Nutrient Composition of Rations for Short-Term, High-Intensity Combat Operations (2006)

Andrew J. Young, US Army Research Institute of Environmental Medicine Gerald A. Darsch, US Army Soldier Systems Center

This report summarizes expert panel deliberations during a workshop organized by the Committee on Military Nutrition Research (CMNR) of the Food and Nutrition Board of the Institute of Medicine (IOM). The CMNR organized the workshop to address questions raised by the US Army Research Institute of Environmental Medicine (USARIEM) regarding optimal nutritional content for a new individual combat ration, First Strike Ration (FSR), being developed by Department of Defense (DoD) Combat Feeding Directorate at the US Army Natick Soldier Center. This new restricted ration was developed for highly mobile soldiers in high-intensity conflict by providing foods that can be eaten “on the move.” As a result, the FSR is smaller and lighter than the main individual operational ration, the Meal, Ready-to-Eat (MRE). In addition to their practicality, the FSR received high customer acceptance during recent deployments (Operation Enduring Freedom, Operation Iraqi Freedom). However, constraints imposed by ration design factors on the range of food components suitable for inclusion in an FSR might limit intake of certain nutrients needed to maintain soldier performance during sustained combat operations. The IOM ad hoc committee, charged with evaluating those concerns and recommending optimal nutrient content for

future versions of the ration, convened a workshop to gather information regarding the nutritional needs of individuals doing high-intensity activities for a short term while under stress.

US Army Field Feeding Doctrine (i.e., fundamental principles by which the military forces guide their actions) calls for supporting soldiers by providing them with “the right meal at the right place at the right time” (US Department of the Army, 1996). To accomplish this, Natick Soldier Center’s DoD Combat Feeding Directorate conducts research, development, testing, evaluation and engineering support for combat rations, field food service equipment and total combat feeding systems for the military services and the Defense Logistics Agency. To that end, the Combat Feeding Directorate has developed an appropriate range of combat rations that are available for requisition through the military supply system. Each of these rations is designed to meet the Military Reference Dietary Intakes (MDRIs) as established in AR 40-25 (US Departments of the Army, Navy, and Air Force, 2001). Detailed descriptions, including menus, nutrient content, and packaging information for the entire spectrum of these operational rations, are documented elsewhere (US Department of Defense, 2004). Table B-1 briefly summarizes key features for several of the most widely used rations.

In those instances when operational conditions preclude serving hot, cafeteria-style rations, military personnel are provided individual operational rations, of which the MRE is the flagship ration. The nutrient requirements of most deployed soldiers can be satisfied when they are provided MREs or other appropriate rations listed in Table B-1. However, due to several factors explained below, the current rations may not completely satisfy nutritional requirements of soldiers in some situations (i.e., during the assault phase of combat operations, certain Special Operations Forces missions, and missions anticipated to be conducted by Future Force Soldiers).

First, daily energy expenditures of personnel engaged in these types of military missions are so high (Tharion et al., 2005) that these soldiers will not maintain an energy balance even when they consume three complete MREs per day, which could lead to adverse physiological effects and detriments in health and performance (see also next section on “Physiological Demands of Combat Operations”). Moreover, in some cases during combat operations, soldiers receive only two MREs, which further exacerbates the situation.

Second, soldiers who must carry heavy loads or engage in strenuous military duties (e.g., light infantry, US Marine Corps, and Special Operation Forces) compound their energy balance problem by “field-stripping” the MREs. To lighten their heavy loads, soldiers often open the individual meal packages, select certain components based on individual preference, and discard the remainder.

Because MREs and other rations were designed to meet the nutritional needs of deployed soldiers who consume the entire daily ration (in which the nutrients are not evenly distributed), such selective consumption will further decrease total intake of energy and/or will compromise adequate intake of specific nutrients. Although field-stripping does, in fact, lighten a soldier’s load, the cost of the discarded components can approach $34 over a three-day period. More importantly, studies at USARIEM and elsewhere have documented a variety of adverse biomedical and performance consequences (Lieberman, 2003; Montain and Young,

2003) when such semistarvation is coupled with other physiological stressors encountered during sustained combat operations (e.g., sleep deprivation, anxiety, dehydration).

The need for a specialized ration for high-tempo, assault-type missions has been recognized since the end of World War II (Samuels et al., 1947) when military planners recommended development of an “Assault Candy Ration.” To better meet the individual’s nutritional needs during these high-intensity operations, Natick Soldier Center’s Combat Feeding Directorate have developed a new smaller, lighter, individual operational ration comprised of eat-on-the-move food components, the FSR. The FSR is intended for use during specific missions such as those described above when soldiers must operate for periods of three days, or possibly longer, with minimal resupply. This ration will serve to “bridge the gap” until operational tempo abates and more nutritionally complete rations can provided. Because of the relevance of the operations for which FSRs are envisioned, their full implementation in the field may occur in an accelerated fashion; in fact, it is estimated that the FSR, pending the military services’ approval, will enter the procurement system in the first part of 2007. Through the use of spiral development generated under an Army Technology Objective (ATO) entitled “Nutritionally Optimized FSR” (IV.MD.2005.02), jointly sponsored by USARIEM and the Natick Soldier Center Combat Feeding Program, science and technology innovations are planned for insertion as part of a preplanned product improvement program. The objective of this ATO is to develop and utilize novel nutrient delivery systems, food formulations, and field feeding strategies to provide on-demand access to specific nutrients to best sustain performance. The specific strategies, when identified, will improve overall energy and nutrient intake by 20 percent and enhance cognitive and physical performance by 20 percent. The DOD asked the IOM committee to provide recommendations that will guide the design of the ration for sustained combat operations and will identify nutritional research to accomplish this objective.

The Committee on Optimization of Nutrient Composition of Military Rations for Short-Term, High-Stress Situations asked the workshop participants to consider the specific requirements for the FSR (size, volume, weight) that constrain the ration’s design such that the ration is unlikely to provide enough energy to match the daily energy expenditures of the soldiers. Table B-2 lists important design features and performance objectives for the FSR development effort. The workshop’s primary objective was to gather information and provide recommendations regarding nutritional strategies suitable for implementation to

make an FSR that would best sustain health and performance despite semistarvation arising from high daily energy expenditure and constrained energy intake. Box B-1 details several specific questions that the workshop was directed to address. The overall question was the following: Given the fact that weight and size limitations preclude the FSR from completely preventing negative energy balance in soldiers subsisting on the ration, would health and performance best be preserved by a nutrient composition that maximizes energy density (i.e., minimize energy deficit) or, alternatively, by a micro- and macronutrient composition that specifically optimizes health status and performance, potentially at the expense of a less than maximum energy density?

Besides addressing nutrient content, the speakers at the workshop were also asked to consider ration design approaches to enhance overall consumption of the ration. The problem of ration underconsumption during field training and operational deployments is well documented and was the focus of an earlier report (IOM, 1995). The CMNR previously concluded that five broad categories of factors contributed to ration under consumption.

The first four categories of factors related to the environment and to behavior that potentially impairs appetite and/or limits food consumption were identified as the following: exposure to harsh climate and danger (environment); social interactions during meals; appropriateness of the meal to time of day (eating situation); and the attitudes toward field-feeding systems held by soldiers and

their leaders (individual). Based on the CMNR recommendations, technical reports and commanders’ guides have been prepared and distributed providing guidance to minimize the effect of those negative factors; however, from a practical standpoint, commanders conducting combat operations are permitted little flexibility to mitigate those kinds of stressors. The fifth category is underconsumption factors, related to a ration’s characteristics that influence customer acceptability and for which the committee offered more practical recommendations to improve consumption. These recommendations included the following: to enhance menu variety; to improve food sensory features, packaging, and ease of use for the rations and components; and to provide smaller snacking or “nibbling” food items as well as energy- and nutrient-rich beverages that could be carried in pockets and consumed quickly while on the move.

Clearly, those recommendations should be the driving focus behind the FSR. All of those approaches have already been incorporated into the newest versions of the MRE and other operational rations during the continuous product improvement programs that Combat Feeding Directorate conducts and they have been recognized by troops who consume combat rations. For this workshop, the panel

of experts was asked to consider how similar, practical approaches could be used to further enhance consumption of the FSR, thereby better satisfying the nutritional needs of soldiers during assault type operations.

Under the auspices of the CMNR, the Committee on Optimization of Nutrient Composition of Military Rations for Short-Term, High-Stress Situations and the IOM organized a workshop to address the questions posed by USARIEM. The workshop was hosted by USARIEM and the Natick Soldier Center in Natick, MA, in August 2004. USARIEM scientists provided the workshop participants with their tasks, overviews of military ration systems, and background briefings on the physiological and medical consequences of combat operations on military personnel. For the remainder of the workshop, invited scientific experts presented information on topics organized into five major categories: optimization of macronutrient composition; optimization of micronutrients and other bioactive compounds; nutritional optimization of the immune system; nutritional preventive medicine; and food product development. Those presentations are the basis for the remainder of this report.

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Scott J. Montain, US Army Research Institute of Environmental Medicine

The combat foot soldiers within the light infantry and special operations units are the military populations targeted for use of next-generation assault rations. These soldiers are required to carry or transport all of the supplies, sometimes exceeding 50 kg, they will need for the operation. Missions often are of the continuous type termed “sustained operations” (SUSOPS) lasting from two to seven days or longer that consist of near-continuous physical work, restricted sleep, and limited breaks for meals. While the energy cost of any single task is not necessarily high, total daily energy expenditures can reach extremely high levels because of long hours of wakefulness. Thus, these soldiers are faced with sustained environmental exposure, exertional fatigue, sleep deprivation, and energy deficits.

The lightweight and small assault ration being developed specifically for these soldiers must be capable of sustaining their performance while in repeated SUSOPS missions lasting for three days when energy expenditures exceed 18 MJ (4,300 kcal)/day, and up to seven days during which daily energy expenditures are expected to be less. This chapter describes the physiological challenges facing combat foot soldiers to facilitate defining their nutritional requirements. This topic has been discussed in greater depth in other publications (Friedl, 2003; Tharion et al., 2005), and the reader is referred to these papers for additional information.

The total daily energy expenditures of combat units during training exercises has ranged from 15.5 to 29.8 MJ (3,700 to 7,120 kcal)/day (Figure B-1); with the highest values occurring during cold-weather operations. The tasks performed typically have included long, sustained periods of low to moderate intensity work (expected metabolic rates of 250 to 450 Watts), with short periods of relatively high-intensity work (expected metabolic rates in excess of 600 Watts). Factors contributing to these high daily energy expenditures have been the relatively long periods of work (> 15 h/day), traversing rough terrain or soft surfaces (e.g., snow, mud, or sand), and carrying heavy loads.

Much of what we know regarding the energy cost of soldier activities comes from investigations of soldiers performing simulated combat missions as part of training courses. In these scenarios, total daily energy expenditures (TDEE) are often quite high. For example, airmen participating in the US Air Force Combat Survival Course averaged 19.7 MJ (4,700 kcal)/day of TDEE (Jones et al., 1992),

FIGURE B-1 Measured troop energy expenditures during military field operations.

NOTE: TEE = total energy expenditure.

SOURCE: Tharion et al. (2005).

soldiers attending the US Army Special Forces Assessment School averaged 21.7 MJ (5,180 kcal)/day (Fairbrother et al., 1995), and marines at the US Marine Corps Infantry Officer Course averaged 22.5 MJ (4,700 kcal)/day of TDEE during cold-weather operations (Hoyt et al., 2001) and 16 to17 MJ (3,820 to 4,060 kcal)/day during hot weather (author’s unpublished results; personal communication, R. Hoyt, US Army Research Institute of Environmental Medicine, 1999). The US Air Force Combat Survival Course is a 5-day course that trains aircrew members in parachuting and survival, evasion, resistance, and escape procedures, as well as simulated prisoner of war interrogations. The US Army Special Forces Assessment School conducts 20-day training and includes activities such as physical fitness tests, battle marches, and long-range movements carrying backpacks, weapons, and other field equipment. In the Marine Corps Infantry Officer Course, marines perform a series of simulated combat operations using dismounted infantry, mounted infantry, and amphibious tactics. In each of these courses, night operations are included, leading to near-continuous physical work, with marines active 16 to 22 h/day.

Students enrolled in the US Army Ranger training course perform a series of physically demanding field exercises intermittently over a 60-day period. While total energy expenditures averaged over the 60-day course are lower than those for many of the shorter, more intense military training courses, they are still quite high, averaging 16.8 MJ (4,010 kcal)/day (Moore et al., 1992) and 17.1 MJ (4,090 kal)/day (Shippee et al., 1994) for more than two months. Combat fundamentals taught during the course include patrolling; squad reconnaissance and ambush; mountaineering; small boat operations; and attack, ambush, and raid drills. The unique aspect of this course is repeated, periodic food restriction and sleep deprivation as one of the intentional stressors—making it a model for studying the physiological strain likely to be imposed on soldiers performing repeated SUSOPS missions during combat, which is the subject of interest in this workshop.

As noted in the introduction, combat foot soldiers carry their own supplies at high energy expenditure costs. The loads they carry can be very heavy depending on what phase of a mission they are performing. A recent study (Dean and Dupont, 2003) in which soldier loads were measured during actual operations in Afghanistan revealed that soldiers in the traveling phase of a mission carried an average of 59.3 kg (131 lb). Their approach load averaged 45.7 kg (101 lb), and their fighting load averaged 28.5 kg (63 lb). When normalized to body weight, these loads were equivalent to carrying 77 percent, 57 percent, and 35 percent of body mass, respectively. Current soldier development efforts are exploring methods to dramatically lower the soldier load, but soldier load remains a major physical stressor during combat execution.

The massive load each soldier carries limits the amount of space and weight that soldiers are willing to reserve for food. The nature of SUSOPS missions also means that food is consumed on the go. These two factors lead to soldiers stripping their personal rations of items that they don’t like or will be unlikely to eat. When voluntary intake has been measured, it typically averages between 10 and 12 MJ (2,390 to 2,870 kcal) (Baker-Fulco, 1995). Since energy expenditure is often much higher than intake, there is demand placed on endogenous energy stores to meet energy demands of the mission.

Blood glucose levels typically decrease over SUSOPS missions, but the average values generally only fall 10 mg/dL (0.5 to 0.6 mM) from baseline values. There are soldiers, however, who demonstrate much higher reductions. In a recent investigation (author’s unpublished results), during which marines consumed 1,600 kcal/day and 210 g of carbohydrate/day while expending

3,850 kcal/day, it was observed that 12 to 23 percent of volunteers had blood glucose values below 76 mg/dL (< 4.2 mM) after four to eight days of SUSOPS. Concomitant with these metabolic changes were substantial increases in blood ketone and free fatty acid concentrations.

The underfeeding accompanying SUSOPS is accompanied by reductions of both fat and lean body mass. For example, Nindl and colleagues (2002) reported fat and lean tissues losses of 1.2 and 1.5 kg, respectively, over a 72 h SUSOPS. Similarly, Moore and colleagues (1992) reported that 38 percent of the 12 kg body mass loss that occurred during Ranger training (when severely underfed) was attributable to nonfat tissue loss.

Opstad and colleagues (1978) found that visual vigilance decreased 4 to 28 percent after three to four days of sustained operations activity. Reaction time and coding declined 12 to 30 percent over the same time period, while prone marksmanship declined 10 percent. Inclusion of three to six hours of continuous sleep once during the five-day operation partially or fully reversed these declines. There was large interindividual variability, but general deterioration occurred due to omissions, not mistakes. Similar results have been reported by others, as Bugge and colleagues (1979) observed, decreased logical reasoning (46 percent), letter cancellation attempts (40 percent), and code test scores (45 percent) after four days of sustained operations. More recently, Tharion and colleagues (1997) reported a reduction in visual vigilance (44 percent), slower processing (21 percent), and fewer correct responses (17 percent) on a four-choice reaction test, and compromised performance on a match to sample task after 73 to 74 h of sleep deprivation and operational stress. Associated with the impaired cognitive performance were increased levels of fatigue, confusion, tension, and depression. Shippee and colleagues (1994) evaluated decoding, memory, reasoning, and pattern recognition during the eight-week US Army Ranger Course. Soldiers maintained near perfect accuracy at decoding and reasoning at the expense of speed (7 to 10 percent fewer attempts). Memory accuracy declined over time. Both speed and accuracy were impaired on the pattern recognition task—particularly during the desert and jungle phases.

Prolonged operations lasting several weeks’ duration and associated with substantial losses of lean body mass (Moore et al., 1992; Shippee et al., 1994) have resulted in reductions (20 percent) in maximal lifting capacity and vertical jump height (15 to 16 percent). Shorter duration studies with minimal lean body mass loss generally showed little or no decrement in muscle strength, power, or fatigability (Bulbulian et al., 1996; Guezennec et al., 1994; Vanhelder and

Radomski, 1989); however, this is not universal (Legg and Patton, 1987). Sustained operations scenarios lasting less than one week have resulted in reduced maximal aerobic power and endurance (Guezennec et al., 1994) as have sleep-deprivation studies (Vanhelder and Radomski, 1989).

Performance of simple and well-learned motor tasks (e.g., weapon handling) do not appear to be compromised by sustained operational stress (Haslam, 1984). However, endurance time is frequently impaired during aerobic exercise tasks (Vanhelder and Radomski, 1989), and there is an increased perception of effort to perform the same task. Nindl and colleagues (2002) recently reported 25 percent lower work productivity on a physical persistence task; in agreement with the hypothesis that SUSOPS compromises prolonged and monotonous tasks (Figure B-2). Independent of energy intake (Rognum et al., 1986), operational effectiveness is also affected if sleep is inadequate.

Marksmanship can be compromised by sustained operation activities particularly when very little restorative sleep is obtained. Tharion and colleagues

FIGURE B-2 Work productivity on a physical persistence task over 72 h of simulated military sustained operations (SUSOPS) training as well as a control week without near-continuous work and underfeeding.

SOURCE: Nindl et al. (2002).

(2003) reported significantly impaired marksmanship after 73 to 74 hours of total sleep deprivation during Navy Seal training. Specifically, they observed greater distance from center of mass (38 percent) increased dispersion of shot groups (235 percent), as well more missed targets (37 percent), all indicative of reduced marksmanship. These adverse findings occurred despite a 53 percent slower sighting time. In contrast, Johnson and colleagues (2001) reported that despite soldiers rating the marksmanship task as more difficult to perform after 48 and 72 h of SUSOPS (2 h of sleep per night), there was no reduction in the number of randomly appearing targets hit during the test. Haslam (1984) reported no negative results during nine days of sustained operations and sleeping either 1.5 or 3 h daily on shot group clustering when troops fired in the prone supported position. However, their ability to acquire and accurately hit a randomly appearing target declined during the course. The group receiving only 1.5 h of daily sleep performed 50 percent below baseline from days 5–9 of the field exercise, whereas the group receiving 3 h of daily sleep had a more modest reduction (the number of hits fell from 6–7 to 4–5).

Similarly, the caloric deficit associated with sustained operations scenarios appears to have inconsistent effects on soldier performance (Montain and Young, 2003). Rognum and colleagues (1986) reported no difference either in time to complete an assault course or in prone marksmanship performance when students were provided 1,500 or 8,000 kcal/day during a five-day scenario. However, Guezennec and colleagues (1994) observed 8 percent reductions in maximal aerobic power when soldiers were restricted to 1,800 kcal/day but no reduction in maximal aerobic power when soldiers were fed 3,200 or 4,200 kcal/day. Similarly, Tharion and Moore (1993) reported reductions in shot group tightness on a marksmanship task after sustained road marching soldiers were fed 250 g of carbohydrate per day, but no change when soldiers consumed a diet with 400 or 550 g of carbohydrate.

Time and content of the previous meal may be an explanation for the divergent results. Montain and colleagues (1997) reported a relationship in that an increase in energy (or carbohydrate) intake sustains uphill run time over three days of physically demanding field training. Moreover, 11 of 13 soldiers who best sustained uphill-run performance had eaten 70 to 378 g of carbohydrate during the four h preceding the uphill run, while 10 of the 13 soldiers with the greatest decrement had eaten none of their rations since the previous night’s meal. All participants in this study were provided with two Meals, Ready-to-Eat each day or approximately 2,600 kcal and 300 g of carbohydrate per day. These data suggest that soldiers subsisting on diets with these energy and carbohydrate levels during high-tempo operations are receiving near the minimum energy necessary to sustain performance, necessitating good food discipline (i.e., eating the food provided), and good food choices (i.e., eat the carbohydrate-containing foods) to preserve physical performance.

