Development of Ventilatory Responses
to Exercise in Normal White Children*
A Longitudinal Study
Thomas W. Rowland, MD; and Lee N.
Cunningham, DPE
Cross-sectional studies have indicated that the pattern of ventilatory responses to exercise evolves
during the course of childhood. This 5-year study was designed to provide a longitudinal
assessment of minute ventilation (Ve), tidal volume (Vt), and breathing frequency (fR) in 20
children (11 girls, nine boys) between the ages of 9 and 13 years. Subjects performed maximal and
identical submaximal steady-state treadmill walking tests annually. No significant gender differ¬
ences were observed in any of the three variables. At submaximal exercise, Vt per kilogram
remained stable, with a progressive fall in fR. As a result, submaximal Ve per kilogram declined
with age. A similar pattern was observed at maximal exercise, but the decrease in Ve per kilogram
was not statistically significant. Ventilatory equivalent for oxygen (Ve/Vo2) fell with age at
submaximal exercise but declined only in the boys with maximal testing. Ve/Vo2 at maximal and
submaximal exercise was greater in the girls at all ages. These findings support previous data
derived from cross-sectional studies. (CHEST
1997; 111:327-32)
Key words: children; exercise; maturation; ventilation
Abbreviations:
fR=breathing rate (frequency);
Vo2=oxygen uptake; Vt=tidal volume
VE minute
=
"IT* nowledge of the normal course of developmen-"*tal exercise physiology is important in under¬
standing aerobic fitness in the pediatric population.
To this end, a series of cross-sectional investigations
has provided a composite picture of the changes in
ventilatory
response to exercise in growing chil¬
dren.1'5 In general, these studies have indicated that
increases in maximal and submaximal ventilation and
tidal volume (Vt) during the course of childhood are
closely linked to age. Over the same period, breath¬
and ventilatory equivalent for oxygen (Ve/
ing
in
Vo2) response to exercise progressively decline.
Longitudinal data regarding ventilatory changes in
exercising children are limited, confined to a single
study ofInNorwegian children between ages 8 and 15
years.6 that investigation, ventilatory responses
were observed during cycle testing, and submaximal
values were reported at similar relative rather than
absolute exercise intensities. In general, findings
mimicked those of the cross-sectional reports.
This 5-year longitudinal study was conducted to
rate
*From the
Department of Pediatrics, Baystate Medical Center,
of Physical Education,
Springfield, Mass, and the Department
Mass.
Fitchburg State
College,
Fitchburg,
Manuscript received May 23, 1996; revision accepted Septem¬
ber 11.
Reprint requests: Dr. Rowland, Department of Pediatrics, Baystate Medical Center, Springfield, MA 01199
ventilation; Ve/Vo2 =ventilatory equivalent for oxygen;
expand our understanding of the normal changes of
ventilatory
responses to exercise during childhood.
Maximal and submaximal data were obtained annu¬
ally from treadmill testing, with submaximal values
determined at the same speed and slope. Particular
attention was focused on the means by which these
serial measurements related to changes in body size.
Materials
and
Methods
Twenty children (11 boys, nine girls) volunteered for annual
treadmill testing over 5 years for assessment of submaximal and
maximal measurements of respiratory exchange variables. Data
from one girl who moved away were not available for the final
testing session. The subjects were generally physically active.
Seventeen were participants on community sports teams, but
none was engaged in regular endurance training. With the
exception of one child, all were white, and all subjects were in
good health, taking no medications that would affect exercise
testing results. Data from these subjects were included in a
previous report of walking economy in children.7
Average age at the start of the study was 9.2 years (range, 7.9
to 10.3 years). At the last testing session, three of the eight girls
reported having experienced menarche, and 7 of the 11 boys had
development of pubic hair, voice change, or facial hair (by
parent-completed questionnaire), indicative of early puberty.
Treadmill testing was performed yearly in an air-conditioned
laboratory (20 to 22°C). Following determination of height and
weight, subjects warmed up on the treadmill for 2 min, walking
at 3.25 mph up a 6% grade. The test protocol involved an initial
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327
4-min walk at 3.25 mph, 8% grade. Treadmill
then increased 2% every minute until subject
exhaustion, with speed individualized between 3.25 and 3.75 mph
steady-state
elevation
was
depending on subject size and fitness. Holding onto handrails was
not permitted.
