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(Journal of Nutrition. 1999;129:1307-1314.)
© 1999 The American Society for Nutritional Sciences


Articles

Energy Metabolism Increases and Regional Body Fat Decreases While Regional Muscle Mass Is Spared in Humans Climbing Mt. Everest

Robert D. Reynolds*{dagger}1, Julie Ann Lickteig**, Patricia A. Deuster{ddagger}, Mary P. Howard{dagger}, Joan M. Conway{dagger}, Anneke Pietersma§, Joyce deStoppelaar and Paul Deurenberg§

* Department of Human Nutrition and Dietetics, M/C 517, University of Illinois at Chicago, Chicago, IL 60612, {dagger} Beltsville Human Nutrition Research Center, US Department of Agriculture, Beltsville, MD 20705, ** College of Business and Management, Cardinal Stritch University, Milwaukee, WI 53217, {ddagger} Department of Military and Emergency Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, § Department of Human Nutrition, Agricultural University of Wageningen, Wageningen, The Netherlands and Laboratory for Health Effects Research, National Institute of Public Health and the Environment, Bilthoven, The Netherlands

1To whom correspondence should be addressed.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The objectives of the study were to determine regional changes in body composition, energy expenditure by means of doubly labeled water, and net energy balance during exposure to high and extreme altitudes (5,300–8,848 m). This study focuses on a subset of subjects who consumed the doubly labeled water (three base camp personnel and seven climbers). Regional body composition was determined by measuring skinfold thicknesses and circumferences at 10 different sites on the body. Energy expenditure was measured by doubly labeled water excretion. Discrepancies between actual energy expenditure and data obtained from diet records and body weight changes suggested a chronic underreporting of dietary energy intake, especially by those subjects who reached the highest altitudes. This underreporting may be due in part to diminished cognition or to a preferential focus on survival, rather than on filling out diet records accurately. Mean adjusted dietary intakes were 10.50 ± 0.65 MJ/d (2510 ± 155 kcal/d) for those who remained at base camp, and 20.63 ± 6.56 MJ/d (4931 ± 1568 kcal/d) for those who climbed above base camp. Energy expenditure averaged 2.5–3.0 times sea level resting energy expenditure. Differential changes in regional body composition suggested a preferential loss of fat mass and a relative sparing of muscle mass, despite insufficient energy intake to maintain body weight.


KEY WORDS: • altitude • anthropometrics • doubly labeled water • energy expenditure • energy intake • body composition • humans


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Until recently, high altitude medicine and physiology were dominated by studies related to the mechanisms of respiratory adaptation, with relatively minimal attention to nutrition. Yet, as stated by Pugh (1965)Citation , energy and fluid intake is at least as important as oxygen. Critical to any successful foray to high altitudes is an adequate supply of foods that provide the energy and macronutrients needed by the climbers for optimal performance and success. Success under varying environmental conditions means, above all else, survival. Tantamount to knowing the amount and types of foods necessary for survival is also knowing the energy requirements for this type of endurance activity. Recently, in an elegant series of articles, Westerterp et al. (1992 and 1994) provided an estimate of the actual amount of energy expended during a climb up Mt. Everest, the highest mountain in the world (8,848 m). These studies, which used the doubly labeled water technique, indicated that climbers expended ~13.6 MJ/d (3,250 kcal/d), which included 6.6 MJ/d (1,610 kcal/d) just for climbing activities. Westerterp et al. (1992)Citation further suggested that this additional energy expenditure "is probably near the maximum aerobic capacity at those altitudes and is compatible with the subject's sense of intensive exertion while climbing Mt. Everest." Pulfrey and Jones (1996)Citation reported that climbing at altitudes near 8,000 m required ~2.2 MJ/d (536 kcal/d) just for acclimation to these altitudes. This did not include energy expenditure for physical exertion. Although not stated, presumably their value for altitude acclimatization included the energy cost of adaptive thermogenesis to the cold.

