Oxidation of exogenous medium-chain during prolonged exercise: comparison
free fatty acids with glucose
D. MASSICOTTE, F. PERONNET, G. R. BRISSON, AND C. HILLAIRE-MARCEL Universite’ du Q&bee ti Mont&al, Universite’ de Montre’al, and Institut National de la Recherche Scientifique-Sante: Montreal, Quebec H3C 3P8, Canada MASSICOTTE, D., F. P~RONNET,G. R. BRISSON,AND C. HILLAIRE-MARCEL.Oxidation of exogenous medium-chain free fatty acids during prolonged exercise: comparison with glucose. J. Appl. Physiol. 73(4): 1334-1339, 1992.-The purpose of this study was to compare the oxidation rate of exogenous 13C-labeled medium-chain triacylglycerols (MCT) with that of an isocaloric amount of exogenous [ 13C]glucose and to evaluate their respective effects on endocrine and metabolic responses to moderate prolonged exercise. To take into account changes in isotopic composition of 13C0, arising from oxidation of endogenous substrates because of exercise and/or substrate ingestion that overestimates the oxidation rate of exogenous substrates, two levels of 13C enrichment were used for each substrate. Six young healthy males (20-26 yr of age) completed five 2-h periods of exercise at 65 * 3% maximal 0, uptake (VO, max) on a cycle ergometer at 7day intervals: one control exercise with water ingestion, two trials with ingestion of 25 g of [13C]MCT (trioctanoate) 1 h before exercise, and two trials with 57 g of [ ‘3C]glucose (dissolved in 1,000 ml of water) ingested during exercise. Exogenous MCT and glucose began to be oxidized within the first 30 min of exercise, and the oxidation rate increased progressively until the end of exercise for both substrates. Over the 2-h period of exercise, 13.6 t 3.5 g of ingested MCT and 36.4 -+ 8.2 g of exogenous glucose were oxidized, which represent 54 and 64%, respectively, of the total amount ingested. The contribution of MCT (119 & 31 kcal) and glucose (140 * 36 kcal) was not significantly different and represented 7 and 8.5%, respectively, of the total energy expenditure. For similar amounts of MCT and glucose ingested before or during a prolonged exercise, the contributions to the energy yield found in the present study are lower than those reported previously. Ingestion of MCT as well as glucose contributed to maintain blood glucose concentration, abolished the decrease in plasma insulin, reduced the rise of glucagon, and blunted the response of plasma epinephrine normally observed during prolonged exercise. Neither exogenous substrate reduced the endogenous carbohydrate utilization. carbon-13 labeling; fat-glucose ketone bodies; catecholamines;
ingestion; insulin
substrate
utilization;
SEVERAL STUDIES that deal with 13Cas tracer have reported that glucose (10, 15, 16, 18-21, 27, 30) and other types of carbohydrates, including fructose (10, 18, 20), glucose polymers (19), maltodextrins (7, 3O), and cornstarch (lo), ingested before or during an exercise period, significantly contribute to the energy yield. On the other hand, only two studies have investigated the oxidation of exogenous fatty acids ingested before a period of exercise (7,30). Satabin et al. (30) reported that only 9% of -44 g 1334
0161-7567/92 $2.00 Copyright
@I
of long-chain triacylglycerols (LCT) ingested 1 h before the . beginning of exercise at 60% maximal 0, uptake (VO 2,,,) were oxidized over a 2-h period of exercise. On the contrary, exogenous medium-chain triacylglycerols (MCT), which are delivered as free fatty acids into the blood more quickly than the ingested LCT (2), are oxidized to a greater extent: 32% of 25 g and 44% of -44 g ingested in the studies by Decombaz et al. (7) and Satabin et al. (30), respectively. These amounts were lower, however, than those of exogenous carbohydrates oxidized [maltodextrins: 45% of 50 g ingested (7); cornstarch: 80% of 100 g ingested (30)]. In all these previous studies, including our own reports (l&20), the production of 13C02at rest or during exercise without substrate ingestion has been used as a reference value to compute the oxidation of exogenous substrates. However, because of the process of isotopic fractioning, which takes place in the biosphere along the metabolic pathways from atmospheric CO, to plant carbohydrates and fat and subsequently to glycogen and to animal fat, the carbohydrate stores have a higher 13C/12Cratio than fat stores (831). Consequently, any changes in the composition of the mixture of oxidized endogenous substrates that are associated with both exercise and ingestion of substrates lead to changes in isotopic composition of expired CO, (3, 14, 25). We recently showed that failure to take into account changes in 13Cbackground enrichment of expired CO, leads to an overestimation of the amount of exogenous substrate oxidized (17,25). We also suggested a method to adequately take into account these changes (25). Accordingly, the goals of the present study were 1) to reassessthe oxidation rate of exogenous [ 13C]MCT ingested before a period of exercise, 2) to compare the oxidation rate of MCT with that of an isocaloric amount of exogenous [13C]glucose, and 3) to compare the effects of MCT and glucose ingestion on endocrine and metabolic responses to prolonged exercise. MATERIALS AND METHODS Subjects. Six healthy males volunteered for the study and gave their written informed consent. Their mean age, mass, height, and Tj0, maxwere 22.8 t 1.5 yr, 69.5 t 7.2 kg, 173.1 -t 6.6 cm, and 60.5 t 6.7 (SE) ml respectively. None was engaged in a regular training program at the time of the study. The subjects refrained from severe exercise and drinking alcohol during the 3 days preceding each test. l
-l.
