The pulmonary system does not typically limit exercise performance in healthy, young men at sea level (4). However, there are some instances, such as expiratory flow limitation (EFL), in which the pulmonary system has been shown to limit exercise tolerance. EFL (and a concomitant dynamic hyperinflation) can limit exercise tolerance in healthy individuals via increased work of breathing and oxygen cost of breathing (1) and decreased inspiratory muscle length and endurance (31). Although the prevalence of EFL has not been firmly established, it is believed to be relatively low in normal healthy men (20). However, women may present a greater prevalence of EFL than men consequent on smaller lungs and airways compared with men (16), resulting in lower maximally achievable flow rates and smaller maximal flow-volume loops (MFVL) (15). Ultimately, these can lead to a higher prevalence of EFL during exercise in women compared with men (9,15).
Similar to women, it has been suggested that EFL prevalence is high (>70%) in both trained and untrained prepubescent children (19). More recently, our laboratory has reported a very high prevalence (∼93%) of EFL in a sample of 40 healthy untrained prepubescent children (20 boys and 20 girls). Our study showed that there were no sex differences in the prevalence of EFL, with both boys (19/20 subjects) and girls (18/20 subjects) displaying a high prevalence of EFL (28). It appears that in both prepubescent boys and girls, the ventilatory demands of exercise often exceed the capacity of the pulmonary system, precipitating a high prevalence of EFL in children.
However, several changes are known to occur during pubertal maturation and growth that might play a role in the decrease in EFL prevalence from childhood to adulthood. Lung and airway size increase during the pubertal growth spurt, resulting in substantial improvements in pulmonary function (e.g., increased forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), and maximal expiratory flow rates) (33). In addition, there is a change in the coupling of CO2 production with ventilation (V˙E/V˙CO2) during exercise from pre- to postpuberty (3,7). Specifically, it has been reported that children breathe “out of proportion” to ventilatory demand, demonstrated by a higher V˙E/V˙CO2 during exercise in children compared with adults (3,7). This decrease in relative ventilatory demand, in concert with increased ventilatory capacity (via larger MFVL), may result in a decrease in EFL prevalence during maximal exercise from pre- to postpuberty. However, no study to date has investigated longitudinal changes in EFL and its determinants across puberty.
Therefore, the purpose of this longitudinal study was to investigate changes in EFL, including sex differences, from pre- to postpuberty in boys and girls. We hypothesized that 1) the prevalence of EFL would be lower in postpuberty compared with prepuberty, 2) postpuberty girls would show a higher prevalence and severity of EFL compared with boys, and 3) postpuberty subjects would exhibit increased lung volume and maximal expiratory flow rates and decreased V˙E/V˙CO2 compared with prepuberty subjects.
We recruited 21 healthy subjects (11 boys and 10 girls) from 40 subjects who were previously tested in our laboratory ∼5 yr ago (28). We were unable to make contact with the remaining 19 subjects. All subjects were nonasthmatic and free of pulmonary disease both at baseline and follow-up, as measured by pulmonary function tests (PFTs) and medical history questionnaire. Approximately 5 yr ago, all children were determined to be prepubescent, as defined by Tanner stage 1 (29). Tanner stage of maturation was also assessed postpuberty. In the prepuberty assessment, Tanner stage was evaluated by the parent, whereas postpuberty, it was determined via self-report. We did not determine menstrual cycle phase in female subjects, but all postpuberty females had reached menses. Each subject had a parent or guardian present for each appointment to provide medical history information and informed consent. All research components were reviewed and approved by the Institutional Review Board of Human Subjects at Kansas State University, Manhattan, KS (IRB approval #6673).
