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Published in: Osteoporosis International 12/2008

01-12-2008 | Original Article

Weight-bearing bones are more sensitive to physical exercise in boys than in girls during pre- and early puberty: a cross-sectional study

Authors: S. Kriemler, L. Zahner, J. J. Puder, C. Braun-Fahrländer, C. Schindler, N. J. Farpour-Lambert, M. Kränzlin, R. Rizzoli

Published in: Osteoporosis International | Issue 12/2008

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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.
Literature
3.
go back to reference 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 32:642–651PubMedCrossRef 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 32:642–651PubMedCrossRef
4.
go back to reference 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 37:457–466PubMedCrossRef 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 37:457–466PubMedCrossRef
5.
go back to reference 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 34:281–287PubMedCrossRef 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 34:281–287PubMedCrossRef
6.
go back to reference Kontulainen SA, Hughes JM, Macdonald HM, Johnston JD (2007) The biomechanical basis of bone strength development during growth. Med Sport Sci 51:13–32PubMedCrossRef Kontulainen SA, Hughes JM, Macdonald HM, Johnston JD (2007) The biomechanical basis of bone strength development during growth. Med Sport Sci 51:13–32PubMedCrossRef
7.
go back to reference 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):1043–1054PubMedCrossRef 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):1043–1054PubMedCrossRef
8.
go back to reference 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 17:363–372PubMedCrossRef 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 17:363–372PubMedCrossRef
9.
go back to reference 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 34:755–764PubMedCrossRef 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 34:755–764PubMedCrossRef
10.
go back to reference Blimkie CJ (1993) Resistance training during preadolescence. Issues and controversies. Sports Med 15:389–407PubMedCrossRef Blimkie CJ (1993) Resistance training during preadolescence. Issues and controversies. Sports Med 15:389–407PubMedCrossRef
11.
go back to reference 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 123:27–31PubMed 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 123:27–31PubMed
12.
go back to reference 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 36:1124–1131PubMedCrossRef 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 36:1124–1131PubMedCrossRef
13.
go back to reference 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 79:7–14PubMedCrossRef 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 79:7–14PubMedCrossRef
14.
go back to reference 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 12:538–547PubMedCrossRef 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 12:538–547PubMedCrossRef
15.
go back to reference 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 82:1603–1607PubMedCrossRef 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 82:1603–1607PubMedCrossRef
16.
go back to reference 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 85:3908–3918PubMedCrossRef 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 85:3908–3918PubMedCrossRef
17.
go back to reference 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 148:793–799PubMedCrossRef 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 148:793–799PubMedCrossRef
18.
go back to reference 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 66:320–324PubMedCrossRef 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 66:320–324PubMedCrossRef
19.
go back to reference 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 36:1003–1011PubMedCrossRef 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 36:1003–1011PubMedCrossRef
20.
go back to reference 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 30:314–319PubMedCrossRef 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 30:314–319PubMedCrossRef
21.
go back to reference 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 40:1120–1127PubMedCrossRef 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 40:1120–1127PubMedCrossRef
22.
go back to reference 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 83:4274–4279PubMedCrossRef 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 83:4274–4279PubMedCrossRef
23.
go back to reference 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 22:434–446PubMedCrossRef 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 22:434–446PubMedCrossRef
24.
go back to reference 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 12:230–238PubMedCrossRef 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 12:230–238PubMedCrossRef
25.
go back to reference 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 6:147PubMedCrossRef 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 6:147PubMedCrossRef
26.
go back to reference Gutin B, Owens S (1999) Role of exercise intervention in improving body fat distribution and risk profile in children. Am J Hum Biol 11:237–247PubMedCrossRef Gutin B, Owens S (1999) Role of exercise intervention in improving body fat distribution and risk profile in children. Am J Hum Biol 11:237–247PubMedCrossRef
27.
go back to reference 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 358:1208–1212PubMedCrossRef 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 358:1208–1212PubMedCrossRef
28.
go back to reference Freedson P, Pober D, Janz KF (2005) Calibration of accelerometer output for children. Med Sci Sports Exerc 37:S523–S530PubMedCrossRef Freedson P, Pober D, Janz KF (2005) Calibration of accelerometer output for children. Med Sci Sports Exerc 37:S523–S530PubMedCrossRef
29.
go back to reference 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 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
30.
go back to reference Jamsa T, Vainionpaa A, Korpelainen R, Vihriala E, Leppaluoto J (2006) Effect of daily physical activity on proximal femur. Clin Biomech (Bristol, Avon) 21:1–7CrossRef Jamsa T, Vainionpaa A, Korpelainen R, Vihriala E, Leppaluoto J (2006) Effect of daily physical activity on proximal femur. Clin Biomech (Bristol, Avon) 21:1–7CrossRef
31.
go back to reference 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 46:419–424PubMed 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 46:419–424PubMed
32.
go back to reference Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920PubMed Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920PubMed
33.
go back to reference 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, 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
34.
go back to reference 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 12:887–894PubMedCrossRef 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 12:887–894PubMedCrossRef
35.
go back to reference 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 35:973–981PubMedCrossRef 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 35:973–981PubMedCrossRef
36.
go back to reference 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 16:1225–1232PubMedCrossRef 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 16:1225–1232PubMedCrossRef
37.
go back to reference 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 38:576–583PubMedCrossRef 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 38:576–583PubMedCrossRef
38.
go back to reference 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 51:137–158PubMedCrossRef 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 51:137–158PubMedCrossRef
39.
go back to reference 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 18:1292–1299PubMedCrossRef 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 18:1292–1299PubMedCrossRef
40.
41.
go back to reference 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 17:2274–2280PubMedCrossRef 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 17:2274–2280PubMedCrossRef
42.
go back to reference Frost HM, Schonau E (2000) The “muscle-bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590PubMed Frost HM, Schonau E (2000) The “muscle-bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590PubMed
43.
go back to reference Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761–1767PubMedCrossRef Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761–1767PubMedCrossRef
44.
go back to reference Sherar LB, Baxter-Jones AD, Mirwald RL (2004) Limitations to the use of secondary sex characteristics for gender comparisons. Ann Hum Biol 31:586–593PubMedCrossRef Sherar LB, Baxter-Jones AD, Mirwald RL (2004) Limitations to the use of secondary sex characteristics for gender comparisons. Ann Hum Biol 31:586–593PubMedCrossRef
45.
go back to reference 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 17:455–463PubMedCrossRef 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 17:455–463PubMedCrossRef
Metadata
Title
Weight-bearing bones are more sensitive to physical exercise in boys than in girls during pre- and early puberty: a cross-sectional study
Authors
S. Kriemler
L. Zahner
J. J. Puder
C. Braun-Fahrländer
C. Schindler
N. J. Farpour-Lambert
M. Kränzlin
R. Rizzoli
Publication date
01-12-2008
Publisher
Springer-Verlag
Published in
Osteoporosis International / Issue 12/2008
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-008-0611-5

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