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O2 kinetics in
heavy exercise revisited
The following is the abstract of the article discussed in the subsequent letter:
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ABSTRACT |
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Tordi, N., S. Perrey, A. Harvey, and R. L. Hughson. Oxygen uptake kinetics during two bouts of heavy cycling separated by
fatiguing sprint exercise in humans. J Appl Physiol 94: 533-541, 2003. First published October 11, 2002;
10.1152/japplphysiol.00532.2002.
We tested the hypothesis that
O2 uptake (
O2) kinetics
at the onset of heavy exercise would be altered in a state of muscle
fatigue and prior metabolic acidosis. Eight well-trained cyclists
completed two identical bouts of 6-min cycling exercise at >85% of
peak O2 separated by three
successive bouts of 30 s of sprint cycling. Not only was baseline
O2 elevated after prior sprint
exercises but also the time constant of phase II
O2 kinetics was faster (28.9 ± 2.4 vs. 22.2 ± 1.7 s; P < 0.05).
CO2 output (CO2) was significantly reduced throughout the second exercise bout. Subsequently O2 was greater at 3 min and
increased less after this after prior sprint exercise. Cardiac output,
estimated by impedance cardiography, was significantly higher in the
first 2 min of the second heavy exercise bout. Normalized integrated
surface electromyography of four leg muscles and normalized mean power
frequency were not different between exercise bouts.
O2 and
CO2 kinetic responses to heavy
exercise were markedly altered by prior multiple sprint exercises.
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LETTER |
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To the Editor: We read with interest the recent paper
of Tordi et al. (12) in which it was reported that prior
high-intensity cycle exercise caused a speeding of the phase II
O2 uptake (O2) kinetics
in a subsequent bout of heavy-intensity cycle exercise. These results
are important because the effect of prior exercise on
O2 kinetics provides important clues
about the control of muscle energetics at exercise onset. However, we
believe that there are a number of significant problems with the data
and their interpretation in the paper (12) that should be
bought to readers' attention.
In discussing their results, Tordi et al. (12) state that
it is important to "optimize" the experimental conditions if the phase II time constant is to be altered. It is then argued that the
large number of previous studies (2-7, 9, 11) that
did not detect a change in the phase II kinetics failed to do so
because 1) the prior exercise did not result in a
sufficiently marked acidosis, 2) the curve fitting in these
studies was not sensitive enough to detect a change in the phase II
time constant, 3) the studies lacked statistical power, and
4) differences in baseline O2 obscured the results. None of
these arguments stands up to scrutiny. First, to support the contention
that the acidosis imposed by previous studies was insufficient, Tordi
et al. should have included a condition in their study whereby a modest
degree of lactacidosis did not speed the phase II
O2 kinetics. They should have also
measured blood lactate concentration and/or pH to demonstrate that
their protocol resulted in a greater lactic acidosis in comparison to
that resulting from a single sprint (5). Thus their
conclusion that "the acidosis probably contributed to enhanced
vasodilatation early in exercise" is made without measuring lactate,
pH, or vasodilatation. Our laboratory (3-6) has
demonstrated no change in the phase II
O2 time constant when baseline whole
blood lactate concentration (not plasma lactate concentration, as
incorrectly stated in Ref. 12) was elevated by up to 7.6 mM and despite indirect evidence that vasodilatation in the exercising
muscle was enhanced (3). Second, performing only one test
for the acquisition of breath-by-breath data, as Tordi et al. did, is
unlikely to provide sufficient confidence in the parameters derived
from curve-fitting procedures (8). Thus Tordi et al. have
no grounds to question the curve-fitting procedures used in previous
studies in which subjects performed two to four transitions
(2-6, 9, 11), since these studies used methods that
were more sensitive than their own. Third, the charge that previous
studies lacked statistical power is also incorrect because the sample
sizes involved previously were equal or superior to those of Tordi et
al. Fourth, the primary time constant is unchanged as a result of prior
heavy exercise irrespective of whether there are differences in
baseline O2 (2, 4, 6, 9,
11).
We are also concerned that Tordi et al. (12) make
inappropriate interpretations from previously reported data in order to support their position that an O2 delivery limitation
exists at the onset of heavy exercise. For example, the authors use the data of Krustrup et al. (10) to show that blood flow (and
O2 availability) is increased at the onset of a second
high-intensity exercise bout and argue that this is responsible for the
higher O2 observed in the early
phase of exercise. However, Krustrup et al. come to the opposite
conclusion based on evidence that muscle O2 delivery was
far in excess of muscle O2
throughout the transient phase of high-intensity exercise even when
prior exercise was not performed (1, 10), indicating that
O2 availability did not limit muscle
O2 during the on transient.
