Glucose and Insulin Responses After Commonly Used Sport Feedings Before and After a I-hr Training Session
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1 International kurnal of Sport Nutrition, 1995, 5, Human Kinetics Publishers, Inc. Glucose and Insulin Responses After Commonly Used Sport Feedings Before and After a I-hr Training Session Zandrie Hofman, Harm Kuipers, Hans A. Keizer, Erik ). Fransen, and Roderique C.). Servais This investigation examined the plasma glucose and insulin response in 6 trained athletes after consumption of four commercially available sport feeding~ 2 hr before as well as immediately after 1 hr of running under common training conditions. Four feedings were compared: Feeding 1, 160-g CHO/ 400 ml; Feeding 2, 69 g CH0/400 ml; Feeding 3, 69 g CHO + 6 g protein/ 400 ml; and Feeding 4, solid 69 g CHO + 5 g protein + 4 g fat. Before the training session, there were no differences between the four sport feedings in the area under the glucose and insulin curves and the insulin/glucose ratio. However, after exercise, Feeding 2 resulted in a significantly greater area under the glucose curve compared with Feedings 1, 3, and 4 (respectively, 352 vs. 241, 251, and 182) and a significantly lower insulin/glucose ratio compared with Feeding 1 (respectively, 6.2 vs. 15.8). Therefore, it is concluded that the kind of sport feeding may influence postexercise glucose and insulin responses. Key Words : nutrition, carbohydrate ingestion, protein ingestion, training conditions Carbohydrate is the most important nutrient for endurance performance. However, carbohydrate stores in the body are limited, and when stores are depleted, athletes cannot exercise intensively and may encounter fatigue (6, 7). Therefore, to delay fatigue during exercise, carbohydrates are ingested before exercise. Preexercise carbohydrate-rich feedings may increase carbohydrate reserves by promoting liver and muscle glycogen synthesis or by providing an absorbable source of blood glucose during exercise that may improve training and performance capabilities. Preexercise feedings should contain 1 to 5 g of carbohydrate per kilogram body weight and should be consumed 1 to 4 hr before Z. Hofman is with the Department of Nutritional Sciences and Information, N.V. Verenigde Bedrijven Nutricia, P.O. Box 1, 2700 MA Zoetermeer, The Netherlands. H. Kuipers, H.A. Keizer, E.J. Fransen, and R.C.J. Sewais are with the Department of Movement Sciences, University of Limburg, P.O. Box 616, 6200 MD Maastricht, The Netherlands.
2 Glucose and Insulin Responses / 195 exercise (20). Recently, it has been shown that the glycemic index of a preexercise carbohydrate feeding may affect exercise performance and blood glucose levels. Thomas et al. (22) showed that, compared with a high glycemic index preexercise meal (potatoes), a low glycemic index preexercise meal (lentils) may prolong endurance time of strenuous exercise by reducing postprandial hyperglycemia and hyperinsulinemia. Furthermore, postexercise carbohydrate feedings in excess of 0.7 g/kg body weight are important for the rapid replenishment of muscle glycogen stores (10, 11). It has been shown that an attenuated blood glucose response in combination with increased blood insulin levels may improve the rate of muscle glycogen storage. This was achieved by adding protein to a carbohydrate drink (27). Glucose and insulin responses after a feeding can be affected by several factors such as the proportion of dietary fructose to glucose, the ratio of amylopectin to amylose, methods of food preparation, and the presence of protein, fat, dietary fiber, or antinutrients like phytates, tannins, and lectins (4, 23). Exercise may also affect glucose and insulin responses, since it has been shown that the magnitude of glycogen depletion influences the rate of muscle glycogen resynthesis during the early hours of postexercise recovery (26). However, little is known about how different preexercise meal compositions influence physical performance and plasma glucose and insulin responses. This is particularly important, since hyperinsulinemia at the onset of exercise may lead to reactive hypoglycemia (1, 5, 15). Furthermore, there is a lack of knowledge on postexercise plasma glucose and insulin responses after different meal compositions that might be important for the rate of glycogen resynthesis (7, 10, 11, 13). And last, there is a need for more information about the influence of the consistency (e.g., solid vs. liquid) of a meal on plasma glucose and insulin responses before, during, and after exercise. Therefore, the aim of this study was to determine the effect of exercise and four different sport feedings (ingested pre- and postexercise), which