Seok-Min Yun; Bong Gu Song; WooYoung Choi; Won Il Park; Sung Yun Kim; Jong Yul Roh; Jungsang Ryou; Young Ran Ju; Chan Park; E-Hyun Shin

doi:10.1016/j.phrp.2012.10.004

Articles

Page Path: HOME > Osong Public Health Res Perspect > Volume 3(4); 2012 > Article

Articles Prevalence of Tick-Borne Encephalitis Virus in Ixodid Ticks Collected from the Republic of Korea During 2011–2012: Seok-Min Yun^a, Bong Gu Song^b, WooYoung Choi^a, Won Il Park^b, Sung Yun Kim^b, Jong Yul Roh^b, Jungsang Ryou^a, Young Ran Ju^c, Chan Park^a, E-Hyun Shin^b; Osong Public Health and Research Perspectives 2012;3(4):213-221.
DOI: https://doi.org/10.1016/j.phrp.2012.10.004
Published online: December 31, 2012

^aDivision of Arboviruses, Korea National Institute of Health, Osong, Korea.

^bDivision of Medical Entomology, Korea National Institute of Health, Osong, Korea.

^cDivision of Zoonoses, Korea National Institute of Health, Osong, Korea.

Corresponding authors. E-mail: chanpark@nih.go.kr (C. Park), ehshin@nih.go.kr (E-H. Shin).

• Received: August 26, 2012 • Revised: October 12, 2012 • Accepted: October 15, 2012

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

3,465 Views
27 Download
28 Crossref
28 Scopus

Full Article

Download PDF

Abstract
1. Introduction
2. Materials and Methods
3. Results
4. Discussion

Abstract

Objectives
In this study, we demonstrated that TBEV-infected ticks have been distributed in the ROK, combined with our previous results. These results suggest that TBEV may exist in the ROK, and H. longicornis, H. flava, and I. nipponensis may be potential vectors of TBEV. In addition, these results emphasize the need for further epidemiological research of TBEV.
Methods
We examined for the presence of RNA of TBEV by reverse transcriptase-nested polymerase chain reaction (RT-nested PCR) using ixodid ticks captured in 25 localities of 10 provinces. Ticks were collected by the flagging and dragging method or using sentinel BG traps at forests, grass thickets, and grassland. A total of 13,053 ticks belonging to two genera and four species were collected and pooled (1292 pools), according to collection site, species of tick, and developmental stage.
Results
Among 1292 pools, the envelope (E) protein gene of TBEV was detected using RT-nested PCR in 10 pools (3 pools of the 1,331 adult ticks and 7 pools of the 11,169 nymph ticks) collected from Gangwon-do province, Jeonrabuk-do province, and Jeju Island. The minimum infection rates for TBEV of Haemaphysalis longicornis, Haemaphysalis flava, and Ixodes nipponensis were 0.06%, 0.17%, and 2.38%, respectively. Phylogenetic analysis based on the partial E protein gene was performed to identify relationships between the TBEV strains. This showed that 10 Korean strains clustered with the Western subtype.
Conclusion
In this study, we investigated the prevalence of tick-borne encephalitis virus (TBEV) in ixodid ticks from various regions of the Republic of Korea (ROK) during 2011–2012 to identify whether TBEV is circulating and to determine the endemic regions of TBEV.
Keywords: envelope gene; ixodid ticks; Republic of Korea; tick-borne encephalitis virus; Western subtype

1. Introduction

Ixodid ticks transmit a number of zoonotic pathogens, such as Borrelia burgdorferi [1], Batonella [2], Ehrlichia and Anaplasma [3,4], Rickettsia [5], and tick-borne encephalitis virus (TBEV) [6] to mammalian hosts. As the causative agent of tick-borne encephalitis (TBE), TBEV is a member of the family Flaviviridae and genus Flavivirus, and one of the most important human infections of the central nervous system [7]. TBE occurs in endemic areas of the Eurasian continents, including Europe, Russia, and Far-Eastern Asia (China and Japan), and has a significant impact on public health in these endemic regions [8]. So far, TBEV has been subdivided into three subtypes: the Far-Eastern subtype, known as Russian spring summer encephalitis virus; the Western or European subtype, known as Central European encephalitis virus; and the Siberian subtype based on phylogenetic analysis [8,9]. The main tick vector of the Western subtype is Ixodes ricinus, and Ixodes persulcatus is the main vector for the other subtypes [10,11]. TBEVis transmitted by tick bite and is maintained in the zoonotic transmission cycle between ixodid ticks and wild vertebrate hosts, such as wild and domestic mammals, birds, and reptiles.

In the Republic of Korea (ROK), although TBE infections have not been reported among humans, we have identified molecular evidence of TBEV infections in infesting ticks of the wild animals or collected ticks such as Haemaphysalis longicornis, Haemaphysalis flava, Haemaphysalis japonica, and Ixodes niponensis, which previously had not been known as TBEV vectors, and have isolated TBEV from lung tissues of the wild rodent, Apodemus agrarius [12,13]. However, unlike our expectation, Korean isolates were identified as the Western subtype of TBEV by sequence and phylogenetic analyses compared with other TBEV strains from neighboring countries, including China, Japan, and northeastern Russia that belong to the Far-Eastern subtype [12,13].

