Fluid Replacement and Heat Stress, 1993

Pp. 23-36. Washington, D.C.

National Academy Press

3

Formulation of Carbohydrate-Electrolyte Beverages

David R. Lamb1

INTRODUCTION

The optimal formulation of carbohydrate-electrolyte beverages for the soldier in the field is an important consideration for the health and combat effectiveness of that soldier. This is especially true for soldiers who are exposed to thermal stress that leads to rapid dehydration and for those who are undergoing prolonged physical exertion that leads to both rapid dehydration and exhaustion. The combination of thermal stress and physical exertion makes beverage formulation even more critical. In this paper it is assumed that the role of the beverages in question is to replenish depleted body fluid stores for the purpose of minimizing dehydration and to supply carbohydrates for the purpose of forestalling exhaustion. Furthermore, the emphasis in this paper is on the role played by rates of gastric emptying and intestinal absorption associated with various beverage formulations in determining the efficacy of those formulations.

1  

David R. Lamb, Exercise Physiology Laboratory School of Health, Physical Education and Recreation, The Ohio State University, Columbus, OH 43210



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FLUID REPLACEMENT AND HEAT STRESS Fluid Replacement and Heat Stress, 1993 Pp. 23-36. Washington, D.C. National Academy Press 3 Formulation of Carbohydrate-Electrolyte Beverages David R. Lamb1 INTRODUCTION The optimal formulation of carbohydrate-electrolyte beverages for the soldier in the field is an important consideration for the health and combat effectiveness of that soldier. This is especially true for soldiers who are exposed to thermal stress that leads to rapid dehydration and for those who are undergoing prolonged physical exertion that leads to both rapid dehydration and exhaustion. The combination of thermal stress and physical exertion makes beverage formulation even more critical. In this paper it is assumed that the role of the beverages in question is to replenish depleted body fluid stores for the purpose of minimizing dehydration and to supply carbohydrates for the purpose of forestalling exhaustion. Furthermore, the emphasis in this paper is on the role played by rates of gastric emptying and intestinal absorption associated with various beverage formulations in determining the efficacy of those formulations. 1   David R. Lamb, Exercise Physiology Laboratory School of Health, Physical Education and Recreation, The Ohio State University, Columbus, OH 43210

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FLUID REPLACEMENT AND HEAT STRESS EFFECTS OF WITHHOLDING WATER BEFORE OR DURING PROLONGED EXERTION Early Experiments In 1944, Pitts et al. reported data from a series of experiments in which men walked on a treadmill for 1 to 4 h at 5.6 km/h up a 2.5% grade with or without fluid replenishment (Table 3-1). The environmental temperatures ranged from 32° to 38°C, the relative humidity was 35% to 83%, and the subjects were allowed to rest for 10 min each hour. When the subjects drank nothing during the walks, their rectal temperatures and pulse rates were usually higher and their sweat rates were lower than Table 3-1 Mean Heart Rates, Rectal Temperatures, and Sweat Rates after 4 h walking at 38°C and 35% relative humidity (n = 3-7) Fluid Type Heart Rate (beat/min) Rectal Temp. (°C) Sweat Rate (liter/h) None 154 38.9 0.76 Water ad libitum 143 38.4 0.74 Water each 15 min at sweat rate 132 38.3 0.08 0.2% NaCl each 15 min at sweat rate 131 38.3 0.81 3.5% Glucose each 15 min at sweat rate 126 38.1 0.71 Source: Pitts et al. (1944). when water, 2% saline, or 3.5% glucose in volumes equivalent to sweat loss were consumed every 15 min or when water was consumed in quantities that just satisfied thirst. These early experiments demonstrated that progressive dehydration during prolonged exertion in the heat can adversely affect cardiovascular function, as reflected by elevated heart rates, and temperature regulation, as indicated by high rectal temperatures and reduced sweat rates. More recent investigators have confirmed these observations (Candas et al., 1988). The experiments of Pitts et al. (1944) also suggested that thirst was not an adequate stimulus for the subjects to replace all of the water they lost as sweat. This was confirmed several years later in an experiment reported by Brown (1947), in which military recruits attempted to complete a 34-km hike in a desert environment at temperatures ranging from 30° to 33°C with or without free access to water. Without water, 7 of 13 subjects became

