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Roy L. P. G. Jentjens, Luke Moseley, Rosemary H. Waring, Leslie K.

Harding and
Asker E. Jeukendrup
J Appl Physiol 96:1277-1284, 2004. First published Dec 2, 2003; doi:10.1152/japplphysiol.00974.2003

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J Appl Physiol 96: 1277–1284, 2004.
First published December 2, 2003; 10.1152/japplphysiol.00974.2003.

Oxidation of combined ingestion of glucose and fructose during exercise


Roy L. P. G. Jentjens,1 Luke Moseley,1 Rosemary H. Waring,2 Leslie K. Harding,3 and
Asker E. Jeukendrup1
1
Human Performance Laboratory, School of Sport and Exercise Sciences, and 2School
of Biosciences, University of Birmingham, Birmingham B15 2TT; and 3Physics and
Nuclear Medicine Department, City Hospital, Birmingham B18 7QH, United Kingdom
Submitted 9 September 2003; accepted in final form 3 November 2003

Jentjens, Roy L. P. G., Luke Moseley, Rosemary H. Waring, ingested. Although direct evidence is lacking, it has been
Leslie K. Harding, and Asker E. Jeukendrup. Oxidation of com- suggested that the absorption capacity of glucose in the intes-
bined ingestion of glucose and fructose during exercise. J Appl tine (31) is a limiting factor for the oxidation of ingested
Physiol 96: 1277–1284, 2004. First published December 2, 2003; glucose (18, 21).
10.1152/japplphysiol.00974.2003.—The purpose of the present study A number of studies have compared the oxidation rates of
was to examine whether combined ingestion of a large amount of
fructose and glucose during cycling exercise would lead to exogenous
various types of ingested CHO with the oxidation of exogenous
carbohydrate oxidation rates ⬎1 g/min. Eight trained cyclists (maxi- glucose during exercise (for review, see Ref. 18). From these
mal O2 consumption: 62 ⫾ 3 ml䡠kg⫺1 䡠min⫺1) performed four exer- studies, it appears that the rate of oxidation of ingested maltose

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cise trials in random order. Each trial consisted of 120 min of cycling (11), sucrose (27, 40), glucose polymer (26), and maltodextrin
at 50% maximum power output (63 ⫾ 2% maximal O2 consumption), (32) is fairly similar to the oxidation rate of ingested glucose.
while subjects received a solution providing either 1.2 g/min of However, significantly lower exogenous CHO oxidation rates
glucose (Med-Glu), 1.8 g/min of glucose (High-Glu), 0.6 g/min of have been reported for fructose (⬃20–25% lower) (1, 15, 25,
fructose ⫹ 1.2 g/min of glucose (Fruc⫹Glu), or water. The ingested 26) and galactose (⬃50% lower) (23) compared with glucose.
fructose was labeled with [U-13C]fructose, and the ingested glucose There have been suggestions that the lower oxidation rate of
was labeled with [U-14C]glucose. Peak exogenous carbohydrate oxi- fructose is due to a lower rate of absorption (1, 18). Further-
dation rates were ⬃55% higher (P ⬍ 0.001) in Fruc⫹Glu (1.26 ⫾ more, both fructose and galactose have to be converted into
0.07 g/min) compared with Med-Glu and High-Glu (0.80 ⫾ 0.04 and
glucose in the liver before they can be oxidized, and this may
0.83 ⫾ 0.05 g/min, respectively). Furthermore, the average exogenous
carbohydrate oxidation rates over the 60- to 120-min exercise period slow down the rate of oxidation.
were higher (P ⬍ 0.001) in Fruc⫹Glu compared with Med-Glu and Intestinal transport of glucose occurs via a sodium-depen-
High-Glu (1.16 ⫾ 0.06, 0.75 ⫾ 0.04, and 0.75 ⫾ 0.04 g/min, dent glucose transporter (SGLT1), which is located in the
respectively). There was a trend toward a lower endogenous carbo- brush-border membrane (8). It is likely that SGLT1-transport-
hydrate oxidation in Fruc⫹Glu compared with the other two carbo- ers are saturated at a glucose ingestion rate of ⬃1 g/min, which
hydrate trials, but this failed to reach statistical significance (P ⫽ could explain why higher glucose intake rates do not result in
0.075). The present results demonstrate that, when fructose and oxidation rates higher than 1.0–1.1 g/min (21, 40). In contrast
glucose are ingested simultaneously at high rates during cycling to glucose, fructose is absorbed from the intestine by GLUT-5,
exercise, exogenous carbohydrate oxidation rates can reach peak a sodium-independent facilitative fructose transporter (4, 8). It
values of ⬃1.3 g/min. is not unlikely that, when a mixture of glucose and fructose is
substrate utilization; carbohydrate absorption; isotopic tracers; metab- ingested, there is less competition for absorption compared
olism with the ingestion of an isoenergetic amount of glucose (or
fructose), and this may increase the availability of CHO into
the bloodstream for oxidation.
IT HAS BEEN SHOWN THAT CARBOHYDRATE (CHO) feedings during To our knowledge, only two studies have attempted to
prolonged moderate- to high-intensity exercise can postpone investigate the oxidation of combined ingestion of glucose and
fatigue and enhance exercise performance when the exercise fructose (1, 33). The results of these studies are contradictory,
duration is ⬃45 min or longer (2, 17, 41). The observed which might be due to differences in study design or subject
improvements in performance with CHO ingestion have con- selection. Riddell et al. (33) studied 12 children who ingested
tributed to better maintenance of plasma glucose concentra- 67.5 g of a mixture of glucose and fructose or an isoenergetic
tions and high rates of CHO oxidation late in exercise (3, 5), amount of glucose during 90 min of exercise at 55% maximal
when muscle and liver glycogen levels are low. O2 consumption (V̇O2 max). No difference was found in exog-
Studies that have used either stable (16, 21, 29, 36, 40) or enous CHO oxidation between the two CHO trials, and peak
radioactive isotopes (3, 11) to quantify exogenous CHO oxi- oxidation rates did not exceed 0.36 g/min. In a study by Adopo
dation during exercise have found peak oxidation rates of ⬃1 et al. (1), six trained subjects cycled for 120 min at 61%
g/min (for review, see Refs. 10, 18, 21). Even when CHO was V̇O2 max while ingesting 100 g of glucose or fructose or a
ingested at high rates (up to 3.0 g/min), oxidation rates did not mixture of 50 g glucose and fructose. The addition of fructose
exceed 1 g/min (16, 21, 29, 36, 40). In most of the above-cited to the glucose drink increased total exogenous CHO oxidation
studies, glucose or glucose polymer was the type of CHO by 27% compared with the isoenergetic glucose drink (0.61 vs.

