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ORIGINAL ARTICLE
Circulatory ‘‘Efficacy’’ during progressive aerobic exercisein children: insights from the Q:VO2 relationship
Thomas Rowland
Accepted: 11 April 2007 / Published online: 3 May 2007
� Springer-Verlag 2007
Abstract The relationship between circulatory flow (Q)
and oxygen uptake (VO2) may provide insights into per-
formance of peripheral mechanisms which govern blood
flow during exercise (circulatory efficacy). This study
evaluated the response of Q relative to VO2 during pro-
gressive upright cycle exercise in a group of 39 preado-
lescent boys (mean age 12.2 ± SD 0.5 years). The Q–VO2
relationship was curvilinear, best described by the cubic
equation Q = 3.60(VO2)3 + 5.24(VO2)2 + 2.40(VO2) –
0.94. Circulatory efficacy, defined as the %DQ/
%DVO2 · 100, fell from 70.4% between the first two
workloads to 49.7% at peak exercise. This decline in cir-
culatory efficacy is consistent with other published data
suggesting a decline in skeletal muscle pump function at
high intensity workloads. The pattern of change in rela-
tionship of Q and VO2 during progressive exercise in these
children is similar to that observed in studies of adults. This
implies that performance of peripheral determinants of
circulatory responses to exercise is not affected by bio-
logical maturation.
Keywords Cardiac output � Cardiovascular fitness �Oxygen uptake
Introduction
Circulatory responses to endurance exercise are mediated
primarily via peripheral mechanisms, particularly arteriolar
dilatation and skeletal muscle pump function (Tschakovsky
et al. 1996; Rowland 2005a). Traditional tenets hold that
during progressive exercise this circulatory response (Q) is
closely coupled with metabolic demand, or oxygen uptake
(VO2) (Astrand et al. 1964; Faulkner et al. 1977). It is
clear, however, that while Q generally rises proportion-
ately to increases in VO2, circulatory supply falls far short
of satisfying the oxygen requirements of exercising muscle
cells. In fact, for any given increase in work rate, oxygen
delivery by the circulation accounts for only approximately
50% of the rise in metabolic demand (Rowland 2001). To
compensate for this perfusion-demand gap, skeletal muscle
extracts an increasing amount of oxygen from each unit
volume delivered to the capillary-cell interface to satisfy
mitochondrial aerobic demands. Consequently, arterial
venous oxygen difference steadily rises as work intensity
increases.
This observation may bear importance in characterizing
the peripheral determinants of circulatory responses to
exercise, particularly the function of the skeletal muscle
pump (SMP). Gotshall et al. (1996) viewed the relative
contribution of Q to a given level of VO2 as a marker of the
efficacy of these responses. That is, according to this
concept, the ratio of Q/VO2 serves as a marker of the
performance of peripheral determinants of circulatory flow,
while arterial venous oxygen difference becomes a nega-
tive index of the adequacy of the circulatory response to
exercise.
It is important to recognize, as well, that evidence exists
that the Q–VO2 relationship is not entirely linear through
the course of a progressive exercise test (Grimby et al.
1966; Yamaguchi et al. 1986; Vella and Robergs 2005).
For example, Vella and Robergs (2005) recently described
a curvilinear relationship between Q and VO2, which
indicated a decrease in Q–VO2 slope of more than 1 l min–1
Q/1 l min–1 VO2 over a VO2 span of 4 l min–1. Others have
T. Rowland (&)
Department of Pediatrics, Baystate Medical Center,
Springfield, MA 01199, USA
e-mail: [email protected]
123
Eur J Appl Physiol (2007) 101:61–66
DOI 10.1007/s00421-007-0472-1
reported a plateau in Q at high work intensities (Yamag-
uchi et al. 1986). These observations imply a decline in
circulatory efficacy—and, by inference, reduced effec-
tiveness of arteriolar dilatation and/or SMP function—as
maximal exercise level is approached.
