MILITARY MEDICINE, 181, 5:488, 2016 Malaria Trends in the Navy and Marine Corps, 2005 2013 Courtney L. Rudiger, MS*; Gosia Nowak, MSc, MPH ABSTRACT U.S. Sailors and Marines routinely deploy to regions where malaria is endemic, such as Africa and Asia. This report describes the trends, demographic characteristics, and exposure type and location for active duty Navy and Marine Corps malaria cases from January 2005 to December 2013. Electronic clinical records for laboratory results and hospitalizations, as well as reported medical events, for malaria were used to identify cases. There were 112 malaria cases identified among Navy and Marine Corps service members during the study time frame. Most cases were associated with travel to Africa (58.9%) and were duty related (60.7%); however, one-fourth of cases were associated with personal travel. The majority of cases exposed while on personal travel were foreign born (74.2%). This comprehensive assessment of trends and burden of malaria among Sailors and Marines is essential to ensure mission readiness and the management and evaluation of malaria control programs. Further analysis may be warranted to explore the relationship between personal travel and foreign-born status in the Department of the Navy to determine potential for additional intervention and education. *Programs and Policy Support Department, Preventive Medicine Directorate, Navy and Marine Corps Public Health Center, 620 John Paul Jones Circle, Suite 1100, Portsmouth, VA 23708. EpiData Center Department, Population Health Directorate, Navy and Marine Corps Public Health Center, 620 John Paul Jones Circle, Suite 1100, Portsmouth, VA 23708. The views expressed in this article are those of the author and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the U.S. Government. doi: 10.7205/MILMED-D-15-00174 INTRODUCTION Malaria is a disease of global concern, particularly within areas of Africa and Southeast Asia. Four parasitic species infect humans with malaria: Plasmodium falciparum, Plasmodium malariae, Plasmodium ovale, and Plasmodium vivax. 1 The Plasmodium parasite is transmitted to humans via the Anopheles mosquito. 1 The infectious process for each Plasmodium species varies, from symptoms appearing about a week after infection for P. falciparum and up to a year for P. ovale and P. vivax. 2 Globally, approximately 3.2 billion people are at risk of malaria infection (1.2 billion at high risk). In high-risk areas, the rate of malaria exceeds 1 per 1,000 population. In 2013, there were an estimated 198 million cases of malaria worldwide and approximately 584,000 deaths (0.3%). 90% of all malaria deaths occur in Africa. 3 Malaria was eliminated from the United States in the 1950s, though Anopheles mosquitoes capable of transmitting malaria remain prevalent. Only about 1,500 to 2,000 cases of malaria are diagnosed and reported in the United States annually. 4 The majority of cases occur in individuals who traveled to visit family in their home or birth country. 5 Other cases in the United States occur because of local transmission (when local mosquitoes become infected by biting persons who were infected in malaria-endemic countries) and transmission via blood transfusion. 4 Malaria is of particular public health importance because of the large global population at risk and infected annually, economic impacts, and effects on development. 6 In malariaendemic regions, there is also an increasing concern of the spread of resistance to most common malaria prevention and treatment options. 7,8 The U.S. military, including the Navy and Marine Corps, routinely engages in missions worldwide and has an increasing presence in Asia and Africa, which are primary locations for malaria transmission. As of December 31, 2014, approximately 36,000 Sailors and Marines were assigned to missions in East Asia and Pacific, over 3,500 were in North Africa and South Asia, and nearly 250 were in sub-saharan Africa. 9 Service members presence in those regions puts them at risk for acquiring malaria and becoming ill, further impacting the mission. Exposures to and infections with malaria are documented for several U.S. military missions where a significant number of cases occurred, including missions in Somalia in 1993, Liberia in 2003, and Haiti in 2010. 10 12 A study of malaria cases in mission-deployed U.S. service members identified that a third of the cases were exposed in one or more malaria-endemic regions. 13 Since 2008, U.S. Africa Command (AFRICOM) has been responsible for military relations with the Africa region and coordination of security and humanitarian support. 14 AFRICOM considers malaria the signature disease of concern for its area of responsibility because of its significant impact on deployers and travelers. 15 There are several resources available for deployers, other travelers, and health care providers within the military. The Deployment Health Clinical Center provides guidance to deployers on malaria risk, education, details on policies, and directives for each Armed Service, and clinical guidance. 16 The Department of the Navy (DON) has a Malaria Prevention and Control Instruction (BUMED Instruction 6230.16), as well as a detailed educational manual on testing, prevention, diagnosis, treatment, and identification. 17,18 As part of the instruction, Navy and Marine Corps Public Health Center developed a reference and information guide for malaria control and prevention which is considered a primary source of guidance. 18 The guide outlines 488 MILITARY MEDICINE, Vol. 181, May 2016
