{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T17:04:40Z","timestamp":1789578280143,"version":"build-2803163510"},"reference-count":56,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,7,22]],"date-time":"2020-07-22T00:00:00Z","timestamp":1595376000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,7,22]],"date-time":"2020-07-22T00:00:00Z","timestamp":1595376000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31700159"],"award-info":[{"award-number":["31700159"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81702008"],"award-info":[{"award-number":["81702008"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Key discipline construction of colleges and universities in Hebei Province","award":["Ji Jiao Gao No. [2013]4"],"award-info":[{"award-number":["Ji Jiao Gao No. [2013]4"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasites Vectors"],"published-print":{"date-parts":[[2020,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n<jats:title>Background<\/jats:title>\n<jats:p>Several members of genus <jats:italic>Babesia<\/jats:italic> are important pathogens causing babesiosis in dogs. In China, at least five <jats:italic>Babesia<\/jats:italic> species have been described in dogs or ticks. This study sought to determine the prevalence and molecular characteristics of various <jats:italic>Babesia<\/jats:italic> spp. in dogs in cities in Shaanxi Province in China, including Xi\u2019an and Hanzhong.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Methods<\/jats:title>\n<jats:p>A total of 371 blood samples were collected from pet dogs presenting to veterinary clinics in the cities of Xi\u2019an and Hanzhong in Shaanxi, China. <jats:italic>Babesia<\/jats:italic> spp. DNA was detected <jats:italic>via<\/jats:italic> amplification of partial <jats:italic>18S<\/jats:italic> rRNA genes by semi-nested PCR. Almost full-length <jats:italic>18S<\/jats:italic> rRNA, ITS, partial <jats:italic>TRAP<\/jats:italic> and complete <jats:italic>cytb<\/jats:italic> genes were recovered for analysis of the genetic characteristics and relationships with known isolates.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Results<\/jats:title>\n<jats:p>A single species, <jats:italic>Babesia gibsoni<\/jats:italic>, was identified in dogs in Xi\u2019an and Hanzhong. Consistently, <jats:italic>B. gibsoni<\/jats:italic> was also detected in 14 ticks collected from positive dogs. Sequence similarities and phylogenetic analysis suggested that the isolates identified herein showed a closer genetic relationship with isolates from East Asian countries rather than India, Bangladesh, or the USA. Sequence analysis based on tandem repeat analysis of the <jats:italic>TRAP<\/jats:italic> gene further revealed that specific haplotypes were circulating in both Xi\u2019an and Hanzhong, with no specific regionality. In addition, 10.9% of all isolates with atovaquone (ATV)-resistance were identified because of M121I mutation in the deduced cytb protein.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Conclusions<\/jats:title>\n<jats:p>This study revealed a high prevalence rate of <jats:italic>Babesia<\/jats:italic> infection. <jats:italic>Babesia gibsoni<\/jats:italic> was the only <jats:italic>Babesia<\/jats:italic> species identified in cases of canine babesiosis in the cities of Xi\u2019an and Hanzhong cities in Shaanxi, China. In addition, the <jats:italic>TRAP<\/jats:italic> gene presented high genetic diversity across isolates. Such information is useful for elucidating the epidemiological characteristics of canine babesiosis, as well as the overall genetic diversity of <jats:italic>Babesia<\/jats:italic> spp. circulating in dog populations in Shaanxi Province.