This conclusion is consistent with recent work by Lut-
jemeier et al. (2005) indicating a decrease in skeletal
muscle pump function at high work intensities due to
increasing intramuscular vascular compression and inflow
occlusion. Others have indicated evidence of limited SMP
activity at maximal work loads (Takahashi and Miyamoto
1998; Rowland and Lisowski 2003). This information
suggests that peripheral factors other than SMP function
(i.e. arteriolar dilatation) may act to limit circulatory flow
in a progressive exercise test.
This study examined the relationship between Q and
VO2 during a standard progressive upright cycle test in a
group of nontrained preadolescent boys using Doppler
echocardiography. Clarifying the nature of this association
in the pediatric age group bears particular importance, as
children characteristically demonstrate a lower Q/VO2
during exercise than adults (Bar-Or 1983). Some have
interpreted this finding as indicative of a ‘‘hypokinetic’’
cardiac response to exercise in young subjects (Faulk
2000). Others have concluded the lower Q/VO2 in children
to be spurious and biologically irrelevant, since (1) children
and adults do not exercise at the same absolute VO2 and (2)
the ratio is explained simply by the lower stroke volume
expected in children (Rowland 2005b). An examination of
the course of the Q/VO2 relationship during progressive
exercise would help resolve these conflicting interpreta-
tions.
Methods
Thirty-nine boys (mean age 12.2 ± 0.5 years) from the
same sixth grade class agreed to perform maximal up-
right cycle exercise with measurements of gas exchange
and cardiovascular variables. Subjects were invited from
quartiles of performance on a standard school one-mile
run/walk and thus represented a full spectrum of car-
diovascular fitness. Data from these boys has previously
been published in reports of the physiologic and
anthropometric determinants of field and laboratory aer-
obic fitness (Rowland et al. 1999a, b) and also in a study
of allometric scaling of one-mile run performance (Nevill
et al. 2004).
The subjects were in good health and none had signifi-
cant obesity. Two-thirds had recently participated on a
community sports team, but none were involved in regular
athletic training. By questionnaire, 14 had onset of voice
change and/or pubic hair indicative of early puberty.
Subjects were asked to refrain from vigorous physical
activity within the 24 h before the exercise test. In an at-
tempt to create some homogeneity of fluid balance, each
boy drank 240 ml of a sports drink one hour before
appearing at the exercise laboratory. Height and weight
were measured with a stadiometer and calibrated balance
beam scale, respectively. Right-sided scapular and triceps
skinfold thicknesses were averaged from triplicate mea-
surements to the nearest 0.1 mm, and body fat was esti-
mated by the equations of Slaughter et al. (1988).
Subjects performed a continuous multi-stage cycle test
to exhaustion in the upright position in an air-conditioned
laboratory (19–21�C). Initial and incremental loads were
25 W, with 3 min stages and a steady pedaling cadence of
60 rpm. Subjects were verbal encouraged to achieve an
exhaustive effort, and the test was terminated when the
pedaling cadence could no longer be maintained. Peak
work capacity (PWC) was defined as the greatest work load
achieved, prorated for incomplete stages.
Heart rate was recorded by an electrocardiogram. Gas
exchange variables were measured by standard open circuit
techniques using a Q-Plex Cardiopulmonary Exercise
System (Quinton Instrument Company, Seattle, WA).
Subjects breathed through a Rudolph valve (94 ml dead
space) into a 6 l mixing chamber from which gas samples
were drawn for analysis (oxygen and carbon dioxide con-
tent by zirconia oxide and infrared analyzers, respectively).
Minute ventilation was measured by a pneumotachometer
in the expiratory line. The system was calibrated before
and after each test with standard gases of known oxygen
and carbon dioxide concentration.