min-‘,
kg
1992 the American
Physiological
Society
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EXOGENOUS
FAT
AND
GLUCOSE
Procedure. Each subject completed at H-day intervals five 2-h periods of exercise on an electrically braked cycle ergometer. The work load was kept constant during each trial (mean 188 t 21 W) and was adjusted for each subject to elicit an energy expenditure equivalent to 65 t 3% of his respective predetermined maximal aerobic power. Each test was conducted in the same environmental conditions (temperature 21 t 1°C; humidity 45 t 5%), between 9 and 12 A.M., after an overnight fast and a standardized breakfast taken 2 h before the beginning of exercise. The breakfast consisted of two slices of toasted brown bread, 50 g of white cheese, and 300 ml of unsweetened orange juice: -15 g protein, -15 g fat, -50 g carbohydrate, 1,500 kJ. The five exercises were one control trial (A) with ingestion of 1,000 ml of water only, two trials (B and C) with ingestion of 25 g of MCT (trioctanoate, Sigma Chemical) corresponding to 219 kcal(1 g = 8.76 kcal) and enriched with [13C]octanoate (Merck Frosst, Montreal, 13C/12Cisotopic ratio = 1.09100 and 1.12876%’ for trials B and C, respectively), and two trials (D and E) with ingestion of 57 g of glucose (Biopharm, Montreal) corresponding to 220 kcal (1 g = 3.87 kcal) and enriched with [13C]glucose (Merck Frosst, Montreal, 13C/12Cisotopic ratio = 1.11482 and l.l3303%l for triaZs D and E, respectively). The MCT were ingested in a hot drink flavored with vanilla 1 h before the beginning of exercise to allow an adequate absorption time (2). The glucose was dissolved in 1,000 ml of water (6%) divided into eight equal volumes (125 ml + 7.1 g of glucose), which were ingested every 15 min from 0 to 105 min during the exercise period. Water was also ingested (125 ml every 15 min) during trials A-C. The order of presentation of the five trials was randomized among the subjects. Measures. All measures (expired gasesand blood) were taken at rest before the ingestions and every 30 min thereafter until the end of the exercise period. Expired gases were collected and analyzed (Pneumoscan, Morgan; S-A3 and CD-3A analyzers, Amteck) for computation of 0, uptake (Tj,z), CO, production #CO,), and respiratory exchange ratio (RER). For 13C/12Canalysis of expired CO,, a 2O-ml sample of expired air was collected in a glass sample holder prevacuumed at 10m2Torr. After removal of water vapor through a two-step trapping [I) in liquid nitrogen (-196”C), then 2) release of CO, by warming with an acetone dry ice slush ( -80°C)], the CO, was introduced into a double-inlet mass spectrometer (Micromass Sira 12) for 13C/12Cdetermination. Blood samples were withdrawn through a flexible catheter (Cathlon IV) from an antecubital vein kept open with a saline line. The samples were analyzed for glucose (reagent kit, Boehringer), free fatty acids (26), ,&hydroxybutyrate, insulin, glucagon (Bio-RIA, Montreal), and catecholamine (Amersham) concentrations. Blood sampling and analysis were done in the control situation and during one of each of the two trials with MCT and glucose ingestion. Exogenous substrate oxidation. The oxidation rates of ingested MCT and glucose were computed with the equation ’ 613C PDB
- 1 = - 29.1%o (B); + 4.5%0 (C);
- 7.8%0 (D);
+ 8.3%0 (E)
OXIDATION
DURING
1335
EXERCISE
x = vco,*
Rexp2 R exo
2 -
R exp R exo
1 . 1
-1 k
where x is the amount of ingested substrate oxidized (in grams); VCO, is the volume of expired CO,; R is the isotopic composition of expired CO, (exp) and ingested substrate (exo); the numbers 1 and 2 correspond to the two experiments with ingestion of the exogenous substrate; and k is the amount of CO, produced by the oxidation of the exogenous substrate (1.2369 liters CO,/g of MCT and 0.7426 liter CO,/g of glucose). This computation procedure takes into account the isotopic composition of expired CO, arising from oxidation of endogenous substrates (13C background), the composition of which can be computed as cRendo) (vco20Rexp~) - (X’k’Rexol) R endo = vco, - (x0 k) As discussed previously (25), the procedure commonly used for computing ex ogenous substrate oxidation does not take into account changes in Rendo due to exercise and/or exogenous substrate ingestion. The alternate procedure suggested by Wolfe et al. (32) for computation of exogenous glucose oxidation takes into account only changes in the isotopic composition of blood glucose due to administration of labeled exogenous glucose but is not appropriate “if there is a marked change in the metabolic state (e.g., exercise)” (Ref. 32, p. 233) and if Rend0is modified. Overall carbohydrate and fat oxidation were computed from VO, and VCO,/VO, taken as a nonprotein respiratory quotient (24). When exogenous substrates were ingested and oxidized, the amounts of endogenous substrates oxidized were computed by difference. Statistics. Comparisons were made by a two-way analvsis of variance with repeated measures (trials X time) for the overall substrate utilization and blood hormonal and biochemical parameters. Significant differences (P < 0.05) were located by a Newman-Keuls post hoc test. RESULTS
Changes in Rexpin response to exercise with ingestion of water, MCT, and glucose are shown in Fig. 1. Exercise with water ingestion was associated with a significant change in the isotopic composition of expired CO, (Rexp= Rendo).Table 1 presents the amounts of exogenous and endogenous fat and carbohydrates oxidized during the exercise period. Over the 2 h, 13.6 t 3.5 g of exogenous MCT and 36.4 t 8.2 g of exogenous glucose were oxidized, representing 54 and 64%, respectively, of the total amounts ingested. For both exogenous substrates, the oxidation rate was larger during the 2nd than during the 1st h of exercise. Only one-third of the total amounts of MCT (4.1 of 13.6 g) and glucose utilized (12.5 of 36.4 g) was oxidized during the 1st h of exercise (Table 1). Ingestion of MCT and glucose did not contribute to the reduction of endogenous carbohydrate utilization. In fact, a reduction of endogenous fat store utilization was observed for both exogenous substrates (Table 1). Although the amount of exogenous MCT oxidized was lower than the amount of exogenous glucose oxidized,
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1336
EXOGENOUS 1.10600
l
CONTROL
n
LEVEL
1
0
LEVEL
2 I
FAT
AND
GLUCOSE
OXIDATION
DURING 5o01
GLUCOSE 1.10400
A LEVEL
1
A LEVEL
2 I
z-
. CONTROL ) n GLUCOSE 400A MCT
MCT
‘;;b 31.10200 G
0
t t t 5 1
!A
1.10000
1.09800 7//I
1
40
-30
1
1
0
30
I
I
60
90
1
120
+-REST*-EXERCISE,-+j TIME (min)
1. Isotopic composition medium-chain triacylglycerols. FIG.
of expired
CO,
(means
+ SE).
MCT,
the contribution of MCT and glucose to the energy yield was not significantly different (119 t 31 vs. 140 t 36 kcal, respectively). In the control trial with water ingestion, the progressive decrease in blood glucose concentration over the exercise period (P < 0.05 at the 120th min) was accompanied by a reduction in plasma insulin concentration and a rise in glucagon, free fatty acids, P-hydroxybutyrate, and epinephrine concentrations (Figs. 2-4). Glucose as well as MCT ingestion contributed to maintain blood glucose concentration during the 2-h period of exercise (Fig. 2). 1. Overall substrate
1
1
I
1
T
T
I
7-
3$
Ok
TABLE
**t * mtt
EXERCISE
I
1
1
-60 -30 ~-REST~~EXE~R~CISE-?
utilization
1
1 90
A * 1
120
TIME (min)
Ingestion Exercise Time, min Substrates O-60 Carbohydrates Total Endogenous Exogenous Fat Total Endogenous Exogenous 60-120 Carbohydrates Total Endogenous Exogenous Fat Total Endogenous Exogenous O-120 Carbohydrates Total Endogenous Exogenous Fat Total Endogenous Exogenous
Water (control)
153.3k24.8 153.3k24.8
25.123.1 25.1k3.1
142.3k21.1 142.3k21.1
Conditions
Glucose
174.8+ 18.5* 162.3k17.9 12.5k2.4 18.3+2.7* 18.3+2.7*
152.8+18.1 128.9+ 19.3 23.9k5.2
2. Plasma glucose, insulin, and glucagon concentrations (means + SE) during control exercise and with glucose or lipid ingestion. “‘7 S’g1 nl ‘f icant (P < 0.05) differences from resting value and control exercise, respectively. FIG.