Address for reprint requests and other correspondence: A. E. Jeukendrup, The costs of publication of this article were defrayed in part by the payment
School of Sport and Exercise Sciences, Univ. of Birmingham, Edgbaston, B15 of page charges. The article must therefore be hereby marked “advertisement”
2TT, Birmingham, UK (E-mail: A.E.Jeukendrup@bham.ac.uk). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

http://www.jap.org 8750-7587/04 $5.00 Copyright © 2004 the American Physiological Society 1277
1278 OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE

0.48 g/min). It should be noted that the amounts of CHO fructose-to-glucose ratio was 1:2), or plain water (Wat). To quantify
ingested in the study of Adopo et al. were relatively small exogenous CHO oxidation, the ingested fructose was enriched with
(⬃0.8 g/min), and, therefore, glucose (and fructose) transport- [U-13C]fructose, and the ingested glucose was labeled with
ers were probably not fully saturated. At present, there are no [U-14C]glucose. The order of the experimental drinks was counter-
studies available in the literature that have investigated whether balanced in a crossover design. Experimental trials were separated by
at least 7 days.
combined ingestion of large amounts of glucose and fructose
Diet and activity before testing. Subjects were asked to record their
can result in exogenous CHO oxidation rates that exceed 1 food intake and activity pattern 2 days before the first exercise trial
g/min. Furthermore, in the study of Adopo et al., it was not and were then instructed to follow the same diet and exercise activities
possible to determine the oxidation rate of both glucose and before the other three trials. In addition, 5–7 days before each
fructose in one trial, because only one of the ingested CHO was experimental testing day, they were asked to perform an intense
isotopically labeled. To measure the total oxidation rate of the training session (“glycogen-depleting” exercise bout) in an attempt to
ingested glucose plus fructose mixture, two separate trials were empty any 13C-enriched glycogen stores. Subjects were further in-
performed, and this may have confounded the results. structed not to consume any food products with a high natural
We hypothesized that combined ingestion of a large amount abundance of 13C (CHO derived from C4 plants: corn, sugar cane) at
of fructose (72 g) and glucose (144 g) during 2 h of exercise least 1 wk before and during the entire experimental period to reduce
would lead to exogenous CHO oxidation rates higher than 1 the background shift (change in 13CO2) from endogenous substrate
g/min. The ingested fructose was labeled with [U-13C]fructose, stores.
Protocol. Subjects reported to the Human Performance Laboratory
and the ingested glucose was labeled with [U-14C]glucose,
in the morning (between 7:00 and 9:00 AM) after an overnight fast
which enabled us to measure the oxidation rates of glucose and (10–12 h) and having refrained from any strenuous activity or drink-

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fructose when ingested simultaneously. ing any alcohol in the previous 24 h. For a given subject, all trials
were conducted at the same time of the day to avoid any influence of
METHODS circadian variance. On arrival in the laboratory, a flexible 21-gauge
Teflon catheter (Quickcath, Baxter BV, Norfolk, UK) was inserted in
Subjects. Eight trained male cyclists or triathletes, aged 29.0 ⫾ 2.7 an antecubital vein of an arm and attached to a three-way stopcock
yr and with a body mass of 75.1 ⫾ 1.8 kg, took part in this study. (Sims Portex, Kingsmead, UK) to allow for repeated blood sampling
Before participation, each of the subjects was fully informed of the during exercise. The catheter was kept patent by flushing with 1.0–1.5
purpose and risks associated with the procedures, and a written, ml of isotonic saline (0.9% Baxter) after each blood sample collection.
informed consent was obtained. All subjects were healthy, as assessed After voiding, subjects were weighed in cycling shorts to the nearest
by a general health questionnaire. The study was approved by the 0.1 kg by using a platform scale (Seca Alpha, Hamburg, Germany).
South Birmingham Local Research Ethics Committee and the UK The subjects then mounted a cycle ergometer, and a resting breath
administration of Radioactive Substance Advisory Committee. sample was collected in 10-ml Exetainer tubes (Labco Brow Works,
Preliminary testing. At least 1 wk before the start of the experi-
High Wycombe, UK), which were filled directly from a mixing
mental trials, an incremental cycle exercise test to volitional exhaus-
chamber in duplicate to determine the 13C-to-12C ratio (13C/12C) in
tion was performed to determine the individual maximum power
the expired air. A second resting breath sample was collected for later
output (Ẇmax) and V̇O2 max. This test was performed on an electro-
determination of 14CO2-specific activity. The expired air of each
magnetically braked cycle ergometer (Lode Excalibur Sport, Gro-
second breath sample was collected in a 6-liter anesthetic gas bag by
ningen, The Netherlands), modified to the configuration of a racing
using a two-way Hans Rudolph valve and subsequently passed
bicycle with adjustable saddle height and handlebar position. After the
subjects reported to the laboratory, body mass (Seca Alpha, Hamburg, through a CO2 trapping solution, containing 1 ml of hyamine hydrox-
Germany) and height were recorded. Subjects then started cycling at ide in 1 M methanol (Zinsser Analytic, Berkshire, UK), 2 ml of 96%
95 W for 3 min, followed by incremental steps of 35 W every 3 min ethanol (BDH Laboratory Supplies, Poole, UK), and one to two drops
until exhaustion. Heart rate (HR) was recorded continuously by a of phenolphthalein (Riedel-de Haën, Seeize, Germany). The expired
radiotelemetry HR monitor (Polar Vantage, Kempele, Finland). air was bubbled for 2–3 min through the pink-colored CO2 trapping
Ẇmax was calculated from the last completed work rate, plus the mixture until the solution became clear, at which point exactly 1 mmol
fraction of time spent in the final, noncompleted work rate, multiplied of CO2 was trapped (37). Seventeen milliliters of liquid scintillation
by the work rate increment. The results were used to determine the cocktail (Ready Gel, Beckman Coulter, High Wycombe, UK) was
work rate corresponding to 50% Ẇmax, which was later employed in then added to the solution, and 14CO2 radioactivity in disintegrations/
the experimental exercise trials. Breath-by-breath measurements were min (dpm, later converted to dpm/mmol) was subsequently counted in
performed throughout exercise by using an online automated gas a liquid scintillation counter (Beckman, LS 1800).
analysis system (Oxycon Alpha, Jaeger, Wuerzberg, Germany). The Next, a resting blood sample (10 ml) was taken and stored on ice
volume sensor was calibrated by using a 3-liter calibration syringe, until centrifugation. Subjects then started a 120-min exercise bout at
and the gas analyzers were calibrated by using a 5.03% CO2-94.97% a work rate equivalent to 50% Ẇmax (63 ⫾ 2% V̇O2 max). Additional
N2 gas mixture. Oxygen consumption (V̇O2) was considered to be blood samples were drawn at 15-min intervals during exercise. Ex-
maximal (V̇O2 max) when at least two of the three following criteria pired breath samples were collected every 15 min until the end of
were met: 1) a leveling off of V̇O2 with increasing workload (increase exercise. V̇O2, carbon dioxide production (V̇CO2), and RER were
of no more than 2 ml䡠kg⫺1 䡠min⫺1), 2) a HR within 10 beats/min of measured every 15 min for periods of 4 min by using an online
predicted maximum (HR 220 minus age), and 3) a respiratory ex- automated gas analysis system, as previously described.
change ratio (RER) ⬎ 1.05. V̇O2 max was calculated as the average During the first 3 min of exercise, subjects drank an initial bolus
oxygen uptake over the last 60 s of the test. The V̇O2 max and Ẇmax (600 ml) of one of the four experimental drinks: Med-Glu, High-Glu,
achieved during the incremental exercise test were 62 ⫾ 3 Fruc⫹Glu, or Wat. Thereafter, every 15 min, a beverage volume of
ml䡠kg⫺1 䡠min⫺1 and 374 ⫾ 12 W, respectively. 150 ml was provided. The total fluid provided during the 120-min
Experimental design. Each subject performed four exercise trials, exercise bout was 1.65 liters. The average rate of glucose intake in the
which consisted of 120 min of cycling at 50% Ẇmax, while ingesting Med-Glu and High-Glu trial was 1.2 and 1.8 g/min, respectively. In
an 8.7% glucose drink (Med-Glu), a 13.1% glucose drink (High-Glu), the Fruc⫹Glu trial, subjects ingested, on average, 0.6 and 1.2 g/min
an isoenergetic fructose plus glucose drink (Fruc⫹Glu) (the ingested of fructose and glucose, respectively.
J Appl Physiol • VOL 96 • APRIL 2004 • www.jap.org
OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE 1279
Subjects were asked every 30 min to fill in a questionnaire to rate CHO oxidation ⫽ 4.55 V̇CO2 ⫺ 3.21 V̇O2 (1)
(possible) gastrointestinal (GI) problems. Immediately after exercise,
subjects voided and were weighed again wearing cycling shorts only. Fat oxidation ⫽ 1.67 V̇O2 ⫺ 1.67 V̇CO2 (2)
All exercise tests were performed under normal and standard envi-
ronmental conditions (20–23°C dry bulb temperature and 50–60% In the Med-Glu and High-Glu trials, the rate of exogenous glucose
relative humidity). During the exercise trials, subjects were cooled oxidation (EGO) was calculated from the following equation
with standing floor fans in order minimize thermal stress.
Experimental drinks. The fructose used in the Fruc⫹Glu trial was
a corn-derived crystalline fructose (Krystar 300, A. E. Staley Manu-
EGO ⫽ V̇CO2䡠 冉 冊冉 冊
CO2䡠6
14

