Skip to main content
Top
Published in: Osteoporosis International 4/2014

01-04-2014 | Original Article

Does lean tissue mass accrual during adolescence influence bone structural strength at the proximal femur in young adulthood?

Authors: S. A. Jackowski, J. L. Lanovaz, C. Van Oort, A. D. G. Baxter-Jones

Published in: Osteoporosis International | Issue 4/2014

Login to get access

Abstract

Summary

The purpose of this study was to identify whether young adult bone structural strength at the hip is associated with adolescent lean tissue mass (LTM) accrual. It was observed that those individuals who accrued more LTM from adolescence to adulthood had significantly greater adult bone structural strength at the hip.

Introduction

The purpose of this study was to identify whether young adult bone cross-sectional area (CSA), section modulus (Z), and outer diameter (OD) at the hip were associated with adolescent LTM accrual.

Methods

One hundred three young adult participants (55 males, 48 females) were tertiled into adolescent LTM accrual groupings. LTM accrual was assessed by serial measures using dual energy X-ray absorptiometry (DXA) from adolescence to young adulthood (21.3 ± 1.3 years). CSA, Z, and OD at the narrow neck (NN) and femoral shaft (S) sites of the proximal femur were assessed in young adulthood (21.3 ± 4.5 years), using hip structural analysis. Group differences were assessed using an analysis of covariance, controlling for adult height, weight, sex, and physical activity levels.

Results

It was found that individuals with higher adjusted adolescent LTM accrual had significantly greater adult adjusted values of NNCSA (2.49 ± 0.06 vs 2.77 ± 0.07 cm2), NN Z (1.18 ± 0.04 vs 1.37 ± 0.04 cm3), NN OD (3.07 ± 0.04 vs 3.21 ± 0.04 cm), SCSA (3.45 ± 0.08 vs 3.88 ± 0.09 cm3), and SZ (1.77 ± 0.05 vs 2.00 ± 0.05 cm3) than individuals with lower LTM accrual (p < 0.05).

