Perspectives on scrub typhus, tick-borne pathogens, and Hantavirus in the Republic of Korea.
Urbanization (Health aspects)
Virus diseases (Development and progression)
Virus diseases (Health aspects)
Lyme disease (Development and progression)
Lyme disease (Health aspects)
Rodent populations (Health aspects)
Scrub typhus (Development and progression)
Scrub typhus (Health aspects)
Stress management (Health aspects)
Uniforms (Health aspects)
Disease transmission (Development and progression)
Disease transmission (Health aspects)
Enzyme-linked immunosorbent assay (Health aspects)
Antibiotics (Health aspects)
Reforestation (Health aspects)
Medical research (Health aspects)
Medicine, Experimental (Health aspects)
Pathogenic microorganisms (Health aspects)
Sames, William J.
Klein, Terry A.
|Publication:||Name: U.S. Army Medical Department Journal Publisher: U.S. Army Medical Department Center & School Audience: Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2009 U.S. Army Medical Department Center & School ISSN: 1524-0436|
|Issue:||Date: July-Sept, 2009|
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In a previous article, (1) we reviewed the status of malaria and Japanese encephalitis in the Republic of Korea (ROK) with the intent of providing the reader useful information on understanding and dealing with these diseases in the ROK. This article is a continuation of that discussion with a focus on one disease (scrub typhus) and 2 disease groups (tick-borne pathogens and hantaviruses).
Scrub typhus, caused by the rickettsial bacterium Orientia tsutsugamushi (Hyashi) that is transmitted by several species of larval mites belonging to the family Trombiculidae, is a disease of major military importance. During World War II (WWII), its presence made such a dramatic impact on US military personnel deployed to southeast Asia and the Pacific islands that the military initiated a research project performed by the US Department of Agriculture on the concept of treating clothing with a repellent to reduce chigger (larval mites) bites. (2-4) This research was conducted in Florida, with field trials in New Guinea, after which it was exported for immediate use on military uniforms of Soldiers deployed to the frontlines. Later, this method was adopted for use against malaria and other diseases caused by vector-borne pathogens, but it was the effects of scrub typhus that eventually led to the development of permethrin uniform treatments used by US military forces and similarly treated clothing made available to nonmilitary consumers.
Scrub typhus was first reported in Korea when 8 United Nations Soldiers were diagnosed with it during the Korean War and shortly after the signing of the armistice (1951-1954). (5) Prior to the Korean War, scrub typhus was not known to occur among the Korean population, although unconfirmed reports based on symptoms of scrub typhus, fever, chills, headache, and rash had been observed during the late autumn to early winter for many years. (6,7) After the Korean War, scrub typhus cases were reported in relatively low numbers in the ROK population. However, reported cases increased dramatically from 1,415 cases in 2003 to 4,698 cases in 2004, and peaking with 6,780 cases in 2005, as shown in Table 1. While mortality rates vary in different areas, the usual fatality rates among untreated patients range from 10% to 20% in the tropics. (8) During WWII, 6,861 cases were reported in Burma, India, and the Philippines, and in some areas more than one of every 4 Soldiers died of the disease during this preantibiotic period. Of those that survived, the disease was often prolonged with an average time loss of 60 to 70 days per Soldier. (8-1) 0
The Koreans use indirect fluorescent antibody tests for definitive diagnosis of scrub typhus, whereas some US medical laboratories frequently use only enzyme linked immunosorbent assay (ELISA) tests. Recent studies suggest the ELISA serological tests are often negative for scrub typhus for up to 30 days following symptoms, as patients may be anergic and not produce antibodies during the early stages of scrub typhus. Further, after 30 days or more, the patients have self-resolved infections, been successfully treated, or died. (11) For example, in Japan, 17 of 1,700 Marines operating in a "scrub typhus endemic" area (Fuji Maneuver Area), demonstrated scrub typhus symptoms, and all were treated with loading doses of doxycycline and recovered uneventfully. (11) All 17 patients tested serologically negative for scrub typhus by ELISA, therefore, either the diagnostic test demonstrated low sensitivity, or another pathogen (eg, spotted fever group (SFG) Rickettsia) was the cause