| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Copenhagen Muscle Research Centre, The August Krogh Institute, University of Copenhagen, DK-2100 Copenhagen, Denmark
 |
ABSTRACT |
|---|
 TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The aim of the present
study was to examine whether ATP production increases and mechanical
efficiency decreases during intense exercise and to evaluate how
previous exercise affects ATP turnover during intense exercise. Six
subjects performed two (EX1 and EX2) 3-min one-legged knee-extensor
exercise bouts [66.2 ± 3.9 and 66.1 ± 3.9 (±SE) W]
separated by a 6-min rest period. Anaerobic ATP production, estimated
from net changes in and release of metabolites from the active muscle,
was 3.5 ± 1.2, 2.4 ± 0.6, and 1.4 ± 0.2 mmol
ATP · kg dry wt
1 · s1
during the first 5, next 10, and remaining 165 s of EX1,
respectively. The corresponding aerobic ATP production, determined from
muscle oxygen uptake, was 0.7 ± 0.1, 1.4 ± 0.2, and
4.7 ± 0.4 mmol ATP · kg dry
wt1 · s1, respectively. The mean
rate of ATP production during the first 5 s and next 10 s was
lower (P < 0.05) than during the rest of the exercise
(4.2 ± 1.2 and 3.8 ± 0.7 vs. 6.1 ± 0.3 mmol
ATP · kg dry wt1 · s1).
Thus mechanical efficiency, expressed as work per ATP produced, was
lowered (P < 0.05) in the last phase of exercise
(39.6 ± 6.1 and 40.7 ± 5.8 vs. 25.0 ± 1.3 J/mmol
ATP). The anaerobic ATP production was lower (P < 0.05) in EX2 than in EX1, but the aerobic ATP turnover was higher
(P < 0.05) in EX2 than in EX1, resulting in the same muscle ATP production in EX1 and EX2. The present data suggest that the
rate of ATP turnover increases during intense exercise at a constant
work rate. Thus mechanical efficiency declines as intense exercise is
continued. Furthermore, when intense exercise is repeated, there is a
shift toward greater aerobic energy contribution, but the total ATP
turnover is not significantly altered.
blood flow; aerobic exercise; anaerobic ATP production; lactate; creatine phosphate
| |
INTRODUCTION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
MUCH KNOWLEDGE
EXISTS about energy production during submaximal exercise, i.e.,
a work intensity lower than that eliciting maximum oxygen uptake
(
O2 max) (36).
Less information has been obtained about ATP turnover and mechanical
efficiency during supramaximal exercise. This may be due to the
difficulties in quantifying the anaerobic energy production and
determining oxygen utilization of the exercising muscles during this
type of exercise.
To estimate the anaerobic energy production, muscle biopsies have been obtained before and after intense dynamic exercise. On the basis of the decrease in muscle ATP and creatine phosphate (CP), as well as accumulation of metabolites like pyruvate and lactate, the anaerobic energy production of the biopsied muscle has been estimated in several studies that employ cycle exercise (13, 35, 37). It is, however, difficult from measurements on muscle biopsy material to determine the anaerobic energy turnover during whole body exercise such as cycling, because the mass and the activity of the muscles involved are unknown. Furthermore, the metabolic response of the biopsied muscle may not be representative of all of the muscles included in the exercise. Another problem is that the release of metabolites into the blood from the exercising muscles is often not taken into account when energy turnover is calculated, although this may represent a substantial contribution to the total energy production when the exercise lasts more than a few seconds (4).
In a few studies, the aerobic contribution to the energy turnover of
the exercising muscles during intense and maximal cycle exercise has
been determined through measurements of the pulmonary oxygen
uptake (O2) (35,
37). However, such estimations require that the mass of the
active muscles be known. Furthermore, it is assumed that the pulmonary
O2 represents the
O2 of the exercising muscle, but this
assumption is not valid in the initial phase of intense exercise, as
there is a time delay in the transport of blood from the exercising
muscle to the lungs (9). The problems in determining the
aerobic and anaerobic ATP and energy yield are minimized by using a
knee-extensor exercise model in which the exercise is confined to the
quadriceps muscle, allowing a rather precise determination of the mass
of the active muscle (3, 4). Furthermore, by insertion of
catheters in the femoral blood vessels, arterial as well as venous
blood draining the exercising muscle can be collected, and blood flow
to the exercising muscle can be measured. The model has been used to
quantify the aerobic and anaerobic energy contribution during an
intense exercise bout (6). However, little information
exists about the muscle metabolic changes and
O2 at the onset of exercise. In a recent
study it was observed that heat production increased during intense
knee-extensor exercise (24), which in part may be related
to differences in the efficiency of the metabolic reactions involved in
the exercise (46). However, it is not clear to what extent
the various metabolic pathways are contributing to ATP turnover
throughout the exercise and whether part of the increase in heat
production is due to an increase in the rate of ATP production during
intense exercise.
Various studies have focused on energy turnover during repeated maximal
exercise, and it has been suggested that the energy turnover per work
unit is lowered when intense exercise is repeated (22,
41). However, in these studies the aerobic energy turnover was
not determined, and the work produced decreased when the exercise was
repeated, which makes it difficult to relate the metabolic changes to
the development of force. In studies using repeated knee-extensor
exercise with a constant exercise intensity, it has been observed that,
when a second exercise bout was performed after both a 2.5-min and a
60-min rest period, the anaerobic energy production per work unit was
significantly reduced without a change in leg
O2 (7, 8). However, in
these studies, the muscle O2 in the
initial phase of exercise could not be determined accurately because of
the limited number of measurements.