MCT
148.5k19.2 148.5kl9.2
27.2k3.8 23.1k3.9 4.1kO.9
144.3k21.6 144.3221.6
32.723.3 32.7k3.3
24.Ok3.8 24.0k3.8
31.1k4.5 21.6t4.3* 9.5t2.2
295.6k56.1 295.6k56.1
327.6+43.4* 291.2k40.6 36.4k9.5
292.8t43.2 292.8k43.2
57.8~16.8 57.8k6.8
42.3-+8.1* 42.3*8.1*
58.3k9.1 44.7+8.7* 13.6k3.5
Values are means + SE in grams. MCT, medium-chain triacylglycerols. * Significantly different (P < 0.05) from control exercise (water).
When compared with the glucose trial, MCT ingestion resulted in similar effects for plasma insulin, glucagon, and catecholamine concentrations, whereas the free fatty acid and P-hydroxybutyrate levels were significantly higher (P < 0.05; Figs. 2-4). DISCUSSION
Exogenous oxidation of MCT vs. glucose. Results indicate that the contributions of exogenous MCT and glucose to energy yield were similar during the exercise period. Indeed, over the 2-h period of exercise, 13.6 t 3.5 g of MCT (corresponding to 119 t 31 kcal) were oxidized compared with 36.4 t 9.5 g (representing 140 t 36 kcal) of glucose (Table 1). This observation is in accordance with previous findings by Decombaz et al. (7), who reported that, over a 60-min period of exercise at 60% . vo 2 maxy exogenous MCT provided 70 t 7 kcal compared with 85 t 6 kcal for exogenous maltodextrins. On the other hand, a higher contribution of exogenous cornstarch (320 vs. 180 kcal for MCT) was observed by Satabin et al. (30) over a 2-h period of exercise performed at 60% ire, max.In both studies, as well as in the present experiment, the MCT were given 1 h before the begin-
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EXOGENOUS 2.5
. 1
FAT
AND
GLUCOSE
CONTROL
n
“t T
GLUCOSE
It
0
2.0
1
I)
+
T
1
OXIDATION
DURING
1337
EXERCISE
those reported in the studies by Decombaz et al. (7) (11 and 14%, respectively) and Satabin et al. (30) (13 and 24%, respectively). As discussed previously (25) dealing with oxidation of exogenous glucose during exercise, these discrepancies are likely to be due to differences in the computation procedures used. In the studies by Decombaz et al. (7) and Satabin et al. (30), it was assumed that Rend0during exercise was similar to that observed at rest. As shown in Fig. 1, changes in the isotopic composition of expired CO, during exercise with water ingestion indicate that Rendois modified by the change in the composition of the mixture of endogenous substrates oxidized (3, 25). This different isotopic composition of endogenous substrates results from the isotopic fractioning along the food chains, the 13C/12Cratio being higher in carbohydrate than in fat stores (8, 31, 33). With the hypothesis that Rend0remains constant, 13Crecovery is overestimated and leads to an overestimation of the amount of exogenous substrates oxidized. In fact, if the method of computation utilized by Decombaz et al. (7) and Satabin et al. (30) is used in the present protocol and Rexpat rest is taken as the reference value for Rendo,the oxidation rate of MCT computed in experiment B (R,,, = 1.12876%) would be 14.7 g during the 1st h and 32.5 g over the 2-h period of exercise, which is greater than the amount ingested. I)
2400
.
CONTROL
L
I)
m GLUCOSE 0 -60
I -30
I 0
I 30
1 60
I 90
1
120
+--REST-+pEXE~~~s~----q
Ii E b --a1600
A MCT
TIME (min) FIG.
tions
3. Plasma free fatty (means t- SE). Symbols
acid and P-hydroxybutyrate as in Fig. 2.
concentra-
ning of exercise to optimize their absorption and availability during the exercise. Unlike LCT, which enter the blood through the lymphatic circulation and consequently are not readily available for oxidation after ingestion, MCT directly enter the bloodstream through the portal circulation (2) and, when taken up by the muscles, cross the mitochondrial membrane through a direct activation process independent of the acylcarnitine transferase system (4). This explains why, as shown by changes in the isotopic composition of expired CO, (Fig. l), MCT begin to be oxidized within the first 30 min of exercise. Obviously, exogenous glucose is much more readily available than MCT and begins to be oxidized within minutes after ingestion (Fig. 1). The oxidation rate of ingested glucose was related to the energy expenditure [glucose (kcal/min) = -1.548 + 0.197 (kcal), r = 0.7961, a phenomenon already outlined by Pirnay et al. (27) in 1982 and recently discussed by Peronnet et al. (23). Data (Fig. 5) indicate that, in the present study, the oxidation rate of exogenous MCT was also related to the energy expenditure [MCT (kcal/ min) = -1.760 + 0.198 kcal, r = 0.5811. However, when expressed in percentage of the total energy yield during the exercise period, the respective contributions of MCT and glucose observed in the present experiment (7.0 t 1.7 and 8.5 t l.4%, respectivelv) are much lower than
2 w Z ii
E
800
g T 0
1200
4/,
I
I
I
1
I
1 I
1
l
sJ^ E 2 800
0 -60 p--
-30 REST
0 30 ~--‘1‘~EXERCISE~~~
60
90
120
TIME (mln) FIG. 4. Plasma bols as in Fig. 2.
catecholamine
concentrations
(means
+ SE).
Sym-
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1338
EXOGENOUS
3.0
PRESENT STUDY DiCOMBAZ et al. 1983 SATABIN et al. 1987
1
FAT n
AND
GLUCOSE
A
AI 0 q 2A2
02
2.5-z .% E 2.0 2A"
2 if 2 1.5z E s l.Ox 0 0.5 J 0 ‘c/r
1 10 ENERGY
1 12 EXPENDITURE
I 14
1 16 (kcal/min)
FIG. 5. Oxidation rate of exogenous substrates: -1.760 + 0.198 kcal, r = 0.581; glucose (kcal) = -1.548 0.796.0, Glucose; & Medium-chain triacylglycerols;
MCT (kcal) = + 0.197 kcal, r = 0, maltodextrins.