for the illness. Either way, the cause of the illness was not definitively determined. Similarly in the ROK, 2 patients with typical scrub typhus symptoms (including eschars), who were also serologically negative, were treated with doxycycline, fully recovered, and returned to duty with no follow-up serology to identify the cause of illness. Eschars, however, may be observed in patients with SFG Rickettsia which is present in the ROK, thus SFG Rickettsia infections could not be ruled out as the source of illness. (12) Complications with diagnostic tests suggest scrub typhus rates in US military personnel may be underreported and suggests a need to evaluate current and possibly find better, more definitive diagnostic tests. (11)
Investigations to identify transmission rates of scrub typhus in US Soldiers deployed to the ROK were initiated as a result of a comprehensive rodent surveillance program at field training sites supported by funding through the Global Emerging Infections Surveillance and Response System and the National Center for Medical Intelligence. These investigations identified scrub typhus infection rates in rodent populations ranging from 11.1% to 100%. (13) In another study, data indicate approximately 0.2% of US Soldiers seroconverted for scrub typhus while deployed to the ROK. (14) In addition, bites by chiggers in Korea, unlike the Americas, usually do not elicit an "itchy" response, thus, Soldiers do not realize they have been bitten. (10) These data demonstrate the value of conducting vector and reservoir surveillance that determines the threat of known diseases, but also identifies the presence of reemerging and unknown infectious disease threats. Furthermore, these surveillance data provide for the development, implementation, and evaluation of scrub typhus mitigation strategies.
Assessment of the risk of scrub typhus to the US Forces Korea (USFK) population is difficult, as few cases are diagnosed in the USFK population compared to the disease presence in the Korean population (Table 1). The reasons for the number of post-deployment positive sera for scrub typhus and few suspected cases is not understood, but may be related to using diagnostic assays with low sensitivity, lack of provider awareness and education of emerging diseases in the ROK, and perhaps presumptive treatment with doxycycline with no serology follow-up to determine the cause of illness. Even though scrub typhus appears to be having a low impact on current USFK populations, a change to hostilities or a natural disaster requiring humanitarian interventions could quickly change this status, especially in light of the relatively high number of cases observed in the Korean population.
Additional studies of scrub typhus should focus on surveillance of small rodents and serological studies of Soldiers with suspected scrub typhus and other rickettsial diseases, eg, SFG rickettsial pathogens. Surveillance of small mammals is needed to provide baseline disease risk threats for selected habitats and sites where Soldiers train. Serological studies of Soldiers with vector-borne pathogen-like illnesses where presumptive treatment with antibiotics resolves disease symptoms should be thoroughly evaluated to determine the pathogen, so appropriate diagnostic tools and preventive measures can be applied. Since they are similar, preventive measures for scrub typhus will be discussed in the tick-borne pathogen section.
Diseases Caused by Tick-Borne Pathogens
Identified in the ROK are 31 species of ticks, listed in Table 2, and 16 tick-borne pathogens, some of which are zoonotic (animal-arthropod-animal/human), as shown in Table 3. Early tick-borne pathogen studies in the ROK focused on agricultural economic damage. However, with advancements in ectoparasite control, tick infestations in agricultural and pet animals can be severely limited. Studies of tick-borne pathogens as they relate to human health came later, but have primarily been related to identifying the pathogen's presence in the ROK or documenting new or novel cases. The prevalence and incidence rate of human diseases caused by tick-borne pathogens in Korea is confounded and not clearly understood for a variety of reasons. These include:
* Koreans self-treated with antibiotics prior to a medical prescription requirement implemented in the year 2000.
* Diseases from tick-borne pathogens are not reportable diseases within the ROK.
* Massive urbanization has significantly reduced human-tick interaction.
* Changes in the ecosystem (eg, reforestation) since the Korean War.
* Operational conditions (hence exposure) may be different for military personnel during armistice than during wartime.
