Muscle glycogen repletion intermittent exercise
after high-intensity
J. D. MAcDOUGALL, G. R. WARD, D. G. SALE, AND J. R. SUTTON Department of Physical Education and Department of Medicine, McMaster Hamilton, Ontario L85 4K1, Canada
MACDOUGALL, J. D., G. R. WARD, D. G. SALE, AND J. R. SUTTON. Muscle glycogen repletion after high-intensity intermittent exercise. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 42(2): 129-132, 1977. -Six subjects exercised to exhaustion on a cycle ergometer at intensities corresponding to approximately 140% of their maximal aerobic power. Subjects attempted to pedal for 1-min intervals with 3-min rest periods between, and continued until 30 s of exercise could no longer be maintained. Venous blood was sampled for lactate and glucose analysis. Muscle biopsies were extracted from the quadriceps before and immediately after exercise and at 2-, 5, 12-, and 24-h intervals thereafter for total glycogen analysis. Three subjects consumed a mixed controlled diet (approx. 3,100 kcal) during the 24 h after exercise, and three consumed the same diet plus an additional 2,50O/kcal carbohydrate. Following exercise, glycogen concentration had dropped to a mean value of approximately 28% of its preexercise value. After 2 h, it had recovered to 39%, at 5 h to 53%, at 12 h to 67%, and at 24 h to 102% of its preexercise value, with no difference in resynthesis rate between the two groups. It was concluded that, following glycogen depletion through intense intermittent exercise, complete recovery to preexercise values may be accomplished within 24 h; and that within this time period, the rate of resynthesis cannot be accelerated by a higher than normal carbohydrate intake. needle biopsy; glycogen
synthase;
glucose; lactate
OF WORKERS have demonstrated the importance of the initial glycogen concentration in skeletal muscle and an athlete’s capacity to sustain heavy exercise (1, 9). In addition the same workers have shown that a high-carbohydrate diet will enhance muscle glycogen synthesis, particularly if preceded by heavy, exhaustive exercise (1, 2). More recently, selective glycogen depletion according to fiber type has been demonstrated with the intensity of the exercise governing the type of fiber to be depleted (4-7). In a team sport such as ice hockey where energy expenditure is intermittent but highly intense (8), glycogen availability may become a major limiting factor to performance. Since contests are often scheduled only 24 h apart, this study examines the time course for replenishing muscle glycogen following depletion through supramaximal intermittent exercise, and whether or not the rate of glycogen resynthesis can be accelerated by a higher-than-normal carbohydrate diet. A NUMBER
University,
PROCEDURES
Six normal subjects were studied after exhaustive, high-intensity intermittent exercise on a cycle ergometer. Subjects PC and CW (Table 1) were highly trained oarsmen, whereas the others, though active in daily training programs were not felt to reflect the same level of fitness. Work loads estimated for each subject approximate an energy expenditure of 140% maximal aerobic power as measured by a direct, progressive exercise tests on the cycle ergometer. The subjects worked at this intensity for 1-min intervals with 3-min rest periods between, until a duration of 30 s could no longer be sustained. Venous blood was collected from a polyethelene catheter inserted in an antecubital vein kept patent by an infusion of heparin-free, isotonic saline. Samples for analysis of lactic acid and glucose were obtained after every second workbout and 2 h after exercise. Needle biopsy samples from the vastus lateralis muscle were taken at rest, after exhaustion, and 2, 5, 12, and 24 h after exercise. The sample at exhaustion was taken within 4 s of the cessation of exercise. In all instances the elapsed time between sampling and freezing in liquid nitrogen was less than 2 s. All tests were begun at 10:00 A.M., and no attempt was made to control the pretest diet except that the subjects were instructed to consume their normal breakfast before 8:00 A.M. After the test, subjects refrained from any food intake until after the 2-h biopsy sample had been taken. Thereafter all subjects were given identical lunch and supper, typifying what was considered to be a normal diet for a physically active athlete. Breakfast the following morning was at the subject’s discretion and all intake was carefully noted and quantified. This totaled approximately 3,020 kcal/subject, of which 50% was estimated to be carbohydrate. In addition three subjects were randomly selected to supplement their meals with an extra intake of pure carbohydrate. The compound used in this case was a high-calorie dietary supplement called Controlyte (Doyle Pharmaceuticals, Minneapolis, Minn.) and amounted to an additional 2,500 kcal or 357 g carbohydrate/subject. Biopsy samples (38-72 mg) were dissected and chipped in a cold chamber at -2OOC to remove adipose tissue, blood, and nonmuscle material. The tissue was then weighed on a torsion balance followed immediately by homogenization in 30 vol ice-cold 1.0 N perchloric acid using a Polytron homogenizer. After centrifugation
129
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130
MAcDOUGALL,
at 4°C the supernatant was neutralized to pH 6-7 using KOH. Glycogen was measured as glucose after acid hydrolysis using enzymatic fluorometric techniques as modified from Passoneau and Lauderdale (14). Plasma lactate and glucose were also determined fluorometritally (21). RESULTS
1. Physical characteristics of subjects PC”
Age, yr mas 7
2
GE
32 196 95 5.93
cm kg
VO
JL
DM
DS
23 186 76.5 3.51
32 183 80.5 4.10
30 175 78 3.43
22 191 81 5.54
. .
