7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 1/18
Oxidation of Carbohydrate FeedingsDuring Prolonged ExerciseCurrent Thoughts, Guidelines and Directions forFuture Research
Asker E. Jeukendrup and Roy Jentjens
Human Performance Laboratory, School of Sport and Exercise Sciences, University of Birmingham,Edgbaston, Birmingham, England
Contents
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4071. Methodological Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 408
1.1 Radioactive Isotopes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4091.2 Stable Isotopes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 409
2. Feeding Strategies and Exogenous Carbohydrate (CHO) Oxidation . . . . . . . . . . . . . . . . . 4102.1 Feeding Schedule . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4102.2 Types of CHO . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 411
2.2.1 Fructose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4112.2.2 Galactose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4122.2.3 Maltose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4122.2.4 Sucrose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4132.2.5 Glucose Polymers – Maltodextrins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4132.2.6 Starch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4132.2.7 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 414
2.3 Multiple Transportable CHOs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4142.4 Osmolality and Concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4152.5 Amount of CHO . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415
3. Factors Affecting Exogenous CHO Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4163.1 Exercise Intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4163.2 Muscle Glycogen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4173.3 Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418
4. Limitations of Exogenous CHO Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4195. Directions for Future Research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4216. Practical Implications, Guidelines and Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
Abstract Although it is known that carbohydrate (CHO) feedings during exercise im-
prove endurance performance, the effects of different feeding strategies are less
clear. Studies using (stable) isotope methodology have shown that not all carbo-
hydrates are oxidised at similar rates and hence they may not be equally effective.
Glucose, sucrose, maltose, maltodextrins and amylopectin are oxidised at high
rates. Fructose, galactose and amylose have been shown to be oxidised at 25 to50% lower rates. Combinations of multiple transportable CHO may increase the
total CHO absorption and total exogenous CHO oxidation. Increasing the CHO
REVIEW ARTICLE Sports Med 2000 Jun; 29 (6): 407-4240112-1642/00/0006-0407/$20.00/0
© Adis International Limited. All rights reserved.
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 2/18
intake up to 1.0 to 1.5 g/min will increase the oxidation up to about 1.0 to 1.1
g/min. However, a further increase of the intake will not further increase the
oxidation rates. Training status does not affect exogenous CHO oxidation. The
effects of fasting and muscle glycogen depletion are less clear.
The most remarkable conclusion is probably that exogenous CHO oxidation
rates do not exceed 1.0 to 1.1 g/min. There is convincing evidence that this
limitation is not at the muscular level but most likely located in the intestine or
the liver. Intestinal perfusion studies seem to suggest that the capacity to absorb
glucose is only slightly in excess of the observed entrance of glucose into the
blood and therate of absorption may thus be a factor contributingto the limitation.
However, the liver may play an additional important role, in that it provides
glucose to the bloodstream at a rate of about 1 g/min by balancing the glucose
from the gut and from glycogenolysis/gluconeogenesis. It is possible that when
large amounts of glucose are ingested absorption is a limiting factor, and the liver
will retain some glucose and thus act as a second limiting factor to exogenous
CHO oxidation.
The number of studies concluding that carbohy-
drate (CHO) feedings during exercise improve ex-
ercise capacity or exercise performance is so large
that, from a scientific point of view, we can con-
sider this relationship true. In the last few years,studies have accumulated to show that CHO feed-
ings during exercise can positively affect perfor-
mance when the exercise duration is about 45 min-
utes or longer.[1,2] The mechanism by which these
CHO feedings exert their effect is believed to be a
maintenance of blood glucose and increased rates
of CHO oxidation during exercise.[2] It has also been
shown that CHO feedings during exercise ‘spare’
liver glycogen.[3-5] However, whether CHO feedings
‘spare’muscle glycogen is still controversial, as somestudies reported glycogen ‘sparing’[6,7] whereas oth-
ers did not.[2,8] This debate has recently been re-
viewed by Tsintzas and Williams.[9] Several studies
have also addressed the questions of which CHO was
most effective, what the most effective feeding
schedule was and the optimal amount of CHO to
be ingested. Additional studies have looked at fac-
tors that can possibly influence the oxidation of
ingested CHO, such as muscle glycogen levels, diet,
and exercise intensity. More recently, studies haveattempted to detect the factors that limit the maxi-
mal rates of exogenous CHO oxidation.
The purpose of this review is not to review the
effects of CHO on exercise performance per se, but
to summarise the factors that determine the efficacy
(i.e. oxidation) of ingested CHO. With the conclu-
sions from this overview, guidelines will be formu-lated for the use of CHO supplements during exer-
cise. Finally, some of the remaining questions and
directions for future research will be discussed.
1. Methodological Considerations
The oxidation of ingested CHO can be measured
by using isotope techniques. Costill et al.[10] were
probably the first to study the oxidation of ingested
CHO. They labeled the CHO in a drink with a ra-
dioactive tracer ([U-14C]glucose) and reported that
only a small amount of an ingested CHO load was
oxidised during exercise. As a result, they concluded
that CHO feedings were of limited importance for
muscle metabolism. However, this result was prob-
ably the result of methodological problems, since
many studies in the following years have shown
significant contributions of ingested CHO to energy
expenditure during exercise. Most studies today use
stable isotopes for the measurement of exogenous
CHO oxidation, since this does not provoke anyhealth hazards in contrast to the potential negative
effects of radioactive isotopes. The advantages and
408 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 3/18
disadvantages of these techniques will be discussed
in sections 1.1 and 1.2.
1.1 Radioactive Isotopes
The oldest method to trace ingested CHO is to
adda[U-14C]glucose tracer to a CHO beverage and
measure 14C in expired gases using a scintillation
counter. The advantage of this technique is that it
is relatively inexpensive compared with the use of
stable isotopes. In addition, shifts in background
enrichments which may occur when using stable
isotopes (see section 1.2) are not a problem, be-cause the background level of 14C is negligible.
An obvious disadvantage of this technique is the
fact that it exposes the volunteer to radioactivity.
Although the radiation dose given is usually low
(<40 uCi/L is consumed), and is calculated to cor-
respond to 0.02 to 0.03 rem, 200 to 250 times lower
than the permissible dose, the actual risks may of-
ten be underestimated.[11] Glucose is not only used
for oxidation, but is also a substrate for other me-
tabolic pathways, including pathways that result in
the formation of DNA. Incorporation of radioac-
tivity in a DNA molecule is of course dangerous
because it may damage genetic material. It is there-
fore advisable to use stable isotopes rather than
radioactive isotopes to study metabolism.
One potential problem with using isotopes (ra-
dioactive or stable) is that part of the CO2 (includ-
ing 14CO2 or 13CO2) may not appear in the expired
gases because it is temporarily trapped in the bicar-
bonate pool.
CO2 + H2O ↓ H2CO3 ↓ HCO3– + H+ (Eq. 1)
This is a very large and only slowly exchanging
pool, in which CO2, arising from various decarbox-
ylation reactions, is retained. In resting conditions,
it may take hours before there is an equilibrium
between 14CO2 and H14CO3– (or 13CO2 and H13CO3
–).
However, during exercise the turnover of this pool
increases severalfold and, especially at high absolute
workloads, equilibrium may be reached within 60
minutes. It has been reported that recovery of 13CO2
approached 100% after 60 minutes of exercise at
60 to 70% maximal oxygen uptake (V.
O2max).[10,12,13]
In many experimental conditions, the entrapment
of 14CO2 or 13CO2 in the bicarbonate pool may cause
a marked underestimation of the true exogenous
CHO oxidation, especially during the first hour of
exercise.
There are a few ways around this problem. One
way is to prime the bicarbonate pool with H14CO3–
or H13CO3–. This would bring the bicarbonate pool
into equilibrium within the first 15 minutes of ex-
ercise.[5,8] A second way is to avoid calculating ex-
ogenous CHO oxidation rates in the first hour.[14]
Finally, it is possible to use an acetate correction
factor as suggested recently.[15] In addition to thetemporary label loss in the bicarbonate pool, it has
also been reported that, in studies using a 13C-tracer
for studying fatty acid metabolism, part of the tracer
may be trapped in exchange reactions with the tri-
carboxylic acid (TCA)-cycle.[15,16] For example,
some 13C-carbons may be incorporated into the glu-
tamate/glutamine pool via α-ketoglutarate (α-KG),
or into phosphoenolpyruvate (PEP) via oxaloace-
tate (OAA).[16] This label fixation results in a de-
creased recovery of label in the expired gases and,in order to correct for this loss, the acetate correc-
tion factor has been proposed.[15] This correction
is based on theassumption that acetate hasimmediate
access to the TCA-cycle and is instantly oxidised.
The percentage of label (13C or 14C) not recovered
in expired CO2 represents the amount of CO2
trapped in exchange reactions with TCA-cycle in-
termediates (TCAI) and the bicarbonate pool. The
label loss is dependent on the metabolic rate. At
high oxygen uptakes (>35 ml/kg/min) less label is
trapped and recovery of the 1-14C-acetate label was
found to be 85 to 90%.[15] Similar results were ob-
tained by Schrauwen et al.[16] when [U-13C]palmi-
tate was used. This implies that studies performed
at low absolute exercise intensities may have under-
estimated exogenous CHO oxidation rates.
