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BASIC SCIENCES: Original Investigations

Exogenous Carbohydrate Spares Muscle Glycogen in Men and Women during 10 h of Exercise

HARGER-DOMITROVICH, STEPHANIE G.; McCLAUGHRY, ANNE E.; GASKILL, STEVEN E.; RUBY, BRENT C.

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Medicine & Science in Sports & Exercise: December 2007 - Volume 39 - Issue 12 - p 2171-2179
doi: 10.1249/mss.0b013e318157a650
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Abstract

It has been well established that exogenous carbohydrate (CHO) supplementation during exercise increases and/or maintains rates of whole-body CHO oxidation (5,19,24). In addition, if exogenous CHO is provided, blood glucose levels are maintained (5,19,24), RPE often decreases (35), hepatic glucose output is suppressed (20), and muscle glycogenolysis may (34) or may not be slowed (6,11,38). It has also been almost conclusively demonstrated that exogenous CHO can increase performance and time to fatigue during exercise in both males and females (5,9,19,20).

The majority of past research involving the use of supplemental CHO has been conducted under relatively short exercise durations (1-5 h) and high intensities (60-80% V˙O2peak). It seems that the longest controlled laboratory exercise trial evaluating the effects of exogenous CHO is a recent study by Jeukendrup et al. (19), where subjects exercised for a period of 5 h at approximately 50% of their maximal workload. To our knowledge, past research has not adequately addressed the effects of exogenous CHO during exercise or work periods longer than 5 h, which would be similar to work shifts associated with manual labor, military operations, or wildfire suppression.

Sex-specific differences in substrate metabolism have demonstrated mixed results in past research. Whereas some researchers demonstrate increased rates of fat oxidation and decreased rates of muscle glycogenolysis in females (1,18,32), others demonstrate no significant differences between the sexes (21,23,25,26,36). Some researchers show that women rely more heavily on lipid oxidation expressed as a percentage of total energy expenditure (1,18,32,33). In studies using stable isotope dilution techniques, similar rates of glucose appearance (Ra) and glucose disappearance (Rd) with carbohydrate supplementation have been observed in both men and women when performing exercise at the same relative intensity (13,17,23,36). Moreover, our laboratory has previously demonstrated minimal differences in whole-body substrate oxidation and glucose kinetics across the sexes during exercise at 70 and 90% of the lactate threshold (LT). However, the relative contribution of blood glucose as a percent of total CHO oxidation was consistently higher in females regardless of the intensity of exercise (26).

Numerous researchers have demonstrated that females may oxidize substrates differently across the menstrual cycle (8,37) and that the primary mechanism for this subtle difference is related to circulating estradiol concentration (8,16,28,37). When amenorrheic females were provided with exogenous estradiol via transdermal delivery, absolute values of plasma glucose Ra and Rd were reduced (29). Interestingly, this finding has been duplicated when estradiol was provided to males (16). These results demonstrate the importance in controlling menstrual cycle status when performing metabolism studies in female subjects. However, it is also important to note that the metabolic effects associated with the reproductive hormonal milieu are far less influential on substrate use in comparison with the effects of exercise intensity, duration, feeding, and the training status of the individual.

Whereas the majority of the past researchers have not demonstrated a decrease in muscle glycogenolysis when exogenous CHO is provided, the exercise durations have not been extended beyond 5 h. In addition, the potential for a sex-dependent metabolic response during extended exercise when exogenous CHO is provided has not been addressed. The purpose of the study was to evaluate the effects of CHO supplementation on whole-body and net muscle substrate use during 10 h of discontinuous exercise in men and women.

We hypothesized that net muscle glycogen use would be suppressed when CHO was provided during extended exercise and that there would be minimal differences in substrate metabolism across the sexes when exercise intensity was controlled relative to the individual ventilatory threshold.

METHODOLOGY

Subjects.

Recreationally trained males (N = 7) and females (N = 6) served as subjects for this investigation (Table 1). Before participation, each subject completed a university institutional review board-approved informed consent form. All female subjects were eumenorrheic and had not been using any form of hormonal contraception for at least 6 months before the study. Preliminary descriptive testing was performed without regard to the menstrual cycle. However, all extended exercise trials were performed during the early follicular phase of the menstrual cycle (1-4 d postmenses). All subjects were asked to maintain their normal exercise and dietary habits between the two trials. Each exercise trial was completed at least 1 wk apart for male subjects and no more than one menstrual cycle apart for female subjects.