Gas exchange variables were determined with a computerized
metabolic cart (Q-Plex Cardio-Pulmonary Exercise System;
Quinton Instrument Co; Seattle) using standard open circuit
techniques. Subjects breathed through a valve (Rudolph) (94 mL
dead space), and a pneumotachometer was used for recording Vt
and minute ventilation (Ve). Expired air traversed a combined
samples from
tubing/mixing chamber volume of 6forL. Expiredandgascarbon
dioxide
the mixing chamber were analyzed oxygen
infrared analyzers, respectively. Data were
by zirconia oxide15andand
to calculate oxygen uptake (Vo2),
averaged every s used
dioxide output, and respiratory
expired ventilation (Ve), carbon
was calibrated before each session
exchange ratio. The system
with standard gases of known oxygen and carbon dioxide concen¬
trations. Heart rate was monitored electrocardiographically.
Submaximal Ve, Vt, and breathing rate (fR) were determined
as the mean of values recorded during the fourth minute of the
steady-state walk. Maximal values were defined as the average of
the two highest measurements during the final minute of exer¬
cise. Subjects were considered to have reached a true maximal
effort if they demonstrated subjective evidence of exhaustion
(unsteady gait, facial flushing, hyperpnea) and either (1) peak
heart rate >190 beats/min or (2) maximal respiratory exchange
ratio >1.00.8
Informed permission was obtained from the parents, and each
child provided assent for participation. This study was approved
review board of the Baystate Medical Center.
by the institutional
in
Changes ventilatory and anthropometric variables were
assessed in regard to time and gender by two-way analysis of
variance. Post hoc paired comparisons were performed by the
Neuman-Keuls test. Statistical significance was defined as
p<0.05.
Results
and height for boys and girls
Changes5 in weight
the years are presented in Table 1. Although
the boys were heavier and taller at all ages, no
significant gender differences were observed. Mean
values (SD) for maximal oxygen uptake (Vo2max) at
the initial testing session were 48.9 (7.2) and 47.7
(6.4) mL/kg/min for the boys and girls, respectively.
These are consistent with previously reported aver¬
for the childhood
over
pop¬
age values of aerobic fitness
ulation.9 All exercise tests conformed to criteria for
maximal effort.
Table
Tables 2 and 3 list physiologic variables for male
and female subjects at submaximal and maximal
exercise. No significant differences were observed by
time for Ve, Vt, and fR, and combined
gender over data
for these variables are presented in
longitudinal
Figures 1-3. The pattern of change for absolute
variables is similar at both submaximal and maximal
exercise intensities: a linear increase in Ve, curvilin¬
ear rise in Vt, and progressive decline in fR. The
average rise in Ve and Vt per year was 8.8 (1.9) and
0.20 (0.10) L, respectively. Maximal Ve increased
with age (A) according to the following equation:
VEmax=-ll.l + 8.46A.
When Ve and Vt were expressed relative to body
similar patterns at submaximal and maximal
exercise with time were again observed. Submaximal
Vt per kilogram did not change significantly over the
5 years, with an average value in the combined
of 21.8 (2.2) mL/kg. As a conse¬
gender group
in submaximal fR from 45 to 36
the
decline
quence,
breaths/min resulted in a progressive fall in Ve per
mass,
kilogram.
