| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Vol. 83, Issue 6, 1877-1883, December 1997
Departments of 1 Medicine and 2 Kinesiology, McMaster University, Hamilton, Ontario, Canada L8S 4K1
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Tarnopolsky, M. A., M. Bosman, J. R. MacDonald, D. Vandeputte, J. Martin, and B. D. Roy. Postexercise
protein-carbohydrate and carbohydrate supplements increase muscle
glycogen in men and women. J. Appl.
Physiol. 83(6): 1877-1883, 1997.
We have
previously demonstrated that women did not increase intramuscular
glycogen in response to an increased percent of dietary carbohydrate
(CHO) (from 60 to 75% of energy intake) (M. A. Tarnopolsky, S. A. Atkinson, S. M. Phillips, and J. D. MacDougall.
J. Appl. Physiol. 78: 1360-1368, 1995). CHO and CHO-protein (Pro) supplementation postexercise can
potentiate glycogen resynthesis compared with placebo (K. M. Zawadzki,
B. B. Yaspelkis, and J. L. Ivy. J. Appl.
Physiol. 72: 1854-1859, 1992). We studied the
effect of isoenergetic CHO and CHO-Pro-Fat supplements on muscle
glycogen resynthesis in the first 4 h after endurance exercise (90 min
at 65% peak O2 consumption) in
trained endurance athletes (men, n = 8; women, tested in midfollicular phase,
n = 8). Each subject completed three
sequential trials separated by 3 wk; a supplement was provided immediately and 1-h postexercise: 1)
CHO (0.75 g/kg) + Pro (0.1 g/kg) + Fat (0.02 g/kg),
2) CHO (1 g/kg), and
3) placebo (Pl; artificial
sweetener). Subjects were given prepackaged, isoenergetic, isonitrogenous diets, individualized to their habitual diet, for the
day before and during the exercise trial. During exercise, women
oxidized more lipid than did men (P < 0.05). Both of the supplement trials resulted in greater
postexercise glucose and insulin compared with Pl
(P < 0.01), with no gender
differences. Similarly, both of these trials resulted in increased
glycogen resynthesis (37.2 vs. 24.6 mmol · kg dry
muscle
1 · h1,
CHO vs. CHO-Pro-Fat, respectively) compared with Pl (7.5 mmol · kg dry
muscle1 · h1;
P < 0.001) with no gender
differences. We conclude that postexercise CHO and CHO-Pro-Fat
nutritional supplements can increase glycogen resynthesis to a greater
extent than Pl for both men and women.
gender; sex differences; defined formula; exercise
INTRODUCTION THE TIMING of the provision of nutrients after exercise
has become a popular subject in recent years (3, 11, 26). It is known
that carbohydrate (CHO) supplements provided within the first several
minutes of completion of exercise result in a more rapid repletion of
muscle glycogen compared with the same supplement provided 2 h after
completion of exercise (11). The mechanism responsible for this
observation is thought to be related to the combined effect of insulin
and contraction-stimulated glucose transport via GLUT-4 transporters
(6). The migration of these transporters from intracellular stores to
the sarcolemma and t tubules of muscle is partially mediated by
phosphatidylinositol 3-kinase (8). The practical implication of these
findings is that it may be possible to accentuate glycogen
repletion by merely altering the timing of nutrient provision (i.e.,
providing nutrients shortly after exercise termination).
It has been suggested that a combination protein (Pro) and CHO
supplement provided immediately postexercise may potentiate insulin
release and, hence, glycogen repletion (26). For example, Zawadzki and
colleagues (26) found that the insulin rise and glycogen repletion rate
was 39% greater with a combined Pro-CHO compared with a CHO
supplement. The confounding factor in this latter study was the
provision of 43% more energy in the Pro-CHO trial compared with the
CHO trial; thus two variables changed simultaneously. Therefore, one
purpose of the present study was to compare the rate of glycogen
resynthesis after endurance exercise when the energy content of both
the postexercise supplement (CHO compared with CHO-Pro-Fat) and the
24-h energy intake of all trials was held constant.
