Clinical Science| Volume 62, ISSUE 12, P1811-1818, December 2013

Physical activity is associated with bone geometry of premenarcheal girls in a dose-dependent manner

Published:September 20, 2013DOI:



      To determine the relationship between habitual physical activity (PA) level and peripheral qualitative computed tomography-determined quantitative tibia characteristics of premenarcheal girls.


      Premenarcheal girls matched for age (10–13 years), bone age and maturity level were assigned into: a) low PA group (LPA, n = 25), b) moderate PA group (MPA, n = 17), and c) high PA group (HPA, n = 18). Participants’ daily dietary intake, tibia’s geometry and serum levels of calcium and vitamin D were assessed.


      Premenarcheal girls demonstrating HPA exhibited greater pericortical thickness, cross-sectional area (CSA) and bone mineral content (BMC) (p < .001) in cortical bone, greater BMC, volumetric bone density (vBMD) and polar stress strength index (SSIp) in trabecular bone (p < 0.001–0.05) and greater total BMC (p < .05) and vBMD (p < .01) when compared to their physically inactive or moderately active counterparts. MPA exhibited greater values of cortical BMC (p < .01) and SSIp (p < .05) than LPA. Partial correlation analysis (adjusted for BMI) revealed modest associations between PA score and bone geometry parameters (r = 0.36–0.49, p < .05) at 38% of tibia length.


      Habitual PA affects geometry of both cortical and trabecular areas of a long bone of premenarcheal girls in a dose-dependent manner. Specifically, PA increases both the density and size of cortical bone but only the density of trabecular bone during preadolescence. Given the importance of peak bone mass for future fracture risk, high levels of PA during childhood could be a major target for public health interventions aimed at optimising bone health in prepubertal children when the greatest bone gains occur.


      PA (Physical activity), MET (Metabolic Equivalent of Task), BMC (Bone mineral content), BMD (Bone mineral density), DXA (Dual energy X-ray absorptiometry), pQCT (Peripheral quantitative computed tomography), vBMD (Volumetric bone mineral density), LPA (Low PA), MPA (Moderate PA), HPA (High PA), BMI (Body mass index), CSA (Cross-sectional area), SSIp (Stress strength index in torsion), MCSA (Muscle cross-sectional area), ANOVA (Analysis of variance), 25(OH)D (Hydroxyvitamin D)