Prior to August 2000, a prescription was not required to buy antibiotics in the ROK, allowing the populace to purchase antibiotics at-will from local pharmacies. (13) Since many diseases from tick-borne pathogens range from mild to severe, are treatable with antibiotics (eg, doxycycline), and may be self-limiting, Koreans may have self-treated their symptoms rather than seek professional medical care. Another reason for potential undocumented cases is that Korean medical authorities do not require medical care providers to report diseases from tick-borne pathogens, hence, these diseases are not tracked within the human population. Thus, the health threat of tick-borne pathogens is not fully realized, even though several early retrospective studies of Korean patients with unidentified diseases were serologically positive for spotted fever group Rickettsia parasites. (31, 32) Surprisingly, recent studies of pre- and postdeployment sera from US Soldiers deployed to the ROK demonstrated a 1.3% seroconversion rate to SFG Rickettsia. Thus, some of the eschars observed in US Soldiers that were suspected to be the result of scrub typhus infections may have actually been SFG Rickettsia infections. (14) Additionally, studies of associated infections of ehrlichiosis and bartonellosis in rodents and ticks resulted in the identification of tick-borne encephalitis (TBE) virus in the ROK. (16,29) The impact of these findings are not known as no human TBE cases have been reported in Korea.
Since the Korean War, the ROK has shifted from an agricultural society to an industrial and technology dominant society, which has led to massive urbanization of metropolitan areas such as Seoul, Busan, Pyeongtaek, and Daegu. Even though many Koreans spend weekends hiking in mountainous areas, the trails and paths are generally well worn and free of tick harborage like vegetation and leaf litter. However, when hikers go off the beaten path into forested areas covered with leaf litter and patches of grasses, the potential for human-tick interaction greatly increases. Still, urbanization appears to have reduced the overall exposure potential of the Korean population to ticks.
Interestingly, very few ticks were found during the Korean War, (33) when Korea was primarily rural. However, in the late 1960s and early 1970s, the ROK government directed the replanting of trees on hills and mountains, which had been deforested during the Japanese occupation of 1910 to 1945. The environmental changes may have increased tick populations in those areas by increasing tick survival due to increased numbers and density of suitable hosts.
Presently, large numbers of ticks (not necessarily all species) can be collected from selected sites, including short-grass and leafy-forest habitats throughout the ROK. For example, 2 US Army medical tick surveys in 2007 resulted in the collection of approximately 6,800 ticks (total 6 species, shown in Table 2) from Jeju Province and along the southern coast in Jeollanam and Gyeongsangnam Provinces, all shown in the Figure. US Army tick surveillance data from this area had been lacking, and the surveys resulted in substantial collections and information about an obscure and uncommonly collected and reported tick species, Haemaphysalis phasiana Saito, Hoogstraal, and Wassef. (34)
Additional surveys in 2008 led to the collection of another rarely collected species, Ixodes pomeranzevi Serdyukova, which was collected in low numbers (4 nymphs, 2 adults) on the striped field mouse, Apodemus agrarius Pallas. However, more than 24 larvae, 9 nymphs, and 17 adults were removed from an Asiatic chipmunk, Tamias sibiricus (Laxmann), which suggested the need for extensive small mammal surveys to identify the host range, prevalence, and associated tick species. (35) In 2008, collaboration with a Korean Migratory Bird Survey on Hong Island (Jeollanam Province) resulted in the discovery of another tick, Haemaphysalis ornithophila Hoogstraal and Kohls, which is at least passing through Korea along the birds' migratory route. (36) Why all the new discoveries? Perhaps, global warming is creating environmental conditions favorable to these species and affecting their distribution in Korea,(37) or perhaps our surveillance activities are just finding what has been present, but not detected earlier due to lack of funding and personnel to conduct vector-borne pathogen surveillance. At any rate, these discoveries demonstrate the need for comprehensive and periodic surveillance of vector populations and reservoir hosts to identify changes in vector populations and disease prevalence that may impact Soldier activities.
