Abstract
Summary
We carried out a cross-section study of the sex-specific relationship between bone mineral content and physical activity at sites with different loading in pre- and early pubertal girls and boys. There was significant sensitivity of bone mineral content of the hip to physical exercise in boys, but not in girls.
Background
Since little is known whether there are sex differences in sensitivity of bone to loading, we investigated sex differences in the cross-sectional association between measures of physical activity (PA) and bone mass and size in pre- and early pubertal children of both sexes.
Methods
We measured bone mineral content/density (BMC/BMD) and fat-free mass (FFM) in 269 6- to 13-year-old children from randomly selected schools by dual-energy X-ray absorptiometry. Physical activity (PA) was measured by accelerometers and lower extremity strength by a jump-and-reach test.
Results
Boys (n = 128) had higher hip and total body BMC and BMD, higher FFM, higher muscle strength and were more physically active than girls (n = 141). Total hip BMC was positively associated with time spent in total and vigorous PA in boys (r = 0.20–0.33, p < 0.01), but not in girls (r = 0.02–0.04, p = ns), even after adjusting for FFM and strength. While boys and girls in the lowest tertile of vigorous PA (22 min/day) did not differ in hip BMC (15.62 vs 15.52 g), boys in the highest tertile (72 min/day) had significantly higher values than the corresponding girls (16.84 vs 15.71 g, p < 0.05).
Conclusions
Sex differences in BMC during pre- and early puberty may be related to a different sensitivity of bone to physical loading, irrespective of muscle mass.
Similar content being viewed by others
References
Seeman E (2002) An exercise in geometry. J Bone Miner Res 17:373–380
Seeman E (2002) Pathogenesis of bone fragility in women and men. Lancet 359:1841–1850
Jarvinen TL, Kannus P, Pajamaki I, Vuohelainen T, Tuukkanen J, Jarvinen M, Sievanen H (2003) Estrogen deposits extra mineral into bones of female rats in puberty, but simultaneously seems to suppress the responsiveness of female skeleton to mechanical loading. Bone 32:642–651
Ducher G, Courteix D, Meme S, Magni C, Viala JF, Benhamou CL (2005) Bone geometry in response to long-term tennis playing and its relationship with muscle volume: a quantitative magnetic resonance imaging study in tennis players. Bone 37:457–466
Daly RM, Saxon L, Turner CH, Robling AG, Bass SL (2004) The relationship between muscle size and bone geometry during growth and in response to exercise. Bone 34:281–287
Kontulainen SA, Hughes JM, Macdonald HM, Johnston JD (2007) The biomechanical basis of bone strength development during growth. Med Sport Sci 51:13–32
Matthews BL, Bennell KL, McKay HA, Khan KM, Baxter-Jones AD, Mirwald RL, Wark JD (2006) Dancing for bone health: a 3-year longitudinal study of bone mineral accrual across puberty in female non-elite dancers and controls. Osteoporos Int 17(7):1043–1054
Petit MA, McKay HA, MacKelvie KJ, Heinonen A, Khan KM, Beck TJ (2002) A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. J Bone Miner Res 17:363–372
MacKelvie KJ, Petit MA, Khan KM, Beck TJ, McKay HA (2004) Bone mass and structure are enhanced following a 2-year randomized controlled trial of exercise in prepubertal boys. Bone 34:755–764
Blimkie CJ (1993) Resistance training during preadolescence. Issues and controversies. Sports Med 15:389–407
Kannus P, Haapasalo H, Sankelo M, Sievanen H, Pasanen M, Heinonen A, Oja P, Vuori I (1995) Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med 123:27–31
Janz KF, Burns TL, Levy SM, Torner JC, Willing MC, Beck TJ, Gilmore JM, Marshall TA (2004) Everyday activity predicts bone geometry in children: the Iowa bone development study. Med Sci Sports Exerc 36:1124–1131
Hasselstrom H, Karlsson KM, Hansen SE, Gronfeldt V, Froberg K, Andersen LB (2006) Sex differences in bone size and bone mineral density exist before puberty. The Copenhagen School Child Intervention Study (CoSCIS). Calcif Tissue Int 79:7–14
Neu CM, Rauch F, Manz F, Schoenau E (2001) Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporos Int 12:538–547
Gilsanz V, Kovanlikaya A, Costin G, Roe TF, Sayre J, Kaufman F (1997) Differential effect of gender on the sizes of the bones in the axial and appendicular skeletons. J Clin Endocrinol Metab 82:1603–1607
Loro ML, Sayre J, Roe TF, Goran MI, Kaufman FR, Gilsanz V (2000) Early identification of children predisposed to low peak bone mass and osteoporosis later in life. J Clin Endocrinol Metab 85:3908–3918
Janz KF, Gilmore JM, Burns TL, Levy SM, Torner JC, Willing MC, Marshall TA (2006) Physical activity augments bone mineral accrual in young children: the Iowa Bone Development study. J Pediatr 148:793–799
McKay HA, Petit MA, Khan KM, Schutz RW (2000) Lifestyle determinants of bone mineral: a comparison between prepubertal Asian- and Caucasian-Canadian boys and girls. Calcif Tissue Int 66:320–324
Macdonald HM, Kontulainen SA, Mackelvie-O’Brien KJ, Petit MA, Janssen P, Khan KM, McKay HA (2005) Maturity- and sex-related changes in tibial bone geometry, strength and bone-muscle strength indices during growth: a 20-month pQCT study. Bone 36:1003–1011
