Malaria in the Republic of Korea, 1993–2007. Variables Related to Re-Emergence and Persistence of Plasmodium Vivax Among Korean Populations and U.S

Home , Anopheles sinensis, Jeju Province, Joint Security Area

MILITARY MEDICINE, 174, 7:762, 2009

Malaria in the Republic of Korea, 1993–2007. Variables Related to Re-emergence and Persistence of Plasmodium vivax Among Korean Populations and U.S. Forces in Korea

Heung-Chul Kim, PhD * ; MAJ Laura A. Pacha , MC USA † ; Won-Ja Lee, PhD ‡ ; Jong-Koo Lee, MD ‡ ; Joel C. Gaydos, MD § ; LTC William J. Sames , USA ¶ ; LTC Hee-Choon S. Lee , MC USA || ; COL Kent Bradley, MC USA ** ; COL Gi-Gon Jeung , VC Korea †† ; LTC Steven K. Tobler, MC USA ‡‡ ; COL Terry A. Klein, USA (Ret.)§§ Downloaded from https://academic.oup.com/milmed/article/174/7/762/4335662 by guest on 29 September 2021

ABSTRACT Malaria was eradicated and the Republic of Korea (ROK) declared “malaria free” in 1979. However, in 1993, a temperate strain of vivax malaria, expressing both latent and nonlatent disease populations, re-emerged near the demilitarized zone (DMZ), rapidly spread to civilian sectors near the DMZ, and increased exponentially in ROK military, veteran, and civilian populations through 1998. Malaria among all ROK populations decreased 5-fold from a high of 4,142 cases in 2000 to a low of 826 cases in 2004, before increasing again to 2,180 cases by 2007. Each malaria case in the ROK is reported in the metropolitan area/province where the diagnosis is made, which may be at some distance from the area where infection occurred. Therefore, it is difﬁ cult to ascertain transmission sites since approximately 60% of vivax malaria in Korea is latent with symptoms occurring >1 month to 24 months after infection. A review of case diagnosis for civilian, veteran, and military populations shows that nearly all malaria south of Gyeonggi and Gangwon Provinces is the result of veterans exposed in malaria high-risk areas along the DMZ and returning to their hometowns where they later develop malaria. Thus, malaria currently remains localized near the DMZ with limited transmission in provinces south of Seoul and has not spread throughout Korea as previously hypothesized. This report describes the re- emergence of vivax malaria cases in civilian and military ROK populations and U.S. military personnel and assesses variables related to its transmission and geographic distribution.

INTRODUCTION soldiers presented with malaria after they returned to the U.S.7 During the Korean War, vivax malaria (Plasmodium vivax) was Cases with onset of illness in the U.S. declined in 1953 with an important cause of military casualties among the Republic the introduction of postexposure terminal chemoprophy- of Korea (ROK) Army, U.S. military, and United Nations laxis treatment protocols using primaquine, although malaria (UN) forces.1–3 Among the ROK Army, malaria caused about remained high in South Korean soldiers with >8,000 cases.5,6,8 15% of febrile illnesses.1,4 Between the start of the war in 1950 In 1993, vivax malaria re-emerged with the fi rst case of through December 1953, 6,199 cases of malaria were reported autochthonous malaria identifi ed in a ROK soldier assigned in U.S. soldiers in Korea.3,5,6 An estimated additional 12,000 to the southern boundary of the demilitarized zone (DMZ),9 a 248-km by 4-km fortifi ed zone that divides the Korean Peninsula into North and South at an acute angle across the *Fifth Medical Detachment, 168th Multifunctional Medical Battalion, 38th parallel. 10,11 The site of re-emergence was consistent with Unit 15247, APO AP 96205-5247. †Department of Preventive Medicine, Martin Army Community Hospital, the reintroduction of the parasite in the Democratic People’s Bldg. 2616, Soldier’s Plaza, Fort Benning, GA 31905. Republic of Korea (DPRK) (North Korea) that was associ- ‡Korea Center for Disease Control and Prevention, Seoul, Republic of ated with increased requests to the World Health Organization Korea 122-701. (WHO) from North Korea for antimalarial drugs (chloro- §U.S. Department of Defense Global Emerging Infections Surveillance and Response System, 2900 Linden Lane, Silver Spring, MD 20910. quine and primaquine), presumed to be a result of increases of 12–15 ¶Defense Logistics Agency, 8725 John J. Kingman Road, Suite 2639, malaria cases and endemic transmission. ATTN: DES-E, Fort Belvoir, VA 22060. The transmission of malaria by potential malaria vectors ||Department of Preventive Medicine, Walter Reed Army Medical Center, in Korea is not fully understood because of insuffi cient data 6900 Georgia Avenue NW, Washington, DC 20307. on malaria vector identifi cations. Early literature includes **Landstuhl Regional Medical Command, CMR 402, APO AE 09180. Anopheles sinensis An. sin- ††Veterinary Corps, ROK Army, Gyeryoung-si, Republic of Korea 321-929. all the members of the Group, ‡‡USACHPPM-Wash., DC, 2900 Linden Lane, Suite 200, Silver Spring, ensis sensu stricto (s.s.), An. pullus (=An. yatsushiroensis ), MD 20910. An. lesteri (=An. anthropophagus ), An. belenrae , and An. §§Department of Preventive Medicine, U.S. Army MEDDAC-Korea, kleini , as An. sinensis sensu lato (s.l.).12,16–18 Thus, An. sinensis Unit 15281, APO AP 96205-5281. s.l. was previously considered the primary vector in the ROK The views expressed are those of the authors and should not be construed to rep- resent the positions of the U.S. Department of the Army or Department of Defense. because studies showed that it exhibited high seasonal popula- This manuscript was received for review in April 2008. The revised tions, zoophilic behavior (but readily bit humans), low infection manuscript was accepted for publication in December 2008. rates, and peak biting activity between 7:00 p.m. and 1:00

