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FLUID REPLACEMENT AND HEAT STRESS Fluid Replacement and Heat Stress, 1993 Pp. 55-68. Washington, D.C. National Academy Press 5 Carbohydrate Supplements During and Immediately Post Exercise John L. Ivy1 INTRODUCTION Since the early studies of Christensen and Hansen (1939a,b), the importance of dietary carbohydrates has been recognized with respect to endurance during sustained, prolonged exercise. Christensen and Hansen (1939a) demonstrated a high-carbohydrate diet would significantly enhance endurance during prolonged exercise. They also observed that time to exhaustion was accompanied by hypoglycemia and that ingestion of a carbohydrate supplement at the time of exhaustion rapidly returned the blood glucose concentration back to normal and allowed considerable additional exercise to be performed (Christensen and Hansen, 1939b). On the basis of these results, Christensen and Hansen (1939a,b) suggested that fatigue during prolonged aerobic exercise was the result of depletion of the body's carbohydrate stores. Since the time of their classic research, many studies have been conducted to examine the role of dietary carbohydrates and carbohydrate supplements on aerobic endurance. In general, these 1 John L. Ivy, Exercise and Physiology and Metabolism Laboratory, The University of Texas at Austin, Austin, TX 78712
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FLUID REPLACEMENT AND HEAT STRESS studies have confirmed that aerobic endurance is directly related to the body's carbohydrate supply and that carbohydrate supplementation can enhance endurance performance. The purposes of this paper are to review the latest information on the effectiveness of carbohydrate supplements to improve aerobic endurance and to review the most effective means of rapidly replenishing the body's carbohydrate stores after exercise. CARBOHYDRATE SUPPLEMENTS DURING EXERCISE Continuous Exercise Christensen and Hansen (1939a,b) reported that a high-carbohydrate diet could delay the onset of hypoglycemia and increase the time to exhaustion during prolonged exercise and that a carbohydrate supplement ingested at the time of exhaustion could rapidly alleviate hypoglycemia and substantially prolong the exercise period. Bagby et al. (1978) demonstrated that continuous infusion of rats with glucose during moderate-intensity running reduced the rate of liver and muscle glycogen utilization and delayed the onset of fatigue. The use of carbohydrate food supplements intermittently during exercise has also been shown to improve endurance performance (Coyle et al., 1983, 1986; Fielding et al., 1985; Hargreaves et al., 1984; Ivy et al., 1979, 1983). To study this effect, we encouraged cyclists to maximize work output during 2 h of isokinetic cycling (Ivy et al., 1979). The subjects were fed either a placebo or 0.2 g of glucose polymer per kilogram of body weight every 15 min during the first 90 min of exercise. There was no improvement in total work accomplished between the placebo and glucose polymer trials. However, during the last 30 min of exercise, the work production for the glucose polymer trial exceeded that of the placebo trial by 11% (Figure 5-1). Of even greater interest was the finding that during the last 10 minutes of the glucose polymer trial, work production was increased to a level in excess of that found over the first 10 min of exercise. These findings were interpreted as indicating that glucose feedings may be of benefit during prolonged exercise lasting longer than 90 min (Ivy et al., 1979). To investigate this possibility, we had subjects walk to exhaustion while consuming a carbohydrate supplement or placebo (Ivy et al., 1983). Subjects walked on a motorized treadmill with the speed and incline set to elicit an exercise intensity of 45% maximal O2 uptake . The carbohydrate
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FLUID REPLACEMENT AND HEAT STRESS FIGURE 5-1 Work (kilopond meter) performed during isokinetic cycling. Source: Ivy et al. (1979). supplement was a 20% glucose polymer solution (120 g) that was administered in four equally divided dosages at 60, 90, 120, and 150 min following the start of exercise. It was found that the glucose polymer supplement prevented a decline in plasma glucose and significantly increased the time to exhaustion by 11.5%. At about this same time Coyle et al. (1983) conducted a study in which they had trained cyclists exercise to fatigue. The initial work rate was 74% , and the point of fatigue was defined as the time the subjects could not maintain an exercise intensity of 64% . The subjects were fed either a placebo or glucose polymer solution during exercise. During the glucose polymer trial, the subjects were fed a 50% solution containing 1.0 g of glucose polymer per kilogram of body weight 20 min after the start of exercise; after 60, 90, and 120 min they were fed a 6% solution containing 0.25 g of glucose polymer per kilogram of body weight. It was found that the glucose polymer supplement was beneficial only for those subjects who became hypoglycemic in the placebo trial. Time to fatigue for these subjects was 126 min during the placebo trial and 156 min during the glucose polymer trial.