<\/jats:p>\n<\/jats:sec>","DOI":"10.1186\/s13071-020-04232-w","type":"journal-article","created":{"date-parts":[[2020,7,22]],"date-time":"2020-07-22T12:03:38Z","timestamp":1595419418000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Molecular detection and genetic characteristics of Babesia gibsoni in dogs in Shaanxi Province, China"],"prefix":"10.1186","volume":"13","author":[{"given":"Wen-Ping","family":"Guo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guang-Cheng","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dan","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng","family":"Su","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rui","family":"Jian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luan-Ying","family":"Du","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,7,22]]},"reference":[{"key":"4232_CR1","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.vetpar.2011.04.023","volume":"181","author":"L Solano-Gallego","year":"2011","unstructured":"Solano-Gallego L, Baneth G. Babesiosis in dogs and cats\u2014expanding parasitological and clinical spectra. Vet Parasitol. 2011;181:48\u201360.","journal-title":"Vet Parasitol."},{"key":"4232_CR2","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/j.pt.2012.07.003","volume":"28","author":"F Dantas-Torres","year":"2012","unstructured":"Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: a one health perspective. Trends Parasitol. 2012;28:437\u201346.","journal-title":"Trends Parasitol."},{"key":"4232_CR3","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.vetpar.2018.03.001","volume":"254","author":"G Baneth","year":"2018","unstructured":"Baneth G. Antiprotozoal treatment of canine babesiosis. Vet Parasitol. 2018;254:58\u201363.","journal-title":"Vet Parasitol."},{"key":"4232_CR4","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1292\/jvms.15-0079","volume":"77","author":"S Kubo","year":"2015","unstructured":"Kubo S, Tateno M, Ichikawa Y, Endo Y. A molecular epidemiological survey of Babesia, Hepatozoon, Ehrlichia and Anaplasma infections of dogs in Japan. J Vet Med Sci. 2015;77:1275\u20139.","journal-title":"J Vet Med Sci."},{"key":"4232_CR5","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.vetpar.2007.10.022","volume":"151","author":"LE Lehtinen","year":"2008","unstructured":"Lehtinen LE, Birkenheuer AJ, Droleskey RE, Holman PJ. In vitro cultivation of a newly recognized Babesia sp. in dogs in North Carolina. Vet Parasitol. 2008;151:150\u20137.","journal-title":"Vet Parasitol."},{"key":"4232_CR6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.vetpar.2016.11.016","volume":"233","author":"S Ozubek","year":"2017","unstructured":"Ozubek S, Aktas M. Molecular evidence of a new Babesia sp. in goats. Vet Parasitol. 2017;233:1\u20138.","journal-title":"Vet Parasitol."},{"key":"4232_CR7","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1016\/j.ijpara.2005.03.018","volume":"35","author":"S Fukumoto","year":"2005","unstructured":"Fukumoto S, Suzuki H, Igarashi I, Xuan X. Fatal experimental transplacental Babesia gibsoni infections in dogs. Int J Parasitol. 2005;35:1031\u20135.","journal-title":"Int J Parasitol."},{"key":"4232_CR8","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1111\/j.1751-0813.2007.00220.x","volume":"85","author":"R Jefferies","year":"2007","unstructured":"Jefferies R, Ryan UM, Jardine J, Broughton DK, Robertson ID, Irwin PJ. Blood, bull terriers and Babesiosis: further evidence for direct transmission of Babesia gibsoni in dogs. Aust Vet J. 2007;85:459\u201363.","journal-title":"Aust Vet J."},{"key":"4232_CR9","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.vetpar.2014.01.022","volume":"203","author":"B V\u00edchov\u00e1","year":"2014","unstructured":"V\u00edchov\u00e1 B, Miterp\u00e1kov\u00e1 M, Igl\u00f3dyov\u00e1 A. Molecular detection of co-infections with Anaplasma phagocytophilum and\/or Babesia canis canis in Dirofilaria-positive dogs from Slovakia. Vet Parasitol. 