In addition, almost all of the research that has been conducted to
examine postexercise supplements has used male subjects exclusively (5,
11, 26). Aside from the inherent gender bias, there is also
accumulating evidence that there are sex differences in the metabolic
response to endurance exercise (22-24). These differences may be
related to our recent finding that men, but not women, increase muscle
glycogen concentration in response to an increase in dietary CHO
content from 60 to 75% of energy intake (21). Therefore, a second
purpose of this study was to examine postexercise glycogen repletion in
both sexes.
We had three a priori hypotheses. 1)
There would be no difference in the rate of glycogen repletion between
CHO and CHO-Pro-Fat supplements, yet there would be a greater rate of
glycogen repletion compared with placebo (Pl).
2) The glycogen repletion rate for women would be less than that observed in men.
3) Women would have a lower
respiratory exchange ratio (RER) during endurance exercise (indicative
of greater lipid oxidation).
METHODS
O2 peak)
of at least 55 ml · kg1 · min1.
Women were matched to the men by training history and required a
O2 peak of at least
50 ml · kg1 · min1.
Equalized matching based on these parameters was confirmed by the
similarity in O2 peak
when expressed per kilogram lean mass (Table
1).
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
O2 peak was
determined on an electrically braked cycle ergometer by using a
computerized open-circuit gas-collection system as previously described
(17). O2 peak was
considered to be the highest value recorded during a standard
incremental cycle ergometer protocol, with termination of the test
after O2 consumption
(O2) values
reached a plateau for three readings, RER was >1.12, and subjects
could not sustain pedal revolutions at ~60 revolutions/min (rpm)
despite vigorous encouragement. Body density was determined by
hydrostatic weighing, and percent body fat was calculated as described
(17).
All subjects collected 4-day diet records, which were analyzed by using
a nutritional analysis software package (Nutritionist IV; First Data
Bank, San Bruno, CA). For each subject, individual diets were designed
that were both isoenergetic and isonitrogenous for the three trials.
The only parameter that was different was the composition of the
postexercise supplement on day 1 (practice day) and day 5 (test day).
For example, on the Pl-testing trial, the Pl drink was given
postexercise and a CHO-Pro-Fat supplement was provided with supper. The
reverse was true for the CHO-Pro-Fat trial; namely, the Pl supplement
was provided with supper. For the CHO trial, a Pro-Fat supplement was
provided with supper (Table 2). Thus, over
a 24-h period, the energy and nutritional composition of each trial was
identical (Table 3). Diets were rigidly controlled over
the 5-day experimental protocol for each of the three trials. Subjects
were instructed to eat only the prepackaged diets provided on
days 1,
4, and
5. Individual checklist diets were
followed on the alternate days (days 2 and 3). Compliance was assessed by
analyzing the diet checklists that were returned by each subject. Furthermore, on the days when food was prepackaged, they returned any
uneaten food for weighing. The apparent energy intake
compliance was >96% of that distributed.
|
|||||||||||||||||||||||||||||||||||||||||
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
O2 peak for 90 min.
Day 1 was designed as a controlled
trial practice session in preparation for day
5 and was performed in the evening (from 1700 to 2000), with postexercise supplements identical to that described below for
day 5. No exercise was performed in
the 24 h before each of these testing days. On day
2, subjects arrived at the laboratory in a fasted state
(at 0700-0900) and performed a high-intensity ride to exhaustion
at a preset load designed to elicit 75% of O2 peak. The ride was
terminated when subjects could not sustain pedal revolutions of >60
rpm. Subjects cycled for 45 min at 65% of
O2 peak on
day 3 and rested on
day 4.
On day 5, subjects arrived in a fasted
state (at 0700-0900), and a 22-gauge plastic catheter was inserted
into the antecubital vein for blood sampling. Blood samples were then
collected into prechilled, heparinized tubes every 30 min during
exercise and every 20 min up to 2 h postexercise. Additional samples
were collected at 3 and 4 h postexercise, and the catheter was then
removed. These tubes were centrifuged immediately, and aliquots of
plasma were stored at 
50°C for subsequent analysis of
glucose and insulin.