preventive measures including personal protective barriers, chemoprophylaxis, vector control, and unit-wide protection, such as training. Analysis of the burden of malaria on military service members is necessary to ensure programs and policies reflect risk and practice. The most recent formal analysis of U.S. military deployment exposures and burden evaluates cases occurring between 2003 and 2005. In 2005, 45 cases in the U.S. military were identified, of which 6 were among Navy and Marine Corps service members. 13 The U.S. military mission continuously evolves, providing changing exposure locations and therefore potential for changes in risk and impact since the time of this study. Annually, the Armed Forces Health Surveillance Center provides a snapshot of the malaria experience among U.S. military service members in the most recent year; the report is strictly based on encounter and admission diagnostic codes with supplemented information about travel from deployment records. 19 For this report, we describe the trends, demographic characteristics, and exposure type and location for Navy and Marine Corps malaria cases from January 2005 to December 2013. Further, we estimate the annual incidence rate of malaria by service branch. The cases were identified using a combination of electronic clinical records to determine information about exposure, laboratory confirmation, and severity of infection. METHODS Malaria cases from January 2005 to December 2013 were identified using three databases: Disease Reporting Systeminternet (DRSi), Health Level 7-formatted laboratory, and the Standard Inpatient Data Record (SIDR). DRSi is used by all U.S. military services to report cases of reportable conditions as indicated by the Armed Forces Reportable Event Guidelines. This analysis used medical event reports (MERs) for malaria from DRSi for Navy and Marine Corps active duty service members reported from any military treatment facility (MTF) from January 2005 to December 2013, based on illness onset date. The EpiData Center Department at Navy and Marine Corps Public Health Center receives clinical health care data originating from the Composite Health Care System (CHCS) via the Defense Health Surveillance System on a daily basis, within approximately 2 days of record generation. The data contain information for Department of Defense (DoD) beneficiaries and their dependents who sought care at a fixed MTF. For this analysis, CHCS microbiology and chemistry databases were queried for malaria tests using the following search wildcard terms: malaria, plasmodium, vivax, ovale, and falciparum. A standardized algorithm for categorizing microbiology and chemistry records was applied to identify positive blood smears and rapid diagnostic tests. Some laboratory records contain tests performed for quality control purposes where the test is attributed to a fake identification number, but appears to be for a real person. To ensure that all positive malaria tests identified in the laboratory data were associated with a service member and were not quality control tests, laboratory cases were matched to Defense Manpower Data Center (DMDC) rosters by a personal identifier. The DMDC rosters contain personnel records for all Navy and Marine Corps service members. Positive malaria tests that were not associated with a service member in DMDC were not included in the analysis (n = 5). The SIDR is an electronic database containing records of inpatient health care services provided to DoD beneficiaries at fixed MTFs. Records originate from patient records entered into CHCS. For active duty service members, some hospitalizations outside the Military Health System are also captured in the data. For this analysis, inpatient records containing the International Classification of Diseases, 9th Revision, Clinical Modification code for malaria (084) in the primary diagnosis field were selected. The primary diagnosis field was used to help ensure that hospitalization records were associated with true malaria cases and not instances of suspected malaria or rule-outs. To be considered a case, a patient required at least one positive malaria record in DRSi, SIDR, or laboratory records. Active duty status was determined using the patient category code in the laboratory and SIDR data and the STATUS variable in DRSi. Active