SA Glu
1
k
(3)

facturing), which has a high natural abundance of 13C [⫺11.9 ␦‰ vs. where 14CO2 is the radioactivity of 1 mmol of expired CO2 (dpm/
Pee Dee Bellemnitella (PDB)]. To increase the 13C content of the mmol) multiplied by 6, because there are 6 carbon atoms per molecule
fructose even further, a trace amount of uniformly labeled 13C of [U-14C]glucose; SA Glu is the specific activity of the ingested
fructose was added {⬃0.083 g [U-13C]fructose/l (ⱖ99%; Cambridge glucose (dpm/mmol); and k is the amount of CO2 (in liters) produced
Isotope Laboratories)}. The fructose provided to the subjects in the by the oxidation of 1 g of glucose (k ⫽ 0.7467 liter CO2/g glucose).
Fruc⫹Glu trial had a 13C enrichment of 134.7 ␦‰ vs. PDB. The 13C The total exogenous CHO oxidation in the Fruc⫹Glu trial was
enrichment of the corn-derived fructose and the experimental fructose determined as the sum of EGO glucose and exogenous glucose
solution was determined by elemental analyzer-isotope ratio mass oxidation derived from ingested fructose [exogenous fructose oxida-
spectrometry (Europa Scientific GEO 20–20, Crewe, UK). tion (EFO)]. EGO in Fruc⫹Glu was calculated by using Eq. 3, and
In all three CHO trials, a wheat-derived glucose (Amylum, London, EFO was calculated from stable isotope measurements (see Eqs. 4 and
UK) was used that has a 13C enrichment of ⫺27.5 ␦‰ vs. PDB. The 5 below).
glucose (⫹fructose) beverages were labeled with a trace amount of The isotopic enrichment was expressed as ␦‰ difference between

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0.45 MBq [U-14C]glucose/l (Amersham Pharmacia Biotech, Little the 13C/12C of the sample and a known laboratory reference standard,
Chalfont, UK), leading to a dose rate of 0.37 MBq/h. Furthermore, to according to the formula of Craig (6)

冋冉 冊 册
all drinks, 20 mmol/l of sodium chloride were added to stimulate fluid
13
absorption. C/ 12C sample
Questionnaires. Subjects were asked to fill out a short question- ␦ 13C ⫽ 13 ⫺ 1 䡠10 3‰ (4)
C/ 12C standard
naire every 30 min during the exercise trials. The questionnaire
contained questions regarding the presence of GI problems at that The ␦ 13C was then related to an international standard (PDB).
moment and addressed the following complaints: stomach problems, EFO was calculated by using the following formula (30)