How to provide the dietary energy necessary to meet the climbers' needs for basal metabolism, physical activity, adaptive thermogenesis, altitude acclimation and thermic effect of foods has been a long-standing problem for expeditions. Previously, it was commonly believed that higher-fat foods should not be consumed and may even be detrimental to the climbers (Anonymous 1938Citation ). However, we recently documented an estimate of energy intake during a 9-wk expedition to Mt. Everest and provided evidence that strongly suggested that high and extreme altitude climbers self-select foods that supply ~30% total energy in the form of fat, 55% total energy in the form of carbohydrate and 14% total energy in the form of protein (Reynolds et al. 1998Citation ). This observation was in contrast to the previously held belief that foods moderate to high in fat are not consumed or well tolerated by high altitude climbers (Anonymous 1938Citation ).

In this present report, we present energy expenditure values for a subset of members of the same research expedition who attempted to reach or did reach the summit of Mt. Everest, as well as changes in regional fat and muscle mass distribution associated with such energy expenditures.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
General.

The research methods were reviewed and approved by the Georgetown University Medical School Human Use Committee and by the US Department of Agriculture Human Studies Committee. Conditions for acceptance into the expedition are described elsewhere (Reynolds et al. 1998Citation ). Prior to acceptance, the full extent of the research question and methods were explained, both verbally and in writing, to the potential subjects. Following this explanation, written, informed consent was obtained from each subject. A more detailed description of the subjects, location, time of study, and the selection and preparation of foods and diets are presented in Reynolds et al. (1998)Citation . Documentation of individual climbing activities and locations was maintained by recording appropriate information on a daily physical symptoms questionnaire.

Subject selection.

Of the five base camp personnel and 10 climbers, three base camp personnel and seven climbers were chosen to receive the doubly labeled water to determine energy expenditure. The remaining two base camp personnel and three climbers received an equivalent volume of deionized tap water obtained from Beltsville, MD (placebo). Changes in baseline urinary excretion of endogenous 18O by the control subjects were used to correct for baseline changes in those subjects who received the doubly labeled water. As energy expenditure data were not available from the control subjects, data from these subjects were not included in any of the other calculations. Selection of which subjects were to receive the stable isotope and which were to receive the placebo was determined by matching as closely as possible the placebo group (1/3 of subjects) with the isotope group (2/3 of subjects) by age, gender, body mass index and anticipated climbing ability. Because of subsequent personal choices in climbing assignments, we were unable to maintain an equalization of subjects in the climbers and those who chose to stay at base camp. This resulted in an unavoidable over-representation of males among the climbers and an over-representation of females among the base camp personnel. All subjects were blinded as to treatment (isotope versus placebo) for the duration of the study. No limitations on actual climbing were placed on the climbers, regardless of which treatment they received, isotope or placebo.

Regional body composition determination.

Of the 10 climbers and the five base camp personnel, anthropometric measurements are reported here only for the seven climbers and three base camp personnel who received the doubly labeled isotope mixture. All anthropometric measures were obtained by the same two persons (A. P., J. dS.), who were trained specifically for this procedure (by P. D.). The researchers who made the anthropometric measures cross-checked their values each measurement day.

A measure of all anthropometric sites was performed upon arrival in base camp, which coincided with the beginning of the doubly labeled water energy expenditure dosing. Body weight was determined with the subject dressed only in minimal underwear and light socks while standing on a battery-operated digital-display balance (Model 22, Novus Electronids, Plainview, NY). Subsequent body composition-related measurements were performed seven times on each subject while the subjects were in base camp. To minimize the effects of dehydration, all anthropometric measurements were performed the morning after returning to base camp to allow time for the subjects to voluntarily rehydrate. Although consumption of water was encouraged by the researchers, rehydration was not controlled and was based on the desires of the climbers for fluid intake during this period. According to the diet records maintained by the climbers, all consumed significant, yet variable amounts of water.

