Am. J. Trop. Med. Hyg., 75(4), 2006, pp. 762-767
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene
INCIDENCE, ETIOLOGY, AND IMPACT OF DIARRHEA AMONG DEPLOYED US MILITARY PERSONNEL IN SUPPORT OF OPERATION IRAQI FREEDOM AND OPERATION ENDURING FREEDOM
MARSHALL R. MONTEVILLE*,
MARK S. RIDDLE,
USHA BAHT,
SHANNON D. PUTNAM,
ROBERT W. FRENCK,
KENNETH BROOKS,
MANAL MOUSTAFA,
JAIME BLAND, AND
JOHN W. SANDERS
US Naval Medical Research Unit No. 3, Cairo, Egypt; US Army Central Command Troop Medical Clinic, Doha, Qatar; US Naval Medical Research Unit No. 2, Jakarta, Indonesia; University of California Los Angeles, Los Angeles, CA
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ABSTRACT
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A health assessment survey was collected from US military personnel deployed to the Middle East taking part in the "Rest and Recuperation" program or on temporary assignment to Camp As Sayliyah Doha, Qatar, from January to December 2004. In addition, a concurrent clinic-based observational study was conducted to determine pathogen etiology and potential risk factors. From 28,322 health assessment surveys, overall self-reported incidence of diarrhea was 4.9 cases per 100 person-months. Disease incidence increased with rank and was higher in Iraq compared with Afghanistan. During this period, 109 US military personnel with acute diarrhea and 85 asymptomatic personnel were enrolled in the observational study. Enterotoxigenic E. coli (ETEC) was the predominant pathogen (32%), followed by enteroaggregative E. coli (12%) and Salmonella spp. (6%). These data are consistent with previous reports implicating ETEC as the primary cause of acute diarrhea for military personnel deployed to this region.
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INTRODUCTION
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Non-combat injuries and illness have historically resulted in a significant decrease in operational readiness of military personnel.1–4 Accurately assessing the incidence, etiology, and impact of these health threats to the deployed population might prove valuable for the development of intervention strategies. Diarrheal illnesses have long been known as one of the most common medical conditions negatively impacting the performance of deployed personnel.2–4 This experience has continued in the present deployments to Iraq and Afghanistan. A survey of US troops at the time of completion of their tour found that 70% of deployed forces were afflicted by at least one episode of diarrhea, and 56% reported having multiple episodes during their deployment (median length deployed = 7.2 months).5 While several epidemiologic studies have recently been reported on the epidemiology of travelers’ diarrhea and other health threats among deployed troops to the Middle East region,5–8 very few have been conducted to systematically evaluate pathogen etiology among these populations. One study was conducted among troops during the initial invasion phase in Iraq; limitations caused by the combat setting reduced inference of the findings.9 We feel it is of continued benefit to conduct ongoing surveillance for the incidence, impact, and causes of diarrhea in areas of military deployment to not only validate previous studies, but to monitor temporal trends. Furthermore, this study was designed to collect information on pathogen attributable etiology from troops deployed to combat areas where there is limited information and where it is challenging to directly obtain in-country data.
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MATERIALS AND METHODS
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The study was conducted at Camp As Sayliyah in Doha, Qatar. The camp provides rest and recuperation (R&R) for US troops deployed in support of operations within Iraq and Afghanistan. On arrival at Camp As Sayliyah, all personnel attend a briefing on base activities and complete a health assessment survey. This information was collected by non-study personnel in attempt to assist the R&R population with medical needs during their brief stay on base. Included in the information collected was demographic information (rank and country of assignment), as well as two questions regarding current or recent history of diarrhea, nausea, or vomiting. The R&R participants were subsequently briefed by study personnel. Individuals were requested to come to the camp medical facility for evaluation if they were currently experiencing diarrhea or developed diarrhea during their stay. For this study, diarrhea was defined as three or more loose or liquid stools in a 24-hour period or two or more loose stools accompanied by fever or other gastrointestinal symptoms including abdominal cramps, nausea, or vomiting.3,10 Individuals presenting to the clinic for evaluation of diarrhea were asked to enroll in the observational study to determine the cause of their illness and to identify risk factors for developing diarrhea. After clinical evaluation, individuals agreeing to enroll in the study provided informed consent followed by completion of a questionnaire. The questionnaire assessed attitudes and behaviors to delineate patterns that may be associated with diarrhea as well as recorded detailed description of symptoms associated with current (cases only) and past episodes of diarrhea. Attitude and behavioral questions pertained to hand washing and consumption of raw vegetables or ice while off military establishments in the region. Finally, participants were asked to provide a stool sample for microbiological evaluation. To assess the significance of microbiological findings, a group was enrolled from personnel evaluated at the clinic for complaints other than diarrhea or fever. These individuals were termed asymptomatic, completed the same study questionnaire and provided a stool specimen, which was processed in an identical manner to acute samples.
