Professional Documents
Culture Documents
Lipid Metabolism During Endurance Exercise1,2,3
Lipid Metabolism During Endurance Exercise1,2,3
ABSTRACT Endogenous triacylglycerols represent an plasma and the delivery of the released fatty acids to skeletal mus-
important source of fuel for endurance exercise. Triacylglycerol cle mitochondria for oxidation. In this article, we will discuss the
oxidation increases progressively during exercise; the specific relation between fatty acid mobilization and fat oxidation during
rate is determined by energy requirements of working muscles, exercise in humans and review the influence of lipid supplementa-
fatty acid delivery to muscle mitochondria, and the oxidation of tion on substrate metabolism during exercise.
other substrates. The catecholamine response to exercise increases
lipolysis of adipose tissue triacylglycerols and, presumably, intra-
muscular triacylglycerols. In addition, increases in adipose tis- LIPID KINETICS DURING REST AND EXERCISE
sue and muscle blood flow decrease fatty acid reesterification and After an overnight fast, most energy needs at rest are provided
facilitate the delivery of released fatty acids to skeletal muscle. by oxidizing fatty acids derived from adipose tissue triacylglyc-
Alterations in fatty acid mobilization and the relative use of adi- erols (1). Adipose tissue lipolytic activity is regulated by the bal-
pose and intramuscular triacylglycerols during exercise depend, ance between hormones that stimulate (primarily catecholamines)
in large part, on degree of fitness and exercise intensity. Com- and those that inhibit hormone-sensitive lipase (primarily
pared with untrained persons exercising at the same absolute insulin), which hydrolyzes triacylglycerols to fatty acids and
intensity, persons who have undergone endurance training have glycerol. At rest, the amount of fatty acids released from adipose
greater fat oxidation during exercise without increased lipolysis. tissue typically exceeds the amount oxidized; fatty acid rate of
Available evidence suggests that the training-induced increase in appearance into plasma (Ra) is approximately twice the rate of
fat oxidation is due primarily to increased oxidation of non- fatty acid oxidation (2). Therefore, a large portion of fatty acids
plasma-derived fatty acids, perhaps from intramuscular triacyl- liberated by lipolysis of adipose tissue triacylglycerols are
glycerol stores. Fat oxidation is lower in high-intensity exercise reesterified back into triacylglycerols, principally by the liver.
than in moderate-intensity exercise, in part because of decreased Mild- or moderate-intensity exercise [25–65% of maximal oxy-
·
fatty acid delivery to exercising muscles. Parenteral lipid supple- gen consumption (VO2max)] is associated with a 5–10-fold
mentation during high-intensity exercise increases fat oxidation, increase in fat oxidation above resting amounts (3) because of
but the effect of ingesting long-chain or medium-chain triacyl- increased energy requirements of muscle and enhanced fatty acid
glycerols on substrate metabolism during exercise is less clear. availability. A large portion of the increased supply of fatty acids
This review discusses the relation between fatty acid mobilization is provided by lipolysis of adipose tissue triacylglycerols, which
and oxidation during exercise and the effect of endurance train- increases 2–3-fold (4, 5) and is mediated by increased -adrenergic
ing, exercise intensity, and lipid supplementation on these stimulation (6, 7). In addition, the percentage of released fatty
responses. Am J Clin Nutr 2000;72(suppl):558S–63S. acids that are reesterified decreases by half (4), presumably
because of alterations in blood flow that facilitate the delivery of
KEY WORDS Adipose tissue, intramuscular triacylglycerol, fatty acids from adipose tissue to working muscles. Moderate-
lipolysis, fatty acids, glycerol, medium-chain triacylglycerol, sta- intensity exercise doubles adipose tissue blood flow (8, 9) and
ble isotopes, exercise, endurance training, lipid supplementation causes a > 10-fold increase in skeletal muscle blood flow (10).
Increasing the removal of fatty acids from adipose tissue by
increasing adipose tissue blood flow may also be necessary to
INTRODUCTION
Endogenous triacylglycerols represent the largest fuel reserve
1
in the body. Most triacylglycerols are stored in adipose tissue From the Department of Internal Medicine, Washington University
(17 500 mmol in a lean adult man), but they are also present School of Medicine, St Louis.