762 MILITARY MEDICINE, Vol. 174, July 2009 Re-emergence and Persistence of Malaria in Korea a.m., when people were active outdoors.19–24 New evidence the re-emergence of malaria in 1993 through 2007 (Table I). In suggests that two recently described species, An. pullus and 1994, the number of reported malaria cases in the ROK military An. kleini , are the primary malaria vectors in the ROK based increased to 18 and for the fi rst time was reported among vet- on anthropophilic behavior, geographical distribution, rela- eran (ROK soldiers discharged for <2 years) and civilian pop- tive abundance associated with malaria high-risk areas, and ulations. The number of cases in the ROK civilian population fi eld collection and laboratory infection studies, although An. lagged behind the ROK military through 1998 when the malaria sinensis s.l. is a secondary vector.25,26 cases in the ROK military peaked (1,657) (Table I, Fig. 1). The objective of this study was to defi ne the occurrence of Malaria continued to increase in the civilian and veteran pop- P. vivax malaria in diverse populations in Korea and to assess ulations through 2000 when 1,580 and 1,273 malaria cases variables related to its re-emergence and persistence. were reported, respectively. From 2001 through 2004, malaria sharply declined in all ROK populations to a low of 864 cases Downloaded from https://academic.oup.com/milmed/article/174/7/762/4335662 by guest on 29 September 2021 METHODS (Fig. 1). From 2005 through 2007, the total number of cases reported among all ROK populations increased annually by Malaria Case Reporting 60.3%, 52.6%, and 7.9%, respectively. The largest increases The Korea Center for Disease Control and Prevention (KCDC), were observed in the ROK civilian population during 2005 Seoul, Korea, provided data on the numbers of malaria cases (81.4%) and 2006 (66.2%), but decreased by 0.5% in 2007 and location of diagnosis (provinces and large metropolitan ( Table I ). During this same period, malaria cases in the ROK areas) among Korean civilians, veterans (ROK soldiers retired military population increased annually by 47.5%, 33.5%, and <2 years), and active duty ROK military members. 43.7%, respectively ( Table I , Fig. 1 ). The percent of increases Malaria cases diagnosed among U.S. and Korean augment- in malaria rates among the veteran population remained rel- ees to the U.S. Army (KATUSA) soldiers and U.S. civilians in atively stable for both 2005 and 2006, 32.8% and 33.3%, Korea were reported to the Offi ce of Force Health Protection respectively, with only a small increase during 2007 (6.9%). (FHP) as described by Klein et al.27 Following notifi cation of Data provided by KCDC for years 2001–2007 showed the U.S. cases diagnosed in Korea, epidemiological investiga- primary source of malaria infections (based on area of diagno- tions, as part of the malaria surveillance program, were con- sis) among all three ROK populations to be northern Gyeonggi ducted to determine the most likely source of infection and and Gangwon Provinces ( Table II , Fig. 2 ). The average num- other factors relating to malaria transmission, e.g., dates of ber of cases in the military and civilian populations in north- exposure and incubation period (USFK Reg. 40-2).28 The ern Gangwon Province was much lower than for Gyeonggi annual number of ROK soldiers placed on chemoprophylaxis Province, most likely because of the mountainous topography (400 mg hydroxychloroquine sulfate weekly from mid-May and lower human and vector populations. Incheon and Seoul through mid-October followed by 14 days terminal chemo- metropolitan areas are located approximately west central in prophylaxis of 15 mg primaquine given daily) was obtained Gyeonggi Province and 50–70 km south of the DMZ. These from the ROK Ministry of National Defense. two metropolitan areas report relatively large numbers of For security reasons, only numerator data are reported malaria cases. However, the number of malaria cases reported herein. We were not aware of any substantial changes in the from these metropolitan districts acquired along the northern Korean civilian and military populations during the period we metropolitan limits or when visiting malaria high-risk areas observed. U.S. military populations were similar from 1993 near the DMZ is unknown as available data only refl ected through the fall of 2004, after which one brigade and several location of diagnosis. South of Gyeonggi and Gangwon other components were redeployed. However, the reduction Provinces, malaria cases were attributed mostly to veteran in force did not change U.S. military training programs in (81.3%) populations that were previously assigned to malaria malaria high-risk areas near the DMZ for the remaining time high-risk areas near the DMZ and subsequently returned to covered by this report. their hometowns. Military and civilian populations in these Malaria cases attributed to exposure in Korea, but diag- same areas accounted for only 3.0% and 15.7% of the cases nosed elsewhere, were reported to the FHP through the during that same period, respectively. As no epidemiologi- Army Medical Surveillance Activity (AMSA) as previously cal follow-up was conducted on military and civilian cases in described by Klein et al.27 AMSA internal data provided these areas, it is unknown whether any of these patients were patient summaries that included previous assignment dates, near the DMZ. travel, deployment history, and comments that indicated the most likely country and site of infection. U.S. Forces Korea (USFK) Malaria Cases From 1993 through 2007 there were a total of 405 malaria RESULTS cases attributed to exposure in the ROK among U.S. (361) and KATUSA (43) soldiers and USFK civilians (1). Patient inter- ROK Civilian, Veteran, and Military Cases views and reports identifi ed the most likely source of infection A total of 25,613 malaria cases were reported among ROK for 171 of the soldiers diagnosed with malaria in Korea from civilian and active duty military and veteran personnel since 1996 through 2007 ( Fig. 3 ). Except for installations located

