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1 From the US Army Research Institute of Environmental Medicine, Natick, MA (RWH, AC, and KEF); the Norwegian Defence Research Establishment, Kjeller, Norway (PKO and A-HH); and the Pennington Biomedical Research Center, Baton Rouge, LA (JPD)
2 The opinions and assertions contained in this manuscript are the personal views of the authors and do not necessarily represent the official views or policy of the US Department of the Army. 3 Supported by the Norwegian Defence Research Establishment, Kjeller, Norway, and the Military Operational Medicine Research Program, US Army Medical Research and Materiel Command, Fort Detrick, MD. 4 Reprints not available. Address correspondence to RW Hoyt, MCMR-BMD, US Army Research Institute of Environmental Medicine, Natick, MA 01760-5007. E-mail: reed.hoyt{at}us.army.mil.
ABSTRACT
Background:A challenging 7-d ranger field exercise (FEX) by cadets in the Norwegian Military Academy provided a venue in which to study the effects of negative energy balance.
Objective:We quantified total energy expenditure (TEE), food intake, and changes in body composition in male and female cadets.
Design:TEE (measured by doubly labeled water), food intake, activity patterns (measured by accelerometry), and body composition (measured by dual-energy X-ray absorptiometry) were measured in 16 cadets (10 men and 6 women aged 21–27 y).
Results:The physically active (
Key Words: Starvation • sustained exercise • body composition • sex • water intake • military rangers • Norway
INTRODUCTION
As part of their training, male and female Norwegian Military Academy cadets participate in a challenging 5–7-d field exercise (FEX) course characterized by sleep and food deprivation and sustained physical activity (1). The inclusion of women in this annual FEX ranger training course provides a unique opportunity to compare responses to extreme physical demands between the sexes. The US Army, in contrast, excludes women from participating in combat arms training courses (2).
Scientific studies of male cadets participating in the FEX course have provided scientific insights into the effects of sleep deprivation (3, 4), alterations in physical and psychological performance under stress (5, 6), and endocrine adaptations (1, 7, 8). However, only a limited amount of information is available on energy expenditure and substrate use by cadets in the FEX, and little is known about the physiologic responses to the FEX in female cadets.
Total energy expenditure (TEE) during FEX training was estimated to be 33–40 MJ/d by the heart rate method (3, 9). A similar TEE was evident in a FEX study in which an average food energy intake of 33 MJ/d was needed to maintain body weight (6). These TEEs, at 4–5-fold the resting metabolic rate (RMR), are similar to the high rates of energy expenditure of US Marines training in mountainous, cold-weather conditions (3–4-fold the RMR) (10) and of Tour de France bicycle racers (5 x the RMR) (11).
The FEX offered an opportunity to study sex differences in substrate use under extreme conditions of physical activity and food deprivation. Laboratory studies of short-term exercise suggest that females maintain a more fat-predominant and less carbohydrate-dependent fuel metabolism than do males (12, 13). Across a range of moderate exercise intensities, both the fractional contribution of fat oxidation to TEE and the rate of fat oxidation per kg fat-free mass (FFM) were reported to be greater in women than in men (12). The apparently greater rate of fat oxidation during submaximal exercise in women appears to be promoted by estrogen (14). However, not all studies report sex differences in substrate oxidation during exercise (15–17), which suggests that further study is warranted.
The present study assessed the responses of healthy male and female soldiers in response to the extreme demands imposed by 7 d of sustained exercise and food deprivation. The specific goals were to accurately quantify TEE and changes in body composition and to compare the responses of men and women.
SUBJECTS AND METHODS
The test subjects gave their informed consent to be studied during their FEX training course after being informed of the purpose, risks, and benefits of the study. The subjects understood that they were free to withdraw from the study at any time. This study was approved by the Institutional Review Boards of the US Army Research Institute of Environmental Medicine and the US Army Medical Research and Materiel Command.
