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* From the Department of Pediatrics (Dr. Rowland, and Mss. Martel and Ferrone), Baystate Medical Center, Springfield, MA; and the Department of Exercise Science (Ms. Goff), University of Massachusetts, Amherst, MA.
Correspondence to: Thomas Rowland, MD, Department of Pediatrics, Baystate Medical Center, Springfield, MA 01199
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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O2max) in boys
than in girls. Design: Comparative group exercise testing.
Setting: Pediatric exercise testing laboratory.
Subjects: Twenty-five prepubertal boys (mean [± SD] age, 12 ± 0.4 years) and 24 premenarcheal girls (mean age, 11.7 ± 0.5 years).
Interventions: Maximal incremental upright cycle exercise.
Measurements and
results: Mean values for O2max
were the following: boys, 47.2 ± 6.1 mL/kg/min; and girls,
40.4 ± 5.8 mL/kg/min (16.8% difference; p < 0.05). The average
maximal stroke index with Doppler echocardiography was 62 ± 9
mL/m2 for boys and 55 ± 9 mL/m2 for girls
(12.7% difference; p < 0.05). No significant gender differences
were seen in maximal heart rate or arterial venous oxygen difference.
When O2max and maximal stroke volume
(SV) were expressed relative to lean body mass, gender differences
declined but persisted, falling to 6.2% and 5.2%, respectively.
Conclusions: These findings indicate that differences in SV
as well as in body composition contribute to gender-related variations
in O2max during childhood. Whether this
reflects small gender differences in relative heart size or dynamic
factors influencing ventricular preload and contractility during
exercise is unknown.
Key Words: cardiac output • children • exercise testing
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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O2max) are consistently
greater in boys than girls throughout the course of childhood. This
gender-related difference in aerobic fitness is evidentwhether
O2max is expressed in absolute
terms or relative to body mass. At 10 years of age, for example, the
average O2max values during
treadmill testing for boys and girls are 1.68 L/min and 1.49 L/min,
respectively. At that age, mass-relative
O2max averages 53 mL/kg/min
for boys and 47 mL/kg/min for girls.1
2
3
At puberty, the
gender gap in O2max widens;
the average O2max is 75%
greater in men than in women at 18 years of age. Relative to body mass,
the mean O2max at that age is
25 to 30% higher in men.
In adults, gender differences in
O2max have been ascribed to a
combination of factors including body composition, blood hemoglobin
concentration, and cardiac size and function.4
5
The mean
body fat content of the young adult woman is approximately 1.7 times
greater than that of her male peers, an inert exercise load that
contributes to the "per kilogram" denominator in expressions of
maximal aerobic power.6
When
O2max comparisons are made
between men and women relative to lean body mass (LBM) instead of total
body mass, the gender difference is reduced by approximately one
half.7
The erythrogenic stimulation of testosterone at puberty gives adult men a 2 g% greater hemoglobin level than women and a correspondingly higher arterial blood oxygen content. Since venous oxygen content at maximal exercise is independent of gender, the maximal arterial venous oxygen difference is typically about 20% greater in adult men.8 In addition, adult women have a smaller heart size, a diminished rise in exercise ejection fraction, and a lower maximal cardiac output than men, even when body size and composition are taken into account.8 9 10 11
Similar factors have been examined when seeking to explain the smaller
gender differences in O2max in
prepubertal children. Even prior to adolescence, boys exhibit lower
average body fat content than girls (13% and 17%, respectively, at
age 10 years).12
As in adults, expressing
O2max relative to LBM, leg
volume, or leg muscle volume reduces, but does not eliminate, gender
differences.13
14
15
Mean blood hemoglobin concentrations
are virtually identical in boys and girls prior to
puberty,16
17
and experimental evidence indicates no
influence of hemoglobin concentration on gender differences in
O2max.18
The higher level of habitual physical activity observed in boys
compared with girls has been proposed as a contributor to differences
in O2max. As pointed out by
Armstrong and Welsman,3
however, research evidence
associating activity with
O2max in children is weak, and
the nature of daily physical activities in the pediatric age group
should not be expected to elicit improvements in aerobic fitness.
