Am. J. Trop. Med. Hyg., 76(2), 2007, pp. 275-279
Copyright © 2007 by The American Society of Tropical Medicine and Hygiene
MALARIA IN U.S. MILITARY FORCES: A DESCRIPTION OF DEPLOYMENT EXPOSURES FROM 2003 THROUGH 2005
PAUL CIMINERA* AND
JOHN BRUNDAGE
Army Medical Surveillance Activity, U.S. Army Center for Health Promotion and Preventive Medicine, Washington, District of Columbia
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ABSTRACT
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U.S. service members are often deployed to regions endemic for malaria. Preventive measures play an important role in mitigating the risk of disease and adverse effects on mission performance. Currently, a large contingent of U.S. forces is deployed in malarious regions in southeast and southwest Asia. The purpose of this study was to describe malaria cases reported by the tri-service reportable medical events system in terms of exposure (deployment history) and latency of infection. We conducted a retrospective analysis of population health data routinely collected for disease surveillance. All malaria reports received into the Defense Medical Surveillance System by January 3, 2006 with a date of onset between January 1, 2000 and December 31, 2005 in which the individual diagnosed is a member of the active or reserve military components linked to personnel and deployment data were analyzed to determine assignment and deployment history. The main outcome measure was the ICD9-CM diagnosis of malaria (Plasmodium vivax, P. falciparum, P. ovale, P. malaria, and unspecified malaria) by date of onset and days from exposure. A total of 423 cases of malaria were reported during the study period. The Army (n = 325) and the Marine Corps (n = 46) had the highest number of reported cases. Plasmodium vivax (n = 242) and P. falciparum (n = 92) caused nearly four-fifths of all reported cases. During the period from 2003 through 2005, 34% of deployed cases were exposed to more than one malaria-endemic region. Seventy-four cases had been assigned in the Republic of Korea, and all were present in Korea during the high risk transmission period. Seventy-eight cases had documented service in Afghanistan; only 4 had off-season exposure and no other documented exposures. Sixty cases had documented exposure during Operation Iraqi Freedom (OIF). Only six seasonally exposed and six off seasonally exposed OIF cases had no other documented exposure. Fifty percent of Korean cases were diagnosed during an exposure season, and only 3% of Afghan cases were diagnosed during an exposure season. Soldiers in today’s military can be exposed to more than one malaria-endemic region prior to diagnosis. This presents new complexities for disease monitoring and prevention policy development.
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INTRODUCTION
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For centuries, malaria has been considered a significant threat to the health and effectiveness of military forces that conduct operations in malaria-endemic areas. Since the end of the Cold War, U.S. military forces have increased the frequency, location, and scope of overseas operations, many of which take place in malaria-endemic areas. In addition, in the 1990s, Plasmodium vivax malaria re-emerged along the demilitarized zone in the Republic of Korea.1 Soldiers who conduct operations or train in areas adjacent to the demilitarized zone during summer-fall transmission seasons (when mosquito vectors of malaria are most abundant and active) are at highest risk for infection. A significant proportion of the malaria infections acquired in the Republic of Korea have long latency periods (typical of temperate strains of P. vivax).2
Since October 2001, many U.S. service members have had multiple, relatively short assignments to malaria-endemic areas, including Afghanistan, Iraq, the Republic of Korea, and various countries in Central America, South America, and Africa. As a result of long latency periods and frequent short deployments, P. vivax malaria acquired in one area may not clinically present until months later when the service member is serving in a different area. This may also occur if there are consecutive assignments during which malaria chemoprophylaxis is taken but terminal prophylaxis with primaquine is never completed. Undoubtedly, in recent years, it has become more difficult to determine the times and locations of malaria infection acquisitions and in turn the effectiveness of prevention policies and practices.
For this report, we summarize frequencies, trends, and demographic and military characteristics of all cases of malaria that were diagnosed and reported among members of the U.S. Armed Forces between January 2000 and December 2005. We also summarize the experiences of reported cases in regard to assignments/deployments/travel to the Republic of Korea, Afghanistan, Iraq, and other countries during the period January 2003 through December 2005. Finally, we estimate the distributions of latency periods based on assignment and estimates of the time of infection acquisitions.
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METHODS
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U.S. military regulations require reporting of all malaria cases. Each military service reports cases through separate public health reporting mechanisms. In turn, these reports are forwarded to the Army Medical Surveillance Activity (AMSA) where they are merged into the Defense Medical Surveillance System (DMSS), the central repository of military health surveillance data for the Department of Defense. The DMSS contains longitudinal records of all service members’ personnel, medical, and serologic information.
