Skip to main content
Log in

Inter-sex differences in structural properties of aging femora: implications on differential bone fragility: a cadaver study

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

In this paper we examined age-related and sex-specific deterioration in bone strength of the proximal femur reflected in mechanical properties from dual energy X-ray absorptiometry (DXA)-based hip structural analysis (HSA) on a cadaveric sample from the Balkans. Cadaveric studies permit more precise measurement of HSA parameters and allow further analyses by micromorphometric methods. DXA and HSA analysis was performed on a total of 138 cadaveric proximal femora (63 female, 75 male, age range 20–101 years) from Belgrade. HSA parameters are reported for three standard regions of the proximal femur (narrow neck, intertrochanteric, and shaft). Major age-related findings include an increase in the radius of gyration (first reported in this study), a decline in the cross-sectional area (CSA), a shift in the centroid towards the medial cortex, higher buckling ratios and lower section moduli. Whereas age appears to affect mostly the neck region in men, weakening is also evident in the intertrochanteric region in women, particularly after the age of 80. Aging femoral neck declines in bending strength and increases in buckling susceptibility. The reduced bone mass tends to be distributed farther from the centroidal axis (increase in radius of gyration with decline in CSA). Bone mass is preferentially lost from the lateral part of the cross-section shifting the centroid towards the medial cortex which may increase fragility of the lateral part during fall impact. Results of this study contribute to the epidemiologic data on gender differences and age trends in aging male and female femora.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Faulkner KG, Cummings SR, Black D, Palermo L, Gluer CC, Genant HK (1993) Simple measurement of femoral geometry predicts hip fracture: the study of osteoporotic fractures. J Bone Miner Res 8:1211–1217

    Article  PubMed  CAS  Google Scholar 

  2. Faulkner KG (2000) Bone matters: are density increases necessary to reduce fracture risk? J Bone Miner Res 15:183–187

    Article  PubMed  CAS  Google Scholar 

  3. Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259

    PubMed  CAS  Google Scholar 

  4. Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J (2000) Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone 26:305–313

    Article  PubMed  CAS  Google Scholar 

  5. Martin RB (2003) Fatigue microdamage as an essential element of bone mechanics and biology. Calcif Tissue Int 73:101–107

    Article  PubMed  CAS  Google Scholar 

  6. Melton LJ III, Atkinson EJ, O’Fallon WM, Wahner HW, Riggs BL (1993) Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res 8:1227–1233

    Article  PubMed  Google Scholar 

  7. Veenland JF, Link TM, Konermann W, Meier N, Grashuis JL, Gelsema ES (1997) Unraveling the role of structure and density in determining vertebral bone strength. Calcif Tissue Int 61:474–479

    Article  PubMed  CAS  Google Scholar 

  8. Genant HK, Cooper C, Poor G, Reid I, Ehrlich G et al (1999) Interim report and recommendations of the World Health Organization task-force for osteoporosis. Osteoporos Int 10:259–264

    Article  PubMed  CAS  Google Scholar 

  9. De Laet CE, van Hout BA, Burger H, Hofman A, Pols HA (1997) Bone density and risk of hip fracture in men and women: cross sectional analysis. BMJ 315:221–225

    PubMed  Google Scholar 

  10. Stone KL, Seeley DG, Lui LY, Cauley JA, Ensrud K, Browner WS, Nevitt MC, Cummings SR (2003) Osteoporotic Fractures Research Group. BMD at multiple sites and risk of fracture of multiple types: long-term results from the Study of Osteoporotic Fractures. J Bone Miner Res 18:1947–1954

    Article  PubMed  Google Scholar 

  11. Schuit SCE, van der Klift M, Weel AEAM, de Laet CEDH, Burger H, Seeman E, Hofman A, Uitterlinden AG, van Leeuwen JP, Pols HA (2004) Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. Bone 34:195–202

