253

Oxidation of Exogenous Carbohydrate During Prolonged Exercise in Fed and Fasted Conditions* D. Massicotte, F. Péronnei, G. Brisson, L. Boivin, and C. Hillaire-Marcel Département de Kinanthropologie, Université du Québec a Montréal, Département d'Educat ion Physique, Université de Montréal and INRS-Santé, Insitut National de Ia Recherche Scientifique, Montréal, Quebec, H3C 3P8, Canada

Abstract

D. Massicotte, F. Péronnet, G. Brisson, L. Boivin, and C. Hillaire-Marcel, Oxidation of Exogenous

Carbohydrate During Prolonged Exercise in Fed and Fasted Conditions. Tnt J Sports Med, Vol 11, No 4, pp 253—

258,1990. Accepted: September 24, 1989

The oxidation of glucose and fructose ingested during moderate exercise performed on a cycle ergometer (120 mm, 52% VO2max) was compared in ten young males fasted (n = 5) or fed (n 5) before exercise. The subjects ingested randomly 1.33 g/kg body weight 96 9 g) of either enriched 3C-glucose (G), 3C-fructose (F), or water oniy (W); the solutions were evenly distributed over the exercise period. The fasted subjects began the three exercises with a lower blood glucose (P 0.05 for F only) and insulin (P 0.05) levels and a higher free fatty

(

acid (FFA) concentration (P 0.05) than the fed ones. Throughout the exercise period, blood glucose level was maintained in fasted as well as in fed group for G and F ingestions, while it decreased (P < 0.05 at the 100th mm in fasted subjects) with water ingestion. Insulin level was similar in both fed and fasted conditions with F and W ingestions and lower than G trials for the fed subjects. For the three ingestions, FFA was lower (P 0.05) in the fasted than in the fed group over the exercise period. Over the 2-h period of exercise, a greater (P 0.05) amount of exogenous F was oxi-

dized in the fasted (49

g) than in the fed (36 5 g)

group, which represent 31 % and 20% of the total carbohy-

drate energy supply, respectively. There was, however, a similar utilization of ingested G in the two groups, while a slightly greater amount of fat was oxidized in the fasted as compared to the fed group. As a consequence, endogenous carbohydrate utilization was lower (P 0.05) in the fasted

During prolonged exercise the main objectives of carbohydrate feeding are the maintenance of the blood glucose level and the reduction of muscle glycogen utilization, which help delay the onset of fatigue and increase the physical performance. The ingestion of glucose before or at the beginning of exercise evoked several drawbacks, such as hyperinsulinemia response induced by the elevation of blood glucose and its subsequent inhibition of fat mobilization (12, 21, 22). As a consequence, the glycogen depletion rate was unchanged (9, 11,20) or increased instead of being reduced (5, 16). Fructose was then suggested as an alternative carbohydrate source to spare glycogen because it seems to trigger a weaker insulin

response than glucose (16, 20, 21, 22), and thus would not cause a concomitant reduction of fat utilization. However, the beneficial effects of fructose ingestion on glycogen use and performance remain unclear and the conflicting results seem to be attributed to the pre-exercise feeding state (2, 11, 16, 20, 26, 28). Since the fructose must be transformed into glucose through the liver before its utilization by the working muscles we have previously reported in fed subjects that ingested 3C-labeled fructose was less readily available and less oxidized than glucose (23, 24); consequently, there was no endogenous carbohydrate sparing effect. This delay might be attributed to the slower absorption of fructose from the gastrointestinal tract (30) and/or to the slow conversion into glucose by the liver (4) when the exercise is performed in a post prandial state. Then the reduction of the pre-exercise liver glycogen content and the blood insulin level with fasting might: 1) accelerate the transformation of fructose into glucose; 2) increase its oxidation; 3) favour fat utilization; 4) contribute to spare carbohydrate stores.

The purpose of this study was to compare the substrate utilization and the exogenous fructose and glucose oxidation when a moderate prolonged exercise is performed in fed and fasted conditions.

than in the fed subjects with either F or G ingestions.

