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Magnitude and duration of excess postexercise oxygen consumption in healthy young subjects
Magnitude and Duration of Excess Postexercise Oxygen Consumption in Healthy Young Subjects Sverre Maehlum,
Michile
Grandmontagne,
Eric A. Newsholme,
and Ole M. Sejersted
Postexercise oxygen consumption was investigated in eight healthy subjects. The subjects exercised for about 80 minutes at 70% of their maximum VO,. Following the exercise the subjects rested in bed for 24 hours. Oxygen uptake was measured continuously during the first hour after exercise, then hourly for the next 11 hours, and finally at 24 hours after exercise. Heart rate and rectal temperature were recorded continuously during the first 12 hours and then at 24 hours after exercise. Blood was sampled hourly after exercise. The results were compared with those of an identical control experiment in which the subjects rested instead of exercising. Oxygen uptake of each time point in each subject was greater after exercise compared with the control experiment. Mean total oxygen consumption after exercise was 211 + 16 L/12 h as compared to 185 + 13 L/12 h in the control experiment (P < 0.001 I. Also, the heart rate was higher during the first 12 hours following exercise than in the control study. No significant differences were observed in rectal temperature in the two experiments after the initial 30 minutes following exercise. The first meal taken after the cessation of exercise increased markedly the rate of oxygen consumption in comparison to the increase observed following the same meal in the control experiment. The respiratory exchange ratios were lower following exercise than in the control study. In conclusion, we have demonstrated that the excess postexercise oxygen consumption (EPOC), may persist for at least 12 hours, and possibly for 24 hours. Also, exercise caused enhancement of the stimulation in oxygen uptake seen after a meal. Thus, endurance exercise may be of importance in body weight control, not only by increasing the energy requirements during exercise, but also through its effect on basal metabolism following exercise. Q 1986 by Grune & Stretton, Inc.
I
T IS GENERALLY accepted that the increased oxygen consumption that occurs during exercise declines only slowly when exercise ceases. IV2This extra oxygen consumption after exercise has been variously known as oxygen debt, recovery oxygen, and, more recently, excess postexercise oxygen consumption (EPOC).3 However, although its existence may be well established, the magnitude, duration, and biochemical or physiologic basis of EPOC are still debated. Thus, estimations of the duration of EPOC vary from 30 minutes to 72 hours2@ The problem may be further complicated by the fact that some workers have divided EPOC into three components: fast, slow, and ultraslow;’ and it is not always clear which component is being studied. Large variations in the magnitude of EPOC have been reported. For example, Benedict & Cathcart* reported that oxygen consumption was 13% above basal seven hours after exercise. Edwards et al4 reported that oxygen consumption was 23% above basal 13 hours after exercise, whereas Dallosso & James’ report no significant increase in energy expenditure during eight hours following exercise. Furthermore, the effect of previous exercise on the magnitude of the thermic effect of food is controversial. Miller et al” observed a marked increase in the thermic effect of food after exercise, whereas Dallosso & James9 observed no effect. There are several variabilities in such studies. These are difficult to control and might explain some of the aforementioned variations. The duration and magnitude of EPOC may depend upon the intensity and duration of the exercise,” it may also depend upon the environmental temperature or the previous dietary history. Resting oxygen consumption may vary diurnally so that control values should be taken at the same time of day as the postexercise values. The thermic response of food may vary with the quantity and nature of the food. The present study was designed to minimize these problems by investigating the effect of standard exercise for a
given duration on oxygen consumption
for 24 hours after
Merabolism, Vol 35, No 5 (May), 1986: pp 425-429
cessation of exercise under controlled conditions. The control measurements were done under exactly the same conditions except that the subjects rested instead of exercised. Finally, the effect of two standard simple meals on oxygen consumption were studied during the control and postexercise experiments. MATERIALS
AND METHODS
Subjects Eight subjects, four males and four females, participated in the study. Data concerning their physical characteristics are presented in Table 1. The nature, purpose, and possible risks involved in the study were carefully explained to all subjects before their written consent to participate was obtained. In addition, the subjects completed a medical examination before starting the experiments. None of the subjects participated in competitive sports at the time of the study. Subject EN used to participate in competitive cycling, but had not done so the last three months prior to the study due to an injury. He trained about 4 to 5 times a week at the time of the study. The four female subjects all exercised for about one hour three times a week. PH, LFH, and BOB exercised 1 to 3 times a week, each session lasting about 45 to 60 minutes. Testing Procedures All subjects were familiarized with the equipment to be used in the testing and the actual experiments (eg, bicycle, mouthpiece, tape recorder) before the start of the tests. Maximal ir0, was determined on a modified Krogh electrically braked bicycle ergometer, using the criteria of Taylor et al.‘?