48
46
51
44
68
ml-kg
* Well-trained
oarsmen.
TABLE 2. Individual values for peak plasma lactate, plasma glucose and muscle glycogen preand postexercise
PC GE JL DM DS cw
.
= J.L. = D.M. . = C.W. c. = P.C.
80
40
20
0
Accumulated Exercise Time at 140% Mir&
5 12 16 9 8 6
min min min min min min
55 50 40 48 30 54
s s s s s s
Peak Plasma Lactate, mmol/l
21.8 8.4 9.5 11.2 11.9 13.9
Muscle Glycogen, mmol/kg wet wt
I
I I
’
Rest
I
I
I
I
0
2
5
12
Hrs.
Post
t
24
exercise
1. Individual values for muscle glycogen concentration preand postexercise, and over 24 h recovery. Dark symbols indicate carbohydrate-loaded subjects and light symbols, subjects on a normal diet. FIG.
Muscle glycogen, m mol/kg wet
wt.
100 80
60
40
20
Plasma Glucose, mmol/l
Preex
Post&x
Preex
Postex
po~~x
85.2 77.9 72.5 74.1 77.7 94.0
50.0 14.4 22.2 22.0 13.1 16.0
5.0 4.2 5.4
8.1 5.7 6.7
5.5 4.4 5.8
4.9
7.1
5.2
0
2
5 Hrs.
CW*
28 173 68 3.26
62
mas9
Subj
Subjects
wt.
100
Rest
l
2
SUTTON
0
1 min+ VO
AND
l
Subject
Ht, wt,
SALE,
60
The accumulated exercise times to “exhaustion,” as defined by an inability to exercise beyond 30 s after a 3min rest, are shown in Table 2. These times varied from 5 min 55 s to 16 min 40 s, with the highly trained subjects incurring the shortest exercise times but performing the greatest absolute power outputs. Plasma lactate and glucose concentration. Plasma lactate concentrations (Table 2) during exercise increased to a mean peak value of 12.8 mmol/l with subjects PC and CW having the highest values. Plasma glucose levels in each subject measured showed the identical pattern of acute increase (by a mean value of 46%) as a result of the exercise and were still elevated (by approximately 12% over resting values) even after 2 h of fasting. Muscle glycogen concentration. Significant muscle glycogen depletion occurred after several minutes of highly intense exercise (Table 2, Fig. 2). The mean glycogen concentration at exhaustion was reduced to approximately 28% of its preexercise value. Individual rates for glycogen repletion are illustrated in Fig. 1. Glycogen resynthesis was most rapid over the first 5 h after exercise, with five of the six subjects displaying considerable repletion during the first 2 h when subjects were still fasting (Fig. 2). With the exception of subject CW, after 24 h all subjects had regained or slightly exceeded their preexercise values for muscle TABLE
Muscle glycogen m mol/kg wet
WARD,
12 Post
24
exercise
2. Mean (*SE) for muscle glycogen concentration for each group. Shaded histograms indicate carbohydrate-loaded group. Caloric intake is depicted in the appropriate square for each group. FIG.