2014;203:167\u201372.","journal-title":"Vet Parasitol."},{"issue":"Suppl. 1","key":"4232_CR10","doi-asserted-by":"crossref","first-page":"S4","DOI":"10.1186\/1756-3305-2-S1-S4","volume":"2","author":"PJ Irwin","year":"2009","unstructured":"Irwin PJ. Canine babesiosis: from molecular taxonomy to control. Parasit Vectors. 2009;2(Suppl. 1):S4.","journal-title":"Parasit Vectors."},{"key":"4232_CR11","doi-asserted-by":"crossref","first-page":"59","DOI":"10.4102\/ojvr.v76i1.66","volume":"76","author":"JP Schoeman","year":"2009","unstructured":"Schoeman JP. Canine babesiosis. Onderstepoort J Vet Res. 2009;76:59\u201366.","journal-title":"Onderstepoort J Vet Res."},{"key":"4232_CR12","doi-asserted-by":"crossref","first-page":"1788","DOI":"10.1016\/j.meegid.2012.07.004","volume":"12","author":"L Schnittger","year":"2012","unstructured":"Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: a world emerging. Infect Genet Evol. 2012;12:1788\u2013809.","journal-title":"Infect Genet Evol."},{"key":"4232_CR13","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.vetpar.2006.01.047","volume":"138","author":"LS Jacobson","year":"2006","unstructured":"Jacobson LS. The South African form of severe and complicated canine babesiosis: clinical advances 1994\u20132004. Vet Parasitol. 2006;138:126\u201339.","journal-title":"Vet Parasitol."},{"key":"4232_CR14","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1186\/s13071-016-1596-0","volume":"9","author":"L Solano-Gallego","year":"2016","unstructured":"Solano-Gallego L, Sainz \u00c1, Roura X, Estrada-Pe\u00f1a A, Mir\u00f3 G. A review of canine babesiosis: the European perspective. Parasit Vectors. 2016;9:336.","journal-title":"Parasit Vectors."},{"key":"4232_CR15","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.3389\/fmicb.2017.01577","volume":"8","author":"L He","year":"2017","unstructured":"He L, Miao X, Hu J, Huang Y, He P, He J, et al. First molecular detection of Babesia gibsoni in dogs from Wuhan, China. Front Microbiol. 2017;8:1577.","journal-title":"Front Microbiol."},{"key":"4232_CR16","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.meegid.2017.11.017","volume":"56","author":"HR Lin","year":"2017","unstructured":"Lin HR, Mei XT, Hong YF, Zhao YB, Guo XN, Yang DJ, et al. Sequence analysis of the thrombospondin-related adhesive protein gene and heat shock protein 70 gene of Babesia gibsoni isolated from dogs in Nanjing, China. Infect Genet Evol. 2017;56:111\u20136.","journal-title":"Infect Genet Evol."},{"key":"4232_CR17","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1292\/jvms.10-0093","volume":"72","author":"CC Lee","year":"2010","unstructured":"Lee CC, Hsieh YC, Huang CC, Tsang CL, Chung YT. Sequence and phylogenetic analysis of the thrombospondin-related adhesive protein (TRAP) gene of Babesia gibsoni isolates from dogs in Taiwan. J Vet Med Sci. 2010;72:1329\u201335.","journal-title":"J Vet Med Sci."},{"key":"4232_CR18","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1089\/vbz.2010.0265","volume":"11","author":"SS Wong","year":"2011","unstructured":"Wong SS, Teng JL, Poon RW, Choi GK, Chan KH, Yeung ML, et al. Comparative evaluation of a point-of-care immunochromatographic test SNAP 4Dx with molecular detection tests for vector-borne canine pathogens in Hong Kong. Vector Borne Zoonotic Dis. 2011;11:1269\u201377.","journal-title":"Vector Borne Zoonotic Dis."},{"key":"4232_CR19","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1186\/s13071-015-1120-y","volume":"8","author":"D Xu","year":"2015","unstructured":"Xu D, Zhang J, Shi Z, Song C, Zheng X, Zhang Y, et al. Molecular detection of vector-borne agents in dogs from ten provinces of China. Parasit Vectors. 