Development of Ventilatory Responses

Transcription

1 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 thatthe pattern ofventilatoryresponses 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 of9and 13 years. Subjects performedmaximaland 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.asimilarpattern was observed atmaximal exercise, but the decrease inve per kilogram was not statistically significant. Ventilatory equivalent for oxygen (Ve/Vo2) fell with age submaximal exercise but declined only in the boys with maximal testing. Ve/Vo2 at 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); VE = minute ventilation; Ve/Vo2=ventilatory equivalent for oxygen; Vo2=oxygen uptake; Vt=tidal volume "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 ventilatory in 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 ing rate and ventilatory equivalent for oxygen (Ve/ Vo2) in response to exercise progressively decline. Longitudinal data regarding ventilatory changes in exercising children are limited, confined to a single study of Norwegian children between ages 8 and 15 years.6 In 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. was conducted to This 5-year longitudinal study *From the Department of Pediatrics, Baystate Medical Center, Springfield, Mass, and the Department of Physical Education, Fitchburg State College, Fitchburg, Mass. Manuscript received May 23, 1996; revision accepted Septem ber 11. Reprint requests: Dr. Rowland, Department of Pediatrics, Baystate Medical Center, Springfield, MA 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 CHEST / 111 / 2 / FEBRUARY,

2 steady-state 4-min walk at 3.25 mph, 8% grade. Treadmill elevation was then increased 2% every minute until subject exhaustion, with speed individualized between 3.25 and 3.75 mph 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 techniques. Subjects breathed through circuit a valve (Rudolph) (94mL dead space), and a pneumotachometer was used for recording and Vt minute ventilation (Ve). Expired air traversed a combined tubing/mixing chamber volume of 6 L. Expired gas samples from the mixingchamberwere analyzed for oxygen and carbon dioxide by zirconia oxide and infrared analyzers, respectively. Data were averaged every 15 s and used to calculate oxygen uptake (Vo2), expired ventilation (Ve), carbon dioxide output, and respiratory exchange ratio. The system was calibrated before each session 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 > Informed permission was obtained from the parents, and each child provided assent for participation. This study was approved by the institutional review board of the Baystate Medical Center. Changes in 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 Changes in weight and height for boys and girls over the 5 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 age values of aerobic fitness for the childhood pop ulation.9 All exercise tests conformed to criteria for maximal effort. Tables 2 and 3 list physiologic variables for male and female subjects at submaximal and maximal exercise. No significant differences were observed by gender over time for Ve, Vt, and fr, and combined longitudinal data for these variables are presented in 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 inve andvt 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 A. When Ve and Vt were expressed relative to body mass, 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 gender group of 21.8 (2.2) ml/kg. As a conse quence, the decline in submaximal fr from 45 to 36 breaths/min resulted in a progressive fall in Ve per kilogram. At maximal exercise, Vt per kilogram was stable over 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 decrease to 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 observed was 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 analysis indicated that absolute VEmax changed rel ative to body mass (M) and height (H) over the 5 years by 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 Table 1.Weight and Height Changes With Age: Mean (SD) Values Weight, kg Height, cm 37.1 (6.1) 35.4(11.1) 142 (4) 140 (9) 42.3 (7.4) 40.2 (14.0) 148 (5) 145 (10) 47.3 (9.2) 43.5 (14.7) 154 (6) 151 (10) 54.3 (12.6) 49.8(16.7) 161 (7) 159 (9) 57.5(14.2) 57.3(18.8) 168 (7) 165 (8) 328 Clinical Investigations

