Tick-borne disease surveillance in the US military in Korea

Terry A. Klein,Heung-Chul Kim,William J. Sames 한국응용곤충학회 2008 한국응용곤충학회 학술대회논문집 Vol.2008 No.10

Ecological changes affecting vector-borne diseases in Korea

Terry A. Klein,Heung Chul Kim 한국응용곤충학회 2009 한국응용곤충학회 학술대회논문집 Vol.2009 No.10

Ecological changes, both man-made and natural, have changed the landscape of the Republic of Korea following the end of Japanese occupation at the end of World War II (1939-1945). During the Japanese occupation, forested hillsides were cleared and wood products shipped to Japan, leaving the hills and mountains largely covered by grasses and other shrub vegetation. Following WWII, the country of Korea was divided into North and South Koreas, with North Korea under communist powers, while South Korea was established as a democratic government. In South Korea poverty was rampant and local populations scavenged for wood for cooking and heating during the cold winters. Just as economic conditions were increasing, South Korea was attached by North Korea, beginning a long drawn-out conflict from 1950 to the summer of 1953, whereby an armistice was signed and an often uneasy peace between the two countries continues today. Again, the Republic of Korea emerged from a War as an impoverished country with treeless country sides, hills, and mountains. In the 1960’s, president Chung-Hee Park established a tree planting policy to reestablish long-ago lavish forested mountains and hillsides that make up more than 70% of the South Korean landscape. Today, mountains and hillsides are generally not used for agriculture and are completely forested, with planted groves and volunteer trees ranging in age from 10-50 years. These forested areas have led to increased protection for large and small mammals and birds, increasing the potential for zoonotic pathogens that there ectoparasites harbor to be transmitted to man during work and leisure activities. While forested areas provided an expanded habitat for some animals, agriculture expanded and modernized, resulting in short-cut grasses on banks separating much of the rice paddies, orchards, ditches, and dry-land farming that increased competition for small mammal habitat. As a result of increased surveillance of small and large animals and their ectoparasites, the increased prevalence of known pathogens and identification of new pathogens, especially those harbored by ticks, has demonstrated the presence of tick-borne encephalitis, several species of spotted fever group Rickettsia, and a host of other zoonotic diseases in wild animals, their ectoparasites, and man. As tick-borne diseases are not reportable diseases in Korea, the extent and impact on civilian and military populations is unknown as diagnoses are often likely sought for the wrong pathogen. While agriculture modernized, military training sites largely consist of unmanaged lands with tall grasses that are conducive to large and small mammal populations, which are host to a number of zoonotic diseases, e.g., hantaviruses, scrub typhus, murine typhus, leptospirosis, tick-borne encephalitis, spotted fever group rickettsial pathogens, Lyme disease, bartonellosis, etc. that impact on military populations training in those areas. The impact of training sites habitat modification has not been assessed, but for many sites is impractical. To reduce health risks of vectorborne diseases, the US Army has established better housing (tents to barracks with screened windows and air conditioning) at some field training sites, reducing the potential for the transmission of mosquito-borne pathogens (malaria and Japanese encephalitis virus). The increased use of permethrin-treated all climate uniforms (ACUs) and repellents, also reduce the potential for transmission of mosquito-, tick-, mite-, and flea-borne pathogens. However, training conditions at some field training sites remain largely unchanged, with personnel working and sleeping in tents that abut to forested areas where animals and their ectoparasites are present. While some training and maneuver sites are well planned for weapons qualifications of wheeled and tracked vehicles, others sites are in areas of unmanaged lands which are rodent infested. Increased surveillance by the 65th Medical Brigade not only provides a baseline and relative distribution for vector-borne diseases in Korea, but also provides disease trends and risk assessments that are necessary for protecting US military personnel training in Korea.

Tick (Acari: Ixodidae)-borne Pathogens in Korea

Joon-Seok Chae,Heung-Chul Kim,Terry A. Klein 한국응용곤충학회 2014 한국응용곤충학회 학술대회논문집 Vol.2014 No.04

Nature conservation in the Republic of Korea (ROK), in addition the effects of global warming has increasingly changed Korea’s weather to a subtropical climate has resulted in increased populations of wild animals in association with their ectoparasites. Increased numbers of animal and bird hosts and warmer climate has resulted in higher populations of members of the Family Ixodidae (hard ticks), in addition to habitat and geographical distributions resulting from reforestation. There are; 6 Genera (Amblyomma, Boophilus, Dermacentor, Haemaphysalis, Ixodes, Rhipcephalus) in the Family Ixodidae, and with 35 species. Studies in the ROK over the past 10 years has resulted in the recognition of 3 Genera of Ixodidae (Haemaphysalis, Ixodes, Amblyomma) and 14 species (H. longicornis, H. flava, H. japonica, H. phasiana, H. ornithophila, H. formosensis, Ixodes nipponensis, I. persulcatus, I. turdus, I. pomerantzevi, I. granulatus, I. vespertilionis, I. simplex, Amblyomma testudinarium). A number of tick-borne pathogens, including severe fever with thrombocytopenia (SFTS) virus, tick-borne encephalitis (TBE) virus, Borrelia, Anaplasma, Ehrlichia, Rickettsia, Bartonella, Theileria and Babesia species, have been detected in ticks collected from the ROK. In addition to detecting these pathogens in zoonotic hosts, they have also been detected from pets, domestic animals, and humans. These pathogens often demonstrate vector and host-specificity, while affecting veterinary and medical health. The analysis of vector and pathogen distributions is crucial for the development of diseased mitigation strategies, requiring additional studies to determine the distributions of animal and bird hosts and vectors and associated pathogens.