Subjects reported to the laboratory on a total of four occasions: two times at baseline (prepuberty) and twice 5 yr later for follow-up (postpuberty). The experimental designs for baseline and follow-up were identical. On the first visit, height and weight for each subject were measured using a calibrated eye-level physical scale with a height rod (Detecto, Webb City, MO). Standard PFTs were then performed after several practice trials to ensure subject competence. These measures included lung volumes, lung diffusing capacity with carbon monoxide (DLCO), maximal inspiratory and expiratory pressures (PImax and PEmax), and MFVL. PImax, PEmax, and MFVL tests were performed in triplicate and averaged, as previously reported (28). The subject then completed an incremental maximal exercise test to exhaustion to determine maximal oxygen uptake (V˙O2max), followed by postexercise PFTs. The subject completed a second exercise test at 105% of maximal workload to verify V˙O2max (22). On the second visit, each subject underwent a dual-energy x-ray absorptiometry (DEXA) scan to determine body composition.
Tests and Measurements
Lung diffusing capacity (DLCO), PImax, maximal expiratory pressure (PEmax), and MFVL were measured before exercise testing at prepuberty and postpuberty (SensorMedics 229 Metabolic Cart; SensorMedics Corp., Yorba Linda, CA). Diffusing capacity of the lung was determined using normalized alveolar air (DLCO/VA) using a test gas mixture of 0.3% acetylene, 0.3% carbon monoxide, 0.3% methane, and 21% O2 with N2 balance via the intrabreath inhalation technique. PEmax was measured at total lung capacity (TLC), and PImax was measured at residual volume. After practice trials, PImax, PEmax, and MFVL tests were performed in triplicate and averaged both before and after (<5 min) the incremental exercise test. We have not reported TLC or residual volume because of technical issues with the nitrogen washout technique of our metabolic cart. However, there are data to suggest that TLC and FVC increase in unison from 6 to 18 yr old in boys and girls (21), making FVC a suitable proxy for TLC in this age group (25).
Maximal aerobic capacity (V˙O2max)
Maximal oxygen uptake (V˙O2max) was determined using a cycle ergometer (Ergometer 800S, SensorMedics Corp.). A 3-L calibration syringe was used to calibrate the flow sensor before testing. Known gas concentrations were used in the calibration of gas analyzers. Before the onset of exercise, resting metabolic measurements were recorded for 3 min. Subjects then began a 2-min warm-up at 20 W. During the prepuberty assessment, subjects were instructed to maintain a pedaling frequency between 50 and 60 rpm, whereas in the postpuberty assessment, subjects pedaled at 60–80 rpm. After approximately 2 min of warm-up, the workload was increased 10 W·min−1 at prepuberty and 25 W·min−1 at postpuberty. During each stage, subjects reported an RPE and dyspnea using the modified Borg scale (2). Arterial oxygen saturation (SaO2) was estimated using a pulse oximeter (Datex-Ohmeda, 3900P, Madison, WI) secured to the left ear lobe. HR was assessed both pre- (4-lead ECG) and postpuberty (Polar HR monitor, Polar Electro Inc., Lake Success, NY). Verbal encouragement from researchers was provided throughout the exercise test. Subjects exercised continuously until reaching volitional exhaustion (<16 min). The exercise test was terminated when the subject could no longer maintain a pedaling frequency within the instructed range for five consecutive revolutions. Ventilatory and metabolic data were measured and monitored continuously throughout the V˙O2max test via breath-by-breath analysis (SensorMedics 229 Metabolic Cart, SensorMedics Corp.). After a rest period of approximately 15 min, subjects completed a second exercise test to volitional exhaustion at 105% of maximal workload (∼2 min) to verify V˙O2max (22).