From the Institute of Muscle Physiology, Oslo and the Department of Biochemistry, University of Oxford, Oxford. England. Address reprint requests to Ole M. Sejersted. MD, Institute of Muscle Physiology, PO Box 8149 DEP, N-0033 Oslo 1, NORWA Y. o I986 by Grune & Stratton, Inc. 0026-0495/s6~3505-0009$03.00/0 425
426
MAEHLUM
Table 1. Physical Characteristics Subject Sex
Age (yr)
Height Weight (cm) {kg)
~O,max 1/min
Wwk w
of Subjects Load % max Go*
Exercise (mini
EN
M
21
189
83
4.66
235
87
MM
F
22
168
64
2.12
100
60
80
ER
F
23
163
52
1.88
75
73
90
90
PH
M
24
184
70
3.99
185
64
75
TH
F
20
176
69
2.96
110
62
65
LFH
M
20
189
80
3.53
165
79
70
BOB
M
24
194
80
4.11
200
78
83
TE
F
23
170
60
3.16
150
66
85
22.1
179.1
69.8
3.30
152.5
71.1
79.8
11.4
10.9
0.97
54.6
9.6
9.1
MEAN SD
1.6
Experimental
ET AL
Protocol
Each subject participated in one exercise and one control experiment. The two experiments were separated by at least one week. Half the subjects performed the exercise experiment first, whereas the other half performed the control experiment first. The general experimental design is shown in Fig 1. The subjects reported to the laboratory at 7 AM after an overnight fast. They travelled to the laboratory by car or by street car to minimize physical activity on the day of the experiment. They did not participate in any strenuous physical activity for the two days prior to the experiment day. Body weight was measured at the start of the experiments. The subjects were connected to an electrocardiograph (Diascope DS 521, Simonsen & Weel, Albertslund, Denmark), using a modified V lead; a thermistor (Type DU 3S, Ellab A/S, Copenhagen), was inserted into the rectum and a flexible catheter was inserted into an antecubital vein. The subjects then rested for about 30 minutes, and subsequently two baseline blood and expiratory air samples were obtained. The subjects exercised on the bicycle at a work load corresponding to about 70% of their maximal VO, for 3 or 4 periods of 10 to 30 minutes duration with a rest period of 5 minutes between each exercise period. When the subjects had exercised for 90 minutes or were unable to complete a IO-minute work period, the exercise was ended. During the control experiments, the subjects rested for 90 minutes in bed in the supine position instead of exercising. Following the exercise or the 90 minute rest period in the control experiments, the subjects rested in bed in the supine position for 24 hours. Sleep was not allowed during the initial 12 hours of recovery, The subjects did not shower following the exercise. They were given three meals during this period (Fig 1); the meals consisted of bread, jam, and skimmed milk. They were allowed to eat ad libitum during their first experiment. The food was weighed, and they were then given the same amount during the second experiment.
Measurement Heart rate and rectal temperature were recorded continuously from 30 minutes before until I2 hours following exercise or the 90
3600
J
L
1
#RECOVERY
14
1
Fig 2. Changes in oxygen uptake (A). rectal temperature (B), and heart rate (Cj in the exercise experiments (open circles). and control experiments (filled circles). Hatched columns denote meals. Values are the mean 5 SEM of eight subjects.
minute rest period. Oxygen uptake was measured during the last I5 minutes of the rest period before exercise and once during the exercise period. Postexercise oxygen uptake was measured continuously for the first hour and then for 10 to I5 minutes in the last 15 minutes of every hour for the next 11 hours. Finally, heart rate,
Table 2. Total Oxygen Consumption
Following Exercise
Ll12h
Exercise L/12 h
EM
248
296
MM
145
165
ER
150
160
PH
200
233
Control
Subject
TH
162
179
LFH
209
242 221
BOB
203
TE
164
189
MEAN
185
211
36
46
SD
POSTEXERCISE OXYGEN CONSUMPTION
427
temperature, and oxygen uptake was measured 24 hours after the start of exercise. Blood was sampled before, during, and hourly after the exercise (Fig 1). Expired air was collected in Douglas bags and the volume was measured in a wet spirometer. Oxygen and carbon dioxide concentrations were determined using the Scholander apparatus.” Enzymatic methods were used for the determination of plasma glucose, lactate, and glycerol.‘4 InsulinI and cortisol’6 were measured with radioimmunological techniques. Free T1 was measured using a ‘*‘I-T4 analog with a one step method (Amersham). All data are given as the mean r SEM unless otherwise stated. Students’ r-test was used to estimate ments.
the significance
of differences
between
experi-
Rectal Temperature
The rectal temperature rose from 36.48 “C to 38.60 “C immediately after exercise (Fig 2B). However, the temperature then decreased rapidly and reached a near baseline level about 30 minutes after exercise. The mean rectal temperatures tended to be higher during the 12 hours following exercise than during the control experiment. The differences, however, did not achieve statistical significance. Heart Rate
The mean basal heart rate was similar in the two experiments (Fig 2C). In the exercise experiment, mean heart rate
RESULTS
Oxygen Consumption
Mean basal oxygen consumption prior to the tests were similar in the control and exercise experiments, being 237 * I8 and 226 c 17 m L/min, respectively (Fig 2A). Oxygen consumption increased to 2397 t 336 mL/min during exercise. After exercise, the oxygen consumption was higher than during the corresponding control experiments throughout the 12-hour observation period (Fig 2A). In addition, we observed significantly higher oxygen consumption 24 hours after exercise in comparison to that observed 24 hours after the start of the control experiment (P K 0.05). Oxygen consumption increased following the ingestion of meals in both experiments (Fig 2A). The increase after the first meal was greater in the exercise than in the control experiment (P =ZI0.05). Mean total oxygen consumption following exercisewas185 + 13and211 i 16L/12hforthecontroland exercise experiments, respectively (Table 2); this difference was statistically significant (P < 0.001).
300 h < z E = 200 Y i F
100
6 0
120
0
0
4
8
12
24
TIME (hrs) EX
Fig 3. Changes in R-value in exercise (open circles) and control experiments (filled circles). Hatched columns indicate meals. Values are the mean k SEM of eight subjects.