2015;8:501.","journal-title":"Parasit Vectors."},{"key":"4232_CR20","first-page":"163","volume":"9","author":"DW Yao","year":"2014","unstructured":"Yao DW, Jiang JY, Yu ZZ, Yao DQ, Yang DJ, Zhao YB. Canine babesiosis in China caused by Babesia gibsoni: a molecular approach. Iran J Parasitol. 2014;9:163\u20138.","journal-title":"Iran J Parasitol."},{"key":"4232_CR21","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.3389\/fmicb.2017.01029","volume":"8","author":"Q Niu","year":"2017","unstructured":"Niu Q, Yang J, Liu Z, Gao S, Pan Y, Guan G, et al. First molecular detection of piroplasm infection in pet dogs from Gansu, China. Front Microbiol. 2017;8:1029.","journal-title":"Front Microbiol."},{"key":"4232_CR22","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1292\/jvms.16-0484","volume":"79","author":"W Zheng","year":"2017","unstructured":"Zheng W, Liu M, Moumouni PF, Liu X, Efstratiou A, Liu Z, et al. First molecular detection of tick-borne pathogens in dogs from Jiangxi, China. J Vet Med Sci. 2017;79:248\u201354.","journal-title":"J Vet Med Sci."},{"key":"4232_CR23","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1186\/1756-3305-7-237","volume":"7","author":"Z Chen","year":"2014","unstructured":"Chen Z, Liu Q, Liu JQ, Xu BL, Lv S, Xia S, et al. Tick-borne pathogens and associated co-infections in ticks collected from domestic animals in central China. Parasit Vectors. 2014;7:237.","journal-title":"Parasit Vectors."},{"key":"4232_CR24","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.parint.2019.03.011","volume":"71","author":"J Wang","year":"2019","unstructured":"Wang J, Liu J, Yang J, Liu Z, Wang X, Li Y, et al. Molecular detection and genetic diversity of Babesia canis canis in pet dogs in Henan Province, China. Parasitol Int. 2019;71:37\u201340.","journal-title":"Parasitol Int."},{"key":"4232_CR25","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1111\/tbed.12894","volume":"65","author":"R Song","year":"2018","unstructured":"Song R, Wang Q, Guo F, Liu X, Song S, Chen C, et al. Detection of Babesia spp., Theileria spp. and Anaplasma ovis in Border Regions, northwestern China. Transbound Emerg Dis. 2018;65:1537\u201344.","journal-title":"Transbound Emerg Dis."},{"key":"4232_CR26","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1016\/j.ttbdis.2019.01.003","volume":"10","author":"J Wang","year":"2019","unstructured":"Wang J, Liu J, Yang J, Wang X, Li Z, Jianlin X, et al. The first molecular detection and genetic diversity of Babesia caballi and Theileria equi in horses of Gansu province, China. Ticks Tick Borne Dis. 2019;10:528\u201332.","journal-title":"Ticks Tick Borne Dis."},{"key":"4232_CR27","first-page":"251","volume":"18","author":"Y Sun","year":"2011","unstructured":"Sun Y, Xu RM, We CC. Haemaphysalis ticks (Ixodoidea, Ixodidae) in China-systematic and key to subgenera. Acta Parasitology Et Medica Entomologica Sinica. 2011;18:251\u20138.","journal-title":"Acta Parasitology Et Medica Entomologica Sinica"},{"key":"4232_CR28","first-page":"294","volume":"3","author":"O Folmer","year":"1994","unstructured":"Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294\u20139.","journal-title":"Mol Mar Biol Biotechnol"},{"key":"4232_CR29","doi-asserted-by":"crossref","first-page":"1708","DOI":"10.3201\/eid1111.041195","volume":"11","author":"VA Rar","year":"2005","unstructured":"Rar VA, Fomenko NV, Dobrotvorsky AK, Livanova NN, Rudakova SA, Fedorov EG, et al. Tickborne pathogen detection, western Siberia, Russia. Emerg Infect Dis. 2005;11:1708.","journal-title":"Emerg Infect Dis."