According to the Fick equation, gender differences in
O2max that remain after body
composition is considered must be explained by variances in maximal
heart rate, stroke volume (SV), or arterial venous oxygen difference.
Little information is available concerning gender-related influences on
cardiac functional capacity in children and how these might contribute
to differences in O2max. In a
group of 11- to 12-year-old children, Miyamura and Honda19
reported mean O2max values of
46.8 mL/kg/min in boys and 41.6 mL/kg/min in girls on cycle testing.
Average maximal cardiac index (measured by the
CO2 rebreathing technique) was 12.2
L/min/m2 in boys and 11.5
L/min/m2 in girls. The mean maximal stroke index
was 64 mL/m2 for boys and 61
mL/m2 for girls. Several studies have
consistently indicated that during submaximal exercise girls have a SV
that is approximately 5 to 10% lower than boys at the same cardiac
output and oxygen uptake (O2)
levels.20
21
22
23
Most reports indicate no gender differences
in maximal heart rate during childhood.24
This study used Doppler echocardiography to examine gender
differences in cardiac responses to maximal exercise in prepubertal
children and to assess the importance of these differences in
accounting for variations in
O2max between boys and girls.
In this analysis, cardiovascular variables were expressed relative to
body size both by the traditional ratio standard (anthropometric factor
raised to the power 1.0) as well as by allometrically scaled
anthropometric variables derived from allometric scaling.
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Materials and Methods |
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The boys were part of a larger group described in reports of the relationship of cardiovascular function with aerobic fitness25 and field performance.26 Findings for the girls have previously been presented in a comparison of cardiovascular fitness in premenarcheal girls and adult women.27
Habitual physical activity was estimated by asking a parent to judge their child’s activity level on a 5-point scale (1 = very sedentary; 5 = highly involved in sports, always active). The average scores for the boys and girls were 3.4 and 3.6, respectively. Nineteen of the boys (76%) were recent participants in community sports teams compared with 88% of the girls. None was involved in any formal athletic training program.
Subjects were asked to avoid vigorous physical activity in the 24 h before testing. Weight while wearing only shorts and shirt was measured with a calibrated balance beam scale, and height was determined by stadiometer. Scapular and triceps skinfold thicknesses on the right side of the body were measured in triplicate using standard techniques. Average values were converted to an estimated percentage of body fat using the equations of Slaughter et al28 LBM then was calculated as (body mass) - (percent fat x body mass).
Immediately before exercise, supine left ventricular dimensions were determined using M-mode echocardiography with two-dimensional guidance from a parasternal long-axis view (Sonos 1000; Hewlett Packard; Andover, MA). All measurements were made just distal to the tips of the mitral valve leaflets and were recorded as the mean of three determinations. Left ventricular end-diastolic dimension (EDD) was determined by the distance from the trailing edge of the ventricular septum to the free wall endocardial surface coincident with the Q wave of the ECG. The shortest distance from the free wall endocardium to the ventricular septum was recorded as the end-systolic dimension. Values were expressed relative to the square root of body surface area (BSA).29 Left ventricular shortening fraction was calculated as the quotient of (EDD - ESD)/EDD x 100 (where ESD is end-systolic dimension).
Testing was conducted in an air-conditioned laboratory with a temperature of 20 to 21°C. Subjects were encouraged to exercise to exhaustion while cycling in the upright position on a mechanically braked ergometer (model 868; Monark; Stockholm, Sweden). Cycling cadence was maintained at 50 revolutions per minute. Prior to testing, seat height was adjusted to provide a small knee angle at full extension. Exercise was performed with initial and incremental workloads of 25 W, with a stage duration of 3 min. The test was stopped when the subject could no longer sustain the pedaling rate. Endurance fitness was measured as the highest workload achieved, prorated for partial stages completed (physical working capacity).
