Skip to main content

Advertisement

SpringerLink
Log in

The muscle–bone unit of peripheral and central skeletal sites in children and young adults

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

Changes and gender differences in the muscle bone unit at different skeletal sites were investigated during pubertal development. Females accrued greater BMC in relation to muscle compared to males; these gender differences were greater after adjustment for height and regional fat mass.

Purpose

To describe changes and gender differences in the muscle–bone unit at different skeletal sites during pubertal development.

Methods

Four hundred forty-two children aged 5–18 years were studied. Measurements of bone mineral content (BMC), lean mass (LM) and fat mass of the whole body (WB), legs, arms and lumbar spine were obtained from dual-energy X-ray absorptiometry. Peripheral quantitative computed tomography was used to measure BMC of the radius diaphysis and cross-sectional muscle area (CSMA) of the mid-forearm. These measurements were used to describe differences between, and within, genders at each pubertal stage in BMC accrual relative to muscle, both before and after adjustment for height, regional fat and muscle at central and peripheral skeletal sites.

Results

In males, there were significant increases in adjusted WB and leg BMC at the end of pubertal development. Unadjusted and adjusted lumbar spine BMC increased at the onset of, and at the end, of puberty. Radius BMC increased at most pubertal stages. In females, there were increases in unadjusted and adjusted whole body BMC at late puberty, in leg BMC at the onset of puberty and at pubertal stage four. Unadjusted arm BMC increased at most pubertal stages; however, after adjustment, an increase occurred at pubertal stage four. Both adjusted and unadjusted lumbar spine BMC increased at pubertal stage four. Unadjusted radius BMC increased at most pubertal stages. Females had greater BMC at all skeletal sites, compared to males, except at the radius, where adjusted BMC was greater in males at pubertal stage four.

Conclusions

Males and females accrue more BMC in relation to lean mass at multiple skeletal sites as puberty proceeds. Females accrue more BMC in relation to lean mass, in comparison to males, at most skeletal sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Notes

  1. Regional fat mass refers to fat mass of either the whole body, arms or legs. Therefore, whole-body BMC and lumbar spine BMC were adjusted for whole-body fat mass, arm and radius BMC for arm fat mass and leg BMC for leg fat mass.

References

  1. Parfitt AM (1994) The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4:382–398

    Article  CAS  PubMed  Google Scholar 

  2. Parfitt AM, Travers R, Rauch F, Glorieux FH (2000) Structural and cellular changes during bone growth in healthy children. Bone 27:487–494

    Article  CAS  PubMed  Google Scholar 

  3. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E (1999) The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest 104:795–804

    Article  CAS  PubMed  Google Scholar 

  4. Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E (2000) Heterogeneity in the growth of the axial and appendicular skeleton in boys: Implications for the pathogenesis of bone fragility in men. J Bone Miner Res 15:1871–1878

    Article  CAS  PubMed  Google Scholar 

  5. Lian JB, Stein GS, Canalis E, Gehron Robey P, Boskey AL (1999) Bone formation: osteoblast lineage cells, growth factors, matrix proteins and the mineralization process. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism Lippincott. Williams and Wilkins, Philadelphia, pp 14–29

    Google Scholar 

  6. Mundy GR, Chen D, Oyajobi BO (2003) Bone remodeling. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism Lippincott. Williams and Wilkins, Philadelphia, pp 46–58

    Google Scholar 

  7. Crabtree NJ, Kibirige MS, Fordham JN, Banks LM, Muntoni F, Chinn D, Boivin CM, Shaw NJ (2004) The relationship between lean body mass and bone mineral content in paediatric health and disease. Bone 35:965–972

    Article  CAS  PubMed  Google Scholar 

  8. Hogler W, Briody J, Woodhead HJ, Chan A, Cowell CT (2003) Importance of lean mass in the interpretation of total body densitometry in children and adolescents. J Pediatr 143:81–88

    Article  CAS  PubMed  Google Scholar 

  9. Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R (2004) The ‘muscle–bone unit’ during the pubertal growth spurt. Bone 34:771–775

    Article  PubMed  Google Scholar 

  10. Schoenau E, Neu CM, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle–bone unit. J Bone Miner Res 17:1095–1101

    Article  PubMed  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. Pludowski P, Matusik H, Olszaniecka M, Lebiedowski M, Lorenc RS (2005) Reference values for the indicators of skeletal and muscular status of healthy Polish children. J Clin Densitom 8:164–177

