Abstract

This report describes a cluster of 11 soldiers with vivax malaria among U.S. military personnel who trained at Dagmar North training area, near the demilitarized zone (DMZ), in the Republic of Korea (ROK) in 2015. Two cases were diagnosed in the ROK in 2015, one of whom subsequently experienced a relapse, and nine other cases were diagnosed in 2016, 8–11 months after the soldiers had returned to the U.S. Vivax malaria poses a health threat to U.S. Forces Korea operating near the DMZ in the ROK. Continuing and enhanced focus on force health protection measures in endemic zones is warranted.

What Are the New findings?

A small outbreak of 11 cases of malaria occurred in 2015-2016 from exposures in Korea localized to the demilitarized zone (DMZ). Nine (82%) of the cases developed their first symptoms of infection 9 or more months after exposure and after their departure from Korea.

What Is the Impact on Readiness and Force Health Protection?

Although rates have declined in recent years, vivax malaria poses a focal health threat to ROK/U.S. military personnel operating near the demilitarized zone (DMZ). Lack of command-directed adherence to force health protection measures for malaria in the absence of routine chemoprophylaxis can result in clusters of malaria infection which can adversely impact military readiness.

Vivax malaria was a major health threat to both Korean and United Nations Forces during the Korean War,^1,2 with more than 15,000 and more than 6,000 malaria cases reported among Republic of Korea (ROK) and U.S. military personnel, respectively.^3–7 Due to latent liver stages, an additional 12,000 or more U.S. military personnel were diagnosed with malaria after returning to the U.S. during the first year of the war.^8,9 With the development of primaquine phosphate, which eliminates liver stage hypnozoites, in 1952, the numbers of returning service members who developed malaria were greatly reduced.⁹

With the establishment of the ROK National Malaria Eradication Service in 195910 and greatly improved living conditions and medical services, the number of malaria cases rapidly declined. By 1979 the World Health Organization declared the ROK malaria free.^7,11,12 However, in 1993, vivax malaria reemerged in the ROK;¹³ the Korean Centers for Disease Control reported a total of 32,576 autochthonous vivax malaria cases among ROK civilian, veteran, and military populations from 1993–2015, with as many as 4,000 cases in a single year (2000). The ecology in and around the demilitarized zone (DMZ) is particularly prone to Plasmodium vivax transmission because of fishermen from malarial regions fishing along the Imjin river (which also borders the Dagmar North training area) during evening hours, an abundance of larval habitat in low-lying flooded areas and rice paddies, potential continued cross-border introduction of malaria by anopheline mosquitoes, and a high proportion of primary vivax malaria vectors belonging to the Anopheles Hyrcanus Group that has resulted in hundreds of cases of vivax malaria annually since 1996. Thus, malaria poses a significant health threat to ROK/U.S. military and civilian personnel residing and operating near the DMZ.^13-15

This paper summarizes a cluster of vivax malaria infections acquired during Aug' 2015 among U.S. soldiers who trained at Dagmar North training area (DNTA) near the DMZ separating South and North Korea.

Methods

Population and setting

Members of an Armored Brigade Combat Team (ABCT) stationed in the U.S. arrived at Osan Air Base, ROK, during 5–12 June 2015 and went directly to Joint Camps Casey/Hovey. Camps Casey/ Hovey are collocated and are bordered by the city of Dongducheon in northeastern Gyeonggi Province (Figure). Soldiers resided and conducted training at Camps Casey/Hovey training sites, except when selected units proceeded to Rodriguez Combined Arms Collective Training Facility (CACTF) near Pocheon in northeastern Gyenoggi Province where they conducted a major field exercise on 15 July–16 Aug. 2015. Selected units then moved to DNTA on 17 Aug. where they conducted live fire training during the daytime at Story CACTF and returned to DNTA where they conducted nighttime exercises and bivouacked before returning to Camps Casey/ Hovey on 22 Aug. After 22 Aug. 2015 and until the ABCT units departed during 2–17 Feb. 2016 for their home base in the U.S., the soldiers resided and trained only at Camps Casey/Hovey.