In this study, we investigated the prevalence of TBEV in ixodid ticks from various regions of the ROK using sensitive reverse transcriptase-nested polymerase chain reaction (RT-nested PCR) method to identify whether TBEV is circulating and to determine the endemic regions of TBEV.

2.1. Collection of ixodid ticks: Ixodid ticks surveys were performed by the flagging and dragging method or using sentinel BG traps in various sites, including grass thicket, grassland, and broad-leaved and coniferous forests in 25 localities of 10 provinces of the ROK during 2011–2012. Figure 1 represents the geographical locations of the collection sites. After collection, ticks were placed in plastic tubes and transported to the medical entomology laboratory of Korea National Institute of Health, where they were identified according to their species and developmental stages under a dissecting microscope according to the classification method of Yamaguti et al [14]. Identified ticks were stored at 4 ℃ until further investigation.
2.2. Tick processing and RNA extraction: A total of 13,053 identified ticks were pooled according to species, developmental stage, and locality. The size of pools ranged from 1 to 50 in larvae, from 1 to 30 in nymphs, and from 1 to 5 in adult males or females (Table 1). All the pooled ticks were homogenized using Precellys 24 homogenizer (Bertin Technologies, Montigny, Bretonneux, France) with a tissue lysis buffer in RNeasy Mini Kit (Qiagen GmbH, Hilden, Germany) and 2.8 mm stainless-steel beads. The homogenate was centrifuged at 10,000 rpm for 5 minutes, and supernatant was used for RNA extraction. RNA was extracted using the RNeasy Mini Kit (Qiagen GmbH) according to the manufacturer’s instructions.; The number of ixodid ticks classified by species and developmental stage, and MIR of TBEV in this study; ^aMIR: number of positive pools/total number of ticks assayed; ^b1–50 larvae/pool; ^c1–30 nymphs/pool; ^d1–5 adults/pool. MIR = minimum infection rate; TBEV = tick-borne encephalitis virus.
2.3. Reverse transcriptase-nested polymerase chain reaction: To examine for the presence of TBEV envelope (E) gene, the one-step RT-PCR was carried out using a Maxime RT-PCR PreMix kit (iNtRON Biotechnology, Gyeonggi, Korea) with previously described primers, TBE-913F (5’-TGCACACAYYTGGAAAA CAGGGA-3’) and TBE-1738R (5’-TGGCCACTTTT CAGGTGGTACTTG-3’) [15]. The one-step RT-PCR reaction was performed in a PCR thermal cycler (GeneAmp PCR system 9700, Applied Biosystems, Foster City, CA, USA) under the following conditions: 30 minutes at 45 ℃ for reverse transcription and 5 minutes at 94 ℃ for denaturation as the initial step, followed by 25 cycles of 30 seconds at 94 ℃, 30 seconds at 52 ℃, and 1 minute at 72 ℃, and a final extension step of 5 minutes at 72 ℃. Nested PCR was carried out using an i-StarMaster Mix PCR kit (iNtRON Biotechnology) with previously designed primers, TBE- 1192F (5’-CAGAGTGATCGAGGCTGGGGYAA-3’) and TBE-1669R (5’-AACACTCCAGTCTGGTCTC CRAGGTTGTA-3’) [15]. The nested PCR reaction consisted of an initial denaturation step of 2 minutes at 94 ℃, followed by 30 cycles of 20 seconds at 94 ℃, 10 seconds at 62 ℃, and 20 seconds at 68 ℃, and a final extension step of 5 minutes at 72 ℃. To confirm the PCR products, we analyzed them by agarose gel electrophoresis, stained with SYBR safe DNA gel stain (Invitrogen, Carlsbad, CA, USA).
2.4. Sequencing and phylogenetic analysis: The TBEV-positive products of RT-nested PCR were purified using a QIAquick gel extraction kit (Qiagen GmbH) according to the manufacturer’s instructions and sequenced using ABI Prism BigDye terminator cycle sequencing kits and ABI 3730xl sequencer (Applied Biosystems) at Solgent Inc. (Daejeon, Korea). Results of sequencing were assembled using the SeqMan program implemented in DNASTAR software (version 5.0.6; DNASTAR Inc., Madison, WI, USA) to determine the consensus sequences. The TBEV strains used for phylogenetic analysis are listed in Table 2; multiple sequence alignments were performed using Clustal W implemented in MEGA software version 5 [16]. Phylogenetic analysis was performed using MEGA software version 5 by the maximum likelihood method. The sequences obtained from TBEV-positive products were submitted to GenBank (accession numbers JX282515–JX282524).; TBEV strains used in the phylogenetic analysis; TBEV = tick-borne encephalitis virus.

