Enhanced Bone Mass and Physical Fitness in Prepubescent Basketball Players

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1 Journal of Clinical Densitometry: Assessment & Management of Musculoskeletal Health, vol. 17, no. 1, 156e162, 2014 Ó Copyright 2014 by The International Society for Clinical Densitometry /17:156e162/$ Section V: Bone Patho-Physiology Enhanced Bone Mass and Physical Fitness in Prepubescent Basketball Players Anis Zribi,*,1 Mohamed Zouch, 1 Hamada Chaari, 1 Elyes Bouajina, 2 Monia Zouali, 1 Ammar Nebigh, 1 and Zouhair Tabka 1 1 Laboratoire de Physiologie et des Explorations Fonctionnelles, Universite de Sousse, Faculte demedecine Ibn Eljazzar, Sousse, Tunisia; and 2 Service de Rhumatologie, CHU Farhat Hached, Sousse, Tunisia Abstract The aim of this study was to examine the effect of basketball practice on bone acquisition in the prepubertal age. In total, 48 prepubescent male basketball players aged yr, Tanner stage 1, were compared with 50 controls matched for age and pubertal stage. Areal bone mineral density, bone mineral content (BMC), and bone area (BA) in deferent sites associated with anthropometric parameters were measured by dual-energy X-ray absorptiometry. Running and jumping tests were performed. Analysis of Student s impaired t-test revealed that basketball players attained better results in all physical fitness tests ( p! 0.05). They also exhibited significantly greater BMC and BA in whole body, upper and lower extremities, trochanter, total hip, and whole right and left radius ( p! 0.001) compared with the controls. No significant differences were observed between groups in right and left ultradistal and third distal radius and spinal regions, BMC, and BA, whereas a significant positive correlation was reported between lean mass, BMC, and BA of lower limbs. In summary, basketball practice in prepubertal age is associated with improved physical fitness and enhanced lean and bone mass in loaded sites. Key Words: BMC; bone area; prepubescent; regular training. Introduction Physical activity has been described as a strategy to optimize skeletal development and widely recommended as one of the key preventative strategies to reduce the risk of osteoporosis, falls, and fractures (1). In adults, exercise produces modest increases in bone mineral density (BMD) of only 1e3% per year (2). By contrast, physical activities undertaken in childhood, particularly activities that apply large forces quickly, convey optimal benefits to bone mass, size, and structure (3). The pre- and early pubertal years seem to be the period with the greatest responsiveness (4e6). The average gain in bone mineral content Received 11/06/12; Revised 03/16/13; Accepted 04/05/13. *Address correspondence to: Anis Zribi, Laboratoire de Physiologie et des Explorations Fonctionnelles, Universite de Sousse, Faculte de Medecine Ibn Eljazzar, Sousse, Tunisia. anis_zribi@ hotmail.fr (BMC) and BMD in controlled trials is in the order of 2e5% per year (2). Kannus et al (4) reported a 2.5 times greater benefit from racquet sports in the premenarchal years compared with the same activity begun after menarche. In addition, the bone mass acquisition in childhood persists for 7 months (7) to 3 years after exercise cessation (8). Studies in children showed the increase of the accrual of BMD from weight bearing physical activities practice particularly in weight-loaded skeletal regions (9,10). In gymnasts, the higher values of BMD in the whole body (11), spine, and lower extremities (9) compared with nonactive counterparts are due to the higher ground reaction forces, which are close to 10 times body mass in young gymnast (12). Soccer participation is associated with enhanced trochanteric BMC and increased femoral and lumbar spine BMD in prepubertal boys (13) and enhanced whole body, lumbar spine, femoral neck, pelvis, and lower limbs BMD and BMC (14). There is increasing evidence that weight-bearing sporting activities involving rapid directional changes, starts, stops, and 156