The test volunteers were 16 healthy and physically fit classmates (10 men and 6 women) from the Norwegian Military Academy, Kjeller, Norway, who participated in the FEX course. The FEX, which is held each summer, seeks to teach cadets combat leadership, an appreciation of personal and team-member responses to stressful conditions, and an ability to endure physical and mental stress. The FEX typically involves severe food restriction, sleep deprivation, and periods of sustained physical activity. Water is freely available. Activities include long-distance foot marches, simulated combat patrols, traversing obstacle courses, and marksmanship training.
The cadets participated in 1 of 2 similar 7-d FEX iterations; the data from these 2 FEX iterations were combined. In the first FEX (study 1), 6 men and 4 women were studied; in the second FEX (study 2), 4 men and 2 women were studied. In addition, urine samples were obtained from a separate set of 4 male cadets (2 per FEX iteration) who were not given doubly labeled water (DLW). As described below, changes in background isotopic 2H2O and H218O enrichments in these samples were used to correct DLW TEE calculations (18). These 4 cadets participated in the same training activities and lost amounts of body weight (7.93 ± 1.16 kg) similar to those in male cadets in the main study group.
The experimental test schedule is shown in Figure 1. The FEXs were conducted in forested military training areas northwest of Oslo, Norway, at an altitude of 500 m, in June, when the weather was warm by day (20–30°C) and cool at night (5–15°C). Meteorologic conditions in the training area were obtained from local weather stations operated by the Norwegian government weather service. Field training activities started at 0400 on day 1 and ended at 1000 on day 8 (total FEX duration: 7.25 d).
FIGURE 1.. Study schedule. The energy balance of 10 male and 6 female military cadets participating in a 7-d field exercise (FEX) involving sustained exercise and food restriction was assessed. Data were collected during 2 FEX iterations (study 1: n = 6 men and 4 women; study 2: n = 4 men and 2 women). Total energy expenditure (TEE) during the FEX was measured by the doubly labeled water (DLW) method. Total body water was determined before and after the FEX by deuterium oxide dilution. Food energy intake was monitored during the FEX. Activity-inactivity patterns were assessed in a subset of subjects with the use of wrist-worn activity monitors (study 1 only; n = 3 men and 2 women). Body composition was assessed before and after the FEX by dual-energy X-ray absorptiometry (DXA).
Total energy expenditure and total water turnover determinations
Daily TEE was assessed by the DLW method. On the morning of day 0, each volunteer, who had refrained from eating or drinking for 12 h, reported to the testing area with a baseline sample of their first-void urine. After providing baseline saliva samples, each subject drank 0.25 g H218O/kg total body water (TBW) (Isotec Inc, Miamisburg, OH), 0.18 g 2H2O/kg TBW (Cambridge Isotope Laboratories, Andover, MA), and 100 mL tap water, which was used to rinse the dose container. TBW was assumed to be 73% of estimated FFM for the purposes of calculating the DLW dose. To confirm isotopic equilibration, saliva samples were collected 3 and 4 h after tracer ingestion. Actual TBW was calculated from isotopic enrichments in the 4-h saliva sample (19). The subjects were free to eat and drink only after the final saliva sample was collected. First-morning void urine samples were collected at the start of the energy expenditure period on day 1 and on day 7 and day 8. A second and final determination of TBW was made on the morning of day 8 with the use of a dose of 0.18 g 2H2O/kg TBW.
Daily TEE was calculated by using the 2-point method, and changes in baseline isotopic abundances and changes in TBW were corrected for. The rate of carbon dioxide production (rCO2) was calculated by using the equations of Schoeller et al (20) with modification (21, 22):
RESULTS
The physical characteristics of the subjects reflected the expected sex dimorphism (Table 1). Significant sex differences were evident, both before and after the FEX, in percentage body fat (before: see Table 1; after: men, 12.7 ± 3.3%; women, 22.6 ± 4.8%), body FM index (in kg/m2; before: men, 3.9 ± 0.9; women, 5.9 ± 1.1; after: men, 2.8 ± 0.8; women, 4.6 ± 1.1), and FFM index (in kg/m2; before: men, 20.4 ± 1.0; women, 16.8 ± 1.4; after: men, 19.1 ± 1.1; women, 15.9 ± 1.3; P < 0.05 for all). However, no significant sex differences were evident before or after the FEX in BMI (before: men, 24.6 ± 1.2; women, 23.0 ± 1.5; after: men, 21.9 ± 1.5; women, 20.5 ± 1.4), estimated fat energy reserves (before: men, 8.4 ± 2.6 kg; women, 9.9 ± 2.9 kg; after: men, 4.9 ± 2.3 kg; women, 6.4 ± 2.8 kg), or the percentage loss of initial FFM (men, –6.3 ± 1.9%; women, –5.6 ± 2.4%; NS).