3 Table 2.Submaximal Physiologic Variables With Age: Mean (SD) Values Ve, L/min Ve, L/kg/min Vt, L Vt, L/kg fr, b/min Ve/Vo (5.0) 34.9(10.0) 0.93(0.11) 1.00(0.13) 0.84(0.10) 0.76(0.18) (0.002) (0.003) 43(8) 47(10) (5.10) (2.80) *p<0.05 for time for the 5 years. fp<0.05 for gender for years 2 to (5.5) 36.6(12.5) 0.86(0.13) 0.92 (0.09) 0.89 (0.10) 0.85 (0.23) 42(8) 44(11) (3.11) (2.47) 39.7 (9.2) 40.2 (17.6) 0.84(0.11) 0.91 (0.12) 1.00 (0.09) 0.90 (0.22) (0.003) 41(9) 43 (9) (2.75) (3.85) 39.8 (9.6) 40.2(14.0) 0.74 (0.08) 0.81 (0.06) 1.08(0.14) 1.04 (0.32) (0.001) (0.003) 38(5) 39(8) (2.88) 30.18(1.89) 40.8 (10.6)* 43.4 (16.2)* 0.71 (0.08)* 0.75 (0.06)* 1.25 (0.17)* 1.19 (0.39)* (0.002) 34 (6)* 38 (9)* (2.66)*f (2.34)*f during the study period in both sexes, except for stable maximal values in the girls (Fig 5). At each year, the value ofve/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 provided in this study can be presumed to provide an accurate assessment of developmental changes ventilatory function during in exercise. In addition, longitudinal observations can be expected to provide 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) Ve, L/min Ve, L/kg/min Vt, L Vt, L/kg fr, b/min Ve/Vo (8.0) 64.1 (11.9) 1.82 (0.35) 1.90 (0.32) 1.07(0.11) 1.07 (0.25) (0.002) (0.002) 65 (10) 63(8) 37.15(3.54) (2.26) 78.2 (9.3) 71.0(14.1) 1.89 (0.27) 1.88 (0.43) 1.27(0.13) 1.17(0.33) (0.003) (0.002) 62(7) 63(10) 35.29(1.72) (3.35) 85.5 (12.3) 76.3 (19.8) 1.85 (0.31) 1.82 (0.34) 1.37(0.17) 1.27 (0.33) (0.002) (0.004) 63(7) 61 (7) (2.32) (2.30) 94.4(13.1) 83.1 (18.0) 1.79 (0.27) 1.74 (0.28) 1.55(0.17) 1.41 (0.38) (0.004) (0.003) 61(7) 60(6) (2.76) (2.04) (16.3)* 95.3 (22.7)* 1.86 (0.31) 1.71 (0.38) 1.95 (0.38)* 1.75 (0.53)* (0.004) (0.004) 57 (9)* 57 (4)* (2.58)* (3.88)*f *p<0.05 for time for the 5 years. fp<0.05 for gender for each of the 5 years. CHEST / 111 / 2 / FEBRUARY,

4 Ve (L min-') f " 8 0 Max Submax Figure 1. Changes in maximal and submaximal Ve with age. fr (b min"1) Max Submax Figure 3. Changes in maximal and submaximal fr with age. level of treadmill work, Ve increases as the child ages. This rise in not, however, simply related to increase in body size. Vt increases in proportion body to mass as the child grows, but the frequency of breathing at a given submaximal work load progres sively declines. As a result, submaximal Ve rises slower with age than would be expected for body mass. This is also reflected in a steady fall in the Ve 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 demonstrating a greater value at all years. The explantation for this effect of gender on ventilatory efficiency is unknown. 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 VT (L) f.16 o- Submax Figure 2. Changes in maximal and submaximal Vt with age. 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 describing children's ventilatory responses to submaximal exercise.1-6 Robinson2 reported ventilatory responses to a treadmill walk at 5.6 km/h in groups of subjects ages 6 to 17 years. Breathing rate declined from 49 to 29/min over that age span while Ve per kilogram fell from 1.05 to kg/min. Only small changes were observed in Vt per kilogram (0.021 L at age 6 years to L at age 17 years). Andersen rate of5 to 10/min et al1 described a fall in breathing 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 children between in ages 8 and 17 years. At the same VEmox 1.80 (LKg-'min-i) Figure 4. Changes in maximalve per kilogram in boys and girls with age. 330 Clinical Investigations

