Acta physiol. scand. 1974. 90. 210-217 From the Department of Physiology, Gymnastik- och idrottshogskolan, and the Military Medical

Examination Center, Stockholm, Sweden

Muscle Glycogen Utilization during Exercise after Physical Training

BY

JAN KARLSSON, LARS-OLOF NORDESJ~ and BENGT SALTIN

Received 22 March 1973

Abstract

KARLSSON, J., L.-0. NORDESJO and B. SALTIN. Muscle glycogen utilization during exercise after physical training. Acta physiol. scand. 1974. 90. 210-217.

5 male subjects exercised at a mean oxygen uptake of 2.3 Ixmin-1 (z 65 % of 00, max) before and after 2 months of physical training for 90 min and 120 min, respectively. Mean maximal oxygen uptake increased by 11 % (p < 0.05), and the mean R-value during the submaximal work decreased from 0.93 to 0.89 (p < 0.01). Plasma levels for FFA and glucose during exercise were unaffected by training. The mean rate of muscle glycogen breakdown in the thigh between 20 and 90 min of prolonged work could be estimated to be 0.66 before and 0.41 mmol glucose units x kg 1 wet muscle x min-1 after training ( p < 0.01 ) . Part of the reduced glycogen utilization could be explained by a less pronounced lactate production in the trained stage. I t is concluded that a short period of physical conditioning results in a decredse in glycogen utilization and an enhanced fat oxidation.

When subjects with different “fitness levels” exercise for a more prolonged period of time at the same absolute work intensity, a lower respiratory exchange ratio (R) is found in the most well-trained subjects (Christensen and Hansen 1939), in- dicating a less pronounced carbohydrate utilization during work in subjects with a high physical work capacity.

Furthermore, it has in cross-sectional studies been found that subjects with dif- ferent physical work capacity had similar rates of glycogen depletion when working at the same relative work load for a prolonged period of time (Hermansen, Hult- man and Saltin 1967). I t has also been found that with increase in the relative work load the glycolytic rate increases (Saltin and Karlsson 1971).

The question then arises as to what extent a short period of physical training leading to an increase in maximal oxygen uptake can produce a change in the metabolic response to prolonged exercise resulting in a glycogen sparing effect.

The aim of the present study was therefore to investigate the muscle glycogen breakdown in the thigh during prolonged work in previously untrained men before and after a couple of months of physical conditioning.

210

MUSCLE GLYCOGEN UTILIZATION DURING EXERCISE 21 1

1.2 - IP -

oa-

w -

o,., -

1 i

REsplRATORY EXCHANGE RATIO

0

a 5 c0.05 P

. c ,

I 1 0 60 120

TIME. rnin.

_. MUSCLE GLYCOOEN mmol g w mitsx b-1 wet muscle'

0 60 120

TIME, mn.

Fig. 1. Mean values for different variables in 5 subjects at rest and during work tests at the same absolute work load (mean oxygen uptake 2.3 Ixmin-1) before and after 8 weeks of interval training. The significance of mean differences at equivalent points of time and between values at 90 and 120 min has been tested by the t-test and the degree of significance has been included in the figure.

m m l glucose units xkg-' wet muscle . ,

TIME, min

Fig. 2. The relationship between the utiliza- tion of muscle glycogen and work time before (0 ) and after (0) training. The significance of mean differences has been tested as in Fig. 1. Mean values for the 3 subjects- who had the same initial content of muscle gly- cogen before (H) and after ([7) training have also been included in the figure.

212 J A N KAKLSSVN, LARS-OLOF NORDESJO AND BENGT SALTIN

TABLE I. Values at rest and during prolonged work at a mean load of 167 W.

Variable Rest Prolonged work, min

5

b a b a

Heart rate beats x min-'

- X

SD -

Oxygen uptake X 1 x min-' SD R X

SD

SD

-

- Muscle glycogen X

mrnol glucose units x kg-' w. m.