3.1. Numbers and identification of ixodid ticks: A total of 13,053 ticks (553 larvae, 11,169 nymphs, 337 males, and 994 females) were collected from 2011 to 2012 in 25 localities of the ROK (Table 1 and Figure 1). The ixodid tick samples were identified to belong to four species in two genera: H. longicornis, H. flava, I. niponensis, and I. persulcatus. Of the identified ticks, H. longicornis (90.8%, 11,856/ 13,053) was the most abundant species in this study, followed by H. flava (8.8%, 1149/13,053), I. niponensis (0.3%, 42/13,053), and I. persulcatus (0.05%, 6/13,053).
3.2. Prevalence of TBEV in ixodid ticks: Of the 13,053 ixodid tick samples, 10 pools were positive for TBEV according to RT-nested PCR method. Among the 10 positive pools, three pools of the adult ticks and seven of the nymph ticks were collected from Gunsan in Jeollabuk-do province, Chuncheon or Sokcho in Gangwon-do province, and Jeju in Jeju Island. Regional prevalence of TBEV for each species was shown in Table 3. The minimum infection rate (MIR, calculated with the assumption that a positive pool contains one infected tick) of TBEV in H. longicornis, H. flava, and Ixodes nipponensis was 0.06%, 0.17%, and 2.38%, respectively (Table 1). Although H. longicornis was the most common species collected in this study, its positive rates of TBEV was lower than that of other species.; The highest MIR of TBEV infection was identified in I. nipponensis collected from Sokcho in Gangwon-do province (5.26%). In the other localities, the MIR of infected ticks varied from 0% to 1.33%. The highest rate of TBEV infection was identified in I. nipponensis nymph (4.35%). The infection rates in males (0.30%) were higher than those in females (0.20%) and nymph (0.06%). The mean TBEV prevalence in 25 collection sites was about 0.08%.; Regional prevalence of TBEV in ixodid ticks (minimum infection rate) collected in the Republic of Korea; ROK = Republic of Korea; TBEV = tick-borne encephalitis virus.
3.3. Sequence and phylogenetic analyses: Nucleotide sequence identities between the 10 Korean strains and the other 32 TBEV strains represented that the 10 Korean strains had high identity with the Western subtype strains with 97.2–99.6%, compared with the Far-Eastern subtype with 81.1–84.3% or the Siberian subtype with 83.9–85.7%.; Phylogenetic trees derived from nucleotide sequences of the E gene showed that the 10 Korean strains (Kor- Vec11-215, KorVec11-224, KorVec11-226, KorVec11-265, KorVec12-1131, KorVec12-1138, KorVec12-1152, KorVec12-1195, KorVec12-1200, and KorVec12-1217) identified in this study belong to the Western subtype. An envelope gene-based phylogenetic tree was divided into three distinct groups such as Far-Eastern, Siberian, and Western subtypes and it was also shown that the 10 Korean strains belonged to the same subgroup as the Western subtype, as shown in Figure 2.

4. Discussion

So far, TBEV vectors have been reported in 10 species of three genera (I. ricinus, I. persulcatus, Ixodes hexagonus, Ixodes arboricola, Ixodes ovatus, Haemaphysalis punctata, Haemaphysalis concinna, Haemaphysalis inermis, Dermacentor marginatus, and Dermacentor reticulatus) [17,18]. Among the known vectors, the total distribution of five species of TBEV vector (I. persulcatus, I. ovatus, Haemaphysalis concinna, D. marginatus, and D. reticulatus) in the ROK have been reported [19]. In our previous study, we suggested that TBE might exist in the ROK based on the following evidence. First, there was molecular evidence of TBEV infection in mammalian hosts and in potential vector ticks (H. longicornis, H. flava, H. japonica, and I. nipponensis) collected from the ROK [12,13,20], although these ticks had not been previously reported as TBEV vectors. Second, we reported on the isolation and identification of five TBEV strains from lung tissue homogenates of wild rodents captured in the ROK using in vitro and in vivo experiments [12]. Contrary to our expectations, the sequence comparisons and phylogenetic analyses based on the complete E gene or fullgenome of TBEV Korean isolates compared with other TBEV strains indicated that all the five Korean strains belonged to the Western subtype [21,22].

Based on this evidence, we carried out more extensive survey throughout the ROK for the prevalence of TBEV in ixodid ticks from various localities to identify whether TBEV is circulating and to determine the endemic areas of TBEV. A total of 13,053 ticks were divided into 1292 pools to identify for TBEV by RTnested PCR method, which detected 10 TBEV-positive pools. Sequence and phylogenetic analyses based on the envelope gene sequence revealed that the 10 Korean strains from infected ticks in this study belonged to the Western subtype, in accordance with our previous results.

The principal tick vector of the Western subtype of TBEV is I. ricinus [8], but in this study, it is reasonable to suppose that H. longicornis, H. flava, and I. nipponensis serve as the potential vectors of TBEV in the ROK. Until recently, the molecular evidence of TBEV infection was identified in ixodid ticks collected from Yangpyeong or Dongducheon in Gyeonggi-do province, Pyeongchang or Jeongseon in Gangwon-do province, and Jeju Island [13,20]. In this study, ixodid ticks such as H. longicornis, H. flava, and I. nipponensis collected from Gunsan in Jeollabuk-do province, Chuncheon or Sokcho in Gangwon-do province, and Jeju in Jeju Island were identified according to the molecular evidence of TBEV infection. These results indicated that TBEV may be endemic in these localities of theROKand H. longicornis, H. flava, and I. nipponensis may be potential vectors of the TBEV Western subtype, combined with previous findings. However, in order to prove these points, isolation of TBEV from infected vectors and characterization of TBEV isolates will be required.

