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 mili- tary, 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.