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Hard Ticks as Vectors Tested Negative for Severe Fever with Thrombocytopenia Syndrome in Ganghwa-do, Korea during 2019-2020

  • Jin, Kyoung (Korea Health Evaluation Institute, Sahmyook University) ;
  • Koh, Yeon-Ja (Department of Infectious Diseases Diagnosis, Incheon Metropolitan City Institute of Public Health and Environment) ;
  • Ahn, Seong Kyu (Department of Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine) ;
  • Cho, Joonghee (Department of Infectious Diseases Diagnosis, Incheon Metropolitan City Institute of Public Health and Environment) ;
  • Lim, Junghwan (Department of Infectious Diseases Diagnosis, Incheon Metropolitan City Institute of Public Health and Environment) ;
  • Song, Jaeyong (Department of Infectious Diseases Diagnosis, Incheon Metropolitan City Institute of Public Health and Environment) ;
  • Lee, Jinyoung (Department of Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine) ;
  • Gong, Young Woo (Department of Infectious Diseases Diagnosis, Incheon Metropolitan City Institute of Public Health and Environment) ;
  • Kwon, Mun Ju (Department of Infectious Diseases Diagnosis, Incheon Metropolitan City Institute of Public Health and Environment) ;
  • Kwon, Hyung Wook (Department of Life Sciences, Incheon National University) ;
  • Bahk, Young Yil (Department of Biotechnology, College of Biomedical and Health Science, Konkuk University) ;
  • Kim, Tong-Soo (Department of Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine)
  • Received : 2021.04.22
  • Accepted : 2021.05.30
  • Published : 2021.06.30

Abstract

This study aimed to characterize the seasonal abundance of hard ticks that transmit severe fever with thrombocytopenia syndrome virus from April to November 2019 and 2020 on Ganghwa-do, Incheon Metropolitan City, Korea. The ticks were collected at grassland, grave site, copse and mountain road using a collection trap method. The ixodid hard ticks comprising three species (Haemaphysalis longicornis, H. flava, and Ixodes nipponensis) collected were 6,622 in 2019 and 3,811 in 2020. H. longicornis was the most frequent (97.9% in 2019 and 96.0% in 2020), followed by H. flava (2.0% and 3.0% in 2019 and 2020, respectively) and I. nipponensis (less than 0.1%). Our study demonstrated that seasonal patterns of the tick populations examined for two years were totally unsimilar. The hard ticks tested using RT-qPCR were all negative for severe fever with thrombocytopenia syndrome virus.

Keywords

Acknowledgement

This study was supported by the Korea Disease Control and Prevention Agency (4851-304-320), the Priority Research Centers Program through the National Research Foundation funded by the Ministry of Education (2020R1A6A1A03041954) and the Inha University Research Fund (65321-1) in Korea.

