Skip to main content

Advertisement

SpringerLink
Log in

Mid-Thigh Cortical Bone Structural Parameters, Muscle Mass and Strength, and Association with Lower Limb Fractures in Older Men and Women (AGES-Reykjavik Study)

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

In a cross-sectional study we investigated the relationship between muscle and bone parameters in the mid-thigh in older people using data from a single axial computed tomographic section through the mid-thigh. Additionally, we studied the association of these variables with incident low-trauma lower limb fractures. A total of 3,762 older individuals (1,838 men and 1,924 women), aged 66–96 years, participants in the AGES-Reykjavik study, were studied. The total cross-sectional muscular area and knee extensor strength declined with age similarly in both sexes. Muscle parameters correlated most strongly with cortical area and total shaft area (adjusted for age, height, and weight) but explained <10 % of variability in those bone parameters. The increment in medullary area (MA) and buckling ratio (BR) with age was almost fourfold greater in women than men. The association between MA and muscle parameters was nonsignificant. During a median follow-up of 5.3 years, 113 women and 66 men sustained incident lower limb fractures. Small muscular area, low knee extensor strength, large MA, low cortical thickness, and high BR were significantly associated with fractures in both sexes. Our results show that bone and muscle loss proceed at different rates and with different gender patterns.

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

Similar content being viewed by others

References

  1. 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

    PubMed  CAS  Google Scholar 

  2. Ferretti JL, Cointry GR, Capozza RF, Frost HM (2003) Bone mass, bone strength, muscle–bone interactions, osteopenias and osteoporoses. Mech Ageing Dev 124:269–279

    Article  PubMed  Google Scholar 

  3. Hart KJ, Shaw JM, Vajda E, Hegsted M, Miller SC (2001) Swim-trained rats have greater bone mass, density, strength, and dynamics. J Appl Physiol 91:1663–1668

    PubMed  CAS  Google Scholar 

  4. Warner SE, Shea JE, Miller SC, Shaw JM (2006) Adaptations in cortical and trabecular bone in response to mechanical loading with and without weight bearing. Calcif Tissue Int 79:395–403

    Article  PubMed  CAS  Google Scholar 

  5. Schoenau E, Fricke O (2006) Interaction between muscle and bone. Horm Res 66:73–78

    Article  CAS  Google Scholar 

  6. Bonnet N, Ferrari S (2010) Exercise and the skeleton: how it works and what it really does. IBMS BoneKEy 7:235–248

    Article  Google Scholar 

  7. Bass SL (2000) The prepubertal years: a uniquely opportune stage of growth when the skeleton is most responsive to exercise? Sports Med 30:73–78

    Article  PubMed  CAS  Google Scholar 

  8. MacKelvie KJ, Khan KM, Petit MA, Janssen PA, McKay HA (2003) A school-based exercise intervention elicits substantial bone health benefits: a 2-year randomized controlled trial in girls. Pediatrics 112:e447–e452

    Article  PubMed  Google Scholar 

  9. Matthews BL, Bennell KL, McKay HA, Khan KM, Baxter-Jones ADG, 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 17:1043–1054

    Article  PubMed  CAS  Google Scholar 

  10. Capozza RF, Cointry GR, Cure-Ramírez P, Ferretti JL, Cure-Cure CA (2004) DXA study of muscle–bone relationships in the whole body and limbs of 2,512 normal men and pre- and post-menopausal women. Bone 35:283–295

    Article  PubMed  CAS  Google Scholar 

  11. Ferretti JL, Capozza RF, Cointry GR, García 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  PubMed  CAS  Google Scholar 

  12. Rittweger J, Beller G, Ehrig J, Jung C, Koch U, Ramolla J, Schmidt F, Newitt D, Majumdar S, Schiessl H, Felsenberg D (2000) Bone–muscle strength indices for the human lower leg. Bone 27:319–326

    Article  PubMed  CAS  Google Scholar 

  13. Szulc P, Beck TJ, Marchand F, Delmas PD (2005) Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men—the MINOS study. J Bone Miner Res 20:721–729

    Article  PubMed  Google Scholar 

  14. Melton LJ 3rd, Riggs BL, Achenbach SJ, Amin S, Camp JJ, Rouleau PA, Robb RA, Oberg AL, Khosla S (2006) Does reduced skeletal loading account for age-related bone loss? J Bone Miner Res 21:1847–1855

    Article  PubMed  Google Scholar 

  15. Cousins JM, Petit MA, Paudel ML, Taylor BC, Hughes JM, Cauley JA, Zmuda JM, Cawthon PM, Ensrud KE (2010) Muscle power and physical activity are associated with bone strength in older men: the osteoporotic fractures in men study. Bone 47:205–211

