Enhanced bone mass and physical fitness in young female handball players

Bone 35 (2004) 1208 – 1215 www.elsevier.com/locate/bone

Enhanced bone mass and physical fitness in young female handball players G. Vicente-Rodrigueza, C. Doradoa, J. Perez-Gomeza, J.J. Gonzalez-Henriquezb, J.A.L. Calbeta,* a

Department of Physical Education, University of Las Palmas de Gran Canaria, Canary Island, Spain b Department of Mathematics, University of Las Palmas de Gran Canaria, Spain Received 23 April 2004; revised 13 June 2004; accepted 18 June 2004 Available online 9 September 2004

Abstract This study evaluates the effect of physical activity on the bone content (BMC) and density (BMD) in 51 girls (14.2 F 0.4 yr). Twenty-four were placed in the handball group as they have been playing handball for at least 1 year (3.9 F 0.4). The other 27 who did not perform in any kind of regular physical activity other than that programmed during the compulsory physical education courses comprised the control group. Bone mass and areal density were measured by dual-energy X-ray absorptiometry (DXA). The maximal leg extension isometric force in the squat position with knees bent at 908 and the peak force, mean power, and height jumped during vertical squat jump were assessed with a force plate. Additionally, 30-m run (running speed) and 300-m run (as an estimate of anaerobic capacity) tests were also performed. Maximal aerobic capacity was estimated using the 20-m shuttle-run tests. Compared to the controls, handballers attained better results in the physical fitness tests and had a 6% and 11% higher total body and right upper extremity lean mass (all P b 0.05). The handballers showed enhanced BMC and BMD in the lumbar spine, pelvic region, and lower extremity (all P b 0.05). They also showed greater BMC in the whole body and enhanced BMD in the right upper extremity and femoral neck than the control subjects (all P b 0.05). As expected, total lean mass strongly correlated with total and regional BMC and BMD (r = 0.79–0.91 P b 0.001). Interestingly, 300-m running speed correlated with BMC and BMD variables (r = 0.59–0.67 and r = 0.60–0.70, respectively; all P b 0.001). Multiple regression analysis showed that the 30-m running speed test, combined with the height and body mass, has also predictive value for whole-body BMC and BMD (R = 0.93 and R = 0.90, P b 0.001). In conclusion, handball participation is associated with improved physical fitness, increased lean and bone masses, and enhanced axial and appendicular BMD in young girls. The combination of anthropometric and fitness-related variables may be used to detect girls with potentially reduced bone mass. D 2004 Published by Elsevier Inc. Keywords: Bone; Physical fitness; Children; Exercise

Introduction Bone health later in life may rely on the bone mass accumulation during growth [1]. In fact, the risk of osteoporosis is affected by the peak bone mass attained, in general, before the age of 20 [1], the bone mass accrual being most marked between 11 and 14 years of age in girls * Corresponding author. Departmento de Educacio´n Fisica, Campus Universitario de Tafira, 35017 Las Palmas de Gran Canaria, Canary Island, Spain. University of Las Palmas de Gran Canaria, Canary Island, Spain. Fax: +34 928 458867. E-mail address: [email protected] (J.A.L. Calbet). 8756-3282/$ - see front matter D 2004 Published by Elsevier Inc. doi:10.1016/j.bone.2004.06.012

[2]. It has been demonstrated that weight-bearing physical activities increase bone mass acquisition, particularly in weight-loaded skeletal regions in young population [3,4]. It becomes interesting to determine what kind and duration of sporting activities are the most beneficial for bone mass development during growth. Most of the investigations studying bone mass accrual in girls had been carried out with a gymnast population [3,5]. Ground reaction forces during gymnastic participation are close to 10 times body mass in child [6]. This high-impact loading has been associated with greater BMD in the whole body [5], spine, and lower extremities [3]. However, these studies show unreal training volumes in day-to-day exercise