Ticks are present in the ROK and researchers are finding a high prevalence of tick-borne pathogens within tick (Table 2) and rodent populations, but where is the corresponding disease? One possibility is that humans are not the preferred host of the primary vectors while other possibilities include human avoidance of tick habitats, unfamiliarity with disease from tick-borne pathogens among the medical community, issues with ordering the correct diagnostic test, and lack of reporting requirements, as discussed earlier.
Operational field conditions for military forces are typically different during a prolonged armistice than intensive combat operations such as during the Korean War. Generally speaking, military personnel operating during noncombat periods can expect to have a clean uniform and perhaps a warm, soapy shower every one to 3 days, and many live or operate out of established base camps, which provide additional opportunities for personal hygiene. These situations allow for frequent body inspections for ticks, plus, the soapy water may injure or kill attached ticks and interfere with or reduce the potential for disease transmission, hence reducing the incidence of tick-borne disease.
In contrast, during major combat operations such as those of World War I, World War II, or the Korean War, military personnel in forward areas were generally not able to sustain the same level of hygiene (even with periodic rotations), due to the extended and austere battlefield conditions, as they would during noncombat operations. Consequently, their exposure to zoonotic tick-borne and other vector-borne pathogens was increased. In addition, they may occupy areas that have higher tick populations, eg, forested areas during hostility operations, and therefore have increased contact with the ground and vegetation harboring questing ticks. Similarly, the civilian population may experience displacement, homelessness, reduced sanitation, increased exposure to vectors and disease, elevated disease levels, and thus increase the risk of spreading the disease through vectors to military forces operating in that region.
These aspects of Korean society and the current hygiene standards of US military personnel make it difficult to estimate the impact of tick-borne pathogens on a military force operating in substandard field conditions during major combat operations in Korea. Hence, the tick-borne pathogen threat to military forces in the ROK is currently an estimate derived from limited reports of the diseases present, the tick population densities and distributions, vector bionomics, potential human exposure rates, disease mitigation actions, season, etc. Increased vector and human disease surveillance would lead to a better understanding of the tick-borne pathogen risks and mitigation strategies required to reduce these risks.
Fortunately, the Department of Defense (DoD) Insect and Arthropod Repellent System, which includes the proper wear of the uniform, wearing permethrin treated uniforms, and applying military formulations of extended duration topical insect and arthropod repellent N,N-diethy-3-methylbenzamide (deet) to exposed human skin, is estimated to reduce virtually all tick exposures in the ROK, significantly mitigating the risk of disease from tick-borne pathogens among US Soldiers. This repellent system also provides protection against other vector-borne pathogens in the ROK, so its implementation to prevent disease from tick-borne pathogens also provides added protection against malaria, Japanese encephalitis, scrub typhus, body lice (epidemic typhus), fleas (murine typhus), and other biting arthropods.
However, the fielding of the flame-retardant Army Combat Uniforms (FRACU) necessitates a reevaluation of the permethrin-fabric properties as they relate to protection against ticks, chiggers, and other blood-feeding arthropods. These evaluations need to determine the protection level of the FRACU compared to the standard (>90% protection after 50 washings) and then determine its effectiveness against blood-feeding arthropods. Currently, permethrin treatment is not approved for use on FRACUs by the military. Permethrin treatments do not meet the Environmental Protection Agency label required permethrin concentration in the uniforms nor provide the required amount of protection against biting arthropods.
General observations during the 2007 surveys in Jeju Province and along the southern coast showed that survey personnel who wore permethrin treated uniforms rarely found a tick on their uniform (in some cases the "found" tick was dead), while those who did not wear permethrin treated uniforms commonly found ticks on their uniform. Of course, personal protective measures have to be implemented and used properly, eg, tucking the trouser leg into the boot and not using blousing garters, for these countermeasures to be most effective.