1.2 Stable Isotopes
Studies in which stable isotope methodology
was used to measure exogenous CHO oxidationhave used 13C-enriched substrates. Some of these
studies have used naturally enriched CHO (derived
Oxidation of Carbohydrate Feedings During Exercise 409
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 4/18
from C4 plants such as corn and cane sugar). These
plants have a naturally high abundance of 13C.
When ingesting these CHOs during exercise, breath13CO2 will become enriched and, together with a
measure of the total CO2 production rate, exoge-
nous CHO oxidation rates can be quantified. In ad-
dition to the problems described above, there is an-
other complication with this technique: shifts in
substrate utilisation may result in a change in back-
ground enrichment.[17,18] Because CHO is usually
more 13C-enriched than fat, glycogen stores may
display higher
13
C-enrichments than endogenousfat stores. Any change in shift in endogenous sub-
strate utilisation can therefore cause a change in the
background 13C-enrichment independent of ingested
CHO. These changes occur for instance in the tran-
sition from rest to exercise, and typically an increase
in 13CO2 in the expired gases is observed. The mag-
nitude of the error depends on the 13C-enrichment
of the ingested CHO relative to the 13C-enrichment
of endogenous glycogen stores. It has been shown
that individuals with a diet in which most CHOsare derived from C4 plants (a typical northern Amer-
ican or Canadian diet) have higher 13C-enrichments
in their muscle glycogen stores compared with Euro-
peans, whose diet is typically derived from C3 plants
such as potato and beet sugar.
In a comparative study at 60% V.
O2max at Ball
State University (Indiana, USA) and Maastricht Uni-
versity (The Netherlands), we have observed that
in northern America, shifts in background enrich-
ment may be 3 to 5 times higher than in Europe(unpublished data). Several investigators have there-
fore instructed their study participants not to con-
sume products with a high natural 13C-abundance,
or have reduced the error by artificially increasing
the 13C-enrichment of the CHO ingested during the
experiment (typically by adding [U-13C]glucose to
a CHO beverage). By adding a tracer to the CHO,
the shift in background remains the same but the
relative error is reduced. Another way around the
problem is to perform control trials with an identi-cal protocol but with ingestion of CHO with a low
natural abundance. The background 13C-enrichments
can then be used to correct the calculated exoge-
nous CHO oxidation.
Exogenous CHO oxidation = V.
CO2 • (ECO2 –
Ebkg)/(Eing – Ebkg) • 1/k (Eq. 2)
where V.
CO2 is the total CO2 production rate, ECO2
is the 13C-enrichment of CO2, Eing is the 13C-
enrichment of the ingested CHO, Ebkg is the back-
ground enrichment determined in a separate exper-
iment with thesame conditions, and k is the amount
of CO2 that will arise from the oxidation of 1g of
glucose (0.7466L CO2 /g glucose).
It is possible to obtain accurate and reliable
measures of exogenous CHO oxidation using (ra-
dioactive or stable) isotopes. However, as was just
discussed, there are several errors that can be made
and have been made in the past. This is important
when interpreting results, especially from some of
the earlier studies. The absolute values reported in
several trials may be overestimated in studies using
CHO with a naturally high 13C-abundance because
no corrections were made for background enrich-
ment. Other studies may have underestimated ex-ogenous CHO oxidation because no correction was
made for label loss or label fixation. We would like
the reader to keep this in mind when interpreting
the results of various studies. Here, we will present
the data of different studies as presented in the orig-
inal papers. We have not tried to correct for the
possible methodological errors because there were
too many unknown variables (e.g. diet, background
enrichments) and often papers did not report suffi-
cient information (e.g. enrichment data) to allowthese corrections to be made. Nevertheless, in most
cases the error will be small (5 to 10%) and correc-
tion would not have altered the conclusions of these
papers since typically 2 or 3 trials are compared in
the same experimental conditions.
2. Feeding Strategies and ExogenousCarbohydrate (CHO) Oxidation
2.1 Feeding Schedule
The typical pattern of exogenous glucose oxida-
tion rates is shown in figure 1. The first appearance
410 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 5/18
of label from ingested CHO can already be ob-
served in the first 5 minutes (unpublished observa-
tions). During the first 75 to 90 minutes of exercise,
exogenous CHO oxidation will continue to rise as
more and more CHO will be emptied from the
stomach and absorbed in the intestine. After 75 to
90 minutes a leveling-off will occur and the exog-
enous CHO oxidation rate will reach its maximum
value and will not further increase. The timing of
CHO feedings seemed to have very little effect on
the slope of this curve or the plateau value. In sev-
eral studies[19-23] the oxidation of a single glucose
load (100g) given at the onset of exercise (90 to
120 minutes) was investigated. They all reported a
very similar oxidation pattern for ingested glucose;
an increase in oxidation rates during the first 75 to
90 minutes and a plateau thereafter. Maximal ex-
ogenous CHO oxidation rates in these studies var-
ied between 0.48 and 0.65 g/min. These rates are
similar to those observed when ingesting similar
amounts of glucose (90 to 100g in 90 to 120 min-
utes) as repetitive feedings during exercise.[24-28]
In a study by Krzentowski et al.,[20] volunteers
walked at a 10% grade (45% V.
O2max) for 4 hours.
They ingested 100g of glucose after 15 or 120 min-
utes. Exogenous CHO oxidation rates followed an
identical pattern from the time of ingestion until 2
hours later. The amount of ingested glucose ox-
idised was similar in the 2 hours following inges-
tion (55g when CHO was ingested after 15 minutes
and 54g when ingested after 120 minutes). This
study showed that the time of ingestion has no ef-
fect on exogenous CHO oxidation. Often repetitivefeeding schedules are adopted because it has been
shown that this accelerates the rate of gastric emp-
tying and hence the delivery of CHO to the intes-
tine.[29,30] However, since gastric emptying does
not usually limit exogenous CHO oxidation,[27,31]
the feeding schedule may have little effect on the
maximum oxidation rates or the time to reach these
high rates of oxidation. Thus, although there are no
studies available that have directly studied the ef-
fect of different feeding schedules on the rate of exogenous CHO oxidation, the literature seems to
suggest that the feeding schedule has very little
impact on the maximal exogenous CHO oxidation
rates or the time to reach this maximum. However,
the feeding schedule should be such that high exo-
genous CHO oxidation rates are achieved as soon
as possible after the onset of exercise and the amount
of CHO ingested should be sufficient to maintain
high rates of exogenous CHO oxidation.
McConell et al.[32]
compared the effects of CHOingestion throughout exercise with ingestion of an
equal amount of CHO late in exercise. In this study,
performance was improved relative to the control
trial only when CHO was ingested throughout ex-
ercise. CHO ingestion late in exercise did not im-
prove performance despite increases in plasma glu-
cose and insulin levels.
2.2 Types of CHO
In figure 2, different types of dietary CHO aredepicted. Different types of CHO may have differ-
ent properties. Differences in osmolality and struc-
ture have effects on taste, digestion, absorption, the
release of various hormones, and the availability
of glucose for oxidation in the muscle. A number
of studies have compared the oxidation rates of
various types of ingested CHO with the oxidation
of glucose during exercise.[26,27,31,33-38] The results
will be discussed in the following sections.
2.2.1 Fructose
There has been considerable interest in fructose
for a variety of reasons.[23,39,40] The first reason is
HI-GLU
LO-GLU
0
0.2
0.4
0.6
0.8
1.0
1.2
0 30 60 90 120 E x o g e n o u s C H O o
x i d a t i o n ( g / m i n )
Time (min)
Fig. 1. Typical pattern of exogenous carbohydrate (CHO) oxi-dation during exercise when beverages are consumed at the
onset of exercise and at regular intervals thereafter. HI-GLU =high glucose ingestion; LO-GLU = low glucose ingestion.
Oxidation of Carbohydrate Feedings During Exercise 411
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 6/18
that adding fructose will generally improve the pal-
atability of a drink. Secondly, fructose will cause a
20 to 30% smaller increase in plasma insulin levels
compared with glucose,[41] and hence it will reduce
lipolysis to a smaller extent. Fructose has also been
used as a pre-exercise feeding to prevent exercise-
induced rebound hypoglycaemia.[23,39,40] Massicotte
and colleagues[26,33] studied the oxidation of fruc-
tose compared with an isoenergetic glucose solution
and found 25% lower oxidation rates for fructose.
Jandrain et al.[42] studied exogenous CHO oxida-
tion rates in 10 healthy but untrained volunteers
during 3 hours of exercise at 45% V.
O2max whileingesting 150g glucose or fructose. The peak oxi-
dation rates for the ingested glucose were 0.67 g/min
and fructose oxidation peaked at 0.50 g/min (25%
lower). Similar findings were reported by oth-
ers.[23,34,43,44] The lower oxidation rates of fructose
are probably due to a lower rate of absorption and
the fact that fructose has to be converted into glu-
cose in the liver before it can be metabolised. The
latter is usually a relatively slow process. Interest-
ingly, during fasting when gluconeogenic pathwaysare activated, similar rates of oxidation were found
for glucose and fructose.[25,34]
2.2.2 Galactose
Only one study has investigated the oxidation
rates of ingested galactose during exercise. Leijssenet al.[35] fed 8 volunteers, who exercised for 2 hours
at 70% V.
O2max, 155g of galactose or glucose and
calculated the oxidation rates of the exogenous CHO.