Thus the aim of the present study was to examine whether ATP turnover increases and mechanical efficiency decreases during supramaximal concentric exercise and to evaluate whether previous exercise altered the ATP production and mechanical efficiency. Subjects performed a 3-min intense knee-extensor exercise bout at a supramaximal work rate, which was repeated after a 6-min rest period. Arterial and femoral venous blood samples were collected, and leg blood flow was measured frequently during the exercise. In addition, a muscle biopsy was taken before and immediately after the exercise and on a separate occasion also twice in the initial phase of exercise.
| |
SUBJECTS AND METHODS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Subjects
Six healthy male subjects ranging in age from 21 to 24 yr, with an average height of 178 (range: 172-183) cm and an average body mass of 72.5 (67.9-78.3) kg, participated in the experiment. The subjects were fully informed of any risks and discomforts associated with the experiments before giving their informed consent to participate. The study was approved by the Frederiksberg, Copenhagen Ethics Committee.Methods
During the experiment, subjects performed one-legged knee-extensor exercise in the supine position on an ergometer that permitted the exercise to be confined to the quadriceps muscle (2). Before the experiment, the subjects had practiced the exercise on more than three separate occasions.The subjects had a light breakfast ~3 h before an experiment, and they reported to the laboratory ~2 h before the experiment. With the subject in the supine position, a catheter was placed in a femoral artery under local anesthesia. The tip was positioned 1-2 cm proximal to the inguinal ligament. A catheter was also placed in the femoral vein of the experimental leg ~1-2 cm distal to the inguinal ligament. A thermistor for measurement of venous blood temperature was inserted through the catheter and was advanced 8-10 cm proximal to the tip.
After ~1 h of rest, the subject performed two 3-min knee-extensor
exercise bouts (EX1 and EX2) with the experimental leg [66.2 ± 3.9 and 66.1 ± 3.9 (±SE) W; kicking frequency: 60.7 ± 0.2 and 60.6 ± 0.2 kicks/min] separated by a 6-min rest
period (Fig. 1). Before each of the
exercise bouts, the leg was passively moved for 5 s to accelerate
the flywheel to obtain a constant power output from onset of exercise.
After 60 min of rest, the entire exercise protocol was repeated with
the same leg to allow for early measurements of thigh blood flow (EX3
and EX4).
|
Blood was drawn from the femoral artery ~10 and 5 s before as well as 2, 5, 10, 15, 30, 45, 60, 90, 115, 150, and 170 s during EX1 and EX2. Femoral venous blood was collected ~15 and 5 s before as well as 2, 6, 9, 14, 29, 59, 89, 113, 145, and 167 s during EX1 and EX2. Femoral venous blood flow was measured by the thermodilution technique (3) approximately every 30 s after ~1 min of EX1 and EX2, as well as 3 s before and 3, 7, 29, 34, 61, 66, 92, and 162 s during EX3 and EX4 performed after 1 h of rest.
Values of blood flow obtained at the same time during the first two exercise bouts (EX1 and EX2) agreed with the corresponding values of the two bouts after 60 min of rest (EX3 and EX4) [100 s: 4.83 ± 0.46 (EX1) vs. 5.13 ± 0.44 (EX3) l/min; 150 s: 5.63 ± 0.70 (EX1) vs. 5.39 ± 0.58 l/min (EX3); 100 s: 5.19 ± 0.64 (EX2) vs. 5.38 ± 0.59 (EX4) l/min; 150 s: 5.51 ± 0.63 (EX2) vs. 5.71 ± 0.61 (EX4) l/min]. Thus blood flow values after the 60-min rest period were used in the calculations. An occlusion cuff placed just below the knee was inflated (220 mmHg) during the exercises to avoid contribution of blood from the lower leg. Before and immediately after each of the exercise bouts, a biopsy was obtained from the m. vastus lateralis. On a separate occasion, the subjects performed the same knee-extensor exercise as in the main experiment for 5 and 15 s, i.e., 5 and 15 kicks, separated by a 45-min rest period, and a muscle biopsy was obtained at rest and after each of the exercise bouts.
Blood analysis.
Oxygen saturation of blood and hemoglobin concentration were determined
spectrophotometrically (Radiometer OSM-3 hemoximeter). The hemoximeter
was calibrated spectrophotometrically by the cyanomethemoglobin method
(18). Hematocrit (Hct) determinations were made in
triplicate by use of microcentrifugation. A part of the blood sample
(100 µl) was hemolyzed within 10 s of sampling by a 1:1 dilution
with a buffer solution (Yellow Spring Instruments, Yellow Springs, OH)
to which were added 20 g/l Triton X-100 for analysis of lactate with a
lactate analyzer (model 23, Yellow Spring Instruments) (21). Another part of the blood sample was immediately
placed in ice-cold water and centrifuged rapidly for 30 s. Then
the plasma was collected and stored at 
80°C until analyzed for
pyruvate using a fluorometric assay (34).
Muscle sampling and analysis.
Muscle biopsies were immediately frozen in liquid N2 and
stored at 80°C. The frozen muscle samples were weighed before and after freeze-drying to determine water content. The freeze-dried sample
was dissected free of blood and connective tissue and extracted in a
solution of 0.6 M perchloric acid (PCA) and 1 mM EDTA, neutralized to
pH 7.0 with 2.2 M KHCO3, and stored at 80°C until
analyzed for CP and lactate by fluorometric assays (34).
Muscle mass. The mass of quadriceps femoris muscles was estimated by use of magnetic resonance imaging. Briefly, for each subject, 30-33 parallel axial T1-weighed images (sections) of the right thigh were obtained with a multi-slice spin-echo FLASH sequence (repetition time = 500 ms, echo time = 15 ms) by use of a body coil. Slice thickness was 3 mm, with a 12-mm interslice gap. Pixel size was 1.2 mm2. This setting was selected to optimize image quality to clearly separate muscle, bone, fat, and connective tissue. Image analysis was performed using NIH Image software. The mean knee-extensor mass of the experimental leg was 2.35 kg, with a range of 1.94-2.79 kg.
Calculations.
O2 and lactate and pyruvate release by
the thigh were calculated by multiplying the blood flow or, for
pyruvate, the plasma flow, by the difference between the femoral venous
and arterial (v-adiff) concentrations, with blood transit
time taken into account (see the next paragraph). A continuous blood
flow curve was constructed for each subject by linear connection of the
consecutive data points to obtain time-matched values of blood flow
with the blood variables.