},{"key":"4232_CR30","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.meegid.2015.01.011","volume":"31","author":"M Terao","year":"2015","unstructured":"Terao M, Akter S, Yasin MG, Nakao R, Kato H, Alam MZ, et al. Molecular detection and genetic diversity of Babesia gibsoni in dogs in Bangladesh. Infect Genet Evol. 2015;31:53\u201360.","journal-title":"Infect Genet Evol."},{"key":"4232_CR31","doi-asserted-by":"crossref","first-page":"3144","DOI":"10.1093\/bioinformatics\/bts578","volume":"28","author":"K Katoh","year":"2012","unstructured":"Katoh K, Frith MC. Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics. 2012;28:3144\u20136.","journal-title":"Bioinformatics."},{"key":"4232_CR32","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/978-1-59745-251-9_5","volume":"537","author":"D Posada","year":"2009","unstructured":"Posada D. Selection of models of DNA evolution with jModelTest. Methods Mol Biol. 2009;537:93\u2013112.","journal-title":"Methods Mol Biol."},{"key":"4232_CR33","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","volume":"33","author":"S Kumar","year":"2016","unstructured":"Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870\u20134.","journal-title":"Mol Biol Evol."},{"key":"4232_CR34","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1093\/nar\/27.2.573","volume":"27","author":"G Benson","year":"1999","unstructured":"Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27:573\u201380.","journal-title":"Nucleic Acids Res."},{"key":"4232_CR35","doi-asserted-by":"crossref","first-page":"D80","DOI":"10.1093\/nar\/gkl1013","volume":"35","author":"Y Gelfand","year":"2007","unstructured":"Gelfand Y, Rodriguez A, Benson G. TRDB\u2014the Tandem Repeats Database. Nucleic Acids Res. 2007;35:D80\u20137.","journal-title":"Nucleic Acids Res."},{"issue":"185","key":"4232_CR36","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.vetpar.2011.09.031","volume":"2012","author":"A Iguchi","year":"2012","unstructured":"Iguchi A, Matsuu A, Ikadai H, Hasanuzzaman Talukder M, Hikasa Y. Development of in vitro atovaquone-resistant Babesia gibsoni with a single-nucleotide polymorphism in cytb. Vet. Parasitol. 2012;2012(185):145\u201350.","journal-title":"Vet. Parasitol."},{"key":"4232_CR37","doi-asserted-by":"crossref","first-page":"593","DOI":"10.4269\/ajtmh.2006.74.593","volume":"74","author":"A Matsuu","year":"2006","unstructured":"Matsuu A, Miyamoto K, Ikadai H, Okano S, Higuchi S. Cloning of the Babesia gibsoni cytochrome b gene and isolation of three single nucleotide polymorphisms from parasites present after atovaquone treatment. Am J Trop Med Hyg. 2006;74:593\u20137.","journal-title":"Am J Trop Med Hyg."},{"key":"4232_CR38","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.vetpar.2015.10.002","volume":"214","author":"J Cao","year":"2015","unstructured":"Cao J, Yang Q, Zhang J, Zhou Y, Zhang H, Gong H, et al. Seroprevalence survey of Babesia gibsoni infection and tick species in dogs in East China. Vet Parasitol. 2015;214:12\u201325.","journal-title":"Vet Parasitol."},{"key":"4232_CR39","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1051\/parasite\/2017036","volume":"24","author":"J Zhang","year":"2017","unstructured":"Zhang J, Liu Q, Wang D, Li W, Beugnet F, Zhou J. Epidemiological survey of ticks and tick-borne pathogens in pet dogs in south-eastern China. Parasite. 2017;24:35.","journal-title":"Parasite."},{"key":"4232_CR40","doi-asserted-by":"crossref","first-page":"101452","DOI":"10.1016\/j.cimid.2020.101452","volume":"70","author":"XW Li","year":"2020","unstructured":"Li XW, Zhang XL, Huang HL, Li WJ, Wang SJ, Huang SJ, et al. Prevalence and molecular characterization of Babesia in pet dogs in Shenzhen, China. Comp Immunol Microbiol Infect Dis. 2020;70:101452.","journal-title":"Comp Immunol Microbiol Infect Dis."