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Effect of Acute Prior Exercise on Glycemic and Insulinemic Indices

Department of Food Science and Human Nutrition (V.E., K.W., W.L., M.S.H., C.L.M.), Colorado State University, Fort Collins, Colorado
Department of Health and Exercise Science (M.S.H.), Colorado State University, Fort Collins, Colorado

Address correspondence to: Christopher L. Melby, Dr.P.H., Professor and Head, Department of Food Science and Human Nutrition, Nutrition and Metabolic Fitness Laboratory, 216 Gifford, Colorado State University Fort Collins, CO 80523. E-mail: Christopher.melby{at}colostate.edu

	ABSTRACT

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Background: Acute exercise is associated with increased insulin sensitivity characterized by increased insulin-induced glucose transport for periods of up to 48h after the bout of exercise. This suggests that the glycemic response to a meal may be altered by prior exercise.

Objective: We tested the hypothesis that the glycemic and insulinemic responses to a test food consumed following exercise would be lower than when consumed without prior exercise.

Design: Four lean males (age: 27 ± 4 y) and 4 females (age: 23 ± 3 y) completed 3 experimental conditions in random order: ExCHO—Subjects exercised on a cycle ergometer at 70% VO_2peak with a net energy cost of 400 kcal, which was followed by consumption of a high carbohydrate (CHO) energy bar; NoExCHO—Same as ExCHO except subjects sat quietly rather than exercised; and NoExGlc—Same as NoExCHO except subjects consumed a 50 g glucose (glc) drink as the reference CHO for GI and insulinemic index (II) determination. For each condition, following exercise or rest, baseline venous blood samples were obtained. Postprandial blood samples were obtained at 15 min intervals for 2 h.

Results: Neither the 2-h glucose area under the curve (AUC) or the GI were different between ExCHO and NoExCHO. The insulin AUC for ExCHO was 28% lower than the insulin AUC for NoExCHO (p = 0.03). The calculated II for the ExCHO condition was 30% lower than that of NoExCHO (p = 0.05).

Conclusions: An acute bout of prior exercise had no effect on the GI of an energy bar compared to that of the same food determined under the standard no-exercise conditions. However, prior exercise resulted in a lower 2-h insulin response to the CHO-rich energy bar.

Key words: exercise, carbohydrate, glycemic index, insulin, humans

	INTRODUCTION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
In 1981, Jenkins et al established the glycemic index (GI) in order to physiologically categorize carbohydrates by the glycemic response they produced [1]. To assign a GI value to a food, the glycemic response (area under the blood glucose curve) of an amount of that food containing 50 g carbohydrate (CHO) was compared to the glucose response of 50 g of glucose or white bread. Many foods have now been classified as low, intermediate, or high GI foods according to the glucose response they produce. A high GI food produces a greater glycemic response than a low GI food.

Since Jenkins first proposed the concept of the GI, several researchers have evaluated the potential application of the GI as a dietary tool to prevent and manage diseases such as diabetes, obesity, and cardiovascular disease [2]. The theory is that foods with a higher GI produce a greater glucose response, therefore initiating a greater insulin response. This greater insulin response may play a role in the progress of the diseases mentioned above. Although some studies have demonstrated associations between GI and disease risk [3–5], use of the GI to aid in disease prevention and treatment remains controversial.

The controversy over the potential application of the GI exists for a number of reasons. First, the GI is a physiological response to a food rather than an inherent property of a food. There are a variety of factors that could influence the physiological response; therefore, the GI of a food may vary from person to person or from situation to situation. Until recently, the only factors identified as influencing the GI were those affecting the rate of appearance of glucose from the gut. Some of these factors in food that can affect its GI include the amount and types of fat, protein, and fiber present with the metabolizable carbohydrates, the quality of the starch (i.e. the amount of amylose vs. amylopectin) and the characteristics of the previous meal. However, because the GI is calculated using area under the blood glucose response curve, it is not only influenced by the rate of appearance of gut and possibly hepatic glucose, but also by the rate of disappearance [6]. Research focusing on the factors influencing the rate of disappearance of glucose is limited.

