Fluid Replacement and Heat Stress, 1993

Pp. 69-83. Washington, D.C.

National Academy Press

6

Gastric Emptying During Exercise: Influence of Carbohydrate Concentration, Carbohydrate Source, and Exercise Intensity

Carl Foster1

INTRODUCTION

Physiologists commonly recommend the consumption of fluid (with or without electrolytes) and carbohydrate (CHO) during prolonged exercise, particularly prolonged exercise in heat. This recommendation is based on data showing improved thermoregulation and enhanced endurance secondary to fluid and CHO consumption, respectively. The rate at which solutions empty from the stomach is generally thought to be the primary limiting step in the process of fluid-energy replacement (Fordtran and Saltin, 1967). A number of factors have been identified that influence the rate of gastric emptying (Brouns et al., 1987), including: CHO concentration (osmolality), CHO source (osmolality), exercise intensity, meal volume, meal temperature, fat and protein in the ingestate, particle size, and dietary fiber. This review

1  

Carl Foster, University of Wisconsin Medical School, Sinai Samaritan Medical Center, 950 N. 12th Street, Milwaukee, WI 53201



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FLUID REPLACEMENT AND HEAT STRESS Fluid Replacement and Heat Stress, 1993 Pp. 69-83. Washington, D.C. National Academy Press 6 Gastric Emptying During Exercise: Influence of Carbohydrate Concentration, Carbohydrate Source, and Exercise Intensity Carl Foster1 INTRODUCTION Physiologists commonly recommend the consumption of fluid (with or without electrolytes) and carbohydrate (CHO) during prolonged exercise, particularly prolonged exercise in heat. This recommendation is based on data showing improved thermoregulation and enhanced endurance secondary to fluid and CHO consumption, respectively. The rate at which solutions empty from the stomach is generally thought to be the primary limiting step in the process of fluid-energy replacement (Fordtran and Saltin, 1967). A number of factors have been identified that influence the rate of gastric emptying (Brouns et al., 1987), including: CHO concentration (osmolality), CHO source (osmolality), exercise intensity, meal volume, meal temperature, fat and protein in the ingestate, particle size, and dietary fiber. This review 1   Carl Foster, University of Wisconsin Medical School, Sinai Samaritan Medical Center, 950 N. 12th Street, Milwaukee, WI 53201

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FLUID REPLACEMENT AND HEAT STRESS focuses on the first four of these factors in their relation to gastric emptying, with some thought to their application to the needs of the military. CARBOHYDRATE CONCENTRATION Early studies of gastric emptying conducted by J. N. Hunt and coworkers (Elias et al., 1968) demonstrated that the presence of mono- and disaccharides slowed the rate of gastric emptying. The magnitude of slowing was generally proportional to the CHO concentration in the test meal. Glucose was shown to be more effective, per osmole, in slowing gastric emptying than galactose. Fructose was shown to be relatively ineffective in slowing gastric emptying. The hypothesized mechanism for the delay of gastric emptying by ingestion of CHO was stimulation of duodenal osmoreceptors. This hypothesis has been supported by studies in which the infusion of glucose into the duodenum produced a profound and long-lasting suppression of gastric emptying (Brener et al., 1983). In a paper that defined the paradigm for exercise-gastric emptying work in the United States, Costill and Saltin (1974) noted a progressive decrease in the rate of gastric emptying with increases in the glucose concentration of the test meal. Their results are summarized in Figure 6-1. Coyle et al. (1978) compared the rate of gastric emptying for three commercially availabel drinks, all glucose/sucrose based, and for water. They noted a decrease in the rate of gastric emptying at CHO concentrations greater than 2.5 g per 100 ml. As with the data of Costill and Saltin (1974), the emptying characteristics of the drinks tested by Coyle et al. (1978) seemed to follow osmotic lines (Figure 6-1). Similar data were presented by Foster et al. (1980) with glucose concentrations as great as 40 g per 100 ml (Figure 6-1). More recent studies with glucose polymers have likewise suggested a reduction in the rate of gastric emptying somewhat proportional to the total CHO concentration. Although these differences are usually presented in the context of the purported advantage of glucose polymers over that of simple CHO relative to gastric emptying, it appears that the same basic response to increasing CHO concentration is followed. This is well illustrated in Figure 6-2, which compares the gastric emptying of various concentrations of glucose and glucose polymers. There has been less systematic work with glucose polymers; however, these early data (Foster et al., 1980) are generally supported in the literature. Seiple et al. (1983) reported no difference between 5% and 7% glucose polymer-fructose drinks. However, Seiple et al. (1983) used 30- and 60-min emptying periods. Examination of

