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Development of muscle strength in relation to training level and testosterone in young male soccer players

1Department

L. HANSEN,1 J. BANGSBO,1 J. TWISK,2 AND K. KLAUSEN1 of Human Physiology, Institute of Exercise and Sport Sciences, University of Copenhagen, DK-2100 Copenhagen, Denmark; and 2Institute for Research in Extramural Medicine, Vrije Universiteit, 1081 Amsterdam, The Netherlands Muscular strength increases more or less linearly with age from early childhood in boys. Strength is known to be related to the physiological cross-sectional area of the muscle and hence, according to a dimensional analysis, related to the second power of body height. During growth the cross-sectional area would then be expected to increase, with the square of the increase in the linear dimension. Some studies have shown that strength development in boys improves more than can be explained by increase in height squared (1, 8), indicating that factors other than quantitative changes play a role in the development of strength. Thus the marked acceleration of muscle strength during puberty observed in boys is possibly related to the elevated levels of circulating androgen hormones in adolescents. In a cross-sectional study of 11- to 13-yr-old athletic boys, Mero et al. (20) found that muscle ber area correlated well with serum testosterone. Maturation of the metabolic response to exercise might be related to the hormonal changes [increases in testosterone, estradiol, growth hormone, and insulinlike growth factor I (IGF-I)] occurring during puberty (9, 19). On the basis of a difference in increase in strength between boys and girls, Parker et al. (21) suggested that testosterone may stimulate muscle growth. The growth-promoting effect of growth hormone is mediated by somatomedins, particularly IGF-I (16). However, no longitudinal study has measured changes in blood hormone concentrations and related them to changes in muscle size and strength of children and adolescents (23). As indicated by Rochcongar et al. (22), soccer training at an elite level might increase leg strength, but it is also possible that the boys selected for the elite level are stronger because of higher levels of circulating hormones. The aim of this investigation was to study the development in strength of boys playing soccer at an elite and a nonelite level and to examine the association between the development in strength and testosterone concentration. Both questions were addressed with correction for age, body size dimensions, and IGF-I.
METHODS

Hansen, L., J. Bangsbo, J. Twisk, and K. Klausen. Development of muscle strength in relation to training level and testosterone in young male soccer players. J. Appl. Physiol. 87(3): 11411147, 1999.Isometric and functional strength of ninety-eight 11-yr-old male soccer players at an elite (E) and nonelite (NE) level were determined (34 times) through a 2-yr period, and the changes were related to growth and maturation. The initial isometric strength for extension with dominant leg [1,502 35 (E) vs. 1,309 39 (NE) N], extension with nondominant leg (1,438 37 vs. 1,267 45 N), extension with both legs (2,113 76 vs. 1,915 72 N), back muscles (487 11 vs. 414 10 N), abdominal muscles (320 9 vs. 294 8 N), and handgrip (304 10 vs. 259 8 N) increased by 1540% during the period. Broad jump increased (P 0.05) by 15 (E) and 10% (NE). The E players had higher (P 0.05) initial isometric strength and broad jump performance compared with NE players, and differences were maintained throughout the period (multiple ANOVA for repeated measures) also when adjustment was made for age, dimensions, testosterone, and insulin-like growth factor I (generalized estimating equations analyses). The development of strength for both E and NE players together was signicantly (P 0.001) related to changes in serum testosterone concentrations. The present data indicate that testosterone is important for development of strength in young boys and that, independent of serum testosterone concentration, E players have developed greater muscle strength compared with NE players. elite and nonelite players; age; dimensions

IN ADULTS, substantial knowledge is present about factors that determine muscle strength and its change with training (e.g. Refs. 13, 15), but less information is available about development of muscle strength in children. Rochcongar et al. (22) found that young French elite soccer players had greater isokinetic leg strength compared with high school students, indicating that soccer training has an effect on the development of muscle strength. In contrast, Maffulli et al. (18) found that athletic boys (including soccer players) until the age of 15 yr had similar isometric quadriceps strength as did nonathletic boys, and after this age the strength of the athletic group was signicantly higher compared with nonathletic boys. The latter nding may indicate that the training responses are affected by maturation.