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FLUID REPLACEMENT AND HEAT STRESS exhausted before completing the hike and lost 7.5% of their body weight. When water was provided, only 1 of 9 subjects became prematurely exhausted, but the subjects still lost 4.5% of their body weight during the hike. More sophisticated contemporary studies have confirmed that during prolonged exertion in hot environments, one must consume more fluid than that which satisfies thirst if progressive dehydration is to be avoided (Hubbard et al., 1984). Reduced Plasma Volume and Increased Body Fluid Osmolality Even in the absence of significant dehydration during prolonged exertion, some of the plasma volume usually moves out of the capillaries and into the interstitial or intracellular spaces, but progressive dehydration during the exertion increases the overall loss of plasma. For example, Costill et al. (1981) measured fluid volume shifts in 7 men who cycled for 2 h at 50% of maximal oxygen uptake in a chamber with a temperature of 30°C and a relative humidity of 46%. After only 10 min of cycling, there was a plasma volume loss of 4.4%, and by the end of 2 h, the plasma volume was 9% less than the baseline. Another study showed a plasma volume loss of as much as 16% during prolonged exercise (Costill and Fink, 1974). A plasma volume loss of this magnitude indicates a significant reduction in the volume of circulating blood that is availabel to meet the increasing demands for blood by muscles for producing force and by skin for dissipating heat. A loss of plasma volume during exercise is often accompanied by a deterioration in the ability of the exerciser to regulate body temperature. However, it is apparent that there is no clear cause-and-effect association between plasma volume losses and failing temperature regulation because experimentally increasing or reducing plasma volume during exercise does not necessarily result in a systematic improvement or deterioration, respectively, in temperature regulation (Fortney et al., 1981, 1984; Nadel et al., 1980). The adverse effects of dehydration on temperature regulation appear to be a complex function of increased body fluid osmolality and decreased plasma volume (Fortney et al., 1984). Thus, even in the absence of a decrease in plasma volume, an increased plasma osmolality caused by dehydration raises the thresholds for initiation of the sweating response and vasodilation in the skin, but a decrease in plasma volume coincident with an increased plasma osmolality additionally reduces the rate of increase in skin blood flow for a given rise in core temperature and reduces the maximal rate of skin blood flow (Fortney et al., 1984; Nadel et al., 1980).

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FLUID REPLACEMENT AND HEAT STRESS Increased Circulatory Strain As plasma volume declines with progressively increasing dehydration and as the cutaneous vascular capacity increases because of greater demands for heat dissipation in prolonged exercise, the actively circulating blood volume decreases. This leads to a reduction in ventricular filling pressure, a fall in stroke volume, and a compensatory increase in heart rate (Candas et al., 1986; Francis, 1979; Rowell et al., 1966) that may be inadequate to prevent a reduction in cardiac output (Fortney et al., 1983; Nadel et al., 1980; Rowell et al., 1966). With increasing dehydration, circulation to the skin decreases to shift a greater percentage of the declining blood volume to the working muscles (Fortney et al., 1983). Unfortunately, this shift of fluids away from the skin reduces the ability of the body to dissipate heat and leads to a progressive increase in heat storage. Decreased Sweating Response Dehydration-induced decrements in plasma volume and increments in body fluid osmolality result in a decreased threshold for the onset of sweating, and a decrease in the rate of sweating for a given increase in core temperature (Fortney et al., 1984; Harrison et al., 1978). This deterioration in sweating leads to a reduced ability to dissipate heat by evaporation and thus leads to a higher core temperature during prolonged exercise in the dehydrated than in the hydrated condition (Candas et al., 1986, 1988; Costill et al., 1970; Francis, 1979; Sawka et al., 1983). Altered Electrolyte Distributions Sodium and chloride are the principal electrolytes lost in sweat, but sweat is hypotonic with respect to blood plasma so that sodium and chloride (and potassium) concentrations in plasma are usually elevated by 1% to 4% during prolonged exercise without fluid replenishment (Costill et al., 1970, 1974, 1976, 1981). Plasma magnesium concentrations either decrease (Costill et al., 1981) or are unchanged from those during rest (Costill et al., 1976). There seem to be no systematic changes with exercise in intracellular concentrations of sodium, chloride, or magnesium in skeletal muscle, perhaps because of variable changes in intracellular water (Costill et al., 1976, 1981). When expressed per unit of wet muscle weight, potassium concentrations in intracellular water typically decrease by 8% to 10% (Costill et al., 1981), but all electrolyte changes in muscle during prolonged