Another methodological problem, when production of 13C0, is used to measure the oxidation rate of 13C-labeled exogenous substrate, concerns the trapping of 13C0, in the bicarbonate pool and/or the delay between 13C0, production in the tissue and the appearance of 13C0, in expired gas. The bicarbonate-carbonate pool, particularly in the form of calcium carbonates in bone tissue, constitutes a very slow exchange pool in which an amount of CO, arising from decarboxylation of energy substrates disappears each minute (l&13,29). At rest, -20% of the CO, produced is irreversibly trapped in this pool, and a correction should be made to compute 13Crelease from expired CO, (12,29). However, due to the increase of CO, production during exercise, the amount of 13C0, lost in the pool becomes negligible. In fact, the amount of CO, recovered approaches 100% (2233). Morever, exogenous substrate oxidation is computed over a long period of time (>l h) in a physiological steady-state condition. This allows enough time to equilibrate 13C0, expired with the plasma 13C0,/H13C0, pool (33). Endocrine and metabolic response to MCT and glucose ingestion. Ingestion of MCT before, as well as glucose during, exercise prevented a small but significant reduction in blood glucose concentration observed at the end of exercise with water ingestion (Fig. 2). Maintenance of blood glucose level abolished the progressive decrease in plasma insulin, reduced the rise of plasma glucagon, and markedly blunted the response of plasma epinephrine concentrations normally observed in response to prolonged exercise (Figs. 2-4) (Ref. 9, p. 12 and 38). These hormonal changes were associated with a significant (P < 0.05) reduction in endogenous fat oxidation, from 57.8 t 6.8 g in the control situation to 42.3 t 8.1 and 44.7 t 8.7 g, respectively, when glucose and MCT were ingested (Table 1). On the other hand, endogenous carbohydrate oxidation was not modified (control 295.6 t 56.1 g; glucose 291.2 t 40.6 g; MCT 292.8 t 43.2 g). Several studies also reported that carbohydrate ingestion fails to spare endogenous carbohydrate stores (5). As for
OXIDATION
DURING
EXERCISE
the effect of exogenous lipids on endogenous carbohydrate utilization, three studies reported that ingestion of large amounts of MCT or LCT 3-5 h before exercise, associated with the activation of lipoprotein lipase by heparin administration, resulted in a marked increase in plasma free fatty acid concentrations and in fat oxidation, with a significant reduction in muscle glycogen utilization and improvement of endurance performance (6, 11,28). However, administration of MCT and LCT without activation of lipoprotein lipase was not associated with an increased contribution of fat to energy yield or a reduction in endogenous carbohydrate utilization (1, 7, 30). Results from the present experiment confirm these previous findings (Table 1). Indeed, the increased availability of free fatty acids from the gastrointestinal tract is compensated by a reduction in endogenous fat store utilization and no sparing of endogenous carbohydrates. This study was supported by grants from the Natural Sciences and Engineering Research Council of Canada, Fonds pour la Formation de Chercheurs et 1’Aide a la Recherche, Gouvernement du Quebec, and Centre de Recherche en Geochimie Isotopique et en Geochronologie, Universiti! du Quebec a Montreal. Address for reprint requests: D. Massicotte, Dept. de Kinanthropologie, Universite du Quebec a Montreal, C. P. 8888, Succursale “A,” Montreal, Quebec H3C 3P8, Canada. Received
3 July
1991; accepted
in final
form
17 April
1992.
REFERENCES 1. AUCLAIR, E., P. SATABIN, E. SERVAN, AND C. Y. GUEZENNEC. Metabolic effects of glucose, medium chain triglyceride and long chain triglyceride feeding before prolonged exercise in rats. Eur. J. Appl. Physiol. Occup. Physiol. 57: 126-131, 1988. 2. BACH, A. C., AND V. K. BABAYAN. Medium chain triglycerides: an update. Am. J. Clin. Nutr. 36: 950-962, 1982. 3. BARSTOW, T. J., D. M. COOPER, S. EPSTEIN, AND K. WASSERMAN. Changes in breath ‘3C0,1’2C02 consequent to exercise and hypoxia. J. Appl. Physiol. 66: 936-942, 1989. 4. BREMER, J. Carnitine and its role in fatty acid metabolism. Trends Biochem. Sci. 2: 207-209, 1980. 5. COGGAN, A. R., AND E. F. COYLE. Carbohydrate ingestion during prolonged exercise: effects on metabolism and performance. Exercise Sport Sci. Rev. 19: l-39, 1991. 6. COSTILL, D. L., E. COYLE, G. DALSKY, W. EVANS, W. FINK, AND D. HOOPES. Effects of elevated plasma FFA and insulin on muscle glycogen usage during exercise. J. Appl. Physiol. 43: 695-699, 1977. 7. DI?COMBAZ, J., M. J. ARNAUD, H. MILON, H. MOESCH, G. PHILLIPPOSSIAN, A. L. THELIN, AND H. HOWALD. Energy metabolism of medium-chain triglycerides versus carbohydrates during exercise. Eur. J. Appl. Physiol. Occup. Physiol. 52: 9-14, 1983. 8. DENIRO, M. J., AND S. EPSTEIN. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science Wash. DC 197: 261-263, 1977. 9. GALBO, H. K. Hormonal and Metabolic Adaptation to Exercise. New York: Thieme-Stratton, 1983. 10. GUEZENNEC, C. Y., P. SATABIN, F. DUFOREZ, D. MERINO, F. PJ~RONNET, AND J. KOZIET. Oxidation of corn starch, glucose, and fructose ingested before exercise. Med. Sci. Sports Exercise 21: 4560, 1989. 11. HICKSON, R. D., M. J. RENNIE, R. K. CONLEE, W. W. WINDER, AND J. 0. HOLLOSZY. Effects of increased plasma fatty acids on glycogen utilization and endurance. J. Appl. Physiol. 43: 829-833, 1977. 12. HOERR, R. A., Y. M. Yu, D. WAGNER, J. F. BURKE, AND V. R. YOUNG. Recovery of 13C in breath from Na H13C02 infused by the gut and the vein: effect of feeding. Am. J. Physiol. 257 (Endocrinol. Metab. 20): E426-E438, 1989. 13. IRVING, C. S., W. W. WONG, R. J. SCHULMAN, E. O’BRIEN SMITH, AND P. D. KLEIN. (‘“C) bicarbonate kinetics in humans: intra vs. interindividual variations. Am. J. Physiol. 245 (Regulatory Integrative Comp. Physiol. 14): R190-R202, 1983. 14. JACOBSON, B. S., B. N. SMITH, S. EPSTEIN, AND G. G. LATIES. The
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EXOGENOUS
15.
16.
17.
18.
19.
20.
21.
22.
23.