glycogen concentration. There was no apparent di.cference in the rates of muscle glycogen repletion between the carbohydrate-loaded subjects and those on the normal mixed diet. DISCUSSION
This study indicates that supramaximal exercise of short duration results in marked muscle glycogen depletion and that within 2 h after exercise there is a significant resynthesis of muscle glycogen in the absence of any food intake. Exercise tolerance time. The concept of a relative supramaximal work load, i.e., 140% Vozmax, is very misleading when it is applied to a heterogeneous group such as in the present study. It results in disproportionately high absolute work loads for the large, welltrained subjects and, as one might expect, the shortest
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GLYCOGEN
REPLETION
FOLLOWING
131
EXERCISE
exercise tolerance times and highest peak lactates for these individuals as well. The fact that peak plasma lactate levels in the present study are somewhat lower than those normally seen after exhaustive supramaxima1 exercise (5, 6) is probably attributable to the progressively shorter workbouts as the subjects approached exhaustion. The lactate levels which were attained are not sufficiently high to suggest that the accompany ‘ing acidosis may have been a limiting factor to exercisetolerance time. Furthermore recent studies have separated the effects of pH and lactate on exhaustion time (19). The low postexercise muscle glycogen values, on the other hand, would suggest that glycogen depletion may have been a major factor contributing to the subject’s inability to tolerate further exercise. Glycogen repletion. Among those factors which have been shown to influence the rate of glycogen synthesis in skeletal muscle are plasma glucose (11, 17) and insulin concentration (13) and the activity of glycogen synthase (3). Although we did not measure plasma insulin concentration in the present study, presumably it was higher in the carbohydrate-loaded subjects. If this was the case, then our findings suggest that the insulin and -glucose availability maintained by the athlete’s normal carbohydrate diet is sufficient to maximize glycogen synthesis. The rate of glycogen resynthesis exhibited by the subjects in the present study was considerably more rapid than those reported by Piehl in a recent similar paper (15) where subjects did not regain preexercise concentrations until after approximately 46 h. In her study, however, subjects first underwent prolonged endurance exercise over 1 h followed by exhaustive intermittent maximal exercise for a 2nd h, which resulted in a relatively greater degree of glycogen depletion. Similarly our findings that resynthesis occurred immediately following exercise and in the absence of food
intake, as contrasted to the implications by Bergstrom et al. (1, 2) that significant resynthesis does not occur until carbohydrate is ingested, can probably be explained on the basis of the manner in which subjects exercised. In the Bergstrom study, exercise was continued to exhaustion over 1.5-2 h and therefore resulted in significantly depressed blood glucose concentrations and presumably also in depleted liver glycogen. By contrast, the highly intense but relatively brief exercise in the present study resulted in a hyperglycemic condition; so that after exercise, glucose and, presumably shortly thereafter, insulin levels (16, 20) were higher than preexercise, thus enabling glycogen resynthesis to begin immediately. This is in contrast to the depressed blood glucose and insulin concentrations observed after prolonged endurance exercise (18) which may have occurred in the Bergstrom study. It is also possible that the lactate generated by this type of exercise may serve, at least partially, as a precursor for muscle glycogen synthesis, whether indirectly by contributing to hepatic glucose output (12) or even directly in the muscle itself (10). We believe that exercise of this nature more closely simulates the demands which would be made on muscle energy substrate by a team sport such as ice hockey (8). Since glycogen measurements were not made after 24 h, the possibility of the high-carbohydrate diet leading to a greater degree of supercompensation subsequently cannot be dismissed. In summary, we conclude that after glycogen depletion through high-intensity intermittent exercise complete recovery to preexercise values may be accomplished within 24 h; and that within this time period, the rate at which glycogen is restored to muscle depots cannot be accelerated by a higher than normal intake of carbohydrate. Received
for publication
18 June
1976.