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FLUID REPLACEMENT AND HEAT STRESS exercise are very minor when expressed per unit of dry weight (Costill et al., 1976, 1981). EFFECTS OF WATER AND SALINE FEEDINGS DURING PROLONGED EXERCISE The early experiments of Pitts et al. (1944) on men marching in the desert showed that consumption of water, 0.2% saline, or 3.5% glucose to replace sweat loss resulted in lower heart rates and core temperatures and sometimes greater sweat rates than were noted in a no-fluid condition. Francis (1979) studied eight men under three different hydration treatments during, intermittent exercise consisting of eight 15-min bouts of cycling at 50% interspersed with 5-min recovery intervals. The room air temperature was 32°C, and the relative humidity was 60% to 65%. During the rest intervals, the subjects consumed either water or an electrolyte solution (20 mM sodium, 10 mM potassium, 1.3% glucose) sufficient to replace sweat losses, or no fluid at all. In the no-fluid condition, plasma volume loss after 2 h was 17.7%; when either fluid replacement beverage was consumed, no significant loss occurred. Similarly, compared with the no-fluid condition, heart rate was 15 to 20 beat/min lower, rectal temperature was 1°C lower, and plasma cortisol concentrations were significantly reduced when either fluid was consumed during exercise. In one experiment, four marathon runners ran on a treadmill for 2 h at 70% under each of three conditions: (1) no fluid, (2) 100 ml of water every 5 min during the first 100 min, or (3) 100 ml of a glucose-electrolyte beverage (20 mM sodium, 15.3 mM chloride, 2.4 mM potassium, 4.4% glucose) every 5 min for the first 100 min (Costill et al., 1970). Compared with the no-fluid treatment, both fluid replacement regimens significantly lowered rectal temperature and reduced the concentrations of sodium and chloride in plasma. Brandenberger et al. (1986) and Candas et al. (1986) compared the effects of five treatments: (1) no fluid, (2) water, (3) a hypotonic beverage (0.4 mM chloride, 0.04% glucose and fructose), (4) an isotonic drink (23.1 mM sodium, 16.7 mM chloride, 3.2 mM potassium, 2.0 mM calcium, 6.8% sucrose), and (5) a hypertonic sugar solution (7.55% glucose, 7.53% fructose) on temperature regulation and cardiovascular function during 4 h of intermittent cycling at a low intensity (mean = 85 watts) in a hot environment (34°C, 10°C dew point). Fluid was consumed every 10 min after 70 min of exercise in amounts calculated to replace 80% of sweat losses. Relative to the no-fluid condition, all four fluid replenishment regimes decreased rectal temperature, heart rate, plasma protein concentration,

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FLUID REPLACEMENT AND HEAT STRESS plasma osmolality, and losses of plasma volume, but did not significantly affect sweat rate or skin temperature. Although the hypertonic sugar solution tended to be less effective in minimizing homeostatic disturbances, there were few significant differences attributable to the beverage composition. One exception to this observation was that plasma volume was actually expanded during the isotonic drink treatment, whereas the other beverages only minimized the plasma volume loss found in the no-fluid condition. Hormones in this experiment were determined only for the no-fluid, water, and isotonic beverage treatments; and both water and the isotonic drink negated the rises in plasma concentrations of cortisol and vasopressin and in renin activity; aldosterone increases during exercise were significantly blunted only by the isotonic drink (Brandenberger et al., 1986). Efficacy of Electrolyte Replacement During Prolonged Exertion Because substantial quantities of sodium, chloride, and to a lesser extent, potassium are lost in the sweat during prolonged exertion, especially in the heat, many are concerned that this electrolyte loss should be replenished during exercise to maintain the appropriate distribution of electrolytes in the various fluid compartments of the body. However, there is little direct evidence of a beneficial effect of electrolyte replacement for any but a small proportion of endurance athletes. The fact that electrolyte concentrations in plasma usually rise during exercise without fluid replacement (Costill et al., 1970, 1974, 1976, 1981) indicates that electrolyte supplements are not needed. Furthermore, during repeated exposures to prolonged physical exertion, the kidneys very effectively conserve sodium and potassium so that the electrolyte balance is usually maintained when an athlete consumes a normal diet or a diet low in potassium (Costill et al., 1976), or a diet high or low in sodium (Armstrong et al., 1985). However, recent case studies have been reported in which athletes who participated in very prolonged exercise experienced severe hyponatremia, i.e., low plasma sodium concentrations during exercise (Hiller et al., 1985; Noakes et al., 1985) or up to 7 days after competition (Noakes et al., 1985). These athletes usually consumed large quantities of water or beverages low in electrolytes. Conceivably, ingestion of electrolyte beverages for soldiers sensitive to the development of hyponatremia could be effective in obliterating or reducing the severity of hyponatremia. It should also be noted that small amounts of sodium chloride in a beverage enhance palatability. Since palatability determines in large measure how much fluid a person will voluntarily ingest (Hubbard et al., 1984), it may well be that electrolytes in beverages are important to encourage consumption of as much fluid as possible. Finally, recent evidence