For this analysis, the surveillance period was January 1, 2000 to December 31, 2005. The surveillance population included all individuals who served in an active or reserve component of the U.S. Armed Forces any time during the surveillance period. A case was defined as a report of malaria in a member of the surveillance population where the date of onset or diagnosis was during the surveillance period.
Each malaria case report includes demographic information, date(s) of clinical onset and/or diagnosis, and pertinent travel history (by country). Reporting guidelines also require laboratory confirmation of diagnoses by blood smear.3 The DMSS business rules assign an event date to reports if they are missing a date of onset in the following precedence: date of entry in the service surveillance hub, date of receipt at the service surveillance hub, or date of receipt at AMSA.
These case reports were merged with assignment and deployment information contained within the DMSS to allow examination of deployments by individual to the Republic of Korea, Operation Enduring Freedom in Afghanistan (OEF-A), and Operation Iraqi Freedom (OIF) in Iraq. Reports received and integrated into the DMSS by January 3, 2006 were used for the analysis.
Nominal exposures of reported cases to malaria risk in the Republic of Korea, Afghanistan, and/or Iraq were characterized based on routinely collected military assignment and overseas deployment histories. Each case was considered exposed in the Republic of Korea, Afghanistan, and/or Iraq if malaria was diagnosed during or after a documented assignment or deployment to the respective location. In addition, the exposure of each case to each location was further characterized in relation to season. Malaria transmission seasons were defined as June through October of each year (periods of highest activity of mosquito vectors in temperate climates).
Finally, the number of days elapsed from the midpoint of the individual’s last seasonal exposure was calculated. For this computation, exposure was terminated upon the date of diagnosis for individuals diagnosed during the exposure season. If an individual had more than one report, the earliest date of onset was used. For latency calculation, Malaria ICD9-CM codes other than malaria, vivax (084.1) and malaria, unspecified (084.6) were excluded. The data was analyzed using SAS version 9.1 software (SAS, Cary N.C.) tabulations. This data was obtained as part of the public and occupational health surveillance of the U.S. military population. Informed consent was not required or obtained for this purpose.
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RESULTS
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During the six-year period, 423 cases of malaria were reported among U.S. service members (Table 1
). The Army (n = 325) and Marine Corps (n = 46) accounted for nearly 90% of the total cases. More cases were reported in 2003 than in any other year of the period. Overall, there was a distinct seasonality in the dates of onset of cases with relative peaks in July and August (Figure 1). Of note, 32 cases among Marines that were received by AMSA from the service surveillance hub in February 2004 were missing a date of onset. According to AMSA business rules, they were assigned an event date of February 2004. These cases were known to be acquired during an operation in Liberia in 2003.4 Plasmodium vivax (n = 242) and P. falciparum (n = 92) caused nearly four-fifths of all reported cases. In most other cases, the species was not reported. Cases of P. vivax peaked in 2003 (55 cases) and decreased sharply in 2004 (Table 2).
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FIGURE 1. Cases of malaria in U.S. military forces by month of onset or diagnosis, 2000–2005. A = Army; F = Air Force; M = Marines; N = Navy.
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Prior to diagnosis, a case may have served in more than one region with malaria transmission risk. Table 3 summarizes the military service experiences (exposures) of cases in relation to malaria transmission seasons in the Republic of Korea, Afghanistan (OEF-A), and Iraq (OIF). Approximately one-third (n = 55, 34%) of deployed cases were exposed to more than one malaria-endemic location prior to diagnosis.
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TABLE 3 Reported exposures to Iraq, Afghanistan, and/or Korea during military assignments in relation to malaria transmission seasons among U.S. military members reported as cases, 2003–2005*
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Republic of Korea.
Seventy-four cases had military service in the Republic of Korea prior to diagnosis. Of these, 58 (78%) had no in-season exposures to malaria risk other than in this country, and 16 (22%) had in-season exposures in Afghanistan and/or Iraq after leaving the Republic of Korea and before diagnosis. There were no cases among individuals with only non-seasonal exposures in the Republic of Korea.
Operation Enduring Freedom in Afghanistan.
Seventy-four cases had documented in-season military service in Afghanistan prior to diagnosis. Of these, 41 (55%) had no exposures to malaria risk other than in Afghanistan; 22 (30%) had off-season exposures in Iraq after leaving Afghanistan. A case series for the Afghanistan-Iraq cohort has been previously reported.5 Seven (9%) had prior in-season exposures in the Republic of Korea. Four cases had off-season service in Afghanistan as their only documented exposures (Table 3
).
