Muscle glycogen storage after prolonged exercise:
effect of the glycemic index of carbohydrate feedings
LOUISE
M. BURKE,
GREG R. COLLIER,
AND MARK
HARGREAVES
Department
of Sports Medicine, Australian Institute of Sport, Australian Capital Territory 2616;
Department of Human Nutrition, Deakin University, Geelong 3217; and Department of Physiology,
The University of Melbourne, Parkville 3052, Australia
BURKE, LOUISE M., GREG R. COLLIER, AND MARK HARGREAVES. Muscle glycogen storage after prolonged exercise: effect
of the glycemic index of carbohydrate
feedings. J. Appl. Physiol.
75(2): 1019-1023, 1993.-The
effect of the glycemic index (GI)
of postexercise carbohydrate
intake on muscle glycogen storage
was investigated. Five well-trained
cyclists undertook an exercise trial to deplete muscle glycogen (2 h at 75% of maximal 0,
uptake followed by four 30-s sprints) on two occasions, 1 wk
apart. For 24 h after each trial, subjects rested and consumed a
diet composed exclusively of high-carbohydrate
foods, with one
trial providing foods with a high GI (HI GI) and the other providing foods with a low GI (LO GI). Total carbohydrate
intake
over the 24 h was 10 g/kg of body mass, evenly distributed
between meals eaten 0,4,8, and 21 h postexercise. Blood samples were drawn before exercise, immediately
after exercise,
immediately
before each meal, and 30, 60, and 90 min postprandially.
Muscle biopsies were taken from the vastus lateralis immediately
after exercise and after 24 h. When the effects
of the immediate postexercise meal were excluded, the totals of
the incremental
glucose and insulin areas after each meal were
greater (P 5 0.05) for the HI GI meals than for the LO GI
meals. The increase in muscle glycogen content after 24 h of
recovery was greater (P = 0.02) with the HI GI diet (106 t 11.7
mmol/kg wet wt) than with the LO GI diet (71.5 * 6.5 mmol/
kg). The results suggest that the most rapid increase in muscle
glycogen content during the first 24 h of recovery is achieved by
consuming foods with a high GI.
recovery;
glucose; insulin
of muscle glycogen Stores is a
critical issue for athletes who undertake prolonged training or competition sessions on the same or successive
days. Accordingly, the success of various postexercise
feeding programs in promoting glycogen storage has
been well investigated (1,6,9,10,13,14,17,18).
Conventional approaches to the study of postexercise glycogen
storage have concentrated on intravenous glucose infusions or oral feedings of glucose, fructose, sucrose, or
glucose polymers (1,9,10,17).
However, in practice, athletes need to eat food, rather than single nutrients, to
meet a complex array of nutritional requirements as well
as for social and practical reasons. Research into the efTHE RAPID RESTORATION
0161-7567/93
$2.00 Copyright
feet of different carbohydrate foods on glycogen storage
has taken a simplistic approach to carbohydrate nutrition, dividing foods into “simple”- or “complex”-carbohydrate foods on the basis of their chemical composition
(2, 6, 18). It has been represented that ingestion of simple-carbohydrate
foods will elicit a large, rapid, and
short-lived rise in blood glucose, whereas the response to
complex-carbohydrate foods will be flatter and more sustained.
In other areas of carbohydrate research, it has been
found that this simplistic model is quite incorrect and
that each carbohydrate food elicits its own individual effect on blood glucose quite separately and unpredictably
from its chemical composition. The glycemic index (GI)
concept has been developed to define carbohydrate foods
(and meals) according to their actual postprandial glycemic impact (11). The GI is determined by measuring the
blood glucose response in a fasted subject after the ingestion of a portion of food providing 50 g of available carbohydrate. The area under the glucose curve is expressed as
a percentage of the mean response to a reference food
containing an equivalent amount of carbohydrate (either
glucose or white bread) in the same subject. Factors influencing the glycemic impact of a food include the nature of the starch (amylopectin or amylose), the nature of
saccharides, the physical form of the food, and any cooking and processing techniques that have been used (for
review, see Ref. 19). With a more physiologically based
classification of foods, researchers have been able to manipulate the metabolic responses to diets to improve glucose control in diabetics (4) and to reduce hyperlipidemias (12). Physiological changes have been reported
with differences as small as 11-13 GI units between the
test diets (4,12). The purpose of the present study was to
examine the effect of different GI diets on postexercise
glycogen storage in elite athletes.
