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The role of dietary carbohydrates in muscle glycogen resynthesis after strenuous running

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This study examined the effect of the type, amount, and the frequency of feeding of carbohydrates on muscle glycogen resynthesis after running. Trained male runners performed a 16.1 km run at 80% VO2 max to decrease gastrocnemius glycogen levels. A complex or simple carbohydrate diet (approximately 3000 kcal) resulted in similar muscle glycogen levels 24 h after exercise. Forty-eight hours after exercise the complex carbohydrate diet resulted in significantly higher (p less than 0.05) muscle glycogen levels. Consuming increasing amounts of carbohydrate, between 88 to 648 g carbohydrate/day, resulted in increasingly larger amounts of muscle glycogen resynthesis (24 h) after exercise. Frequent feedings of a high carbohydrate diet did not enhance muscle glycogen synthesis when compared to equal amounts of carbohydrates in two meals. It appears that muscle glycogen can be normalized between daily strenuous running activity.
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1831
The role of dietary carbohydrates in muscle
glycogen resynthesis after strenuous running1’ 2
D. L. Costill,3 W. M. Sherman, W. J. Fink, C. Maresh, M. Witten, and J. M. Miller
ABSTRACT This study examined the effect of the type, amount, and the frequency of feeding
of carbohydrates on muscle glycogen resynthesis after running. Trained male runners performed
a 16. 1 km run at 80% VO2 max to decrease gastrocnemius glycogen levels. A complex or simple
carbohydrate diet (-3000 kcal) resulted in similar muscle glycogen levels 24 h after exercise. Forty-
eight hours after exercise the complex carbohydrate diet resulted in significantly higher (p <0.05)
muscle glycogen levels. Consuming increasing amounts of carbohydrate, between 188 to 648 g
carbohydrate/day, resulted in increasingly larger amounts of muscle glycogen resynthesis (24 h)
after exercise. Frequent feedings of a high carbohydrate diet did not enhance muscle glycogen
synthesis when compared to equal amounts of carbohydrates in two meals. It appears that muscle
glycogen can be normalized between daily strenuous running activity. Am. J. Clin. Nutr. 34:
1831-1836, 1981.
KEY WORDS Dietary carbohydrate, glycogen, physical exertion
The importance of muscle glycogen for
prolonged strenuous exercise is well docu-
mcnted (1-3), and various studies have cx-
amined exercise-dietary regimens to enhance
muscle glycogen stores before performance
(1, 3). None of these studies, however, has
examined the influence of the amount or type
of dietary carbohydrate consumed on glyco-
gen resynthesis during the 24 h after stren-
uous running. Therefore, the purpose of this
study was to determine the following: 1)
What effect does the form of carbohydrate
have on glycogen rcsynthcsis following exer-
cisc? 2) What effect does consuming different
quantities of carbohydrate have on muscle
gbycogen resynthesis during the 24 h after
strenuous exercise? 3) What effect does the
frequency of carbohydrate feedings have on
gbycogen resynthesis during the 24 h after
exercise? In addition, the effect of muscle
glycogen levels on muscle metabolism during
sprint and endurance activity was examined.
Answers to these questions will provide
guidelines for the management of the nutri-
tion of athletes who engage in daily strenuous
exercise.
Methods
Subjects
Six trained male runners participated in phase I of
this study, whereas four trained male runners partici-
pated in phase 2. The physical characteristics of both
groups of runners appear in Table I. The subjects con-
sumed the same diet (50% of calories derived from
carbohydrate) and performed the same activity (30 mm
running) the 2 days preceding each trial. The subjects
were fully informed of all risks associated with partici-
pation in this study before giving their written consent to
participate. A flow chart of the experimental protocol for
phase 1 and 2 appears in Figure 1.
Phase 1
To determine the effects of different forms of carbo-
hydrate on muscle glycogen resynthesis after strenuous
running, the subjects were fed isocaloric diets containing
either simple sugars (glucose, sucrose, fructose) or com-
plex carbohydrate (starches). The exercise consisted of a
16. 1 km run at 80% VO2 max immediately followed by
five 1-mm sprint runs (3 mm rest intervals) on the
treadmill at speeds requiring 130% V02 max. After this
exercise, the subjects consumed one of two randomly
assigned carbohydrate diets (two meals per 24 h) for the
next 48 h and were restricted from any vigorous activity.