O2 and
metabolite exchange rise progressively; therefore, it is essential to
know the blood transit time from the artery to the collection point of the venous blood samples to obtain comparable arterial and venous measurements. Therefore, to determine the transit time of the blood
from the femoral artery to the collecting site in the femoral vein,
four of the subjects carried out the experimental protocol on a
separate occasion. The experimental conditions, including positioning
of the catheters, were the same as in the main experiment. Before and
frequently during EX1 and EX2, 2 mg of indocyanine green (ICG,
Becton-Dickinson) in a concentration of 5 mg/ml were injected rapidly
into the femoral artery, immediately followed by a flush with isotonic
saline (5 ml). Blood was withdrawn from the femoral vein, and
densitometer output was sampled with a computer. The time from
injection to the time when the curve peaked, corrected by transit time
of the catheters (the dead space of the catheters divided by the pump
flow), was used as the mean transit time (MTT). MTT (n = 4) was 10.8 ± 0.5, 7.0 ± 0.5, 6.4 ± 0.4, and
6.4 ± 0.5 s after 5, 25, 65, 152 s of EX1,
respectively, and was 9.5 ± 0.7, 7.3 ± 0.5, 6.4 ± 0.3, and 6.1 ± 0.3 s, respectively, in EX2. To determine the blood transit time from the femoral artery to
the capillaries, ICG concentration was determined at
three positions of the quadriceps muscle with a NIRO300
(Hamamatsu Photonics) with dual-channel near infrared (NIR) laser
diodes. It was observed that this time accounted for about one-third of
the MTT at various time points during exercise. When this value and the
MTT for each individual were used, the average time that the collected
artery and venous blood represented capillary blood was
estimated. Average values were used for the two subjects for whom MTT
was not determined. All blood variables are presented in relation to
mean time at the capillary level.
Anaerobic ATP production of the quadriceps muscle for the time periods
0-5, 5-15, and 15-180 s was calculated as: 
ATP and CP + 3/2 muscle lactate + 3/2 (lactate and pyruvate
release) + others, where ATP represents the net utilization of
ATP, with the assumption that the change in ATP only occurred after
15 s of exercise (27). "Others" represent ATP
production related to accumulation of pyruvate assumed to be 1/30 of
accumulated muscle lactate (42), lactate uptake by
inactive tissues in the exercising leg (5), accumulation
of glycolytic intermediates (42), and accumulation and
release of alanine (31), in total amounting to 0.33, 0.33, and 0.06 mmol ATP/s during 0-5, 5-15, and 15-180 s,
respectively. It is assumed that net ATP utilization was the same in
EX2 as in EX1 (8), because ATP was not determined for EX2.
Muscle O2 was determined as measured net
thigh O2 plus estimated myoglobin (Mb)
oxygen desaturation. Oxygen utilization from Mb was assumed to be 3, 1.5, and 0 ml/kg wet wt for 0-5, 5-15, and 15-180 s,
respectively, on the basis of an assumption of a total Mb oxygen
content (MbO2) of 2 mmol/kg wet wt (26) and a
50% Mb desaturation occurring in the initial 15 s of intense exercise (40). Aerobic utilization expressed in
milliliters was converted to millimoles of ATP by use of a volume of
22.4 liters per mole of oxygen (STPD) and a
phosphorus-to-O2 ratio (P/O) of 2.5 (28). To
this value, the ATP production related to the glycolytic part of
carbohydrate oxidation was added. Mechanical efficiency was defined as
the ratio between work rate, including internal work corresponding to
17 W (19), and the rate of ATP turnover.
Statistics
Two-way ANOVA with repeated measures was used for evaluation of changes during the exercises as well as between EX1 and EX2. If a significant F value was observed, then the Newman-Keuls post hoc tests were used to locate the differences. A significance level of 0.05 was chosen. Standard error of the mean (±SE) is given in the text only when this value cannot be obtained from data in Figs. 1-7.
|
|
|
|
|
|
| |
RESULTS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Anaerobic Energy Production
Muscle CP of 79.8 ± 3.8 mmol/kg dry wt at rest decreased (P < 0.05) by 14 and 23% during the first 5 and 15 s, respectively, reaching 23.6 ± 11.3 mmol/kg dry wt at the end of EX1. The rate of CP degradation was higher (P < 0.05) during the first 5 and after 10 s than during the remaining 165 s (Fig. 2A). Muscle CP had returned to resting level before EX2, and it decreased to the same level as during EX1 (24.2 ± 2.3 mmol/kg dry wt). Muscle ATP decreased (P < 0.05) from 23.8 ± 0.6 to 20.7 ± 0.6 mmol/kg dry wt during EX1.Muscle lactate was 4.7 ± 0.7 mmol/kg dry wt at rest, and it
increased (P < 0.05) in the first 5 and 15 s of
EX1 to 9.2 ± 2.5 and 13.3 ± 4.1 mmol/kg dry wt,
respectively. At the end of EX1, muscle lactate was 84.1 ± 12.8 mmol/kg dry wt. The rate of muscle lactate accumulation was 0.9 ± 0.5 mmol · kg dry wt1 · s1
during the first 5 s, which was not significantly different from the remaining part of EX1 (Fig. 2B). Muscle lactate at the
end of EX2 (77.5 ± 8.0 mmol/kg dry wt) was the same as at the end of EX1, but it was higher (P < 0.05) before EX2
(27.1 ± 4.3 mmol/kg dry wt) than before EX1. Thus muscle lactate
accumulation was lower (P < 0.05) in EX2 than in EX1
(Fig. 2B).
Thigh blood flow was 1.71 ± 0.09 l/min immediately before EX1, and it increased rapidly during exercise, reaching 3.85 ± 0.35 l/min after 29 s and 5.39 ± 0.82 l/min at the end of exercise. Before EX2, thigh blood flow (3.13 ± 0.33 l/min) was higher (P < 0.05) than before EX1, and it remained higher (P < 0.05) until 165 s of exercise.
Estimated net release of lactate (blood flow × v-adiff lactate) was significant after 14 s (1.7 mmol/min), and it increased (P < 0.05) to 12.7 mmol/min during exercise (Fig. 3). The mean rate of lactate efflux was lower (P < 0.05) during the first 5 s and next 10 s than during the remaining 165 s of exercise (Fig. 2B). In EX2 the release of lactate was higher (P < 0.05) during the first 9 s compared with EX1, whereas after 60 s and toward the end of exercise, lactate release was higher (P < 0.05) in EX1 than in EX2 (Fig. 3). The total release of lactate during EX1 was higher (P < 0.05) than in EX2 (Fig. 2B).
The rate of lactate production by the quadriceps muscle, determined as the sum of the rates of lactate release and lactate accumulation, was not different in the various phases of exercise (Fig. 2B). The mean rate of lactate production was less (P < 0.05) during EX2 than during EX1 (Fig. 2B).