At
maximal exercise, Vt per kilogram was stable
the 5 years with a mean value of 29.8 (1.5)
mL/kg. Breathing rate declined from 64 to 57
breaths/min. A trend for VEmax per kilogram to
decrease was observed, but the change did not reach
statistical significance (p>0.05). However, a gender
difference was apparent in this trend, as a steady
decline in VEmax per kilogram across the years was
observed in female subjects, while values remained
stable in male subjects (Fig 4). Average combined
VEmax per kilogram was 1.83 (0.04) L/kg. Allometric
indicated that absolute VEmax changed rel¬
analysis
ative to body mass (M) and height (H) over the 5
years by
over
VEmax=0.38M92
VEmax=03.6H 2.50
The rise with age in absolute Ve at both maximal
and submaximal exercise lagged behind increases in
total body metabolic rate. Ve/Vo2 fell progressively
1.Weight and Height Changes With Age: Mean (SD) Values
Year
Weight, kg
Boys
Girls
Height, cm
Boys
Girls
(6.1)
35.4(11.1)
37.1
142
140
(4)
(9)
42.3 (7.4)
40.2 (14.0)
148
145
(5)
(10)
47.3 (9.2)
43.5 (14.7)
154
151
(6)
(10)
57.5(14.2)
57.3(18.8)
54.3 (12.6)
49.8(16.7)
161
159
(7)
(9)
328
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168
165
Clinical
(7)
(8)
Investigations
Table 2.Submaximal Physiologic Variables With Age: Mean
(SD) Values
Year
Ve, L/min
Boys
34.2 (5.0)
34.9(10.0)
36.0 (5.5)
36.6(12.5)
39.7 (9.2)
40.2 (17.6)
39.8 (9.6)
40.2(14.0)
40.8 (10.6)*
43.4 (16.2)*
0.93(0.11)
1.00(0.13)
0.86(0.13)
0.92 (0.09)
0.84(0.11)
0.91 (0.12)
0.74 (0.08)
0.81 (0.06)
0.71 (0.08)*
0.75 (0.06)*
0.84(0.10)
0.76(0.18)
0.89 (0.10)
0.85 (0.23)
1.00 (0.09)
0.90 (0.22)
1.08(0.14)
1.04 (0.32)
1.25 (0.17)*
1.19 (0.39)*
Boys
0.023 (0.002)
0.028 (0.003)
0.021 (0.002)
0.021 (0.002)
0.020 (0.001)
0.021 (0.003)
0.022 (0.002)
0.021 (0.002)
Boys
43(8)
47(10)
42(8)
44(11)
41(9)
43 (9)
38(5)
39(8)
34 (6)*
38 (9)*
31.45 (5.10)
32.28 (2.80)
28.61 (3.11)
30.90 (2.47)
28.27 (2.75)
27.74 (2.88)
30.18(1.89)
26.34 (2.66)*f
29.05 (2.34)*f
Girls
Ve,
L/kg/min
Boys
Girls
Vt, L
Boys
Girls
Vt,
L/kg
Girls
fR, b/min
Girls
0.021
0.021
(0.003)
(0.002)
Ve/Vo2
Boys
Girls
30.66
(3.85)
*p<0.05 for time for the 5 years.
fp<0.05 for gender for years 2 to 5.
during the study period in both sexes, except for
stable maximal values in the girls (Fig 5). At each
year, the value of Ve/Vo2 was significantly greater in
the female subjects, the only statistically significant
gender-related variable observed in this study.
Discussion
Unlike other links in the oxygen delivery chain,
such as cardiac output and muscle aerobic activity,
the components of ventilation (Ve, Vt, and fR) are
easily measured during exercise testing. Thus, bar¬
ring technical error, reported data such as that
in this study can be presumed to provide an
provided
accurate assessment of developmental changes in
ventilatory function during exercise. In addition,
observations can be expected to provide
longitudinal
a clearer picture of such changes compared with
cross-sectional investigations.
The findings in this study indicate that at a given
Table 3.Maximal Physiologic Variables With Age: Mean Values (SD)
Year
Ve, L/min
65.9 (8.0)
64.1 (11.9)
78.2 (9.3)
71.0(14.1)
85.5 (12.3)
76.3 (19.8)
94.4(13.1)
83.1 (18.0)
105.1 (16.3)*
95.3 (22.7)*
1.82 (0.35)
1.90 (0.32)
1.89 (0.27)
1.88 (0.43)
1.85 (0.31)
1.82 (0.34)
1.79 (0.27)
1.74 (0.28)
1.86 (0.31)
1.71 (0.38)
1.07(0.11)
1.27(0.13)
1.17(0.33)
1.37(0.17)
1.07 (0.25)
1.27 (0.33)
1.55(0.17)
1.41 (0.38)
1.95 (0.38)*
1.75 (0.53)*
Boys
0.029 (0.002)
0.030 (0.002)
0.030 (0.003)
0.029 (0.002)
0.029 (0.002)
0.029 (0.004)
0.029 (0.004)
0.028 (0.003)
0.034 (0.004)
0.031 (0.004)
Boys
65 (10)
63(8)
62(7)
63(10)
63(7)
(7)
61(7)
60(6)
57 (9)*
57 (4)*
37.15(3.54)
39.64 (2.26)
35.29(1.72)
39.22 (3.35)
34.44 (2.32)
37.98 (2.30)
35.90 (2.76)
39.50 (2.04)
34.05 (2.58)*1
39.37 (3.88)*f
Boys
Girls
Ve,
L/kg/min
Boys
Girls
Vt, L
Boys
Girls
Vt, L/kg
Girls
fR, b/min
Girls
Ve/Vo2
Boys
Girls
61
*p<0.05 for time for the 5 years.
fp<0.05 for gender for each of the 5 years.
