INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

DURING GROWTH AND maturation, absolute peak oxygen consumption (O₂, ml/min) increases as a function of body size (1, 21). A major question related to this observation is, Are the growth-related improvements in physiological capacity a function of increasing body size or qualitative changes in the structural and functional capacity independent of body size or both (30, 40)? To provide answers to this question, the potentially confounding effect of variation in body size must be partitioned appropriately.

Age- and sex-associated variation in peak O₂ has been studied extensively in the general population (1, 21). Several cross-sectional studies have characterized the physiological profile of young endurance athletes, but longitudinal studies of the development of peak O₂ in young athletes, especially girls, are rather limited (7, 9, 12, 22, 24, 27, 34). These studies generally include small sample sizes, are limited to a narrow age range (i.e., 11-15 yr), and therefore do not describe the growth-related changes in peak O₂ across the entire adolescent period. Longitudinal studies are important to identify individual and population growth patterns. Thus there is a need for analyses of longitudinal data examining the age- and sex-associated variation of peak O₂ in young athletes from various sports.

Traditionally and conventionally, peak O₂ is expressed as a ratio standard, or per kilogram of body mass (ml · kg¹ · min¹). When expressed as the simple ratio standard, peak O₂ remains stable in boys and declines in girls during adolescence (21). By expressing peak O₂ in this manner, it is assumed that peak O₂ is "normalized" and the influence of body mass is removed. However, the theoretical and statistical limitations of the ratio standard have been widely addressed yet largely ignored (37, 40). Therefore, alternate statistical models, including analysis of covariance (ANCOVA), allometric scaling, and multilevel modeling, have been used to create a "size-free" expression of peak O₂. The mathematical model that is widely used to create a size-free variable is allometry. Besides the calculation of cross-sectional allometric scaling factors, intraindividual, or ontogenetic, scaling factors can be calculated from longitudinal records. Ontogenetic allometry refers to differential growth in the individual growth process (15). Few studies have employed ontogenetic allometry to examine growth-related changes of peak O₂ in young athletes (9, 27, 34).

The purpose of this study is to examine age- and sex-associated variation of peak O₂ in competitive young distance runners from an allometric scaling perspective.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

Design

Subjects

YRS I. Runners between the ages of 8 and 15 yr, who consistently placed within the top five finishers of road races of 10 km or more by age and sex, were identified and contacted for the study. Race results were obtained from a statewide running publication, Michigan Runner, between May and August 1981. Of the runners contacted (response rate unknown), 27 boys and 27 girls agreed to participate in the study. Subjects entered the study at 8.0-15.7 yr of age and were followed annually. Twenty boys and 17 girls were followed at approximately annual intervals for 3-5 yr. The remaining subjects (7 boys and 10 girls) participated in either one or two annual visits. Each age and sex group included only one observation per subject; thus, the subjects were treated as independent in each age group. Totals of 99 and 84 annual measurements were available for boys and girls, respectively. In a subsample of subjects (16 boys, 19 girls), reported training volumes were 38.9 ± 17.6 and 35.8 ± 15.2 (SD) km/wk in boys and girls, respectively. Parental consent and child assent was obtained before the study. The study was approved by the Michigan State University Committee for Research Involving Human Subjects.

YRS II. Forty-eight boys and 22 girls, 10-19 yr of age, agreed to participate in the study. Eligible subjects participating on local Michigan junior or senior high school cross-country teams or local track clubs during fall 1999 and spring 2000 were invited to participate. Subjects who had trained <30-40 wk/yr or nonconsecutively during the past three consecutive months were excluded to ensure a sample engaged in regular participation in long-distance running. Reported training volumes were 47.7 ± 22.8 and 35.2 ± 13.8 (SD) km/wk in boys and girls, respectively. Parental consent and child assent was obtained before the study. The study was approved by the Michigan State University Committee for Research Involving Human Subjects.

Anthropometry

YRS I. Chronological age was calculated as the difference between observation date and birth date and was expressed as a decimal age. Anthropometry was conducted by two experienced anthropometrists according to standard procedures (38). Stature was measured with a fixed stadiometer. Body mass was measured with the subject attired in gym shorts and T-shirt without shoes on a balance beam scale. Measurements were conduced between early morning and midafternoon. Intra- and/or interobserver reliabilities were not reported.