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Subjects. One hundred and ten young male soccer players from seven successful clubs in the area of Copenhagen, at the highest level in their age category, were recruited as subjects. All participants and their parents gave their informed consent, and the study was approved by the Ethics Committee of Copenhagen, Denmark (KF 01132/95). Clubs that had at least four teams in the same age categories were selected (to ensure differences between elite and nonelite players). The
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1999 the American Physiological Society

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STRENGTH AND DEVELOPMENT IN YOUNG SOCCER PLAYERS

boys were included in the study at the age of 1012 yr according to the selection age at the competition levels. One-half of the boys were recruited from the best team to which they were selected by the coach (elite players), and the other one-half were recruited from the lowest ranked team (nonelite players) from the same club. Measurements were taken three times at 0.5-yr intervals for all the boys, and, in addition, 28 of the subjects (16 elite, 12 nonelite) were also studied a fourth time. Eight boys were excluded from the study because they were not members of the same team during the whole study, two because they did not want to participate after the rst test and two because they moved to another part of the country. Thus 98 subjects were included with 48 boys in the elite group and 50 boys in the nonelite group. During the study some boys stopped playing soccer and were then excluded from subsequent tests. Thus 87 boys were tested three times, and 28 of these were also tested a fourth time. The players included in the study had participated in organized soccer for 6.3 (elite) and 4.4 (nonelite) yr with a signicant difference (1.9 yr; P 0.05) between the groups. As shown in Table 1, the elite players were playing soccer for more hours per week and were in general more physically active compared with the nonelite players. The leisure time activity registered consisted mostly of soccer with friends but also roller-skating and high-activity play as well as participation in other organized sports. The age of the subjects was assessed to the nearest 0.01 yr. Standing and sitting height were measured by a stadiometer to the nearest 0.1 cm, and body weight was measured to the nearest 0.1 kg by using a spring balance. The body mass index (BMI) was calculated as body weight (kg) divided by height (m) squared. Bicipital, tricipital, subscapular, and suprailiacal skinfolds were measured with a Harpenden skinfold caliper, and the sum of these four skinfolds was calculated. The pubertal developmental stages were recorded by one experienced pediatric endocrinologist on the basis of assessment of secondary sex characteristics by using the criteria of Tanner (25) and from testicular volume estimated from measurements of the size of the testes by using a Prader orchidometer (29). Blood samples were drawn from an antecubital vein between 1600 and 1730 and were centrifuged. Serum was stored at 20C and later analyzed for levels of testosterone and IGF-I. The sensitivity of the assay for IGF-I was 0.041 g/l (12), and the sensitivity for testosterone was 0.23 nmol/l. Values less than assay sensitivity were assigned the value of assay sensitivity. Strength measurements. The subjects were all familarized with the testing procedures as well as with the investigators before the test. All subjects had a standardized warm-up period, including 5 min of cycling on a Monarck bike, before the strength measurements. All subjects started with the broad jump followed by measurements of isometric strength. Broad jump was performed as a two-foot takeoff and landing. The takeoff was from behind a line on the oor, and the

landing was on a 2-cm-thick mat on which the subjects were instructed to land on their feet. The distance from the takeoff to the point where the nearest heel touched the mat was measured, and the best of three recorded trials was used as the performance score (cm). The maximal voluntary isometric strength [maximal voluntary contraction (MVC)] of the leg extensors was measured by using a strain-gauge dynamometer in a standardized seated position with support of the back (4). To measure MVC of the trunk muscles in a standing position, a strain-gauge dynamometer was connected to a frame placed around the trunk 20 cm below the shoulders by the use of two straps (4). Grip strength was measured with a hand dynamometer in subjects while seated and for the dominant arm only. The boys were all encouraged to the highest effort by the investigators, and the best of three attempts was accepted as maximal. The training regimen and competition intensity were evaluated for a subgroup of the original subjects (n 30, 10 teams). The competition intensity was evaluated from heart rate measurements by a heart rate monitor (Polar) both during competition and while the subjects ran on a treadmill with simultaneous measurements of oxygen uptake. The elite players had higher relative oxygen uptake in competition compared with the nonelite group (79.4 5.3 vs. 67.3 10%; P 0.05). For the elite and nonelite players, 27 vs. 7% of the training consisted of tness training (sprint run, etc.), 61 vs. 39% was technical training, and 12 vs. 54% was play. No supplemental weight training was used. Statistics. To assess the longitudinal relationship between strength and soccer ability (elite or nonelite), two analyses were carried out. 1) In the rst analysis, the differences in longitudinal development of strength measurements between elite and nonelite soccer players were analyzed with multiple ANOVA (MANOVA) for repeated measures (SPSS; Ref. 24). 2) In the second analysis, the longitudinal relationship between strength and soccer ability (elite or nonelite) was analyzed with generalized estimating equations (GEEs) (30), a longitudinal linear regression technique that is extensively described elsewhere (26, 27). The advantages of using this method are that all available longitudinal data are used to estimate the regression coefficients and that the method is suitable for designs with unequally spaced time intervals. Furthermore, it allows a correction for both time-dependent and time-independent covariates and the method takes into account that the repeated observations on each individual are not independent. GEE analysis was also carried out to analyze the longitudinal relationship between strength parameters and testosterone concentration. For all GEE analysis, a univariate analysis was carried out rst. After that, separate analyses were carried out correcting for age, body size dimensions, and IGF-I concentration. All GEE analyses were carried out with the Statistical Package for Interactive Data Analysis (10). Signicance was accepted at P 0.05.