T RECOVERY
$
/$
I
Fig 4. Changes in the plasma concentration of glycerol (upper panel), insulin (middle panel), and glucose (lower panel) in the exercise experiments (open circles) and control experiments (filled circles). Hatched columns indicate meals. Values are the mean + SEM of eight subjects.
428
MAEHLUM
basal preexercising rate, but the duration and magnitude of this extra oxygen consumption has been markedly variable.‘vc7 In the present work, the intensity and durqtion of the exercise was standardized at 70% of maximum V02 for 90 minutes and, in addition, oxygen consumption was measured each hour for 12 hours after the exercise and also at 24 hours after exercise. A control experiment was carried out on each subject under identical conditions except that no exercise was taken. The results demonstrate that the rate of oxygen consumption for each subject at each time point was greater after exercise compared to the control condition. These findings rule out the possibility that the higher rates of oxygen consumption after exercise were due to poor control data or diurnal variations in oxygen consumption. An important finding in this work was that the first meal, taken 2 hours after cessation of exercise, markedly increased the rate of oxygen consumption in comparison to the increase observed in the response to the same meal in the same subject when no exercise had been taken. However, the second meal, which was taken some eight hours after the cessation of exercise, caused no statistically significant further increase in oxygen consumption in the exercise experiment. Hence the effect of a meal on the magnitude of EPOC may depend on when the meal is taken after the exercise has finished. The R-value remained lower after exercise for almost all of the time points measured in comparison to the nonexercise controls. This indicates that more fat (presumably fatty acid) is oxidized in the recovery period after exercise and that this increased fat oxidation is maintained for at least 24 hours postexercise. This finding suggests that the plasma fatty acid level is elevated for the 24-hour period postexercise, and the elevated plasma glycerol levels (Fig 4) are consistent with this suggestion. This proposed increase in the rate of fatty acid oxidation could account for the higher plasma levels of glucose observed after meals (Fig 4), which cannot be explained by lower insulin levels (Fig 4); the oxidation of fatty acid is known to decrease the rate of glucose utilisation and oxidation, known as the glucose/fatty acid cycle.” A decreased rate of glucose utilization and oxidation after exercise may permit more of the ingested glucose to be used for repletion of glycogen in the muscle. Upon refeeding after exercise, muscle glycogen is synthesised before that in the liver,18 and the present findings suggest that the elevated rate of fatty acid oxidation may
increased to 178 k 5 beats/min. The heart rate then decreased rapidly the first 30 minutes after exercise. However, the mean heart rate following exercise was significantly higher than during the control experiment all through the 12-hour observation period (Fig 2C). Respiratory Exchange Ratio (R-value}
The mean basal R-value was similar in the morning of both experiments (Fig 3). During exercise the R-value increased to 0.88 and then fell sharply immediately following exercise. With the exception of the values at five and seven hours after exercise, for the first nine hrs after exercise the recovery R-values were significantly lower than those obtained during the control experiment. In addition, the R-values at 12 and 24 hours after exercise were significantly lower than the corresponding control R-values (Fig 3). Glucose, insulin, and Glycerol Resting plasma glucose concentration was similar in both experiments (Fig 4). No change was observed in response to exercise. The glucose concentration increased in response to the meals in both experiments. However, the increase was larger following both meals after exercise than after rest (P < 0.05). No statistically significant differences were observed in plasma insulin concentration between the exercise and control experiments (Fig 4). Plasma glycerol concentration increased in response to exercise and stayed elevated above the values in the control experiment all through the recovery period (Fig 4). Free T, and Cortisol No statistically significant differences were observed in plasma free T4 concentration in the four subjects tested throughout the experiments (Table 3). Plasma cortisol concentrations were elevated during the exercise period and for one hour postexercise. After this time no statistically significant differences were observed between the two experiments (Table 3). DISCUSSION
Previous studies have shown that, following a period of exercise, resting oxygen consumption is elevated above the Table
3.
Changes
ET AL
in Cortisol
and
Free
T4 Concentration
Hours Postexercise Variable
(Basal)
(Basal)
1
2
3
4
5
6
7
8
9
10
11
12
24
Cortisol (pmol/L) Control exp
Exercise exp
436
348
332
322
+48
+60
k80
k90
334 k116
246
232
243
256
263
205
154
124
105
409
t63
+66
*57
*55
t76
*60
+5B
*46
*39
k74
468
780
602
455
311
231
158
173
218
256
181
117
i46
i42
*45
*41
+-35
*33
+28
A39
+31
i40
+30
*22
92 +19
109
357
r37
k39
Free Tl (pmol/LI Control exp
Exercise exp
Values Control
are mean exp refers
15.1
13.7
13.7
14.5
14.6
13.9
14.0
13.3
14.0
12.8
kO.7
20.8
21.3
+1.0
+0.7
*1.1
kO.5
k1.1
kO.6
+0.6
13.5 +0.6
14.3
12.8
12.6
13.2
kO.7
?0.6
to.8
to.9
14.0
15.2
15.3
14.4
14.6
14.2
14.6
14.8
14.0
14.7
14.9
13.1
13.6
13.1
15.2
t1.5
*I.3
kl.9
+1.6
*2.2
*1.5
*I.1
*0.9
*I.1
*0.4
*to.2
io.3
e1.2
to.7
k1.2
f
SE. to two
experiment
days
with
bed rest:
exercise
exp refers
to exercise
followed
by bed rest.
