Page 1 of 13
Articles in PresS. J Appl Physiol (June 14, 2007). doi:10.1152/japplphysiol.00595.2007
Point: Counterpoint Stroke volume does/ does not decline during exercise at
maximal effort in healthy individuals.
Point: Stroke volume does decline during exercise at maximal effort in healthy individuals
José González-Alonso
Centre for Sports Medicine and Human Performance
Brunel University, Uxbridge
Middlesex UB8 3PH
United Kingdom
A wide-held theory explaining the physiological factors limiting maximal aerobic power
(VO2max) in humans postulates that the perfusion capacity of skeletal muscle greatly exceeds
the capacity of the heart to pump blood into the systemic circulation (1, 2, 20, 22, 27). This
theory implies that any human being would be able to recruit more motor units and produce more
work during maximal exercise if cardiac output (Q) did not reach such a hypothetical upper limit.
In this debate, I will argue that the decline in stroke volume (SV) underpinning the plateau or
drop in Q during incremental and constant maximal exercise supports the idea of a regulatory
limit of the heart. The approach is necessarily integrative to be able to support the contention that
SV does decline during exercise at maximal effort in healthy individuals. It is emphasized that
the question under debate is whether or not the SV value preceding fatigue (i.e., 10-30 s before
exhaustion) is lower than the values observed at submaximal intensities during incremental
exercise to exhaustion or during the initial stages of maximal constant-load exercise. It is
important to note, however, that due to methodological difficulties only a handful of studies in
the literature report measures of SV and Q in the few seconds before exhaustion. The common
observation that heart rate and systemic a-vO2 difference increase progressively during exercise
to maximum makes the behaviour of Q the central issue of the debate.
A number of observations made with a variety of experimental techniques provide evidence that
SV declines during maximal incremental exercise in humans a response that accompanies the
attenuation in the rate of rise, the plateau or the decline in Q (9, 10, 12, 14, 16, 18, 21, 25, 26, 28,
29). In the early 1980s, Keul et al. (16) provided the first echocardiographic data supporting that
SV falls during upright cycling to exhaustion. Using right heart catheterization, radionuclide
angiography and expired gas analysis, Higginbotham et al. (14) later showed a slight decline in
SV at peak exercise following the “classic” plateau response from 40-50% VO2max (3), which
was attributed to the effects of tachycardia on left ventricular filling. In the same year and using a
dye-dilution method for determining Q, Yamaguchi et al. (30) reported a decline in SV during
incremental supine cycling in 31 subjects showing an attenuation or levelling off in Q. Adding
inconsistency to their results, however, they reported a plateau in SV in 9 subjects displaying a
linear increase in Q and a conflicting levelling off in the calculated systemic a-vO2 difference
above 50% VO2max (30). In the 1990s, a number of independent research groups showed an 811% decline in SV at peak exercise using angiographic, acetylene rebreathing and
echocardiographic techniques (9, 25, 26). Recent experiments employing the Fick principle to
estimate Q expand on these early observations by showing a significant fall in SV during
Copyright © 2007 by the American Physiological Society.
Page 2 of 13
incremental exercise accompanying non-linear locomotor muscle blood flow and Q dynamics
leading to a plateau in exercising limb muscle VO2 (19, 28, 29). Of note is the strikingly similar
pattern of response in Stringer et al.’s (28, 29) and in our recent study during incremental
exercise to exhaustion (19). Both studies found a significant decline in SV at peak exercise
compared to at 50% VO2max, which accompanied the attenuation and subsequent plateau in Q
above 90% VO2max (19, 28, 29). Because the methods available to assess heart rate, a-vO2
difference and VO2 are more sensitive than the methods used to measure SV or Q, a concerted
examination of components of the Fick equation (VO2= Q x a-vO2 difference, where Q = SV x
heart rate) is warranted to ascertain the validity of the measured or estimated SV. In our study,
heart rate and VO2 increased in a linear fashion (r2=0.99; P< 0.001) in agreement with studies in
the literature. Interestingly, Stringer et al. (28, 29) showed that systemic a-vO2 differences
display a linear rather than a hyperbolic profile, thus indicating that Q as a function of VO2 must
be curvilinear and that SV must decline during incremental exercise to exhaustion. Indeed, direct
measures of blood oxygen content demonstrate that systemic and leg oxygen extraction increases
continuously until exhaustion, reaching values ranging from 80 to 95%, with the extraction
across the exercising legs being higher than across the systemic circulation (6, 10, 12, 23, 24).