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FLUID REPLACEMENT AND HEAT STRESS To determine the mechanism by which carbohydrate supplements enhance aerobic endurance, Coyle et al. (1986) had trained cyclists exercise at 70% to fatigue while ingesting a placebo in one trial or a glucose polymer solution (i.e., 2.0 g per kilogram of body weight at 20 min and 0.4 g per kilogram every 20 min thereafter) during another trial. Muscle biopsies were taken from the vastus lateralis to determine the rate of muscle glycogen utilization. During the placebo trial, fatigue occurred after 3 h of exercise as the plasma glucose declined to 2.5 mM and the respiratory exchange ratio declined from 0.85 to 0.80. When the subjects were fed the glucose polymer supplement, plasma glucose and carbohydrate oxidation were prevented from declining and exercise was tolerated for an additional hour. The pattern of muscle glycogen utilization, however, was not different during the first 3 h of exercise with the placebo or the carbohydrate feedings. The additional hour of exercise performed when carbohydrate was fed was accomplished with little reliance on muscle glycogen and without compromising carbohydrate oxidation. It was concluded that carbohydrate supplements used at a relatively high rate could provide the carbohydrate needed to sustain activity during the latter stages of prolonged exercise, when the muscle and liver glycogen stores have been severely reduced. Intermittent Exercise The effect of carbohydrate supplementation on endurance during intermittent work has been investigated by Hargreaves et al. (1984) and Fielding et al. (1985). In the study by Hargreaves et al. (1984), 10 trained cyclists exercised for 4 h, during which time they performed repeated 20-min bouts of cycling at 50% followed by 10 min of intense intermittent exercise (30 s at 100% followed by 2 min of rest). During the last sprint bout the subjects were timed to exhaustion. The subjects received a placebo or a sucrose supplement before and at various intervals during exercise. It was found that the sucrose feeding prevented blood glucose from declining and increased the final sprint performance by 45%. A similar exercise protocol was used by Fielding et al. (1985), but subjects were fed every hour or every half-hour. When subjects were fed sucrose every hour, blood glucose declined late in exercise and sprint performance was not different from that which occurred during the placebo treatment. However, when the subjects were fed at half-hour intervals, their blood glucose was prevented from declining and their sprint performance was significantly improved.
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FLUID REPLACEMENT AND HEAT STRESS Summary There is overwhelming evidence that carbohydrate supplements can improve endurance during prolonged physical activity of a continuous or intermittent nature. For the supplement to be effective, it must be taken in sufficient amounts to prevent a significant decline in blood glucose. This would require a carbohydrate intake of about 1 g/min, consumed at 15- to 30-min intervals and starting at least 30 min before blood glucose starts to decline. CARBOHYDRATE SUPPLEMENTS IMMEDIATELY AFTER EXERCISE Because of the paramount importance of muscle glycogen during intense, prolonged exercise (Ahlborg et al., 1967; Bergstrom et al., 1967; Hermansen et al., 1967) as well as exercise of an anaerobic nature (Jacobs, 1981; Klausen and Sjogaard, 1980), methods for increasing its concentration above normal (supercompensation) and replenishing the glycogen stores on a day-to-day basis have been studied extensively. Bergstrom and Hultman (1967a) observed that glycogen synthesis occurred most rapidly in muscle depleted of its glycogen stores. They also found that consumption of a high-carbohydrate diet for 3 days would elevate the glycogen concentration of muscle above normal, and that this phenomenon was restricted to muscle in which glycogen was previously depleted by exercise (Bergstrom et al., 1967). Subsequent studies by Costill et al. (1981) found that muscle glycogen could be resynthesized to normal pre-exercise concentrations within 24 hours, provided there had not been prior glycogen supercompensation and sufficient carbohydrate was made availabel. Costill