EFL and tidal volume regulation
A bidirectional mass flow sensor was used to measure and record tidal flow-volume loops during the V˙O2max test. Tidal flow-volume loops were placed inside the largest (postexercise) MFVL (12). Subjects performed inspiratory capacity (IC) maneuvers from end-expiratory lung volume (EELV) with ∼20 s remaining in each stage throughout the incremental exercise test. IC maneuvers were used for the accurate placement of tidal flow-volume loops within the postexercise MFVL. Subjects were given clear and concise instruction regarding the correct performance of IC maneuvers and were allowed to practice in a resting state before testing. Maximal IC maneuvers have been used previously for the accurate determination of EFL in children during maximal exercise (19). Ventilatory drift was automatically accounted and corrected for appropriately via the metabolic cart. Specifically, any drift in the exercise tidal flow-volume loop was placed correctly based on the subjects’ IC maneuver. EFL was deemed to be present when the tidal flow-volume loop intersected the exercise flow-volume loop to a degree of 5% or greater. EELV and end-inspiratory lung volume, expressed as ratios of expiratory reserve volume and inspiratory reserve volume (ERV/FVC, IRV/FVC), were used to describe changes in tidal volume regulation during the incremental exercise test. During testing, any changes to breathing regulation or flow sensor drift were monitored by allowing for approximately five tidal breaths before performance of an IC maneuver. The largest MFVL (typically postexercise) was used in the determination of EFL to account for any bronchodilation. It is important to note that the true dimensions of the MFVL can be underestimated when flow rate and volume are measured at the airway opening due to thoracic gas compression (TGC). This underestimation of the MFVL could potentially lead to the false detection of EFL during exercise (8). TGC is best accounted for by using a body plethysmograph or performing graded expiratory efforts (8). Because we did not have subjects perform graded expiratory efforts during either the pre- or postpuberty assessment, it is possible that EFL could have been falsely detected in some of our subjects. However, to our knowledge, there are no existing data regarding the effects of TGC on detection of EFL in children.
A whole-body DEXA system (v5.6; GE Lunar Corp., Milwaukee, WI) was used to measure total body composition. Subjects removed metal objects and shoes before scanning and were instructed to lay in a supine position with legs slightly spaced apart and arms separated from the trunk. The subjects were directed to lay as still as possible during scanning. DEXA scans are a validated means of determining lean body mass (LBM), body fat percentage, and body fat distribution via differences in absorption of two different high-energy x-ray beams (10).
SigmaPlot statistical software version 11 (Systat Software, Inc., San Jose, CA) was used for data analysis. Table data are expressed as mean ± SD. Figure data are expressed as mean ± SE. A 2 × 2 mixed factorial ANOVA (time vs group) was used to determine differences between sexes and pre- and postpuberty. A chi-square two-tailed test of independence was used to determine an association between sex and prevalence of EFL. Significance was set at P < 0.05 for all analyses.
Pre- and postpuberty subject characteristics are displayed in Table 1. The male-to-female ratio was nearly equal (n = 10 girls, n = 11 boys). There was no sex difference (P > 0.05) in age prepuberty, but postpuberty boys were significantly older than postpuberty girls. Prepuberty boys had significantly greater LBM (kg and %) and lower body fat (BF) (%) compared with prepuberty girls. Postpuberty boys had significantly greater age, height, LBM (kg and %), and lower BF (%) compared with postpuberty girls. All variables were significantly different from pre- to postpuberty in boys and girls, except LBM (%) and BF (%).
Table 1 also presents resting pulmonary function. Prepuberty boys showed greater (P < 0.05) ERV at rest, DLCO, FVC, FEV1, and peak expiratory flow compared with prepuberty girls. Forced expiratory flow between 25% and 75% FVC (FEF25%–75%), FEV1/FVC, forced expiratory flow at 50% FVC (FEF50%), and PImax were not significantly greater in postpuberty boys compared with postpuberty girls. All resting pulmonary function values were significantly greater in postpuberty boys compared with prepuberty boys, except FEV1/FVC and PImax. Similarly, resting pulmonary function values were significantly greater in postpuberty girls than prepuberty girls, with the exception of FEV1/FVC and PEmax.
Data recorded during maximal exercise for pre- and postpuberty boys and girls are displayed in Table 2. Absolute V˙O2max, ventilation, tidal volume, V˙CO2, V˙E/V˙CO2, RER, and work rate were greater (P < 0.05) in postpuberty boys and girls compared with prepuberty. Postpuberty girls showed significantly greater V˙O2 relative to LBM than prepuberty. Relative V˙O2, absolute V˙O2, ventilation, V˙CO2, and work rate were greater (P < 0.05) in prepuberty boys than girls. Postpuberty boys displayed significantly greater relative V˙O2, absolute V˙O2, ventilation, tidal volume, V˙CO2, and work rate. VD/VT decreased significantly from pre- to postpuberty in both boys and girls, and there was no sex difference with regard to VD/VT at either time point. Because of experimental limitations, valid dyspnea measures were unattainable during the prepuberty measurement. When measured postpuberty, boys reported greater levels of dyspnea compared with girls during maximal exercise. Furthermore, subjects that experienced EFL reported higher levels of dyspnea compared with subjects that did not experience EFL during maximal exercise (EFL: 9.29 ± 0.49; NEFL: 7.21 ± 2.05; P < 0.05).