冉 冊冉 冊
GI cramping, bloated feeling, diarrhea, nausea, dizziness, headache,
belching, vomiting, and urge to urinate or defecate. While subjects ␦ Exp ⫺ ␦ Expbkg 1
EFO ⫽ V̇CO2䡠 (5)
were on the cycle ergometer and continued their exercise, each ␦ Ing ⫺ ␦ Expbkg k
question was answered by simply ticking a box on the questionnaire
that corresponded to the severity of the GI problem addressed. The where ␦ Exp is the 13C enrichment of expired air during exercise with
items were scored on a 10-point scale (1 ⫽ not at all, 10 ⫽ very, very Fruc⫹Glu ingestion at different time points, ␦ Ing is the 13C enrich-
much). The severity of the GI symptoms was divided into two ment of the fructose in the Fruc⫹Glu solution, and ␦ Expbkg is the 13C
categories, severe and nonsevere symptoms, as was previously de- enrichment of expired air in the Wat trial (background) at different
scribed by Jeukendrup et al. (20). Severe complaints included nausea, time points.
stomach problems, bloated feeling, diarrhea, urge to vomit, and A methodological consideration when using 13CO2 and/or 14CO2 in
stomach and intestinal cramps, because these are symptoms that expired air to calculate exogenous substrate oxidation is the trapping
commonly impair performance and may bring with them health risks. of 13CO2 and/or 14CO2 in the bicarbonate pool, in which an amount
The above symptoms were only registered as severe symptoms when of CO2 arising from decarboxylation of energy substrates is tempo-
a score of ⱖ5 out of 10 was reported. When a score ⬍5 was given, rarily trapped (34). However, during exercise, the V̇CO2 increases
they were registered as nonsevere. All other symptoms were regis- severalfold so that a physiological steady-state condition will occur
tered as nonsevere, regardless of the score reported. relatively rapidly, and 13CO2 and 14CO2 in the expired air will be
Analyses. Blood samples were collected into prechilled tubes con- equilibrated with the 13CO2/H13CO⫺ 3 and
14
CO2/H14CO⫺ 3 pool, re-
taining potassium oxalate and sodium fluoride (Beckton Dickinson, spectively. Recovery of 13CO2 (and 14CO2) from oxidation will
Plymouth, UK) and were centrifuged at 2,300 g and 4°C for 10 min. approach 100% after 60 min of exercise when dilution in the bicar-
Aliquots of plasma were immediately frozen in liquid nitrogen and bonate pool becomes negligible (28, 34). As a consequence of this, all
stored at ⫺70°C until analyses of glucose and lactate. Glucose calculations on substrate oxidation were performed over the last 60
(glucose HK kit, Sigma-Aldrich, Dorset, UK) and lactate (lactate kit, min of exercise (60–120 min).
Sigma-Aldrich) were analyzed on a COBAS BIO semiautomatic Statistical analyses. The data from the four trials were compared by
analyzer (La Roche, Basel, Switzerland). using a two-factor (time and treatment) ANOVA for repeated mea-
Breath samples were analyzed for 13C/12C by gas chromatography sures. A Tukey post hoc test was applied to locate differences when
continuous flow isotope ratio mass spectrometry (Europa Scientific, ANOVA revealed a significant interaction. Data evaluation was per-
Crewe, UK). Furthermore, a second series of breath samples was formed by using SPSS for Windows version 10.0 software package
measured for 14CO2 radioactivity. These breath samples were counted (Chicago, IL). All data are reported as means ⫾ SE. Statistical
for 10 min in a liquid scintillation counter, and all counts were significance was set at P ⬍ 0.05.
corrected for differences in quench and background. From indirect
calorimetry (V̇O2 and V̇CO2), stable isotope measurements (breath RESULTS
13
CO2/12CO2), and radioactive isotope measurements (breath 14CO2
activity), oxidation rates of total fat, total CHO, and exogenous
Stable and radioactive isotope measurements. The 13C en-
glucose and fructose were calculated. richment of the resting breath samples in the Fruc⫹Glu trial
Calculations. From V̇CO2 and V̇O2 (l/min), total CHO and fat and the Wat trial were ⫺26.11 ⫾ 0.09 and ⫺26.01 ⫾ 0.22 ␦‰
oxidation rates (g/min) were calculated by using stoichiometric equa- vs. PDB, respectively (data not shown). Changes in isotopic
tions of Frayn (9), with the assumption that protein oxidation during composition of expired CO2 in response to exercise with
exercise was negligible ingestion of Wat or Fruc⫹Glu are shown in Fig. 1A. In the
J Appl Physiol • VOL 96 • APRIL 2004 • www.jap.org
1280 OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE

Fig. 2. Exogenous CHO oxidation during exercise with ingestion of Med-Glu,


High-Glu, or Fruc⫹Glu. EGO, exogenous glucose oxidation in Fruc⫹Glu;
EFO, exogenous fructose oxidation in Fruc⫹Glu. Values are means ⫾ SE; n ⫽
8. aSignificantly different from Med-Glu and High-Glu, P ⬍ 0.01.

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tion rates between Med-Glu and High-Glu. The average EGO
rates over the 60- to 120-min exercise period were 0.75 ⫾ 0.04,
0.75 ⫾ 0.04, and 0.77 ⫾ 0.04 g/min for Med-Glu, High-Glu,
and Fruc⫹Glu, respectively (P ⬎ 0.05) (Table 1). There were
no significant differences in EGO among the three CHO trials.
In the Fruc⫹Glu trial, the average EFO rate during the final
60 min of exercise was 0.38 ⫾ 0.02 g/min, and this resulted in
a total exogenous CHO oxidation rate (EGO ⫹ EFO) of 1.16 ⫾
0.06 g/min. Exogenous CHO oxidation in the Fruc⫹Glu trial
was ⬃55% higher (P ⬍ 0.001) compared with that in the
Fig. 1. A: change in breath 13CO2 enrichment during exercise (compared with isoenergetic glucose trial (High-Glu) and the Med-Glu trial
resting breath sample) without ingestion of carbohydrate (CHO) [plain water (Table 1 and Fig. 2).
(Wat)] or with ingestion of fructose and glucose (Fruc⫹Glu). B: breath 14CO2 Endogenous CHO oxidation was calculated by subtracting
radioactivity during exercise (corrected for background) with ingestion of exogenous CHO oxidation from total CHO oxidation (Table 1
moderate amounts of glucose (Med-Glu), with ingestion of large amounts of
glucose (High-Glu), or with ingestion of Fruc⫹Glu. Values are means ⫾ SE; and Fig. 3). There were no significant differences in endoge-
n ⫽ 8. PDB, Pee Dee Bellemnitella. nous CHO oxidation rates among trials. However, there was a
trend for a lower endogenous CHO oxidation in Fruc⫹Glu
compared with Med-Glu and High-Glu (P ⫽ 0.075).
Fruc⫹Glu trial, there was a significant increase (P ⬍ 0.001) in V̇O2, RER, total CHO, and fat oxidation. Data for V̇O2, RER,
the 13C enrichment of expired breath, reaching an enrichment total CHO, and fat oxidation over the 60- to 120-min exercise
difference of ⬃17 ␦‰ vs. PDB toward the end of the 120-min
exercise (compared with corresponding resting breath sample). Table 1. Oxygen uptake, respiratory exchange ratio, total
During the Wat trial, there was a small but significant increase carbohydrate oxidation, total fat oxidation, endogenous
in 13C enrichment of the expired air (P ⬍ 0.05). The rise in carbohydrate oxidation, and exogenous glucose and fructose
breath 13CO2 enrichment during the Wat trial was relatively oxidation during the 60- to 120-min period of exercise
small (⬍4%) compared with the increase in breath 13CO2
enrichment observed during the Fru⫹Glu trial. However, al- Trial
though the background shift was small in the present study, a Wat Med-Glu High-Glu Fruc⫹Glu
background correction was made for the calculation of EFO in
the Fruc⫹Glu trial by using the data from the Wat trial. V̇O2, l/min 3.05⫾0.12 3.09⫾0.12 3.09⫾0.10 3.08⫾0.12
RER 0.84⫾0.01 0.90⫾0.01* 0.91⫾0.01* 0.90⫾0.01*
The 14CO2 radioactivity of expired breath samples (cor- CHOtot, g/min 1.85⫾0.23 2.67⫾0.18* 2.86⫾0.18* 2.77⫾0.15*
rected for background) is shown in Fig. 1B. In all three CHO Fattot, g/min 0.82⫾0.05 0.54⫾0.07* 0.47⫾0.07* 0.50⫾0.06*
trials, the 14C activity of the expired CO2 increased signifi- Endogenous CHO,
cantly (P ⬍ 0.001) during exercise and leveled off after 90 min g/min 1.85⫾0.23 1.92⫾0.18 2.11⫾0.19 1.61⫾0.13
of exercise. EGO, g/min 0.75⫾0.04 0.75⫾0.04 0.77⫾0.04
EFO, g/min 0.38⫾0.02
Exogenous and endogenous CHO oxidation. Peak exoge-
nous CHO oxidation rates were reached at the end of exercise Values are means ⫾ SE; n ⫽ 8 subjects; V̇O2, oxygen uptake; RER,
(120 min) and were significantly higher (P ⬍ 0.001) in the respiratory exchange ratio; CHO, carbohydrate; CHOtot, total CHO oxidation;
Fattot, total fat oxidation; EGO, exogenous glucose oxidation; EFO, exogenous
Fruc⫹Glu trial (1.26 ⫾ 0.07 g/min) compared with the Med- fructose oxidation; Wat, plain water; Med-Glu, medium glucose; High-Glu,
Glu and High-Glu trials (0.80 ⫾ 0.04 and 0.83 ⫾ 0.05 g/min, high glucose; Fruc⫹Glu, fructose plus glucose. *Significantly different from
respectively) (Fig. 2). No difference was found in peak oxida- Wat, P ⬍ 0.05.