A significant (P < 0.05) net release of pyruvate was
observed after 14 s of EX1 (45 ± 13 µmol/min), and it
peaked after 59 s at 183 ± 35 µmol/min. The mean rate of
pyruvate release was lower (P < 0.05) during the first
5 s and after 10 s than during the rest of EX1 (6 ± 8 and 24 ± 10 vs. 141 ± 26 µmol/min). In EX2, a release
(P < 0.05) was observed before and during the first 6 s, but after 14 s and throughout the rest of exercise,
pyruvate release was less in EX2 than in EX1. The total release of
pyruvate was less (P < 0.05) in EX2 than in EX1
(0.39 ± 0.07 vs. 0.17 ± 0.05 mmol).
The rate of CP utilization during the first 5 s, next 10 s,
and remaining 165 s corresponded to rates of ATP production of 1.5 ± 0.6, 1.1 ± 0.4, and 0.2 ± 0.1 mmol
ATP · kg dry wt1 · s1,
respectively (Fig. 4). For the same time
periods, lactate production corresponded to rates of ATP production of
1.4 ± 0.7, 0.7 ± 0.3, and 1.0 ± 0.1 mmol
ATP · kg dry wt1 · s1,
respectively (Fig. 4). By adding ATP production associated with pyruvate release and other sources (see METHODS), the rate
of total anaerobic ATP production was estimated. It was higher
(P < 0.05) during 0-5 and 5-15 s than during
the rest of EX1 (Fig. 4). The mean rate of anaerobic ATP production was
less (P < 0.05) in EX2 than in EX1 (1.2 ± 0.1 vs. 1.6 ± 0.1 mmol ATP · kg dry wt1 · s1).
Aerobic Energy Production
ThighO2 increased
(P < 0.05) from 0.03 l/min immediately before EX1 to
0.13 l/min after 9 s, reaching 0.79 l/min at the end of EX1,
respectively (Fig. 5). The mean rate of
O2 during the first 5 s was less
(P < 0.05) than during the next 10 s, which was
smaller (P < 0.05) than during the remaining 165 s of exercise (0.10 ± 0.01 and 0.19 ± 0.03 vs. 0.63 ± 0.06 l/min), leading to corresponding differences in aerobic rate of
ATP production (Fig. 4). In EX2, thigh
O2 was higher (P < 0.05) than in EX1 during the first 119 s of exercise, whereafter
no differences were observed. The mean rates of
O2 and aerobic ATP production by the
thigh were higher (P < 0.05) in EX2 than in EX1
(0.69 ± 0.08 vs. 0.59 ± 0.06 l/min and 5.1 ± 0.5 vs.
4.4 ± 0.3 mmol ATP · kg dry
wt1 · s1).
ATP Production and Mechanical Efficiency
The mean rate of ATP production (determined as the sum of the rates of anaerobic and aerobic ATP production) was 4.2 ± 1.2 and 3.8 ± 0.7 mmol ATP · kg dry wt1 · s1 during the first 5 s
and next 10 s, which were lower (P < 0.05) than
during the remaining 165 s of EX1 (6.1 ± 0.3 mmol
ATP · kg dry wt1 · s1; Fig.
4). Because the external work was constant, mechanical efficiency,
expressed as work per ATP production, was significantly lower
(P < 0.05) from 15 to 180 s than from 0 to
15 s of EX1 (25.0 ± 1.3 vs. 39.3 ± 5.1 J/mmol ATP),
corresponding to a decrease in efficiency of 36 ± 9% (Fig.
6).
The mean rate of ATP production was the same in EX1 and EX2 (6.0 ± 0.4 vs. 6.3 ± 0.5 mmol ATP · kg dry
wt1 · s1), but a greater
(P < 0.05) fraction was provided from anaerobic sources during EX1 than during EX2 (27 ± 3 vs. 20 ± 1%;
Fig. 5). Thus the average work output per ATP production was not
different between EX1 and EX2 (Fig. 6).
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The present data show that the rate of ATP turnover increases during intense exercise performed at a constant work rate. Thus mechanical efficiency declines as intense exercise is continued. Furthermore, when intense exercise is repeated within some minutes, there is a shift toward greater aerobic energy contribution, but the total ATP production and mechanical efficiency are not significantly altered.
ATP Production During Intense Exercise
It was observed that ATP utilization during a constant load exercise was ~55% higher during the last phase of exercise compared with the first 15 s, which resulted in a decrease in the mechanical efficiency from 39 to 25 J/mmol ATP. It should, however, be considered how reasonable the estimations of ATP turnover are. The most critical assumption in the calculations is the P/O, which on the basis of in vitro studies on rat liver mitochondria has been suggested to be 2.5 (28). It should be noted that, if the in vivo P/O had been as unrealistically low as 0.9, there would not have been a difference between the first 15 s of exercise and the remainder of exercise. Likewise, a fall in P/O from 2.5 at the start to 1.2 at the end of exercise would be required to make the work performed per ATP produced constant throughout the exercise. However, even though there are indications from in vitro studies that mitochondrial respiration can be partly uncoupled at an increased intercellular Ca2+ concentration (25), it is unlikely that P/O changes that much. This notion is supported by the observation that P/O determined in mitochondria isolated from a human muscle biopsy obtained immediately after intense exhaustive exercise was the same as at rest (U. F. Rasmussen, P. Krustrup, J. Bangsbo, and H. N. Rasmussen, unpublished observation). The contribution of oxygen released from Mb is also uncertain, but because the assumed 50% reduction in MbO2 used in the present study may be in the high range (43), the difference in ATP turnover between the first and later phases of exercise would be even greater if the MbO2 utilized was actually smaller. Together, these considerations suggest that it is reasonable to conclude that the ATP production per work unit is lower in the first period of exercise. It should also be noted that the value for the last phase of exercise is of the same magnitude as the value found in animal studies using isolated muscle [for examples, 13-24 J/mmol ATP (17); 27 J/mmol ATP (33)].The question is what causes the change in ATP production per work unit during concentric exercise. On the basis of in vitro studies on isolated muscles, it has been suggested that factors such as lowered pH, as well as elevated temperature and increased Pi levels, lower mechanical efficiency of contracting muscles through an increase in both Ca2+-ATPase and myosin-ATPase activity (12, 15, 16, 47).