    Article  PubMed  CAS  Google Scholar 

  12. NIH Consensus Statement (2000) Osteoporosis prevention, diagnosis and therapy. NIH Consens Statement 17:1–45

    Google Scholar 

  13. Passi N, Gefen A (2005) Trabecular bone contributes to strength of the proximal femur under mediolateral impact in the avian. J Biomech Eng 127:198–203

    Article  PubMed  CAS  Google Scholar 

  14. 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 25:6–18

    Article  PubMed  CAS  Google Scholar 

  15. Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW (2000) Structural trends in the aging femoral neck and proximal shaft: analysis of the Third National Health and Nutrition Examination Survey dual-energy X-ray absorptiometry data. J Bone Miner Res 15:2297–2304

    Article  PubMed  CAS  Google Scholar 

  16. Crabtree NJ, Kroger H, Martin A, Pols HA, Lorenc R, Nijs J, Stepan JJ, Falch JA, Miazgowski T, Grazio S, Raptou P, Adams J, Collings A, Khaw KT, Rushton N, Lunt M, Dixon AK, Reeve J (2002) Improving risk assessment: hip geometry, bone mineral distribution and bone strength in hip fracture cases and controls. The EPOS study. European Prospective Osteoporosis Study. Osteoporos Int 13:48–54

    Article  PubMed  CAS  Google Scholar 

  17. Yates LB, Karasik D, Beck TJ, Cupples LA, Kiel DP (2007) Hip structural geometry in old and old-old age: similarities and differences between men and women. Bone 41:722–732

    Article  PubMed  Google Scholar 

  18. Nelson DA, Barondess DA, Hendrix SL, Beck TJ (2000) Cross-sectional geometry, bone strength, and bone mass in the proximal femur in black and white postmenopausal women. J Bone Miner Res 15:1992–1997

    Article  PubMed  CAS  Google Scholar 

  19. Khoo BCC, Beck TJ, Qiao QH, Parakh P, Semanick L, Prince RL, Singer KP, Price RI (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 37:112–121

    Article  PubMed  Google Scholar 

  20. Takada J, Beck TJ, Iba K, Yamashita T (2007) Structural trends in the aging proximal femora in Japanese postmenopausal women. Bone 41:97–102

    Article  PubMed  Google Scholar 

  21. Yan L, Crabtree NJ, Reeve J, Zhou B, Dequeker J, Nijs J, Falch JA, Prentice A (2004) Does hip strength analysis explain the lower incidence of hip fracture in the People’s Republic of China? Bone 34:584–588

    Article  PubMed  CAS  Google Scholar 

  22. 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 

  23. Eckstein F, Wunderer C, Boehm H, Kuhn V, Priemel M, Link TM, Lochmüller EM (2004) Reproducibility and side differences of mechanical tests for determining the structural strength of the proximal femur. J Bone Miner Res 19:379–385

    Article  PubMed  Google Scholar 

  24. Looker AC, Beck TJ, Orwoll ES (2001) Does body size account for gender differences in femur bone density and geometry? J Bone Miner Res 16:1291–1299

    Article  PubMed  CAS  Google Scholar 

  25. Duan Y, Beck TJ, Wang XF, Seeman E (2003) Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res 18:1766–1774

    Article  PubMed  Google Scholar 

  26. Seeman E (2001) Sexual dimorphism in skeletal size, density and strength. J Clin Endocrinol Metab 86:4576–4584

    Article  PubMed  CAS  Google Scholar 

  27. Duan Y, Turner CH, Kim BT, Seeman E (2001) Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res 16:2267–2275

    Article  PubMed  CAS  Google Scholar 

  28. Duan Y, Seeman E, Turner CH (2001) The biomechanical basis of vertebral body fragility in men and women. J Bone Miner Res 16:2276–2283

    Article  PubMed  CAS  Google Scholar 

  29. Djuric M, Djonic D, Milovanovic P, Nikolic S, Marshall R, Marinkovic J, Hahn M (2010) Region-specific sex-dependent pattern of age-related changes of proximal femoral cancellous bone and its implications on differential bone fragility. Calcif Tissue Int 86:192–201