FAT
AND
GLUCOSE
prevalence of carbon-13 in respiratory carbon dioxide as an indicator of the type of endogenous substrate. J. Gen. Physiol. 55: l-17, 1970. JANDRAIN, B. J., F. PIRNAY, M. LACROIX, F. MOSORA, A. J. SCHEEN, AND P. LEFEBVRE. Effect of osmolality on availability of glucose ingested during prolonged exercise in humans. J. Appl. Physiol. 67: 76-82, 1989. KRZENTOWSKI, G., B. JANDRAIN, F. PIRNAY, F. MOSORA, M. LACROIX, A. LUYCKX, AND P. LEFEBVRE. Availability of glucose given orally during exercise. J. AppZ. Physiol. 56: 315-320, 1984. LEFEBVRE, P., F. MOSORA, M. LACROIX, F. PIRNAY, A. SCHEEN, G. KRZENTOWSKI, B. JANDRAIN, J. F. GAUTHIER, N. PALLIKARAKIS, J. P. RIOU, S. NORMAND, C. PACHIACIDI, AND Y. KHASALLAH. Letter to the editor. J. AppZ. Physiol. 71: 2059-2061, 1991. MASSICOTTE, D., F. P~RONNET, C. ALLAH, C. HILLAIRE-MARCEL, M. LEDOUX, AND G. BRISSON. Metabolic response to [‘“Clglucose and [ ‘3C]fructose ingestion during exercise. J. Appl. Physiol. 61: 1180-l 184, 1986. MASSICOTTE, D., F. PI~RONNET, G. BRISSON, K. BAKKOUCH, AND C. HILLAIRE-MARCEL. Oxidation of a glucose polymer during exercise: comparison with glucose and fructose. J. AppZ. Physiol. 66: 179-183, 1989. MASSICOTTE, D., F. P~RONNET, G. BRISSON, L. BOIVIN, AND C. HILLAIRE-MARCEL. Oxidation of exogenous carbohydrate during prolonged exercise in fed and fasted conditions. Int. J. Sports Med. 11: 253-258, 1990. PALLIKARAKIS, N., B. JANDRAIN, F. PIRNAY, F. MOSORA, M. LACROIX, A. LIJYCKX, AND P. LEFEBVRE. Remarkable metabolic availability of oral glucose during long-duration exercise in humans. J. AppZ. Physiol. 60: 1035-1042, 1986. PALLIKARAKIS, N., N. SPHIRIS, AND P. LEFEBVRE. Influence of the bicarbonate pool and on the occurrence of 13C0, in exhaled air. Eur. J. AppZ. Physiol. Occup. Physiol. 63: 179-183, 1991. PI%RONNET, F., E. ADOPO, AND D. MASSICOTTE. Exogenous substrate utilization during prolonged exercise: studies with 13C-la-
OXIDATION
24. 25.
26. 27.
28.
29.
30.
31.
32.
33.
DURING
EXERCISE
1339
beling. In: MuscZe Fatigue Mechanisms in Exercise and Training, edited by P. Marconnet, B. Saltin, 0. M. Sejersted, and P.V. Komi. Basel: Karger, 1992, p. 195-207. P~RONNET, F., AND D. MASSICOTTE. Table of nonprotein respiratory quotient: an update. Can. J. Sport Sci. 16: 23-29, 1991. P~RONNET, F., D. MASSICOTTE, G. R. BRISSON, AND C. HILLAIREMARCEL. Use of 13C substrates for metabolic studies in exercise: methodological considerations. J. AppZ. Physiol. 69: 1047-1052, 1990. PINELLI, A. A new calorimetric method for plasma fatty acid analysis. CZin. Chim. Acta 44: 385-390, 1973. PIRNAY, F., J. M. CRIELAARD, N. PALLIKARAKIS, M. LACROIX, F. MOSORA, G. KRZENTOWSKI, A. LUYCKX, AND P. LEFEBVRE. Fate of exogenous glucose during exercise of different intensities in man. J. AppZ. Physiol. 53: 1620-1624, 1982. RENNIE, M. J., W. W. WINDER, AND J. 0. HOLLOSZY. A sparing effect of increased plasma fatty acids on muscle and liver glycogen content in the exercising rat. Biochem. J. 156: 647-655, 1976. ROBERT, J. J., J. KOZIET, D. CHAUVET, D. DARMAUN, J. F. DESJEUX, AND V. R. YOUNG. Use of 13C-labeled glucose for estimating glucose oxidation: some design considerations. J. AppZ. Physiol. 63: 1725-1732, 1987. SATABIN, P., P. PORTERO, G. DEFER, J. BRICOUT, AND C. Y. GUEZENNEC. Metabolic and hormonal responses to lipid and carbohydrate diet during exercise in man. Med. Sci. Sports Exercise 19: 218-233,1987. SCHOELLER, D. A., M. MINAGAWA, R. SLATER, AND I. R. KAPLAN. Stable isotopes of carbon, nitrogen and hydrogen in the contemporary North American human food web. EcoZ. Food Nutr. 18: 159170, 1986. WOLFE, R. R., J. H. F. SHAW, E. R. NADEL, AND M. H. WOLFE. Effect of substrate intake and physiological state on background ‘“CO, enrichment. J. AppZ. Physiol. 56: 230-234, 1984. WOLFE, R. R., M. H. WOLFE, E. R. NADEL, AND J. H. F. SHAW. Isotopic determination of amino acid-urea interactions in exercise in humans. J. AppZ. Physiol. 56: 221-229, 1984.
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free fatty acids with glucose
D. MASSICOTTE, F. PERONNET, G. R. BRISSON, AND C. HILLAIRE-MARCEL Universite’ du Q&bee ti Mont&al, Universite’ de Montre’al, and Institut National de la Recherche Scientifique-Sante: Montreal, Quebec H3C 3P8, Canada MASSICOTTE, D., F. P~RONNET,G. R. BRISSON,AND C. HILLAIRE-MARCEL.Oxidation of exogenous medium-chain free fatty acids during prolonged exercise: comparison with glucose. J. Appl. Physiol. 73(4): 1334-1339, 1992.-The purpose of this study was to compare the oxidation rate of exogenous 13C-labeled medium-chain triacylglycerols (MCT) with that of an isocaloric amount of exogenous [ 13C]glucose and to evaluate their respective effects on endocrine and metabolic responses to moderate prolonged exercise. To take into account changes in isotopic composition of 13C0, arising from oxidation of endogenous substrates because of exercise and/or substrate ingestion that overestimates the oxidation rate of exogenous substrates, two levels of 13C enrichment were used for each substrate. Six young healthy males (20-26 yr of age) completed five 2-h periods of exercise at 65 * 3% maximal 0, uptake (VO, max) on a cycle ergometer at 7day intervals: one control exercise with water ingestion, two trials with ingestion of 25 g of [13C]MCT (trioctanoate) 1 h before exercise, and two trials with 57 g of [ ‘3C]glucose (dissolved in 1,000 ml of water) ingested during exercise. Exogenous MCT and glucose began to be oxidized within the first 30 min of exercise, and the oxidation rate increased progressively until the end of exercise for both substrates. Over the 2-h period of exercise, 13.6 t 3.5 g of ingested MCT and 36.4 -+ 8.2 g of exogenous glucose were oxidized, which represent 54 and 64%, respectively, of the total amount ingested. The contribution of MCT (119 & 31 kcal) and glucose (140 * 36 kcal) was not significantly different and represented 7 and 8.5%, respectively, of the total energy expenditure. For similar amounts of MCT and glucose ingested before or during a prolonged exercise, the contributions to the energy yield found in the present study are lower than those reported previously. Ingestion of MCT as well as glucose contributed to maintain blood glucose concentration, abolished the decrease in plasma insulin, reduced the rise of glucagon, and blunted the response of plasma epinephrine normally observed during prolonged exercise. Neither exogenous substrate reduced the endogenous carbohydrate utilization. carbon-13 labeling; fat-glucose ketone bodies; catecholamines;
ingestion; insulin
substrate
utilization;
SEVERAL STUDIES that deal with 13Cas tracer have reported that glucose (10, 15, 16, 18-21, 27, 30) and other types of carbohydrates, including fructose (10, 18, 20), glucose polymers (19), maltodextrins (7, 3O), and cornstarch (lo), ingested before or during an exercise period, significantly contribute to the energy yield. On the other hand, only two studies have investigated the oxidation of exogenous fatty acids ingested before a period of exercise (7,30). Satabin et al. (30) reported that only 9% of -44 g 1334