The continuously increasing a-vO2 difference and the linear increase in heart rate during
incremental exhausting exercise suggest that the fall in SV may be more accentuated in
individuals showing a plateau in VO2max because Q must decline in that setting (4, 17).
Another approach to determine whether SV declines during exercise at maximal effort is to
examine the hemodynamic responses to short duration (3 to 10 min) constant-load exercise. An
advantage of this protocol is that it assesses the capacity of the body to sustain VO2max and the
capacity of the cardiovascular system to sustain maximal systemic and locomotor muscle blood
flow and O2 delivery. In 3 studies involving 29 subjects, we have consistently observed
significant reductions in SV and Q prior to exhaustion both in the presence and absence of heat
stress (10, 12, 19). These responses were associated with high core temperature, catecholamines
and plasma ATP, near-maximal heart rate, altered or stable central venous and mean arterial
pressures and reduced locomotor muscle blood flow. This suggests that the fall in SV might have
resulted from the interaction of several factors transiently depressing preload and/or left
ventricular function. The similar cardiovascular instability during exhausting incremental and
constant-load exercise points towards an upper limit in cardiovascular regulation, which might
implicate both central and peripheral factors (4-6, 10, 12, 19). Interestingly, the rate-pressure
product of heart rate and mean arterial pressure increases until exhaustion, indicating that
myocardial oxygen demand is rising when SV declines during constant and incremental maximal
exercise. Under these conditions, an increase in myocardial VO2 can only occur by an increase in
O2 delivery provided by augmented coronary blood flow because the O2 extraction reserve is
minimal. The blunted Q raises the possibility that impaired coronary circulation sets a limit to
cardiac function (19), an inference already advanced by Hill & Lupton 84 years ago (15).
The cardiovascular instability described here is not unique to maximal exercise. A similar drop
in SV occurs during prolonged submaximal exercise as part of the classical phenomenon termed
“cardiovascular drift”(7, 8) or the cardiovascular strain evoked by dehydration and hyperthermia,
which also features reductions in Q and exercising muscle blood flow (11, 13). In conclusion,
comprehensive studies measuring Q and other components of the Fick principle during both
incremental and constant load cycling support the position that SV does decline during exercise
Page 3 of 13
at maximal effort. These observations are consistent with the idea of a central limitation to
VO2max.
ACKNOWLEGMENTS
The author would like to thank all the co-investigators who made possible the research projects
discussed in this article. The studies were supported by the CMRC, Team Denmark and the
GSSI.
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Page 5 of 13
Stroke volume does not decline during exercise at maximal effort in healthy individuals.
Darren E. R. Warburton 1 and Norman Gledhill 2
1. Cardiovascular Physiology and Rehabilitation Laboratory, Experimental Medicine
Program, Faculty of Medicine, University of British Columbia, Vancouver, Canada
2. Kinesiology and Health Science, York University, Toronto, Canada
Lack of agreement regarding the stroke volume (SV) response to exercise is not new; in fact it
dates back to the mid 1900s. However, in 1994 Gledhill et al. provided clear evidence that the
SV of endurance athletes increases throughout incremental to maximal exercise while the SV of
untrained individuals plateaus early in progressive exercise (9). Considerable previous and
subsequent findings strongly support the ability of the healthy human heart to maintain and even
increase SV during short-term, incremental upright exercise. Nevertheless, the evidence that SV
does not decline, but is maintained and even increases during maximal exercise is still
questioned, as reflected by this point-counterpoint debate. Following is the chronologicallyordered evidence to support our “point”.
Research on humans in 1950s and 1960s illustrated that there were varied SV responses to
exercise, but in general it supported the contention that SV could increase during incremental
exercise with no decline during maximal exercise (2). For example, Chapman et al. reported that
although there was variability among individuals, the mean SV of 26 healthy men increased
progressively during incremental exercise (2). Often overlooked from the landmark work of
Astrand et al. (1) is the fact that 11 of the 23 (48%) participants reached their highest SV during
maximal exercise. It is important to point out that the average fitness levels of these participants
suggests that they were normally-to-moderately active (females = 41.4 and males = 54 mL·kg1
·min-1).