Mosley JR, Lanyon LE (2002) Growth rate rather than gender determines the size of the adaptive response of the growing skeleton to mechanical strain. Bone 30:314–319
Wallace JM, Rajachar RM, Allen MR, Bloomfield SA, Robey PG, Young MF, Kohn DH (2007) Exercise-induced changes in the cortical bone of growing mice are bone- and gender-specific. Bone 40:1120–1127
Jones G, Dwyer T (1998) Bone mass in prepubertal children: gender differences and the role of physical activity and sunlight exposure. J Clin Endocrinol Metab 83:4274–4279
Macdonald HM, Kontulainen SA, Khan KM, McKay HA (2007) Is a school-based physical activity intervention effective for increasing tibial bone strength in boys and girls? J Bone Miner Res 22:434–446
Sundberg M, Gardsell P, Johnell O, Karlsson MK, Ornstein E, Sandstedt B, Sernbo I (2001) Peripubertal moderate exercise increases bone mass in boys but not in girls: a population-based intervention study. Osteoporos Int 12:230–238
Zahner L, Puder JJ, Roth R, Schmid M, Guldimann R, Puhse U, Knopfli M, Braun-Fahrlander C, Marti B, Kriemler S (2006) A school-based physical activity program to improve health and fitness in children aged 6–13 years (“Kinder-Sportstudie KISS”): study design of a randomized controlled trial [ISRCTN15360785]. BMC Public Health 6:147
Gutin B, Owens S (1999) Role of exercise intervention in improving body fat distribution and risk profile in children. Am J Hum Biol 11:237–247
Bonjour JP, Chevalley T, Ammann P, Slosman D, Rizzoli R (2001) Gain in bone mineral mass in prepubertal girls 3.5 years after discontinuation of calcium supplementation: a follow-up study. Lancet 358:1208–1212
Freedson P, Pober D, Janz KF (2005) Calibration of accelerometer output for children. Med Sci Sports Exerc 37:S523–S530
Janz K, Rao S, Baumann HJ, Schultz JL (2003) Measuring children’s vertical ground reaction forces with accelerometry during walking, running, and jumping: the Iowa Bone Development Study. Pediatr Exerc Sci 15:34–43
Jamsa T, Vainionpaa A, Korpelainen R, Vihriala E, Leppaluoto J (2006) Effect of daily physical activity on proximal femur. Clin Biomech (Bristol, Avon) 21:1–7
Lara AJ, Abian J, Alegre LM, Jimenez L, Aguado X (2006) Assessment of power output in jump tests for applicants to a sports sciences degree. J Sports Med Phys Fitness 46:419–424
Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920
Molgaard C, Sandstorm B, Michaelsen KF (1998) Evaluation of a food frequency questionnaire for assessing of calcium, protein and phosphorus intakes in children and adolescents. Scand J Nutr 42:2–5
Molgaard C, Thomsen BL, Michaelsen KF (2001) The influence of calcium intake and physical activity on bone mineral content and bone size in healthy children and adolescents. Osteoporos Int 12:887–894
Forwood MR, Bailey DA, Beck TJ, Mirwald RL, Baxter-Jones AD, Uusi-Rasi K (2004) Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone 35:973–981
Iuliano-Burns S, Stone J, Hopper JL, Seeman E (2005) Diet and exercise during growth have site-specific skeletal effects: a co-twin control study. Osteoporos Int 16:1225–1232
Forwood MR, Baxter-Jones AD, Beck TJ, Mirwald RL, Howard A, Bailey DA (2006) Physical activity and strength of the femoral neck during the adolescent growth spurt: a longitudinal analysis. Bone 38:576–583
Hughes JM, Novotny SA, Wetzsteon RJ, Petit MA (2007) Lessons learned from school-based skeletal loading intervention trials: putting research into practice. Med Sport Sci 51:137–158
Jarvinen TL, Pajamaki I, Sievanen H, Vuohelainen T, Tuukkanen J, Jarvinen M, Kannus P (2003) Femoral neck response to exercise and subsequent deconditioning in young and adult rats. J Bone Miner Res 18:1292–1299
Peacock M, Turner CH, Econs MJ, Foroud T (2002) Genetics of osteoporosis. Endocr Rev 23:303–326
Bass SL, Saxon L, Daly RM, Turner CH, Robling AG, Seeman E, Stuckey S (2002) The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17:2274–2280
Frost HM, Schonau E (2000) The “muscle-bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590
Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761–1767
Sherar LB, Baxter-Jones AD, Mirwald RL (2004) Limitations to the use of secondary sex characteristics for gender comparisons. Ann Hum Biol 31:586–593
Vainionpaa A, Korpelainen R, Vihriala E, Rinta-Paavola A, Leppaluoto J, Jamsa T (2006) Intensity of exercise is associated with bone density change in premenopausal women. Osteoporos Int 17:455–463
Acknowledgements
We thank all the children, parents, and teachers who volunteered to participate in this study. We thank the foundation AETAS, Switzerland, for the use of their DXA bus, and we greatly appreciate the help of Giulio Conicella and Chantal Genet for their competent help with the bone measurements. We also thank the Federal Council of Sports, Magglingen, Switzerland, for their financial support of the study.
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kriemler, S., Zahner, L., Puder, J.J. et al. Weight-bearing bones are more sensitive to physical exercise in boys than in girls during pre- and early puberty: a cross-sectional study. Osteoporos Int 19, 1749–1758 (2008). https://doi.org/10.1007/s00198-008-0611-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-008-0611-5