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* From the Service de pneumologie et d’allergologie pédiatriques, Hôpital Necker-Enfants Malades, Paris, France.
Correspondence to: Chantal Karila, MD, Service de pneumologie et d’allergologie pédiatriques, Hôpital Necker-Enfants Malades, Paris, France
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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O2] plateau, maximal
respiratory exchange ratio > 1.1). Design: Prospective clinical study.
Setting: Pediatric exercise testing laboratory.
Subjects: Ninety-two children aged 5 to 17 years with various cardiac and respiratory diseases (33 with asthma, 11 with bronchopulmonary dysplasia, 6 with cystic fibrosis, 10 with congenital heart disease, and 32 miscellaneous).
Interventions: Individualized maximal
incremental exercise testing. The increase in workload was adapted to
the individual and was calculated from predicted maximal oxygen uptake
(O2max) for each child. The test lasted
10 to 12 min.
Results: The exercise test was well
tolerated by all children and was maximal in all but seven patients. A
total of 65.7% of children reached the predicted
O2max and 68.4% satisfied the criteria
for a O2 plateau at peak exercise. The
predicted HRmax was achieved in all but two children. The mean maximal
respiratory exchange ratio was 1.06.
Conclusion: The
individualized protocol for increasing workload, based on
O2 rather than power, was well tolerated
by children. In our view, the best two criteria for assessing the
maximality of the tests were clinical exhaustion and HRmax, especially
if the O2 plateau was not reached. These
results suggest that individualized protocols could be used instead of
standardized tests for exercise testing in children.
Key Words: children • exercise testing • individualized workload
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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The methodology of exercise tests has largely been described, and there
are many protocols for use in adults. Maximum oxygen uptake
(O2max) is widely recognized
to be the best single index of aerobic fitness. Its measurement
requires the patient to achieve maximal exercise.1
However, the criteria for maximal exercise described in adults are
rarely satisfied in children. No criterion specific for children has
been precisely described. Results obtained with small numbers of
children2
3
have shown that various ventilation and
cardiac variables (such as ventilation, respiratory exchange ratio
[RER], respiratory rate, oxygen pulse, heart rate [HR]) measured
during exercise tests have maximal values in children that are very
different from those in adults.
An individualized methodologic approach to exercise testing has been used in adult patients with pulmonary diseases.4 In this case, the maximum workload and the increase in load during the test are adapted to each individual. Could this individualized approach be extended to children? Would it be tolerated by children?
This prospective study was carried out in our pediatric pulmonary function laboratory from February 1997 to February 1999, and focused on the methodology used for the tests performed. Its principal aim was to investigate the feasibility of an individualized methodology for exercise testing in ill children. Moreover, we investigated whether this approach makes it possible to satisfy the criteria for maximal exercise generally required in adults.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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O2]) being a
reproducible, quantifiable index).
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Materials
The exercise tests were performed on a cycle ergometer with an
electromagnetic braking (Lode BV; Groningen, The Netherlands) or a
motor-driven treadmill (Marquette Electronics; Milwaukee, WI). The
choice of ergometer depended on the height of the child (minimum height
of 125 cm for the cycle), the indication for the exercise test, and, in
some cases, the preferences of the child. The cycle ergometer was used
most frequently because it facilitated an increase in load and the
monitoring of clinical parameters with a 12-lead ECG (Marquette Max-1;
Marquette Electronics), oxygen saturation by pulse oximetry (Ohmeda
3700; Ohmeda; Louisville, CO), and BP.
Respiratory exchange was measured over three respiratory cycles, using a mixing chamber with a variable volume (Gould 9000; Sensormedics; Dayton, OH). Children wore a nose clip and breathed through a mouthpiece attached to a low-resistance valve (large 2700 valve; Hans Rudolph; Kansas City, MO) with 100 mL of dead space. On the expiratory side, this apparatus was connected via large tubing (internal diameter of 3.5 cm) to a pneumotachograph located at the entrance of the mixing chamber, for flow measurement. Gas samples were taken from the mixing chamber over three respiratory cycles and were analyzed using an infrared analyzer for carbon dioxide and a paramagnetic analyzer for oxygen.
Mean values for O2, carbon
dioxide output, RER, and minute ventilation were calculated over 20-s
intervals. The system was calibrated prior to each individual test
using standard gas mixtures of known oxygen and carbon dioxide
content.
