{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T18:57:54Z","timestamp":1792522674508,"version":"4.5.0"},"reference-count":42,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2024,12,8]],"date-time":"2024-12-08T00:00:00Z","timestamp":1733616000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Animal and Plant Quarantine Agency, Korea","award":["1543061-2022-22-01"],"award-info":[{"award-number":["1543061-2022-22-01"]}]},{"name":"Animal and Plant Quarantine Agency, Korea","award":["2024-ER2111-00"],"award-info":[{"award-number":["2024-ER2111-00"]}]},{"name":"Korea, National Institute of Health Research Project","award":["1543061-2022-22-01"],"award-info":[{"award-number":["1543061-2022-22-01"]}]},{"name":"Korea, National Institute of Health Research Project","award":["2024-ER2111-00"],"award-info":[{"award-number":["2024-ER2111-00"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Tick-borne diseases are a public health problem and a significant burden on the livestock industry. The seasonal abundance of ticks and tick-borne pathogens strongly correlates with the prevalence of these diseases. To investigate the seasonal variation in ticks and tick-borne pathogens, ticks were collected from Gangwon State, Korea, and the tick-borne pathogens Borrelia, Anaplasma, Babesia, and Theileria were examined. In total, 14,748 ticks were collected, comprising ticks from two genera and three species: Haemaphysalis\u00a0longicornis, Haemaphysalis\u00a0flava, and Ixodes\u00a0nipponensis, with H. longicornis being the predominant species. Of 7445 ticks (455 pools) examined for pathogens, Theileria was detected in 61 pools, whereas Borrelia and Anaplasma were observed in 17 pools. H. longicornis nymphs and adults were collected beginning in April, with nymph numbers peaking in May and June and adult ticks peaking in June and July. In contrast, the larvae were collected in May and peaked in September. Tick-borne pathogens were detected in April, peaking in July and September. Borrelia, the causative agent of Lyme disease, exhibits a temporal association between its detection in ticks and its occurrence in humans. In conclusion, tick-borne diseases seem to be closely linked not only to changes in tick numbers throughout the seasons but also to the seasonal variations of the pathogens within them.<\/jats:p>","DOI":"10.3390\/pathogens13121079","type":"journal-article","created":{"date-parts":[[2024,12,9]],"date-time":"2024-12-09T04:01:37Z","timestamp":1733716897000},"page":"1079","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Seasonal Dynamics of Ticks and Tick-Borne Pathogens in Republic of Korea"],"prefix":"10.3390","volume":"13","author":[{"given":"Sezim","family":"Monoldorova","sequence":"first","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sungkyeong","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seungri","family":"Yun","sequence":"additional","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sunho","family":"Park","sequence":"additional","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jong-Uk","family":"Jeong","sequence":"additional","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiro","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"},{"name":"Department of Clinical Laboratory Science, Cheju Halla University, Jeju 63092, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"In-Yong","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Tropical Medicine and Institute of Tropical Medicine, Yonsei University College of Medicine, Seoul 03722, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-8364-3047","authenticated-orcid":false,"given":"Hojong","family":"Jun","sequence":"additional","affiliation":[{"name":"Department of Medical Environmental Biology and Tropical Medicine, School of Medicine, Kangwon National University, Chuncheon 24341, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chan-Ho","family":"Park","sequence":"additional","affiliation":[{"name":"Gangwon State Veterinary Service & Research Institute, Chuncheon 24203, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyeon-Seop","family":"Byeon","sequence":"additional","affiliation":[{"name":"Chungbuk Province Veterinary Service & Research Institute, Cheongju 28135, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mina","family":"Han","sequence":"additional","affiliation":[{"name":"Chungbuk