Vivax malaria diagnosis

Blood was drawn from patients suspected of having malaria when reporting to a hospital or clinic with febrile illness. Patients were tested for Plasmodium sp. infections using BinaxNOW® (Alere Scarborough Inc., Scarborough, ME) malaria test, examination of blood films for the presence of malaria parasites, and/or by polymerase chain reaction (PCR). The BinaxNOW malaria test distinguishes among P. falciparum, non-falciparum Plasmodium species (P. vivax, P. ovale, and P. malariae), and mixed infections.  Based on the manufacturer’s documentation, the assay has a sensitivity of 93.5% and a specificity of 99.8% for P. vivax. All military patients diagnosed with vivax malaria were reported through the Department of Defense Disease Reportable Systems internet (DRSi).

Epidemiologic investigations

The Public Health Nurse (PHN), Force Health Protection & Preventive Medicine (FHP&PM), 65th Medical Brigade, ROK, was notified through DRSi of malaria cases among U.S. service members. The PHN contacted the PHN at the reporting installation outside of Korea to determine whether the malaria infections were attributed to exposure in the ROK or other malaria endemic countries. Malaria patients suspected of acquiring malaria in the ROK were contacted, and epidemiologic investigations were conducted by FHP&PM and the reporting installation. Epidemiologic investigations involved gathering information related to each patient's training activities, exposures (including training dates, field training conditions, mosquito bite prevention measures, and estimates of the relative numbers of mosquitoes observed and bites received), symptoms, date of symptom onset, and medical care received (treatment type, days and number of medical visits from onset of symptoms to diagnosis, and method of diagnosis). These data were collected from interviews with patients and from a review of their medical records. During interviews a standardized set of questions was asked of all patients whenever possible. Written epidemiologic reports were submitted to the Commanders, 65th Medical Brigade and Brian Allgood Army Community Hospital, ROK; the Surgeons of the U.S. Forces Korea, the Eighth Army, and the 2nd Infantry Division; the Chief, FHP± and others as appropriate.

Results

A total of 11 soldiers with malaria were reported among U.S. soldiers assigned to the ABCT who deployed to the ROK from 5–12 June 2015 through 2–17 Feb. 2016 (Table 1). Two patients were diagnosed with vivax malaria in Korea during 2015, demonstrating symptoms 1–14  and 9–14 days following the training exercise at DNTA, and nine different patients with presumptive exposure at DNTA demonstrated symptoms 8–11 months later (2 May–22 July 2016), after they had returned to the U.S. (Table 2). Patients were diagnosed with malaria using the BinaxNOW® malaria kit (three cases), BinaxNOW® + blood film (four cases), BinaxNOW® + blood film+PCR (one case), or blood film only (three cases) (Table 2). Based on epidemiologic reports, transmission was most likely due to exposure at DNTA during 17–22 Aug., because the soldiers with malaria reported few or no mosquito bites at Camps Casey/Hovey or Rodriguez CACTF but reported numerous bites at DNTA. In addition, there were no cases of malaria among soldiers belonging to the ABCT rotational unit who had not trained at DNTA during 17–22 Aug.

With few exceptions, the malaria patients had documented fever (up to 104°F) and reported chills, sweats, headache, body aches, and malaise. Some patients also reported having nausea, vomiting, and diarrhea. The two patients diagnosed in the ROK in 2015 were initially treated with hydroxychloroquine (Patient #7-2015) or atovaquone/proguanil (Malarone®; #8-2015). Both patients also received primaquine phosphate; however, one was given only 26.3 mg per day for 14 days and subsequently experienced a relapse 9 months later after returning to the U.S. The other patient (#8-2015) received 52.6 mg primaquine phosphate daily for 14 days (Table 3). All patients diagnosed with malaria after returning to the U.S., including the one relapse case, were treated with chloroquine phosphate (n=9) or chloroquine+Lariam® (n=1) for blood stage parasites (Table 3), followed by primaquine phosphate (52.6 mg per day for 14 days) for latent liver stage parasites. Some soldiers reported being initially diagnosed with an influenza-like illness and receiving symptomatic treatment for headache and fever. From the time of onset of symptoms to diagnosis, the malaria patients reported being seen in clinic one to four times over 3–31 days (Tables 2, 3).