    Article  PubMed  Google Scholar 

  13. Frost HM (1987) Bone “mass” and the “mechanostat”: a proposal. Anat Rec 219:1–9

    Article  CAS  PubMed  Google Scholar 

  14. Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101

    Article  PubMed  Google Scholar 

  15. Frost HM, Schoenau E (2000) The “muscle–bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 13:571–590

    CAS  PubMed  Google Scholar 

  16. Schiessl H, Frost HM, Jee WS (1998) Estrogen and bone–muscle strength and mass relationships. Bone 22:1–6

    Article  CAS  PubMed  Google Scholar 

  17. Ferretti JL, Capozza RF, Cointry GR, Garcia SL, Plotkin H, Alvarez Filgueira ML, Zanchetta JR (1998) Gender-related differences in the relationship between densitometric values of whole-body bone mineral content and lean body mass in humans between 2 and 87 years of age. Bone 22:683–690

    Article  CAS  PubMed  Google Scholar 

  18. Schoenau E, Neu CM, Mokov E, Wassmer G, Manz F (2000) Influence of puberty on muscle area and cortical bone area of the forearm in boys and girls. J Clin Endocrinol Metab 85:1095–1098

    Article  CAS  PubMed  Google Scholar 

  19. Tothill P, Hannan WJ (2002) Bone mineral and soft tissue measurements by dual-energy X-ray absorptiometry during growth. Bone 31:492–496

    Article  CAS  PubMed  Google Scholar 

  20. Clark EM, Ness AR, Tobias JH (2006) Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab 91:2534–2541

    Article  CAS  PubMed  Google Scholar 

  21. Janicka A, Wren TA, Sanchez MM, Dorey F, Kim PS, Mittelman SD, Gilsanz V (2007) Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92:143–147

    Article  CAS  PubMed  Google Scholar 

  22. Weiler HA, Janzen L, Green K, Grabowski J, Seshia MM, Yuen KC (2000) Percent body fat and bone mass in healthy Canadian females 10 to 19 years of age. Bone 27:203–207

    Article  CAS  PubMed  Google Scholar 

  23. Ackerman A, Thornton JC, Wang J, Pierson RN Jr, Horlick M (2006) Sex difference in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity (Silver Spring) 14:819–825

    Article  Google Scholar 

  24. Ashby RL, Ward KA, Roberts SA, Edwards L, Mughal MZ, Adams JE (2009) A reference database for the Stratec XCT-2000 peripheral quantitative computed tomography (pQCT) scanner in healthy children and young adults aged 6–19 years. Osteoporos Int 20:1337–1346

    Article  CAS  PubMed  Google Scholar 

  25. Ward KA, Ashby RL, Roberts SA, Adams JE, Zulf Mughal M (2007) UK reference data for the Hologic QDR Discovery dual-energy x ray absorptiometry scanner in healthy children and young adults aged 6–17 years. Arch Dis Child 92:53–59

    Article  PubMed  Google Scholar 

  26. Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920

    CAS  PubMed  Google Scholar 

  27. Tanner JM (1969) Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity. Blackwell, Oxford

    Google Scholar 

  28. Wardhaugh B (2003) Pubertal staging. Available online: http://www.endocrinology.org/SFE/training/ent00/ent00_war.htm [Accessed September 2003].

  29. National Osteoporosis Society (2004) A practical guide to bone densitometry in children. Camerton, Bath, UK

    Google Scholar 

  30. Thomas SR, Kalkwarf HJ, Buckley DD, Heubi JE (2005) Effective dose of dual-energy X-ray absorptiometry scans in children as a function of age. J Clin Densitom 8:415–422

    Article  PubMed  Google Scholar 

  31. Watson SJ, Jones AL, Oatway WB, Hughes JS (2005) Ionising radiation exposure of the UK population: 2005 review. In. Health Protection Agency Centre for Radiation, Chemical and Environmental Hazards Radiation Protection Division, Chilton, Didcot, Oxfordshire, UK.