REFERENCES 1. BERGSTROM, J., L. HERMANSEN, E. HULTMAN, AND B. SALTIN. Diet, muscle glycogen and physical performance. Acta PhysioZ. Stand. 71: 140-150, 1967. 2. BERGSTROM, J., AND E. HULTMAN. Muscle glycogen synthesis after exercise: an enhancing factor localized to muscle cells in man. Nature 210: 309-310, 1966. 3. BERGSTROM, J., E. HULTMAN, AND A. E. ROCH-NORLUND. Muscle glycogen synthetase in normal subjects. &and. J. CZin. Lab. Invest. 29: 231-236, 1972. 4. COSTILL, D. L., P. D. GOLLNICK, E. D. JANSSON, B. SALTIN, AND E. M. STEIN. Glycogen depletion pattern in human muscle fibres during distance running. Acta PhysioZ. Stand. 89: 383-394, 1973. 5. GOLLNICK, P. D., R. B. ARMSTRONG, W. L. SEMBROWICH, R. E. SHEPERD, AND B. SALTIN. Glycogen depletion pattern in human skeletal muscle fibers after heavy exercise. J. AppZ. PhysioZ. 34: 615-618, 1973. 6. GOLLNICK, P. D., K. PIEHL, AND B. SALTIN. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J. PhysioZ., London 241: 45-57, 1975. 7. GOLLNICK, P. D., K. PIEHL, C. W. SAUBERT IV, R. B. ARMSTRONG, AND B. SALTIN. Diet, exercise, and glycogen changes in human muscle fibers. J. AppZ. Physiol. 33: 421-425, 1972. 8. GREEN, H., P. BISHOP, M. HOUSTON, R. MCKILLOP, R. NORMAN, AND P. STOTHART. Time-motion and physiological assessments of ice hockey performance. J. AppZ. Physiol. 40: 159-163, 1976.
9. HERMANSEN L., E. HULTMAN, AND B. SALTIN. Muscle glycogen during prolonged severe exercise. Acta PhysioZ. &and. 71: 129139, 1967. 10. HERMANSEN, L., AND I. STENSVOLD. Production and removal of lactate during exercise in man. Acta. PhysioZ. Stand. 86: 191201, 1972. 11. HULTMAN, E. Physiological role of muscle glycogen in man, with special reference to exercise. CircuZation Res. 20, Suppl. 1: 99114, 1967. 12. ISSEKUTZ, B., W. A. S. SHAW, AND A. C. ISSEKUTZ. Lactate metabolism in resting and exercising dogs. J. AppZ. Physiol. 40: 312-319, 1976. 13. NUTTALL, F. W., J. BARBOSA, AND M. C. GANNON. The glycogen synthase system in skeletal muscle of normal humans and patients with myotonic dystrophy: Effect of glucose and insulin administration. MetaboZism 23: 561-568, 1974. 14. PASSONEAU, J. V., AND V. R. LAUDERDALE. A comparison of three methods of glycogen measurements in tissues. AnaZ. Biochem. 60: 405-412, 1974. 15. PIEHL, K. Time course for refilling of glycogen stores in human muscle fibres following exercise-induced glycogen depletion. Acta PhysioZ. Stand. 90: 297-302, 1974. 16. PRUETT, E. D. R. Plasma insulin concentrations during prolonged work at near maximal oxygen uptake. J. AppZ. Physiol. 29: 155-158, 1970. 17. ROCH-NORLUND, A. E., J. BERGSTROM, AND E. HULTMAN. Muscle
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132 glycogen and glycogen synthetase in normal subjects and in patients with diabetes mellitus. Effect of intravenous glucose and insulin administration. Stand. J. CZin. Lab. Invest. 30: 7784, 1972. 18. SUTTON, J. R., M. J. COLEMAN, A. P. MILLAR, L. LAZARUS, AND P. Russo. The medical problems of mass participation in athletic competition. Med. J. AustraZia 2: 127-133, 1972. 19. SUTTON, J. R., N. L. JONES, AND C. J. TOEWS. Growth hormone
MAcDOUGALL,
WARD,
SALE,
AND
SUTTON
secretion in acid-base alterations at rest and during exercise. CZin. Sci. MOL. Med. 50: 241-247, 1976. 20. SUTTON, J. R., J. D. YOUNG, L. LAZARUS, J. B. HICKIE, AND J. MAKSVYTIS. The hormonal response to physical exercise. AustraZasian Ann. Med. 18: 84-90, 1969. 21. TOEWS, C. J., C. LOWY, AND N. B. RUDERMAN. The regulation of gluconeogenesis. J. BioZ. Chem. 245: 818-824, 1970.