2
Supported by National Institutes of Health grants DK 37948, RR-0036
in skeletal muscle (300 mmol) and plasma (0.5 mmol). The
(General Clinical Research Center), RR-00954 (Mass Spectrometry Resource),
total amount of energy stored as triacylglycerol (560 MJ) is
AG-13629 (Claude Pepper Older American Independence Center), AG-00078
> 60 times the amount stored as glycogen (9 MJ). Thus, fatty (Institutional National Research Service Award), and DK-56341 (Clinical
acid oxidation during endurance exercise permits sustained phys- Nutrition Research Unit).
ical activity and delays the onset of glycogen depletion and hypo- 3
Address reprint requests to S Klein, Washington University School of
glycemia. The use of fatty acids as a fuel requires hydrolysis of Medicine, 660 South Euclid Avenue, Box 8127, St Louis, MO 63110-1093.
triacylglycerols (ie, lipolysis) from adipose tissue, muscle, and E-mail: sklein@imgate.wustl.edu.
558S Am J Clin Nutr 2000;72(suppl):558S–63S. Printed in USA. © 2000 American Society for Clinical Nutrition
EXERCISE AND LIPID METABOLISM 559S
in muscle (55, 56). Malonyl-CoA, in turn, inhibits the enzyme FUTURE DIRECTIONS
responsible for long-chain fatty acid (ie, fatty acids with > 12 car- Future studies designed to determine the factors regulating the
bon atoms) entry into mitochondria (carnitine O-palmitoyltrans- mobilization and oxidation of fatty acids derived from different
ferase-I, or CPT-I) (57–59). Thus, high rates of glycogenolysis sources may improve our understanding of how to use this vast
during high-intensity exercise may modify fat oxidation by energy store during exercise. The available data suggest that the
impairing long-chain fatty acid transport into the mitochondria regulation of lipolysis is different for muscle and adipose tissue
via CPT-I inhibition (54). triacylglycerols. Moreover, adipose tissue metabolism is hetero-
geneous, depending on the anatomical site of the depot (visceral,
subcutaneous abdominal, or subcutaneous gluteal or femoral).
EFFECT OF LIPID SUPPLEMENTATION Little is known about the relative contribution of fatty acids
Providing a lipid emulsion with heparin intravenously during derived from these different triacylglycerol sources to energy
exercise can increase fat oxidation by 30% when low endoge- production during exercise. As discussed, indirect or imprecise
nous fatty acid Ra and plasma fatty acid concentrations limit the methods of measuring IMTG concentration have resulted in con-
rate of fat oxidation, such as during high-intensity exercise (52, flicting findings regarding the use of IMTG during exercise.
60, 61). However, lipid infusion before or during exercise is not Improved techniques of measuring IMTG concentration will elu-
a practical approach to enhancing fat oxidation. Eating a high- cidate the importance of this energy source during exercise.
fat meal, which consists primarily of long-chain triacylglycerol To date, the relative contribution of plasma triacylglycerols to
(LCT), before exercise is also not practical as a direct source of energy production during exercise remains unclear. Because fat
fat during exercise because of delayed and limited availability ingestion increases plasma triacylglycerol concentration, quanti-
of ingested fat for skeletal muscle oxidation. LCTs are emptied fying the contribution of this energy source during exercise will
slowly from the stomach and must be packaged into chylomi- resolve whether lipid supplementation (ie, fat ingestion) can
crons, which are secreted into the lymphatic system before contribute substantially to energy production during exercise.
entering the bloodstream. Only a small portion of exogenous
LCT is oxidized within 6 h of ingestion (62). Furthermore,
although the addition of LCT to a high-glycemic carbohydrate SUMMARY
meal blunts the glucose and insulin responses to carbohydrate Endogenous triacylglycerols present in adipose tissue and
ingestion at rest (63–66), it does not significantly alter fat oxi- skeletal muscle are an important source of fuel during
dation or plasma glucose, fatty acid, and glycerol concentra- endurance exercise. The increased use of triacylglycerol during
tions during the subsequent exercise bout (63). exercise represents a careful integration of neural, hormonal,
Unlike LCTs, medium-chain triacylglycerols (MCTs) (ie, those circulatory, and muscular events that increase energy require-
primarily containing fatty acids with 8 and 10 carbon atoms) are ments and facilitate delivery of fatty acids from adipose tissue
emptied rapidly from the stomach and are rapidly absorbed and and IMTG stores to skeletal muscle mitochondria for oxida-
hydrolyzed by the small intestine (67). Furthermore, medium- tion. Exogenous triacylglycerol supplementation, via lipid and
chain fatty acids are not reesterified and are more easily trans- heparin infused directly into the circulation, indeed increases
ported into the mitochondria for subsequent oxidation than are fat oxidation when endogenous plasma fatty acid concentration
fatty acids from LCT (67, 68). The potential usefulness of MCT as is low. However, lipid ingestion in the form of either LCT or
a readily available source of energy has led to its inclusion as an tolerated amounts of MCT has a limited effect on substrate
ingredient in some commercially available sports bars. metabolism during exercise.