Body composition was assessed according to the anatomical locations suggested by Jackson and Pollock (1985)Citation for males and females by using triceps skinfold and circumference, subscapular, chest and suprailiac skinfolds, abdominal skinfold and circumference, thigh skinfold and circumference and mid-calf circumference. Skinfold thicknesses were determined by a Lange skinfold caliper (Cambridge Scientific Industries, Cambridge, MD), and circumferences were determined by a nonstretch, plastic-coated, cloth tape measure. Body density for males was calculated by and for females by , as suggested by Jackson and Pollock (1985)Citation :


where D = body density; X1 = sum of chest, abdomen and thigh skinfolds; X2 = age in years; and X3 = sum of triceps, thigh and suprailium skinfolds. Body fat percentages were calculated according to Siri (1961)Citation , shown here as :

where BF = body fat. Fat mass was calculated by multiplying percent body fat times body weight at each time point. Percent muscle mass was calculated using , according to Heymsfield et al. (1982)Citation :

where MM = muscle mass in kg and cAMA is corrected bone-free arm muscle area. cAMA is calculated according to for males and 6 for females (Heymsfield et al. 1982Citation ):


where MAC = midarm circumference (cm) and TSF = triceps skinfold (cm). The above equations were derived from measurements of persons with a wide variety of body compositions. As our subjects ranged from those with a very low body fat mass to those with a more normal body composition (Tables 1Citation and 2), we felt it was reasonable to use the above equations rather than ones that may have been used solely for persons with extremely low body fat.


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Table 1. Subject description and baseline body composition measures1,2

 
Calculation of energy intake and distribution.

For the entire 9-wk study, all subjects completed a daily food record, irrespective of the altitude reached. Intake of food and fluid was determined by means of monitored entries in daily food records (Reynolds et al. 1998Citation ). The relative energy contributions from protein, carbohydrate, fat and alcohol as well as food quotients were calculated (Black et al. 1986Citation ).

Determination of resting energy expenditure.

Approximately 2 mo prior to departure from the US for the expedition, all subjects (except subject 8c) were placed in an indirect room calorimeter overnight to determine resting energy expenditure (REE) (Rumpler et al. 1990Citation , Seale et al. 1991Citation ). Heat emission and respiratory gas exchange were measured for ~12 h. An average energy expenditure over a 6-h sleep period was multiplied by 4 to obtain a 24-h daily REE. Repeatability of sleeping energy expenditures within subjects is ~3% (Seale et al. 1991Citation ).

Determination of total energy expenditure.

Deuterium oxide (99.9 atom % 2H) was obtained from MSD Isotopes (Montreal, Canada) and H218O (14.98 atom % 18O) was obtained from EG&G Mound Applied Technologies (Miamisburg, OH). The doubly labeled water was prepared by mixing 0.577 parts (by weight) 2H2O with 0.423 parts (by weight) H218O and administering 2.37 g/kg body weight of the mixture at precisely 1900 h to the subjects regardless of where they were on the mountain at the time. Subjects drank the entire dose provided and rinsed the cup with local snow-melt water to consume the entire dose of isotope. This dose of isotope provided 0.05 mol 2H/kg body weight and 0.01 mol 18O/kg body weight and was sufficient to permit detection of stable isotope in the urine for up to 3 wk. For logistic reasons, energy expenditure data are available only for a subset of the expedition members who participated in the doubly labeled water energy expenditure phase of the study, during either the first or the first and third of the three 3-wk study periods.

Administration of the stable isotope coincided with the beginning of each 3-wk phase. Coordination of the administration of the stable isotope was done via radio contact with subjects in each of the camps. Body weights were determined (in base camp) and the dose for climbers was calculated within 3 d of its administration. Isotope and placebo doses were weighed at base camp and sent in sealed bottles to the camps where the climbers were located.

Following stable isotope administration, the first morning urine was discarded and 24-h urine collections were obtained in a preweighed 4-L brown screw-cap plastic bottle (Fisher Scientific, Chicago, IL) on d 1, 2, 3, 8, 9, 10, 18, 19 and 20, regardless of where the subjects were on the mountain. A 24-h urine specimen was also collected on the day prior to administration of the next dose of stable isotope to provide a baseline concentration. No preservative was added to any of the collection or storage containers to avoid diluting the isotopes. Completed 24-h urine collections were returned to base camp where the full container was again weighed, the urine slowly thawed (if necessary) and mixed. Specific gravity was determined by a Schuco temperature-compensated clinical refractometer (Fisher Scientific). Total 24-h urine volume was measured in a 2-L plastic graduated cylinder. Two 50-mL aliquots of each urine collection were placed in 60-mL screw-cap vials and returned to the US for determination of relative isotope concentrations. During the stay in base camp, the vials were kept at ambient temperature (mainly below freezing) but were not kept frozen during transit to the US. Upon receipt in the US, the vials were kept frozen at -20° until analysis for stable isotope concentration.

