|Protein-Energy Interactions (IDECG, 1991, 437 p.)|
|Exercise, aging and protein metabolism|
The substantial energy requirements of endurance exercise are primarily met by the oxidation of skeletal muscle glycogen and triglycerides as well as hepatic glycogen and adipocyte triglyceride stores as blood-born glucose and free fatty acids. These fuels can satisfy 90 to 95% of the total energy requirement. The remainder is met by the oxidation of protein which, unlike fats and carbohydrate, is a non-renewable source of energy.
This review will focus on the relationship between endurance and strengthening exercise and protein metabolism, and the evidence for increased dietary protein requirements. For the most part, two experimental approaches have been used. Early studies used the appearance of nitrogen-containing waste products, especially urea, in blood and urine as an index of protein oxidation. Changes in the oxidation of individual amino acids using isotope labels as tracers have been employed more recently.
The theory of the great German chemist JUSTUS VON LIEBIG (1870) that protein was the primary fuel of working muscle was tested by a number of 19th century scientists. FICK and WISCLICENUS (1866) hiked up the Faulhorn in 1865 and collected their urine for nitrogen analysis before and during the hike. Unfortunately, they confounded their results by placing themselves on a protein-free diet the day be fore their climb, thereby certainly reducing their urinary nitrogen excretion. They also stopped their urine collection upon completion of the climb and, therefore, eliminated the detection of any post-exercise rise in urinary nitrogen loss. They concluded that protein oxidation provided only a small portion of the energy required to make their climb. In a review, CATHCART (1925) also reached the conclusion that a slight increase in nitrogen excretion during and following work confirms the notion that protein oxidation does not provide the major source of energy for the working muscles.
The availability of carbohydrate as a fuel during exercise influences the oxidation of protein. LEMON and MULLIN (1980) estimated that the oxidation of protein (from serum, urine, and sweat urea losses) during prolonged submaximal exercise, when their subjects were glycogen-depleted, was double (up to 12% of the total energy demand) when compared to similar exercise in the glycogen-loaded state.
Paradoxically, exercise in the heat (30°C) is associated with a lower rate of protein utilization when compared to that seen during and for two days following similar exercise in 5° and 20°C. Exercise in a hot environment has been demonstrated to increase the rate of glycogen utilization (FINK, COSTILL and VAN HANDEL, 1975), a condition which should be associated with increased rates of protein utilization.
Gender differences in substrate utilization during prolonged submaximal exercise have also been seen. TARNOPOLSKY and coworkers (1990) have shown that a group of female athletes, matched to males by age and VO2 max, used significantly less glycogen and protein (estimated from 24-hour urinary nitrogen excretion) than did men while running on a treadmill at 65% VO2 max.
A number of studies have used the primed, constant infusion of 13C-leucine to measure the rate of oxidation of this essential amino acid during exercise. These studies indicate that submaximal exercise does not alter leucine flux, but substantially increases the rate of whole-body leucine oxidation (KNAPIK et al., 1991; MILLWARD et al., 1982; RENNIE et al., 1980). RENNIE and co-workers (1981) demonstrated that the increase in leucine oxidation rates was directly related to the intensity of exercise. KNAPIK and co-workers (1991) found that a complete 3.5-day fast did not cause an increase in leucine flux during exercise but caused a 44% increase in the rate of leucine oxidation.
We demonstrated that high-intensity exhaustive exercise caused a significant 48% accumulation of muscle a-ketoisocaproic acid (KIC) (FIELDING et al., 1986). The elevation in muscle KIC concentration was not reflected in simultaneous changes in plasma KIC levels, suggesting a limited diffusion rate from muscle to blood. This study indicates that brief high-intensity exercise is associated with accelerated transamination of leucine.
DEVLIN et al. (1990) examined recovery from 3 hours of cycling at 75 % of VO2 max and found that whole-body protein breakdown was not increased above resting levels, leucine oxidation was decreased and non-oxidative leucine disposal (synthesis) was increased when compared to pre-exercise resting values. Using a much lower exercise intensity (4 hours at 40% VO2 max), CARRARO and co-workers (1990) also examined post-exercise recovery. They found a significant increase in the muscle fractional synthetic rate during the recovery period.