From an entomological perspective, very little was known about Korean ticks during the Korean War. Ticks were reported as being uncommon, and very few Soldiers complained of tick bites. (33) In 1971, US Army personnel assigned to the 406th Medical Laboratory, Camp Zama, Japan published a comprehensive systematic and bionomical work on ticks in Japan and the ROK, even though limited Korean tick data were available for inclusion. (15) This document, however, remains useful as many of the ticks found in Japan are also found in the ROK, and it is still the primary document for identifying Korean ticks. Since 1971, few US military or ROK tick surveillance field studies have been reported in professional literature, so knowledge about the current status of tick populations and disease prevalence is lacking.
Articles have been published on diseases specifically caused by Korean tick-borne pathogens, but no tick-borne pathogen list or comprehensive discussion of the importance of tick-borne pathogens in the ROK could be found. To prevent surprises during a time of stress (major combat operations) and to develop a better understanding of tick-borne pathogens in the ROK, there is a need for surveillance which targets host and vector species to determine relationships between vectors, pathogens, reservoirs, and hosts. This surveillance should include a peninsula-wide tick collection to better understand tick distributions, habitat, population densities, and the potential for disease transmission by each species, (eg, human attraction, infection rates, and relative abundance, seasonal distribution, environmental factors limiting its distribution, and host-parasite life cycles), and an entire season's collection to show each species' seasonal activity and disease cycle.
Ten US Army studies since 2003, such as Chae et al, (38) Lee et al, (39) and Kim et al, (40) have addressed these deficiencies. A bibliography on the ticks of the ROK is being created based upon an extensive literature search and review for all tick-related information for the ROK and surrounding countries, ie, North Korea, Japan, northeastern China, and southeastern Russia. The bibliography and the accompanying PDF files (currently about 284 citations with about 69% as PDF files) of the articles are being incorporated into the Defense Pest Management Information Analysis Center for access by DoD personnel. Tick collections described within these articles and from recent US Army tick surveys are being compiled as a record of known tick locations and will be used to create graphical tick distribution maps and a list of diseases caused by tick-borne pathogens with vector associations for the ROK. Table 2 represents our initial attempt at extracting vector and disease associations from published literature.
There are 4 known rodent-borne hantaviruses in the ROK: Hantaan virus (Korean Hemorrhagic Fever (KHF)), Seoul virus, Soochong virus, and Muju virus. Reservoirs of each have primary reservoir hosts with the striped field mouse, Apodemus agrarius coreae, vectoring KHF; the common roof rat, Rattus rattus Linnaeus, and the Norway rat, Rattus norvegicus Berkenhout, vectoring Seoul virus; the Korean field mouse, Apodemus peninsulae Thomas, vectoring Soochong virus; and the royal vole, Myodes regulus Thomas, vectoring Muju virus. (41,42) A fifth hantavirus (Imjin virus) in an insectivore, Crocidura lasiura Dobson, has recently been identified. (43)
Transmission is associated with inhalation of aerosolized particles, such as dusts, that have been contaminated with rodent excreta and/or secreta (feces, urine, and saliva). It also can be contracted through a rat or mouse bite, so precautions should be made when handling them and they should never be kept as mascots or pets.
Hantaan virus, commonly referred to as KHF, is the most common and virulent of the group and fits into the hemorrhagic fever with renal syndrome (HFRS) disease group. These diseases are characterized by leakage of blood from the circulatory system and abnormal kidney function. Conditions during the Korean War led to 2,158 hantavirus cases in US forces. (44) Most of these cases occurred north of Seoul and with a large majority occurring north of the 38th parallel. (45)
While the risk for HFRS is always present in the ROK, cases in the Korean population show a very small transmission peak in May and June, and a much larger transmission peak from September through December. These transmission periods appear to be associated with agricultural practices (planting for May and June, draining/drying and harvesting rice fields for September and October), which results in significant human-rodent interaction and hence exposure. However, more recent evidence suggests that the primary peak is associated with the rodent's reproductive behavior (primary brood production in the early fall preceding the peak transmission) that produces large numbers of naive rodents. (46) When associated with high local infection rates, movement, and competition for overwintering habitat, the results are acute infections with high viremias and shedding of virus. Consequently, when farmers are actively harvesting their fields or military personnel are training in the field during these periods, there is an increased risk of acquiring hantavirus. (47) Generally, the risk of HFRS in the ROK can be characterized as having a low frequency of occurrence, but a severe outcome if acquired, and field training activities that lead to human-rodent interactions at any time of the year can result in Soldiers contracting HFRS. The incubation period may be as long as 50 days before symptoms occur, so Soldiers should be informed of HFRS symptoms (early symptoms are often flu-like), and if they become ill, they should alert their medical-care providers with information as to their travel or field training history.