While glucose was oxidised at a rate of 0.85 g/min
during the last hour, galactose oxidation was only
half of that (0.41 g/min). It was suggested that the
absorption or the conversion into glucose in the
liver was limiting. Galactose on its own therefore
seemed an inappropriate source of CHO for sports
drinks.
2.2.3 Maltose
Hawley et al.[36] investigated the oxidation of
maltose and glucose during 90 minutes of exercise
at 70% V.
O2max. Trained volunteers ingested 180g
of glucose or maltose during exercise and exogen-
ous CHO oxidation was measured using radioactive
isotopes. High peak oxidation rates were reached
at the end of exercise and equaled 0.9 g/min for
glucose and 1.0 g/min for maltose. These differ-ences were not statistically significant and it was
concluded that maltose and glucose are oxidised at
Glucose Fructose Galactose
Maltose Sucrose Lactose
Amylopectinstarch
Amylosestarch
Maltodextrin
C
CC
C
OC
OH
C
OH OH
OH
OH
Fig. 2. Overview of different carbohydrates and their structure. There are 3 monosaccharides (glucose, fructose and galactose) and3 disaccharides (maltose, sucrose and lactose). Glucose polymers (maltodextrins) and starch consist of a series of coupled glucosemolecules.
412 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 7/18
similar rates. In addition, these authors found no
differences in the absorption rates of these CHOs.
2.2.4 Sucrose
Few studies have investigated the oxidation of
ingested sucrose. In a study by Moodley et al., [27]
volunteers ingested 90g of sucrose during 90 min-
utes of exercise at 70% V.
O2max. Sucrose oxidation
rates peaked at approximately 0.4 g/min. Although
these rates may seem quite low, similar oxidation
rates were reported for glucose and the low values
may therefore be a result of the methodology used
in that study. Wagenmakers et al.
[37]
gave theirstudy participants an 8% sucrose solution during 2
hours of cycling exercise at 65% V.
O2max. The total
amount of sucrose ingested during the 2 hours was
145g, and it was estimated that 81g was oxidised.
The peak oxidation rate was 0.87 g/min, a value
similar to that observed after glucose ingestion in
other studies.[8,14,25-28,36,45] It can therefore be con-
cluded that sucrose can be oxidised at similar rates
as glucose and the efficacy of these 2 CHOs may
be similar.
2.2.5 Glucose Polymers – Maltodextrins
Because of their neutral taste and their relatively
low osmotic value, maltodextrins have been used
by many manufacturers of sports drinks to increase
the CHO content of these beverages. In a study by
Rehrer et al.,[31] a 17% maltodextrin solution was
compared with a 17% glucose solution. The total
amount of CHO that was ingested during 80 min-
utes of exercise at 70% V.
O2max was 220g. Oral
CHO oxidation was measured and was found to be
similar for the glucose and the maltodextrin drink
(42 and 39g for glucose and maltodextrin, respec-
tively). A peak oxidation rate of 0.78 g/min was
reported for glucose and 0.75 g/min for malto-
dextrins. These results indicate that there is no dif-
ference in the oxidation of maltodextrins and glu-
cose. In addition, it was found that the rates of
gastric emptying and thus the rate of delivery of
CHO to the intestine was similar between glucose
and the glucose polymer. These results also imply
that the digestion (hydrolysis of the bonds betweenglucose molecules of a glucose polymer) is not a
rate-limiting step for exogenous CHO oxidation.
Wagenmakers et al.[37] found similar results when
feeding volunteers maltodextrin solutions ranging
from 4 to 16%. Increasing rates of CHO ingestion
seemed to increase oral CHO oxidation up to a rate
of 1.0 to 1.1 g/min. Ingestion of more than 1.2 g/min
had very little or no additional effect on the oxida-
tion rates.[37] However, these high rates of inges-
tion did result in high oral CHO oxidation rates
(0.53 to 1.07 g/min) that were similar to the rates
observed with glucose ingestion in other studies.
2.2.6 Starch
There are 2 major types of starch: amylopectin
and amylose. Amylopectin is a highly branched mol-
ecule, whereas amylose is a long straight chain of glucose molecules (fig. 2) twisted into a helical
coil. Branches in starch are created by 1,6 bonds
between glucose units, whereas 1,4 glucosidic bonds
will result in a straight chain of glucose units.
Starches with a relatively large amount of amylo-
pectin are rapidly digested and absorbed, whereas
those with a high amylose content will have a slow
rate of hydrolysis. Starches make up approximately
50% of our total daily CHO intake and most natu-
rally occurring starches are a mixture of amylose
and amylopectin (see table I). One study[38] com-
pared the rate of gastric emptying and the oxidation
rate of an insoluble starch consisting of 23% amy-
lose and 77% amylopectin with a soluble starch
consisting of 100% amylopectin. Volunteers ingested
316g during 2.5 hours of cycling exercise at 68%
V.
O2max. The amount of CHO delivered to the in-
testine seemed somewhat lower in the case of the
insoluble starch, but this difference did not reach
statistical significance. However, the insoluble starch
was oxidised at a lower rate (75g of insoluble starchcompared with 126g of soluble starch). Peak oxi-
dation rates were 1.1 and 0.8 g/min for the soluble
Table I. Amylose andamylopectin content of various plantstarches
Plant starches Amylose (%) Amylopectin (%)
Maize 24 76
Potato 20 80
Rice 19 81
Tapioca 17 83
Wheat 25 75
Oxidation of Carbohydrate Feedings During Exercise 413
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 8/18
starch and the insoluble starch, respectively, while
the insoluble starch seemed to cause some gastro-
intestinal discomfort.[38] The oxidation of amylose
only was not measured but can be assumed to be
very low. Although one study reported a very high
rate of oxidation for insoluble starch,[46] this has
been shown to be due to a methodological error.[38]
In conclusion, amylopectin is oxidised at higher
rates than amylose and is therefore a more appro-
priate energy source in CHO beverages for athletes.
Furthermore, insoluble starch may provoke gastro-
intestinal symptoms.[38]
2.2.7 Summary
The results of various studies are summarised in
figure 3. This figure shows the peak oxidation rates,
which may depend on a variety of factors including
the exercise intensity, the amount of CHO ingested,
and the timing of these feedings. Fructose and ga-
lactose appear to be oxidised at relatively low rates,whereas glucose, sucrose, maltose, maltodextrins
and soluble starch seem to be oxidised at relatively
high rates. Maximal oral CHO oxidation seems to
be around 1 g/min. The horizontal line depicts the
absolute maximum just below 1.1 g/min. The dot-
ted line represents the line of identity, where CHO
ingestion equals CHO oxidation. From this graph
it can be concluded that oral CHO oxidation may
be optimal at rates of ingestion around 1.0 to 1.5
g/min. This implies that athletes should ensure a
CHO intake of about 60 to 70g per hour for optimal
CHO delivery. Adopting an ingestion rate of 60 to
70 g/h will optimise exogenous CHO oxidation.
2.3 Multiple Transportable CHOs
A study by Shi and colleagues[47] suggested that
the inclusion of 2 or 3 CHOs (glucose, fructose and
sucrose) in a drink may increase water and CHO
absorption despite increased osmolality. This effect
was attributed to the separate transport mechanisms
across the intestinal wall for glucose, fructose andsucrose.[47] Interestingly, fructose absorption from
sucrose is also more rapid than the absorption of an
0
1
2
3
0 1 2 3
O
r a l C H O o
x i d a t i o n r a t e ( g / m i n )
CHO ingestion rate (g/min)
Glucose
Fructose
GalactoseSucrose
MaltoseMD
Starch
Fig. 3. Peak oxidation rates of oral carbohydrates (CHOs) are depicted against the CHO ingestion rate of different types of CHO.Fructose and galactose appear to be oxidised at relatively low rates whereas glucose, sucrose, maltose, maltodextrins and solublestarch seem to be oxidised at relatively high rates. The horizontal line depicts the absolute maximum for oral CHO oxidation. Thedotted line represents the line of identity, where CHO ingestion equals CHO oxidation.
414 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 9/18
equimolar amount of fructose. In an elegant study,
Adopo et al.[44] fed 6 volunteers CHO at the onset of
2 hours of exercise at 61% V. O2max. The CHO feed-
ings were 50g of glucose, 50g of fructose, 100g of
glucose, 100g of fructose or 50g of glucose plus
50g of fructose. It was found that adding fructose
to a glucose solution increases the oral CHO oxi-
dation by 21% compared with an iso-energetic glu-
cose solution (fig. 3). The oxidation rate of 50g
glucose plus 50g fructose in a combined drink was
higher than the oxidation rate of either 100g glu-
cose or 100g fructose. However, amounts ingested
were relatively small and it remains to be estab-lished whether combined ingestion of glucose and
fructose can increase exogenous CHO oxidation
more than theingestion of large amounts of a single
CHO. Whether addition of galactose to a glucose
drink can increase total exogenous CHO oxidation
in a similar way to glucose and fructose needs to
be determined.
These data suggest that it might be useful to
include multiple types of CHO in CHO drinks for
athletes. More studies are needed to identify opti-mal combinations of different CHOs.
