Carbohydrate feedings 1 h before improves cycling performance13 William
M Sherman,
ABSTRACT
amounts abolic
M Christine
The
of liquid responses
effects
of
carbohydrate during
Peden, consuming
1 h before
exercise
and David
and
on
two
exercise exercise
exercise
A Wright
different
on the metperformance
were determined. Subjects consumed either 1 1 g (LC) or 2.2 g (HC) carbohydrate/kg body mass or a placebo (P). Subjects cycled at 70% of maximal oxygen consumption (VO2max) for 90 .
mm and then
underwent responses during
insulin
a performance exercise were
trials. Total carbohydrate hydrate trials compared nificantly
improved
concentrations
an initial and erately
drop
2.2 g liquid intense
LC
start
in blood
and
prolonged
KEY WORDS bohydrate oxidation,
HC.
of and
elevated
exercise,
consumption body
exercise carbohydrate
Exhaustion, preexercise
Despite
during
glucose,
carbohydrate/kg
presumably via enhanced Nutr 199 1 ;54:866-70.
Blood glucose and among the three
oxidation was greater for the carbowith P. Time-trial performance was sig-
by
at the
trial. different
mass can
despite
of between 60 mm
improve oxidation.
exertion, feeding
insulin
and
blood
before
1.1 mod-
performance,
Am J Clin
glucose,
car-
performance was improved 15% when moderately trained recreational cyclists consumed 4.5 g carbohydrate/kg body mass 4 h before exercise. The fact that the present study used highly trained cyclists and a cycling time-trial athletic competition was important. Early studies by Costill et al (1 3) and
Athletes often train and compete after an overnight fast and consume less-than-optimal quantities of dietary carbohydrate (1). This may cause body carbohydrate reserves (liver and muscle glycogen) to be less than normal during exercise performance. Because fatigue occurs during many types ofexercise when blood glucose or muscle glycogen is lowered ( 1 , 2), maintaining or elevating body carbohydrate reserves may optimize exercise performance. Although not always advocated, preexercise carbohydrate feedings have the potential to increase liver (3, 4) and muscle glycogen (5) concentrations during the hours before exercise. Further, preexercise carbohydrate feedings may be absorbed via the small intestine during exercise and help maintain blood glucose concentrations (6). Although some studies found no positive effects (7-9), several studies reported ergogenic effects of preexercise carbohydrate feedings on exercise performance (6, 10-12). Two ofthe positive studies used time to fatigue at a fixed exercise intensity as the performance criterion (1 1, 12). This performance task, however, is unlike athletic competition, which requires the athlete to vary
the exercise intensity and to traverse a given distance as fast as possible. Only Sherman et al (6) used a performance task, 95 mm ofintermittent cycling followed by a time-trial performance, that simulated competition. Compared with placebo, time-trial 866
Am J C/in Nuir
l99l;S4:866-70.
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
to simulate
Foster et al (14) suggested that preexercise carbohydrate feedings might impair exercise performance by causing a sudden drop in blood glucose and an accompanying acceleration of muscle glycogenolysis and glucose oxidation. The accelerated carbohydrate oxidation was thought to be the result ofelevated insulin concentrations at the start of and during exercise. Because different amounts of ingested carbohydrate elicit different insulin responses both at rest and during exercise, it is important to examine the effects ofingesting varying amounts of preexercise carbohydrate feedings on exercise performance.
In a study
by Gleeson
et al (1 1), subjects
improved
endurance time to exhaustion by 13% when 1.0 g carbohydrate! kg body mass was consumed 60 mm before exercise, despite significantly elevated insulin concentrations at the start of cxercise and a drop in blood glucose early in exercise. It is conceivable,
Introduction
performance
however,
that
a greater
insulin
response
from
will result
consuming > 75 g carbohydrate 1 h before exercise and that this would accelerate muscle glycogenolysis and glucose oxidation and impair exercise performance. On the other hand, if the preexercise carbohydrate feeding continues to empty from the gut and be absorbed by the small intestine during exercise, performance may be either unaffected or further improved. The present study used highly trained cyclists to determine whether ingesting 1.1 g liquid carbohydrate/kg body mass (LC) 1 h before
exercise
performance additional
would
when purpose
result
compared was
in improved
with
to determine
response
resulting from consuming (HC) in a preexercise feeding
mass
ingesting
cycling
time-trial
a placebo
whether
the
larger
2.2 g carbohydrate/kg would further affect
(P). An insulin body
perfor-
mance. Methods Subjects Nine jects
unpaid
were
active
male
volunteers
college-aged
completed students
the who
could
study. cycle
The
sub-
contin-
I From the Exercise Physiology Laboratory, School ofHealth, Physical Education, and Recreation, The Ohio State University, Columbus, OH. 2 Supported in part by Ross Laboratories, Columbus, OH.
Reprints Received Accepted 3
Printed
not available. February 1 1 , 1991. for publication April in USA.
24, 1991.
© 1991 American
Society
for Ginical
Nutrition
PREEXERCISE uously
for
(VO2max).
90
mm
at
70%
of maximal
oxygen
CARBOHYDRATE Exercise
consumption
The physical
and physiological characteristics of the subjects were as follows (i ± SE): age 24 ± 1 y, height 170 ± 1 cm,weight7l ± 2 kg,%bodyfat 12 ± 1,andVO2max4.l ± 0.2 L/min. This study was reviewed and approved by the University’s Biomedical Sciences Review Committee and the subjects voluntarily provided written informed consent. Cont rol period
workboads,
and
the criteria
for VO2max
included
contained
45%,
35%,
and
fat, and protein, respectively, caffeinated beverages.
20%
and
ofenergy
did
not
ratings
every
alcohol
45 mm
or
Each
four trials in the fasted state (10 h) each trial. After completing a familiarization trial to ensure that the subject could complete the exercise tasks, the subjects were randomly assigned to the three experimental trials by using a counterbalanced, double-blind design. The experimental trials required the subjects to consume a placebo or one oftwo carbohydrate solutions 60 mm before exercise. The placebo was a nonnutritive solution whereas LC provided 1.1 g carbohydrate/kg body mass and HC provided 2.2 g carbohydrate/kg body mass. with
7-10
subject
completed
d separating
Subjects ercise.
.