The amount of MCT that can be tolerated at one time is lim-
ited to 25–30 g; ingesting larger amounts causes adverse gas-
trointestinal symptoms, such as nausea and diarrhea (69, 70). REFERENCES
Ingesting 25–30 g MCT before exercise does not increase total 1. Klein S, Young VR, Blackburn GL, Bistrian BR, Wolfe RR. Palmi-
fat oxidation (69, 71) or spare muscle glycogen (70) during exer- tate and glycerol kinetics during brief starvation in normal weight
cise, because this amount of ingested MCT is oxidized at a rate young adult and elderly subjects. J Clin Invest 1986;78:928–33.
of only 6–9 g/h (71, 72) and therefore provides only a small 2. Klein S, Peters EJ, Holland OB, Wolfe RR. Effect of short- and
long-term beta-adrenergic blockade on lipolysis during fasting in
amount of energy (0.2–0.3 MJ/h). More MCT can be tolerated
humans. Am J Physiol 1989;257:E65–73.
when small aliquots are ingested throughout prolonged exercise 3. Krogh A, Lindhard J. The relative value of fat and carbohydrate as
(73, 74). Van Zyl et al (73) found that, compared with carbohy- sources of muscular energy. Biochem J 1920;14:290–363.
drate ingestion alone, the ingestion of MCT (30 g/h) added to 4. Wolfe RR, Klein S, Carraro F, Weber JM. Role of triglyceride-fatty
·
carbohydrate during 2 h of cycling at 60% of VO2max reduced acid cycle in controlling fat metabolism in humans during and after
the calculated rate of muscle glycogen oxidation and slightly exercise. Am J Physiol 1990;258:E382–9.
improved performance (3%) during a simulated 40-km time 5. Klein S, Coyle EF, Wolfe RR. Fat metabolism during low-intensity
trial. In contrast, Jeukendrup et al (74) found that the addition of exercise in endurance-trained and untrained men. Am J Physiol
85 g MCT to a 10%-carbohydrate solution ingested while 1994;267:E934(40.
· 6. Hall PE, Smith SR, Jack DB, Kendall MJ. The influence of beta-
cycling for 2 h at 60% of VO2max neither altered muscle glyco-
adrenoceptor blockade on the lipolytic response to exercise. J Clin
gen use nor improved cycling performance during a subse-
Pharm Ther 1987;12:101–16.
quent 15-min time trial. Thus, ingestion of a large dose of MCT 7. Arner P, Kriegholm E, Engfeldt P, Bolinder J. Adrenergic regulation
(85 g) in addition to carbohydrate during a 2-h period of exer- of lipolysis in situ at rest and during exercise. J Clin Invest 1990;
cise may reduce muscle glycogenolysis and slightly improve 85:893–8.
performance during a subsequent exercise bout lasting 1 h (73) 8. Bulow J, Madsen J. Adipose tissue blood flow during prolonged,
but not during shorter bouts (lasting 15 min) (74). heavy exercise. Pflugers Arch 1976;363:231–4.
562S HOROWITZ AND KLEIN
9. Bulow J, Madsen J. Influence of blood flow on fatty acid mobiliza- 32. Kiens B, Lithell H. Lipoprotein metabolism influenced by training-
tion from lipolytically active tissue. Pflugers Arch 1981;390:169–74. induced changes in human skeletal muscle. J Clin Invest 1989;
10. McArdle WD, Katch FI, Katch VL. Exercise physiology: energy, 83:558–64.
nutrition, and human performance. Philadelphia: Lea & Febiger, 33. Holloszy JO. Biochemical adaptations to exercise: aerobic metabo-
1991:335. lism. In: Wilmore J, ed. Exercise and sport sciences reviews. New
11. Hodgetts V, Coppack SW, Frayn KN, Hockaday TDR. Factors con- York: Academic Press, 1973:45–71.
trolling fat mobilization from human subcutaneous adipose tissue 34. Henriksson J. Training induced adaptation of skeletal muscle and
during exercise. J Appl Physiol 1991;71:445–51. metabolism during submaximal exercise. J Physiol (Lond) 1977;