et al. (1981) reported that the consumption of 150 to 600 g of carbohydrate per day resulted in proportionately greater muscle glycogen restoration during the 24-h period after exercise and that consumption of more than 600 g of carbohydrate per day was of no additional benefit. It was also demonstrated by Costill et al. (1971) that when the carbohydrate concentration of the diet was inadequate, successive days of intense, prolonged exercise resulted in gradual reduction in the muscle glycogen stores and a deterioration in performance (Figure 5-2). Although means of increasing muscle glycogen to above-normal levels in preparation for competition and maintaining normal glycogen levels on a day-to-day basis have been defined, there has been little research on how to maximize glycogen storage during the hours immediately following exercise. It should also be pointed out that the maximum amount of muscle glycogen stored when the subject eats a high-carbohydrate diet during the
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FLUID REPLACEMENT AND HEAT STRESS FIGURE 5-2 Effect of low-carbohydrate diet (45% of the calories) on muscle glycogen during 3 consecutive days of repeated 2-h running sessions at 70% . Source: Costill et al. (1971). 24 h immediately after exercise is approximately 80 µmol/g. Thus, it is possible that intensive exercise training could result in deficient muscle glycogen stores even when one is consuming a high-carbohydrate diet. Glycogen Storage Immediately After Exercise When a carbohydrate supplement is provided immediately after exercise, the rate of glycogen storage has generally been reported to be between 5 and 8 µmol/g (wet weight) per hour (Keizer et al., 1986; Maehlum et al., 1977, 1978). Maehlum et al. (1978) found that ingestion of 100 g (1.44 g per kilogram of body weight) of glucose 15 min after an exhaustive bicycle exercise resulted in a 7.1 µmol/g (wet weight) per hour glycogen storage rate in the quadriceps during the subsequent 135 min. Maehlum et al. (1977) also found a similar rate of glycogen storage following exercise when a carbohydrate-rich diet was consumed. Keizer et al. (1986) reported that providing approximately 300 g of carbohydrate either in liquid or solid form after exercise resulted in a glycogen storage rate of approximately 5 µmol/g (wet weight) per hour over the first 5 h of recovery.
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FLUID REPLACEMENT AND HEAT STRESS Time of Postexercise Carbohydrate Consumption In agreement with previous research findings, we have observed rates of glycogen storage between 5 and 8 µmol/g (wet weight) per hour during the hours immediately after exercise when a carbohydrate supplement was provided (Ivy et al., 1988a,b; Reed et al., 1989). In the first of three studies, we investigated the effect of the time of administration of the carbohydrate supplement on muscle glycogen recovery after exercise. Two grams of glucose polymer per kilogram of body weight was administered in a 25% solution either immediately after exercise (P-EX) or 2 h after exercise (2P-EX) (Ivy et al., 1988a). During the first 2 h after exercise, the rate of muscle glycogen storage was 7.7 µmol/g (wet weight) per hour for the P-EX treatment, but only 2.5 µmol/g (wet weight) per hour for the 2P-EX treatment. During the second 2 h of recovery, the rate of glycogen storage slowed to 4.3 µmol/g (wet weight) per hour during treatment P-EX, but increased to 4.1 µmol/g (wet weight) per hour during treatment 2P-EX (Figure 5-3). However, even with the increase, the rate of storage during the 2P-EX treatment was still 45% slower than that for the P-EX treatment during the first 2 h of recovery. The FIGURE 5-3 Muscle glycogen storage during the first 2 h and second 2 h of recovery for the P-EX treatment (open bars) and the 2P-EX treatment (closed bars). The asterisk means the value is significantly different from the basal rate of storage, which is represented by the glycogen storage rate during the first 2 h after exercise of treatment (2P-EX). P-EX, ingestion of the supplement immediately after exercise; 2P-EX, ingestion of the supplement 2 h after exercise. f means significantly different than treatment 2P-EX during the second 2 h of recovery (p<0.05). Source: Ivy et al. (1988a).