5 Ve/Vq Figure 5. Changes in Ve/Vo2 at maximal and submaximal exercise in boys and girls according to age. relative intensity (65 to 70% Vo2max), Ve increased Max 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 frequency fell from 39 to 28 and 36 to 26 in the boys 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 girls. In this study, no influence of age on submaxi mal Ve/Vo2 was observed. Previous reports ofchanges 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 ofboys 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 study as well as the report of Rutenfranz et al6 that maximalvt during exercise is linearly related to volume. lung 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 tionship of maximal Ve per kilogram to age in boys 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 ventilatory rates for a given metabolic demand 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 ofvt and respiratory that would provide the rate 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 ofthe 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 study with those of Vo2max and cardiac output. At 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 ofinterest to compare such changes with those of ventilation, CHEST / 111 / 2 / FEBRUARY,

6 however, since both are characterized by volume (cardiac output, Ve) that a minute is determined by size-dependent volume (stroke volume, Vt) and a a size-independent rate (heart rate, fr). At a given submaximal exercise, the responses are similar: as the child ages, the volume variable increases in parallel to body size, while the rate variable de 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 closely linked to body size during growth, while fr gradually declines. This results in a fall in Ve per kilogram at submaximal exercise. Such a decline has also been described by others at maximal exercise, but in the present study, the decrease in Ve per kilogram at maximal exercise was not statistically significant. Children demonstrate a greater ventila tory efficiency during exercise as they grow, with a progressive decline in submaximal and.at least in boys.maximal Ve/Vo2. References 1 Andersen KL, Seliger V, Rutenfranz J, et al. Physical perfor mance capacity of children in Norway: II. Respiratory re sponses to graded exercise loadings.population parameters in a rural community. Eur J Appl Physiol 1974; 33: Robinson S. Experimental studies of physical fitness in relation to age. Arbeitsphys 1938; 10: Mercier J, Varray A, Ramonatxo M, et al. Influence of anthropometric characteristics on changes in maximal exer cise ventilation and breathing pattern during growth in boys. Eur ] Appl Physiol 1991; 63: Astrand PO. Experimental studies of physical working capac ity in relation to sex and age. Copenhagen: Munksgaard, Morse M, Schultz FW, Cassels DE. Relation of age physiological to responses of the older boy (10-17 years) to exercise. J Appl Physiol 1949; 1: Rutenfranz J, Lange Andersen K, Seliger V, et al. Exercise ventilation during the growth spurt period: comparison be tween two European countries. Eur J Pediatr 1981; 136: Rowland TW, Cunningham LN. Walking economy and stride frequency in children.a longitudinal study [abstract]. Med Sci Sports Exerc 1995; 27(suppl):S93 8 RowlandTW. Aerobic exercise testing protocols. In: Rowland TW, ed. Pediatric laboratory exercise testing. Champaign, 111: Human Kinetics Publishers, 1993; Bar-Or O. Pediatric sports medicine for the practitioner. New York: Springer-Verlag, 1983; 5 10 Gaultier C, Perret L, Boule M, et al. Occlusion pressure and breathing pattern in healthy children. Respir Physiol 1981; 46: Cooper DM, Kaplan MR, Baumgarten L, et al. Coupling of ventilation and C02 production during exercise in children. Pediatr Res 1987; 2L Gratas-Delamarche A, Mercier J, Ramonatxo M, et al. Ven tilatory response of prepubertal boys and adults to carbon dioxide at rest and during exercise. Eur J Appl Physiol 1993; 66: Cotes JE. Lung function: assessment and application medicine. 4th ed. Oxford: Blackwell Scientific Publications, in 1979; Lanteri CJ, Sly PD. Changes in respirator)7 mechanics with age. J Appl Physiol 1993; 74: Clinical Investigations