In summary, we found that TBEV-infected ticks have been distributed in some localities of the ROK. These results emphasize the need for further epidemiological research of TBEV and preventive measures against the occurrence of TBE in the ROK.

Acknowledgements

This research was funded by a grant from the Korea National Institute of Health.

1. Burgdorfer W Barbour AG Hayes SF et al.. Lyme disease-a tickborne spirochetosis? Science 6;1982;216(4552). 1317−9. PMID: 7043737.Article PubMed
2. Kim CM Kim JY Yi YH et al.. Detection of Bartonella species from ticks, mites and small mammals in Korea. J Vet Sci. 12;2005;6(4). 327−34. PMID: 16293997.Article PubMed
3. Chae JS Kim CM Kim EH et al.. Molecular epidemiological study for tick-borne disease (Ehrlichia and Anaplasma spp.) surveillance at selected U.S. military training sites/installations in Korea. Ann N Y Acad Sci 6;2003;990:118−25. PMID: 12860612.Article PubMed
4. Kim CM Kim MS Park MS et al.. Identification of Ehrlichia chaffeensis, Anaplasma phagocytophilum, and A. bovis in Haemaphysalis longicornis and Ixodes persulcatus ticks from Korea. Vector Borne Zoonotic Dis Spring;2003;3(1). 17−26. PMID: 12804377.Article PubMed
5. Kim CM Yi YH Yu DH et al.. Tick-borne rickettsial pathogens in ticks and small mammals in Korea. Appl Environ Microbiol 9;2006;72(9). 5766−76. PMID: 16957192.Article PubMed PMC
6. Silber LA Soloviev VD. . Eastern tick-borne springesummer (spring) encephalitis. Am Rev Sov Med 1946;1(80). Spec Suppl..
7. Dumpis U Crook D Oksi J. . Tick-borne encephalitis. Clin Infect Dis 4;1999;28(4). 882−90. PMID: 10825054.Article PubMed
8. Ecker M Allison SL Meixner T et al.. Sequence analysis and genetic classification of tick-borne encephalitis viruses from Europe and Asia. J Gen Virol 1;1999;80(Pt. 1). 179−85. PMID: 9934700.Article PubMed
9. Lindquist L Vapalahti O. . Tick-borne encephalitis. Lancet 5;2008;371(9627). 1861−71. PMID: 18514730.Article PubMed
10. Bakhvalova VN Rar VA Tkachev SE et al.. Tick-borne encephalitis virus strains of Western Siberia. Virus Res 9;2000;70(1-2). 1−12. PMID: 11074120.Article PubMed
11. Gritsun TS Nuttall PA Gould EA. . Tick-borne flaviviruses. Adv Virus Res. 2003;61:317−71. PMID: 14714436.Article PubMed
12. Kim SY Yun SM Han MG et al.. Isolation of tick-borne encephalitis viruses from wild rodents, South Korea. Vector Borne Zoonotic Dis Spring;2008;8(1). 7−13. PMID: 18240970.Article PubMed
13. Kim SY Jeong YE Yun SM et al.. Molecular evidence for tickborne encephalitis virus in ticks in South Korea. Med Vet Entomol 3;2009;23(1). 15−20. PMID: 19239610.Article PubMed
14. Yamaguti N Tipton VJ Keegan HL et al.. Ticks of Japan, Korea, and the Ryukyu Islands. Brigham Young Univ Sci Bull Biol Ser 1971;15:1−226.
15. Ternovoi VA Kurzhukov GP Sokolov YV et al.. Tick-borne encephalitis with hemorrhagic syndrome, Novosibirsk region, Russia, 1999. Emerg Infect Dis 6;2003;9(6). 743−6. PMID: 12781020.Article PubMed PMC
16. Tamura K Peterson D Peterson N et al.. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 10;2011;28(10). 2731−9. PMID: 21546353.Article PubMed PMC
17. Suss J. . Epidemiology and ecology of TBE relevant to the production of effective vaccines. Vaccine 4;2003;21(Suppl. 1). S19−35. PMID: 12628811.Article PubMed
18. Takeda T Ito T Chiba M et al.. Isolation of tick-borne encephalitis virus from Ixodes ovatus (Acari: Ixodidae) in Japan. J Med Entomol 5;1998;35(3). 227−31. PMID: 9615539.Article PubMed
19. Lee HI. . Medical entomologydfamily acari.. Komunsa Press; Seoul: 1999. 2nd ed.pp 365−412.
20. Ko S Kang JG Kim SY et al.. of tick-borne encephalitis virus in ticks fromsouthern Korea. JVetSci 9;2010;11(3). 197−203.
21. Yun SM Kim SY Han MG et al.. Analysis of the envelope (E) protein gene of tick-borne encephalitis viruses isolated in South Korea. Vector Borne Zoonotic Dis 6;2009;9(3). 287−93. PMID: 19480604.Article PubMed
22. Yun SM Kim SY Ju YR et al.. First complete genomic characterization of two tick-borne encephalitis virus isolates obtained from wild rodents in South Korea. Virus Genes 6;2011;42(3). 307−16. PMID: 21286797.Article PubMed