MILITARY MEDICINE, Vol. 174, July 2009 763 Re-emergence and Persistence of Malaria in Korea Total 6,595 8,079 10,939 25,613 (6.9) (7.9) 2007 (43.7) (−0.5) 462 447 1,271 2,180 (66.2) (34.2) (33.5) (52.6) 432 311 2006 1,278 2,021

FIGURE 1. Number of military, veteran, and civilian malaria cases reported Downloaded from https://academic.oup.com/milmed/article/174/7/762/4335662 by guest on 29 September 2021 by Korea Center for Disease Control and Prevention. Veterans were ROK 2005 (81.1) (32.0) (47.5) (60.3) 769 322 233 service members that had been retired or discharged for ≤2 years. KATUSA 1,324

eran, and military populations, 1993–2007 eran, and military populations, 1993–2007 (Korean Augmentation Troops to the U.S. Army) soldiers, while serving with the U.S. Army are reported as “U.S. military cases,” but are reported as “veterans” within 2 years following discharge from the ROK military. 2004 424 244 158 826 (−24.3) (−10.9) (−42.1) (−25.4)

adjacent to the DMZ (e.g., Camp [Cp] Greaves and JSA), 560 274 273 most malaria transmission occurred at U.S. and ROK operated 2003 (−36.7) (−41.9) (−32.8) (−37.2) 1,107 training sites near the DMZ. Warrior Base Complex, approximately 5 km south of JSA, was the most frequently identiﬁ ed training site where malaria transmission occurred. Except for 885 472 406 2002 (−17.1) (−36.9) (−39.7) (−29.1) 1,763 Cp Greaves (closed in the fall of 2004), only three soldiers who resided at other Cps north of Seoul (e.g., Cp Casey and Cp Hovey) developed malaria that reported no previous expo- 748 673 2001 (−32.5) (−41.2) (−47.8) (−39.9) 1,067 2,488 sure at training sites during the malaria season. Two soldiers that resided and trained near Pyeongtaek (Cp Humphreys) reported that they did not train or visit the malaria high-risk (3.0) (27.8) (18.9) (14.4) 2000 1,580 1,273 1,289 4,142 areas north of Seoul. There were 7/9 and 10/13 KATUSA soldiers that developed malaria during 1997 and 1998, respectively, that were (34.2) (−7.9) 996 (−11.6) (−34.6) 1999 1,541 1,084 3,621 assigned to the Joint Security Area (JSA) adjacent to the DMZ at Panmunjom and at Cp Greaves located 3 km south of Cp Bonifas. In 1998, all soldiers at the JSA and Cp Greaves were 1998 (43.3) (218.0) (444.4) (128.1) 1,148 1,127 1,657 3,932 placed in a mandatory chemoprophylaxis program. The small number of cases reported among KATUSAs in the following years was because of the KATUSA soldiers at Cp Greaves 1997 361 207 (684.8) (728.0) (305.6) (384.3) 1,156 1,724 and the JSA being placed on chemoprophylaxis and the later closure of Cp Greaves in the fall of 2004. 285 356 (557.1) (108.3) (223.9) (232.7) 1996 DISCUSSION Vivax malaria is distributed throughout much of the world today and before its identiﬁ cation in Korea (1913),29 was known as “Haru-geori” (every other day fever attack). 30,31 (388.9) (409.5) 1995 Malaria associated with the ROK has been characterized as Veterans are ROK service members that were discharged from active duty for less than 2 years. Veterans are ROK service members that were discharged from active duty for less than 2 years. b epidemic (unstable) or temperate zone malaria, with a May- through-October transmission season that requires “latent”