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329
104+
96
88
80
72
Max
Max
Ve 64f
56
(L min-') 48
fR
(b min"1)
40
32
24
Submax
Submax
16"
8
0
Year
Figure 1.
Year
Changes in maximal and submaximal Ve with age.
level of treadmill work, Ve increases as the child
ages. This rise in not, however, simply related to
increase in
size. Vt increases in proportion to
body
the child grows, but the frequency of
load
body at
submaximal work
breathing a given
progres¬
As
a
declines.
result, submaximal Ve rises
sively
slower with age than would be expected for body
mass. This is also reflected in a steady fall in the Ve
mass as
response to a given submaximal metabolic rate (ie,
decline in (Ve/Vo2) with age. When the influence of
sex was examined, only the magnitude of the Ve/Vo2
was observed to be gender related, with the girls
value at all years. The
demonstrating a greater
effect
for
this
explantationis unknown. of gender on ventilatory
efficiency
Virtually the same patterns were observed at
maximal exercise. Vt per kilogram remained stable
while fR declined. The scaling exponent of 0.92 for
Ve relative to mass indicates that body mass rose
more rapidly than Ve during the 5-year study. At
maximal exercise, however, the fall the maximal Ve
Figure 3.
per kilogram was not statistically significant. Ve/Vo2
fell with advancing age only in the boys, with greater
values again evident in the girls.
These findings support those of previous studies
children's ventilatory responses to subdescribing
maximal exercise.1-6 Robinson2 reported ventilatory
responses to a treadmill walk at 5.6 km/h in groups of
rate declined
subjects ages 6 to 17overyears. Breathing while
Ve per
that age span
from 49 to 29/min
fell from 1.05 to 0.67 1 kg/min. Only small
kilogramwere
observed in Vt per kilogram (0.021 L
changes
at age 6 years to 0.025 L at age 17 years). Andersen
et al1 described a fall in breathing rate of 5 to 10/min
between the ages of 8 and 16 years when children
were cycling at 50% and 75% of maximal Vo2. The
decline in submaximal Ve/Vo2 with age observed in
the present study has also been described in crosssectional studies.1
Rutenfranz et al6 reported longitudinal findings in
children between ages 8 and 17 years. At the same
1.92
1.764
VT
(L)
1.60
1.44
1.28
1.12
.96
.80
.64
.48
VEmox
Submax
Changes in maximal and submaximal fR with age.
(LKg-'min-i)
2.00
1.96
1.92
1.88
1.841.80
1.76
1.72
1.68
1.64
Girls
.32f
.16
o-
2
3
Year
Year
Figure 4.
Figure 2.
Changes in maximal and submaximal Vt with age.
with age.
Changes in maximal Ve per kilogram in boys and girls
330
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Clinical
Investigations
Ve/Vq2
40-3938
37
36
353433
32
31
30
29
28
27
26
Max
Boys
Boys
Year
Figure 5.
exercise in
Changes in Ve/Vo2 at maximal
boys and girls according to age.
and submaximal
relative intensity (65 to 70% Vo2max), Ve increased
from 52.2 to 68.1 L/min over this age span in the
male subjects but changed little in the female sub¬
jects (47.8 and 47.6 L/min, respectively). Breathing
fell from 39 to 28 and 36 to 26 in the boys
frequency
and girls, respectively. Vt increased from 1.58 to
2.48 L in the boys and from 1.52 to 1.87 L in the
In this study, no influence of age on submaxi¬
girls.
mal Ve/Vo2 was observed.
Previous reports of changes in ventilatory findings
at maximal exercise in growing children have been
less consistent. Moreover, to what degree increases
in lung and body size are responsible for improve¬
ments in VEmax with age remains problematic.
Mercier et al3 found that VEmax scaled to the mass
exponent of 0.68 and height exponent of 2.06 in a
study of boys ages 10.5 to 15.5 years. Compared with
the present study, then, these data indicate that
maximal Ve increased significantly slower relative to
body mass as children became larger. Mercier et al3
described a close relationship between the develop¬
ment of maximal Vt and body mass (scaling expo¬
nent, 0.96). This supports the finding of a constant
Vt per kilogram with age in the present longitudinal
as well as the report of Rutenfranz et al6 that
study
maximal Vt during exercise is linearly related to lung
volume.