Dramatic changes in the blood hormonal milieu arise during sustained operations protocols and persist during both rest and exercise. In the five day Norwegian Ranger Course, in which food and sleep are kept to a minimum, there was a progressive increase in catecholamine concentration (Rognum et al., 1981) as well as cortisol, growth hormone, and aldosterone levels (Opstad, 1992; Opstad and Aakvaag, 1981) and a reciprocal fall in testosterone and prolactin (Opstad and Aakvaag, 1982) as well as other adrenal and testicular androgens (Opstad, 1992). The increase in catecholamine concentration is associated with a downregulation of adrenergic receptors on white blood cells (Opstad et al., 1994). Similar observations have been reported for soldiers participating in the US Army Ranger Selection Course (Moore et al., 1992; Shippee et al., 1994).

The decline in testosterone (up to 70 percent from baseline) and other anabolic hormones may be due in part to the caloric and/or protein restriction imposed during the courses. Short periods of refeeding quickly reverse declines in insulin-like growth factor-1 (IGF-1) (Friedl et al., 2000) (Figure B-3). When additional energy of a mixed diet of protein, fat, and carbohydrate have been provided (400 and 1,400 kcal), reductions in IGF-1 and testosterone were attenuated (Friedl et al., 2000; Guezennec et al., 1994). However, when additional calories (4,900 kcal) have been provided predominately by carbohydrate alone, testosterone reductions were only modestly lowered (Opstad and Aakvaag, 1982), suggesting that the testosterone and IGF-1 changes may have been consequent to energy deficit and possibly insufficient amino acid intake (Sanchez-Gomez et al., 1999).

The effects of sustained operations on immune function remain poorly understood. The outbreak of infectious disease among soldiers participating in US Army Ranger and Special Forces Assessment Schools suggests that multistress environments can compromise immune defense mechanisms (Moore et al., 1992). Changes in immune cell parameters and in vitro responses to stress have varied from study to study, but they appear related to the duration and severity of the sustained operations stress.

The five day Norwegian Ranger Course produced a general leukocytosis, predominantly due to two- to threefold increase in neutrophils and monocytes (Boyum et al., 1996). Lymphocyte numbers decreased as did CD4 T cells, CD8 T cells, CD16 natural killer cells, and CD19 B cells. Neutrophil chemotaxis and oxidative burst capacity increased during the course before returning to baseline levels (or below) after five days of training (Wiik et al., 1996). These changes have been attributed to sleep deprivation and appear relatively insensitive to changes in caloric (carbohydrate) intake (Wiik et al., 1996). Immunoglobulin M

FIGURE B-3 Insulin-like growth factor-1 (IGF-1) response to US Army Ranger Training under two levels of underfeeding and response to several days of refeeding during the course. Letters indicate means that are not significantly different (Scheffe’s test).

NOTE: Different letters indicate a significant difference in IGF-1 response (e.g., a versus b).

SOURCE: Friedl et al. (2000).

and immunoglobulin A decrease 20 to 30 percent during the course, while mitogenic responses to antigen exposure have not been consistent from course to course (Boyum et al., 1996).

The activities of the eight week US Army Ranger School appear to modify immune function, although the magnitude varies among the type of response. For example, Moore and colleagues (1992) found a similar percentage of positive delayed hypersensitivity responses to streptococcus and tetanus over the course despite relatively severe sleep deprivation and a 16 percent drop in body mass. There was no change in immunoglobulin concentrations during the course. However, as lymphocyte proliferation to mitogen stimulation declined during the course, an increasing number of students became pneumonia carriers, and 25 percent of the students sought medical attention for infections during the final portion of the course (swamp and desert phases).

Additional ranger studies (Bernton et al., 1995) revealed reductions in cell mediated immunity responses among the trainees. Shippee and colleagues (1994) examined immunological responses after students were provided additional calories during the course. Only 2 to 8 percent of the students required medical attention during the mountain and swamp phases. Immunoglobulin levels did not change, and neutrophil oxidative burst capability increased during the course. There was a general leukocytosis, due primarily to increased granulocytes, but lymphocyte concentrations fell. The ability of leukocytes to proliferate in response to mitogen stimulation was suppressed but was less than reported in previous courses when underfeeding was more severe (Moore et al., 1992). These latter responses suggest a possible shift in proportion of lymphocytes of the T-helper type 1 (T_H1) phenotype (cell-mediated) to the T-helper type 2 (T_H2) phenotype (antibody-mediated). This immune system adaptation occurs after trauma (Decker et al., 1996; Mack et al., 1997; O’Sullivan et al., 1995) and with disease (Raziuddin et al., 1998) and can immunocompromise the host to certain types of infectious agents (Mack et al., 1997; O’Sullivan et al., 1995).

The goal of the US military developmental assault ration, currently called the First Strike Ration, is to sustain troop health and performance for at least 96 h of unsupported military operations. To accomplish this objective, the nutritional components must sustain a soldier commonly expending in excess of 18 MJ (4,300 kcal) of energy per day and carrying loads in excess of 45 to 50 kg during while exposed to environmental extremes. It is well documented that the mission stress can challenge immune and neuroendocrine homeostasis and if sutained too long or repeated too frequently, that troop health and performance can be compromised. Likewise, there is evidence that nutritional support can reduce the physiological strain. The challenge is in defining the proper mix of macro- and micro-nutrients to sustain the soldier within a ration system the soldiers will choose to carry and consume during mission execution.

The views, opinions and/or findings in this report are those of the authors, and should not be construed as an official Department of the Army position, policy, or decision, unless so designated by other official documentation.

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Jørn Wulff Helge, Copenhagen Muscle Research Center

This paper addresses the optimal distribution of fat and carbohydrate to be included in the macronutrient composition of military assault rations as well as the specific types of fat to be used in these rations, and describes possible related performance and health issues. The purpose of this paper is to provide guidance regarding questions that may be used to make recommendations for an optimal ration composition, the task of the Committee on Optimization of Nutrient Composition of Military Rations for Short-Term, High-Stress Situations. To provide practical guidance for the complex and broad issues when improving fat and carbohydrate composition of assault rations, this paper focuses on these specific questions:

What is the optimal fat–carbohydrate balance in the ration?

• Is it possible to perform strenuous physical tasks/training on a high-fat diet?

• Is there a performance enhancement under short-term exposure to a fat-rich diet?

• What do we know about the effects of energy deficit and heavy physical demand on the carbohydrate/fat balance–substrate stores?

Are there specific types of fat that are optimal for the ration?

• Do specific fatty acids affect performance?

• Do specific fatty acids affect health issues?

These questions are addressed using the assumptions specified for the military assault situation: The ration is targeted for well-trained male soldiers, with an average weight of 80 kg, undergoing average daily energy expenditures of

4,000 to 4,500 kcal, and deployed to repeatable three- to seven-day missions with recovery periods of one to three days. During these missions, they are carrying a heavy load while engaged in prolonged, low- to moderate-intensity activity (up to 20 h/day) interspersed with brief, high-intensity activity.

It is well known that work performed at higher exercise intensities requires a large contribution of carbohydrates (Brooks and Mercier, 1994). Furthermore, there is evidence that short-term, high-fat diet adaptation can be used to spare muscle glycogen and decrease carbohydrate oxidation during exercise and, hypothetically, increase high-intensity exercise capacity (Burke and Hawley, 2002; Helge, 2000). Unfortunately, such carbohydrate sparing after short-term, high-fat diet adaptation is often accompanied by a reduced muscle (Phinney et al., 1983) and liver (Hultman and Nilsson, 1971) glycogen storage in comparison with the results from consumption of a short-term, high-carbohydrate diet. It is, therefore, pertinent to know whether high-intensity exercise capacity can be upheld when dietary fat contribution is high.

Stepto and colleagues (2002) studied seven elite trained endurance athletes who underwent two four-day dietary periods consuming either a high-carbohydrate diet (70 to 75 percent carbohydrate) or a high-fat diet (> 65 percent fat) in a crossover design with an 18-day washout period in between. During the dietary adaptation period, subjects performed two controlled exercise sessions on days one and four, during which they exercised for 20 minutes at 65 percent of VO₂max and subsequently performed eight 5-minute exercise bouts at 86 percent of VO₂max interspersed with 60-second breaks. In addition to the training performed in the laboratory, the subjects also undertook training outside, but no difference in duration of training was apparent between dietary adaptation periods. The subjects were capable of performing the training, except during one high-intensity exercise bout, while consuming the fat-rich diet. Despite these results, the subjective rating of perceived exertion was higher on day four in the last few bouts after a fat-rich diet when compared with the results of a carbohydrate-rich diet (Table B-3). These results indicate that, for at least four days, elite athletes are capable of performing training at a reasonably high intensity while consuming a fat-rich diet but with a higher subjective rate of perceived exertion.

Consistent with these data, we noted that in our studies involving moderately untrained male subjects during long-term training and high-fat diet adaptation, the subjects on a high-fat diet were able to train and exercise at moderate and high intensities but perceived increased mental effort as compared with subjects on a high-carbohydrate diet (Helge, 2002). There is currently no explanation for this higher mental effort, but previous studies of subjects on a short-

term adaptation to a fat-rich diet (Galbo et al., 1979; Jansson et al., 1982) found a higher catecholamine response and heart rate during submaximal exercise as compared with subjects on a carbohydrate-rich diet. The possible influence of a high-fat diet adaptation on the sympathetic nervous system response during exercise might cause mental strain; however, the mechanistic coupling between the increase in sympathetic response induced by a high-fat diet and the increased perception of exertion during submaximal exercise remains to be explained.

The coupling between muscle glycogen storage and endurance exercise capacity, which was demonstrated by Bergstrom and colleagues (1967), spurred researchers to investigate means to manipulate glycogen storage and use or both. One approach was a fat-rich diet adaptation, which induces markedly higher fat oxidation during exercise and reduced carbohydrate use (Christensen and Hansen, 1939; Phinney et al., 1983). This higher fat oxidation, however, occurs at the expense of a muscle glycogen concentration that is, at best, maintained and, in many cases, lower than that in those consuming a carbohydrate-rich diet (Helge et al., 1998b; Phinney et al., 1983). Despite these conflicting adaptations, a number of studies have manipulated the dietary fat content to achieve an improved performance capacity. In this context, short-term exposure to fat-rich diets is defined as adaptation periods lasting less than eight days and having a fat content contributing more than 40 percent of total energy in the diet. The studies are

listed in Table B-4, and overall, only one study shows an increased capacity to perform exercise after short exposure to a fat-rich diet. This study, by Muoio and colleagues (1994), has been extensively criticized in the literature due to a nonrandomized use of diet adaptation. The remaining ten studies found either an unchanged (three studies) or decreased (seven studies) exercise capacity after a short-term, fat-rich diet, indicating a lack of performance enhancement after such consumption and, in the worst case, a decreased performance. However, because of the number of variables influencing these findings (such as the content of fat:carbohydrate in the diet, the subjects’ training background, the exercise intensity, and the type of exercise test applied to test performance enhancement [Helge et al., 1998b]), caution should be used when drawing final conclusions. A more detailed discussion on the effects of short-term, high-fat adaptation can be found elsewhere (Burke and Hawley, 2002; Helge, 2000).

An essential goal for the assault ration is to enable soldiers to perform prolonged, low-intensity activity interspersed with high-intensity activity, with a daily energy deficit estimated to be approximately 2,000 kcal.

Only few studies are available in which the conditions mimicked those experienced by the soldiers. At the Copenhagen Muscle Research Centre, we have studied two groups of moderately to well-trained men who, fully self-supported and on cross-country skis pulling heavy sledges, traversed the Greenland ice cap (Helge et al., 2003; unpublished results). The dietary macronutrient compositions and basic subject characteristics are given in Table B-5. The two groups crossed the ice cap in 42 and 32 days and experienced a weight loss of approximately 6 and 7 kg, respectively, of which the majority was fat and the remainder, lean body mass (Figure B-4). Based on standard calculations, these losses are equivalent to a daily energy deficit of approximately 1,000 to 1,500 kcal. Albeit the differences in study design (e.g., the two interventions are for longer terms than those for the assault rations), the results may provide useful information for developing assault rations. The skiers’ maximal oxygen uptake remained unchanged in upper-body exercise (arm cranking), but it decreased in lower-body exercise (normal bicycle) (Helge et al., 2003; unpublished results). Accordingly, the muscle biopsy data, enzyme activities, and capillarization data indicated that the arm muscle response tended to be positive, whereas the leg muscle response was neutral or negative. Overall, this would suggest that despite the energy deficit and the type and large amount of physical work, the macronutrient compositions did provide sufficient substrate to almost fully fuel and retain the capacity for physical activity. Based on the available evidence, the fat content could probably be increased up to 50 percent without causing adverse effects. Unfortunately, due to the study design and the timing of muscle biopsies,

muscle substrates during the traverse are unavailable. Of particular interest in this context, however, is whether the muscle triacylglycerol stores, a main substrate source during prolonged, low- to moderate-intensity exercise in well-trained soldiers, are replenished by the ration. Several research groups recently have suggested that repletion of muscle triacylglycerol stores after physical activity could be important to optimize muscle recovery and exercise capacity (Berggren et al., 2004; Johnson et al., 2004; Spriet and Gibala, 2004). Decombaz and colleagues (2001) suggested that daily consumption of fat at a level of 2 g/kg of body mass would be sufficient to fully restore muscle triacylglycerol levels. This would imply that an average soldier at 80 kg would need to consume fat at a level of 160 g/day, which is achieved if the ration contains approximately 55 percent of total energy as fat. The macronutrient composition in the ration must be optimized such that the replenishment of both muscle glycogen and triacylglycerol is sufficiently increased within the given energy limitation of the ration.

In the literature, animal studies have demonstrated preferential mobilization (Raclot and Groscolas, 1993) and oxidation (Jones et al., 1992; Leyton et al., 1987; Shimomura et al., 1990) of unsaturated versus saturated fatty acids. As mentioned, interventions that spare carbohydrate use may benefit performance capacity. The available evidence showing that a difference in dietary fatty acid composition will affect endurance is, however, sparse. In rats, endurance performance, measured in vitro in rat extensor digitorum longus muscle after intermit-

tent, low-frequency stimulation, was lower after nine weeks’ adaptation to a diet rich in n-6 fatty acids as compared with adaption to a diet rich in n-3 fatty acids; both diets contained 10 percent fat (w/w) (Ayre and Hulbert, 1996). Another study in rats found no effect of dietary fatty acid composition on endurance performance in trained or sedentary animals after high-fat diet adaptation, but substrate oxidation was affected (higher oxidation) by the dietary fatty acid composition (Helge et al., 1998a, see Figure B-5). Studies in salmon (McKenzie et al., 1998; Wagner et al., 2004) have also addressed the effects of dietary fatty acid composition on performance capacity, but the data show no consistent trends. In humans, the evidence is limited: A study (n = 3) found that endurance performance measured at 70 to 75 percent VO₂max decreased after consumption

FIGURE B-5 Endurance time to exhaustion in sedentary and trained male rats after four weeks’ adaptation to one of two fat-rich diets containing either unsaturated or saturated fatty acids or to a carbohydrate-rich diet.

NOTE: Values are means ± standard error (n = 7–11). CHO = carbohydrate; MONO = monounsaturated fat; n = number in sample; SAT = saturated fat. * = significantly different from the sedentary groups (p < 0.05).

SOURCE: Helge et al. (1998a).

of a polyunsaturated fat-rich diet as compared with a saturated-fat diet (Lukaski et al., 2001). The author’s unpublished observations found that the consumption of a saturated-fat diet, versus a polyunsaturated-fat diet, had no effect on endurance performance. Thus, insufficient data are available to support a role for dietary fatty acid composition on exercise performance.

Are there adverse or positive effects of including different fatty acids in the ration? This question includes a number of complex issues that are incompletely resolved; space limitations prevent their being addressed here, but the following list of potential roles for dietary fatty acids should be considerd for further research:

• The influence of dietary fatty acid composition on membrane function (Pan et al., 1994).

• The influence of dietary fatty acid composition (particularly the content of n-3 and n-6 fatty acids) on immune function (Venkatraman et al., 2000).

• The potential hypolipedemic effects of n-3 fatty acids (Harris, 1997).

• The effects of saturated fatty acids on decreasing insulin sensitivity (Pan et al., 1994).

• The interactions with and effects of specific fatty acids on gene expression in muscle (Spriet and Gibala, 2004; Venkatraman et al., 2000).

The amount of physical activity performed by these soldiers as well as their good training status suggests that shorter term modifications of dietary fatty acid composition and dietary fat content would have insignificant effects on their general health and function.

The following arguments confer positive and negative aspects of adding increased amounts of fat to the ration. The positive effects of adding more fat include an increased energy content of the ration and a faster repletion of muscle triacylglycerol stores. The negative effects of adding more fat include increased rates of perceived exertion and mental strain during physical activity and a potential lowering of muscle glycogen stores (possibly liver glycogen). There may be an additional increased risk of inducing higher ketone levels but, in my opinion, such a risk does not pose a problem in this situation.

Insufficient evidence exists to verify the effects of specific dietary fatty acids on performance capacity. Some data suggest health and metabolic benefits from the consumption of specific fatty acids. However, in fit and healthy younger men exposed to intense physical activity, these effects, if indeed present, would have more influence on long-term health status rather than on short-term exer-

cise capacity and health. Therefore, the fatty acid composition in the ration should adhere to the requirements established by the Institute of Medicine (IOM, 2002).

Based on the issues addressed above the recommendations for the ration are the following:

• The fat content in the ration can be between 30 to 50 percent (of total energy) without reducing physical capacity; however, increasing the fat content may lead to slightly higher mental strain.

• When protein requirements are met and sufficient carbohydrate for high-intensity tasks is given, fat can be used to increase the energy content of the ration.

• While no specific fatty acid types improve performance, adequate essential fatty acids must be included in the ration at the current recommended levels (IOM, 2002).

The author is affiliated with the Copenhagen Muscle Research Centre, which is supported by grants from the University of Copenhagen, from the faculties of science and of health sciences at this university, and from the Copenhagen Hospital Corporation.

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Kevin D. Tipton, University of Birmingham, UK

Proper nutrition for military personnel has long been an important consideration for military planners. Nutrition may be especially important for military combat personnel performing duties that entail short-term, strenuous physical tasks in high-stress situations. Stress during military operations results from a combination of increased energy expenditure, decreased energy intake, and a lack of sleep for extended periods. These multiple stressors on mental and physical capabilities may decrease muscle performance enough to compromise both lives and military success. Sufficiently effective nutrients in combat rations would enhance the soldiers’capabilities and reduce both the loss of combat effectiveness and the number of casualties. Protein and carbohydrate consumption may contribute to optimal muscle performance during these situations.

The unique circumstances in the field make it difficult for soldiers to consume sufficient protein and carbohydrate as well as overall energy during their missions. For example, weight and size that soldiers can carry is limited and evidence shows that high-stress combat can suppress appetite (Popper et al., 1989). These factors lead to large energy deficits and macronutrient deficiencies for the three- to seven-day periods of these operations. These energy and macronutrient deficits could lead to metabolic disturbances that impair muscular performance during demanding and intense military operations.

The combination of stressors—decreased energy and protein intake, sleep deprivation, extreme physical activity, and high stress levels—that soldiers face

during these missions represents a complex and unique situation. Unfortunately, little, if any, direct information is available about muscular metabolic response to these stressors and about the appropriate nutrient intake that would be optimal for these capabilities.

This review uses data collected during periods of physiological stress to develop strategies to enhance protein and carbohydrate intake during sustained military operations. Because of a paucity of such data, however, this review provides a speculative guideline for recommendations. The following are specific questions that this review addresses:

• What would be the optimal macronutrient balance between protein and carbohydrate for an assault ration to enhance muscle performance during combat missions? Does the intensity of activity (i.e., high-tempo, stressful, repetitive combat missions) alter the optimal balance?

• What protein intake is recommended to best sustain homeostasis while people are eating reduced calories and exercising?

• What are the types and levels of macronutrients (e.g., complex versus simple carbohydrates, proteins with specific amino acid profiles, other sources of nitrogen, etc.) that would optimize such an assault ration to enhance muscle performance during combat missions?