1994 populations to maintain the cycle since adult mosquitoes over- winter as noninfected nulliparous females. 8,31 Before its erad-

1993 ication from Korea in 1979, malaria posed a serious health threat and survived the temperate climate through latent popu- Number of reported malaria cases and percent increase () or decrease (−) over the previous year among Korean civilian, vet 0 1 12 25 b 0 2 7 46

a lations of the parasite that do not express themselves in the blood until the following malaria season. 32 These latent or Year Civilian Veterans Military 1 18 88 Total 1 21 107 long prepatent populations were observed early on in 1926 TABLE I. TABLE

Does not include imported cases. Does not include imported cases. 27,33–36 a and later conﬁ rmed and reported by others.

764 MILITARY MEDICINE, Vol. 174, July 2009 Re-emergence and Persistence of Malaria in Korea

TABLE II. Mean, range, and percentage of malaria cases, by provinces and large metropolitan areas, among ROK civilian, veteran (discharged within 2 years from the military), and active duty military populations, 2001–2007

Province/ Civilian Veterans Military Total Metropolitan Area Mean a Range b % Cases c Mean Range % Cases c Mean Range % Cases c Mean Range % Cases d Busan3.9 1–8 9.834.4 14–61 87.6 1.0 1–5 2.639.3 15–65 2.3 Chungbuk5.2 0–10 29.412.3 5–21 68.2 0.4 0–1 2.418.0 8–27 1.1 Chungnam4.3 2–6 21.414.7 6–28 73.6 1.0 0–3 5.020.0 11–34 1.2 Daegu2.9 0–5 13.019.0 7–30 86.4 0.1 0–1 0.622.0 10–36 1.3 Daejeon2.4 0–5 14.913.6 7–29 83.3 0.3 0–1 1.816.3 7–32 1.0 Gangwon62.6 17–79 34.313.1 9–21 7.2 106.9 37–122 58.5182.6 64–216 10.9 Gwangju1.6 0–3 10.313.7 6–28 89.7 0.0 0 0.015.3 7–30 0.9 Gyeongbuk4.7 0–10 16.621.9 14–33 76.9 1.9 0–6 6.528.4 15–42 1.7 Downloaded from https://academic.oup.com/milmed/article/174/7/762/4335662 by guest on 29 September 2021 Gyeonggi420.7 243–574 58.2 77.0 42–111 10.7 224.4 109–325 31.1 722.1 394–999 43.1 Gyeongnam3.7 0–9 12.126.0 10–57 84.6 1.0 0–3 3.330.7 12–61 1.8 Incheon237.3 87–417 84.428.0 11–46 9.9 16.0 7–31 5.7281.3 164–482 16.8 Jeju0.3 0–2 10.02.6 0–6 90.0 0.0 0 0.02.9 0–6 0.2 Jeonbuk4.0 1–8 16.520.0 10–38 82.3 0.3 0–2 1.224.3 12–39 1.5 Jeonnam5.4 1–13 26.214.3 5–29 69.0 1.0 0–4 4.820.7 10–36 1.2 Seoul134.1 53–186 57.597.0 59–185 41.6 2.1 0–8 0.9233.3 121–346 13.9 Ulsan1.6 0–4 9.614.3 8–28 86.9 0.6 0–2 3.516.4 9–32 1.0 Unknown0.0 0 0.00.0 0 0.0 1.0 1 100.00.1 1 <0.1