After the exercise was completed, a muscle biopsy was obtained from the
vastus lateralis by using a suction-modified Bergstrom needle-biopsy
technique. A supplement (CHO-Pro-Fat in trial
1, CHO in trial 2, and
Pl in trial 3) was given immediately
after the muscle biopsy [time 0 (t = 0)] and at 1 h
(t = +1) after the first supplement. A
second needle biopsy was performed on the contralateral vastus
lateralis 4 h after the first supplement (t = +4). All biopsy samples were
blotted and dissected free of visible connective tissue, quenched in
liquid nitrogen, and then stored at 50°C for later analysis
of muscle glycogen.
During each trial, 24-h urine collections were completed over
day 4 (rest) and day
5 (exercise). Aliquots were taken and stored at
50°C for subsequent analysis of creatinine and total urea nitrogen.
Plasma and urine.
All plasma samples were assayed for insulin by radioimmunoassay
(Diagnostics Products, Los Angeles, CA). Glucose was determined by
spectrophotometry (kit 135, Sigma Diagnostics, St. Louis, MO). Intra-assay coefficient of variation for glucose and insulin was <5%.
Rest and exercise 24-h urine collections were assayed by using
spectrophotometry to determine urea nitrogen (procedure 640, Sigma
Diagnostics) and urine creatinine (kit 555-A, Sigma Diagnostics).
Muscle glycogen analysis.
Before analysis, the muscle samples were lyophilized and powdered, and
any visible remaining blood or connective tissue was removed before
weighing. Glycogen concentration was determined by a method adapted
from that described by Bergmeyer (1). Briefly, 160 µl of NaOH were
added to ~2.0-4.0 mg of dry muscle (dm) tissue and mixed
thoroughly. After incubation at 80°C for 10 min, 640 µl of a
combined acid-buffer solution (HCl-citrate) were added to
neutralize the sample. Then 40 µl of a reagent solution were added
[in mM: 375 triethanolamine, 150 KOH, 112.5 Mg(Ac)2-H2O, 3.75 EDTA-Na2-H2O], along with 5 µl of 45 mM ATP solution, 5 µl of 60 mM
dithiothreitol solution, and 10 µl of 30 mM NAD
solution. Background absorbance measures were then made
with an ultraviolet spectrophotometer at 340 nm (model 1201; Shimadzu,
Tokyo, Japan). Then 4 µl were added of a combined glucose 6-phosphate
dehydrogenase/HK solution (200 units of glucose 6-phosphate
dehydrogenase with 200 U HK, dissolved in 800 µl doubly distilled
water; Sigma Chemical, St. Louis, MO). Absorbance at 340 nm was then measured 15 min after the addition of the enzyme solution.
Background absorbance was then subtracted from the reaction absorbance,
and the obtained value was plotted against a glycogen standard (Sigma
Chemical) curve for determination of glycogen concentration. Muscle
glycogen concentrations are presented as millimoles of glycogen per
kilogram of dm weight per hour.
Calculations.
Muscle glycogen resyntheses rate was calculated from the equation: Rate = (Gpost Gpre)/t,
where Gpre is the muscle glycogen concentration immediately postexercise,
Gpost is the muscle glycogen concentration 4 h postexercise, and t
is the time between the two biopsies.
Statistics.
Muscle and blood data were analyzed by using repeated-measures analysis
of variance (gender × time × condition) (version 5.0 Statistica, Statsoft, Tulsa, OK). When a significant interaction was
found, Tukey's post hoc analysis was used to locate the pairwise differences. Integrated area under the curve data for glucose and
insulin was analyzed by using a one-way repeated-measures analysis of
variance (version 5.0 Statistica). P < 0.05 was accepted as statistical significance. Values are expressed
as means ± SD.
RESULTS
O2 or heart rate for any of
the three trials (Table 4). There were no
differences between the trials in 24-h urea nitrogen or creatinine.