Figure & Data

References

Citations

Citations to this article as recorded by

TBE in South Korea
Joon Young Song
Tick-borne encephalitis - The Book.2023;[Epub] CrossRef
Molecular detection and phylogenetic analysis of tick‐borne encephalitis virus in ticks in northeastern China
Xiaohui Li, Hongwei Ji, Di Wang, Lihe Che, Li Zhang, Liang Li, Qing Yin, Quan Liu, Feng Wei, Zedong Wang
Journal of Medical Virology.2022; 94(2): 507. CrossRef
TBE in South Korea
Song Joon Young
Tick-borne encephalitis - The Book.2022;[Epub] CrossRef
Genomic Determinants Potentially Associated with Clinical Manifestations of Human-Pathogenic Tick-Borne Flaviviruses
Artem N. Bondaryuk, Nina V. Kulakova, Ulyana V. Potapova, Olga I. Belykh, Anzhelika V. Yudinceva, Yurij S. Bukin
International Journal of Molecular Sciences.2022; 23(21): 13404. CrossRef
TBE in South Korea
Song Joon Young
Tick-borne encephalitis - The Book.2021;[Epub] CrossRef
Hard Ticks as Vectors Tested Negative for Severe Fever with Thrombocytopenia Syndrome in Ganghwa-do, Korea during 2019-2020
Kyoung Jin, Yeon-Ja Koh, Seong Kyu Ahn, Joonghee Cho, Junghwan Lim, Jaeyong Song, Jinyoung Lee, Young Woo Gong, Mun Ju Kwon, Hyung Wook Kwon, Young Yil Bahk, Tong-Soo Kim
The Korean Journal of Parasitology.2021; 59(3): 281. CrossRef
Nationwide Temporal and Geographical Distribution of Tick Populations and Phylogenetic Analysis of Severe Fever with Thrombocytopenia Syndrome Virus in Ticks in Korea, 2020
Min-Goo Seo, Byung-Eon Noh, Hak Seon Lee, Tae-Kyu Kim, Bong-Goo Song, Hee Il Lee
Microorganisms.2021; 9(8): 1630. CrossRef
Seroepidemiologic survey of emerging vector-borne infections in South Korean forest/field workers
Ji Yun Noh, Joon Young Song, Joon Yong Bae, Man-Seong Park, Jin Gu Yoon, Hee Jin Cheong, Woo Joo Kim, Nam-Hyuk Cho
PLOS Neglected Tropical Diseases.2021; 15(8): e0009687. CrossRef
European subtype of tick-borne encephalitis virus. Literature review
Yu. S. Savinova
Acta Biomedica Scientifica.2021; 6(4): 100. CrossRef
Tick-Borne Encephalitis Virus: An Emerging Ancient Zoonosis?
Andrei A. Deviatkin, Ivan S. Kholodilov, Yulia A. Vakulenko, Galina G. Karganova, Alexander N. Lukashev
Viruses.2020; 12(2): 247. CrossRef
Characterization of tick-borne encephalitis virus isolated from a tick in central Hokkaido in 2017
Yuji Takahashi, Shintaro Kobayashi, Mariko Ishizuka, Minato Hirano, Memi Muto, Shoko Nishiyama, Hiroaki Kariwa, Kentaro Yoshii
Journal of General Virology.2020; 101(5): 497. CrossRef
A history of the introduction, establishment, dispersal and management ofHaemaphysalis longicornisNeumann, 1901 (Ixodida: Ixodidae) in New Zealand
Allen C. G. Heath
New Zealand Journal of Zoology.2020; 47(4): 241. CrossRef
Four Year Surveillance of the Vector Hard Ticks for SFTS, Ganghwa-do, Republic of Korea
Myung-Deok Kim-Jeon, Seung Jegal, Hojong Jun, Haneul Jung, Seo Hye Park, Seong Kyu Ahn, Jinyoung Lee, Young Woo Gong, Kwangsig Joo, Mun Ju Kwon, Jong Yul Roh, Wook-Gyo Lee, Young Yil Bahk, Tong-Soo Kim
The Korean Journal of Parasitology.2019; 57(6): 691. CrossRef
TBE in South Korea
Joon Young Song
Tick-borne encephalitis - The Book.2019;[Epub] CrossRef
Ixodid ticks and tick-borne encephalitis virus prevalence in the South Asian part of Russia (Republic of Tuva)
Ivan Kholodilov, Oxana Belova, Ludmila Burenkova, Yuri Korotkov, Lidiya Romanova, Lola Morozova, Vitalii Kudriavtsev, Larissa Gmyl, Ilmira Belyaletdinova, Alexander Chumakov, Natalia Chumakova, Oyumaa Dargyn, Nina Galatsevich, Anatoly Gmyl, Mikhail Mikhai