During the first 24 h the subjects consumed 3700 kcal,
which was calculated to meet the day’s caloric expendi-
ture; similarly, during the second 24 h the subjects con-
sumed 2383 kcal. The carbohydrate, fat, and protein
content represented 70:20: 10% of the calories consumed,
respectively, and totaled 648 and 415 g of carbohydrate
for the 1st and 2nd days, respectively. The amount of
kcal consumed was calculated to meet only the subjects’
iFrom the Human Performance Laboratory, Ball
State University, Muncie, IN 47306.
2Supported by a grant from the National Dairy Coun-
cil (1979).
3Author to whom requests for reprints should be
addressed.
The American Journal ofClinical Nutrition 34: SEPTEMBER 1981, pp. 1831-1836. Printed in U.S.A.
©1981 American Society for Clinical Nutrition
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2383 keol
415 gco
( 24tw ) 4. biopsy
1832 COSTILL ET AL.
FIG. 1. Flow chart depicting the sequence ofdepletion and dietary intake for phase 1 and 2.
energy expenditure in order to elucidate differences in
glycogen resynthesis as a result of the two forms of
carbohydrate. We did not wish to examine the differen-
tial effect of the two forms of carbohydrate on supercom-
pensating muscle glycogen stores.
Muscle samples were obtained by percutaneous
needle biopsy from the gastrocnemius immediately after
and at 24 and 48 h after exercise. These samples, weigh-
ing 15 to 30 mg, were dissected into three samples,
weighed and frozen at -I 80#{176}C.The muscle sample
weights were corrected for evaporative water and ana-
lyzed for muscle glycogen according to the method of
Passonneau and Lauderdale (4). The average glycogen
value determined from the dissected samples was used
for statistical analysis and the standard error of duplicate
samples was ±1.5%.
Phase 2
The influence of the frequency of feedings and the
amount of carbohydrate consumed on glycogen resyn-
thesis during the 24 h after exercise was investigated
using the following dietary treatments (3000 kcal): 1) low
carbohydrate (CHO), 188 g CHO/day in two meals; 2)
mixed diet, 375 g CHO/day in two meals; 3) high
carbohydrate, 525 g CHO/day in seven feedings (high
-7): 4) high carbohydrate, 525 g CHO/day in two meals
(high -2). The exercise was that described earlier and
the order of the diets was randomized with at least one
week separating each trial. Since the subjects could
differentiate between high and low carbohydrate diets,
randomization of trials eliminates any systematic effect
on subsequent measurements due to the “nonblinded-
ness” of the diet.
Muscle biopsies were obtained from the gastrocne-
mius immediately after exercise and 24 h later. These
tissue samples were handled and analyzed for muscle
TABLE 1
Mean (±SD) characteristics of the subjects in phases I
and 2
Age Fit wt VOmax ST
Phase I
(n=6)
yr
24.5
(2.7)
cm
179
(7.4)
kg
71.8
(4.0)
mi/kg mEn
56.1
(3.1)
%
59.6
(11.0)
Phase 2
(n =4) 25.5
(4.4) 184
(6.1) 79.7
(6.8) 59.7
(4.6) 57.6
(3.7)
APeientage slow twitch fibers.
glycogen as previously described. In addition, the effect
of the glycogen levels (after the dietary treatments) on
300 m sprint performance was examined. Total time and
split times for 100 and 200 m were recorded, and 5mm
after the sprint a blood sample was obtained and ana-
lyzed for lactic acid (5). In addition, the subjects per-
formed a 30 mm treadmill run at 70% VO2 max 1 h after
the 300 m sprint. At 10-mm intervals samples of expired
gases were collected via the semiautomated gas collection
system described by Wilmore and Costill (6). From this
measurement the respiratory exchange ratio was calcu-
lated. Heart rate and perceived exertion (7) were also
taken at 10-mm intervals. Immediately after the run, a
blood sample was obtained and analyzed for lactic acid
(5).
Statistical analysis
Phase 1-mean values for all variables were tested for
significance using the Student’s ttest for paired obser-
vations (8). Phase 2-a one-way analysis of variance was
used to determine significant treatment effects. When a
significant F was observed, multiple range testing was
used to determine significant differences between treat-
ments (8). The level of probability was set at p <0.05.