2.4 Osmolality and Concentration
Gastric emptying and absorption may depend
on the concentration and osmolality and hence the
type and amount of CHO, and the volume of the
ingested beverage. Recent studies seem to suggest
that CHO content is a more important determinant
of gastric emptying than osmolality.[48] Therefore,
the CHO type may have little or no effect on the
rate of gastric emptying.[49] It has become clear that
the CHO type and osmolality of a solution can in-
fluence intestinal absorption of fluid and CHO. Rel-
atively large amounts of glucose in the form of glu-
cose polymers introduced to the gastrointestinal tract
without changing the osmotic load can increase the
glucose delivery and induce greater water absorp-
tion.[50] Jandrain et al.[19] investigated the oxidation
of a 50g glucose load dissolved in either 200, 400
or 600ml of water. Although both the concentrationand osmolality were different in these drinks, no dif-
ferences were observed in exogenous CHO oxidation
during 4 hours of exercise at 45% V.
O2max. This
study suggests that the total amount of CHO seems
to be a more important determinant of exogenous
CHO oxidation than osmolality or CHO concentra-
tion.
2.5 Amount of CHO
The amount of CHO that needs to be ingested
in order to obtain optimal performance is important
from a practical point of view. The optimal amount
is likely to be the amount of CHO resulting in max-
imal exogenous CHO oxidation rates. Pallikarakiset al.[51] found that doubling the amount of CHO
ingested from 200 to 400g during 285 minutes of
exercise at 45% V.
O2max increased exogenous CHO
oxidation. However, exogenous CHO oxidation rates
did not double and the percentage of the CHO in-
gested that was oxidised was slightly lower (59.5
and 56.8%, respectively). Here we will refer to this
phenomenon as a lower oxidation efficiency with
the larger dose of CHO.
Oxidation efficiency = exogenous CHOoxidation rate/ingestion rate • 100% (Eq. 3)
Rehrer et al.[31] studied the oxidation of differ-
ent amounts of CHO ingested during 80 minutes of
cycling exercise at 70% V.
O2max. In a randomised
cross-over design, volunteers received a 4.5% glu-
cose solution (a total of 58g glucose during 80 min-
utes of exercise) or a 17% glucose solution (220g
during 80 minutes of exercise). Exogenous CHO
oxidation was measured and these were slightly
higher with the larger CHO dose (42 and 32g in 80
minutes, respectively). Thus, even though the am-
ount of CHO ingested was increased almost 4-fold,
the oxidation rates were barely affected. The oxi-
dation efficiency was much lower with the large
amount of CHO (19% for the 17% glucose solution
versus 55% for the 4.5% glucose solution). Inges-
tion of a 17% maltodextrin solution lead to the same
conclusion (i.e. there was a lower oxidation effi-
ciency with the more concentrated solution). In a
study by Wagenmakers et al.,[37] participants exer-cised for 120 minutes at 65% V
.O2max on 5 occa-
sions and received 4 doses of maltodextrin ranging
Oxidation of Carbohydrate Feedings During Exercise 415
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 10/18
from 72 to 289g. Calculated average ingestion rates
were 0.6, 1.2, 1.8 and 2.4 g/min. Although oxida-
tion rates increased with increasing intake, exoge-
nous CHO oxidation seemed to level off after an
intake of 1.2 g/min. Oxidation rates were 0.53,
0.86, 1.00 and 1.07 g/min, respectively. Also in this
study, the oxidation efficiency decreased with in-
creasing intake (72, 52, 39 and 32%, respectively).
More recently, Jeukendrup et al.[5] investigated
the oxidation rates of even larger CHO intakes on
exogenous CHO oxidation. In this study, well trained
volunteers exercised at a relatively low exercise
intensity of 50% V.
O2max for 120 minutes while in-gesting 70 or 360g of glucose. With the low dose
of glucose (average ingestion rate of 0.58 g/min)
exogenous CHO oxidation rates averaged 0.34
g/min, while with the high dose (average ingestion
rate 3.00 g/min) these rates increased up to 0.94
g/min. This study also demonstrated a decreased
CHO oxidation efficiency with increasing inges-
tion rates (59 vs 31%). It is interesting to note that
although ingestion rates increased up to 2.4 to 3.0
g/min,[5,37]
in none of these studies did CHO oxi-dation rates exceed 1.1 g/min.
The results of all studies currently available in the
literature were used to construct figure 3. Although
this graph needs to be interpreted with caution (it
includes studies at different exercise intensities,
different feeding schedules, different volunteer
populations, etc.), it must be concluded that the
maximal rate at which ingested CHO can be oxi-
dised is 1.0 to 1.1 g/min. Increasing the CHO intake
during exercise may increase oxidation rates until
the intake exceeds 1.0 to 1.2 g/min. Clearly, the rate
of oxidation of ingested CHO is limited. However,
the factors limiting exogenous CHO oxidation are
still largely unknown. Possible mechanisms will be
discussed in section 3.
3. Factors Affecting ExogenousCHO Oxidation
3.1 Exercise Intensity
With increasing exercise intensity, the exercis-
ing muscle becomes more and more dependent on
CHO as a source of energy. Both an increased mus-
cle glycogenolysis and increased plasma glucose
oxidation will contribute to the increased energy
demands.[52] It is therefore reasonable to suspect
that exogenous CHO oxidation might increase with
increasing exercise intensities. Indeed, an early study
by Pirnay et al.[53] reported lower exogenous CHO
oxidation rates at low exercise intensities compared
with moderate intensities, but exogenous CHO ox-
idation tended to level off between 51 and 64%
V.
O2max. In this study, participants exercised for 90
minutes on a treadmill on 4 different occasions atdifferent percentages of their maximal aerobic ca-
pacity. They ingested 100g of glucose during exer-
cise. The average oxidation rates of the ingested
glucose were 0.18, 0.36, 0.46 and 0.49 g/min at 22,
39, 51, and 64% V.
O2max, respectively. The exoge-
nous CHO oxidation rates did not further increase
when the exercise intensity was increased from 51
to 64% V.
O2max.
Recently, the same group of researchers found
an almost similar relationship between the exoge-nous CHO oxidation rate and the power output on
a cycle ergometer.[54] The oxidation rate of the in-
gested CHO increased with increasing metabolism
for intensities below 60% V.
O2max. However, when
the exercise intensity was increased from 60 to 75%
V.
O2max the oxidation rate leveled off or even de-
creased (0.51 and 0.42 g/min, respectively). One
possible explanation for the reduced exogenous oxi-
dation rate during high exercise intensities (>70 to
75% V
.
O2max) might be the limitation of intestinaldigestion and/or absorption, although to our knowl-
edge such a limitation has not been shown at exer-
cise intensities below 80% V.
O2max. Massicotte et
al.[28] examined a group of individuals with a wide
variety of fitness levels during exercise at 60% of
their individual V.
O2max. Although volunteers exer-
cised at the same relative workload (60% V.
O2max),
there were large differences in the metabolic rate
(absolute workload). In agreement with the find-
ings of Pirnay et al.,[53,54] a linear relationship be-tween the metabolic rate and the oxidation rate of
100g ingested CHO was found.
416 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 11/18
However, it could be argued that these findings
are an artifact caused by the stable isotopic meth-
ods used, rather than a physiological phenomenon.
As discussed in section 1, some label may be lost
in exchange reactions with the TCA-cycle. It was
also shown that at low metabolic rates recovery of
the label was only 60 to 70%, whereas at high work
rates recovery of the label can be 90% or more.[13]
Because no correction was made for label loss in
the studies cited above, the calculated exogenous
CHO oxidation rates could have been underesti-
mated, especially at lower metabolic rates. We
therefore corrected the values for label loss accord-ing to Sidossis et al.[13] However, although the dif-
ferences were less pronounced after correction,
they were still present. Van Loon et al.[55] did not
observe differences in exogenous CHO oxidation
rates when trained cyclists exercised at 38 or 55%
V.
O2max. It is therefore possible that lower exoge-
nous CHO oxidation rates are only observed at very
low exercise intensities when the reliance on CHO
as an energy source is minimal. In this situation,
part of the ingested CHO may be directed towardsnon-oxidative glucose disposal (storage in the liver
or muscle) rather than towards oxidation. Studies
with CHO ingestion during intermittent exercise
have suggested that glycogen can be resynthesised
during low intensity exercise.[56]
It seems fair to conclude that at exercise inten-
sities below 50 to 60% V.
O2max, exogenous CHO
oxidation will increase with increasing total CHO
oxidation rates, whereas above approximately 50
to 60% V.
O2max
, oxidation rates will not usually
increase further.
3.2 Muscle Glycogen
Although determinants of exogenous CHO ox-
idation have been intensively investigated for al-
most 30 years, the effect of pre-exercise glycogen
levels on exogenous CHO oxidation during exer-
cise are still largely unknown and studies have pro-
duced different results. In a study conducted by
Ravussin et al.,[57] the oxidation rate of exogenousglucose was studied in individuals with normal and
low glycogen levels. The 2 groups were observed
for 2 hours at 40% V.
O2max on a cycle ergometer, 1
hour after ingestion of 100g of glucose. The oxida-
tion rates of the ingested CHOs were similar: 41g
in the group with normal glycogen availability and
38g in the group with reduced glycogen availabil-
ity. However, the study had no cross-over design,
which may have influenced the results. Although
the absolute rates of exogenous CHO were not dif-
ferent between groups, due to the 20% higher en-
ergy expenditure observed in the group of glycogen-
depleted individuals, exogenous CHO oxidation
provided only 16% of the energy yield versus 20%in the group with normal glycogen levels. Thus, the
lower glycogen level was associated with a decreased
contribution of exogenous CHO oxidation to en-
ergy expenditure during moderate intensity exercise.