a Mean number (in boldface type) of vivax malaria cases, excluding imported cases, for each civilian, veteran, and military population and all populations combined. b Minimum and maximum number of vivax malaria cases observed annually from 2001 through 2007. Range of number of cases among all populations for years 2001–2007. c Percent of vivax cases reported from each of the provinces and metropolitan areas. d Percent of total vivax cases for each of the provinces and metropolitan areas for combined populations.

After South Korea was declared malaria free, vivax malaria re- was then reintroduced into South Korea along the DMZ via emerged in 1993 when a Korean soldier stationed near the DMZ infected mosquitoes, from civilian farmers residing in villages that had no travel history outside of the ROK became ill.10,12,32 (e.g., Daeseongdong) within the DMZ that became infected Although vivax malaria, attributed to exposure in Korea, was by mosquitoes from North Korea, or the Joint Security Area fi rst reported in the USFK military population in 1994, a U.S. where North Korean military and ROK and U.S. soldiers are soldier assigned to Korea during 1992 with no travel history to in close proximity. other malaria areas developed malaria in 1993, suggesting that To further support the reintroduction of malaria from North malaria transmission may have occurred as early as 1992.37,38 Korea, although anopheline species are generally considered to The reintroduction of malaria most likely occurred as a have a fl ight range of only 2–3 km, Cho and colleagues found result of a resurgence of malaria in North Korea, especially that 12.4% of recaptured females of members of the An. sin- along the DMZ (earliest documented report with nearly 96,000 ensis group (not identifi ed to species) traveled 6–12 km from reported cases in 1999), following a declaration that North their release site, showing that some members of this species Korea also was malaria free in the 1970s.39,40 This strongly complex were capable of crossing the 4-km DMZ.46,47 However, suggests that malaria was present before this time and avail- Strickman 48 showed that when blood meals were available, able data suggest that the malaria patterns in North Korea, An. sinensis ’ range extended only about 1 km. Additionally, although much higher, are similar to those along the DMZ small villages within the DMZ (e.g., Daeseongdong) decrease in the ROK.17,18,31,39,41–44 With the lack of an accurate report- the distance required for infected mosquitoes to travel while ing system in North Korea, it cannot be determined when the seeking blood meals and residents of the village may spend reintroduction of malaria was fi rst documented there and if the time in other villages along the southern border of the DMZ source of the reintroduced parasites re-emerged locally from or seek medical treatment there, increasing the opportunity to North Korea.31 However, characterization of P. vivax parasites infect mosquitoes. However, there is no data on when malaria in ROK and U.S. soldiers demonstrate that there are at least appeared in these populations residing within the DMZ. two vivax malaria strains circulating in the ROK that were Vivax malaria is a public health concern in Korea. 8,49–51 identifi ed as North Korea and northern Chinese strains, indi- Since 1993, nearly all malaria in the ROK was associated with cating that there were at least two reintroductions of malaria transmission near the DMZ and it was believed that it would across the border13,15,45 (C. Ockenhouse, personal communi- rapidly spread south.8,40,44,49,52,53 Vivax malaria is reportable cation ). Because little information is available from North in Korea and patients are categorized as civilians, veterans Korea on when malaria re-emerged in that country, it might (<2 years after discharge), and active duty military members. be presumed that malaria became endemic before 1993 and Although Korea follows soldiers (as veterans) after they are