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OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE 1281
significantly higher (P ⬍ 0.05) compared with lactate concen-
trations at rest. During the first 75 min of exercise, plasma
lactate concentrations were significantly higher (P ⬍ 0.05) in
Fruc⫹Glu compared with Med-Glu and Wat.
GI discomfort. GI and related complaints were registered by
a questionnaire. The results of the questionnaires obtained
during the four experimental trials are presented in Table 2.
The most frequently reported complaints were bloated feeling,
nausea, belching, flatulence, and urge to urinate and vomit.
More subjects reported severe GI discomfort (bloated feeling,
urge to vomit) in the High-Glu trial compared with the Med-
Glu and the Fruc⫹Glu trial. None of the subjects vomited or
suffered from diarrhea during the exercise trails.
Body mass loss. Body mass losses during exercise were not
different among the four experimental trials (on average, 2.0 ⫾
0.1 kg).
Fig. 3. Relative contributions of substrates to total energy expenditure calcu- DISCUSSION
lated for the 60- to 120-min period of exercise with ingestion of Wat, Med-Glu,
High-Glu, or Fruc⫹Glu. Values are means ⫾ SE; n ⫽ 8. bSignificantly To our knowledge, this study is the first to report exogenous

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different from Wat, P ⬍ 0.01. CHO oxidation rates during cycling exercise ⬎1.1 g/min
(1.26 ⫾ 0.07 g/min). Previous studies that have investigated
exogenous CHO oxidation during cycling exercise have re-
period are shown in Table 1. There was no difference in V̇O2
among the four trials. RER in the Wat trial was significantly
lower (P ⬍ 0.01) compared with that in the three CHO trials
(Table 1). CHO oxidation was significantly higher (P ⬍ 0.01)
after CHO ingestion compared with Wat ingestion. No signif-
icant differences in total CHO oxidation were found among
CHO trials. Total fat oxidation was markedly suppressed with
CHO ingestion (P ⬍ 0.01). During the final 60 min of exercise,
total fat oxidation rates were 0.82 ⫾ 0.05, 0.54 ⫾ 0.07, 0.47 ⫾
0.07, and 0.50 ⫾ 0.06 g/min for Wat, Med-Glu, High-Glu, and
Fruc⫹Glu, respectively. The relative contribution of substrates
to total energy expenditure is depicted in Fig. 3.
Plasma metabolites. Plasma glucose and lactate concentra-
tions at rest and during exercise are shown in Fig. 4, A and B,
respectively. Fasting plasma glucose concentrations were sim-
ilar in the four trials (on average, 4.7 ⫾ 0.1 mmol/l). With the
ingestion of large amounts of CHO at the start of exercise,
plasma glucose concentrations in the three CHO trials peaked
within the first 15 min of exercise (P ⬍ 0.01) at values around
6.0–6.4 mmol/l. Plasma glucose concentrations then dropped
and were maintained at values of 4.9–5.4 mmol/l for the entire
duration of exercise. Plasma glucose concentrations during
Wat decreased from 4.6 ⫾ 0.1 mmol/l at the start of exercise
to 4.0 ⫾ 0.1 mmol/l by the end of exercise (P ⬍ 0.01). Plasma
glucose concentrations were higher throughout exercise in the
CHO trials compared with the Wat trial, although Med-Glu
failed to reach statistical significance between time ⫽ 30 and
60 min (P ⬎ 0.05).
In addition, during the second hour of exercise, plasma
glucose concentrations were significantly lower in Med-Glu
compared with High-Glu (P ⬍ 0.05). No other differences in
plasma glucose concentrations were found among the three
CHO trials.
Resting concentrations of plasma lactate were not different
among trials (on average, 0.8 ⫾ 0.1 mmol/l) (Fig. 4B). Plasma
lactate levels increased (P ⬍ 0.05) during the first 15 min of Fig. 4. Plasma glucose (A) and lactate (B) during exercise with ingestion of
Wat, Med-Glu, High-Glu, or Fruc⫹Glu. Values are means ⫾ SE; n ⫽ 8.
exercise in all four trials. Thereafter, plasma lactate concentra- Significant differences: cWat vs. High-Glu and Fruc⫹Glu, dWat vs. Med-Glu,
tions gradually declined until the end of exercise. At all time e
Med-Glu vs. High-Glu, fFruc⫹Glu vs. Wat and Med-Glu, gFruc⫹Glu vs.
points during exercise, plasma lactate concentrations were Wat: P ⬍ 0.05.