T1-10
TABLE 1:
Subjects' descriptive characteristics (N = 13).

Anthropometric measurements.

To determine body density, hydrostatic weighing was performed on an electronic scale (Exertech, La Crescent, MN), using estimated residual lung volume (15). Body density was then used to determine body fat percentage using the age- and sex-specific equations (22).

Exercise testing.

All subjects reported to the human performance laboratory after abstaining from calories, nicotine, and caffeine for 12 h before testing. Graded exercise tests to volitional exhaustion to determine maximal oxygen uptake (V˙O2peak) and ventilatory threshold (VT) were performed on two separate days using an electronically braked Cardgirus cycle ergometer (CE) (Cardgirus, Spain), and a Quinton Q65 treadmill (TM) (Quinton, Seattle, WA). The testing protocol for the CE consisted of a ramped protocol progressing at 40 W·min−1 until volitional exhaustion, or until a cadence of 50 rpm could not be maintained. The testing protocol for the TM consisted of a speed set at 1.8 m·s−1, with an increase of 1% grade every 30 s. At a respiratory exchange ratio (RER) greater than 1.0, the speed was increased 0.23 m·s−1, every 30 s until volitional exhaustion.

Expired gas data were continuously collected using a two-way mouthpiece (Hans Rudolph, Inc., Kansas City, MO) and a ParvoMedics metabolic cart (ParvoMedics, Salt Lake City, UT) calibrated before each expired gas collection. Heart rate was continuously recorded via telemetry (Polar USA, Lake Success, NY). Three methods (V-slope, ventilatory equivalents, and excess CO2) were used concurrently to determine the VT for the purpose of determining workload for the CE and TM segments of the extended exercise trials according to Gaskill et al. (14). Two trained technicians determined ventilatory threshold separately, and the results were compared. When differences in VT determination occurred, the subject was retested, and VT was reevaluated.

After performing the graded treadmill test, subjects used an upper-body ergometer (UBE) (CardiO2cycle Exercise Dynamometer, ErgometRx, St. Paul, MN) to simulate the cross-country poling motion. Subjects self-selected a resistance that was equal to a Borg rating of perceived exertion (RPE) of 9-10. The resistances performed during this test were noted and used during the extended exercise trials. Watts were monitored throughout the trial using Extend Software (SMI, St. Paul, MN).

Extended exercise trials.

Each subject performed two 10-h exercise trials in a double-blind, random crossover design. Subjects received either CHO [20% maltodextrin (0.6 g·kg−1 FFM·h−1)] or an artificially sweetened, noncaloric placebo (PLA) drink of the same flavor, temperature, and volume each hour.

To ensure similar muscle glycogen levels between trials, each subject was provided with a standardized meal plan (5.6 g·kg−1 FFM CHO, and 1.3 g·kg−1 FFM protein, 0.8 g·kg−1 FFM fat) for the 24 h before each trial. Although subjects were allowed to add to the meal plan before the first trial, the same dietary intake was duplicated before the second trial. Dietary analysis was conducted using Food Processor Nutrition Analysis Software (ESHA, Salem, OR). Subjects refrained from any type of exercise, nicotine, or caffeine for 24 h before each trial.

Subjects reported to the human performance lab at 0500 h. An indwelling glucose sensor (Medtronic Minimed, Northridge, CA) with a flexible catheter was placed in the subcutaneous fat just above the right gluteus maximus, to continuously monitor blood glucose. One hour was needed for equilibration of the glucose sensor (2,10). The One Touch-Ultra glucometer (LifeScan, Milpitas, CA) was used to calibrate the glucose sensor immediately before exercise, before lunch, and after exercise.

Before exercise, subjects voided their bladders, and a preexercise weight was obtained using a calibrated, digital scale (Befour Inc, Cedarburg, WI). A preexercise muscle biopsy was obtained from the midsection of the vastus lateralis, using local anesthetic and a Bergstrom needle with modified suction. Visible connective tissue and fat were dissected from the muscle tissue, and the sample was flash frozen in liquid nitrogen and stored at −80°C for subsequent analysis.