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FLUID REPLACEMENT AND HEAT STRESS suggests that sodium in fluid replacement beverages is important for maintaining the osmotic drive for drinking during recovery from prolonged exertion (Nose et al., 1988). Summary of Effects of Water and Saline Replacement on Homeostasis During Prolonged Exertion Fluid replacement during strenuous prolonged exertion is unquestionably beneficial in minimizing the adverse effects of dehydration on cardiovascular function and temperature regulation. Although not all studies have demonstrated significant improvements in all markers of cardiovascular function and temperature regulation, there is overwhelming cumulative evidence that fluid replacement lowers cardiovascular strain and improves thermoregulation when compared with cardiovascular strain and thermoregulation under conditions in which fluid is withheld during prolonged exertion. The value of electrolytes added to fluids consumed during prolonged exertion has yet to be conclusively demonstrated, but individuals susceptible to hyponatremia with water feedings alone may profit from electrolyte supplements. Also, sodium may be important for optimal rehydration following prolonged exertion. Furthermore, the low concentrations of electrolytes found in most fluid replacement beverages (Table 3-2) are apparently benign and may encourage fluid consumption by enhancing beverage palatability. Table 3-2 Approximate Composition of Beverages That May Be Consumed During Prolonged Exercise Beverage Type Sodium (mM) Potassium (mM) Sucrose (%) Glucose (%) Polymers (%) Fructose (%) Apple juice 2 31.0 2.9 9.0a - - Body fuel 450 16 2.0 - - 4.5 - Cola drinks 4 0.1 3.7 6.8a - - Exceed 10 5.0 - - 5.0 2.0 Gatorade 20 3.0 4.0 2.0 - - Gookinaid ERG 16 10.0 - 5.0 - - Isostar 23 5.0 6.8 0.1 0.1 - Lemonade 1 5.0 2.6 7.0a - - Orange juice 1 52.0 7.0 5.0a - - a variable mixture of glucose and fructose