References

  1. de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE. Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 2008; 13: 6938-6946. https://doi.org/10.2741/3200
  2. Mansfield KL, Jizhou Lv, Phipps LP, Johnson N. Emerging tickborne viruses in the twenty-first century. Front Cell Infect Microbiol 2017; 7: 298. https://doi.org/10.3389/fcimb.2017.00298
  3. Sonenshine DE, Roe RM. Biology of Ticks, Vol. 2. Oxford University Press. Oxford, UK. 2013, pp180-210. https://global.oup.com/academic/product/biology-of-ticks-volume-2-9780199744060?cc=kr&lang=en&
  4. Kim KH, Yi J, Kim G, Choi SJ, Jun KI, Kim NH, Choe PG, Kim NJ, Lee JK, Oh MD. Severe fever with thrombocytopenia syndrome, South Korea, 2012. Emerg Infect Dis 2013; 19: 1892-1894. https://doi.org/10.3201/eid1911.130792
  5. Takahashi T, Maeda K, Suzuki T, Ishido A, Shigeoka T, Tominaga T, Kamei T, Honda M, Ninomiya D, Sakai T, Senba T, Kaneyuki S, Sakaguchi S, Satoh A, Hosokawa T, Kawabe Y, Kurihara S, Izumikawa K, Kohno S, Azuma T, Suemori K, Yasukawa M, Mizutani T, Omatsu T, Katayama Y, Miyahara M, Ijuin M, Doi K, Okuda M, Umeki K, Saito T, Fukushima K, Nakajima K, Yoshikawa T, Tani H, Fukushi S, Fukuma A, Ogata M, Shimojima M, Nakajima N, Nagata N, Katano H, Fukumoto H, Sato Y, Hasegawa H, Yamagishi T, Oishi K, Kurane I, Morikawa S, Saijo M. The first identification and retrospective study of Severe Fever with Thrombocytopenia Syndrome in Japan. J Infect Dis 2014; 209: 816-827. https://doi.org/10.1093/infdis/jit603
  6. Gai ZT, Zhang Y, Liang MF, Jin C, Zhang S, Zhu CB, Li C, Li XY, Zhang QF, Bian PF, Zhang LH, Wang B, Zhou N, Liu JX, Song XG, Xu A, Bi ZQ, Chen SJ, Li DX. Clinical progress and risk factors for death in severe fever with thrombocytopenia syndrome patients. J Infect Dis 2012; 206: 1095-1102. https://doi.org/10.1093/infdis/jis472
  7. Park SW, Lee CS, Kim JH, Bae IG, Moon C, Kwak YG, Kim BN, Lee JH, Ryu SY, Jang HC, Hur J, Jun JB, Jung Y, Chang HH, Kim YK, Hwang JH, Kim YS, Jeong HW, Song KH, Park WB, Kim ES, Oh MD. Severe fever with thrombocytopenia syndrome: comparison with scrub typhus and clinical diagnostic prediction. BMC Infect Dis 2019; 19: 174. https://doi.org/10.1186/s12879-019-3773-1.
  8. Korean Centers for Disease Control and Prevention. Disease Web Statistics System [Internet]. Available from: http://is.kdca.go.kr/dstar/jsp/stat/stat0001.jsp
  9. Kim WY, Choi W, Park SW, Wang EB, Lee WJ, Jee Y, Lim KS, Lee HJ, Kim SM, Lee SO, Choi SH, Kim YS, Woo JH, Kim SH. Nosocomial transmission of severe fever with thrombocytopenia syndrome in Korea. Clin Infect Dis 2015; 60: 1681-1683. https://doi.org/10.1093/cid/civ128
  10. Jeong EJ, Song JY, Lim CS, Lee I, Park MS, Choi MJ, Jeon JH, Kang SH, Jung BK, Yoon JG, Hyun HJ, Noh JY, Cheong HJ, Kim WJ. Viral shedding from diverse body fluids in a patient with severe fever with thrombocytopenia syndrome. J Clin Virol 2016; 80: 33-35. http://dx.doi.org/10.1016/j.jcv.2016.04.018
  11. Yun SM, Lee WG, Ryou J, Yang SC, Park SW, Roh JY, Lee YJ, Park C, Han MG. Severe fever with thrombocytopenia syndrome virus in ticks collected from humans, South Korea. 2013. Emerg Infect Dis 2014; 20: 1358-1361. https://doi.org/10.3201/eid2008.131857.
  12. Dobson ADM, Taylor JL, Randolph SE. Tick (Ixodes ricinus) abundance and seasonality at recreational sites in the UK: hazards in relation to fine-scale habitat types revealed by complementary sampling methods. Ticks Tick Borne Dis 2011; 2: 67-74. https://doi.org/10.1016/j.ttbdis.2011.03.002
  13. Dominguez L, Miranda RJ, Torres S, Moreno R, Ortega J, Bermudez SE. Hard tick (Acari: Ixodidae) survey of Oleoducto trail, Soberania National Park, Panama. Ticks Tick Borne Dis 2019; 10: 830-837. https://doi.org/10.1016/j.ttbdis.2019.04.001