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after high-intensity
J. D. MAcDOUGALL, G. R. WARD, D. G. SALE, AND J. R. SUTTON Department of Physical Education and Department of Medicine, McMaster Hamilton, Ontario L85 4K1, Canada
MACDOUGALL, J. D., G. R. WARD, D. G. SALE, AND J. R. SUTTON. Muscle glycogen repletion after high-intensity intermittent exercise. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 42(2): 129-132, 1977. -Six subjects exercised to exhaustion on a cycle ergometer at intensities corresponding to approximately 140% of their maximal aerobic power. Subjects attempted to pedal for 1-min intervals with 3-min rest periods between, and continued until 30 s of exercise could no longer be maintained. Venous blood was sampled for lactate and glucose analysis. Muscle biopsies were extracted from the quadriceps before and immediately after exercise and at 2-, 5, 12-, and 24-h intervals thereafter for total glycogen analysis. Three subjects consumed a mixed controlled diet (approx. 3,100 kcal) during the 24 h after exercise, and three consumed the same diet plus an additional 2,50O/kcal carbohydrate. Following exercise, glycogen concentration had dropped to a mean value of approximately 28% of its preexercise value. After 2 h, it had recovered to 39%, at 5 h to 53%, at 12 h to 67%, and at 24 h to 102% of its preexercise value, with no difference in resynthesis rate between the two groups. It was concluded that, following glycogen depletion through intense intermittent exercise, complete recovery to preexercise values may be accomplished within 24 h; and that within this time period, the rate of resynthesis cannot be accelerated by a higher than normal carbohydrate intake. needle biopsy; glycogen
synthase;
glucose; lactate
OF WORKERS have demonstrated the importance of the initial glycogen concentration in skeletal muscle and an athlete’s capacity to sustain heavy exercise (1, 9). In addition the same workers have shown that a high-carbohydrate diet will enhance muscle glycogen synthesis, particularly if preceded by heavy, exhaustive exercise (1, 2). More recently, selective glycogen depletion according to fiber type has been demonstrated with the intensity of the exercise governing the type of fiber to be depleted (4-7). In a team sport such as ice hockey where energy expenditure is intermittent but highly intense (8), glycogen availability may become a major limiting factor to performance. Since contests are often scheduled only 24 h apart, this study examines the time course for replenishing muscle glycogen following depletion through supramaximal intermittent exercise, and whether or not the rate of glycogen resynthesis can be accelerated by a higher-than-normal carbohydrate diet. A NUMBER
University,
PROCEDURES
Six normal subjects were studied after exhaustive, high-intensity intermittent exercise on a cycle ergometer. Subjects PC and CW (Table 1) were highly trained oarsmen, whereas the others, though active in daily training programs were not felt to reflect the same level of fitness. Work loads estimated for each subject approximate an energy expenditure of 140% maximal aerobic power as measured by a direct, progressive exercise tests on the cycle ergometer. The subjects worked at this intensity for 1-min intervals with 3-min rest periods between, until a duration of 30 s could no longer be sustained. Venous blood was collected from a polyethelene catheter inserted in an antecubital vein kept patent by an infusion of heparin-free, isotonic saline. Samples for analysis of lactic acid and glucose were obtained after every second workbout and 2 h after exercise. Needle biopsy samples from the vastus lateralis muscle were taken at rest, after exhaustion, and 2, 5, 12, and 24 h after exercise. The sample at exhaustion was taken within 4 s of the cessation of exercise. In all instances the elapsed time between sampling and freezing in liquid nitrogen was less than 2 s. All tests were begun at 10:00 A.M., and no attempt was made to control the pretest diet except that the subjects were instructed to consume their normal breakfast before 8:00 A.M. After the test, subjects refrained from any food intake until after the 2-h biopsy sample had been taken. Thereafter all subjects were given identical lunch and supper, typifying what was considered to be a normal diet for a physically active athlete. Breakfast the following morning was at the subject’s discretion and all intake was carefully noted and quantified. This totaled approximately 3,020 kcal/subject, of which 50% was estimated to be carbohydrate. In addition three subjects were randomly selected to supplement their meals with an extra intake of pure carbohydrate. The compound used in this case was a high-calorie dietary supplement called Controlyte (Doyle Pharmaceuticals, Minneapolis, Minn.) and amounted to an additional 2,500 kcal or 357 g carbohydrate/subject. Biopsy samples (38-72 mg) were dissected and chipped in a cold chamber at -2OOC to remove adipose tissue, blood, and nonmuscle material. The tissue was then weighed on a torsion balance followed immediately by homogenization in 30 vol ice-cold 1.0 N perchloric acid using a Polytron homogenizer. After centrifugation
129
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130
MAcDOUGALL,
at 4°C the supernatant was neutralized to pH 6-7 using KOH. Glycogen was measured as glucose after acid hydrolysis using enzymatic fluorometric techniques as modified from Passoneau and Lauderdale (14). Plasma lactate and glucose were also determined fluorometritally (21). RESULTS
1. Physical characteristics of subjects PC”
Age, yr mas 7
2
GE
32 196 95 5.93
cm kg
VO
JL
DM
DS
23 186 76.5 3.51
32 183 80.5 4.10
30 175 78 3.43
22 191 81 5.54
. .