Key words

Fasting, glucose, fructose, stable isotope '3C, substrate utilization, insulin

Material and Methods Subjects: Ten active male subjects volunteered to participate in this study. None of the them had a history of diabetes mellitus. After giving their informed consent, the sub*

Int.J. Sports Med. 11(1990)253—258

Georgmieme Verlag StuttgartNewYork

The study was supported by grants from the National Sciences and

Engineering Research Council of Canada, the Fonds pour la Formation de Chercheurs et I'Aide ala Recherche (Gouv. du Québec) and the Laboratoire de géochimie isotopique et de géochronologie (GEOTOP), Université du Québec a Montréal.

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Introduction

D. Massicotte, F. Péronnet, G. Brisson, L. Boivin, and C. Hillaire-Marcel

254 mt. J. Sports Med. 11 (1990)

jects performed a progressive and maximum bicycle ergo-

The l3 12 ratio was determined by a double

meter test to determine their VO2max and their individual experimental work load. In order to assure similar physiological characteristics in both experimental groups, the subjects were

inlet mass spectrometer (Micromass Sira 9. The technique of

paired on the basis of their VO2max (mlkg min 5 and assigned to either the fed or fasted groups. The physical par-

viously been detailed (23, 24). Briefly, the following two equations were used:

C02 purification, determination of 13C/ C ratio, and computation of hexogenous carbohydrate oxidized have pre-

ameters for both the fed and fasted groups, respectively, were

as follows (means±SE): age, 22.1±2.6, 24.8±3.1 yrs; 57.7

'3C/ '2C sample —l

5.0,

cI 12 standard

mlkg'min

Experimental protocol: All subjects performed three exercises of 120 mm duration on an electrically braked cycle ergometer (Quinton). The work load was held constant 115±14 Wattsmini to elicit 52%±6% of each individual's VO2max. The three trials were performed at 7-day intervals at the same time in the morning in a room controlled

(=

for temperature (21 °C I °C) and humidity (45% 5%).

x (7)

13 o 13'.-refO '..-obs

x 1.34 1CO2

Hexose (g) 6 13CrefS13Ctr

REF = Values with water ingestion; OBS Values with glucose or fructose ingestions; TR tracers (glucose — 10.30 %o). The 6 13C was expressed by reference to the International

Five subjects exercised in a fed condition (FED) and the remaining five subjects exercised in a fasted state (FAST). The fed condition consisted of an 10-hour overnight fast (water ad libitum) followed by a breakfast (identical for the three trials) taken 3 h prior to the exercise. The breakfast included two

Standard PDB. The quantification of oxidized CHO and

wheat muffins, 50 g of white cheese, and 300 ml of unsweetened orange juice (proteins 15 g; lipids 15 g; carbo-

using a three way analysis of variance with repeated measures on the last two factors (fed-fast conditions x glucose — fructose — water ingestions x measures across time). Significant differences (P 0.05) were located by a Newman Keuls post hoc test.

hydrates50 g; totall700 kJ). For the fasted condition, the subjects were instructed to ingest nothing but water from 1 8h00 until the exercise test the next morning, which resulted in a 15-h fast. During the three days preceeding each test, the subjects did not participate in any intensive physical activities. Diet was controlled and recorded for two days before each

trial. Ingestion of foods derived from sugar cane or corn, which contain large amounts of '3C, was identified and avoided during the experimental period.

During the exercise the subjects randomly in-

ested 1.33 grams per kg body weight (gkg5 of enriched 3C-glucose or 13C-fructose ( = 96 9 g: Fisher Scientific)

dissolved in water at 7% concentration, or water only

(1390± 130 ml). The beverages were ingested in six equal quantities (232 22 ml of solution containing 16 g of either glucose or fructose, or water only) every 20 minutes from 0 to 100 mm during exercise. The average carbohydrate ingestion

rates were 11 mgkg min

Measurements:

Measurements were taken at

rest prior to exercise and every 20 mm during the exercise period. Expiratory gases were analysed for computation of V02,

'7C02, and respiratory exchange ratio (R) through an open system (CD4 spirometer, Beckman; M- 11 and LB2 analysers for 02 and CO2 contents, respectively). The heart rate was continuously recorded during exercise (CM 5). Simultaneously

with 102 and VCO2 determinations, an expired air sample was collected into a 20 ml glass sample holder (vacuumed at lO2Torr) for 13C/ '2C ratio analysis. Blood samples were withdrawn from an anticubital vein through a flexible catheter (Cathlon IV), which was kept patent by slow infusion of sterile isotonic saline (125— 150 ml over the 2-h period of exercise). Plasma samples were analysed for glucose (reagent kits from Calbiochem — Behring), insulin (radio-immunoassay, Bio/ Ria Montréal), and free fatty acids (29) concentrations.

lipids at each interval time were calculated from R taken as a non-protein respiratory quotient.