YRS II. Chronological age was calculated as the difference between observation date and birth date and was expressed as a decimal age. Stature and body mass were measured according to the procedures of the International Biology Program (38). Stature was measured with a fixed stadiometer. Body mass was measured with the subject attired in gym shorts and T-shirt without shoes on a balance beam scale. The stadiometer and scale were calibrated periodically during the study. Intraobserver reliability was conducted on a small subsample by the principal investigator (Eisenmann). The intraclass correlation coefficient was 0.99 for both stature and body mass, whereas the intraobserver technical errors of measurement were 0.42 cm for stature and 0.08 kg for body mass.

Measurement of maximal O₂

YRS I. An intermittent progressive treadmill protocol consisting of 3-min work intervals and 3-min rest intervals until volitional exhaustion was used to determine peak O₂. The protocol began with a warm-up at 6 mph and 0% grade. After the warm-up, the grade was increased to 5%. Speed increased 1 mph, and grade increased 1% in each subsequent stage until volitional exhaustion. Expired gases were collected using the Douglas bag method. Gas concentrations were analyzed with Beckman oxygen and carbon dioxide analyzers within 2 min after collection. Gas volumes were measured with a Parkinson-Cowan CD2 dry gas meter. Before testing, expired gas volumes were calibrated with a 3-liter syringe, and gas concentrations were calibrated with standard gases of known concentrations. Heart rate (HR) was monitored using a commercial electrocardiogram. End-of-test criteria were established by volitional exhaustion, HR 90% of age-predicted maximum, respiratory exchange ratio >1.0, and a plateau in O₂ (defined by an increase in O₂ of <2.0 ml · kg¹ · min¹ with increasing workload). Two of the latter three criteria must have been met for a subject to be included in the analysis.

YRS II. A maximal exercise test was conducted on a motorized treadmill to exhaustion in an air-conditioned laboratory (20-22°C, relative humidity 45-60%). The treadmill protocol was determined by the subject's estimated 5-km race pace. Subjects walked/jogged at a speed of 3 and 4.5 miles/h for 1 min each. This initial warm-up period was followed by 4-min stages at 6, 7.5, and 8 miles/h (depending on an estimated 5-km race pace) and then increased in grade of 2.5% every minute until exhaustion or test termination. Expired gases were collected for the measurement of O₂, carbon dioxide production, and minute ventilation. Expired gases were continually sampled and averaged every 20 s via the open-circuit method using a metabolic cart (model 2900; Gould, Dayton, OH). Expired gas volumes were measured with a flow probe anemometer, and expired gas concentrations were measured by electronic analyzers. Before testing, expired gas volumes were calibrated with a 3-liter syringe, and gas concentrations were calibrated with standard gases of known concentrations. HR was monitored continually by pulse telemetry (Polar Advantage). End-of-test criteria were established by volitional exhaustion, HR 90% of age-predicted maximum, respiratory exchange ratio >1.0, and a plateau in O₂ (defined by an increase in O₂ of <2.0 ml · kg¹ · min¹ with increasing workload). Two of the latter three criteria must have been met to be included in the analysis.

Statistical Analysis

Allometric Scaling

1

1

The allometric relationship between body size and peak O₂ is based on the general allometric equation

(1)

where y is absolute peak O₂, x is body mass, b is a scaling factor, and a is the proportionality constant. The statistical approach to allometry is to use a logarithmic transformation as follows

(2)

where b is the slope of the linear regression line on a double logarithmic plot. The slope is calculated by regression analysis, where b in the regression output is equal to the scaling factor, and the inverse log of log a is equivalent to the constant (a) in Eq. 1. ANCOVA of log-transformed data was used to confirm the allometric analysis and generate adjusted means for age- and sex-specific groups.

Ontogenetic Allometry

Regression Diagnostics

0.75

1

	RESULTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

Age- and sex-specific anthropometric and peak O₂ values are reported in Tables 1 and 2. Stature reaches a plateau at 17 yr in boys and 15 yr in girls. Body mass progressively increases across age in both sexes. Before 14 yr, girls are taller and heavier than boys; thereafter, boys are taller and heavier than girls. Mean statures for both boys and girls approximate the medians of U.S. reference values (16), and mean body mass for both boys and girls is somewhat below the reference medians. Stature and mass also maintain their position relative to the reference values across age (13).

View this table: [in this window] [in a new window]   Table 1.   Age-specific values for body size and peak O2 in male distance runners

View this table: [in this window] [in a new window]   Table 2.   Age-specific values for body size and peak O2 in female distance runners

Means for absolute peak O₂ (ml/min) increase with age in both sexes (P < 0.05). Absolute differences between the sexes are small (134-186 ml/min) before 14 yr, when the differences increase sharply in each age group and reach a mean difference of 1000-1,500 ml/min in the oldest age groups (P < 0.05).

