Tick surveillance in Korea Kim, Heung Chul PhD

Tick surveillance in Korea Kim, Heung Chul PhD 5 th Medical Detachment, 168 th Multifunctional Medical Brigade, 65 th Medical Brigade, Unit # 15247, APO AP 96206-5247

Tick-borne Diseases Lyme disease Tick-Borne Encephalistis (TBE) Spotted Fever Group (SFG) Rickettsioses Typhoid Group (TG) Rickettsioses Ehrlichiosis Bartonellosis Anaplasmosis Tick bite

Environmental Changes Following the Korean War Korea is devastated by WWII and politically divided. June 1950, North Korean forces attack South Korea Armistice signed in 1953, 38 th parallel 4 Km wide DMZ Modern South Korea Numerous multistory apartments Booming economy Forested hillsides/mountains Increased wildlife populations Reduced agriculture

Life cycle (I) One-host tick Two-host tick

Life cycle (II) Three-host tick

Haemaphysalis and Ixodes

Tick Surveillance Rodent ticks Drag ticks Migratory bird ticks Mammals ticks Bat ticks

Rodents Myodes regulus Apodemus agrarius Rattus rattus Apodemus peninsulae Crocidura lasiura Rattus norvegicus

(1) Rodent tick surveillance Gangwon Province Gyeonggi Province (Northern part) Gyeonggi Province (Southern part)

Rodent tick surveillance, 2004-2008

Systematic & Applied Acarology 15 (2): 100-108 (2010) ISSN 1362-1971 Tick surveillance of small mammals captured in Gyeonggi and Gangwon Provinces, Republic of Korea, 2004-2008 HEUNG CHUL KIM 1, SUNG TAE CHONG 1, WILLIAM J. SAMES 2, PETER V. NUNN 1, STEPHEN P. WOLF 3, RICHARD G. ROBBINS 4, 6 & TERRY A. KLEIN 5 1 5 th Medical Detachment, 168 th Multifunctional Medical Battalion, 65 th Medical Brigade, Unit 15247, APO AP 96205-5247, U.S.A. 2 OD/AFPMB, Walter Reed Army Medical Center, Washington, DC 20307-5001, U.S.A. 3 Medical Entomology Services, Detachment 3, US Air Force School of Aerospace Medicine, Unit 5213, Kadena AB, Okinawa, APO AP 96368-5213, Japan 4 ISD/AFPMB, Walter Reed Army Medical Center, Washington, DC 20307-5001, U.S.A. 5 Force Health Protection and Preventive Medicine, 65 th Medical Brigade/U.S. Army MEDDAC-Korea, Unit 15281, APO AP 96205-5281, U.S.A. Abstract A total of 4,575 ticks were collected from 5,953 small mammals captured from March 2004 to December 2008 at 19 military training areas and 6 US military installations, Gyeonggi and Gangwon Provinces, Republic of Korea. Ixodes nipponensis (98.9%; 753 nymphs, 3,771 larvae) was the most frequently collected tick, found on six of the 11 small mammal species captured, followed by Ixodes pomeranzevi (1.1%; 17 females, 9 nymphs, 24 larvae) found on three species. While only one T. sibiricus was collected, it was infested with 44 ticks, with an infestation rate of 100.0%, followed by Rattus norvegicus (16.7%, n=18), A. agrarius (14.6%, n=5,397), Crocidura lasiura (7.5%, n=265), Microtus fortis (7.3%, n=82), Myodes regulus (5.7%, n=53), and Micromys minutus (4.8%, n=63). No ticks were collected from Apodemus peninsulae (n=3), Mus musculus (n=58), Tscherskia triton (n=12), and Mogera wogura (n=1). Key words: Ixodes nipponensis, Ixodes pomeranzevi, Haemaphysalis flava, hosts, distribution, seasonality

Ixodes pomerantzevi Serdyukova, 1941

(2) Drag tick surveillance Forest Area Warrior Base North Carolina Range ROK Obstacle Course near Story Range

