35 l
Respiration Physiology (1986) 65, 351-364 Elsevier
BREATHING PATTERN AND OCCLUSION PRESSURE DURING EXERCISE IN PRE- AND PERIPUBERTAL SWIMMERS
M. RAMONATXO l, J. MERCIER 1, R. EL-FASSI-BEN ABDALLAH 2, P. VAGO 1 and Ch. PRI~FAUT 1 1Service d'Exploration de la Fonction Respiratoire, H6pital Aiguelongue, avenue du Major Flandre, 34059, Montpellier Cedex, France, and 2Laboratoire de Physiologie, Facult~ de M~decine, Rabat, Morocco
Abstract. In two groups of young swimmers (prepubertal stage: group A; peripubertal stage: group B), the ventilatory response to graded exercise work with a cycle ergometer was studied. Ventilatory variables (ventilation, ~'E, tidal volume, VT, respiratory frequency, f, ratio between inspiratory period and total breath duration, TI/TTOT, and mean inspiratory flow, VT/TI) as well as mouth occlusion pressure measured at 100 msec (Po.l), effective impedance of the respiratory system (Po.I/VT/TO, inspiratory power for breathing (V¢) and 02 uptake ('¢o2) were measured during the third minute of each work load. At the same level of exercise both groups showed identical values of VT/TI, but ~'E was higher in group A individuals. This resulted from higher values of respiratory frequency with higher TI/TToT ratios. P0.~, Po.~/(VT/T0 and '0¢ were also much higher during work load in group A than in peripubertal subjects. When the above results were related to the same percentage of ",/o2max, Po.~, $~¢,respiratory frequency and duty cycle did not differ within both groups. However, '¢E, VT and VT/TI were lower in group A subjects with a higher P0.1/(VT/T0 ratio. Further corrections of VT, VT/TI and Po.~/(VT/TO ratios by body weight cancelled all these differences. In conclusion, our results strongly suggest that biometric factors only determined interindividual differences in ventilatory response to exercise in prepubertal and peripubertal swimmers. Breathing pattern Exercise
Growth Human
Mouth occlusion pressure Swimming
Studies concerning the adaptation of ventilatory control to muscular exercise during the growth period have been limited, so far, to measuring ventilation as an indicator of the activity of respiratory centers, (Gadhoke et al., 1969; Davies et al., 1972). However, ventilation is the result, on the one hand, of central control, and on the other, of the impedance of the respiratory system. As the stage of pubertal growth is accompanied by modifications in the mechanical properties of the respiratory system (Gaultier and Girard, 1980), ventilation is perhaps not a faithful image of the central activity. It has Accepted for publication 19 May 1986 0034-5687/86/$03.50
© 1986 Elsevier Science Publishers B.V. (Biomedical Division)
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been demonstrated, on the other hand, by Siafakas et al. (1979), Sergysels et al. (1981), and Hesser and Lind (1983), that the occlusion pressure and its relationship to inspiratory flow were good indicators of this control and of the 'effective impedance' of the respiratory system during muscular exercise. Thus we compared these latter parameters as well as the ventilatory variables in two groups of children, one at a prepubertal stage and the other at a peripubertal stage, during maximal exercise in order to find out: (1) whether there were any differences in ventilatory control between the two groups; and (2) in the case of possible differences whether they were the result of mechanical properties or of different biometric factors.
Material and Methods
Seventeen young trained swimmers (7 girls, 10 boys) participated in this study. They were divided into two groups, A and B. Group A was composed of 8 prepubertal subjects (2 girls, 6 boys), group B of 9 peripubertal subjects (5 girls, 4 boys). Mean values of their physical characteristics are shown in table 1. Prepubertal or peripubertal stages were determined according to the tests of Tanner (1974), by examination of pubic and penile hair and testicular developments for males and by examination of the bosom in females. All children were submitted to an endurance training program for an average of 5 h a week. They had been familiarized with the equipment and experimental procedures, for at least one year, in order to control their physical aptitude. The nature of the study was explained and informed consent was obtained from the subjects and their parents. Two or three days before the experiment, they performed an incremental-load exercise so that their maximal oxygen uptake could be determined. Subjects.