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 6-1 Relationship of CHO concentration and osmolality of 400 ml of a test drink to the volume of a test drink emptied in 15-30 minutes. Data are adapted from Costill and Saltin (1974), Coyle et al. (1978), and Foster et al. (1980). In general, lower concentrations of simple CHO in the test drink result in a greater volume of the original drink emptied. The CHO concentration appears to exert its effect primarily through the hypothesized duodenal osmoreceptors.

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 6-2 Comparison of emptying curves for isocaloric test drinks based on glucose (G) or glucose polymers (P). At 5% CHO, the glucose polymer-based drink emptied significantly faster than glucose. At all other CHO concentrations, there were no differences in the amount of the drink emptied. The data on osmolality versus the amount emptied suggest considerable hydrolysis of the glucose polymer proximal to the duodenal osmoreceptors. Adapted from Foster et al. (1980).

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FLUID REPLACEMENT AND HEAT STRESS their data (Figure 6-3) indicates that at 30 min several of the subjects had already completely emptied their stomachs. The serial recovery method used in this study depends upon the ability to recover some of the original drink. Otherwise, there is no way to determine when the subjects stomach was empty, and thus make an estimate of gastric emptying rate. Thus, the data of Seiple et al. (1983) must be viewed very conservatively. Rehrer et al. (1989), using a different technique, the double sampling method, also demonstrated a reduction in the rate of emptying proportional to the concentration with maltodextrin (glucose polymer)-based drinks. Previously unpublished data from my laboratory (Figure 6-4) suggest that the gastric emptying rates of both glucose and glucose polymers decline with increasing CHO concentration. Even very low concentrations (<2 g per 100 ml) of simple CHO decrease the rate of emptying to less than that of water. Glucose polymers may allow gastric emptying in the range of water up to about 5 g per 100 ml. Our recent experience confirms our earlier data (Foster et al., 1980), suggesting that beyond 5 g per 100 ml the gastric emptying rates of glucose and glucose polymers are very similar. FIGURE 6-3 Individual and mean data for the emptying of 5% and 7% malto-dextrin (MD) based drinks. Neither drink was significantly different from water. However, the prolonged emptying period (30 min) allowed complete emptying for some subjects and may invalidate the results. Adapted from Seiple et al. (1983).

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 6-4 Average emptying rates of various concentrations of glucose- and glucose polymer-based drinks in subjects performing mild exercise. The boxed area represents the 95% confidence interval (mean ± 2 standard errors) for water. Beyond about 3% CHO the average emptying rate for simple CHO-based drinks is less than that of water. Beyond about 5% CHO, the average emptying rate for glucose polymer-based drinks is less than that of water. CARBOHYDRATE SOURCE Early studies by Hunt and Spurrell (1951) demonstrated that test meals containing starch left the stomach more rapidly than did meals containing glucose. This advantage was apparently related more to an initial more rapid emptying rate of starch. Foster et al. (1980) demonstrated that a 5% glucose polymer solution left the stomach more rapidly than isocaloric glucose did. More concentrated solutions of glucose and and glucose polymer left the stomach at similar rates (Figure 6-2). Neufer et al. (1986) showed that the addition of glucose to a polymer-glucose mixture slowed gastric emptying at total CHO concentrations within the range of 5 to 7.5 g per 100 ml. Supportive data for the advantage of polymer-based drinks over glucose-based drinks was provided by Rehrer et al. (1989), who demonstrated that a polymer-fructose (18% CHO)-based drink emptied faster than a less concentrated (15.2% CHO) glucose solution did. Previously unpublished data from my laboratory demonstrate that a 5% polymer-fructose-based drink empties at about the same rate as a 3% to 4% sucrose-based drink (Figure 6-4).