In the present study, muscle lactate increased progressively during the
intense exercise, leading to an estimated decrease in pH from 7.1 to
~6.7 (29), which may have affected mechanical efficiency. In several human studies, it has been observed that O2 progressively increases when
submaximal exercise is continued, but only at intensities leading to a
significant accumulation of lactate in the blood (23), and
it has been suggested that lowered muscle pH elevates
O2 and thus decreases mechanical efficiency. However, the finding of the same ATP turnover during EX1
and EX2, even though muscle pH probably was lower in the initial phase
of EX2 (7), does indicate that any effect of lowered muscle pH is small. In accordance, in a previous study, the rate of ATP
turnover was found to be the same whether intense knee-extensor exercise was preceded without or with intense arm exercise, with the
latter condition leading to a further reduction of muscle pH
(10). However, in that study and during EX2 in the present study, muscle pH may only during a minor fraction of the exercise have
been lower than in EX1; therefore, it cannot be excluded that pH has an
effect on ATP turnover and mechanical efficiency during intense exercise.
In separate experiments, it was observed that the muscle temperature
increased from ~34.5 to 36.0°C during intense exercise at an
intensity similar to that used in the present study. It is possible
that the increase in temperature affected the mechanical efficiency,
because, among other effects, it has been shown in vitro to decrease
P/O (45), causing an increase in
O2 solely to maintain the rate of ATP
production. During submaximal cycle exercise at a frequency of 60 rpm,
it has been observed that O2 was higher
when muscle temperature was elevated by prior passive heating
(20). However, in that study the difference was only ~5%, suggesting that any effect of temperature was small, which is
supported by the fact that total ATP turnover and mechanical efficiency
were the same during EX1 and EX2 in the present study, although the
mean temperature was ~0.5°C higher in EX2 (data not shown). An
increase in ATP turnover during the exercise may also be related to a
lowering of molar free energy in ATP hydrolysis (G) caused by
increases in metabolites like ADP and Pi, as well as
lowering of pH and increasing temperature. It is, however, unclear
whether a lowering of G will change the work done per ATP split
(46).
An increase in the total muscle ATPase activity as exercise progressed may have been due to recruitment of more fibers or more ATP-consuming fibers, i.e., fibers that have a high ATP utilization per force produced. However, it is not established whether there is a difference in efficiency between the various fiber types during concentric contractions in vivo. In in vitro studies, with use of either isolated muscles or single muscle fibers, it is observed that the efficiency of the different fiber types is closely related to the velocity, pattern, and type of contraction (11, 12, 14, 17). At low contraction velocities, the efficiency of slow-twitch (ST) fibers is higher than for fast-twitch (FT) fibers, whereas it appears to be the opposite at high speeds (11). In the present study, the quadriceps muscle was contracting at an average speed of ~135°/s, corresponding to ~20% of maximal velocity (1), which has been suggested to be within the optimum speed of ST fibers and nonoptimal for FT fibers (11, 17). Thus the higher ATP utilization during the last phase of exercise may be explained by a greater recruitment of FT fibers. However, further studies are needed to examine fiber type recruitment and efficiency of the different fibers during intense exercise.
ATP Production During Repeated Intense Exercise
When the intense exercise was repeated, muscleO2 was elevated in the initial phase of
exercise, which was associated with a higher activation state of
pyruvate dehydrogenase (data not reported), but it is unclear whether
this caused the greater muscle respiration. On the other hand, in
accordance with a number of other studies (7, 8), muscle
lactate production was reduced during the second exercise bout. Thus
ATP production and mechanical efficiency were the same when intense
exercise was repeated. It cannot be excluded, however, that a
difference existed during the exercise. In an additional experiment, a
4-min exercise bout was performed twice, with bouts separated by 2 min
of rest. Biopsies were obtained before and after 20 s of each
exercise bout. It was observed that CP degradation during the first
20 s was the same for the first and second exercise bouts
(1.8 ± 0.2 and 1.7 ± 0.2 mmol · kg dry
wt1 · s1), whereas muscle lactate
accumulation was less (P < 0.05) in the second
exercise bout (1.0 ± 0.2 vs. 0.3 ± 0.3 mmol · kg
dry wt1 · s1). Combining these data
with those for O2 and lactate/pyruvate release in the present study, the rate of ATP production during the
first 20 s was the same during the two exercise bouts [4.2 (EX1)
vs. 4.0 (EX2) mmol · kg dry
wt1 · s1]. These findings suggest
that the rate of ATP turnover was the same in EX1 and EX2 in both the
initial and the later phases of exercise. In other studies when
repeated knee-extensor exercise was used, mechanical efficiency was
observed to be unaltered, as in the present study, when exercise was
repeated after a 2.5-min rest period but elevated when the rest period
was 60 min (7, 8). The latter observation may be explained
by the longer duration of the first exercise bout compared with the
second bout (3.7 vs. 3.0 min), because the present study suggests that
ATP turnover increases as exercise progresses, but it could also be
related to the longer rest period between the exercise bouts compared with the present study. It should be noted that studies using repeated
intense cycle exercise or isolated contracting muscles have suggested
that mechanical efficiency is higher when exercise is repeated with a
recovery period of <4 min (22, 41). However, in these
studies the metabolic response of the exercising muscles could not be
accurately determined and related to the work performed.
Energy Production During Intense Exercise
On the basis of net change in reactant levels of the metabolic reactions, it is possible to estimate the total energy production by use of average values of energy produced in each of the reactions determined in vitro. A molar enthalpy change (H) value of 55 kJ/mol
ATP for the net CP breakdown (43) and 67 kJ/mol ATP for glycolysis, with glycogen assumed as substrate (16), may
be used (the corresponding value for oxidative phosphorylation is 95 kJ/mol ATP for a P/O of 2.5). Muscle aerobic contribution can be
converted to energy production by use of a caloric value of 21.2 kJ/l
O2 (38), if we assume that only pyruvate was
oxidized. This assumption seems reasonable, because no glucose uptake
was observed (data not reported), and fat oxidation during this type of
exercise appears to be negligible (7). The mean rate of energy production can then be estimated to be 149 ± 29 and
275 ± 23 J/s during the first 15 and the remaining 165 s of
exercise, respectively, corresponding to an increase (P < 0.05) in the energy production per work unit of ~85%. These
values correspond to a decrease (P < 0.05) in
mechanical efficiency, expressed as the ratio of work rate to the rate
of energy production, from 57.9 ± 6.6% in the first 15 s to
an average of 30.8 ± 1.6% during the remainder of the intense
exercise. The observation that the rate of energy turnover is smaller
in the initial phase of concentric exercise is in agreement with
findings in another knee-extensor exercise study in which the rate of
muscle energy turnover was estimated from heat production and power
output (24). The rate of heat production during intense
dynamic knee-extensor exercise doubled over 3 min of intense exercise,
with one-half of the increase occurring in the first 40 s of
exercise. The mean rate of energy turnover was 164 ± 12 J/s, and
mechanical efficiency was 50.2 ± 5.8% during the first 15 s, which is similar to the values obtained in the present study (Fig.