All tests took place in the morning. During the test, the subjects breathed through a low-resistance breathing valve (dead space of 50 ml) and large caliber tubing (i.d. 3.5 cm), into a 5-L mixing chamber. Inspiratory airflow was measured with a Fleisch No. 3 pneumotachograph and a Validyne MP 45 pressure transducer with a measuring range of + 2 cm H 2 0 . The pneumotachograph was placed on the inspiratory tubing in order to avoid problems due to water vapor. The flow signals were electrically integrated to give tidal volume. Oxygen uptake (Vo2) was calculated after analysing fractions of expired 02 and CO2 (FEo2 and FEco2) in the mixing chamber, with a Beckman OM 11 0 2 analyser and a Cosma Rubis 3000 CO 2 analyser. Every analyser was calibrated before and after each test according to standard gases. Ventilatory measurements.
The occlusion was realized with a silent electromagnetic operated valve. This was performed during expiration until the first 150 msec of the occluded inspiration. The subjects could see neither the occlusion valve nor the operator and therefore were unable to anticipate airway occlusion. Mouth Occlusion pressure and breathing pattern.
BREATHING DURING EXERCISE IN SWIMMERS
353
pressure was measured using a Validyne electromanometer ( + 35 cm H:O ). All signals were displayed on a multichannel UV Schlumberger recorder with a paper speed of 100 mm/sec for measurement of Po.~. From the flow signal the following variables were calculated: tidal volume (VT), breathing frequency (f), inspiratory and expiratory time (TI and TE), total breath duration (TTOT) and the ratios VT/TI and TI/TTOT. From the measure of Po.~ we derived the ratio Po.1/(VT/TI) •
Inspiratorypowerfor breathing.
If we assume that pressure developed by the respiratory muscles increases linearly during inspiration, we can measure the mean inspiratory pressure Pl which is equal to 0.5 x (Po.l x 10) × TI. From this value and those of VT/TI and Tt/TTOT we derived the inspiratory power for breathing ~¢, equal to PI × VT/TI X TI/TTOT.
Exercise protocol. Maximal exercise tests were performed in the sitting position on an electronically braked cycle ergometer (EPC 7701 Gauthier). The electrocardiogram was continuously monitored with a cardioscope. Heart rate (HR, min-1) was measured from 5 recorded ventricular complexes at the end of each step of work load. After a 10 min rest period, each subject performed an incremental-load exercise (30 W every 3 min) until exhaustion, with an average pedalling rate of 60 rpm. At this step, the subject stopped pedalling but continued to breathe through the mouth-piece for 5 min. The selected starting load was at an average of 40-50~o of maximal aerobic capacity determined two or three days before. For each work load, measurements were taken during the third minute. Four occlusion pressures were recorded during this period: their mean value was used to characterize Po.1. The different values of ventilatory variables which made it possible to determine the breathing pattern at each step of the work load were the mean values calculated for ten cycles during the third minute. The oxygen uptake was measured between 2.5 and 3 min.
Expression of results. The results were In'st expressed in relation to the work load. However, as the prepubertal subjects performed a comparatively more difficult exercise than the peripubertal ones, the ventilatory variables were also related to the percentage of Vo:max of the individuals. Furthermore, in order to take into account the differences in body weight between the two groups, VE was expressed as ml/kg of body weight°75 (Dejours, 1975), and VT, and VT/TI divided by weight. In group B, which was composed of children of both sexes, we also compared the breathing pattern and occlusion pressure of the 4 boys and 5 girls at different stages of work load levels.