Prevalence and severity of EFL
Figure 1 shows the change in EFL prevalence from pre- to postpuberty in boys and girls. Ten of eleven (∼91%) prepuberty boys and nine of ten (90%) prepuberty girls exhibited EFL at V˙O2max. Five of eleven (∼45%) postpuberty boys and two of ten (20%) postpuberty girls experienced EFL at V˙O2max. There was no sex difference in EFL prevalence prepuberty (P > 0.05), but postpuberty boys showed a greater prevalence of EFL (5 of 11 subjects) than postpuberty girls (2 of 10 subjects, P < 0.05). Figure 2 demonstrates the severity (%VT) of EFL experienced during maximal exercise measured pre- and postpuberty in boys (A) and girls (B). There was a significant decrease in severity of EFL at V˙O2max from pre- to postpuberty in both boys (10/11 subjects) and girls (9/10 subjects). Boys that displayed EFL both pre- and postpuberty displayed similar (P > 0.05) V˙O2max and V˙E but lower maximal expiratory midflow rates (i.e., FEF25%–75% and FEF50%) compared with postpuberty boys that did not exhibit EFL. Girls that experienced EFL pre- and postpuberty showed similar (P > 0.05) maximal expiratory midflow rates but greater V˙O2max compared with postpuberty girls that did not experience EFL.
Determinants of EFL
Figure 3 demonstrates minute ventilation relative to CO2 production (V˙E/V˙CO2) in pre- and postpuberty boys and girls at different exercise intensities. Prepuberty boys displayed greater (P < 0.05) V˙E/V˙CO2 than postpuberty boys at 80% and 100% V˙O2max, whereas prepuberty girls showed greater (P < 0.05) V˙E/V˙CO2 compared with postpuberty girls at all exercise intensities, reflecting a decreased relative ventilatory response during exercise from pre- to postpuberty in boys and girls.
Figure 4 displays changes in EELV and end-inspiratory lung volume normalized to vital capacity (expressed as ERV/FVC (%) and IRV/FVC (%), respectively) at V˙O2max from pre- to postpuberty in boys and girls. ERV/FVC (%) during maximal exercise significantly increased in boys from pre- to postpuberty but did not in girls (P > 0.05). However, there was a significant decrease from pre- to postpuberty in IRV/FVC (%) at V˙O2max in both sexes.
The purpose of this study was to assess changes in EFL during exercise from pre- to postpuberty in boys and girls. The primary finding was that the prevalence of EFL decreased from pre- to postpuberty from >90% to ∼33%. Surprisingly, although there was no sex difference in the prevalence of EFL prepuberty, more postpuberty boys exhibited EFL than postpuberty girls. The decreased prevalence of EFL postpuberty was likely due to substantial increases in lung size and maximal expiratory flow rates relative to improvements in aerobic capacity and exercise ventilation. Finally, both postpuberty boys and girls regulated tidal breathing at significantly higher lung volumes (relative to FVC) during maximal exercise, despite the significantly lower prevalence of EFL compared with prepuberty.
Prevalence of EFL
There were no sex differences in the prevalence of EFL when measured prepuberty. Previous data from our laboratory has described an equally high prevalence of EFL (>90%) in both prepubescent boys and girls (28). Interestingly, in the current study, we found a higher prevalence of EFL in postpuberty boys compared with postpuberty girls. Studies investigating adult populations point to a greater prevalence of EFL in women because of smaller lungs and airways and reduced maximal flow rates (9,15). Consequently, we hypothesized that we would see a greater decrease in EFL prevalence in postpuberty boys compared with girls. However, this was not the case. It is likely (as discussed below) that this can be partly explained by differences between boys and girls in the timing of growth and maturation of the pulmonary system during puberty (26).