are commercially available and commonly used by athletes, on plasma glucose and insulin responses. To mimic sport practice and to study possible differences in pre- and postexercise responses, the feedings were given 2 hr before and immediately after 1 hr of running. Three of the feedings had comparable carbohydrate contents (approximately 69 g), however, the composition (protein, fat, electrolytes) and consistency (liquid vs. solid) of the feedings were different. One liquid feeding contained a greater amount of carbohydrates (160 g). The products were chosen to assess plasma glucose and insulin responses before and after exercise as a function of (a) the amount of carbohydrate, (b) the effect of protein, and (c) the consistency of the feedings. Subjects Methods Eight male subjects volunteered for this study. An inclusion criterion was that the subjects were able to run for at least 1 hr continuously at about 70%V02max. Prior to their participation, each of the subjects was informed of the purpose, methods, and possible risks associated with the study, and written informed consent was obtained. One subject could not complete the study due to a car
3 1 96 / Hofman, Kuipers, Keizer, Fransen, and Servais accident unrelated to the study. Another subject showed extremely high plasma glucose and insulin levels (peak levels of 16 mmol/l and 146 miu/l, respectively) as well as different glucose and insulin curves compared with the other subjects. These curves are considered as outliers; therefore, this subject was excluded from further analysis. Thus, 6 subjects were included in the study analysis. The characteristics of the 6 subjects are presented in Table 1. Percent body fat was estimated by the triceps, subscapular, suprailiac, and biceps skinfolds using the Durnin and Womersley (9) equations. Experimental Procedure Each subject performed four trials in random order, in which one of the four test sport feedings was consumed 2 hr before as well as immediately after 1 hr of running. Because not all subjects were able to visit the laboratory at the same time of the day, half of the subjects arrived at the laboratory at 8:00 a.m. after a 10-hr overnight fast, whereas the other half of the subjects were tested at 1:00 p.m., after an overnight fast and a small, standardized breakfast at 9:00 a.m. However, each subject was retested at exactly the same time of the day. A cannula (18-gauge, Quick cath., Baxter B.V., Utrecht, The Netherlands) on which a threeway stop cock was attached was inserted in an antecubital vein for blood sampling. The catheter was kept patent by a slow-drip infusion with saline. After two 1- ml blood samples were collected, one of the four sport feedings was consumed within 4 min and a stopwatch was started (t = 0). The subject remained seated in a chair, and blood was sampled every 10 min for 120 min. Subsequently, the cannula was removed and the subject started running on a hilly trail of about 12 km, starting and ending in the laboratory. All subjects were well accustomed to hill training, and they were instructed to run at a comfortable pace, well below racing intensities. The exercise intensity was not standardized, and running times were all within the range of 52 to 59 min. Immediately after exercise, a new cannula was inserted into a forearm vein of the contralateral arm as described before, and the subject received the same Table 1 Characteristics of Subjects Age Weight Body fat Height Subject (years) (kg) (%) (cm) Mean SEM
4 Glucose and Insulin Responses / 197 sport feeding as before exercise. Again, subjects remained seated for 120 min, and every 10 min blood samples were drawn. All blood samples were collected in a heparin-coated syringe and transferred into precooled tubes placed in an ice bath. Blood plasma was separated from blood cells after centrifugation for 1 min at rpm and subsequently was stored at -25 "C until further analysis. Blood Analyses. Plasma glucose concentration was assayed using the UV Hexokinase method of Beckman (Part No ) on a Synchrom SX4 CE Clinical System (Beckman Instruments, Inc., Brea, CA, USA). Plasma insulin concentration was determined in duplicate with a Coat-A-Count radioimmunoassay (TKlN5, Diagnostic Products Corporation, Los Angeles, CA, USA) using a LKB 1275 mini gamma gammacounter (Pharmacia-Wallac, Turku, Finland). Feedings. The four sport feedings were as follows: Feeding 1, 400 ml of a highly concentrated carbohydrate drink with a total carbohydrate content of 160 g (Extran Energydrink, Nutricia, Zoetermeer, The Netherlands); Feeding 2, 400 ml of a diluted carbohydrate drink with a total carbohydrate content of 69 g; Feeding 3, 400 ml of a carbohydrate drink containing a small