Conclusions

These findings suggest that the amount of LTM accrued from adolescence to young adulthood has a positive influence on adult bone structural strength at the proximal femur.
Literature
1.
go back to reference Skaggs DL, Loro ML, Pitukcheewanont P, Tolo V, Gilsanz V (2001) Increased body weight and decreased radial cross-sectional dimensions in girls with forearm fractures. J Bone Miner Res 16:1337–1342PubMedCrossRef Skaggs DL, Loro ML, Pitukcheewanont P, Tolo V, Gilsanz V (2001) Increased body weight and decreased radial cross-sectional dimensions in girls with forearm fractures. J Bone Miner Res 16:1337–1342PubMedCrossRef
2.
go back to reference Rudang R, Ohlsson C, Oden A, Johansson H, Mellstrom D, Lorentzon M (2010) Hip fracture prevalence in grandfathers is associated with reduced cortical cross-sectional bone area in their young adult grandsons. J Clin Endocrinol Metab 95:1105–1114PubMedCrossRef Rudang R, Ohlsson C, Oden A, Johansson H, Mellstrom D, Lorentzon M (2010) Hip fracture prevalence in grandfathers is associated with reduced cortical cross-sectional bone area in their young adult grandsons. J Clin Endocrinol Metab 95:1105–1114PubMedCrossRef
4.
go back to reference Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A: Discov Mol Cell Evol Biol 275:1081–1101CrossRef Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A: Discov Mol Cell Evol Biol 275:1081–1101CrossRef
5.
go back to reference Schoenau E (2005) From mechanostat theory to development of the “functional muscle-bone-unit”. J Musculoskelet Neuronal Interact 5:232–238PubMed Schoenau E (2005) From mechanostat theory to development of the “functional muscle-bone-unit”. J Musculoskelet Neuronal Interact 5:232–238PubMed
6.
go back to reference Burr DB (1997) Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 12:1547–1551PubMedCrossRef Burr DB (1997) Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 12:1547–1551PubMedCrossRef
7.
go back to reference Ashe MC, Liu-Ambrose TY, Cooper DM, Khan KM, McKay HA (2008) Muscle power is related to tibial bone strength in older women. Osteoporos Int 19:1725–1732PubMedCrossRef Ashe MC, Liu-Ambrose TY, Cooper DM, Khan KM, McKay HA (2008) Muscle power is related to tibial bone strength in older women. Osteoporos Int 19:1725–1732PubMedCrossRef
8.
go back to reference Beck BR (2009) muscle forces or gravity—what predominates mechanical loading on bone?: introduction. Med Sci Sports Exerc 4:2033–2036CrossRef Beck BR (2009) muscle forces or gravity—what predominates mechanical loading on bone?: introduction. Med Sci Sports Exerc 4:2033–2036CrossRef
9.
go back to reference Daly RM, Stenevi-Lundgren S, Linden C, Karlsson MK (2008) Muscle determinants of bone mass, geometry and strength in prepubertal girls. Med Sci Sports Exerc 40:1135–1141PubMedCrossRef Daly RM, Stenevi-Lundgren S, Linden C, Karlsson MK (2008) Muscle determinants of bone mass, geometry and strength in prepubertal girls. Med Sci Sports Exerc 40:1135–1141PubMedCrossRef
10.
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
11.
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
12.
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
13.
go back to reference Jackowski SA, Faulkner RA, Farthing JP, Kontulainen SA, Beck TJ, Baxter-Jones AD (2009) Peak lean tissue mass accrual precedes changes in bone strength indices at the proximal femur during the pubertal growth spurt. Bone 44:1186–1190PubMedCrossRef Jackowski SA, Faulkner RA, Farthing JP, Kontulainen SA, Beck TJ, Baxter-Jones AD (2009) Peak lean tissue mass accrual precedes changes in bone strength indices at the proximal femur during the pubertal growth spurt. Bone 44:1186–1190PubMedCrossRef
14.
go back to reference Klein CS, Allman BL, Marsh GD, Rice CL (2002) Muscle size, strength, and bone geometry in the upper limbs of young and old men. J Gerontol Ser A Biol Sci Med Sci 57:M455–M459CrossRef Klein CS, Allman BL, Marsh GD, Rice CL (2002) Muscle size, strength, and bone geometry in the upper limbs of young and old men. J Gerontol Ser A Biol Sci Med Sci 57:M455–M459CrossRef
16.
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
17.
go back to reference DiVasta AD, Beck TJ, Petit MA, Feldman HA, Leboff MS, Gordon CM (2007) Bone cross-sectional geometry in adolescents and young women with anorexia nervosa: a hip structural analysis study. Osteoporos Int 18:797–804PubMedCentralPubMedCrossRef DiVasta AD, Beck TJ, Petit MA, Feldman HA, Leboff MS, Gordon CM (2007) Bone cross-sectional geometry in adolescents and young women with anorexia nervosa: a hip structural analysis study. Osteoporos Int 18:797–804PubMedCentralPubMedCrossRef
18.
go back to reference Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA (2008) A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone 43:1101–1107PubMedCrossRef Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA (2008) A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone 43:1101–1107PubMedCrossRef
19.
go back to reference Evans W, Hurley B (1995) Age, gender, and muscular strength. J Gerontol 50:41–44CrossRef Evans W, Hurley B (1995) Age, gender, and muscular strength. J Gerontol 50:41–44CrossRef
20.
go back to reference Baxter-Jones AD, Eisenmann JC, Mirwald RL, Faulkner RA, Bailey DA (2008) The influence of physical activity on lean mass accrual during adolescence: a longitudinal analysis. J Appl Physiol 105:734–741PubMedCrossRef Baxter-Jones AD, Eisenmann JC, Mirwald RL, Faulkner RA, Bailey DA (2008) The influence of physical activity on lean mass accrual during adolescence: a longitudinal analysis. J Appl Physiol 105:734–741PubMedCrossRef
