Abstract
To investigate the prevalence of Anaplasma, Ehrlichia, Bartonella and Theileria, we collected ticks from small mammals in six counties of Zhejiang Province in southeastern China. Polymerase chain reaction (PCR) amplification was performed to test Anaplasma, Ehrlichia, Bartonella and Theileria in tick samples. Positive PCR products were sequenced and then compared with previously published sequences deposited in GenBank using BLAST. About 292 adult ticks were captured and the dominant tick species were Ixodes sinensis and Haemaphysalis longicornis. Overall, 34 ticks (11.6%) were tested positive for at least one pathogen of Anaplasma, Ehrlichia, Bartonella and Theileria. Rates of PCR-positivity to Anaplasma, Ehrlichia, Bartonella and Theileria were 5.5, 1.7, 2.4 and 2.4%, respectively. Positive rates of Anaplasma, Bartonella and Theileria were significantly different among ticks of different species. Prevalence of Anaplasma and Theileria varied significantly among ticks of different counties. Anaplasma, Ehrlichia, Bartonella and Theileria were widely prevalent in ticks in Zhejiang Province suggesting other tick-borne pathogens should also be suspected if patients had history of tick bites.
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References
Bai HM, Yang FL, Yang H, Zhang Q (2005) Study on Bartonella species in rodents in western Yunnan, China. Chin J Epidemiol 26:868–870
Bai Y, Kosoy MY, Maupin GO, Gage KL, Dong XQ, Ma YK (2002) Discovery of Bartonella species in rodents in Yunnan. Chin J Zoon 18:5–9
Bown KJ, Begon M, Bennett M, Woldehiwet Z, Ogden NH (2003) Seasonal dynamics of Anaplasma phagocytophilum in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerg Infect Dis 9:63–70
Cao WC, Zhao QM, Zhang PH, Dumler JS, Zhang XT, Fang LQ, Yang H (2000a) Granulocytic Ehrlichiae in Ixodes persulcatus ticks from an area in China where Lyme disease is endemic. J Clin Microbiol 38:4208–4210
Cao WC, Gao YM, Zhang PH, Zhang XT, Dai QH, Dumler JS, Fang LQ, Yang H (2000b) Identification of Ehrlichia chaffeensis by nested PCR in ticks from Southern China. J Clin Microbiol 38:2778–2780
Casati S, Sager H, Gern L, Piffaretti JC (2006) Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med 13:65–70
Chen Z, Liu Q, Liu JQ, Xu BL, Lv S, Xia S, Zhou XN (2014) Tick-borne pathogens and associated co-infections in ticks collected from domestic animals in central China. Parasit Vector 7:737
Cumming GS (1998) Host preference in African ticks (Acari: Ixodia): a quantitative data set. Bull Entemol Res 88:379–406
Dantas-Torres F, Chomel BB, Otranto D (2012) Ticks and tick-borne diseases: a one Health perspective. Trends Parasitol 28:437–446
Dong T, Qu Z, Zhang L (2013) Detection of A. phagocytophilum and E. chaffeensis in patient and mouse blood and ticks by a duplex real-time PCR assay. PLoS ONE 8:e74796
Esser HJ, Herre EA, Blüthgen N, Loaiza JR, Bermudez SE, Janse P (2016) Host specificity in a diverse Neotropical tick community: an assessment using quantitative network analysis and host phylogeny. Parasit Vector 9:372