12. Spector AA. Fatty acid binding to plasma albumin. J Lipid Res 270:661–75.
1975;16:165–79. 35. Holloszy JO. Effects of exercise on mitochondrial oxygen uptake
13. Kanaley JA, Cryer PE, Jensen MD. Fatty acid kinetic responses to and respiratory enzyme activity in skeletal muscle. J Biol Chem
1967;242:2278–82.
exercise. Effects of obesity, body fat distribution, and energy-
36. Saltin B, Gollnick PD. Skeletal muscle adaptability: significance for
restricted diet. J Clin Invest 1993;92:255–61.
metabolism and performance. In: Peachy LD, Adrian RH, Geiger
14. Romijn JA, Coyle EF, Sidossis L, et al. Regulation of endogenous
SR, eds. Handbook of physiology—skeletal muscle. Baltimore:
fat and carbohydrate metabolism in relation to exercise intensity and
Williams & Wilkins, 1983:555–631.
duration. Am J Physiol 1993;265:E380–91. 37. Mole PA, Oscai LB, Holloszy JO. Adaptation of muscle to exercise.
15. Martin WH 3rd, Dalsky GP, Hurley BF, et al. Effect of endurance Increase in levels of palmityl CoA sythetase, carnitine palmityl-
training on plasma free fatty acid turnover and oxidation during transferase, and palmityl CoA dehydrogenase and in the capacity to
exercise. Am J Physiol 1993;265:E708–14. oxidize fatty acids. J Clin Invest 1971;50:2323–30.
16. Carlson LA, Eklund LG, Froberg SO. Concentration of triglyc- 38. Turcotte LP, Kiens B, Richter EA. Saturation kinetics of palmitate
erides, phospholipids, and glycogen in skeletal muscle and of free uptake in perfused skeletal muscle. FEBS Lett 1991;279:327–9.
fatty acids and -hydroxybutyric acid in blood in man in response 39. Turcotte LP, Swenberger JR, Tucker MZ, Yee AJ. Training-induced
to exercise. Eur J Clin Invest 1971;1:248–54. elevation in FABPpm is associated with increased palmitate use in
17. Froberg SO, Mossfeldt F. Effect of prolonged strenuous exercise on contracting muscle. J Appl Physiol 1999;87:285–93.
the concentration of triglycerides, phospholipids, and glycogen in 40. Despres JP, Bouchard C, Savard R, Tremblay A, Marcotte M, The-
muscles of man. Acta Physiol Scand 1971;82:167–71. riault G. Level of physical fitness and adipocyte lipolysis in
18. Essen B. Intramuscular substrate utilization during prolonged exer- humans. J Appl Physiol 1984;56:1157–61.
cise. Ann N Y Acad Sci 1977;301:30–44. 41. Crampes F, Beauville M, Riviere D, Garrigues M. Effect of physi-
19. Hurley BF, Nemeth PM, Martin WH 3rd, Hagberg JM, Dalsky GP, cal training in humans on the response of isolated fat cells to epi-
Holloszy JO. Muscle triglyceride utilization during exercise: effect nephrine. J Appl Physiol 1986;61:25–9.
of training. J Appl Physiol 1986;60:562–7. 42. Crampes F, Riviere D, Beauville M, Marceron M, Garrigues M.
20. Jansson E, Kaijser L. Substrate utilization and enzymes in skeletal Lipolytic response of adipocytes to epinephrine in sedentary and
muscle of extremely endurance-trained men. J Appl Physiol 1987; exercise trained subjects: sex-related differences. Eur J Appl Phys-
62:999–1005. iol 1989;59:249–55.
21. Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GJ, Grant 43. Riviere D, Crampes F, Beauville M, Garrigues M. Lipolytic
SM. Progressive effect of endurance training on metabolic adapta- responses of fat cells to catecholamines in sedentary and exercise-
tions in working skeletal muscle. Am J Physiol 1996;270:E265–72. trained women. J Appl Physiol 1989;66:330–5.