Protocol
This study was carried out in the Pulmonary Function Laboratory
of the Pediatric Pneumology Department of Necker Enfants-Malades
Hospital (Paris, France). The same protocol was used for all 92
patients. A pediatric pulmonologist and an experienced technician
observed the children during the exercise test and watched for
excessive stress (eg, severe wheezing, chest pain, lack of
coordination) or adverse signs (eg, ECG abnormalities,
falling BP, large decrease in oxygen saturation). Resuscitation
equipment and a defibrillator were always available during tests.
A 12-lead ECG and spirometry were first carried out at rest, making it possible to calculate the predicted maximum ventilation of the child,5 as FEV1 x 35. The test procedure was then explained to the child.
Individualized Protocol for Workload Increase
The exercise test was a progressive incremental
test.5
The increase in workload was individualized for
each child, as previously described for adults.4
Individualization was based on the predicted
O2max of each child, converted
into maximum watts (Wmax), to make it easier to increase the load (in
watts) during the test.
Basal O2 was calculated as
(height in centimeters x 2) - 100, and predicted
O2max was calculated according
to the Wasserman norms6
as a function of sex, weight, and
the age of the child. We then calculated the difference between
O2max and basal
O2. Wmax corresponding to this
difference was calculated as follows:
Wmax = (predicted
O2max - basal
O2)/10.3,
where 10.3 mL of O2/min/W is the equivalent in oxygen of each watt.7 8 So, we achieved maximal power to reach Wmax.
The total duration of the test was 10 to 12 min. The test involved four consecutive periods: (1) a 3-min to 5-min rest period; (2) a 3-min period of warm-up against a workload corresponding to 20% of the calculated Wmax; and (3) an 8-min exercise period. The remaining 80% of the workload was divided by eight to define the increase in workload for each 1-min stage (Fig 1 ). Based on clinical evaluation and the experience of the physician, the workload was increased more slowly for the last few minutes in some children to prevent muscle limitation, which would have made it necessary to stop the exercise prematurely before maximal exercise was achieved. A recovery period (4), with a workload equivalent to that used for the warm-up period, took at least 2 min, to prevent fainting and to accelerate lactate removal. Finally, there were 3 min of passive recovery.
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Throughout the exercise and recovery periods, continuous ECG monitoring was carried out. BP and oxygen saturation were determined at each stage. We allowed the parents to be present throughout the exercise test. They were very curious and wanted to understand the apparatus and the meaning of the measures and results. We asked them to help us to encourage their child to achieve exhaustion during the final stages.
The following criteria for maximal exercise were those used in
progressive incremental cardiopulmonary exercise testing in
adults6
9
10
: (1) exhaustion of the subject or inability
to maintain the required pedaling speed (60 revolutions per minute)
despite strong verbal encouragement; (2)
O2 plateau
reached1
8
11
(the
O2 plateau is considered to
have been reached if the final increase in
O2 does not exceed 2 mL/kg/min
for an increase in work of 5 to 10%12
; peak
O2 is the highest
O2 elicited during the
exercise test, if a O2 plateau
is not observed; we considered the predicted
O2max to have been reached if
the O2max value recorded was
85% of the predicted value); (3) predicted maximum HR (HRmax)
achieved (210 - [0.65 x age]) ± 10%) [we considered the
predicted HRmax to have been achieved if the HR recorded was 90%
of the predicted value]; and (4) maximal RER (RERmax) of
> 11
(in adults, the RERmax must be > 1.1. Three of
these criteria must be satisfied for maximal exercise to be considered
to have been achieved).
We used Student’s t test to compare
O2max values between
boys and girls. The 
2 test was used to compare
the O2 values
obtained from prepubescent and pubescent children; RERmax values in
those who had and had not achieved a
O2 plateau, and
between children who had and had not reached HRmax; and HRmax values in
those who had and had not achieved a
O2 plateau.
Statistical significance was defined as p < 0.05.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Predicted O2max was achieved
in 65.7% of patients (62 of 92 tests). If we exclude the seven
children for whom the test was not maximal (lack of motivation or
dyspnea), 73% of the tests resulted in the predicted
O2max being achieved. The mean
O2max (± SD) measured was
38.1 ± 10.7 mL/kg/min for a mean workload of 127.7 ± 67.7
W. The mean O2max achieved by
the girls was 32.2 ± 7.7 mL/kg/min, whereas that achieved by the
boys was 41.3 ± 11.1 mL/kg/min (28.4% difference, p < 0.001).