Fang LQ, Liu K, Li XL, Liang S, Yang Y, Yao HW, Sun RX, Sun Y, Chen WJ, Zuo SQ, Ma MJ, Li H, Jiang JF, Liu W, Yang XF, Gray GC, Krause PJ, Cao WC (2015) Emerging tick-borne infections in mainland China: an increasing public health threat. Lancet Infect Dis 15:1467–1479
Hou J, Ling F, Chai CL, Lu Y, Yu XH, Lin JF, Sun JM, Chang Y, Ye XD, Gu SP, Pang WL, Wang CW, Zheng XH, Jiang JM, Chen ZP, Gong ZY (2014) Prevalence of Borrelia burgdorferi Sensu Lato in Ticks from Eastern China. Am J Trop Med Hyg 92:262–266
Hu MX, Zhang J, Fan DH, Fu WM, Sun XF, Yang LW (2009) Detection of rodent infected by new tick pathogens in Suifenhe and Dongning Ports. Chin J Vector Biol Control 20:573–576
Kilpatrick AM, Randolph SE (2012) Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380:1946–1955
Li DM, Liu QY, Yu DZ, Zhang JZ, Gong ZD, Song XP (2007) Phylogenetic analysis of Bartonella detected in rodent fleas in Yunnan, China. J Wildlife Dis 43:609–617
Liu AH, Yin H, Guan GQ, Schnittger L, Liu ZJ, Ma ML, Dang ZS, Liu JL, Ren QY, Bai Q, Ahmed JS, Luo JX (2007) At least two genetically distinct large Babesia species infective to sheep and goats in China. Vet Parasitol 147:246–251
Liu QY, Sun JM, Lu L, Fu GM, Ding GQ, Song XP, Meng FX, Wu HX, Yang TC, Ren ZY, Chen EF, Lin JF, Lv HK, Chai CL (2010) Detection of Bartonella species in small mammals from Zhejiang Province, China. J Wildlife Dis 46:179–185
Luo J, Lu W (1997) Cattle theileriosis in China. Trop Anim Health Pro 29:4–7
Luo J, Yin H (1997) Theileriosis of sheep and goats in China. Trop Anim Health Pro 1997b 29:8–10
Qin XR, Han FJ, Luo LM, Zhao FM, Han HJ, Zhang ZT, Liu JW, Xue ZF, Liu MM, Ma DQ, Huang YT, Sun Y, Sun XF, Li WQ, Zhao L, Yu H, Yu XJ (2018) Anaplasma species detected in Haemaphysalis longicornis tick from China. Ticks Tick-borne Dis 9:840–843
Sun JM, Chai CL, Lv HK, Lin JF, Wang CW, Chen EF, Zhang YJ, Chen ZP, Liu SL, Gong ZY, Jiang JM (2014) Epidemiological characteristics of severe fever with thrombocytopenia syndrome in Zhejiang Province, China. Int J Infect Dis 25:180–185
Sun JM, Lin JF, Gong ZY, Chang Y, Ye XD, Gu SP, Pang WL, Wang CW, Zheng XH, Hou J, Ling F, Shi XG, Jiang JM, Chen ZP, Lv HK, Chai CL (2015) Detection of spotted fever group Rickettsiae in ticks from Zhejiang Province, China. Exp Appl Acarol 65:403–411
Sun JM, Liu QY, Lu L, Ding GQ, Guo JQ, Fu GM, Zhang JB, Meng FX, Wu HX, Song XP, Ren DS, Li DM, Guo YH, Wang J, Li GC, Liu JL, Lin HL (2008) Coinfection with four genera of bacteria (Borrelia, Bartonella, Anaplasma, and Ehrlichia. in Haemaphysalis longicornis and Ixodes sinensis ticks from China. Vector-Borne Zoonot Dis 8:791–795
Sun X, Zhang GL, Liu XM, Zhao Y, Zheng Z (2013) Investigation of tick species and tick-borne pathogens in Hoxud County of Xinjiang Uyghur Autonomous Region, China. Chin J Vector Biol Control 2013 24:5–10
Teng K, Jiang Z (1991) Economic insect fauna of Chinese Fasc 39 Acari: Ixodidae. Science Press, Beijing
Unsworth NB, Stenos J, Graves SR, Faa AG, Cox GE, John RD, Boutlis CS, Lane AM, Shaw MD, Robson J, Nissen MD (2007) Flinders Island spotted fever rickettsioses caused by “marmionii” strain of Rickettsia honei, Eastern Australia". Emerg Infect Dis 13:566–573