Laboratory testing.
Stool samples were cultured and incubated at 37°C on MacConkey, hektoen, thiosulfate citrate bile sucrose (TCBS), and blood agar plates. Skirrow media incubated at 42°C was used to culture for Campylobacter organisms. Up to five E. coli–like colonies were picked and preserved in trypticase soy broth containing 15% glycerol and stored at –70°C until further testing was performed at NAMRU-3. Enterotoxigenic E. coli (ETEC) were identified using previously described criteria.11,12 Enteroaggregative (EAEC) and enteropathogenic (EPEC) E. coli were identified by polymerase chain reaction (PCR) analysis using gene-specific primers after DNA preparation directly from stool.13–15 In addition, microscopic examination of preserved stool specimens was conducted at NAMRU-3 by a trained parasitologist to identify any existing ova or parasites.
Statistical analysis.
Descriptive analysis on the self-report health assessment data were conducted using Poisson regression to estimate illness incidence (diarrhea or nausea/vomiting) and evaluate differences in incidence caused by potential predictor variables of country, rank, and calendar month. For the observational study, to test the statistical significance among discrete variables (i.e., proportions), the Mantel-Haenszel 
2 or Fisher exact tests were used. For two-group significant testing between continuous variables, either the Student t test (parametric) or the Wilcoxon rank (non-parametric) were used. Where there was more than two group comparison, the Kruskal-Wallis or an ANOVA was used.
All data was double entered into Epi-Info version 6. Stata Version 9 (College Station, TX) and SAS Version 8 (Cary, NC) were used for all analyses. Statistical significance was two-tailed and set at P < 0.05 for each analysis. The health assessment survey description was conducted on de-identified data that was collected solely for health screening purposes by non-study personnel and thus was exempt from the requirement for Institutional Review Board approval. The observational study was conducted under Institutional Review Board reviewed protocol DoD# NAMRU3.2004.0009.
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RESULTS
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Health assessment survey.
Between January 2004 and December 2004, 28,322 health assessment surveys were collected and available for analysis. Seventy-five percent of the respondents listed their duty station on the survey, with 60% (N = 17,055) of the active duty population reporting serving in Iraq, 15% (N = 4,098) in Afghanistan, and 0.6% (N = 187) in Uzbekistan or other countries in the region. The 25% (N = 6,982) of troops that failed to list their duty station were considered to be stationed in Iraq or Afghanistan based on statistics of personnel invited to participate in the R&R program.
From the answers on the health assessment survey completed on arrival at the camp, we calculated a diarrhea incidence of 4.9 cases per 100 person-months (95% CI, 4.6–5.1), with nausea and/or vomiting occurring at a rate of 3.9 cases per 100 person-months (95% CI, 3.5–4.5). There seemed to be a bimodal distribution of diarrhea incidence during the year, with a primary peak in the summer and a second peak in the fall (Figure 1
). In additional to temporal changes, there were differences based on country of assignment and military rank, with troops from Iraq reporting a higher incidence than those from Afghanistan (5.1 versus 4.1 cases per 100 person-months, IRR = 1.23, P = 0.01). The clinic screening also identified higher military rank to be associated with increased risk of self-reported diarrhea, with junior enlisted (E1–E4), mid-level enlisted (E5/E6), senior enlisted (E7–E9), and officers reporting rates of 4.1, 5.5, 6.2, and 6.9 episodes per 100 person-months, respectively (P < 0.0001 for trend across ordinal rank). Because country of deployment and rank were both associated with diarrhea and with each other, a multivariate Poisson regression model for the outcomes and covariates of country of deployment and rank were fit. Both covariates remained independent predictors and did not change the univariate effect estimates by > 10% (Iraq versus Afghanistan, unadjusted IRR = 1.23, adjusted IRR = 1.25).
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FIGURE 1. Self-reported diarrhea and vomiting incidence by month among R & R troops during January to December 2004. *Incidence is equal to episodes per 100 person-months.
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Clinic-based observational study.