L. The average
chain
length
ofthe
maltodextrins
was 6 glucosyl
24.0
Blood
sampling
and
were
served
from
were obtained before after the feeding.
an
opaque
the feeding
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
were
phase
as quickly
as possible.
during
another,
cadence
and
which
would
time
a
result
variables
immediately
to time
the subtherefore
trial.
and
were
before During
were
com-
the
time
vigorously
ver-
1 50 mL water every fan cooled during
also
conditions
(1 ± SE)
during
± 0.6 torr,
and
± 1.4%
environmental to 38.5
62.0
and
#{176}C after
exercise
60 mm
1S ex-
exercise relative
conditions,
of exercise
and
( 12).
and analysis
8 mL
blood
nontoxic
was
obtained
iv catheter
at each
(B & D Inc,
sampling
time
Rutherford,
NJ)
via that
was inserted into an antecubital vein. A 0.5-mL sample of blood was deproteinized with 1.5 mL cold 8% perchloric acid and centrifuged
at
1700
X g for 30 mm
at 4 #{176}C. The
for lactic acid (21). The remaining
analyzed on ice,
and
serum
was
recovered
supernatant
blood
was
was coagulated
by centrifugation
at 1 700
X
g
for 30 mm at 4 #{176}C. Serum samples were stored in separate tubes for subsequent analysis ofglucose (22), free fatty acids (20, 23), and insulin (ICN Biomedical, RSL, Carson, CA). To reduce variability, blood samples from all three trials for each subject were run in duplicate within the same analysis. The intraassay variability was 1.2%, 2.4%, 3.7%, and 3.2% for glucose, insulin,
lactic
acid,
variability lactic
Inspired (Rayfield,
and
free
fatty
3.5%,
and
fatty
free
ofrespiralory volumes Waitsfield,
spirometer
(Warren
pired
were
gases
acids,
was 4.2%, acid,
Measurement
5.1%, acids,
respectively.
and
The
5.7%
inter-
for glucose,
respectively.
gases
were measured by using a dry-gas meter VT) that was calibrated by using a Tissot E Collins,
Inc,
continuously
Braintree,
sampled
and
MA).
Mixed
analyzed
ex-
for oxygen
(model 5A3, Applied Electrochemistry, Pittsburgh) and carbon dioxide (LB-2, Beckman, Fullerton, CA). Electrical signals from these instruments were directed into an A/D converter and into a computer for calculation of oxygen consumption (i’O2) and
RER.
These
Statistical
color
these
temperature rises remains constant
in taste,
and
#{176}C, 745.9
Under
dation.
texture,
for the
blinded
environmental ± 0.2
humidity.
units. The volume of the preexercise feeding was adjusted relative to body weight to provide the required amount of carbohydrate. The average (±SE) volume of the preexercise feedings was 391 ± 12 mL. All three solutions were made as similar as possible water bottle. Blood samples and 15, 30, 45, and 60 mm
distance were
samples
the metabolic
Physiological and
were required to consume exercise. Subjects were
The
were
insulin,
The carbohydrate solutions were formulated to deliver the two amounts of carbohydrate to the blood within similar time intervals (18). Carbohydrate solutions > 20% (wt:vol) have similar rates of gastric emptying (19). Therefore, LC and HC were chosen to be 20% and 40%, respectively. Because osmolarity also affects gastric emptying (20), the osmolarity for the two beverages was equated by varying the relative amounts of glucose and maltodextrins for LC and HC. Both solutions had the same molar concentration (I 1 mol/L); LC contained 200 g glucose/ L and HC contained 160 g glucose/L and 240 g maltodextrins/
time.
rate,
time trial requiring equivalent to an-
VO2max,
distance
70%
heart
encouraged.
assay
Preexerciseftedings
VO2max
and percent
required
subjects
mm during
core then
blood
After
a higher
performance
the the
bally
to maintain
at
RER,
and
one trial than
at one-halfthe
pleting trial
at 70%
during
output
Roughly
design
of cycling
a shorter
measured
(RPE),
exercise.
carbo-
continuously
a cycling-performance the number of revolutions
have
a sterile,
Experimental
exertion
better
power
of the preexercise
cycled
consumption,
15 mm during
subjects undertook them to complete
would
effects
subjects
Oxygen
of perceived
obtained
in
as carbohydrate,
contain
the
for 90 mm.
VO2max
higher a
the metabolic
feedings,
To perform
leveling offofVO2 with increasing workloads and a respiratoryexchange ratio (RER) > 1.0. Body density was determined by the underwater-weighing procedure (1 5). Percent body fat and lean body mass were calculated according to the equation of Siri (16). Exercise and diet were controlled during the 2 d before each experimental trial in an attempt to equate body carbohydrate reserves among trials ( 17). Exercise was restricted to cycling in the laboratory at 70% VO2max for 40 and 20 mm, respectively, for the 2-d control period. The diet (12.6 MJ) during the control period
To determine
ject
867
protocol
hydrate
other
The physiological characteristics of the subjects were determined within 7 d of the first experimental trial. Calibrated Schwinn Bio-Dyne cycle ergometers (Excelsior Fitness Inc, Chicago) were used for all trials. VO2max was determined by using incremental
FEEDINGS
tified
variables
were
The gas analyzers by the
(Gaithersburg,
National
MD)
used
to estimate
were calibrated Institute
and
carbohydrate
against
of Standards
previously
analyzed
a tank and
oxi-
gas cer-
Technology
by
chemical
methods.
analysis
Standard procedures SEs for the dependent
were used to calculate variables. Areas under
the means the glucose-
and and
868
SHERMAN 6
ET
AL
exercise. During was not different
-J
E E
glucose
was
ercise
compared
response
significantly
curves
± 12, and
w
431
spectively).
U) 0 04
the remaining 60 mm ofexercise, blood between LC and P. For HC, however,
higher
higher
with
both
were
similar
after
LC and
among
± 10 mmol-min
During
the
60,
trials
for the carbohydrate
for
blood
trials
90 mm
under
the trials -L’
time
75, and
P. Areas
of ex-
the glucose-
(406
P, LC,
± 12, 384 and
glucose
compared
glucose blood
HC,
tended
with
re-
to be
P. At the end
-J
of the
ci
0
than
time
trial,
Compared
s-s
PLACEBO 75 g CHO
-A
15OgCHO
0-0
glucose
for HC
was
significantly
greater
for P.