None of the malaria patients remembered receiving a medical threat brief prior to their departure to the ROK, during in-processing, or prior to conducting field training at Rodriguez CACTF and DNTA, and none had been forewarned of the presence of large numbers of mosquitoes at DNTA or that malaria was endemic near the DMZ. Soldiers were not placed on malaria chemoprophylaxis, because it was not routinely recommended for soldiers in the ROK due to low numbers of malaria cases in previous years and very low mortality (no deaths from 1993 to present). Pop-up permethrin-treated bed nets were not available for military units training in field environments. While at Camps Casey/Hovey, patients stated that they saw few mosquitoes present during the evening hours, and none reported being bitten by mosquitoes. From 15 July through 17 Aug. 2016, selected units of the ABCT trained at Rodriguez CACTF. There they slept in air-conditioned barracks during the evening hours and saw few mosquitoes during the evening hours; none reported being bitten by mosquitoes. Several units then moved from Rodriguez CACTF to DNTA on 17 Aug. where they bivouacked and conducted nighttime exercises until 22 Aug. when they returned to Camps Casey/Hovey (Table 1). All except one of the malaria patients trained at Rodriguez CACTF before moving to DNTA.

The units that trained at DNTA consisted mainly of tracked vehicle (e.g., Abrams tank) operators and crew members who wore Nomex® (fire retardant) uniforms, while mechanics wore coveralls and command staff wore all climate uniforms (ACU). Most of the patients were unaware if their uniforms had been factory-treated with permethrin. Tank operators and crewmen slept in or on their tracked vehicles during the evening hours in sleeping bags in Nomex® uniforms or ACUs to protect themselves from biting mosquitoes, while others (mechanics and administrative and command groups) slept in physical training uniforms in screened tents (Table 1). Vivax malaria patients who slept in or on their vehicles were unprotected from biting mosquitoes and reported numerous mosquitoes biting during the evening. On a scale of 0 (none) to 5 (too many to count) for presence of mosquitoes, most patients (73%) noted "5" (too many mosquitoes present to count), and, for the number of mosquitoes bites, the majority (55%) reported "5" (too many bites to count) (Table 1). Two patients slept in a two-man screened tent and reported keeping the screen tightly closed to keep mosquitoes from entering the tent, while two others slept in a large ill-kempt general purpose tent where the screened entrance was left unsecure and they reported the presence of numerous mosquitoes and having been frequently bitten while inside the tent.

Soldiers were not issued arthropod repellents to protect themselves from mosquitoes and other biting arthropods while training. However, seven of 11 patients (64%) reported that they brought personal repellents, mostly consisting of spray-on DEET formulations or unknown creams and liquids (Table 1).

After the departure of the ABCT from Korea to the U.S. during 2–17 Feb. 2016 and until the time that the malaria patients demonstrated symptoms, none reported any recent travel outside the U.S. Although several patients stated that they heard rumors that several members of their units had contracted malaria due to exposure in the ROK, the patients stated that the command did not inform them that members in their units were diagnosed with malaria, nor were they informed about the symptoms of vivax malaria.

Editorial Comments

Because of the low numbers of malaria cases in previous years (10 cases or fewer annually between 2008 and 2014; less than 0.2 per 1,000 population at-risk) and the extremely low mortality rate,^14,16 U.S. military personnel in the ROK, with the exception of Marines, are not routinely placed on malaria chemoprophylaxis. Ree reported that during 1998, none of the "properly administered" ROK soldiers training near the DMZ developed malaria, whereas 11% of inadequately monitored ROK soldiers on chemoprophylaxis developed malaria and 89% of untreated soldiers developed malaria.17 U.S. soldiers in the ROK are recommended to use appropriate wear (e.g., permethrin-treated uniforms with the sleeves rolled down, pants tucked into the boots) and effective arthropod repellents (e.g., DEET >20% or picaridin). Factory permethrin-treated ACUs replaced the non-permethrin ACUs for sale in military clothing sales stores in Oct. 2012 and factory permethrin-treated ACUs replaced non-permethrin-treated ACUs as an Army clothing bag item in Feb. 2013. Previous to the implementation of factory treatment, U.S. soldiers treated their uniforms with permethrin using 6 oz. spray cans or individual dynamic absorption (IDA) kits. Although U.S. soldiers are currently issued permethrin-treated uniforms, uniforms purchased before the era of factory permethrin-treated uniforms were often treated by other methods. In addition, most soldiers were unaware whether or not they were wearing permethrin-treated uniforms, and that factory permethrin-treated uniforms are not authorized to be retreated by other methods. In addition, several soldiers who utilized factory permethrin-treated uniforms during the field exercise noted that the uniforms were beyond the lifetime of repellent effectiveness. The consequences of wearing "outdated" permethrin-treated uniforms are unclear, but their use may result in diminished protection from insect bites.