Drag ticks 2004-2005 Number Collected Adult Male Adult Female KOR04-(1-90) Larvae Nymphs H. flava 5687 2776 2746 85 80 H. longicornis 14186 9616 3885 213 472 I. nipponensis 968 778 152 23 15 TOTAL 20841 13170 6783 321 567 KOR05-(1-46) Number Collected Larvae Nymphs Adult Male Adult Female H. longicornis 3549 565 2662 139 183 H. flava 2034 1331 620 46 37 I. nipponensis 237 35 88 111 3 TOTAL 5820 1931 3370 296 223

2006 Cheorwon Yanggu Dongducheon Inje Hwacheon Chuncheon Pocheon Gangneung Hongcheon Gyeonggi P. Pyeongtaek Chungcheongnam P. Hoengseong Jeongseon Pyeongchang Wonju Gangwon P. Chungcheongbuk P. Chungju Mungyeong Gyeongsangbuk P. Sangju Gunwi Jeollabuk P. Waegwan Daegu Gyeongsangnam P. KOR06-(1-56) Jeollanam P. KOR06-154(1-4) Total Larvae Nymphs Adult (M) Adult (F) H. Flava 589 117 367 60 45 H. longicornis 414 252 159 0 3 H. japonica 13 0 0 8 5 I. nipponensis 41 1 7 25 8 I. persulcatus 7 0 3 1 3 TOTAL 1064 370 536 94 64 Jeju

2007 KOR07-(1-11) Total Larvae Numphs Adults(M) Adults(F) longicornis 41 0 41 0 0 flava 27 0 21 2 4 nipponensis 1 0 1 0 0 TOTAL 69 0 63 2 4 Jeollabuk P. Gyeongsangbuk P. (Collection #1-11) 36 o Gyeongsangnam P. (Collection #70-88) Jeollanam P. (Collection #89-113) KOR07-(70-113) Total Larvae Numphs Adults(M) Adults(F) longicornis 2979 44 2923 6 6 flava 1004 0 880 54 70 nipponensis 23 0 11 7 5 phasiana 72 0 70 0 2 testudinarium 25 0 24 1 0 TOTAL 4103 44 3908 68 83 34 o 126 o 128 o 130 o

Jeju (Collection #12-69) 25 65 68 46 52 KOR07-(12-68) Total Larvae Numphs Adults(M) Adults(F) longicornis 1964 21 1936 1 6 flava 492 7 384 52 49 phasiana 144 0 144 0 0 turdus 16 6 9 0 1 TOTAL 2616 34 2473 53 56

2008 Pocheon Cheorwon Gyeonggi P. Gangwon P. Chungcheongnam P. Pyeongtaek Jeollabuk P. Chungcheongbuk P. Danyang Chungju Gyeongsangbuk P. Gunwei Yeongcheon Pohang Angang Gyeongju Gyeongsangnam P. Jeollanam P. KOR08-(1-19) Total Larvae Numphs Adults(M) Adults(F) longicornis 1494 1290 145 18 41 flava 1092 766 229 65 32 nipponensis 39 26 6 6 1 TOTAL 2625 2082 380 89 74 Jeju

2009 Ganghwa Gimpo Chungcheongnam P. Pocheon Gyeonggi P. Pyeongtaek Seosan Cheorwon Chungcheongbuk P. Chuncheon Hongseong Wonju Jaecheon Chungju Gangwon P. Gyeongsangbuk P. Jeollabuk P. Gochang Gyeongsangnam P. Jeju Jeollanam P. Muan Haenam KOR09-(1-51) Total Larva Nymph Adult (M) Adult (F) H. flava 4039 2870 1039 80 50 H. longicornis 4706 2936 1707 19 44 I. nipponensis 528 442 80 4 2 I. turdus 1 0 1 0 0 A. testudinarium 1 0 1 0 0 TOTAL 9275 6248 2828 103 96

Haemaphysalis (Ornithophysalis)phasiana Saito, Hoogstraal and Wassef 1974

6 6 독수리 6 저어새 (3) Bird tick surveillacne 뒷부리도요큰기러기 5 두루미 1 4 재두루미 5 7 8 8115 흑두루미 2 2 큰기러기 3 쇠기러기 범례 1 뒷부리도요 2 큰기러기 3 쇠기러기 4 재두루미 5 두루미 6 독수리 7 흑두루미 8 저어새 9 쇠제비갈매기 10 붉은어깨도요 11 큰뒷부리도요 12 알락꼬리마도요 13 꼬까도요 14 붉은가슴도요 15 민물도요 9 1 10 1112 뒷부리도요 10 붉은어깨도요 큰뒷부리도요 한국에도래하는철새들의이동경로 1112 101412 11121314 알락꼬리마도요

Heuksan-do FIGURE 1. Location of Mokpo ( ) and Hong Island, collection site of ticks removed from migratory birds, Jeollanam Province, Korea.