  32. Landau S, Everitt B (2004) A handbook of statistical analyses using SPSS. Chapman & Hall/CRC, Boca Raton, Florida

    Google Scholar 

  33. Lunt M, Felsenberg D, Reeve J, Benevolenskaya L, Cannata J, Dequeker J, Dodenhof C, Falch JA, Masaryk P, Pols HA, Poor G, Reid DM, Scheidt-Nave C, Weber K, Varlow J, Kanis JA, O’Neill TW, Silman AJ (1997) Bone density variation and its effects on risk of vertebral deformity in men and women studied in thirteen European centers: the EVOS Study. J Bone Miner Res 12:1883–1894

    Article  CAS  PubMed  Google Scholar 

  34. Ismail AA, Pye SR, Cockerill WC, Lunt M, Silman AJ, Reeve J, Banzer D, Benevolenskaya LI, Bhalla A, Bruges Armas J, Cannata JB, Cooper C, Delmas PD, Dequeker J, Dilsen G, Falch JA, Felsch B, Felsenberg D, Finn JD, Gennari C, Hoszowski K, Jajic I, Janott J, Johnell O, Kanis JA, Kragl G, Lopez Vaz A, Lorenc R, Lyritis G, Marchand F, Masaryk P, Matthis C, Miazgowski T, Naves-Diaz M, Pols HA, Poor G, Rapado A, Raspe HH, Reid DM, Reisinger W, Scheidt-Nave C, Stepan J, Todd C, Weber K, Woolf AD, O’Neill TW (2002) Incidence of limb fracture across Europe: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int 13:565–571

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  PubMed  Google Scholar 

  36. Iuliano-Burns S, Mirwald RL, Bailey DA (2001) Timing and magnitude of peak height velocity and peak tissue velocities for early, average, and late maturing boys and girls. Am J Hum Biol 13:1–8

    Article  CAS  PubMed  Google Scholar 

  37. Neu CM, Rauch F, Rittweger J, Manz F, Schoenau E (2002) Influence of puberty on muscle development at the forearm. Am J Physiol Endocrinol Metab 283:E103–107

    CAS  PubMed  Google Scholar 

  38. Rauch F (2005) Bone growth in length and width: the yin and yang of bone stability. J Musculoskelet Neuronal Interact 5:194–201

    CAS  PubMed  Google Scholar 

  39. Rauch F, Schoenau E (2001) The developing bone: slave or master of its cells and molecules? Pediatr Res 50:309–314

    Article  CAS  PubMed  Google Scholar 

  40. Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner 2:73–85

    CAS  PubMed  Google Scholar 

  41. van der Meulen MC, Ashford MW Jr, Kiratli BJ, Bachrach LK, Carter DR (1996) Determinants of femoral geometry and structure during adolescent growth. J Orthop Res 14:22–29

    Article  PubMed  Google Scholar 

  42. Zanchetta JR, Plotkin H, Alvarez Filgueira ML (1995) Bone mass in children: normative values for the 2–20-year-old population. Bone 16:393S–399S

    CAS  PubMed  Google Scholar 

  43. van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, de Muinck Keizer-Schrama SM (2002) Reference data for bone density and body composition measured with dual energy X-ray absorptiometry in white children and young adults. Arch Dis Child 87:341–347

    Article  PubMed  Google Scholar 

  44. Schoenau E, Neu CM, Rauch F, Manz F (2001) The development of bone strength at the proximal radius during childhood and adolescence. J Clin Endocrinol Metab 86:613–618

    Article  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. Molgaard C, Michaelsen KF (1998) Changes in body composition during growth in healthy school-age children. Appl Radiat Isot 49:577–579

    Article  CAS  PubMed  Google Scholar 

  47. Maynard LM, Guo SS, Chumlea WC, Roche AF, Wisemandle WA, Zeller CM, Towne B, Siervogel RM (1998) Total-body and regional bone mineral content and areal bone mineral density in children aged 8–18 y: the Fels Longitudinal Study. Am J Clin Nutr 68:1111–1117

    CAS  PubMed  Google Scholar 

  48. Magarey AM, Boulton TJ, Chatterton BE, Schultz C, Nordin BE, Cockington RA (1999) Bone growth from 11 to 17 years: relationship to growth, gender and changes with pubertal status including timing of menarche. Acta Paediatr 88:139–146

    Article  CAS  PubMed  Google Scholar 

  49. Landin L, Nilsson BE (1981) Forearm bone mineral content in children. Normative data Acta Paediatr Scand 70:919–923

    Article  CAS  Google Scholar 

  50. Faulkner RA, Bailey DA, Drinkwater DT, McKay HA, Arnold C, Wilkinson AA (1996) Bone densitometry in Canadian children 8–17 years of age. Calcif Tissue Int 59:344–351

    Article  Google Scholar 

  51. Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol 30:160–175

    Article  CAS  PubMed  Google Scholar 

  52. van Coeverden SC, Netelenbos JC, de Ridder CM, Roos JC, Popp-Snijders C, Delemarre-van de Waal HA (2002) Bone metabolism markers and bone mass in healthy pubertal boys and girls. Clin Endocrinol (Oxf) 57:107–116