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FLUID REPLACEMENT AND HEAT STRESS HOW IMPORTANT IS THE GASTRIC EMPTYING RATE OF A BEVERAGE CONSUMED DURING PROLONGED EXERTION A comprehensive analysis of the literature on gastric emptying and intestinal absorption related to beverages consumed during exercise has been published recently (Murray, 1987). Only highlights of this issue are addressed here. The first study of gastric emptying and intestinal absorption of beverages consumed during exercise was that of Fordtran and Saltin (1967). They studied the gastric emptying characteristics of water and a glucose-electrolyte solution (13.3% glucose, 0.3% sodium chloride) and the intestinal absorption of six sugar-saline solutions in five subjects at rest and after an hour of treadmill running at 70% . They found that gastric emptying rates were slightly reduced during exercise and that the effects of exercise on water absorption in the intestine were highly variable. Furthermore, gastric emptying rates for the 13.3% glucose solution were substantially slower than those for water. Subsequently, Costill and Saltin (1974) systematically varied the intensity of cycling exercise and the glucose content, temperature, and volume of beverages ingested during cycling. They showed that cycling at intensities up to 60% did not significantly reduce gastric emptying rates; intensities greater than 70% did. Having demonstrated that gastric emptying during moderate-intensity exercise was similar to that during rest, Costill and Saltin (1974) tested gastric emptying characteristics of various beverages in resting subjects. One of their findings was that a solution of 2.5% glucose in 34 mM saline had emptied as rapidly after 15 min as did the saline alone, whereas 5%, 10%, and 15% glucose added to the saline progressively slowed gastric emptying. These findings with measurements of gastric emptying 15 to 20 min after beverage ingestion were generally confirmed by others (Brener et al., 1983; Coyle et al., 1978; Foster et al., 1980; Hunt et al., 1985; Neufer et al., 1986). Gastric emptying of carbohydrate-containing beverages seems to be regulated to provide a fairly constant rate of energy delivery (i.e., 2.0 to 2.5 kcal/min) to the small intestine, regardless of the energy density or osmolality of the ingested beverage (Brener et al., 1983; Hunt et al., 1985). In other words, after a few minutes of unregulated emptying into the intestine, a solution containing 10% glucose should empty approximately half as quickly as a solution of 5% glucose to deliver energy to the intestine at the same rate. The gastric emptying rate for water is approximately 15 ml/min for the first 15 min and that for 5% carbohydrate is about 12 ml/min; solutions containing progressively greater concentrations of carbohydrate empty progressively more slowly (Brener et al., 1983). If the maximal rate of energy delivery from the stomach to the intestine is 2.0 to 2.5 kcal/min (120

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FLUID REPLACEMENT AND HEAT STRESS to 150 kcal/h), approximately 36.0 to 37.5 g of carbohydrate could be delivered to the intestine per hour. Thus, if a 6% carbohydrate solution were ingested, 600 to 625 ml would have to be emptied from the stomach each hour to provide maximal rates of energy delivery. At emptying rates of approximately 10 ml/min for such a solution, this maximal rate of energy delivery is clearly possible and practical (e.g., with 150 to 250 ml feedings of a 6% solution every 15 to 20 min). Theoretically, the difference between delivery of water and a 6% carbohydrate solution from the stomach to the intestine would be approximately 275 to 300 ml/h. If water and the glucose solution were absorbed from the intestine at similar rates, it would appear that fluid replenishment would be improved by 275 to 300 ml/h from the consumption of water compared with that of a 6% carbohydrate solution. However, because glucose stimulates water absorption from the intestine (Sladen and Dawson, 1969), this apparent advantage of water over a moderately concentrated glucose solution for fluid replacement may not exist (Murray, 1987). It should be noted that the previously cited studies of gastric emptying characteristics of ingested beverages typically did not include measurements of cardiovascular or thermoregulatory function or performance capacity while subjects were consuming the beverages during exercise. Nevertheless, it is widely believed that cardiovascular function, temperature regulation, and physical performance are adversely affected during prolonged exertion if the ingested beverages contain sugar concentrations greater than 2.5%. This belief is unfounded. EVIDENCE THAT MODERATELY CONCENTRATED CARBOHYDRATE-ELECTROLYTE SOLUTIONS ARE EFFECTIVE IN MAINTAINING HOMEOSTASIS, ARE ADVANTAGEOUS TO THE MAINTENANCE OF CARBOHYDRATE FUEL, AND MAY IMPROVE PERFORMANCE In a study of champion marathoners, Costill et al. (1970) found similar gastric residues remaining in the stomachs of three of four runners after a 2-h run at 70% , regardless of whether they drank 100 ml of water or a glucose-electrolyte beverage (4.4% glucose, 20 mM sodium, 2.4 mM K+) every 5 min for the first 100 min of the run. More importantly, rectal temperatures, heart rates, ventilation rates, oxygen uptakes, sweat rates, and hemoconcentration values were similar for both drink treatments. Our group investigated the effects of four beverages differing in their carbohydrate and electrolyte contents on homeostasis and performance in a cycling task to exhaustion (Brodowicz et al., 1984). Cyclists were asked to