Surveillance studies have shown that the reservoir of HFRS is very common throughout the country and seasonal Hantaan virus rodent infection rates were as high as 60% during some trapping periods at some of the field training sites. (48,49) These studies have also shown that a portion of the Hantaan virus genome was descriptive for selected sites and made it possible to identify transmission sites for HFRS case studies for 4 Soldiers that demonstrated incubation periods from a minimum of 6 to 22 days to a maximum of 15 to 35 days. (50)
Studies also have shown that high populations of rodents are present in tall grassy and scrub habitats. (51) In training sites, areas of tall, unmanaged vegetation bordering fighting positions (artillery firing points, trenches, and foxholes) increase human-rodent interactions along the border vegetation, as well as the often barren training area interface that may become potentially contaminated with virus laden rodent excreta. Also, dust produced when firing large weapons such as field artillery may increase the risk of infection as rodent urine and fecal particles become airborne from the muzzle blast of these weapons. Similarly, the dust from vehicles going through dry vegetated areas, trails, or dirt roads bordered by grassy/scrub vegetation may increase hantavirus infection risks as rodents traversing these grassy borders produce virus laden excreta on these trails and roads. These risks can be reduced by discouraging rodents from being attracted to fighting positions through vegetation control (maintaining vegetation cut short to reduce ground cover) and sanitary measures, such as frequent removal of trash and debris. Fighting positions should be located away from heavily traveled roads to prevent exposure to potentially infected dusts. Artillery personnel should use sanitary measures to discourage rodent infestations where they fire their weapons, and should take personal preventive measures to reduce inhalation of dust from the muzzle blast.
Exposures in closed spaces have the greatest risk, thus military personnel should not bring potentially infested materials, such as rice straw for flooring or bedding, into closed areas such as tents, barns, houses, or other buildings. Additionally, military personnel in the field should avoid sleeping on the ground or placing vegetation that was lying on the ground into their helmets.
Scrub typhus, tick-borne pathogens, and hantaviruses present challenges to the protection of military forces in the ROK, and surveillance studies focused on the improvement of our knowledge of these diseases and how to prevent them need continual support. While the distribution of scrub typhus has been well described, the distribution and prevalence of tick-, flea-, and rodent-borne pathogens affecting man are largely unknown. The rickettsial agents are currently under investigation and are just now being identified to species, which will provide future endeavors to determine their distribution and prevalence in rodent and human populations. As these parasites are identified, appropriate laboratory assays can be developed to identify the incidence of disease among military and civilian populations in the ROK. Similarly, assays to identify Imjin virus, which does not serologically cross react with the other rodent-borne hantaviruses, can be developed to determine if it causes human disease. As an awareness of the presence of tick-, mite-, flea-, and rodent-borne pathogens are developed, the Korea Center for Disease Control and Prevention may place new zoonotic pathogens on the reportable disease list, which, in conjunction with an understanding of the transmission cycle, will enhance our ability to determine health risks among US military and civilian populations in the ROK.
Information gathered as a result of surveillance studies must be prepared and disseminated through channels where actions can be taken by commanders at all levels to reduce risks to Soldiers from often preventable diseases and nonbattle injuries during hostilities, while training, or off-duty.
Indeed, the real value of such surveillance work is reflected in the sentiments of His Royal Highness, Prince Mahidol of Songkla (Thailand, 1892-1929):
True success is not in the learning, but its application to the benefit of mankind. (52)
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LTC Sames is currently deployed in Iraq as the Chief, Multinational Corps-Iraq Force Health Protection, and the Iraq Theater Entomologist and Pest Management Consultant.