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1282 OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE

Table 2. Gastrointestinal and related complaints during Fruc⫹Glu could be fully attributed to the oxidation of ingested
120 min of exercise fructose (Table 1, Figs. 2 and 3).
When large amounts of glucose or glucose polymer are
Complaint Wat Med-Glu High-Glu Fruc⫹Glu
ingested (⬎1.0 g/min) during exercise, intestinal absorption
Nonsevere and/or disposal by the liver may be limiting factors for exog-
Stomach problems 1 2 2 1 enous CHO oxidation (18, 21). Glucose is absorbed from the
Nausea 0 3 2 1 intestine by SGLT1 (8), and suggestions have been made that
Dizziness 0 0 0 0 the upper limit for glucose absorption (at rest) is ⬃1.0 g/min
Headache 0 1 0 0 (31). However, others have suggested slightly higher values
Flatulence 0 2 2 2
Urge to urinate 0 3 1 4 (1.3–1.7 g/min) (7). Although speculative, SGLT1 transporters
Urge to defecate 0 1 2 1 may become “saturated” at a glucose ingestion rate of 1.0–1.2
Urge to vomit 0 3 2 1 g/min, and, therefore, no increase in EGO is observed when
Belching 1 5 3 2 glucose intake is further increased (Ref. 40 and present results).
Stomach burn 0 0 1 1
Bloated feeling 0 2 2 2
Fructose is absorbed from the intestine by GLUT-5 transport-
Stomach cramps 0 0 1 0 ers (4, 8), and this differs from intestinal glucose transport
Intestinal cramps 0 0 1 0 (SGLT1). Interestingly, a study by Shi et al. (38) showed that
Side aches left 0 0 1 0 beverages containing two or three transportable CHOs (fruc-
Side aches right 0 0 0 0 tose, glucose, and/or sucrose) may increase CHO and water
Reflux 0 1 1 1
absorption. A solution that contained glucose and fructose

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Severe especially was found to result in almost 65% higher CHO
Stomach problems 0 0 1 0 absorption rates compared with an isoenergetic glucose solu-
Nausea 0 0 1 0 tion. This effect was attributed to the fact that glucose and
Urge to vomit 0 0 2 0
Bloated feeling 0 1 4 1 fructose are absorbed by separate intestinal transport mecha-
Stomach cramps 0 0 0 1 nisms. Furthermore, it has been shown that fructose absorption
is stimulated by the presence of glucose (13, 35), and hence
n ⫽ 8 Subjects. Stomach cramps, urge to vomit, nausea, bloated feeling, and
stomach problems were registered as severe when a score of 5 or higher (out
this may further contribute to a faster intestinal CHO absorp-
of 10) was given. tion rate when glucose and fructose are ingested simulta-
neously. A faster intestinal CHO absorption might increase the
availability of exogenous CHO in the bloodstream, and this
might have caused the higher exogenous CHO oxidation rates
ported peak oxidation rates of ⬃1.0 g/min (3, 11, 21, 36, 40) in Fruc⫹Glu. Adopo et al. (1) also reported higher oxidation
for exercise durations up to 180 min. Another interesting rates when a mixture of glucose and fructose was ingested
finding was that a mixture of glucose and fructose when compared with the ingestion of an isoenergetic amount of
ingested at a high rate resulted in ⬃55% higher exogenous glucose. However, the rate of CHO intake in the study of
CHO oxidation rates compared with ingestion of an iosoener- Adopo et al. was relatively low (⬃0.8 g/min), and intestinal
getic amount of glucose only. CHO transporters were probably not saturated. As a result of
In the present study, exogenous CHO oxidation rates did not this exogenous CHO oxidation, rates did not exceed 1 g/min.
increase when the rate of glucose ingestion was increased from The present data show that, when fructose and glucose are
1.2 to 1.8 g/min (Table 1 and Fig. 2). Peak oxidation rates were ingested simultaneously at high rates during cycling exercise,
0.80 ⫾ 0.04 and 0.83 ⫾ 0.05 g/min for Med-Glu and High- exogenous CHO oxidation rates can reach peak values of ⬃1.3
Glu, respectively. These results are in close agreement with the g/min.
findings of a study by Wagenmakers et al. (40), who investi- It should be noted that, over the 2-h exercise period, the
gated the effect of four different doses of maltodextrin inges- percentage of ingested CHO that was not oxidized was much
tion on exogenous CHO oxidation. Calculated average CHO larger in High-Glu (68 ⫾ 2%) compared with Fruc⫹Glu (49 ⫾
ingestion rates during 120 min of cycling exercise were 0.6, 3%) and Med-Glu (51 ⫾ 3%) (data not shown). This suggests
1.2, 1.8, and 2.4 g/min. Exogenous CHO oxidation was higher that, in the High-Glu trial, more CHO was accumulating in the
when maltodextrin was ingested at a rate of 1.2 g/min com- body, most likely in the stomach or gut. Malabsorption of CHO
pared with 0.6 g/min (0.87 ⫾ 0.13 vs. 0.53 ⫾ 0.17 g/min). during exercise may increase the risk of GI complications (32).
However, a further increase in the rate of maltodextrin inges- The higher prevalence of severe GI discomfort in the High-Glu
tion did not lead to a significant increase in exogenous CHO trial compared with the Fruc⫹Glu trial may indicate that less
oxidation, and oxidation rates leveled off at 1.0–1.1 g/min. CHO is leaving the GI tract and further supports the hypothesis
Interestingly, in the present study, combined ingestion of that exogenous CHO oxidation in High-Glu was limited at the
fructose and glucose resulted in peak oxidation rates of 1.26 ⫾ level of intestinal absorption.
0.07 g/min (Fig. 3), and average oxidation rates during the final In the present study, CHO ingestion suppressed fat oxidation
60 min of exercise were 1.16 ⫾ 0.06 g/min (Table 1). Further- (Table 1) compared with fasting (Wat). The contribution of fat
more, ingestion of fructose in combination with glucose re- oxidation to total energy expenditure was 54 ⫾ 4% during
sulted in ⬃55% higher exogenous CHO oxidation rates com- Wat, and this value decreased to 34 ⫾ 4, 29 ⫾ 4, and 31 ⫾ 3%
pared with the ingestion of glucose only (Med-Glu and High- during Med-Glu, High-Glu, and Fruc-Glu, respectively (P ⬍
Glu) (Table 1 and Fig. 2). EGO in the Fruc⫹Glu trial was 0.01) (Fig. 3). A decreased fat oxidation with CHO ingestion
similar compared with EGO in the Med-Glu and High-Glu during exercise has been found in several other studies (1, 19,
trial, and hence the higher exogenous CHO oxidation rate in 21, 24, 40). When CHO is ingested during prolonged low- to
J Appl Physiol • VOL 96 • APRIL 2004 • www.jap.org
OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE 1283
moderate-intensity exercise, plasma insulin concentrations ACKNOWLEDGMENTS
may increase (19, 21). Insulin has been shown to be a potent The authors thank Amylum UK, London (UK) for donating glucose
inhibitor of lipolysis and the rate of appearance of free fatty monohydrate and A. E. Staley Manufacturing (US) for donating fructose. We
acids (FFA) (14). Although plasma insulin and FFA concen- also thank Dr. Bob Harris for technical assistance during the 14CO2 measure-
ments and Dr. Guz Zabierck for valuable comments and suggestions through-
trations were not measured in the present study, it is likely that out the study.
higher plasma insulin concentrations and a decreased FFA
availability have contributed to lower fat oxidation rates in the GRANTS
CHO trials compared with the Wat trial. CHO ingestion also This study was supported by a grant from Glaxo SmithKline Consumer
resulted in higher plasma glucose concentrations (Fig. 4A) and Healthcare, UK.
higher rates of CHO oxidation (Table 1) compared with Wat.
In a study by Jeukendrup et al. (19), it was shown that, when REFERENCES
large amounts of CHO are ingested during exercise, plasma 1. Adopo E, Peronnet F, Massicotte D, Brisson GR, and Hillaire-Marcel
glucose oxidation can contribute to ⬃40% of total energy C. Respective oxidation of exogenous glucose and fructose given in the
expenditure and fully accounts for the increase in total CHO same drink during exercise. J Appl Physiol 76: 1014–1019, 1994.
oxidation. In the present study, we did not measure plasma 2. Below PR, Mora-Rodrı́guez R, González-Alonso J, and Coyle EF.
Fluid and carbohydrate ingestion independently improve performance
glucose oxidation, liver-derived glucose, and muscle glycogen during 1 h of intense exercise. Med Sci Sports Exerc 27: 200–210, 1995.
oxidation, and hence we can only speculate what might have 3. Bosch AN, Dennis SC, and Noakes TD. Influence of carbohydrate
caused the higher CHO oxidations rates. It is, however, more ingestion on fuel substrate turnover and oxidation during prolonged
exercise. J Appl Physiol 76: 2364–2372, 1994.