Gas exchange values, including VO2, were averaged and
recorded at 15 s intervals. Submaximal VO2 levels were
determined as the average of values over the third minute
of each work stage, while peak VO2 was defined as the
mean of the two highest values in the final minute of
exercise. Peak VO2 was assumed to reflect VO2max with
peak heart >185 bpm and peak respiratory exchange ratio
(VCO2/VO2) >1.00, accompanied by subjective evidence
of fatigue (hypernpea, flushing or pallor, sweating).
Stroke volume was estimated at rest and during sub-
maximal and maximal exercise by standard Doppler
echocardiographic techniques (Rowland and Obert 2002).
Velocity in the ascending aorta was measured by a
1.9 MHz (Pedof) transducer directed inferiorly from the
suprasternal notch. Integration of velocity versus time
(VTI) was averaged for the 5–10 beats with highest con-
sistent values and stroke volume was estimated by multi-
plying this value times the aortic cross-sectional area (sino-
tubular junction) measured by two-dimensional echocar-
diography in the seated position at rest. Stroke volume was
determined at rest, in the final minute of each workload,
and in the final 30–60 s of exercise. Cardiac output was
62 Eur J Appl Physiol (2007) 101:61–66
123
calculated as the product of stroke volume and simulta-
neously measured heart rate. Circulatory efficacy was
examined quantitatively by two definitions: (1) the ratio of
scope (multiple of resting value) of Q versus VO2, and (2)
the percent change in Q relative to percent change in VO2
between successive workloads, expressed as a percent.
(i.e., the extent that change in VO2 could be accounted for
by change in Q). Arterial venous oxygen difference was
calculated as VO2/Q.
Reports of the validity and reliability of the Doppler
echocardiographic technique for estimating cardiac output
during maximal exercise have been previously published
from this laboratory (Rowland and Popowski 1997; Row-
land et al. 1998). This method is particularly useful for this
investigation, as Q and VO2 can be obtained simulta-
neously, measurement is nonobtrusive, and steady state is
not necessary.
The configuration of the relationship of Q to VO2 with
increasing workloads was examined by curve fitting using
commercial statistical software (SPSS 11.0 for Windows,
SPSS, Inc., Chicago, IL). Comparisons were made using
linear, cubic, quadratic, log, and exponential models,
defining the best fit as the model with the highest coeffi-
cient of determination (r2).
Results
Average weight and height of the subjects was
45.6 ± 10.1 kg and 153 ± 9 cm, respectively, with a mean
19.4 ± 6.5% estimated body fat. Two subjects did not sat-
isfy criteria for VO2max, but by staff observations both had
achieved a true exhaustive effort, and their data are included
in this analysis. Average VO2max was 47.0 ± 5.8 ml kg–1
min–1 with a mean PWC of 135 ± 21 W. Mean values of
maximal stroke index (related to body surface area) and
cardiac index were 61 ± 11 ml per m2 and 11.98 ± 2.33 l
min–1 per m2, respectively. Calculated arterial venous
oxygen difference rose progressively from a resting value of
5.8 ± 1.6 ml 100 ml–1 to 13.0 ± 2.5 ml 100 ml–1 at peak
exercise.
Figure 1 indicates a curvilinear relationship of Q and
VO2 during progressive exercise. The greatest r2 (1.00)
was defined by a cubic model, with the equation
Q = 3.60(VO2)3 + 5.24(VO2)2 + 2.40(VO2) – 0.94. The
linear equation (r2 = .989) was Q = 3.86VO2 + 6.24.
By both definitions, circulatory efficacy fell as exercise
intensity increased. Scope values for submaximal work-
loads 1–4 (25–100 W) and maximum (135 ± 12 W) were
1.49, 1.84, 2.21, 2.60, and 3.04 for Q, respectively, and
2.29, 3.06, 4.03, 5.10, and 6.87 for VO2. As demonstrated
in Fig. 2, this indicated a decline in circulatory efficacy
that reached <50% at high work loads.