7). During the remaining 165 s, the mean rate of energy turnover was somewhat lower and the mechanical efficiency higher than in the present study (Fig. 7). Nevertheless, with two independent methods, it has been demonstrated that energy turnover increases, and thus mechanical efficiency decreases, during
intense exercise.
Since Krogh and Lindhard (32) in the early part of the
last century determined the oxygen deficit as the difference between energy demand and O2, oxygen deficit has
been frequently used as a measure of the anaerobic energy production
(30, 35). The calculations have been based on the
assumptions that the relation between energy turnover and power output
is linear from moderate submaximal to supramaximal exercise, i.e., a
work output higher than the intensity eliciting
O2 max, and that the energy turnover is
constant during intense exercise. The first assumption has been
questioned (4), and the present study demonstrates that
the latter assumption is not valid. Apparently, in the initial phase of
intense exercise, the mechanical efficiency of the exercising muscle is
higher than during steady-state submaximal exercise, whereas as the
intense exercise progresses, it may be lower compared with submaximal
exercise. This means that the oxygen deficit determined in the
traditional way overestimates the anaerobic energy turnover if the
exercise time is short (<2 min). Thus, for exhaustive intense exercise, the magnitude of the true oxygen deficit depends on the
duration and intensity of the exercise. This can also explain the
observation of an agreement between the oxygen deficit and the
anaerobic energy production determined from muscle and blood metabolic
measurements for an exhaustive knee-extensor exercise bout lasting 3.2 min (6). It may be that the magnitude of overestimation of
the true anaerobic energy turnover by the oxygen deficit method in the
first phase of the exercise corresponded to the underestimation in the
last phase of exercise.
Summary
The present data show that ATP production increases and mechanical efficiency decreases during intense exercise at a constant intensity, which may in part be due to a change in fiber type recruitment, an elevated temperature, and a lowered pH. However, further studies are needed to clarify the cause of the increase in ATP production per work unit during intense exercise and its functional importance. When intense exercise is repeated, the total ATP turnover is not changed if the exercise duration is the same.| |
ACKNOWLEDGEMENTS |
|---|
We thank Merete Vannby, Ingelise Kring, and Winnie Tagerup for excellent technical assistance.
| |
FOOTNOTES |
|---|
This study was supported by a grant from The Danish National Research Foundation (504-14). In addition, support was obtained from Team Danmark and The Sports Research Council (Idrættens Forskningsråd).
Address for reprint requests and other correspondence: J. Bangsbo, The August Krogh Institute, LHF, Universitetsparken 13, DK-2100 Copenhagen Ø, Denmark (E-mail: jbangsbo{at}aki.ku.dk).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 20 June 2000; accepted in final form 23 January 2001.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Aagaard, P,
Trolle M,
Simonsen EB,
Klausen K,
and
Bangsbo J.
Moment and power generation during maximal knee extension performed at low and high speeds.
Eur J Appl Physiol Occup Physiol
69:
376-381,
1994[Medline].
2.
Andersen, P,
Adams RP,
Sjøgaard G,
Thorboe A,
and
Saltin B.
Dynamic knee extension as model for study of isolated exercising muscle in humans.
J Appl Physiol
59:
1647-1653,
1985
3.
Andersen, P,
and
Saltin B.
Maximal perfusion of skeletal muscle in man.
J Physiol (Lond)
366:
233-249,
1985
4.
Bangsbo, J.
Quantification of anaerobic energy production during intense exercise.
Med Sci Sports Exerc
30:
47-52,
1998[Web of Science][Medline].
5.
Bangsbo, J,
Aagaard T,
Olsen M,
Kiens B,
Turcotte LP,
and
Richter EA.
Lactate and H+ uptake in inactive muscles during intense exercise in man.
J Physiol (Lond)
422:
539-559,
1995
6.
Bangsbo, J,
Gollnick PD,
Graham TE,
Juel C,
Kiens B,
Mizuno M,
and
Saltin B.
Anaerobic energy production and O2 deficit-debt relationship during exhaustive exercise in humans.
J Physiol (Lond)
422:
539-559,
1990.
7.
Bangsbo, J,
Graham TE,
Johansen L,
Strange S,
Christensen C,
and
Saltin B.
Elevated muscle acidity and energy production during exhaustive exercise in man.
Am J Physiol Regulatory Integrative Comp Physiol
263:
R881-R899,
1992.
8.
Bangsbo, J,
Graham TE,
Kiens B,
and
Saltin B.
Elevated muscle glycogen and anaerobic energy production during exhaustive exercise in man.
J Physiol (Lond)
451:
205-227,
1992
9.
Bangsbo, J,
Krustrup P,
González-Alonso J,
Boushel R,
and
Saltin B.
Muscle oxygen kinetics at onset of intense dynamic exercise in humans.
Am J Physiol Regulatory Integrative Comp Physiol
279:
R899-R906,
2000
10.
Bangsbo, J,
Madsen K,
Kiens B,
and
Richter EA.
Effect of muscle acidity on muscle metabolism and fatigue during intense exercise in man.
J Physiol (Lond)
495:
587-596,
1996
11.
Barclay, CJ.
Mechanical efficiency and fatigue of fast and slow muscles of the mouse.
J Physiol (Lond)
497:
781-794,
1996
12.
Barclay, CJ,
Constable JK,
and
Gibbs CL.
Energetics of fast- and slow-twitch muscles of the mouse.
J Physiol (Lond)
472:
61-80,
1993
13.
Boobis, LH.
Metabolic aspects of fatigue during sprinting.
In: Exercise. Benefits, Limits, and Adaptations, edited by Macloed RJ,
Maughan R,
Nimmo M,
Reilly T,
and Williams TC.. London: Spon, 1987, p. 116-143.
14.