Statistical analysis. Data for each group were expressed as mean + SD. Differences in means were tested for statistical significance by a Newman-Keuls multiple range test with unequal sample sizes (Zar, 1974, p. 155). Differences in slopes (a) and ordinates (b) of the regression lines obtained in the two groups of subjects were tested using the Student's test (Zar, 1974, p. 228).
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Regression analysis was carried out for first and second polynomials by the method of least squares. An F-test was carried out to see whether the regression was linear or parabolic.
Results P H Y S I C A L F I T N E S S IN T H E 2 G R O U P S
Table 1 summarizes the different mean values of maximal work, maximal heart rate (H.R.) and maximal oxygen uptake (Vo2max) in the two groups. The different values of ~'o2max .in LSTPD" m i n - 1 were significantly higher in group B (P < 0.001), but the means of Vo2max in ml. min- ~ • kg- 1 did not differ significantly between the two groups. Figure 1 shows the values of'¢o2 in L. min - ~ (mean + SD) plotted against the TABLE 1 Mean values of physical characteristics and maximal cardiorespiratory variables of the two groups of subjects, A and B, Values are m e a n s + SD. Group
A (n=8) B (n=9)
Age (yr)
11.4 ±0.6 14.5 ±1.3
Height (cm)
148 ±5.9 167.5 ±5.2
~/02
Weight (kg)
37.7 ±7.3 54 ±4.8
Maximal work (W)
138.7 ±15.5 196.7 ±21.8
H.R.max (min- l )
197 ±6 191 ±7
~'o2max LSTPD
mlSTPD
rain
min. kg
1.84 ±0.17 2.67 ±0.36
49.9 ±8,1 49,3 ±6.4
( LSTPO.min-1 I
group A 2.0"
NS
group B
1,5"
NS 1.0"
60
90
20 POWER
150 (watts)
Fig. 1. Mean values + SD of oxygen uptake ('¢o:, LSTPD" m i n - ~) during incremental exercise in the two groups of subjects, A and B. For 60, 90, and 120 W: group A, n = 8; group B, n = 9. For 150 W: group A, n = 5; group B, n = 9. *P < 0.05; **P < 0.01 ; ***P < 0.001 ; NS: not significant.
355
BREATHING DURING EXERCISE IN SWIMMERS
TABLE 2 Comparison of the mean values of Po.1, VT/T1 and TI/TToT between the 5 girls and the 4 boys of group B during incremental exercise. Power
Po.~ (cm H20)
Girls Boys
VT/T~
Girls
(L" sec z) Boys
VI/TTOT
Girls Boys
60W
90W
120W
150W
180W
5.1 + 1.3 3.6 -+ 1.6
7.6 -+ 1.9 7.1 + 0.7
9.6 + 1.7 9.3 -+0.7
13.1 -+2.0 12.3 -+2.0
17.2 -+0.9 16.2 + 1.2
1.15 +0.11 1.08 -+0.14
1.40 +0.16 1.42 -+0.14
1.64 -+0.15 1.64 -+0.10
2.00 -+0.15 2.04 -+0.28
2.49 +0.42 2.45 -+0.27
0.42 + 0.04 0.43 _+0.05
0.45 + 0.03 0.45 + 0.02
0.45 _+0.05 0.46 + 0.02
0.48 + 0.03 0.48 _+0.05
0.51 + 0.05 0.49 + 0.03
w o r k load. F o r the different w o r k l o a d s (60, 90 a n d 120 W), the m e a n Vo2 was identical in the two groups. Only at 150 W was the difference significant (P < 0.05).
COMPARISON OF THE BREATHING PATTERN AND THE OCCLUSION PRES SURE BETWEEN THE GIRLS AND BOYS OF GROUP B Table 2 shows that no significant difference exists in the VT/TI, the TI/TToT and the Po.1 at any w o r k l o a d level between the boys and girls o f this group.