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FLUID REPLACEMENT AND HEAT STRESS ride as long as possible at an intensity equal to 74% of their maximal oxygen uptake under each of the four drink conditions (Table 3-3). Rectal temperature, heart rate, plasma volume change, sweat rate, and ratings of perceived exertion and gastrointestinal distress were similar under all drink conditions. Blood glucose was higher with the carbohydrate beverages; and mean ride times (min) were 68.9, 70.8, 73.1, 75.1 for beverages P, M, L, and S, respectively (P<0.05 for P vs. S; Table 3). Glucose polymers provided no advantage over simple sugars in this experiment or in those reported by others (Massicotte et al., 1989; Mitchell et al., 1988; Murray et al., 1987; Owen et al., 1986). Because of the discrepancy between the published data showing slower rates of gastric emptying for beverages containing carbohydrate and electrolytes and the finding that assumed rates of gastric emptying Table 3-3 Beverages Used in the Study of Brodowicz et al. (1984) Beverages Composition P Flavored water, 0.1 mM Na+ L 2.5% Glucose, 10.2 mM Na+ M 6% Glucose polymers, 10.2 mM Na+ S 4.6% Sucrose, 2% glucose, 20.4 mM Na+ had no apparent bearing on homeostasis or performance, we developed a simplified procedure to track the accumulation in plasma of deuterium oxide (D2O) from D2O-labeled beverages (Davis et al., 1987). We used this D2O accumulation as an index of relative rates of fluid entry into the blood after ingestion of various beverages. We found that the technique could easily distinguish between D2O accumulation rates for drinks with known differences in gastric emptying characteristics. Profiles for D2O accumulation in plasma of rested subjects were indistinguishable for water and drinks containing carbohydrate concentrations up to 10% (Davis et al., 1990). We also found that D2O accumulation profiles for water and for beverages containing carbohydrate concentrations of 2.5% and 6% were indistinguishable during prolonged exertion (Davis et al., 1988a). However, D2O accumulation was significantly retarded by beverages containing 12% carbohydrate (Davis et al., 1988b). The 12% carbohydrate beverage was also closely associated with symptoms of gastrointestinal discomfort and failure to complete the required cycling task. Owen et al. (1986) compared water, a 10% glucose polymer solution, and a 10% glucose solution ingested in volumes of 200 ml every 30 min during treadmill running at 65% for 2 h in a hot environment; they detected no significant beverage effects on gastric emptying, plasma volume

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FLUID REPLACEMENT AND HEAT STRESS changes, rectal or mean skin temperatures, or sweat rates. In another comparison of water and beverages containing 5%, 6%, or 7.5% carbohydrate, it was found that all carbohydrate beverages improved performance relative to water in maximal 12-min cycling sprints following seven 12-min sprints at 70% interspersed with 3-min rest intervals (Mitchell et al., 1988). Furthermore, no important beverage-related effects were detected for plasma volume changes, weight loss, oxygen uptake, or gastric emptying. Presumably, the fact that fluid feedings in this experiment were given in relatively small volumes (167 ml) intermittently as opposed to a 400-ml single feeding (Costill and Saltin, 1974) explained the lack of gastric emptying differences among the different beverages. Coupled with numerous other reports (see Costill, 1988, and Murray, 1987, for reviews) that show benefits to prolonged exercise performance when carbohydrate is consumed during exercise, the studies cited in this section show that any differences in gastric emptying that may exist among water and beverages with moderate (5% to 8%) concentrations of carbohydrate are of little importance in determining the efficacy of a beverage for minimizing disturbances in homeostasis and for maximizing performance. In fact, moderately concentrated carbohydrate-electrolyte solutions improve the supply of carbohydrates to the tissues and are usually associated with improved physical performance. Finally, despite numerous comparisons of alternative formulations, there seems to be no evidence that any of these are superior to those of many of the availabel commercial beverages. REFERENCES Armstrong, L.E., D.L. Costill, W.J. Fink, D. Bassett, M. Hargreaves, I. Nishibata, and D.S. King. 1985 Effects of dietary sodium on body and muscle potassium content during heat acclimation. Eur. J. Appl. Physiol. 54:391-397. Brandenberger, G., V. Candas, M. Follenius, J.P. Libert, and J.M. Kahn. 1986Vascular fluid shifts and endocrine responses to exercise in the heat: effect of rehydration. Eur. J. Appl. Physiol. 55:123-129. Brener, W., T.R. Hendrix, and P.R. McHugh. 1983Regulation of the gastric emptying of glucose. Gastroenterology 85:76-82. Brodowicz, G.R., D.R. Lamb, T.S. Baur, and D.F. Connors. 1984Efficacy of various drink formulations for fluid replenishment in the heat. Med. Sci. Sports Exercise 16:138. Brown, A.H. 1947Dehydration exhaustion. Pp. 208-225 in Physiology of Man in the Desert, E.F. Adolph and Associates, eds. Interscience, New York. Candas, V., J.P. Libert, G. Brandenberger, J.C. Sagot, C. Amoros, and J.M. Kahn. 1986Hydration during exercise: effects on thermal and cardiovascular adjustments. Eur. J. Appl. Physiol. 55:113-122.