Operation Iraqi Freedom.
Sixty cases had documented military service in Iraq prior to diagnosis. Of these, 29 (48%) had in-season exposures in Iraq; however, 10 also served in the Republic of Korea during a transmission season and 6 also served in Afghanistan (5 during a transmission season). Of 14 cases with in-season Iraq exposure and no other deployment related exposures prior to diagnosis, seven reported exposures in other malaria-endemic areas (e.g., Nigeria, Honduras, Senegal) (Table 4).
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TABLE 4 Characteristics of malaria cases with military assignments in Iraq (during malaria transmission season) but none in Afghanistan or Korea, U.S. military, 2003–2005
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Thirty-one (52%) cases served in Iraq only during the off-season. Of these, 22 had preceding service in-season in Afghanistan,6 two had preceding in-season service in the Republic of Korea, one had documented preceding service in Afghanistan in the off-season only, and three reported travel to Afghanistan (n = 2) or Djibouti (n = 1). Six cases (Navy, n = 3; Army, n = 2; Marines, n = 1) with documented service in Iraq during the off-season had no other documented or reported exposures to an area with a malaria risk (Table 3).
Other exposures.
Sixty-five cases did not have documented military service in the Republic of Korea, Afghanistan, or Iraq prior to a malaria diagnosis (Table 5). Of these, 18 (28%) reported travel to malaria-endemic countries of which Honduras (n = 5) was the most common, and 47 (72%) had no documented histories of service or travel in a malaria-endemic area (Marines, n = 34; Navy, n = 11; Army, n = 1; Air Force, n = 1). Liberia was reported in the travel histories of only three cases. However, many cases were acquired during (but not reported as related to) a large outbreak of P. falciparum malaria that affected a U.S. military force in Liberia in August–September 2003.4
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TABLE 5 Reported exposures (by country) of malaria cases with no military assignments in Iraq, Korea, or Afghanistan, by U.S. military service, 2003–2005
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Distributions of latency periods for cases diagnosed with P. vivax or other malaria.
Time from infection to the first clinical manifestation of malaria was estimated in relation to deployment experiences for 126 cases of P. vivax" or other malaria (Table 6). Among these, 62 cases were seasonally exposed in the Republic of Korea but not in Afghanistan and 64 cases were seasonally exposed in Afghanistan but not in the Republic of Korea. Of the 62 cases associated with the Republic of Korea, 31 (50%) were diagnosed in this country during the same transmission season (short latency) and were presumably infected (2 were assigned during more than one season). Of the others, three (5%) were diagnosed within 240 days and 28 (45%) were diagnosed more than 240 days (long latency) after the mid-points of their last in-season periods of service in the Republic of Korea. Of the six cases with the longest latencies, five served in Iraq after leaving the Republic of Korea and before their first clinical manifestations of malaria.
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TABLE 6 Estimated latency periods (days from midpoint of estimated exposure to clinical presentation) of Plasmodium vivax and unspecified malaria cases considered acquired in Korea or Afghanistan, U.S. military, 2003–2005*
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Of the 64 Afghanistan-associated cases, 2 (3%) were diagnosed in Afghanistan during the same transmission seasons and were presumably infected (one was assigned during more than one season). Of the others, 19 (29%) were diagnosed within 240 days and 43 (66%) were diagnosed more than 240 days after the midpoints of their last in-season periods of service in Afghanistan.
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DISCUSSION
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In the past three years, approximately one-third of deployed U.S. service members diagnosed with malaria had recent exposures in more than one malaria-endemic area. In many cases, malaria infections were likely acquired during assignments other than those that immediately preceded their initial clinical manifestations. For example, of 60 service members diagnosed with malaria after service in Iraq, only 20 did not have service in Korea and/or Afghanistan prior to that in Iraq, and most of those without such service had at least one reported exposure in another malaria-endemic area. Thus, although many cases of malaria had initial clinical presentations shortly after service members returned from Iraq, relatively few malaria infections were likely acquired there. Implications in regard to assessing location-specific risks, determining indicated countermeasures, and monitoring the effectiveness of prevention practices are significant.