Analysis of the Criteria for a Maximal Exercise Test
In all but the seven tests cited above, complete exhaustion of the
subject was achieved. For another nine tests, it appeared that an
additional increment in workload would have been supported by the child
as clinical exhaustion was not clear. However, for six of the nine
tests, a O2max value at least
90% of the predicted value was achieved.
A O2 plateau was reached in 63
of the 92 tests (68.4%), and peak
O2 was recorded for the other
29 tests. Sixty-two percent of the children (18 of 29 subjects) for
whom peak O2 was recorded were
prepubescent, vs 58.7% (37 of 63 subjects) of those for whom
O2 reached a plateau (not
significant, p = 0.76).
Two children with congenital heart disease were receiving negative
chronotropic treatment: amiodarone (n = 1) and digoxin (n = 1). In
68 of the other 90 children (75.5%), the predicted HRmax was reached,
with a mean value of 191 ± 12.3 beats/min. The 22 children who did
not achieve the predicted HRmax included the 7 patients with nonmaximal
test results. A HRmax of > 180 beats/min was recorded in 69 of 90
children (76.6%). Twenty-eight children had a HRmax of > 200
beats/min (35%). A significant correlation was found between
achievement of HRmax and a O2
plateau (p = 0.02).
The mean RERmax (±SD) was 1.06 ± 0.11 (range, 0.9 to 1.44). This
variable was not a decisive criterion for maximal exercise. No
significant correlation was found between a RERmax of > 1 and a
O2 plateau being reached (not
significant, p = 0.27) or between a RERmax of > 1 and a HRmax
90% of the predicted value (not significant, p = 0.27).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Cardiopulmonary exercise testing with an individualized protocol for increasing workload was feasible in children aged 5 to 17 years, regardless of the ergometer used. The individualized increase in the workload of the exercise was largely responsible for the high level of acceptability of the test to children. In our experience, and as suggested by others,5 13 a nonindividualized increase in work, with large increments, may lead to the premature cessation of exercise before cardiac or respiratory limits are reached, due to exhaustion of the muscles of the lower limbs, especially the quadriceps, particularly if the test is carried out with a cycle ergometer. The game-like nature of the apparatus and the challenge of maintaining the speed of pedaling contributed to the acceptability of the protocol. The duration of exercise (10 to 12 min) is sufficiently short not to discourage the child.
Clinical tolerance was good. In the studied population, there were no deleterious events. Cardiac complications (repolarization defects, arrhythmias) are rare in children not suffering from heart disease, and there were only nine children with heart disease in the studied population. Respecting the absolute contraindications (Table 2 ) for exercise tests limited the risk of cardiovascular problems. These contraindications are rare in children. Fainting, generally a frequent complication, was prevented by the active recovery against a workload equivalent to that used during the warm-up (20% of the maximum workload achieved). Dyspnea was not considered a side effect of exercise, but as an indication of poor adaptation to exercise. At the end or after the exercise test, some asthmatic children had an exercise-induced bronchospasm. This was considered undesirable and led us to modify treatment and to propose a training program to reduce exercise asthma.14
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O2max and
the ventilatory threshold are the two parameters currently used for
aerobic aptitude assessment.16
The progressive incremental test proposed herein, with
individualization of the increase in workload, is safe and feasible,
making it possible to obtain both maximal and submaximal data in a
single test. The value of maximal cardiopulmonary exercise tests lies
in the definition of these tests itself, "a test making possible an
integrated exploration of lung, cardiac and muscular functions... in
conditions in which the body makes use of its
reserves."5
17
The achievement of a maximum value for
O2, normally as a plateau,
demonstrates the integrated response of all the systems involved in
exercise. This test can be used to detect abnormalities that are
undetectable during rest or less intensive activities. For example, in
bronchopulmonary dysplasia, the correlation between resting function
and exercise tolerance has been shown to be weak18
19
; in
some children, we observed hypoxemia only at peak
O2. Moreover, in our
population, it was necessary to achieve maximal exercise for several
reasons: (1) to assess objectively (in the safe conditions of a
laboratory test) the child’s possibilities in terms of physical
activities (and the limits authorized) [this was recently well
described by McManus and Leung20
for congenital heart
diseases]; (2) to reassure parents of a child with a chronic disease
(such as cystic fibrosis or heart disease) by showing them that the
child can carry out maximal exercise without problems or negative
effects on the disease; and (3) to achieve
O2max, a quantifiable index
(to follow, with repetition of the tests, the functional handicap
and progression of the chronic disease; to help in
prognosis as shown by Nixon et al21
for cystic fibrosis;
to measure and express the ventilatory threshold [as a percent of
O2max]). A precondition of
the determination of ventilatory threshold is the achievement of
O2max.22
The HR
measured at the ventilatory threshold level was used to initiate
individualized readaptation in children with cystic
fibrosis23
24
25
and in children with severe asthma who
suffered dyspnea when running or practicing other endurance activities.