A B FIGURE 3. Tick-infested birds on Hong-do. (A) Emberiza elegans with Haemaphysalis flava attached at neck; (B) Zoothera sibirica with Ixodes nipponensis attached below eye.

Haemaphysalis ornithophila Hoogstraal and Kohls 1959

FIGURE 2. Monthly changes in total number of banded migratory birds, and ticks collected from them, on Hong-do, Jeollanam Province, Korea.

(4) Mammal tick surveillance Host Name Tick species Larvae Nymphs Adult Adult Number tested Male Female TOTAL Sciuridae Tamias sibiricus 1 Ixodes pomeranzevi 24 5 0 15 44 2 Haemaphysalis flava 0 1 0 0 1 Talpidae Mogera wogera 1-0 0 0 0 0 Equidae Equus caballus 1 Haemaphysalis longicornis 0 0 0 1 1 Canis lupus familiaris 3 Ixodes nipponensis 0 0 0 1 1 Canidae Cervidae Nyctereutes procyonoides 1 Hydropotes inermis 40 Haemaphysalis longicornis 0 0 0 9 9 Haemaphysalis flava 14 43 32 16 105 Haemaphysalis longicornis 77 179 116 86 458 Haemaphysalis flava 15 29 65 37 146 Haemaphysalis japonica 0 0 1 0 1 Ixodes persulcatus 1 0 15 24 40 Ixodes nipponensis 0 0 6 6 12 Felidae Capreolus pygargus 4 Haemaphysalis longicornis 0 7 6 12 25 Haemaphysalis flava 0 0 6 4 10 Ixodes nipponensis 0 0 0 1 1 Prionalurus bengalensis 2 Ixodes nipponensis 0 0 2 4 6 Felis catus 21 Ixodes persulcatus 0 0 0 2 2 Ixodes nipponensis 0 0 14 34 48 Mustela siberica 1 Ixodes nipponensis 0 0 1 2 3 Mustelidae Meles leucurus 1 Haemaphysalis longicornis 0 0 1 6 7 TOTAL 78 131 264 265 260 920

Mammal ticks Tick species Larvae Nymphs Male Female TOTAL Haemaphysalis longicornis 77 186 123 114 500 Haemaphysalis flava 29 73 103 57 262 Haemaphysalis japonica 0 0 1 0 1 Ixodes persulcatus 1 0 15 26 42 Ixodes nipponensis 0 0 23 48 71 Ixodes pomerantzevi 24 5 0 15 44 TOTAL 131 264 265 260 920

Mammal ticks Bat ticks Tamias sibiricus Equus caballus Canis lupus familiaris Nyctereutes procyonoides Hydropotes inermis Capreolus pygargus Prionalurus bengalensis Felis catus Mustela siberica Meles leucurus

Mammal ticks (Korean water deer) Seoul (5/1) 100.0 33.5 53.2 1.7 Gangwon-do (173/9) 42.9 57.1 TOTAL 1.8 22.4 69.7 Chungcheongbuk-do (7/2) Daejeon (29/1) 86.2 80.0 Gyeongsangbuk-do (10/2) 2.4 75.0 21.7 3.3 88.7 Ulsan (373/18) Jeollanam-do (60/6) Haemaphysalis longicornis Haemaphysalis flava Haemaphysalis japonica Ixodes persulcatus Ixodes nipponensis