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TABLE 1. Baseline characteristics of the subjects1
The differences in food energy intake and the timing of the pre-FEX DXA measurements between study 1 and study 2 did not appear to be significant factors in the data analysis. Food energy intake in study 1 (0.2 MJ/d; n = 6 men and 4 women) and study 2 (1.9 MJ/d; n = 4 men and 2 women) met 1% and 9% of the cadet’s energy needs, respectively. This difference in food energy intake was not associated with any significant between-study differences in the absolute or relative change in FM, FFM, or body weight (P = 0.60–0.85). In addition, body weight measurements and total body energy calculations indicated the study 1 subjects were in energy balance between the day –4 DXA measurements and the day that the FEX started (day 0). Body weight increased from day –4 to day 0 (1.57 ± 1.87 kg; n = 10; P < 0.05), and no significant difference in the amount of weight gained by the men (1.67 ± 2.47 kg; n = 6) and women (1.43 ± 0.58 kg; n = 4) was observed. This body weight gain was within the normal day-to-day variation in TBW in army recruits (34) and probably did not reflect a change in body energy stores. Estimated total body energy did not change significantly from day –4 to day 0 (–19 ± 64 MJ; n = 10).
Activity monitor data from a subset (n = 5) of subjects from study 1 showed that the cadets were not sleep deprived immediately before the FEX (apparent sleep: day –2, 8.6 ± 2.0 h/d; day –1, 6.4 ± 0.6 h/d; day 0, 5.4 ± 1.1 h/d). In contrast, during the FEX, the subjects were inactive (apparently asleep) <1 h/d. During the first 4 d of the FEX (day 1 to day 4), apparent sleep averaged 0.8 ± 0.7 (day 1), 0.8 ± 0.5 (day 2), 1.1 ± 0.8 (day 3), and 1.1 ± 0.3 (day 4) h/d.
The group mean DLW TEE was 24.8 ± 3.1 MJ/d (range: 19.1–29.5 MJ/d; n = 16). In study 2 (n = 6), the estimated intake-balance TEE (23.6 ± 3.6 MJ/d; range: 20.1–28.7 MJ/d) did not differ significantly from the corresponding DLW TEE (23.6 ± 3.4 MJ/d; range: 19.1–27.8 MJ/d).
Data derived from the DLW measurements are shown in Table 2. Baseline TBW was 46.8 ± 3.8 kg for men and 34.5 ± 2.5 kg for women (P < 0.05). The oxygen-18 elimination rate (kO) on day–1 was –0.1456 ± 0.0167 for men and –0.1552 ± 0.0326 for women; kD on day–1 was –0.1056 ± 0.0152 for men and –0.1090 ± 0.0307 for women. Total RH2O averaged 4.4 ± 1.0 L/d (n = 16). Absolute RH2O was greater in the men than in the women (P < 0.05), but no significant difference was evident when RH2O was expressed relative to FFM or body weight. The relations of RH2O to FFM [RH2O = (–0.705 x FFM) – 0.368; x intercept = –5.2 kg; R2 = 0.46; n = 16] and of RH2O to body weight [RH2O = (–0.777 x body wt) +1.179; x intercept = 15.2 kg; R2 = 0.46; n = 16] were used to calculate mass-specific RH2O. No significant sex differences were evident in FFM-specific RH2O (men, –69.7 ± 9.6 mL · kg corrected FFM–1 · d–1; women, –72.5 ± 19.2 mL · kg corrected FFM · d–1) or in body weight–specific RH2O (men, –77.2 ± 11.2 mL · kg corrected body wt–1 · d–1; women, –78.0 ± 21.6 mL · kg corrected body wt–1 · d–1).