POSTEXERCISEOXYGEN CONSUMPTION
429
play a role in facilitating glucose conversion to glycogen in the muscle. The biochemical basis for EPOC is not known. The possibility that an increased rate of substrate (futile) cycling in muscle and/or other tissues could be responsible for some of the EPOC has been discussed previously.‘9~” Furthermore, catecholamines have been shown to increase the rate of the triglyceride/fatty acid cycle in white and brown adipose tissue in viva” and the fructose 6-phosphate/fructose bisphosphate cycle in muscIe22 in vitro,23 and catecholamines are known to be calorigenic.22 It is also known that plasma catecholamine levels are elevated for some time after exercise.24S25Hence, it is suggested that, during postexercise periods, the plasma levels of catecholamines are increased, leading to a stimulation of the rate of some substrate cycles,
which demand energy expenditure; this could account for some of the extra oxygen consumption after exercise. Whatever the mechanism of EPOC, the fact that it can persist for a long period of time, that a greater rate of fat oxidation occurs, and that the stimulation of oxygen consumption by a meal is considerably enhanced after exercise, supports the view that regular endurance exercise may be of value in body weight control.‘9.20
ACKNOWLEDGMENT
The present study was initiated by the late Director of the Institute of Muscle Physiology, Lam Hermansen. We are indebted to the Hormone Laboratory, Aker Hospital, Oslo, for performing the insulin, cortiso!, and free T,-analysis.
REFERENCES
I. Hill AV, Long CNH, Lupton H: Muscular exercise, lactic acid, and the supply and utilization of oxygen. Part V. The recovery process after exercise in men. Proc R Sot Lond 97:96-l 38, 1924 2. Margaria R, Edwards HT, Dill DB: The possible mechanisms of contracting and paying the oxygen debt and the role of lactic acid in muscular contraction. Am J Physio! 106:689-715, 1933 3. Gaesser GA, Brooks GA: Metabolic bases of excess postexercise oxygen consumption: a review. Med Sci Sports Exert 16:29-43, 1984 4. Edwards HT, Thorndike A Jr, Dill DB: The energy requirement in strenuous muscular exercise. N Eng! J Med 213:532-535, 1935 5. Herxheimer H, Wissing E, Wolff E: Spatwirkungen erschiipfender muskelarbeit auf den Sauerstoffverbrauch. Z Schr F Exp Med 5 1:9 16-928, 1926 6. Passmore P, Johnsen RE: Some metabolic changes following prolonged moderate exercise. Metabolism 9:452-456, 1960 7. deVries HA, Gray DE: After effects of exercise upon resting metabolic rate. Res Q 34:314-321, 1963 8. Benedict FG, Cathcart EP: Muscular work-a metabolic study with special reference to the efficiency of the human body as a machine. Washington DC, Carnegie Mellon Institute of Research, 1913, No. 187 9. Dallosso H, James WPT: Dietary thermogenesis and exercise. Proc Nutr Sot 41:35A, 1982 10. Miller DS, Mumford P, Stock MJ: Gluttory 2. Thermogenesis in overeating man. Am J Clin Nutr 20:1223-1229, 1967 11. Knuttgen HG: Oxygen debt after submaximal physical exercise. J App! Physio! 29:651-657, 1970 12. Taylor HL, Buskirk E, Henschel A: Maxima! oxygen intake as an objective measure of cardiorespiratory performance. J App! Physio! 8:73-80, 1955 13. Scholander PF: Analyzer for accurate estimation of respiratory gases in one half cubicmeter samples. I Biol Chem 167:235249, 1947
14. Lowry OH, Passonneau JV: A Flexible System of Enzymatic Analysis. Orlando, Fla, Academic, 1972 15. Fdlling I, Norman N: Hyperglycemia, hypoglycemic attacks and production of antiinsulin antibodies without previous known immunization. Diabetes 21:8 14-826, 1972 16. Opstad PK, Aakvaag A, Rognum T: Altered hormonal response to short-term bicycle exercise in young men after prolonged physical strain, caloric deficit, and sleep deprivation. Eur J Applied Physiol45:5 l-62, 1980 17. Newsholme EA. Leech AR: Biochemistry for the Medical Sciences, pp. 336-342. Wiley, Chichester, UK, 1983 18. Maehlum S, Felig P, Wahren J: Splanchnic glucose and muscle glycogen metabolism after glucose feeding during postexercise recovery. Am J Physiol235:E255-E260, 1978 19. Newsholme EA: Substrate cycles: Their metabolic, energetic and thermic consequences in man. B&hem Sot Symp 43: 183-205, 1978 20. Newsholme EA: A possible metabolic basis for the control of body weight. N Eng! J Med 302:40&405,1980 21. Brooks BJ, Arch JRS, Newsholme EA: Effect of some hormones on the rate of the triag!ycero!/fatty-acid substrate cycle in adipose tissue of the mouse in vivo. Biosc Rep 3:263-267, 1983 22. Steinberg D: Fatty acid mobilization-mechanisms of regulation and metabolic consequences. Biochem Sot Symp 24: 11I-144, 1963 23. Challiss RAJ, Arch JRS, Newsholme EA: The rate of substrate cycling between fructose 6-phosphate and fructose 1.6biphosphate in skeletal muscle. Biochem J 221: 153-l 6 1, 1984 24. KIrki NT: The urinary excretion of noradrenaline and adrenaline in different age groups, its diurnal variation, and the effect of muscular work on it. Acta Physiol Stand 39, 1956 (supp! 132) 25. Maron MB, Horvath SM, Wilkerson JE: Blood biochemical alterations during a recovery from competitive marathon running. Eur J Applied Physiol 36:231-238, 1977
Michile
Grandmontagne,
Eric A. Newsholme,
and Ole M. Sejersted