Mosquito species distribution and larval breeding habitats with taxonomic identification of Anopheline mosquitoes in Korea

김흥철,Terry A. KLEIN,이원자,Brett W. COLLIER,정승태,William J. SAMES,이인용,이영재,이동규 한국곤충학회 2007 Entomological Research Vol.37 No.1

In 2005, adult and larval mosquito surveillance was conducted at selected sites in Korea to associate larval habitats with species distribution of mosquitoes of the Anopheles Hyrcanus Group (An. sinensis, An. lesteri, An. pullus, An. belenrae and An. kleini) and other mosquito species. Anopheles specimens belonging to the Anopheles Hyrcanus Group were identified to species level by molecular confirmation using the internal transcribed spacer (ITS)-2 within nuclear ribosomal (r)DNA. A total of 6644 mosquitoes from resting and light trap collections (4451; 67.0%) and larval collections (2193; 33.0%) comprising 32 species and nine genera (Culex [11], Anopheles [8], Ochlerotatus [5], Aedes [3], Armigeres [1], Coquillettidia [1], Mansonia [1], Tripteroides [1] and Lutzia [1]) were collected. Larval habitats were characterized into 14 categories. Of a total of 4534 Anopheles spp. collected (3766 resting and light trap collections and 768 larval collections), Anopheles sinensis (3194; 70.4%) was the most frequently captured, followed by An. kleini (813; 17.9%), An. pullus (299; 6.6%) and An. belenrae (129; 2.8%). Fourspecies of Anopheles (An. lesteri, An. sineroides, An. koreicus and An. lindesayi) were infrequently collected (<3.0%) at all sites surveyed by all methods of collection. Anopheles kleini, An. pullus and An. belenrae were collected in greater proportions in malaria high-risk areas north of Seoul, and were infrequently collected in other parts of Korea, where An. sinensis was the predominant Anopheles spp. captured. A total of 2110 culicine mosquitoes (685 adult collections and 1425 larval collections) comprising 24 species and eight genera were collected.

Introduction of Non-Native Ticks Collected from Fresh Migratory Bird Carcasses on a Stopover Island in the Republic of Korea

최창용,김흥철,Terry A. Klein,남현영,빙기창 대한기생충학ㆍ열대의학회 2022 The Korean Journal of Parasitology Vol.60 No.1

When free-ranging birds are accidentally killed or die, there may be greater potential for their associated ticks to detach, seek alternate hosts, and become established. We examined 711 carcasses of 95 avian species for ticks at a stopover island of migratory birds in the Republic of Korea where only Ixodes nipponensis and I. persulcatus were previously reported from local mammals and vegetation. A total of 16 ticks, I. turdus and Haemaphysalis flava, were collected from 8 fresh carcasses belonging to 5 avian species. Despite their known abundance on migratory birds and mainland Korea, these species had not colonized the isolated insular ecosystem possibly due to the low abundance and diversity of local hosts. The results imply that increasing human impact, such as the anthropogenic mortality of migratory birds and the introduction of non-native mammalian hosts, will increase the potential invasion and colonization risk of ticks. This finding also suggests that tick surveillance consisting of fresh carcasses of dead migratory birds may provide additional information, often ignored in surveillance of ticks on live birds, for the potential introduction of non-native ticks and associated pathogens affecting animal and human health.

Surveillance of vivax malaria vectors and civilian patients for malaria high-risk areas in northern Gyeonggi and Gangwon Provinces near the demilitarized zone, Republic of Korea

심재철,이동규,Terry A. KLEIN,김흥철,이원자,임흥구 한국곤충학회 2010 Entomological Research Vol.40 No.4

After re-emergence of malaria in 1993, a continued increase in Plasmodium vivax cases was observed from 1993 to 2006 in northern Gyeonggi and Gangwon Provinces adjacent to the demilitarized zone separating North from South Korea. Annual parasite incidence per 1000 people ranged from 0.33 in 2004 to 0.89 in 2006. While malaria case rates declined (22.6%) in 2004, they increased 75.1% in 2005 and 51.7% in 2006 from the previous years. An initial incorrect diagnosis of 46.8% of malaria cases as common cold resulted in a mean delay of 1.3 days for the detection malarial parasites. Of the total cases, 10.2% from December to May were due to latent intrinsic incubation infections acquired the previous malaria season and the rest of the cases from June to November were either latent or short incubation infections. Overall, the peak anopheline population occurred from July to September, resulting in a similar peak in malaria cases. While malaria cases increased during 2005–2006, anopheline populations, based on trap indices, were not significantly different during 4 years of surveillance. To decrease the malaria patient infective period to mosquitoes, public health centers in Paju and Cheorwon in 2006 prescribed chloroquine + primaquine at days 0–3 after initial malaria diagnosis followed by an additional 11 days of primaquine (early primaquine treatment), rather than chloroquine on days 0–3 and primaquine on days 4–17 (delayed primaquine treatment). A reduction in the malaria parasite incidence during 2007 was recorded for the two locations offering the early primaquine treatment relative to other locations using the delayed primaquine treatment.

