carbohydrate feedings during exercise

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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

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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)



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




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





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.





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.





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-


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





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.





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





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.





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.





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-





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).





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-


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]





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).





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.

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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]


Adi I t ti l Li it d All i ht d S t M d 2000 J 29 (6)

carbohydrate feedings during exercise

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