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FLUID REPLACEMENT AND HEAT STRESS EXERCISE INTENSITY Early studies by Campbell et al. (1928) and Hellebrandt and Teper (1934) suggested a slightly inhibitory effect of exercise on the gastric emptying rate. Subsequently, Fordtran and Saltin (1967) demonstrated that while the rate of emptying of water was slightly delayed at an exercise intensity of 71% of maximal O2 uptake (), there was no exercise-induced delay in the slower emptying rate of a 13% glucose solution. Costill and Saltin (1974) demonstrated essentially no effect of exercise in the rate of gastric emptying up to about 65%-70% . Neufer et al. (1986) demonstrated an enhanced rate of gastric emptying during mild exercise (50%-70% ) (Figure 6-5). Rehrer et al. (1989) indicated that CHO-containing drinks empty more slowly, at least initially, during exercise. The gastric emptying rate of water was unaffected, at least up to 70% of Wmax. FIGURE 6-5 Data from Neufer et al. (1986) demonstrating the increase in gastric emptying with mild exercise for both water- and CHO drinks containing malto-dextrin (M), glucose (G), and fructose (F). The slower emptying attributable to the presence of glucose in test drinks is also apparent in these data. Thompson and Foster (1988) demonstrated a slightly enhanced rate of gastric emptying during mild exercise for both water and a concentrated (23% CHO) polymer-based drink. Previously unpublished data from my laboratory suggest that beyond 60% there is a progressive slowing of gastric emptying and that at high exercise intensities (90% ) even water empties very slowly (Figure 6-6). Commercially availabel drinks based on sucrose (5.9% CHO) and polymers-fructose (7.1% CHO) emptied signifi

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 6-6 Average gastric emptying rates with two commercially availabel drinks in relation to exercise intensity. At rest and at moderate exercise intensities, water empties significantly more rapidly than either CHO-containing drink does. At high exercise intensities, everything empties slowly. cantly more slowly than water up through 70% . At higher exercise intensities, the gastric emptying rate of water slowed down to those of the two CHO-containing drinks. The similar emptying rates of the two CHO-containing drinks is consistent with established effects attributable to the CHO source (Figure 6-4). The data on exercise intensity generally follow with increases in exercise intensity (Rowell et al., 1964). The frequency of abdominal complaints and symptoms during high-intensity or competitive exercise (Brouns et al., 1987) suggests that attempting to feed while the gastric emptying rate is suppressed by high-intensity exercise may be inherently futile. INDIVIDUALITY OF GASTRIC EMPTYING RATES Much of the data regarding gastric emptying has, properly, focused on the characteristics of the ingestate or the circumstances of the subject. Less appreciated are the differences between subjects in gastric emptying characteristics. In Figure 6-7 are presented previously unpublished data regarding the effect of exercise intensity on the gastric emptying rates of water and two commercially availabel CHO-containing drinks. The data presented in Figure 6-7 represent raw data for the averages presented in

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 6-7 Individual (thin lines) and mean (heavy line) gastric emptying rates of water and two commercially availabel CHO-containing drinks in relation to exercise intensity. Note the wide variation in individual emptying rates.

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FLUID REPLACEMENT AND HEAT STRESS Figure 6-5. Note the nearly fourfold difference in the individual emptying rates of all three drinks. Also note that at rest and during mild exercise, some individuals empty CHO-containing drinks faster than the group average for water at rest. Similar data have been observed in subjects at rest by using different concentrations of glucose and glucose polymers (Figure 6-8). FIGURE 6-8 Individual (thin lines) and mean (heavy line) gastric emptying rates of glucose and glucose polymers in relation to CHO concentration. Note the variations in individual emptying rates. Adapted from Foster et al. (1980).