Ticks and Tick-borne Diseases.2019; 10(5): 959. CrossRef
Current Status of Tick-Borne Diseases in South Korea
Jae Hyoung Im, JiHyeon Baek, Areum Durey, Hea Yoon Kwon, Moon-Hyun Chung, Jin-Soo Lee
Vector-Borne and Zoonotic Diseases.2019; 19(4): 225. CrossRef
Molecular characterization of Haemaphysalis longicornis-borne rickettsiae, Republic of Korea and China
Ju Jiang, Huijuan An, John S. Lee, Monica L. O’Guinn, Heung-Chul Kim, Sung-Tae Chong, Yanmin Zhang, Dan Song, Roxanne G. Burrus, Yuzhou Bao, Terry A. Klein, Allen L. Richards
Ticks and Tick-borne Diseases.2018; 9(6): 1606. CrossRef
Molecular detection of Rickettsia species in ticks collected from the southwestern provinces of the Republic of Korea
Yoontae Noh, Yeong Seon Lee, Heung-Chul Kim, Sung-Tae Chong, Terry A. Klein, Ju Jiang, Allen L. Richards, Hae Kyeong Lee, Su Yeon Kim
Parasites & Vectors.2017;[Epub] CrossRef
Necessity of a Surveillance System for Tick-borne Encephalitis
Seok-Ju Yoo, Ji-Hyuk Park
Osong Public Health and Research Perspectives.2017; 8(2): 155. CrossRef
Tick-borne encephalitis in Japan, Republic of Korea and China
Kentaro Yoshii, Joon Young Song, Seong-Beom Park, Junfeng Yang, Heinz-Josef Schmitt
Emerging Microbes & Infections.2017; 6(1): 1. CrossRef
Molecular detection of severe fever with thrombocytopenia syndrome and tick-borne encephalitis viruses in ixodid ticks collected from vegetation, Republic of Korea, 2014
Seok-Min Yun, Ye-Ji Lee, WooYoung Choi, Heung-Chul Kim, Sung-Tae Chong, Kyu-Sik Chang, Jordan M. Coburn, Terry A. Klein, Won-Ja Lee
Ticks and Tick-borne Diseases.2016; 7(5): 970. CrossRef
The characterization of TBEV of European subtype circulating in Siberia, Russia
I. V. Kozlova, T. V. Demina, S. E. Tkachev, Yu. S. Savinova, E. K. Doroshchenko, O. V. Lisak, Yu. P. Dzhioev, O. V. Suntsova, M. M. Verkhozina, A. I. Paramonov, N. V. Tikunova, V. I. Zlobin, D. . Ruzek
Epidemiology and Vaccine Prevention.2016; 15(6): 30. CrossRef
Detection of SFTS Virus inIxodes nipponensisandAmblyomma testudinarium(Ixodida: Ixodidae) Collected From Reptiles in the Republic of Korea
Jae-Hwa Suh, Heung-Chul Kim, Seok-Min Yun, Jae-Won Lim, Jin-Han Kim, Sung-Tae Chong, Dae-Ho Kim, Hyun-Tae Kim, Hyun Kim, Terry A. Klein, Jaree L. Johnson, Won-Ja Lee
Journal of Medical Entomology.2016; 53(3): 584. CrossRef
Epidemiological Features and Clinical Manifestations of Lyme Borreliosis in Korea during the Period 2005^|^ndash;2012
Shinje Moon, Yeongseon Hong, Kyu-Jam Hwang, Suyeon Kim, Jihye Eom, Donghyok Kwon, Ji-Hyuk Park, Seung-Ki Youn, Aeree Sohn
Japanese Journal of Infectious Diseases.2015; 68(1): 1. CrossRef
Characteristics and Factors Associated with Death among Patients Hospitalized for Severe Fever with Thrombocytopenia Syndrome, South Korea, 2013
Jaeseung Shin, Donghyok Kwon, Seung-Ki Youn, Ji-Hyuk Park
Emerging Infectious Diseases.2015; 21(10): 1704. CrossRef
Review: Sentinels of tick-borne encephalitis risk
Maren Imhoff, Peter Hagedorn, Yesica Schulze, Wiebke Hellenbrand, Martin Pfeffer, Matthias Niedrig
Ticks and Tick-borne Diseases.2015; 6(5): 592. CrossRef
Louping ill virus (LIV) in the Far East
Galina N. Leonova, Ilya G. Kondratov, Olga S. Maystrovskaya, Ikuo Takashima, Sergei I. Belikov
Archives of Virology.2015; 160(3): 663. CrossRef
Prevalence of severe fever with thrombocytopenia syndrome virus in Haemaphysalis longicornis ticks in South Korea
Sun-Whan Park, Bong Gu Song, E-Hyun Shin, Seok-Min Yun, Myung-Guk Han, Mi Yeoun Park, Chan Park, Jungsang Ryou
Ticks and Tick-borne Diseases.2014; 5(6): 975. CrossRef