0161-7567/92 $2.00 Copyright
@I
of long-chain triacylglycerols (LCT) ingested 1 h before the . beginning of exercise at 60% maximal 0, uptake (VO 2,,,) were oxidized over a 2-h period of exercise. On the contrary, exogenous medium-chain triacylglycerols (MCT), which are delivered as free fatty acids into the blood more quickly than the ingested LCT (2), are oxidized to a greater extent: 32% of 25 g and 44% of -44 g ingested in the studies by Decombaz et al. (7) and Satabin et al. (30), respectively. These amounts were lower, however, than those of exogenous carbohydrates oxidized [maltodextrins: 45% of 50 g ingested (7); cornstarch: 80% of 100 g ingested (30)]. In all these previous studies, including our own reports (l&20), the production of 13C02at rest or during exercise without substrate ingestion has been used as a reference value to compute the oxidation of exogenous substrates. However, because of the process of isotopic fractioning, which takes place in the biosphere along the metabolic pathways from atmospheric CO, to plant carbohydrates and fat and subsequently to glycogen and to animal fat, the carbohydrate stores have a higher 13C/12Cratio than fat stores (831). Consequently, any changes in the composition of the mixture of oxidized endogenous substrates that are associated with both exercise and ingestion of substrates lead to changes in isotopic composition of expired CO, (3, 14, 25). We recently showed that failure to take into account changes in 13Cbackground enrichment of expired CO, leads to an overestimation of the amount of exogenous substrate oxidized (17,25). We also suggested a method to adequately take into account these changes (25). Accordingly, the goals of the present study were 1) to reassessthe oxidation rate of exogenous [ 13C]MCT ingested before a period of exercise, 2) to compare the oxidation rate of MCT with that of an isocaloric amount of exogenous [13C]glucose, and 3) to compare the effects of MCT and glucose ingestion on endocrine and metabolic responses to prolonged exercise. MATERIALS AND METHODS Subjects. Six healthy males volunteered for the study and gave their written informed consent. Their mean age, mass, height, and Tj0, maxwere 22.8 t 1.5 yr, 69.5 t 7.2 kg, 173.1 -t 6.6 cm, and 60.5 t 6.7 (SE) ml respectively. None was engaged in a regular training program at the time of the study. The subjects refrained from severe exercise and drinking alcohol during the 3 days preceding each test. l
-l.
min-‘,
kg
1992 the American
Physiological
Society
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EXOGENOUS
FAT
AND
GLUCOSE
Procedure. Each subject completed at H-day intervals five 2-h periods of exercise on an electrically braked cycle ergometer. The work load was kept constant during each trial (mean 188 t 21 W) and was adjusted for each subject to elicit an energy expenditure equivalent to 65 t 3% of his respective predetermined maximal aerobic power. Each test was conducted in the same environmental conditions (temperature 21 t 1°C; humidity 45 t 5%), between 9 and 12 A.M., after an overnight fast and a standardized breakfast taken 2 h before the beginning of exercise. The breakfast consisted of two slices of toasted brown bread, 50 g of white cheese, and 300 ml of unsweetened orange juice: -15 g protein, -15 g fat, -50 g carbohydrate, 1,500 kJ. The five exercises were one control trial (A) with ingestion of 1,000 ml of water only, two trials (B and C) with ingestion of 25 g of MCT (trioctanoate, Sigma Chemical) corresponding to 219 kcal(1 g = 8.76 kcal) and enriched with [13C]octanoate (Merck Frosst, Montreal, 13C/12Cisotopic ratio = 1.09100 and 1.12876%’ for trials B and C, respectively), and two trials (D and E) with ingestion of 57 g of glucose (Biopharm, Montreal) corresponding to 220 kcal (1 g = 3.87 kcal) and enriched with [13C]glucose (Merck Frosst, Montreal, 13C/12Cisotopic ratio = 1.11482 and l.l3303%l for triaZs D and E, respectively). The MCT were ingested in a hot drink flavored with vanilla 1 h before the beginning of exercise to allow an adequate absorption time (2). The glucose was dissolved in 1,000 ml of water (6%) divided into eight equal volumes (125 ml + 7.1 g of glucose), which were ingested every 15 min from 0 to 105 min during the exercise period. Water was also ingested (125 ml every 15 min) during trials A-C. The order of presentation of the five trials was randomized among the subjects. Measures. All measures (expired gasesand blood) were taken at rest before the ingestions and every 30 min thereafter until the end of the exercise period. Expired gases were collected and analyzed (Pneumoscan, Morgan; S-A3 and CD-3A analyzers, Amteck) for computation of 0, uptake (Tj,z), CO, production #CO,), and respiratory exchange ratio (RER). For 13C/12Canalysis of expired CO,, a 2O-ml sample of expired air was collected in a glass sample holder prevacuumed at 10m2Torr. After removal of water vapor through a two-step trapping [I) in liquid nitrogen (-196”C), then 2) release of CO, by warming with an acetone dry ice slush ( -80°C)], the CO, was introduced into a double-inlet mass spectrometer (Micromass Sira 12) for 13C/12Cdetermination. Blood samples were withdrawn through a flexible catheter (Cathlon IV) from an antecubital vein kept open with a saline line. The samples were analyzed for glucose (reagent kit, Boehringer), free fatty acids (26), ,&hydroxybutyrate, insulin, glucagon (Bio-RIA, Montreal), and catecholamine (Amersham) concentrations. Blood sampling and analysis were done in the control situation and during one of each of the two trials with MCT and glucose ingestion. Exogenous substrate oxidation. The oxidation rates of ingested MCT and glucose were computed with the equation ’ 613C PDB
- 1 = - 29.1%o (B); + 4.5%0 (C);
- 7.8%0 (D);
+ 8.3%0 (E)
OXIDATION
DURING
1335
EXERCISE
x = vco,*
Rexp2 R exo
2 -
R exp R exo
1 . 1
-1 k
where x is the amount of ingested substrate oxidized (in grams); VCO, is the volume of expired CO,; R is the isotopic composition of expired CO, (exp) and ingested substrate (exo); the numbers 1 and 2 correspond to the two experiments with ingestion of the exogenous substrate; and k is the amount of CO, produced by the oxidation of the exogenous substrate (1.2369 liters CO,/g of MCT and 0.7426 liter CO,/g of glucose). This computation procedure takes into account the isotopic composition of expired CO, arising from oxidation of endogenous substrates (13C background), the composition of which can be computed as cRendo) (vco20Rexp~) - (X’k’Rexol) R endo = vco, - (x0 k) As discussed previously (25), the procedure commonly used for computing ex ogenous substrate oxidation does not take into account changes in Rendo due to exercise and/or exogenous substrate ingestion. The alternate procedure suggested by Wolfe et al. (32) for computation of exogenous glucose oxidation takes into account only changes in the isotopic composition of blood glucose due to administration of labeled exogenous glucose but is not appropriate “if there is a marked change in the metabolic state (e.g., exercise)” (Ref. 32, p. 233) and if Rend0is modified. Overall carbohydrate and fat oxidation were computed from VO, and VCO,/VO, taken as a nonprotein respiratory quotient (24). When exogenous substrates were ingested and oxidized, the amounts of endogenous substrates oxidized were computed by difference. Statistics. Comparisons were made by a two-way analvsis of variance with repeated measures (trials X time) for the overall substrate utilization and blood hormonal and biochemical parameters. Significant differences (P < 0.05) were located by a Newman-Keuls post hoc test. RESULTS