2 Bone Mass and Physical Fitness in Basketball Players 157 great reaction forces enhance bone mineral accrual in prepubertal age (13,14). Basketball, a weight-bearing intermittent sport, is played worldwide by more than 450 million people (15). During the match, players cover about 4500e5000 m with a variety of multidirectional movements such as running, starts, stops, shuffling and dribbling at variable velocities, and jumping (16). Upper extremities are also solicited in many actions such as dribbling, throwing, and blocking the ball. These actions generate strain and compressive forces and stimulate bone remodeling process (17). Therefore, basketball may be considered as an excellent osteogenic sport for adults and adolescents (18). It has been reported that adolescent basketball players displayed greater bone mass in most of the measured sites compared with swimmers and nonathletes (18). Participation of male adolescents in a range of high-impact activities such as basketball for 1 h or more a day is associated with greater bone size and mineral content, especially at the hip (19). However, to the best of our knowledge, the effects of practicing basketball, osteogenic sport for adults and adolescents, on bone mass and their effects in prepubertal age have not been studied. The purpose of this study was to determine whether prepubescent boys practicing basketball for 3 h/wk for at least 1 yr have additional osteogenic effects compared with those obtained from the compulsory school education session. We hypothesized that prepubescent children practicing basketball would have greater enhancement in bone mass than control subjects matched for age and pubertal stage. Materials and Methods Subjects Ninety-eight healthy boys aged 10e12 yr belonging to Tanner stage 1 participated in this cross-sectional study. They were divided into 2 groups depending on their physical patterns. Forty-eight were assigned to the basketball group (BG) as, in addition to a weekly physical education session at school, they practiced basketball in a primary training center for 3 h/wk for at least 1 yr ( yr). The other 50, participated only in the compulsory physical education curriculum at school (1 weekly session of 50 min), were assigned to the control group (CG). This study was approved by the Independent Ethics Committee of Farhat Hached Tunisian Hospital and had been led according to the World Health Organization s recommendation elaborated at Helsinki. All children s parents were asked to read and sign an informed consent document before participation. Anthropometric Measurements Standard calibrated scale and stadiometer were used to determine height and body mass in stockinged feet and underwear to the nearest 5 mm and 100 g, respectively. Body mass index (BMI) was then calculated (body mass/height 2 ). The Calcium Intake The amount of calcium consumed per day (mg/d) was measured by using the Bilnut SCDA Nutrisoft (Cerelles, France) program. Bone Measurements Areal BMD (abmd, g/cm 2 ), BMC (g), and bone area (BA, cm 2 ) for the whole body; lumbar spine (L2eL4); femoral neck of the dominant leg, right, and left radius; lean mass (kg); and fat mass (kg) were measured by dual-energy X- ray absorptiometry (DXA) using Lunar Prodigy (model DXAP 2004, software version 3.6; GE Healthcare, Madison, WI). The coefficients of variation of abmd, BMC, and BA were less than 1% in lumbar spine, femoral neck, and whole body and 2.5% in upper and lower limbs. Physical Fitness Aerobic Maximal Power VO 2 max The maximum oxygen uptake (VO 2 max ) was estimated by the multistage 20-m shuttle-test (20). Anaerobic Capacity Anaerobic capacity was estimated by using 300-m running test. Running Speed Test Photoelectric cell (Cell Kit Speed Brower, USA) was used to measure the time needed to run 30 m. Jump Tests Squat jump and countermovement jump were performed using an Opto Jump (Microgate, Bolzano, Italy) and horizontal jump and 5-jump test (21) using a dual Dkm. Basal Physical Activity Level Basal activity level was calculated by using the Bratteby s questionnaire, which estimates the level of daily physical activities during a typical day without basketball training (22). Pubertal Status Tanner pubertal status was determined by serum rates of follicle-stimulating hormone, luteinizing hormone, and testosterone (23) and confirmed by a clinical method of recognized validity and reliability (24). Statistical Analysis Means (standard deviation) are given as descriptive statistics. Differences between groups were established using Student s unpaired t-test. The analyses of covariance entering height and lean mass as covariates were performed to evaluate differences in BMC and BA between the 2 groups. Bivariate correlation and linear stepwise multiple regression was applied to identify the relationship between lean mass and bone variables. Statistical significance was set at p! 0.05.