Table 1. Amount of time with organized soccer training (including competitions) and with physical activity in leisure time, including participation in other sports
Test Round 1 Organized Leisure Organized 2 Leisure Organized 3 Leisure Organized 4 Leisure

Elite Nonelite

6.1* 5.1

11.7* (19) 6.4 (26)

6.2* 5.2

10.7* (16) 7.0 (20)

6.5* 4.8

11.9 (19) 10.6 (9) 0.05.

7.4* 5

11.4 (9) 10.2 (10)

Values are given in h/wk with % in parentheses. * Signicant different from nonelite players, P

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Table 2. Characteristics of subjects


Test Round 1 Elite Nonelite Elite 2 Nonelite Elite 3 Nonelite Elite 4 Nonelite

Age, yr n Height, cm Body mass, kg BMI, kg/m2 Skinfold, mm Testes volume, ml n

11.9 48 152.7 41.0 17.5 27.6 5.8 45

0.5 6.8 5.9 1.6 6.9 3.5

11.6 0.7 50 147.4 6.6 37.9 6.5 17.4 2.1 33.7 14.3 3.9 1.9 49

12.4 0.5 44 155.7 7.3 43.6 5.97 17.9 1.5 28.3 6.8 7.6 4.9 43

12.1 0.7 47 150.1 6.9 40.0 7.0 17.7 2.3 35.1 15.4 5.0 3.3 47

12.9 0.5 44 160 8.3 46.6 7.1 18.1 1.6 27.5 6.4 9.3 5.4 43

12.5 0.7 43 154.3 8.1 43.0 7.7 17.8 2.1 36.1 15.6 6.6 3.9 42

13.5 0.6 16 166.3 10.0 53.2 8.8 19.1 2.1 29.2 7.3 12.1 6.5 16

13.8 0.4 12 160.4 7.2 47.7 7.3 18.5 2.7 39.3 18.5 9.3 5.4 12

Values are means SD; n, no. of subjects. BMI, body mass index; skinfold, sum of 4 skinfolds (biceps, triceps, subscapularis, suprailiac). For height, body mass, BMI, and skinfold n is the same as for age. Each test round was carried out at 0.5-yr intervals. RESULTS

The characteristics of the subjects are presented in Table 2. The elite players were slightly older than the nonelite players (0.4 yr; P 0.05). When adjustment was made for age, the elite players were signicantly taller (P 0.05) and had lower values for skinfold measurements (P 0.05). The elite players had greater testicular volume than did the nonelite players and higher serum testosterone concentration (Fig. 1; P 0.05). No signicant differences between the groups in BMI or IGF-I (Fig. 2) were present. Figures 36 show the development in strength parameters for elite and nonelite players. Differences in development between the two groups were analyzed by MANOVA for repeated measures. The results of these analyses (Table 3) showed that elite players had higher values (P 0.05) compared with nonelite players for all strength parameters throughout the measurement period. The increase in strength over time was, however, similar in both groups, i.e., no signicant elite/nonelitetime interaction for any of the strength parameters. No