amount of protein with a total carbohydrate and protein (80% casein, 20% whey protein) content of 69 and 6 g, respectively (Extran Energydrink on yoghurt basis, Nutricia, Zoetermeer, The Netherlands); Feeding 4, a 91-g muesli bar added with water for a total volume of 400 ml (Extran Mueslireep, Nutricia, Zoetermeer, The Netherlands). The compositions of the four feedings are shown in Table 2. The volume of the feedings was kept constant, since volume is an important factor influencing the gastric emptying rate (17). A comparison between Feedings 1 and 2 shows the effect of the amount of carbohydrate intake on glucose and insulin response, while a comparison between Feedings 2 and 3 shows the effect of additional protein intake, although the type of carbohydrate differs between the feedings. Differences between liquid and solid feedings are shown by a comparison of Feedings 3 and 4. However, these feedings are not exactly comparable with respect to the amount of fat and protein and type of carbohydrates. Table 2 Composition of Sport Feedings (per 400 mi) Feeding 1 Feeding 2 Feeding 3 Feeding 4 Energy Carbohydrate g (% En) Glucose g (% En) Maltose g (% En) Polysacch. g (% En) Other g (% En) Protein g (% En) Fat g (% En) Na (mg) Ca (mg) P (mg) C1 (mg)
5 1 98 / Hofman, Kuipers, Keizer, Fransen, and Servais Data Analysis Results are expressed as mean f SEM. The areas under the curves are calculated assuming that the base of the curve is a line drawn horizontally at the lowest level, which is the method suggested by Vorster et al. (24). The results from the four trials were compared using a two-way (condition vs. time) ANOVA for repeated measures and the Tukey significant difference test. Statistical significance for all comparisons was set at the.05 level of confidence (two-tailed probability). Due to technological problems, some blood samples for analysis of insulin concentrations were lost. Therefore, preexercise insulin samples are not the same as postexercise insulin samples, and therefore no pre- versus postexercise comparisons on variables including insulin were performed. The insulin-based variables were compared using a one-way ANOVA. Results Plasma glucose responses to the four feedings before and after exercise are shown in Figures 1 and 2. Time points at which the sport feedings are significantly different from each other are marked in the figures. All subjects reached peak plasma glucose concentrations at 20 to 30 min after consumption of each sport feeding pre- and postexercise. Glucose levels did not differ between pre- and postexercise samples except for Feeding 1, which showed a significantly higher glucose level at t = 0 after exercise compared with fasting blood glucose levels before exercise. Postexercise, Feeding 2 showed a significantly greater area under the curve than Feedings 1, 3, and 4 (see Table 3). There were no differences between pre- and postexercise areas under the curves. Plasma insulin responses to the four feedings before and after exercise are shown in Figures 3 and 4. Time points at which the sport feedings are significantly different from each other are marked in the figures. Due to analytical problems, no insulin data are available at 10 and 30 min before exercise. The areas under the curve of the feedings were not statistically different. The insuiin/glucose ratios are shown in Table 3. Preexercise, the differences between the feedings did not reach significance. Postexercise, Feeding 1 showed a significantly greater insulin/glucose ratio than Feeding 2. Discussion In this investigation, the effects of different sport feedings and exercise on glucose and insulin responses under common training conditions were studied. Therefore, in contrast to other studies that focused on the effect of feeding and exercise on glucose and insulin responses in a postabsorptive state (18,26,27), in this study the subjects had a feeding 2 hr before starting a run on a hilly terrain. The amount of carbohydrate intake was within general recommended ranges either pre- or postexercise (10, 11,20). With the exception of Feeding 2, which is a dilution of Feeding 1, the products are commercially available and are being used by athletes. Effect of Exercise This study did not demonstrate any differences between pre- and postexercise glucose levels. This was not in line with our expectations, since exercise increases the permeability of muscle to glucose even in the absence of insulin (10, 19)