  14. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F. World map of the Koppen-Geiger climate classification updated. Meteorologische Zeitschrift 2006; 15: 259-263. https://doi.org/10.1127/0941-2948/2006/0130
  15. Yamaguti N, Tipton VJ, Keegan HL, Toshioka S. Ticks of Japan, Korea, and the Ryukyu Islands. Vol. 15. Brigham Young University. Provo, USA. pp 1-227. https://scholarsarchive.byu.edu/cgi/viewcontent.cgi?article=1066&context=byuscib
  16. Azad AF. Mites of Public Health Importance and Their Control. Vector Biology and Control Division, World Health Organization. 1986, pp 1-52. https://apps.who.int/iris/handle/10665/58177
  17. Yun SM, Lee YJ, Choi W, Kim HC, Chong ST, Chang KS, Coburn JM, Klein TA, Lee WJ. Molecular detection of severe fever with thrombocytopenia syndrome and tick-borne encephalitis viruses in ixodid ticks collected from vegetation, Republic of Korea, 2014. Ticks Tick Borne Dis 2016; 7: 970-978. https://doi.org/10.1016/j.ttbdis.2016.05.003
  18. Kim-Jeon MD, Jegal S, Jun H, Jung H, Park SH, Ahn SK, Lee J, Gong YW, Joo K, Kwon MJ, Roh JY, Lee WG, Bahk YY, Kim TS. Four-year surveillance of the vector hard ticks for SFTS Ganghwado, Republic of Korea. Korean J Parasitol 2019; 57: 691-698. https://doi.org/10.3347/kjp.2019.57.6.691
  19. Shin J, Park J, Kwon D. Epidemiologic and clinical characteristics of severe fever with thrombocytopenia syndrome in the Republic of Korea. Publ Health Weekly Rep 2014; 7: 493-498. https://www.researchgate.net/publication/285716160
  20. Lee WT, Lim JW, Lee SY, Lee IY. Redistribution of Haemaphysalis flava and Ixodes tanuki collected from raccoon dog in Korea. Korean J Parasitol 1997; 35: 1-8 (in Korean). https://doi.org/10.3347/kjp.1997.35.1.1
  21. Jo YS, Kang JG, Chae JB, Cho YK, Shin JH, Jheong WH, Chae JS. Prevalence of severe fever with thrombocytopenia syndrome virus in Haemaphysalis longicornis ticks in Seoul, Korea. Ticks Tick Borne Dis 2014; 5: 975-977. https://doi.org/10.1016/j.ttbdis.2014.07.020
  22. Yun SM, Song BG, Choi W, Park WI, Kim SY, Roh JY, Ryou J, Ju YR, Park C, Shin EH. Prevalence of tick-borne encephalitis virus in Ixodid ticks collected from the Republic of Korea during 2011-2012. Osong Public Health Res Perspect 2012; 3: 213-221. https://doi.org/10.1016/j.phrp.2012.10.004
  23. Kleiner J. Korea, a Century of Change. World Scientific. New Jersey, USA. https://books.google.co.kr/books?id=nTCC2ZheFu0C&printsec=frontcover&hl=ko&source=gbs_gesummary_r&cad=0#v=onepage&q&f=false
  24. Chung YS, Yoon MB, Kim HS. On climate variations and changes observed in South Korea. Climate Change 2004; 66: 151-161. https://doi.org/10.1023/B:CLIM.0000043141.54763.f8
  25. Kim BJ, Kripalani RH, Oh J-H, Moon SE. Summer monsoon rainfall patterns over South Korea and associated circulation features. Theor Appl Climatol 2002; 72: 65-74. https://doi.org/10.1007/s007040200013
  26. Yun SM, Song BG, Choi W, Roh JY, Lee YJ, Park WI, Han MG, Ju YR, Lee WJ. First isolation of severe fever with thrombocytopenia syndrome virus from Haemaphysalis longicornis ticks collected in severe fever with thrombocytopenia syndrome outbreak areas in the Republic of Korea. Vector Borne Zoonotic Dis 2016; 16: 66-70. https://doi.org/10.1089/vbz.2015.1832
  27. Wang S, Li J, Niu G, Wang X, Ding S, Jiang X, Li C, Zhang Q, Liang M, Bi Z, Li D. STFS virus in ticks in an endemic area of China. Am J Trop Med Hyg 2015; 92: 684-689. https://doi.org/10.4269/ajtmh.14-0008
  28. Chae JB, Kang JG, Kim HC, Chong ST, Lee IY, Shin NS, Chae JS. Identification of tick species collected from wild boars and habitats of wild boars and domestic pigs in the Republic of Korea. Korean J Parasitol 2017; 55: 185-191. https://doi.org/10.3347/kjp.2017.55.2.185