(P
525% 500
blood
0.05). All subjects completed the time trials faster after consuming the preexercise carbohydrate feeding. Time-trial performance was significantly improved by an average 12.5% for the carbohydrate-feeding trials (Fig 3). Power output during the time trials averaged 13. 1% higher for the carbohydrate-feeding trials comtotal
pared
with
P. Similarly,
with P, the percent and LC, respectively.
at completion
VO2max
was
ofthe
time
17% and
trial
compared
1 1% higher
for HC
130
TiME
As liver
An important finding ofthis study is that exercise performance was improved 12.5% when cyclists consumed 1.1 g carbohydrate/ kg body mass (75 g) 60 mm before 90 mm ofsubmaximal cycling followed by an intense time-trial performance. Note that exercise performance
was
neither
further
preexercise
2.2 g carbohydrate/kg
improved
carbohydrate body
mass
nor
feeding
impaired
when
was increased
(1 50 g). After
90 mm
to
of con-
tinuous cycling at 70% VO2max, subjects were requested to complete as fast as possible the number of revolutions equivalent to an additional 45 mm of cycling at 70% VO2max. Subjects maintained
84%
VO2max
during
the
time
trial
for LC and
HC
compared with 68% VO2max during the time trial for P. A similar improvement in cycling time-trial performance was observed by Sherman et al (6). Their moderately trained subjects consumed either 0, 45, 156, or 312 g carbohydrate 4 h before intermittent cycling for 95 mm followed by a time trial identical to that used in the present study. When 3 12 g carbohydrate was consumed,
using time Gleeson
time-trial
performance
was improved
15%.
Similarly,
to fatigue during steady-state exercise as the criterion, et al (11) and Wright et al (12) observed a 13% and
18% improvement
in time
to fatigue,
respectively,
when
either
1 g carbohydrate/kg body mass or 5 g carbohydrate/kg body mass was consumed either 1 or 3 h before exercise, respectively. Although three studies reported no significant effects of preexercise
carbohydrate
feedings
on performance
(7-9),
the
studies
et al (11), Neuffer et al (10), Sherman et al (6), Wright et al (12), and the present study support the principle that preexercise carbohydrate feedings improve cycling performance. ofGleeson
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
90
DURING
(mm)
EXERCISE
FIG 3. Heart-rate responses during exercise for the three experimental trials, and performance times for the time-trial performances for the three experimental trials. For this test, a shorter performance time means improved performance.
Discussion
the 60-mm
60
120
and
the perception be stopped
Blood
muscle
glucose
and
P, indicating production
glycogen
become
depleted
RER
gradually
that availability was gradually
exercise
during
trations
and
diminishing.
P totally because
declined
later
amounts; stages
servation
Because
diminished
thus,
that
when
performance
there
was
This
possibility
blood
it is unlikely
carbohydrate
body
the time-trial
of exercise.
feedings during late in exercise, the
exercise,
during exercise for to support energy
ofcarbohydrate
durance test to exhaustion, it is likely that bohydrate feedings increased carbohydrate normal
during
of effort increases and ultimately exercise has to or the intensity of exercise significantly reduced.
glucose
a higher
that
concennot
an en-
the preexercise oxidation
was
carabove
work
rate
is supported
is maintained
during
the
by the
ob-
by carbohydrate
exercise, blood glucose is oxidized at high even when muscle glycogen concentrations
rate of glycogenolysis Although it is possible
are low that the
rates and
(2, 24-26).
preexercise feeding stimulated the 1 h before exercise (3-5), it is unlikely that the small amount ofglycogen that was synthesized accounted for the significant improvements in time-trial performance resulting from the preexercise carbohydrate feedings. Further, muscle
other
glycogen
studies
synthesis
report
similar
exercise
after a preexercise
is more
likely
carbohydrate
that
during
rates
of muscle
carbohydrate improved performance
availability
during
exercise.
oxidation averaged 12% higher for the feeding trials compared with P. Increased
glycogenolysis
during
meal (5, 8, 9). Rather, it was related to greater
The rate of carbohydrate preexercise
carbohydrate-
carbohydrate availability may have been the result of the effects of liver glycogen synthesis during the hour after the preexercise feeding resulting in increased hepatic
glucose
production
(27).
However,
increased
carbohydrate
870
SHERMAN
availability is most likely the of the preexercise carbohydrate mated
absorption
rate
al (28)
were
suggest
used,
and
60%
of HC
fact
that
the
treatments although
blood blood
of LC and that
were
absorbed. insulin
significantly glucose
HC, This
the results
during
from
different
for
emptying The estiof Hunt
et
of exercise, 100% of LC finding is supported by the
responses
exercise
for
other.
each
the
Further,
similar
to P after
30 mm
30 mm
ofexercise
was signif-
LC was
for HC after
glucose
when
gastric exercise.
by 60 mm
integrated were
exercise,
result of continued feeding during
of
than blood glucose for IC and P. Apparently, for continued to empty from the gut during exercise and was absorbed at a rate that exceeded whole-body glucose disposal. The observations of rapid declines in blood glucose early in icantly
higher
HC, glucose
exercise
and
cogenolysis
increased during
carbohydrate
exercise
after
to support not be consumed during have
been
results
Sherman
present
study
and
those
et al (6) demonstrate
insulin
concentrations
initial
a preexercise
roughly
15 mm
at the
1 mmol/L
of exercise,
that
drop
and
exercise
in blood
performance.
preexercise
glucose
(29).
The
combination
at the start
effects
of exercise
ofthe
is probably
effects
an first
feedings
ofinsulin
on muscle
on glucose
contraction responsible
and the
improve become fatigued the RPE did not exercise intensity lowering of blood
carbohydrate
ofmuscle
elevated
during
Although
and the insulin-like
(1 3, 14). The et al (1 1) and
exercise,
glucose
glyfeeding
significantly
during
some individuals during exercise when blood glucose is lowered, increase and subjects continued the required and were apparently insensitive to the transient cycling
muscle carbohydrates
of Gleeson
that despite start
and carbohydrate
the recommendation the hours before
used
of the
oxidation
for the
uptake
initial
drop
in blood glucose (30). Subsequently, blood glucose is maintained by increased splanchnic glucose output or reduced stimulation of glucose uptake by insulin and contraction. It is probable that if insulin
were
elevated
independent
of
increased
carbohydrate
performance would be impaired. Regardless of the factors regulating the blood glucose and insulin responses during exercise after preexercise carbohydrate feedings, consuming I 1-2.2 g carbohydrate/kg body mass 1 h before cycling exercise and time-trial performance significantly improves exercise availability,
exercise
.
capacity. We thank Jeff Betts, Art Dernbach, Leo D’Aquisto, and Lynda Peel for their various contributions to this study. We also thank the subjects for their cooperation during the study.