After the biopsy, a standardized breakfast (1.9 g·kg−1 FFM CHO, 0.4 g·kg−1 FFM protein, 0.3 g·kg−1 FFM fat) was provided for the subjects. Average time from breakfast to exercise was 23 ± 8 and 22 ± 6 min for the PLA and CHO trials, respectively. Exercise began after equilibration and calibration of the glucose sensor.

The 10-h exercise protocol consisted of three different modes of exercise repeated each hour (Fig. 1). Subjects began with upper-body ergometry (UBE) (ErgometRx, St. Paul, MN) exercise at a self-selected speed and constant resistance for 9 min. A 1-min transition was allowed to the CE, where exercise was performed at 71 ± 3% Tvent (43 ± 6% V˙O2peak) for 19 min. Another 1-min transition was allowed to the TM, where exercise was performed at 72 ± 4% Tvent (44 ± 5% V˙O2peak) for 20 min. Subjects then took a 10-min break and consumed equal volumes of either a PLA or CHO [20% maltodextrin (0.6 g·kg−1 FFM·h−1)] drink. Between hours 5 and 6, subjects took a 40-min lunch break where they consumed a standardized lunch (1.9 g·kg−1 FFM CHO, 0.4 g·kg−1 FFM protein, 0.3 g·kg−1 FFM fat) in place of the PLA/CHO feeding.

F1-10
FIGURE 1:
Experimental protocol.

Heart rate (HR) was monitored continuously using a telemetry heart rate monitor (Polar USA, Lake Success, NY). The average HR during the last 5 min of each hour of CE and TM portions of exercise was calculated to compare the PLA and CHO trials.

Immediately on completion of the last hour, blood glucose was measured with the glucometer, and the glucose sensor was recalibrated. Subjects voided their bladders before obtaining a postexercise weight. Collection of a second muscle biopsy occurred from a second incision in the vastus lateralis, approximately 2 cm proximal to the initial biopsy site on the same leg.

Metabolic data.

Collection of expired gases occurred during the initial 5 min on the CE to ensure that the appropriate workload (V˙O2 (L·min−1)) was prescribed. The workload was adjusted as needed. After this time, expired gases were collected during the last 5 min of the TM segment during hours 1, 3, 5, 6, 8, and 10.

Whole-body substrate use.

Whole-body substrate use was calculated from the steady-state V˙O2 and VCO2 data (12) collected during the TM exercise. The last 2.5 min of expired gas data collected on the TM was averaged to determine V˙O2, VCO2, fat oxidation (μmol·kg−1·min−1, μmol·kg−1 FFM·min−1), and CHO oxidation (μmol·kg−1·min−1, μmol·kg−1 FFM·min−1) (12).

Muscle glycogen assay.

Muscle glycogen was analyzed using a spectrophotometric method (Infinity glucose reagent, Thermo Electron, Melbourne, Australia) after tissue preparation. Samples weighing about 20 mg w.w. (actual 19.7 ± 3.9 mg w.w.) were weighed on removal from a −80°C freezer. Samples were placed in 1000 μL of 1 N HCl solution and homogenized using a manual mortar and pestle tissue grinder. Once homogenized, samples were incubated at 95.6°C for 3 h. After the incubation, 500 μL of 1 N NaOH was added to 500 μL of boiled tissue sample to normalize pH. Samples were analyzed in triplicate, after pipetting 40 μL of sample into 1 mL of the Infinity glucose reagent, and the mixture was incubated at room temperature for 15 min, using a spectrophotometer (Spectronic 402, Milton Roy, Rochester, NY), against glycogen and glucose controls using methods similar to those of Ruby et al. (27). Muscle glycogen was expressed in millimoles per kilogram wet weight of muscle.

Statistical procedures.

Descriptive data are expressed as means ± SD. All descriptive data were analyzed across sex using an independent, two-tailed t-test. Other statistical analysis used a mixed design ANOVA with repeated measures (Abacus Concepts, Inc, Berkley, CA). Main effects and interactions were analyzed using a series of a priori, planned comparisons with a Bonferroni correction where necessary. The level of significance for the experiment was set at an overall alpha of 0.05.