(5) Bat tick surveillance Host species Toal Number of bats No. infested Tick species Chiroptera ( 익수목 ) Rhinolophidae ( 관박쥐과 ) Vespertilionidae ( 애기박쥐과 ) 관박쥐 Rhinolophus ferrumequinum 45 6 Ixodes vespertilionis(3), Ixodes simplex(3) 문둥이박쥐 Eptesicus serotinus 12 0 - 집박쥐 Pipistrellus abramus 10 0 - 검은집박쥐 Hypsugo alaschanicus 9 0 - 우수리박쥐 Myotis petax 14 0 - 붉은박쥐 Myotis formosus 1 0 - 쇠큰수염박쥐 Myotis ikonnikovi 5 0 - 큰발윗수염박쥐 Myotis macrodactylus 12 0 - 긴가락박쥐 Myiniopterus schreibersii 30 1 Ixodes simplex(1) 관코박쥐 Murina leucogaster 3 0 - TOTAL 141 7 (4.96%) 7 ticks

Hwacheon Gangwon P. Gyeonggi P. Chungcheongbuk P. Chungcheongnam P. Gongju Daejeon Danyang Gyeongsangbuk P. Jeollabuk P. Shinan Jeollanam P. Haenam Gyeongsangnam P. Tongyeong Jeju Ixodes vespertilionis Ixodes simplex Bat collection sites

Ixodes simplex Neumann, 1906

Summary Tick species Rodents Drag Birds Mammanls Bats Haemaphysalis longicornis 29429 21 500 Haemaphysalis flava 12 14964 52 262 Haemaphysalis japonica 13 1 Haemaphysalis phasiana* 216 Haemaphysalis ornithophila* 2 Ixodes nipponensis 6748 1837 28 71 Ixodes persulcatus 7 42 Ixodes turdus 17 147 Ixodes pomerantzevi* 6 44 Ixodes granulatus 7 Ixodes vespertilionis 3 Ixodes simplex* 4 Amblyomma testudinarium 26 * New record TOTAL 6773 46509 250 920 7

Summary Tick species Rodents Drag Birds Mammanls Bats Haemaphysalis longicornis X X X Haemaphysalis flava X X X X Haemaphysalis japonica X X Haemaphysalis phasiana* X Haemaphysalis ornithophila* X Ixodes nipponensis X X X X Ixodes persulcatus X X Ixodes turdus X X Ixodes pomerantzevi* X X Ixodes granulatus X Ixodes vespertilionis Ixodes simplex* Amblyomma testudinarium X X X * New record

Publications Kim, Heung Chul, Sung Tae Chong, William J. Sames, Peter V. Nunn, Stephen P. Wolf, and Terry A. Klein, 2010. Tick surveillance of small mammals captures at Gyeonggi and Gangwon Provinces in Republic of Korea, 2004-2008. Systematic and Applied Acarology 15(2): 100-108 Ko, Sungjin, Jun-Gu Kang, Su Yeon Kim, Terry A. Klein, Heung Chul Kim, Sung Tae Chong, William J. Sames, Seok Min Yun, Young Ran Ju, and Joon Seok Chae, 2010. Prevalence of Tick-borne Encephalitis Virus from ticks in Southern Republic of Korea. Journal of Veterinary Science 11(3): 197-203. Kim, Heung Chul, Sung Jin Ko, Sung Tae Chong, Chang Yong Choi, HyunYoung Nam, HeeYoung Chae, Terry A. Klein, William J. Sames, Richard G. Robbins, and Joon Seok Chae, 2009. Migratory bird tick surveillance, including a new record of Haemaphysalis ornithophila Hoogstraal and Kohls, 1959 (Acari: Ixodidae) at Hong Island, Republic of Korea. Systematic and Applied Acarology 14(1): 3-10. Kim, Heung Chul, Jin Han Kim, Yeong Seok Jo, Sung Tae Chong, William J. Sames, Richard G. Robbins, and Terry A. Klein, 2009. Records of Ixodes pomerantzevi Serdyukova, 1941 (Acari: Ixodidae) from small mammals in northern Gyeonggi and Gangwon Provinces, Republic of Korea. Systematic and Applied Acarology 14(2): 129-135. Sames, William J., Heung Chul Kim, Sung Tae Chong, In Yong Lee, Dmitry A. Apanaskevich, Richard G. Robbins, Joshua Bast, Robert Moore, and Terry A. Klein, 2008. Haemaphysalis phasiana (Acari: Ixodidae) in the Republic of Korea: Two Province Records and Habitat Descriptions. Systematic and Applied Acarology 13(1): 43-50. Chae, Joon-Seok, Do-Hyeon Yu, Smriti Shringi, Terry A. Klein, Heung Chul Kim, Sung-Tae Chong, In-Yong Lee, and Janet Foley, 2008. Microbial pathogens in ticks, rodents and a shrew in northern Gyeonggi-do near the DMZ, Korea. Journal of Veterinary Science 9 (3): 285-293. Chae, Joon-Seok, Jennifer Zipper Adjemian, Heung Chul Kim, Sung-Jin Ko, Terry A. Klein, and Janet Foley, 2008. Predicting the emergence of tick-borne infections based on climate changes in Korea. Vector-Borne and Zoonotic Diseases 8(2): 265-275. Kim, Chul Min, Ying Hua Yi, Do Hyeon Yu, Mi Jin Lee, Mae Rim Cho, Atul R. Desai, Smriti Shringi, Terry A. Klein, Heung Chul Kim, Jin Won Song, Sung Tae Chong, Monica L. O Guinn, John S. Lee, In Yong Lee, Jin Ho Park, Janet Foley, and Joon Seok Chae, 2006. Tick-borne rickettsial pathogens in ticks and small mammals in Korea. Applied and Environmental Microbiology 72(9): 5766-5776. Kim, Chul Min, Ji Young Kim, Ying Hua Yi, Mi-Jun Lee, Mae Rim Cho, Devendra H. Shah, Terry A. Klein, Heung Chul Kim, Jin Won Song, Sung Tae Chong, Monica L. O Guinn, John S. Lee, In Yong Lee, Jin Ho Park, and Joon Seok Chae, 2005. Detection of Bartonella species from ticks and small mammals in Korea. Journal of Veterinary Science 6(4):327-334.