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FLUID REPLACEMENT AND HEAT STRESS EFFECTS OF GASTRIC EMPTYING METHODOLOGY Until the past 5 years the dominant method for studying gastric emptying was the serial recovery method. This method was introduced by J. N. Hunt in the 1950s (Hunt and Spurrell, 1951). Results by this method suggested that CHO concentrations of greater than about 5% produced significant delays in gastric emptying and that glucose polymers had some small advantage over simple sugars as the source of CHO for drinks designed for sports participants. More recent reports from several laboratories (Mitchell et al., 1988; Owen et al., 1986; Ryan et al., 1989) in which the serial feeding method was used, have suggested that much higher concentrations of CHO can be emptied fairly completely during exercise. Owen et al. (1986) showed that with the serial feeding of 200 ml of water, 10% glucose polymer or 10% glucose every 20 min, as much as 40%-60% of the drink is emptied after 2 h of exercise in the heat. The expected differences attributable to CHO source were evident, and the emptying of water was delayed in a hot environment, presumably secondary to the reduction in splanchnic blood flow attributable to prolonged exercise in the heat (Figure 6-9). Mitchell et al. (1988) demonstrated that as much as 90% of several drinks, FIGURE 6-9 Relative emptying of different drinks during 2 h of exercise in the heat. These data were adapted from Owen et al. (1986) who used the serial feeding method and demonstrated surprisingly favorable emptying of relatively concentrated glucose and glucose polymer (GP) drinks. Note the general suppression of gastric emptying secondary to thermal stress.

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FLUID REPLACEMENT AND HEAT STRESS water and several glucose-sucrose-polymer variants in the range of 5%-7.5% CHO, emptied during 2 h of interval exercise when 8.5 ml of the test drink per kilogram of body weight per hour was consumed during the interval. This represented an average of about 165 ml every 15 min. Ryan et al. (1989) demonstrated that as much as 90% of several drinks, water (5% glucose, 5% glucose polymer, or 5% glucose polymer-fructose) could be emptied during 3 h of exercise (60% ) in the heat when 350 ml was given every 20 min. This represents the greatest effective rate of emptying that has yet been demonstrated during exercise, particularly with fairly concentrated CHO-containing solutions. The mechanism that allows this rate of emptying has been apparent, but largely ignored, for many years. Hunt and Spurrell (1951) demonstrated nearly 40 years ago that the rate of gastric emptying increased with increasing volumes of ingestate. Similar data were presented by Costill and Saltin (1974), at least up to ingestate volumes of 600 ml, which is 1.5 times the standard 400 ml used in many studies using the serial recovery method (Costill and Saltin, 1974; Coyle et al., 1978; Foster et al., 1980; Neufer et al., 1986; Seiple et al., 1983; Thompson and Foster, 1988). Contemporary data from Hunt et al. (1985) support the notion of accelerated gastric emptying with larger meal volumes. Recent data from Rehrer et al. (1989), using the double sampling method, demonstrate that the emptying rate of CHO-containing drinks relative to that of water declines as the stomach becomes progressively less filled. This seems to be more important during exercise (Figure 6-10) than at rest (Figure 6-11). Thus, recent methodological variations lead to the conclusion that maintenance of a high gastric volume may override some of the inhibitory effects on gastric emptying attributable to the presence of CHO in the ingestate. MILITARY APPLICATIONS Just as military needs vary greatly with mission characteristics, the need for fluid and CHO replacement varies with the requirements of the individuals who are required to perform defined functions. During high-intensity exercise, gastric emptying is very slow secondary to the low splanchnic blood flow. If high-intensity exercise is required, then drinking during rest intervals becomes the only logical alternative. During more prolonged exercise, frequent (every 15-20 min) consumption of moderate (150 ml) to large (350 ml) volumes of drink are possible with favorable results. Some individuals may be particularly intolerant to forced drinking, however. Whether the ability to tolerate high intragastric volumes can be improved with training remains to be determined. However, it seems that the

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FLUID REPLACEMENT AND HEAT STRESS FIGURE 6-10 Normalized rate of emptying of various drinks in relation to the relative fullness of the stomach during moderate to heavy exercise. Note that CHO-containing beverages empty relatively more slowly as the overall emptying rate slows down as the stomach becomes relatively less full. These data support the hypothesis that high gastric volumes can accelerate gastric emptying and override the suppression of emptying attributable to the presence of CHO. This suppression becomes important at lower gastric volumes. Adapted from Rehrer et al. (1989). FIGURE 6-11 Normalized rate of gastric emptying of various drinks in relation to the relative fullness of the stomach at rest. Note the minimal effect of CHO at high gastric volumes (similar to that in Figure 6-10) and the less overall importance of CHO during rest compared with the slower emptying rates in Figure 6-10. Adapted from Rehrer at al. (1989).