BREATHING PATTERN, OCCLUSION PRESSURE AND INSPIRATORY POWER FOR BREATHING IN THE TWO GROUPS OF SUBJECTS
As a power function Breathing pattern. M e a n values o f VE, VT/TI, f a n d TI/TTOT during incremental load exercise for the two groups are r e p o r t e d in fig. 2. All p a r a m e t e r s increased linearly with the load. Average values o f VE were slightly but significantly higher in group A than in group B at two w o r k loads, 120 W (P < 0.001) and 150 W (P < 0.05). This resulted from less increment in respiratory frequency with w o r k in group B. Such discrepancies between changes in ventilatory timing were a s s o c i a t e d with modifications in the duty cycle (TI/TTOT) which was lower in group B than in group A at steps o f 60, 90 and 120 W. VT values were never significantly different.
356
M. RAMONATXO et al. VE
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Occlusion pressure (PO,I) and ‘effective inspiratory impedance’ of the respiratory system (P,,,/(I/TITr)). Mean values ofP,, and P,,, /(VT/TI) are shown in fig. 2. The occlusion
pressure increased linearly with the load. At every work load, children at prepubertal stage showed much higher values than the older children. All the differences were significant (P < 0.001). P,J(VT/TI) rose with the load. Consequently VT/TI increased less than P,, during exercise. These ratios were much higher in group A than in group B and the differences were highly significant (P -C 0.001).
B R E A T H I N G D U R I N G EXERCISE IN SWIMMERS
357
~/ waifs 12 10 8 6 4 2
60
rill 90
120
POWER
150 wails
Fig. 3. Mean values + SD ofinspiratory power for breathing (XJ¢, watt) during incremental exercise in the two groups of subjects, A and B. For 60, 90, 120 W: group A, n = 8; group B, n = 9. For 150 W: group A, n = 5; group B, n = 9. * P < 0.05; * * P < 0.01; ***P< 0.001.
Inspiratorypowerfor breathing. Inspiratory power for breathing ('v;v')increased linearly with the power and was significantly higher in group A than in group B (60 W: P < 0.01 ; 9 0 W and 120W: P < 0.001; 150W: P < 0.05) (fig. 3).
In percentage of i/o2max When results were expressed in relation to the percentage of ~'o2max, all subjects showed the same occlusion pressure, the same timing as expressed by TI/TTOT and the same respiratory frequency (fig. 4). In fact, the slopes (a) and the ordinates (b) of the regression lines of groups A and B were not significantly different. On the other hand, as shown in fig. 4, children in group A had lower minute ventilation and tidal volume owing to lower mean inspiratory flow rate (VT/TI). Moreover the slopes of the regression line were significantly different for VE (P < 0.02) and VT/TI ( P < 0.001). Consequently the effective inspiratory impedance of the respiratory system (Po.I/(VT/TI)) was higher in group A than in group B (fig. 4). The ordinates of the two regression lines were significantly different (P < 0.001). If the inspiratory power for breathing (VV) was expressed in percentage of Vo2max, the differences were not significant. When VE was normalized to body weight °75 and VT and VT/TI divided by body weight, all subjects showed the same breathing pattern. Furthermore, Po.~/(VT/T0 normalized to body weight was similar in the two groups of children (fig. 5). Discussion
This study shows that, at the same work load, subjects at a prepubertal stage show a higher ventilation, occlusion pressure and inspiratory power for breathing. As the values
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B R E A T H I N G D U R I N G EXERCISE IN S W I M M E R S
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of VT/TI are identical in the two groups, the increase in ventilation results from an increase in breathing frequency and in the ratio TI/TTOT. At a same percentage of "¢o2max, Po.l, W, f and TI/TTo'r are identical in the two groups, whereas ~'E, VT and V-r/TI are lower and Po.