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        • Maïmoun L.
        • Coste O.
        • Mariano-Goulart D.
        • et al.
        In peripubertal girls, artistic gymnastics improves areal bone mineral density and femoral bone geometry without affecting serum OPG/RANKL levels.
        Osteoporos Int. 2011; 22: 3055-3066
        • Hind A.M.
        • Burrows M.
        Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials.
        Bone. 2007; 40: 14-27
        • Sundberg M.
        • Gärdsell P.
        • Johnell O.
        • et al.
        Physical activity increases bone size in prepubertal boys and bone mass in prepubertal girls: a combined cross-sectional and 3-year longitudinal study.
        Calcif Tissue Int. 2002; 7: 406-415
        • McKay H.A.
        • Bailey D.A.
        • Mirwald R.L.
        • et al.
        Peak bone mineral accrual and the age at menarche in adolescent girls: a 6-year longitudinal study.
        J Pediatr. 1998; 133: 682-687
        • Kohrt W.M.
        • Bloomfield S.A.
        • Little K.D.
        • et al.
        American College of Sports Medicine position stand: physical activity and bone health.
        Med Sci Sports Exerc. 2004; 36: 1985-1996
        • Valdimarsson O.
        • Linden C.
        • Johnell O.
        • et al.
        Daily physical education in the school curriculum in prepubertal girls during 1 year is followed by a increase in bone mineral accrual and bone width — data from the prospective Malmo Paediatric Osteoporosis Prevention Study.
        Calcif Tissue Int. 2006; 78: 65-71
        • Baxter-Jones A.D.G.
        • Kontulainen S.A.
        • Faulkner R.A.
        • et al.
        A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescent to young adulthood.
        Bone. 2008; 43: 1101-1107
        • McKay H.A.
        • Petit M.A.
        • Schutz R.W.
        • et al.
        Augmented trochanteric bone mineral density after modified physical education classes: a randomized school-based exercise intervention study in prepubescent and early pubescent children.
        J Pediatr. 2000; 136: 156-162
        • Macdonald H.
        • Kontulainen S.
        • Petit M.
        • et al.
        Bone strength and its determinants in pre- and early pubertal boys and girls.
        Bone. 2006; 39: 598-608
        • Troiano R.P.
        • Berrigan D.
        • Dodd K.W.
        • et al.
        Physical activity in the United States measure by accelerometer.
        Med Sci Sports Exerc. 2008; 40: 181-188
        • Seeman E.
        • Delmas R.D.
        Bone quality—the material and structural basis of bone strength and fragility.
        N Engl J Med. 2006; 354: 2250-2261
        • Dowthwaite J.N.
        • Rosenbaum P.F.
        • Scerpella T.A.
        Site-specific advantages in skeletal geometry and strength at the proximal femur and forearm in young female gymnasts.
        Bone. 2012; 50: 1173-1183
        • Hamilton C.J.
        • Jamal S.A.
        • Beck T.J.
        • et al.
        Evidence for impaired skeletal load adaptation among Canadian women with type 2 diabetes mellitus: Insight into the BMD and bone fragility paradox.
        Metabolism. 2013; ([epub ahead of print, pii: S0026-0495(13)00145-5. PMID: 23768546])
        • Tournis S.
        • Michopoulou E.
        • Fatouros I.G.
        • et al.
        Effect of rhythmic gymnastics on volumetric bone mineral density and bone geometry in premenarcheal female athletes and controls.
        J Clin Endocrinol Metab. 2010; 95: 2755-2762
        • McKay H.
        • Liu D.
        • Egeli D.
        • et al.
        Physical activity positively predicts bone architecture and bone strength in adolescent males and females.
        Acta Paediatr. 2011; 100: 97-101
        • Suuriniemi M.
        • Mahonen A.
        • Kovanen V.
        • et al.
        Association between exercise and pubertal bmd is modulated by estrogen receptor genotype.
        J Bone Miner Res. 2004; 19: 1758-1765
        • Tschudy M.M.
        • Arcara K.M.
        The Harriet Lane handbook: a manual for pediatric house officers.
        19th ed. Elsevier-Mosby, Philadelphia2012
        • Tanner J.M.
        Foetus into man.
        Harvard Press, Cambridge, MA1978
        • Greulich W.
        • Pyle S.
        Radiographic atlas of skeletal development of the hand and wrist.
        Stanford University Press, Stanford, CA1959
        • Argiropoulou E.C.
        • Michalopoulou M.
        • Aggeloussis N.
        • et al.
        Validity and reliability of physical activity measures in Greek high school age children.
        J Sports Sci Med. 2004; 3: 147-159
        • Blair S.N.