Reporting bias may underestimate cases diagnosed and treated in theatre as the communication channels and laboratory capability in OIF and OEF are not as developed or robust as those available in the Republic of Korea. Multiple military health activities, including AMSA, are actively monitoring for cases and correspond with the submitting facilities to improve case reporting. We realize this report is based on routinely collected surveillance data, and as with any such system, the data are inevitably incomplete and inaccurate. For example, we are aware of recent large outbreaks of malaria among U.S. service members that were not completely or accurately reported through routine surveillance mechanisms (and as a matter of policy, details of case reports submitted from field sites are not modified at the surveillance center).6 However, summaries of cases reported to the system are informative regarding prevention and treatment policies and practices.
In this report, there were approximately equal numbers of cases of malaria presumably acquired in the Republic of Korea with short (i.e., clinically manifested during the same transmission season) and long (i.e., clinically manifested during the next transmission season or later) incubation times. Other studies have reported approximately 3:1 distributions of long and short incubation periods, respectively, for malaria cases acquired in the Republic Korea. During this surveillance, chemoprophylaxis was not routinely given to U.S. service members in the Republic of Korea. It is possible that liver-stage infections of some cases acquired in this country were radically cured (before they could be clinically expressed) during prophylactic courses of primaquine at the end of subsequent assignments in malaria-endemic areas. Assessments of the times and locations of malaria infection acquisitions are complicated by the significant variability of latency periods of temperate zone P. vivax. Molecular epidemiologic studies may be able to provide a more precise estimate of origin. The Walter Reed Army Institute of Research (WRAIR) encourages clinicians to send samples from military cases to WRAIR for further laboratory analysis.
Finally, few (3%) cases acquired in Afghanistan during the surveillance period had short incubation times. There were much higher proportions of short incubation cases acquired in the Republic of Korea during the same period and among cases acquired in Afghanistan among Russian soldiers in the 1980s.7 The difference undoubtedly reflects the suppression of blood stage infections by chemoprophylactic drugs used routinely by U.S. service members in Afghanistan, but not Russian soldiers in Afghanistan or U.S. soldiers in the Republic of Korea.
Received September 25, 2006.
Accepted for publication November 10, 2006.
Acknowledgments: We thank the Army, Air Force and Navy preventive medicine community for their continued vigilance and timely reporting of malaria cases in U.S. service members.
Disclosure: The authors are employees of the U.S. Department of Defense and wrote this paper as part of their daily activities.
Disclaimer: The views expressed in this paper are those of the authors and do not reflect the official policy or position of the Department of the Army, Department of Defense, or the U.S. Government.
* Address correspondence to Paul Ciminera, Army Medical Surveillance Activity, Building T-20, Room 213, (Attn: MCHB-TS-DMS) 6900 Georgia Avenue, NW, Washington, DC 20307-5001. E-mail: paul.ciminera{at}us.army.mil 
Authors’ address: Paul Ciminera and John Brundage, Army Medical Surveillance Activity, Building T-20, Room 213, (Attn: MCHB-TS-DMS) 6900 Georgia Avenue, NW, Washington DC, 20307-5001, Telephone: 202-782-0471, E-mails: paul.ciminera{at}us.army.mil and john.brundage1{at}us.army.mil.
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- Feighner BH, Pak SI, Novakoski WL, Kelsey LL, Strickman D, 1998. Reemergence of Plasmodium vivax malaria in the republic of Korea. Emerg Infect Dis 4: 295–297.[ISI][Medline]
- Oh MD, Shin HS, Shin DH, Kim US, Lee SH, Kim NJ, Choi MH, Chai JY, Choe KW, 2001. Clinical features of vivax malaria. Am J Trop Med Hyg 65: 143–146.[Abstract]
- Army Medical Surveillance Activity, 2004. Tri-Service Reportable Events, Guidelines and Case Definition. Available from http://amsa.army.mil/documents/DoD_PDFs/May04TriServREGuide.pdf
- Susi B, Whitman T, Blazes DL, Burgess TH, Martin GJ, Freilich D, 2005. Rapid diagnostic test for Plasmodium falciparum in 32 Marines medically evacuated from Liberia with a febrile illness. Ann Intern Med 142: 476–477.[Free Full Text]
- Kotwal RS, Wenzel RB, Sterling RA, Porter WD, Jordan NN, Petruccelli BP, 2005. An outbreak of malaria in US Army Rangers returning from Afghanistan. JAMA 293: 212–216.[Abstract/Free Full Text]
- Armed Forces Epidemiologic Board (AFEB) Presentation, 2004. Malaria Outbreak August 2003. Available from www.ha.osd.mil/afeb/meeting/021704meeting/AFEB%20Winter%202004%20Day%202%20McMillan.ppt#259
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TOP
ABSTRACT
INTRODUCTION