Downloaded from jap.physiology.org on November 2, 2007


than likely that an increased plasma glucose oxidation has 4. Burant CF, Takeda J, Brot-Laroche E, Bell GL, and Davidson NO.
contributed to the higher CHO oxidation rates in the CHO trials Fructose transporter in human spermatozoa and small intestine is GLUT5.
(19). Of note, endogenous CHO oxidation tended to be lower J Biol Chem 267: 14523–14526, 1992.
in the Fruc⫹Glu trial compared with the two glucose trials 5. Coyle EF, Coggan AR, Hemmert MK, and Ivy JL. Muscle glycogen
utilization during prolonged strenuous exercise when fed carbohydrate.
(P ⫽ 0.075), and this might be due to lower muscle and/or liver J Appl Physiol 61: 165–172, 1986.
glycogen oxidation. More studies are required to assess the 6. Craig H. Isotopic standards for carbon and oxygen and correction factors.
effect of combined glucose and fructose ingestion on liver and Geochim Cosmochim Acta 12: 133–149, 1957.
muscle glycogen oxidation. 7. Duchman SM, Ryan AJ, Schedl HP, Summers RW, Bleiler TL, and
Gisolfi CV. Upper limit for intestinal absorption of a dilute glucose
In the present study, plasma lactate concentrations during solution in men at rest. Med Sci Sports Exerc 29: 482–488, 1997.
the first 75 min of exercise were significantly higher in the 8. Ferraris RP and Diamond J. Regulation of intestinal sugar transport.
Fruc⫹Glu trial compared with the Med-Glu and Wat trial. This Physiol Rev 77: 257–302, 1997.
is in agreement with the findings of a study by Koivisto et al. 9. Frayn KN. Calculation of substrate oxidation rates in vivo from gaseous
exchange. J Appl Physiol 55: 628–634, 1983.
(22) who found 20–25% higher lactate concentrations during 10. Hawley JA, Dennis SC, and Noakes TD. Oxidation of carbohydrate
exercise when fructose was ingested in the hour before exer- ingested during prolonged endurance exercise. Sports Med 14: 27–42,
cise. Fructose is rapidly phosphorylated in the liver to fructose- 1992.
1-phosphate, a reaction catalyzed by the enzyme fructokinase 11. Hawley JA, Dennis SC, Nowitz A, Brouns F, and Noakes TD. Exog-
enous carbohydrate oxidation from maltose and glucose ingested during
(12). It has been suggested that the activity of fructokinase is prolonged exercise. Eur J Appl Physiol 64: 523–527, 1992.
higher than the activity of hexokinase and glucokinase, 12. Henry RR, Crapo PA, and Thorburn AW. Current issues in fructose
which phosphorylate glucose. Therefore, after ingestion of metabolism. Annu Rev Nutr 11: 21–39, 1991.
13. Holdsworth CD and Dawson AM. The absorption of monosaccharides in
fructose, there is a large increase in the fructose-1-phos- man. Clin Sci 27: 371–379, 1964.
phate concentration, which will enhance the activation of 14. Horowitz JF, Mora-Rodriquez R, Byerley LO, and Coyle EF. Lipolytic
pyruvate kinase, and hence this will stimulate the formation suppression following carbohydrate ingestion limits fat oxidation during
of pyruvate and lactate (12, 39). In addition, fructolysis can exercise. Am J Physiol Endocrinol Metab 273: E768–E775, 1997.
15. Jandrain BJ, Pallikaris N, Normand S, Pirnay F, Lacroix M, Mosora
also occur without passing through the main rate-controlling F, Pachiaudi C, Gautier JF, Scheen AJ, Riou JP, and Lefèbvre PJ.
step in glycolysis catalyzed by phosphofructokinase. There- Fructose utilization during exercise in men: rapid conversion of ingested
fore, fructose is rapidly phosphorylated, resulting in in- fructose to circulating glucose. J Appl Physiol 74: 2146–2154, 1993.
creased concentrations of glycolytic intermediates, which 16. Jeukendrup AE, Borghouts LB, Saris WH, and Wagenmakers AJ.
Reduced oxidation rates of ingested glucose during prolonged exercise
will lead to an increased glycolytic flux, evidenced by with low endogenous CHO availability. J Appl Physiol 81: 1952–1957,
elevated plasma lactate concentrations. 1996.
In summary, this is the first study to show that exogenous 17. Jeukendrup AE, Brouns F, Wagenmakers AJM, and Saris WHM.
CHO oxidation rates during cycling exercise can reach values Carbohydrate feedings improve 1 H trial cycling performance. Int J Sports
Med 18: 125–129, 1997.
⬎1.1 g/min when a mixture of glucose and fructose is ingested. 18. Jeukendrup AE and Jentjens R. Oxidation of carbohydrate feedings
Furthermore, combined ingestion of glucose and fructose re- during prolonged exercise: current thoughts, guidelines and directions for
sulted in ⬃55% higher exogenous CHO oxidation rates com- future research. Sports Med 29: 407–424, 2000.
pared with the ingestion of an isocaloric amount of glucose. 19. Jeukendrup AE, Raben A, Gijsen A, Stegen JH, Brouns F, Saris
WHM, and Wagenmakers AJM. Glucose kinetics during prolonged
The present data suggest that, when high exogenous CHO exercise in highly trained human subjects: effect of glucose ingestion.
oxidation rates (⬎1.1 g/min) are required during exercise, J Physiol 515: 579–589, 1999.
ingestion of multiple-transportable CHOs is preferred above 20. Jeukendrup AE, Vet-Joop K, Sturk A, Stegen JH, Senden J, Saris
WHM, and Wagenmakers AJM. Relationship between gastro-intestinal
that of large amounts of a single CHO. More studies are needed complaints and endotoxaemia, cytokine release and the acute-phase reac-
to determine the combination of CHOs that would lead to tion during and after a long-distance triathlon in highly trained men. Clin
maximal exogenous CHO oxidation rates. Sci (Lond) 98: 47–55, 2000.