Heart rate was recorded by ECG. Subjects breathed through a mouthpiece
attached to a 94-mL dead space valve (Rudolph Instruments; Fairfield,
NJ). Gas exchange variables were determined using standard open
circuit techniques (Q-Plex Cardio-Pulmonary Exercise System; Quinton
Instrument Co; Seattle, WA). Expired air samples were drawn from a 6-L
mixing chamber and were analyzed for oxygen and carbon dioxide content
using zirconia oxide and infrared analyzers, respectively. Minute
ventilation was determined by a pneumotachometer in the expiratory
line. Mean values for O2,
carbon dioxide output, carbon dioxide
output/O2 ratio (respiratory
exchange ratio [RER]), and minute ventilation were calculated over
15-s intervals. The system was calibrated prior to each individual test
using standard gases of known oxygen and carbon dioxide content.
The average of the two highest values (15-s averages) of
O2 over the final minute of
exercise was used to define peak
O2. Peak
O2 was considered to reflect
O2max if subjects demonstrated
subjective evidence of exhaustion with a maximal heart rate > 185
beats per minute (bpm), a maximal RER > 1.00, or both.
Standard Doppler echocardiographic techniques were utilized to estimate cardiac output at rest, during submaximal exercise, and at exhaustion.30 The velocity of blood in the ascending aorta was measured with a 1.9-Mhz transducer (Pedof) directed from the suprasternal notch. By tracing the contour of this velocity curve, an integral of velocity over time (velocity-time integral [VTI]) was obtained for individual beats. VTI values at rest, during the final minute of each submaximal workload, and in the last 30 s of exercise were determined by averaging the 3 to 10 curves with the highest values and most distinct spectral contours. Data indicating the reproducibility and validity of this technique previously have been reported from this laboratory.31 32
SV was estimated as the product of the VTI and the aortic
cross-sectional area, calculated from the aortic diameter measured at
rest. The maximal diameter of the ascending aorta (measured at the
sinotubular junction from inner edge to inner edge) was determined by
two-dimensional echocardiography (parasternal long-axis view) with the
subject seated on the cycle ergometer. The aortic cross-sectional area
was calculated from the average of 5 to 10 diameter determinations,
assuming the aorta to be circular. Cardiac output was calculated as the
product of heart rate and SV, and arterial venous oxygen difference was
calculated by dividing absolute
O2 by cardiac output. Values
for peak aortic velocity were obtained from the zenith of the
velocity-time curves.
Student’s t test comparisons of cardiovascular variables
between boys and girls were performed after values were adjusted to
body size by traditional anthropometric measures
(O2 per kilogram of
body mass, SV, and cardiac output per BSA) and by allometrically
derived anthropometric variables calculated from these specific subject
populations. In the latter analysis, the scaling exponent b
was identified in the allometric equation
Y = aXb, where Y is the physiologic
variable, X is the anthropometric scaling variable (mass or BSA), and
a is a constant multiplier. To obtain b, log
transformation of both the Y and X was performed, and least squares
regression identified b in the equation log (Y) = log
(a) + b log (X). Statistical significance for
differences in gender values for Y and X was defined as p < 0.05.
Informed consent and assent were obtained from the parents and children, respectively. This study was reviewed and approved by the Institutional Review Board of the Baystate Medical Center.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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O2max. Average maximal RERs of
1.07 ± 0.04 for boys and 1.06 ± 0.05 for girls indicated an equal
exercise effort in the two groups. Endurance fitness was 27% greater
in the boys (physical working capacity, 3.12 ± 0.45 vs
2.46 ± 0.43 W/kg; p > 0.05).
No significant relationship was observed between either maximal heart
rate or maximal arterial venous oxygen difference and the
anthropometric measures (mass or BSA) for either group. Therefore,
these variables were expressed in absolute terms in gender comparisons.
Maximal values for O2, cardiac
output, and SV were positively associated with body mass and surface
area (r = 0.65 to 0.80). Allometric equations relating maximal
physiologic variables to body dimensions were the following:
Boys
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As genders differences for the exponent b were insignificant for all these measures, average values of b were utilized for gender comparisons.