More recently, Jeukendrup et al.[45] manipulated
pre-exercise glycogen levels by glycogen lowering
exercise in combination with CHO restriction (LG
trial) or rest in combination with CHO loading (HG
trial). In a randomised cross-over design, volun-
teers received an average of 127g glucose during120 minutes of exercise at 57% V. O2max. In contrast
to the conclusion of Ravussin et al.,[57] it was found
that exogenous glucose oxidation was 28% lower
in the LG trial compared with the HG trial: 36g of
glucose was oxidised during 60 to 120 minutes of
exercise during LG, whereas 50g was oxidised with
HG. Péronnet et al.[58] studied the effect of endog-
enous CHO availability, after high and low CHO
diets, on the oxidation of exogenous CHOs during
120 minutes of exercise at 64% V
.
O2max. Volunteersrelied more on exogenous CHO oxidation after the
low CHO diet, when glycogen availability was pre-
sumably low, than after the high CHO diet, when
glycogen availability was presumably high. Between
40 and 80 minutes of the exercise period, exoge-
nous CHO oxidation was significantly higher after
the low CHO diet compared with the high CHO
diet (0.63 vs 0.52 g/min, respectively). These re-
sults are inconsistent with the results of Ravussin
et al.[57] and Jeukendrup et al.,[45] and are likelyattributed to differences in experimental conditions
of exercise and the amounts of CHO ingestion.
Oxidation of Carbohydrate Feedings During Exercise 417
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 12/18
Because of the higher relative workload in the
study of Péronnet et al.[58] (64 vs 40 and 57% V.
O2max
in the studies by Ravussin et al.[57] and Jeukendrup
et al.,[45] respectively) and the larger amount of glu-
cose ingested (200 vs 100 and 127g in the studies
by Ravussin et al.[57] and Jeukendrup et al.,[45] re-
spectively) volunteers relied more on CHO oxida-
tion and less on fat oxidation after both diets. The
increased reliance on CHO oxidation at this higher
exercise intensity, when glycogen levels are reduced,
might explain why exogenous CHO oxidation was
higher.Another explanation could be that the extent to
which glycogen levels were reduced was responsi-
ble for the different findings between the studies.
Although none of the above studies measured gly-
cogen levels, the glycogen depletion protocol used
in the study by Jeukendrup et al.[45] has previously
been shown to result in very low muscle glycogen
levels (<140 mmol/kg dry weight),[59] and to lead
to low plasma insulin levels and high plasma free
fatty acids. The 2 to 3 times higher plasma free fatty
acid level and the lower plasma insulin level when
glycogen levels were low[45,57] could have reduced
plasma glucose uptake and oxidation.[60] Péronnet
et al.[58] found a smaller difference in free fatty acid
levels between their experimental trials, whereas
insulin levels were not different. This was possibly
due to the moderate glycogen depletion regimen
applied in their study, which might therefore ex-
plain why exogenous CHO oxidation did not de-crease when glycogen availability was low.
The effect of muscle glycogen on exogenous CHO
oxidation per se is unknown at present. Studies have
attempted to manipulate muscle glycogen stores by
altering the dietary CHO intake and employing ex-
ercise programmes but, by doing so, other vari-
ables (i.e hormonal changes, high free fatty acid
levels) have been changed as well and these changes
may have been responsible for the variable results
in different studies. More studies are required toelucidate the role of muscle glycogen on the oxida-
tion rate of ingested CHO.
3.3 Training
Endurance training has a marked effect on sub-
strate utilisation and generally results in a shift from
CHO towards fat metabolism. There is a decreased
reliance on CHO metabolism after training at the
same absolute workload.[61-64] However, some con-
troversy still exists regarding whether the reliance
on CHO as a fuel is also decreased at the same
relative exercise intensity. Several studies suggest
that even though the exercise after training is per-
formed at the same relative intensity (and thus a
higher absolute intensity), there is a decreased re-liance on blood glucose and muscle glycogen.[63-65]
However, some studies did not find a change in
glucose uptake after training when compared at the
same relative exercise intensity,[61,62] although
plasma glucose oxidation was decreased.[62] Train-
ing induces several adaptations at the muscular level
including an increased GLUT-4 content,[66] increased
insulin action[67] and an increased capillary bed.
All these adaptations would favour glucose uptake
and could possibly alter the handling of blood glu-cose and thus of exogenous glucose.
A few studies have investigated the effects of
training (or training status) on exogenous CHO ox-
idation rates.[24,55,68,69] In an early study by Krzen-
towski et al.,[68] volunteers trained for 6 weeks and
substrate utilisation was measured at the same ab-
solute exercise intensity before and after the train-
ing programme. The authors concluded that exog-
enous CHO oxidation was increased by 17% after
training. However, the results seem difficult to in-
terpret. Firstly, the V. O2max of the participants was
increased by an unphysiological amount (29%). Sec-
ondly, in contrast to the literature and despite the
improved aerobic capacity after training, no differ-
ence in total CHO and fat oxidation was observed.
More recently, van Loon et al.[55] reported that the
contribution of CHO to energy expenditure was
lower in well trained cyclists compared with healthy
untrained controls at the same absolute intensity.
The reduction in CHO oxidation was due to a re-
duction in muscle glycogen oxidation (0.10 and 0.75g/min) and endogenous glucose production (0.20
and 0.13 g/min), respectively (fig. 4). However, de-
418 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 13/18
spite these differences in substrate utilisation, ex-
ogenous glucose oxidation rates were unaffected
(0.7 g/min in trained and untrained cyclists).
Burelle et al.[24] also compared exogenous CHO
oxidation in trained and sedentary individuals dur-
ing exercise at the same absolute workload. Volun-
teers cycled for 90 minutes at 140W and received
100g 13C-enriched glucose during exercise. Sur-
prisingly, no differences were found in total CHO
and fat oxidation between trained and untrained
volunteers. However, although blood glucose oxi-
dation rates were not different, exogenous CHO
oxidation rates were higher in trained individuals.
Differences in the results of van Loon et al.[55] and
Burelle et al.[24] may also be caused by differences
in the experimental protocol (amount of CHO in-
gested, exercise intensity and timing of feedings).
For instance, Burelle et al.[24] gave their first feed-
ing (25g glucose) 30 minutes before exercise, which
means that glycogen stores may have been pre-la-
beled, particularly in the trained volunteers who
are more insulin sensitive and will have an increased
muscle glucose uptake after an oral glucose load.
This would result in an overestimation of exoge-
nous CHO oxidation rates during exercise in the
trained volunteers. If trained individuals stored 20%
more of the initial glucose gift (5g) than the un-
trained individuals, this could explain the entire
observed difference in exogenous CHO oxidation.
This seems a reasonable assumption since it has
been shown that post-exercise, glycogen resynthe-
sis can be twice as fast after endurance training.[71]
Three studies have investigated the effects of exogenous CHO oxidation during exercise at the
same relative exercise intensity.[24,55,69] Two stud-
ies showed no effect of training on the oxidation of
ingested CHO, whereas Burelle et al.[24] reported
higher oxidation rates in trained compared with un-
trained individuals at 68% V.
O2max.
The difference between these studies may be
related to the fact that the latter study showed an
increase in total CHO oxidation in trained individ-
uals, whereas no changes in CHO oxidation werefound in the studies by van Loon et al.[55] and Jeu-
kendrup et al.[69] Burelle et al.[24] also reported in-
creased muscle glycogen use, which is in contrast
with most of the literature showing either no changeor a decreased intramuscular glycogen breakdown
after training at the same relative intensity.[61,62]
In section 4 of this review we will discuss how
maximal exogenous CHO oxidation rates are reg-
ulated. This concept, which is based on the premise
that the liver and intestine play a crucial role in
glucose homeostasis, describes that a maximal glu-
cose output by the liver controls maximal exogenous
CHO oxidation rates.This concept would predict that
exogenous CHO oxidation rates are similar in trainedand untrained individuals at the same absolute and
relative workload. Higher exogenous CHO oxida-
tion rates in trained individuals would suggest a
superior absorption or more exogenous glucose
would escape from the liver. There are currently no
data available to support these potential differences
between trained and untrained individuals.
4. Limitations of ExogenousCHO Oxidation
As depicted in figure 3, exogenous CHO oxida-
tion seems to be limited to rates of 1.0 to 1.1 g/min.
0
0.2
0.4
0.6
0.8
1.0
1.2
R a g l u c o s e ( g / m i n )
Fast LO-GLU HI-GLU
Glucose from liverGlucose from feedings
Fig. 4. Glucose delivery to the blood from the liver and gastro-
intestinal tract (feedings) during exercise. During a fast, no glu-cose feedings were provided and all glucose appearing in theblood stream was derived from the liver. When a small amountof glucose was provided (LO-GLU) the total delivery of carbo-hydrate (CHO) increased but the contribution of liver glucosedeclined.When largeamounts ofCHOwere ingested (HI-GLU),the total delivery of CHO was further increased. Liver glucoseoutputwasnegligible andallglucose wasderived from thefeed-ings. Ra = rate of appearance (adapted from Jeukendrup etal.,[70] with permission).