    Article  PubMed  Google Scholar 

  16. Sherrington C, Whitney JC, Lord SR, Herbert RD, Cumming RG, Close JC (2008) Effective exercise for the prevention of falls: a systematic review and meta-analysis. J Am Geriatr Soc 56:2234–2243

    Article  PubMed  Google Scholar 

  17. Lanyon L, Skerry T (2001) Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis. J Bone Miner Res 16:1937–1947

    Article  PubMed  CAS  Google Scholar 

  18. Sigurdsson G, Aspelund T, Chang M, Jonsdottir B, Sigurdsson S, Eiriksdottir G, Gudmundsson A, Harris TB, Gudnason V, Lang TF (2006) Increasing sex difference in bone strength in old age: the age, gene/environment susceptibility-Reykjavik study (AGES-Reykjavik). Bone 39:644–651

    Article  PubMed  Google Scholar 

  19. Kaptoge S, Dalzell N, Loveridge N, Beck TJ, Khaw KT, Reeve J (2003) Effects of gender, anthropometric variables, and aging on the evolution of hip strength in men and women aged over 65. Bone 32:561–570

    Article  PubMed  Google Scholar 

  20. Khosla S, Riggs BL (2005) Pathophysiology of age-related bone loss and osteoporosis. Endocrinol Metab Clin North Am 34:1015–1030

    Article  PubMed  CAS  Google Scholar 

  21. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61:1059–1064

    Article  PubMed  Google Scholar 

  22. Reid IR (2008) Relationships between fat and bone. Osteoporos Int 19:595–606

    Article  PubMed  CAS  Google Scholar 

  23. Blain H, Jaussent J, Thomas E, Micallef JP, Dupuy AM, Bernard PL, Mariano-Goulart D, Cristol JP, Sultan C, Rossi M, Picot MC (2010) Appendicular skeletal muscle mass is the strongest independent factor associated with femoral neck bone mineral density in adult and older men. Exp Gerontol 45:679–684

    Article  PubMed  Google Scholar 

  24. Owings TM, Pavol MJ, Grabiner MD (2002) Lower extremity muscle strength does not independently predict proximal femur bone mineral density in healthy older adults. Bone 30:515–520

    Article  PubMed  CAS  Google Scholar 

  25. Andersen S, Boeskov E, Laurberg P (2005) Ethnic differences in bone mineral density between Inuit and Caucasians in north Greenland are caused by differences in body size. J Clin Densitom 8:409–414

    Article  PubMed  Google Scholar 

  26. Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138:160–169

    PubMed  CAS  Google Scholar 

  27. Segal NA, Torner JC, Yang M, Curtis JR, Felson DT, Nevitt MC (2008) Muscle mass is more strongly related to hip bone mineral density than is quadriceps strength or activity level in adults over age 50. J Clin Densitom 11:503–510

    Article  PubMed  Google Scholar 

  28. Halle JS, Smidt GL, O’Dwyer KD, Lin SY (1990) Relationship between trunk muscle torque and bone mineral content of the lumbar spine and hip in healthy postmenopausal women. Phys Ther 70:690–699

    PubMed  CAS  Google Scholar 

  29. Taaffe DR, Pruitt L, Lewis B, Marcus R (1998) Relationship between bone mineral density of the proximal femur and strength of the hip muscles in postmenopausal women. Am J Phys Med Rehabil 77:477–482

    Article  Google Scholar 

  30. Orwoll ES, Bauer DC, Vogtthe TM, Fox KM (1996) Axial bone mass in older women. Study of osteoporotic fractures research group. Ann Intern Med 124:187–196

    PubMed  CAS  Google Scholar 

  31. Frank AW, Lorbergs AL, Chilibeck PD, Farthing JP, Kontulainen SA (2010) Muscle cross sectional area and grip torque contraction types are similarly related to pQCT derived bone strength indices in the radii of older healthy adults. J Musculoskelet Neuronal Interact 10:136–141

    PubMed  CAS  Google Scholar 

  32. Binkley TL, Specker BL (2008) Muscle–bone relationships in the lower leg of healthy pre-pubertal females and males. J Musculoskelet Neuronal Interact 8:239–243

    PubMed  CAS  Google Scholar 

  33. Rittweger J (2008) Ten years muscle–bone hypothesis: what have we learned so far? J Musculoskelet Neuronal Interact 8:174–178

    PubMed  CAS  Google Scholar 

  34. Lang T, LeBlanc A, Evans H, Lu Y, Genant H, Yu A (2004) Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res 19:1006–1012

    Article  PubMed  Google Scholar 

  35. 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  PubMed  CAS  Google Scholar 