Physiologic variables related to both the ratio standard
(X1.0) and the averaged empirically derived
allometric denominator (Xb) are presented
in Table 2
. The 7.6% greater mean value for absolute
O2max in boys
increased to 16.8% when related to body mass and decreased to 6.2%
when expressed with respect to LBM. However, the difference in
O2max per kilogram
of LBM between the boys and girls remained significant.
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O2max and maximal SV were not
significantly altered when values were expressed relative to
allometrically derived denominators. Values for maximal heart rate and maximal arterial venous oxygen difference in the two groups were almost identical. No significant difference was observed in maximal peak aortic velocity, suggesting that cardiac contractility and/or afterload at peak exercise was gender-independent.
Stroke index (SV/BSA) at rest was 45 ± 8 mL/m2
for both boys and girls. With the initial increased workload, SV rose
in the boys to reach a plateau at approximately 50% of
O2max. The girls demonstrated
a similar pattern but with a smaller increase (Fig 1
). Consequently, the stroke index at maximal exercise was significantly
greater in the boys (62 ± 9 vs 55 ± 9
mL/m2, respectively). Mean values for maximal VTI
and resting aortic cross-sectional area were greater in the boys, but
neither achieved statistical significance. The boys demonstrated a
significantly larger ratio of maximal SV to rest SV than the girls
(1.42 ± 0.23 vs 1.26 ± 0.22).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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O2max expressed relative to
body mass is approximately 15% higher in 12-year-old boys than in
girls the same age.1
2
3
In the present study, the boys
exhibited an average mass-relative
O2max that was 16.8%
higher than that of the girls.
Differences in body composition were responsible for approximately two
thirds of this gender difference. The average percent of body fat was
20.0% for the boys and 26.2% for the girls, and when
O2max was expressed relative
to LBM the gender gap narrowed to 6.2%. This influence of body fat on
gender differences in O2max
per kilogram mimics that reported by Sunnegardh and
Bratteby14
in 8-year-old Swedish boys and girls. Mean
O2max per kilogram of body
mass was 52.7 mL/kg/min for the boys and 45.9 mL/kg/min for the girls
(a 14.8% difference). When
O2max was expressed relative
to LBM, the difference narrowed to 6.8%, a difference that remained
statistically significant.
It is evident, then, that additional factors must contribute to gender
differences in aerobic fitness in children besides body composition.
Hemoglobin levels were not determined in this study. However, it may be
assumed that hemoglobin concentration played no role in the observed
gender differences in aerobic fitness since the mean values for maximal
arterial venous oxygen difference were virtually identical in the boys
and girls. At 12 years of age, little or no gender differences in
hemoglobin concentration are expected.16
17
In a study in
which significant differences in
O2max per kilogram were
observed in 10- to 11-year-old children, Armstrong et al33
found that mean hemoglobin concentrations were similar in boys and
girls. These data suggest that hemoglobin concentration does not
contribute to gender differences in
O2max during the prepubertal
years.
Armstrong and Welsman3
have argued that the level of
habitual activity in boys and girls, although typically greater in
boys, is unlikely to play an important role in defining differences in
aerobic fitness. Daily activity in children typically lacks the
intensity and duration sufficient to improve
O2max, and studies examining
the relationship of activity and
O2max in children have shown
no conclusive association.34
In the present study, the
boys and girls were, by parental report, similar in level of habitual
activity as well as in involvement in community sports teams.
Doppler echocardiography affords the opportunity to safely and
conveniently compare gender-related cardiac responses to exercise in
children. In this study, maximal SV was the sole variable
distinguishing cardiovascular findings at peak cycle exercise in boys
and girls. The average maximal stroke index was 62 ± 9
mL/m2 in the boys and 55 ± 9
mL/m2 in the girls. This 12.7% difference was
reduced to a statistically insignificant 5.2% when body fat
differences were taken into account. These findings correspond closely
to the gender differences observed in
O2max, which were 16.8% when
related to body mass and 6.2% when expressed relative to LBM
(p < 0.05). The mean values of maximal heart rate (boys, 199 ± 11
bpm; girls, 198 ± 9 bpm) and the maximal arterial venous oxygen
difference (boys, 12.3 ± 1.9 mL/100 mL; girls, 12.2 ± 1.7 mL/100
mL) were almost identical in the two groups. This information indicates
that gender differences in maximal SV in prepubertal children are small
but real, and that they account for differences in
O2max between boys and girls
after body fat content is considered.