The observational study was conducted between May and November 2004. Of ~18,419 troops participating in the R&R program during that period, 109 were evaluated at the base clinic for gastrointestinal symptoms and enrolled in the observational study. An additional 85 individuals reporting to the clinic for evaluation, who were not currently experiencing diarrhea, agreed to enroll as part of the asymptomatic population. The mean age of the 194 participants (cases plus asymptomatic individuals) was 32 years (range, 19–56 years). The study population was 92% men, and 87% were enlisted personnel (Table 1). Participants were deployed for a median of 4.8 months (95% CI, 4.2–5.5) in country before arriving for R&R. One hundred seventeen of 194 participants (60%) reported at least one episode of diarrhea during their deployment. From these data, we calculated a minimal incidence estimate of 12.6 (95% CI, 10.5–14.9) episodes of diarrhea per 100 person-months among those who had been deployed for at least 7 days.
A total of 49% of cases had at least one enteric pathogen isolated from their stool compared with 14% of asymptomatic individuals (Table 2). Co-pathogens (more than one bacterial pathogen) were identified in five cases and in one asymptomatic individual. Of the pathogens identified, ETEC was found to be the most prevalent being isolated in the stool of 35 (32%) cases compared with 7 (8%) of asymptomatic individuals (OR = 4.6; 95% CI, 1.9–11.0). Of the ETEC isolated from the cases, 60% were found positive for heat-stable toxin (ST), 23% for heat-labile toxin (LT), 6% for both LT and ST, and 11% for mixed toxin profiles indicating simultaneous infection by multiple unique isolates. Various colonization factors including CS6 (20%), CS2/CS3 (14%), CS2 (3%), and CFA1 (3%) were identified. An additional 17% of isolates had mixed colonization factors, and 43% were determined untypeable. Among the isolates recovered from asymptomatic individuals, 86% and 14% were positive for LT and ST, respectively. All isolates recovered from this population were CFA1 positive. A total of 98% of the ETEC isolates were determined to be sensitive to ciprofloxacin, a commonly used antibiotic to treat bacterial induced diarrhea in deployed troops. EAEC was isolated from 12% of the cases and 7% of those asymptomatic at the time of enrollment (no statistically significant difference). The distribution of pathogens identified was not statistically significant regardless of the country of the primary assignment of the study subject (Table 3).
Case subjects were typically ill for 2 days before visiting the clinic, and 35% reported self-treating (i.e., use of loperamide, bismuth subsalicylate, or antibiotics) before evaluation in the clinic (Table 4). Seventy-eight percent of case subjects complained of watery diarrhea and had a median of 10 loose stools before coming to the clinic for evaluation. Associated symptoms were common and consisted of abdominal cramps (75%), fever (29%), nausea (42%), vomiting (23%), headaches (43%), myalgias (38%), and arthralgias (27%), but gross blood in the stools was unusual, reported in only 8% of subjects. Orthostasis was observed in 22% of individuals at the time of presentation to the clinic. All those presenting with evidence of orthostasis were given intravenous fluids. An additional 11% of case subjects were administered intravenous fluids, a common practice among deployed US military, because of more aggressive treatment practices and anticipation of return to duty in an environment where there is a relatively higher risk of dehydration.16
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TABLE 4 Description of presenting symptoms, physical findings, and disposition among acutely ill patients and prior episodes of all volunteers in observational study
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In addition to description of current episodes of diarrhea, all volunteers were asked about history of prior episodes and to describe their illness. The symptoms associated with past episodes of diarrhea were found to be similar to that observed among the case population within the observational study (Table 4
). However, participants reported a tendency toward more frequent use loperamide or prescribed antibiotics during prior episodes compared with acute cases reporting to the clinic.
In addition to symptomology and treatment, those enrolled were asked to describe the individual and operational impact associated with past diarrheal episodes. Of those individuals who experienced a diarrheal episode during their current deployment, a decrease in work performance, for a median of 3 days (IQR, 1–5) was reported, not including actual days of work lost (Table 4). Furthermore, among the 24% of individuals who reported missing work because of their illness, a median number of 2 days of work were lost. In addition, 9% of individuals reporting diarrhea required back-up personnel to cover their shift, whereas 3% reported a shift change resulting directly from their illness. Last, a total of 12% of those enrolled reported that operational readiness was impacted because of diarrheal disease.