signicant differences in development between the groups according to Tanner stages were present (MANOVA for repeated measures). The results from the GEE analysis regarding the longitudinal relationship between being an elite player/ nonelite player and strength development are presented in Table 4. In univariate analysis a signicant positive relationship was found between all strength parameters and being an elite player. In general, with an adjustment for age, the regression coefficients for elite/nonelite players decreased slightly; a more marked decrease was found for the relationship with leg extension by using both legs. Adjustment for body dimensions also led to a decrease in regression coefficients. When the relationships between elite/nonelite player and strength were adjusted for height, weight, and sum of skinfolds, as well as for numbers of years of training in organized soccer, only the relationships with back muscles and handgrip remained signicant (P 0.05). When adjustment was made for serum testosterone and IGF-I, a small decrease in regression coefficients was observed; however, the positive relationships between all strength parameters and being an elite player remained highly signicant.

Fig. 1. Serum testosterone concentrations. Measurements were taken at 0.5-yr intervals starting when the subjects had a mean age of 11.9 0.5 (SD) (elite) and 11.6 0.7 yr (nonelite). Values are means SE; n, no. of subjects. Dotted line indicates that the last test round included a reduced number of players (n 28). Difference (adjusted for age) between groups is signicant for 4 test rounds (P 0.015) with a tendency for signicance present for 3 test rounds (P 0.076).

Fig. 2. Insulin-like growth factor I levels in elite and nonelite young male soccer players. Values are means SE; n, no. of subjects. No signicant difference between elite and nonelite players was present.

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Fig. 3. Isometric strength for abdominal and back muscles measured in standing elite and nonelite young male soccer players. Values are means SE. Measurements were taken at 0.5-yr intervals starting when the subjects had a mean age of 11.9 0.5 (SD) (elite) and 11.6 0.7 yr (nonelite). Values are means SE; n, no. subjects for elite players/nonelite players in each test round. Difference between the groups is signicant: abdominal, P 0.011; and back, P 0.001.

Fig. 5. Isometric strength for leg extensors measured in seated elite (E) and nonelite (N-E) young male soccer players. Values are means SE; n, no. of subjects for elite players/nonelite players in each test round. Differences between the groups are signicant: both legs, P 0.004; dominant leg, P 0.002; and nondominant leg, P 0.01. DISCUSSION

The results of the GEE analysis regarding the longitudinal relationship between strength and serum testosterone are presented in Table 5. Univariate analysis showed a signicant positive relationship between development in all strength parameters and serum testosterone concentration. Adjustment for age, body dimensions, and IGF-I showed more or less the same picture as for the longitudinal relationships between being an elite/nonelite player and strength, i.e., in general, a decrease in regression coefficients. The adjustment for body weight, height, and sum of skinfolds led to a dramatic decrease in regression coefficients; i.e., none of the relationships between serum testosterone and strength parameters was signicant.

The present study showed that both elite and nonelite players through a 2-yr period had an increase in strength that was related to the levels of serum testosterone, indicating that testosterone is important for development of muscle strength in young boys. In addition, a strong positive relationship between being an elite player and the level of strength was observed. This relationship was independent of testosterone and IGF-I, indicating that the greater strength was not solely due the level of serum testosterone. Increases in muscle strength with age in young boys cannot simply be explained by growth, because it has been shown in both prepubertal and pubertal boys that strength increases more rapidly than does height (6). It

Fig. 4. Isometric handgrip strength (dominant hand) in elite and nonelite young male soccer players. Values are means SE; n, no. of subjects. Differences between the groups are signicant, P 0.002.

Fig. 6. Broad jump performance in elite and nonelite young male soccer players. Values are means SE; n, no. of subjects. Difference between the groups is signicant, P 0.002.

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Table 3. Results of MANOVA for 3 test rounds, carried out at 0.5-yr intervals on isometric strength and broad jump, testing the effects of team (elite/nonelite), time by team, and time of measurement
Team Time by Team Time of Measurement

Handgrip Abdomen Back Both legs Nondominant leg Dominant leg Broad jump

0.002 0.011 0.001 0.004 0.010 0.002 0.002

0.594 0.052 0.371 0.191 0.762 0.999 0.696

0.001 0.001 0.001 0.001 0.001 0.001 0.001

Values are P values adjusted for age (age as covariate). MANOVA, multiple ANOVA for repeated measures.