Changes in Rexpin response to exercise with ingestion of water, MCT, and glucose are shown in Fig. 1. Exercise with water ingestion was associated with a significant change in the isotopic composition of expired CO, (Rexp= Rendo).Table 1 presents the amounts of exogenous and endogenous fat and carbohydrates oxidized during the exercise period. Over the 2 h, 13.6 t 3.5 g of exogenous MCT and 36.4 t 8.2 g of exogenous glucose were oxidized, representing 54 and 64%, respectively, of the total amounts ingested. For both exogenous substrates, the oxidation rate was larger during the 2nd than during the 1st h of exercise. Only one-third of the total amounts of MCT (4.1 of 13.6 g) and glucose utilized (12.5 of 36.4 g) was oxidized during the 1st h of exercise (Table 1). Ingestion of MCT and glucose did not contribute to the reduction of endogenous carbohydrate utilization. In fact, a reduction of endogenous fat store utilization was observed for both exogenous substrates (Table 1). Although the amount of exogenous MCT oxidized was lower than the amount of exogenous glucose oxidized,
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1336
EXOGENOUS 1.10600
l
CONTROL
n
LEVEL
1
0
LEVEL
2 I
FAT
AND
GLUCOSE
OXIDATION
DURING 5o01
GLUCOSE 1.10400
A LEVEL
1
A LEVEL
2 I
z-
. CONTROL ) n GLUCOSE 400A MCT
MCT
‘;;b 31.10200 G
0
t t t 5 1
!A
1.10000
1.09800 7//I
1
40
-30
1
1
0
30
I
I
60
90
1
120
+-REST*-EXERCISE,-+j TIME (min)
1. Isotopic composition medium-chain triacylglycerols. FIG.
of expired
CO,
(means
+ SE).
MCT,
the contribution of MCT and glucose to the energy yield was not significantly different (119 t 31 vs. 140 t 36 kcal, respectively). In the control trial with water ingestion, the progressive decrease in blood glucose concentration over the exercise period (P < 0.05 at the 120th min) was accompanied by a reduction in plasma insulin concentration and a rise in glucagon, free fatty acids, P-hydroxybutyrate, and epinephrine concentrations (Figs. 2-4). Glucose as well as MCT ingestion contributed to maintain blood glucose concentration during the 2-h period of exercise (Fig. 2). 1. Overall substrate
1
1
I
1
T
T
I
7-
3$
Ok
TABLE
**t * mtt
EXERCISE
I
1
1
-60 -30 ~-REST~~EXE~R~CISE-?
utilization
1
1 90
A * 1
120
TIME (min)
Ingestion Exercise Time, min Substrates O-60 Carbohydrates Total Endogenous Exogenous Fat Total Endogenous Exogenous 60-120 Carbohydrates Total Endogenous Exogenous Fat Total Endogenous Exogenous O-120 Carbohydrates Total Endogenous Exogenous Fat Total Endogenous Exogenous
Water (control)
153.3k24.8 153.3k24.8
25.123.1 25.1k3.1
142.3k21.1 142.3k21.1
Conditions
Glucose
174.8+ 18.5* 162.3k17.9 12.5k2.4 18.3+2.7* 18.3+2.7*
152.8+18.1 128.9+ 19.3 23.9k5.2
2. Plasma glucose, insulin, and glucagon concentrations (means + SE) during control exercise and with glucose or lipid ingestion. “‘7 S’g1 nl ‘f icant (P < 0.05) differences from resting value and control exercise, respectively. FIG.
MCT
148.5k19.2 148.5kl9.2
27.2k3.8 23.1k3.9 4.1kO.9
144.3k21.6 144.3221.6
32.723.3 32.7k3.3
24.Ok3.8 24.0k3.8
31.1k4.5 21.6t4.3* 9.5t2.2
295.6k56.1 295.6k56.1
327.6+43.4* 291.2k40.6 36.4k9.5
292.8t43.2 292.8k43.2
57.8~16.8 57.8k6.8
42.3-+8.1* 42.3*8.1*
58.3k9.1 44.7+8.7* 13.6k3.5
Values are means + SE in grams. MCT, medium-chain triacylglycerols. * Significantly different (P < 0.05) from control exercise (water).
When compared with the glucose trial, MCT ingestion resulted in similar effects for plasma insulin, glucagon, and catecholamine concentrations, whereas the free fatty acid and P-hydroxybutyrate levels were significantly higher (P < 0.05; Figs. 2-4). DISCUSSION
Exogenous oxidation of MCT vs. glucose. Results indicate that the contributions of exogenous MCT and glucose to energy yield were similar during the exercise period. Indeed, over the 2-h period of exercise, 13.6 t 3.5 g of MCT (corresponding to 119 t 31 kcal) were oxidized compared with 36.4 t 9.5 g (representing 140 t 36 kcal) of glucose (Table 1). This observation is in accordance with previous findings by Decombaz et al. (7), who reported that, over a 60-min period of exercise at 60% . vo 2 maxy exogenous MCT provided 70 t 7 kcal compared with 85 t 6 kcal for exogenous maltodextrins. On the other hand, a higher contribution of exogenous cornstarch (320 vs. 180 kcal for MCT) was observed by Satabin et al. (30) over a 2-h period of exercise performed at 60% ire, max.In both studies, as well as in the present experiment, the MCT were given 1 h before the begin-
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EXOGENOUS 2.5
. 1
FAT
AND
GLUCOSE
CONTROL
n
“t T
GLUCOSE
It
0
2.0
1
I)
+
T
1
OXIDATION
DURING
1337
EXERCISE
those reported in the studies by Decombaz et al. (7) (11 and 14%, respectively) and Satabin et al. (30) (13 and 24%, respectively). As discussed previously (25) dealing with oxidation of exogenous glucose during exercise, these discrepancies are likely to be due to differences in the computation procedures used. In the studies by Decombaz et al. (7) and Satabin et al. (30), it was assumed that Rend0during exercise was similar to that observed at rest. As shown in Fig. 1, changes in the isotopic composition of expired CO, during exercise with water ingestion indicate that Rendois modified by the change in the composition of the mixture of endogenous substrates oxidized (3, 25). This different isotopic composition of endogenous substrates results from the isotopic fractioning along the food chains, the 13C/12Cratio being higher in carbohydrate than in fat stores (8, 31, 33). With the hypothesis that Rend0remains constant, 13Crecovery is overestimated and leads to an overestimation of the amount of exogenous substrates oxidized. In fact, if the method of computation utilized by Decombaz et al. (7) and Satabin et al. (30) is used in the present protocol and Rexpat rest is taken as the reference value for Rendo,the oxidation rate of MCT computed in experiment B (R,,, = 1.12876%) would be 14.7 g during the 1st h and 32.5 g over the 2-h period of exercise, which is greater than the amount ingested. I)
2400
.