There was a trend for 24-h urea nitrogen and creatine to be greater on
the exercise day compared with the rest day [not significant
(NS)]. There were no differences between men and women in 24-h
urea nitrogen and creatinine. The total energy cost of the 90-min
exercise bout at 65%
O2 peak for the men was
1,214, 1,198, and 1,214 kcal for the CHO-Fat/Pro, CHO, and Pl trials, respectively. Similarly, the total energy cost for the women at 65%
O2 peak
was 910, 899, and 963 kcal for the CHO-Fat/Pro, CHO, and Pl trials,
respectively. Lipid contributed to ~29% of the total energy cost for
the women and 23% for the men of the 90-min exercise bout over the
three trials (P < 0.005). CHO
contributed 75% of the energy cost of the three trials for the men and
68% for the women (P < 0.005). Pro
contributed 2% to the energy cost of the 90 min of exercise for the
men and 3% for the women (NS; calculated from RER and urea by using
equations from Ref. 9).
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
1 · h1
in CHO-Pro-Fat vs. CHO vs. Pl trials, respectively;
P < 0.01). There were
no significant differences between men and women.
There were no differences between the three trials in plasma glucose concentration at baseline or during exercise. The CHO trial resulted in significantly higher plasma glucose at 40, 60, 80, 100, and 120 min compared with the Pl trial (P < 0.01; Fig. 1A). The CHO-Pro-Fat trial resulted in an increase in glucose vs. the Pl trial, although only the 40-min time point was statistically significant (P < 0.05). The area under the glucose curve was not statistically different between the CHO-Pro-Fat and the CHO trial (4.75 vs. 5.35 mM/h, respectively) but these were both greater than the Pl trial (4.06 mM/h; P < 0.05; Fig. 1A, right). There were no significant differences between men and women. Glycogen. The rates of postexercise muscle glycogen recovery for both the CHO-Pro-Fat and the CHO trials were significantly higher (P < 0.05) compared with the Pl trials [in mmol · kg dm
1 · h1
(men vs. women, respectively): CHO-Pro-Fat, 25.5 vs.
23.5; CHO, 40.0 vs. 34.5; Pl, 3.0 vs. 12.0].
There were no significant differences in muscle glycogen recovery rates
between men and women for any of the three trials (Fig.
2). For both the CHO-Pro-Fat
and the CHO trials, the muscle glycogen concentration was significantly higher (P < 0.001) at
t = +4 h compared with the
immediate postexercise time point (t = 0) (CHO-Pro-Fat, from 142.4 ± 69 to 245.2 ± 75 mmol/kg dm; CHO,
from 163.4 ± 53.6 to 312.8 ± 56 mmol/kg dm). The Pl trial did
not result in an increased muscle glycogen concentration after 4 h
(from 210 ± 68 to 237 ± 80 mmol/kg dm; NS). Post hoc analysis
demonstrated that the glycogen concentration at
t = 0 was greater for the Pl trial
compared with the CHO-Pro-Fat and CHO trials
(P < 0.01).
DISCUSSION
We have demonstrated that postexercise muscle glycogen resynthesis rates are similar for both CHO and isoenergetic CHO-Pro-Fat supplements and that both of these are greater than for a Pl. Contrary to our other hypothesis, the resynthesis rate was similar for men and women.
Some have questioned the practical value of postexercise supplements because of the observation that muscle glycogen concentrations were not different 8 and 24 h after exercise cessation when CHO was provided immediately or after a 2-h time delay (16). However, there are several examples where early postexercise supplementation may be of practical benefit: 1) when an athlete is training or competing more than once per day, 2) when an athlete exercises in the evening on one day and again the next morning, and 3) when an athlete may not be able to consume a high-CHO diet over the ensuing 24-h postexercise period.