Muscle lactate X

mmol x kg-' w. m. SD Blood lactate X inn101 x 1-' blood SD Blood glucose X

rnrnol x 1-' blood SD

-

-

-

FFA in plasma mmol x 1-'

- X SD

84.4 16.6

0.88 0.15 1.48 0.22 3.92 0.57 0.53 0.09

77.2 14.3

57.7 2.0

140.0 139.0 13.3 14.0

65.4 5.2

0.86 0.09 1.26 0.17 4.00 0.56 0.54 0.1 1

8.80 3.37 5.12 1.58

6.66 3.52 4.00 1.72

b = before training a = after 2 months interval training c after 2 months training heart rate at 90 min was 159.4 (SD = 14.5) beats xmin-' d value at 15 min. After 30 min work the values were 4.40 (b) and 3.34 (a)

Subjects 5 conscripts volunteered to participate in the study. Prior to the study they were fully in- formed about the procedure to be used. At induction the subjects were on an average 20 years old (range 19-21 years), with a mean height of 179 cm (fange 173-184 cm) and a mean weight of 74.0 kg (range 65-83 kg), which is 7.6 kg more ( p < 0.05) than for a random sample of 18-year-old boys (Ahlborg e t al. 1972). Maximal oxygen uptake before training averaged 3.56 1 x min-1 (48 m i x kg-1 x min-l), which is 9 c/o higher than the mean value for two groups of conscripts of the same age (unpublished data). The maximal work load that could be sustained for 6 min was 270 watt, which is 14 % higher than for conscripts at registra- tion (Linroth 1969).

All 5 subjects had physically very light occupations prior to induction. One of the subjects was physically inactive in his spare time. The remaining 4 subjects were somewhat activt. (grade 2 on a 4-graded score; Saltin and Grimby 1968).

Methods and Procedure The subjects underwent a series of preliminary tests including a short submaximal work test to habituate the subjects.

A few days later a graded submaximal work test was performed. After half an hour of rest the subjects performed maximally on a constant load. This procedure was repeated two days later. On the basis of the maximal tests a work load, which could easily be sustained for 90 min was calculated and used during a prolonged exercise test 5 days later. T h e same procedure and identical work loads were repeated after two months of training with the difference that the prolonged exercise now continued for 120 min and with some variation in the number of days between maxirrial and prolonged work tests. This variation is of negligible importance for the results.

MUSCLE GLYCOGEN UTILIZATION DURING EXERCISE 213

20 60 90 120

b a b a b a

163.8 15.4 2.33 0.24 0.95 0.05

55.2 10.7

7.56 3.62 5.066 1.40 3.46 0.73 0.51 0.14

147.8 12.3 2.32 0.26 0.91 0.04

45.8 3.5

5.94 4.56 3.70" 1.39 3.87 0.37 0.41 0.06

171.6 18.7

28.7 10.3

6.12 2.57 3.34 0.83

0.92 0.73 0.2 1

3.80

155.4 9.7

25.0 10.3

1.84 0.75 2.52 0.70 3.54 0.43 0.72 0.20

178.0c 15.9 2.52 0.23 0.90 0.05

8.8 4.0

4.76 2.61 3.12 0.61 3.84 1.02 1.01 0.28

161.4 14.4

2.48 0.27 0.87 0.05 9.8 7.1

I .52 0.73 2.02 0.47 3.23 0.29 1.00 0.18

During the training period the subjects underwent 21 sessions of physical conditioning, which was characterized by repeated, short (15 s ) maximal or close to maximal runs with intervening periods (15 s ) of jogging or walking ("interval training"). The total running time at maximum was 6 h. A detailed description of the training is given elsewhere (Knuttgen et al. 1973).

During the work tests ECG was recorded on a Elema Mingograf 34, and the heart rate was calculated from 20 R-R intervals. Expired air was collected in Douglas bags from the 4th min onwards in the maximal work tests and after 20 and 90 (or 120) min of exercise during the prolonged work test. Gas analyses were performed by the Haldane technique. The highest 00, before and after training are both mean values of two trials. Capillary samples of blood were taken after the maximal and during the prolonged work tests and the lactate content was determined by an enzymatic method (Scholz et al. 1959).

On the day of the prolonged work test the subjects came to the laboratory after a light breakfast. In conjunction with the prolonged work test samples of venous blood were taken at rest and after 20, 60, and 90 (or 120) min of exercise for the determination of glucose (Hjelm and de Verdier 1963) and FFA (Trout, Estes and Friedberg 1960).