Table 1 indicates submaximal and maximal data for Q
and VO2. Efficacy defined as %D Q relative to %D VO2
between successive work loads fell from 70.4% at light
work to 49.7% at high work intensity.
Discussion
Abundant evidence has accumulated supporting a critical
role for peripheral mechanisms (arteriolar dilatation, skel-
etal muscle pump function) in facilitating and controlling
circulatory responses to exercise (Rowland 2001, 2005a).
Delineating the functional characteristics of these factors,
2.22.01.81.61.41.21.00.80.66
7
8
9
10
11
12
13
14
15
16
17
QL min-1
VO2 L min-1
Fig. 1 Cardiac output (Q) ± standard deviation plotted relative to
oxygen uptake (VO2) during progressive exercise to exhaustion. Data
are presented at 25, 50, 75, 100, and 135 ± 21 W (max)
6.05.04.03.02.01.00
1.0
2.0
3.0
4.0
5.0
6.0
Q
50%
100%
VO2
Fig. 2 Scope of VO2 and Q (expressed as multiples of resting values)
with progressive exercise. The solid line of identity indicates 100%
circulatory efficacy (i.e., identical slope), while the dashed linedenotes 50% efficacy
Eur J Appl Physiol (2007) 101:61–66 63
123
however, has proven challenging. A number of experi-
mental approaches have been utilized, including compari-
son of exercise Q to flow with pathologic arterial venous
fistulae (Binak et al. 1960) and use of pharmacologic
vasodilators (Panchev et al. 2005) (to simulate local arte-
riolar dilatation during exercise conditions) and muscle
compression (Tschakovsky et al. 1996), electrical muscle
stimulation (Raymond et al. 1999), effect of changes in
cycling cadence and force (Sheriff 2002), and immediate
post-exercise flow measurements (Lutjemeier et al. 2005)
to assess skeletal muscle pump function.
As examined in the present study, the relationship be-
tween Q and VO2 may be interpreted as an indicator of
circulatory efficacy during exercise, and, by extension, a
marker of arteriolar dilatation and/or skeletal muscle pump
function. The findings in this group of 12-year old boys
using Doppler ultrasound indicated a non-linear relation-
ship between Q and VO2 during progressive exercise,
consistent with diminishing circulatory efficacy as muscle
contractile force and metabolic demand intensified. As a
consequence, efficacy (defined as the magnitude of in-
creased oxygen demand satisfied by a rise in Q) fell pro-
gressively during exercise.
This finding is consistent with recent reports in adult
subjects as well as earlier research information (see Clau-
sen 1976, for review). Vella and Robergs (2005) described
a curvilinear relationship between Q and VO2 in trained
adult male athletes throughout the duration of a progressive
upright cycling test while using the carbon dioxide reb-
reathing method for measuring Q. Using the dye dilution
technique in untrained adult men, Yamaguchi et al. found a
linear association between Q and VO2 in the submaximal
exercise intensity range (1986). However, above ~70%
VO2max the majority of subjects demonstrated a tapering
of Q and decreasing Q/VO2. On the other hand, others have
indicated no change in Q/VO2 during progressive exercise
in adults when Q was estimated by impedance cardiogra-
phy (Miyamoto et al. 1992) or carbon dioxide rebreathing
(Faulkner et al. 1977). McCole et al. (2001), utilizing the
acetylene rebreathing method, noted that demonstration of
a dissociation beween Q and VO2 at maximal exercise was
dependent on the duration of the testing protocol.
While the peripheral factors explaining this decline in
efficacy remain to be clarified, recent observations by
Lutjemeier et al. (2005) of a decline in SMP function at
high workloads may be particularly pertinent. Evidence
indicates that net performance of the SMP depends on the
balance of (1) enhanced flow from venous compression
(assisted by venous valves) and the negative suction effect
created by muscle contraction, and (2) inhibition of inflow
caused by the high pressures accompanying vascular
compression (Folkow et al. 1970; Sheriff et al. 1993). By
comparing muscle blood flow during and immediate after
exercise, Lutjemeier and her colleagues were able to con-
clude that the negative effect of compression became rel-
atively greater than flow enhancement as work intensity
increased. That is, at high work rates, mechanisms of en-
hanced flow by the SMP were not capable of compensating
for impairment of inflow due to the increasing force of
muscle contraction.