48
46
51
44
68
ml-kg
* Well-trained
oarsmen.
TABLE 2. Individual values for peak plasma lactate, plasma glucose and muscle glycogen preand postexercise
PC GE JL DM DS cw
.
= J.L. = D.M. . = C.W. c. = P.C.
80
40
20
0
Accumulated Exercise Time at 140% Mir&
5 12 16 9 8 6
min min min min min min
55 50 40 48 30 54
s s s s s s
Peak Plasma Lactate, mmol/l
21.8 8.4 9.5 11.2 11.9 13.9
Muscle Glycogen, mmol/kg wet wt
I
I I
’
Rest
I
I
I
I
0
2
5
12
Hrs.
Post
t
24
exercise
1. Individual values for muscle glycogen concentration preand postexercise, and over 24 h recovery. Dark symbols indicate carbohydrate-loaded subjects and light symbols, subjects on a normal diet. FIG.
Muscle glycogen, m mol/kg wet
wt.
100 80
60
40
20
Plasma Glucose, mmol/l
Preex
Post&x
Preex
Postex
po~~x
85.2 77.9 72.5 74.1 77.7 94.0
50.0 14.4 22.2 22.0 13.1 16.0
5.0 4.2 5.4
8.1 5.7 6.7
5.5 4.4 5.8
4.9
7.1
5.2
0
2
5 Hrs.
CW*
28 173 68 3.26
62
mas9
Subj
Subjects
wt.
100
Rest
l
2
SUTTON
0
1 min+ VO
AND
l
Subject
Ht, wt,
SALE,
60
The accumulated exercise times to “exhaustion,” as defined by an inability to exercise beyond 30 s after a 3min rest, are shown in Table 2. These times varied from 5 min 55 s to 16 min 40 s, with the highly trained subjects incurring the shortest exercise times but performing the greatest absolute power outputs. Plasma lactate and glucose concentration. Plasma lactate concentrations (Table 2) during exercise increased to a mean peak value of 12.8 mmol/l with subjects PC and CW having the highest values. Plasma glucose levels in each subject measured showed the identical pattern of acute increase (by a mean value of 46%) as a result of the exercise and were still elevated (by approximately 12% over resting values) even after 2 h of fasting. Muscle glycogen concentration. Significant muscle glycogen depletion occurred after several minutes of highly intense exercise (Table 2, Fig. 2). The mean glycogen concentration at exhaustion was reduced to approximately 28% of its preexercise value. Individual rates for glycogen repletion are illustrated in Fig. 1. Glycogen resynthesis was most rapid over the first 5 h after exercise, with five of the six subjects displaying considerable repletion during the first 2 h when subjects were still fasting (Fig. 2). With the exception of subject CW, after 24 h all subjects had regained or slightly exceeded their preexercise values for muscle TABLE
Muscle glycogen m mol/kg wet
WARD,
12 Post
24
exercise
2. Mean (*SE) for muscle glycogen concentration for each group. Shaded histograms indicate carbohydrate-loaded group. Caloric intake is depicted in the appropriate square for each group. FIG.
glycogen concentration. There was no apparent di.cference in the rates of muscle glycogen repletion between the carbohydrate-loaded subjects and those on the normal mixed diet. DISCUSSION
This study indicates that supramaximal exercise of short duration results in marked muscle glycogen depletion and that within 2 h after exercise there is a significant resynthesis of muscle glycogen in the absence of any food intake. Exercise tolerance time. The concept of a relative supramaximal work load, i.e., 140% Vozmax, is very misleading when it is applied to a heterogeneous group such as in the present study. It results in disproportionately high absolute work loads for the large, welltrained subjects and, as one might expect, the shortest
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on July 28, 2018. Copyright © 1977 American Physiological Society. All rights reserved.