~/(VT/TI) higher in the youngest subjects. Corrections of VT, VT/TI and Po.I/(VT/T1) by weight cancel these differences. All the subjects studied were swimmers who followed the same training programs for at least one year and were familiar with Vo2max measures. At the same work load, the oxygen uptake in LSTPD • min - i was identical in the two groups. Furthermore, the mean oxygen uptake expressed in ml/kg was similar in the two groups. As this is a good indication to estimate the subjects' capacity to perform a muscular exercise (Shephard et al., 1968), the differences in the ventilatory pattern and control cannot be due to a difference in physical fitness between the two groups. The number of boys and girls was not the same: there were more girls in group B. There was no evidence of differences in the ratios, VT/TI, TI/TTOT or in the occlusion pressure between girls and boys at rest (Jammes et al., 1979; Gaultier et al., 1981). However, we checked to see whether it was the same during muscular exercise. We therefore compared the ventilatory response of the 5 girls and 4 boys in group B at different work-load levels. There was no significant difference in occlusion pressure, mean inspiratory flow and timing between the two groups. Occlusion pressure, introduced by Whitelaw et al. (1975), is supposed to be independent of airway resistance and modifications in compliance and it reflects respiratory control. Its relation to mean inspiratory flow makes it possible to evaluate satisfactorily the effective impedance of the respiratory system (Derenne et al., 1976), but the values of occlusion pressure are usually considered to be modified by changes in intrathoracic volume. The ventilatory level is modified during exercise (Lind, 1984) and we do not know whether modifications in the ventilatory level are identical in children at the prepubertal and peripubertal stage. However we known that relative resting volumes (FRC/TLC) of children do not change in relation to age (Collombier et al., 1969) and that in normal adult subjects (Siafakas et al., 1979; Hesser and Lind, 1983) as well as in patients with chronic obstructive lung diseases (Sergysels etal., 1981) occlusion pressure during exercise is a good indicator of the central inspiratory control in spite of change in ventilatory level. This is consistent with the study of Grassino et al. (1981) which states that modifications in FRC induce hardly any change in occlusion pressure. Relationship of respiratory variables and occlusion pressure to the work load The general evolution of the different variables is identical in the two groups. The occlusion pressure, ventilation and mean inspiratory flow increased in a linear fashion with the work load. As previously reported by Clark etal. (1983), we observed an increase in the ratios TI/TTOT with the work load. The decrease in TTOT that we also found means that the expiratory flow increases faster than the inspiratory flow. This increase in the expiratory flow could be due to the action of the muscular afferents which would induce either an increase in the activity of expiratory muscles or a decrease in the expiratory braking mechanism by a central action. In fact, in humans, Jammes et al.
362
M. RAMONATXO et al.
(1984) showed that the biceps tendon stimulation induced, during muscular exercise, an increase in the ratio TI/TToT. Therefore it is possible that during progressive exercise an increase in the discharges of the neural muscle spindles or of other receptors can induce an increase in expiratory activity. Furthermore, a decreased expiratory braking due to the bronchodilatator action of muscular afferents could contribute to this increase as has been shown by Coleridge et al. (1982) in dogs and Longhurst (1984) in cats. The ratio Po.1/(VT/TI) increases with the work load. Thus the ventilatory output decreases and the respiratory system impedance increases with exercise in children as was previously observed in adults (Sergysels et al., 1981). This increase is likely to be connected with a decrease in pulmonary compliance due to vascular overloading (Stubbing et al. 1980). When we compare the values for the different parameters at every step of work load we observe that the mean inspiratory flow values are identical in the two groups with very small standard deviations. This result is in agreement with Lind's study (1984): in adults, during muscular exercise, he observed very close values of VT/TI among the different subjects, at a given work load. The inspiratory flow is thus a parameter independent of the subject's age and growth, but determined by the work intensity in the same way as oxygen uptake. While oxygen uptake was the same in the two groups, ventilation values were slightly higher in prepubertal subjects than in peripubertal subjects. This shows that prepubertal subjects had a smaller ventilatory output. This ventilatory output is very likely associated with the parameters which play a part during oxygen transfer. In fact, Astrand (1952) showed that the total quantity of hemoglobin related to the subject's weight was