Skip to main content
Log in

3D characterization of pores in the cortical bone of human femur in the elderly at different locations as determined by synchrotron micro-computed tomography images

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

Abstract

Summary

Diaphysis, inferior, and lateral superior regions of the femoral neck are subjected to diverse mechanical loads. Using micro-CT based on synchrotron radiation, three-dimensional morphology and connectivity of the pore network are location dependent, underlying different remodeling mechanisms.

Introduction

The three-dimensional (3D) morphology and connectivity of the pore network at various locations in human femurs subjected to diverse mechanical loads were assessed using micro-CT based on synchrotron radiation.

Methods

The cortex from 20 human femurs (mean age, 78.3 ± 12.4 years) was taken from the diaphysis (D), the inferior (IN), and the lateral superior (LS) regions of the femoral neck. The voxel size of the 3D reconstructed image was 7.5 μm. Cortical thickness and pore volume/tissue volume (Po.V/TV), pore diameter (Po.Dm) and spacing (Po.Sp) were determined. The pore surface/pore volume ratio (Po.S/Po.V), the number of pores (Po.N), the degrees of anisotropy (DA), and the connectivity density (ConnD), the degree of mineralization (DMB) were also determined.

Results

The characteristics of the pore network in femoral cortical bone were found to be location dependent. There was greater porosity, Po.Dm, and Po.N, and more large (180–270 μm), extra-large (270–360 μm) and giant pores (>360 μm) in the LS compared to the IN and D. The difference in porosity in between the periosteal and endosteal layers was mostly due to an increase of Po.Dm rather than Po.N. There was a lower DMB of bone in the LS, which is consistent with a higher remodeling rate.

Conclusion

The results provide evidence for large variations in the structure of the internal pore network in cortical bone. These variations could involve different underlying remodeling mechanisms.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761–1767, Review

    Article  PubMed  Google Scholar 

  2. Holzer G, von Skrbensky G, Holzer LA, Pichl W (2009) Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res 24:468–474

    Article  PubMed  Google Scholar 

  3. Schaffler MB, Burr DB (1988) Stiffness of compact bone: effects of porosity and density. J Biomech 21:13–16

    Article  PubMed  CAS  Google Scholar 

  4. Martin RB, Ishida J (1989) The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech 22:419–426

    Article  PubMed  CAS  Google Scholar 

  5. McCalden RW, McGeough JA, Barker MB, Court-Brown CM (1993) Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg Am 75:1193–1205

    PubMed  CAS  Google Scholar 

  6. Yeni YN, Norman TL (2000) Fracture toughness of human femoral neck: effect of microstructure, composition, and age. Bone 26:499–504, Erratum in: Bone 2000 27:327

    Article  PubMed  CAS  Google Scholar 

  7. Stout SD, Brunsden BS, Hildebolt CF, Commean PK, Smith KE, Tappen NC (1999) Computer-assisted 3D reconstruction of serial sections of cortical bone to determine the 3D structure of osteons. Calcif Tissue Int 65:280–284

    Article  PubMed  CAS  Google Scholar 

  8. Müller R (2009) Hierarchical microimaging of bone structure and function. Nat Rev Rheumatol 5:373–381

    Article  PubMed  Google Scholar 

  9. Bousson V, Peyrin F, Bergot C, Haussard M, Sautet A, Laredo J (2004) Cortical bone in the human femoral neck: three-dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res 19:794–801

    Article  PubMed  Google Scholar 

  10. Cooper DM, Erickson B, Peele AG, Hannah K, Thomas CD, Clement JG (2011) Visualization of 3D osteon morphology by synchrotron radiation micro-CT. J Anat 219:481–489

    Article  PubMed  CAS  Google Scholar 

  11. Wachter NJ, Augat P, Krischak GD, Mentzel M, Kinzl L, Claes L (2001) Prediction of cortical bone porosity in vitro by microcomputed tomography. Calcif Tissue Int 68:38–42

    Article  PubMed  CAS  Google Scholar 

  12. Cooper DML, Turinsky AML, Jensen CW, Hallgrimsson B (2003) Quantitative 3D analysis of the canal network in cortical bone by microcomputed tomography. Anat Rec 274:169–179

    Article  CAS  Google Scholar 

  13. Cooper DM, Thomas CD, Clement JG, Turinsky AL, Sensen CW, Hallgrímsson B (2007) Age-dependent change in the 3D structure of cortical porosity at the human femoral midshaft. Bone 40:957–965

    Article  PubMed  Google Scholar 

  14. Cooper D, Turinsky A, Sensen C, Hallgrimsson B (2007) Effect of voxel size on 3D micro-CT analysis of cortical bone porosity. Calcif Tissue Int 80:211–219

    Article  PubMed  CAS  Google Scholar 

  15. Basillais A, Bensamoun S, Chappard C, Brunet-Imbault B, Lemineur G, Ilharreborde B, Ho Ba Tho M, Benhamou C (2007) Three-dimensional characterization of cortical bone microstructure by microcomputed tomography: validation with ultrasonic and microscopic measurements. J Orthop Sci 12:141–148

    Article  PubMed  Google Scholar 

  16. Chen H, Zhou X, Shoumura S, Emura S, Bunai Y (2010) Age- and gender-dependent changes in three-dimensional microstructure of cortical and trabecular bone at the human femoral neck. Osteoporos Int 21:627–636

    Article  PubMed  CAS  Google Scholar 

  17. Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E (2010) Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet 15:1729–1736