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practice of ordinary physically active girls. The latter, combined with the increasing problem of sedentary behavior in children, has intensified the interest in exercise modes easy to prescribe with clear osteogenic effects for the general child population. There is clear evidence demonstrating that weight-bearing sporting activities involving rapid directional changes, starts, stops, and great ground reaction forces, promote bone deposition in prepuberal [7,8] and postpuberal [9] age. We have recently observed that prepuberal boys involved in this kind of activities had higher BMC and areal density than their weight-matched nonphysically active counterparts [7]. Girls are usually less physically active than boys [10]. However, handball is a sport widely practiced by girls around the world. In fact, apart from the recreational participants, 736,326 (26,291 from Spain) junior girls were affiliated to the International Handball Federation (IHF) in 2003 (Frank Birkefeld, IHF Managing Director, personal communication). This sport involves several sprints, which provoke high mechanical stress on lower extremity bones due to high reaction forces during sprinting [11]. During handball participation, a great number of rapid directional changes, starts, stops, jumps, and landings occur. Additionally, the upper extremities have a relevant role in this sport, as they are involved in different actions like throwing, fall landings, and ball blocks during defensive actions. All together, handball actions may entail excellent osteogenic properties on axial and appendicular bones [12]. However, to the best of our knowledge, we are not aware of studies examining the effect of recreational handball participation on bone mass in girls. This information could be used to propose scientifically grounded guidelines for sport participation designed to promote bone accumulation in girls. Therefore, the purpose of our study was to determine whether young girls participating in handball, at least 3 h per week, for a minimal period of 1 year, have additional osteogenic benefits to those obtained from the compulsory school physical education sessions (60–90 min of effective practice in Spain). A secondary aim was to determine to what extent BMC and BMD could be predicted by physicalfitness-related variables in girls.

Materials and methods Subjects A representative sample of Gran Canaria child and adolescent population was obtained by multiage stratified sampling, using as a reference the database of the ISTAC (Instituto Canario de Estadı´stica). In total, 325 healthy children and adolescent girls, aged between 7 and 20 years, were recruited from different schools and sports clubs of Gran Canaria. However, only 52 (14.2 F 0.4 year, mean F SEM) were included in the present investigation. Both parents and children were informed about the aims and

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procedures of the study, as well as the possible risks and benefits. Children and parents gave their written informed consent before the start of the study. The subjects were divided into two groups depending on their physical activity patterns. Twenty-four were assigned to the handball group as they have been playing handball for at least 1 year (3.9 F 0.4) and at least 3 times per week. The other 28, whose physical activities were limited to those included in the compulsory physical education curriculum (2 weekly sessions of 45 min each), were assigned to the control group. Most of handball players were recruited from sports clubs, while all the control group subjects were recruited from schools. The control group subjects did not participate in any kind of sport other than occasional children’s games, nor had they done so for at least 1 year before the study as they answered during a personal interview. The girls answered a medical and physical activity questionnaire, and their parents gave additional medical information. Daily intake of dairy products was obtained from every subject to calculate calcium intake, as was information regarding physical activity, past injuries, medication, and known diseases. In general, handball training sessions lasted for 1 h, including about 10 min of low-intensity games and stretching exercises, 10–25 min of technical handball exercises (throwing actions, dribbling, jumping, and running with fast accelerations and decelerations), and 20–30 min of handball match practice. Pubertal status assessment Tanner pubertal status was determined by autoevaluation, a method of recognized validity and reliability [13]. Physical fitness Dynamic and maximal isometric force The forces generated during vertical jumps were measured with a force plate (Kistler, Winterthur, Switzerland). Each girl performed a Squat Jump (SJ) and a countermovement jump (CMJ). The SJ started with knees bent at 908 and without previous counter movement. The CMJ started from the upright position. The jumping height (Hj), the peak force (Fp, being Fp=maximal force-body mass), and the mean power (Mp) generated were determined in the best of three trials. The maximal isometric force (MIF) during leg extension in the squat position (knees bent at 908) was also measured with the same force plate, described previously [14]. The knee angle was measured with a digital goniometer (Lafayette Instrument Company, Lafayette, IN). Briefly, for 5 s, subjects were encouraged to exert the highest strength in the lowest time possible. The best of three attempts, with 1 min rest period in between, was recorded. Anaerobic capacity A 300-m running test was used to estimate the anaerobic capacity because the anaerobic capacity is the first determi-