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FLUID REPLACEMENT AND HEAT STRESS results suggested that delaying the ingestion of a postexercise carbohydrate supplement reduces the rate of muscle glycogen storage. It was also noted that the fall in the glycogen storage rate during the P-EX treatment was accompanied by a decline in the blood glucose and insulin levels. We therefore investigated the possibility that the initial rate of glycogen storage following a postexercise carbohydrate supplement could be sustained by maintaining elevated blood glucose and insulin concentrations with multiple supplements. We also investigated whether the rate of muscle glycogen storage could be enhanced during the initial 4-h period after exercise by substantially increasing the amount of the carbohydrate consumed (Ivy et al., 1988b). The Effect of Multiple Supplements and Different Amounts of Glucose Polymer Subjects cycled for 2 h on three separate occasions to deplete their muscle glycogen stores. Immediately after and 2 h after exercise, they consumed 0 g (placebo, P), 1.5 g (low, L), or 3.0 g (high, H) of glucose polymer per kilogram of body weight from a 50% glucose polymer solution. Blood glucose and insulin declined significantly during exercise in each of the three treatments. They remained below the preexercise concentrations during recovery during the P treatment, but increased significantly above the preexercise concentrations during the L and H treatments. By the end of the 4-h recovery period, blood glucose and insulin were still significantly above the preexercise concentrations in both treatments. Consequently, the rate of muscle glycogen storage over the second 2 h of recovery remained similar to that which occurred during the first 2 h of recovery (Ivy et al., 1988a). This is in agreement with the recent finding of Blom et al. (1987) that providing a carbohydrate supplement at 2-h intervals resulted in a consistent rate of muscle glycogen storage during the first 6 h after exercise. Although there was a substantial difference in the amount of glucose consumed for the L (225 g) and H (450 g) treatments, there were no differences in the rates of muscle glycogen storage for these treatments (Figure 5-4). Supporting these results are previous studies demonstrating that a consistent rate of muscle glycogen storage occurs the first few hours following prolonged exhaustive exercise if the amount of carbohydrate consumed is above a threshold level (Blom et al., 1987; Keizer et al., 1986; Maehlum et al., 1977). For example, Blom et al. (1987) found that during the 6 h immediately following exhaustive exercise, the average glycogen storage rate was 5.7 µmol/g (wet
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FLUID REPLACEMENT AND HEAT STRESS weight) per hour whether 0.7 or 1.4 g of glucose per kilogram of body weight was consumed at 2-h intervals. When the carbohydrate supplement FIGURE 5-4 Muscle glycogen storage during the first 2 h and second 2 h of recovery for the placebo (P, solid bar), low (L, open bar), and high (H, cross-hatched bar) treatments. The asterisk indicates a significant difference from the placebo treatment. Source: Ivy et al. (1988b). was reduced to 0.35 g per kilogram, however, the rate of storage was reduced by approximately 50%. Effect of Glucose Infusion To determine the role of gastric emptying in muscle glycogen restoration after exercise, we compared the rates of glycogen storage after administering an oral glucose supplement and after bypassing gastric emptying by intravenous infusion of glucose (Reed et al., 1989). Following exercise bouts that resulted in depleted muscle glycogen stores, subjects received 3 g of glucose per kilogram of body weight in a liquid form (50% glucose polymers) or intravenously (20% sterile glucose). The liquid supplement was divided into two equal doses and was administered immediately after and 120 min after exercise. During the infusion treatment, glucose was administered continuously during the first 235 min of the 240-min recovery period. Providing the glucose by infusion as opposed to
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FLUID REPLACEMENT AND HEAT STRESS providing it orally resulted in a significantly greater rise in blood glucose, suggesting that gastric emptying had restricted the amount of glucose availabel to the muscle for storage (Figure 5-5). However, the rates of gly FIGURE 5-5 Blood glucose concentrations during exercise and recovery. Values are expressed as means ± standard errors of the mean in mg per 100 ml at each time point. Significant differences (p<0.05) between treatments are denoted by asterisks. Open squares, liquid treatment; closed squares, solid treatment; closed triangles, infusion treatment. Source: Reed et al. (1989). cogen storage were not significantly different between the liquid and infusion treatments ( Figure 5-6). These results indicate that the rate of glycogen storage after exercise is not limited by the gastric emptying rate of the supplement if the supplement contains sufficient carbohydrate. Differences in the Simple Carbohydrates Fructose, sucrose, and glucose are common dietary carbohydrates that are consumed during postexercise recovery for the purpose of restoring the