GLYCOGEN
REPLETION
FOLLOWING
131
EXERCISE
exercise tolerance times and highest peak lactates for these individuals as well. The fact that peak plasma lactate levels in the present study are somewhat lower than those normally seen after exhaustive supramaxima1 exercise (5, 6) is probably attributable to the progressively shorter workbouts as the subjects approached exhaustion. The lactate levels which were attained are not sufficiently high to suggest that the accompany ‘ing acidosis may have been a limiting factor to exercisetolerance time. Furthermore recent studies have separated the effects of pH and lactate on exhaustion time (19). The low postexercise muscle glycogen values, on the other hand, would suggest that glycogen depletion may have been a major factor contributing to the subject’s inability to tolerate further exercise. Glycogen repletion. Among those factors which have been shown to influence the rate of glycogen synthesis in skeletal muscle are plasma glucose (11, 17) and insulin concentration (13) and the activity of glycogen synthase (3). Although we did not measure plasma insulin concentration in the present study, presumably it was higher in the carbohydrate-loaded subjects. If this was the case, then our findings suggest that the insulin and -glucose availability maintained by the athlete’s normal carbohydrate diet is sufficient to maximize glycogen synthesis. The rate of glycogen resynthesis exhibited by the subjects in the present study was considerably more rapid than those reported by Piehl in a recent similar paper (15) where subjects did not regain preexercise concentrations until after approximately 46 h. In her study, however, subjects first underwent prolonged endurance exercise over 1 h followed by exhaustive intermittent maximal exercise for a 2nd h, which resulted in a relatively greater degree of glycogen depletion. Similarly our findings that resynthesis occurred immediately following exercise and in the absence of food
intake, as contrasted to the implications by Bergstrom et al. (1, 2) that significant resynthesis does not occur until carbohydrate is ingested, can probably be explained on the basis of the manner in which subjects exercised. In the Bergstrom study, exercise was continued to exhaustion over 1.5-2 h and therefore resulted in significantly depressed blood glucose concentrations and presumably also in depleted liver glycogen. By contrast, the highly intense but relatively brief exercise in the present study resulted in a hyperglycemic condition; so that after exercise, glucose and, presumably shortly thereafter, insulin levels (16, 20) were higher than preexercise, thus enabling glycogen resynthesis to begin immediately. This is in contrast to the depressed blood glucose and insulin concentrations observed after prolonged endurance exercise (18) which may have occurred in the Bergstrom study. It is also possible that the lactate generated by this type of exercise may serve, at least partially, as a precursor for muscle glycogen synthesis, whether indirectly by contributing to hepatic glucose output (12) or even directly in the muscle itself (10). We believe that exercise of this nature more closely simulates the demands which would be made on muscle energy substrate by a team sport such as ice hockey (8). Since glycogen measurements were not made after 24 h, the possibility of the high-carbohydrate diet leading to a greater degree of supercompensation subsequently cannot be dismissed. In summary, we conclude that after glycogen depletion through high-intensity intermittent exercise complete recovery to preexercise values may be accomplished within 24 h; and that within this time period, the rate at which glycogen is restored to muscle depots cannot be accelerated by a higher than normal intake of carbohydrate. Received
for publication
18 June
1976.