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TABLE 2. Daily total energy expenditure (TEE), food energy intake, water turnover, physical activity level (PAL), and activity energy expenditure (AEE) in male and female cadets participating in a 7-d ranger field exercise with sustained exercise and food restriction1
The significant correlation of TEE to body weight is shown in Figure 2. Similar relations of AEE to body weight (AEE = 0.189 x body weight + 4.086; R2 = 0.57; SEE = 1.54; n = 16), of AEE to FFM [AEE = 8.166 + (0.166 x FFM); R2 = 0.55, SEE = 1.57; n = 16], and of TEE to FFM [TEE = 10.234 + (0.256 x FFM); R2 = 0.73, SEE = 1.65; n = 16] were also evident. In addition, in study 1, TEE was correlated with total weight, ie, with estimated load plus body weight [TEE = (0.199 x total weight) + 4.654; R2 = 0.65, n = 10]; the load averaged 32.9 ± 3.1 kg (men: 34.3 ± 3.0 kg, n = 6; women: 30.7 ± 2.1 kg, n = 4; P < 0.05).
FIGURE 2.. Correlation of total energy expenditure (TEE) with body weight in male (n = 10; •) and female (n = 6; ) cadets participating in a 7-d field exercise involving sustained exercise and semistarvation. TEE was measured by the doubly labeled water method.
Absolute TEE was greater in the men than in the women (P < 0.05; n = 10 men and 6 women). However, mass-specific TEEs did not differ significantly between sexes (n = 10 men and 6 women). Specifically, the use of FFM and body weight values corrected for the nonzero intercepts in the linear relations of TEE to FFM [TEE = (0.256 x FFM) + 10.234; x intercept = –40 kg; R2 = 0.73; n = 16) and of TEE to body weight [TEE = (0.286 x body weight) + 4.342; x intercept = –15 kg; R2 = 0.72; n = 16] showed that no significant sex differences (n = 10 men and 6 women) were evident in FFM-specific TEE (men, 255 ± 15 kJ · kg corrected FFM–1 · d–1; women, 257 ± 21 kJ · kg corrected FFM–1 · d–1) or in body weight–specific TEE (men, 287 ± 21 kJ · kg corrected body wt–1 · d–1; women, 285 ± 15 kJ · kg corrected body wt–1 · d–1). Similarly, no significant sex differences in TEE were evident after correction for covariance by either body weight or FFM (n = 10 men and 6 women).
During the FEXs, body weight decreased from 71.6 ± 9.1 kg (day 0) to 64.6 ± 8.1 kg (day 8) (n = 16; P < 0.05). On average, the daily loss of body weight was 1 kg (men, –1.06 kg/d; women, –0.85 kg/d; P < 0.05) including a 0.5-kg loss in FM (men, –0.49 kg/d; women, –0.50 kg/d; NS). On average, the cadets lost 10% of their body weight during the FEX, with the absolute body weight loss of the men exceeding that of the women (P < 0.05; n = 10 men and 6 women; Table 3); the men lost more FFM than did the women (P < 0.05). Both the men and the women lost 6% of FFM. However, FFM loss expressed as a percentage of body weight loss was significantly greater in the male than in the female cadets (men, 53 ± 11%; women, 41 ± 11%; P < 0.05). Absolute FM loss was not significantly different between the men and the women (3.4 kg), but the men had a significantly larger percentage loss of initial FM (28.3 ± 5.9%) than did the women (22.1 ± 3.6%). About 50% of the total loss of FM was derived from the trunk (men, –2.1 ± 0.6 kg; women, –1.7 ± 0.3 kg); the men lost 45.3 ± 12.4% and the women lost 36.1 ± 8.7% (P = 0.064) of initial truncal fat mass.
