Limits to sustainable human metabolic rate
Department of Human Biology, Maastricht University, PO Box 616, 6200 MD Maastricht, The Netherlands
*e-mail: K.Westerterp{at}HB.Unimaas.NL
Accepted June 28, 2001
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Summary |
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Key words: doubly labelled water, food intake, energy expenditure, energy balance, body composition, physical activity, exercise, high altitude.
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Introduction |
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Daily energy expenditure consists of four components, the sleeping metabolic rate (SMR), the energy cost of arousal, the thermic effect of food, or diet-induced energy expenditure (DEE), and the activity-induced energy expenditure (AEE). Daily energy expenditure is sometimes divided into three components, taking sleeping metabolic rate and the energy cost of arousal together as energy expenditure for maintenance or basal metabolic rate (BMR). BMR is usually the main component of average daily metabolic rate (ADMR). DEE is assumed to be 10% of ADMR in subjects consuming the average mixed diet and being in energy balance. AEE is the remaining and most variable component of ADMR. Physical activity can be limited by sustainable metabolic rate.
The doubly labelled water method has provided truly quantitative estimates of AEE in daily life. Subsequently, however, there is no consensus on the way to normalize AEE for differences in body size. A frequently used method to quantify physical activity is by expressing ADMR as a multiple of BMR or SMR (FAO/WHO/UNU, 1985). This assumes that variations in ADMR are due to body size and physical activity. The effect of body size on ADMR is corrected for by expressing ADMR as a multiple of BMR or SMR. Physical activity level (PAL) is equal to ADMR/BMR or ADMR/SMR.
The focus of the current review is on PAL in the general population, exercise-induced possibilities to increase energy intake and thus to increase PAL, changes in body composition and limits to PAL at high altitude.
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Physical activity level in the general population |
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Exercise-induced changes in energy intake |
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The upper limit of power output during endurance activities can be increased when energy-dense, carbohydrate-rich food is eaten during the exercise, a practice common in endurance sports. Energy-rich drinks make up a substantial proportion of energy intake in professional athletes. Sjödin et al. (Sjödin et al., 1994) reported a contribution of 16% of energy intake and 25% of carbohydrate consumption by carbohydrate-rich formulae in athletes with a PAL of up to 4.5 over a 6-day training period. Subjects were cross-country skiers in the Swedish national team studied in a training camp. It was shown that energy intake matched energy turnover at the high PAL. The mean difference between energy turnover and energy intake for the group of four women and four men was 0.1±1.9MJday-1. In the Tour de France of 1984, athletes maintained energy balance at a PAL of 3.55.5 (Westerterp et al., 1986). Body mass and body composition did change significantly over the 23-day race. None of the studies of soldiers during field training mentions the use of energy-dense, carbohydrate-rich liquid formulae during exercise.
The question remains as to whether a further increase in food intake would result in an upward shift of the limit of sustainable PAL of approximately 5, the value achieved in professional athletes. The capacity to eat and process food certainly limits the energy supply. The absorption capacity of the small intestine is thought to be a limiting factor. The evolutionary design of the intestinal nutrient absorption system is adequate but not too great (Diamond, 1991). Brouns et al. (Brouns et al., 1989) showed that athletes maintained energy balance during a Tour de France simulation in a respiration chamber on a conventional solid diet with a high carbohydrate content and supplemented with a 20% enriched carbohydrate liquid. The energy intake was 510MJday-1 too low when the same diet was available ad libitum without the supplement.
In conclusion, the upper limit of sustainable metabolic rate in professional athletes is twice the upper limit in the general population. Two important contributors to the upward shift in PAL are that endurance athletes have learned to ingest large amounts of food and incorporate a significant amount of carbohydrate-rich drinks in their diet. They often follow a continuous eating pattern consisting of many small meals at short intervals.
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Exercise-induced changes in body composition |
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To allow comparisons of FFM and FM among subjects, the components need to be corrected for differences in body height. FFM and FM are expressed as indices, FFMI and FMI, respectively, where FFMI=FFM/height2 and FMI=FM/height2 (FM and FFM are in kg and height is in m). The correction is by analogy with the body mass index (BMI)(Quetelet, 1871): BMI=FFMI+FMI. In the normal, sedentary population, there is a highly significant relationship between FFMI and FMI in both sexes (Westerterp et al., 1992c). Subjects with a higher FM have a higher FFM. Plotting FFMI against FMI in a linear regression analysis resulted in approximately the same slope for both sexes. The slope of the regression of 0.260.36 meant that a subject with 1.00kg more FM has on average 0.260.36kg more FFM, comparable with the composition of mass gain in obese subjects. Fig.2 shows the calculated linear regression lines for FFMI plotted against FMI for the subjects with PALs presented in Fig.1. Data for elite athletes, four women and four men from the Swedish national cross-country ski team, are also plotted. PAL was 3.4±0.3 for the female skiers and 4.0±0.5 (means ± S.D.) for the male skiers (Sjödin et al., 1994). The athletes clearly show an increased FFMI, adjusted for FMI. All subjects, women as well as men, fall well above the sex-specific regression line and the upper 95% confidence limits for the general population. The lower value for one of the four women was for a subject with a previous history of anorexia nervosa.