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FIGURE 2. Map of the Republic of Korea showing relative number of malaria cases among ROK military, veterans, and civilians, 2001–2006 diagnosed at large metropolitan areas and provinces. 1, ROK military, veterans, and civilians; 2, ROK civilians; 3, ROK military (active duty); 4, ROK veterans (retired). (A) Incheon metropolitan area; (B) Gyeonggi Province; (C) Seoul metropolitan area; (D) Gangwon Province; (E) Chungnam Province; (F) Daejeon metropolitan area; (G) Chungbuk Province; (H) Gyeongbuk Province; (I) Daegu metropolitan area; (J) Ulsan metropolitan area; (K) Busan metropolitan area; (L) Gyeongnam Province; (M) Jeonbuk Province; (N) Gwangju metropolitan area; (O) Jeonnam Province; (P) Jeju Province (Island).

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FIGURE 3. Number of malaria cases for U.S. soldiers assigned to Korea and the most likely site of malaria transmission at U.S. military training sites and installations, 1996–2007. Warrior Base (WB) Complex consists of a number of training areas and fi ring points, e.g., Story Impact Range, Dragon Head, Texas Range, Mohawk Range, and others normally used for daytime fi ring with a base camp at the WB Cantonment Area. Warrior Base is adjacent to a ROK military base and approximately 3 km from the Joint Security Area (JSA) (Cp Bonifas) where numerous Anopheles mosquitoes are present, especially when higher concentrations of military are present. After the 2006 season, permanent barracks were built and the tent bivouac areas were disbanded. Cp Casey: Several U.S. installations are located within the city limits of Dongducheon, including Cps Castle, Casey, Hovey, etc. Transmission may have occurred on or off post. Limited transmission is suspected to occur primarily on the periphery of the city perimeter, but may also occur at military installations and in town as Anopheles mosquitoes are present. Cp Greaves: Personnel were previously on chemoprophylaxis from 1999 through 2002. Cp Greaves closed as of fall 2004. Joint Security Area (JSA): JSA personnel were on chemoprophylaxis from 1999 through 2007. Persons not assigned to JSA were not on chemoprophylaxis. discharged, U.S. soldiers who separated from the military and itary further expanded their chemoprophylaxis program to subsequently developed malaria and sought civilian medical include 200,000 soldiers to combat the increasing malaria case care are not identifi ed and are not reported here. Additionally, trend. Even though chemoprophylaxis was extended, malaria discharged KATUSA soldiers that resided and trained with the rates continued to increase in the ROK military and veteran U.S. military in Korea and later developed malaria (<2 years populations through 2007, although numbers of cases in the after being discharged) were reported as “veterans” by KCDC civilian populations remained stable for years 2006–2007. and not captured as U.S. cases. Thus, the actual number of Reasons for increases in malaria from 2005 through 2007 are malaria cases among U.S. and KATUSA soldiers, attributed not understood, but one possible explanation for increases to exposure in Korea, is likely underreported. during 2006 was a late fall (warmer than normal tempera- Malaria was fi rst reported in the military along the DMZ and tures extended through the fi rst week of November allowing in 1994 spread to the local civilian communities with numbers for continued larval development and emergence of adults) of cases quickly surpassing those observed in the military pop- whereby mosquito larvae and adults were collected in abun- ulation. Many individuals in the veteran population returned to dance through the fi rst week of November (T. A. Klein, their hometowns south of malaria high-risk areas and became unpublished data). ill with malaria, increasing the potential for the rapid spread of With the reintroduction and exponential increases in malaria malaria throughout Korea. As a countermeasure to suppress from 1993 through 1998, it was presumed that malaria would the spread of malaria from military to civilian populations, the rapidly spread throughout Korea, in part because of the veter- ROK military instituted a limited chemoprophylaxis program ans returning to their hometowns, developing latent malaria, in “malaria high-risk” areas. The chemoprophylaxis program and renewing malaria transmission into nonendemic sectors. was expanded annually to include 90,000 soldiers by the year However, sites of malaria diagnosis among ROK civilian and 2000 when malaria cases peaked. Further increases to a total active duty military populations demonstrate that malaria of 165,000 soldiers on chemoprophylaxis by 2003, educa- has remained localized in northern Gyeonggi and Gangwon tion, and other control measures instituted by the local health Provinces, although returning veterans (<2 years after dis- departments led to decreases in malaria rates to a low of <900 charge) account for nearly all malaria diagnosed south of cases by 2004. However, increases in the number of malaria Gyeonggi and Gangwon Provinces (Ree 2000, K-CDC 2005). cases occurred in 2005 in all populations and the ROK mil- Also, during a survey of 339 ROK civilian patients residing in