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TABLE 3. Changes () in body composition and the associated change in body weight in male and female cadets in response to a 7-d ranger field exercise with sustained exercise and food restriction1
Absolute and relative fat oxidation and the percentage contribution of FM to TEE are shown in Table 4. Absolute rates of fat oxidation were not significantly different between the women and the men, despite differences in body size; however, fat oxidation per kg FFM in the women exceeded that in the men (P < 0.05). Regression analysis showed that fat oxidation per kg FFM was positively related to FM (Figure 3). Fat oxidation per kg FM, or, alternatively, FM/initial FM (men, –29 ± 6%; women, –22 ± 4%), were significantly greater in the men than in the women (P < 0.05). However, this difference was not significant when apparent sex differences in fat energy reserves were taken into account. In other words, fat oxidation per kg fat reserves, or FM/estimated fat reserves (men, –44 ± 13%; women, –37 ± 10%), did not differ significantly between the male and the female cadets. Finally, the fractional contribution of FM to TEE of the women significantly exceeded that of the men.
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TABLE 4. Fat oxidation rates and the relative contribution of fat mass (FM) to total daily energy expenditure (TEE) in male and female cadets participating in a 7-d ranger field exercise with sustained exercise and food restriction1
FIGURE 3.. Correlation of fat oxidation per kg fat-free mass (FFM) with fat mass in male (n = 10; •) and female (n = 6; ) cadets participating in a 7-d field exercise involving sustained exercise and semistarvation. Body composition was assessed by dual-energy X-ray absorptiometry (DXA).
DISCUSSION
In response to a week of sustained exercise and food deprivation, the female cadets oxidized more body fat per kg FFM and had a greater fractional contribution of FM to TEE than did the male cadets. Our findings are consistent with most (12–14, 35), but not all (15–17), less-extreme, short-term exercise studies that have found that women use more fat and less carbohydrate and protein than men. In addition, the positive relation of fat oxidation per kg FFM and FM among the cadets suggested that fuel metabolism becomes more fat-predominant as FM increases, although other factors, such as circulating hormones (14), are also likely to be important.
Our finding that female cadets maintained a more fat-predominant fuel metabolism than did males implies reduced glycogen use, a significant capacity for endurance exercise, and less loss of FFM. Reduced glycogen use would tend to limit decrements in maximum sustainable endurance exercise intensity that normally accompanies carbohydrate deprivation (36). Running performance in female athletes apparently approaches that of men as race distances increase, reaching parity in a 90-km ultramarathon race (37).
With prolonged underfeeding, FFM loss is 25% of the weight lost, with fat accounting for the balance, although extreme energy deficits, as in the present study, can increase the contribution of FFM (38). Using less glycogen would tend to decrease protein use for gluconeogenesis and reduce the loss of FFM (38, 39). Women are reported to use less glycogen and excrete less urea nitrogen than men in response to 95 min of moderate-intensity exercise (35). The loss of FFM during the FEX was a smaller percentage of body weight loss in the women than in the men.
Absolute FM loss and the absolute rate of fat oxidation to meet energy needs were not significantly different between the male and the female cadets, but fat oxidation per kg FFM and the percentage contribution of FM to TEE were greater in the female cadets. This contrasted with the typical pattern in which absolute differences between the sexes were not evident when calculated on a relative basis. For example, the male cadets lost more FFM than did the female cadets, but no sex difference was evident in the percentage loss of initial FFM. The female cadets were physically smaller and had lower TEEs than did the male cadets, but PAL, AEE, and relative TEE were similar between the sexes.
The body weights and body fat levels of the cadets were near the ideal for fit young men (76 kg, or 15%) and women (60 kg, 25%) and were similar to those of US Army soldiers (40) and cadets in previous FEX studies (6, 41). Although body FM index values were normal, the FFM index values for the fit cadets were at the high end of the normal range (42).
The cadets were inactive 1 h/d, as in previous FEX studies (3, 43), and they had PALs equivalent to 23 h/d of heavy work (44); the PALs exceeded those of climbers of Mount Everest [2.2 x basal metabolic rate (BMR)] (45), soldiers training for jungle warfare (2.5 x BMR) (46), hill walkers (2.8 x BMR) (47), US Army Rangers in training (48), and others (49). However, the cadets were less physically active than were US Marines training for mountain warfare (PAL: 4) (10), Arctic explorers (PAL: 4.5) (50), and Tour de France cyclists (4.3–5.3 x BMR) (11). The TEEs of our cadets, determined either by intake-balance or DLW methods, were less than the TEE estimates for previous FEXs (3, 6, 9). Our cadets had TEEs that were 50–75% of the TEEs estimated in previous studies (33–46 MJ/d) in which the duration of the FEXs was 3–5 d (3, 6, 9), as opposed to 7 d in the present study. On the other hand, average daily losses of body weight (–0.76 to –0.90 kg/d) (6, 41, 51) and of FM (–0.60 to –0.69 kg/d) (6, 41) in previous FEX studies suggest TEEs of 27–29 MJ/d.