That the SMP plays a limited role in Q at peak exercise
is supported by other investigations. In a study involving
both men and boys, Rowland and Lisowski (2003) found
that cardiac output fell only 10–15% in the first 15–20 s
after the SMP was abruptly stopped at maximal or sub-
maximal exercise. Similarly, Takahashi and Miyamoto
(1998) reported a decrease in average cardiac output from
12.7 to 11.1 l min–1 in the first 20 s after submaximal
upright cycling in adult men. These observations would
suggest that the decline in Q/VO2 at higher work intensities
documented in this and other studies may reflect a decline
in circulatory efficacy resulting from decreased contribu-
tion of SMP.
It should be recognized that central (i.e. cardiac) as well
as peripheral factors can influence values of Q/VO2. Pa-
tients with congestive heart failure, for instance, exhibit
lower Q/VO2 during exercise (Clausen 1976). In this study
of healthy children, however, it would seem unlikely that
cardiac factors would have a negative influence on Q/VO2.
This study also provided an opportunity to assess the
possible effect of biological maturation on circulatory
efficacy during exercise. Bar-Or (1983) first brought
attention to the fact that any given absolute VO2 during
exercise is met with a lower Q in children compared to
adults. Combining data from several studies, he demon-
strated that such values of Q in children clustered at the
bottom of the normal range for adults as VO2 rose.
This ‘‘hypokinetic’’ cardiovascular response to exercise
by children has been considered to bear implications for
aerobic fitness in youth, particularly in respect to matura-
tional differences in performance in hot ambient tempera-
tures (Faulk 2000). Others have considered this observation
biologically spurious, an expression of the child’s obvi-
Table 1 Mean (standard deviation) values of cardiac output (Q) and
oxygen uptake (VO2) during progressive exercise
Q (l min–1) VO2 (l min–1) Efficacy (%)
25 W 8.11 (1.41) 0.71 (0.08)
50 W 10.04 (1.73) 0.95 (0.09) 70.4
75 W 12.08 (1.95) 1.25 (0.11) 64.2
100 W 14.15 (2.51) 1.58 (0.12) 64.8
Max (135 ± 21 W) 16.60 (3.48) 2.13 (0.41) 49.7
Efficacy = %D Q relative to %D VO2 between individual stages,
expressed as a percent
64 Eur J Appl Physiol (2007) 101:61–66
123
ously smaller stroke volume, with no physiologic or per-
formance importance (Rowland 2005b). This latter argu-
ment has been supported by data indicating that when the
response of cardiovascular variables to exercise are related
appropriately to body size, no differences are observed
between children and adults (Rowland et al. 1997; Nottin
et al. 2002).
The present study supports the latter viewpoint. As
indicated in Fig. 3, the observed curvilinear pattern of
decline of Q relative to VO2 with progressive exercise was
similar to that previously reported in adult subjects. (Dif-
ferences in absolute values in these different studies may
be explained by variations in measurement technique and
body position.) By inference, then, the magnitude of de-
cline in circulatory efficacy with increasing work intensity
is no different in children than adults.
In summary, the findings in this exercise study of 12-
year old boys using Doppler ultrasound indicate a non-
linear relationship between Q and VO2, consistent with the
concept of diminishing circulatory efficacy as work inten-
sifies. This reduced efficacy may reflect a reduction of
skeletal muscle pump performance at high work loads. In
addition, this investigation failed to reveal evidence of
maturational differences in the pattern of circulatory re-
sponses to progressive endurance exercise.
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