The concentration of urea in plasma and urine increases during submaximal exercise and remains high for some time later, also in proportion to the intensity and duration of the exercise (LEMON, DOLNY and YARESHESKI, 1984; HARALAMBIE and BERG, 1976). The increased oxidation of indispensable amino acids during submaximal exercise must, therefore, increase the need for dietary protein.
While the experiments examining protein metabolism using 13C-leucine (or other labeled amino acids) indicate increased oxidation during exercise, these studies do not directly show an increased requirement for dietary protein. GONTZEA, SUTZESCU and DUMITRACHE (1974) conducted a carefully controlled study in which 30 healthy young men consumed a diet containing 1.0 g protein/kg body weight. Nitrogen balance determinations were performed for three periods, a sedentary adaptation period, a 4-day exercise period, and a 4-day sedentary post-exercise period. The daily exercise consisted of six 20-minute intervals on a cycle ergometer at an intensity of 8-10 kcal/min, separated by 30-minute breaks. Energy intake was adjusted during the exercise period to provide an extra 50 kcal/kg body weight/d. Sweat nitrogen losses were included in the calculation of nitrogen balance. The mean became negative during the exercise period and did not become positive, even when the dietary protein intake was increased to 1.5 g/kg/d. A follow-up study examined the effect of a longer training period on nitrogen balance using a similar exercise load and a diet containing 1.0 protein/kg/d. Nitrogen balance became negative with the onset of the exercise period, but approached equilibrium by 2 weeks of training. The subjects in these studies were initially sedentary, and therefore the studies of GONTZEA, SUTZESCU and DUMITRACHE (1974; 1975) do not address the question of whether athletes, who have adapted to a high-level training intensity and duration, have a high protein requirement when energy demands are met.
TARNOPOLSKY, MacDOUGALL and ATKINSON (1988) attempted to determine the protein requirements in body builders and endurance-trained men. They examined nitrogen balance in these athletes on two different dietary protein intakes, both of which were above the amount required for achievement of balance. By extrapolating a line connecting the balance figures on two levels of protein intake, they estimated that bodybuilders required 1.12 times and endurance athletes required 1.67 times more daily protein than did sedentary controls. However, these protein requirements were extrapolated from nitrogen balance obtained with protein intakes of 1.7 and 2.65 g/kg/d and almost certainly overestimated protein requirements when compared with results that were closer to zero and included negative values.
Using nitrogen balance to estimate dietary protein requirement at three different dietary intakes (0.6, 0.9 and 1.2 g/kg/d of high-quality protein over three separate 10-day periods), we (MEREDITH et al., 1989b) found that habitual endurance exercise was associated with dietary protein needs greater than the current Recommended Dietary Allowance of 0.8 g/kg/d and average 0.94 ± 0.05 g/kg/d. No age-related differences in protein requirements were seen in the six young (20-30 years) and six middle-aged (48-59 years) men examined in this study. Whole-body protein turnover, using 15N glycine as a tracer, and 3-methylhistidine excretion were not different from values reported for sedentary men, and were not different between the two age groups. Protein requirements expressed as a percent of energy needs (averaging 3910 ± 240 kcal/d) showed that these subjects needed only 6.9 ± 0.5% of total dietary calories as protein. These results suggest that well-trained individuals, consuming an average American diet (12-15% protein) and adequate amounts of energy, are not likely to have an inadequate dietary protein intake.
We examined the dietary intake of a group of eumenorrheic and amenorrheic athletes with similar exercise habits (NELSON et al., 1986). There were no differences between the two groups in VO2 max, number of miles run per week, or in body composition.
When compared to the eumenorrheic athletes, the amenorrheic women reported consuming less energy (1730 ± 152 vs 2250 ± 141 kcal) and protein (0.7 ± 0.1 vs 1.0 ± 0.1 g/kg/d). This implicates inadequate dietary energy and/or protein as a potential cause of athletic amenorrhea. When compared to the eumenorrheic women, the amenorrheic athletes have lower estradiol, estrone, LH (and LH pulse amplitudes), FSH, and T3 levels (FISHER et al., 1986), a hormone profile often seen in women on severely hypocaloric diets or women suffering from protein-energy malnutrition.