Energy intake plays a major role in body protein metabolism. Operational requirements, as noted above, limit the intake of available energy in rations during short-term, high-stress missions. Such limitations in energy intake, combined with high levels of physical activity, ensure that participants are in an energy deficit for the three- to seven-day duration of a mission. Measurements made during simulated sustained operations do not clearly demonstrate muscle loss (Montain and Young, 2003; Nindl et al., 2002); however, body composition measures may not have the sensitivity to detect small changes over a short time. Nevertheless, the evidence provided below suggests that energy deficits that occur during these missions will lead to muscle loss.

Many classic studies from the laboratory of Calloway and Butterfield have demonstrated the importance of energy balance to maintain body nitrogen balance. Todd and colleagues (1984) clearly demonstrated that nitrogen balance is better maintained when energy balance is positive or, at least, zero (Figure B-6). Nitrogen balance could not be maintained when energy intake was 15 percent less than energy output. Presumably, the body’s predominant and accessible source, muscle protein, would also be the major site of this nitrogen loss. Energy restriction over longer periods (e.g., 10 weeks) results in the loss of lean mass during very low calorie dieting (Layman et al., 2003); however, the metabolic mechanisms for this loss remain unexplained.

FIGURE B-6 Nitrogen (N) balance during differing levels of energy intake (E) and physical activity (X) at two different levels of protein intake. Each bar is at either energy balance or 15 percent deficit due to increased exercise. These data illustrate that nitrogen balance is negative during energy deficits and improved by low-intensity exercise. Nitrogen balance is not positive in any combination of energy intake and exercise on the lowest (0.57 g·kg^–1·d^–1) level.

SOURCE: Adapted from Todd et al. (1984).

Muscle protein synthesis is reduced by 65 percent in food-deprived rats (Anthony et al., 2000), and perturbations in muscle metabolism from energy deficits could occur very rapidly. Recently, Tipton et al. (2003) demonstrated that the release of amino acids from leg muscle in healthy volunteers occurred in the first 24 h of energy restriction (80 percent of their weight maintenance levels). In that study, the volunteers were resting and consumed their habitual level of dietary protein. It seems that reducing energy intake by only 20 percent immediately stimulates a catabolic situation in muscle, suggesting that soldiers participating in missions where their energy intake is half of their energy output would be losing nitrogen, most likely from muscle. Unfortunately, it is not clear how the energy restriction and negative energy balance inherent for these sustained operations reduces muscle performance (Friedl, 1995).

A portion of the uncertainty about the effects of energy balance on muscle performance in short-term military missions with concomitant stressors, such as high-physical activity, sleep loss, and dietary restrictions, can be attributed to the complexity of the situation and the lack of information from studies. Protein use can be improved by physical activity (Butterfield and Calloway, 1984; Todd et al., 1984) (Figure B-6). Increased energy intake to support increased physical

activity improves the nitrogen balance, and the physical activity improves nitrogen retention (Butterfield and Calloway, 1984; Todd et al., 1984). Following an acute bout of resistance exercise, muscle protein synthesis and net muscle protein balance are increased, even in trained individuals (Biolo et al., 1995; Phillips et al., 1997, 1999). Muscle protein synthesis was increased following four hours of walking (Carraro et al., 1990), but no balance data are available for that type of activity.

Whereas these data could be interpreted to suggest that the physical activity common during military maneuvers may improve protein balance and have a good effect on muscle protein, there are reasons to believe otherwise. There is typically a period of adaptation to physical activity in which nitrogen balance is diminished (Butterfield, 1987; Butterfield and Calloway, 1984; Gontzea et al., 1975). This transient increase in protein loss peaks at four to ten days following initiation of the exercise program; easily encompassing the time typically used for these missions. However, these data are from untrained individuals initiating physical activity, so the applicability of these data to the situations being discussed for soldiers is unclear. It is easy to accept that the habitual level of training before participating in difficult missions could be protective, but there are no data to support this contention. Furthermore, the data supporting a benefit to nitrogen balance from activity were obtained during an energy balance (Todd et al., 1984). Positive nitrogen balance could not be maintained when energy balance was negative, despite increased physical activity (Figure B-6). Thus, it seems that the conditions intrinsic to the sustained operations missions will result in negative nitrogen balance and loss of muscle protein.

The intensity of the activity necessary for successful completion of the missions may increase the loss of muscle protein and, thus, exacerbate the effects of the negative energy balance. Given that the logistical limitations to the rations for these missions preclude carrying additional rations to accommodate the increased activity, any increase in activity will result in increased energy deficits. Furthermore, there is evidence that high-intensity exercise is debilitating for muscle protein metabolism. Whereas muscle protein synthesis has been demonstrated to increase following both resistance (Biolo et al., 1995; Phillips et al., 1997, 1999) and endurance (Carraro et al., 1990) exercise in humans, it is depressed following prolonged, high-intensity exercise in rats (Anthony et al., 1999; Gautsch et al., 1998). It is possible that species-specific differences in the response of muscle to exercise may explain the differential. On the other hand, the response of muscle protein synthesis to resistance exercise in rats (Farrell et al., 1999; Hernandez et al., 2000) is similar to that for humans (Biolo et al., 1995; Phillips et al., 1997, 1999). It is more likely that the intensity of the exercise during the treadmill running was severe and resulted in decreased muscle protein synthesis. The rats ran at approximately 80 percent of VO₂max for approximately two hours, roughly equivalent to the effort that only an elite runner could maintain for a marathon. Furthermore, if relative life span is taken into

account, two hours on a treadmill for a rat could be considered equivalent to the effort of several days for humans. Thus, it is conceivable that this intense physical exercise would also result in reduced muscle protein synthesis in humans. The evidence presented suggests that, rather than increasing protein use, the physical activity involved in prolonged military missions may be detrimental to muscle protein metabolism. The energy deficit, combined with high-tempo, stressful physical activity, suggests that muscle protein metabolism will be altered during missions of this type.

As with energy intake, protein intake during these missions can be limited by operational factors. There is a great deal of controversy in the sports science community about the protein requirements for athletes and active individuals; however, little question remains that increased protein intake would be advantageous in an energy deficit made worse by high levels of physical activity. Todd and colleagues (1984) demonstrated that, at low levels of protein intake (0.57 g/kg per day), nitrogen balance was negative during both energy balance and energy deficit. Increasing protein intake from 0.57 to 0.85 g/kg per day improved nitrogen balance when energy intake was 15 percent less than energy output (Figure B-6). Either way, nitrogen balance was negative during both intakes. At this time, there is no way to determine if the loss of body protein could be ameliorated by higher protein intakes and, if so, what would constitute the optimal level of protein intake. A question also remains of a ceiling effect whereby no further improvement is possible with increased protein intake. Unknown as well is whether positive balance is feasible during the conditions inherent to military operations. In addition, it is impossible to determine whether eliminating negative nitrogen balance is necessary to improve the performance and health of the military. A recent study demonstrated that a greater proportion of weight lost during energy restriction comes from fat, rather than lean, mass when protein intake is increased (Layman et al., 2003). Data from this study suggest that increasing protein intake spares body protein during periods of negative energy balance. However, the applicability to soldiers during sustained operations is limited because this study was conducted on obese female subjects in weight-loss situations and did not involve exercise.

Loss of nitrogen likely is exacerbated by the combination of higher protein intakes before missions and lower protein intake during missions. Millward and colleagues demonstrated that body protein is lost when dietary protein intake is decreased (Pacy et al., 1994; Price et al., 1994; Quevedo et al., 1994). Data from these studies suggest an adaptation period that takes several days (often the time expected for most of these missions) (Figure B-7). These data also suggest that the sudden decline in protein intake expected when soldiers undertake these missions would contribute to a loss of body proteins, most likely from muscle.

However, in these studies, the subjects were in energy balance and did not exercise, so it is unclear how applicable these data are to sustained operations.

The available information suggests that decreasing protein intake during these missions will be detrimental to muscle protein metabolism. The recommendation to maximize protein intake during the missions seems prudent; however, there are sufficient questions to prevent a specific recommendation from being made with any confidence.

There is no question that carbohydrate intake is critical for optimal muscle performance during strenuous activity. Maintenance of blood glucose and glycogen for muscle fuel are important for muscular performance (Burke et al., 2004; Coyle, 2004; Hargreaves et al., 2004). Several studies have demonstrated that increased carbohydrate intake improved performance in military tasks (Montain and Young, 2003; Montain et al., 1997). Severe muscle glycogen depletion has been shown during four- to five-day field operations (Jacobs et al., 1983). Although provision of extra carbohydrates did not increase the glycogen levels in these soldiers (Jacobs et al., 1983) sufficient carbohydrate intake seems important for performance maintenance during sustained military operations (Montain and Young, 2003).

Carbohydrate intake may also enhance muscle protein metabolism. Acute provision of carbohydrates increases net muscle protein balance following exercise,

FIGURE B-7 Change in nitrogen (N) balance due to change from the first three days of high-protein (HP) to low-protein (LP) intake.

SOURCE: Quevedo et al. (1994).

presumably through the action of insulin (Borsheim et al., 2004b). Nevertheless, any increase in net muscle protein balance from ingestion of carbohydrate is much less than that from ingestion of an amino acid source (Borsheim et al., 2004a; Miller et al., 2003). On a whole body level, Gaudichon and colleagues (1999) demonstrated that carbohydrate ingestion increased postprandial use of dietary protein to a greater extent than did lipids. It is likely that increased use of available nutrients by the body is especially important in situations of limited nutrient availability. Replacing carbohydrate with fat has been demonstrated to increase nitrogen balance during hypocaloric situations (Richardson et al., 1979). On the other hand, Boirie and colleagues have presented a series of studies (Boirie et al., 1997; Dangin et al., 2003) suggesting that, after protein ingestion, amino acids released slowly into the blood provide a superior anabolic response. Given that lipids do slow the digestion of nutrients, it could be argued that lipids may improve the anabolic response in the muscle. We recently tested this notion in our laboratory, and despite equivalent protein ingestion during two small, separate meals, net muscle protein balance was greater from proteins when fat was included in the meal (Elliot et al., unpublished data). Thus, including both carbohydrates and lipids in the ration should maximize the accretion of ingested protein into muscle when nutrients are limited. The exact composition of such nutrients remains unknown.

Amino acids provided by protein ingestion stimulate the accretion of muscle protein. Evidence from acute metabolic studies suggests that increased muscle protein synthesis and net muscle protein synthesis result only from the provision of essential amino acids; that is, nonessential amino acids are unnecessary to stimulate muscle protein accretion (Borsheim et al., 2002; Tipton and Wolfe, 2001; Tipton et al., 1999, 2003). Furthermore, the response of muscle protein balance to essential amino acids seems dose dependent (Borsheim et al., 2002). Aside from increasing amino acid availability for protein synthesis, essential amino acids may act as signals for stimulating protein synthesis. Essential amino acids, particularly leucine, activate translational signaling (Anthony et al., 2000; Kimball and Jefferson, 2001; Kimball et al., 2002). In rats, leucine stimulates muscle protein synthesis that was diminished by severe exercise (Anthony et al., 1999), but feeding carbohydrates only did not (Gautsch et al., 1998). Essential amino acids may be particularly effective during sustained operations when physical activity is extreme.

More evidence for the potential efficacy of essential amino acids during sustained military operations comes from acute metabolic studies performed in our laboratory. Following resistance exercise, ingesting 12 g of essential amino acids resulted in an amino acid uptake that was more than double that from ingesting 20 g of whole proteins (Borsheim et al., 2002; Tipton et al., 2004)

(Figure B-8). Consuming only 60 percent of the volume more than doubled the anabolic response, which means a superior response was obtained for less mass/volume. Furthermore, essential amino acids, combined with exercise, ameliorated the amino acid release from muscle in response to a 20 percent energy deficit (Tipton et al., 2003). These factors suggest that essential amino acids could be important for ration design.

The metabolic demands endured by soldiers on sustained military operations are severe and unique. Very little research exists that specifically examines the results from missions that involve underfeeding and high-activity levels as well as high stress on muscle metabolism and performance. The indirectly available information suggests that optimal ration development should include maximizing the energy and protein content within the operational limits. Carbohydrate and fat are clearly important, but it is unclear what quantity each should represent in the overall composition. Recent evidence from acute metabolic studies suggests that essential amino acids may be an important component of a ration for sustained missions. The anabolic response to essential amino acids seems to be superior to a larger amount of intact protein, thus offering higher efficiency. Further research is necessary to determine the effects of these various nutrients on muscle metabolism and performance in specific situations experienced during sustained military operations.

FIGURE B-8 Phenylalanine uptake during three hours (h) following ingestion of 12 g of free essential amino acids (EAA), 20 g of casein (CS), or 20 g of whey proteins (WP).

SOURCE: Borsheim et al. (2002); Tipton et al. (2004).

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Edward F. Coyle, University of Texas at Austin

The Committee on Optimization of Nutrient Composition of Military Rations for Short-Term, High-Stress Situations was charged with making recommendations on the composition of a food ration (assault ration) that will best sustain physical and cognitive performance for short-term use by highly-trained soldiers during high-tempo, stressful, repetitive combat missions; in addition, the food ration will also prevent possible adverse health consequences under the conditions of a hypocaloric diet. Stress may be due to high physical and cognitive workloads such as exercise, extreme environmental temperature, dehydration, heat exhaustion, threat to personal safety, sleep deprivation, and other operational demands. Important health concerns for soldiers during combat missions are the optimization of gastrointestinal processes and prevention of diarrhea, dehydration, hyperthermia, kidney stones; optimization of the function of immune system; and prevention of infections. The expected daily expenditure of these soldiers is approximately 4,000 to 4,500 kcal/day. The assault ration will provide approximately 2,400 kcal/day for three to seven days with one to three days of recovery.

This paper focuses on several aspects of the design of such a ration. Although a lot of the literature presented is from the sports and exercise community, their conclusions can be used to support recommendations for the assault ration described above. This paper attempts to answer the following questions:

• What would be the optimal amount of carbohydrates for an assault ration to enhance performance during combat missions?

• What are the types and levels of macronutrients (e.g., complex verses simple carbohydrates) that would optimize an assault ration to enhance performance during combat missions?

• How much is performance going to decline when there is a reduction in both carbohydrates and calories?

Despite long-ago evidence that carbohydrate ingestion during exercise improved athletic performance, the discovery in the 1960s and 1970s of muscle glycogen’s importance as a source of carbohydrate energy for athletes (Bergstrom et al., 1967) seemed to have overshadowed, until the mid-1980s, the potential energy contribution from carbohydrate ingested during the period of exercise (Coggan and Coyle, 1991; Coyle et al., 1986; Hargreaves, 1996). Costill and

Miller (1980) emphasized the need for fluid intake during exercise but recommend against ingesting very much carbohydrate. This recommendation is understandable for that period of time, given that the physiological benefits of fluid replacement were beginning to be established, as reflected in the 1975 American College of Sports Medicine (ACSM) position-statement, whereas the physiological benefits of carbohydrate ingestion for blood glucose supplementation as well as the physiological mechanisms explaining this benefit were not yet established (Hargreaves, 1996). In the 1980s, the observation that adding carbohydrate to water temporarily slowed the gastric emptying rate was interpreted to suggest that fluid replacement solutions should not contain much carbohydrate (Coyle et al., 1978). It was also thought, albeit mistakenly, that “ingested glucose contributes very little to the total energy utilized during exercise” (Costill and Miller, 1980). Therefore, the prevailing recommendation in 1980 was that “under conditions that threaten the endurance athlete with dehydration and hyperthermia, fluid replacement solutions should contain little sugar (> 25 g/L or > 2.5 percent) and electrolytes” (Costill and Miller, 1980).

Later in the 1980s, it was established that ingested carbohydrate and blood glucose can indeed be oxidized at rates of approximately 1 g/minute and that this exogenous carbohydrate becomes the predominant source of energy late in a bout of prolonged, continuous exercise (Convertino et al., 1996). Carbohydrate ingestion can delay muscle fatigue during prolonged cycling and running, and it also improves the power output that can be maintained (Hargreaves, 1996; Millard-Stafford, 1992; Millard-Stafford et al., 1997). It is now understood that the slight slowing of gastric emptying caused by solutions containing up to 8 percent of carbohydrate is a relatively minor factor in fluid replacement rate compared with the large influence of increased fluid volume for increasing gastric emptying and fluid replacement rate (Coyle and Montain, 1992a, b; Maughan, 1991; Maughan and Noakes, 1991; Maughan et al., 1993). Therefore, it is generally recommended that endurance athletes ingest carbohydrate at a rate of 30 to 60 g/h (Casa et al., 2000; Convertino et al., 1996). The type of carbohydrate can be glucose, sucrose, maltodextrins, or some high-glycemic starches. Fructose intake should be limited to amounts that do not cause gastrointestinal discomfort (Casa et al., 2000; Convertino et al., 1996). This rate of carbohydrate ingestion can be met by drinking solutions containing 4 to 8 percent of carbohydrates (4 to 8 g/100 mL) (Casa et al., 2000; Convertino et al., 1996; Rehrer, 1994; Rehrer et al., 1993).

Benefits of carbohydrate ingestion during performance of high-intensity, intermittent exercise attempted after at least 60 minutes of continuous moderate-intensity exercise (i.e., 65 to 80 percent VO₂max) was the focus of study beginning in the late 1980s. Power output measured over 5 to 15 minutes of high-

intensity and predominantly aerobic exercise has been generally observed to increase by ingesting carbohydrate (Coggan and Coyle, 1988; Mitchell et al., 1989; Murray et al., 1987; Sugiura and Kobayashi, 1998) In the 1996 ACSM position statement on Exercise and Fluid Replacement, it was concluded that “During intense exercise lasting longer than 1 h, it is recommended that carbohydrates be ingested at a rate of 30–60 g/h to maintain oxidation of carbohydrates and delay fatigue” (Convertino et al., 1996).

During the past decade, attention has focused on determining if carbohydrate intake during sporting events such as soccer and tennis improves various indices of performance. As discussed below, carbohydrate ingestion appears to frequently benefit performance as demonstrated in tests of “shuttle-running” ability, which simulates the stop-and-start nature of many sports requiring bursts of speed and some fatigue resistance (Nicholas et al., 1995). Physiological mechanisms for this ergogenic effect of carbohydrate ingestion are not clear and have been theorized to involve more than simply skeletal muscle metabolism, implying a neuromuscular component. The challenges now are identifying the types of physical activity and sporting situations during which carbohydrate ingestion is advisable and those during which such a recommendation is not effective or even counterproductive.

Performance or fatigue resistance can be governed by numerous physiological factors involving, primarily, the skeletal muscle, the cardiovascular system, and the nervous system. Some primary causes of fatigue are not influenced by carbohydrate ingestion during exercise; for example, the negative effects of hyperthermia on performing prolonged exercise in a hot environment [e.g., 33°C to 35°C (91.4°F to 96°F)] do not appear to be lessened by carbohydrate ingestion (Febbraio et al., 1996; Fritzsche et al., 2000). However, during exercise in a cool environment [i.e., 5°C (41°F)] (Febbraio et al., 1996) that is not limited by hyperthermia, or when subjects drink fluids during exercise in a hot environment and also do not become hyperthermic (Fritzsche et al., 2000), carbohydrate ingestion improves performance. Under conditions not eliciting hyperthermia, the most important factor for performing prolonged, intense exercise appears to be maintaining carbohydrate availability and thus carbohydrate oxidation, especially from blood glucose oxidation as muscle glycogen concentration declines. This goal was better achieved by ingesting 7 percent carbohydrate solutions as compared with a 14 percent solution (Febbraio et al., 1996).

Another example of a condition when carbohydrate ingestion during exercise would not be expected to improve performance is when the cause of fatigue is the accumulation of hydrogen ion in skeletal muscle (e.g., low muscle pH), as occurs during a single bout of intense exercise performed continuously for 2 to

30 minutes. Performing exercise that is not sufficiently stressful to cause fatigue, as evidenced by reduced power production, or that does not require high levels of effort to maintain power, as reflected, for example, by high levels of various stress hormones, would not benefit from carbohydrate ingestion. Furthermore, carbohydrate intake is not generally recommended during events, performed either continuously or intermittently, that are completed in 30 to 45 minutes or less. Although this last concept has not been extensively studied to date, it is a valid assumption based on the practices of athletes competing in events lasting only 30 to 45 minutes. As discussed, carbohydrate ingestion does not appear to lessen fatigue from hyperthermia or dehydration-induced hyperthermia, even when the durations of exercise are prolonged (e.g., one to three hours) (Febbraio et al., 1996; Fritzsche et al., 2000). Thus, there does not appear to be any benefit of adding carbohydrate to fluid replacement solution under these conditions. Accordingly, people who exercise at moderate intensity for less than one hour and do not experience fatigue do not appear to benefit from carbohydrate ingestion during exercise. Yet ingesting carbohydrate at a rate of 30 to 60 g/h does not appear to present a general physiological risk to people who do not experience gastrointestinal discomfort.