    Article  PubMed  CAS  Google Scholar 

  30. LaCroix A, Beck T, Cauley J, Lewis C, Bassford T, Jackson R, Wu G, Chen Z (2010) Hip structural geometry and incidence of hip fracture in postmenopausal women: what does it add to conventional bone mineral density? Osteoporos Int 21:919–929

    Article  PubMed  CAS  Google Scholar 

  31. Uusi-Rasi K, Beck TJ, Semanick LM, Daphtary MM, Crans GG, Desaiah D, Harper KD (2006) Structural effects of raloxifene on the proximal femur: results from the multiple outcomes of raloxifene evaluation trial. Osteoporos Int 17:575–586

    Article  PubMed  CAS  Google Scholar 

  32. Uusi-Rasi K, Semanick L, Zanchetta J, Bogado C, Eriksen E, Sato M, Beck T (2005) Effects of teriparatide [rhPTH (1–34)] treatment on structural geometry of the proximal femur in elderly osteoporotic women. Bone 36:948–958

    Article  PubMed  CAS  Google Scholar 

  33. Travison TG, Beck TJ, Esche GR, Araujo AB, McKinlay JB (2008) Age trends in proximal femur geometry in men: variation by race and ethnicity. Osteoporos Int 19:277–287

    Article  PubMed  CAS  Google Scholar 

  34. Bonnick SL (2007) HSA: beyond BMD with DXA. Bone 41:s9–s12

    PubMed  Google Scholar 

  35. Verhulp E, van Rietbergen B, Huiskes R (2006) Comparison of micro-level and continuum-level voxel models of the proximal femur. J Biomech 39:2951–2957

    Article  PubMed  CAS  Google Scholar 

  36. Lee T, Choi JB, Schafer BW, Segars WP, Eckstein F, Kuhn V, Beck TJ (2009) Assessing the susceptibility to local buckling at the femoral neck cortex to age-related bone loss. Ann Biomed Eng 37:1910–1920

    Article  PubMed  Google Scholar 

  37. Kaptoge S, Beck TJ, Reeve J, Stone KL, Hillier TA, Cauley JA, Cummings 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 

  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. Baudoin C, Fardellone P, Sebert JL (1993) Effect of sex and age on the ratio of cervical to trochanteric hip fracture. A meta-analysis of 16 reports on 36, 451 cases. Acta Orthop Scand 64:647–653

    Article  PubMed  CAS  Google Scholar 

  40. Lesić A, Jarebinski M, Pekmezović T, Bumbasirević M, Spasovski D, Atkinson HD (2007) Epidemiology of hip fractures in Belgrade, Serbia Montenegro, 1990–2000. Arch Orthop Trauma Surg 127:179–183

    Article  PubMed  Google Scholar 

  41. Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J (2005) Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 366:129–135

    Article  PubMed  Google Scholar 

  42. Rudman KE, Aspden RM, Meakin JR (2006) Compression or tension? The stress distribution in the proximal femur. Biomed Eng Online 5:12–19

    Article  PubMed  CAS  Google Scholar 

  43. Li W, Kornak J, Harris T, Keyak J, Li C, Lu Y, Cheng X, Lang T (2009) Identify fracture-critical regions inside the proximal femur using statistical parametric mapping. Bone 44:596–602

    Article  PubMed  Google Scholar 

  44. Kalmey JK, Lovejoy CO (2002) Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading? Bone 31:327–332

    Article  PubMed  CAS  Google Scholar 

  45. Fox JC, Keaveny TM (2001) Trabecular eccentricity and bone adaptation. J Theor Biol 212:211–221

    Article  PubMed  CAS  Google Scholar 

  46. Beck TJ, Oreskovic TL, Stone KL, Ruff CB, Ensrud K, Nevitt MC, Genant HK, Cummings SR (2001) Structural adaptation to changing skeletal load in the progression toward hip fragility: the study of osteoporotic fractures. J Bone Miner Res 16:1108–1119