Statistical analysis: Comparisons were made

Results Throughout the exercise period, blood glucose level was maintained with glucose and fructose ingestion in fasted as well as in fed subjects (Fig. 1). As anticipated with water ingestion, blood glucose slightly decreased over time in both groups, but the decline was more pronounced (P 0.05 at the 100th mm) in fasted subjects. For the three ingestion conditions, there was a clearer trend to lower blood glucose levels at the onset of and during exercise in the fasted than in the fed group. The difference was statistically signilicant (P 1 .0 UUJ

0.5

U-

0

1

I

I

I

I

I

I

TI

0.40.2—

00

20

40

60

80

100 120

EXERCISE TIME (mm)

Ui

I

I

I

I

Fig. 4 Significant differences (P < 005) of exogenous glucose and fructose oxidations (means SE) between fed and fasted condi-

FRUCTOSE 2.5

2.0 1 .5

1.0

0.5 0

r!t!1I I

I

I

I

I

0

20

40

60

80

I

tions (').

(15) have reported a similar rate of oxidation during the first

hour of moderate exercise performed in a fasting condition. Considering that the carbohydrates were ingested during exercise in the present study, the results are in accordance with these previous data.

I

100 120

EXERCISE TIME (mm) Fig. 3 Significant differences (P 0.05) of plasma free fatty acid

concentrations (means SE) between fed and fasted conditions (*) arid from resting values (+).

gen content was substantially reduced following the 15-h fast

(27). These observations would explain the greater amount of exogenous fructose that was oxidized by the fasted as compared to the fed subjects. The difference between fed and fast conditions on fructose oxidation may also be partly attributed to the role of the kidney in the conversion of fructose into glucose (17). In fasted man at rest, Bergstrom Ct al. (1) and Björkman et a!. (3) observed that a substantial amount of fructose administered intravenously was taken up by the kidney, then stimulating the release of glucose.

When exercise is performed in fed state, we have previously reported that the amount of ingested fructose oxidized was smaller than ingested glucose (23, 24). Over the

2-h period of exercise, the present results corroborate the greater utilization of exogenous glucose (56 7 g) than fructose (36 5 g) in the fed group, while a similar oxidation of these two exogenous hexoses was observed in fasted subjects (Table 1). With the ingestion of 13C-fructose and 13C-glucose 1 h before the exercise, Décombaz et al. (8) and Guézennec et al.

The major metabolic consequence of the greater oxidation of exogenous fructose when the exercise was

performed in the fasting condition is the significant lower utilization of endogenous carbohydrates when compared to control trial or fed state (Table 1). No endogenous carbohydrate sparing effect was observed between control and fructose trials in the fed condition. This observation differed from our previous study which reported a significant reduction of

endogenous carbohydrate utilization when fructose was ingested during 2-or 3-h exercise periods (23, 24) performed in a fed state and at a similar relative work intensity. This discrepency can be explained by the difference in duration of exercise and by the fitness level of the subjects. During the 3-h trial

(24) the endogenous carbohydrate sparing effect occurred only in the last 90 mm of exercise. The previous 2-h study (23)

was performed with very well-trained subjects (average

VO2max 66 6 as compared to 58 4 mI/kg-mm in the present report). Coyle et al. (6) have mentioned that when fed

with carbohydrates, highly trained endurance athletes are capable of oxidizing carbohydrates at relatively high rates from sources other then muscle glycogen. For the same amount of ingested fructose, the exogenous oxidation was 18% higher in well-trained (23) subjects as compared to the present results.