Upon return to the US, the urine aliquots were thawed and filtered through Whatman #40 filter paper (Clifton, NJ) to remove precipitates and particulates. Filtered aliquots were used for stable isotope determination. Relative 2H concentration in the urine samples was determined by modified semiautomated flow, infra-red spectroscopy on shell-frozen aliquots (Stansell and Mojica 1968Citation , as modified by Seale et al. 1990Citation ). Relative 18O concentration was determined by specific ion ratio mass spectroscopy (Kreuger Enterprises, Cambridge, MA). The energy expenditure was calculated from the difference in slopes of the 2H and 18O disappearance curves by the method of Seale (1995Citation , Seale et al. 1989 and 1991Citation Citation ). Calculation of loss of each isotope was performed by averaging the concentration of the endogenous 2H and 18O concentrations in the placebo-dosed urine collections of the subjects at the respective day of collection, and subtracting this value from the concentration of isotope in the stable isotope-dosed urine collections. This corrected for the diminishing 2H and 18O isotope concentrations in the snow used for drinking water at the higher camps as well as in the home water supply of the expedition members. No measurement of total energy expenditure was made for any subject while at sea level and thus no energy expenditures comparisons can be made between these altitudes.

In contrast to the report by Pulfrey and Jones (1996)Citation , all data points in the present study were used to calculate a least squares regression line of best fit over the 3-wk dosing periods. The two point doubly labeled water model assumes a constant disappearance rate of isotope and body water volume. However, we chose the least squares regression model of all data because a major energy expenditure by a subject on the day immediately preceding a urine collection may have resulted in a falsely low second point value. The two point model would have produced a falsely greater apparent energy expenditure for that period than what actually occurred over the entire 3 wk (Seale et al. 1989Citation ).

Statistical analysis of data.

Means, standard deviations and significance of differences among pairs of data sets were calculated by using Student's alternate unpaired, two-tailed t test, that assumes Gaussian distribution of the data with different standard deviations, with the Instat statistical program (GraphPad Software, San Diego, CA). Spearman's nonparametric correlation was performed to determine correspondence between expected weight loss and actual weight loss values. Because of the small sample size of the base camp personnel and the climbers reported in this study, significance was set at P <= 0.10 for all comparisons, rather than the customary value of P <= 0.05. Where significant differences were found, actual P-values are reported. We must emphasize that, although significant differences were found between the climbers and the base camp personnel, any significant differences may not be biologically meaningful because of the unavoidable differences in subject distribution based on gender, body weight, body mass index, and physical activity between the two groups.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Changes in body composition.

All base camp personnel and climbers were physically fit upon arrival at base camp (Table 1)Citation , as indicated by the low percent body fat. All subjects lost body weight throughout the expedition (Table 2)Citation . To determine if body mass was lost preferentially from different sites on the body, each anthropometric measure during exposure to altitude was expressed as a percentage of the value obtained upon initial arrival at base camp (Table 3Citation ).


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Table 2. Changes in muscle mass and fat mass of base camp personnel and climbers during the expedition1

 

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Table 3. Regional and whole body anthropometric measures in base camp personnel and climbers following 9 wk exposure to high altitude1

 
Because the loss of regional body mass occurred gradually, the final measure for each subject (which was almost always the lowest measurement) was compared to the value obtained upon arrival in base camp. These decreases in site-specific body composition were then averaged for base camp personnel (exposure to altitude) and the climbers (exposure to higher altitudes plus additional physical exertion) and ranked according to those body sites most affected in the climbers. Table 3Citation shows three of the four trunk skinfolds (abdomen, suprailiac, and chest) were markedly affected by exposure to altitude. Also affected were triceps and thigh skinfolds, followed by triceps, thigh and calf circumference, with abdomen circumference and subscapular skinfold being least affected (Table 3)Citation . Only changes in thigh and calf circumferences were significantly different (P = 0.06 and P = 0.04, respectively) between base camp personnel and climbers.