The explanation for gender differences in maximal SV in children is not clear. Turley and Wilmore20 suggested that SV differences in boys and girls might be explained by a relatively larger heart size in boys. The evidence cited was a report by Shephard et al,35 involving children from Toronto who ranged in age between 9 and 13 years, that stated the absolute mean heart volume estimated by chest radiograph to be 379 ± 77 mL in boys and 356 ± 69 mL in girls (the average weight of the boys was 0.5 kg more than the girls). However, Maresh36 could find no difference in the average cardiothoracic ratio (ratio of the transverse cardiac diameter to the internal chest diameter) on chest radiographs of 12-year-old boys and girls (0.41 for both groups). Scholz et al37 reported that the average expected weight of the heart was 168 g in a 40-kg boy compared to 160 g in a 40-kg girl.
The longitudinal echocardiographic study of Nagasawa et al38 indicated a small but significant gender influence on the development of left ventricular EDD during childhood. Their results indicted that the predicted EDD values for boys and girls 150 cm in height were 45.2 mm and 43.3 mm, respectively. However, Nidorf et al39 found that the pattern of growth of left ventricular dimensions in childhood was independent of gender. Similar values of resting left ventricular EDD (related to body height) in boys and girls were also described by Gutin et al.40
It is not clear, then, whether prepubertal girls truly have smaller hearts relative to their body size than boys. Heart size may be most accurately related to LBM,41 and these studies did not take into account body composition differences between boys and girls.
In the present study, no significant gender difference was observed in resting, supine, left ventricular diastolic dimension (related to the square root of BSA), and the average stroke indexes for boys and girls while sitting upright on the cycle were identical (45 ± 8 mL/m2). The characteristic of the cardiac response to progressive exercise that distinguished the boys and girls was a lower rise at the onset of exercise in the latter. This suggests that factors influencing SV during exercise (skeletal muscle pump function, systemic vascular resistance, and adrenergic responses) rather than intrinsic left ventricular size may be responsible for the small gender differences in maximal SV during childhood.
In this study, the performance on a non-weight-bearing endurance task was 27% greater in the boys than the girls, a difference in excess of that indicated by physiologic measures. This finding is consistent with the observation of others that performance in girls is lower, relative to their physiologic potential, than in boys.42 In the current study, motivation and level of involvement in physical activity and sports could not account for this gap, suggesting that other determinants that were not measured (such as anaerobic fitness) are important in gender differences in endurance performance. Previous reports indicate that performance on anaerobic tests is lower in girls, even when body composition is taken into account.43 44 For example, Van Praagh et al43 found that anaerobic power measured by the force-velocity test was 33% greater in 12-year old boys than in girls. When expressed relative to fat-free mass, the difference fell to 15%.
In summary, the findings in this study suggest the following: (1)
cardiac functional capacity as well as body composition and size
account for the differences in
O2max between prepubertal boys
and girls; (2) maximal SV is the sole cardiac variable responsible; (3)
gender differences in maximal SV reflect a blunted response during
exercise in girls compared with boys; and (4) anthropometric and
aerobic physiologic factors cannot entirely account for the magnitude
of gender differences in progressive cycle performance.
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Footnotes |
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O2 = oxygen uptake;
O2max = maximal oxygen uptake;
VTI = velocity-time integral Received for publication April 23, 1999. Accepted for publication August 9, 1999.
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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 S Eiberg, H Hasselstrom, V Gronfeldt, K Froberg, J Svensson, and L B Andersen Maximum oxygen uptake and objectively measured physical activity in Danish children 6-7 years of age: the Copenhagen school child intervention study Br. J. Sports Med., October 1, 2005; 39(10): 725 - 730. [Abstract] [Full Text] [PDF]
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