    Article  Google Scholar 

  53. Wang Q, Alen M, Nicholson PH, Halleen JM, Alatalo SL, Ohlsson C, Suominen H, Cheng S (2006) Differential effects of sex hormones on peri- and endocortical bone surfaces in pubertal girls. J Clin Endocrinol Metab 91:277–282

    Article  CAS  PubMed  Google Scholar 

  54. Frost HM (1999) On the estrogen–bone relationship and postmenopausal bone loss: A new model. J Bone Miner Res 14:1473–1477

    Article  CAS  PubMed  Google Scholar 

  55. Libanati C, Baylink DJ, Lois-Wenzel E, Srinvasan N, Mohan S (1999) Studies on the potential mediators of skeletal changes occurring during puberty in girls. J Clin Endocrinol Metab 84:2807–2814

    Article  CAS  PubMed  Google Scholar 

  56. Wang Q, Alen M, Nicholson P, Lyytikainen A, Suuriniemi M, Helkala E, Suominen H, Cheng S (2005) Growth patterns at distal radius and tibial shaft in pubertal girls: a 2-year longitudinal study. J Bone Miner Res 20:954–961

    Article  PubMed  Google Scholar 

  57. Hogler W, Blimkie CJ, Cowell CT, Kemp AF, Briody J, Wiebe P, Farpour-Lambert N, Duncan CS, Woodhead HJ (2003) A comparison of bone geometry and cortical density at the mid-femur between prepuberty and young adulthood using magnetic resonance imaging. Bone 33:771–778

    Article  CAS  PubMed  Google Scholar 

  58. Bechtold S, Rauch F, Noelle V, Donhauser S, Neu CM, Schoenau E, Schwarz HP (2001) Musculoskeletal analyses of the forearm in young women with Turner syndrome: a study using peripheral quantitative computed tomography. J Clin Endocrinol Metab 86:5819–5823

    Article  CAS  PubMed  Google Scholar 

  59. Parfitt AM (2004) The attainment of peak bone mass: what is the relationship between muscle growth and bone growth? Bone 34:767–770

    Article  CAS  PubMed  Google Scholar 

  60. Seeman E, Hopper JL, Young NR, Formica C, Goss P, Tsalamandris C (1996) Do genetic factors explain associations between muscle strength, lean mass, and bone density? A twin study. Am J Physiol 270:E320–327

    CAS  PubMed  Google Scholar 

  61. Ferretti JL, Cointry GR, Capozza RF (2002) Noninvasive analysis of bone mass, structure and strength. In: An YH (ed) Orthopaedic issues in osteoporosis. CRC, Florida, pp 145–167

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the research subjects and their families for taking part in this study and the schools where recruitment was undertaken. Thanks are also due to Mr Mike Machin, database manager, for preparation of the bone density databases used. We gratefully acknowledge financial support from the National Osteoporosis Society (Camerton, Bath, United Kingdom) who awarded Rebecca Ashby a Linda Edwards Memorial PhD Studentship in 2003 and awarded a project grant for the initial part of the study, and the Central Manchester University Hospitals NHS Foundation Trust Research Endowment Fund, which funded the study.

Conflicts of interest

None.

Author information

Authors and Affiliations

  1. Clinical Radiology, Imaging Sciences and Biomedical Engineering, The University of Manchester, Manchester, UK

    R. L. Ashby, J. E. Adams & K. A. Ward

  2. Department of Health Sciences, The University of York, York, UK

    R. L. Ashby

  3. Health Methodology Research Group, Manchester Academic Health Science Centre, The University of Manchester, Manchester, UK

    S. A. Roberts

  4. Department of Paediatric Medicine, Royal Manchester Children’s Hospital, Manchester, UK

    M. Z. Mughal

  5. Nutrition and Bone Health, Medical Research Council-Human Nutrition Research, Fulbourn Road, Cambridge, CB1 9NL, UK

    K. A. Ward

Authors
  1. R. L. Ashby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. E. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. A. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Z. Mughal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. A. Ward
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. A. Ward.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ashby, R.L., Adams, J.E., Roberts, S.A. et al. The muscle–bone unit of peripheral and central skeletal sites in children and young adults. Osteoporos Int 22, 121–132 (2011). https://doi.org/10.1007/s00198-010-1216-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-010-1216-3

Keywords

Search

Navigation