Province Veterinary Service & Research Institute, Cheongju 28135, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"So-Youn","family":"Youn","sequence":"additional","affiliation":[{"name":"Bacterial and Parasitic Disease Division, Department of Animal & Plant Health Research, Animal and Plant Quarantine Agency, Gimcheon 39660, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1346-7067","authenticated-orcid":false,"given":"Yun-Sang","family":"Cho","sequence":"additional","affiliation":[{"name":"Bacterial and Parasitic Disease Division, Department of Animal & Plant Health Research, Animal and Plant Quarantine Agency, Gimcheon 39660, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Young-Min","family":"Yun","sequence":"additional","affiliation":[{"name":"Department of Veterinary Internal Medicine, College of Veterinary Medicine, Jeju National University, Jeju 63243, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7831-5905","authenticated-orcid":false,"given":"Kwang-Jun","family":"Lee","sequence":"additional","affiliation":[{"name":"Division of Zoonotic and Vector Borne Disease Research, Center for Infectious Diseases Research, Korea National Institute of Health, Cheongju 28159, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4314-216X","authenticated-orcid":false,"given":"Bo-Young","family":"Jeon","sequence":"additional","affiliation":[{"name":"Department of Biomedical Laboratory Science, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju 26493, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e00083-18","DOI":"10.1128\/CMR.00083-18","article-title":"Emerging tick-borne diseases","volume":"33","author":"Kramer","year":"2020","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1354","DOI":"10.1016\/j.ttbdis.2018.04.001","article-title":"Controlling ticks and tick-borne diseases\u2026 looking forward","volume":"9","year":"2018","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/j.pt.2012.07.003","article-title":"Ticks and tick-borne diseases: A One Health perspective","volume":"28","author":"Chomel","year":"2012","journal-title":"Trends Parasitol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"S11","DOI":"10.1093\/infdis\/jiae230","article-title":"Lyme disease sur veillance and epidemiology in the United States: A historical perspective","volume":"230","author":"Mead","year":"2024","journal-title":"J. Infect. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Binetruy, F., Garnier, S., Boulanger, N., Talagrand-Reboul, \u00c9., Loire, E., Faivre, B., No\u00ebl, V., Buysse, M., and Duron, O. (2020). A novel Borrelia species, intermediate between Lyme disease and relapsing fever groups, in neotropical passerine-associated ticks. Sci. Rep., 10.","DOI":"10.1038\/s41598-020-66828-7"},{"key":"ref_6","unstructured":"Korea Disease Control and Prevention Agency (KDCA) (2024, September 01). Statistical Information on Outbreaks of Infectious Disease. Available online: https:\/\/npt.kdca.go.kr\/pot\/index.do."},{"key":"ref_7","first-page":"307","article-title":"Isolation of Borrelia burgdorferi, the causative agent of Lyme disease, from Ixodes ticks in Korea","volume":"27","author":"Park","year":"1992","journal-title":"J. Korean Soc. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Kim, S.Y., Kim, T.K., Kim, T.Y., and Lee, H.I. (2020). Geographical Distribution of Borrelia burgdorferi sensu lato in ticks collected from wild rodents in the Republic of Korea. Pathogens, 9.","DOI":"10.3390\/pathogens9110866"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e0012313","DOI":"10.1371\/journal.pntd.0012313","article-title":"Human granulocytotropic anaplasmosis-A systematic review and analysis of the literature","volume":"18","author":"Schudel","year":"2024","journal-title":"PLoS Negl. Trop. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1128\/jcm.32.3.589-595.1994","article-title":"Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease","volume":"32","author":"Chen","year":"1994","journal-title":"J. Clin. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1686","DOI":"10.4269\/ajtmh.16-0529","article-title":"Clinical Isolation of Anaplasma phagocytophilum in South Korea","volume":"97","author":"Lee","year":"2017","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kim, D.Y., Seo, J.W., Yun, N.R., Kim, C.M., and Kim, D.M. (2021). Human granulocytic anaplasmosis in a Single University Hospital in the Republic of Korea. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-90327-y"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1016\/j.ttbdis.2016.04.011","article-title":"First molecular detection and phylogenetic analysis of Anaplasma phagocytophilum in shelter dogs in Seoul, Korea","volume":"7","author":"Lee","year":"2016","journal-title":"Ticks Tick Borne Dis."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Miranda, E.A., Han, S.W., Cho, Y.K., Choi, K.S., and Chae, J.S. (2021). Co-Infection with Anaplasma Species and Novel Genetic Variants Detected in Cattle and Goats in the Republic of Korea. Pathogens, 10.","DOI":"10.3390\/pathogens10010028"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2018","DOI":"10.1128\/jcm.35.8.2018-2021.1997","article-title":"Ehrlichia phagocytophila genogroup rickettsiae in ixodid ticks from California collected in 1995 and 1996","volume":"35","author":"Barlough","year":"1997","journal-title":"J. Clin. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1128\/JCM.37.1.209-210.1999","article-title":"Identity of ehrlichial DNA sequences derived from Ixodes ricinus ticks with those obtained from patients with human granulocytic ehrlichiosis in Slovenia","volume":"37","author":"Petrovec","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1089\/153036603765627424","article-title":"Identification of Ehrlichia chaffeensis, Anaplasma phagocytophilum, and A. bovis in Haemaphysalis longicornis and Ixodes persulcatus ticks from Korea","volume":"3","author":"Kim","year":"2003","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1767","DOI":"10.1001\/jama.2016.2884","article-title":"Diagnosis, treatment, and prevention of Lyme disease, human granulocytic anaplasmosis, and babesiosis: A review","volume":"315","author":"Sanchez","year":"2016","journal-title":"JAMA"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1089\/vbz.2008.0116","article-title":"Epidemiologic and clinical surveys in dogs infected with Babesia gibsoni in South Korea","volume":"9","author":"Lee","year":"2009","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2084","DOI":"10.1128\/JCM.01334-06","article-title":"First case of human babesiosis in Korea: Detection and characterization of a novel type of Babesia sp. (KO1) similar to ovine babesia","volume":"45","author":"Kim","year":"2007","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.cvfa.2024.01.006","article-title":"Transboundary Tick and Tick-Borne Pathogen Threats to Cattle","volume":"40","author":"Teel","year":"2024","journal-title":"Vet. Clin. N. Am. Food Anim. Pract."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.parint.2019.01.005","article-title":"Differential diagnosis and molecular characterization of Theileria spp. in sika deer (Cervus nippon) in Hokkaido","volume":"70","author":"Lee","year":"2019","journal-title":"Japan Parasitol. Int."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Almaz\u00e1n, C., Scimeca, R.C., Reichard, M.V., and Mosqueda, J. (2022). Babesiosis and Theileriosis in North America. Pathogens, 11.","DOI":"10.3390\/pathogens11020168"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Moon, M.Y., Kim, H.K., Chung, S.J., Byun, J.H., Kim, H.N., Lee, W., Lee, S.W., Monoldorova, S., Lee, S., and Jeon, B.Y. (2023). Genetic Diversity, Regional Distribution, and Clinical Characteristics of Severe Fever with Thrombocytopenia Syndrome virus in Gangwon Province, Korea, a highly prevalent region, 2019\u20132021. Microorganisms, 11.","DOI":"10.3390\/microorganisms11092288"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1093\/jme\/tjx106","article-title":"Borrelia species detected in ticks feeding on wild Korean Water Deer (Hydropotes inermis) using molecular and genotypic analyses","volume":"54","author":"VanBik","year":"2017","journal-title":"J. Med. Entomol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1093\/jme\/tjab170","article-title":"Surveillance and molecular identification of Borrelia species in ticks collected at U.S. Army Garrison Humphreys, Republic of Korea, 2018\u20132019","volume":"59","author":"Lee","year":"2022","journal-title":"J. Med. Entomol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Lee, H., Lee, S.H., Shin, S.S., and Kwak, D. (2021). Molecular Identification of Borrelia spp. from ticks in pastures nearby livestock farms in Korea. Insects, 12.","DOI":"10.3390\/insects12111011"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1086\/313948","article-title":"Human granulocytic ehrlichiosis","volume":"31","author":"Bakken","year":"2000","journal-title":"Clin. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1708","DOI":"10.3201\/eid2010.131680","article-title":"Human granulocytic anaplasmosis, South Korea, 2013","volume":"20","author":"Kim","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"35","DOI":"10.7853\/kjvs.2016.39.1.35","article-title":"Detection ratio of bacterial and viral pathogens of diarrhea from Korean indigenous goat feces in Gyeongbuk province","volume":"39","author":"Sohn","year":"2016","journal-title":"Korean J. Vet. Serv."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Kwak, D., and Seo, M.G. (2020). Genetic Diversity of Bovine Hemoprotozoa in South Korea. Pathogens, 9.","DOI":"10.3390\/pathogens9090768"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Chung, C.U., Lee, H., Seo, M.G., Lee, S.H., Kim, K.T., Nazim, K., Song, J.S., Bae, D.H., Rhee, M.H., and Kwon, O.D. (2023). Molecular Detection and Genotyping of Theileria spp. in Deer (Cervidae) in Korea. Microorganisms, 11.","DOI":"10.3390\/microorganisms11112740"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"106780","DOI":"10.1016\/j.actatropica.2022.106780","article-title":"Molecular epidemiology of Theileria species in ticks and its potential threat to livestock in the Republic of Korea","volume":"238","author":"Alkathiri","year":"2023","journal-title":"Acta Trop."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Seo, M.G., Noh, B.E., Lee, H.S., Kim, T.K., Song, B.G., and Lee, H.I. (2021). Nationwide Temporal and Geographical Distribution of Tick Populations and Phylogenetic Analysis of Severe Fever with Thrombocytopenia Syndrome Virus in Ticks in Korea, 2020. Microorganisms, 9.","DOI":"10.3390\/microorganisms9081630"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Jang, H., Casel, M.A.B., Jang, S.G., Choi, J.H., Gil, J., Rollon, R., Cheun, S.Y., Kim, Y.I., Song, M.S., and Choi, Y.K. (2024). Seasonal dynamics of Haemaphysalis tick species as SFTSV vectors in South Korea. Microbiol. Spectr., 12.","DOI":"10.1128\/spectrum.00489-24"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1186\/s13071-024-06341-2","article-title":"Comprehensive meta-analysis of severe fever with thrombocytopenia syndrome virus infections in humans, vertebrate hosts and questing ticks","volume":"17","author":"Xu","year":"2024","journal-title":"Parasit. Vectors"},{"key":"ref_37","unstructured":"Yamaguti, N., Tipton, V.J., Keegan, H.L., and Toshioka, S.Y. (1971). Ticks of Japan, Korea, and the Ryukyu islands. Brigh Young Univ. Sci. Biol. Ser., 15."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1099\/00207713-44-4-743","article-title":"Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons","volume":"44","author":"Postic","year":"1994","journal-title":"Int. J. Syst. Bacteriol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1099\/jmm.0.47663-0","article-title":"Presence of pathogenic Borrelia burgdorferi sensu lato in ticks and rodents in Zhejiang, south-east China","volume":"57","author":"Chu","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/0304-4017(95)00904-3","article-title":"Nested polymerase chain reaction for detection of Ehrlichia equi genomic DNA in horses and ticks (Ixodes pacificus)","volume":"63","author":"Barlough","year":"1996","journal-title":"Vet. Parasitol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/S0304-4017(01)00488-5","article-title":"Detection of haemoparasites in cattle by reverse line blot hybridisation with a note on the distribution of ticks in Sicily","volume":"99","author":"Georges","year":"2001","journal-title":"Vet. Parasitol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: Molecular evolutionary genetics analysis version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/12\/1079\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:49:55Z","timestamp":1760114995000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/12\/1079"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,8]]},"references-count":42,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["pathogens13121079"],"URL":"https:\/\/doi.org\/10.3390\/pathogens13121079","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,8]]}}}