},{"key":"4232_CR41","doi-asserted-by":"publisher","DOI":"10.1155\/2014\/741785","author":"A Singh","year":"2014","unstructured":"Singh A, Singh H, Singh NK, Singh ND, Rath SS. Canine babesiosis in northwestern India: molecular detection and assessment of risk factors. Biomed Res Int. 2014. https:\/\/doi.org\/10.1155\/2014\/741785.","journal-title":"Biomed Res Int."},{"key":"4232_CR42","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1111\/avj.12293","volume":"93","author":"SF Hii","year":"2015","unstructured":"Hii SF, Traub RJ, Thompson MF, Henning J, O\u2019Leary CA, Burleigh A, et al. Canine tick-borne pathogens and associated risk factors in dogs presenting with and without clinical signs consistent with tick-borne diseases in northern Australia. Aust Vet J. 2015;93:58\u201366.","journal-title":"Aust Vet J."},{"key":"4232_CR43","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.vetpar.2011.04.015","volume":"181","author":"G Baneth","year":"2011","unstructured":"Baneth G. Perspectives on canine and feline hepatozoonosis. Vet Parasitol. 2011;181:3\u201311.","journal-title":"Vet Parasitol."},{"key":"4232_CR44","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.micpath.2018.10.033","volume":"126","author":"H Nayyar Ghauri","year":"2019","unstructured":"Nayyar Ghauri H, Ijaz M, Farooqi SH, Ali A, Ghaffar A, Saleem S, et al. A comprehensive review on past, present and future aspects of canine theileriosis. Microb Pathog. 2019;126:116\u201322.","journal-title":"Microb Pathog."},{"key":"4232_CR45","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1186\/s13071-015-0649-0","volume":"8","author":"\u00c1 Sainz","year":"2015","unstructured":"Sainz \u00c1, Roura X, Mir\u00f3 G, Estrada-Pe\u00f1a A, Kohn B, Harrus S, et al. Guideline for veterinary practitioners on canine ehrlichiosis and anaplasmosis in Europe. Parasit Vectors. 2015;8:75.","journal-title":"Parasit Vectors."},{"key":"4232_CR46","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1111\/jsap.12328","volume":"56","author":"S Schuller","year":"2015","unstructured":"Schuller S, Francey T, Hartmann K, Hugonnard M, Kohn B, Nally JE, et al. European consensus statement on leptospirosis in dogs and cats. J Small Anim Pract. 2015;56:159\u201379.","journal-title":"J Small Anim Pract."},{"key":"4232_CR47","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1128\/CMR.00012-12","volume":"25","author":"F Sim\u00f3n","year":"2012","unstructured":"Sim\u00f3n F, Siles-Lucas M, Morch\u00f3n R, Gonz\u00e1lez-Miguel J, Mellado I, Carret\u00f3n E, et al. Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev. 2012;25:507\u201344.","journal-title":"Clin Microbiol Rev."},{"key":"4232_CR48","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.meegid.2016.03.025","volume":"41","author":"MN Singh","year":"2016","unstructured":"Singh MN, Raina OK, Sankar M, Rialch A, Tigga MN, Kumar GR, et al. Molecular detection and genetic diversity of Babesia gibsoni in dogs in India. Infect Genet Evol. 2016;41:100\u20136.","journal-title":"Infect Genet Evol."},{"key":"4232_CR49","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1098\/rstb.2008.0157","volume":"364","author":"P Schmid-Hempel","year":"2009","unstructured":"Schmid-Hempel P. Immune defence, parasite evasion strategies and their relevance for \u2018macroscopic phenomena\u2019 such as virulence. Philos Trans R Soc Lond B Biol Sci. 2009;364:85\u201398.","journal-title":"Philos Trans R Soc Lond B Biol Sci."},{"key":"4232_CR50","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/S0169-4758(98)01346-5","volume":"14","author":"S Naitza","year":"1998","unstructured":"Naitza S, Spano F, Robson KJ, Crisanti A. The thrombospondin-related protein family of apicomplexan parasites: the gears of the cell invasion machinery. Parasitol Today. 1998;14:479\u201384.","journal-title":"Parasitol Today."