3 158 Zribi et al. Statistical analysis was performed using Statistica software (version ; StatSoft, Maisons-Alfort, France). Results Anthropometric Measures The subject s age, anthropometric, and body composition data are summarized in Table 1. BGs and CGs were similar in age, BMI, fat mass, and dietary calcium intake, but the basketball players were taller, heavier, and had higher lean mass in upper, lower limbs and in whole body than the controls ( p! 0.05). Physical Fitness As shown in Table 2, the basal physical activity did not show any significant difference between the 2 groups, but the basketball players showed better performances in all physical fitness tests. Bone Measurements After adjustment for height and lean mass, whole-body DXA scans did not reveal any significant difference in abmd between groups in most sites, except in right and left legs; basketball players showed greater abmd in right ( vs ; p ) and left leg ( vs ; p ). BMC and BA values adjusted for height and lean mass are displayed in Tables 3 and 4. The basketball players exhibited significantly greater BMC and BA in whole body, upper and lower limbs, trochanter, total hip, and whole radius for right and left forearms compared with the control subjects Table 1 Subject s Age, Anthropometric, Calcium Intake, and Pubertal Status (Means SD) Variables Basketball players Controls p Value Age (yr) NS Height (cm) !0.05 Weight (kg) !0.05 Lean mass, right arm (kg) !0.05 Lean mass, left arm (kg) !0.05 Lean mass, right leg (kg) !0.05 Lean mass, left leg (kg) !0.05 Lean mass (kg) !0.05 Fat mass (kg) NS BMI (kg/m 2 ) NS Calcium intake (mg)/d NS FSH (mui/ml) NS LH (mui/ml) NS Testosterone (mui/ml) NS Abbr: BMI, body mass index; FSH, follicle-stimulating hormone; LH, luteinizing hormone; NS, nonsignificant; SD, standard deviation. Table 2 Physical Fitness Measurements for Basketball Players and Control Subjects (Mean SD) Variables ( p! 0.001), whereas controls showed higher head BMC ( p! 0.01). No significant differences were observed between groups in both right and left ultradistal and third distal radius, femoral neck, and lumbar spine BMC and BA (Tables 3 and 4). A close correlation was observed between right and left legs lean mass and BMC (r and r 5 0.9, respectively; p! 0.001) and BA (r and r , respectively; p! 0.001) of lower limbs (Fig. 1). Discussion Basketball players Controls p Value VO 2max (ml/kg/min) !0.01 T 30 (s) !0.05 T 300 (s) !0.01 SJ (cm) !0.01 CMJ (cm) !0.01 HJ (m) ! Jump test (m) !0.01 PAL NS Abbr: CMJ, countermovement jump (cm); HJ, horizontal jump; NS, nonsignificant; PAL, physical activity level; SD, standard deviation; SJ, squat jump (cm); T 30, time in 30 m (s); T 300, time in 300 m (s); VO 2max, maximum oxygen uptake (ml/kg/min). Two major findings emerge from this study. First, loading from basketball participation is the most significant contributor to increased BMC and BA among prepubescent boys. Second, basketball participation is associated with better physical fitness and enhanced lean mass in upper and lower limbs. These findings are consistent with results of previous studies in which bone mass was positively related to physical activity in children in Tanner stage 1 (25,26). DXA scans revealed significant enhanced BMC and BA in whole body, upper and lower limbs, trochanter, and total hip of basketball players compared with controls (Tables 3 and 4). Our results agree with previous studies showing increases in BMC and BA in the weight-bearing bones associated with prepubertal stages (14,25,27) but contrast others, which showed no obvious BA variation in prepubescent soccer players (28). The main effects of skeletal loading induced by basketball practice were at bone sites that consisted of predominantly trabecular bone (trochanter and total hip). These data support the view that trabecular bones are more responsive to mechanical load than cortical ones. Surprisingly, lumbar spine (L2eL4), which consists of trabecular bone, seems to be not sensitive enough to mechanical stress elicited by basketball practice. Similar findings were

4 Bone Mass and Physical Fitness in Basketball Players 159 Table 3 Cross-sectional Analysis of Bone Parameters (BMC) Adjusted for Height and Lean Mass in Whole Body, Radius, Spinal, and Femoral Regions Between Basketball Players and Control Subjects (Means SD) Variables Basketball players Controls p Value Whole body !0.001 Head !0.01 Right arm !0.01 Left arm !0.001 Right leg !0.001 Left leg !0.001 Radius regions Right ultradistal radius NS Right third distal radius NS Left ultradistal radius NS Left third distal radius NS Whole right radius !0.01 Whole left radius !0.01 Spinal regions Lumbar spine (L2eL4) NS Femoral regions Femoral neck NS Trochanter !0.01 Total hip !0.01 Abbr: BMC, bone mineral content; NS, nonsignificant; SD, standard deviation. Table 4 Cross-sectional Analysis of Bone Parameters (BA) Adjusted for Weight and Lean Mass in Whole Body, Radius, Spinal, and Femoral Regions Between Basketball Players and Control Subjects (Means SD) Variables Basketball players Controls p Value Whole body !0.001 Head NS Right arm !0.01 Left arm !0.01 Right leg !0.01 Left leg !0.001 Radius regions Right ultradistal radius NS Right third distal radius NS Left ultradistal radius NS Left third distal radius NS Whole right radius !0.01 Whole left radius !0.01 Spinal regions Lumbar spine (L2eL4) NS Femoral regions Femoral neck NS Trochanter !0.01 Total hip !0.01 Abbr: BA, bone area; NS, nonsignificant; SD, standard deviation.