Systematic & Applied Acarology 14(2): 129 135 (2009) ISSN 1362-1971 Records of Ixodes pomerantzevi Serdyukova, 1941 (Acari: Ixodidae) from small mammals in northern Gyeonggi and Gangwon Provinces, Republic of Korea HEUNG CHUL KIM 1, JIN HAN KIM 2, YEONG SEOK JO 2, SUNG TAE CHONG 1, WILLIAM J. SAMES 3, TERRY A. KLEIN 4 & RICHARD G. ROBBINS 5,6 1 5th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO AP 96205-5247 U.S.A. 2 Division of Vertebrates Research, National Institute of Biological Resources, Incheon, 404-170 Republic of Korea 3 8725 John J. Kingman Road, Suite 2639 DES-E, Fort Belvoir, VA 22060-6221 U.S.A. 4 Force Health Protection and Preventive Medicine, 65th Medical Brigade/U.S. Army MEDDAC-Korea, Unit 15281, APO AP 96205-5281 U.S.A. 5 DPMIAC/AFPMB, Walter Reed Army Medical Center, Washington, DC 20307-5001, U.S.A. 6 Corresponding author. E-mail: richard.robbins@osd.mil Abstract During 2008, small mammals were captured and examined for ticks at Chipori (Gangwon Province) and Nightmare (Gyeonggi Province) Ranges near the Demilitarized Zone, Republic of Korea (ROK). Ixodes nipponensis Kitaoka and Saito (75 nymphs, 835 larvae) was collected from Apodemus agrarius (Pallas), Micromys minutus (Pallas), and Crocidura lasiura Dobson, while Ixodes pomerantzevi Serdyukova (2 females, 4 nymphs) was collected only from A. agrarius. Separately, I. pomeranzevi (15 females, 5 nymphs, 24 larvae) was collected from Tamias sibiricus (Laxmann) near Bidulginang Falls (Gyeonggi Province). This is the first record of I. pomeranzevi from Apodemus agrarius in the ROK. Key words: Ixodes pomeranzevi, Ixodes nipponensis, hosts, distribution, seasonality