6 .. **, glucose (mmol/ll Glucose and Insulin Responses / 199 -C sport feedii >...*... y--. -I-- sport feeding 2 8 sport feeding % % 31 1 I I I I I I I I I I I I I I I I I I I I I I I I I time (min) Figure 1 - Glucose response before exercise. "Significantly different (p <.05). n = 6. and activates glycogen synthase (3). Therefore, it is feasible that the clearance of glucose from the blood into the muscle cell is different pre- and postexercise. Although the magnitude of glycogen depletion does influence the rate of muscle glycogen resynthesis during the early hours of postexercise recovery (26), the magnitude of glycogen depletion in our study after 1 hr of endurance running may not have been sufficient to show an effect. The lack of precise control of exercise intensity might have influenced the results as well. However, the subjects ran at a comfortable pace that did not lead to complete glycogen depletion and exhaustion. Effect of Protein Comparison of Feedings 2 and 3 did not show an insulin-enhancing effect of protein, which disagrees with the finding of Spiller et al. (21). By introducing the glycemic index of foods as a physiological basis for carbohydrate exchange, Jenkins et al. (12) showed an inverse relation between the amount of protein per 50 g carbohydrate and the glycemic index. In accordance with this finding, Spiller et al. (21) showed that when subjects consume 16 to 50 g of protein together with 58 g of carbohydrate, the areas under the glucose and insulin curves are lower and greater, respectively, compared with a 58-g carbohydrate feeding alone. Zawadzki et al. (27) also showed increased insulin and decreased glucose responses postabsorptive and postexercise when 41 g of protein was added to 112 g of carbohydrate. The amount of protein used in the present study, 6 g, is
7 200 / Hofman, Kuipers, Keizer, Fransen, and Servais glucose (mmol/l) sport feeding 2...*...-.min g o... sport feeding I I I I I I I I I I I I I I I I I I time (min) Figure 2 - Glucose response after exercise. "Significantly different (p c.05). n = 6. Table 3 Areas Under Glucose and Insulin Curves and Insulin/Glucose Ratio (n = 6), Pre- and Postexercise Area under Area under Insulin/glucose glucose curve insulin curve ratio Feeding Pre Post Pre Post Pre Post Note. Values are mean + SEM. 'Feeding 2 significantly different from Feedings 1, 3 and 4. bfeeding 1 significantly different from Feeding 2.
8 Glucose and Insulin Responses / 201 insulin (mlu/l) *... &....-I-., sport feeding C.. sport feeding 1 t * sport feeding sport feeding %# I I I I I I I I I I I I I time (min) Figure 3 -Insulin response before exercise. *Significantly different (p <.05). n = 6. much smaller than that used in the cited studies and is below the threshold level of 8 g as suggested by Day et al. (8). On the other hand, Westphal et al. (25) did not find an insulin-enhancing effect when adding up to 50 g of protein to 50 g of glucose but did find a threshold protein intake. Below this threshold there was no change in area response of a-amino nitrogen and glucagon of 9 and 5 g, respectively. Consistency (Solid Vs. Liquid) of Sport Feeding Although the liquid Feeding 3 did not have exactly the same composition as the solid Feeding 4, the amounts of carbohydrate and protein were approximately the same. The fat content of the solid feeding was somewhat higher, which may have decreased gastric emptying and consequently altered glucose response. Postexercise, the area under the glucose curve was lower after the solid feeding. However, there was no difference between the solid and liquid feedings as far as glucose or insulin levels were concerned at any time point. The solid muesli bar was given with 327 ml water in order to keep the volume of all feedings constant. The solid feeding can therefore be considered as a solid-liquid meal of which the sugar would be likely to dissolve in the liquid phase and would empty more quickly, followed by a slower emptying of the solid phase. As shown in other studies (13, 18), there seems to be no preference for a solid or a liquid feeding after exercise, since there seems to be no difference in rate of muscle glycogen resynthesis. Ivy (ll), however, recommended liquid
9 202 / Hofrnan, Kuipers, Keizer, Fransen, and Servais insulin (mluil C sport feeding ; sport feeding 2 I.....