J Appl Physiol • VOL 96 • APRIL 2004 • www.jap.org


1284 OXIDATION OF COMBINED INGESTION OF GLUCOSE AND FRUCTOSE

21. Jeukendrup AE, Wagenmakers AJM, Stegen JHCH, Gijsen AP, 32. Rehrer NJ, Wagenmakers AJM, Beckers EJ, Halliday D, Leiper JB,
Brouns F, and Saris WHM. Carbohydrate ingestion can completely Brouns F, Maughan RJ, Westerterp K, and Saris WHM. Gastric
suppress endogenous glucose production during exercise. Am J Physiol emptying, absorption and carbohydrate oxidation during prolonged exer-
Endocrinol Metab 276: E672–E683, 1999. cise. J Appl Physiol 72: 468–475, 1992.
22. Koivisto VA, Karonen SL, and Nikkila EA. Carbohydrate ingestion 33. Riddell MC, Bar-Or O, Wilk B, Parolin ML, and Heigenhauser JF.
before exercise: comparison of glucose, fructose, and sweet placebo. Substrate utilization during exercise with glucose and glucose plus
J Appl Physiol 51: 783–787, 1981. fructose ingestion in boys ages 10–14 yr. J Appl Physiol 90: 903–911,
23. Leijssen DP, Saris WHM, Jeukendrup AE, and Wagenmakers AJM. 2001.
Oxidation of exogenous [13C]galactose and [13C]glucose during exercise. 34. Robert JJ, Koziet J, Chauvet D, Darmaun D, Desjeux JF, and Young
J Appl Physiol 79: 720–725, 1995.
VR. Use of 13C-labeled glucose for estimating glucose oxidation: some
24. Massicotte D, Peronnet F, Adopo E, Brisson GR, and Hillaire-Marcel
design considerations. J Appl Physiol 63: 1725–1732, 1987.
C. Effect of metabolic rate on the oxidation of ingested glucose and
fructose during exercise. Int J Sports Med 15: 177–180, 1994. 35. Rumessen JJ and Gudmand-Hoyer E. Absorption capacity of fructose
25. Massicotte D, Peronnet F, Allah C, Hillaire-Marcel C, Ledoux M, and in healthy adults. Comparison with sucrose and its constituent monosac-
Brisson G. Metabolic response to [13C]glucose and [13C]fructose inges- charides. Gut 27: 1161–1168, 1986.
tion during exercise. J Appl Physiol 61: 1180–1184, 1986. 36. Saris WH, Goodpaster BH, Jeukendrup AE, Brouns F, Halliday D,
26. Massicotte D, Peronnet F, Brisson G, Bakkouch K, and Hillaire- and Wagenmakers AJ. Exogenous carbohydrate oxidation from different
Marcel C. Oxidation of a glucose polymer during exercise: comparison carbohydrate sources during exercise. J Appl Physiol 75: 2168–2172,
with glucose and fructose. J Appl Physiol 66: 179–183, 1989. 1993.
27. Moodley D, Noakes TD, Bosch AN, Hawley JA, Schall R, and Dennis 37. Scherrer S, Haldimann B, Kruper A, Reubi F, and Bircher J. Hepatic
SC. Oxidation of exogenous carbohydrate during prolonged exercise: the metabolism of aminopyrine in patients with chronic renal failure. Clin Sci
effects of the carbohydrate type and its concentration. Eur J Appl Physiol Mol Med 54: 133–140, 1978.
64: 328–334, 1992. 38. Shi X, Summers RW, Schedl HP, Flanagan SW, Chang R, and

Downloaded from jap.physiology.org on November 2, 2007


28. Pallikarakis N, Sphiris N, and Lefebvre P. Influence of the bicarbonate Gisolfi CV. Effects of carbohydrate type and concentration and solu-
pool and on the occurrence of 13CO2 in exhaled air. Eur J Appl Physiol 63: tion osmolality on water absorption. Med Sci Sports Exerc 27: 1607–
179–183, 1991. 1615, 1995.
29. Pirnay F, Crielaard JM, Pallikarakis N, Lacroix M, Mosora F, 39. Van den Berghe G. Fructose: metabolism and short-term effects on
Krzentowski G, Luyckx AS, and Lefebvre PJ. Fate of exogenous carbohydrate and purine metabolic pathways. Prog Biochem Pharmacol
glucose during exercise of different intensities in humans. J Appl Physiol
21: 1–32, 1986.
53: 1620–1624, 1982.
40. Wagenmakers AJM, Brouns F, Saris WHM, and Halliday D. Oxida-
30. Pirnay F, Lacroix M, Mosora F, Luyckx A, and Lefèbvre PJ. Glucose
oxidation during prolonged exercise evaluated with naturally labeled tion rates of orally ingested carbohydrates during prolonged exercise in
[13C]glucose. J Appl Physiol 43: 258–261, 1977. man. J Appl Physiol 75: 2774–2780, 1993.
31. Radziuk J and Bondy DC. Abnormal oral glucose tolerance and glucose 41. Wright DA, Sherman WM, and Dernbach AR. Carbohydrate feedings
malabsorption after vagotomy and pyloroplasty. Gastroenterology 83: before, during, or in combination improve cycling endurance performance.
1017–1025, 1982. J Appl Physiol 71: 1082–1088, 1991.

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