The prevalence of EFL in postpuberty boys differs from what has been reported in men. Lungs in adult men with aerobic capacity <165% predicted are typically considered to be “overbuilt” with regard to the ventilatory demand placed on them during exercise (4). Hence, the finding that 45% of our boys experienced EFL during the postpuberty assessment deserves attention. This occurred despite an average V˙O2max (∼43 mL·kg−1·min−1 ) in this group. A likely explanation is that the boys in our study had not yet achieved full maturation of the pulmonary system because maturation of the lungs and airways has been shown to occur at approximately 18 yr old in males (26). In our sample, the five boys who demonstrated EFL exhibited significantly lower maximal expiratory flow rates (FEV1/FVC, FEF25%–75%, and FEF50%) compared with boys who did not exhibit EFL despite no differences in body composition, V˙Emax, or V˙O2max. Because growth of the pulmonary system has been shown to lag behind anthropometric growth during puberty (26,33), it is likely that the boys in the current study were still experiencing maturation of the lungs and airways.
It is believed that girls reach full maturation of the pulmonary system at approximately 14 yr old (26). In this context, it is likely that postpuberty girls presently studied (age ∼14 yr) had nearly mature lungs and airways. This postulation is supported by the finding that only 20% of our postpuberty girls exhibited EFL during exercise. Furthermore, the two girls who demonstrated EFL displayed appreciably greater V˙O2max compared with non-EFL girls, which agrees with previous research (15). However, the prevalence of EFL found in our postpuberty girls is actually lower than that reported in other studies investigating EFL in untrained adult women (5,32). This low prevalence of EFL in our postpuberty girls can most likely be attributed to their low aerobic capacity (33.0 ± 6.7 mL·kg−1·min−1; 6).
Determinants of EFL
Several possibilities exist to explain the reduced prevalence of EFL from pre- to postpuberty, including increase in lung size, decrease in V˙E/V˙CO2, and changes in aerobic capacity. Pertaining to increased lung size, it has been documented that the lungs and airways grow from birth until approximately the age of 14 yr in girls and 18 yr in boys (26), demonstrated by improved functional measurements (e.g., FVC, FEV1, and FEF25%–75%) from childhood through the end of puberty (33). As expected, data from the current study demonstrate a substantial growth in lung and airway size from pre- to postpuberty, reflected by approximately twofold increases in FVC, FEV1, FEF25%–75%, and DLCO in both boys and girls. It is likely that the improvement in resting pulmonary function had a considerable effect on reducing EFL prevalence from pre- to postpuberty.
It has been well documented that prepubescent boys have larger lungs and airways than girls, even when matched for standing height (13,30). Our data are supportive of this previous work, as prepuberty boys exhibited significantly greater FVC and maximal flows compared with girls at rest, despite no difference in height between sexes. Similarly, postpuberty boys in our study also showed significantly greater lung volumes and maximal flows compared with postpuberty girls. In adults, it is thought that this sex difference in pulmonary function contributes to an increased prevalence of EFL in women compared with men (9,15). However, in our subjects, despite greater resting pulmonary function in postpuberty boys compared with girls, more boys displayed EFL than girls.
Decreased ventilatory response during exercise could also reduce the prevalence of EFL. It has been described that children breathe “out of proportion” to ventilatory demand (3) and that the slope of V˙E and V˙CO2 decreases with age (18). Consequently, we also hypothesized that subjects would display a decreased V˙E/V˙CO2 from pre- to postpuberty. This hypothesis was supported by our data because during high-intensity exercise (80% and 100% V˙O2max), both postpuberty boys and girls exhibited significantly lower V˙E/V˙CO2 levels compared with prepuberty. Thus, there was a decrease in the relative ventilatory response to CO2 production. This also aligns with previous research suggesting a decline in chemoresponsiveness from pre- to postpuberty in boys and girls (14), which might explain in part a decrease in EFL prevalence during puberty. We also found a decrease in the dead space to tidal volume ratio (VD/VT) from pre- to postpuberty in boys and girls. The decrease in relative dead space ventilation, alongside a potential decrease in chemoresponsiveness, possibly speaks to an overall increase in ventilatory economy from pre- to postpuberty.