*. I time (min) Figure 4 -Insulin response after exercise. "Significantly different (p c -05). n = 6. supplements because they are easy to digest and are less filling and, therefore, tend to not adversely affect one's normal appetite. They also provide fluid for rapid rehydration. Amount of Carbohydrate In our study, the area under the glucose curve after the high carbohydrate intake of 160 g with Feeding 1 was significantly lower than the 69 g of carbohydrate intake with Feeding 2. Since the composition of Feeding 2 was the same as Feeding 1, except for the concentration of all nutrients, the only reason for the attenuation of the glucose response seems to be the carbohydrate density or osmolarity. One might expect that by increasing the amount of carbohydrate intake, the glucose and insulin levels would also increase, resulting in greater areas under the curves. Indeed, Jenkins et al. (12) found that the glycemic index increased when the amount of carbohydrate intake was doubled from 50 to 100 g. However, the increment in glycemic index was not linear with the increment in carbohydrate intake. The glycemic index increased only by 20%. Besides ingested volume, which was kept constant, carbohydrate content is a very important factor affecting gastric emptying (17). A slower gastric emptying probably results in a slower release of glucose to the gastrointestinal tract and blood. Mourot et al. (16) showed a significant correlation between gastric emptying rate and glucose response among young healthy adults. The finding in the present investigation that the postexercise blood glucose level at
10 Glucose and Insulin Responses / 203 t = 0 after Feeding 1 was higher than after the other feedings is in agreement with the slower release of glucose. Possibly, Feeding 1 decreased the gastric emptying rate to such an extent that the carbohydrate delivery to the small intestine was slower than after Feeding 2, resulting in an attenuated glucose response. If glucose levels had been measured for more than 2 hr, it is possible that the area under the glucose curve would have been higher, since a secondary late blood glucose peak is sometimes seen (2). However, during the 2 hr before exercise, the high-carbohydrate Feeding 1 showed a lower glycemic response, which may be of benefit, since a low glycemic preexercise meal has been shown to prolong endurance during strenuous exercise by inducing less postprandial hyperglycemia and hyperinsulinemia (22). Furthermore, the results of the present study indicate that after preexercise feeding, blood glucose and insulin levels were almost normalized, thus reducing the risk for rebound hypoglycemia during exercise while there still may be carbohydrate delivery from the gut to the blood and muscles. It is suggested that preexercise carbohydrate feedings may increase carbohydrate reserves either by promoting liver and/or muscle glycogen synthesis or by providing an absorbable source of blood glucose during exercise (20). None of the subjects reported gastrointestinal problems or any other discomfort. After exercise, the insulin response to the high-carbohydrate Feeding 1 was different compared with the other insulin curves. After 40 min, the insulin levels remained high and were significantly higher at t = 80, 100, and 120 min. This distinct response is probably a second feeding effect rather than an exercise effect, since the blood glucose level at t = 0 after exercise is significantly higher compared with the blood glucose level at t = 0 postabsorptively before exercise. The increased insulin levels resulted in a significantly higher insulin/glucose ratio. This may be of benefit since results of Kiens et al. (14) and Zawadzki et al. (27) showed that increased rates of muscle glycogen storage after exercise may be the result of increased clearance of blood glucose due to increased plasma insulin response. Keizer et al. (13) and Reed et al. (18), however, did not show an increased glycogen resynthesis with increased insulin levels. Whether the increased insulin/ glucose ratio is truly of benefit remains to be established. In summary, exercise under our training conditions does not affect glucose response. No difference in glucose and insulin responses between a solid and a liquid feeding was detected either before or after exercise. In addition, 6 g of protein together with 69 g of carbohydrate did not have an insulin-enhancing effect compared with 69 g of carbohydrate alone. Furthermore, it seems that 400 ml of highly concentrated carbohydrate drink has a lower glucose response compared with 400 ml of a less concentrated carbohydrate drink. This may be attributed to a lower gastric emptying rate. After exercise, the concentrated carbohydrate Feeding 1 showed a higher insulin/glucose ratio than the less concentrated carbohydrate Feeding 2. Therefore it is concluded that postexercise, the type of sport feeding does influence glucose and insulin responses. The amount of carbohydrate intake seems to be an important factor in this. References 1. Ahlborg, G., and P. Felig. Substrate utilization during prolonged exercise preceded by ingestion of glucose. Am. J. Physiol. 233:E188-E194, Amelsvoort, J.M.M. van, P. van Stratum, G.P. Dubbelman, and R.N. Lussenberg. Effects of meal size reduction on postprandial variables in male volunteers. Ann. Nutr. Metah. 34: , 1990.