The finding of similar postexercise insulin responses with different supplements is consistent with some (5, 18a) but not all (21, 26) studies. Zawadzki and colleagues (26) found that plasma insulin concentrations and glycogen resynthesis rates were greater for CHO-Pro compared with CHO supplements. However, it is not possible to separate the cointervention of added energy intake (+43%) from the macronutrient compositional changes in their study (26). Our finding of no difference in glycogen resynthesis between isoenergetic CHO and CHO-Pro-Fat supplements suggests that energy intake may have contributed to the observations in the latter study (26). The finding of similar insulin and glucose responses was also confirmed in other studies where isoenergetic CHO and CHO-Pro (5) and CHO-Pro-Fat (unpublished observations by B. D. Roy and M. A. Tarnopolsky) were compared after resistance exercise. It may be argued that the minimal fat content of the supplement used in our study may have confounded the results by inhibiting gastric emptying and, thus, potentially inhibiting the rapid provision of CHO to the muscle and CHO-Pro to the pancreas for insulin release. We do not feel that gastric inhibition was a factor, because insulin rose rapidly in the CHO-Pro-Fat trial and was not statistically different from the CHO trial at any time after the supplement. Furthermore, over a 24-h period after endurance exercise, the addition of similar amounts of fat to the diet did not impair glycogen resynthesis in a study of eight well-trained endurance athletes (3). The CHO source used in the current study was sucrose (contains fructose) and glucose polymers rather than glucose in the study by Zawadzki et al. (26). However, there were very similar insulin responses observed in Zawadzki's study (26) compared with the present study. Thus it is unlikely that this could have altered the results. Furthermore, the most important comparison in the present study was that between the CHO and CHO-Pro-Fat trial, and the CHO source was identical in these.
It could also be argued that the order of the trials in our study could
have influenced the results. However, we found no difference between
the trials in O2, heart rate,
RER, insulin, or glucose during exercise. Because we
studied trained endurance athletes who were accustomed to this training
intensity and we separated the trials by nearly 1 mo, a training effect
would be further negated. However, the postexercise glycogen
concentration was significantly greater for the Pl trial compared with
the other trials because of two outliers (1 in each gender). These
subjects were predominantly runners, and it is possible that they
developed a more efficient cycling form in subsequent trials. A greater reliance on the gastrocnemius and hamstrings (by use of toeclips) would
reduce the work of the quadriceps muscles. Lower glycogen concentrations can result in greater glycogen resynthesis rates per se
(18, 27). However, this difference is only significant when muscle
glycogen concentrations are <120 mmol/kg dm (18). The 27% difference
in glycogen concentration between the two supplement trials compared
with the Pl trial fell within the range (120-280 mmol/kg dm) that has been shown to have no effect on glycogen resynthesis rates (18). Furthermore, the postexercise glycogen values
for the CHO-Pro-Fat and CHO trials were nearly identical, and the
comparison between these two trials was the most important measurement
in the present study.
A strength of the present study was the provision to each of the subjects in each trial of prepackaged diets that were isoenergetic to the subjects' habitual diet. We also controlled for 24-h energy intake by providing complimentary blinded supplements later in the day to ensure that the macronutrient composition over the 24-h period was consistent. This is important to examine the true effect of the timing of macronutrient provision not confounded by supplemental energy. A practical advantage of this approach is that we have found that women and those on restricted energy intakes are reluctant to consume additional energy. Another advantage of combination postexercise supplements is that they provide "balanced" macronutrients. For example, if one were to give a 1 g/kg CHO drink after exercise at t = 0 and +1 h to a woman weighing 60 kg, the energy content would be 480 kcal. With an energy intake of ~2,000 kcal, this would amount to ~25% of daily intake as a simple sugar. If this were part of a habitual diet, it might limit intake of vitamins, calcium, iron, and other minerals (25) that may be of particular concern for the female athlete (7, 12). Furthermore, habitual endurance training increases protein requirements for male (14, 23) and female (17) athletes.
Our group has previously demonstrated that men, but not women, increased muscle glycogen concentration in response to an increase in dietary CHO from 60 to 75% of energy intake (24). The results of the present study, however, were contradictory to our a priori hypothesis and did not show a difference between the genders in the rate of glycogen repletion. This is an important finding for female athletes, who may have a limited ability to supercompensate (24). Whether the provision of supplements in the early postexercise period may permit glycogen supercompensation in women remains to be explored.