One factor that may influence the rate of disappearance of glucose is prior exercise. Exercise has been shown to increase glucose uptake via insulin-independent glucose uptake [7–10] and increased insulin sensitivity [11–16], suggesting that physical activity could lower both the GI and the insulinemic index (II). Such an effect could have health implications for individuals with type 2 diabetes and insulin resistance, such that a bout of exercise prior to ingestion of moderate and high glycemic index meals could attenuate the untoward postprandial elevations of both glucose and insulin, thus resulting in better glycemic control. No research to our knowledge, however, has evaluated the effect of an acute bout of exercise on the GI and II of a food consumed immediately post-exercise. Therefore, the purpose of this study was to evaluate the effect of an acute bout of exercise on the 2-h postprandial GI and II of a high CHO energy bar consumed immediately post-exercise. We hypothesized that both the GI and II of a high CHO energy bar would be lower when consumed immediately following a bout of acute exercise compared to when the same food was consumed using the standard, resting GI testing conditions.

	MATERIALS AND METHODS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Subjects
Eight healthy, nondiabetic, physically active individuals (4 males and 4 females) volunteered to participate in the study. Enrollment criteria for the study included participation in aerobic activity an average of at least 3 days/week for the previous 6 months, body mass index (BMI) 27, weight stable within 2 kg during the previous 6 months, non-smoker, and eumenorrheic. A medical history questionnaire was completed to rule out self-reported history of chronic health problems, eating disorders, and use of medications that could influence the glycemic response, metabolic rate, substrate oxidation rate, or appetite. The study protocol was approved by the Colorado State University Human Research Committee. Informed consent was obtained from each subject prior to participation in the study.

Experimental Design and Testing Protocol
Each subject completed the following three different treatment conditions in random order:

1. Exercise/Carbohydrate (ExCHO): Moderate intensity exercise (70% VO_2peak) on a cycle ergometer for a length of time sufficient to expend a net 400 kcals, followed by consumption of a high CHO energy bar.
   
2. No Exercise/Carbohydrate (NoExCHO): Same as condition (a), but in place of cycling, subjects sat quietly for an equivalent period of time.
   
3. No Exercise/Glucose (NoExGlc): Same as condition (b), with the subject consuming a reference standard of 50 g glucose drink rather than the high CHO energy bar.
   

The exercise duration was calculated using the caloric equivalent per liter of oxygen per minute at 70% VO_2peak for each subject. The resting metabolic rate (RMR) was then subtracted from the 70% VO_2peak caloric expenditure rate to determine the net caloric expenditure per minute.

For females, each condition was performed between day 7 and 14 of their menstrual cycle to ensure that testing outcomes were not confounded by different phases of the menstrual cycle. A 3-day wash out period was required between treatments, thus only allowing two conditions to be completed during days 7–14 of the monthly cycle. Therefore, more than one month was required to complete all testing conditions. In addition, all subjects were instructed to refrain from exercise 24 hours prior to each testing condition.

Subjects reported to the Nutrition and Metabolic Fitness Laboratory at Colorado State University between 0630 h and 0730 h on each testing day. Subjects were weighed on a calibrated balance beam scale and then completed 15 min of indirect calorimetry while sitting quietly in a comfortable chair. On exercise days, the subjects then completed the exercise protocol using a Monark® bicycle ergometer (Stockholm). The protocol began with a 5-minute warm up period designed to produce an exercise intensity of 70% VO_2peak at the end of the 5^th minute. The subjects continued pedaling at this intensity for a time period (mean ± SD = 47.2 ± 8.3 minutes) sufficient to produce a net cost of 400 kcal. Continuous indirect calorimetry (CPX Express\R, MedGraphics) using a respiratory face mask was used throughout the exercise to ensure that exercise intensity remained close to 70% VO_2peak. The respiratory mask was removed for a brief period every 15 minutes to allow the subject to consume water. Heart rate and RPE were monitored throughout the exercise test. The actual average percentage of VO_2peak and the actual net energy expenditure for the exercise bout (71.38 ± 2.92% and 418 ± 17 kcal, respectively) only slightly exceeded the targets. During the non-exercise conditions, subjects sat quietly in a comfortable chair for a time period equivalent to the exercise time.

Following the exercise or non-exercise period, a flexible, indwelling catheter was placed in the superficial forearm vein. A baseline blood sample (5 ml) was drawn. The subject then consumed a glucose beverage (Sun-Dex 100 Glucose Tolerance Beverage, Fisher® HealthCare) or high CHO energy bar (Gatorade®, Barrington, IL), both containing 50 g of carbohydrate. The energy bar also contained 19.7 g of protein and 6.6 g of fat. Additional blood samples were taken at 15 minute intervals for a 2-hour period following the food or beverage consumption for determination of the glucose and insulin responses over time.