Our male cadets used 45 ± 15% of their body fat reserves, assuming 5% body fat as a minimum (31). This was similar to the 50% fat reserve depletion with FEX training in male cadets (6). Female cadets used 37 ± 10% of their fat reserves, assuming 10% as the minimum percentage body fat in healthy young women. The disproportionately large contribution of trunk fat to the total FM loss, found in both the male and the female cadets, is consistent with earlier findings in male cadets (41). Rognum et al (41) sampled cadets’ fat cells from 3 sites and found large decreases in fat cell size in abdominal and gluteal adipocytes but not in the more peripheral femoral site adipocytes.
In addition to the known relation of RMR to FFM, an analogous but less-defined relation between TEE and FFM or body weight has been reported (18). Among the cadets, both TEE and AEE were correlated with FFM, body weight, and estimated total weight. This was expected, given that body weight is a key determinant of the metabolic cost of locomotion (52), and the primary activity of the cadets was prolonged foot marches. Kram and Taylor (52) showed that the metabolic cost of locomotion is primarily determined by the cost of supporting body weight and the rate at which this force is generated. In one study, Schoeller and Fjeld (53) attributed most of the variance in DLW TEE to individual differences in FFM (men, R2 = 0.87; women, R2 = 0.68). In a study of obese women, DLW TEE was correlated with FFM (R2 = 0.52) and body weight (R2 = 0.59) (54). During a winter trek on Mount Rainier, DLW TEE was also correlated with FFM (R2 = 0.89, P < 0.01) and total weight (R2 = 0.95, P < 0.01) (19). In US Marines engaged in varied cold-weather training activities, DLW TEE was less-well correlated with FFM (R2 = 0.35, P < 0.05) (10). The relations between TEE and body weight and of TEE to FFM were also less evident in sedentary soldiers (27). The relation of TEE to FFM appears to be more evident when subjects share a common locomotion task and is less evident in sedentary groups.
The present study had limitations. A definitive examination of sex differences in fuel oxidation during sustained stress requires a larger sample size. We were restricted by the limited number of female cadets participating in FEX training. Second, because of a schedule conflict, the DXA measurements in study 1 were made 4 d before the FEX rather than immediately before the FEX. The subjects were probably in energy balance during this period, given that calculated total body energy was unchanged. The difference in food energy intake between study 1 (1% of TEE; n = 6 men and 4 women) and study 2 (9% of TEE; n = 4 men and 2 women) probably contributed to the variability of the data. Finally, aerobic capacity was not measured. However, previous studies found the cadets to be moderately fit (maximal oxygen uptake = 50–58 mL/kg · min–1) (9, 55), which suggests that our cadets, who were engaged in common training, were also moderately fit. We conservatively assumed that relative aerobic fitness and exercise intensity during the FEX were not significantly different between the men and women. If the women worked at a higher intensity than the men, the effect would be to decrease fat oxidation and minimize any sex difference in fuel oxidation.
In conclusion, most of the sex differences in energy expenditure, RH2O, and FFM loss in response to the FEX were attributed to differences in body size. However, the female cadets maintained a more fat-predominant fuel metabolism and achieved an absolute rate of fat oxidation similar to that of the physically larger male cadets.
ACKNOWLEDGMENTS
We thank the selfless test volunteers from the Norwegian Military Academy, who made this study possible; Daniel P Redmond for assistance with the actigraphy data analysis; and Arne Høiseth for help with the DXA measurements.
RWH, PKO, JPD, AC, and KEF participated in the study design and manuscript preparation. RWH, PKO, AHH, and AC conducted the study. All authors participated in one or more aspects of data analysis and interpretation. None of the authors had a conflict of interest.
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