Our finding of a lower RER for the women in the present study has been
demonstrated in three of our previous studies (17, 22, 24) and by
others (2, 15, 10). The RER finding indicates a greater lipid and
lesser CHO oxidation for women during endurance exercise at 65%
O2 peak. We found a
trend toward a higher urea excretion on the exercise day for both men
and women. This suggested a trend toward an increased whole body
protein oxidation consequent to the exercise stress (17). Contrary to our work in nutrient supplementation after resistance exercise (unpublished observations by B. D. Roy and M. A. Tarnopolsky), we did
not demonstrate a suppression of urea excretion for the two supplement
trials compared with the placebo trial. This may relate to differing
metabolic situations after these types of activity. After resistance
exercise, for example, we found that the reduction in urea excretion
for the early supplement trial paralleled a decline in
3-methylhistidine excretion (indicative of lesser myofibrillar protein
degradation) (18a). Although 3-methylhistidine was not
measured in this study, it is unlikely that habitual
endurance exercise at 65%
O2 peak would be
associated with myofibrillar protein breakdown (4). Therefore, the
trend toward an increased urea excretion on the exercise day was likely
caused by an increased protein oxidation during (13, 17) and not after
exercise.
In summary, we have demonstrated that, compared with a Pl drink, CHO and CHO-Pro-Fat supplements when given early after endurance exercise result in more rapid glycogen resynthesis rates. Importantly, this finding is true for both male and female athletes.
ACKNOWLEDGEMENTS
We thank Roxanna Birsan for technical assistance.
FOOTNOTES
Address for reprint requests: M. Tarnopolsky, Depts. of Neurology, Physical Medicine, and Kinesiology, Rm. 205, Ivor Wynne Centre, McMaster Univ., Hamilton, Ontario, Canada L8S 4K1 (E-mail: tarnopol{at}mcmaster.ca).
Received 29 May 1997; accepted in final form 28 July 1997.
REFERENCES
| 1. | Bergmeyer, H. U. (Editor). Methods of Enzymatic Analysis. New York: Academic, 1985, vol. VI, p. 11-18. |
| 2. | Blatchford, F. K., R. G. Knowlton, and D. A. Schneider. Plasma FFA responses to prolonged walking in untrained men and women. Eur. J. Appl. Physiol. 53: 343-347, 1985[Medline]. |
| 3. |
Burke, L. M.,
G. R. Collier,
S. K. Beasley,
P. G. Davis,
P. A. Fricker,
P. Heeley,
K. Walder,
and
M. Hargreaves.
Effect of coingestion of fat and protein with carbohydrate feedings on muscle glycogen storage.
J. Appl. Physiol.
78:
2187-2192,
1995 |
| 4. |
Calles-Escandon, J.,
J. J. Cunningham,
R. Jacob,
J. Loke,
G. Husgaar,
and
P. Felig.
Influence of exercise on urea, creatinine, and 3-methylhistidine excretion in normal man.
Am. J. Physiol.
246 ((Endocrinol. Metab. 9):
E334-E338,
1984 |
| 5. |
Chandler, R. M.,
H. K. Byrne,
J. G. Patterson,
and
J. L. Ivy.
Dietary supplements affect the anabolic hormones after weight-training exercise.
J. Appl. Physiol.
76:
839-845,
1994 |
| 6. | Coderre, L., K. V. Kandror, G. Vallega, and P. F. Pilch. Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle. J. Biol. Chem. 46: 27584-27588, 1995. |
| 7. | Deuster, P. A., S. B. Kyle, P. B. Moser, R. A. Vigersky, A. Singh, and E. B. Schoomaker. Nutritional survey of highly trained women runners. Am. J. Clin. Nutr. 45: 954-962, 1986. |
| 8. | Folli, F., M. J. Saad, J. M. Backer, and C. R. Kahn. Regulation of phosphatidylinositol 3-kinase in liver and muscle of animal models of insulin-resistant and insulin-deficient diabetes mellitus. J. Clin. Invest. 92: 1787-1794, 1993. |
| 9. |
Frayn, K. N.
Calculation of substrate oxidation rates in vivo from gaseous exchange.
J. Appl. Physiol.
55:
628-634,
1983 |
| 10. | Froberg, K., and P. K. Pedersen. Sex differences in endurance capacity and metabolic response to prolonged, heavy exercise. Eur. J. Appl. Physiol. 52: 446-450, 1984. |
| 11. | Ivy, J. L., A. L. Katz, C. L. Cutler, W. M. Sherman, and E. F. Coyle. Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J. Appl. Physiol.: 1480-1485, 1988. |
| 12. | Janssen, G. M. E., C. J. J. Graef, and W. H. M. Saris. Food intake and body composition during a training period to run a marathon. Int. J. Sports Med. 10 Suppl. 1: S17-S21, 1989. |
| 13. |
Lamont, L. S.,
D. G. Patel,
and
S. C. Kalhan.
Leucine kinetics in endurance-trained humans.