Results
Phase 1
The strenuous running resulted in mean SE) mus-
dc glycogen of 53.4 ±7.5 and 56. 1 ±7. 1 mmol/kg wet
tissue before consuming the complex and simple carbo-
hydrate diets, respectively. Glycogen restoration during
the first 24 h period was similar for both the complex
and simple carbohydrate diets (Fig. 2). The next 24 h (24
to 48 h), however, resulted in a significantly greater
muscle glycogen storage (p <0.05) with the complex
carbohydrate diet (Fig. 2). The mean SE) change in
muscle glycogen during this period was 22.1 ±13.1 and
7.8 ±1 1.5 for the complex and simple carbohydrate
diets, respectively.
Phase 2
Mean (± SE) muscle glycogen content after the run-
ning exercise was 71.3 ±14.3, 49.3 ±9.4, 55.3 ±12.0,
and 46.8 ±9.4 mmol/kg wet tissue for the low, mixed
high 2 and high -7 carbohydrate diet trials, respectively.
There is no significant difference (p >0.05) between
these mean glycogen values. Twenty-four hours later,
muscle glycogen levels were 66.6 ±7.8, 74.2 ±3.9, 125.6
,-PHASE I
St
EXERCISE
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58Irnrnsprkits43O% J
PHASE 2
(‘.4)
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hiCHO -525 ‘ -
PIICHO -525 -7fe.nqs
300m stt
30mm irs,yiilrtji
(70%VO2mos)
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TIME AFTER EXERCISE (hr..)
FIT
CARBOHYDRATES AND GLYCOGEN STORAGE 1833
±10.9, and 101.2 ±20.9 mmol/kg wet tissue for the low,
mixed, high-2 and high-7 carbohydrate diet trials, re-
spectively. The change in muscle glycogen during the 24-
h feeding periods for each trial is depicted in Figure 3.
The low carbohydrate diet resulted in a significant re-
duction (p <0.05) of muscle glycogen while the high-2
carbohydrate diet resulted in a significant gain (p <0.05)
in muscle glycogen when compared to the mixed diet
trial. The different initial muscle glycogen levels had no
effect on either the 300 m sprint performance or the 100
and 200 m splits. In addition, there was no significant
difference (p >0.05) in lactate levels measured 5 mm
after each sprint (Table 2).
During the treadmill performance runs there was no
FIG. 2. Muscle glycogen levels (means ±SE) after
exhaustive exercise with diets composed of 70% simple
(i.e., glucose, fructose and sucrose) and complex (i.e.,
starch) CHO.
TABLE 2
significant difference (p >0.05) in either the calculated
oxygen uptake and total caloric cost or the measured
heart rate and blood lactate accumulation between the
trials (Table 2). The calculated oxidation of carbohydrate
and fat, however, was affected by the diets. After the low
carbohydrate diet the respiratory exchange ratio was
lower (p <0.05) and the grams of fat combusted were
higher (p <0.05) than the respiratory exchange ratio and
the grams of fat combusted after the mixed diet. On the
other hand, the high-7 diet resulted in a higher (p <0.5)
respiratory exchange ratio and larger (p <0.05) gram
carbohydrate oxidation than did the mixed diet trial
(Table 2).
80
70
60
50
40
30
z
‘Ii
0
0
N
In.
z  20
! 0
25% 50% 70% 70%
CHO DIETS (% of coloriss)
FIG. 3. Effects of varied CHO diets on the restorage
of muscle glycogen. Asterisk denotes a significant differ-
ence between that mean and the mean change in muscle
glycogen observed during the mixed diet (50% of cal
from CHO).
Mean SE) data obtaine d during the 300 m and 30 mm treadmill runs after each of the diets*
LowCHO Mixed HighCHO
(2 meals) I-ImghCHO
(7 meals)
300m(s) 47.8
(2.1)
48.1
(2.2)
47.8
(1.7)
47.5
(1.8)
HLa(mM) 9.6
(0.6) 9.1
(0.4) 9.0
(0.6) 8.6
(0.5)
V02 3.39
(0.17) 3.25
(0.18) 3.37
(0.14) 3.39
(0.37)
R (VCO2/V02) 0.8Olt
(0.006) 0.843
(0.007) 0.844
(0.01 1) 0.873t
(0.002)
HR(beats/min) 154
(1.6) 156
(2.3) 155
(2.0) 156
(1.4)
PE l0.6t
(0.6) 9.7
(0.5) 8.6t
(0.6) 9.3
(0.6)
HLa(mM) 1.8
(0.1) 1.3
(0.1) 1.6
(0.1) 1.5
(0.1)
C oxygen consumption; R, respiratory exchange ratio; HR. heart rate: PE, perceived exertion (Borg scale):
HLa, blood lactate.
tDenotes significant difference (p <0.05) between identified mean and the “mixed” (50% CHO) diet.