References 1. Sherman WM, Lamb DR. Nutrition and prolonged exercise. In: Lamb DR. Murray RM, eds. Perspectives in exercise science and sports medicine. Indianapolis: Benchmark, 1988:213-80. 2. Coyle EF, Coggan AR. Effectiveness ofcathohydrate feeding in delaying fatigue during prolonged exercise. Sports Med l984;l:446-58. 3. Nilsson LH, Hultman E. Liver glycogen in man-the effect of total starvation or a carbohydrate-poor diet followed by carbohydrate refeeding. Scand J Clin Lab Invest l973;32:325-30. 4. Maehlum 5, Felig P, Wahren J. Splanchnic glucose and muscle glycogen metabolism after glucose feeding during postexercise recovery. Am J Physiol l978;235:E255-60. 5. Coyle EF, Coggan AR, Hemmert MK, Lowe RC, Walters TJ. Substrate usage during prolonged exercise following a preexercise meal. J Appl Physiol l985;S9:429-33. 6. Sherman WM, Brodowicz G, Wright DA, Allen WK, Simonsen JC, Dernbach A. Effects of 4 h preexercise carbohydrate feedings on cycling performance. Med Sci Sports Exerc l989;2l:S98-604.
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
ET
AL
7. Devlin IF, Calles-Escandon J, Horton ES. Effects ofpre.exercise snack feeding on endurance cycling exercise. J Appl Physiol 1986;6&.980-5. 8. Hargreaves M, Costill DL, Fink WJ, King DS, Fielding PA. Effect of pre-exercise carbohydrate feedings on endurance cycling performance. Med Sci Sports Exerc 1987;19:33-6. 9. Koivisto V, Karonen S-L, Nikkila EO. Carbohydrate ingestion before exercise: comparison ofglucose, fructose, and sweet placebo. J Appl Physiol 198l;51:783-7. 10. Neuffer PD, Costill DL, Flynn MG, Kirwan JP, Mitchell JB, Houmard J. Improvements in exercise performance: effects of carbohydrate feedings and diet. J AppI Physiol 1987;62:983-8. 1 1. Gleeson M, Maughan Ri, GreenhaffPL. Comparison ofthe effects ofpre-exercise feeding ofglucose, glycerol and placebo on endurance
and fuel homeostasis
in man. Eur J Appl Physiol
l986;55:646-53.
12. Wright DA, Sherman WM, Dernbach AR. Carbohydrate feedings before, during, and in combination improves cycling performance. J Appl Physiol (in press). 13. Costill DL, Coyle EF, Dalsky G, Evans W, Fink W, Hoopes D. Effects ofelevated plasma FFA and insulin on muscle glycogen usage during exercise. J Appl Physiol l977;43:69S-9. 14. Foster C, Costill DL, Fink WJ. Effects of preexercise feedings on endurance performance. Med Sci Sports Exerc l979;ll:l-5. 15. McArdle WD, Katch FI, Katch VL EXereiSepIIysiO1Og eneray, nutrition and performance. Malvern, PA: Lea & Febiger, 1981:95-104. 16. Sin WE. Body composition from fluid spaces and density analysis of methods. In: Brozek J, Heusen A, eds. Techniques for measuring body composition. Washington, DC: National Academy Press, 1961:212-6. 17. Sherman WM, Costill DL, Fink WJ, Miller JM. Effect of exercisediet manipulation on muscle glycogen and its subsequent utilization during performance. Int J Sports Med 198 l;2: 114-8. 18. Murray R. The effects of consuming carbohydrate-electrolyte beverages on gastric emptying and fluid absorption during and following exercise. Sports Med 1987;4:322-51. 19. Brener W, Hendrix T, McHugh P. Regulation of gastric emptying ofglucose. Gastroenterology 1983;85:76-82. 20. Duncombe W. The colorimetric micro-determination of non-esterified fatty acids in plasma. Gin Clam Acts l964;9:l22-S. 21. Gutman I, Wahlefeld AW. L4+)-lactate. Determination with lactate dehydrogenase and NAD. In: Bergmeyer HU, ed. Methods of enzymatic analysis. 2nd ed. New Yoric Academic Press, 1974:1464-8. 22. Cooper GR, McDaniel V. The determination ofglucose by the orthotoluidine method (filtrate and direct procedure). In: MacDonald RP, ed. Standard methods in clinical chemistry. New York: Academic Press, 1970:159-70. 23. Noma A, Okabe H, Kita M. A new colorimetric micro.determination of free fatty acids in plasma. Clin Clam Acts 1973;43:317-20. 24. Coggan AR, Coyle EF. Reversal of fatigue during prolonged exercise by carbohydrate infusion or ingestion. J Appl Physiol l987;63:238895. 25. Coggan AR, Coyle EF. Effect ofcarbohydrate feedings during high. intensity exercise. J AppI Physiol l985;65: I 703-9. 26. Coyle EF, Coggan AR, Hemmert MK, Ivy JL. Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J Appl Physiol 1986;6 1:16S-72. 27. Vissing J, Wallace JL, Galbo H. Effect ofliver glycogen content on glucose production in running rats. J Appl Physiol 1989;66:318-22. 28. Hunt JN, Smith JL, Jiang CL. Effect of meal volume and energy density on the gastric emptying ofcarbohydrates. Gastroenterobogy 1985;89: 1326-30. 29. Coyle EF, HagbergJM, Hurley BF, Martin WH, Ehsani AA, Holloszy
JO. Carbohydrate
feeding during
prolonged
strenuous
exercise can
delay fatigue. J Appl Physiol l983;S5:230-5. 30. DeFronzo RA, Ferrannini E, Sato Y, Felig P, Wahren J. Synergistic interaction between exercise and insulin on peripheral glucose uptake. J Clin Invest l98l;68:l468-74.