5 160 Zribi et al. Fig. 1. Correlations between lean mass of right and left legs and BMC and bone area of lower limbs in basketball players. BMC, bone mineral content. reported by Haapasalo et al (29) among prepubertal and peripubertal female tennis players. The significant increase in spine BMD among those children appeared only at pubertal age, supporting the view that structural benefits may need longer period before reaching significance (30). So, we expect such results for our BG especially in the pubertal age, marked by hormonal impregnations. According to this cross-sectional study, basketball players showed greater BMC and BA in whole radius for 2 forearms but not in third and ultradistal radius. Our results contrast with those presented by Dowthwaite et al (31) among premenarchal gymnasts. These differences may be attributable to the variation of mechanical stress induced by every sport modality in the stimulated region. Furthermore, it has been showed that the osteogenic response to loading in humerus was greater in peri- compared with prepubertal male tennis players (32). This suggests that improving bone mass in third and ultradistal radius bones may need longer period of basketball training. Elevated BMC and BA levels of lower limbs found in young basketball players compared with controls is an indicator of responsive loaded sites to the significant amount of mechanical loads induced by basketball practice in prepubertal age. In fact, during running, sprinting, starts, stops, and jumping actions, loading bones are under tensile, compressive, shear, bending, and torsional stress, which produce high strains stimulus on lower body. This confirms Yang PF s findings, suggesting that basketball rebounding induced greater principal strains than normal activities (33). Interestingly, young basketball players also reported better performances in all physical tests and higher lean mass in whole body and in right and left leg. Similar findings were reported by Vicente-Rodriguez et al (13,34) among prepubescent soccer players. This supports the view that there is a link between lean mass and physical activity participation. Furthermore, our data clearly demonstrate a positive correlation between lean mass, BMC, and BA of lower limbs (Fig. 1). Thus, the mechanical forces that act on the lower limbs may be generated not only by the high reaction forces produced by impact with the ground in running, sprinting, and jumping but also by muscular contractions pulling on their bony attachment. This finding is in accordance with previous knowledge (35), showing that physical activity has not only a direct osteogenic effect on bone mass but also an indirect effect through its relationship with lean mass (36). Interestingly, young basketball players showed lower head BMC than controls but no variation in head BA between them. Similarly, Courteix et al (37) reported significantly lower head BMC in gymnasts compared with swimmers and controls ( p! 0.001). This could be explained by the fact

6 Bone Mass and Physical Fitness in Basketball Players 161 that response to mechanical loads elicited by basketball practice, there could be a transfer of calcium from nonloaded (head) to the loaded bearing bones (lower limbs). This concept of calcium transfer seems to be an important physiological mechanism that could also explain bone adaptation observed in bedridden subjects and astronauts. In fact, after a long space flight, a bone loss was reported at bone bearing sites, whereas no change at nonbearing sites among astronauts (38). Despite the enhancement in BMC and BA of loaded bones responsive to mechanical forces produced by basketball practice through impact with the ground in running, sprinting, jumping, and muscular contractions pulling on their bony attachment, we reported no variation in abmd in most sites except in lower limbs. This could be explained by the low amount of daily calcium intake by our basketball players (720 mg/d), which is roughly half recommended by the official Institute of Medicine (1300 mg/d) and especially the lack of hormonal impregnations in prepubescent period. Probably, a longer training period is needed to lead to better benefits in abmd. In conclusion, 2 sessions (90 min each) per week of basketball practice is associated with better physical fitness, lean mass hypertrophy in whole body, upper and lower limbs, and enhanced BMC and BA in loaded sites among prepubescent boys. Acknowledgments The authors thank the staff of the Rheumatology and Biochemistry departments for their excellent technical assistance. References 1. Nikander R, Siev anen H, Heinonen A, et al Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med 8: Suominen H Muscle training for bone strength. 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