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FLUID REPLACEMENT AND HEAT STRESS Candas, V., J.P. Libert, G. Brandenberger, J.C. Sagot, and J.M. Kahn. 1988Thermal and circulatory responses during prolonged exercise at different levels of hydration. J. Physiol. ( London) 83:11-18. Costill, D.L. 1988Carbohydrates for exercise: dietary demands for optimal performance Int. J. Sports Med. 9:1-18. Costill, D.L., and W.J. Fink. 1974Plasma volume changes following exercise and thermal dehydration. J. Appl. Physiol. 37:521-525. Costill, D.L., and B. Saltin. 1974Factors limiting gastric emptying during rest and exercise. J. Appl. Physiol. 37:679-683. Costill, D.L., W.F. Kammer, and A. Fisher. 1970Fluid ingestion during distance running. Arch. Environ. Health. 21:520-525. Costill, D.L.,L. Branam, D. Eddy, and W. Fink. 1974Alterations in red cell volume following exercise and dehydration J. Appl. Physiol. 37:912-916. Costill, D.L., R. Cote, and W. Fink. 1976Muscle water and electrolytes following varied levels of dehydration in man. J. Appl. Physiol. 40:6-11. Costill, D.L., R. Cote, W.J. Fink, and P. Van Handel. 1981Muscle water and electrolyte distribution during prolonged exercise Int. J. Sports Med. 2:130-134. >Coyle, E.F., D.L. Costill, W.J. Fink, and D.G. Hoopes. 1978Gastric emptying rates for selected athletic drinks. Res. Q. 49:119-124. Davis, J.M., D.R. Lamb, W.A. Burgess, and W.P. Bartoli. 1987Accumulation of deuterium oxide in body fluids after ingestion of D2O-labeled beverages. J. Appl. Physiol. 63:2060-2066. Davis, J.M., D.R. Lamb, R.R. Pate, C.A. Slentz, W.A. Burgess, and W.P.Bartoli. 1988aCarbohydrate-electrolyte drinks: effects on endurance cycling in the heat. Am. J. Clin. Nutr. 48:1023-1030. Davis, J.M., W.A. Burgess, C.A. Slentz, W.P. Bartoli, and R.R. Pate. 1988bEffects of ingesting 6% and 12% glucose/electrolyte beverages during prolonged intermittent cycling in the heat. Eur. J. Appl. Physiol. 57:563-569. Davis, J.M., W.A. Burgess, C.A. Slentz, and W.P. Bartoli. 1990Fluid availability of sports drinks differing in carbohydrate type and concentration. Am. J. Clin. Nutri. 51:1054-1057. Fordtran, J.S., and B. Saltin. 1967Gastric emptying and intestinal absorption during prolonged severe exercise. J. Appl. Physiol. 23:331-335. Fortney, S.M., E.R. Nadel, C.B. Wenger, and J.R. Bove. 1981Effect of blood volume on sweating rate and body fluids in exercising humans. J. Appl. Physiol. 51:1594-1600. Fortney, S.M., C.B. Wenger, J.R. Bove, and E.R. Nadel. 1983Effect of blood volume on forearm venous flow and cardiac stroke volume during exercise. J. Appl. Physiol. 55:884-890. Fortney, S.M.,C.B. Wenger,J.R. Bove, and E.R. Nadel. 1984Effect of hyperosmolality on control of blood flow and sweating. J. Appl. Physiol. 57:1688-1695.

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