J. Appl. Physiol.
69:
1-6,
1990 |
| 14. |
Meredith, C. N.,
M. J. Zackin,
W. R. Frontera,
and
W. J. Evans.
Dietary protein requirement and body protein metabolism in endurance trained men.
J. Appl. Physiol.
66:
2850-2856,
1989 |
| 15. | Nygaard, E. Women and exercise: with special reference to muscle morphology and metabolism. In: Biochemistry of Exercise, edited by J. Poortmans, and G. Niset. Baltimore, MD: Univ. Park Press, 1981, vol. IV-B, p. 161-175. |
| 16. | Parkin, J. A., M. F. Carey, I. K. Martin, L. Stojanovska, and M. A. Febbraio. Muscle glycogen storage following prolonged exercise: effect of timing of ingestion of high glycemic index food. Med. Sci. Sports Exerc. 29: 220-224, 1997[Medline]. |
| 17. |
Phillips, S. M.,
S. A. Atkinson,
M. A. Tarnopolsky,
and
J. D. MacDougall.
Gender differences in leucine kinetics and nitrogen balance in endurance athletes.
J. Appl. Physiol.
75:
2134-2141,
1993 |
| 18. |
Price, T. B.,
D. L. Rothman,
R. Taylor,
M. J. Avison,
G. I. Shulman,
and
R. G. Shulman.
Human muscle glycogen resynthesis after exercise: insulin-dependent and -independent phases.
J. Appl. Physiol.
76:
104-111,
1994 |
| 18a. |
Roy, B. D.,
M. A. Tarnopolsky,
J. D. MacDougall,
J. Fowles,
and
K. E. Yarasheski.
Effect of glucose supplement timing on protein metabolism after resistance training.
J. Appl. Physiol.
82:
1882-1888,
1997 |
| 19. | Roy, D., and A. Marette. Exercise induces the translocation of GLUT-4 to transverse tubules from an intracellular pool in rat skeletal muscle. Biochem. Biophys. Res. Commun. 223: 147-152, 1996[Medline]. |
| 21. |
Spiller, G. A.,
C. D. Jensen,
T. S. Pattison,
C. S. Chuck,
J. H. Whittim,
and
J. Scala.
Effect of protein dose on serum glucose and insulin response to sugars.
Am. J. Clin. Nutr.
46:
474-480,
1987 |
| 22. |
Tarnopolsky, L. J.,
J. D. MacDougall,
S. A. Atkinson,
M. A. Tarnopolsky,
and
J. R. Sutton.
Gender differences in substrate for endurance exercise.
J. Appl. Physiol.
68:
302-308,
1990 |
| 23. |
Tarnopolsky, M. A.,
S. A. Atkinson,
and
J. D. MacDougall.
Influence of protein intake and training status on nitrogen balance and lean body mass.
J. Appl. Physiol.
64:
187-193,
1988 |
| 24. |
Tarnopolsky, M. A.,
S. A. Atkinson,
S. M. Phillips,
and
J. D. MacDougall.
Carbohydrate loading and metabolism during exercise in men and women.
J. Appl. Physiol.
78:
1360-1368,
1995 |
| 25. | Van Erp-Baart, A. M. J., W. M. H. Saris, R. A. Binkhorst, J. A. Vos, and J. W. H. Elvers. Nationwide survey on nutritional habits in elite athletes. Part II. Mineral and vitamin intake. Int. J. Sports Med. 10 Suppl.: S11-S14, 1989. |
| 26. |
Zawadzki, K. M.,
B. B. Yaspelkis III,
and
J. L. Ivy.
Carbohydrate-protein complex increases the rate of muscle glycogen storage after exercise.