is more likely to be due to an interrelationship between several factors such as age, stature, weight, muscle size, and maturation (endocrine and neurological). From experimental data and from the recognition that testosterone has a prominent anabolic effect, it has been suggested that testosterone is responsible for the in-

crease in strength in male individuals at puberty (5). In the present study this is conrmed by a signicant positive relationship between development in all strength parameters and serum testosterone concentration. This relationship is dependent on anatomic dimensions and skinfold thickness, indicating that these factors also play a role in the development of strength. Asmussen and Heebll-Nielsen (2) suggested that, besides dimensions, age per se has a positive inuence on muscular strength, especially in tests that require a high degree of neuromuscular coordination. We found that the relationship between strength development and changes in serum testosterone was independent of age, except for leg extension with both legs. It has been shown for both children and adults (14, 28) that MVC for leg extension with both legs are less than the sum of MVC for each leg, indicating a limit in neural output. Furthermore, in the present study the percentile difference between the sum of the strength of each leg and both legs decreased with age [from 39 to 15% (elite) and from 34 to 22% (nonelite)], which is in agreement with Asmussen and Heebll-Nielsen (3), who showed a

Table 4. Longitudinal relationships between being an elite or a nonelite player and development of isometric strength/broad jump, adjusted for confounding factors
Leg Extension Univariate Analysis Abdominal Muscles Back Muscles Handgrip Dominant leg Nondominant leg Both legs Broad Jump

Elite/nonelite P 95% CI Adjusted for age P 95% CI Adjusted for dimensions: Height and body mass P 95% CI Height, body mass 4 skinfolds P 95% CI Adjusted for serum testosterone P 95% CI Adjusted for IGF-I P 95% CI Adjusted for years of training P 95% CI

0.000 44.1 67.320.8 0.048 22.1 44 to 0.17

0.000 71.3 101.3 to 41.3 0.000 54.1 81.0 to 27.3

0.000 49 72.8 to 25.2 0.000 41.9 63.4 to 20.3

0.000 239.3 354.3 to 124.2 0.057 112.8 228.93.2

0.000 242.8 365.4 to 120.2 0.046 121.7 241.4 to 2.1

0.001 413.4 651.2 to 175.6 0.226 165.4 433.5102.6

0.000 13.3 19 to 7.7 0.001 9.8 15.8 to 3.8

0.214 11.6 29.96.7

0.000 46.8 67.2 to 26.3

0.000 30.7 47.8 to 13.6

0.014 100.6 181.2 to 20.1

0.029 93.8 177.8 to 9.8

0.073 180 376.5 to 1.45

0.058 6.1 12.50.2

0.502 6.2 24.4 to 11.9

0.000 31.4 47.6 to 15.1

0.005 25.3 43 to 7.6

0.133 67.5 155.520.6

0.316 44.9 132.542.7

0.428 79.4 275.7117

0.507 1.9 7.43.7

0.006 29.4 50.4 to 8.5 0.003 35.4 59.1 to 11.7 0.91 1.6 29.4 to 29.4

0.000 62.2 89 to 35.4 0.000 66.8 94.9 to 38.7 0.038 34.4 66.9 to 1.9

0.000 39.7 61.1 to 18.3 0.000 46 69.2 to 22.8 0.004 34.3 57.8 to 10.7

0.004 158.1 266.5 to 49.9 0.002 185.6 301.7 to 69.4 0.763 22.2 122.2166.4

0.008 152.0 264.4 to 45.8 0.003 178.8 298.1 to 59.6 0.97 2.9 145.4151.1

0.032 249.8 478.5 to 21.1 0.014 305.7 550 to 61.4 0.719 54.7 353.4243.9

0.001 9.9 15.7 to 4.1 0.000 11.5 17.4 to 5.5 0.159 4.9 11.81.9

Values are P values, longitudinal regression coefficients ( ), and 95% condence intervals (CI) obtained from generalized estimating equations analysis. IGF-I, insulin-like growth factor I.