The rate of increase in work affects the value of
O2max achieved, with protocols
involving large increments resulting in lower values of
O2max due to a lack of muscle
power.22
Similarly, a low rate of increase in workload
prolongs the duration of the test, making it a test of endurance, with
lower values of O2max
recorded. The duration of the test used herein made it possible to
approach O2max in children.
The optimal duration recommended, as stated by Buchfuhrer et
al,22
is 10 ± 2 min, to make it possible for the
maximum O2max to be achieved.
This O2max is probably that
which approaches most closely the original definition of
O2max,17
enabling
the body to make use of its reserves to increase its major vital
functions to their maximum.
In the studied ill children, the
O2max predicted at the start
of exercise was achieved in 65.7% of the tests. The mean
O2max recorded differed
between the sexes,26
with a mean value of 32.2 ± 7.7
for girls and 41.3 ± 11.1 for boys. These values are lower than
those for healthy children of the same age, with a "symptom-limited
O2max" being reached, lower
than the predicted value in many of these children. This limitation was
essentially respiratory in nature.
This protocol favors maximization of
O2max rather than power. The
relationship between O2 and
power during exercise tests in healthy adults was determined by Hansen
et al.8
This relationship was used in the individualized
protocol (10.3 mL of O2/W/min). If a test is
maximal, as shown by the O2max
achieved, cardiac and respiratory adaptations, muscular aerobic
oxidative potential, and muscular contractility come into
play.27
Costill et al28
demonstrated in
athletes the dissociation of muscular power, the role of the
contractile capacity of muscle, and
O2, which depends on muscular
aerobic potential. Healthy children have a high
O2max (mean value of about 50
mL/kg/min), but their muscular power is poorly
developed.11
Thus, protocols in children should favor the
maximization of O2max rather
than workload.
The relationship between O2
and power has been described in patients with respiratory
diseases6
and in normal children.3
However,
in these two populations, the Wmax obtained for a given
O2max is usually lower than
that calculated using the
O2/power relationship because
the ventilatory yield is low and much of the oxygen consumed is used by
the muscles of the respiratory system. This relationship between
O2 and power, often deficient
in children who are also ill, accounts for the changes in workload that
we made in some cases during the final increments, if we estimated that
the O2 achieved was likely to
be higher than that predicted for the power developed.
Analysis of the criteria for maximality included exhaustion of the
subject, O2
plateau, HRmax, and RERmax. The motivation of the child to
reach exhaustion was in most cases evident (profuse sweating, inability
to maintain the desired exercise intensity, dyspnea, unsteady gait).
The explanation of the test before its performance was important. The
child knew that the exercise to be supported would be maximal and we
insisted on this in the last stages, which were particularly difficult.
If exhaustion did not appear to us to be clinically clear, we kept the
child at the same workload for a few extra seconds, or simply increased
the workload again, but to a lesser extent than for the previous
increments, to check that the variables monitored (ventilation and HR)
and O2 did not
increase. Our experience led us to seek the exhaustion of the subject.