METHODS
Five elite junior cyclists [18.2 t 0.2 (SE) yr, 68.7 t 4.6
kg, maximal 0, uptake = 4.8 t 0.3 l/min] agreed to participate in the study, which was approved by the Human
0 1993 the American
Physiological
Society
1019
1020
GLYCEMIC INDEX AND POSTEXERCISE
DIET
TABLE 1. Diets fed to subjects during 24 h of recovery after prolonged exercise
Diet
LO GI
Food
Meals I (t = 0 h)
and 4 (t = 21 h)
Total
meal
Meal
2 (t = 4 h)
Total
Rolled oats cooked
Skim milk
Sourdough
bread
Tomato
Low joule cordial
HI GI
Amount
into
porridge
GI
190 g dry
240 ml
70 g
120
g
500 ml
GI
Cornflakes
Whole milk
Skim milk
Wholemeal
bread
Tomato
Low joule cordial
Amount
GI
100
121
g
300 ml
100 ml
180
160
g
g
White pasta, boiled
Baked beans
Margarine
Low joule cordial
175 g dry
350 g
7g
500 ml
45
70
500 ml
104
Wholemeal
Tomato
Low joule
Polycose
bread
cordial
375
g
210
g
500 ml
30 g
56
Parboiled
rice
Lentils,
boiled
Tomato
sauce
Low joule cordial
165 g dry
175g
40 g
500 ml
54
36
44
46
100
88
meal GI
MeaZ 3 (t = 8 h)
89
46
90
Food
100
138
107
Mashed
instant
potato
Skim milk
Tomato
sauce
Wholemeal
bread
Low joule cordial
Polycose
530 g
100 ml
40 g
75 g
500 ml
30 g
120
46
100
138
Total
meal GI
50
118
Total
diet GI
71
108
Nutrient
(24
h)
intake
Diets provided
Ref. 19).
730 g carbohydrate
50 g fat
145 g protein
75 g fiber
16.04 MJ
10 g carbohydrate
per kg body
730 g carbohydrate
49 g fat
140 g protein
76 g fiber
15.96 MJ
mass per 24 h. Sample
Experimentation
Committee
of Victoria University
of
Technology. They were informed of the risks associated
with participation
before providing
written consent.
Subjects reported to the laboratory in the morning after
an overnight fast on two occasions 21 wk apart. Diet and
activity records were kept over the previous days to standardize carbohydrate intake and to ensure that no strenuous exercise had been undertaken for 236 h before each
trial. An exercise bout was undertaken to lower muscle
glycogen levels, with subjects riding their own bicycles
mounted on a wind trainer, for 2 h at a heart rate equivalent to -75% of maximal 0, uptake, followed by four
30-s “all-out”
sprints with a 2-min recovery period.
Within 5-10 min of cessation of exercise, a muscle sample was obtained from vastus lateralis by use of the percutaneous needle biopsy technique and was quickly frozen
in liquid nitrogen. A catheter was positioned in a forearm
vein for blood sampling and was kept patent by periodic
flushing with 0.9% saline containing a small amount of
heparin (10 U/ml).
The recovery diet provided a total of 10 g of carbohydrate per kilogram body weight over the next 24 h and
was composed almost entirely of high-carbohydrate
foods of either high GI (HI GI) or low-to-moderate
GI
(LO GI). Small quantities of other foods (e.g., margarine
or milk) were added to make the meals palatable or to
manipulate the nutrient content of the meal. The GI of
the total diets was calculated from the weighted means of
diet is for 73-kg
subj. LO and HI GI, low and high glycemic
indexes
(from
the GI values for the component foods (19), and the difference between the diets was estimated to be 37 GI units
(Table 1). The subjects were assigned to each diet in randomized order: three subjects completed the LO GI trial
first followed by the HI GI trial 1 wk later, while the other
two subjects completed the trials in the reverse order.
Food intake was divided into four meals of equal carbohydrate content (2.5 g/kg body wt), and the food was
eaten immediately
after the first biopsy (t = 0) and after
4,8, and 21 h of recovery. Foods were carefully chosen so
that each meal was matched (HI GI vs. LO GI) for fat,
protein, and fiber. Foods high in fructose and sucrose
were avoided; in effect, each recovery diet provided equal
amounts of glucose. The average composition
of each
meal was 74% carbohydrate, 11% fat, and 15% protein. A
description of the diets is provided in Table 1. No exercise or strenuous activity was permitted during the recovery period.
Venous blood samples were obtained immediately
before each meal and 30, 60, and 90 min after each meal.