Specific Procedures
Resting Metabolic Rate.
Resting metabolic rate (RMR) was measured to help determine each subject’s exercise duration and daily energy requirements. Each subject arrived at the lab the morning following a 10-hour fast and before participating in any physical activity. Indirect calorimetry using the CPX Express® (Medical Graphics, Model No. 762035-001R, St. Paul, MN) was used to determine RMR. Prior to testing, subjects were familiarized with the testing procedure, and the metabolic cart was calibrated with known gas concentrations. Subjects were fitted with a noseclip and mouthpiece and lay comfortably in a bed. Resting VO₂ and VCO₂ values were obtained for a 30-minute period. The deWeir equation [17] was used to convert the gas exchange values into kilocalories expended.

Exercise Testing.
Peak oxygen consumption (VO_2peak) was determined using a Monark® bicycle ergometer (Stockholm) and a progressive maximal workload protocol. The subject began with a 2-minute warm-up period pedaling at 80–100 rpm against a zero workload. The workload was increased 25 watts every minute until the subject could no longer reach the minimum cadence required (20 rpm), or until there was no further increase in oxygen uptake with increasing workloads. The CPX Express® (Medical Graphics, Model No. 762035-001R, St. Paul, MN) measured oxygen consumption via indirect calorimetry. A wireless heart rate monitor (Polar Target^TM, Model No. 1902091, Hong Kong) monitored heart rate during testing. Each minute the subject indicated rate of perceived exertion (RPE) on a scale of 1 to 20 [18].

Diet Standardization.
Participants were provided with outpatient standardized meals two days prior to each testing condition. The meals were designed to maintain energy balance with the macronutrient composition of 60% CHO, 25% fat, and 15% protein. The energy content of the meals was determined based on RMR x 1.5 two days prior to testing and RMR x 1.3 one day before testing to account for the lack of exercise that day. These energy requirements correspond to a moderate activity day and a very light activity day, respectively. Subjects were instructed to consume all foods provided for the respective days and return any uneaten foods. In addition, supplemental food modules containing the same macronutrient composition (60% CHO, 25% fat, 15% protein) were given for optional consumption of up to 400 kcal. This allowed compensation for the imprecision in determining energy balance over the short period. Ad libitum water intake was allowed both days prior to testing. Subjects were instructed to consume their final snack at 2130 h the evening prior to testing and report to the laboratory the following morning in a fasted state.

Plasma Assays.
Blood samples were collected in EDTA tubes and kept on ice until all blood samples had been drawn. The samples were then centrifuged (2500 rpm x 12 min.) to collect plasma samples. Plasma was transferred to plastic bullet tubes and frozen at –70 degrees Celsius until glucose and insulin analyses could be completed. Plasma glucose concentrations were determined via the glucose oxidase method using an automated glucose analyzer (YSI 2300 Stat Plus®, Yellow Springs Instruments, Inc, Yellow Springs, OH). Plasma insulin concentrations were determined at the Endocrinology Laboratory at the University of Colorado Health Sciences Center using an enzyme-linked immunosorbent sandwich assay.

Determination of Glycemic and Insulinemic Indexes.
The GI of the high CHO energy bar was determined for both the no exercise condition and the exercise condition using the following equations:

Exercise

No Exercise

Glucose AUC was determined using the method of Wolever [19]. The insulin AUC and the insulinemic index (II) were determined in the same manner.

Statistical Analysis of Data
A power test was used to determine the sample size. Specifically, we estimated exercise-induced decreases in the GI and II on the order of 25 points (e.g. a drop in GI or II from 85 to 60, with the standard deviation of the difference estimated to be 25 points). Using an alpha of p = 0.05 (one-tailed), 8 paired subjects would yield a power of 0.81. Data were analyzed using the Statistical Package for the Social Sciences® (SPSS, Chicago, IL) software. A two-way repeated measures analysis of variance (ANOVA) (condition x time) was used to examine differences in both the glucose and insulin responses among the three conditions (ExCHO, NoExCHO, and NoExGlc) across the 9 time points. Posthoc tests (Bonferroni test with adjustment for multiple comparisons) were used to determine the specific time points at which blood glucose and insulin differed between the ExCHO and the NoExCHO conditions. There were occasional blood draws that could not be obtained at each 15 minute interval due to difficulties with the catheter. When this occurred, an average of the insulin and glucose values for the 15 minutes before and after the missed value was substituted. A one-way way within subjects ANOVA was used to examine differences in glucose area under the curve (AUC) and insulin AUC among the three conditions. When the ANOVA was significantly different, differences between conditions were further analyzed using least significant difference (LSD) tests. A paired samples t test was performed to examine GI and II differences between the Ex/CHO and NoEx/CHO conditions. Statistical significance was set at P < 0.05, using a one-tailed test based on the directional hypothesis. Values are expressed as means ± standard deviations except where indicated otherwise.