duty status was confirmed in DMDC. The date of the malaria event was determined using the earliest date among all malaria records for a case (laboratory: collection date, SIDR: admission date, DRSi: date of onset). Country of birth and rank information were obtained from DMDC personnel records. Since travel is a key risk factor for malaria, it was necessary to ensure that travel information for all cases was as complete as possible. The country of exposure and exposure status (duty or personal travel) were identified in DRSi, if completed. Cases with missing travel exposure information were further reviewed using the Armed Forces Health Longitudinal Technology Application (AHLTA), the electronic medical record system for all DoD MTFs. AHLTA includes provider notes and diagnoses for outpatient encounters, laboratory results, and other clinical notes. Countries were grouped into regions based on mission relevance (Africa, Middle East, Southeast Asia, Caribbean, Unknown). The Plasmodium species identified in the laboratory result was considered most accurate for species description. If a species was not specified in the laboratory result, the species listed in DRSi was considered. If no species information was available in either data source, the case was categorized as malaria unspecified. The length of stay for a hospitalization was calculated using the difference between admission and discharge dates in the SIDR. Population counts (person-years) for Navy and Marine Corps active duty service members in each year of analysis were retrieved from the Defense Medical Epidemiology Database maintained by the Armed Forces Health Surveillance MILITARY MEDICINE, Vol. 181, May 2016 489
Center. These counts were used as denominators for calculating yearly malaria incidence rates by service. Statistical Analysis Software v9.2 (SAS Institute, Cary, North Carolina) was used to organize and analyze the data. Frequencies and rate calculations were used to describe the data. RESULTS There were 112 malaria cases identified among Navy and Marine Corps service members from January 2005 to December 2013. Figure 1 shows the frequency of malaria cases by year. Overall, the majority of cases were males (92.9%), age 20 to 29 (62.5%), and Navy service members (61.6%) (Table I). Eighty-five percent of cases were enlisted service members, most of which were ranks E4 to E6 (noncommissioned officers). Half of the malaria cases were caused by P. falciparum; however, nearly one-third of cases had unspecified Plasmodium species (29.5%). Fifty-five percent (n = 62) of malaria cases were hospitalized, with an average length of stay of 3 days. The summer months had the greatest frequency of malaria cases (32.1%), followed by the spring months (31.3%). Malaria incidence rates are displayed by year and service in Figure 2. Rates among Navy personnel generally increased to a peak of 4.9 per 100,000 service members in 2010, and decreased in the following years. Rates among Marine Corps personnel were highest in 2011 (6.5 per 100,000 service members) but varied widely from year to year. Malaria rates were higher among Marine Corps service members compared to Navy service members in 5 of the 9 years of analysis. Travel characteristics of malaria cases are described in Table II. Most cases were associated with travel to Africa (58.9%), followed by the Middle East (23.2%). Middle Eastern exposures (n = 26) were primarily in Afghanistan (73.1%), whereas African exposures (n = 66) were primarily in Ghana (22.7%), Liberia (12.1%), or Nigeria (12.1%). All but one Caribbean exposure occurred in Haiti in 2010. Most travel exposures were duty-related (60.7%) and just over one-fourth were related to personal travel. The majority of personal travel exposures were travel to Africa (93.3%). Most duty FIGURE 1. Frequency of malaria cases by year (n = 112), DON active duty members, 2005 2013. TABLE I. Demographic, Travel, and Clinical Characteristics of Malaria Cases (n = 112), DON Active Duty Service Members, 2005 2013 Count Percent Service Marine Crops 43 38.4 Navy 69 61.6 Gender Female 8 7.1 Male 104 92.9 Age Group <20 2 1.8 20 29 70 62.5 30 39 25 22.3 40 49 12 10.7 50+ 2 1.8 Unknown 1 0.9 Rank E1 E3 22 19.6 E4 E6 65 58.0 E7 E9 9 8.0 O1 O7 8 7.1 Unknown 8 7.1 Country of Birth United States 75 67.0 Foreign Born 32 28.6 Africa 26 81.3 Europe 2 6.3 Asia 2 6.3 Caribbean 2 6.3 Unknown 5 4.5 Region of Exposure Africa 66 59.9 Caribbean 8 7.1 Middle East 26 23.2% Southeast Asia 8 7.1 Unknown 4 3.6 Exposure Type Duty 68 60.7 Personal 30 26.8 Unknown 14 12.5 Species P. falciparum a 56 50.0% P. ovale 3 2.7% P. vivax a 21 18.8% Unspecified 33 29.5% a One dual falciparum/vivax case was counted once for each species. Datasources: CHCS microbiology and chemistry, DRSi, SIDR, DMDC, AHLTA. exposures were also travel to Africa (45.6%), however, many were travel to the Middle East (36.8%). The most frequent locations for duty exposures differed by service; the most frequent location of duty-related exposures was the Middle East for Marines (46.9%) and Africa for Sailors (58.3%). Differences in country of birth in relation to exposure type were observed. The majority of cases exposed while on duty (n = 68) were U.S. born (91.2%), whereas the majority of cases exposed while on personal travel (n = 30) were foreign born (74.2%). Of foreign-born personnel exposed 490 MILITARY MEDICINE, Vol. 181, May 2016