Distribution of insect repellents is a unit supply function and should be based on recommendations to the Commander by the field sanitation team (FST), and repellents must be procured prior to training exercises through the Defense Logistics Agency or purchased locally. The unit that trained at DNTA did not procure repellents for their soldiers to reduce mosquito bites and protect them from vector-borne diseases. Some soldiers reported purchasing repellents locally, but their ingredients and efficacy were unknown. Soldiers with and without repellents reported receiving numerous bites, and some reported to sick call with "numerous red bumps," suggesting a lack of protection. Additionally, insecticide application to the exterior and interior of tents should be considered as it may reduce biting populations inside tents while soldiers are resting or sleeping.

From 2008 through 2013, the number of malaria cases decreased sharply among U.S. Forces Korea, in part due to the replacement of ill-kempt tents at Warrior Base with air conditioned barracks¹⁴. However, at DNTA, a combination of factors may have led to increased numbers of malaria cases among U.S. personnel in 2014–2015,¹⁶ including local transmission among ROK soldiers and civilians, an abundance of larval habitat, low-lying flooded areas and rice paddies that border DNTA, and potential for continued introduction of malaria by anopheline mosquitoes from North Korea.¹⁷ Thus, a combination of factors that included Plasmodium-infected mosquitoes and concurrent training activities that exposed soldiers to biting mosquitoes (e.g., non-use of repellents, non-use of permethrin impregnated uniforms and mosquito nets, and sleeping unprotected in/on vehicles or ill-kempt tents) increased the potential for malaria transmission.

In healthy nonimmune young adults, P. vivax infections in the ROK cause a debilitating, but non-life-threatening, acute febrile illness that reduces military effectiveness. Informing commanders, soldiers, and medical personnel at all levels is imperative to increase their knowledge of potential malaria risks and to rapidly diagnose infections to minimize morbidity, disruption of military operations, and risk of continued autochthonous transmission both in the ROK and the U.S. Soldiers described in this report who developed malaria were unaware of the risks of malaria transmission or the presence of other vector-borne and zoonotic disease risks in the ROK. Soldiers were not informed of malaria risks in the ROK, so they may have delayed reporting to a medical clinic in the U.S. after they developed symptoms of malaria. In addition, the possibility that medics were often unaware of the signs and symptoms of malaria may have delayed diagnosis and increased the risk for autochthonous transmission to civilian communities in the U.S. Providers at all levels should be cognizant of the signs and symptoms of malaria and should review the travel histories of febrile patients to determine if they had deployed or trained in malaria endemic areas.

Author affiliations: Armed Forces Health Surveillance Branch, Global Emerging Infections Surveillance Section (Dr. Seyoum and Dr. Forshey); Force Health Protection and Preventive Medicine (FHP&PM), MEDDAC-Korea/65th Medical Brigade (Dr. H-C Kim, Dr. Klein, COL Ellis, Ms. Yi, Ms. M-S Kim, LTC Jackson); Force Health Protection, U.S. Forces Korea/Combined Forces Command (COL McCall); Chief, Entomology Section, Eighth U.S. Army (MAJ Tucker).

Disclaimer: The views expressed herein are those of the authors and do not necessarily reflect the official policy or position of the Army, the Department of Defense, or the United States Government.

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