Systematic & Applied Acarology 14 (1): 3-10 (2009) ISSN 1362-1971 Migratory Bird Tick Surveillance, including a new record of Haemaphysalis ornithophila Hoogstraal and Kohls 1959, (Acari: Ixodidae) at Hong-do (Island), Republic of Korea HEUNG CHUL KIM 1, SUNG JIN KO 2, CHANG YONG CHOI 3, HYUN YOUNG NAM 3, HEE YOUNG CHAE 3, SUNG TAE CHONG 1, TERRY A. KLEIN 4, WILLIAM J. SAMES 5, RICHARD G. ROBBINS 6, JOON- SEOK CHAE 2* 1 5 th Medical Detachment, 168 th Multifunctional Medical Battalion, 65 th Medical Brigade, USAMEDDAC-Korea, Unit 15247, APO AP 96205-5247 2 Veterinary Internal Medicine, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Korea. 3 Korea Migratory Birds Center, National Park Research Institute, Korea National Park Service, Shinan-Gun, Jeonnam Province 535-916, Korea 4 Force Health Protection, 65 th Medical Brigade, USAMEDDAC-Korea, Unit 15281, APO AP 96205-5281 5 8725 John J. Kingman Road, Suite 2639 DES-E, Fort Belvoir, VA 22060-6221 6 DPMIAC/AFPMB, Walter Reed Army Medical Center, Washington, DC 20307-5001 Abstract Tick surveillance of migratory birds was conducted in 2008 at Hong-do (Island), Jeonnam Province, Korea. Seventy-seven ticks belonging to two genera and four species, Ixodes turdus Nakatsuji (51 ticks), Haemaphysalis flava Neumann (21), I. nipponensis Kitaoka and Saito (3), and H. ornithophila Hoogstraal and Kohls (2) were collected from 12 species of birds belonging to nine genera. Two male H. ornithophila, an uncommonly collected species, were collected from a White s ground thrush, Zoothera dauma at Hong-do. H. ornithophila is distributed throughout much of Southeast Asia where it was transported to Korea during the spring migration of the White s ground thrush to its breeding ground in Russia. This is the first report of H. ornithophila Hoogstraal and Kohls 1959 in Korea and has implications for the introduction of exotic tick species. Key words: Haemaphysalis ornithophila, Ixodes, bird ticks, migratory bird, Korea

Journal of Veterinary Science 11 (3): 197-203 (2010) Prevalence of Tick-borne Encephalitis Virus from Ticks from Southern Korea Sungjin Ko 1, Jun-Gu Kang 1, Su Yeon Kim 2, Heung-Chul Kim 3, Terry A. Klein 4, Sung-Tae Chong 4, William J. Sames 5, Seok-Min Yun 2, Young-Ran Ju 2*, and Joon-Seok Chae 1* 1 Veterinary Internal Medicine, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul 151-742, Republic of Korea 2 Division of Arboviruses, Center for Immunology and Pathology, Korea National Institute of Health, Seoul, 122-701, Republic of Korea 3 5 th Medical Detachment, 168 th Multifunctional Medical Battalion, 65 th Medical Brigade, Unit #15247, APO AP 96205-5247, Seoul, Republic of Korea 4 Force Health Protection and Preventive Medicine, 65 th Medical Brigade, Unit #15281, APO AP 96205-5281, Seoul, Republic of Korea 5 Defense Logistics Agency, 8725 John J. Kingman Road, Suite 2639 Attn: DES-EQ, Fort Belvoir, VA 22060-6221 Abstract The prevalence of tick-borne encephalitis virus (TBEV) in southern Republic of Korea (ROK) was determined by collecting ticks using tick drags. A total of 4,077 of 6,788 ticks collected were pooled (649 pools) according to collection site, species, and developmental stage and assayed for TBEV. The TBEV protein E and NS5 gene fragments were detected using RT-nested PCR in six pools of nymphs collected from Jeju-do (2,491 ticks). The minimum field detection rates for TBEV were 0.17% and 0.14% for Haemaphysalis longicornis and H. flava nymphs, respectively. The 252 bp NS5 and 477 bp protein E gene amplicons were sequenced. Phylogenetic analysis showed that the NS5 and protein E genes of the Jeju strain were clustered with Western subtype (98% and 99.4% identity, respectively). The Western subtype of TBEV is endemic in the ROK, including Jeju-do, and vector and zoonotic host susceptibility to TBEV is required to understand its potential impact on public health. Key words: Tick-borne encephalitis virus, Haemaphysalis longicornis, Haemaphysalis flava, tick, Republic of Korea.

작은소참진드기 (Haemaphysalis longicornis)

개피참진드기 (Haemaphysalis flava)

일본참진드기 (Ixodes nipponensis)