When changes in body weight, percent body fat, percent fat mass, and percent muscle mass were compared over the 9-wk study period, only changes in body weight were significantly lower (P = 0.07) in the climbers compared to the base camp personnel (Table 3)Citation . Also, the calculated percent fat mass (in kg) for all of the subjects, both upon arrival in base camp and at the end of the expedition, was significantly lower (P = 0.06 and P = 0.05, respectively) in the climbers than in the base camp personnel. Neither base camp personnel nor the climbers had a significantly lower percent body fat at the end of the expedition compared to the value obtained upon arrival in base camp, prior to prolonged exposure to high altitude.

Energy intakes and expenditures.

For each of the study periods, the total energy intakes were calculated from the diet records completed by the subjects (Table 4Citation , Reported intake, from Reynolds et al. 1998Citation ). Base camp personnel reported consuming 8.99 ± 0.93 MJ/d (2149 ± 222 kcal/d), and climbers reported consuming a mean of 12.25 ± 4.05 MJ/d (2928 ± 968 kcal/d), during the first and third 3-wk periods. The difference between groups was significant (P = 0.052).


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Table 4. Energy intakes in base camp personnel and climbers as reported, calculated, and adjusted, and energy expenditures determined from doubly labeled water excretion

 
At the first and the third 3-wk testing periods, mean energy expenditure over the 3-wk period was determined by measuring excretion of 2H and 18O in periodic 24-h urine collections (Table 4Citation , Energy expenditure). Energy expenditures ranged from a low of 11.19 MJ/d (2675 kcal/d, subject 2C-3) up to a high of 32.93 MJ/d (7871 kcal/d, subject 6C - 1). The mean average daily energy expenditure for base camp personnel (13.70 ± 2.26 MJ, 3274 ± 540 kcal) was significantly less than that of climbers (22.57 ± 6.55 MJ, 5394 ± 1565 kcal, P = 0.007). These energy expenditures ranged from 1.85 up to 3.82 times the REE (Table 5Citation ) measured at sea level prior to departure from the US, with a mean of 2.43 ± 0.45 for the base camp personnel compared to a mean of 2.98 ± 0.70 for the climbers. Subject 2C, who expended 3.68 times her REE during period 1, dropped to 1.85 times her REE in period 3, whereas Subject 7C increased his energy expenditure from 3.60 times his REE during period 1 up to 3.82 times his REE during period 3. Subject 7C was one of four who attempted to reach the summit twice during period 3.


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Table 5. Relation of energy expenditures to resting energy expenditures in base camp personnel and climbers

 
The difference between reported energy intake and measured energy expenditure for each subject reflects an apparent energy deficit (Table 4)Citation . The mean apparent energy deficit was 4.71 ± 1.49 MJ/d (1126 ± 356 kcal/d) for the base camp personnel and 10.31 ± 7.41 MJ/d (2464 ± 1771 kcal/d) for the climbers (P = 0.061). These data indicate that all subjects were in a prolonged negative energy balance; as such, they experienced a loss in body weight, grossly under-reported their energy intake or a combination of both.

Approximate changes in gross body composition for each subject were determined by subtracting kg fat mass at the end of study period 1 from kg fat mass upon arrival at base camp, and similarly for muscle mass at these same times (Table 2)Citation . This number was then summed for each subject and divided by 21 (the number of days in each study cycle) (Table 4Citation , Expected wt. loss.) Where appropriate, the same calculation was performed for study period 3. All base camp personnel showed an expected weight loss, as did most of the climbers, but Climber 5C-1 had a negative expected weight loss (i.e., weight gain), which resulted from a slight increase in both total muscle mass and fat mass (and perhaps total body water) during this first 3 wk of the study (Table 2)Citation .

As actual body weights were routinely measured by means of a digital scale during the expedition, we then calculated the average daily weight loss during the 21-d study period based on measurement of body weights (Table 4Citation , Actual wt. loss.) In contrast to the expected wt. loss, in which the mean values indicated that the base camp personnel would have been expected to lose more body weight per day than the climbers, the actual measured average daily weight loss was not significantly different for the climbers or for the base camp personnel, (0.139 ± 0.060 versus 0.086 ± 0.048 kg/d, respectively). There was no significant correlation between expected wt. loss and actual wt. loss for either base camp personnel or climbers.