RESULTS

Descriptive data.

Subject descriptive data are summarized in Table 1. Males were heavier, with a lower percent body fat, higher FFM, absolute (L·min−1) and relative (mL·kg−1·min−1, mL·kg−1 FFM·min−1) V˙O2peak, and absolute VT (L·min−1) (P < 0.05). When values for VT were expressed relative to body mass, FFM, and peak oxygen consumption (% V˙O2peak), there were no significant differences between sexes.

Exercise descriptive data.

The workload intensities for VT and 70% VT are summarized in Table 2. There were no differences between males and females for the exercise intensities in either mode of exercise when expressed relative to VT. However, when the exercise intensity was expressed relative to V˙O2peak, values were significantly higher for the females during the TM. Also, males performed exercise at a significantly higher absolute workload (W) on the cycle ergometer compared with females.

T2-10
TABLE 2:
Exercise intensities (N = 13).

There were no differences between males and females for HR or RPE for either trial (Table 3). Slight increases were noted in RPE for the PLA trial compared with the CHO trial, but values were not statistically significant.

T3-10
TABLE 3:
Rate of perceived exertion (RPE) and heart rate response (N = 13).

Blood glucose.

Blood glucose (BG) demonstrated no statistically significant differences between the sexes (Fig. 2). There was no interaction for blood glucose between PLA and CHO trials. The data demonstrated a main effect for time, indicating that blood glucose decreased with exercise time. However, the preexercise values for BG were taken an average of 22 ± 3 min after consumption of the standardized breakfast.

F2-10
FIGURE 2:
Blood glucose (mM) for the two exercise trials. d = P < 0.05 vs pre for males and females and CHO and PLA trial. Main effect for time.

Substrate oxidation.

Total energy expenditure was higher in males across all times and trials. However, RER was similar between sexes (Table 4).

T4-10
TABLE 4:
Respiratory exchange ratio and energy expenditure (N = 13).

Values for CHO oxidation (expressed relative to total body weight and to FFM) were significantly higher during the CHO trial compared with the PLA trial for both males and females. There were no significant differences between the males and females during the CHO trial. However, females maintained a significantly higher rate of whole-body CHO oxidation during the PLA trial compared with the males (Fig. 3). The time × trial interaction (males and females pooled) was also statistically significant. All time points after hour 1 demonstrated significantly higher rates of CHO oxidation values for the CHO trial compared with the PLA trial. In addition, CHO oxidation demonstrated a significant decrease after hour 1 in the PLA trial, but it was maintained until late in the day during the CHO trial (Fig. 3).

F3-10
FIGURE 3:
Whole-body carbohydrate oxidation (μmol·kg−1 FFM·min−1) for the two exercise trials. a = P < 0.05 vs PLA (time × trial interaction). b = P < 0.05 vs hour 1 (time × trial interaction). c = P < 0.05 vs females for PLA (sex × trial interaction).

Whole-body fat oxidation (expressed relative to total body weight and to FFM) demonstrated no sex-specific significant interactions (Fig. 4). Values for fat oxidation were significantly higher for the PLA trial compared with the CHO trial for both sexes. The time × trial interaction (males and females pooled) was statistically significant for fat oxidation, demonstrating increased fat oxidation in hours 3, 5, and 10 in the CHO trial, and in all hours in the PLA trial, when compared with hour 1 in either trial. Also, fat oxidation was maintained at higher rates during the PLA trial compared with the CHO trial in all hours after hour 1 (Fig. 4).

F4-10
FIGURE 4:
Whole-body fat oxidation (μmol·kg−1 FFM·min−1) for the two exercise trials. a = P < 0.05 vs CHO (time × trial interaction). b = P < 0.05 vs hour 1 (time × trial interaction).

Glycogen.

For the measure of muscle glycogen, there was no significant effect of sex. However, the trial × time interaction (males and females pooled) indicated a significant decrease in muscle glycogen for both PLA and CHO trials. In addition, the PLA trial preexercise glycogen concentration was slightly higher compared with the CHO trial, and the postexercise glycogen was significantly lower in the PLA trial compared with the CHO trial. When glycogen was expressed in millimoles per kilogram wet weight, the interaction (males and females pooled) demonstrated a significantly higher (52%) net muscle glycogen use for the PLA trial compared with the CHO (Fig. 5).