Oxidation of Carbohydrate Feedings During Exercise 419
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 14/18
This finding seems supported by the vast majority
of studies using either radioactive[3,36] or sta-ble[5,37,45,53,69] isotopes to quantify exogenous CHO
oxidation during exercise. One of the limiting fac-
tors could be gastric emptying. However, Rehrer et
al.[31] showed that gastric emptying is unlikely to
affect exogenous CHO oxidation rates. In their study,
participants ingested 220g glucose during 80 min-
utes of exercise at 70% V.
O2max. After 80 minutes,
100g of glucose was present in the stomach and
thus 120g was delivered to the duodenum. How-
ever, at 80 minutes only 38g of the ingested CHOwas oxidised. These results were later confirmed
by others using slightly different exercise protocols
and feeding schedules.[27,38] Because in these studies
only 32 to 48% of the CHO delivered to the intes-
tine was oxidised, it was concluded that gastric emp-
tying was not limiting exogenous CHO oxidation.
Another potential rate-limiting factor is intesti-
nal absorption of CHO. Studies using a triple lu-
men technique have measured duodenojejunal glu-
cose absorption and estimated whole body intestinal
absorption rates of a 6% glucose-electrolyte solu-
tion.[72] It was estimated that the maximal absorp-
tion rate of the intestine ranged from 1.3 to 1.7
g/min. Recent studies using stable isotope method-
ology have tried to quantify the appearance of glu-
cose from the gut into the systemic circulation (Ra
gut). When a low dose of CHO was ingested during
exercise, the rate of appearance of glucose from the
gut equaled the rate of CHO ingestion during the
second hour (both 0.43 g/min).[5] This implies that
at low ingestion rates absorption is not limiting and
there is no net storage of glucose in the liver. In-
stead, all ingested glucose appears in the blood
stream. It was also found that the glucose appearing
in the bloodstream was taken up at similar rates to
its Ra and 90 to 95% of this glucose was oxidised
during exercise. When a larger dose of CHO was
ingested (3 g/min), Ra gut was one-third the rate of
CHO ingestion (0.96 to 1.04 g/min). Thus, only
part of the ingested CHO entered the systemic cir-
culation. However,the glucose appearing in the blood
was taken up and 90 to 95% was oxidised. It was
therefore concluded that entrance into the systemic
circulation is a limiting factor for exogenous glu-
cose oxidation, rather than intramuscular factors.This is further supported by glucose infusion stud-
ies. Hawley et al.[73] bypassed both intestinal ab-
sorption and hepatic glucose uptake by infusing
glucose in volunteers exercising at 70% V.
O2max.
When large amounts of glucose were infused and
volunteers were hyperglycemic (10 mmol/L), it was
possible to raise blood glucose oxidation rates above
1 g/min.
These studies provide evidence that exogenous
CHO oxidation is limited by the rate of digestion,absorption and subsequent transport of glucose into
the systemic circulation rather than the rate of up-
>2.0 g/min
0-1.0 g/min1.0 g/min
1.0 g/min
1.0 g/min
1.0 g/min
CO2
1.2-1.7 g/min
Gastrointestinal tract
? g/min
Glucogen
Glucose
Liver
Blood
Muscle
CHOingestion rate
Fig. 5. Regulation of hepatic glucose production and the controlof glucose appearance into the systemic circulation with carbo-hydrate (CHO) ingestion. CHO can be ingested at fairly highrates up to about 3 g/min before causing gastrointestinal symp-toms. This CHO will then be digested and absorbed at a rate of1.2 to 1.7 g/min, which has been suggested to be the maximalabsorptive capacity of the intestine. CHOwill then enter the liver
through the portal vein. Amaximum of 1 g/min will escape fromthe liver and enter the bloodstream. The CHO entering thebloodstream may be derived from ingested CHO (in extremeconditions 1 g/min), can be derived from the liver (glycogenoly-sis and gluconeogenesis) at a rate of 0 to 1 g/min, or can bederived from a combination of both. Whether glucose from in-gested CHO can be directed towards liver glycogen during ex-ercise has not been established. Glucose will be taken up bythe muscle and can be oxidised at virtually similar rates. Thisgraph was composed with results from various studies.[5,8,72]
420 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 15/18
take and oxidation by the muscle. The maximal
rates of intestinal absorption seem to be slightly in
excess of the maximal appearance of glucose from
the gut into the bloodstream.[5] It is important to
note that during high intensity exercise, a reduced
mesenteric blood flow may result in a decreased
absorption of glucose and water[50] and hence a low
Ra gut relative to the rate of ingestion. However,
this may only apply to exercise at very high inten-
sities.[50] Taken together, this suggests that intesti-
nal absorption is a factor contributing to the limi-
tation to oxidise ingested CHO at rates higher than
1.0 to 1.1 g/min, but it may not be the sole factor.The liver may play an additional important role.
Hepatic glucose output is highly regulated and it is
possible that the glucose output derived from the
intestine and from hepatic glycogenolysis and glu-
coneogenesis will not exceed 1.0 to 1.1 g/min even
though the absorption is slightly in excess of this
rate (fig. 5). If supply from the intestine is too large
(>1.0 g/min), glycogenesis may be activated in the
liver. Recent findings by Jeukendrup et al.[5] support
the role of the liver. Ingestion of small CHO dosesduring exercise suppressed endogenous (mainly
liver) glucose production (fig. 6). Very high rates
of CHO intake (3 g/min) completely suppressed en-
dogenous glucose production. However, despite
these high rates of ingestion the total Ra did not
exceed 1 g/min. Assuming that CHO was absorbed
at a rate slightly in excess of 1 g/min, this would
suggest glycogenesis in the liver during exercise.
The hormonal profile as observed after ingesting
large amounts of glucose during exercise (higher
plasma insulin and lower plasma glucagon levels)
would support glycogenesis by activating hepatic
glycogen synthase activity,[74] GLUT-2 transporter
expression,[75] increased glucose kinase expres-
sion[76] or liver cell swelling.[77]
5. Directions for Future Research
Although many advances have been made in the
last few years, several questions remain to be an-
swered. One of the intriguing questions is the fateof excess amounts of ingested CHO. Recent stud-
ies have revealed that glucose, when ingested at
very high rates, may not enter the systemic circu-
lation at these high rates. The relative role of ab-
sorption and the liver retaining glucose remain to
be determined. With the recent developments in
nuclear magnetic resonance spectroscopy it should
be possible to more accurately determine the role
of the liver.[78]
Another question, which may be beyond the scope
of this review, is related to the performance effects
of glucose feedings during exercise. It has been
shown that CHO feeding during exercise can im-
prove performance when the exercise duration is
only about 60 minutes.[1,79,80] It was calculated that
by this time only 5 to 15g of the ingested glucosecould have been oxidised,[1] and it is therefore un-
likely that this small contribution causes the rela-
tively large effect on performance. However, alter-
native mechanisms are currently unknown. Other
questions, which may have important practical im-
plications, are related to exercise in extreme con-
ditions (heat, altitude). Formulated guidelines are
primarily based on studies in thermoneutral and
sea level conditions.
However, it is possible that these guidelines arenot suitable for exercise in the heat or at high alti-
tude. Both conditions have been shown to result in
*
*
*
*
0
1
2
3
S u b s t r a t e u t i l i s a t i o n ( g / m i n )
T1 UT T2
Fat
Muscle glycogen
Hepatic glucose outputExogenous carbohydrate
Fig. 6. Substrate utilisation in untrained (UT) and trained indi-viduals at thesame absolute (T1) andrelativeexercise intensity(T2). UT and T1 is exercise at 148W [55 and 38% maximaloxygenuptake(V
.O2max), respectively] andT2 isexerciseat200W
(55% V.O2max).
Oxidation of Carbohydrate Feedings During Exercise 421
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 16/18
marked changes in substrate utilisation at rest and
during exercise.[81,82] Prolonged exercise in the heat
will lead to distribution of blood to the skin to allow
for evaporative cooling.[83] As a consequence, blood
flow to other organs such as the liver, kidney, inac-
tive tissue and the gut will be reduced.[84,85] A re-
duced blood flow to the gut may impair gut func-
tion, especially during ultra-endurance exercise, as
recently suggested.[70] Absorption of CHO(and other
nutrients) may be impaired, which may finally lead
to a reduced oxidation rate of ingested CHO. This
may also partly explain why CHO feeding during
exercise in the heat has no effect on endurance per-formance.[86-88] Future studies are therefore needed
to investigate the effect of heat on exogenous CHO
oxidation during exercise to prevent needless in-
take of excess CHO, which can not be absorbed and
functions as a potential risk factor for gastrointes-
tinal problems.
6. Practical Implications, Guidelinesand Conclusion
The above findings have some practical appli-
cations, some of which are summarised here:
• Athletes should ensure a CHO intake of approx-
imately 1.0 to 1.1 g/min (60 to 70 g/h).
• The bulk of ingested CHO should be a rapidly
oxidisable CHO: glucose, maltose, sucrose,
maltodextrins or amylopectin (soluble starch).
• Small amounts of fructose or sucrose may be
added to a glucose or maltodextrin solution (up
to 20% of the total CHO content may be fruc-
tose).
• Untrained individuals may benefit as much as
trained athletes since exogenous CHO oxidation
rates and effects on performance appear to be
similar.