J. Appl. Physiol.
72:
1854-1859,
1992 |
| 27. | 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 synthesis. Med. Sci. Sports Exerc. 23: 44-48, 1991[Medline]. |
This article has been cited by other articles:
|
|
 |
|
  C. Roepstorff, M. Donsmark, M. Thiele, B. Vistisen, G. Stewart, K. Vissing, P. Schjerling, D. G. Hardie, H. Galbo, and B. Kiens Sex differences in hormone-sensitive lipase expression, activity, and phosphorylation in skeletal muscle at rest and during exercise Am J Physiol Endocrinol Metab, November 1, 2006; 291(5): E1106 - E1114. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. J. Horton, G. K. Grunwald, J. Lavely, and W. T. Donahoo Glucose kinetics differ between women and men, during and after exercise J Appl Physiol, June 1, 2006; 100(6): 1883 - 1894. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. C. Venables, J. Achten, and A. E. Jeukendrup Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study J Appl Physiol, January 1, 2005; 98(1): 160 - 167. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. M. Burke, G. R. Collier, E. M. Broad, P. G. Davis, D. T. Martin, A. J. Sanigorski, and M. Hargreaves Effect of alcohol intake on muscle glycogen storage after prolonged exercise J Appl Physiol, September 1, 2003; 95(3): 983 - 990. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Ivy, H. W. Goforth Jr., B. M. Damon, T. R. McCauley, E. C. Parsons, and T. B. Price Early postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement J Appl Physiol, October 1, 2002; 93(4): 1337 - 1344. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. J. Tunstall, K. A. Mehan, G. D. Wadley, G. R. Collier, A. Bonen, M. Hargreaves, and D. Cameron-Smith Exercise training increases lipid metabolism gene expression in human skeletal muscle Am J Physiol Endocrinol Metab, July 1, 2002; 283(1): E66 - E72. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. C. Ruby, A. R. Coggan, and T. W. Zderic Gender differences in glucose kinetics and substrate oxidation during exercise near the lactate threshold J Appl Physiol, March 1, 2002; 92(3): 1125 - 1132. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Roepstorff, C. H. Steffensen, M. Madsen, B. Stallknecht, I.-L. Kanstrup, E. A. Richter, and B. Kiens Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects Am J Physiol Endocrinol Metab, February 1, 2002; 282(2): E435 - E447. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. E. Campbell, D. J. Angus, and M. A. Febbraio Glucose kinetics and exercise performance during phases of the menstrual cycle: effect of glucose ingestion Am J Physiol Endocrinol Metab, October 1, 2001; 281(4): E817 - E825. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. L. P. G. Jentjens, L. J. C. van Loon, C. H. Mann, A. J. M. Wagenmakers, and A. E. Jeukendrup Addition of protein and amino acids to carbohydrates does not enhance postexercise muscle glycogen synthesis J Appl Physiol, August 1, 2001; 91(2): 839 - 846. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Tarnopolsky, C. Zawada, L. B. Richmond, S. Carter, J. Shearer, T. Graham, and S. M. Phillips Gender differences in carbohydrate loading are related to energy intake J Appl Physiol, July 1, 2001; 91(1): 225 - 230. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. L. Carter, C. Rennie, and M. A. Tarnopolsky Substrate utilization during endurance exercise in men and women after endurance training Am J Physiol Endocrinol Metab, June 1, 2001; 280(6): E898 - E907. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Carter, S. McKenzie, M. Mourtzakis, D. J. Mahoney, and M. A. Tarnopolsky Short-term 17{beta}-estradiol decreases glucose Ra but not whole body metabolism during endurance exercise J Appl Physiol, January 1, 2001; 90(1): 139 - 146. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Carrithers, D. L. Williamson, P. M. Gallagher, M. P. Godard, K. E. Schulze, and S. W. Trappe Effects of postexercise carbohydrate-protein feedings on muscle glycogen restoration J Appl Physiol, June 1, 2000; 88(6): 1976 - 1982. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Walker, G. J. F. Heigenhauser, E. Hultman, and L. L. Spriet Dietary carbohydrate, muscle glycogen content, and endurance performance in well-trained women J Appl Physiol, June 1, 2000; 88(6): 2151 - 2158. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. McKenzie, S. M. Phillips, S. L. Carter, S. Lowther, M. J. Gibala, and M. A. Tarnopolsky Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans Am J Physiol Endocrinol Metab, April 1, 2000; 278(4): E580 - E587. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