M Sherman,
ABSTRACT
amounts abolic
M Christine
The
of liquid responses
effects
of
carbohydrate during
Peden, consuming
1 h before
exercise
and David
and
on
two
exercise exercise
exercise
A Wright
different
on the metperformance
were determined. Subjects consumed either 1 1 g (LC) or 2.2 g (HC) carbohydrate/kg body mass or a placebo (P). Subjects cycled at 70% of maximal oxygen consumption (VO2max) for 90 .
mm and then
underwent responses during
insulin
a performance exercise were
trials. Total carbohydrate hydrate trials compared nificantly
improved
concentrations
an initial and erately
drop
2.2 g liquid intense
LC
start
in blood
and
prolonged
KEY WORDS bohydrate oxidation,
HC.
of and
elevated
exercise,
consumption body
exercise carbohydrate
Exhaustion, preexercise
Despite
during
glucose,
carbohydrate/kg
presumably via enhanced Nutr 199 1 ;54:866-70.
Blood glucose and among the three
oxidation was greater for the carbowith P. Time-trial performance was sig-
by
at the
trial. different
mass can
despite
of between 60 mm
improve oxidation.
exertion, feeding
insulin
and
blood
before
1.1 mod-
performance,
Am J Clin
glucose,
car-
performance was improved 15% when moderately trained recreational cyclists consumed 4.5 g carbohydrate/kg body mass 4 h before exercise. The fact that the present study used highly trained cyclists and a cycling time-trial athletic competition was important. Early studies by Costill et al (1 3) and
Athletes often train and compete after an overnight fast and consume less-than-optimal quantities of dietary carbohydrate (1). This may cause body carbohydrate reserves (liver and muscle glycogen) to be less than normal during exercise performance. Because fatigue occurs during many types ofexercise when blood glucose or muscle glycogen is lowered ( 1 , 2), maintaining or elevating body carbohydrate reserves may optimize exercise performance. Although not always advocated, preexercise carbohydrate feedings have the potential to increase liver (3, 4) and muscle glycogen (5) concentrations during the hours before exercise. Further, preexercise carbohydrate feedings may be absorbed via the small intestine during exercise and help maintain blood glucose concentrations (6). Although some studies found no positive effects (7-9), several studies reported ergogenic effects of preexercise carbohydrate feedings on exercise performance (6, 10-12). Two ofthe positive studies used time to fatigue at a fixed exercise intensity as the performance criterion (1 1, 12). This performance task, however, is unlike athletic competition, which requires the athlete to vary
the exercise intensity and to traverse a given distance as fast as possible. Only Sherman et al (6) used a performance task, 95 mm ofintermittent cycling followed by a time-trial performance, that simulated competition. Compared with placebo, time-trial 866
Am J C/in Nuir
l99l;S4:866-70.
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
to simulate
Foster et al (14) suggested that preexercise carbohydrate feedings might impair exercise performance by causing a sudden drop in blood glucose and an accompanying acceleration of muscle glycogenolysis and glucose oxidation. The accelerated carbohydrate oxidation was thought to be the result ofelevated insulin concentrations at the start of and during exercise. Because different amounts of ingested carbohydrate elicit different insulin responses both at rest and during exercise, it is important to examine the effects ofingesting varying amounts of preexercise carbohydrate feedings on exercise performance.
In a study
by Gleeson
et al (1 1), subjects
improved
endurance time to exhaustion by 13% when 1.0 g carbohydrate! kg body mass was consumed 60 mm before exercise, despite significantly elevated insulin concentrations at the start of cxercise and a drop in blood glucose early in exercise. It is conceivable,
Introduction
performance
however,
that
a greater
insulin
response
from
will result
consuming > 75 g carbohydrate 1 h before exercise and that this would accelerate muscle glycogenolysis and glucose oxidation and impair exercise performance. On the other hand, if the preexercise carbohydrate feeding continues to empty from the gut and be absorbed by the small intestine during exercise, performance may be either unaffected or further improved. The present study used highly trained cyclists to determine whether ingesting 1.1 g liquid carbohydrate/kg body mass (LC) 1 h before
exercise
performance additional
would
when purpose
result
compared was
in improved
with
to determine
response
resulting from consuming (HC) in a preexercise feeding
mass
ingesting
cycling
time-trial
a placebo
whether
the
larger
2.2 g carbohydrate/kg would further affect
(P). An insulin body
perfor-
mance. Methods Subjects Nine jects
unpaid
were
active
male
volunteers
college-aged
completed students
the who
could
study. cycle
The
sub-
contin-
I From the Exercise Physiology Laboratory, School ofHealth, Physical Education, and Recreation, The Ohio State University, Columbus, OH. 2 Supported in part by Ross Laboratories, Columbus, OH.
Reprints Received Accepted 3
Printed
not available. February 1 1 , 1991. for publication April in USA.
24, 1991.
© 1991 American
Society
for Ginical
Nutrition
PREEXERCISE uously
for
(VO2max).
90
mm
at
70%
of maximal
oxygen
CARBOHYDRATE Exercise
consumption
The physical
and physiological characteristics of the subjects were as follows (i ± SE): age 24 ± 1 y, height 170 ± 1 cm,weight7l ± 2 kg,%bodyfat 12 ± 1,andVO2max4.l ± 0.2 L/min. This study was reviewed and approved by the University’s Biomedical Sciences Review Committee and the subjects voluntarily provided written informed consent. Cont rol period
workboads,
and
the criteria
for VO2max
included
contained
45%,
35%,
and
fat, and protein, respectively, caffeinated beverages.
20%
and
ofenergy
did
not
ratings
every
alcohol
45 mm
or
Each
four trials in the fasted state (10 h) each trial. After completing a familiarization trial to ensure that the subject could complete the exercise tasks, the subjects were randomly assigned to the three experimental trials by using a counterbalanced, double-blind design. The experimental trials required the subjects to consume a placebo or one oftwo carbohydrate solutions 60 mm before exercise. The placebo was a nonnutritive solution whereas LC provided 1.1 g carbohydrate/kg body mass and HC provided 2.2 g carbohydrate/kg body mass. with
7-10
subject
completed
d separating
Subjects ercise.
.