:1:Denotes significant difference (p <0.05) between identified mean and the high CHO (two meals) diet.
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1834 COSTILL ET AL.
Discussion
Phase 1 examined the effect of the type of
dietary carbohydrate on muscle glycogen re-
synthesis during the 48-h period after stren-
uous running. The type of carbohydrate, sim-
plc or complex, had no differential effect on
the change in muscle glycogen during the
first 24 h after exercise. Reasons for the sig-
nificantly (p <0.05) larger change in muscle
glycogen, and higher bevels of muscle glyco-
gen after the complex carbohydrate diet dur-
ing the second 24 h, is presently unknown
and might be explained by other factors.
The different responses in insulin and glu-
cose as a result of the complex and simple
carbohydrate diets has been reported by other
investigators (1 1,1 2). Hodges and Krehb (1 1)
demonstrated that the insulin levels after a
starch feeding were lower but remained dc-
vated longer when compared to an equivalent
g/g glucose meal. In addition, the activation
of gbycogcn synthetase by insulin is well doc-
umented (13). Therefore, it is possible that
maintained elevation of serum insulin occur-
ring as a result of the complex carbohydrate
diet is responsible for the enhanced muscle
glycogen storage during the second 24-h pe-
riod.
The strenuous bout of running exercise was
sufficient to reduce muscle glycogen levels to
an average of 55 mmol/kg wet tissue. This
represents about 1 g/lOO g ofmuscbc glycogen
and is slightly higher than the bevels of muscle
glycogen reported following cycling to cx-
haustion (1, 9). The recruitment pattern of
muscle fibers as determined by periodic acid-
Schiff staining has shown gbycogen-filled fast
twitch fibers after 2 h of running at 80% V02
max (10). Thus, the glycogen remaining in
the muscle sample in nonrecruited fibers fol-
lowing the strenuous bout of running might
account for these slightly higher muscle gly-
cogen levels.
As was anticipated, increasing amounts of
carbohydrate 24 h after reduction of muscle
glycogen resulted in increasing amounts of
glycogen stored in the gastrocnemius (Fig. 3).
This relationship was found to be significant
r=0.84, (p <0.05) when data from phase 1
(first 24-h period) and phase 2 were com-
bined. It is obvious that a platcauing of the
change in muscle gbycogcn/24 h was not dem-
onstrated up to 648 g CHO/day and that
larger carbohydrate meals might maximize
muscle glycogen storage during the 24 h after
strenuous running. Indeed, Bbom et al. (14)
reported that maximal glycogen storage was
attained when exercise-exhausted subjects
(cycling) consumed between 1.4 to 2.0 g glu-
cose/kg body weight every 2 h. They did not
report muscle gbycogcn levels, but this
amounts to 588 to 840 g CHO/day ifa subject
weighed 70 kg and consumed glucose for 12
h. O’Dea and Pubs (15) demonstrated that
nibbling-fed rats incorporated more labeled
glucose into glycogen and had higher muscle
glycogen levels than meal-fed rats. This sug-
gests that carbohydrate ingested at intervals
after exercise might result in a greater glyco-
gen storage than carbohydrate consumed in
only two meals and indicates that an optimal
glucose load might exist for gbycogcn synthe-
sis during recovery from exercise. This, how-
ever, did not occur since the change in muscle
glycogcn during the high-7 trial was not sig-
nificantly different (p >0.05) from the mixed
diet trial.
Bergstrom and Hubtman (9) and Kochan
et al. (16) reported normal muscle glycogen
bevels 24 h after exhaustive cycling exercise.
Therefore, consistent with previous findings,
both phase one (glucose and starch) and
phase two (high-2) normalized muscle gby-
cogen levels in 24 h. This is based on the fact
that depletion levels averaged 55 mmob/kg
wet tissue and the subsequent change in mus-
dc glycogen was 81 and 70 mmol/kg wet
tissue for the two diets, respectively. This
would bring muscle glycogen levels to ap-
proximately 130 mmol/kg wet tissue, which
is normal for rested, well-trained runners (17,
18). Thus, it appears that consuming between
525 to 648 g of carbohydrate during the 24 h
after strenuous running will result in normal
muscle glycogen bevels.