There is no significant age-related trend for peak O₂ expressed as the simple ratio standard (ml · kg¹ · min¹; P > 0.05). Means of relative peak O₂ remain stable in boys between 9 and 15 yr (61-63 ml · kg¹ · min¹) and are insignificantly higher in the older age groups (65-67 ml · kg¹ · min¹). In girls, means for relative peak O₂ remain stable between 9 and 15 yr of age (55-58 ml · kg¹ · min¹) and decrease insignificantly in the oldest age groups (52-53 ml · kg¹ · min¹). Sex differences vary between 5 and 7 ml · kg¹ · min¹ before 16 yr and increase to 12-15 ml · kg¹ · min¹ in the oldest age groups (P < 0.005). When peak O₂ is expressed to the theoretical value of body mass 0.75, it increases significantly with age (P < 0.05). Similar to absolute values, sex differences are small before 15 yr and then increase (P < 0.05 at all age groups).

Peak O₂ adjusted for body mass also shows a significant age-related increase (P < 0.05). The largest differences in adjusted means occur in the youngest and oldest age groups (600-750 ml/min). Mean differences between 12 and 15 yr of age are 410-475 ml/min, and there is a significant age group × sex interaction in adjusted means (P = 0.001).

Results of the cross-sectional allometric analysis are shown in Table 3. Overall, body mass exponents are 1.01 ± 0.03 (SE) and 0.85 ± 0.05 (SE) in boys and girls, respectively. The adjusted r² is 0.89 in boys and 0.75 in girls. Age-specific scaling factors are closer to the theoretical values of 0.67 and 0.75 in boys, but do not fit the model closely, and in two age groups are not significantly different from zero. In girls, three of the eight age-specific models are not significantly different from zero. The significant models have scaling factors between 0.53 and 0.89. In general, the age-specific models fit better in boys than girls. The cumulative effect of multiple age groups on the overall scaling factor is also shown in Table 3. Although age-specific scaling factors differ from those calculated for the entire sample, this may be due to small age-specific sample sizes and a lack of variation in body mass and peak O₂ within age-specific groups. Scaling factors begin to approximate the overall sex-specific scaling factor when multiple age groups are considered.

The computation of Tanner's "special circumstance" (37) and other diagnostic results are reported in Table 4. Body mass is significantly related to absolute peak O₂ in boys (r = 0.95) and girls (r = 0.87). As a group, there is a similarity between r (body mass and absolute peak O₂) and CV for boys. Age-specific calculations produce divergent ratios, especially in girls, suggesting a nonlinear relationship. As a group, the correlations between the simple ratio standard and body mass are 0.07 and 0.41 in boys and girls, respectively. Correlations between scaled peak O₂ and body mass are 0.71 and 0.03 in boys and girls, respectively. Correlations between absolute residuals and log body mass are 0.07 and 0.11 in boys and girls, respectively. Age-specific correlations vary between the sexes, with coefficients approaching zero in some age groups when peak O₂ is expressed per unit body mass 0.75. Correlations do not approach zero in any age group in girls.

View this table: [in this window] [in a new window]   Table 4.   Diagnostic criteria for the relationships between peak O2 and body size

In general, the intraindividual (ontogenetic) linear regression shows a better fit in boys than girls. In boys, 4 of 20 scaling factors are not significantly different from zero (P > 0.10). Logarithmically transformed peak O₂ and mass are highly related (r > 0.85) in all but one male subject. In contrast, scaling factors are significantly different from zero in 6 of 17 girls. The relationship between logarithmically transformed peak O₂ and mass is high (r > 0.85) in eight girls and moderate (0.40-0.85) in seven others. Based on a combination of the correlation coefficients and least-squares regression model, one male and two female subjects were eliminated from the analysis.

Ontogenetic scaling factors show considerable variation (range, 0.51-1.31 and 0.29-0.90 in boys and girls, respectively). Five boys exhibit scaling factors 0.99. The mean (95% confidence interval) ontogenetic scaling factors are 0.81 (0.71-0.92) and 0.61 (0.50-0.72) in boys and girls, respectively (P = 0.002 between-group differences).

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

This study examined age- and sex-associated variation in peak O₂ of 9- to 19-yr-old distance runners and provides unique information from three perspectives. First, previous studies are generally limited to a relatively narrow age range (i.e., 11-15 yr) and therefore do not describe growth-related changes in peak O₂ across the entire adolescent period. Second, only one longitudinal study (7) has included girls across a broad age range in childhood and adolescence. No study has included young distance runners of both sexes 9-19 yr. Third, this study used allometric scaling techniques to interpret the age- and sex-associated variation in peak O₂ of young distance runners.