MILITARY MEDICINE, Vol. 174, July 2009 767 Re-emergence and Persistence of Malaria in Korea nonmalarious areas during 1998, 157 (46.3%) indicated that monitoring malaria incidence. We appreciate the support of the personnel of they had visited malaria high-risk areas during the transmis- the U.S. Army Medical Surveillance Activity, Walter Reed Army Medical Center, Forest Glen, MD, who provided data and information on malaria in sion season, further indicating that the sites of primary trans- U.S. soldiers worldwide. Funding for portions of this work was provided by 31 mission are near the DMZ. the U.S. Department of Defense Global Emerging Infections Surveillance and The hypothesis of rapid spread of malaria throughout Korea Response System, Silver Spring, MD. was based on the assumption that An. sinensis sensu stricto was the primary vector of malaria in Korea.19,22,40,54,55 REFERENCES However, recent studies demonstrated that An. sinensis is a 1. 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Korean J Parasitol 1994 ; 32 : 281 – 4 . Malaria became re-established in the ROK as early as 1993 and 12. Chai JY : Re-emerging Plasmodium vivax malaria in the Republic of Korea . Korean J Parasitol 1999 ; 37 : 129 – 43 . its eradication is unlikely in the near future without concerted 13. Kho WG , Park YH , Chung JY , et al : Two new genotypes of Plasmodium efforts of both South and North Korea to eliminate malaria vivax circumsporozoite protein found in the Republic of Korea . Korean J along the DMZ where malaria transmission is reported. Parasitol 1999 ; 37 : 265 – 70 . Further studies to increase our knowledge of the epidemiol- 14. Lee HW , Lee JS , Lee WJ , Lee HS : DNA sequencing and expression ogy of malaria in Korea are necessary for the development of the circumsporozoite protein of Plasmodium vivax Korean isolate in Escherichia coli . J Microbiol 1999 ; 37 : 234 – 42 . and implementation of control measures that target the source 15. World Health Organization : Malaria still a priority problem in DPRK . of infection to conserve limited manpower and funding. EPR Highlights 2002 ; 1 : 4 . 16. Lee HI , Lee JS , Shin EH , Lee WJ , Kim YY , Lee KR : Malaria transmis- Anopheles sinensis ACKNOWLEDGMENTS sion potential by in the Republic of Korea. Korean J Parasitol 2001 ; 39 : 185 – 92 . We thank personnel from the 121st Combat Support Hospital (formerly 17. Yeom JS , Ryu SH , Oh S , et al : Status of Plasmodium vivax malaria in Seoul Army Community Hospital and 121st General Hospital) and the Troop the Republic of Korea during 2001–2003 . Am J Trop Med Hyg 2005 ; 73 : Medical Clinics, 168th Multifunctional Medical Battalion, 18th Medical 604 – 8 . Command, and the health care providers of the 2nd Infantry Division for 18. Yeom JS , Kim TS , Oh S , et al : Plasmodium vivax malaria in the Republic their support and timely reporting. We thank Angelene Hemingway, Renee of Korea during 2004–2005: changing patterns of infection. Am J Trop Nelson, and Marie Price, Community Health Nurse Consultants, 18th Med Hyg 2007 ; 76 : 865 – 8 . MEDCOM, and their staff for there support in administering questionnaires 19. Shim JC , Shin EH , Yang DS , Lee WK : Seasonal prevalence and feeding and epidemiological reporting. We acknowledge Ms. Suk-Hee Yi for provid- time of mosquitoes (Diptera: Culicidae) at outbreak regions of domestic ing data analysis and the Korean Ministry for Health, Welfare and Family malaria ( P. vivax ) in Korea . Korean J Entomology 1997 ; 27 : 265 – 77 . Affairs (Korea Center for Disease Control and Prevention and Korea National 20. World Health Organization : World malaria situation in 1994 . Wkly Institutes of Health) and Regional Medical Commands for their assistance in Epidemiol Rec 1997 ; 72 : 269 – 83 .

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