  29. Chae JB, Cho YS, Cho YK, Kang JG, Shin NS, Chae JS. Epidemiological investigation of tick species from near domestic animal farms and cattle goat, and wild boar in Korea. Korean J Parasitol 2019; 57: 319-324. https://doi.org/10.3347/kjp.2019.57.3.319
  30. Chong ST, Kim HC, Lee IY, Kollars TM Jr, Sancho AR, Sames WJ, Klein TA. Comparison of dragging and sweeping methods for collecting ticks and determining their seasonal distributions for various habitats, Gyeonggi Province, Republic of Korea. J Med Entomol 2013; 50: 611-618. https://doi.org/10.1603/me12032
  31. Chong ST, Kim HC, Lee IY, Kollars TM Jr, Sancho AR, Sames WJ, Chae JS, Klein TA. Seasonal distribution of ticks in four habitats near the demilitarized zone, Gyeonggi-do (province), Republic of Korea. Korean J Parasitol 2013; 51: 319-325. https://doi.org/10.3347/kjp.2013.51.3.319
  32. Ko S, Kang JG, Kim SY, Kim HC, Klein TA, Chong ST, Sames WJ, Yun SM, Ju YR, Chae JS. Prevalence of tick-borne encephalitis virus in ticks from southern Korea. J Vet Sci 2010; 11: 197-203. https://doi.org/10.4142/jvs.2010.11.3.197
  33. Lin TL, Ou SC, Maeda K, Shimoda H, Chan JP, Tu WC, Hsu WL, Chou CC. The first discovery of severe fever with thrombocytopenia syndrome virus in Taiwan. Emerg Microbes Infect 2020; 9: 148-151. https://doi.org/10.1080/22221751.2019.1710436
  34. Jiao Y, Zeng X, Guo X, Qi X, Zhang X, Shi Z, Zhou M, Bao C, Zhang W, Xu Y, Wang H. Preparation and evaluation of recombinant severe fever with thrombocytopenia syndrome virus nucleocapsid protein for detection of total antibodies in human and animal sera by double-antigen sandwich enzyme-linked immunosorbent assay. J Clin Microbiol 2012; 50: 372-377. https://doi.org/10.1128/JCM.01319-11
  35. Zhang X, Liu Y, Zhao L, Li B, Yu H, Wen H, Yu XJ. An emerging hemorrhagic fever in China caused by a novel bunyavirus SFTSV. Sci China Life Sci 2013; 56: 697-700. https://doi.org/10.1007/s11427-013-4518-9
  36. Huang XY, Du YH, Wang HF, You AG, Li Y, Su J, Nie YF, Ma HX, Xu BL. Prevalence of severe fever with thrombocytopenia syndrome virus in animals in Henan Province, China. Infect Dis Poverty 2019; 8: 56. https://doi.org/10.1186/s40249-019-0569-x
  37. Park SW, Han MG, Yun SM, Park C, Lee WJ, Ryou J. Severe fever with thrombocytopenia syndrome virus, South Korea, 2013. Emerg Infect Dis 2014; 20: 1880-1882. https://doi.org/10.3201/eid2011.140888
  38. Choi SJ, Park SW, Bae IG, Kim SH, Ryu SY, Kim HA, Jang HC, Hur J, Jun JB, Jung Y, Chang HH, Kim YK, Yi J, Kim KH, Hwang JH, Kim YS, Jeong HW, Song KH, Park WB, Kim ES, Oh MD. Severe fever with thrombocytopenia syndrome in South Korea, 2013-2015. PLoS Negl Trop Dis 2016; 10: e0005264. https://doi.org/10.1371/journal.pntd.0005264
  39. Im JH, Baek J, Durey A, Kwon HY, Chung MH, Lee JS. Current status of tick-borne diseases in South Korea. Vector Borne Zoonotic Dis 2019; 19: 225-233. https://doi.org/10.1089/vbz.2018.2298
  40. Park SW, Song BG, Shin EH, Yun SM, Han MG, Park MY, Park C, Ryou J. Prevalence of severe fever with thrombocytopenia syndrome virus in Haemaphysalis longicornis ticks in South Korea. Ticks Tick Borne Dis 2014; 5: 975-977. https://doi.org/10.1016/j.ttbdis.2014.07.020
  41. Ham H, Jo S, Jang J, Choi S. No detection of severe fever with thrombocytopenia syndrome virus from Ixodid ticks collected in Seoul. Korean J Parasitol 2014; 52: 221-224. https://doi.org/10.3347/kjp.2014.52.2.221
  42. Jo YS, Kang JG, Chae JB, Cho YK, Shin JH, Jheong WH, Chae JS. Prevalence of severe fever with thrombocytopenia syndrome virus in ticks collected from national parks in Korea. Vector Borne Zoonotic Dis 2019; 19: 284-289. https://doi.org/10.1089/vbz.2018.2338.