However, others have described stable values for
VEmax per kilogram across the childhood years.2-5 In
the study of Robinson,2 the 6- and 15-year-olds
demonstrated a mean value of 1.59 and 1.60 L/kg/
min, respectively. Morse et al5 could find no rela¬
of maximal Ve per kilogram to age in boys
tionship
whose ages ranged from 10 to 17 years. The longi¬
tudinal data from Rutenfranz et al6 describe a linear
relation of VEmax to stature in female subjects until
a height of 160 cm was reached. Above this
height,
values decreased. In male subjects, the relationship
between height and maximal ventilation remained
linear throughout the study.
As with submaximal exercise, Rutenfranz et al6
were unable to demonstrate a fall in Ve/Vo2 at
maximal effort as their subjects aged. This is a
contradiction to findings in the present study as well
as those of Astrand4 and Andersen et al1 which
indicate a decline in maximal Ve/Vo2 with increas¬
ing age in children.
The explanation for these patterns.an increasing
reliance on Vt for maintenance of exercise ventila¬
tion and the improvements in ventilatory "efficiency"
(decline in Ve/Vo2).in the growing child is un¬
clear. There is some evidence that younger children
possess a greater central ventilatory neural drive and
a lower carbon dioxide set point, resulting in greater
rates for a given metabolic demand.10-12
ventilatory
Others have considered such age-dependent pat¬
terns to reflect variations in ventilatory mechanics.13
Work of ventilation, for instance, is strongly influ¬
enced by the balance of lung compliance and airway
resistance. Since these factors may not develop in
parallel during childhood, a change in their relation¬
ship might alter the ratio of Vt and respiratory rate
that would provide the most "economical" means of
accomplishing Ve during exercise.14
Level of sexual development was not assessed in
this study. As indicated by the brief parent-com¬
pleted
questionnaire, many subjects were certainly
in the early stages of puberty before the completion
of the study. However, no growth spurt was observed
in either height or weight. Also, with the exception of
a late acceleration of Vt in the boys, no clear-cut
alterations in patterns of changes in ventilation, Vt,
fR and ventilatory equivalent were observed in the
latter years of the study. This suggests that as far as
the children had progressed in sexual development,
puberty had no significant impact on ventilatory
responses to exercise.
As ventilation plays a key role in the oxygen
delivery chain, it is of interest to compare the
patterns observed during growth in this longitudinal
with those of Vo2max and cardiac output. At
study
submaximal treadmill exercise, the energy demands
relative to body size progressively decrease with age
in children. This decline in Vo2 per kilogram mimics
that of Ve per kilogram, although, as noted above,
Ve/Vo2 during submaximal exercise declines with
age during childhood. At maximal exercise, Vo2 per
kilogram remains relatively stable during childhood
in boys but gradually declines in girls. This pattern
was duplicated in the current study.
Cardiac responses to exercise, particularly at high
intensities, are often difficult to study. It is of interest
to compare such changes with those of ventilation,
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331
however, since both are characterized by a minute
volume (cardiac output, Ve) that is determined by a
size-dependent volume (stroke volume, AtVt)a and a
size-independent rate the(heart rate, fR).are similar:givenas
submaximal exercise,
responses
the child ages, the volume variable increases in
to body size, while the rate variable de¬
parallel
creases. As a consequence, the minute volume vari¬
able increases in absolute terms but declines relative
to body mass. At maximal exercise, however, venti¬
latory and cardiac patterns may differ, since maximal
heart rate remains constant across ages during child¬
hood, while the maximal fR decreases.
In summary, this 5-year longitudinal descriptive
study provides a picture of ventilatory responses to
exercise in children that generally supports that
created by previous cross-sectional studies. Vt is
to body size during growth, while fR
closely linked
This results in a fall in Ve per
declines.
gradually at submaximal
exercise. Such a decline has
kilogram
also been described by others at maximal exercise,
but in the present study, the decrease in Ve per
maximal exercise was not statistically
kilogram atChildren
demonstrate a greater ventila¬
significant.
tory efficiency during exercise as they grow, with a
progressive decline in submaximal and.at least in
boys.maximal Ve/Vo2.
1 Andersen
mance
sponses
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Clinical
Investigations