PubReader
Cite

Cite

export Copy Format

Close

XML Download

Figure

Related articles

Trends of legionellosis reported in Jeju Province, Republic of Korea, 2015–2022

Species	Developmental stages	Number of ticks	Number of pools	Positive pools	MIR (%)^a

Haemaphysalis longicornis	Larvae^b	350	22	0	0
	Nymph^c	10,436	460	6	0.06
	Adult (male)^d	221	106	0	0
	Adult (female)^d	849	329	1	0.12
	Subtotal	11,856	917	7	0.06
Haemaphysalis flava	Larvae	197	11	0	0
	Nymph	710	163	0	0
	Adult (male)	108	79	1	0.93
	Adult (female)	134	91	1	0.75
	Subtotal	1,149	344	2	0.17
Ixodes nipponensis	Larvae	0	0	0	0
	Nymph	23	9	1	4.35
	Adult (male)	8	8	0	0
	Adult (female)	11	11	0	0
	Subtotal	42	28	1	2.38
Ixodes persulcatus	Larvae	6	3	0	0
	Nymph	0	0	0	0
	Adult (male)	0	0	0	0
	Adult (female)	0	0	0	0
	Subtotal	6	3	0	0
Total	Larvae	553	36	0	0
	Nymph	11,169	632	7	0.06
	Adult (male)	337	193	1	0.30
	Adult (female)	994	431	2	0.20
	Total	13,053	1,292	10	0.08

Strain	Subtype	Source of virus	Geographical origin	Year of isolation	GenBank accession no.

Hypr	Western	Human blood	Czech Republic	1953	X75286
Neudoerfl	Western	Ixodes ricinus	Austria	1971	U27495
K23	Western	I. ricinus	Germany	1975	AF091010
Abesettarov	Western	Human blood	Russia	1951	AF091005
Kem I	Western	I. ricinus	Hungary	1952	AF091011
KrM 93	Western	A. agrarius	Republic of Korea	2006	EU276109
KrM 213	Western	A. agrarius	Republic of Korea	2006	EU276110
KrM 215	Western	A. agrarius	Republic of Korea	2006	EU276111
KrM 216	Western	A. agrarius	Republic of Korea	2006	EU276112
KrM 219	Western	A. agrarius	Republic of Korea	2006	EU276113
Oshima 5-10	Far-Eastern	Dog blood	Japan	1995	AB001026
Sofjin-HO	Far-Eastern	Human brain	Russia	1937	AB022703
Senzhang	Far-Eastern	Human brain	China	1953	AY174188
Oshima I-1	Far-Eastern	Ixodes ovatus	Japan	1996	AB022292
Oshima 5-11	Far-Eastern	Dog blood	Japan	1995	AB022290
KH98-2	Far-Eastern	Ixodes persulcatus	Russia	1998	AB022295
KH98-5	Far-Eastern	I. persulcatus	Russia	1998	AB022296
KH98-10	Far-Eastern	I. persulcatus	Russia	1998	AB022297
Crimea	Far-Eastern	I. persulcatus	Ukraine	1987	AF091008
D1283	Far-Eastern	Human brain	Russia	1998	AB049347
RK1424	Far-Eastern	I. persulcatus	Latvia	1977	AF091015
T-blood	Far-Eastern	Human blood	Russia	1939	AF091019
VL99-m11	Far-Eastern	I. persulcatus	Russia	1999	AB049345
N132	Far-Eastern	I. persulcatus	Russia	1979	AF091013
Vasilchenko	Siberian	Human blood	Russia	1969	M97659
Aina	Siberian	Human blood	Russia	1963	AF091006
IR99-1m1	Siberian	I. persulcatus	Russia	1999	AB049348
IR99-1m4	Siberian	I. persulcatus	Russia	1999	AB049349
IR99-2m3	Siberian	I. persulcatus	Russia	1999	AB049350
IR99-2m7	Siberian	I. persulcatus	Russia	1999	AB049351
IR99-2f7	Siberian	I. persulcatus	Russia	1999	AB049352
IR99-2f13	Siberian	I. persulcatus	Russia	1999	AB049353

Collection site	Larvae	Nymph	Male	Female	Total	Larvae	Nymph	Male	Female	Total

	Haemaphysalis flava: no. infected/no. examined (%)					Haemaphysalis flava: no. infected/no. examined (%)