Postexercise oxygen consumption was investigated in eight healthy subjects. The subjects exercised for about 80 minutes at 70% of their maximum VO,. Following the exercise the subjects rested in bed for 24 hours. Oxygen uptake was measured continuously during the first hour after exercise, then hourly for the next 11 hours, and finally at 24 hours after exercise. Heart rate and rectal temperature were recorded continuously during the first 12 hours and then at 24 hours after exercise. Blood was sampled hourly after exercise. The results were compared with those of an identical control experiment in which the subjects rested instead of exercising. Oxygen uptake of each time point in each subject was greater after exercise compared with the control experiment. Mean total oxygen consumption after exercise was 211 + 16 L/12 h as compared to 185 + 13 L/12 h in the control experiment (P < 0.001 I. Also, the heart rate was higher during the first 12 hours following exercise than in the control study. No significant differences were observed in rectal temperature in the two experiments after the initial 30 minutes following exercise. The first meal taken after the cessation of exercise increased markedly the rate of oxygen consumption in comparison to the increase observed following the same meal in the control experiment. The respiratory exchange ratios were lower following exercise than in the control study. In conclusion, we have demonstrated that the excess postexercise oxygen consumption (EPOC), may persist for at least 12 hours, and possibly for 24 hours. Also, exercise caused enhancement of the stimulation in oxygen uptake seen after a meal. Thus, endurance exercise may be of importance in body weight control, not only by increasing the energy requirements during exercise, but also through its effect on basal metabolism following exercise. Q 1986 by Grune & Stretton, Inc.
I
T IS GENERALLY accepted that the increased oxygen consumption that occurs during exercise declines only slowly when exercise ceases. IV2This extra oxygen consumption after exercise has been variously known as oxygen debt, recovery oxygen, and, more recently, excess postexercise oxygen consumption (EPOC).3 However, although its existence may be well established, the magnitude, duration, and biochemical or physiologic basis of EPOC are still debated. Thus, estimations of the duration of EPOC vary from 30 minutes to 72 hours2@ The problem may be further complicated by the fact that some workers have divided EPOC into three components: fast, slow, and ultraslow;’ and it is not always clear which component is being studied. Large variations in the magnitude of EPOC have been reported. For example, Benedict & Cathcart* reported that oxygen consumption was 13% above basal seven hours after exercise. Edwards et al4 reported that oxygen consumption was 23% above basal 13 hours after exercise, whereas Dallosso & James’ report no significant increase in energy expenditure during eight hours following exercise. Furthermore, the effect of previous exercise on the magnitude of the thermic effect of food is controversial. Miller et al” observed a marked increase in the thermic effect of food after exercise, whereas Dallosso & James9 observed no effect. There are several variabilities in such studies. These are difficult to control and might explain some of the aforementioned variations. The duration and magnitude of EPOC may depend upon the intensity and duration of the exercise,” it may also depend upon the environmental temperature or the previous dietary history. Resting oxygen consumption may vary diurnally so that control values should be taken at the same time of day as the postexercise values. The thermic response of food may vary with the quantity and nature of the food. The present study was designed to minimize these problems by investigating the effect of standard exercise for a
given duration on oxygen consumption
for 24 hours after
Merabolism, Vol 35, No 5 (May), 1986: pp 425-429
cessation of exercise under controlled conditions. The control measurements were done under exactly the same conditions except that the subjects rested instead of exercised. Finally, the effect of two standard simple meals on oxygen consumption were studied during the control and postexercise experiments. MATERIALS
AND METHODS
Subjects Eight subjects, four males and four females, participated in the study. Data concerning their physical characteristics are presented in Table 1. The nature, purpose, and possible risks involved in the study were carefully explained to all subjects before their written consent to participate was obtained. In addition, the subjects completed a medical examination before starting the experiments. None of the subjects participated in competitive sports at the time of the study. Subject EN used to participate in competitive cycling, but had not done so the last three months prior to the study due to an injury. He trained about 4 to 5 times a week at the time of the study. The four female subjects all exercised for about one hour three times a week. PH, LFH, and BOB exercised 1 to 3 times a week, each session lasting about 45 to 60 minutes. Testing Procedures All subjects were familiarized with the equipment to be used in the testing and the actual experiments (eg, bicycle, mouthpiece, tape recorder) before the start of the tests. Maximal ir0, was determined on a modified Krogh electrically braked bicycle ergometer, using the criteria of Taylor et al.‘?