	RESULTS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Subject Characteristics
Physical characteristics of the subjects are shown in Table 1. Subjects were young, non-obese, physically active men and women. As expected, there were significant differences between females and males for body mass, height, RMR, and peak VO₂ (P < 0.05).

View larger version (13K): [in this window] [in a new window]   Fig. 1. 2-h postprandial plasma glucose response (X ± SEM) for the three experimental conditions.

The glucose AUC values for each condition are shown in Fig. 2. The within subjects ANOVA was significant (P < 0.05), with pairwise comparisons revealing a significant difference in the glucose AUC between the NoExGlc and ExCHO conditions (2163 ± 1173 vs. 1353 ± 1057 mg/dl · min., P < 0.05) and between the NoExGlc and NoExCHO conditions (2163 ± 1173 vs. 1205 ± 788 mg/dl · min., P < 0.05). There was no significant difference between the glucose AUC of the ExCHO and NoExCHO conditions. A paired samples t test showed no significant difference between the GI of the high energy CHO bar consumed following the exercise and no exercise conditions (63.3 ± 50.7 vs. 66.3 ± 52.8, respectively; P = 0.85).

View larger version (35K): [in this window] [in a new window]   Fig. 2. Plasma glucose area under the curve (AUC) (X ± SEM) for the 2-h postprandial period in the three experimental conditions.

View larger version (15K): [in this window] [in a new window]   Fig. 3. 2-h postprandial plasma insulin response (X ± SEM) for the three experimental conditions.

View larger version (35K): [in this window] [in a new window]   Fig. 4. Plasma insulin area under the curve (AUC) (X ± SEM) for the three experimental conditions.

	DISCUSSION

Major Findings
The major finding of this study is that when an energy bar containing 50 g of carbohydrate was consumed shortly after an acute bout of endurance exercise, the glycemic response was no different than when the energy bar was consumed without prior exercise. However, prior exercise did produce a significantly lower insulin response to the energy bar.

Glucose Response
Our findings do not support our hypothesis that the glycemic response to a test carbohydrate would be lower following exercise compared to a no-exercise testing protocol. We found no effect of prior acute exercise on the glycemic response over time, the 2-h glucose AUC, or the calculated glycemic index. We hypothesized that because glycemic and insulinemic responses are so closely associated, both would be similarly affected by the single exercise bout. The finding that these two interrelated variables did not respond in a similar fashion to the exercise perturbation was unexpected.

The lack of an effect of the exercise bout on the glycemic response to the test carbohydrate is not without some support from previous work. Ben-Ezra et al examined the effect of 50 min of treadmill exercise on glucose and insulin responses to oral glucose ingestion in women 15–17 h after the exercise bout [25]. There was no difference in the glucose AUC during a 150-min postprandial period in compared to a non-exercise control condition. There was, however, lower insulin AUC. Obviously, there was a much longer time interval between the exercise and the carbohydrate challenge in this study compared to ours Folch and colleagues compared the effect of a 90-minute cycling bout at 50% VO_2max to a 90-minute resting condition on the glycemic response to a large pasta meal consumed 30 minutes post-exercise [26]. The glucose response to the meal was not different between the exercise and control conditions. Postprandial insulin responses were not reported.

One possible explanation for the lack of decrease in the glycemic response following exercise may be due to changes in both the rate of appearance (Ra) from the gut and the rate of disappearance (Rd) of glucose from the systemic circulation. Several studies in dogs have demonstrated an increased efficiency in which orally consumed glucose is made available to systemic circulation following exercise [21, 27]. If found to be true in humans, this would result in an initial increase in the Ra of gut glucose. If this phenomenon was in turn coupled with an elevated Rd associated with increased insulin sensitivity in the previously active muscles, the concurrent increase in the Ra and Rd of glucose could cancel each other out, with no differences in postprandial blood glucose concentrations following exercise compared to no exercise.