L. The average
chain
length
ofthe
maltodextrins
was 6 glucosyl
24.0
Blood
sampling
and
were
served
from
were obtained before after the feeding.
an
opaque
the feeding
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
were
phase
as quickly
as possible.
during
another,
cadence
and
which
would
time
a
result
variables
immediately
to time
the subtherefore
trial.
and
were
before During
were
com-
the
time
vigorously
ver-
1 50 mL water every fan cooled during
also
conditions
(1 ± SE)
during
± 0.6 torr,
and
± 1.4%
environmental to 38.5
62.0
and
#{176}C after
exercise
60 mm
1S ex-
exercise relative
conditions,
of exercise
and
( 12).
and analysis
8 mL
blood
nontoxic
was
obtained
iv catheter
at each
(B & D Inc,
sampling
time
Rutherford,
NJ)
via that
was inserted into an antecubital vein. A 0.5-mL sample of blood was deproteinized with 1.5 mL cold 8% perchloric acid and centrifuged
at
1700
X g for 30 mm
at 4 #{176}C. The
for lactic acid (21). The remaining
analyzed on ice,
and
serum
was
recovered
supernatant
blood
was
was coagulated
by centrifugation
at 1 700
X
g
for 30 mm at 4 #{176}C. Serum samples were stored in separate tubes for subsequent analysis ofglucose (22), free fatty acids (20, 23), and insulin (ICN Biomedical, RSL, Carson, CA). To reduce variability, blood samples from all three trials for each subject were run in duplicate within the same analysis. The intraassay variability was 1.2%, 2.4%, 3.7%, and 3.2% for glucose, insulin,
lactic
acid,
variability lactic
Inspired (Rayfield,
and
free
fatty
3.5%,
and
fatty
free
ofrespiralory volumes Waitsfield,
spirometer
(Warren
pired
were
gases
acids,
was 4.2%, acid,
Measurement
5.1%, acids,
respectively.
and
The
5.7%
inter-
for glucose,
respectively.
gases
were measured by using a dry-gas meter VT) that was calibrated by using a Tissot E Collins,
Inc,
continuously
Braintree,
sampled
and
MA).
Mixed
analyzed
ex-
for oxygen
(model 5A3, Applied Electrochemistry, Pittsburgh) and carbon dioxide (LB-2, Beckman, Fullerton, CA). Electrical signals from these instruments were directed into an A/D converter and into a computer for calculation of oxygen consumption (i’O2) and
RER.
These
Statistical
color
these
temperature rises remains constant
in taste,
and
#{176}C, 745.9
Under
dation.
texture,
for the
blinded
environmental ± 0.2
humidity.
units. The volume of the preexercise feeding was adjusted relative to body weight to provide the required amount of carbohydrate. The average (±SE) volume of the preexercise feedings was 391 ± 12 mL. All three solutions were made as similar as possible water bottle. Blood samples and 15, 30, 45, and 60 mm
distance were
samples
the metabolic
Physiological and
were required to consume exercise. Subjects were
The
were
insulin,
The carbohydrate solutions were formulated to deliver the two amounts of carbohydrate to the blood within similar time intervals (18). Carbohydrate solutions > 20% (wt:vol) have similar rates of gastric emptying (19). Therefore, LC and HC were chosen to be 20% and 40%, respectively. Because osmolarity also affects gastric emptying (20), the osmolarity for the two beverages was equated by varying the relative amounts of glucose and maltodextrins for LC and HC. Both solutions had the same molar concentration (I 1 mol/L); LC contained 200 g glucose/ L and HC contained 160 g glucose/L and 240 g maltodextrins/
time.
rate,
time trial requiring equivalent to an-
VO2max,
distance
70%
heart
encouraged.
assay
Preexerciseftedings
VO2max
and percent
required
subjects
mm during
core then
blood
After
a higher
performance
the the
bally
to maintain
at
RER,
and
one trial than
at one-halfthe
pleting trial
at 70%
during
output
Roughly
design
of cycling
a shorter
measured
(RPE),
exercise.
carbo-
continuously
a cycling-performance the number of revolutions
have
a sterile,
Experimental
exertion
better
power
of the preexercise
cycled
consumption,
15 mm during
subjects undertook them to complete
would
effects
subjects
Oxygen
of perceived
obtained
in
as carbohydrate,
contain
the
for 90 mm.
VO2max
higher a
the metabolic
feedings,
To perform
leveling offofVO2 with increasing workloads and a respiratoryexchange ratio (RER) > 1.0. Body density was determined by the underwater-weighing procedure (1 5). Percent body fat and lean body mass were calculated according to the equation of Siri (16). Exercise and diet were controlled during the 2 d before each experimental trial in an attempt to equate body carbohydrate reserves among trials ( 17). Exercise was restricted to cycling in the laboratory at 70% VO2max for 40 and 20 mm, respectively, for the 2-d control period. The diet (12.6 MJ) during the control period
To determine
ject
867
protocol
hydrate
other
The physiological characteristics of the subjects were determined within 7 d of the first experimental trial. Calibrated Schwinn Bio-Dyne cycle ergometers (Excelsior Fitness Inc, Chicago) were used for all trials. VO2max was determined by using incremental
FEEDINGS
tified
variables
were
The gas analyzers by the
(Gaithersburg,
National
MD)
used
to estimate
were calibrated Institute
and
carbohydrate
against
of Standards
previously
analyzed
a tank and
oxi-
gas cer-
Technology
by
chemical
methods.
analysis
Standard procedures SEs for the dependent
were used to calculate variables. Areas under
the means the glucose-
and and
868
SHERMAN 6
ET
AL
exercise. During was not different
-J
E E
glucose
was
ercise
compared
response
significantly
curves
± 12, and
w
431
spectively).
U) 0 04
the remaining 60 mm ofexercise, blood between LC and P. For HC, however,
higher
higher
with
both
were
similar
after
LC and
among
± 10 mmol-min
During
the
60,
trials
for the carbohydrate
for
blood
trials
90 mm
under
the trials -L’
time
75, and
P. Areas
of ex-
the glucose-
(406
P, LC,
± 12, 384 and
glucose
compared
glucose blood
HC,
tended
with
re-
to be
P. At the end
-J
of the
ci
0
than
time
trial,
Compared
s-s
PLACEBO 75 g CHO
-A
15OgCHO
0-0
glucose
for HC
was
significantly
greater
for P.