The observed values for absolute and relative peak O₂ expressed per unit body mass in this sample of young distance runners are similar to those previously reported in longitudinal studies of young endurance athletes (Figs. 1 and 2). Limited information is available on the age-related trend in female athletes. In the general population of normal, healthy girls, relative peak O₂ decreases during adolescence (21). In the only study that reported age (maturity)-specific values, relative peak O₂ remains stable at ~52 ml · kg¹ · min¹ in pre-, mid-, and late-pubertal swimmers (7). More evidence is needed to establish if the age-related decline of peak O₂ in adolescent girls is attenuated with exercise training.

View larger version (17K): [in this window] [in a new window]   Fig. 1.   Longitudinal studies of absolute peak oxygen consumption (O2) in male athletes.

View larger version (19K): [in this window] [in a new window]   Fig. 2.   Longitudinal studies of relative peak O2 in young athletes. Solid lines represent age-related changes in the general population.

Many authors have argued the interpretation of the growth-related changes in peak O₂ on the basis of theoretical and statistical limitations of the simple ratio standard (1, 7, 34, 40). Therefore, alternate statistical models, including allometric scaling, ANOVA, and multilevel modeling, have been used in an attempt to create a size-free expression of peak O₂. The use of alternate models has resulted in different interpretations of growth-related changes in peak O₂ when expressed per body mass^0.75. Previous studies have shown an increase in scaled peak O₂ in boys (20, 29, 32, 34, 39). Armstrong and colleagues (1, 2, 39) have used adjusted means produced from ANCOVA (controlling for body mass) to explore age- and growth-related changes in peak O₂ of normal, healthy children and adolescents. The results generally indicate an increase in adjusted means across age and maturity groups in boys and an increase in adjusted means from prepuberty to puberty and similar values between puberty and young adulthood in girls. The results suggest that peak O₂ remains constant from late adolescence into young adulthood in girls.

Recently, multilevel modeling has been applied to investigate the growth-, maturity-, and training-related changes in peak O₂ (7, 40). Multilevel modeling attempts to partition the independent and multiplicative effects of age, body size and composition, pubertal status, and exercise training on a dependent variable (e.g., peak O₂). Studies using multilevel modeling have demonstrated size-independent effects of sex and maturity on peak O₂ (3, 7). Results from the Training of Young Athletes (TOYA) study indicate that peak O₂, controlling for age and body size, increases with pubertal status in male and female athletes, although an increase between mid- and postpubescent groups in boys is not evident in girls (7). The results are intriguing, given past assumptions about growth-related changes in peak O₂. However, despite acclaimed usefulness in the analysis of longitudinal data, the biological significance of the results derived from the multilevel modeling approach is difficult to interpret.

Sex differences in peak O₂ during growth and maturation are well documented in the general population of normal, healthy children and adolescents (1, 21). Less information is available on age-specific differences of young athletes due to the lack of longitudinal studies of female athletes and the narrow age ranges reported in cross-sectional studies. A significant age × sex group interaction in the present study indicates a progressive divergence in peak O₂ that can probably be related to differences in body composition, hematological factors, and perhaps exercise training volume and intensity.

Mean cross-sectional scaling factors are similar to those reported for body mass and peak O₂ in cross-sectional analyses of longitudinal data of other male athletes (23, 27) and cross-sectional analysis of 6- to 17-yr-old boys and girls (11). However, mean scaling factors reported in the literature show considerable variability (14). Age-specific scaling factors in this study show considerable disparity with estimates for the total sample (Table 4). In both sexes, age-specific scaling models do not represent a good fit, as indicated by adjusted r² values and nonsignificant log-linear regression models. This observation probably reflects the small range of body size within an age group (10), small age-specific sample sizes, confounding influences of biological maturity status (9), and differences in body composition, especially among girls. Indeed, when multiple age groups were considered, scaling factors began to approximate the overall sex-specific scaling factor.