FIGURE 2. Incidence rates of malaria by year and service, DON active duty service members, 2005 2013. TABLE II. Region of Exposure by Exposure Type for Malaria Cases (n=112), DON Active Duty Service Members, 2005 2013 Duty (n = 68) Exposure Type Personal (n = 30) Unknown (n = 14) Region of Exposure n % n % n % Africa 31 45.6 28 93.3 7 50.0 Caribbean 5 7.4 1 3.3 2 14.3 Middle East 25 36.8 1 3.3 0 Southeast Asia 7 10.3 0 1 7.1 Unknown 0 0 4 28.6 Datasources: DRSi, AHLTA. while on personal travel (n = 22), most were born in Africa and were traveling there when exposed (95.5%). DISCUSSION As Navy and Marine Corps service members continue to support a variety of missions worldwide, particularly to malaria-endemic areas such as Africa and Asia, the risk for malaria infection continues. It is important to track trends in malaria incidence in this population to ensure policies and programs for prevention reflect the current burden of disease. Results from this analysis showed that the incidence of malaria among Navy and Marine Corps active duty service members varied widely from 2005 to 2013, and case counts were relatively small. No clear trends were observed; most peaks in incidence were related to clusters associated with particular units deployed to endemic areas. Sailors and Marines often have different missions and in turn impact on their deployment locations. The Navy service members often provide global support with deployment of construction battalions, who help establish infrastructures including roadways, hospitals and facilities. Many such missions require deployments to desolate areas, frequently with no embedded medical capabilities. 20,21 Since the beginning of Operations Iraqi and Enduring Freedom, Marines have had a consistent presence in the Middle East in the role of security, training, combat, and logistics operations. 22 This difference is visible in this analysis, where the most frequent location of duty-related exposures was the Middle East for Marines (46.9%) and Africa for Sailors (58.3%). The historical threat of malaria for U.S. troops deploying to Africa has been well documented. 10 Over the time frame of this analysis, U.S. military operations in Africa increased rapidly and in 2007, the African Command (AFRICOM) became operational. Before this, U.S. military operations in Africa fell under three different Commands (European Command, Central Command, and Pacific Command). The creation of a new Unified Combatant Command in Africa resulted in an increase of Navy and Marine Corps personnel deployed there. For example, Naval Construction Battalions ( Seabees ) were needed to establish permanent sites in the region. 20,21 As the number of units deployed to Africa increased, the potential for a rise in malaria cases increased as well, and our analyses show an increase in malaria rates for both Sailors and Marines from 2007 to 2011. In addition, the majority of all duty-related cases among Sailors were associated with travel to Africa (21/36, 58.3%). In 2010, a directly observed therapy policy was implemented for malaria prophylaxis in response to the increase in cases. 18 Results of these analyses suggest that this policy was effective, with rates in both services decreasing in 2012 and 2013. However, it may be too early to see the true impact of this policy and analyses should be revisited. There were 7 cases of malaria in the spring of 2010 that were related to travel to Haiti. Five of these were duty-related, and the remaining 2 cases had an unknown exposure type. These cases were all likely related to recovery efforts in response to the earthquake that occurred in Haiti in January 2010, and highlight the increased risk for malaria when responding to disaster recovery missions. Increased risk arises from large amount of time spent outside, flooding/pooling of water, and very fluid and often disorganized environments. Malaria cases acquired in Haiti during this time were previously documented in the Centers for Disease Control and Prevention s Morbidity and Mortality Weekly Report. 12 Malaria outbreaks are not often associated with earthquakes. In an analysis of infectious disease outbreaks related to geophysical disasters over a 20-year period, only one instance of a malaria outbreak related to an earthquake was observed. The outbreak was related to P. vivax malaria in Costa Rica following an earthquake and heavy rainfall in 1991. 23 Despite the relatively minimal occurrence of malaria outbreaks in these situations, it remains important to exercise proper disease prevention measures when responding to earthquakes or other natural disasters in malaria-endemic regions. The high proportions of exposure status and country of birth suggest leisure travel for foreign-born service members may be a considerable issue within the Navy and Marine MILITARY MEDICINE, Vol. 181, May 2016 491