(P
525% 500
blood
0.05). All subjects completed the time trials faster after consuming the preexercise carbohydrate feeding. Time-trial performance was significantly improved by an average 12.5% for the carbohydrate-feeding trials (Fig 3). Power output during the time trials averaged 13. 1% higher for the carbohydrate-feeding trials comtotal
pared
with
P. Similarly,
with P, the percent and LC, respectively.
at completion
VO2max
was
ofthe
time
17% and
trial
compared
1 1% higher
for HC
130
TiME
As liver
An important finding ofthis study is that exercise performance was improved 12.5% when cyclists consumed 1.1 g carbohydrate/ kg body mass (75 g) 60 mm before 90 mm ofsubmaximal cycling followed by an intense time-trial performance. Note that exercise performance
was
neither
further
preexercise
2.2 g carbohydrate/kg
improved
carbohydrate body
mass
nor
feeding
impaired
when
was increased
(1 50 g). After
90 mm
to
of con-
tinuous cycling at 70% VO2max, subjects were requested to complete as fast as possible the number of revolutions equivalent to an additional 45 mm of cycling at 70% VO2max. Subjects maintained
84%
VO2max
during
the
time
trial
for LC and
HC
compared with 68% VO2max during the time trial for P. A similar improvement in cycling time-trial performance was observed by Sherman et al (6). Their moderately trained subjects consumed either 0, 45, 156, or 312 g carbohydrate 4 h before intermittent cycling for 95 mm followed by a time trial identical to that used in the present study. When 3 12 g carbohydrate was consumed,
using time Gleeson
time-trial
performance
was improved
15%.
Similarly,
to fatigue during steady-state exercise as the criterion, et al (11) and Wright et al (12) observed a 13% and
18% improvement
in time
to fatigue,
respectively,
when
either
1 g carbohydrate/kg body mass or 5 g carbohydrate/kg body mass was consumed either 1 or 3 h before exercise, respectively. Although three studies reported no significant effects of preexercise
carbohydrate
feedings
on performance
(7-9),
the
studies
et al (11), Neuffer et al (10), Sherman et al (6), Wright et al (12), and the present study support the principle that preexercise carbohydrate feedings improve cycling performance. ofGleeson
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
90
DURING
(mm)
EXERCISE
FIG 3. Heart-rate responses during exercise for the three experimental trials, and performance times for the time-trial performances for the three experimental trials. For this test, a shorter performance time means improved performance.
Discussion
the 60-mm
60
120
and
the perception be stopped
Blood
muscle
glucose
and
P, indicating production
glycogen
become
depleted
RER
gradually
that availability was gradually
exercise
during
trations
and
diminishing.
P totally because
declined
later
amounts; stages
servation
Because
diminished
thus,
that
when
performance
there
was
This
possibility
blood
it is unlikely
carbohydrate
body
the time-trial
of exercise.
feedings during late in exercise, the
exercise,
during exercise for to support energy
ofcarbohydrate
durance test to exhaustion, it is likely that bohydrate feedings increased carbohydrate normal
during
of effort increases and ultimately exercise has to or the intensity of exercise significantly reduced.
glucose
a higher
that
concennot
an en-
the preexercise oxidation
was
carabove
work
rate
is supported
is maintained
during
the
by the
ob-
by carbohydrate
exercise, blood glucose is oxidized at high even when muscle glycogen concentrations
rate of glycogenolysis Although it is possible
are low that the
rates and
(2, 24-26).
preexercise feeding stimulated the 1 h before exercise (3-5), it is unlikely that the small amount ofglycogen that was synthesized accounted for the significant improvements in time-trial performance resulting from the preexercise carbohydrate feedings. Further, muscle
other
glycogen
studies
synthesis
report
similar
exercise
after a preexercise
is more
likely
carbohydrate
that
during
rates
of muscle
carbohydrate improved performance
availability
during
exercise.
oxidation averaged 12% higher for the feeding trials compared with P. Increased
glycogenolysis
during
meal (5, 8, 9). Rather, it was related to greater
The rate of carbohydrate preexercise
carbohydrate-
carbohydrate availability may have been the result of the effects of liver glycogen synthesis during the hour after the preexercise feeding resulting in increased hepatic
glucose
production
(27).
However,
increased
carbohydrate
870
SHERMAN
availability is most likely the of the preexercise carbohydrate mated
absorption
rate
al (28)
were
suggest
used,
and
60%
of HC
fact
that
the
treatments although
blood blood
of LC and that
were
absorbed. insulin
significantly glucose
HC, This
the results
during
from
different
for
emptying The estiof Hunt
et
of exercise, 100% of LC finding is supported by the
responses
exercise
for
other.
each
the
Further,
similar
to P after
30 mm
30 mm
ofexercise
was signif-
LC was
for HC after
glucose
when
gastric exercise.
by 60 mm
integrated were
exercise,
result of continued feeding during
of
than blood glucose for IC and P. Apparently, for continued to empty from the gut during exercise and was absorbed at a rate that exceeded whole-body glucose disposal. The observations of rapid declines in blood glucose early in icantly
higher
HC, glucose
exercise
and
cogenolysis
increased during
carbohydrate
exercise
after
to support not be consumed during have
been
results
Sherman
present
study
and
those
et al (6) demonstrate
insulin
concentrations
initial
a preexercise
roughly
15 mm
at the
1 mmol/L
of exercise,
that
drop
and
exercise
in blood
performance.
preexercise
glucose
(29).
The
combination
at the start
effects
of exercise
ofthe
is probably
effects
an first
feedings
ofinsulin
on muscle
on glucose
contraction responsible
and the
improve become fatigued the RPE did not exercise intensity lowering of blood
carbohydrate
ofmuscle
elevated
during
Although
and the insulin-like
(1 3, 14). The et al (1 1) and
exercise,
glucose
glyfeeding
significantly
during
some individuals during exercise when blood glucose is lowered, increase and subjects continued the required and were apparently insensitive to the transient cycling
muscle carbohydrates
of Gleeson
that despite start
and carbohydrate
the recommendation the hours before
used
of the
oxidation
for the
uptake
initial
drop
in blood glucose (30). Subsequently, blood glucose is maintained by increased splanchnic glucose output or reduced stimulation of glucose uptake by insulin and contraction. It is probable that if insulin
were
elevated
independent
of
increased
carbohydrate
performance would be impaired. Regardless of the factors regulating the blood glucose and insulin responses during exercise after preexercise carbohydrate feedings, consuming I 1-2.2 g carbohydrate/kg body mass 1 h before cycling exercise and time-trial performance significantly improves exercise availability,
exercise
.
capacity. We thank Jeff Betts, Art Dernbach, Leo D’Aquisto, and Lynda Peel for their various contributions to this study. We also thank the subjects for their cooperation during the study.