REFERENCES 1. BERGSTROM, J., L. HERMANSEN, E. HULTMAN, AND B. SALTIN. Diet, muscle glycogen and physical performance. Acta PhysioZ. Stand. 71: 140-150, 1967. 2. BERGSTROM, J., AND E. HULTMAN. Muscle glycogen synthesis after exercise: an enhancing factor localized to muscle cells in man. Nature 210: 309-310, 1966. 3. BERGSTROM, J., E. HULTMAN, AND A. E. ROCH-NORLUND. Muscle glycogen synthetase in normal subjects. &and. J. CZin. Lab. Invest. 29: 231-236, 1972. 4. COSTILL, D. L., P. D. GOLLNICK, E. D. JANSSON, B. SALTIN, AND E. M. STEIN. Glycogen depletion pattern in human muscle fibres during distance running. Acta PhysioZ. Stand. 89: 383-394, 1973. 5. GOLLNICK, P. D., R. B. ARMSTRONG, W. L. SEMBROWICH, R. E. SHEPERD, AND B. SALTIN. Glycogen depletion pattern in human skeletal muscle fibers after heavy exercise. J. AppZ. PhysioZ. 34: 615-618, 1973. 6. GOLLNICK, P. D., K. PIEHL, AND B. SALTIN. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J. PhysioZ., London 241: 45-57, 1975. 7. GOLLNICK, P. D., K. PIEHL, C. W. SAUBERT IV, R. B. ARMSTRONG, AND B. SALTIN. Diet, exercise, and glycogen changes in human muscle fibers. J. AppZ. Physiol. 33: 421-425, 1972. 8. GREEN, H., P. BISHOP, M. HOUSTON, R. MCKILLOP, R. NORMAN, AND P. STOTHART. Time-motion and physiological assessments of ice hockey performance. J. AppZ. Physiol. 40: 159-163, 1976.
9. HERMANSEN L., E. HULTMAN, AND B. SALTIN. Muscle glycogen during prolonged severe exercise. Acta PhysioZ. &and. 71: 129139, 1967. 10. HERMANSEN, L., AND I. STENSVOLD. Production and removal of lactate during exercise in man. Acta. PhysioZ. Stand. 86: 191201, 1972. 11. HULTMAN, E. Physiological role of muscle glycogen in man, with special reference to exercise. CircuZation Res. 20, Suppl. 1: 99114, 1967. 12. ISSEKUTZ, B., W. A. S. SHAW, AND A. C. ISSEKUTZ. Lactate metabolism in resting and exercising dogs. J. AppZ. Physiol. 40: 312-319, 1976. 13. NUTTALL, F. W., J. BARBOSA, AND M. C. GANNON. The glycogen synthase system in skeletal muscle of normal humans and patients with myotonic dystrophy: Effect of glucose and insulin administration. MetaboZism 23: 561-568, 1974. 14. PASSONEAU, J. V., AND V. R. LAUDERDALE. A comparison of three methods of glycogen measurements in tissues. AnaZ. Biochem. 60: 405-412, 1974. 15. PIEHL, K. Time course for refilling of glycogen stores in human muscle fibres following exercise-induced glycogen depletion. Acta PhysioZ. Stand. 90: 297-302, 1974. 16. PRUETT, E. D. R. Plasma insulin concentrations during prolonged work at near maximal oxygen uptake. J. AppZ. Physiol. 29: 155-158, 1970. 17. ROCH-NORLUND, A. E., J. BERGSTROM, AND E. HULTMAN. Muscle
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on July 28, 2018. Copyright © 1977 American Physiological Society. All rights reserved.
132 glycogen and glycogen synthetase in normal subjects and in patients with diabetes mellitus. Effect of intravenous glucose and insulin administration. Stand. J. CZin. Lab. Invest. 30: 7784, 1972. 18. SUTTON, J. R., M. J. COLEMAN, A. P. MILLAR, L. LAZARUS, AND P. Russo. The medical problems of mass participation in athletic competition. Med. J. AustraZia 2: 127-133, 1972. 19. SUTTON, J. R., N. L. JONES, AND C. J. TOEWS. Growth hormone
MAcDOUGALL,
WARD,
SALE,
AND
SUTTON
secretion in acid-base alterations at rest and during exercise. CZin. Sci. MOL. Med. 50: 241-247, 1976. 20. SUTTON, J. R., J. D. YOUNG, L. LAZARUS, J. B. HICKIE, AND J. MAKSVYTIS. The hormonal response to physical exercise. AustraZasian Ann. Med. 18: 84-90, 1969. 21. TOEWS, C. J., C. LOWY, AND N. B. RUDERMAN. The regulation of gluconeogenesis. J. BioZ. Chem. 245: 818-824, 1970.
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on July 28, 2018. Copyright © 1977 American Physiological Society. All rights reserved.