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nant of performance in maximal all-out efforts eliciting exhaustion between 30 and 60 s [15]. The test was performed on a 400-m track, and timings were measured manually. The girls were asked to run the 300 m as fast as possible. Running speed test The time needed to cover 30 m (T 30) was measured with photoelectric cells (General ASDE, Valencia). The timer is automatically activated when the subject crosses the first cell, every 5 m thereafter. The girls were motivated to run as fast as they could, and the best performance achieved in three trials separated by at least 1 min rest period was taken as the representative value of this test. Aerobic maximal power The maximal oxygen uptake (VO2 max) was estimated using a maximal multistage 20-m shuttle run test as devised by Luc Leger [16]. Subjects were required to run back and forth on a 20-m course and be on the 20-m line at the same time that a beep is emitted from a tape. The frequency of the sound signals increases in such a way that running speed starts at 8.5 kmd h 1 and is increased by 0.5 kmd h 1 each minute. The time the subjects were able to run for was recorded to calculate the VO2 max. This test has been shown to be valid and reliable for the prediction of the VO2 max [16]. Bone and lean mass The bone mass and lean mass (body mass [fat mass + bone mass]) were measured using dual-energy Xray absorptiometry (DXA) (QDR-1500, Hologic Corp., Software version 7.10, Waltham, MA). DXA equipment was calibrated using a lumbar spine phantom and following the Hologic guidelines. Subjects were scanned in supine position and the scans were performed at high resolution. Lean mass (g), fat mass (g), total area (cm2), and BMC (g) were calculated from total and regional analysis of the whole body scan. BMD (g cm 2) was calculated using the formula BMD = BMC area 1. The regional analysis was performed as described elsewhere [17]. Lean mass of the limbs was assumed to be equivalent to the muscle mass. Two additional examinations were conducted to estimate bone mass at the lumbar spine and proximal region of the femur. Bone mineral content and density values of the femoral neck, greater trochanter, intertrochanteric, and Ward’s triangle subregions are also reported. Statistical analysis Mean and standard error of the mean (SEM) are given as descriptive statistics. Differences between groups were established using Student’s unpaired t test. Analyses of covariance (ANCOVA) were performed to evaluate differ-

ences in bone and lean mass, entering height and body mass as covariates. The reason for using these covariates is based on evidence identifying height and body mass as influential factors on the growing skeleton [18]. Additionally, bivariate correlation and linear stepwise multiple regression was applied to identify the relationship between physical fitness, lean mass, and bone mass variables. To test the similarity of slopes and intercepts of these relationships, the corresponding t test was applied for the model: Yij = a i + b i X ij + e ij for i = 1, 2 (1 = footballers, 2 = controls) and j = 1,. . .,n 1 being e ij i.i.d. random variables following a distribution N(0,r 1). SPSS package (SPSS Inc, Chicago, USA) for Personal Computer was used for the statistical analysis. Significant differences were assumed when P b 0.05.

Results Physical characteristics and physical fitness The subject’s age, anthropometric, body composition, calcium intake, and physical fitness data are summarized in Table 1. When comparing handball and control groups, both were similar in height, age and body mass, but the handballers had 11.5% ( P = 0.05) higher body lean mass than the control group, while no differences were observed in the percentage of body fat between groups. The handballers attained better results in aerobic maximal power, anaerobic capacity, running speed, and mean power in CMJ, while no difference was observed in other physical fitness variables between the groups (Table 1). Body composition Height- and age-adjusted whole body lean mass and the mean upper extremity muscle mass were higher in the handballers than in the controls ( P b 0.05; Table 2). The handballers’ mean muscle mass in upper extremities was 9% greater due to a 11% higher right arm muscle mass (both P b 0.05; Table 2), but nonsignificant differences were observed in the left arm and the lower extremities muscle mass between groups (Table 2). The handballers exhibited significantly greater BMC and BMD in the pelvic region and both lower extremities; in addition they had greater BMC in the whole body and enhanced BMD in the right upper extremity compared with the control subjects (all P b 0.05; Table 3). Both lumbar spine BMC and BMD were higher in the handball group than in the control group ( P b 0.05; Table 3). Hip BMC and BMD values are displayed in Table 3. No differences were found between groups in total or regional femoral BMC and BMD except in the femoral neck BMD, which was greater in the handballers than in the controls (+6%, P b 0.05).