We would also point out an inconsistency between the data presented by
Tordi et al. (12) in their Fig. 4 and the data presented in their Table 1. Figure 4 demonstrates an increased phase II O2 amplitude with no obvious change
in the rate of adaptation, as has been shown previously
(2-7). Therefore, the response profile that they
present does not support their interpretation (based on the data in
their Table 1) that phase II O2
kinetics are speeded. These inconsistencies highlight the limited
sensitivity of the methods and analyses employed in the paper.
In summary, the paper of Tordi et al. (12) is at odds with
the large body of work that demonstrates that prior high-intensity (including sprint) exercise does not speed the phase II
O2 kinetics during subsequent heavy
or severe upright cycle exercise (2-7, 9, 11). We
believe that this difference is related to significant methodological
shortcomings in their study, as well as to marked differences in data interpretation.
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REFERENCES |
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Bangsbo, J,
Krustrup P,
Gonzalez-Alonso J,
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ATP production and efficiency of human skeletal muscle during intense exercise: effect of previous exercise.
Am J Physiol Endocrinol Metab
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Bearden, SE,
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O2 and heart rate kinetics in cycling: transitions from an elevated baseline.
J Appl Physiol
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Burnley, M,
Doust JH,
Ball D,
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Effects of prior heavy exercise on O2 kinetics during heavy exercise are related to changes in muscle activity.
J Appl Physiol
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Burnley, M,
Doust JH,
Carter HH,
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Jones AM.
Effects of prior exercise and recovery duration on oxygen uptake kinetics during heavy exercise in humans.
Exp Physiol
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Burnley, M,
Doust JH,
and
Jones AM.
Effects of prior heavy exercise, prior sprint exercise and passive warming on oxygen uptake kinetics during heavy exercise in humans.
Eur J Appl Physiol
87:
424-432,
2002[ISI][Medline].
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Burnley, M,
Jones AM,
Carter H,
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Doust JH.
Effects of prior heavy exercise on phase II pulmonary oxygen uptake kinetics during heavy exercise.
J Appl Physiol
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Fukuba, Y,
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O2 kinetics in heavy exercise is not altered by prior exercise with a different muscle group.
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Gerbino, A,
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The effect of prior high-intensity cycling exercise on the O2 kinetics during high-intensity cycling exercise is situated at the additional slow component.
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Krustrup, P,
Gonzalez-Alonso J,
Quistorff B,
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Bangsbo J.
Muscle heat production and anaerobic energy turnover during repeated intense dynamic exercise in humans.
J Physiol
536:
947-956,
2001
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Scheuermann, BW,
Hoelting BD,
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The slow component of O2 is not accompanied by changes in EMG during repeated bouts of heavy exercise.
J Physiol
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12.
Tordi, N,
Perrey S,
Harvey A,
and
Hughson RL.
Oxygen uptake kinetics during two bouts of heavy cycling separated by fatiguing sprint exercise in humans.
J Appl Physiol
94:
533-541,
2003
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Mark Burnley Department of Sport and Exercise Science University of Wales Aberystwyth SY23 3DA, United Kingdom E-mail: mhb{at}aber.ac.uk | ||||||||||||
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Andrew M. Jones Department of Exercise and Sports Science Manchester Metropolitan University Alsager ST7 2HL, United Kingdom E-mail: a.m.jones{at}mmu.ac.uk |
To the Editor: Burnley and Jones have asked us to
believe that a mechanism exists so "that muscle O2
delivery was far in excess of muscle
In their first point, Burnley and Jones failed to recognize that we
referenced prior work showing that three repetitions of sprint exercise
would cause a more marked and sustained metabolic acidosis (13, 16)
than the single sprint employed by Burnley et al. (3). They did not
appreciate that an enhanced, sustained acidosis would facilitate
vasodilation at the onset of exercise as well as enhance O2
off-loading from the hemoglobin to exercising tissues (10, 12). The
second and third points of Burnley and Jones reveal a misrepresentation
of statistics and statistical confidence. The signal-to-noise ratio
determines the confidence for curve-fitting parameters [note the high
signal-to-noise ratio in Fig. 4 and the clear separation of means and
95% confidence intervals for Returning to the notion that "O2 delivery was far in
excess of muscle Previously (9, 18), we and our colleagues described the elegant work of
Wilson and Rumsey (20) and Arthur et al. (1), who demonstrated the
O2 dependence of muscle metabolism. For any given ATP flux
rate, the intracellular redox and phosphorylation potentials must
change if mitochondrial PO2 is less than ~20
Torr. Clearly, from the work of Richardson et al. (14) showing that intracellular PO2 is
REPLY
O2 throughout the transient phase of
high intensity exercise." They suggest also that, despite over 20 years of experience collecting and analyzing breath-by-breath
O2 (7), "there are a number of
significant problems with the data" from our laboratory. We will
first deal with the erroneous and selective referencing by Burnley and
Jones, and then we will attempt once again to explain why the system
properties that we observed are consistent with known human physiology
and basic concepts of control theory.