smaller in younger boys. The difference in ventilation between the two groups is due to an increase in respiratory frequency and in the ratio TI/TTOT. Subjects of group A when compared with subjects of group B, showed a 'rapid shallow breathing'. This observation is in agreement with the studies of Taussig et al. (1977), Gaultier and Girard (1980) and with the well known fact that in mammals the breathing frequency is higher in smaller animals (Mead, 1960). The fact that the ratio TI/TTOT increases with the work-load and is higher in young subjects at the same work-load level perhaps minimizes the increase in ventilatory work. In fact, ventilation being the result of VT/TI multiplied by TI/TTOT, for a given ventilatory level, the increase of TI/TTOT allows a proportional reduction of VT/TI. In addition, Lind (1984), has shown that the occlusion pressure and the VT/TI ratio are connected by the relationship Po.~ = a(VT/T0 b in which b represents the slope of the line of regression and a the value ofPo. ~when VT/TI equals 1.0 L. sec - ~. Consequently the mean inspiratory work-load and the inspiratory effort required to reach such an inspiratory flow are reduced. This seems to confirm the hypothesis put forward by Yamashiro et al. (1975), who showed that the relative duration of inspiration and expiration were regulated in such a way that ventilatory effort is minimized.
BREATHING DURING EXERCISE IN SWIMMERS
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Relationship of respiratory variables and occlusion pressure to the percentage of ~Zo2max. As the prepubertal subjects performed a comparatively more difficult exercise than the peripubertal subjects, we compared the different parameters at a same percentage of Vo2max. From this relationship, it follows that three parameters are identical in the two groups: the occlusion pressure, the inspiratory power for breathing and the timing. These results show that during the growth period, the level of the central inspiratory control and the timing does not depend on the absolute power. They depend either on the metabolite rate or on the relative power, i.e. on the ratio of oxygen uptake at a given level to the maximal oxygen uptake. Indeed, as mean Vo2max expressed in ml/kg was identical in the two groups, the same percentage of'~/o~max correspond to the same mean metabolic rate and we cannot distinguish between both, metabolic rate and relative power. At a same percentage of X/o~max, three parameters were different in the two groups. Younger subjects have lower ventilation and mean inspiratory flow. Consequently, the 'effective' impedance of their respiratory system is higher. However, when VT is corrected by weight, VTBw/TI and Po.1/(VTBw/TI) are identical in the two groups. The differences we observed are thus essentially due to biometric factors. Therefore, the pubertal peak of growth does not induce a change in the 'specific' impedance of the respiratory system during muscular exercise. This result confirms during exercise the finding of Gaultier et aL (1981) who showed that during growth the respiratory system impedance is constant at rest. In conclusion, this study shows that during pubertal growth, some parameters vary in relation to the absolute power. There are oxygen consumption and mean inspiratory flow. For the other parameters, i.e. occlusion pressure and timing, the question is open to know whether they depend on the reached metabolic level or on the relative power. Our results strongly suggest that biometric factors only determined inter-individual differences in ventilatory response to exercise in prepubertal and peripubertal swimmers.
Acknowledgements.The authors wish to express their gratitude to Dr. Yves Jammes for helpful criticism and comments in the preparation of the manuscript. They also thank Mrs. RoselyneJoly for her secretarial assistance and Mr. Robert Assie and Raymond Puech for their assistance in statistical analysis.
References •strand, P.O. (1952). Experimental Studies of Physical Working Capacity in Relation to Sex and Age. Copenhagen, Ejnar Munksgaard. Clark, J.M., F.C. Hagerman and R. Gelfand (1983). Breathing pattern during submaximal and maximal exercise in elite oarsmen. J. Appl. Physiol. 55: 440-446. Coleridge, J.C.G., H.M. Coleridge, A.M. Roberts, M.P. Kaufman and D.G. Baker (1982). Tracheal contraction and relaxation initiated by lung and somatic afferentsin dogs.J. Appl. Physiol. 52: 984-990.
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