Bottinelli, R,
Pellegrino MA,
Canepari M,
Stienen GJM,
and
Reggiani C.
Single fibre studies of human muscle fibres; contractile and energetic properties.
J Physiol (Lond)
506P:
4S,
1998.
15.
Cooke, R,
Franks K,
Luciani GB,
and
Pate E.
The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate.
J Physiol (Lond)
395:
77-97,
1988
16.
Curtin, NA,
and
Woledge RC.
Energy changes and muscular contraction.
Physiol Rev
58:
690-761,
1978
17.
Di Prampero, PE,
Boutellier U,
and
Marguerat A.
Efficiency of work performance and contraction velocity in isotonic tetani of frog sartorius.
Pflügers Arch
412:
455-461,
1988[Web of Science][Medline].
18.
Drabkin, DL,
and
Austin JH.
Spectrophometric studies. II. Preparations from washed blood cells, nitric oxide hemoglobin and sulhemoglobin.
J Biol Chem
122:
51-56,
1935.
19.
Ferguson, RA,
Aagaard P,
Ball D,
Sargeant AJ,
and
Bangsbo J.
Total power output generated during dynamic knee extensor exercise at different contraction frequencies.
J Appl Physiol
89:
1912-1918,
2000
20.
Ferguson, RA,
Ball D,
and
Sargeant AJ.
Effect of muscle temperature on oxygen consumption and metabolic responses to whole body exercise in humans at different movement frequencies.
J Physiol (Lond)
511.P:
8P,
1999.
21.
Foxdal, P,
Bergqvist Y,
Eckerblom S,
and
Sandhagen B.
Improving lactate analysis with the YSI 2300 GL: hemolyzing blood samples makes results comparable with those for deproteinized whole blood.
Clin Chem
38:
2110-2114,
1992[Abstract].
22.
Gaitanos, GC,
Williams C,
Boobis LH,
and
Brooks S.
Human muscle metabolism during intermittent maximal exercise.
J Appl Physiol
75:
712-719,
1993
23.
Gerbino, G,
Ward S,
and
Whipp B.
Effects of prior exercise on pulmonary gas-exchange kinetics during high-intensity exercise in humans.
J Appl Physiol
80:
99-107,
1996
24.
González-Alonso, J,
Quistorff B,
Krustrup P,
Bangsbo J,
and
Saltin B.
Heat production in human skeletal muscle at the onset of intense dynamic exercise.
J Physiol
524:
603-615,
2000
25.
Halestrap, AP,
Griffiths EJ,
and
Connern CP.
Mitochondrial calcium handling and oxidative stress.
Biochem Soc Trans
21:
353-358,
1993[Web of Science][Medline].
26.
Harris, RC,
Hultman E,
Kaijser L,
and
Nordesjö LO.
The effect of circulatory occlusion on isometric exercise capacity and energy metabolism of the quadriceps muscle in man.
Scand J Clin Lab Invest
35:
87-95,
1975[Web of Science][Medline].
27.
Hellsten, Y,
Richter EA,
Kiens B,
and
Bangsbo J.
AMP deamination and purine exhange in human skeletal muscle during and after intense exercise.
J Physiol (Lond)
520:
909-919,
1999
28.
Hinkle, PC,
Kumar MA,
Resetar A,
and
Harris DL.
Mechanistic stoichiometry of mitochondrial oxidative phosphorylation.
Biochemistry
30:
3576-3582,
1991[Medline].
29.
Juel, C,
Bangsbo J,
Graham TE,
and
Saltin B.
Lactate and potassium fluxes from skeletal muscle during intense dynamic knee-extensor exercise in man.
Acta Physiol Scand
140:
147-159,
1990[Web of Science][Medline].
30.
Karlsson, J,
and
Saltin B.
Lactate, ATP, and CP in working muscle during exhaustive exercise in man.
J Appl Physiol
29:
598-602,
1970[Web of Science].
31.
Katz, A,
Broberg S,
Sahlin K,
and
Wahren J.
Muscle ammonia and amino acid metabolism.
Clin Physiol
6:
365-379,
1986[Web of Science][Medline].
32.
Krogh, A,
and
Lindhard J.
The changes in respiration at the transition from work to rest.
J Physiol (Lond)
53:
431-437,
1920.
33.
Kushmerick, MJ,
and
Davies RE.
The chemical energetics of muscle contraction. The chemistry, efficiency and power of maximally working sartorius muscle.
Proc R Soc Lond B Biol Sci
174:
315-353,
1969[Medline].
34.
Lowry, OH,
and
Passonneau JV.
A Flexible System of Enzymatic Analysis. New York: Academic, 1972.
35.
Medbø, JI,
and
Tabata I.
Anaerobic energy release in working muscle during 30 s and 3 min of exhausting bicycling.
J Appl Physiol
75:
1654-1660,
1993
36.
Morgan, W,
Martin PW,
and
Krahenbuhl GS.
Factors affecting running economy.
Sports Med
7:
310-330,
1989[Web of Science][Medline].
37.
Nevill, M,
Bogdanis GC,
Boobis LH,
Lakomy HKA,
and
Williams C.
Muscle metabolism and performance during sprinting.
In: Biochemistry of Exercise IX, edited by Maughan RJ,
and Shirreffs SM.. Champaign, IL: Human Kinetics, 1996, p. 243-259.
38.
Nicholls, DG,
and
Ferguson SJ.
Bioenergetics 2.
In: Textbook of Biochemistry. New York: Academic, 1992.
40.
Richardson, RS,
Noyszewski EA,
Kendrick KF,
Leigh JS,
and
Wagner PD.
Myoglobin O2 desaturation during exercise.
J Clin Invest
96:
1916-1926,
1995.
41.
Spriet, LL,
Lindinger MI,
McKelvie S,
Heigenhauser GJF,
and
Jones NL.
Muscle glycogenolysis and H+ concentration during maximal intermittent cycling.
J Appl Physiol
66:
8-13,
1989
42.
Spriet, LL,
Söderlund K,
Bergstrøm M,
and
Hultman E.
Anaerobic energy release in skeletal muscle during electrical stimulation in men.
J Appl Physiol
62:
611-615,
1987
43.
Tran, TK,
Sailasuta N,
Kreutzer U,
Hurd R,
Chung Y,
Mole P,
Kuno S,
and
Jue T.
Comparative analysis of NMR and NIRS measurements of intracellular PO2 in human skeletal muscle.