O2 in
Fig. 5 of Tordi et al. (17)]. In contrast to Burnley and Jones'
visual misanalysis of our data, the phase II time constants were 20.6 and 16.4 s for pre- and postexercise, respectively. Furthermore,
statistical power is not determined by sample size alone, as suggested
by Burnley and Jones, but also by differences between mean values and
standard deviation of differences between the means (SAS System for
Windows, release 8.01). The fourth point by Burnley and Jones that
"the primary time constant is unchanged" simply is not true as our
data, as well as the recent results of Rossiter et al. (15), have
clearly shown a faster phase II time constant after prior heavy exercise.
O2," it is
important for Burnley and Jones to understand what is meant by
"transient phase of high intensity exercise." Grassi et al. (4)
referred to the "early phase of the transient," in which during the
first ~15 s O2 extraction was not increased. Also, the
data of Bangsbo et al. (2) showed that O2 delivery minus
O2 increased only during the first
~15 s. As our laboratory has previously indicated (9, 18), the excess
delivery of O2 within the first 15 s of exercise is to
be expected because the muscle pump "indiscriminately" increases
flow throughout the muscle and because substrates for oxidative
metabolism increase (5). The main point here is that the first 15 s does not constitute the entire transient phase as implied by Burnley
and Jones; another approximately five times the time constant (at least
100 s) occurs before the transient phase is complete.
O2 delivery is dependent on appropriate vasodilation to
match blood flow to the sites of metabolic demand. Although some
feedforward-type controls for muscle blood flow such as muscle pump and
flow-mediated dilation do exist, "the prevailing view is that
skeletal muscle functional hyperemia ... [is] mediated primarily
by local control mechanisms" and that "oxygen delivery to the
tissues, not blood flow per se, is the controlled variable producing
exercise hyperemia" (11), although myogenic, endothelial, and
baroreflex factors can also influence blood flow. Studies that have
measured O2 extraction across exercising muscle show that
this variable reaches an upper limit relatively early (40-60 s)
and that further increases in muscle
O2 are related to further increases
in blood flow (2, 8, 10, 19).
5 Torr across a wide
range of work rates and from the more recent work from members of the
same team (6) that demonstrated dependence of phosphocreatine kinetics
on blood PO2 during recovery, the intracellular
environment is in this dependent region. That is, both O2
delivery and O2 utilization must adapt during the transient
phase of exercise to attain the appropriate ATP flux rates (18). This
precludes simple one-component kinetics even during the so-called
primary phase (phase II) and points strongly to O2 delivery
being one of the key factors determining O2 kinetics. Thus, in
"optimizing" the conditions of our experiment by achieving a high,
sustained level of metabolic acidosis, we enhanced O2
delivery so that we were able to detect a statistically significant
acceleration of the phase II time constant where previous experiments
did not (3). These data and conclusions are consistent with the notion
that, like other exquisite feedback control systems in the human body,
the delivery of O2 to muscle during heavy exercise is also
regulated by feedback control of skeletal muscle blood flow.
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FOOTNOTES |
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10.1152/japplphysiol.00045.2003
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REFERENCES |
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Effects of prior heavy exercise, prior sprint exercise and passive warming on oxygen uptake kinetics during heavy exercise in humans.
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2002[ISI][Medline].
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Muscle heat production and anaerobic energy turnover during repeated intense dynamic exercise in humans.
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2001
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Oxygen uptake kinetics during two bouts of heavy cycling separated by fatiguing sprint exercise in humans.
J Appl Physiol
94:
533-541,
2003.
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Richard L. Hughson Department of Kinesiology University of Waterloo Waterloo, Ontario, Canada N2L 3G1 E-mail: hughson{at}uwaterloo.ca | ||||||||||||
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Nicolas Tordi Laboratoire des Sciences du Sport 25030 Besançon Cedex, France | ||||||||||||
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Stephane Perrey UPRES-EA 2991, Faculté des Sciences du Sport 34090 Montpellier, France |
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