Metabolic response to exercise is known to be influenced by hormonal modification (13, 14) and substrate availability (5, 26). Fasting did not influence the amount of cx-

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2.5

E

Oxidation of Exogenous Carbohydrate During Prolonged Exercise in Fed and Fasted Conditions

mt. J. Sports Med. 11 (1990) _Z_

Table 1 Overall Substrate Utilization (g: means SE) Experimental Conditions

Substrates (g)

C

CHO — total —

0—60

—

endo exo

Fat

CHO — total —

60—120

—

endo exo

Fat

CHO — — —

0—120

total

endo exo

Fat

80± 8 80± 8

Fed G 101

C

F

a

72± 7 72± 7

85±lOa

13± 2

79± 8 6± 2b

29± 3

23± 3

28± 4

34± 4

68± 6 68± 6

99±118

59± 6 59± 6

39±5

24± 38

g0±lOa 60± 6a 30± 4b 30± 4a

148±16 148±16

200±23a 144±15

175±198 139±13

131±14 131±14

36± 5b

68±9

56± 7 47± 6a

88±10

56± 68 43± 4

39±4

73±9

58± 7b

Fast G

F

86± 9a

78± 6

64±

61± 78C 17± 2C

6C

22± 3C 26± 3

83± g8 47± 4a 36± 4 29±38 169±198c 111±12ac 58± 7 55± 7a

28± 3 81± 98

49± 58. 34± 3

C

28± 3a

159±l78bC 11O±lOac 49± 6C 56± 6a

C = Control (Water); G = Glucose; F = Fructose. 8 = Significantly different from control in fasted or fed group b = Significantly different from glucose ingestion in fasted or fed group = Significantly different between fasted and fed groups.

ogenous glucose oxidized. In spite of lower blood glucose (Fig. 1), higher FFA concentration (Fig. 3), and lower liver glycogen content in fasted than in fed subjects, the amount of ingested glucose oxidized was similar in both groups (Table 1). The rate of exogenous glucose oxidation was higher in fasted

than in fed subjects during the first hour of exercise only; a contrary situation was observed during the second hour (Fig. 4). The greater availability of plasma free fatty acids (Fig. 3) combined with a lower insulin blood level in fasted than in fed subjects enhanced fat oxidation (Table 1). Even though this in-

crease was not significant (P 0.16), endogenous carbohydrate utilization was lower (P 0.05) in fasted as compared to fed subjects with glucose ingestion or the control trial (Table 1).

6 Coyle E. F., Coggan A. R., Kemmert M. K., Ivy J. L.: Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrates.JApplPhysiol6l: 165—171,1986. Craig H.: Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. GeochimCosmochimActa 12: 133—149, 1957. 8 Décombaz J., Sartori D., Arnaud M. J., Thélin A. L., Schürch P., Howald H.: Oxidation and metabolic effects of fructose or glucose ingested before exercise. IntJSportsMed6: 282—286, 1985. Devlin J. T., Calles-Escadon J., Horton E. S.: Effects of pre-exercise snack

feeding 980—985, 1986. 10

amount of exogenous hexose oxidized, but increases fat utilization. As a consequence, the endogenous carbohydrate utilization is significantly reduced with either fructose or glucose in-

12 13

14

15

17 18

BjOrkman 0., Felig P.: Role of kidney in the metabolism of fructose in 60-hour fasted human. Diabetes 31: 516—520, 1982. Chen M., Whistler R. L.: Metabolism of D-fructose. Adv Carbhydr ChemBiochem 34:285—343,1977. Costill D. L., Coyle E., Daisky G., Evans W., Fink W., Hoopes D.:

Effects of elevated plasma free fatty acids and insulin on muscle glycogen usage during exercise. JApplPhysiol43: 695—699, 1977.

ActaPhysiolScand 107: 19—32,1979. Guézennec C. Y., Satabin P., Duforez

Oxidation of

before exercise.

Bergstrom J., Huitman E.: Synthesis of muscle glycogen in man

'I

1981. Gaibo H., Hoist J. J., Christensen N. J.: The effect of different diets

Koziet J.: 16

2

in well-trained runners. Eur J App! Physiol56: 225—229, 1987. Foster C., Costill D. L., Fink J.: Effect of pre-exercise feedings on endurance performance. Med Sci Sports 11: 1—5, 1979. Galbo H., Christensen N. J., Mikines K. J., Sonne B., Hilsed J., Hagen C., Fahrenkrug J.: The effect of fasting on the hormonal response to graded exercise. JC!in EndocrinolMetab 52: 1106—1112,

and of insulin on the hormonal response to prolonged exercise.

References after glucose and fructose infusion. Acta Med Scand 182: 93— 107, 1967. Björkman 0., Sablin K., Hagenfeldt L., Wahren J.: Influence of glucose and fructose ingestion on the capacity for long term exercise in well-trained men. Clin PhysiolOxf4: 483—494, 1984.