References 1. Sherman WM, Lamb DR. Nutrition and prolonged exercise. In: Lamb DR. Murray RM, eds. Perspectives in exercise science and sports medicine. Indianapolis: Benchmark, 1988:213-80. 2. Coyle EF, Coggan AR. Effectiveness ofcathohydrate feeding in delaying fatigue during prolonged exercise. Sports Med l984;l:446-58. 3. Nilsson LH, Hultman E. Liver glycogen in man-the effect of total starvation or a carbohydrate-poor diet followed by carbohydrate refeeding. Scand J Clin Lab Invest l973;32:325-30. 4. Maehlum 5, Felig P, Wahren J. Splanchnic glucose and muscle glycogen metabolism after glucose feeding during postexercise recovery. Am J Physiol l978;235:E255-60. 5. Coyle EF, Coggan AR, Hemmert MK, Lowe RC, Walters TJ. Substrate usage during prolonged exercise following a preexercise meal. J Appl Physiol l985;S9:429-33. 6. Sherman WM, Brodowicz G, Wright DA, Allen WK, Simonsen JC, Dernbach A. Effects of 4 h preexercise carbohydrate feedings on cycling performance. Med Sci Sports Exerc l989;2l:S98-604.
Downloaded from https://academic.oup.com/ajcn/article-abstract/54/5/866/4694357 by University of Glasgow user on 03 April 2018
ET
AL
7. Devlin IF, Calles-Escandon J, Horton ES. Effects ofpre.exercise snack feeding on endurance cycling exercise. J Appl Physiol 1986;6&.980-5. 8. Hargreaves M, Costill DL, Fink WJ, King DS, Fielding PA. Effect of pre-exercise carbohydrate feedings on endurance cycling performance. Med Sci Sports Exerc 1987;19:33-6. 9. Koivisto V, Karonen S-L, Nikkila EO. Carbohydrate ingestion before exercise: comparison ofglucose, fructose, and sweet placebo. J Appl Physiol 198l;51:783-7. 10. Neuffer PD, Costill DL, Flynn MG, Kirwan JP, Mitchell JB, Houmard J. Improvements in exercise performance: effects of carbohydrate feedings and diet. J AppI Physiol 1987;62:983-8. 1 1. Gleeson M, Maughan Ri, GreenhaffPL. Comparison ofthe effects ofpre-exercise feeding ofglucose, glycerol and placebo on endurance
and fuel homeostasis
in man. Eur J Appl Physiol
l986;55:646-53.
12. Wright DA, Sherman WM, Dernbach AR. Carbohydrate feedings before, during, and in combination improves cycling performance. J Appl Physiol (in press). 13. Costill DL, Coyle EF, Dalsky G, Evans W, Fink W, Hoopes D. Effects ofelevated plasma FFA and insulin on muscle glycogen usage during exercise. J Appl Physiol l977;43:69S-9. 14. Foster C, Costill DL, Fink WJ. Effects of preexercise feedings on endurance performance. Med Sci Sports Exerc l979;ll:l-5. 15. McArdle WD, Katch FI, Katch VL EXereiSepIIysiO1Og eneray, nutrition and performance. Malvern, PA: Lea & Febiger, 1981:95-104. 16. Sin WE. Body composition from fluid spaces and density analysis of methods. In: Brozek J, Heusen A, eds. Techniques for measuring body composition. Washington, DC: National Academy Press, 1961:212-6. 17. Sherman WM, Costill DL, Fink WJ, Miller JM. Effect of exercisediet manipulation on muscle glycogen and its subsequent utilization during performance. Int J Sports Med 198 l;2: 114-8. 18. Murray R. The effects of consuming carbohydrate-electrolyte beverages on gastric emptying and fluid absorption during and following exercise. Sports Med 1987;4:322-51. 19. Brener W, Hendrix T, McHugh P. Regulation of gastric emptying ofglucose. Gastroenterology 1983;85:76-82. 20. Duncombe W. The colorimetric micro-determination of non-esterified fatty acids in plasma. Gin Clam Acts l964;9:l22-S. 21. Gutman I, Wahlefeld AW. L4+)-lactate. Determination with lactate dehydrogenase and NAD. In: Bergmeyer HU, ed. Methods of enzymatic analysis. 2nd ed. New Yoric Academic Press, 1974:1464-8. 22. Cooper GR, McDaniel V. The determination ofglucose by the orthotoluidine method (filtrate and direct procedure). In: MacDonald RP, ed. Standard methods in clinical chemistry. New York: Academic Press, 1970:159-70. 23. Noma A, Okabe H, Kita M. A new colorimetric micro.determination of free fatty acids in plasma. Clin Clam Acts 1973;43:317-20. 24. Coggan AR, Coyle EF. Reversal of fatigue during prolonged exercise by carbohydrate infusion or ingestion. J Appl Physiol l987;63:238895. 25. Coggan AR, Coyle EF. Effect ofcarbohydrate feedings during high. intensity exercise. J AppI Physiol l985;65: I 703-9. 26. Coyle EF, Coggan AR, Hemmert MK, Ivy JL. Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J Appl Physiol 1986;6 1:16S-72. 27. Vissing J, Wallace JL, Galbo H. Effect ofliver glycogen content on glucose production in running rats. J Appl Physiol 1989;66:318-22. 28. Hunt JN, Smith JL, Jiang CL. Effect of meal volume and energy density on the gastric emptying ofcarbohydrates. Gastroenterobogy 1985;89: 1326-30. 29. Coyle EF, HagbergJM, Hurley BF, Martin WH, Ehsani AA, Holloszy
JO. Carbohydrate
feeding during
prolonged
strenuous
exercise can
delay fatigue. J Appl Physiol l983;S5:230-5. 30. DeFronzo RA, Ferrannini E, Sato Y, Felig P, Wahren J. Synergistic interaction between exercise and insulin on peripheral glucose uptake. J Clin Invest l98l;68:l468-74.