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Table 1 Subject’s age, anthropometrics, calcium intake, physical fitness results, and group differences in percentage (%Dif.) (mean F SEM) Variables

Handballers

Age (year) Height (cm) Body mass (kg) Lean mass (kg) %BF Calcium (mg) VO2max T 30 T 300 MIF

14.2 158.4 53.6 36.9* 26.1 994.7 47.75* 5.21* 60.13* 74.5*

Countermovement jump Height jumped (cm) Peak force (Kp) Mean power (W)

F F F F F F F F F F

Controls 0.4 1.1 1.8 1.2 0.9 107.2 1.22 0.08 1.35 5.0

14.3 157.3 50.6 33.6 27.3 1016.4 43.5 5.48 70.45 56.6

22.0 F 0.01 76.730.06 F 4.0 514.8* F 34.1

Squat jump Height jumped (cm) Peak force (Kp) Mean power (W)

F F F F F F F F F F

0.6 1.2 1.9 1.0 1.4 113.2 1.1 0.08 2.70 4.0

21.9 F 0.01 67.71 F 2.7 436 F 21.50

20.2 F 0.01 52.96 F 3.0 286.73 F 23.7

19.3 F 0.01 52.51 F 2.7 284.96 F 17.4

%Dif.

N

0.7 +0.6 +5.9 +9.8* 4.6 2 +9.7* 5.1* 17.1* +38.7*

24–27 24–27 24–27 24–27 24–27 24–27 24–27 24–27 24–27 23–26

+0.4 +13.30.06 +18.1*

21–27 21–27 21–27

+4.6 +0.8 +0.6

16–26 16–26 16–26

%BF = percentage of body fat; VO2max = maximum oxygen uptake (mld kg 1d min 1); T 30 = time in 30 m (s); T 300 = time in 300 m (s); MIF = maximal isometric force (Kp). * P b 0.05, handballers vs. controls.

Relationship between physical fitness and bone mass and density

Side-to-side intragroup asymmetries It can be seen in Fig. 1 that marked differences exist between dominant and contralateral arm in the handballers for the area occupied by the osseous pixels, BMC and BMD. Muscle mass was also greater in the dominant arm (1.74 F 0.07 vs. 1.58 F 0.07 kg, P b 0.05). The control group showed similar results to those observed in handballers in osseous area and BMC (Fig. 1), also muscle mass was higher in their dominant arm (1.52 F 0.05 vs. 1.43 F 0.06 kg, P b 0.05), but BMD was similar in both arms in the control group. Minor asymmetries were observed at the lower extremity level in handballers, only BMD was higher in contralateral leg (Fig. 1). However, the controls had higher osseous area (Fig. 1) and lower muscle mass (5.46 F 0.20 vs. 5.55 F 0.19 kg, P b 0.05) in their dominant leg than in their contralateral leg.

Table 2 Height- and age-adjusted lean mass from the whole-body scan (mean F SEM) and group differences in percentage (%Dif.) Whole body scan

Lean mass (kg) Handballers

Controls

Whole body Arms (mean) Right arm Left arm Legs (mean) Right leg Left leg

36.21* F 1.63* F 1.71* F 1.55 F 5.86 F 5.83 F 5.89 F

34.16 F 1.49 F 1.54 F 1.45 F 5.63 F 5.59 F 5.67 F

0.50 0.04 0.05 0.04 0.11 0.11 0.11

*P b 0.05, handballers vs. controls.