11 204 / Hofrnan, Kuipers, Keizer, Fransen, and Servais 3. Bak, J.F., and 0. Pedersen. Exercise-enhanced activation of glycogen synthase in human skeletal muscle. Am. J. Physiol. 248:E957-E963, Beek, E.J. van der. Slow-release carbohydrates and treatment of diabetes mellitus. In Low Digestibility Carbohydrates, D.C. Leegwater, V.J. Feron, and R.J.J. Hermus (Eds.). Wageningen, The Netherlands: Pudoc, 1987, pp Costill, D.L., E.F. Coyle, G. Dalsky, W. Evans, W. Fink, and D. Hoopes. Effects of elevated plasma FFA and insulin on muscle glycogen usage during exercise. J. Appl. Physiol. 43: , Costill, D.L., and M. Hargreaves. Carbohydrate nutrition and fatigue. Sports Medicine , Coyle, E.F. Carbohydrate feedings: Effects on metabolism, performance and recovery. In Advances in Nutrition and Top Sport (Vol. 32), F. Brouns (Ed.). Basel, Switzerland: Karger, 1991, pp Day, J.L., K. Johansen, O.P. Ganda, J.S. Soeldner, R.E. Gleason, and W. Midgley. Factors governing insulin and glucagon responses during normal meals. Clin. Endocrinol. 9: , Dumin, J.V.G.A., and J. Womersley. Body fat assessed from total body density and its estimation from skinfold thickness measurements on 481 men and women aged from 16 to 72 years. Br. J. Nutr. 32:77-97, Friedman, J.E., P.D. Neufer, and G.L. Dohm. Regulation of glycogen resynthesis following exercise, dietary considerations. Sports Medicine 11: , Ivy, J.L. Muscle glycogen synthesis before and after exercise. Sports Medicine 11:6-19, Jenkins, D.J.A., T.M.S. Wolever, R.H. Taylor, H. Baker, H. Fielden, J.M. Baldwin, A.C. Bowling, H.C. Newman, A.L. Jenkins, and D.V. Goff. Glycemic index of foods: Physiological basis for carbohydrate exchange. Am. J. Clin. Nutr. 34: , Keizer, H.A., H. Kuipers, G. van Kranenburg, and P. Geurten. Influence of liquid and solid meals on muscle glycogen resynthesis, plasma fuel hormone response and maximal physical working capacity. Int. J. Sports Med. 8:99-104, Kiens, B., A.B. Raben, A.K. Valeur, and E.A. Richter. Benefit of dietary simple carbohydrates on the early postexercise muscle glycogen repletion in male athletes (abstract). Med. Sci. Sports Exerc. 22:S89, Koivisto, V., S.L. Karonen, and E.O. Nikkila. Carbohydrate ingestion before exercise: Comparison of glucose, fructose and sweet placebo. J. Appl. Physiol. 51: , Mourot, J., P. Thouvenot, C. Couet, J.M. Antoine, A. Krobicka, and G. Debry. Relationship between the rate of gastric emptying and glucose and insulin responses to starchy foods in young healthy adults. Am. J. Clin. Nutr. 48: , Noakes, T.D., N.J. Rehrer, and R.J. Maughan. The importance of volume in regulating gastric emptying. Med. Sci. Sports Exerc. 23: , Reed, M.J., J.T. Brozinick, M.C. Lee, and J.L. Ivy. Muscle glycogen storage postexercise: Effect of mode of carbohydrate administration. J. Appl. Physiol. 66: , Richter, E.H., T. Ploug, and H. Galbo. Increased muscle glucose uptake after exercise: No need for insulin during exercise. Diabetes 34: , Sherman, W.M. Carbohydrate feedings before and after exercise. In Ergogenics, Enhancement of Performance in Exercise and Sport, D.R. Lamb & M.H. Williams (Eds.). Ann Arbor, MI: Brown & Benchmark, 1991, pp
12 Glucose and Insulin Responses / Spiller, G.A., C.D. Jensen, T.S. Pattison, C.S. Chuck, J.H. Whittarn, and J. Scala. Effect of protein dose on serum glucose and insulin response to sugars. Am. J. Clin. Nutr. 46: , Thomas, D.E., J.R. Brotherhood, and J.C. Brand. Carbohydrate feeding before exercise: Effect of glycaemic index. Int. J. Sports Med. 12: , Truswell, A.S. Glycaemic index of foods. Eur. J. Clin. Nutr. 46(Suppl. 2):S91- S101, Vorster, H.H., C.S. Venter, and N. Silvis. Glycaemic index of foods: A critical evaluation. S. Afr. J. Fd. Sci. Nutr. 2: 13-17, Westphal, S.A., M.C. Gannon, and F.Q. Nuttall. Metabolic response to glucose ingested with various amounts of protein. Am. J. Clin. Nutr. 52: , Zachwieja, J.J., D.L. Costill, D.D. Pascoe, R.A. Robergs, and W.J. Fink. Influence of muscle glycogen depletion on the rate of resynthesis. Med. Sci. Sports Exerc. 23(1):44-48, Zawadzki, K.M., B.B. Yespelkis, and J.L. Ivy. Carbohydrate-protein complex increases the rate of muscle glycogen storage after exercise. J. Appl. Physiol. 72(5): , 1992.
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