Carbohydrate ingestion during prolonged exercise can benefit performance if inadequate carbohydrate energy from blood glucose is the cause of fatigue (Coggan and Coyle, 1991; Febbraio et al., 1996). This effect on performance is a well-documented physiological mechanism by which the ergogenic benefit of carbohydrate ingestion during exercise can be explained. However, carbohydrate ingestion has been observed to improve performance under conditions in which fatigue is not clearly caused by a lack of aerobic or anaerobic carbohydrate energy. For example, when the duration of continuous exercise is extended to approximately 60 minutes and thus the intensity is 80 to 90 percent VO₂max, carbohydrate ingestion during exercise has been shown to improve power output by 6 percent during the 50- to 60-minute period (Below et al., 1995).

Other recent studies have also reported a performance benefit of carbohydrate feeding when the total duration of the performance bout is approximately 60 minutes or more by breaking the time into shorter exercise durations, thereby simulating the demands of many sports (basketball, soccer, hockey) in which high-intensity exercise is interspersed with periods of recovery (Mitchell et al., 1989; Murray et al., 1987). Carbohydrate ingestion is ergogenic during 15-minute bouts of intermittent “shuttle running,” performed numerous times (e.g., five times) as well as during repeated high-intensity intervals of one minute’s duration and a three-minute recovery (Davis et al., 1997, 1999, 2000; Nicholas et al., 1995; Welsh et al., 2002). The total duration of these work–rest bouts was more

than 60 minutes. The physiological mechanisms responsible for these performance benefits from carbohydrate ingestion are not clear and have been theorized to involve the central nervous system, skeletal muscle, and the cardiovascular system. It is likely that carbohydrate feeding influences the interactions of all three systems, possibly through the actions of neurotransmitters, hormones, and peptides that are already known (e.g., insulin, catecholamines, and serotonin), that are newly recognized (e.g., interluken-6), or that have yet to be discovered. Regardless, sufficient evidence is accumulating to recommend carbohydrate ingestion during exercise bouts of continuous or intermittent exercise that lasts for 60 minutes or longer and cause fatigue from factors other than hyperthermia.

It is recommended that carbohydrate be ingested at a rate of 30 to 60 g/h during exercise (Convertino et al., 1996), recognizing that ingesting more does not increase oxidation rate but can produce gastrointestinal discomfort in many people (Rehrer et al., 1992; Wagenmakers et al., 1993). In the latter case, carbohydrate feeding can be counterproductive when ingested in amounts (> 60 to 90 g/h) or concentrations (> 7 to 8 percent) that are too large (Febbraio et al., 1996; Galloway and Maughan, 2000).

If it produced gastrointestinal discomfort, carbohydrate ingestion at 30 to 60 g/h during exercise can impair performance as compared with no carbohydrate ingestion, a factor that is likely to vary from sport to sport and athlete to athlete. Carbohydrate ingestion should be used with caution during events lasting approximately 15 to 45 minutes and requiring repeated bouts of intense exercise lasting several minutes followed by several minutes of rest because these events may cause large swings in blood glucose and insulin concentration. Feeding plans must be specific to the varied intensity and time demands of the event. Those feeding schedules might be more than those described below, yet without data or experience to make more specific recommendations; all that can be done at present, besides recognizing these limitations, is to encourage systematic trial and error.

From a practical perspective, the recommendation of ingesting 30 to 60 g/h of carbohydrate during exercise should emphasize that this be accomplished by taking feedings every 10 to 30 minutes, as allowed by the event. The goal of the feeding schedule should be to create a steady flow of carbohydrate into the blood stream, which will then provide a steady flow of exogenous glucose into the blood. In other words, if carbohydrate feeding is begun during an event, it should be continued throughout the event in a manner that allows for a steady flow of exogenous glucose into the blood with minimal gastrointestinal discomfort. Avoid giving a large bolus of carbohydrate (i.e., more than 30 to 60 g) early in an event and then discontinuing carbohydrate feeding. This practice will prime the body for glucose metabolism, reduce fat oxidation, and then deprive the body of the fuel it has been primed to metabolize.

During exercise that lasts longer than one hour and that causes fatigue, physically active people are advised to ingest 30 to 60 g/h of carbohydrate that can be rapidly converted to blood glucose because doing so generally improves performance. There is not a clear physiological need to consume any fluid or fuel when beginning exercise while reasonably hydrated and proceeding to exercise at low or moderate intensity for less than one hour without experiencing undo fatigue. However, there is no apparent reason for people to avoid fluid or carbohydrate intake if this is their preference and is well tolerated.

The author is a member of the Sports Medicine Review Board of the Gatorade Sports Science Institute. Portions of this manuscript are similar to a recent review by the author published in 2004. Coyle EF. 2004. Fluid and fuel intake during exercise. Journal of Sports Sciences 22:39–55.

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Randall J. Kaplan, Canadian Sugar Institute

The importance of nutrition for cognitive performance in military settings has long been recognized. The Committee on Military Nutrition Research (CMNR) of the Food and Nutrition Board, Institute of Medicine (IOM) of the National Academies has published several volumes on this topic, including reports on the cognitive effects of performance-enhancing food components (IOM, 1994); inadequate energy intakes (IOM, 1995); protein and amino acids (IOM, 1999); and caffeine (IOM, 2001).

Cognitive performance refers to intellectual behaviors such as memory, reasoning, attention, vigilance, and choice reaction time. Mood (e.g., happy, sad, calm, tense) and psychomotor performance (e.g., sensation, perception, agility) are distinct from cognitive performance, but they can have a considerable influence on it (Mays, 1995; Spring et al., 1994) and are therefore relevant to this discussion. The aspects of cognition that are important in combat settings include the ability to perceive, attend to, and respond appropriately to cues; make prompt decisions; and sustain vigilance (IOM, 1994; Mays, 1995).

The Committee on Optimization of Nutrient Composition of Military Rations for Short-Term, High-Stress Situations, an ad hoc committee of the CMNR, has been given the task of recommending the nutrient composition of a ration for combat missions to optimize physical and cognitive performance and to prevent adverse health consequences.

This daily ration is intended for repeated short-term use (three to seven days followed by one to three days of ad libitum recovery) by fit male soldiers during high-tempo, stressful combat missions. Stress may be caused by physical and cognitive workloads, extreme temperature, threats to safety, and sleep deprivation, all of which can interfere with cognitive performance (Lieberman et al., 2002b; Owen et al., 2004).

The purpose of this report is to briefly review relevant evidence on the effects of energy and macronutrients (i.e., carbohydrate, protein, and fat) on cognitive performance and mood, and to provide recommendations for the macronutrient composition of the assault ration, including types of each macronutrient, to enhance cognitive performance. Because factors associated with combat operations are likely to lead to cognitive deficits relative to normal functioning, the realistic goal in optimizing the nutrient composition of the ration should be to decrease these deficits, rather than to enhance performance beyond normal bounds.

To address this task this paper discusses the following specific questions:

• Should the energy content of the ration (energy density) be maximized so as to minimize the energy debt, or is there a more optimal “mix” of macronutrients and micronutrients, not necessarily producing maximal energy density?

• What would be the optimal macronutrient balance between carbohydrate, protein, and fat for such an assault ration to enhance cognitive performance during combat missions?

• What are the types and levels of macronutrients (e.g., complex verses simple carbohydrates, proteins with specific amino acid profiles, type of fat, etc.) that would optimize such an assault ration to enhance cognitive performance during combat missions?

For the purpose of this paper, it has been assumed that other nutrional requirements of the soldiers (e.g., water, micronutrients) will be met. If these other requirements are not met, the results could override the importance of macronutrient requirements. For instance, it is well established that hypohydration (Wilson and Morley, 2003) and iron deficiency (Sandstead, 2000) present significant detriments to cognitive performance. In the combat situation, particularly during extreme temperatures, the highest priority for reducing cognitive impairment is adequate hydration (IOM, 1995).

The maximum weight of the macronutrient component of a 1,360 gram-ration is approximately 500 g [calculated from a standard, approximately 2,400-kcal ration, comprising 50 percent of energy as carbohydrate (300 g), 30 percent as fat (80 g), and 20 percent as protein (120 g)], with the remaining 860 g comprised of noncaloric components, including moisture, fiber, and micronutrients. Theoretically, 500 g could provide between 2,000 kcal (i.e., entirely protein and carbohydrate) and 4,500 kcal (i.e., entirely fat), in which case the energy needs of the soldiers (4,000 to 4,500 kcal/day) could be met within the weight limitation of the ration if energy density were increased as much as possible. The question is: Should the energy content of the ration be maximized, or is there a more optimal ratio of macronutrients for cognitive performance?

The acute effects (hours) of energy ingestion on cognitive performance have been examined in a number of studies in healthy, nonstressed subjects. Several reviews of the literature have concluded that the provision of energy in the morning (breakfast) generally improves cognitive performance over the next 30 minutes to 2 h, compared with no energy provision, with more robust effects on tests of memory and less consistent effects on tests of attention or vigilance (Bellisle et al., 1998; Dye and Blundell, 2002; Kanarek, 1997; Leigh Gibson and

Green, 2002; Pollitt and Matthews, 1998). The mechanism for these results has not been elucidated, but likely both gut-mediated and centrally acting postabsorptive signals are involved (Kaplan et al., 2001).

By contrast to the breakfast studies, large meals provided at mid-day (lunch) consistently impair cognitive performance (e.g., memory, vigilance, and reaction time) and mood (e.g., alertness and fatigue) over the next one to two hours, compared with the effects of those consuming no lunch or a light lunch. This phenomenon is known as the “post-lunch dip” and is likely related to normal changes in daily circadian rhythm as well as changes to habitual intake patterns (Bellisle et al., 1998; Dye et al., 2000; Kanarek, 1997; Leigh Gibson and Green, 2002).

A few studies have examined the short-term effects of energy intake on cognitive performance and mood under stressful conditions, showing the benefits of increased energy intake. One study found no changes in mood after low-energy intake during breakfast and lunch (264 kcal) as compared with a higher energy intake (1,723 kcal; consistent with energy needs of the subjects) during a nonstressful condition (Macht, 1996). However, when participants were subjected to emotionally stressful white noise, those with a low-energy intake experienced a degradation in mood (i.e., more irritability and less relaxation), whereas those with a higher energy intake did not.

Another study strongly supports a beneficial effect of increased energy ingestion on cognitive performance and mood under stressful conditions (Lieberman et al., 2002a). In this study, 143 male subjects from an elite combat unit were tested during periods of intense physical activity over 10 h, during which energy needs were not met with regular meals (approximately 765 kcal) (Lieberman et al., 2002a). Energy supplementation (carbohydrate-containing drink) throughout the day improved vigilance and mood (i.e., increased vigor, decreased confusion) in a dose-dependent manner compared with the effects of a noncaloric placebo drink. The strongest effects on performance resulted from the highest energy drink (approximately 1,309 kcal), followed by the medium-energy drink (approximately 654 kcal), and the placebo (0 kcal) (Figure B-9). It is impossible to determine from this study whether the beneficial effects were caused by an increase in energy ingestion or an increase in carbohydrate ingestion.

The medium-term effects (days) of dieting to lose weight consistently impair cognitive performance and mood (Leigh Gibson and Green, 2002). The effects are attributed to the act of dieting, rather than to inherent differences between dieters and nondieters because the impedence on performance is not observed when the same individuals are not dieting (Green and Rogers, 1995). It has been suggested that this impairment is caused more by a psychological pre-occupation with food and feelings of hunger than by a physiologic effect of low

FIGURE B-9 Vigilance performance of soldiers who received carbohydrate (CHO) beverages or placebo in addition to regular meals (providing approximately 765 kcal) while engaging in various activities over 10 h.

NOTE: A higher number on the y-axis represents improved performance.

SOURCE: Adapted from Lieberman et al. (2002a) with permission by the American Journal of Clinical Nutrition © Am J Clin Nutr. American Society for Clinical Nutrition.

energy intake (Leigh Gibson and Green, 2002). This conclusion is based on evidence that (1) individuals perform worse on cognitive tests when they are dieting, even when no actual weight is lost; (2) the magnitude and structure of the deficits is comparable to those caused by anxiety and depression; and (3) performance is not clearly affected by weight loss in the absence of other stress. It has been hypothesized that task-irrelevant feelings of hunger and thoughts of food may impair performance by interfering with normal working memory function. Working memory can be conceptualized as “the fundamental cognitive processing system, in that it serves to allocate limited cognitive processing capacity to other ongoing cognitive operations in order of their relevance or importance to an individual” (Leigh Gibson and Green, 2002).

A study using a similar eating pattern as would be consumed by combat soldiers (several days of hypocaloric intake followed by ad libitum intake) supports the hypothesis that energy restriction impedes performance in the absence of significant weight loss (Laessle et al., 1996). In this study, healthy female subjects consumed a low-calorie diet (approximately 651 kcal/day) for four days, followed by ad libitum intake (approximately 2,876 kcal/day) for three days each week for four weeks. During the low-calorie periods, subjects reported stronger feelings of hunger and thoughts about food as well as demonstrating

worse moods, more irritability, difficulties concentrating, and greater fatigue than during the ad libitum periods even though weight loss was minimal. Repeated episodes of low energy intakes over the 4 weeks did not reduce feelings of hunger. The implication of this study is that the negative effects of hunger are unlikely to be reduced during periods of low energy intake when soldiers repeatedly eat hypocaloric diets followed by ad libitum recovery periods. In other words, it may be very difficult to train soldiers to ignore their hunger feelings. It should be noted, however, that this study was performed with women and not under the unique added stressors of combat missions.

The hypothesis presented suggests that psychological feelings of hunger contribute to cognitive deficits during periods of low energy intake; however, the physiologic consequences of low energy intake and negative energy balance cannot be ruled out as contributing factors because other acute evidence (presented earlier) and longer term evidence under the stressful conditions presented below do not clearly indicate the mechanism involved. Most likely, both psychological and physiological factors associated with low energy intake, particularly under stressful conditions, contribute to the performance deficit.

The evidence that increased appetite interferes with the ability to perform optimally suggests that reducing hunger may be beneficial for mood and cognitive performance. Indeed, declining hunger sensations have been associated with being more energetic, lively, calm, and relaxed (Fischer et al., 2004). The macronutrient composition of foods can play an important role in minimizing hunger. Protein consistently and robustly induces greater satiety than carbohydrate or fat on a per calorie basis (Westerterp-Plantenga, 2003) and has a greater effect on satiety than do substantially higher energy intakes from the other macronutrients (Stubbs and Whybrow, 2004; Stubbs et al., 2000) (Figure B-10). Carbohydrate appears to induce greater satiety than fat does on a per calorie basis (Stubbs et al., 2000), but the differences are minimal when palatability and energy density of foods are matched (Rolls and Bell, 1999). Thus, to reduce the negative effects of hunger on cognitive performance and mood, it may be beneficial to increase the protein content of hypocaloric military rations and to reduce the fat content.

Various types of each macronutrient also have different effects on satiety (Stubbs et al., 2000). A review concluded that high glycemic index carbohydrates (i.e., rapidly raise blood glucose concentration) have a greater effect on satiety than low glycemic index carbohydrates over the short term (up to one hour after carbohydrate ingestion), whereas lower glycemic index carbohydrates have a stronger effect on satiety over the longer term (i.e., up to 6 h after carbohydrate ingestion) (Anderson and Woodend, 2003). However, these effects are not likely caused entirely by changes in blood glucose (Kaplan and Greenwood, 2002). The data implicating different effects of fat type on satiety are mixed, with some suggesting that polyunsaturated fatty acids have a stronger effect on increasing satiety than monounsaturated or saturated fatty acids do (French and Robinson, 2003; Lawton et al., 2000), whereas others have found no differences between

FIGURE B-10 Effect of increasing energy content of macronutrient loads on satiety over 3.25 h.

NOTE: Data were collated from a number of studies.

SOURCE: Adapted from Stubbs and Whybrow (2004).

the two (Alfenas and Mattes, 2003; Flint et al., 2003). Medium-chain triglycerides, which are rapidly metabolized, have been shown to exert a stronger effect on satiety than long-chain triglycerides do; however, only a few human studies are available and the results are inconclusive (French and Robinson, 2003; St-Onge and Jones, 2002). Research on the effects of protein type on satiety is also limited because evidence in human studies suggesting that some proteins might suppress appetite more than others is inconsistent (Anderson and Moore, 2004; Westerterp-Plantenga, 2003).

It is important to note that, although it is argued here that reducing hunger in soldiers consuming hypocaloric rations may be beneficial for cognitive performance, this may not be relevant if appetite is suppressed by hypohydration, physical activity, or stress to the extent that feelings of hunger and thoughts of food are eliminated. It is well documented that soldiers tend to underconsume foods, and this may be partially due to a suppression of appetite (IOM, 1995). Thus, it is important to determine whether the expected increase in appetite

associated with the hypocaloric intake of combat soldiers is stronger or weaker than the suppression of appetite that will be caused by other factors. There is evidence, however, that when military rations provide only 60 percent of energy needs (i.e., energy intake and energy expenditure was 1,946 kcal and 3,200–3,300 kcal, respectively), the entire rations are consumed (Shukitt-Hale et al., 1997), suggesting that soldiers’ appetites are strong under these circumstances. These data would support the argument that strong feelings of hunger will be present in combat soldiers consuming assault rations containing approximately 2,400 kcal/day when their needs are > 4,000 kcal/day.

The long-term effects (weeks or months) of energy intake on cognitive performance are not relevant if soldiers are able to consume enough excess energy during the one- to- three-day ad libitum recovery period to make up for the negative energy balance during the three to seven days, such that they do not lose weight. By contrast, if soldiers are in a state of negative energy balance over weeks and months because of repeated consumption of hypocaloric diets and inadequate recovery periods, then the long-term effects of low energy intake are relevant.

Evidence on the long-term effects of low energy intake on cognitive performance shows that those effects are minimal in the absence of significant stress but are significant if stress is present. In a review of the effects of underconsumption of military rations on cognitive performance, Mays (1995) concluded that underconsumption leading to weight loss up to 6 percent over 10 to 45 days does not affect performance in the absence of significant stress. A more recent study over a 30-day trial supports this conclusion (Shukitt-Hale et al., 1997). However, consistent with the long-term dieting data (e.g., Kretsch et al., 1997), underconsumption combined with stress during military operations (e.g., exercise, sleep deprivation, and danger) significantly degrades performance within a few days (Mays, 1995). Based on the available data, Mays proposed a relationship between long-term negative energy balance and cognitive performance (Figure B-11). These data suggest that consumption levels of 75 to 90 percent of requirements may actually enhance performance in the first 3 to 15 days, whereas consumption of 50 percent or less of requirements degrades performance, particularly under stressful conditions. Over the longer term, performance continues to degrade along with negative energy balance. Thus, if repeated short-term periods of low energy intake during combat operations lead to long-term negative energy balance, deficits in cognitive performance can be expected.

FIGURE B-11 Proposed relationship between energy intake as a percentage of energy expenditure and cognitive performance over two months, based on the results of several studies.

SOURCE: Adapted from Mays (1995).

For the purposes of this paper, “carbohydrate” refers to digestible or glycemic carbohydrates that provide energy (primarily sugars and starches). It does not include dietary fiber, resistant starch, or other nondigestible carbohydrates that do not provide energy as a carbohydrate.

A large number of studies conducted over the past 20 years have shown beneficial effects of glucose ingestion on cognitive performance as compared with noncaloric sweetened placebos (e.g., aspartame, saccharin) in animals and humans over the short term—from 15 minutes to 3 h after ingestion (Greenwood, 2003; Korol, 2002; Korol and Gold, 1998; Messier, 2004). Cognitive impairments associated with hypoglycemic episodes have also been a consistent finding

(McCall, 1992). Early studies suggested that the cognitive-enhancing effects of glucose were only evident when an existing deficit was present, such as in elderly subjects and in patients with Alzheimer’s disease, schizophrenia, and Down syndrome, but not in healthy young adults (Korol and Gold, 1998). Since that time, others have shown that consuming glucose can improve performance in young adults if cognitive tasks are sufficiently demanding (Benton, 2001); however, the magnitude of the effects depends on glucose regulation and baseline cognitive abilities (Awad et al., 2002; Greenwood, 2003; Kaplan et al., 2000; Messier, 2004).