    Article  PubMed  CAS  Google Scholar 

  47. Beck TJ, Stone KL, Oreskovic TL, Hochberg MC, Nevitt MC, Genant HK, Cummings SR (2001) Effects of current and discontinued estrogen replacement therapy on hip structural geometry: the study of osteoporotic fractures. J Bone Miner Res 16:2103–2110

    Article  PubMed  CAS  Google Scholar 

  48. Crabtree N, Lunt M, Holt G, Kroger H, Burger H et al (2000) Hip geometry, bone mineral distribution, and bone strength in European men and women: the EPOS study. Bone 27:151–159

    Article  PubMed  CAS  Google Scholar 

  49. Szulc P, Garnero P, Marchand F, Duboeuf F, Delmas PD (2005) Biochemical markers of bone formation reflect endosteal bone loss in elderly men––MINOS study. Bone 36:13–21

    Article  PubMed  CAS  Google Scholar 

  50. Szulc P, Uusi-Rasi K, Claustrat B, Marchand F, Beck TJ, Delmas PD (2004) Role of sex steroids in the regulation of bone morphology in men. The MINOS study. Osteoporos Int 15:909–917

    Article  PubMed  CAS  Google Scholar 

  51. Kaptoge S, Dalzell N, Jakes RW, Wareham N, Day NE, Khaw KT, Beck TJ, Loveridge N, Reeve J (2003) Hip section modulus, a measure of bending resistance, is more strongly related to reported physical activity than BMD. Osteoporos Int 14:941–949

    Article  PubMed  CAS  Google Scholar 

  52. Caeiro Rey JR, Dapía Robleda S, del Río Barquero L, Carpintero Benítez P, Esteban Jódar GJ, Muñiz García G (2007) Análisis morfológico, biomecánico y textural de imágenes de densitómetro central DEXA como complemento diagnóstico de la osteoporosis. [Morphological, textural and biomechanical analysis of central DXA images as a diagnostic complement of osteoporosis]. Patol Apar Locomotor 5:55–67

    Google Scholar 

  53. Uusi-Rasi K, Sievänen H, Heinonen A, Beck TJ, Vuori I (2005) Determinants of changes in bone mass and femoral neck structure, and physical performance after menopause: a 9-year follow-up of initially peri-menopausal women. Osteoporos Int 16:616–622

    Article  PubMed  Google Scholar 

  54. Kaptoge S, Jakes RW, Dalzell N, Wareham N, Khaw KT, Loveridge N, Beck TJ, Reeve J (2007) Effects of physical activity on evolution of proximal femur structure in a younger elderly population. Bone 40:506–515

    Article  PubMed  CAS  Google Scholar 

  55. Kannus P, Parkkari J, Sievänen H, Heinonen A, Vuori I, Järvinen M (1996) Epidemiology of hip fractures. Bone 18:57S–63S

    Article  PubMed  CAS  Google Scholar 

  56. Löfman O, Berglund K, Larsson L, Toss G (2002) Changes in hip fracture epidemiology: redistribution between ages, genders and fracture types. Osteoporos Int 13:18–25

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant from the Ministry of Science of the Republic of Serbia, subproject name: “Age-Related Microarchitectural and Mechanical Bone Properties: Implications for Increased Fragility” within the project: “Functional, Functionalized and Advanced Nano Materials”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marija Djuric.

About this article

Cite this article

Djonic, D., Milovanovic, P., Nikolic, S. et al. Inter-sex differences in structural properties of aging femora: implications on differential bone fragility: a cadaver study. J Bone Miner Metab 29, 449–457 (2011). https://doi.org/10.1007/s00774-010-0240-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-010-0240-x

Keywords

Navigation