From the above described calculated losses in kg body fat mass and muscle mass, an expected energy deficit was then calculated (Table 4)Citation based on the assumption that a loss of 1 kg body fat mass is equivalent to 32.22 MJ (7700 kcal), and a loss of 1 kg body muscle mass is equivalent to 23.01 MJ (5500 kcal); these values were summed for each study period and divided by 21. Similar to the differences in the "Expected wt. loss" column, calculations for the base camp personnel resulted in a greater expected energy deficit than for climbers, albeit not significantly (3.21 ± 2.88 versus 1.30 ± 1.20 MJ/d; 767 ± 688 versus 311 ± 287 kcal/d, respectively). The negative value for Climber 5C-1 resulted from the corresponding negative values for expected wt. loss, which was derived from the same estimated changes in body fat and muscle mass.

The expected energy deficit value for each subject was then subtracted from the apparent energy deficit. This value, the unaccounted energy deficit, accounted for changes in body composition and may be considered to approximate the magnitude of underreporting (positive values) or overreporting (negative values) of energy intake on the diet records by the subjects. There was a significant difference (P = 0.029) between mean values for base camp personnel and climbers (1.50 ± 1.48 versus 7.99 ± 7.06 MJ/d; 358 ± 354 versus 1910 ± 1687 kcal/d, respectively). It is uncertain, however, whether this difference is due to differences in physical exertion or to differences in subject profile for the two groups.

The unaccounted energy deficit value for each subject was added to the reported energy intake value (Table 4)Citation to yield an estimated adjusted energy intake. This value may more closely represent the actual average daily energy intake for each subject because it takes into account actual changes in body composition and body weight as well as reported energy intakes. The mean adjusted energy intake for the climbers was significantly greater (P = 0.002) than for the base camp personnel (20.63 ± 6.56 versus 10.50 ± 0.65 MJ/d; 4931 ± 1568 versus 2510 ± 155 kcal/d, respectively).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Subjects in the present study steadily lost weight, as has been reported in numerous other studies conducted at high altitude (Butterfield et al. 1992Citation , Hoyt et al. 1994Citation , Pugh 1962Citation , Pulfrey and Jones 1996Citation , Westerterp et al. 1992 and 1994Citation Citation ). The causes of this weight loss include transient increased basal metabolic rate (reviewed in Butterfield 1990Citation ), physical exertion, and decreased energy intake (Armellini et al. 1997Citation , Butterfield et al. 1992Citation , Hoyt et al. 1994Citation , Pulfrey and Jones 1996Citation , Reynolds et al. 1998Citation , Westerterp et al. 1992 and 1994Citation Citation ). The composition of this weight loss, however, is not clear, but was reported to include loss of fat mass, fat-free mass and body water (Armellini et al. 1997Citation , Braun et al. 1997Citation , Butterfield et al. 1992Citation , Kayser 1992 and 1994Citation Citation , Kayser et al. 1993Citation , Roberts et al. 1996Citation ). We provide here an estimation of reported and adjusted energy intakes, energy expenditures and regional changes in body composition that account for the deficit between energy intakes and expenditures during a climb to high and extreme altitudes.

Accurate determination of anthropometric measurements under extreme exertion and environmental conditions is difficult (Fulco et al. 1985Citation ). Factors, such as rapid loss of body mass of undetermined composition, marked or severe fluid shifts and significant cyclic dehydration, all impact upon the measured circumferences and skinfold thicknesses as well as any body composition measures calculated from these values. Also, changes in body composition of only a few kg can not be accurately determined by the methodologies used in this or other studies. Thus, any anthropometric measurements obtained under these circumstances must be regarded with some suspicion, as was recently emphasized by Pulfrey and Jones (1996)Citation . To minimize such skewing of our own measurements, we had the same two researchers make all measurements, with constant cross-checking of their measurements, and no measurements were performed on the day climbers returned to base camp. Instead, we allowed the climbers time to voluntarily rehydrate overnight before making any measurements, including that of body weight, and we encouraged generous ingestion of fluids during this period.