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FLUID REPLACEMENT AND HEAT STRESS body's glycogen stores. However, the blood glucose and insulin concentrations following their consumption differ considerably. For example, the rise FIGURE 5-6 Glycogen storage rates during recovery. Values are expressed as ± standard errors of the mean in µmol/g during each 120-min period. Open bar, liquid treatment; closed bar, solid treatment; hatched bar, infusion treatment. Source: Reed et al. (1989). in blood glucose and insulin following the ingestion of fructose is significantly lower than that following the ingestion of glucose (Blom et al., 1987). Because the ingestion of fructose, sucrose and glucose have different effects on blood glucose and insulin, several studies have been conducted to investigate their impact on glycogen restoration after exercise. Blom et al. (1987) found that ingestion of glucose and sucrose were twice as effective as the ingestion of fructose for the restoration of muscle glycogen. Blom et al. (1987) suggested that the differences between the glucose and fructose supplements were due to the ways the body handles these sugars. Fructose metabolism takes place predominantly in the liver (Zakin et al., 1969), whereas most glucose appears to bypass the liver to be stored or oxidized by muscle (Bergstrom and Hultman, 1967a). When infused, fructose gives rise to four times as much liver glycogen storage as glucose (Nilsson and Hultman, 1974). On the other hand, a considerably higher storage of muscle glycogen has been demonstrated in skeletal muscle after glucose infusion than after fructose infusion (Bergstrom and Hultman, 1967b). The similar rates of glycogen storage for the sucrose and glucose supplements could not be accounted for by Blom et al. (1987). Sucrose contains equimolar amounts of glucose and fructose. If muscle glycogen storage was chiefly dependent upon the glucose moiety of the disaccharide,
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FLUID REPLACEMENT AND HEAT STRESS one should expect a lower rate of glycogen storage from sucrose than from a similar amount of glucose. One possible explanation provided by Blom et al. (1987) was that fructose by virtue of its rapid metabolism in the liver compared with that of glucose (Zakin et al., 1969), inhibits postexercise hepatic glucose uptake, thereby rendering a larger proportion of absorbed glucose availabel for muscle glycogen synthesis. Summary The results suggest that the rate of muscle glycogen storage for the 2h immediately after exercise range between 5 and 8 µmol/g (wet weight) per hour, provided that a glucose supplement in excess of 1.0 g per kilogram of body weight is ingested. This rate of storage can be maintained up to 6 h after exercise if the blood glucose and insulin concentrations are sustained by providing supplements at 2-h intervals. Increasing the amount of carbohydrate consumption above 1.0 g/kg of body weight appears to have little affect on the rate of muscle glycogen storage. Additionally, it appears that carbohydrate supplements composed of glucose or glucose polymers would be more effective for the restoration of muscle glycogen after exercise than would supplements composed predominately of fructose. On the other hand, fructose appears to be a more effective carbohydrate for the replenishment of liver glycogen. Finally, it is suggested that gastric emptying does not limit the rate of muscle glycogen storage after exercise if sufficient carbohydrate is provided. REFERENCES Ahlborg, B., J. Bergstrom, L.G. Ekelund, and E. Hultman. 1967 Muscle glycogen and muscle electrolytes during prolonged physical exercise. Acta Physiol. Scand. 70:129-142. Bagby, G.J., H.L. Green, S. Katsuta, and P.D. Gollnick. 1978 Glycogen depletion in exercising rats infused with glucose, lactate, or pyruvate. J. Appl. Physiol. 45:425-429. Bergstrom, J., and E. Hultman. 1967a. Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210:309-310. Bergstrom, J., and E. Hultman. 1967b Synthesis of muscle glycogen in man after glucose and fructose infusion Acta Med. Scand. 182:93-107. Bergstrom, J., L. Hermansen, E. Hultman, and B. Saltin. 1967 Diet, muscle glycogen and physical performance. Acta Physiol. Scand. 71:140-1-50.