Dr Kim is the senior civilian Research Entomologist with the 5th Medical Detachment, Yongsan Army Garrison, Republic of Korea.
COL (Ret) Klein is a consultant to the 65th Medical Brigade, Yongsan Army Garrison, Republic of Korea.
LTC William J. Sames, MS, USA Heung-Chul Kim, PhD
COL (Ret) Terry A. Klein, MS, USA
Table 1. Number of scrub typhus, leptospirosis, and hantavirus (hemorrhagic fever with renal syndrome) cases reported by year, 1997-2008. * Disease 1997 1998 1999 2000 2001 2002 Scrub Typhus-ROK 277 1,140 1,342 1,758 2,637 1,919 Leptospirosis-ROK 4 90 130 106 133 122 Hantavirus-ROK 104 215 196 203 323 336 Hantavirus-US 2 4 1 2 2 0 Disease 2003 2004 2005 2006 2007 2008 Scrub Typhus-ROK 1,415 4,698 6,780 6,480 6,022 6,035 Leptospirosis-ROK 119 141 83 119 208 100 Hantavirus-ROK 392 427 421 422 450 376 Hantavirus-US 3 0 4 0 0 0 * Data from the Korea Center for Disease Control and Prevention (http://dis.cdc.go.kr/english/index.htm). Table 2. Tick species reported from Korea. * Amblyomma testudinarium Haemaphysalis phasiana ([dagger]) ([dagger]) Argas boueti Ixodes acuminatus Argas japonicus Ixodes cavipalpus Argas vespertilionis Ixodes granulatus Dermacentor marginatus Ixodes nipponensis ([dagger]) Dermacentor reticulates Ixodes ovatus Dermacentor silvarum Ixodes persulcatus ([double dagger]) Haemaphysalis campanulata Ixodes pomeranzevi ([double dagger]) Haemaphysalis concinna Ixodes ricinus Haemaphysalis cornigera Haemaphysalis flava Ixodes signatus ([dagger]) Haemaphysalis japonensis Ixodes turdus ([dagger]) Haemaphysalis japonica Ixodes vespertilionis ([double dagger]) Haemaphysalis kutchensis Rhipicephalus annulatus ([paragraph]) Haemaphysalis longicornis Rhipicephalus microplus ([paragraph]) ([dagger]) Haemaphysalis ornithophila Rhipicephalus sanguineus ([section]) * Sources: Yamaguti et al, (15) Ree, (16) and as individually annotated. ([dagger]) US Army tick surveys, 2007 ([double dagger]) US Army tick surveys, 2002-2008 ([section]) Captured in 2008 on migratory birds on Hong Island, southwestern Korea. ([paragraph]) Formerly Boophilus spp Table 3. Human and other animal pathogen associations with tentative tick vectors in the Republic of Korea. Pathogen Vector(s) Anaplasma bovis Haemaphysalis longicornis (17) Anaplasma phagocytophilum * Haemaphysalis longicornis, Ixodes persulcatus (17) Anaplasma platys Haemaphysalis longicornis (18) Babesia spp * Haemaphysalis longicornis (19) Bartonella elizabethae * Haemaphysalis longicornis (20) Bartonella spp * Haemaphysalis longicornis (20) Borrelia afzelii * Ixodes persulcatus (21) Borrelia burgdorferi sensu lato * Ixodes granulatus, I nipponensis, I persulcatus (22-24) Borrelia garinii * Ixodes persulcatus (21) Borrelia valaisiana * Ixodes nipponensis (25) Coxiella spp * Haemaphysalis longicornis (26) Ehrlichia canis Haemaphysalis longicornis (18) Ehrlichia chaffeensis * Haemaphysalis longicornis, Ixodes persulcatus (17,18,27) Ehrlichia ewingii * Haemaphysalis longicornis (18) Theileria sergenti Haemaphysalis longicornis (28) Tick-borne encephalitis virus, Haemaphysalis longicornis, Western subtype * H flava (29,30) * Causes disease in humans.
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