The data in Table 3Citation show that there was a preferential loss of body fat reserves, indicated by the greater impact on skinfold compared to circumference measurements. Skinfold measurements predominantly determine fat, whereas circumferences determine fat, muscle and bone (plus organs, where located). In fact, a substantial loss of percent fat mass in both climbers and base camp personnel with a relative increase in percent muscle mass in both groups was noted (Table 3)Citation . This latter observation may result in part from a sparing of muscle tissue during a time of concomitant loss of fat tissue. The final outcome is an apparent increase in muscle mass when, in fact, there is simply an increase in relative muscle mass rather than an increase in absolute muscle mass (Table 2Citation versus Table 3Citation ). This was also reported by Armellini et al. (1997)Citation . The differences between thigh and calf circumferences between base camp personnel and climbers may be related to gender differences between the two groups rather than to differential exposures to altitude and physical exertion.

Increased dietary energy intake can partially prevent or offset body mass losses (Pulfrey and Jones 1996Citation ), but because of the continued loss of body mass documented in this and previous studies (Hoyt et al. 1994Citation , Pugh 1962Citation , Pulfrey and Jones 1996Citation , Westerterp et al. 1992 and 1994Citation Citation ), increased dietary energy intake alone appears to be insufficient to meet the needs of some of the climbers (Table 4Citation , climbers 6C-1, 7C-1, 7C-3) to stem such losses at the altitudes experienced in this study. This is in contrast to the beneficial aspects of increased energy consumption at lower altitudes of 4,300 m (Butterfield et al. 1992Citation ). Accurate reports of energy intake at high and extreme altitudes have been sparse, but some recent high altitude climbing expeditions focusing on nutrition have provided some measure of confidence (Kayser 1992Citation , Pulfrey and Jones 1996Citation , Reynolds et al. 1998Citation , Westerterp et al. 1992Citation ).

Using a subset of the same subjects in our previous report (Reynolds et al. 1998Citation ), we focused on those who received a doubly labeled dose of water for the purpose of determining energy expenditure at high and extreme altitudes. During the expedition, energy expenditure, as measured by doubly labeled water excretion, averaged 2.43–2.98 times the REE for all subjects. These physical activity levels are greater than that of 1.9 reported for men working at 4,300 m (Butterfield et al. 1992Citation ), comparable to those of 2.2–2.4 reported by Westerterp et al. (1992 and 1994) and of 3.5 reported by Hoyt et al. (1994)Citation , but lower than the 5.0 reported by Westerterp et al. (1986)Citation and Saris et al. (1989)Citation for Tour de France cyclists. The comparability among values we obtained and those reported by others for high and extreme altitude climbers indicates the validity and similarity of our methods and procedures.

From the doubly labeled water experiment, energy expenditure was greater than reported dietary energy intake for all subjects studied (Table 4)Citation . This produced an apparent energy deficit which led, at least in part, to a loss of body mass (Table 2)Citation . However, the loss in measured body mass (actual wt. loss) was greater than expected (expected wt loss) from the difference between diet records and energy expenditure studies (actual weight loss being greater than expected weight loss, Table 4Citation ). Because all anthropometric measurements were made on the morning after return to base camp, which allowed time for voluntary rehydration, it is unlikely that loss of body water from the physical exertion of climbing could have accounted for this difference. This difference, then, resulted in an unaccounted energy deficit (Schoeller et al. 1990Citation , and Table 4Citation ) which, we believe, is attributable to a chronic and near unanimous under reporting of energy intakes during the research expedition. It is interesting to note that the climbers had a significantly greater mean unaccounted energy deficit than did the base camp personnel. This difference may be attributed to a greater focus by the climbers on surviving the environmental conditions on the mountain, and a diminished focus on maintaining accurate diet records, even though the principal author of this study was one of the climbers and focused intently on preparing an accurate and complete diet record.

As an anecdote to this situation, the principal author would, on numerous occasions during the expedition, fill out his food record while eating the evening meal, yet temporarily forget to include on the food record the food he was consuming at the time the record was being completed. This may have been a consequence of diminished cognition, which occurs at high altitude (Cavaletti et al. 1990Citation , Hornbein et al. 1989Citation , Regard et al. 1991Citation ), as well as to concentration on survival while on the mountain. Conversely, the three negative unaccounted energy deficit values (Table 4Citation , 4B-1, 8C-1 and 10C-1) suggest that there may also have been a slight amount of over reporting of foods consumed by a few subjects.