Finally, changes in aerobic capacity with maturation could explain the reduced prevalence of EFL. It has been postulated that the prevalence of EFL during exercise is determined in part by aerobic capacity, with both highly fit men (11) and women (9,15) demonstrating a high prevalence of EFL. This was true for postpuberty girls, as the two girls that demonstrated EFL presented a greater relative V˙O2max compared with girls that did not experience EFL. However, there was no difference in V˙O2max between flow-limited boys and those that did not exhibit EFL. Consequently, the relative importance of V˙O2max in determining the prevalence of EFL, specifically with regard to changes from pre- to postpuberty, remains to be elucidated.
Regulation of tidal volume during exercise
Overall, we found that postpuberty subjects breathed at a higher ERV/FVC and lower IRV/FVC throughout the exercise protocol compared with when tested prepuberty. These findings extend to both subjects that exhibited EFL and those that did not. Conversely, our prepuberty subjects increased ERV/FVC relatively less compared with when measured postpuberty and displayed a high prevalence of EFL. A possible explanation could be that our postpuberty subjects breathed at higher relative lung volumes during exercise as a “strategy” to avoid EFL, utilizing the higher flow rates available with a leftward shift of the tidal flow-volume loop within the maximal flow volume loop, as has been suggested elsewhere (5,17). However, this conclusion should be drawn with caution, considering the lack of static lung volume measurements in the present investigation. Without measurement of static lung volumes, such as TLC, residual volume, and functional residual capacity we cannot exclude the possibility that the higher dynamic lung volumes seen in the postpuberty subjects were not simply an artifact of a substantially altered FRC from pre- to postpuberty. There are a number of changes that occur during the pubertal period with regard to breathing mechanics, such as altered lung and chest wall compliance, which could influence changes in FRC. As it is, by describing dynamic lung volume regulation via ERV/FVC and IRV/FVC, we can only see part of the picture, versus a comprehensive view, of alterations in lung volume regulation across pubertal growth. This is an unfortunate limitation to the present study but merits worthwhile future investigation.
The results of the present study raise additional questions for future research. First, although considerable pubertal growth had occurred in all of our subjects from pre- to postpuberty, our subjects had not yet reached full maturity according to the Tanner stage of maturation scale. As expected, the results of our postpuberty subjects differ slightly from previous data reported in adults. It would be worthwhile to further track our subjects from this “snapshot” of puberty into adulthood, thus providing resolution to the story of EFL from childhood to adulthood. Next, a deeper look into other factors that may contribute to the decreased prevalence of EFL from pre- to postpuberty would be valuable. Specifically, dysanapsis (lung and airway size mismatch) has been shown to be a strong determinant of EFL in adults (5,27). An investigation into changes in the dysanapsis ratio from pre- to postpuberty may prove worthwhile. Also, it has been shown that modifiable lifestyle factors, such as physical activity and excess adiposity, can affect pulmonary function in children (23,24). The extent to which lifestyle habits such as diet and physical activity during maturation affect lung function and EFL during exercise is yet to be determined.
The findings of the present study indicate that the prevalence of EFL decreases from pre- to postpuberty in both boys and girls. The contributory moderators of this change are twofold increases in lung size (i.e., FVC) and maximal midflows (i.e., FEF50%, FEF25%–75%) and less of a ventilatory response to stimuli (represented by V˙E/V˙CO2) compared with prepubescence. However, there was also a ∼110% increase in absolute V˙O2max. Interestingly, there appears to be a change in lung volume regulation, with prepuberty subjects (demonstrating a high prevalence of EFL) regulating tidal breathing at lower lung volumes during exercise compared with postpuberty subjects. The difference in lung volume regulation could also help explain differences in prevalence of EFL from pre- to postpuberty. However, it is likely that other variables contribute to the decrease in EFL prevalence, such as dysanapsis and lifestyle factors, and we recommended that these be explored in the future.
The authors would like to thank Dr. David C. Poole for his insights and suggestions.
No funding sources were used for this study. None of the authors have any conflicts of interest to declare.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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