21.
go back to reference Gunter KB, Almstedt HC, Janz KF (2012) Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev 40:13–21PubMedCentralPubMedCrossRef Gunter KB, Almstedt HC, Janz KF (2012) Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev 40:13–21PubMedCentralPubMedCrossRef
22.
go back to reference Janz KF, Burns TL, Levy SM, Torner JC, Willing MC, Beck TJ et al (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 et al (2004) Everyday activity predicts bone geometry in children: the Iowa Bone Development Study. Med Sci Sports Exerc 36:1124–1131PubMedCrossRef
23.
go back to reference Janz KF, Gilmore JM, Levy SM, Letuchy EM, Burns TL, Beck TJ (2007) Physical activity and femoral neck bone strength during childhood: the Iowa Bone Development Study. Bone 41:216–222PubMedCentralPubMedCrossRef Janz KF, Gilmore JM, Levy SM, Letuchy EM, Burns TL, Beck TJ (2007) Physical activity and femoral neck bone strength during childhood: the Iowa Bone Development Study. Bone 41:216–222PubMedCentralPubMedCrossRef
24.
go back to reference Kaptoge S, Dalzell N, Jakes RW, Wareham N, Day NE, Khaw KT et al (2003) Hip section modulus, a measure of bending resistance, is more strongly related to reported physical activity than BMD. Osteoporos Int 14:941–949PubMedCrossRef Kaptoge S, Dalzell N, Jakes RW, Wareham N, Day NE, Khaw KT et al (2003) Hip section modulus, a measure of bending resistance, is more strongly related to reported physical activity than BMD. Osteoporos Int 14:941–949PubMedCrossRef
25.
go back to reference McKay H, Liu D, Egeli D, Boyd S, Burrows M (2010) Physical activity positively predicts bone architecture and bone strength in adolescent males and females. Acta Paediatr 100:97–101PubMedCrossRef McKay H, Liu D, Egeli D, Boyd S, Burrows M (2010) Physical activity positively predicts bone architecture and bone strength in adolescent males and females. Acta Paediatr 100:97–101PubMedCrossRef
26.
go back to reference Sayers A, Mattocks C, Deere K, Ness A, Riddoch C, Tobias JH (2011) Habitual levels of vigorous, but not moderate or light, physical activity is positively related to cortical bone mass in adolescents. J Clin Endocrinol Metab 96:E793–E802PubMedCentralPubMedCrossRef Sayers A, Mattocks C, Deere K, Ness A, Riddoch C, Tobias JH (2011) Habitual levels of vigorous, but not moderate or light, physical activity is positively related to cortical bone mass in adolescents. J Clin Endocrinol Metab 96:E793–E802PubMedCentralPubMedCrossRef
28.
go back to reference Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA (1999) A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the university of Saskatchewan bone mineral accrual study. J Bone Miner Res 14:1672–1679PubMedCrossRef Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA (1999) A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the university of Saskatchewan bone mineral accrual study. J Bone Miner Res 14:1672–1679PubMedCrossRef
29.
go back to reference Bailey DA (1997) The Saskatchewan Pediatric Bone Mineral Accrual Study: bone mineral acquisition during the growing years. Int J Sports Med 18(Suppl 3):S191–S194PubMedCrossRef Bailey DA (1997) The Saskatchewan Pediatric Bone Mineral Accrual Study: bone mineral acquisition during the growing years. Int J Sports Med 18(Suppl 3):S191–S194PubMedCrossRef
30.
go back to reference Bailey DA, Faulkner RA, McKay HA (1996) Growth, physical activity, and bone mineral acquisition. Exerc Sport Sci Rev 24:233–266PubMedCrossRef Bailey DA, Faulkner RA, McKay HA (1996) Growth, physical activity, and bone mineral acquisition. Exerc Sport Sci Rev 24:233–266PubMedCrossRef
31.
go back to reference Ross W, Marfell-Jones M (1991) Kinanthropometry. In: Green H (ed) Physiological testing of the high performance athlete. Human Kinetics, Champaign, pp 223–307 Ross W, Marfell-Jones M (1991) Kinanthropometry. In: Green H (ed) Physiological testing of the high performance athlete. Human Kinetics, Champaign, pp 223–307
32.
go back to reference Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU (1990) Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol 25:6–18PubMedCrossRef Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU (1990) Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol 25:6–18PubMedCrossRef
33.
go back to reference Martin RB, Burr DB (1984) Non-invasive measurement of long bone cross-sectional moment of inertia by photon absorptiometry. J Biomech 17:195–201PubMedCrossRef Martin RB, Burr DB (1984) Non-invasive measurement of long bone cross-sectional moment of inertia by photon absorptiometry. J Biomech 17:195–201PubMedCrossRef
34.
go back to reference Beck TJ (2002) Hip structural analysis (HSA) program (BMD and structural geometry methodology): as used to create NHANES III dataset Beck TJ (2002) Hip structural analysis (HSA) program (BMD and structural geometry methodology): as used to create NHANES III dataset
35.
go back to reference Beck T (2003) Measuring the structural strength of bones with dual-energy X-ray absorptiometry: principles, technical limitations, and future possibilities. Osteoporos Int 14:81–88CrossRef Beck T (2003) Measuring the structural strength of bones with dual-energy X-ray absorptiometry: principles, technical limitations, and future possibilities. Osteoporos Int 14:81–88CrossRef
36.