The beneficial effects of consuming glucose are dependent on the type of cognitive test, task difficulty, and glucose dose (Greenwood, 2003; Messier, 2004). In contrast with the data showing the benefits of eating breakfast and the detriments of eating lunch, the effects of consuming glucose appear to be positive in both the morning and the afternoon (Sunram-Lea et al., 2001). The effects of glucose are strongest on functions mediated by the medial temporal lobe and surrounding areas, including long-term verbal memory, and less robust for other tasks, including short-term memory, attention, and reaction time. Glucose consumption can, however, improve performance on a wide range of tasks as long as the tasks are of sufficient difficulty. For instance, Kennedy and Scholey (2000) found glucose ingestion improved performance in young adults on a difficult test (serial sevens, which requires subjects to count backwards by sevens), but not on two easier tests (Figure B-12). These findings suggest that an increased brain requirement for glucose is needed before benefits of glucose ingestion can be observed. Conditions for which glucose could reverse deficits in performance caused by increased brain requirements for glucose include those of aging (McNay and Gold, 2001), increased cognitive demand (Fairclough and Houston, 2004), and physical activity (Brun et al., 2001; Grego et al., 2004; Nybo and Secher, 2004). Thus, carbohydrate ingestion is likely to benefit cognitive performance during combat operations for which brain glucose requirements would likely be increased because of the demanding nature of the tasks and high levels of physical activity.

The dose of glucose that enhances cognitive performance follows an inverted U-shaped response in humans and animals. Consistently, low doses have no effect on performance, intermediate doses (25 to 75 g) improve performance, and high doses have no effect or impair performance (Greenwood, 2003; Greenwood et al., 2003; Messier, 2004; Parsons and Gold, 1992) (Figure B-13). Taken together, these findings suggest that a moderate amount of glucose improves performance on a range of demanding cognitive tests in young adults, or on tasks in demanding situations (e.g., stress, physical activity), but glucose is unlikely to improve performance on simpler tasks under nonstressful conditions.

There is no consensus on the mechanism that explains the effects of glucose on cognitive performance, but several hypotheses have been proposed. The following effects of glucose ingestion have been most commonly suggested as

FIGURE B-12 Mean number of responses (subtractions or words produced) made on each of three tasks after ingestion of noncaloric saccharin-sweetened placebo or of 25 g glucose drinks.

*p < 0.01 compared with corresponding placebo group.

SOURCE: Adapted from Kennedy and Scholey (2000).

possible mechanisms: replenishes brain extracellular glucose that declines during difficult tasks; increases synthesis of the brain neurotransmitter acetylcholine; increases central insulin; or influences peripheral signals that are relayed to the brain via the vagus nerve (Greenwood, 2003; Messier, 2004; Park, 2001).

As noted earlier, one study found that a carbohydrate-containing beverage provided in addition to regular hypocaloric meals benefited vigilance and mood during combat training (Figure B-9), but it is impossible to determine whether the benefits were due to increased energy intake or to carbohydrate intake (Lieberman et al., 2002a). The authors suggested that the benefits could have been due to an increased supply of glucose to the brain, which could have helped

FIGURE B-13 Logical memory scores in elderly subjects 5 and 40 minutes after glucose ingestion, presented as differences from placebo (saccharin). Significant memory enhancement was observed after 25 g glucose, but not at the higher or lower doses.

* p < 0.05 versus placebo.

SOURCE: Adapted from Parsons and Gold (1992), used with permission from Elsevier.

prevent a reduction in the synthesis of neurotransmitters protecting the brain from the consequences of an energy deficit.

Other studies suggest that carbohydrate, independent of energy intake, benefits performance under hypocaloric (Wing et al., 1995) and physically demanding (Achten et al., 2004) circumstances that are relevant for combat operations. Wing and colleagues (1995) found that a low-energy (549 kcal/day), low-carbohydrate–high-fat diet was associated with impaired performance on a test of general brain function after one week as compared with the results of an equal-energy, high-carbohydrate–low-fat diet. In addition, during 11 days of intense running training, Achten and colleagues (2004) found that higher carbohydrate–lower fat diets improved overall mood and reduced fatigue as compared with the results of equal-energy (approximately 3,900 kcal/day), low-carbohydrate–high-fat diets.

Under nonexercise, adequate energy situations, carbohydrate ingestion has been associated with both better and worse moods (Benton, 2002; Leigh Gibson and Green, 2002), which may be dependent on the testing time after ingestion. Carbohydrate may improve mood up to 30 minutes after ingestion, but it is

associated with a sedative effect after about 2 h (Benton, 2002). The sedating effect may be caused by a carbohydrate-induced increased tryptophan/large neutral amino acid ratio, which increases both the brain tryptophan levels and the synthesis of the neurotransmitter serotonin (Spring et al., 1994). However, the effect of carbohydrate on serotonin is abolished with the ingestion of as little as 4-percent protein (Benton, 2002; Benton and Donohoe, 1999; Benton and Nabb, 2003; Spring et al., 1994), so these findings are likely not relevant for military rations with mixed macronutrient composition. Another hypothesis suggests that beneficial effects of carbohydrate on mood are related to an increased release of endorphins relevant to the ingestion of any palatable food, rather than to carbohydrate per se (Benton, 2002).

The type of carbohydrate may be important for cognitive performance although research in this area is limited to two studies. In one study in healthy elderly subjects, 50 g of carbohydrate from glucose, potato (high glycemic index), or barley (low glycemic index) all improved performance on memory and a test of general brain function up to one hour after ingestion, particularly in subjects with poorer baseline memory and glucose regulation (Kaplan et al., 2000). The cognitive-enhancing effects of barley, which raised blood glucose to 6 mmol/L, were novel because it had previously been believed that blood glucose must be at a concentration of 8 to 10 mmol/L for a benefit to be observed. These findings were supported by a recent study that found that a high-carbohydrate meal with a lower glycemic index improved memory in young adults up to 3 h after ingestion, but a higher glycemic index meal did not (Benton et al., 2003). The findings could not be related to blood glucose levels, but these data, along with the evidence showing an inverted U-shaped dose response for glucose, suggest that a prolonged increase in blood glucose and insulin levels, rather than rapid fluctuations, may be beneficial.

It is noteworthy that virtually all studies examining the effects of carbohydrate on cognitive performance or mood have used glucose or glucose polymers (e.g., starches). A few studies have examined the effects of fructose which is metabolized differently from glucose, in rats, but the evidence is mixed (Messier, 2004). Until evidence to the contrary is available in humans, it should be assumed that the beneficial effects of carbohydrate are limited to sources of glucose or glucose polymers.

Protein has the potential to influence cognitive performance because several amino acids, including tryptophan, tyrosine, phenylalanine, arginine, histadine,

and threonine, are precursors of neurotransmitters or neuromodulators and can influence their synthesis (Lieberman, 2003). Indeed, individual amino acids have been shown to influence cognitive performance; however, these effects are likely not relevant when examining the effects of protein consumed as part of a food ration (Greenwood, 1994). In particular, tyrosine benefits cognitive performance in sleep deprived, stressed subjects, likely by its role as a precursor for the neurotransmitters norepinephrine and dopamine (Lieberman, 2003). Tryptophan may be beneficial as a sleep aid, by way of its effects on increasing synthesis of serotonin, and it improves vigilance by way of increasing the release of melatonin (Lieberman, 2003). However, any potential benefits of these amino acids would likely be as between-meal supplements, rather than as part of normal meals (Greenwood, 1994).

As noted in the carbohydrate section above, several reports have concluded that high-carbohydrate–low-protein meals are sedating because they cause an increase in serotonin synthesis, whereas protein-rich meals are arousing and can improve reaction time and vigilance (Dye and Blundell, 2002; IOM, 1994; Leigh Gibson and Green, 2002). However, as noted, these findings are likely not relevant for mixed macronutrient military rations because as little as 4 percent protein prevents the effect on serotonin. Moreover, other data do not support a negative influence on mood by consumption of a high-carbohydrate–low-protein diet. A review by Benton and Donohoe (1999) concluded that diets higher in carbohydrate and lower in protein are associated with less depression, anger, and tension and with being more energetic.

Although the fat content of diets can have an effect on cognitive performance over the long term (i.e., months or years) (Greenwood and Young, 2001; Kaplan and Greenwood, 1998), fat likely only has limited effects over the short term (i.e., hours or days), possibly related to the fact that rates of fat and carbohydrate oxidation are not influenced by the fat content of a meal (Flatt et al., 1985). Nevertheless, some studies have found acute effects of fat on performance and mood, but the data are inconsistent. Recent reviews concluded that in general, high-fat–low-carbohydrate meals can lead to declines in alertness and reaction time, particularly when they differ from habitual fat intake (Dye and Blundell, 2002; Leigh Gibson and Green, 2002).

Few direct comparisons between pure macronutrients have been made. Kaplan and colleagues (2001) found that in healthy elderly persons, pure protein, carbohydrate, and fat could all improve memory performance 15 minutes after ingestion compared with a noncaloric placebo, suggesting a general benefit of energy ingestion, likely mediated by a peripheral mechanism, which could include gut peptides or signals to the brain by way of the vagus nerve. However, it was also found that each macronutrient had unique effects on performance. For instance, as shown in Figure B-14, only glucose tended to improve memory 60 minutes after ingestion, and performance on a visual-motor task; and protein was the only macronutrient to slow the rate of forgetting. Various peripheral and

central mechanisms could account for these specific effects. Another study also found unique effects of each macronutrient in healthy young adults (Fischer et al., 2001). Carbohydrate improved choice reaction and short-term memory time after one hour; protein improved choice reaction time after two hours; fat improved performance on short-term memory and attention.

Taken together, several reviews have concluded that, although macronutrients have been shown to have different effects on cognitive performance, the effects have been inconsistent, and few overall conclusions can be made at this time about an optimal ratio of macronutrients for cognitive performance (Bellisle et al., 1998; Dye and Blundell, 2002; Dye et al., 2000; Kanarek, 1997; Lieberman, 2003).

Despite discrepancies in the literature, some conclusions can be made about the effects of energy ingestion on cognitive performance. (1) Energy ingestion approaching the level of energy needs generally improves cognitive performance and mood over the short term (several hours) compared with no energy or very low energy ingestion; the fact that benefits seem to be independent of weight loss suggest that feelings of hunger and thoughts of food contribute to the cognitive and mood deficits. Thus, minimizing hunger may minimize the negative effects on performance. Hunger can be minimized with higher protein and lower fat ingestion. (3) Over longer periods (weeks or months), there is a gradual impairment in cognitive performance associated with negative energy balance and weight loss, with greater and more rapid deficits associated with very low energy intakes (< 50 percent of energy requirements), particularly under stressful conditions.

The review of the research presented in this paper shows that the scientific literature in this area is inconsistant and contradictory; therefore, it is difficult to make definitive recommendations regarding the questions posed in the introduction. The research, although not conclusive, supports the following conclusions described below.

The following are desired characteristics of an assault ration designed for cognitive performance:

• Adequate and sustained glucose supply to the brain. The provision of glucose or carbohydrate to the brain improves mood and performance when brain glucose requirements increase, which appears to occur during cognitively demanding tasks, particularly under hypocaloric, stressful, or physically demanding conditions.

• Moderate fluctuations in blood glucose. Consistent evidence shows that both hypoglycemia and hyperglycemia impair cognitive performance; that intermediate, but not high or low, doses of glucose improve performance;

and that limited evidence shows that low glycemic index carbohydrates improve performance over a longer period than do higher glycemic index carbohydrates. Thus moderate, rather than extreme, fluctuations in blood glucose are desirable.

• Minimize feelings of hunger. Hypocaloric intakes are associated with deficits in cognitive performance and mood, and this is caused, in part, by feelings of hunger and thoughts of food interfering with normal cognitive processes. Reducing feelings of hunger is desirable.

• Minimize long-term negative energy balance. Sufficient data indicate that long-term energy deficits resulting in negative energy balance and weight loss are associated with deficits in cognitive performance and mood under stressful situations. Long-term negative energy balance should be minimized.

The optimal composition of the assault ration for cognitive performance would be characterized by the following:

• A maximized carbohydrate content of the ration to provide an adequate and sustained supply of glucose to the brain, because of their hypocaloric nature and the fact that substantial carbohydrate will be required to sustain physical activity. The carbohydrate source should ideally provide glucose (e.g., glucose, sucrose, starch) rather than other monosaccharides (e.g., fructose) as the beneficial effects of carbohydrate have only been shown with glucose. The effect of the ration on blood glucose should be moderate for optimal and sustained cognitive performance and should also reduce feelings of hunger. Importantly, the carbohydrate source may have a high or low glycemic index to give the overall ration a moderate effect on blood glucose, because the other components of the ration could affect blood glucose. For instance, both protein (increases insulin release) and fiber can lower blood glucose. Higher protein and fiber content rations may necessitate higher glycemic index carbohydrates to obtain a ration with a moderate effect on blood glucose.

• If feelings of hunger are strong and long-term energy balance is not a major problem (i.e., energy balance can be maintained by high energy intakes during the recovery periods between combat operations), then protein content of the ration should be increased and fat content should be decreased to increase satiety and reduce feelings of hunger. In this case, the energy density of the ration will not be maximized. Not enough evidence exists to recommend a specific amino acid or fatty acid profile that will optimize cognitive performance compared with any other profile. It seems prudent to supply minimum amino acid requirements.

• If feelings of hunger are weak because of stress or hypohydration out-weighing the effects on appetite of the low calorie diet, and long-term

negative energy balance and weight loss are expected, then minimum protein requirements should be met for nitrogen balance, and fat content should be increased to maximize energy intake over the long term. In this case, additional protein to reduce hunger would be less important than increasing long-term energy intake by maximizing fat content and energy density of the ration.

• To reduce long-term negative energy balance, high-energy intake should be encouraged during the recovery periods. Thus, intake during recovery should consist of energy-dense foods with minimal effects on satiety (i.e., high-fat, low-protein foods).

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R. J. Jandacek, University of Cincinnati

The objective of this paper is to address the question of whether structured lipids offer advantages as a source of energy for hypocaloric, high-energy expenditure stress conditions of short-term combat operations (repetitive three- to seven-day missions with recovery periods of one to three days). A review of structured lipids and their metabolism is followed by a discussion of the question provided and the recommendation.

Virtually all of the fat that we consume is in the form of triacylglcyerols, three long-chain fatty acids bonded to glycerol. The chain length of most dietary fatty acids is 16 and 18 carbon atoms.

It was found by Rubner (1885) and Atwater and Bryant (1900) that the energy in food that is available to support metabolic and other activity is equivalent to that produced by oxidation of the carbon and hydrogen atoms of the compounds in food macronutrients. In a bomb calorimeter, the oxidation of carbohydrates generates 4 kcal/g (16.7 kJ/g). The oxidation of fatty acids with 18-carbon chains yields 9.5 kcal/g (39.7 kJ/g). Fatty acids of shorter chain length contain a higher fraction of carbon atoms bonded to oxygen and therefore give off less energy when oxidized. Heat produced by the oxidation of octanoic acid is 8 kcal/g (33.4 kJ/g).

Although we have understood this concept for a century, the equivalence of the bomb calorimeter and the human body is a remarkable discovery. The β-oxidation of palmitic acid that produces acetyl CoA and carbon dioxide (CO₂) via the TCA (tricarboxylic acid) cycle provides the same amount of heat and work as the bomb calorimeter. The sum of the reactions in the body is the same as that in the bomb calorimeter: fat plus oxygen produces heat, CO₂, and water.

The chemical energy contained in the C-C and C-H bonds of fatty acids is the densest source of energy available in foods, where C is carbon and H is hydrogen. The energy of ingested fat is stored if total caloric intake exceeds energy expenditure, or it is used to meet energy needs. The sections that follow briefly review the types of dietary fat and the unique properties of fats made with medium-chain fatty acids.

Dietary fat comprises triacylglycerols, phospholipids, and sterols. Phospholipids and sterols are important in health, but triacylglycerols provide essentially all of the energy in dietary lipids.

A triacylglycerol molecule contains an asymmetric carbon atom (carbon 2 of the glycerol) if the fatty acids in the 1 and 3 positions are different. Fatty acid positions in the 1 and 3 positions are hydrolyzed by pancreatic lipase. The chemical structure of a triacylglycerol molecule (trilaurin) is shown in Figure B-15.

Figure B-16 shows dietary fatty acids in animal and vegetable triacylglycerols. The long-chain fatty acids account for a majority of the fat consumed by people. Docosahexaenoic acid is found in fatty fish such as salmon and tuna.

In addition to these long-chain fatty acids in common foods, small quantities of shorter fatty acids are part of the triacylglycerols of butterfat. These fatty acids include butyric, hexanoic (caproic), octanoic (caprylic), decanoic (capric), and dodecanoic (lauric) acids. Octanoic and decanoic acids make up approximately 4 percent of butterfat fatty acids.

Octanoic and decanoic acids account for approximately 13 percent of the fatty acids in coconut oil. They became commercially available as byproducts of coconut oil fractionation to obtain lauric acid, an ingredient for detergent products. These byproducts made it possible to synthesize medium-chain fatty acid triacylglycerols (MCT, MCT oil).

FIGURE B-15 A triacylglycerol, trilaurin (C₃₉H₇₄O₆).

FIGURE B-16 Principal long-chain fatty acids found in dietary fat. Octanoic acid is a medium-chain fatty acid that is a principal component of structured lipids.

Synthetic triacylglycerols were also made from mixtures of long-chain and medium-chain fatty acids; these esters were termed “structured lipids,” even though the fatty acid distribution in the three positions of the glycerol was completely random and unstructured. More recently, enzymatic techniques have made it possible to synthesize triacylglycerols with medium-chain fatty acids in the 1 and 3 positions, and long-chain fatty acids in the 2 position.

MCT oil was found to have therapeutic advantages in cases of pancreatic insufficiency because its intestinal hydrolysis is more rapid than that of long-chain fats. MCT oil is absorbed from the intestine in subjects with subnormal pancreatic lipase, such as patients with cystic fibrosis. The hydrolysis products are transported via the portal vein rather than via the lymphatic route. MCT does not provide the essential fatty acids linoleic and α-linolenic acids.

Structured lipids were proposed to have benefits in providing energy to patients who were not able to consume food through the gastrointestinal tract and therefore required intravenous nutritional support (i.e., total parenteral nutrition, TPN). The provision of intravenous energy has successfully used emulsions of fat in small particles. It was found that these particles in blood circulation acquire surface lipoproteins (e.g., apolipoprotein C-II, C-III, E) from high-density lipoproteins. The lipid is hydrolyzed by endothelial lipoprotein lipase and the lipolytic products are used by peripheral tissues.

Medium-chain fatty acids are rapidly hydrolyzed from triacylglycerol and do not require carnitine for tissue uptake; however, acidosis can result from this high rate of hydrolysis. For this reason, physical mixtures of MCTs or structured lipids with medium-chain fatty acids and long-chain fatty acids (including essential fatty acids) bonded to the same glycerol molecule may have advantages for TPN compared with long-chain triacylglycerols (Bellantone et al., 1999; Rubin et al., 2000). Some reported advantages of structured lipids in TPN were summarized previously (Jandacek, 1994).

In addition to use in TPN, another hypothetical nutritional advantage for medium-chain fatty acids (and therefore for structured lipids) was explored. This hypothesis suggests that the rapid absorption of medium-chain fatty acids via the portal vein to the liver results in rapid mitochondrial oxidation of these acids that can then reduce the body’s use of glycogen as a fuel. It was also suggested that the use of MCTs in place of carbohydrate would reduce insulin elevation and hypoglycemia. As reviewed previously (Jandacek, 1994), studies did not support these hypotheses in human exercise trials, and a more recent trial also found no performance improvement with a specific structured lipid (Vistisen et al., 2003).