From the Institute of Muscle Physiology, Oslo and the Department of Biochemistry, University of Oxford, Oxford. England. Address reprint requests to Ole M. Sejersted. MD, Institute of Muscle Physiology, PO Box 8149 DEP, N-0033 Oslo 1, NORWA Y. o I986 by Grune & Stratton, Inc. 0026-0495/s6~3505-0009$03.00/0 425
426
MAEHLUM
Table 1. Physical Characteristics Subject Sex
Age (yr)
Height Weight (cm) {kg)
~O,max 1/min
Wwk w
of Subjects Load % max Go*
Exercise (mini
EN
M
21
189
83
4.66
235
87
MM
F
22
168
64
2.12
100
60
80
ER
F
23
163
52
1.88
75
73
90
90
PH
M
24
184
70
3.99
185
64
75
TH
F
20
176
69
2.96
110
62
65
LFH
M
20
189
80
3.53
165
79
70
BOB
M
24
194
80
4.11
200
78
83
TE
F
23
170
60
3.16
150
66
85
22.1
179.1
69.8
3.30
152.5
71.1
79.8
11.4
10.9
0.97
54.6
9.6
9.1
MEAN SD
1.6
Experimental
ET AL
Protocol
Each subject participated in one exercise and one control experiment. The two experiments were separated by at least one week. Half the subjects performed the exercise experiment first, whereas the other half performed the control experiment first. The general experimental design is shown in Fig 1. The subjects reported to the laboratory at 7 AM after an overnight fast. They travelled to the laboratory by car or by street car to minimize physical activity on the day of the experiment. They did not participate in any strenuous physical activity for the two days prior to the experiment day. Body weight was measured at the start of the experiments. The subjects were connected to an electrocardiograph (Diascope DS 521, Simonsen & Weel, Albertslund, Denmark), using a modified V lead; a thermistor (Type DU 3S, Ellab A/S, Copenhagen), was inserted into the rectum and a flexible catheter was inserted into an antecubital vein. The subjects then rested for about 30 minutes, and subsequently two baseline blood and expiratory air samples were obtained. The subjects exercised on the bicycle at a work load corresponding to about 70% of their maximal VO, for 3 or 4 periods of 10 to 30 minutes duration with a rest period of 5 minutes between each exercise period. When the subjects had exercised for 90 minutes or were unable to complete a IO-minute work period, the exercise was ended. During the control experiments, the subjects rested for 90 minutes in bed in the supine position instead of exercising. Following the exercise or the 90 minute rest period in the control experiments, the subjects rested in bed in the supine position for 24 hours. Sleep was not allowed during the initial 12 hours of recovery, The subjects did not shower following the exercise. They were given three meals during this period (Fig 1); the meals consisted of bread, jam, and skimmed milk. They were allowed to eat ad libitum during their first experiment. The food was weighed, and they were then given the same amount during the second experiment.
Measurement Heart rate and rectal temperature were recorded continuously from 30 minutes before until I2 hours following exercise or the 90
3600
J
L
1
#RECOVERY
14
1
Fig 2. Changes in oxygen uptake (A). rectal temperature (B), and heart rate (Cj in the exercise experiments (open circles). and control experiments (filled circles). Hatched columns denote meals. Values are the mean 5 SEM of eight subjects.
minute rest period. Oxygen uptake was measured during the last I5 minutes of the rest period before exercise and once during the exercise period. Postexercise oxygen uptake was measured continuously for the first hour and then for 10 to I5 minutes in the last 15 minutes of every hour for the next 11 hours. Finally, heart rate,
Table 2. Total Oxygen Consumption
Following Exercise
Ll12h
Exercise L/12 h
EM
248
296
MM
145
165
ER
150
160
PH
200
233
Control
Subject
TH
162
179
LFH
209
242 221
BOB
203
TE
164
189
MEAN
185
211
36
46
SD
POSTEXERCISE OXYGEN CONSUMPTION
427
temperature, and oxygen uptake was measured 24 hours after the start of exercise. Blood was sampled before, during, and hourly after the exercise (Fig 1). Expired air was collected in Douglas bags and the volume was measured in a wet spirometer. Oxygen and carbon dioxide concentrations were determined using the Scholander apparatus.” Enzymatic methods were used for the determination of plasma glucose, lactate, and glycerol.‘4 InsulinI and cortisol’6 were measured with radioimmunological techniques. Free T1 was measured using a ‘*‘I-T4 analog with a one step method (Amersham). All data are given as the mean r SEM unless otherwise stated. Students’ r-test was used to estimate ments.
the significance
of differences
between
experi-
Rectal Temperature
The rectal temperature rose from 36.48 “C to 38.60 “C immediately after exercise (Fig 2B). However, the temperature then decreased rapidly and reached a near baseline level about 30 minutes after exercise. The mean rectal temperatures tended to be higher during the 12 hours following exercise than during the control experiment. The differences, however, did not achieve statistical significance. Heart Rate
The mean basal heart rate was similar in the two experiments (Fig 2C). In the exercise experiment, mean heart rate
RESULTS
Oxygen Consumption
Mean basal oxygen consumption prior to the tests were similar in the control and exercise experiments, being 237 * I8 and 226 c 17 m L/min, respectively (Fig 2A). Oxygen consumption increased to 2397 t 336 mL/min during exercise. After exercise, the oxygen consumption was higher than during the corresponding control experiments throughout the 12-hour observation period (Fig 2A). In addition, we observed significantly higher oxygen consumption 24 hours after exercise in comparison to that observed 24 hours after the start of the control experiment (P K 0.05). Oxygen consumption increased following the ingestion of meals in both experiments (Fig 2A). The increase after the first meal was greater in the exercise than in the control experiment (P =ZI0.05). Mean total oxygen consumption following exercisewas185 + 13and211 i 16L/12hforthecontroland exercise experiments, respectively (Table 2); this difference was statistically significant (P < 0.001).
300 h < z E = 200 Y i F
100
6 0
120
0
0
4
8
12
24
TIME (hrs) EX
Fig 3. Changes in R-value in exercise (open circles) and control experiments (filled circles). Hatched columns indicate meals. Values are the mean k SEM of eight subjects.