Gyeonggi-do
Yangpyeong	–	0/12(0)	–	0/3(0)	0/15(0)	–	0/238(0)	0/4(0)	0/9(0)	0/251(0)
Gimpo	–	–	0/2(0)	0/1(0)	0/3(0)	–	0/4(0)	–	0/1(0)	0/5(0)
Incheon
Ganghwa	–	0/7(0)	–	0/1(0)	0/8(0)	–	0/523(0)	0/47(0)	0/43(0)	0/613(0)
Gangwon-do
Chuncheon	–	0/64(0)	1/6(16.67)	0/5(0)	1/75(1.33)	–	2/354(0.56)	–	0/4(0)	2/358(0.56)
Pyeongchang	0/17(0)	0/6(0)	0/11(0)	0/11(0)	0/45(0)	0/147(0)	0/1(0)	–	–	0/148(0)
Sokcho	–	0/125(0)	0/3(0)	1/6(16.67)	1/134(0.75)	–	1/122(0.82)	0/1(0)	0/5(0)	1/128(0.78)
Chungcheongbuk-do
Boeun	0/17(0)	0/217(0)	0/52(0)	0/59(0)	0/506(0)	0/190(0)	0/3598(0)	0/25(0)	0/353(0)	0/4166(0)
Chungcheongnam-do
Boryeong	–	0/18(0)	0/3(0)	0/5(0)	0/26(0)	–	0/436(0)	0/14(0)	0/27(0)	0/477(0)
Cheonan	–	0/1(0)	–	0/1(0)	0/2(0)	–	0/232(0)	–	0/41(0)	0/273(0)
Gongju	–	0/23(0)	0/2(0)	0/4(0)	0/29(0)	0/1(0)	0/359(0)	0/12(0)	0/19(0)	0/391(0)
Jeollabuk-do
Muju	–	0/14(0)	0/1(0)	0/3(0)	0/18(0)	–	0/29(0)	–	–	0/29(0)
Gunsan	–	0/42(0)	0/10(0)	0/7(0)	0/59(0)	–	1/516(0.19)	–	0/18(0)	1/534(0.19)
Jeonju	–	0/3(0)	–	–	0/3(0)	–	0/9(0)	–	0/2(0)	0/11(0)
Jeollanam-do
Boseong	–	0/11(0)	0/1(0)	0/2(0)	0/14(0)	–	0/269(0)	0/3(0)	0/18(0)	0/290(0)
Gokseong	–	0/5(0)	–	0/2(0)	0/7(0)	–	0/109(0)	0/1(0)	0/32(0)	0/142(0)
Wando	–	0/3(0)	0/2(0)	0/1(0)	0/6(0)	–	0/38(0)	0/28(0)	0/47(0)	0/113(0)
Gyeongsangbuk-do
Uiseong	–	0/21(0)	0/2(0)	0/2(0)	0/25(0)	–	0/76(0)	0/1(0)	0/2(0)	0/79(0)
Yeongju	–	0/57(0)	0/1(0)	0/5(0)	0/63(0)	–	0/83(0)	–	–	0/83(0)
Yeongyang	–	0/12(0)	–	–	0/12(0)	–	0/422(0)	0/14(0)	0/81(0)	0/517(0)
Uljin	–	0/15(0)	0/1(0)	0/3(0)	0/19(0)	–	0/574(0)	0/22(0)	0/69(0)	0/665(0)
Gyeongsangnam-do
Haman	–	0/1(0)	–	–	0/1(0)	–	0/52(0)	0/9(0)	0/33(0)	0/94(0)
Hamyang	–	0/3(0)	0/3(0)	0/2(0)	0/8(0)	–	0/1(0)	0/1(0)	–	0/2(0)
Miryang	–	0/6(0)	0/6(0)	0/7(0)	0/19(0)	–	0/80(0)	–	0/1(0)	0/81(0)
Jeju-do
Jeju	–	0/35(0)	–	–	0/35(0)	0/6(0)	2/1,418(0.14)	0/25(0)	1/26(3.85)	3/1,475(0.20)
Seogwipo	0/2(0)	0/9(0)	0/2(0)	0/4(0)	0/17(0)	0/6(0)	0/893(0)	0/14(0)	0/18(0)	0/931(0)
Total	0/197(0)	0/710(0)	0/710(0) 1/108(0.93)	1/134(0.75)	2/1,149(0.17)	0/350(0)	6/10,436(0.06)	0/221(0)	1/849(0.12)	7/11,856(0.06)

Gyeonggi-do
Yangpyeong	–	–	–	–	–	–	–	–	–	–
Gimpo	–	–	–	–	–	–	–	–	–	–
Incheon
Ganghwa	–	–	–	–	–	–	–	–	–	–
Gangwon-do
Chuncheon	–	0/1(0)	–	0/1(0)	0/2(0)	–	–	–	–	–
Pyeongchang	–	–	–	–	–	0/6(0)	–	–	–	0/6(0)
Sokcho	–	1/18(5.56)	0/1(0)	–	1/19(5.26)	–	–	–	–	–
Chungcheongbuk-do
Boeun		0/2(0)	0/4(0)	0/8(0)	0/14(0)	–	–	–	–	–
Chungcheongnam-do
Boryeong	–	–	0/1(0)	–	0/1(0)	–	–	–	–	–
Cheonan	–	–	–	–	–	–	–	–	–	–
Gongju	–	0/1(0)	-	–	0/1(0)	–	–	–	–	–
Jeollabuk-do
Muju		–	–	0/1(0)	0/1(0)	–	–	–	–	–
Gunsan		0/1(0)	–	–	0/1(0)	–	–	–	–	–
Jeonju		–	–	–	–	–	–	–	–	–
Jeollanam-do
Boseong	–	–	–	–	–	–	–	–	–	–
Gokseong	–	–	–	–	–	–	–	–	–	–
Wando	–	–	–	–	–	–	–	–	–	–
Gyeongsangbuk-do
Uiseong	–	–	0/1(0)	-	0/1(0)	–	–	–	–	–
Yeongju	–	–	0/1(0)	0/1(0)	0/2(0)	–	–	–	–	–
Yeongyang	–	–	–	–	–	–	–	–	–	–
Uljin	–	–	–	–	–	–	–	–	–	–
Gyeongsangnam-do
Haman	–	–	–	–	–	–	–	–	–	–
Hamyang	–	–	–	–	–	–	–	–	–	–
Miryang	–	–	–	–	–	–	–	–	–	–
Jeju-do
Jeju	–	–	–	–	–	–	–	–	–	–
Seogwipo	–	–	–	–	–	–	–	–	–	–
Total	-	1/23(4.35)	0/8(0)	0/11(0)	1/42(2.38)	0/6(0)	–	–	–	0/6(0)