Table 5 provides a summary of longitudinal studies using ontogenetic scaling. The mean ontogenetic scaling factor of 0.81 in boys is considerably less than previous studies of highly trained adolescent athletes (27, 34). In contrast, similar results have been obtained for active boys in the Saskatchewan Growth Study (unpublished observation) and early- and late-maturing boys training in Polish sports schools (track, wrestling, or basketball; see Ref. 9). The mean scaling factor in the present study is actually higher than that in late-maturing boys from the Polish sports schools. The mean ontogenetic scaling factor in female distance runners is higher than maturity-grouped girls from Polish sports schools (track or rowing; see Ref. 9) and lower than recreational sport participants (32). Ontogenetic scaling factors in 10 of 16 female distance runners are not significantly different from zero, indicating that the growth of peak O₂ is not related to growth in body mass. The lack of fit in female runners also reflects a plateau or decline in peak O₂ with age (9), as typically observed in female adolescents. Therefore, the higher scaling factor found by Rowland et al. (32) may be due to age-associated variation, as the mean age at entry in their study was 9.2 yr, whereas most of the female subjects in the present study entered at 12-14 yr of age.

Previous studies also show considerable variability in individual scaling factors (Table 5). It has been suggested that variability in scaling exponents is due to factors other than body mass, including individual variation in geometric similarity, changes in the ratio of leg muscle mass to body mass, differences in physical activity and/or training level, and individual differences in rates of development of size-independent factors such as skeletal muscle oxidative enzyme capacity or myocardial contractility (32). The last-mentioned factors would suggest that qualitative changes in the functional capacity of specific subcomponents of the oxygen transport system also contribute to the growth-related changes in peak O₂. The observed variability in the ontogenetic scaling factors may be related to a maturity-associated variation in body mass and peak O₂. Given the individuality of timing and tempo of maturation, year-to-year changes in body mass and peak O₂ may have been masked by maturity effects. Maturity-associated variation in peak O₂ has been estimated recently using various statistical models (2, 7-9). Peak O₂ increases at a slightly higher rate in early and average-maturing boys than expected from the increase in body mass (unpublished observation; see Ref. 9). In one study, the increase is smaller than expected in later-maturing boys (9). In the present sample of distance runners, differences in biological maturity were evident, as determined by skeletal age estimated from the hand-wrist X-ray obtained on the first visit. The mean difference between chronological age and skeletal age was 0.52 in 12 boys and 0.57 in 10 girls. Unfortunately, an insufficient number of subjects was available for the analysis of skeletal maturity. Future studies should consider maturity-associated variation in peak O₂.

Most important to this study is the identification of an appropriate model to interpret growth-related changes in peak O₂ of young distance runners, and children and adolescents in general. Several authors argue that peak O₂ should be expressed in accordance with theoretical values according to the dimensionality theory (i.e., ml · kg^0.67 · min¹ or ml · kg^0.75 · min¹; see Refs. 1, 17, 19, 25, 29, 36). The first step in the investigation of appropriate scaling procedures should involve the calculation of Tanner's special circumstances (5). If r is equal, or approximately equal, to the ratio of the CVs, a linear relationship is evident, and the simple ratio standard (ml · kg¹ · min¹) is appropriate. Conversely, if these two terms are not similar, a linear relationship does not exist, and the appropriate power function ratio should be calculated. Other regression diagnostics used in this study (i.e., correlations between residuals, simple and power function ratios, and body mass) were used to examine if the influence of body mass was removed (i.e., the correlation should not be different from 0 if the influence of body mass has been removed; see Refs. 5 and 39). On the basis of these criteria, the simple ratio standard could be empirically justified in boys, whereas the power function ratio could be empirically justified in girls (Table 3). Other authors (4, 6) have also concluded that the mass exponent for peak O₂ is close to unity.

In conclusion, the results of this study suggest that the interpretation of growth-related changes in peak O₂ of young distance runners is dependent on the expression of peak O₂ relative to body size and/or the statistical technique employed. Considerable variability in individual growth patterns in scaled peak O₂ points to the fact that determining a single scaling factor is difficult and may actually be problematic given the genetic, environmental, and genetic-environmental interactions that influence peak O₂. The most appropriate means of normalizing peak O₂ for body size still remains problematic (31, 32). Exercise scientists have been criticized for not recognizing the imperfections of ratio standards and being unaware of alternative methods for partitioning the effects of body size in human studies (40). However, it remains to be demonstrated if allometric scaling among a small magnitude of variation in body size warrants such statistical manipulation. According to Calder (10), small size ranges within a species obscure overall trends, patterns, and constraints of size. Thus scaling differences in body size among a small range of body sizes to understand variation in biological function may be of limited value. In contrast, others argue that scaling body size helps us to understand the growth and maturation of the oxygen transport system and its response to submaximal and maximal exercise (1). To solve the problem of the structural and functional consequences of changes in size or scale among growing and maturing children and adolescents, pediatric exercise scientists should perhaps collaborate with comparative mammalian physiologists for whom the statistical tool of allometry has been central for many years.