go back to reference Beck TJ (2007) Extending DXA, beyond bone mineral density: understanding hip structure analysis. Curr Osteoporos Rep 5:49–55PubMedCrossRef Beck TJ (2007) Extending DXA, beyond bone mineral density: understanding hip structure analysis. Curr Osteoporos Rep 5:49–55PubMedCrossRef
37.
go back to reference Khoo BC, Beck TJ, Qiao QH, Parakh P, Semanick L, Prince RL et al (2005) In vivo short-term precision of hip structure analysis variables in comparison with bone mineral density using paired dual-energy X-ray absorptiometry scans from multi-center clinical trials. Bone 37:112–121PubMedCrossRef Khoo BC, Beck TJ, Qiao QH, Parakh P, Semanick L, Prince RL et al (2005) In vivo short-term precision of hip structure analysis variables in comparison with bone mineral density using paired dual-energy X-ray absorptiometry scans from multi-center clinical trials. Bone 37:112–121PubMedCrossRef
38.
go back to reference Jackowski SA, Kontulainen SA, Cooper DM, Lanovaz JL, Jones AD (2011) The timing of bone mineral density and geometric adaptation at the proximal femur from childhood to early adulthood in males and females: a longitudinal study. J Bone Miner Res 26:2753–2761PubMedCrossRef Jackowski SA, Kontulainen SA, Cooper DM, Lanovaz JL, Jones AD (2011) The timing of bone mineral density and geometric adaptation at the proximal femur from childhood to early adulthood in males and females: a longitudinal study. J Bone Miner Res 26:2753–2761PubMedCrossRef
39.
go back to reference Copeland J, Kowalski KC, Donen RM, Tremblay MS (2005) Convergent validity of the physical activity questionnaire for adults: the new member of the PAQ family. J Phys Act Health 2:216–229 Copeland J, Kowalski KC, Donen RM, Tremblay MS (2005) Convergent validity of the physical activity questionnaire for adults: the new member of the PAQ family. J Phys Act Health 2:216–229
40.
go back to reference Heinonen A, McKay HA, Whittall KP, Forster BB, Khan KM (2001) Muscle cross-sectional area is associated with specific site of bone in prepubertal girls: a quantitative magnetic resonance imaging study. Bone 29:388–392PubMedCrossRef Heinonen A, McKay HA, Whittall KP, Forster BB, Khan KM (2001) Muscle cross-sectional area is associated with specific site of bone in prepubertal girls: a quantitative magnetic resonance imaging study. Bone 29:388–392PubMedCrossRef
41.
go back to reference Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB (2005) Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568–576PubMedCrossRef Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB (2005) Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568–576PubMedCrossRef
42.
go back to reference Travison TG, Araujo AB, Esche GR, Beck TJ, McKinlay JB (2008) Lean mass and not fat mass is associated with male proximal femur strength. J Bone Miner Res 23:189–198PubMedCentralPubMedCrossRef Travison TG, Araujo AB, Esche GR, Beck TJ, McKinlay JB (2008) Lean mass and not fat mass is associated with male proximal femur strength. J Bone Miner Res 23:189–198PubMedCentralPubMedCrossRef
43.
go back to reference Kohrt WM, Barry DW, Schwartz RS (2009) Muscle forces or gravity: what predominates mechanical loading on bone? Med Sci Sports Exerc 4:2050–2055CrossRef Kohrt WM, Barry DW, Schwartz RS (2009) Muscle forces or gravity: what predominates mechanical loading on bone? Med Sci Sports Exerc 4:2050–2055CrossRef
44.
go back to reference Turner CH, Robling AG (2003) Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev 31:45–50PubMedCrossRef Turner CH, Robling AG (2003) Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev 31:45–50PubMedCrossRef
45.
go back to reference Ruff C (2003) Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317–329PubMedCrossRef Ruff C (2003) Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317–329PubMedCrossRef
46.
go back to reference Ruff C (2005) Growth tracking of femoral and humeral strength from infancy through late adolescence. Acta Paediatr 94:1030–1037PubMedCrossRef Ruff C (2005) Growth tracking of femoral and humeral strength from infancy through late adolescence. Acta Paediatr 94:1030–1037PubMedCrossRef
47.
go back to reference Nurzenski MK, Briffa NK, Price RI, Khoo BC, Devine A, Beck TJ et al (2007) Geometric indices of bone strength are associated with physical activity and dietary calcium intake in healthy older women. J Bone Miner Res 22:416–424PubMedCrossRef Nurzenski MK, Briffa NK, Price RI, Khoo BC, Devine A, Beck TJ et al (2007) Geometric indices of bone strength are associated with physical activity and dietary calcium intake in healthy older women. J Bone Miner Res 22:416–424PubMedCrossRef
48.
go back to reference Baxter-Jones A, Mirwald RL (2004) Multilevel modeling. In: Hauspie RC, Cameron N, Molinari L (eds) Methods in human growth research. Cambridge University Press, Cambridge, pp 306–330CrossRef Baxter-Jones A, Mirwald RL (2004) Multilevel modeling. In: Hauspie RC, Cameron N, Molinari L (eds) Methods in human growth research. Cambridge University Press, Cambridge, pp 306–330CrossRef
Metadata
Title
Does lean tissue mass accrual during adolescence influence bone structural strength at the proximal femur in young adulthood?
Authors
S. A. Jackowski
J. L. Lanovaz
C. Van Oort
A. D. G. Baxter-Jones
Publication date
01-04-2014
Publisher
Springer London
Published in
Osteoporosis International / Issue 4/2014
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-013-2592-2

Other articles of this Issue 4/2014

Osteoporosis International 4/2014 Go to the issue