%Dif. 0.47 0.04 0.04 0.04 0.10 0.10 0.11

+5.7* +8.6* +9.9* +6.5 +3.9 +4.1 +3.7

Among all physical fitness variables, maximal isometric leg extension force showed the highest correlation with total and regional bone mass. Especially with whole body, upper and lower extremities, femoral and lumbar BMC (r = 0.60– 0.80, all P b 0.01), and BMD (r = 0.68–0.79, P b 0.01). In addition, peak force (maximal ground reaction force during a vertical jump) and mean power generated during a squat jump, as well as the mean velocity in a 30-m running sprint test also correlated with bone variables in all scanned regions (r = 0.48–0.69, all P b 0.05). Whole-body and lower-extremity lean mass (an estimation of limb muscle mass) showed a close correlation with total and regional BMC (r = 0.80–0.92, P b 0.001) and BMD (r = 0.78 – 0.84, P b 0.001). Mean hip BMC was linearly related to the lower extremity lean mass in both groups, this relationship being stronger in the handballers than in the control subjects (r = 0.85 and r = 0.66, both P b 0.001). However, both groups showed similar slopes and intercepts for this linear relationship. Multiple regression analysis showed that body mass, age, and time needed to complete a 30-m running sprint test (T 30) were the variables with the highest predictive value for whole body BMC (BMCt) and BMD (BMDt) in young girls, as reflected in the following equations: BMCt (g) = 28.9 body mass (kg) 288.8 T 30 (s) + 35.4 age (year) + 1388.1 (R = 0.93, SEE = 171.9 P b 0.001); BMDt = 0.015 age (year) + 0.006 body mass (kg) 0.094 T 30 (s) +1.005 (R = 0.90, SEE = 0.06 P b 0.001). Although less accurately than whole body BMC, femoral and lumbar

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Table 3 Body weight-, height-, and age-adjusted bone mineral content (BMC) and density (BMD) from the whole-body, femoral, and lumbar scans (mean F SEM), and group differences in percentage (%Dif.) Whole-body scan Whole body Head Pelvic Arms (mean) Right arm Left arm Legs (mean) Right leg Left leg Spinal regions Lumbar (mean L1–L4) Femoral regions Proximal femur (mean) Femoral neck Trochanter Intertrochanteric zone Ward’s triangle

BMD (g cm 2)

BMC (g) Handballers

Controls

1901.0* F 35.2 375.9 F 10.9 233.2* F 7.1 108.2 F 2.7 111.2 F 2.8 105.2 F 2.9 389.0* F 7.3 386.9* F 7.0 391.2* F 7.7

1794.4 381.9 202.5 102.8 104.7 101.0 362.7 364.1 361.3

12.5* F 0.4

29.2 4.1 7.5 17.8 1.03

F F F F F

0.9 0.1 0.3 0.6 0.2

F F F F F F F F F

33.1 10.3 6.7 2.6 2.6 2.7 6.8 6.6 7.2

%Dif.

Handballers

Controls

+5.6* 1.6 +13.2* +5.0 +5.8 +4.0 +6.8* +5.9* +7.6*

1.035 1.716 1.165* 0.664 0.672* 0.657 1.166* 1.157* 1.162*

1.001 1.766 1.091 0.642 0.642 0.642 1.100 1.094 1.102

F F F F F F F F F

0.014 0.040 0.019 0.009 0.009 0.009 0.016 0.015 0.017

11.4 F 0.3

+8.8*

0.969* F 0.021

27.9 3.8 7.1 17.0 0.97

+4.5 +7.3 +5.3 +4.7 +6.1

0.961 0.908* 0.793 1.026 0.856

F F F F F

0.8 0.1 0.3 0.6 0.2

F F F F F

0.020 0.018 0.019 0.036 0.023

F F F F F F F F F

%Dif. 0.013 0.038 0.018 0.008 0.009 0.009 0.015 0.014 0.016

0.907 F 0.20

0.927 0.857 0.754 1.052 0.821

F F F F F

0.019 0.016 0.018 0.034 0.022

+3.3 +2.9 +6.4* +3.3 +4.5* +2.3 +5.7* +5.4* +5.2*

+6.4

+3.5 +5.6* +4.9 +2.5 +4.1

* P b 0.05, handballers vs. controls.