Blood glucose was measured using an automated glucose
oxidase method (Yellow Springs Instruments
23 AM analyzer, Yellow Springs, OH). Plasma insulin levels were
measured by a commercially
available double-antibody
radioimmunoassay
kit (Phadeseph Insulin RIA, Pharmacia Diagnostic, Uppsala, Sweden). Blood glucose and
plasma insulin profiles were drawn, and the incremental
area after each meal was calculated using the trapezoid
GLYCEMIC
m
4
‘k
2507
‘E
A
i
<
200’
E
E
%
g
INDEX
AND
POSTEXERCISE
2I
c
LO (3
HI (;I
50-
l-
1
Total of
4 meals
2
o
Total minus
meal 1
LO GI
HI (;I
0
.‘E 40 0 0
q
-; 15000 .I
E
00
q
loo-
q
.If
3
g
0
r
150-
5000
E
600
3
Meal
A
i
ti
1021
DIET
LO GI
HI (;I
E
4.
3000
;.
g 10000 W
.
.I2=
Y
r”
5000 -
2000
1000
0
Meal
I
4
.
1. Incremental
blood glucose (top) and plasma insulin1. areas
(bottom)
after each meal in 5 subjs. HI GI, high glycemic index; LO GI,
low glycemic
index. * Significantly
different
from HI GI (P = 0.03).
FIG.
rule, taking the immediate premeal value as baseline and
including all time points until the baseline level was restored. In all subjects, plasma glucose and insulin levels
returned
to baseline values by or before the 90-min
reading.
Twenty-four
hours after the recovery diet was commenced, a second muscle sample was obtained from vastus lateralis, 23 cm distal to the first biopsy site (5). This
sample, together with the immediate postexercise
sample, was analyzed for glycogen content by use of an enzymatic fluorometric
technique (16).
Data for the two trials were compared using analysis of
variance for repeated measures, with significance
accepted at the 0.05 level. Specific differences
between
means were located using Newman-Keuls
post hoc test.
Total areas under the glucose and insulin curves and 24h glycogen storage were compared between trials with a
paired t test. All data are reported as means t SE.
RESULTS
Even with the small number of subjects, differences
were observed between the two diets. The incremental
glucose and plasma insulin areas after each meal are
shown in Fig. 1. Although the meal immediately after
exercise elicited exaggerated blood glucose and plasma
insulin responses that were similar for the LO GI and HI
GI meals, for the remainder of the 24 h the LO GI meals
elicited lower glucose and insulin responses than the HI
GI meals. As shown in Fig. 2, when the glucose and insulin responsesto the first meal (immediately postexercise)
are separated from those of the remaining meals, the
0 ’
Total of
4 meals
Total minus
meal 1
FIG. 2. Total
incremental
blood glucose (top) and plasma insulin
areas (bottom)
(sum of 4 meals) plus total areas less incremental
area
after first meal in 5 subjs. Significantly
different
from HI GI: * P =
0.03; + P = 0.05.
total incremental
glucose and plasma insulin areas resulting from the HI GI diet are significantly
greater than
those resulting from the LO GI diet (P = 0.05 and P =
0.03 for glucose and plasma insulin, respectively).
The degree of muscle glycogen depletion was similar in
the two trials (Table 2). Glycogen storage after 24 h was
greater (P = 0.02) with the HI GI diet (106.1 t 11.7
mmol/kg wet wt) than with the LO GI diet (71.5 t 6.5
mmol/kg wet wt).
DISCUSSION
The results of this study show
carbohydrate
foods after prolonged
nificantly greater glycogen storage
LO GI carbohydrate
foods. Other
that intake of HI
exercise produces
than consumption
data on the effect
GI
sigof
of
2. Muscle glycogen concentration after prolonged
exercise and after 24 h of recovery with LO GZ or HZ GZ
carbohydrate meals
TABLE
Oh
LO GI
HI GI
34.9k5.9
26.3t6.0
24 h
106.4k7.7
132.4*7.5*
A
71.5k6.5
106.1-tll.7*
Values are means + SE of 5 subjs, expressed
in mmol/kg
wet wt. 0 h,
after exercise; 24 h, after 24 h of recovery.
* Significantly
different
from
LO GI (P < 0.05).