Insulin Response
There are several possible explanations for the lower insulin AUC following a bout of exercise. Acute exercise, by way of increased circulating catecholamines, reduces insulin secretion. Possibly this exercise-induced blunting of pancreatic insulin secretion could carry over into the recovery period when the energy bar was consumed. Note, however, that the lower plasma insulin concentrations following the exercise condition were during the final 75 minutes of recovery, a time when the exercise-induced catecholamine concentrations would have decreased substantially. The plasma insulin concentrations during the early phase of recovery (when catecholamines would still be elevated from exercise), were not lower for ExCHO than NoExCHO. The well-known increase in insulin sensitivity following exercise could have contributed to the lower insulin AUC for the ExCHO compared to NoExCHO. If a single bout of exercise increases the efficiency of insulin-stimulated glucose clearance, then less insulin would be required to produce the same glucose response to the test carbohydrate. After the exercise condition, insulin concentrations initially increased similar to the non-exercise condition, but then decreased more quickly. It is possible that the acute state of energy deficit for ExCHO relative to NoExCHO (i.e. the caloric content of the energy bar was the same for both ExCHO and NoExCHO conditions, but for former, subjects had just expended the 400 additional kcals in exercise) contributed to the lower plasma insulin in the ExCHO condition. We have previously shown that insulin concentrations are sensitive to acute changes in energy balance [28].

Another reason for the decreased insulin response for the ExCHO compared to NoExCHO condition may be that of increased insulin clearance following exercise. Insulin clearance is not as clearly understood as insulin secretion, but there has been at least one study that has demonstrated an increase in insulin clearance following exercise. Tuominen et al used a euglycemic insulin clamp to determine insulin clearance in healthy men under resting conditions and again 12 hours following a marathon or 44 hours following a 2-hour treadmill test [29]. They observed a significantly greater insulin clearance following the exercise conditions compared to the resting condition. Obviously, the 12 and 44-hour intervals between exercise and determination of insulin clearance in the Tuominen study are much greater than the very short time interval (10–15 minutes) between the cessation of exercise and measurement of glucose and insulin responses in our study. Nevertheless, it is possible that greater insulin clearance following the exercise bout contributed to the lower insulin AUC.

Caveats
There are several caveats which deserve discussion. We used venous blood samples as opposed to arterial samples. We considered using arterialized venous blood from capillary finger-prick samples, but we determined that multiple finger-sticks over the 2-h postprandial period would be too burdensome for our study subjects. Also, the finger prick methods would preclude the measurement of insulin. Another possible limitation to our study relates to possible gender differences in response to the energy bar. One recent study observed sex differences in whole body insulin-induced glucose clearance (males lower than females) when measured 3 to 4 hours post-exercise [30]. However, we did not observe any differences in glucose and insulin response between males and females in our study. Each subject served as his/her own control, suggesting that our results are not likely confounded by gender. The sample size for this study was small. However, the GI values between the ExCHO and NoExCHO conditions are so similar that the failure of the data to support our research hypothesis cannot be attributed to an inadequate number of study subjects. On the other hand, the insulinemic index for the energy bar was significantly lower following exercise, even with a sample of only eight subjects. Finally, this study only included healthy, non-diabetic, nonobese subjects. Therefore, inferences cannot be made about the effect of exercise on glucose and insulin response in insulin resistant individuals.

Implications
With the current understanding that postprandial hyperinsulinemia is associated with increased risk for various chronic diseases such as cardiovascular disease and type 2 diabetes [31, 32], our observations suggest yet another possible benefit that exercise may provide in lowering risk for these diseases. Large randomized trials have demonstrated that exercise may significantly reduce the risk of developing type 2 diabetes [33, 34]. It may be possible that the role of acute prior exercise in decreasing the postprandial insulin requirement contributes to less pancreatic beta-cell fatigue, lower cellular mitogenic responses, and lower risk for type 2 diabetes. Further research is required in order to better understand the possible protective effect of exercise-related reductions in postprandial insulinemia.

	CONCLUSION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
In conclusion, when compared to the standard, non-exercise control condition, we observed a lower postprandial insulinemic response to a high carbohydrate energy bar when consumed immediately following an acute bout of cycling exercise at 70% VO_2peak, with a net energy expenditure of approximately 400 kcal. The glycemic index of the test food, however, was not significantly affected by the exercise bout. Future studies should examine the effect of such exercise on the acute glycemic and insulinemic responses to various foods in those individuals most likely to benefit from a lower postprandial insulin response, i.e. those with insulin resistance and type 2 diabetes.

	ACKNOWLEDGMENTS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

	FOOTNOTES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
C.L.M. has received past speaking honoraria from Gatorade, Inc., who donated the energy bars. The other authors report no potential conflicts of interest.

Received June 3, 2005. Accepted December 23, 2005.

	REFERENCES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 

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