Based on a relatively large number of studies,
guidelines for CHO feeding during exercise are now
quite detailed. However, future research should elu-
cidate whether these guidelines apply to all condi-
tions (altitude, heat, cold) and whether combination
of different CHO can lead to exogenous CHO ox-idation rates higher than 1 g/min. If this is the case,
guidelines may have to be adjusted accordingly.
Acknowledgements
The authors want to acknowledge the invaluable supportfrom and fruitful discussions with Dr Anton Wagenmakers,
Professor Wim Saris and Dr Fred Brouns at Maastricht
University in The Netherlands. We also want to thank Pro-
fessor Mike Gleeson for his careful and critical reviewing of
this manuscript.
References1. Jeukendrup AE, BrounsF,WagenmakersAJM, et al.Carbohydrate
feedings improve 1 h time trial cycling performance. Int J
Sports Med 1997; 18: 125-9
2. Coyle EF, Coggan AR, Hemmert MK, et al. Muscle glycogen
utilization during prolonged strenuous exercise when fed car-bohydrate. J Appl Physiol 1986; 61: 165-72
3. Bosch AN, Dennis SC, Noakes TD. Influence of carbohydrateingestion on fuel substrate turnover and oxidation during pro-
longed exercise. J Appl Physiol 1994; 76: 2364-72
4. McConnell G, Fabris S, Proietto J, et al. Effect of carbohydrate
ingestion on glucose kinetics during exercise. J Appl Physiol1994; 77 (3): 1537-41
5. Jeukendrup AE, Wagenmakers AJ, Stegen JH, et al. Carbohydrateingestion can completely suppress endogenous glucose pro-
duction during exercise. Am J Physiol 1999; 276: E672-83
6. Tsintzas OK, Williams C, Boobis L, et al. Carbohydrate ingestionand single muscle fiber glycogen metabolism during prolongedrunning in men. J Appl Physiol 1996; 81: 801-9
7. Tsintzas OK, Williams C, Boobis L, et al. Carbohydrate ingestion
and glycogen utilisation in different muscle fibre types in man.J Physiol 1995; 489: 243-50
8. Jeukendrup AE, Raben A, Gijsen A, et al. Glucose kineticsduringprolonged exercise in highly trained human subjects: effect of glucose ingestion. J Physiol (Lond) 1999; 515: 579-89
9. Tsintzas K, Williams C. Human muscle glycogen metabolismduring exercise: effect of carbohydrate supplementation. Sports
Med 1998; 25: 7-23
10. Costill DL, Bennett A, Branam G, et al. Glucose ingestion atrest and during prolonged exercise. J Appl Physiol 1973; 34:764-9
11. Beckers EJ, HallidayD, Wagenmakers AJ. Glucosemetabolism
and radioactive labeling: what are the real dangers? Med SciSports Exerc 1994; 26: 1316-8
12. Robert JJ, Koziet J, Chauvet D, et al. Use of 13C-labeled glucosefor estimating glucose oxidation: some design considerations.
J Appl Physiol 1987; 63: 1725-32
13. Sidossis LS, Coggan AR, Gastaldelli A, et al. A new correctionfactor for usein tracer estimationsof plasmafatty acidoxidation.Am J Physiol 1995; 269: E649-56
14. Jeukendrup AE, Wagenmakers AJM, Brouns F, et al. Effects of carbohydrate (CHO) and fat supplementation on CHO meta-
bolism during prolonged exercise. Metabolism1996;45: 915-21
15. Sidossis LS, Coggan AR, Gastadelli A, et al. Pathways of free
fatty acid oxidation in human subjects: implications for tracerstudies. J Clin Invest 1995; 95: 278-84
16. Schrauwen P, van Aggel-Leijssen DP, van Marken LichtenbeltWD, et al. Validation of the [1,2-13C]acetate recovery factor
for correction of [U-13C]palmitate oxidation rates in humans.
J Physiol (Lond) 1998; 513: 215-2317. Péronnet F, Massicotte D, Brisson G, et al. Use of 13C substrates
for metabolic studies in exercise: methodological considera-tions. J Appl Physiol 1990; 69: 1047-52
422 Jeukendrup & Jentjens
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 17/18
18. Wagenmakers AJM, Rehrer NJ, Brouns F, et al. Breath 13CO2
background enrichment at rest and during exercise: diet re-
lated differences between Europe and America. J Appl Physiol1993; 74: 2353-7
19. Jandrain BJ, Pirnay F, LaCroix M, et al. Effect of osmolality onavailability of glucose ingested during prolonged exercise in
humans. J Appl Physiol 1989; 67: 76-82
20. Krzentowski G, Jandrain B, Pirnay F, et al. Availability of glucose
given orally during exercise. J Appl Physiol 1984; 56: 315-20
21. Pirnay F, Lacroix M, MosoraF,et al. Effect of glucose ingestionon energy substrate utilization during prolonged exercise inman. Eur J Appl Physiol 1977; 36: 1620-4
22. Pirnay F, Lacroix M, Mosora F, et al. Glucose oxidation during
prolonged exercise evaluated with naturally labelled [13C] glu-cose. J Appl Physiol 1977; 43: 258-61
23. Guezennec CY, Satabin P, Duforez F, et al. Oxidation of cornstarch, glucose, and fructose ingested before exercise. Med
Sci Sports Exerc 1989; 21: 45-5024. Burelle Y, Péronnet F, Charpentier S, et al. Oxidation of an oral
[13C]glucose load at rest and prolonged exercise in trainedand sedentary subjects. J Appl Physiol 1999; 86: 52-60
25. Massicotte D, Péronnet F, Brisson G, et al. Oxidation of exoge-nous carbohydrateduringprolonged exercise in fed and fasted
conditions. Int J Sports Med 1990; 11: 253-8
26. Massicotte D, Péronnet F, Brisson G, et al. Oxidation of a glucosepolymer during exercise: comparison with glucose and fruc-tose. J Appl Physiol 1989; 66: 179-83
27. Moodley D, Noakes TD,Bosch AN,et al.Oxidation ofexogenouscarbohydrate during prolonged exercise: the effects of the
carbohydrate type and its concentration. Eur J Appl Physiol1992; 64: 328-34
28. Massicotte D, Péronnet F, Adopo E, et al. Effect of metabolicrate on the oxidation of ingested glucose and fructose during
exercise. Int J Sports Med 1994; 15: 177-80
29. Rehrer NJ, Brouns F, Beckers EJ, et al. Gastric emptying withrepeated drinking during running and bicycling. Int J SportsMed 1990; 11: 238-43
30. Noakes TD, Rehrer NJ, Maughan RJ. The importance of volumein regulating gastric emptying. Med Sci Sports Exerc 1991;
23: 307-13
31. Rehrer NJ, Wagenmakers AJM, Beckers EJ, et al. Gastric emp-tying, absorption and carbohydrate oxidation during prolonged
exercise. J Appl Physiol 1992; 72: 468-75
32. McConell G, Kloot K, Hargreaves M. Effect of timing of carbo-
hydrate ingestion on endurance exercise performance. MedSci Sports Exerc 1996; 28 (10): 1300-4
33. Massicotte D, Péronnet F, Allah C, et al. Metabolic response to[13C] glucose and [13C] fructose ingestion during exercise. J
Appl Physiol 1986; 61: 1180-4
34. Décombaz J, Sartori D, Arnaud M-J, et al. Oxidation and meta-
bolic effects of fructose and glucose ingested before exercise.Int J Sports Med 1985; 6: 282-6
35. Leijssen DPC, Saris WHM, Jeukendrup AE, et al. Oxidation of orally ingested [13C]-glucose and [13C]-galactose during ex-
ercise. J Appl Physiol 1995; 79: 720-5
36. Hawley JA, DennisSC, Nowitz A, et al. Exogenous carbohydrate
oxidation from maltose and glucose ingested during prolongedexercise. Eur J Appl Physiol 1992; 64: 523-7
37. Wagenmakers AJM, Brouns F, Saris WHM, et al. Oxidationrates of orally ingested carbohydrates duringprolonged exercise
in man. J Appl Physiol 1993; 75: 2774-8038. Saris WHM, Goodpaster BH, Jeukendrup AE, et al. Exogenous
carbohydrate oxidation from different carbohydrate sourcesduring exercise. J Appl Physiol 1993; 75: 2168-72
39. Okano G, TakedaH, Morita I, etal. Effect ofpre-exercise fructoseingestion on endurance performance in fed man. Med Sci
Sports Exerc 1988; 20: 105-940. Koivisto VA, Karonen S-L, Nikkila EA. Carbohydrate ingestionbefore exercise: comparison of glucose, fructose and placebo.