Tabanid Flies (Diptera: Tabanidae) of the Northern Part of Gyeonggi Province, Republic of Korea

서상재,김흥철,Terry A. KLEIN,정성태,이원자,권용정 한국곤충학회 2005 Entomological Research Vol.35 No.3

Tabanid flies were surveyed using New Jersey light traps and Mosquito Magnet. traps at US Army installations and training sites in the northern part of Gyeonggi Province, Republic of Korea. A total of 344 tabanid flies, comprising 14 species and 5 genera, were collected from June to August during 2003-2004. Dominant species were Chrysops vanderwulpi (57.3%), Haematopota sinensis (29.1%), Haematopota koryoensis (4.4%) and Tabanus mandarinus (2.3%). Mosquito Magnet traps that generated CO2 through the combustion of propane gas were nearly 6 times more effective in collecting tabanid flies than New Jersey light traps. Based on Mosquito Magnet trap collections, peak populations occurred from mid-June to early July.

Mosquito Species Composition and Plasmodium vivax Infection Rates on Baengnyeong-do (Island), Republic of Korea

Desmond H. Foley,Terry A. Klein,In-Yong Lee,Myung-Soon Kim,Richard C. Wilkerson,Genelle Harrison,Leopoldo M. Rueda,Heung Chul Kim 대한기생충학열대의학회 2011 The Korean Journal of Parasitology Vol.49 No.3

Vivax malaria is a significant military and civilian health threat in the north of the Republic of Korea (ROK). The island of Baengnyeong-do is the westernmost point of the ROK and is located close to the southwestern coast of the Democratic People’s Republic of Korea (DPRK). Mosquitoes were collected using a black light trap on Baengnyeong-do, and Anopheles spp. were assayed by PCR, to identify the species, and screened for sporozoites of Plasmodium vivax. Of a subsample of 257 mosquitoes, Anopheles lesteri was the most frequently collected (49.8%), followed by Anopheles sinensis (22.6%), Anopheles pullus (18.7%), Anopheles kleini (7.8%), and Anopheles belenrae (1.2%). The overall sporozoite rate was 3.1%, with the highest rates observed in An. kleini (15.0%), An. sinensis (5.2%), and An. lesteri (1.6%). No sporozoite positive An. pullus or An. belenrae were observed. The results extend our knowledge of the distribution and potential role in malaria transmission of An. kleini, An. lesteri, and An. sinensis, for an area previously considered to be at a low risk for contracting vivax malaria.

Serological Surveillance of Scrub Typhus, Murine Typhus, and Leptospirosis in Small Mammals Captured at Firing Points 10 and 60, Gyeonggi Province, Republic of Korea, 2001-2005

O'Guinn, Monica L.,Klein, Terry A.,Lee, John S.,Richards, Allen L.,Kim, Heung-Chul,Ha, Si Jung,Shim, So Hee,Baek, Luck Ju,Song, Ki-Joon,Chong, Sung-Tae,Turell, Michael J.,Burkett, Douglas A.,Schuster, Mary Ann Liebert 2010 Vector borne and zoonotic diseases Vol.10 No.2

Microbial pathogens in ticks, rodents and a shrew in northern Gyeonggi-do near the DMZ, Korea

Joon-Seok Chae,유도현,Smriti Shringi,Terry A. Klein,Heung-Chul Kim,Sung-Tae Chong,In-Yong Lee,Janet Foley 대한수의학회 2008 Journal of Veterinary Science Vol.9 No.3

A total of 1,618 ticks [420 individual (adults) and pooled (larvae and nymphs) samples], 369 rodents (Apodemus agrarius, Rattus norvegicus, Tscherskia triton, Mus musculus, and Myodes regulus), and 34 shrews (Crocidura lasiura) that were collected in northern Gyeonggi-do near the Demilitarized Zone (DMZ) of Korea during 2004-2005, were assayed by PCR for selected zoonotic pathogens. From a total of 420 individual and pooled tick DNA samples, Anaplasma (A.) phagocytophilum (16), A. platys (16), Ehrlichia (E.) chaffeensis (63), Borrelia burgdorferi (16), and Rickettsia spp. (198) were detected using species-specific PCR assays. Out of 403 spleens from rodents and shrews, A. phagocytophilum (20), A. platys (34), E. chaffeensis (127), and Bartonella spp. (24) were detected with species-specific PCR assays. These results suggest that fevers of unknown causes in humans and animals in Korea should be evaluated for infections by these vector-borne microbial pathogens.