Corps. A previous study of malaria in association with country of birth among military service members found that rates were higher among those born in western Africa compared to other countries. 24 Of the cases that occurred during personal travel in this study, over 90% were born in Africa (data not shown). The relationship between personal travel and foreign born status should be explored further to determine potential for intervention, education, and protection. Malaria risk related to personal travel to visit friends or relatives in countries of origin is also a concern in the civilian population. 4,5,25 The military population is not very different in terms of motivation or reason for travel in these cases, except military travelers experience the potential impact on mission readiness if they become ill. Military service members may also have improved access to health care for prophylaxis and education compared to the civilian population. However, such travelers, both military and civilian, may not fully realize or accept the risk for malaria in their native countries and as a result may not be fully compliant with prophylaxis. There are data limitations to consider while interpreting the results of this analysis. DRSi is a passive medical event reporting system that allows users to document events on a case-by-case basis. Medical event report completeness and validity is reliant upon accurate data entry. Reportable medical events identified outside the Military Health System, such as at community hospitals, are not recorded in DRSi unless the case is reported to a local military command. Supplementing DRSi with laboratory and inpatient encounter data can help assure the validity of reported cases. Laboratory data maintained at the EpiData Center Department are generated within the CHCS at fixed MTFs. These data do not include records from shipboard facilities, battalion aid stations, purchased care, or in-theater facilities. This is primarily a concern for exposures in Afghanistan, where providers in forward deployed clinics may treat empirically and underestimate the number of P. vivax cases from the region. On the other hand, it is likely that most Africa exposures are captured, where exposures are primarily to P. falciparum and require provider vigilance to avoid severe morbidity and mortality. These cases are often evacuated to a fixed facility, where testing and reporting would be captured in CHCS. Laboratory testing may be done in host country facilities and such cases are not considered confirmed until DoD public health personnel confirm the diagnosis. When a case of malaria is identified in a unit, there is concern whether appropriate preventive procedures and protections were followed by the unit. Therefore, other members of the unit may be tested to evaluate malaria exposure, not necessarily infection. In these situations, those members that test positive are not considered cases until symptoms arise, though they would be counted as cases in this analysis because of the way cases are defined. Typically these practices do not change from year to year and so the trends illustrated here likely represent true disease burden. CONCLUSIONS Providing a comprehensive assessment of trends and distribution of malaria among military service members is essential to ensuring mission readiness and the management and evaluation of malaria control programs. The goal of the U.S. Navy malaria control program is not only prevention and control, but also assessment of risk in active duty service members and other beneficiaries. Results of this analysis suggest that strategies specifically targeting foreign-born service members conducting personal travel to malaria-endemic countries may need to be examined and further developed. In addition, routine surveillance of malaria cases is necessary for quick response to cases as they arise. Malaria surveillance can consist of the identification of laboratory-confirmed specimens, suspected infection based on exposure and symptoms, as well as direct identification of those at risk. Timely and accurate reporting to DRSi can ensure that all cases are reported and documented correctly for notification and future analysis purposes. ACKNOWLEDGMENTS The authors would like to thank Asha Riegodedios for providing perspective and guidance on malaria impact and programs, as well as CAPT William Padgett for support with detailed case validation. REFERENCES 1. Centers for Disease Control and Prevention: About malaria: Frequently asked questions. 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