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FLUID REPLACEMENT AND HEAT STRESS frequent complaints of gastrointestinal symptoms by athletes during competition are as much a function of the unfamiliarity of exercising with a full stomach as of delays in gastric emptying solely attributable to the CHO source or exercise intensity. Under most circumstances it appears that glucose polymer-based drinks have some advantage over simple CHO-based drinks, particularly at the higher end of the emptying rate spectrum. REFERENCES Brener, W., T.R. Hendrix, and P.R. McHugh. 1983 Regulation of the gastric emptying of glucose. Gastroenterology 85:76-82. Brouns, F., W.H. Saris, and N.J. Rehrer. 1987 Abdominal complaints and gastrointestinal function during long-lasting exercise. Int. J. Sports Med. 8:175-189. Campbell, J.M.H., G.O. Mitchell, and A.T.W. Powell. 1928 The influence of exercise on digestion. Guy's Hosp. Rep. 78:279-293. Costill, D.L., and B. Saltin. 1974 Factors limiting gastric emptying during rest and exercise. J. Appl. Physiol. 37:679-683. Coyle, E.F., D.L. Costill, W.J. Fink, and D.G. Hoopes. 1978 Gastric emptying rates for selected athletic drinks. Res. Q. 49:119-124. Elias, E., G.J. Gibson, L.F. Greenwood, J.N. Hunt, and J.H. Tripp. 1968 The slowing of gastric emptying by monosaccharides and disaccharides in test meals. J. Physiol. ( London) 194:317-326. Fordtran, J.S., and B. Saltin. 1967 Gastric emptying and intestinal absorption during prolonged severe exercise. J. Appl. Physiol. 23:331-335. Foster, C., D.L. Costill, and W.J. Fink. 1980 Gastric emptying characteristics of glucose and glucose polymer solutions Res. Q. Exercise Sport 51:299-305. Hellebrandt, F.A., and R.H. Teper. 1934 Studies on the influence of exercise on the digestive work of the stomach. II. Its effect on emptying time. Am. J. Physiol. 107:355-363. Hunt, J.N., and W.R. Spurrell. 1951 The pattern of emptying of the human stomach. J. Physiol. ( London) 113:157-168. Hunt, J.N., J.L. Smith, and C.L. Jiang. 1985 Effect of meal volume and energy density on the gastric emptying of carbohydrates. troenterology 89:1326-1330. Mitchell, J.B., D.L. Costill, J.A. Houmard, M.G. Flynn, and J.D. Beltz. 1988 Effects of carbohydrate ingestion on gastric emptying and exercise performance. Med. Sci. Sports Exercise 20:110-115. Neufer, P.D., D.L. Costill, W.J. Fink, J.P. Kirwan, R.A. Fielding, and M.G. Flynn. 1986 Effects of exercise and carbohydrate composition on gastric emptying Med. Sci. Sports Exerc. 18:658-662. Owen, M.D., K.C. Kregel, P.T. Wall, and C.V. Gisolfi. 1986 Effects of ingesting carbohydrate beverages during exercise in the heat. Med. Sci. Sports Exercise 18:568-575.

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FLUID REPLACEMENT AND HEAT STRESS Rehrer, N.J., E. Beckers, F. Brouns, F. ten Hoor, and W.H.M. Saris. 1989 Exercise and training effects on gastric emptying of carbohydrate beverages. Med. Sci. Sports Exercise 21(5):540-549. Rowell, L.B., J.R. Blackman, and R.A. Bruce. 1964 Indocyanine-green clearance and estimated hepatic blood flow during mild exercise in upright men. J. Clin. Invest. 43:1677-1690. Ryan, A.J., T.L. Bleiler, J.E. Carter, and C.V. Gisolfi. 1989 Gastric emptying during prolonged cycling exercise in the heat.Med. Sci. Sports Exercise 21:51-58. Seiple, R.S., V.M. Vivian, E.L. Fox, and R.L. Bartels. 1983 Gastric-emptying characteristics of two glucose polymer-electrolyte solutions. Med. ci. Sports Exercise 15:366-369. Thompson, N.N., and C. Foster. 1988 Sequential gastric emptying: effect of preceeding feedings. Med. Sci. Sports Exercise 20:S19 (Abstr. 114)

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