A further refinement to structured lipids was the synthesis of “truly structured” lipids, in which the positions of the medium- and long-chain fatty acids were specific rather than random. The advantage of this kind of structure is that the placement of the medium-chain fatty acids in the exterior 1 and 3 positions would result in their rapid lipase-catalyzed hydrolysis (Jandacek et al., 1987). Specific position structured lipids would be capable of providing essential fatty acids (in the 2 position) with rapidly hydrolyzed octanoic or decanoic acid in the

1 and 3 positions. This kind of molecule could therefore be advantageous in providing fat in patients with pancreatic insufficiency.

The isomerization of monoacylglycerols may affect the metabolism of structured lipids. The preferred (low energy) form of monoacylglycerols is the 1(3)-monoacylglycerol. Isomerization of the 2-monoacylglycerol to the 1(3) isomer is accelerated by heat is rapid for short- and medium-chain fatty acids and for long-chain polyunsaturated fatty acids. It is likely that a significant fraction of 2-monoacylglycerols of medium-chain fatty acids formed in the intestine is isomerized (and then hydrolyzed) within the time frame of intestinal transit. A comparison of the absorption of long-chain fatty acid triacylglycerols, MCTs, and structured lipids is shown in Figure B-17. The structured lipid is shown as a “specific” triacylglycerol.

Based on the physical properties and metabolism of structured fatty acids, three areas of discussion address the question of whether or not structured lipids have any of the following advantages in energy deficit status during high stress circunstances: (1) intestinal absorption, (2) energy content, (3) energy utilization, and (4) appetite.

Current data indicate that there is no advantage in the absorption of medium-chain fatty acids in structured lipids, as long as the subjects have normal levels of pancreatic lipase. There is no need to optimize the hydrolysis rate in the small intestine of normal healthy individuals. There is a 20-fold excess capacity for the absorption of fat, suggesting that there are more than adequate levels of lipase, bile salts, enterocyte capacity, and chylomicron formation. Evidence for this is supported by the work of Kinsell and colleagues (1953). They fed vegetable oil as the entire diet to subjects for a week and observed not only that there were no ill effects, but also that there were reductions in serum cholesterol. Work by Kasper (1970) found that when dietary fat was raised to three times the normal consumption at a level of 300 g/day, the body was able to compensate, and this level of fat was well absorbed. He then pushed the system further with a diet of 639 g fat/day. This amount also was well tolerated by a subject during a 20-day trial, further confirming that normal humans have an excess capacity for the absorption of fat. These results negate the need to optimize the hydrolysis rate in the small intestine of healthy individuals. Furthermore, there is no evidence that subjects stressed by several days of caloric deficit will absorb less than normal levels of dietary fat. The use of a fat that is hydrolyzed rapidly will therefore not enhance caloric use relative to normal, well-absorbed, long-chain fats in people with normal pancreatic lipase levels.

As discussed above, the maximum energy content of macronutrients available to a person is the heat of combustion. For long-chain fats this value is 9.5 kcal (39.7 kJ)/g. The caloric energy of the fatty acids is dependent on chain length, and the energy that can be used from octanoic acid is 8 kcal (33.5 kJ)/g. Although the difference in caloric density of long-chain and medium-chain fatty acids is small, it seems prudent to maximize the energy provided per unit weight of the food provided in anticipated caloric deprivation.

The energy provided by macronutrient metabolism results in storage, work, or heat. In the case of excessive caloric intake, a portion of the energy is directed toward storage, principally in the form of triacylglycerol fatty acids in adipose tissue. In negative caloric balance, ingested energy is converted to heat and work. In a situation of energy stress in a high-temperature environment, it would be desirable to maximize ingested energy as work (ATP production).

A study of high relevance to this topic was reported by Bendixen and coworkers (2002). They compared four types of triacylglycerol fats in 11 normal, healthy men ranging in age from 22 to 28 years. The fats included a conventional long-chain triacylglcyerol; a positionally specific structured fat (octanoic acid in the 1(3) position); a randomly structured lipid; and a mixture of MCT with long-chain triacylglycerols. All three fats that included medium-chain fatty acids resulted in higher postprandial energy expenditure than did the long-chain dietary fat. This result is consistent with rapid absorption of medium-chain fatty acids via the portal vein and, because elongation is not favored, they are directed toward mitochondrial oxidation. If this oxidation is not entirely coupled to the production of ATP (e.g., peroxisomal oxidation) then the result would be a negative energy balance. In this study there was no difference among fats in subjective appetite measures or ad libitum energy consumption. Total energy expenditure was smaller after the conventional fat meal, relative to the other fats. Diet-induced thermogenesis was lower after the conventional fat than after the random structured lipid. In the 5-hour postprandial period there was a (nonsignificant) trend toward lower oxidation of fat from the long-chain fat (1.65 g/5 h versus 3.1–3.5 g/5 h), and a trend toward higher carbohydrate oxidation in this group (13.9 versus 11.1–13.1 g/5 h). The authors concluded that “structured fats do not change short-term postprandial appetite sensations or ad libitum energy intakes, but do result in higher postprandial energy expenditure than do conventional fats and hence promote negative energy and fat balance” (Bendixen et al., 2002).

During hypocaloric stress it is possible that a nutrient that provides satiety would be advantageous. There was no difference in the satiating effect of the different fats in the Bendixen study in terms of subjective tests and in terms of ad libitum caloric intake (Bendixen et al., 2002). However, in some reports long-chain fatty acids have been reported to be more satiating than medium-chain fatty acids (Cox et al., 2004; Feltrin et al., 2004).

There is no reason to substitute structured lipids for long-chain fatty acid triacylglycerols to meet the needs of stress resulting from high energy expenditure and low energy intake. Maximizing caloric density is the optimal approach. During a relatively short duration of five to ten days, essential fatty acids are not limiting factors. In terms of the fat composition, triacylglycerols that are oxidatively stable, high in energy density, and readily digested are recommended. Oils high in oleic acid and low in polyunsaturated acids (e.g., high oleic oils from cultivars of sunflower and safflower oils) meet these criteria.

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Bendixen H, Flint A, Raben A, Hoy CE, Mu H, Xu X, Bartels EM, Astrup A. 2002. Effect of 3 modified fats and a convential fat on appetite, energy intake, energy expenditure, and substrate oxidation in healthy men. Am J Clin Nutr 75(1):47–56.

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L. John Hoffer, Jewish General Hospital

The goal of this workshop is to advise the military in developing a hypocaloric ration that maximizes physical and mental performance. As currently envisioned, rations of 2,400 kcal per day will be consumed by soldiers expending approximately 4,000 to 4,500 kcal per day for three to seven days followed by one to three days of recovery. What is the optimum protein content of such a ration? Should the energy deficit be minimized, or are other aspects of the ration more important?

The main concerns when a person’s energy expenditure consistently exceeds intake—that is, when he or she is starving—are depletion of the fat store and loss of muscle mass and function. The 32 young men who participated in the famous Minnesota human starvation experiment (Keys et al., 1950) consumed approximately 1,500 kcal per day and, during the subsequent 26 weeks, they lost approximately 25 percent of their lean tissue mass. This occurred despite their consumption of 50 g of protein per day, an amount that exceeded the average protein requirement of 0.6 g/kg of body weight and was close to the current Recommended Dietary Allowance (RDA) of 0.8 g/kg (IOM, 2002). By the 24th week of the study, physiologic adaptation had restored energy and nitrogen equilibrium despite continuing starvation. This adaptation is crucial for survival during starvation (Hoffer, 1999a, b).

The Minnesota experiment illustrates what has long been known (Elwyn et al., 1979; Munro, 1964; Pellett and Young, 1992) and recently reemphasized (IOM, 2002; Millward, 2004; Tipton and Wolfe, 2004): starvation induces body protein loss. For a variety of reasons analyzed earlier by the Committee on Military Nutrition Research (CMNR) (IOM, 1995), soldiers in a stressful, high-energy-expenditure environment typically fail to increase their energy intake enough to match their energy expenditure. This situation fits the definition of starvation, and in keeping with its cardinal features, these soldiers lose fat and lean tissue mass. Their physiologic state appears to be the same as that of starvation that is induced simply by low food consumption. Thus, despite ample carbo-

hydrate intake, circulating concentrations of insulin-like growth factor-1 and 3,5,3′-triiodothyronine are decreased as occurs in conventional starvation, and they increase when the energy gap is narrowed, even if there is no other change in the stressful environment (Friedl et al., 2000).

Carbon oxidation always equals energy expenditure, and when energy expenditure exceeds food energy consumption, the body draws on endogenous fat, its chief energy store. Fat loss is therefore an essential feature of starvation. But the situation with regard to protein loss is unclear. Why does it occur? How avoidable is it? Factors that affect its magnitude are enumerated below.

Mineral deficiencies, particularly those of potassium (Rudman et al., 1975), phosphorus (Rudman et al., 1975), zinc (Khanum et al., 1988; Wolman et al., 1979), and, presumably, magnesium, impair the normal protein-sparing adaptation to starvation.

Tissue injury, inflammation, and systemic infection reverse the physiologic adaptation to starvation and increase body nitrogen loss (Hoffer, 1999b).

This phenomenon is illustrated by a study in which male volunteers with a body mass index (BMI) of 24.5 kg/m² participated in an 8-week US Army Ranger course (Friedl, 1997; Friedl et al., 2000). The program consisted of four periods of an initial several days of ad libitum feeding followed by seven to ten days of food restriction in a setting of daily energy expenditures of 4,000 to 4,500 kcal, thermal stress, and sleep deprivation. In the first of two studies, food intake was restricted to 1,400 kcal, with 52 g of protein per day (similar to the Minnesota study). In the second study, supplemental food provided an additional 400 kcal and 15 g of protein. In both experiences food intake during the brief recovery periods did not fully compensate for the deficits incurred during the restriction periods. The greater intake of energy (but also of protein; see below) by the second group produced marked benefits. In particular, the better-fed group experienced less weight loss and their percentage of fat-free mass (FFM) was significantly greater at the end of the study (Friedl et al., 2000).

Some experts claim that very obese, starving people lose body nitrogen more slowly (and have a slower rate of nitroten loss as a fraction of total weight

loss) than starving people of normal weight (Elia et al., 1999; Van Itallie and Yang, 1977). Since severely obese people invariably lose FFM during therapeutic starvation, it would seem that starving, nonobese soldiers must inevitably experience FFM loss. It should be borne in mind, however, that severe obesity increases the lean tissue compartment (Drenick, 1975; Henry et al., 1986), and at least some of the lean tissue loss during therapeutic starvation occurs simply because a smaller body requires less muscle to be lifted and moved. From this perspective, normal-weight or only mildly obese people may actually conserve body protein more effectively than severely obese ones during starvation.

It is certainly true that very obese people tolerate starvation with a greater sense of well-being and survive it for longer time. Adults of normal weight die after fasting for approximately 2 months, whereas severely obese people have survived fasts lasting many months (Barnard et al., 1969; Thomson et al., 1966). The longest monitored fast on record was by a 27-year-old man who initially weighed 207 kg and survived 382 days of uninterrupted fasting (Stewart and Fleming, 1973). Friedl and colleages (1994) cite a description of the starvation that occurred among the British forces during the Turkish siege of Kut from December 1915 to April 1916. Soldiers who began with superabundant fat stores survived, whereas those who began with a smaller fat reserve soon died in the cold winter climate (Hehir, 1922).

A study by Friedl and colleagues (1994) provides important insight into this phenomenon. The body composition of 55 men was determined before and after their successful completion of an 8-week US Army Ranger course in which energy intake was unusually low (1,300 kcal per day during the restriction periods). Body fat was an average of 14.3 percent at the start and decreased to an average of 5.8 percent at the end of the course. The remarkable finding was that, during progressive starvation, body fat stabilized at a minimum of 5 percent. The men who reached this limit continued to lose weight, but the source of the weight loss was now FFM. This observation suggests that 5 percent body fat represents a biological limit that is essential for successful adaptation to starvation. US Army data reviewed by Friedl (1995) suggest the contribution of lean tissue loss to total weight loss increases gradually as body fat falls below 10 percent. Nevertheless, the 5 percent limit appears to represent a “metabolic floor” that also approximately coincides with the psychological limit of voluntary participation (Friedl, 1995). As long as body fat remains above this critical level, a high-protein intake can spare body protein, but once it falls below it, protein-sparing is no longer possible. Obese people therefore survive prolonged starvation longer than lean ones because it takes longer to deplete their fat store to the critical level below which protein catabolism accelerates and disability becomes marked.

Comparison has been made between the Minnesota study and modern calorie-restriction studies like the Biosphere 2 study which involved normal-weight individuals (Heilbronn and Ravussin, 2003). This comparison is complicated by the fact that the average BMI of the Minnesota volunteers was only 21.4 when

they embarked on their starvation regimen. Thus, even before they began to starve, the Minnesota volunteers had BMIs comparable to modern adults who would be considered calorie restricted. The BMIs of most fit young men of the 21st century typically range from 23 to 25. The crucial determinant of well-being and physical function is more likely to be the absolute lean tissue mass that exists for a given body structure than a percentage reduction. At the end of the starvation phase of the Minnesota study, the average BMI had fallen to 16.3; this was associated with a severity of fat and lean tissue depletion that was incompatible with normal physiologic function. Had the baseline BMI of the Minnesota volunteers been greater, their final BMI would presumably have been closer to the range reported in modern calorie-restriction experiences. Taken together, these considerations suggest that elite soldiers being considered for extended hypocaloric field maneuvers should have normal fat and muscle stores as indicated by a normal physical examination, a BMI not less than approximately 23, and body fat not less than an appropriate minimum, such as 15 percent.

While it is true that energy deficiency worsens nitrogen balance, it is also true that an increase in protein intake improves nitrogen balance over a wide range of energy intakes from deficient to maintenance (Munro, 1964; Shaw et al., 1983). It was not at first appreciated that a high protein intake protects the lean tissue store during starvation because the early studies were of short duration. Short-duration studies are confounded by a transient loss of body nitrogen, called “labile protein,” that occurs immediately after energy (or protein) intake is reduced, and by the failure to allow sufficient time for physiologic adaptation to the new diet. When nitrogen balance studies are carried out long enough for the transient effect of labile protein loss to end and metabolic adaptation to take effect—a process that requires several days (Hoffer, 1999a, b)—high protein intakes are protein sparing in many energy-deficient states (Hoffer, 2003).

The protein-sparing effect of increased dietary protein is not necessarily limited to obese persons. In one study, nonobese men were calorie restricted for 10 weeks while consuming 93 g of protein per day. The men lost 7.4 kg (BMI fell from 24.9 to 22.6), 83 percent of which was fat (Velthuis-te Wierik et al., 1995). This is the composition of adipose tissue, which is approximately 85 percent fat and 15 percent FFM (Garrow, 1982; Grande and Keys 1980; Waki et al., 1991). In the Biosphere 2 experiment, eight normal men and women starved for 6 months, then remained in energy equilibrium for 18 months during which they consumed 2,200 kcal per day including 82 g of protein (Walford et al., 2002; Weyer et al., 2000). The men’s BMI decreased from 23.7 to 19.3 and the women’s from 21.2 to 18.5 (Walford et al., 2002). In the five persons in whom it was measured, body fat fell to 10 percent (significantly less than the 20 percent body fat in a matched normal comparison group), but their FFM was normal

(Weyer et al., 2000). Several studies in the obesity field have demonstrated zero nitrogen balance in normally active, moderately obese people adhering to very low energy diets supplying 1.5 g of protein per kg of ideal body weight per day (Gelfand and Hendler, 1989; Piatti et al., 1994). The proposition that lean tissues need not be lost during starvation is further supported by data from military trainees who lost body fat (i.e., starved) during basic training without food restriction. In one study, moderately obese female army trainees lost 2.2 kg of fat but simultaneously gained 1.7 kg of FFM (Friedl, 1995). In a study of obese male army recruits, basic training was associated with an average of loss of 12.5 kg within the first 3 months, virtually all of it as fat (Lee et al., 1994). Protein intakes in all these studies were substantially greater than in the Minnesota study and in published US Army Ranger field studies. One may conclude that important protein sparing may well be achievable in starving, normal-weight soldiers by increasing the protein content of their rations.

Another issue to be considered is whether the high level of physical activity required during maneuvers increases the protein requirement. Sports experts advise athletes to consume approximately 1.5 g of protein per kg of body weight every day. This is nearly twice the RDA (IOM, 2002) and nearly three times the average minimum requirement (Fielding and Parkington, 2002; Tipton and Wolfe, 2004). Could the increased protein requirement incurred by exercise add to the high-protein requirement induced by starvation? This issue was addressed by the CMNR (IOM, 1999), who found there was insufficient evidence to conclude that high-level physical activity increases the normal protein requirement. More recent reviews have come to the same conclusion (Fielding and Parkington, 2002; Tipton and Wolfe, 2004). Since the increased food intake necessary to meet a high-energy requirement automatically increases protein intake, the most cogent reason for advising athletes to consume a lot of protein is that this is what they naturally do.

In summary, lean tissues can be conserved during starvation by four mechanisms: (1) the only modest adipose tissue unloading—and hence less absolute weight loss and less disuse muscle atrophy—that occurs when baseline fat stores are normal or only moderately increased; (2) a high, or at least maintained, level of physical activity (Ballor and Poehlman 1994; Prentice et al., 1991); (3) the prevention of a severe depletion of the fat reserve; and (4) substantially greater protein intake than in the Minnesota experiment. Despite the common assumption that protein wasting is unavoidable in the presence of energy deficiency (IOM, 1995), there are good reasons to predict that the lean tissue stores of soldiers in the field can in fact be largely, if not completely, protected by increasing their protein intake. The daily ration currently under consideration provides 2,400 kcal. If, like other US Army rations (Cline and Warber, 1999), 15 percent of the energy is from protein, this ration will provide 90 g of protein per day, or 1.15 g of protein per kilogram of body weight for the average 78 kg US male soldier (IOM, 1999). This may be sufficient to prevent starvation-induced

lean tissue loss. Indeed, US Army Ranger course participants who consumed considerably less than 90 g/day suffered only modest losses of FFM and their physical performance appeared to be maintained (Friedl, 1995, 1997). In the Ranger study described earlier, in which daily energy and protein intakes during restriction periods were 1,800 kcal and 67 g of protein, respectively, FFM decreased by 6 percent or 4 kg (Friedl et al., 2000). Upper arm muscle cross-sectional area decreased from 68 to 60 cm², but 60 cm² remains at the upper 85th percentile for normal age-matched men. Will 90 g of protein per day prevent even these losses? Would 120 g of protein per day (1.5 g of protein per kg) be even more effective? This larger amount of protein would be provided by a 2,400 kcal ration with 20 percent of energy from protein and would conform to the current expert recommendation of 1.5 g/kg for athletes (Fielding and Parkington, 2002; Tipton and Wolfe, 2004). Although 120 g of protein per day seems to exceed the military protein RDA (MRDA) of 100 g per day, first established in 1947, it actually does not. In 1947 the average male soldier weighed only 68 kg (IOM, 1999); the original MRDA was therefore equivalent to a protein intake of 1.5 g/kg of body weight.

Potential drawbacks to a high-protein diet include unpalatability, early satiety, and increased obligatory urine volume to eliminate the additional urea osmoles (Friedl, 1999). However, an increase of protein intake from 90 to 120 g per day would not increase obligatory urine volume because urea is an “ineffective osmole” (Kamel et al., 2004). With regard to satiety and palatability, it is worth recalling that protein comprised 30 to 35 percent of the daily energy intake of paleolithic humans. This is equivalent to 2.5 to 3.5 g/kg (Eaton and Cordain, 1997; Eaton et al., 1996). It seems very likely that a palatable diet providing a “mere” 1.5 g/kg of protein could be devised.

If soldiers are required to starve for only three to seven days before refeeding, it does not matter how much protein they consume, and the design of the ration should focus on features such as palatability. Field studies do show, however, that ad libitum feeding over the few days following seven to ten days of food restriction is insufficient to make up the energy deficit incurred, so soldiers returning too quickly to the field will experience progressive starvation (Friedl et al., 1994). It is also possible that a highly successful ration could be put to use for longer periods than initially planned for. The following conclusions and suggestions are offered with these possibilities in mind.

Contrary to what is commonly assumed, it is very likely that the lean tissue store of normal-weight persons can be largely conserved during starvation through a combination of a high-protein intake, physical activity, and avoidance of severe body fat loss. This hypothesis has not been tested in a field situation. The prediction is that a hypocaloric ration providing 2,400 kcal and 90 g of

protein per day will spare the lean tissue store of soldiers on extended stressful maneuvers. It would be interesting and useful to determine whether a ration providing 2,400 kcal and 120 g of protein is even more effective, as well as practical and palatable. The protein-sparing effect of high-protein intakes will not be demonstrable unless balance studies are long enough to allow for metabolic adaptation.