BMD could be predicted from physical fitness and anthropometric variables, using the following equations: femoral BMD = 0.008 body mass (kg) 0.142 T 30 (s) + 1.268 (R = 0.81, SEE = 0.09 P b 0.001); and lumbar BMD = 0.002 age (year) + 0.001 body mass (kg) 0.14 T 30 (s) + 0.9 (R = 0.89, SEE = 0.09 P b 0.001).

Discussion This study shows that handball participation is associated with higher axial and appendicular BMC and BMD during early puberty in girls. Moreover, as expected, handballers have enhanced muscle mass and better physical fitness than their nonactive matched counterparts. Another relevant finding of this study is that the same stimuli producing skeletal muscle hypertrophy produces a proportional development of bone mass in young girls. These findings add further evidence of the response of growing bone to mechanical overload [9]. The greater BMD observed in the dominant arm of the handball players can only be explained as an adaptive response to the mechanical loading imposed by the participation in handball because the environmental, nutritional, or genetic variables influencing bone remodeling [19] can be considered similar for both arms in the same subject. These findings concur with previous studies carried out with other unilateral sports like tennis, in both adult [14,20] and child [21] populations. Weight-bearing activities, particularly those that involve impact actions, have been associated with increased bone mass and density [12,14,17,22,23]. In fact, sports like football, badminton, or ice hockey, which involve a large

number of jumps, rapid directional changes, starts, stops, and landings had been demonstrated to enhance BMC and BMD in boys [7,9]. The results of the present investigation show that girls participating in handball, which involves actions similar to football, have greater whole-body, lowerextremity, and lumbar BMC than their age- height- and weight-matched nonactive counterparts. Interestingly, all loaded bone regions like arms, especially the dominant arm mainly used in handball, lumbar spine, and lower-extremities BMD were significantly higher in handballers than in the controls. Actually, our results show that the leg contralateral to the dominant arm, which is mainly used for take off and landing in handball, had enhanced BMD compared to the dominant leg in the handballers, despite similar osseous area and BMC in both legs. The femoral neck area appears to be particularly sensitive to mechanical stress elicited by sport actions [7,12]. Interestingly, only femoral neck BMD of all hip analyzed subregions was higher in the handball group than in the controls. Because gains in bone mass seem to be retained over the long term [24], given the fact that just 1 SD enhancement of BMD is expected to decrease the prevalence of proximal femur fractures in adults by 50% or more [25], the 6% greater femoral BMD observed in our handballers may be translated into a reduced fracture risk later in life. Similar osteogenic benefits have been previously described in girl gymnasts [3]. However, handball participation produces this osteogenic effect with a substantially lower exercise volume, just with 3 h per week compared to the several hours per day that gymnasts usually devote to training. This implies that handball, which is widely

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Fig. 1. Side-to-side bone asymmetries in the handball players and the controls. *P b 0.05 intragroup differences. #Pb 0.05, handballers vs. controls differences in percentage.

practiced by girls around the world, is a suitable way to easily improve not only physical fitness but also bone mass and density in girls. Given the cross-sectional design of our study, we cannot rule out the influence of a self-selection bias, since girls naturally endowed with increased muscle mass and bone mass could have chosen to play handball. However, the increases in bone mass in the playing arm, as well as the correlation with muscle mass both support a cause-and-effect relationship; that is, the observed differences in bone mass, BMD, and physical fitness between handballers and the nonphysically active girls are a direct consequence of handball participation rather than of selfselection. It has been an issue of debate whether sports participation might be able to elicit muscle mass hypertrophy in children [26]. Our data indicate that handballers had higher wholebody lean mass than that observed in the controls. Both groups had higher muscle mass (equivalent to lean mass in the extremities) in their dominant arm; however, handballers’ muscle mass in the dominant arm was 11% greater than