Grimby et al. (11) reported that four out of nine (44%) endurance-trained masters level athletes
(mean VO2max = 51.5 mL·kg-1·min-1) attained their highest SV during maximal exercise.
Similarly, Ekblom and Hermansen (5) reported a progressive increase in SV with increasing
exercise intensity (between 40-80% VO2max) in 8 elite (VO2max = 74.6 mL·kg-1·min-1) and 5
regional level (VO2max = 66.0 mL·kg-1·min-1) endurance athletes. Nine of these athletes (69%)
achieved their highest SV during maximal exercise.
In the 1970s and 1980s, a number of investigators using both non-invasive and invasive
measurement techniques supported the ability of humans (in particular endurance athletes) to
increase SV during incremental exercise (3, 17, 18). For example, Spriet et al. (18) using dye
dilution, found that elite endurance runners increased their SV while progressing from 91 to
100% VO2max.
Recent literature has provided even more compelling evidence that endurance-trained individuals
increase their SV throughout incremental to maximal exercise (9, 13, 25, 26, 28, 29). This SV
Page 6 of 13
response has been reported by several international laboratories using various (invasive and noninvasive) techniques in a variety of populations; young men (4, 9, 13, 14, 16, 19, 29, 30), young
women (8, 16, 29), older women (28) and even patients with heart disease (12, 27). An analysis
of individual SV responses to exercise indicates that many untrained or moderately trained
individuals achieve their highest SV during maximal exercise (1, 8, 9, 13) and close to 100% of
endurance athletes achieve their highest SV during maximal exercise (8, 9, 13, 19, 25) (Figure
1).
Collectively, the evidence is overwhelming that the SV of endurance-trained athletes is
maintained and generally increased throughout incremental to maximal exercise. The only
question concerns the prevalence of this response in untrained and moderately trained
individuals. Investigators have reported that the SV of untrained individuals plateaus at
submaximal exercise levels and may decline at near maximal exercise (16, 30), and others have
reported a small increase in SV during maximal exercise (2, 8, 9, 13, 15, 22). It is important to
point out that, generally, when a supramaximal exercise protocol was employed, untrained
individuals exhibited a small, secondary increase in SV during maximal exercise (8, 9, 13, 15).
Additionally, untrained individuals with high blood volumes increased their SV during maximal
exercise (15).
As discussed in the early 1970s (21), the “possibility exists that the intensity of exercise induced
by previous studies in which left ventricular dimensions were measured in experimental animals
or man was not maximal and that the Frank-Starling mechanism does play a role in the response
to severe exertion.” This is a very important point, as SV often shows smaller increases at
submaximal exercise intensities (when multiple exercise stages are employed) then reaches its
highest level at maximal exercise (9, 13, 25, 28, 29). This point also raises the necessity of
utilizing SV measurement techniques that are valid and reliable during maximal exercise (23,
24).
Certainly there is variability among individuals in the SV response to exercise that appears to be
highly reliant upon fitness level. For example, similar to Janicki and coworkers in patients with
chronic heart failure (12), we have identified three major SV patterns during exercise. Most
endurance-trained athletes exhibit an increase in SV throughout incremental to maximal exercise
(9, 13, 19, 26). However, there is considerably more variability in the response of untrained and
moderately trained individuals. Some (like the endurance-trained individuals) are able to
progressively increase their SV during strenuous exercise, some exhibit a plateau at submaximal
levels then maintain their SV at or near this level throughout incremental exercise, and some
display a reduction in SV at higher exercise intensities. In our experience, only the least fit
exhibit a decrease in SV at higher intensities, a pattern that is consistent with reduced myocardial
compliance and marked pericardial constraint (12, 27).