CONTROL
L
I)
m GLUCOSE 0 -60
I -30
I 0
I 30
1 60
I 90
1
120
+--REST-+pEXE~~~s~----q
Ii E b --a1600
A MCT
TIME (min) FIG.
tions
3. Plasma free fatty (means t- SE). Symbols
acid and P-hydroxybutyrate as in Fig. 2.
concentra-
ning of exercise to optimize their absorption and availability during the exercise. Unlike LCT, which enter the blood through the lymphatic circulation and consequently are not readily available for oxidation after ingestion, MCT directly enter the bloodstream through the portal circulation (2) and, when taken up by the muscles, cross the mitochondrial membrane through a direct activation process independent of the acylcarnitine transferase system (4). This explains why, as shown by changes in the isotopic composition of expired CO, (Fig. l), MCT begin to be oxidized within the first 30 min of exercise. Obviously, exogenous glucose is much more readily available than MCT and begins to be oxidized within minutes after ingestion (Fig. 1). The oxidation rate of ingested glucose was related to the energy expenditure [glucose (kcal/min) = -1.548 + 0.197 (kcal), r = 0.7961, a phenomenon already outlined by Pirnay et al. (27) in 1982 and recently discussed by Peronnet et al. (23). Data (Fig. 5) indicate that, in the present study, the oxidation rate of exogenous MCT was also related to the energy expenditure [MCT (kcal/ min) = -1.760 + 0.198 kcal, r = 0.5811. However, when expressed in percentage of the total energy yield during the exercise period, the respective contributions of MCT and glucose observed in the present experiment (7.0 t 1.7 and 8.5 t l.4%, respectivelv) are much lower than
2 w Z ii
E
800
g T 0
1200
4/,
I
I
I
1
I
1 I
1
l
sJ^ E 2 800
0 -60 p--
-30 REST
0 30 ~--‘1‘~EXERCISE~~~
60
90
120
TIME (mln) FIG. 4. Plasma bols as in Fig. 2.
catecholamine
concentrations
(means
+ SE).
Sym-
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1338
EXOGENOUS
3.0
PRESENT STUDY DiCOMBAZ et al. 1983 SATABIN et al. 1987
1
FAT n
AND
GLUCOSE
A
AI 0 q 2A2
02
2.5-z .% E 2.0 2A"
2 if 2 1.5z E s l.Ox 0 0.5 J 0 ‘c/r
1 10 ENERGY
1 12 EXPENDITURE
I 14
1 16 (kcal/min)
FIG. 5. Oxidation rate of exogenous substrates: -1.760 + 0.198 kcal, r = 0.581; glucose (kcal) = -1.548 0.796.0, Glucose; & Medium-chain triacylglycerols;
MCT (kcal) = + 0.197 kcal, r = 0, maltodextrins.
Another methodological problem, when production of 13C0, is used to measure the oxidation rate of 13C-labeled exogenous substrate, concerns the trapping of 13C0, in the bicarbonate pool and/or the delay between 13C0, production in the tissue and the appearance of 13C0, in expired gas. The bicarbonate-carbonate pool, particularly in the form of calcium carbonates in bone tissue, constitutes a very slow exchange pool in which an amount of CO, arising from decarboxylation of energy substrates disappears each minute (l&13,29). At rest, -20% of the CO, produced is irreversibly trapped in this pool, and a correction should be made to compute 13Crelease from expired CO, (12,29). However, due to the increase of CO, production during exercise, the amount of 13C0, lost in the pool becomes negligible. In fact, the amount of CO, recovered approaches 100% (2233). Morever, exogenous substrate oxidation is computed over a long period of time (>l h) in a physiological steady-state condition. This allows enough time to equilibrate 13C0, expired with the plasma 13C0,/H13C0, pool (33). Endocrine and metabolic response to MCT and glucose ingestion. Ingestion of MCT before, as well as glucose during, exercise prevented a small but significant reduction in blood glucose concentration observed at the end of exercise with water ingestion (Fig. 2). Maintenance of blood glucose level abolished the progressive decrease in plasma insulin, reduced the rise of plasma glucagon, and markedly blunted the response of plasma epinephrine concentrations normally observed in response to prolonged exercise (Figs. 2-4) (Ref. 9, p. 12 and 38). These hormonal changes were associated with a significant (P < 0.05) reduction in endogenous fat oxidation, from 57.8 t 6.8 g in the control situation to 42.3 t 8.1 and 44.7 t 8.7 g, respectively, when glucose and MCT were ingested (Table 1). On the other hand, endogenous carbohydrate oxidation was not modified (control 295.6 t 56.1 g; glucose 291.2 t 40.6 g; MCT 292.8 t 43.2 g). Several studies also reported that carbohydrate ingestion fails to spare endogenous carbohydrate stores (5). As for
OXIDATION
DURING
EXERCISE
the effect of exogenous lipids on endogenous carbohydrate utilization, three studies reported that ingestion of large amounts of MCT or LCT 3-5 h before exercise, associated with the activation of lipoprotein lipase by heparin administration, resulted in a marked increase in plasma free fatty acid concentrations and in fat oxidation, with a significant reduction in muscle glycogen utilization and improvement of endurance performance (6, 11,28). However, administration of MCT and LCT without activation of lipoprotein lipase was not associated with an increased contribution of fat to energy yield or a reduction in endogenous carbohydrate utilization (1, 7, 30). Results from the present experiment confirm these previous findings (Table 1). Indeed, the increased availability of free fatty acids from the gastrointestinal tract is compensated by a reduction in endogenous fat store utilization and no sparing of endogenous carbohydrates. This study was supported by grants from the Natural Sciences and Engineering Research Council of Canada, Fonds pour la Formation de Chercheurs et 1’Aide a la Recherche, Gouvernement du Quebec, and Centre de Recherche en Geochimie Isotopique et en Geochronologie, Universiti! du Quebec a Montreal. Address for reprint requests: D. Massicotte, Dept. de Kinanthropologie, Universite du Quebec a Montreal, C. P. 8888, Succursale “A,” Montreal, Quebec H3C 3P8, Canada. Received
3 July
1991; accepted
in final
form
17 April
1992.
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