T RECOVERY
$
/$
I
Fig 4. Changes in the plasma concentration of glycerol (upper panel), insulin (middle panel), and glucose (lower panel) in the exercise experiments (open circles) and control experiments (filled circles). Hatched columns indicate meals. Values are the mean + SEM of eight subjects.
428
MAEHLUM
basal preexercising rate, but the duration and magnitude of this extra oxygen consumption has been markedly variable.‘vc7 In the present work, the intensity and durqtion of the exercise was standardized at 70% of maximum V02 for 90 minutes and, in addition, oxygen consumption was measured each hour for 12 hours after the exercise and also at 24 hours after exercise. A control experiment was carried out on each subject under identical conditions except that no exercise was taken. The results demonstrate that the rate of oxygen consumption for each subject at each time point was greater after exercise compared to the control condition. These findings rule out the possibility that the higher rates of oxygen consumption after exercise were due to poor control data or diurnal variations in oxygen consumption. An important finding in this work was that the first meal, taken 2 hours after cessation of exercise, markedly increased the rate of oxygen consumption in comparison to the increase observed in the response to the same meal in the same subject when no exercise had been taken. However, the second meal, which was taken some eight hours after the cessation of exercise, caused no statistically significant further increase in oxygen consumption in the exercise experiment. Hence the effect of a meal on the magnitude of EPOC may depend on when the meal is taken after the exercise has finished. The R-value remained lower after exercise for almost all of the time points measured in comparison to the nonexercise controls. This indicates that more fat (presumably fatty acid) is oxidized in the recovery period after exercise and that this increased fat oxidation is maintained for at least 24 hours postexercise. This finding suggests that the plasma fatty acid level is elevated for the 24-hour period postexercise, and the elevated plasma glycerol levels (Fig 4) are consistent with this suggestion. This proposed increase in the rate of fatty acid oxidation could account for the higher plasma levels of glucose observed after meals (Fig 4), which cannot be explained by lower insulin levels (Fig 4); the oxidation of fatty acid is known to decrease the rate of glucose utilisation and oxidation, known as the glucose/fatty acid cycle.” A decreased rate of glucose utilization and oxidation after exercise may permit more of the ingested glucose to be used for repletion of glycogen in the muscle. Upon refeeding after exercise, muscle glycogen is synthesised before that in the liver,18 and the present findings suggest that the elevated rate of fatty acid oxidation may
increased to 178 k 5 beats/min. The heart rate then decreased rapidly the first 30 minutes after exercise. However, the mean heart rate following exercise was significantly higher than during the control experiment all through the 12-hour observation period (Fig 2C). Respiratory Exchange Ratio (R-value}
The mean basal R-value was similar in the morning of both experiments (Fig 3). During exercise the R-value increased to 0.88 and then fell sharply immediately following exercise. With the exception of the values at five and seven hours after exercise, for the first nine hrs after exercise the recovery R-values were significantly lower than those obtained during the control experiment. In addition, the R-values at 12 and 24 hours after exercise were significantly lower than the corresponding control R-values (Fig 3). Glucose, insulin, and Glycerol Resting plasma glucose concentration was similar in both experiments (Fig 4). No change was observed in response to exercise. The glucose concentration increased in response to the meals in both experiments. However, the increase was larger following both meals after exercise than after rest (P < 0.05). No statistically significant differences were observed in plasma insulin concentration between the exercise and control experiments (Fig 4). Plasma glycerol concentration increased in response to exercise and stayed elevated above the values in the control experiment all through the recovery period (Fig 4). Free T, and Cortisol No statistically significant differences were observed in plasma free T4 concentration in the four subjects tested throughout the experiments (Table 3). Plasma cortisol concentrations were elevated during the exercise period and for one hour postexercise. After this time no statistically significant differences were observed between the two experiments (Table 3). DISCUSSION
Previous studies have shown that, following a period of exercise, resting oxygen consumption is elevated above the Table
3.
Changes
ET AL
in Cortisol
and
Free
T4 Concentration
Hours Postexercise Variable
(Basal)
(Basal)
1
2
3
4
5
6
7
8
9
10
11
12
24
Cortisol (pmol/L) Control exp
Exercise exp
436
348
332
322
+48
+60
k80
k90
334 k116
246
232
243
256
263
205
154
124
105
409
t63
+66
*57
*55
t76
*60
+5B
*46
*39
k74
468
780
602
455
311
231
158
173
218
256
181
117
i46
i42
*45
*41
+-35
*33
+28
A39
+31
i40
+30
*22
92 +19
109
357
r37
k39
Free Tl (pmol/LI Control exp
Exercise exp
Values Control
are mean exp refers
15.1
13.7
13.7
14.5
14.6
13.9
14.0
13.3
14.0
12.8
kO.7
20.8
21.3
+1.0
+0.7
*1.1
kO.5
k1.1
kO.6
+0.6
13.5 +0.6
14.3
12.8
12.6
13.2
kO.7
?0.6
to.8
to.9
14.0
15.2
15.3
14.4
14.6
14.2
14.6
14.8
14.0
14.7
14.9
13.1
13.6
13.1
15.2
t1.5
*I.3
kl.9
+1.6
*2.2
*1.5
*I.1
*0.9
*I.1
*0.4
*to.2
io.3
e1.2
to.7
k1.2
f
SE. to two
experiment
days
with
bed rest:
exercise
exp refers
to exercise
followed
by bed rest.
