan GQ, Liu GY, Luo JX, Yin H (2016) Molecular epidemiological surveillance to assess emergence and re-emergence of tick-borne infections in tick samples from China evaluated by nested PCRs. Acta Trop 158:181–188

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported financially by The National Key Research and Development Program of China (2017YFD0501200); NSFC (Nos. 31502054, 31502091 and 31471967); ASTIP; NBCIS CARS-38; 973 Program (2015CB150300); and the Jiangsu Co-innovation Center Programme for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, State Key Laboratory of Veterinary Etiological Biology Project.

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Authors and Affiliations

  1. State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, 730046, Gansu, People’s Republic of China

    Peifa Yu, Zhijie Liu, Qingli Niu, Jifei Yang, Mirza Omar Abdallah, Ze Chen, Guangyuan Liu, Jianxun Luo & Hong Yin

  2. Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, People’s Republic of China

    Hong Yin

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  1. Peifa Yu
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  2. Zhijie Liu
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  3. Qingli Niu
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  4. Jifei Yang
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  5. Mirza Omar Abdallah
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Correspondence to Jianxun Luo or Hong Yin.

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Yu, P., Liu, Z., Niu, Q. et al. Molecular evidence of tick-borne pathogens in Hyalomma anatolicum ticks infesting cattle in Xinjiang Uygur Autonomous Region, Northwestern China. Exp Appl Acarol 73, 269–281 (2017). https://doi.org/10.1007/s10493-017-0162-6

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