The energy deficit should be minimized. Protein sparing is only possible when body fat is above a minimum of approximately 5 percent of body weight. Energy-deficient states are psychologically very unpleasant and appear to be increasingly so as the lower fat limit is approached (Friedl, 1997). The psychological unpleasantness of hypocaloric rations may well be their most debilitating short-term feature (Keys et al., 1950). As has already been pointed out (Friedl, 1995; Friedl et al., 1994), it is important, when selecting elite soldiers for stressful missions, to consider their starting body composition. Under starvation conditions, very lean and muscular does not translate into better.

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Maret G. Traber, Oregon State University

Angela Mastaloudis, Pharmanex

This paper attempts to address the effects of exercise on oxidative stress and immune function and whether increasing the intake of antioxidants would reduce this stress, first in energy balance conditions and then in energy deficit conditions. Findings from our studies in ultramarathon runners may help answer this and the specific following questions:

1. What are the types and levels of direct antioxidants (e.g., vitamins C and E, carotenoids) that could be added to rations for short-term use by soldiers during high-tempo, stressful, repetitive combat missions to enhance performance and/or improve recovery during combat missions?

2. Would certain nonvitamin antioxidants help performance?

3. What is the impact of exercise on oxidative stress and immune function? Will increasing the intake of antioxidants reduce this stress in energy balance conditions and then in energy deficit conditions?

4. Is there any concern with megadoses of antioxidants—should soldiers be already taking supplements? For example, could megadoses of antioxidants negatively affect performance or adaptation?

The human body continuously produces reactive oxygen species (ROS) as a result of normal metabolism in the mitochondria (Halliwell and Gutteridge, 1999). ROS are an unavoidable but necessary byproduct of cellular respiration. ROS also have a beneficial role in that leukocytes use radicals to help kill bacteria. This action produces a large increase in oxygen use, called a “respiratory burst,” to catalyze hydrogen peroxide with chloride ions to create a strongly antiseptic hypochlorite ion. Unfortunately, hypochlorite is also a strong oxidizing agent and can produce free radicals.

In response to endurance exercise, the body’s oxygen consumption can increase 10 to 20 times (Åstrand and Rodahl, 1986), while skeletal muscle oxygen consumption can increase 100 to 200 times (Halliwell and Gutteridge, 1999). This increased oxygen consumption may produce ROS in amounts that exceed the body’s antioxidant supplies. Clearly, exercise can cause oxidative stress resulting in lipid peroxidation (Alessio, 2000; Child et al., 1998; Duthie et al., 1990; Hessel et al., 2000; Marzatico et al., 1997; Mastaloudis et al., 2001; Rokitzki et al., 1994), DNA damage (Hartmann and Niess, 2000), and, possibly, protein oxidation (Alessio, 2000; Tirosh and Reznick, 2000).

Electrons “leaking” from the mitochondria during exercise are considered a main source of oxidative stress (Halliwell and Gutteridge, 1999). Other potential sources of ROS during exercise include enhanced purine oxidation, damage to iron-containing proteins, disruption of Ca²⁺ homeostasis (Jackson, 2000), and NADPH oxidase (Hessel et al., 2000). These exercise-induced ROS are also thought to modulate acute phase inflammatory responses (Cannon and Blumberg, 2000).

We found that during an ultramarathon race (32-mile forest trail through hilly terrain), as compared with a sedentary trial, deuterium-labeled vitamin E disappeared from the plasma faster (disappearance rates of 2.8 × 10^–4 versus 2.3 × 10^–4, p < 0.03) and lipid peroxidation increased (75 ± 7 pg/ml at prerace to 131 ± 17 at postrace (p < 0.02) (Mastaloudis et al., 2001). Lipid peroxidation

was assessed by measuring plasma F₂-isoprostanes (F₂-IsoPs), prostaglandin-like compounds produced by free-radical catalyzed lipid peroxidation of arachidonic acid (20:4 n-6, a long-chain polyunsaturated fatty acid) (Morrow et al., 1990). F₂-IsoPs are widely accepted as sensitive and reliable measures of in vivo lipid peroxidation (Roberts, 1997). Importantly, F₂-IsoPs have proatherogenic biological activity, including vasoconstriction and activation of platelet aggregation (Nieman et al., 2002; Roberts and Morrow, 2000). Moreover, they have been shown to recruit proatherogenic monocytes and induce monocyte adhesion (Leitinger et al., 2001). Thus, endurance exercise not only increases oxidative stress, but also increases a proatherogenic response.

Based on our findings that an ultramarathon race increases oxidative stress (Mastaloudis et al., 2001), we hypothesized that prior supplementation with antioxidants (vitamins C and E) would decrease oxidative stress during distance running (Mastaloudis, 2004; Mastaloudis et al., 2004a, b). If the antioxidant supplements decreased oxidative stress, they should decrease lipid peroxidation and inflammation, slow α-tocopherol use, decrease DNA damage, decrease muscle damage, and improve recovery. To test these hypotheses, we carried out a randomized, double-blind study in ultramarathon runners (n = 11 women, 11 men) who consumed either (1) antioxidants (AO) [1,000 mg vitamin C (500 mg twice daily) and 300 mg vitamin E (400 IU RRR-α-tocopheryl acetate)] or (2) matching placebos (PL) for seven weeks (six weeks before through one week after the race). The race was a 50 km (32 mile) ultramarathon that took place in the hills of Corvallis, Oregon. The study design is shown in Figure B-18.

Subjects were approximately 40 years of age and were recreationally trained endurance runners. Complete descriptions of the subjects have been published (Mastaloudis, 2004; Mastaloudis et al., 2004b). Plasma α-tocopherol and ascorbic acid concentrations were similar in the two groups before supplementation (Mastaloudis, 2004). Following six weeks of supplementation, the PL-group plasma concentrations were unchanged. In contrast, the AO-group α-tocopherol plasma concentrations increased from 28 ± 2 to 45 ± 3 µM (p < 0.0001) and were higher than in the PL group (p < 0.0007). Similarly, the AO group had a higher ascorbic acid plasma concentration, 121 ± 9 µM, than did the PL group, 78 ± 9 µM (p < 0.0007) following supplementation. Note that in both the PL and AO groups the ascorbic acid concentrations are well into the range for repleted subjects (Levine et al., 1996, 2001).

All subjects completed the race. Run times and intensity were similar among

FIGURE B-18 Study Design. Subjects (n = 22) were randomly assigned in a double-blind fashion to one of two groups: (1) PL [(1,000 mg of citric acid (500 mg twice daily) and 300 mg of soybean oil] or (2) AO [1,000 mg ascorbic acid (500 mg twice daily) and 300 mg RRR-α-tocopheryl acetate]. Blood samples were obtained before supplementation (baseline); after three weeks of supplementation (compliance); 24, 12, and 1 hours before the race. Samples were also taken at mid-race at kilometer 27 (~ 5 h), immediately postrace, 2 h postrace (approximately 10 h), and daily for six days postrace (1–6 days, 24–144 h). All samples were fasting morning blood draws except 12 h, mid-, post-, and two h post-race.

NOTE: AO = antioxidant; PL = placebo.

SOURCE: Summarized from Mastaloudis (2004); Mastaloudis et al. (2004a), used with permission from Elsevier.

treatment groups and genders: 7.1 ± 0.2 h at a pace of 13.7 ± 0.4 minutes per mile and a heart rate of 146 ± 2 beats per minute. Energy expenditure was calculated based on the average heart rate during the run and the corresponding oxygen consumption (VO₂), multiplied by the time it took each subject to finish the race (Mastaloudis et al., 2004b). Energy expenditure was approximately 7,000 kcal for men and 5,000 kcal for women; both consumed about 2,000 kcal on race day and were in caloric deficit (Table B-6).

Vitamins C and E intakes from foods consumed during race day were compiled. During the run vitamin C intake was < 50 mg for most subjects, and vitamin E intake was < 5 mg.

Plasma F₂-isoprostanes (F₂-IsoP) concentrations increased in the PL group in response to the race, but prior supplementation with vitamins C and E completely suppressed the increase in the AO group (Figure B-19) (Mastaloudis et al., 2004a). At postrace, when oxidative stress was maximal, F₂-IsoP concentrations were inversely correlated with both the ratio for α-tocopherol:lipids (R = −0.61, p < 0.003) and with ascorbic acid (R = −0.41, p = 0.05) (Mastaloudis et al., 2004a), providing further documentation that antioxidants were responsible for preventing lipid peroxidation.

Both men and women in the PL group responded to the run with similar F₂-IsoP concentration increases (Mastaloudis et al., 2004a). However, men’s and

FIGURE B-19 Antioxidant supplementation prevents the increase in lipid peroxidation as observed in ultramarathon runners. Plasma F₂-isoprostanes concentrations increased from pre- to postrace only in the placebo (PL) group (28 ± 2 to 41 ± 3 pg/ml; p < 0.01). Additionally, postrace F₂-isoprostanes concentrations were significantly higher in the PL group than in the antioxidant group (p < 0.001).

SOURCE: Mastaloudis et al. (2004a), used with permission from Elsevier.

women’s responses were markedly different during recovery. In PL women, F₂-IsoP concentrations returned to baseline within two hours postrace, while in PL men, higher F₂-IsoP concentrations persisted for the duration of the study (six days) (Mastaloudis et al., 2004a). This difference in oxidative stress in men and women has been observed previously. Healthy young men compared with age-matched women had greater concentrations of markers of oxidative stress (plasma TBARS [thiobarbituric acid reactive substances] and urinary 8-Iso-PGF₂). Following antioxidant supplementation (600 mg vitamin C and 300 mg vitamin E daily for 4 weeks), levels of lipid peroxidation markers were normalized to concentrations similar to those observed in the women (Ide et al., 2002). Thus, men in comparison with women are subjected to continued higher oxidative stress in the absence of antioxidant supplementation.

Very few studies have examined the effects of antioxidants on both exercise-induced oxidative stress and inflammation (Childs et al., 2001; Nieman et al., 2002). We found that AO supplementation had no effect on exercise-induced increases in tumor necrosis factor (TNF)-a, interleukin (IL)-6, C-reactive protein (CRP), or IL-1, despite the finding that increases in lipid peroxidation were prevented (Mastaloudis et al., 2004a). Similarly, ascorbic acid (1,500 mg/day) consumption for one week before an ultramarathon did not prevent exercise-induced increases in plasma F₂-IsoPs, lipid hydroperoxides, or IL-6 (proinflammatory cytokine) (Nieman et al., 2002). Postexercise supplementation with vitamin C (approximately 1,000 mg/day) and n-acetyl-cysteine for one week also had no effect on exercise-induced IL-6 increases (Childs et al., 2001). Army recruits that participated in an intensive 48-hour final military endurance exercise were also shown to have increased CRP, but the effect of antioxidants were not tested (Brull et al., 2004). In general, antioxidants do not modulate increases in cytokine concentrations in response to exercise.

The ultramarathon was a sufficiently strenuous exercise that, by mid-race, the runners exhibited DNA damage as assessed with the comet assay (a whole-cell electrophoresis assay that estimates DNA damage) (Mastaloudis et al., 2004b). However, the proportion of cells with DNA damage returned to baseline by the end of the race, declined below baseline values two days after the race, and remained low for six days after the race (Mastaloudis et al., 2004b). Both men and women within each treatment group had similar circulating AO levels, but the women had a higher proportion of DNA damage after the race. In addition, the women in the AO group were more protected, showing a decrease in the

proportion of DNA damage on the day following the ultramarathon race, while men experienced little benefit.

Overall, this exercise appeared to induce a temporary increase in DNA damage. This increase, however, has no apparent adverse effects and may be beneficial because it appears to induce the replacement of damaged cells.

Runners experienced muscle damage after the ultramarathon: deficits in maximal force production by the knee extensors and flexors were documented (Mastaloudis et al., in press). Prior supplementation with vitamins C and E did not prevent muscle damage or fatigue or improve recovery. The ultramarathon run may have been so damaging that it overwhelmed the protective effects of the antioxidants. For example, vitamin C was found to be protective in a more moderate exercise protocol (60 minutes of box-stepping exercise), in which supplementation enhanced the rate of recovery from maximal force deficit (Jakeman and Maxwell, 1993).

Plasma markers of muscle damage were increased by the endurance exercise in our study (Mastaloudis et al., in press) and were unaffected by AO supplementation. Both lactate dehydrogenase (LDH) and creatine kinase (CK) increased in response to the race; LDH peaked at postrace and CK reached maximal values 2 h and 1 day postrace; neither was affected by AO treatment. These observations are in agreement with others. There was no influence on increased CK concentrations in response to a 90 minute treadmill run by two weeks prior supplementation with 500 mg vitamin C and 400 mg vitamin E (Petersen et al., 2001). Our findings are in contrast, however, with other studies (Rokitzki et al., 1994) that reported prior supplementation with 200 mg vitamin C and 400 IU vitamin E for 4.5 weeks diminished increases in CK following a 90 km ultramarathon.

Our study also showed that vitamins C and E did not prevent LDH increases after distance running. However, daily supplementation with 1,200 IU α-tocopherol for four weeks prior to running diminished LDH increases following six successive days of running (Itoh et al., 2000), suggesting that a larger dose of vitamin E is required to reduce muscle damage resulting from endurance exercise. The results seem influenced not only by the level of exercise but also by the amount, duration, and type of supplemental AO.

Plasma ascorbic acid concentrations increased in both the AO and PL groups during the 50 km ultramarathon run, with significant increases at mid-race, and at postrace compared with levels measured prerace; levels returned to prerace values two hours after the race (Mastaloudis et al., 2004a, b). Increases in plasma

ascorbic acid in response to vigorous exercise have been reported in some (Duthie et al., 1990; Kaikkonen et al., 1998; Mastaloudis et al., 2001; Petersen et al., 2001; Rokitzki et al., 1994; Viguie et al., 1993), but not all (Meydani et al., 1993; Peters et al., 2001a, b) studies. Exercise-related increases in circulating cortisol has been suggested to promote efflux of ascorbic acid from the adrenal gland and the mobilization of ascorbic acid from other tissue sites such as leukocytes or erythrocytes (Gleeson et al., 1987). Similarly, some (Nieman et al., 2000; Peters et al., 2001a, b), but not all (Nieman et al., 2002), studies demonstrated that exercise-related increases in circulating cortisol diminish with vitamin C supplementation. Taken together, these findings suggest that oxidative stress may regulate cortisol secretion.

Plasma uric acid concentrations also increased in response to the run, consistent with the findings of others (Hellsten et al., 1997; Liu et al., 1999; Rokitzki et al., 1994), and the increase may be explained by enhanced purine oxidation resulting from exercise (Hellsten et al., 1997; Liu et al., 1999; Rokitzki et al., 1994).

Concurrent increases in plasma ascorbic and uric acids may reflect the body’s response to extreme exercise by enhancing AO defenses, including increased AO enzymes (Marzatico et al., 1997) and AO nutrients (Child et al., 1998; Rokitzki et al., 1994; Viguie et al., 1993).

Some studies investigating the effects of vitamin E supplementation on endurance runners have reported increases in plasma α-tocopherol concentrations in both the AO and the PL groups following exercise (Buchman et al., 1999; Rokitzki et al., 1994; Vasankari et al., 1997). We (Mastaloudis et al., 2004a) observed increased plasma α-tocopherol concentrations during exercise in the AO group only. Plasma tocopherols are transported entirely within lipoproteins and fluctuate with lipoprotein concentrations (Traber and Jialal, 2000) and after correcting α-tocopherol for lipids, no significant changes in α-tocopherol/lipid concentrations were observed in either group (Mastaloudis et al., 2004a). In the only other study to report both α-tocopherol and α-tocopherol/lipid concentrations (Buchman et al., 1999), fluctuations in lipoproteins explained the differential responses in the AO and PL groups. Thus, the increase in plasma α-tocopherol concentrations during the exercise may be a result of fluctuations in lipoprotein concentrations rather than an actual increase due to exercise.

Plasma lipids (total cholesterol plus triglycerides) increased during the race, but decreased to below prerace levels two hours after the race and remained low for three days (Figure B-20). These data suggest that extreme endurance exercise depletes lipid stores that subsequently remain depleted for several days. Rations should provide adequate fat content and total kcals to ensure that tissue stores of lipids are maintained for endurance and multi-day physical work in the field.

FIGURE B-20 Plasma lipids increase during the race but are depleted for three days postrace. No differences in plasma total lipids (total cholesterol plus triglycerides) were observed between genders or among treatment groups within each gender.

NOTE: *Compared with prerace levels, plasma total lipids were higher at mid-race (p < 0.004), but were lower two hours (p < 0.01), one day (p < 0.0001), two days (p < 0.0001), and three days (p < 0.01) postrace.

SOURCE: Adapted from Mastaloudis (2004), used with permission.

ROS generated in response to exercise cause oxidative damage (Mastaloudis et al., 2001, 2004a), stimulate an inflammatory response (Vassilakopoulos et al., 2003), and damage skeletal muscle (Cannon and Blumberg, 2000; Sjodin et al., 1990). Hypothetically, AO supplementation could prevent exercise-induced oxidative damage, inflammation, and muscle damage. We found, however, that while supplementation with vitamins C and E prevented increases in lipid peroxidation in response to endurance exercise (Mastaloudis et al., 2004a), they had no apparent effect on DNA damage (Mastaloudis et al., 2004b), inflammation (Mastaloudis et al., 2004a), or muscle damage (Mastaloudis et al., in press). These results suggest that the mechanism of oxidative damage is operating independently of the inflammatory and muscle damage responses (Nieman et al., 2002).

Preventing production and enhancing clearance of F₂-IsoPs may be more beneficial than preventing inflammation. F₂-IsoPs have demonstrated proatherogenic biological activity, including vasoconstriction and activation of platelet aggregation (Nieman et al., 2002; Roberts and Morrow, 2000). In addition, they are known to recruit proatherogenic monocytes and induce monocyte

adhesion (Leitinger et al., 2001). In contrast, the muscle damage-induced inflammatory response stimulates recovery from exercise by inducing regeneration of damaged tissue and recruitment of satellite cell proliferation (Malm, 2001). In our studies, AO supplementation proved to prevent the damaging increase in lipid peroxidation without influencing inflammation. This is especially important because preventing exercise-induced inflammation could inhibit muscular adaptation to physical activity, the so-called “training effect” of exercise.

Supplementation of both vitamins C and E appears beneficial in exercise. Certainly, the ultramarathon runners were adequately nourished with respect to vitamin C, but studies in cigarette smokers suggest that vitamin C is necessary to maintain vitamin E concentrations (Bruno et al., 2005). Prior supplementation with vitamin E alone may be possible, but the assault ration should contain vitamin C not only for its own benefits but also for maintaining vitamin E concentrations.

In healthy adults, there are no obvious adverse effects of either vitamin C or E supplements alone or in combination (Hathcock et al., 2005), and the Tolerable Upper Intake Levels are 2,000 and 1,000 mg, respectively (IOM, 2000). A recent meta-analysis assessed the combined results of 19 clinical trials of vitamin E supplementation for various diseases reported that patients who took supplements of 400 IU/day or more were 6 percent more likely to die from any cause than those who did not take vitamin E supplements (Miller et al., 2005). However, three other meta-analyses that combined the results of randomized controlled trials designed to evaluate the efficacy of vitamin E supplementation in cardiovascular disease found no evidence that vitamin E supplementation up to 800 IU/day significantly increased or decreased cardiovascular disease mortality or all-cause mortality (Eidelman et al., 2004; Shekelle et al., 2004; Vivekananthan et al., 2003). At present, there is no convincing evidence that vitamin E itself increases the risk of death from cardiovascular disease or other causes. Therefore, AO vitamin supplements could be added to assault rations to prevent the adverse increase in lipid peroxidation as described in the ultramarathon runners in our study (Mastaloudis et al., 2004a).

We thank the runners and the support from National Institute of Environmental Health Sciences Grant ES11536 and National Institutes of Health Grant DK59576. The following individuals provided supplements and ergogenic aids: Jim Clark, Cognis Health and Nutrition; Klaus Krämer, BASF; Tim Corliss, Clif Bar; Jeff Zachwieja, Gatorade.