F5-10
FIGURE 5:
Net muscle glycogen (mmol·kg−1 w.w.) for the two exercise trials (males and females pooled). a = P < 0.05 vs PLA (time × trial interaction). b = P < 0.05 vs pre (time × trial interaction).

DISCUSSION

The effects of CHO supplementation on sex-specific whole-body and muscle substrate metabolism during exercise lasting for more than 5 h in duration has not been investigated. Numerous researchers have demonstrated conflicting results with regard to sex-specific substrate oxidation during exercise at shorter durations. The present study was designed to address both net muscle glycogen use during prolonged exercise and questions concerning sex-specific differences in substrate use across this extended time. In the present study, subjects maintained a low-intensity workload, which was prescribed relative to their VT closely representing "real-life" extended work intensities (31). This model was developed to imitate the work output performed throughout a typical manual labor, military operation, or wildfire suppression work shift, and it included segments of upper- and lower-body exercise and short periods of recovery during each hour of activity. Intensity and mode of exercise, energy expenditure, caloric intake, and proportions of macronutrients and rest periods for the subjects were controlled to better simulate a field situation. Although previous researchers have addressed the effects of exogenous carbohydrate feeding on whole-body and muscle substrate oxidation, the majority of these studies include exercise durations from 60 to 240 min. Because some occupations and exercise competitions far exceed this range, the present exercise protocol was designed to better evaluate the effects of carbohydrate feeding on substrate metabolism during extended muscle work. Moreover, conclusions regarding sex-specific carbohydrate and fat oxidation are usually based on relatively short exercise sessions. Our intention at including a sex comparison was to better evaluate the potential differences and/or similarities in substrate oxidation during extended occupational and ultraendurance work. The work intensities were selected relative to VT to account for possible individual differences in RER that may be noted when scaling work relative to V˙O2peak, and to allow comparisons of sex-specific substrate oxidation during extended work scenarios. Another unique aspect of this study was that subjects were not completely fasted during either trial. During the PLA trial, subjects were fed a standardized breakfast and lunch to more closely resemble a typical occupational setting.

To standardize exercise intensities, past researchers have matched subjects on the basis of background exercise habits, competitive history, and V˙O2peak (4,21,25,32,33). Exercise intensity in the present study was expressed relative to VT to ensure similar metabolic states between sexes. Although females exercised at a significantly higher workload for the treadmill when expressed as percent V˙O2peak, there was no difference in the percentage of VT between the sexes, and there were no differences in ratings of perceived exertion or RER (Table 2). This matching ensured similar work intensities, relative to training, for both modes of exercise between males and females. Scaling exercise intensity relative to VT ensures that subjects are exercising relative to their most frequent training zone or long-duration sustainable workload (31). This also ensures a similar metabolic demand for each subject regardless of trained state or sex.

The results from this study demonstrate no significant sex-specific differences in whole-body substrate oxidation when values were expressed relative to body mass or FFM. The results from this study are in contrast to those of Horton et al. (18), who have demonstrated that females oxidize a higher relative amount of fat in comparison with males in response to 2 h at 40% V˙O2peak. However, the current results are similar to the data of Riddell et al. (24), who have demonstrated a diminished effect of sex when subjects were tested in the fed versus fasted state. Interestingly, during the current PLA trial, females demonstrated a significantly higher rate of CHO oxidation compared with males, which is in opposition with the majority of previous sex comparative research. However, these current findings may be supported by the findings of Zderic et al. (37), who have demonstrated that females use a higher amount of CHO during the follicular phase of the menstrual cycle, which is when females in the current study were investigated.