General behavioral risks and attitudes were assessed for both cases and asymptomatic individuals, and no significant differences were found between the two groups. Few individuals in either group reported "always or frequently" eating cooked meals off-base (10% cases versus 4% asymptomatics), eating raw vegetables off-base (5% cases versus 2% asymptomatics), or consuming drinks from the local community that contain ice (19% cases versus 15% asymptomatics). Reported adherence to handwashing recommendations after eating (73% cases versus 65% asymptomatics) and after using the latrine (78% cases versus 68% asymptomatics) were equivalent among cases and asymptomatic individuals.
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DISCUSSION
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In this study, we were able to broadly sample the population of US troops deployed in support of Operation Iraqi Freedom and Operation Enduring Freedom. The establishment of an R&R facility at Camp As Sayliyah, in Doha, Qatar, provided us the unique opportunity to obtain data from troops stationed over a wide area within days of leaving their theaters of operation. Additionally, the presence of a medical clinic at the camp allowed for the evaluation of individuals who became acutely ill during their stay.
Overall, we identified a relatively low incidence of self-reported diarrheal illness compared with previous studies on similar populations deployed in the region. Estimates of diarrhea incidence ranged from 4.9 cases per 100 person-months based on data collected from the health assessment survey to 12.2 cases per 100 person-months using data collected from participants in the clinic based observational study. In contrast, in a previous study conducted by our group evaluating illness among troops serving in Iraq and Afghanistan, the incidence of diarrhea was estimated to be 29 per 100 person-months.8 The reasons for the different estimates on diarrhea incidence are not certain but may be related to a number of factors. The initial study was performed using questionnaires with a total focus on diarrhea, whereas in this study, the health assessment survey contained questions about numerous conditions with only two questions focused directly on diarrhea. Additionally, the initial survey collected data from troops who were in the region before, during, and after combat operations, whereas this study involved individuals who only were involved in post-combat operations. We previously showed a decline in reported diarrhea after the combat phase of the war compared with pre- and during combat periods. This decline was thought to be caused by improved public health during non-combat operations.13 Alternatively, multiple deployments to the region by the same individuals may have resulted in a level of limited immunity or changes in risk behaviors as a result of prior experiences. It is also possible that, in this study, subjects were less likely to answer affirmatively to any of the health screening questions because they may have perceived that this would require them to make an appointment with the Troop Medical Clinic and thus interfere with R&R activities. Last, the estimate of incidence from the health prospective observation study should be considered a minimum incidence estimate (did not account for multiple episodes) and likely underestimates the true burden of disease. Further studies of the temporal changes in incidence are needed.
In concordance with our previous studies, the incidence of diarrhea among troops stationed in Iraq was significantly higher than among those stationed in Afghanistan.5,8 We again found the incidence of diarrhea was higher among the senior enlisted and officer ranks compared with the lower enlisted ranks. The reasons for the differences in incidence of diarrhea by geographic region or military rank are beyond the scope of this study; however, potential causes may include regional differences in infrastructure, host behavior, and infectious agent exposures. These factors may include differences in preventive medicine assets and function in Iraq compared with Afghanistan caused in part by increased insurgent activities in Iraq, different preventive medicine efforts (i.e., verbal training) being focused on the more junior troops, and senior enlisted and officers having more opportunities to eat at local establishments. Further research should be focused on better understanding of the impact each of these factors have on the risk of diarrheal illness.
In this study, ETEC was the most prevalent pathogen identified (32%). These data support other studies that have shown ETEC to be the most common cause of diarrhea among deployed troops. Recently, a systematic review among studies published between 1990 and 2005 reporting on diarrhea in US military and similar traveler populations described a 28% prevalence (99% CI, 21–36%) of ETEC among 13 studies of traveler populations to the Middle East region.17 However, results of this study are in contrast to a previous report of diarrhea among troops stationed in Iraq that implicated norovirus (23%) and Shigella spp. (20%) as the predominant etiological agents of diarrhea.14 A major limitation of that particular study was the sampling strategy used. Laboratory supplies were distributed to more than 30 Battalion Aid Stations throughout the area, and specimens were collected from only acute individuals. Furthermore, combat operations in the area significantly increased the duration of time necessary between collection and plating. These methods likely resulted in a bias toward sampling of pathogens commonly associated with epidemic diarrhea rather than sporadic diarrhea in deployed settings.18 Last, only four stool samples were tested for ETEC, making it impossible for the study to know the impact of ETEC on the incidence of diarrhea. In this study, focus was on bacterial and parasitic agents, but stool was collected and archived to allow us to test in the future for viral pathogens associated with diarrhea. Because a pathogen was not identified in nearly 50% of the stool samples in this study, it is possible that viral agents could be pathogens in a significant portion of these cases. An additional commensal finding of interest was the relatively frequent finding of protozoa. While not recognized as pathogens, they do seem to be a good surrogate marker for exposure.