The following individuals played key roles in our study: Dawn W. Hopkins, The Department of Exercise and Sport Science, Linus Pauling Institute, Oregon State University, Corvallis; Scott Leonard, Linus Pauling Institute, Oregon State University, Corvallis; David Yu, Linus Pauling Institute, Oregon State Univer-

sity, Corvallis; Robert P. O’Donnell, Statistics, Oregon State University, Corvallis; Roderick H. Dashwood, Linus Pauling Institute, Oregon State University, Corvallis; Balz Frei, Linus Pauling Institute, Oregon State University, Corvallis; Jason D. Morrow, Departments of Medicine and Pharmacology, Vanderbilt University School of Medicine, Nashville, Tennessee; and Sridevi Devaraj, Department of Pathology, the University of California Medical Center, Sacramento; Jeffrey J. Widrick, The Department of Exercise and Sport Science, Oregon State University, Corvallis.

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Henry C. Lukaski and James G. Penland, USDA-ARS Grand Forks Human Nutrition Research Center

Military personnel are exposed to environmental, physical, and mental stressors during combat and require adequate dietary intakes of energy, water, and micronutrients for optimal performance. During deployment, soldiers decrease food consumption up to 50 percent, resulting in a suboptimal intake of energy and micronutrients (Baker-Fulco, 1995). Thus, reduced food intake and increased losses of minerals during assault operations suggest the need to evaluate mineral nutrition of military personnel (Shippee, 1993).

Only male soldiers participate in first-strike assault operations. These missions occur for repetitive brief periods (three to seven days), followed by short recovery periods (one to three days) that can last for months. Under these circumstances, it is unlikely that such brief durations of reduced micronutrient intake will elicit severe mineral deficiencies. However, repeated bouts of first-strike assaults without adequate replenishment of minerals may predispose soldiers to a reduced mineral nutritional status and result in impaired physiological and psychological function and performance.

This review addresses the mineral needs of male soldiers. It does so by comparing the prevalence of inadequate mineral intakes of civilian and military men and summarizing the effects of restricted and supplemental mineral intakes on their performance. Additionally, it provides a strategy for increasing food and nutrient intake to promote optimal performance of the male combat soldier. Findings from studies of women with documented mineral depletion are described to highlight impairments in performance that would be applicable to men with similarly reduced mineral nutritional status.

The following are specific questions that this review attempts to answer:

• Which of the minerals might reach deficit levels, given the high-stress, high-intensity scenario? Given existing information that suggests that soldiers probably consume insufficient amounts of zinc during military

operations, and that they could become zinc deficient, are there potential effects on health or performance?

• What are the types and levels of cofactors in antioxidant and other biochemical reactions with high metabolic flux (e.g., zinc, manganese, copper, selenium, or others) that could be added to assault rations to enhance performance during combat missions? Does the presence of preexisting malnutrition make a difference?

• Is there any concern with taking megadoses of minerals; should soldiers be already taking supplements?

Estimating a group’s adequate intake of a nutrient is achieved through comparison with the Estimated Average Requirement (EAR). If an EAR is not available, then the Adequate Intake (AI) is used. The Recommended Dietary Allowance (RDA) is not used to assess the adequacy of nutrient intakes by groups (IOM, 2000a).

Epidemiological surveys using dietary recall reveal (NHANES III, Continuing Survey of Food Intake of Individuals, and US Food and Drug Administration Total Diet Study) that intakes of some minerals by the US population do not meet the Dietary Recommended Intake (DRI) recommendations. Among men ages 19 to 50 years, 50 percent did not meet the AI for calcium or the EAR for magnesium (Table B-7). Inadequate zinc intakes were found among 10 percent of men, but iron intakes generally met the EAR (6 mg) (IOM, 1997, 2000b, 2001).

Nutritional surveys reveal wide-ranging estimates of possible copper deficiency in the US population (IOM, 2001). Although findings of the NHANES III and Continuing Survey of Food Intake of Individuals showed no men with copper intakes less than the EAR, the US Food and Drug Administration Total Diet Study revealed that 25 percent of men consume less than the EAR for copper. Analyses of diets from ten multinational studies indicated that copper intakes were less than the EAR in 11 percent of the population (Klevay et al., 1993). Another study analyzed duplicate diets of randomly selected adults in Baltimore, Maryland, and found that 36 percent of the adults had dietary copper intakes less than the EAR (Pang et al., 2001).

Based on observation of the foods soldiers consume (Rose et al., 1987), soldiers frequently have inadequate intakes of certain minerals. Zinc and magne-

sium intakes of male marine engineers fed standard rations were less than the recommended amounts (Tharion et al., 2000). The addition of hot meals to standard rations, compared with provision of only standard rations, promoted adequate mineral intakes for the soldiers (Thomas et al., 1995). However, feeding a customized, high-carbohydrate diet, compared with standard rations, during training in a hot, humid environment decreased the proportion of elite male soldiers with inadequate intakes of calcium (50 versus 95 percent) but not magnesium (75 versus 75 percent) or zinc (20 versus 25 percent) (personal communication, S. Montain, USARIEM, August 9, 2004; Savannah Ranger Study, 1996). Male hospital personnel were studied during operational training to compare the effects of meal-based versus standard rations on the resulting adequacy of mineral intakes (Baker-Fulco et al., 2002). Compared with the standard ration, the high-carbohydrate, meal-based ration was associated with more soldiers consuming adequate calcium, similar percentages consuming adequate magnesium, but fewer consuming adequate zinc (Table B-8). Thus, magnesium, zinc, and calcium intake levels are limited in civilian and military men, and data on copper and selenium in soldiers are lacking.

Mineral intakes affect human biological functions. Controlled studies of restriction and supplementation of mineral intakes reveal deficits and enhance-

ments, respectively, in measures of physiological and psychological function and performance.

Zinc is required for the structure and activity of more than 300 enzymes (Vallee and Falchuk, 1993). Because zinc functions in all physiological systems, adequate zinc status is needed for optimal physiological and psychological performance.

Low zinc status impairs muscle and cardiorespiratory functions (Table B-9). Adolescent gymnasts with decreased serum zinc concentrations, compared with age-matched, nonathletic controls, experienced reduced muscle strength (Brun et al., 1995). Male athletes with low, in contrast with normal, serum zinc concentrations had decreased power output (physical work capacity, watts) and increased blood lactate concentrations during peak exercise tests (Khaled et al., 1997).

Controlled feeding studies with low zinc intakes show adverse physiological function. Men fed severely zinc deficient diet (< 1 versus 12 mg/day of zinc) had decreased muscle strength and work capacity (Van Loan et al., 1999). Physically active men fed a moderately low zinc diet (5 versus 18 mg/day) had impaired cardiorespiratory function during peak and prolonged submaximal exercise (Lukaski, 2005).

Low zinc intakes and status have been related to deficits in memory, perception, attention, and motor skills, while zinc supplementation has improved memory (Table B-10). Low serum zinc in otherwise well-nourished men fed 5, compared with 15, milligrams per day of zinc was associated with faster, but less accurate, performance on memory for digits and several perceptual tasks (Tucker and Sandstead, 1984). Contrasted to a control period when men were fed adequate zinc (10 mg/day), low zinc intakes (1, 2, 3, or 4 mg/day) resulted in

decreased performance on psychomotor (tracking and connect-the-dots), attention (orienting and misdirection), memory (letter, shape, and cube recognition), perceptual (search-count), and spatial (maze) tasks. However, there was no evidence of a “dose–response” effect of dietary zinc on cognitive performance (Penland, 1991). Reaction times during word recall were significantly slower when men were fed low amounts of zinc (5 versus 14 mg/day) (Kretsch et al., 2000).

Magnesium, a cofactor in more than 300 enzyme reactions in which food is metabolized and new products are formed, regulates many biological functions (Shils, 1997). Thus, it is a potentially limiting nutrient for human performance.

The dietary restriction of magnesium reduced the magnesium status and impaired physiological function and performance in untrained adults. As shown in Table B-9, physically active men supplemented with magnesium (250 mg/day for four weeks) experienced increased endurance and decreased oxygen use during submaximal exercise (Brilla and Gunter, 1995).

Supplementation with magnesium salts improved cellular function. Men receiving 370 mg of magnesium daily for four weeks had reduced serum lactate concentration and oxygen uptake during a progressive rowing test (Golf et al., 1994). Magnesium supplementation (250 mg/day for seven weeks) increased muscle strength and power in men participating in a strength training regimen (Brilla and Haley, 1992). Although modest strength gains occurred with magnesium intakes of 540 mg/day (290 mg from diet and 250 mg from supplements), increases were achieved at intakes greater than the RDA of 420 mg/day (IOM, 1997).

Whereas severe magnesium deficiency has been associated with numerous neurological and psychological disturbances (Dubray and Rayssiguier, 1997), few reports have described neuropsychological effects from marginal magnesium restriction (Delorme et al., 1992; Table B-10). Male athletes with low, compared with normal, erythrocyte magnesium had significantly less alpha activity in the right occipital region as recorded by an electroencephalogram (EEG) (Delorme et al., 1992), which suggests that magnesium is involved in regulating cortical activity related to motor function.

Copper is a cofactor of many metalloenzymes and, thus, copper status may affect diverse biological functions. It regulates iron absorption, neurotransmitter metabolism, antioxidant defense, and oxygen use. Longitudinal studies of diet and physical training showed an adaptation in antioxidant protection (Table B-9). Collegiate swimmers training for competition increased dietary copper from 1 to 1.4 mg/day, resulting in an increased erythrocyte superoxide dismutase activity and no change in plasma copper, whereas nontraining control subjects did not change enzyme activity at the same intakes of copper (Lukaski et al., 1989, 1990). Adequate copper intake is needed for adaptation in antioxidant protection during physical training.

Marginal copper intake reduces energy metabolism. Men fed less (0.9 versus 1.6 mg/day) dietary copper showed increased oxygen use, heart rate, and postexercise lactate concentrations during submaximal exercise (Lukaski and Johnson, 2005). Muscle cyctochrome c oxidase activity decreased with the marginal dietary copper (Table B-9). Thus, restricted copper intake appears to increase energy use during low-level work.

Many of the studies to measure cognition and behavioral effects of copper deficiencies have been conducted with women. Restricted dietary copper has been associated with impaired verbal memory, and disrupted sleep and mood states in women (Table B-10). Increased sleep times, longer latency to sleep, and feeling less rested upon awakening as well as increased confusion, depression, and total mood disturbances were reported when dietary copper was low (0.8 versus 2 mg/day) (Penland, 1988). Short-term memory and immediate recall of verbally presented words (list recall) worsened with low dietary copper (1 versus

3 mg) (Penland et al., 2000). Low copper intakes were also associated with increased difficulty in discriminating between relevant and irrelevant responses. Sufficient plasma copper and ceruloplasmin are associated with improved verbal and long-term memory, increased clustering of verbal material (strategy), and fewer distractions (Penland et al., 2000).

Iron is needed to deliver oxygen to tissues and to use oxygen at the cellular level. It serves as a functional component of iron-containing proteins needed for efficient energy use as well as for catecholamine metabolism.

Whereas the adverse effects of iron deficiency anemia on work capacity and endurance are well established (Tobin and Beard, 1997), there is growing interest in the functional effects of tissue iron depletion without anemia. Iron deficiency anemia in men is rare, except with excessive blood loss. Estimates of tissue iron depletion in men range from 5 to 15 percent despite only a 5 percent prevalence of low iron intake (IOM, 2001). Accumulating evidence shows that a low-iron status without anemia (e.g., low serum ferritin or transferrin saturation) elicits impaired physical performance, including time used to complete standard running distance (Hinton et al., 2000), endurance training adaptation (Brownlie et al., 2002), and muscle function (Brutsaert et al., 2003) that are all ameliorated with increased iron intake.

Male soldiers participating in Ranger training maintained normal hematology with increased ferritin and decreased serum iron (Shippee, 1993). Various measures of muscle strength and endurance decreased with the training. Because food intake as well as body and fat-free mass concomitantly decreased, one may conclude that reduced iron status contributed to the impaired physical performance.

Iron status has been related to attention, memory, and learning. Iron supplementation in young women (180 mg/day for 30 days) improved attention and short-term memory (Groner et al., 1986), while verbal learning and memory improved significantly in nonanemic, iron-deficient women supplemented similarly with iron (Bruner et al., 1996). Accuracy and reaction times on tasks measuring attention, memory, and learning were improved in women with the highest, compared with the lowest, ferritin and transferrin saturation in the absence of anemia (Murray-Kolb et al., 2004).

Sleep and mood disturbances have been related to dietary iron restriction. Nonanemic women and menstruating women fed low dietary iron (5 versus 15 mg/day) reported more frequent night-time awakenings and more total sleep duration (Penland, 1988). This low iron intake also increased reports of depression, fatigue, and total mood disturbances (Penland, 1989).

Select patterns of cortical activity (measured by EEG) have been predicted by iron status in nonanemic men. Consistent with depressed alertness, lower serum iron and ferritin were associated with more low-frequency EEG activity

and lower amplitude-evoked potentials in response to visual stimuli (Tucker and Sandstead, 1981; Tucker et al., 1982, 1984).

Selenium acts through its association with proteins as an antioxidant and a regulator of thyroid hormone metabolism. The independent role of selenium in exercise performance and metabolism is not well understood because of its interdependence with vitamin E and other nutrients in antioxidant defense.

Endurance-trained men supplemented with selenium (180 µg/day as selenomethionine versus a placebo) significantly increased plasma selenium and glutathione peroxidase activity with no effect on performance (Tessier et al., 1995b). Improvements in peak oxygen uptake were significantly correlated with glutathione peroxidase activity only in the men supplemented with selenium. Young men supplemented with 240 µg/day of selenium (selenomethionine) and trained for endurance had no performance benefit but a significant increase in muscle glutathione peroxidase activity (Tessier et al., 1995a). Thus, supplemental selenium upregulates biochemical markers of selenium status without enhancing performance.

Several studies have shown an effect of selenium intakes and status on mood states in both men and women (Table B-10). Women and men supplemented with selenium (100 µg/day) reported less anxiety and depression and more energy (Benton and Cook, 1991). Men fed supplemental selenium (230 versus 30 µg/day) reported less confusion and depression (Penland and Finley, 1995). Activity of glutathione peroxidase, a selenium enzyme, in platelets was positively correlated with all mood states (Finley and Penland, 1998).

Although its role in bone metabolism is emphasized, calcium acts in mediating vascular, muscular, and nerve functions. Adverse effects of inadequate calcium intake on physical performance are not well studied. However, calcium is required to regulate glycolysis and glycogenolysis and to control protein breakdown. Studies of the effects of calcium restriction or supplementation on human metabolism are lacking despite evidence that calcium intake for 50 percent of adult men is less than the AI (IOM, 1997).

Military personnel participating in training and operational exercises consistently decrease food intake, thus consuming inadequate amounts of minerals. Blood biochemical markers of nutritional status, however, do not reveal overt

mineral deficiencies although assessments of hormonal and immune functions show decreases (Booth et al., 2003; Shippee, 1993). Failure to detect nutritional deficiencies is explained by a lack of sensitive biochemical markers of mineral status, brief durations of restricted intakes, and mineral mobilization from stores into the blood with increased metabolic demands and loss of body weight.

Measurable impairments in aerobic capacity or muscle power occur when body weight decreases about 10 percent with a 5 percent loss in muscle mass (Friedl, 1995). Cognitive function declines when significant weight loss (> 6 percent) occurs (Mays, 1995). When energy restriction (50 percent decrease) occurs with strenuous activity, sleep deprivation and mental stress, cognitive performance may fall by more than 33 percent within a few days (Mays, 1993). Decreased food intake plus physical and mental stressors for 12 days increase reports of fatigue and sleep impairment, even at modest levels of weight loss (3 percent) (Booth et al., 2003). Thus, brief and prolonged periods of exposure to nutritional, environmental, physical, and mental stressors impair cognitive performance, including attention, perception, memory, and reasoning (Mays, 1993).

Some reports describe decreased nutritional status during military operations. Shippee (1993) found decreased iron and altered copper and zinc status in Ranger II. Also, Booth and colleagues (2003) reported a decline in iron status in both 12- and 23-day training activities. It is unclear if these findings reflect a response to stress and inflammation or to inadequate intakes of these minerals.

Repeated assault operations may result in mineral depletion because of inadequate intake, and increased turnover and losses of minerals may promote marginal deficiencies under stressful conditions. Also, entry into operations with marginal mineral status may predispose individuals to deficiency status and functional deficits, particularly with repetitive assaults without replenishment of depleted mineral reserves.

Replacing standard combat rations with fresh food and hot meals may alleviate the adverse effects on body weight, physical performance, and cognitive function (Booth et al., 2003; Tharion et al., 2004). This approach, however, is not feasible for soldiers in assault operations. Therefore, new strategies are needed to provide soldiers with proper nutrition.

One approach is to increase the nutrient density of assault rations. Mineral nutrient densities should meet the military standards for reduced-energy rations for men (Baker-Fulco et al., 2001; US Departments of the Army, Navy, and Air Force, 2001). Thus, with reduced energy intake, soldiers would still have adequate mineral intakes.

Steps to improve food intake should be further explored (Hirsch and Kramer, 1993). These include adding new, fortified foods and using stages of change

models to foster healthful nutrition habits (Veverka et al., 2003). Increasing emphasis on maintaining adequate hydration and sleep, particularly during recovery periods, will support these efforts.

Active efforts to prevent marginal mineral depletion should be employed. Some suggestions include:

• Develop and support an active nutrition education program.

• Provide palatable, mineral-rich food items in the rations, including on-the-go foods.

• Increase the availability of mineral-rich foods during recovery periods.

• Encourage unit leaders and peers to be models of healthful eating behaviors.

Evidence shows that military personnel fail to consume adequate amounts of magnesium, zinc, and calcium. These minerals, as well as copper, selenium, and iron, play key roles in promoting optimal physiological and psychological function and performance. Limited data on mineral intakes and the resulting status of soldiers in various types of training do not provide evidence of overt nutritional deficiencies. A lack of sensitive biochemical markers of nutritional status hinders interpretation of available data. It is difficult to discriminate the independent effect of severely restricted energy intake on potential micronutrient impairments. Nevertheless, physiological and psychological impairments found in civilians with marginal mineral deficits are consistent with perturbations reported in soldiers during operations and suggest similarities, particularly when the low mineral intakes have been noted in the soldiers.

Based on limited evidence of inadequate intakes of zinc and magnesium, and the presumption of increased zinc losses associated with increased physical activity and elevated rates of sweat, zinc and magnesium status may be compromised. With repeated bouts of these conditions and inadequate replenishment of zinc and magnesium stores, soldiers may manifest marginal zinc and magnesium depletion and experience limitations in work capacity, recovery after deployment, perception, and attention. Furthermore, zinc depletion may attenuate immune function and increase the potential for acute bouts of gastrointestinal distress. Evidence of reduced antioxidant defense is generally lacking in military personnel during short-term assault missions. However, recurrent intermittent periods of inadequate intakes of copper, selenium, zinc, and manganese without adequate intakes during recovery may lead to decreased activity of protective antioxidant enzymes.

Generalized use of multiple vitamin and mineral supplements at intakes not exceeding recommended levels should not be hazardous to soldiers participating in assault missions. The use of single nutrient supplements in amounts exceeding

the recommended intake should be avoided to eliminate potential adverse interactions with other nutrients, particularly mineral elements.

Initiating a proactive approach to decrease the potential of adverse effects of limited mineral intakes is recommended. Increasing the mineral densities of assault rations should be advantageous. Adopting an active nutrition education program with palatable, mineral-rich foods and encouraging leaders to model healthy eating behaviors also should be useful to reverse the high rates of low-mineral intakes of soldiers.

There is a need to determine the nutrient intakes, markers of nutritional status, and physiological and psychological performance of military personnel during training and operations. This information is needed to critically evaluate the adequacy of rations provided to and consumed by soldiers exposed to multiple stressors. Findings of this research will enhance the development of rations that promote optimal nutrition and, accordingly, the performance of soldiers engaged in assault operations.

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Lynn B. Bailey and Kristina von Castel-Dunwoody, University of Florida

The primary objective of this paper is to evaluate the potential effect of inadequate B vitamin intake in relation to the consumption of assault rations under extreme physical stress during intense military combat operations. The goal is to characterize the optimal B vitamin content for future rations that will be designed to maximize the physical and mental performance of soldiers