Am J Physiol Regulatory Integrative Comp Physiol
276:
R1682-R1690,
1999
44.
Walsh, TH,
and
Woledge RC.
Heat production and chemical change in tortoise muscle.
J Physiol (Lond)
206:
457-469,
1970
45.
Willis, WT,
and
Jackman MR.
Mitochondrial function during heavy exercise.
Med Sci Sports Exerc
26:
1347-1354,
1994[Web of Science][Medline].
46.
Woledge, RC,
Curtin NA,
and
Homsher E.
Energetic Aspects of Muscle Contraction. London: Academic, 1985.
47.
Wolosker, H,
Rocha JB,
Engelender S,
Panizzutti R,
De Miranda J,
and
Meis L.
Sarco/endoplasmic reticulum Ca2+-ATPase isoforms: diverse responses to acidosis.
Biochem J
321:
545-550,
1997.
This article has been cited by other articles:
|
|
 |
|
  B. J. Whipp Point: The kinetics of oxygen uptake during muscular exercise do manifest time-delayed phases J Appl Physiol, November 1, 2009; 107(5): 1663 - 1665. [Full Text] [PDF]
|
|
|
|
 |
|
 G. Layec, A.él. Bringard, Y. Le Fur, C. Vilmen, J.-P. Micallef, S.ép. Perrey, P. J. Cozzone, and D. Bendahan Effects of a prior high-intensity knee-extension exercise on muscle recruitment and energy cost: a combined local and global investigation in humans Exp Physiol, June 1, 2009; 94(6): 704 - 719. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Vanhatalo and A. M. Jones Influence of prior sprint exercise on the parameters of the \#8216;all-out critical power test' in men Exp Physiol, February 1, 2009; 94(2): 255 - 263. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. R. Light, R. W. Hughen, J. Zhang, J. Rainier, Z. Liu, and J. Lee Dorsal Root Ganglion Neurons Innervating Skeletal Muscle Respond to Physiological Combinations of Protons, ATP, and Lactate Mediated by ASIC, P2X, and TRPV1 J Neurophysiol, September 1, 2008; 100(3): 1184 - 1201. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Mourtzakis, T. E. Graham, J. Gonzalez-Alonso, and B. Saltin Glutamate availability is important in intramuscular amino acid metabolism and TCA cycle intermediates but does not affect peak oxidative metabolism J Appl Physiol, August 1, 2008; 105(2): 547 - 554. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Ferguson, B. J. Whipp, A. J. Cathcart, H. B. Rossiter, A. P. Turner, and S. A. Ward Effects of prior very-heavy intensity exercise on indices of aerobic function and high-intensity exercise tolerance J Appl Physiol, September 1, 2007; 103(3): 812 - 822. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Jones, N. J. A. Berger, D. P. Wilkerson, and C. L. Roberts Effects of "priming" exercise on pulmonary O2 uptake and muscle deoxygenation kinetics during heavy-intensity cycle exercise in the supine and upright positions J Appl Physiol, November 1, 2006; 101(5): 1432 - 1441. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. A. Ferguson, P. Krustrup, M. Kjaer, M. Mohr, D. Ball, and J. Bangsbo Effect of temperature on skeletal muscle energy turnover during dynamic knee-extensor exercise in humans J Appl Physiol, July 1, 2006; 101(1): 47 - 52. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. R. Gray, G. De Vito, M. A. Nimmo, D. Farina, and R. A. Ferguson Skeletal muscle ATP turnover and muscle fiber conduction velocity are elevated at higher muscle temperatures during maximal power output development in humans Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2006; 290(2): R376 - R382. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. D. Paterson, J. M. Kowalchuk, and D. H. Paterson Effects of prior heavy-intensity exercise during single-leg knee extension on vO2 kinetics and limb blood flow J Appl Physiol, October 1, 2005; 99(4): 1462 - 1470. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Stary and M. C. Hogan Intracellular pH during sequential, fatiguing contractile periods in isolated single Xenopus skeletal muscle fibers J Appl Physiol, July 1, 2005; 99(1): 308 - 312. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Sahlin, J. B. Sorensen, L. B. Gladden, H. B. Rossiter, and P. K. Pedersen Prior heavy exercise eliminates VO2 slow component and reduces efficiency during submaximal exercise in humans J. Physiol., May 1, 2005; 564(3): 765 - 773. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Koga, D. C. Poole, T. Shiojiri, N. Kondo, Y. Fukuba, A. Miura, and T. J. Barstow Comparison of oxygen uptake kinetics during knee extension and cycle exercise Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2005; 288(1): R212 - R220. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Mourtzakis, J. Gonzalez-Alonso, T. E. Graham, and B. Saltin Hemodynamics and O2 uptake during maximal knee extensor exercise in untrained and trained human quadriceps muscle: effects of hyperoxia J Appl Physiol, November 1, 2004; 97(5): 1796 - 1802. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. P. Wilkerson, K. Koppo, T. J. Barstow, and A. M. Jones Effect of prior multiple-sprint exercise on pulmonary O2 uptake kinetics following the onset of perimaximal exercise J Appl Physiol, October 1, 2004; 97(4): 1227 - 1236. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Krustrup, Y. Hellsten, and J. Bangsbo Intense interval training enhances human skeletal muscle oxygen uptake in the initial phase of dynamic exercise at high but not at low intensities J. Physiol., August 15, 2004; 559(1): 335 - 345. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Burnley, A. M. Jones, R. L. Hughson, N. Tordi, and S. Perrey Interpreting VO2 kinetics in heavy exercise revisited J Appl Physiol, June 1, 2003; 94(6): 2548 - 2550. [Full Text] [PDF]
|
|
|
|
|
|
P. Krustrup, R. A Ferguson, M. Kjaer, and J. Bangsbo ATP and heat production in human skeletal muscle during dynamic exercise: higher efficiency of anaerobic than aerobic ATP resynthesis J. Physiol., May 15, 2003; 549(1): 255 - 269. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Bangsbo, M. J. Gibala, P. Krustrup, J. Gonzalez-Alonso, and B. Saltin Enhanced pyruvate dehydrogenase activity does not affect muscle O2 uptake at onset of intense exercise in humans Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2002; 282(1): R273 - R280. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
) and
EX2 (
). Values are means ± SE. *Significantly
(P < 0.05) different from EX1.