Previous researchers have demonstrated that estradiol affects substrate oxidation (8,16,29,32,37,38). The results from these studies have demonstrated that the female hormonal milieu is complex and may affect fat and CHO oxidation at rest and during exercise. Although past research has suggested that estradiol may exert subtle metabolic effects on substrate metabolism during submaximal exercise, these variations may be overridden by the stress associated with the duration of the present exercise model. The subjects in this study were recreationally trained subjects, and they did not perform exercise completely fasted. This exercise trial was also performed at an intensity below 50% V˙O2peak, and for a period of 10 h, a much longer duration and generally lower intensity than has been studied in the past. Therefore, the effects of the exercise protocol may have more influence on substrate metabolism compared with the effects associated with the reproductive hormonal milieu (3,21,23-26,30,36).

Levels of estrogen and progesterone may have an impact on the source of CHO in females during exercise (8,16,37). Ruby et al. (26) have also suggested that females demonstrate a higher relative contribution from blood glucose as a CHO source for energy during submaximal exercise compared with males. This has also been suggested by Friedlander et al. (13), where males and females were exercise trained to determine changes in substrate oxidation at the same absolute and relative exercise intensities. However, in the present study, blood glucose was not significantly different across trials or between the sexes. This further suggests that static measures of blood glucose cannot adequately represent the complex patterns of glucose kinetics resulting from hepatic and gut Ra or muscle glucose uptake and oxidation.

It has been demonstrated that CHO feedings administered at a high rate (1.0-1.7 g·min−1) can completely suppress liver glycogenolysis, but there are conflicting data regarding the effects on muscle glycogenolysis (4,6,11,20,34,36). Muscle glycogen is expressed as net glycogen in the current investigation because muscle glycogen use may be slowed with CHO supplementation, but there may also be an increased rate of muscle glycogen resynthesis during the rest periods of this exercise protocol. In the present study, net muscle glycogen use was approximately 52% higher for the PLA trial compared with the CHO trial.

Previous researchers have demonstrated that females display lower RER values compared with males during exercise at the same percent V˙O2peak, and, in turn, they use a higher percentage of energy contribution from fat sources. Moreover, some researchers have demonstrated that females use less glycogen and have lower blood glucose concentrations at the end of exercise at intensities relative to V˙O2peak (1,18,32,33). Although this has been demonstrated, many researchers have not controlled for differences in muscle glycogen before the onset of exercise. During the present investigation, there were no differences between glycogen content before exercise in males and females, and no differences in net muscle glycogen use were observed between the sexes. These data are supported by the recent findings of Zehnder et al. (38). Although they demonstrate a significant reduction in muscle glycogen and intramuscular triglyceride use, there were no differences between the males and females in muscle glycogen use after 3 h of cycling at 50% V˙O2peak.

In arduous field settings and ultraendurance activities, performance is important. In these settings, work output may be increased when CHO is provided, and physical activity may be maintained at higher intensities (5,7,9,19,20). In three different CHO supplementation studies, Cuddy et al. (7) have demonstrated that the RPE in individuals remained the same when they were provided with CHO, but that about 20% more work was accomplished by the individuals on these Wildland Firefighter (WLFF) crews. This difference was especially noticeable during the later portions of the 12-h work shift. Many studies have shown the link between exogenous CHO supplementation and increased performance in both males and females (5,9,19,20). In field operations with the military or WLFF work settings, glycogen and/or carbohydrate availability may be linked to safety. Although this link has not clearly been studied in a research setting, the previous research that demonstrates increased time to fatigue and increased performance measures would support this concept. If more endogenous CHO were available during periods of higher-intensity work, performance in a sprint to safety may be increased. The higher postexercise muscle glycogen concentration noted for the CHO trial in the current study highlights the importance of regular CHO feedings in arduous work settings and ultraendurance exercise.

In conclusion, the results from this study indicate that females and males exhibit similar patterns of whole-body and muscle glycogen use when fed CHO during 10 h of exercise. Although past research has demonstrated that estradiol exerts a subtle effect on metabolism, dominant control of whole-body and muscle substrate oxidation is likely provided by training status, exercise intensity and duration, and exogenous feeding. These results suggest that future research should also further evaluate the potential of muscle glycogen sparing during long-duration exercise of varying intensity. Measures of physical and cognitive performance could also be included in this type of design to answer questions of safety and performance in ultraendurance and occupational settings.

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Keywords:

SUBSTRATE OXIDATION; GENDER; SEX-SPECIFIC HORMONES; GLYCOGENOLYSIS

©2007The American College of Sports Medicine