  36. Lee K, Jessop H, Suswillo R, Zaman G, Lanyon L (2003) Bone adaptation requires oestrogen receptor-α. Nature 424:6947

    Google Scholar 

  37. Price J, Sugiyama T, Galea GL, Meakin LB, Sunters A, Lanyon LE (2011) Role of endocrine and paracrine factors in the adaptation of bone to mechanical loading. Curr Osteoporos Rep 9:76–82

    Article  PubMed  Google Scholar 

  38. Rivadeneira F, Zillikens MC, De Laet CE, Hofman A, Uitterlinden AG, Beck TJ, Pols HA (2007) Femoral neck BMD is a strong predictor of hip fracture susceptibility in elderly men and women because it detects cortical bone instability: the Rotterdam study. J Bone Miner Res 22:1781–1790

    Article  PubMed  Google Scholar 

  39. Kaptoge S, Beck TJ, Reeve J, Stone KL, Hillier TA, Cauley JA, Cumming SR (2008) Prediction of incident hip fracture risk by femur geometry variables measured by hip structural analysis in the study of osteoporotic fractures. J Bone Miner Res 23:1892–1904

    Article  PubMed  Google Scholar 

  40. Giangregorio L, McCartney N (2006) Bone loss and muscle atrophy in spinal cord injury: epidemiology, fracture prediction, and rehabilitation strategies. J Spinal Cord Med 29:489–500

    PubMed  Google Scholar 

  41. Jørgensen L, Jacobsen BK, Wilsgaard T, Magnus JH (2000) Walking after stroke: does it matter? Changes in bone mineral density within the first 12 months after stroke. A longitudinal study. Osteoporos Int 11:381–387

    Article  PubMed  Google Scholar 

  42. Lauretani F, Bandinelli S, Griswold ME, Maggio M, Semba R, Guralnik JM, Ferrucci L (2008) Longitudinal changes in BMD and bone geometry in a population-based study. J Bone Miner Res 23:400–408

    Article  PubMed  Google Scholar 

  43. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S (2008) A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res 23:205–214

    Article  PubMed  Google Scholar 

  44. Bailey CA, Kukuljan S, Daly RM (2010) Effects of lifetime loading history on cortical bone density and its distribution in middle-aged and older men. Bone 47:673–680

    Article  PubMed  Google Scholar 

  45. Daly RM, Bass SL (2006) Lifetime sport and leisure activity participation is associated with greater bone size, quality and strength in older men. Osteoporos Int 17:1258–1267

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by NIH contract N01-AG-1-2100, the NIA Intramural Research Program, Hjartavernd (the Icelandic Heart Association), the Althingi (the Icelandic Parliament), and the memorial fund of Helga Jonsdottir and Sigurlidi Kristjansson. G.S. acknowledges support from the University of Iceland Research Fund. The study was approved by the Icelandic National Bioethics Committee (VSN 00-063). The researchers are indebted to the participants for their willingness to participate in the study.

Author information

Authors and Affiliations

  1. University of Iceland, Reykjavik, Iceland

    Fjola Johannesdottir, Thor Aspelund, Brynjolfur Mogensen, Vilmundur G. Gudnason & Gunnar Sigurdsson

  2. Icelandic Heart Association, Kopavogur, Iceland

    Thor Aspelund, Kristin Siggeirsdottir, Sigurdur Sigurdsson, Vilmundur G. Gudnason & Gunnar Sigurdsson

  3. Malmö University Hospital, Malmö, Sweden

    Brynjolfur Y. Jonsson

  4. Landspitali University Hospital, IS-108, Fossvogur, Reykjavik, Iceland

    Brynjolfur Mogensen & Gunnar Sigurdsson

  5. National Institute on Aging, Bethesda, MD, USA

    Tamara B. Harris

  6. University of California, San Francisco, CA, USA

    Thomas F. Lang

Authors
  1. Fjola Johannesdottir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thor Aspelund
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kristin Siggeirsdottir
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brynjolfur Y. Jonsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brynjolfur Mogensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sigurdur Sigurdsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tamara B. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vilmundur G. Gudnason
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Thomas F. Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gunnar Sigurdsson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gunnar Sigurdsson.

Additional information

The authors have stated that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johannesdottir, F., Aspelund, T., Siggeirsdottir, K. et al. Mid-Thigh Cortical Bone Structural Parameters, Muscle Mass and Strength, and Association with Lower Limb Fractures in Older Men and Women (AGES-Reykjavik Study). Calcif Tissue Int 90, 354–364 (2012). https://doi.org/10.1007/s00223-012-9585-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-012-9585-6

Keywords

Search

Navigation