Wielinga PR, Gaasenbeek C, Fonville M, Deboer A, Vries AD, Dimmers W, Jages GAO, Schouls LM, Borgsteede F, van der Giessen JWB (2006) Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Appl Environ Microb 72:7594–7601
Yang JF, Liu ZJ, Guan GQ, Liu Q, Li YQ, Chen Z, Ma ML, Liu AH, Ren QY, Luo JX, Yin H (2013) Prevalence of Anaplasma phagocytophilum in ruminants, rodents and ticks in Gansu, northwestern China. J Clin Microbiol 62:254–258
Yin H, Luo J, Guan G, Gao Y, Lu B, Zhang Q, Ma M, Lu W, Lu C, Yuan Z, Guo S, Wang B, Du H, Schnittger L, Ahmed J, Jongejan F (2002) Transmission of an unidentified Theileria species to small ruminants by Haemaphysalis qinghaiensis ticks collected in the field. Parasitol Res 88:25–27
Yin H, Schnittger L, Luo J, Seitzer U, Ahmed JS (2007) Ovine theileriosis in China: a new look at an old story. Parasitol Res 101:191–195
Ying B, Kosoy MY, Maupin GO, Tsuchiya KR, Gage KL (2002) Genetic and ecologic characteristics of Bartonella communities in rodents in southern China. Am J Trop Med 66:622–627
Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, Zhang L, Zhang QF, Popov VL, Li C, Qu J, Li Q, Zhang YP, Hai R, Wu W, Wang Q, Zhan FX, Wang XJ, Kan B, Wang SW, Wan KL, Jing HQ, Lu JX, Yin WW, Zhou H, Guan XH, Liu JF, Bi ZQ, Liu GH, Ren J, Wang H, Zhao Z, Song JD, He JR, Wan T, Zhang JS, Fu XP, Sun LN, Dong XP, Feng ZJ, Yang WZ, Hong T, Zhang Y, Walker DH, Wang Y, Li DX (2011) Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 364:1523–1532
Zhang L, Cui F, Wang L, Zhang LL, Zhang JS, Wang SW, Yang SX (2011) Investigation of anaplasmosis in Yiyuan County, Shandong Province, China. Asian Pac J Trop Med 4:568–572
Zhang LJ, Liu H, Xu BL, Lu QY, Li L, Chang LT, Zhang XC, Fan DS, Li GH, Jin YM, Cui F, Shi YL, Li WH, Xu JG, Yu XJ (2012) Anaplasma phagocytophilum infection in domestic animals in ten provinces/cities of China. Am J Trop Med Hyg 87:185–189
Zhao QL, Huang L, Yang X, Meng QL, Li R, Chen PB, Duan XD, Sheng JL (2013) 16 s rRNA sequence analysis of Anaplasma and Ehrlichia in rodents from parts area of Xinjiang. Chin J Zoon 29:743–747
Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS (2003) Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Microbiol Rev 16:622–636
Zou YX, Jin HT, Wang QY, Fu ZX, Gao HW, Liu PP, Liu Q, Chen LF (2011) Molecular detection of Anaplasma phagocytophilum in Ixodid Ticks in Hebei Province, China. Vector-borne Zoonot Dis 11(10):1323–1327
Funding
This study was supported by National Natural Science Funds of China (Grant No. 81872675), Medical Research Program of Zhejiang Province (Grant Nos. 2017KY291, 2018KY338) and the State Project for Scientific & Technological Development of the 13th Five-year Plan in China (Grant No. 2017ZX10303404008002).
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Hou, J., Ling, F., Liu, Y. et al. A molecular survey of Anaplasma, Ehrlichia, Bartonella and Theileria in ticks collected from southeastern China. Exp Appl Acarol 79, 125–135 (2019). https://doi.org/10.1007/s10493-019-00411-2
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DOI: https://doi.org/10.1007/s10493-019-00411-2