the muscle mass in the same arm of the controls. The handballers use the dominant arm for throwing and bouncing the ball while the contralateral usually has a similar activity to the controls contralateral arm. This suggests that handball participation enhances muscle mass in girls during growth. This fact is important because a greater muscle mass may facilitate bone mass accumulation. In fact, previous studies in children have identified body mass and especially lean mass development as the best predictor of bone mass deposition [27], possibly because greater muscles are able to elicit greater forces in the bone where they attached. It should be taken into account that muscle forces, not body mass, are the main actors eliciting bone remodeling and bone mass accumulation [28]. In the present study, we report a close relationship between lean mass and bone variables in all the scanned regions. In this regard, it should be mentioned that both muscle mass and BMD were significantly higher in the dominant arm of the handball players when compared to the control girls. Surprisingly, in contrast to what we have previously

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Fig. 2. Relationship between whole-body lean mass and bone mineral content (BMC) and areal density (BMD) in handball players (black circles) and non-physically active girls (white circles), as well as in male football players from the same population. Male football players were matched for age, body mass, and height with the girls (unpublished observations). * Differences in slope between boys and girls at level P b 0.05.

observed in boys [7], this difference in BMD disappears after accounting for arm muscle mass, suggesting that this enhanced BMD could be directly explained by the higher muscle mass. The latter implies that, in this case, exercise exerts an indirect effect on bone mass throughout the enhancement of muscle mass, or at least, we cannot distinguish an independent effect of exercise on bone as happened in boys [7]. This may be because exercise intensity could be lower in girls than in boys, or because the hypertrophy response to exercise is more accentuated in boys than in girls. Assuming a gender dimorphism in the muscular hypertrophic response to exercise, the relationship between lean mass and bone mass could be also different between boys and girls during growth (Fig. 2). A reason may be differences in the hormonal milieu during the peripuberal years in males and females [29]. Animal experiments have shown that in postpuberal female rats, bone is less responsive to loading than in ovariectomized rats or male rats of similar age [29]. More experiments will be needed to definitively clarify if the bone of girls is less responsive to loading when the exercise is started during the estrogen replete period compared to that started before puberty [23,30]; our results point in this direction because

our handballers started their participation 1.9 years before the menarche. This study also shows that some physical-fitness-related variables have a close relationship with bone mass and density. Among them, the time needed to cover 30 m as fast as possible has predictive value to estimate bone mass and density in young girls. The performance in this test depends on muscle power, which results from the optimal combination between force and velocity. Force is mainly determined by muscle mass in children [31] and muscle contraction velocity depends on the proportion of type II muscular fibers. So, the relationship between 30-m running test and bone mass could be explained first by the relationship between muscle mass and BMC and second because type II fibers could potentially generate greater strains on their bones [32], as it has been previously suggested [7]. The increase of muscle power elicited by sports like handball may be particularly interesting in cases of reduced muscle power, as occurs for example in elderly people, to more efficiently prevent falls. In conclusion, 3 h per week of handball participation is associated with better physical fitness, muscle mass hypertrophy, and enhanced bone mass and density in young postmenarcheal girls. However, longitudinal studies are needed to verify whether the high values of BMC and BMD observed in this population are latter translated into a greater peak bone mass in the adulthood, and if this can truthfully reduce the risk of skeletal fractures in old age.

Acknowledgments Special thanks are given to Jose´ Navarro de Tuero for their excellent technical assistance and to Betty Burgess for the revision of the English style and grammar. This study was supported by Ministerio de Educacio´n, Cultura y Deportes (AP2000-3652), Universidad de Las Palmas de Gran Canaria, Gobierno de Canarias (PI2000/067), Consejo Superior de Deportes (27/UNI10/00), and Ministerio de Ciencia y Tecnologı´a (BFI2003-09638).

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