During the prolonged work test muscle biopsies were taken with the Bergstrom technique (1962) from the lateral portion of the quadriceps muscle at rest and after 5, 20, 90 (or 120) min of work. The samples of muscle tissue were analyzed for glycogen, glucose and lactate according to technique described by Karlsson (1971). The water content of the samples varied from 76 '% at rest to 77 and 78 % during exercise, respectively.

The submaximal and the maximal work tests were performed on a calibrated, electrically braked bicycle ergometer (Elema-Schonander model AM 369) and the prolonged work test on an older model (AM 361; Holrngren and Mattson 1954). During the work tests the room temperature varied between 21" and 24" C.

Convential statistical methods were used, and the results of training were evaluated by means of a common t-test applied to the mean of differences between paired observations (Snedecor and Cochran 1967).

214 J A N KARLSSON, LARS-OLOF NORDESJO A N D BENCT SALTIN

I 1 I

BLOOD GLUCOSE, mmlxI'l blood -

4.0-

30-

2.0 - before training

D after -.- 1.0-

A I

0 60 120 TIME, min

1 BLOOD GLUCOSE, m m l I 1-l blood

4.0 "1 before training

0 60 120 TIME, min

I 1 I I

lo- PLASMA FFA

w- C

0 60 120 TIME, mn

1

0 60 120 TIME, rnin

0 60 120 TIME, min.

Fig. 3. See legend for Fig. 1

Results

Maximal oxygen uptake increased in all subjects as an effect of the physical training. The mean improvement was from 3.56 to 3.95 1Xmin-l or 11 % (p < 0.05). Table I gives the values at rest and during the prolonged work test for the studied variables. During the prolonged work period significantly lower heart rates were observed after training as compared to before training (Fig. 1 ) . Both before and after training the oxygen uptake during the prolonged work test (Fig. 1) was about 2.3 1Xmin-' after 20 min of work and slightly higher (p < 0.01) at the end of the exercise (90 or 120 min).

Before training the R-values averaged 0.95 after 20 min of work and 0.90 at the end. After training the corresponding values were 0.91 and 0.87, respectively (Fig. 1). The differences at 20 min and at the end of work were significant at the 0.05 level.

After training muscle glycogen was significantly lower at rest ( p < 0.05) and after 5 min of work (p < 0.05). During the remainder of the work the values of muscle glycogen were not significantly different before and after training (Fig. 1). The amount of muscle glycogen broken down during the first 5 min of exercise was very similar before and after training (Fig. 2 ) . From then on its appears as if less glycogen has been utilized after physical conditioning and at the end of work a significantly (p < 0.05) lower amount of glycogen has been broken down.

MUSCLE GLYCOGEN UTILIZATION DURING EXERCISE 215 The concentration of lactate in muscle and blood averaged at rest about 0.9

mmolxkg'l wet muscle and 1.4 m m o l ~ l . ~ blood both before and after training. At onset of exercise there was a marked increase in lactate concentration reaching 8.8 mmol x kg-l wet muscle (Fig. 3) and 5.1 mmol x 1-1 blood (Fig. 3) after 5 min of exercise before training. The increases were significantly lower after training than before ( p < 0.05 and 0.01, respectively). From the 5th rnin onwards the lactate concentrations gradually declined during the prolonged work, but only after physical conditioning did muscle lactate approach the resting level.

Blood glucose averaged 4.0 mmol x 1-l at rest and no significant change occurred during exercise (Fig. 3 ) . FFA concentration was 0.53 mmol x 1-1 before exercise and after an initial lag it gradually increased and values around 1 m m o l ~ l - ~ were reached at the end of the exercise (Fig. 3) . Physical conditioning did not result in any significant changes in blood glucose or FFA concentration either at rest or during exercise.

Discussion Heart rate, oxygen uptake and the R-value changed during the prolonged work test as described earlier (Christensen 1931, Christensen and Hansen 1939). The change in these variables as well as in maximal oxygen uptake as a result of physical con- ditioning was in accordance with what could be expected from cross-sectional and longitudinal training studies (Christensen 193 1, 1932, Christensen and Hansen 1939. Beveg%rd, Holmgren and Jonsson 1963, Saltin et al. 1968).