22. Dyck DJ, Bonen A. Muscle contraction increases palmitate esterifi- 44. Stallknecht B, Simonsen L, Bulow J, Vinten J, Galbo H. Effect of
cation and oxidation and triacylglycerol oxidation. Am J Physiol training on epinephrine-stimulated lipolysis determined by micro-
1998;275:E888–96. dialysis in human adipose tissue. Am J Physiol 1995;269:E1059–66.
23. Kiens B, Essen-Gustavsson B, Christensen NJ, Saltin B. Skeletal 45. Galbo H, Richter EA, Holst JJ, Christensen NJ. Diminished hor-
muscle substrate utilization during submaximal exercise in man: monal responses to exercise in trained rats. J Appl Physiol 1977;43:
953–8.
effect of endurance training. J Physiol 1993;469:459–78.
46. Winder WW, Hickson RC, Hagberg JM, Ehsani AA, Mclane JA.
24. Kiens B, Richter EA. Utilization of skeletal muscle triacylglycerol
Training-induced changes in hormonal and metabolic responses to
during postexercise recovery in humans. Am J Physiol 1998;275:
submaximal exercise. J Appl Physiol 1979;46:766–71.
E332–7.
47. Martin WH III, Coggan AR, Spina RJ, Saffitz JE. Effects of fiber
25. Starling RD, Trappe TA, Parcel AC, Kerr CG, Fink WJ, Costill DL.
type and training on -adrenoceptor density in human skeletal mus-
Effects of diet on muscle triglyceride and endurance performance.
cle. Am J Physiol 1989;257:E736–42.
J Appl Physiol 1997;82:1185–9.
48. Klein S, Weber JM, Coyle EF, Wolfe RR. Effect of endurance train-
26. Bergman BC, Butterfield GE, Wolfel EE, Casazza GA, Lopaschuk
ing on glycerol kinetics during strenuous exercise in humans.
GD, Brooks GA. Evaluation of exercise and training on muscle lipid
Metabolism 1996;45:357–61.
metabolism. Am J Physiol 1999;276:E106–17. 49. Kjaer M, Christensen NJ, Sonne B, Richter EA, Galbo H. Effect of
27. Wendling PS, Peters SJ, Heigenhauser GJF, Spriet LL. Variability of exercise on epinephrine turnover in trained and untrained male sub-
triacylglycerol content in human skeletal muscle biopsy samples. jects. J Appl Physiol 1985;59:1061–7.
J Appl Physiol 1996;81:1150–5. 50. Kjaer M, Galbo H. Effect of physical training on the capacity to
28. Ryan WG, Schwartz TB. Dynamics of plasma triglyceride turnover secrete epinephrine. J Appl Physiol 1988;64:11–6.
in man. Metabolism 1965;14:1243–54. 51. Jones NL, Heigenhauser JF, Kuksis A, Matsos CG, Sutton JR, Toews
29. Wolfe RR, Shaw JH, Durkot MJ. Effect of sepsis on VLDL kinetics: CJ. Fat metabolism in heavy exercise. Clin Sci 1980;59:469–78.
responses in basal state and during glucose infusion. Am J Physiol 52. Romijn JA, Coyle EF, Zhang X-J, Sidossis LS, Wolfe RR. Fat oxi-
1985;248:E732–40. dation is impaired somewhat during high-intensity exercise by lim-
30. Turcotte LP, Richter EA, Kiens B. Increased plasma FFA uptake and ited plasma FFA mobilization. J Appl Physiol 1995;79:1939–45.
oxidation during prolonged exercise in trained vs. untrained 53. Rosell S, Belfrage E. Blood circulation in adipose tissue. Physiol
humans. Am J Physiol 1992;262:E791–9. Rev 1979;59:1078–104.
31. Mackie BG, Dudley GA, Kaciuba-Uscilko H, Terjung RL. Uptake 54. Sidossis LS, Gastaldelli A, Klein S, Wolfe RR. Regulation of
of chylomicron triglycerides by contracting skeletal muscle in rats. plasma fatty acid oxidation during low- and high-intensity exercise.
J Appl Physiol 1980;49:851–5. Am J Physiol 1997;272:E1065–70.