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FLUID REPLACEMENT AND HEAT STRESS Blom, P.C., A.T. Hostmark, O. Vaage, K.R. Kardel, and S. Maehlum. 1987 Effect of different post-exercise sugar diets on the rate of muscle glycogen synthesis. Med. Sci. Sports Exercise 19:491-496. Christensen, E.H., and O. Hansen. 1939a Arbeitsfahigkeit und Ermundung. Skand. Arch. Physiol. 81:160-171. Christensen, E.H., and O. Hansen. 1939b Hypoglykamie, Arbeitsfahigkeit und Ermundung. Skand. Arch. Physiol. 81:160-171. Costill, D.L., R. Bowers, G. Branam, and K. Sparks. 1971 Muscle glycogen utilization during prolonged exercise on successive days. J. Appl. Physiol. 31:834-838. Costill, D.L., W.M. Sherman, W.J. Fink, C. Maresh, M. Witten, and J.M. Miller. 1981 The role of dietary carbohydrates in muscle glycogen resynthesis after strenuous running. Am. J. Clin. Nutr. 34:1831-1836. Coyle, E.F., J.M. Hagberg, B.F. Hurley, W.H. Martin, A.A. Ehsani, and J.O. Holloszy. 1983 Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J. Appl. Physiol. 55:230-235. Coyle, E.F., A.R. Coggan, M.K. Hemmert, and J.L. Ivy. 1986 Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J. Appl. Physiol. 61:165-172. Fielding, R.A., D.L. Costill, W.J. Fink, D.S. King, M. Hargreaves, and J.E. Kovaleski. 1985 Effect of carbohydrate feeding frequencies and dosage on muscle glycogen use during exercise. Med. Sci. Sports Exercise 17:472-476. Hargreaves, M., D.L. Costill, A. Coggan, W.J. Fink, and I. Nishibata. 1984 Effect of carbohydrate feedings on muscle glycogen utilization and exercise performance. Med. Sci. Sports Exercise 16:219-222. Hermansen, L., E. Hultman, and B. Saltin. 1967 Muscle glycogen during prolonged severe exercise. Acta Physiol. Scand. 71:129-139. Ivy, J.L., D.L. Costill, W.J. Fink, and R.W. Lower. 1979 Influence of caffeine and carbohydrate feedings on endurance performance Med. Sci. Sports Exercise 11:6-11. Ivy, J.L., W. Miller, V. Dover, L.G. Goodyear, W.H. Sherman, S. Farrell, and H. Williams. 1983 Endurance improved by ingestion of a glucose polymer supplement. Med. Sci. Sports Exercise 15:466-471. Ivy, J.L., M.C. Lee, J.T. Bronzinick, Jr., and M.J. Reed. 1988a Muscle glycogen storage after different amounts of carbohydrate ingestion J. Appl. Physiol. 65:2018-2023. Ivy, J.L., A.L. Katz, C.L. Cutler, W.M. Sherman, and E.F. Coyle. 1988b Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J. Appl. Physiol. 64:1480-1485. Jacobs, I. 1981 Lactate, muscle glycogen and exercise performance in man. Acta Physiol. Scand. Suppl. 495:1-35. Keizer, H.A., H. Kuipers, G. van Kranengurg, and P. Guerten. 1986 Influence of lipid and solid meals on muscle glycogen resynthesis, plasma fuel hormone response, and maximal physical work capacity Int. J. Sports Med. 8:99-104.
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FLUID REPLACEMENT AND HEAT STRESS Klausen, K., and G. Sjogaard. 1980 Glycogen stores and lactate accumulation in skeletal muscle of man during intense bicycle exercise. Scand. J. Sports Sci. 2:7-12. Maehlum, S., A.T. Hostmark, and L. Hermansen. 1977 Synthesis of muscle glycogen during recovery after prolonged severe exercise in diabetic and non-diabetic subjects. Scand. J. Clin. Lab. Invest. 37:309-316. Maehlum, S., P. Felig, and J. Wahren. 1978 Splanchnic glucose and muscle glycogen metabolism after glucose feeding after-exercise recovery. Am. J. Physiol. 235:E255-260. Nilsson, L.H., and E. Hultman. 1974 Liver and muscle glycogen in man after glucose and fructose infusion Scand. J. Clin. Lab. Invest. 33:5-10. Reed, M.J., J.T. Bronzinick, Jr., M.C. Lee, and J.L. Ivy. 1989 Muscle glycogen storage postexercise: effect of mode of carbohydrate administration. J. Appl. Physiol. 66:720-726. Zakin, D., R.H. Herman, and W.C. Gordan. 1969 The conversion of glucose and fructose to fatty acids in human liver Biochem. Med. 2:427-437.
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