Body position clearly affects the SV response to exercise and likely explains some of the
discrepancies in the literature (26). In the supine position, the myocardium appears to approach
its limits for diastolic filling (i.e. a reduced diastolic reserve capacity) and although endurance
athletes are still able to increase their end-diastolic volume and SV during maximal exercise in
the supine position, the relative changes are significantly smaller than that observed during
Page 7 of 13
upright exercise (26). Thus, the SV response to exercise is highly dependent upon the loading
conditions of the heart and the interplay of intra- and extra-myocardial factors (6, 7).
There are several well-described mechanisms that collectively maintain (or increase) SV at high
heart rates in healthy humans including increased venous return (via the abdominothoracic and
skeletal muscle pump, and venoconstriction), increased atrial and ventricular inotropy, and
enhanced lusitropy (ventricular relaxation) (10). Moreover, there are several training-induced
changes in diastolic and systolic function that allow endurance-trained athletes to increase their
SV throughout progressive exercise. Diastolic filling, in particular, appears to be enhanced
throughout incremental to maximal exercise (despite a reduced time for diastolic filling) (9, 13,
20, 26). Several training-related adaptations are thought to enhance the capacity for diastolic
filling including increased myocardial compliance, reduced diastolic ventricular interaction,
increased left ventricular internal cavity dimensions, increased early filling (i.e., E/A ratio),
increased transmitral pressure gradient and flow velocity (e.g. enhanced diastolic suction),
training-induced hypervolemia, increased rate of LV pressure decline (-dP/dt), and/or increased
rate of calcium uptake within the sarcoplasmic reticulum (6, 10, 20).
In summary, the evidence is compelling that the human heart is able to maintain and even
increase SV during maximal exercise. The only question in our opinion concerns the prevalence
of this response in untrained and moderately trained individuals.
Page 8 of 13
Figure 1: Individual stroke volume responses during incremental exercise in endurancetrained men and women. In each investigation 100% of the athletes achieved their maximal
stroke volume during maximal exercise.
Gledhill et al. 1994 Young Males
Krip et al. 1997 Young Males
Warburton et al. 1999 Young Males
Ferguson et al. 2001 Young Females
-1
Stroke Volume (mL·beat )
250
200
150
100
50
0
0
40
60
80
100
120
140
160
Heart Rate (beats·min-1)
180
200
220
Page 9 of 13
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Rebuttal
González-Alonso
Plato’s Myth of the Cave came to mind when reading my opponents argument: “the SV of
endurance-trained athletes is maintained and generally increased throughout progressive
maximal exercise.” Have my esteemed opponents been looking at “the shadow” or “the true”
cardiac response to maximal exercise? In the context of this debate, Dr. Warburton and Dr.
Gledhill argue that maximal SV and thus Q is achieved in healthy individuals at the point of
fatigue based primarily on their data showing a continuous increase in SV from ~50 ml/beat at a
resting heart rate of ~60 beats/min to ~150 ml/beat (range ~100-200 ml/beat) at a heart rate of
Page 11 of 13
~190 beats/min (Fig. 1)(4, 5, 8, 10). A thorough examination of the experimental protocol is
warranted to determine the validity of these findings.
My opponents have repeatedly determined cardiac function during the last ~2 min of each ~4-6
min exercise stage in incremental exercise tests using protocols that matched subjects for heart
rate, rather than VO2 (4, 5, 8, 10). During the maximal workload, however, Q was determined
early in exercise to avoid fatigue limiting the ability to complete the acetylene-rebreathing
maneuver. The lower maximal a-vO2 difference in their studies (5, 8, 10) compared to others (1,
6, 7, 9) (138-155 versus 170-180 ml/l, respectively) and the 3-4 l/min higher Q in trained
compared to untrained subjects at the untrained VO2max (5) suggest that Q was indeed measured
before fatigue and/or Qmax was overestimated. Thus, a major limitation of these and other
studies in the literature to answer the debated question is that Q is not measured in the few
seconds before exhaustion when found to be blunted (6, 7, 9).
Another explanation for the ever-increasing SV during incremental exercise is that the heart ratematched protocol elevates heart rate values for a given VO2 (3). Incidentally, the heart rate and
SV data up to 50% VO2max of Gledhill et al. (5) agree closely with the findings of Mortensen et
al. (9), who used a protocol including a warm-up period that elevated the initial heart rate to ~90
beats/min. Hence, the pattern of the SV response during incremental exercise is greatly
dependent on the level of heart rate (2, 3). In summary, my opponents’ argument that “the human
heart is able to maintain and even increase SV during maximal exercise” lacks “the true”
maximal measures of SV and is confounded by the elevated heart rate for a given VO2.