J Appl Physiol 1981; 51: 783-7
41. Samols E, Dormandy TL. Insulin response to fructose and ga-lactose. Lancet 1963; I: 478-9
42. Jandrain BJ, Pallikarakis N, Normand S, et al. Fructose utilizationduring exercise in men: rapid conversion of ingested fructose
to circulating glucose. J Appl Physiol 1993; 74: 2146-54
43. Burelle Y, Péronnet F, Massicotte D, et al. Oxidation of 13C-glucose and 13C-fructose ingested as a preexercise meal: effect
of carbohydrate ingestion during exercise. Int J Sport Nutr1997; 7: 117-27
44. Adopo E, Péronnet F, Massicotte D, et al. Respective oxidation
of exogenous glucose and fructose given in the same drink during exercise. J Appl Physiol 1994; 76: 1014-9
45. Jeukendrup AE, Borghouts L, Saris WHM, et al. Reduced oxi-dation rates of orally ingested glucose during exercise afterlow CHO intake and low muscle glycogen. J Appl Physiol1996; 81: 1952-7
46. HawleyJA, DennisSC, LaidlerBJ, et al. High rates of exogenous
carbohydrate oxidation from starch ingested during prolongedexercise. J Appl Physiol 1991; 71: 1801-6
47. Shi X, SummersR, Schedl H, et al. Effectsof carbohydrate type
and concentration and solution osmolality on water absorption.Med Sci Sports Exerc 1995; 27: 1607-15
48. Brouns F, Senden J, Beckers EJ, et al. Osmolarity does not
affect the gastric emptying rate of oral rehydration solutions.J Parent Enter Nutr 1995; 19: 403-6
49. Shi X, Gisolfi CV. Fluid and carbohydrate replacement during
intermittent exercise. Sports Med 1998; 25: 157-72
50. Brouns F, Beckers E. Is the gut an athletic organ? Digestion,absorption and exercise. Sports Med 1993; 15: 242-57
51. Pallikarakis N, Jandrain B, Pirnay F, et al. Remarkable metabolicavailability of oral glucose during long-duration exercise in
humans. J Appl Physiol 1986; 60: 1035-42
52. Romijn JA, Coyle EF, Sidossis LS, et al. Regulation of endog-enous fat and carbohydrate metabolism in relation to exercise
intensity. Am J Physiol 1993; 265: E380-91
53. Pirnay F, Crielaard JM, Pallikarakis N, et al. Fate of exogenousglucose during exercise of different intensities in humans. JAppl Physiol 1982; 53: 1620-4
54. Pirnay F, Scheen AJ, Gautier JF, et al. Exogenous glucose oxi-
dation during exercise in relation to the power output. Int JSports Med 1995; 16: 456-60
55. van Loon LJ, Jeukendrup AE, Saris WH, et al. Effect of trainingstatus on fuel selection during submaximal exercise with glu-cose ingestion. J Appl Physiol 1999; 87: 1413-20
56. Kuipers H, Saris WHM, Brouns F, et al. Glycogen synthesis
during exercise and rest with carbohydrate feeding in malesand females. Int J Sports Med 1989; 10: S63-7
57. Ravussin E, Pahud P, Dorner A, et al. Substrate utilization duringprolonged exercise preceded by ingestion of 13C-glucose inglycogen depleted and control subjects. Pflügers Arch 1979;
382: 197-202
58. Péronnet F, Rheaume N, Lavoie C, et al. Oral [13C]glucoseoxidation during prolonged exercise after high- and low-carbo-
hydrate diets. J Appl Physiol 1998; 85 (2): 723-3059. Kuipers H, Keizer HA, Brouns F, et al. Carbohydrate feeding
and glycogen synthesis during exercisein man. Pflügers Arch1987; 410: 652-6
Oxidation of Carbohydrate Feedings During Exercise 423
Adis International Limited. All rights reserved. Sports Med 2000 Jun; 29 (6)
7/31/2019 Carbohydrate Feedings During Exercise
http://slidepdf.com/reader/full/carbohydrate-feedings-during-exercise 18/18
60. Hargreaves M, Kiens B, Richter EA. Effect of increased plasmafree fatty acid concentrations on muscle metabolism in exer-
cising men. J Appl Physiol 1991; 70: 194-20161. Bergman BC,Butterfield GE, Wolfel EE,et al. Muscle net glucoseuptake and glucose kinetics after endurance training in men.
Am J Physiol 1999; 277: E81-92
62. FriedlanderAL, CasazzaGA, HorningMA, etal. Training inducedalterations of glucose flux in men. J Appl Physiol 1997; 82:1360-9
63. Coggan AR, Kohrt WM,Spina RJ, et al.Plasmaglucosekinetics
during exercise in subjects with high and low lactate thresholds.J Appl Physiol 1992; 73: 1873-80
64. Coggan AR, Raguso CA, Williams BD, et al. Glucose kinetics
during high-intensity exercise in endurance-trained and un-trained humans. J Appl Physiol 1995; 78: 1203-7
65. Jansson E, Kaijser L. Substrate utilization and enzymes in skeletalmuscle of extremely endurance-trained men. J Appl Physiol
1987; 62: 999-1005
66. Richter EA, Kiens B, Saltin B, et al. Skeletal muscle glucoseuptake during dynamic exercise in humans: role of muscle
mass. Am J Physiol 1988; 254: E555-61
67. Dela F, Mikines KJ, von Linstow M, et al. Effect of training oninsulin-mediated glucoseuptake in human muscle.Am J Physiol
1992; 263: E1134-43
68. Krzentowski GB, Pirnay F, Luyckx AS, et al. Effect of physicaltraining on utilization of a glucose load given orally duringexercise. Am J Physiol 1984; 246: E412-7
69. Jeukendrup AE, Mensink M, Saris WHM, et al. Exogenous glu-
cose oxidation during exercise in endurance-trained and un-trained subjects. J Appl Physiol 1997; 82: 835-40
70. Jeukendrup AE, Vet-Joop K, Sturk A, et al. Relationship between
gastro-intestinal complaints and endotoxaemia, cytokine re-lease and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci (Colch) 2000;98: 47-55
71. Greiwe JS, Hickner RC, Hansen PA, et al. Effects of enduranceexercise training on muscle glycogen accumulation in humans.
J Appl Physiol 1999; 87: 222-6
72. Duchman SM, Ryan AJ,Schedl HP, et al. Upper limit forintestinalabsorption of a dilute glucose solution in men at rest. Med Sci
Sports Exerc 1997; 29: 482-8
73. Hawley JA, Bosch AN, Weltan SM, et al. Glucose kinetics duringprolonged exercise in euglycemic and hyperglycemic subjects.Pflügers Arch 1994; 426: 378-86
74. Mandarino LJ, Consoli A, Jain A, et al. Differential regulation
of intracellular glucose metabolism by glucose and insulin inhuman muscle. Am J Physiol 1993; 265: E898-905
75. Postic C, Burcelin R, Rencurel F, et al. Evidence for a transient
inhibitory effect of insulin on GLUT2 expression in the liver:studies in vivo and in vitro. Biochem J 1993; 293: 119-24
76. Iynedjian PB, Gjinovci A, Renold AE. Stimulation by insulin of
glucokinase gene transcription in liver of diabetic rats. J Biol
Chem 1988; 263: 740-477. Al-Habori M, Peak M, Thomas TH, et al. The role of cell swelling
in the stimulation of glycogen synthesis by insulin. Biochem
J 1992; 282: 789-96
78. Casey A, Mann R, Banister K, et al. Effect of carbohydrate
ingestion on glycogen resynthesis in human liver and skeletal
muscle, measured by (13)C MRS. Am J Physiol Endocrinol
Metab 2000; 278 (1): E65-75
79. Anantaraman R, Carmines AA, Gaesser GA, et al. Effects of
carbohydrate supplementation on performance during 1 h of
high intensity exercise. Int J Sports Med 1995; 16: 461-5
80. Below PR, Mora-Rodríguez R, Gonzáles Alonso J, et al. Fluid
and carbohydrate ingestion independentlyimproveperformance
during 1 h of intense exercise. Med Sci Sports Exerc 1995;
27: 200-1081. Febbraio MA, Snow RJ, Hargreaves M, et al. Muscle metabolism
during exercise and heat stress in trained men: effect of accli-
mation. J Appl Physiol 1994; 76: 589-97
82. Hargreaves M, Angus D, Howlett K, et al. Effect of heat stress
on glucose kinetics during exercise. J Appl Physiol 1996; 81:
1594-7
83. Johnson JM, Park MK. Reflex control of skin blood flow by
skin temperature: role of core temperature. J Appl Physiol
1979; 47: 1188-93
84. Williams JH, Mager M, Jacobson ED. Relationship of mesenteric
blood flow to intestinal absorption of carbohydrates. J Lab
Clin Med 1964; 63: 853-63
85. Clausen JP. Effect of physical training on cardiovascular adjust-
ments to exercise in man. Physiol Rev 1977; 57: 779-81586. Febbraio M, Murton P, Selig S, et al. Effect of CHO ingestion
on exercise metabolism and performance in different ambient
temperatures. Med Sci Sports Exerc 1996; 28: 1380-7
87. Davis JM, Lamb DR, Pate RR, et al. Carbohydrate-electrolyte
drinks: effects on endurance cycling in the heat. Am J Clin
Nutr 1988; 48: 1023-30
88. Millard-Stafford M, Sparling PB, Rosskopf LB, et al. Carbohy-
drate-electrolyte replacement during a simulated triathlon in
the heat. Med Sci Sports Exerc 1990; 22: 621-8
Correspondence and offprints: Dr Asker E. Jeukendrup, Hu-
man Performance Laboratory, School of Sport and Exercise
Sciences, University of Birmingham, Edgbaston, Birming-
ham B15 2TT, England.E-mail: [email protected]
424 Jeukendrup & Jentjens
Adi I t ti l Li it d All i ht d S t M d 2000 J 29 (6)