POSTEXERCISEOXYGEN CONSUMPTION
429
play a role in facilitating glucose conversion to glycogen in the muscle. The biochemical basis for EPOC is not known. The possibility that an increased rate of substrate (futile) cycling in muscle and/or other tissues could be responsible for some of the EPOC has been discussed previously.‘9~” Furthermore, catecholamines have been shown to increase the rate of the triglyceride/fatty acid cycle in white and brown adipose tissue in viva” and the fructose 6-phosphate/fructose bisphosphate cycle in muscIe22 in vitro,23 and catecholamines are known to be calorigenic.22 It is also known that plasma catecholamine levels are elevated for some time after exercise.24S25Hence, it is suggested that, during postexercise periods, the plasma levels of catecholamines are increased, leading to a stimulation of the rate of some substrate cycles,
which demand energy expenditure; this could account for some of the extra oxygen consumption after exercise. Whatever the mechanism of EPOC, the fact that it can persist for a long period of time, that a greater rate of fat oxidation occurs, and that the stimulation of oxygen consumption by a meal is considerably enhanced after exercise, supports the view that regular endurance exercise may be of value in body weight control.‘9.20
ACKNOWLEDGMENT
The present study was initiated by the late Director of the Institute of Muscle Physiology, Lam Hermansen. We are indebted to the Hormone Laboratory, Aker Hospital, Oslo, for performing the insulin, cortiso!, and free T,-analysis.
REFERENCES
I. Hill AV, Long CNH, Lupton H: Muscular exercise, lactic acid, and the supply and utilization of oxygen. Part V. The recovery process after exercise in men. Proc R Sot Lond 97:96-l 38, 1924 2. Margaria R, Edwards HT, Dill DB: The possible mechanisms of contracting and paying the oxygen debt and the role of lactic acid in muscular contraction. Am J Physio! 106:689-715, 1933 3. Gaesser GA, Brooks GA: Metabolic bases of excess postexercise oxygen consumption: a review. Med Sci Sports Exert 16:29-43, 1984 4. Edwards HT, Thorndike A Jr, Dill DB: The energy requirement in strenuous muscular exercise. N Eng! J Med 213:532-535, 1935 5. Herxheimer H, Wissing E, Wolff E: Spatwirkungen erschiipfender muskelarbeit auf den Sauerstoffverbrauch. Z Schr F Exp Med 5 1:9 16-928, 1926 6. Passmore P, Johnsen RE: Some metabolic changes following prolonged moderate exercise. Metabolism 9:452-456, 1960 7. deVries HA, Gray DE: After effects of exercise upon resting metabolic rate. Res Q 34:314-321, 1963 8. Benedict FG, Cathcart EP: Muscular work-a metabolic study with special reference to the efficiency of the human body as a machine. Washington DC, Carnegie Mellon Institute of Research, 1913, No. 187 9. Dallosso H, James WPT: Dietary thermogenesis and exercise. Proc Nutr Sot 41:35A, 1982 10. Miller DS, Mumford P, Stock MJ: Gluttory 2. Thermogenesis in overeating man. Am J Clin Nutr 20:1223-1229, 1967 11. Knuttgen HG: Oxygen debt after submaximal physical exercise. J App! Physio! 29:651-657, 1970 12. Taylor HL, Buskirk E, Henschel A: Maxima! oxygen intake as an objective measure of cardiorespiratory performance. J App! Physio! 8:73-80, 1955 13. Scholander PF: Analyzer for accurate estimation of respiratory gases in one half cubicmeter samples. I Biol Chem 167:235249, 1947
14. Lowry OH, Passonneau JV: A Flexible System of Enzymatic Analysis. Orlando, Fla, Academic, 1972 15. Fdlling I, Norman N: Hyperglycemia, hypoglycemic attacks and production of antiinsulin antibodies without previous known immunization. Diabetes 21:8 14-826, 1972 16. Opstad PK, Aakvaag A, Rognum T: Altered hormonal response to short-term bicycle exercise in young men after prolonged physical strain, caloric deficit, and sleep deprivation. Eur J Applied Physiol45:5 l-62, 1980 17. Newsholme EA. Leech AR: Biochemistry for the Medical Sciences, pp. 336-342. Wiley, Chichester, UK, 1983 18. Maehlum S, Felig P, Wahren J: Splanchnic glucose and muscle glycogen metabolism after glucose feeding during postexercise recovery. Am J Physiol235:E255-E260, 1978 19. Newsholme EA: Substrate cycles: Their metabolic, energetic and thermic consequences in man. B&hem Sot Symp 43: 183-205, 1978 20. Newsholme EA: A possible metabolic basis for the control of body weight. N Eng! J Med 302:40&405,1980 21. Brooks BJ, Arch JRS, Newsholme EA: Effect of some hormones on the rate of the triag!ycero!/fatty-acid substrate cycle in adipose tissue of the mouse in vivo. Biosc Rep 3:263-267, 1983 22. Steinberg D: Fatty acid mobilization-mechanisms of regulation and metabolic consequences. Biochem Sot Symp 24: 11I-144, 1963 23. Challiss RAJ, Arch JRS, Newsholme EA: The rate of substrate cycling between fructose 6-phosphate and fructose 1.6biphosphate in skeletal muscle. Biochem J 221: 153-l 6 1, 1984 24. KIrki NT: The urinary excretion of noradrenaline and adrenaline in different age groups, its diurnal variation, and the effect of muscular work on it. Acta Physiol Stand 39, 1956 (supp! 132) 25. Maron MB, Horvath SM, Wilkerson JE: Blood biochemical alterations during a recovery from competitive marathon running. Eur J Applied Physiol 36:231-238, 1977