The important new finding was that two months of physical training with a total of 6 h of running also resulted in a less pronounced depletion in muscle glycogen during exercise at the same absolute work load. This difference was not detectable in the early phase of the exercise, but well established when comparisons are made for the whole work period.

Two major objections may be raised when making a comparison between the glycogen utilized before and after training. One is that the content of muscle glycogen at start of work was not the same, although both values were within normal limits (Karlsson 1971). On the basis of the results in Bergstrom et al. (1967), where muscle glycogen was varied between 19 and 289 mmol glucose unitsxkg-' wet muscle, it can be calculated that a difference of 20 mmol, as in the present study, does not significantly alter the glycolytic rate during work. This conclusion is further supported by the data for 3 of the subjects, who had the same initial content of muscle glycogen before and after training. The 3 subjects demonstrated the same rate of glycogen utilization as all 5 subjects (Fig. 2 ) .

The other problem is related to the fact that the final muscle biopsies were not taken at the same time of exercise (90 us. 120 min) in the 2 expts. Since a fairly constant glycolytic rate was observed after 20 min of work and since a complete glycogen depletion had not occurred in any subject the comparisons in Fig. 2 are valid. If the rate of glycogen utilization between 20 and 90 (observed or estimated) rnin is calculated this is found to be 0.41 mmol x kg-l x min-' after as compared to 0.66 mmol x kg-l x min-l before training ( p < 0.01 ) .

216 JAN KARLSSON, LARS-OLOF NORDESJO A N D BENGT SALTIN

Any exact quantifications to what extent a reduced production of lactate and/or oxidation of pyruvate is present after physical conditioning cannot be settled on the basis of the present data. There is, however, indirect evidence of a less pronounced energy yield from both anaerobic and aerobic glycogen breakdown. 5 min after onset of the submaximal work muscle and blood lactate were lower as compared to before training. This could have been aaticipated as it has been shown that muscle lactate is related to the oxygen deficit at start of exercise, which in turn is a function of the relative work level (Karlsson 1971, Linnarsson et al. 1973). However, the lac- tate concentration depends not only on production but also on the turn-over in the body. It has been suggested that lactate is turned over faster in prolonged work after physical training (Karlsson and Jorfeldt 1971, Karlsson et al. 1972). In this study the relationship between the muscle and blood lactate concentrations was very similar in the two conditions implying an unchanged distribution and turn-over rate for lactate. Consequently the lower muscle and blood lactate a t onset of exercise after training might indicate that less glycogen has been used anaerobically.

The lower glycogen depletion and the lower R-values during exercise in the presence of the same oxygen uptake point to a reduced oxidative use of carbohydrates after training. I t has been proposed (Saltin and Karlsson 1971) that the enhanced fat oxidation and the reduced carbohydrate oxidation as indicated by the decrease in the R-value observed in trained subjects are brought about by an increased recruitment of “red” (high oxidati\ie-slow twitch-see Gollnick et al. 1972 for a further characterization) fibres. At the work levels used in this study (65 ”/c of vo2 max before and 59 ”/o after training) it is highly probable that the slow twitch fibres are predominantly engaged regardless of the training status (Gollnick et al. 1973 a ) . Thus, the training effect does not seem to be the result of a change in recruitment pattern. Moreover, it has not been possible to demonstrate a change in the percentage of slow twitch fibres with physical training in humans (Gollnick et al. 1973 b) . On the other hand, an enhanced oxidative capacity of all the fibres of human skeletal muscle has been observed after physical training (Gollnick et al. 1973 b) . Further- more, in animal muscle it has been demonstrated that along with the increase in oxidative enzymes goes an increase in the capacity to oxidize fatty acids (MolC, Oscai and Holloszy 1971). Thus, the decreased glycogen consumption observed in thir study most probably is due to enhanced oxidative capacity, which in turn leads to a higher capacity to oxidize fat.

‘This work was supported by grants from the Delegation for Applied Medical Defence Research and Swedish Medical Research Council (4OX-2203).

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