},{"key":"4232_CR51","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.pt.2008.11.004","volume":"25","author":"BJ Morahan","year":"2009","unstructured":"Morahan BJ, Wang L, Coppel RL. No TRAP, no invasion. Trends Parasitol. 2009;25:77\u201384.","journal-title":"Trends Parasitol."},{"key":"4232_CR52","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.molbiopara.2006.03.015","volume":"148","author":"J Zhou","year":"2006","unstructured":"Zhou J, Fukumoto S, Jia H, Yokoyama N, Zhang G, Fujisaki K, et al. Characterization of the Babesia gibsoni P18 as a homologue of thrombospondin related adhesive protein. Mol Biochem Parasitol. 2006;148:190\u20138.","journal-title":"Mol Biochem Parasitol."},{"key":"4232_CR53","doi-asserted-by":"crossref","first-page":"2603","DOI":"10.1128\/JCM.39.7.2603-2609.2001","volume":"39","author":"S Fukumoto","year":"2001","unstructured":"Fukumoto S, Xuan X, Nishikawa Y, Inoue N, Igarashi I, Nagasawa H, et al. Identification and expression of a 50-kilodalton surface antigen of Babesia gibsoni and evaluation of its diagnostic potential in an enzyme-linked immunosorbent assay. J Clin Microbiol. 2001;39:2603\u20139.","journal-title":"J Clin Microbiol."},{"key":"4232_CR54","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.vetpar.2009.02.025","volume":"162","author":"H Jia","year":"2009","unstructured":"Jia H, Aboge GO, Terkawi MA, Goo YK, Nishikawa Y, Kuriki K, et al. Genetic diversity of two selected antigen loci in Babesia gibsoni Asian genotype obtained from Japan and Jeju island of South Korea. Vet Parasitol. 2009;162:142\u20136.","journal-title":"Vet Parasitol."},{"key":"4232_CR55","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1292\/jvms.12-0140","volume":"74","author":"M Sakuma","year":"2012","unstructured":"Sakuma M, Fukuda K, Takayama K, Kobayashi Y, Shimokawa Miyama T, Setoguchi A, et al. Molecular epidemiological survey of the Babesia gibsoni cytochrome b gene in western Japan. J Vet Med Sci. 2012;74:1341\u20134.","journal-title":"J Vet Med Sci."},{"key":"4232_CR56","doi-asserted-by":"crossref","first-page":"589","DOI":"10.3347\/kjp.2018.56.6.589","volume":"56","author":"WQ Zheng","year":"2018","unstructured":"Zheng WQ, Xuan XN, Fu RL, Tao HY, Liu YQ, Liu XQ, et al. Tick-borne pathogens in Ixodid ticks from Poyang Lake Region, southeastern China. Korean J Parasitol. 2018;56:589\u201396.","journal-title":"Korean J Parasitol."}],"container-title":["Parasites &amp; Vectors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-020-04232-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13071-020-04232-w\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-020-04232-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,21]],"date-time":"2021-07-21T23:54:14Z","timestamp":1626911654000},"score":1,"resource":{"primary":{"URL":"https:\/\/parasitesandvectors.biomedcentral.com\/articles\/10.1186\/s13071-020-04232-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,22]]},"references-count":56,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["4232"],"URL":"https:\/\/doi.org\/10.1186\/s13071-020-04232-w","relation":{},"ISSN":["1756-3305"],"issn-type":[{"value":"1756-3305","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,22]]},"assertion":[{"value":"22 February 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 July 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 July 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"All blood samples were collected under the permission from the owners of the pet dogs, and performed according to Guidance for Experimental Animal Welfare and Ethical Treatment by the Ministry of Science and Technology of China (). This study was approved by the Scientific Ethic Committee of Chengde Medical University (number 2017020).","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"366"}}