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To summarize, in elite endurance athletes, maintenance metabolic rate is increased for two reasons: FFM is higher than in subjects with a lower PAL (Fig.2), and maintenance metabolic rate adjusted for FFM is also higher. The suggestion that an increased substrate flux is a determinant of the increased maintenance metabolic rate is confirmed by the value of BMR for the skier with a previous history of anorexia nervosa. She had a much lower BMR (by 16%) than those of the other female skiers but matched the sedentary controls as well as theoretical calculations (Sjödin et al., 1996). The effect of exercise on maintenance metabolic rate was not observed in intervention studies in which (sedentary) subjects reached a PAL in the range 2.02.5, the upper limit observed in the general population (Fig.1)(Westerterp, 1998).
The absence of a long-term effect of exercise on RMR is surprising. Most studies show an exercise-induced change in FFM, the main determinant of RMR. We induced an increase in FFM from 49.5±7.3 to 52.2±7.6kg (means ± S.D., N=23, P<0.001) in novice athletes participating in a 44-week training programme to run a half-marathon. SMR did not increase; in fact, the opposite occurred: SMR decreased by 0.3±0.5MJday-1 (mean ± S.D., N=23, P<0.05)(Westerterp et al., 1994). SMR as a function of FFM was lower after 40 weeks of exercise training than before training (Fig.3). The decrease in SMR was related to a decrease in body mass (r=0.62, P<0.01), possibly as a defence mechanism by the body to maintain body mass. The results contrast with findings for elite athletes, who maintain their body mass at extremely high values of PAL.
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Limits to sustainable metabolic rate at high altitude |
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The decrease in energy intake at high altitude is probably one of the determinants of a reduction in sustained metabolic scope. The average daily metabolic rate of the men exposed to a 31-day simulated stay at several altitudes up to the peak of Mount Everest, as described above, was higher than their energy intake, and the discrepancy increased during the exposure (Westerterp et al., 2000). Fig.4 shows the change in energy expenditure as a function of the change in energy intake from normoxia to progressive hypoxia. The reduction in ADMR was on average approximately one-third of the reduction in energy intake. A reduction in ADMR in a hypoxic environment where stresses such as cold exposure and exercise were avoided implicates mainly a reduction in energy expenditure for physical activity. Maintenance requirement at altitude is thought to be increased (Mawson et al., 2000) and, thus, at a given level of energy expenditure, there is less energy available for diet-induced and activity-induced energy expenditure. Only approximately 10% of the reduction in energy intake can be explained by a reduction in DEE because DEE is assumed to be 10% of ADMR in subjects consuming the average mixed diet and being in energy balance. The major proportion of a reduction in ADMR at high altitude will therefore be due to a reduction in AEE.
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Discussion |
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There are at least three explanations for the increase in the energetic ceiling in professional athletes. First, professional athletes are a selection of the population. Few people are born to be athletes. Second, they have to train for many years to reach their high level of performance. For many sports, training has to start at a young age for athletes to be able to compete successfully. Third, training includes exercise and the maintenance of energy balance at a high level of energy turnover. The latter implicates the supplementation of the diet with carbohydrate-rich liquid formulae. Highly trained athletes have learned how to eat the maximum amount of food during hard physical work.
An important aspect of performance at a high level of energy turnover is the machinery of the power supply. There are few data on endurance exercise and energy balance and fat-free mass. Fig.2 compares data for highly trained athletes with data for subjects from the general population. Endurance athletes are characterized by a high FFM adjusted for height and FM. Values for two of the four women were comparable with those for the four men, although women generally have a considerably lower FFM than men. Sustainable metabolic rate is probably limited by FFM. Maintaining FFM requires exercise training and energy balance. The resulting substrate flux increases BMR, even after adjustment for the enlargement of the FFM. The absolute value of BMR of 79MJday-1 (Sjödin et al., 1996) is equivalent to ADMR for a sedentary subject. Subjects such as novice athletes preparing for a half-marathon run increased FFM but did not show the FFM-adjusted increase in SMR (Fig.3) observed in professional athletes. This might be a reflection of the limitations of subjects from the general population to increase the substrate flux and thus the normal PAL ceiling of 2.02.5.
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Acknowledgments |
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