Overall, 60% of individuals in this study that completed the health assessment survey reported having had an episode of diarrhea and/or vomiting during their deployment, 30% of individuals reported seeking care for their episode, 12% reported receiving intravenous fluid rehydration, and 2% were hospitalized. These findings are consistent with previous estimates reported in this deployed population.7,8 If these rates are expanded to the > 180,000 troops currently deployed in the region, a considerable health care burden of illness is identified. However, more important than the health care–associated burden of disease is the probable human performance and mission readiness impact of these illnesses on troops. One of five individuals who became ill with diarrhea while deployed reported not being able to work because of their illness (missing on average 2 days), and an additional two of these five reported that their work performance was decreased because of their illness. With multiple episodes of diarrhea during deployment, this equates to a large number of lost and impacted duty days of the war-fighter and is cause for concern.
This clinic-based observational study and health screening assessment survey contributes to our expanding knowledge of the incidence, impact, and pathogens responsible for causing diarrhea among deployed troops. Enteropathogenic E. coli are again identified as primary pathogens of concern, and based on the high rates of illness and parasites recovered, it seems that environmental control of diarrheal infection remains a challenge. We feel these data provide continued support for the robust research program in the Department of Defense and private sectors to identify primary interventions for the prevention of diarrheal disease.
Received March 15, 2006.
Accepted for publication June 30, 2006.
Acknowledgments: We thank Army Central Command and the Camp As Sayliyah Troop Medical Clinic for assistance with this research project. Furthermore, we thank Dr. Hind Shaheen and Marilou Salamat for laboratory technical assistance. Lastly, we thank Dr. Anne Marie Svennerholm for providing reagents used to detect enterotoxigenic E. coli toxins.
Financial support: This project was funded by the Military Infectious Disease Research Program work unit 6000.RAD1.DE0301.
Disclaimer: The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the US Government.
* Address correspondence to Marshall R. Monteville, NAMRU-3 PSC 452 Box 5000, FPO AE, 09835. E-mail: montevillem{at}namru3.med.navy.mil 
Copyright assignment statement: Some of the authors are military service members (or employees of the US Government). This work was prepared as part of their official duties. Title 17 U.S.C. 
105 provides that "Copyright protection under this title is not available for any work of the United States Government." Title 17 U.S.C. 101 defines a US Government work as a work prepared by a military service member or employee of the US Government as part of that person’s official duties.
Authors’ addresses: Marshall R. Monteville, NAMRU-3 PSC 452 Box 5000, FPO AE, 09835, Telephone: 011-202-342-1375 ext. 379, E-mail: montevillem{at}namru3.med.navy.mil. Mark S. Riddle, NAMRU-3 PSC 452 Box 5000, FPO AE, 09835, Telephone: 011-202-342-1375 ext. 451, E-mail: riddlem{at}namru3.med.navy.mil. Usha Baht, ASG QA, ATTN TMC/508, APO AE 09898, Telephone: 009-74-438-4251, E-mail: ubhatuk{at}yahoo.co.uk. Shannon D. Putnam, NAMRU-2, Box 3 Unit 8132, FPO AP 96520, E-mail: putnam{at}namru2.org. Robert W. Frenck, Jr. UCLA Center for Vaccine Research, 1124 W. Carson St., Torrance, CA 90502, Telephone: 310-781-3636, E-mail: rfrenck{at}uclacvr.labiomed.org. Kenneth S. Brooks, ASG QA, ATTN TMC/508, APO AE 09898, E-mail: Kenneth.s.brooks{at}us.army.mil. Manal Moustafa, NAMRU-3 PSC 452 Box 5000, FPO AE, 09835, E-mail: manalm{at}namru3.med.navy.mil. Jaime Bland, ASG QA, ATTN TMC/508, APO AE 09898, Telephone: 009-74-460-8333, E-mail: Jaime.Bland{at}qatar.army.mil. John W. Sanders, NAMRU-3 PSC 452 Box 5000, FPO AE, 09835, E-mail: jwsanders{at}Bethesda.med.navy.mil.
Reprint requests: Marshall R. Monteville, NAMRU-3 PSC 452 Box 5000, FPO AE, 09835. E-mail: montevillem{at}namru3.med.navy.mil.
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ABSTRACT
INTRODUCTION