This is particularly important in children, because even children with
chronic diseases are more physically active than adults. The level of
activity or physical training and the
O2max measured are
correlated in children,7
29
30
and physical activity
should lead to a higher
O2max being reached
in ill children than in ill adults. Clearly, the values obtained in an
exercise test depend on the level of exercise, and it is extremely
important to encourage ill children as strongly as healthy children to
prevent bias in the interpretation of results.15
The
subjective criteria for maximal exercise tests, including evaluation of
the clinical exhaustion of the subject, depend, however, on the
experience of the technician in the performance of these
tests.31
There are many criteria for the achievement of a
O2 plateau. The criterion used
herein was an increase in O2
of no more than 2 mL/kg/min for an increase in work of 5 to
10%.12
This criterion appeared to us to be the most
suitable for our system of measurement and for an increase in workload
every minute. A O2 plateau was
achieved in 68.4% of all children (63 of 92 subjects), and in 58.7%
of the prepubescent children (37 of 63, not significant). In published
studies, only about a third of prepubescent children have been reported
to achieve a O2 plateau; for
others, a peak O2 is
reported.2
31
32
The individualized protocol thus makes it
possible to achieve a O2
plateau in a higher proportion of children (two of three subjects, in
our experience) than with other protocols, regardless of the state of
the child with respect to puberty.
The achievement or lack of achievement of a
O2 plateau is extremely
variable for an individual subject, depending on the averaging of
respiratory exchanges and the increase in workload.33
Several elements probably contributed to the high frequency with which
O2 plateaus were achieved in
these exercise tests: (1) the choice of system for monitoring gaseous
exchange, using a mixing chamber; (2) the large number of samples for
measured O232
(herein, respiratory exchanges were averaged over a long interval
[20 s], including several respiratory cycles); and (3) the
discontinuous increase in workload that, unlike continuous increases in
workload, favors the observation of a
O2 plateau.32
34
In ill children, is it of value to obtain
O2 values over several seconds
or cycles, as is now possible using apparatus for measuring gaseous
exchange from cycle to cycle? Armstrong et al2
and
Rowland35
have demonstrated that in children, a peak
O2 taken over several seconds
is an index of maximal exercise, even in the absence of a plateau. This
individualized protocol thus made it possible to achieve a
O2 plateau in most of the
children, whatever the O2max
achieved and the age of the child.
HRmax (except in children with failing chronotropic function, the
number of which was small in this study) was achieved in almost all of
our patients. The mean HRmax was > 190 beats/min, and HRmax values of
205 to 215 beats/min were frequently recorded. HRmax determination is
essential. It is therefore important to encourage children to perform
"supermaximal" tests, which are without risk, except in rare cases
of children presenting with ischemic complications or cardiac rhythm
problems like those encountered in adults. According to Armstrong et
al,2
the achievement of HRmax is one of the most reliable
criteria in children; our results are consistent with this hypothesis,
with a strong correlation between achievement of HRmax and of a
O2 plateau.
Armstrong et al2
also found that RERmax was a reliable
criterion for maximal exercise. In adults, the criterion used is a
RERmax > 1.1, and this is usually the best criterion for maximal
exercise. In our experiments, RERmax was one of the least useful
criteria for the determination of maximal exercise because nothing
during the test predicted whether the RERmax of the child would be 0.9
or 1.1. The mean RERmax recorded herein (1.06) is similar to that
generally observed in children.3
26
We found no
correlation between a RERmax >1 and achievement of a
O2 plateau or a HRmax of 90%
the predicted value.
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Conclusion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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O2 over power and the optimum
duration of the test (10 to 12 min). We found that the two best
criteria for confirming that exercise was maximal (especially if a
O2 plateau was not reached)
were clinical exhaustion and HRmax (except in children with cardiac
disease). The achievement of a
O2max plateau is also a
criterion often found in this type of protocol. The use of
preestablished protocols does not appear to us to be desirable in
children. This individualized methodology should make it possible to
expand the use of cardiopulmonary exercise tests in pediatrics, both
for diagnosis and treatment.16
The indications for such
tests are diverse, and include assessment of dyspnea, discrimination of
simple breathlessness in prepubescent children, poor physical
conditioning, and true pathologic limitation, in which examinations
at rest are insufficient. The follow-up of chronic diseases
(eg, cystic fibrosis, interstitial lung diseases) and the
evaluation of treatment (eg, efficacy of a long-acting
bronchodilator to prevent exercise-induced bronchospasm) are also
frequent indications in pediatric patients.
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Footnotes |
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O2 = oxygen uptake;
O2max = maximal oxygen uptake;
Wmax = maximum watts Received for publication July 7, 2000. Accepted for publication February 21, 2001.
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References |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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O2 during cycle and treadmill exercise in severe chronic obstructive pulmonary disease. Thorax 50,829-833[Abstract]
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