    Article  Google Scholar 

  18. Currey JD (2002) Bone: structure and mechanics. Chapter 1. Princeton University Press, Princeton

  19. Brown CU, Yeni YN, Norman TL (1998) Fracture toughness of the femoral neck, femoral shaft, and tibial shaft in aged bone. Adv Bioeng 39:279–280

    Google Scholar 

  20. Lotz JC, Cheal EJ, Hayes WC (1995) Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int 5:252–261

    Article  PubMed  CAS  Google Scholar 

  21. 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 

  22. Nuzzo S, Peyrin F, Cloetens P, Baruchel J, Boivin G (2002) Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography. Med Phys 29:2672–2681

    Article  PubMed  Google Scholar 

  23. Chappard C, Basillais A, Benhamou L, Bonassie A, Brunet-Imbault B, Bonnet N, Peyrin F (2006) Comparison of synchrotron radiation and conventional x-ray microcomputed tomography for assessing trabecular bone microarchitecture of human femoral heads. Med Phys 33:3568–3577

    Article  PubMed  Google Scholar 

  24. Salome M, Peyrin F, Cloetens P, Odet C, Laval-Jeantet AM, Baruchel J, Spanne P (1999) A synchrotron radiation microtomography system for the analysis of trabecular bone samples. Med Phys 26:2194–2204

    Article  PubMed  CAS  Google Scholar 

  25. Hildebrand T (1997) A new method for the model independent assessment of thickness in three dimensional images. J Microsc 185:67–75

    Article  Google Scholar 

  26. Lorensen WE, Cline HE (1988) Marching cubes: a high resolution 3D surface construction algorithm. Comput Graph 21(Suppl 1):7–12

    Google Scholar 

  27. Ulrich D, Van Rietbergen B, Laib A, Ruegsegger P (1999) The ability of three dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25:55–60

    Article  PubMed  CAS  Google Scholar 

  28. Whitehouse WJ (1974) The quantitative morphology of anisotropic trabecular bone. J Microsc 101:153–156

    Article  PubMed  CAS  Google Scholar 

  29. Odgaard A (1997) Three-dimensional methods for quantification of cancellous bone architecture. Bone 20:315–328

    Article  PubMed  CAS  Google Scholar 

  30. Odgaard A, Gundersen HJ (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14:173–182

    Article  PubMed  CAS  Google Scholar 

  31. Norman GR, Streiner DL (2000) Biostatistics: the bare essentials. BC Becker Inc

  32. Cooper DM, Matyas JR, Katzenberg MA, Hallgrimsson B (2004) Comparison of microcomputed tomographic and microradiographic measurements of cortical bone porosity. Calcif Tissue Int 74:437–447

    Article  PubMed  CAS  Google Scholar 

  33. Peyrin F, Salome M, Nuzzo S, Cloetens P, Laval-Jeantet AM, Baruchel J (2000) Perspectives in three-dimensional analysis of bone samples using synchrotron radiation microtomography. Cell Mol Biol 46:1089–1102

    PubMed  CAS  Google Scholar 

  34. Szulc P, Seeman E (2009) Thinking inside and outside the envelopes of bone. Osteoporos Int 20:1281–1288

    Article  PubMed  CAS  Google Scholar 

  35. Bell KL, Loveridge N, Power J, Garrahan N, Meggitt BF, Reeve J (1999) Regional differences in cortical porosity in the fractured femoral neck. Bone 24:57–64

    Article  PubMed  CAS  Google Scholar 

  36. Stein M, Feik S, Thomas C, Clement J, Wark J (1999) An automated analysis of intracortical porosity in human femoral bone across age. J Bone Miner Res 14:624–632

    Article  PubMed  CAS  Google Scholar 

  37. Pfeiffer S, Crowder C, Harrington L, Brown M (2006) Secondary osteon and Haversian canal dimensions as behavioral indicators. Am J Phys Anthropol 131:460–468

    Article  PubMed  Google Scholar 

  38. Bell KL, Loveridge N, Reeve J, Thomas CD, Feik SA, Clement JG (2001) Super-osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec 264:378–386

    Article  PubMed  CAS  Google Scholar 

  39. Orwoll ES (2003) Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18:949–954, Review

    Article  PubMed  Google Scholar 

  40. Allen MR, Burr DB (2005) Human femoral neck has less cellular periosteum, and more mineralized periosteum, than femoral diaphyseal bone. Bone 36:311–316

    Article  PubMed  Google Scholar 

  41. Muller R, Van Campenhout H, Van Damme B, Van Der Perre G, Dequeker J, Hildebrand T, Ruegsegger P (1998) Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone 23:59–66

    Article  PubMed  CAS  Google Scholar 

  42. Thomas CD, Feik S, Clement JG (2006) Increase in pore area, and not pore density, is the main determinant in the development of porosity in human cortical bone. J Anat 209:219–230

    Article  PubMed  Google Scholar 

  43. Peter Z, Bousson V, Bergot C, Peyrin F (2008) A constrained region growing approach based on watershed for the segmentation of low contrast structures in bone micro-CT images. Pattern Recogn 41:2358–2368

    Article  Google Scholar 

Download references

Acknowledgments

None.

Conflicts of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Chappard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chappard, C., Bensalah, S., Olivier, C. et al. 3D characterization of pores in the cortical bone of human femur in the elderly at different locations as determined by synchrotron micro-computed tomography images. Osteoporos Int 24, 1023–1033 (2013). https://doi.org/10.1007/s00198-012-2044-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-012-2044-4

Keywords

Navigation