Although muscle gbycogen storage is
known to play a critical role in activities
lasting longer than 1 h (19), its significance in
short term highly anaerobic exercise has not
been examined during running. Anaerobic
metabolism predominates as the energy pro-
ducing system in events of high intensity
lasting 0.75 to 3.0 mm (20), and muscle gly-
cogen is the substrate oxidized during such
an exercise bout. Studies have demonstrated
higher blood lactate levels during submaxi-
mab workboads when muscle glycogen was
elevated as compared to lower bevels of mus-
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CARBOHYDRATES AND GLYCOGEN STORAGE 1835
dc gbycogen (2 1,22). Therefore, higher levels
of muscle glycogen preceding anaerobic ac-
tivity might result in impaired performance
resulting from enhanced lactate production.
Table 3 illustrates that the mean performance
time and blood lactate concentrations were
not significantly different between any of the
trials. Differences in initial muscle glycogen
levels, therefore, had no effect on flux
through the anaerobic energy producing sys-
tems which might impair performance.
The influence of dietary carbohydrate dur-
ing exercise was first reported by Christensen
and Hansen in 1939 (23). Although the mech-
anisms regulating a substrate shift with high
and low carbohydrate diets have not been
fully explained, the current data suggest that
the amount of time between the final carbo-
hydrate meal and the onset of exercise may
have some bearing on the use of carbohydrate
by muscle. This is supported by the fact that,
although muscle gbycogcn was elevated after
both high carbohydrate diets (two meals and
seven feedings), only the seven feeding regi-
men produced an increase in carbohydrate
oxidation during exercise. When the carbo-
hydrate was taken in only two meals, nearly
15 h had elapsed between the second feeding
and the 30-mm treadmill run. In the seven
feeding regimen, however, the final meal was
consumed only 8 h before the exercise. Since
carbohydrate availability, as measured by
glucose levels (D. L. Costill, W. M. Sherman,
W. J. Fink, C. Maresh, M. Witten, and J. M.
Miller, unpublished data) and muscle glyco-
gen content did not differ between the trials,
the enhanced rate of carbohydrate oxidation
may be related to a greater insulin sensitivity
and/or activity after the seven feedings trial.
This concept is supported by studies with
juvejile diabetic runners who show normal
muscle glycogen use, increased glucose up-
take and an accelerated rate of carbohydrate
oxidation when insulin is administered 3 h
before exercise (24). When deprived of insu-
lin for 24 h these men oxidized the same
amount of muscle glycogen but experienced
a marked reduction in glucose uptake and
total carbohydrate metabolism during exer-
cisc. U
The authors would like to thank Pete Watson and
Rick Sharp who assisted in the data collection and the
subjects for their cooperation during the study.
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... In this study, participants recover their muscle glycogen content by consuming typical Japanese meals, rather than sports foods. Costill et al. [31] reported that the carbohydrate sources for their study were sugar, starch, and drinks, whereas Burke et al. [10] used cornflakes, whole wheat bread, instant mashed potato, and Polycose ® as test dishes. On the other hand, rice, pasta, bread, and fruits were used as carbohydrate sources in this study. ...
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... However, in endurance athletes' habitual eating practices, postexercise CHO intake often remains inadequate (Burke et al., 2003;Heikura et al., 2019;Keay et al., 2018); therefore, optimizing recovery meal composition may help to improve glycogen replenishment. Although dietary CHO provides the major source for glycogen resynthesis (Blom et al., 1987;Costill et al., 1981), addition of protein to the postexercise recovery meal has been shown to augment short-term glycogen replenishment when CHO intake is inadequate (Ivy et al., 2002;van Loon et al., 2000). Protein may augment glycogen restoration by stimulating glucose uptake through enhanced membrane permeability both via insulin-dependent (Hirshman et al., 1990;Ivy & Kuo, 1998) and insulin-independent (Nishitani et al., 2002) mechanisms. ...
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... This may be of greater importance for bodybuilders who are aiming to refill glycogen stores in a short time window (e.g. after making weight), as high glycemic carbohydrates have demonstrated superior glycogen resynthesis rates [122]. However, over a longer timeframe (i.e. 8 + hours), glycogen stores can be replenished similarly, regardless of feeding frequency [124], when consuming an adequate total amount of carbohydrates [125]. Additionally, data have demonstrated that combining protein with carbohydrates can enhance glycogen resynthesis [126]. ...
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