        How to assess exercise habits and physical fitness.
        in: Matazazzo J.D. Miller N.E. Weiss S.M. Herd J.A. Behavioral health: a handbook of health enhancement and disease prevention. John Wiley & Sons, NY1984: 126-142
        • Ridley K.
        • Ainsworth B.E.
        • Olds T.S.
        Development of a compendium of energy expenditures for youth.
        Int J Beh Nutr Phys Act. 2008; 5: 45
        • Baecke J.A.
        Questionnaire of habitual physical activity.
        Med Sci Sports Exerc. 1997; 29: 15-18
        • Capozza R.F.
        • Feldman S.
        • Mortarino P.
        • et al.
        Structural analysis of the human tibia by tomographic (pQCT) serial scans.
        J Anat. 2010; 216: 470-481
        • Shaw N.
        A practical approach to hypocalcemia in children.
        Endocr Dev. 2009; 16: 73-92
        • Tobias J.H.
        • Steer C.D.
        • Mattocks C.
        • et al.
        Habitual levels of physical activity influence bone mass in 11-year-old children from the UK: findings from a large population-based cohort.
        J Bone Miner Res. 2007; 22: 101-109
        • Sayers A.
        • Mattocks C.
        • Deere K.
        • et al.
        Habitual levels of vigorous, but not moderate or light, physical activity is positively related to cortical bone mass in adolescents.
        J Clin Endocrinol Metab. 2011; 96: 793-802
        • Gracia-Marco L.
        • Moreno L.A.
        • Ortega F.B.
        • et al.
        Levels of physical activity that predict optimal bone mass in adolescents: the HELENA Study.
        Am J Prev Med. 2011; 40: 599-607
        • Vicente-Rodriguez G.
        How does exercise affect bone development during growth?.
        Sports Med. 2006; 36: 561-569
        • Janz K.F.
        • Gilmore J.M.
        • Levy S.M.
        • et al.
        Physical activity and femoral neck bone strength during childhood: the Iowa Bone Development Study.
        Bone. 2007; 41: 216-222
        • Hasegawa Y.
        • Schneider P.
        • Reiners C.
        Age, sex, and gripstrength determine architectural bone parameters assessed by peripheral quantitative computed tomography (pQCT) at the human radius.
        J Biomech. 2001; 34: 497-503
        • Maïmoun L.
        • Coste O.
        • Philibert P.
        • et al.
        Peripubertal female athletes in high-impact sports show improved bone mass acquisition and bone geometry.
        Metabolism. 2013; 62: 1088-1098
        • Specker B.
        • Binkley T.
        Randomized trial of physical activity and calcium supplementation on bone mineral content in 3- to 5-yearold children.
        J Bone Miner Res. 2003; 18: 885-892
        • Macdonald H.M.
        • Kontulainen S.A.
        • Khan K.M.
        • et al.
        Is a school-based physical activity intervention effective for increasing tibial bone strength in boys and girls?.
        J Bone Miner Res. 2007; 22: 434-446
        • Sienkiewicz E.
        • Magkos F.
        • Aronis K.
        • et al.
        Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women.
        Metabolism. 2011; 60: 1211-1221
        • Park H.A.
        • Lee J.S.
        • Kuller L.H.
        • Cauley J.A.
        Effects of weight control during the menopausal transition on bone mineral density.
        J Clin Endocrinol Metab. 2007; 92: 3809-3815
        • Lorentzon M.
        • Mellstrom D.
        • Ohlsson C.
        Association of amount of physical activity with cortical bone size and trabecular volumetric BMD in young adult men: the GOOD Study.
        J Bone Miner Res. 2005; 20: 1936-1943
        • Ward K.A.
        • Roberts S.A.
        • Adams J.E.
        • et al.
        Bone geometry and density in the skeleton of pre-pubertal gymnasts and school children.
        Bone. 2005; 36: 1012-1018
        • Farr J.N.
        • Tomás R.
        • Chen Z.
        • et al.
        Lower trabecular volumetric BMD at metaphyseal regions of weight-bearing bones is associated with prior fracture in young girls.
        J Bone Miner Res. 2011; 26: 380-387
        • Hinton P.S.
        • Rector R.S.
        • Thomas T.R.
        Weight-bearing, aerobic exercise increases markers of bone formation during short-term weight loss in overweight and obese men and women.
        Metabolism. 2006; 55: 1616-1618
        • Daly R.M.
        • Saxon L.
        • Turner C.H.
        • et al.
        The relationship between muscle size and bone geometry during growth and in response to exercise.
        Bone. 2004; 34: 281-287
        • Maïmoun
        • Sultan C.
        Effects of physical activity on bone remodeling.
        Metabolism. 2011; 60: 373-388