References
1.
2.
3.
4.
5.
6.
7.
8.
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and maximal work. J Appl Physiol 19: 268-274, 1964.
Boushel R, Calbet JAL, Rådegran G, Søndergaard H, Wagner PD, and Saltin B.
Parasympathetic neural activity accounts for the lowering of exercise heart rate at high
altitude. Circulation 104: 1785-1791, 2001.
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Ferguson S, Gledhill N, Jammik VK, Wiebe C, and Payne N. Cardiac performance in
endurance-trained and moderately active young women. Med Sci Sports Exerc 33: 11141119, 2001.
Gledhill N, Cox D, and Jammik R. Endurance athlete’s stroke volume does not plateau:
major advantage is diastolic function. Med Sci Sports Exerc 26: 1116-1121, 1994.
González-Alonso J, and Calbet JA. Reductions in systemic and skeletal muscle blood flow
and oxygen delivery limit maximal aerobic capacity in humans. Circulation 107: 824-830,
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and Secher NH. Brain and central haemodynamics and oxygenation during maximal
exercise in humans. J Physiol 557: 331-342, 2004.
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Page 12 of 13
9.
Mortensen SP, Dawson EA, Yoshiga CC, Dalsgaard MK, Damsgaard R, Secher NH,
and González-Alonso J. Limitations to systemic and locomotor limb muscle oxygen
delivery and uptake during maximal exercise in humans. J Physiol 566: 273-285, 2005.
10. Warburton DER, and Gledhill N. Counterpoint: Stroke volume does not decline during
exercise at maximal effort in healthy individuals. J Appl Physiol.
Rebuttal
Warburton and Gledhill
It is important to clarify that this point:counterpoint debate refers to maximal exercise, when
VO2 is at its highest value, not supramaximal exercise when VO2 often declines. In our
counterpoint, we attempted to provide a balanced assessment of the literature, acknowledging
variability in the SV response, but highlighting the ability of the trained myocardium to increase
SV during incremental to maximal exercise. There is clear evidence that in endurance athletes
(VO2max > 65 mL/kg/min) the SV at VO2max is higher than that attained at submaximal and
supramaximal workloads (2, 5, 9, 10).
It is instructive to address the inherent assumptions and/or inferences that serve as the foundation
for Dr. González-Alonso’s point (3). For example, the relationship between heart rate and
workload during incremental exercise cannot strictly be considered linear (6). Furthermore, a
high heart rate does not by default cause a reduction in SV. The left ventricular diastolic
pressure-volume relationship is only affected at heart rates above 170 bpm. Ventricular
interaction, reduced myocardial compliance, and/or pericardial constraint likely explain the
invariant filling and SV at much lower heart rates in sedentary individuals (1, 4). Also, it remains
that many untrained and moderately trained individuals are able to maintain and even increase
SV during maximal exercise (5).
Clearly, it is difficult to attain valid and reliable measures of cardiac output during maximal
exercise (8). When familiarization procedures and supramaximal confirmatory intensities
(plateau or decreasing VO2 values) are used, previous research from independent laboratories
supports the ability to achieve maximal SV at VO2max (2, 10). Moreover, techniques that are not
as affected by movement artifact and that are reliable during strenuous exercise reveal the ability
to increase SV in the face of increasing workload (particularly in endurance athletes) (2, 5). It
should be noted that studies reporting a decline in SV during exercise often evaluated individuals
that were not highly trained and who exercised at peak power outputs well below predicted.
We believe that owing to the potential for cardiac fatigue (7) and marked changes in vascular
volumes, the discussion of cardiac function during prolonged strenuous exercise provides little
insight into the SV response to short-term incremental upright exercise.
There is considerable inter-individual variability in the response to most cardiovascular
parameters during exercise, and much is lost in the translation of this knowledge when mean data
is reported from small sample sizes. Individual results from various studies reveal that most
trained and many untrained individuals maintain or increase their SV during maximal exercise.
Page 13 of 13
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