EXERCISE AND LIPID METABOLISM 563S
55. Elayan IM, Winder WW. Effect of glucose infusion on muscle mal- 65. Collier G, McLean A, O’Dea K. Effect of co-ingestion of fat on the
onyl-CoA during exercise. J Appl Physiol 1991;70:1495–9. metabolic responses to slowly and rapidly absorbed carbohydrates.
56. Saddik M, Gamble J, Witters LA, Lopaschuk GD. Acetyl-CoA car- Diabetologia 1984;26:50–4.
boxylase regulation of fatty acid oxidation in the heart. J Biol Chem 66. Welch IM, Bruce C, Hill SE, Read NW. Duodenal and ileal lipid
1993;268:25836–45. suppresses postprandial blood glucose and insulin responses in man.
57. McGarry JD, Mannaerts GP, Foster DW. A possible role for mal- Clin Sci 1987;72:209–16.
onyl-CoA in the regulation of hepatic fatty acid oxidation and keto- 67. Bach AC, Babayan VK. Medium-chain triglycerides: an update. Am
genesis. J Clin Invest 1977;60:265–70. J Clin Nutr 1982;36:950–62.
58. Robinson IN, Zammit VA. Sensitivity of carnitine acyltransferase I 68. Saggerson ED, Carpenter CA. Carnitine palmitoyltransferase and car-
to malonyl-CoA and related compounds with mitochondria from nitine octanoyltransferase activities in liver, kidney cortex, adipocyte,
different rat tissues. Biochem J 1982;206:177–9. lactating mammary gland, skeletal muscle, and heart. FEBS Lett
59. McGarry JD, Mills SE, Long CS, Foster DW. Observations on the 1981;129:229–32.
affinity for carnitine, and malonyl-CoA sensitivity, of carnitine 69. Ivy JL, Costill DL, Fink WJ, Maglischo E. Contribution of medium
palmitoyltransferase I in animal and human tissues. Demonstration and long chain triglyceride intake to energy metabolism during pro-
of the presence of malonyl-CoA in non-hepatic tissues of the rat. longed exercise. Int J Sports Med 1980;1:15–20.
Biochem J 1983;214:21–8. 70. Decombaz J, Arnaud MJ, Milon H, et al. Energy metabolism of
60. Dyck DJ, Putman CT, Heigenhauser JF, Hultman E, Spriet LL. Reg- medium chain triglycerides versus carbohydrates during exercise.
ulation of fat-carbohydrate interaction in skeletal muscle during Eur J Appl Physiol 1983;52:9–14.
intense aerobic cycling. Am J Physiol 1993;265:E852–9. 71. Massicotte D, Peronnet F, Brisson GR, Hillaire-Marcel C. Oxida-
61. Vukovich MD, Costill DL, Hickey MS, Trappe SW, Cole KJ, Fink tion of exogenous medium-chain fatty acids during prolonged exer-
WJ. Effect of fat emulsion infusion and fat feeding on muscle glyco- cise: comparison with glucose. J Appl Physiol 1992;73:1334–9.
gen utilization during cycle exercise. J Appl Physiol 1993;75: 72. Jeukendrup AE, Saris WHM, Schrauwen P, Brouns F, Wagenmakers
1513–8. AJM. Metabolic availability of medium-chain triglycerides coingested
62. Binnert C, Pachiaudi C, Beylot M, et al. Metabolic fate of an oral with carbohydrates during prolonged exercise. J Appl Physiol 1995;
long-chain triglyceride load in humans. Am J Physiol 1996;270: 79:756–62.
E445–50. 73. Van Zyl CG, Lambert EV, Hawley JA, Noakes TD, Dennis SC.
63. Horowitz JF, Coyle EF. Metabolic responses to preexercise meals Effects of medium-chain triglyceride ingestion on fuel metabolism
containing various carbohydrates and fat. Am J Clin Nutr 1993;58: and cycling performance. J Appl Physiol 1996;80:2217–25.
235–41. 74. Jeukendrup AE, Thielen JJ, Wagenmakers AJ, Brouns F, Saris WH.
64. Collier G, O’Dea K. The effect of coingestion of fat on the glucose, Effect of medium-chain triacylglycerol and carbohydrate ingestion
insulin, and gastric inhibitory polypeptide responses to carbohy- during exercise on substrate utilization and subsequent cycling per-
drate and protein. Am J Clin Nutr 1983;37:941–4. formance. Am J Physiol 1998;67:397–404.