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glycogen use during exercise

gestion when the exercise is performed in a fasting as compared to a fed condition.

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John P.:

In conclusion, these results indicate that inthe fasted than in the fed state, fat utilization being similar. When glucose is ingested, fasting does not influence the

L., Beeker R. T., Israel R. G., Tapscott E. B.: Metabolic

responses 1

gested fructose during moderate exercise is more readily available for the working muscles and oxidized at a higher rate in

Dohm G.

on endurance cycle exercise. JAppi Physiol 60:

19

Hargreaves M.,

F., Merino D., Péronnet F.,

corn starch, glucose, and fructose ingested

Med Sci Sports Exerc 21:45—50, 1989. Costill D. L., Katz A., Fink W. J.: Effect of fructose

ingestion on muscle glycogen usage during exercise. Med Set SportsExercl7:360—363, 1985. Heinz F., Schlegel F., Krause P. H.: Enzymes of fructose metabolism in human kidney. Enzyme 19:85—92,1975. Jansson E., Kjemdahl P., Kajser L.: Diet induced changes in sympathoadrenal activity during submaximal exercise in relation to substrate utilization in man. Acta Physiol Scand 114: 171—178, 1982.

Knapik J., Mederith C. N., Jones B. H., Suek L., Young V. R., Evans W. J.: Influence of fasting on carbohydrate and fat metabolism during rest and exercise in men. J App! Physiol 64: 1923— 1929, 1988.

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Exercise time (mm)

258 mt. J. Sports Med. 11(1990)

D. Massicotte, F. Péronnet, G. Brisson, L. Boivin, and C. Hillaire-Marcel

20

Koivisto V. A., Karkonen M., Karonen S. L., Group P. H., Elovainio R., Ferrannini E., SaccaL., DeFronzo R. A.: Glycogen depletion during prolonged exercise: influence of glucose, fructose, orplacebo.JApplPhysiol58: 731 —737,1985. 21 Koivisto V. A., Karonen S. L. Nikkila E. A.: Carbohydrate inges-

D. Massicotte

Département de Kinanthropologie Université du Québec a Montréal Case Postale 8888 Succursale "A" Montréal P. Q., Canada tion before exercise: comparison of glucose, fructose, and sweet H3C 3P8 placebo.JApplPhysiols 1:783—787,1981. 22 Levine L., Evans W. J., Cadarette B. S., Fisher E. C., Bullen B. A.: Fructose and glucose ingestion and muscle glycogen use during subniaximal exercise. JApp!Physiol43: 695—699, 1983.

23 Massicotte D., Péronnet F., Brisson G., Bakkouch K., HillaireMarcel C.: Oxidation of a glucose polymer during exercise: comparison with glucose and fructose. J App! Physiol 66: 179—183, 1989. 24 Massicotte D., Péronnet F., Allah C., Hillaire-Marcel C., Ledoux M., Brisson G.: Metabolic response to [ 3C] glucose and f DCI fructose ingestion during exercise. JApplPhysio!6 1: 1180—1184, 1986.

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sis. C/in ChimActa 44: 385—390,1983.

30 Ravich W. J., Bayless T. M., Thomas M.: Fructose: incomplete intestinal absorption in humans. Gastroenterology 84: 26—29, 1983. 31 Sonne B., Mikines K. J., Galbo H.: Glucose turnover in 48-hourfasted running rats. Am JPhysiol252 (Reg mt Comp Physiol 21) R587—R593,l987.

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E329, 1980.

26 Neufer P. D., Costill D. L., Flynn M. G., Kirwan J. P., Mitchell J. B., Houmard J.: Improvements in exercise performance: effects of carbohydrate feedings and diet. JApplPhysiol62: 983— 988, 1987. 27 Nilsson L. H., Hultman E.: Liver glycogen in man. The effect of total starvation or a carbohydrate-poor diet followed by carbohydrate refeeding. ScandJClinLabln vest 32:325—330, 1973. 28 Okano G., Takeda H., Morita I., Katch M., Mu Z., Miyake S.: Effect of pre-exercise fructose ingestion on endurance performance infedmen.MedSciSportsExerc2o: 105—109,1988. 29 Pinelli A.: A new colorimetric method for plasma fatty acid analy-