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Table 5. Longitudinal relationships, for both elite and nonelite players as one group, between serum testosterone levels and development of isometric strength/broad jump, adjusted for confounding factors
Leg Extension Univariate Analysis Abdominal Muscles Back Muscles Handgrip Dominant leg Nondominant leg Both legs Broad Jump

Testosterone P 95% CI Adjusted for age P 95% CI Adjusted for dimensions Height and body mass P 95% CI Height, body mass 4 skinfolds P 95% CI Adjusted for IGF-I P 95% CI

0.000 11 7.914.1 0.011 3.1 0.75.6

0.000 11.2 7.714.8 0.001 5.7 2.49.0

0.000 6.4 3.19.8 0.012 4.1 0.97.4

0.000 56.6 36.776.4 0.055 13 0.326.2

0.000 60 37.982.1 0.029 17.9 1.833.9

0.000 99.1 50.7147.6 0.442 14.4 22.351

0.000 2.3 1.72.9 0.000 1.1 0.51.7

0.829 0.3 2.32.8

0.165 2.3 0.95.5

0.575 0.9 2.24.1

0.484 5.0 9.119.2

0.572 5.2 12.723.0

0.636 9.6 30.149.3

0.029 0.8 0.11.4

0.604 0.7 3.31.9 0.000 8.8 5.212.4

0.726 0.7 3.25.1 0.000 8.9 4.613.2

0.790 0.5 1.12 0.000 6.1 2.99.3

0.991 0.1 14.113.9 0.000 46.3 22.770.3

0.834 1.9 19.215.4 0.000 46.7 20.972.6

0.758 5.8 42.831.1 0.008 86.9 22.6151.2

0.466 0.3 0.41 0.000 2.2 1.52.9

gradual decrease of this difference in male subjects aged 1535 yr. Thus dependency of age when examining extension with two legs (with some degree of neuromuscular coordination) could be explained by a requirement for a neuromuscular maturation possibly related to age. The nonelite players, while not as strong as the elite players, had almost the same strength values as did Danish schoolboys, aged 11 yr, who were examined in 1981 (11). It seems likely that the development of leg muscle strength in particular would give an advantage to the elite soccer player. Leatt et al. (17) showed a greater isokinetic and explosive strength in Canadian national soccer players who were under 18 yr old compared with the national players who were under 16 yr old. The elite players in the present study were also stronger compared with the nonelite players when a correction was made for the small difference in age between the two groups. The elite players were taller and more mature compared with the nonelite players, so the increase could be due to growth, maturation, or competition level. To examine this relationship, the GEE analysis was carried out. The difference in strength between elite players and nonelite players appears not to be due to the difference in height between the two groups because the difference was independent of dimensions, except for leg extension with both legs and broad jump, which only revealed a tendency for independence (P 0.073 and P 0.058, respectively). The relationship between strength development and elite/ nonelite was independent of serum testosterone and IGF-I, indicating that the development in strength was related to factors associated with being an elite player

independent of testosterone concentration. The reason for this increase in strength may be due to a greater relative increase in muscle mass of the elite players and thus a larger cross-sectional area of the muscles. Alternatively, it may have been caused by qualitative changes in the muscles such as a lower ratio of connective tissue to muscle tissue so that the same mass of musculature may be brought to produce more tension in the elite players. Leatt et al. found that elite players had more lean body mass compared with normal subjects. In the present study no difference in BMI was found between the two groups, but the elite players had less subcutaneous fat evaluated from skinfold measurements, which indicate a larger lean body mass in the elite players, possibly caused by muscle hypertrophy as a response to training. When the sum of skinfolds was included with dimensions in the GEE analysis of relationships between elite/nonelite and strength development, a dependency was found for leg extensions, abdominal muscles, and broad jump but not for back muscles and handgrip strength. This indicates that the development in strength is related to some extent to a hypertrophy of the muscles. It is also plausible that part of the difference in strength may result from a better mastery of the neuromuscular system in the elite players caused by the training regimen that the elite players were exposed to from an early age. The fact that the elite players were initially stronger compared with the nonelite players could partly explain why the increase in strength for the elite players during the test period did not lead to an increase in the difference between the two groups because strength is known to increase more from lower initial levels (e.g., Ref. 7). It cannot, how-

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ever, be excluded that the differences between the elite and nonelite players are due to an early selection of boys with higher strength for the elite group. In summary, development of isometric strength and performance in broad jump was related to changes in serum testosterone concentrations but also inuenced by body size, indicating that testosterone is important for development of strength in young boys. Furthermore, elite players were stronger than nonelite players independent of testosterone concentration also with correction for body size, indicating that being an elite player per se affected the development of strength.
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