1022
GLYCEMIC
INDEX
AND
different carbohydrate foods on muscle glycogen storage
are scarce and inconsistent. Costill et al. (6) reported
that a diet of simple carbohydrates (sucrose/glucose/
fructose) was as effective in restoring muscle glycogen
levels 24 h after exercise depletion as a diet based on
“starchy”
or complex-carbohydrate
foods. However,
after 48 h the complex-carbohydrate
diet resulted in
greater muscle glycogen gains than the simple-carbohydrate diet. It was speculated that the consumption of
starchy carbohydrate foods might enhance glycogen
storage by maintaining elevated insulin levels; however,
insulin levels were not measured in their study. The activation of glycogen synthase by insulin is well documented (3, 8). Roberts et al. (18) proposed that simple
carbohydrates are absorbed rapidly and may be useful as
an immediate substrate in the early stages of glycogen
restoration but will be less useful in later stages when
they may be stored as fat rather than glycogen. The
slower absorption of complex-carbohydrate sources was
suggested to be more valuable during the latter stages of
glycogen storage (18). However, in their study of muscle
glycogen storage after depletion and 72 h of high carbohydrate intake, simple- and complex-carbohydrate foods
were reported to be equally successful in producing increased muscle glycogen stores.
Although these studies examine different time courses
of glycogen restoration, the major source of confusion
lies in the classification of simple and complex carbohydrates and the assumption that they produce separate
and consistent glycemic responses. Different effects on
muscle glycogen storage have already been documented
within the ranks of the simple carbohydrates (mono- and
disaccharides). Fructose, a LO GI sugar, has been shown
to promote only very modest increases in muscle glycogen, whereas sucrose and glucose result in higher rates of
muscle glycogen restoration (1). Complex carbohydrates
do not all produce a flattened glycemic response; indeed,
foods such as bread, cornflakes, and mashed potato produce a large glycemic impact, similar to that of glucose
itself (11). Because glycogen storage studies using simple- and complex-carbohydrate foods fail to give full description of the foods used or to report the glycemic response to meals, it is difficult to judge the results critically.
Only Kiens et al. (14) attempted to study carbohydrate
foods and muscle glycogen storage on the basis of the
actual, rather than assumed, glycemic responses to the
foods. In a brief summary, they reported that a high-carbohydrate diet based on foods with a HI GI produced
greater storage of muscle glycogen after 6 h of postexercise recovery than a diet based on LO GI carbohydrate
foods. However, at 20,32, and 44 h of recovery, there was
no difference in muscle glycogen levels between the diets.
Plasma insulin levels during the first 6 h were 98% higher
with the high GI diet, but blood glucose and insulin levels
at all other time points were similar for both diets (14).
Because the diets are described interchangeably as simple carbohydrate/HI
GI and complex carbohydrate/LO
GI and no descriptions of the actual foods are available,
there is some confusion in interpreting the results.
In the present study, care was taken to choose diets of
different GI. Our results show that the meal immediately
after exercise produced a large glucose and insulin response that was independent of the GI of the foods eaten
POSTEXERCISE
DIET
and a significantly larger response than when the same
meal was consumed 24 h later. This effect is possibly
related to a selective hepatic insulin insensitivity. Indeed, Maehlum et al. (15) observed greater hepatic
escape of an oral glucose load after exercise. With the
exception of the immediate postexercise meal, meals
eaten over the 24-h recovery period produced the expected trend in glucose and insulin response; the consumption of HI GI foods resulted in generally greater
blood glucose and insulin levels than consumption of LO
GI foods, with the totals of the incremental areas under
the blood glucose and insulin response curves being significantly greater with the HI GI than with the LO GI
diet. Significantly greater muscle glycogen storage was
associated with the HI GI diet. It is interesting that the
difference in glycogen storage between diets appears to
be more dramatic than might be expected from the differences in blood glucose and insulin levels. It is possible
that the decreased muscle storage with the LO GI diet
may be due to other factors, such as malabsorption of
carbohydrate from LO GI foods (19). Although further
research is awaited to fully explain the results of our
findings, these preliminary data confirm the hypothesis
of Coyle (7) that postexercise nutrition is based on foods
of moderate-to-high GI.
The authors
acknowledge
the medical
assistance
of Dr. Paul
McCrory.
This study was conducted
at the Victoria
University
of Technology
(Footscray
Campus)
and was supported
by Mars Australia.
Present
addresses:
G. R. Collier, Dept. of Human
Nutrition,
Deakin
University,
Waurn
Ponds, Victoria
3217, Australia;
M. Hargreaves,
Dept. of Physiology,
The University
of Melbourne,
Parkville,
Victoria
3052, Australia.
Address for reprint
requests:
L. M. Burke, Dept. of Sports Medicine,
Australian
Institute
of Sport, PO Box 176, Belconnen,
ACT 2616, Australia.
Received
9 November
1992; accepted
in final
form
19 April
1993.
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