If one then adds the unaccounted energy deficit values to the reported energy intakes (Table 4)Citation , we obtained an adjusted energy value that may better represent actual energy intakes for the periods studied. However, it is not known whether a climber can actually consume in excess of 30 MJ (7200 kcal) energy while living and climbing under such extreme altitude circumstances (Table 4Citation , subject 6–1, ). It was reported that competitors in the Tour de France (Saris et al. 1989Citation , Westerterp et al. 1986Citation ) and bicyclists in the Race Across America (Clark et al. 1992Citation ) routinely consume energy in this range. If the values given in the Table 4Citation , Adjusted energy intake, do represent reasonable approximations of actual energy intake during the expedition, then such high intakes suggest a need to re-think the types and amounts of foods that should be made available to persons climbing to high and extreme altitudes. Such amounts of energy can generally only be provided by including adequate amounts of lipid in the diets, as was recommended by Imray et al., (1992)Citation and Reynolds et al. (1998)Citation .

The adjusted energy intakes reported here were higher than intakes for similar altitude exposures reported by others (Kayser 1992Citation , Pulfrey and Jones 1996Citation , Rose et al. 1988Citation , Westerterp et al. 1992Citation and 1994). The reason for this difference is not known, especially because we observed similar multiples over REE of energy expenditure. Perhaps the uncertainty in food and energy intakes as well as errors inherent in the calculations given in Table 4Citation can account for some of these differences. The uncertainties in obtaining accurate food and energy intakes in current sea level laboratory-based studies (Schoeller et al., 1990Citation ) only serve to emphasize the difficulty in obtaining accurate values under the more adverse environmental conditions that exist at high and extreme altitudes.

Because of the differences in body composition of the expedition personnel and the differences in energy expenditures (as measured by doubly labeled water technique), we attempted to determine if the energy expenditure was a function of either total body weight or of muscle mass. When we regressed daily energy expenditures per subject against kg body weight at the beginning of each of the two study periods, we found r = 0.50, r2 = 0.27 and P = 0.055. When we regressed daily energy expenditures per subject against the calculated kg muscle mass at the beginning of each of the two study periods, we found r = 0.52, r2 = 0.27 and P = 0.048. Although these regressions moved the interpretation from nonsignificant to significant (P = 0.055 versus P = 0.048), the actual correlation differences were minimal. We conclude that individual energy expenditures under these circumstances may be as much the result of mental determination as they are a function of muscle mass.

In summary, the data presented in this report indicate that there is an energy deficit during exposure to high and extreme altitudes that results in a loss of body mass but with a sparing of muscle mass. This energy deficit appears to not be met by traditional dietary patterns alone. In conjunction with our previous report on this expedition (Reynolds et al. 1998Citation ) and that of Helge et al. (1998)Citation , more attention needs to be given to inclusion and consumption of energy-dense foods and fluids to enhance physical endurance activities, such as occurs in climbing to high and extreme altitudes. The energy deficit experienced by climbers appears to result in a preferential loss of body fat reserves, which has also been reported by Armellini et al. (1997)Citation and Westerterp et al. (1992)Citation , and a relative sparing of muscle mass. The estimated adjusted energy intakes by the subjects in this study should serve as guidelines for selecting foods with adequate dietary energy for those who venture into harsh environments in the future.

Finally, this report would not be complete without a note of respect to the numerous unnamed colleagues of ours whose bodies yet remain in the frozen mountains as a silent reminder of the dangers and risks associated with climbing to high and extreme altitudes. Rest in peace, Friends.


    ACKNOWLEDGMENTS
 
Grateful appreciation is extended to James L. Seale and William V. Rumpler, Beltsville Human Nutrition Research Center, USDA, for their invaluable assistance and contributions to the dual label water energy expenditure and resting energy expenditure measurements. Without their help, this study could not have been accomplished. Sincere appreciation is also expressed to many persons at the US Embassy, Kathmandu, whose generous and innovative efforts made this entire study possible. Special appreciation is extended to Hunt Janin, Joan and George Smith, and Ambassador Milton Frank.


    FOOTNOTES
 
2 Abbreviation used: REE, resting energy expenditure. Back

Manuscript received November 5, 1998. Initial review completed December 23, 1998. Revision accepted April 13, 1999.


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