Skip to main content
Log in

Bone Quality is Dependent on the Quantity and Quality of Organic–Inorganic Phases

  • Original Article
  • Published:
Journal of Medical and Biological Engineering Aims and scope Submit manuscript

Abstract

Background

‘Bone quality’ is widely used in biomedical and clinical communities, to collectively describe all bone characteristics (except bone mineral density) that influence the bone’s resistance to fracture. However, a quantitative relationship between bone quality at the tissue level and bone compositions has not been established.

Methods

We considered bone as an organic–inorganic composite material and proposed that the quality of the bone as well as its organic–inorganic phases is measured by stiffness (Young’s modulus), strength (yield and peak stress) and toughness (energy to failure) at the tissue level. To establish a relationship between bone quality and organic–inorganic compositions, we fabricated 400 cylindrical specimens from bovine leg bones. We tested their mechanical properties under axial compression (N = 200) or axial tension (N = 200). The tested specimens were then fully ashed to determine their organic and inorganic mass fractions. The stiffness, strength and toughness of bone organic–inorganic phases were determined from the tested mechanical properties and phase mass fractions using nonlinear regression.

Results

A novel regression equation was developed to describe the relationships between bone quality and bone compositions.

Conclusion

With recent advances in technologies for in vivo measurement of bone inorganic and organic content, the equation may provide new insight into bone aging and diseases.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Silva, M. J. (2006). Biomechanics of osteoporotic fractures. Injury,38(Suppl 3), S69–S76.

    Google Scholar 

  2. Bouxsein, M. L. (2006). Biomechanics of osteoporotic fractures. Clinical Reviews in Bone and Mineral Metabolism,4, 143–154.

    Article  Google Scholar 

  3. Turber, C. H. (2005). The biomechanics of hip fracture. The Lancet,366, 98–99.

    Article  Google Scholar 

  4. Rubin, K. H., Friis-Holmberg, T., Hermann, A. P., Abrahamsen, B., & Brixen, K. (2013). Risk assessment tools to identify women with increased risk of osteoporotic fracture: Complexity or simplicity? A systematic review. Journal of Bone and Mineral Research,28, 1701–1717.

    Article  Google Scholar 

  5. Marques, A., Ferreira, R. J. O., Santos, E., Loza, E., Carmona, L., & da Silva, J. (2015). The accuracy of osteoporotic fracture risk prediction tools: A systematic review and meta-analysis. Annals of the Rheumatic Diseases,74(Suppl2), 531.

    Google Scholar 

  6. Helgason, B., Perilli, E., et al. (2008). Mathematical relationships between bone density and mechanical properties: A literature review. Clinical Biomechanics,23, 135–146.

    Article  Google Scholar 

  7. Havaldar, R., Pilli, S. C., & Putti, B. B. (2014). Insights into the effects of tensile and compressive loadings on human femur bone. Advanced Biomedical Research,3, 101.

    Article  Google Scholar 

  8. Evans, F. G., & Lissner, H. R. (1957). Tensile and compressive strength of human parietal bone. Journal of Applied Physiology,10, 493–497.

    Article  Google Scholar 

  9. Keaveny, T. M., Wachtel, E. F., Ford, C. M., & Hayes, W. C. (1994). Differences between the tensile and compressive strengths of bovine tibial trabecular bone depend on modulus. Journal of Biomechanics,27, 1137–1146.

    Article  Google Scholar 

  10. Weaver, C. M., Gordon, C. M., Janz, K. F., Kalkwarf, H. J., Lappe, J. M., Lewis, R., et al. (2016). The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: A systematic review and implementation recommendations. Osteoporos International,27, 1281–1386.

    Article  Google Scholar 

  11. Hendrickx, G., Boudin, E., & Van Hul, W. (2015). A look behind the scenes: The risk and pathogenesis of primary osteoporosis. Nature Reviews Rheumatology,11, 462–474.

    Article  Google Scholar 

  12. Santos, L., Elliott-Sale, K. J., & Sale, C. (2017). Exercise and bone health across the lifespan. Biogerontology,18, 931–946.

    Article  Google Scholar 

  13. Cefalu, C. A. (2004). Is bone mineral density predictive of fracture risk reduction? Current Medical Research and Opinion,20, 341–349.

    Article  Google Scholar 

  14. Wilkin, T. J. (2001). For and against: Bone densitometry is not a good predictor of hip fracture. BMJ,323, 795–799.

    Article  Google Scholar 

  15. McClung, M. R. (2012). To FRAX or Not To FRAX. Journal of Bone and Mineral Research,27, 1240–1242.

    Article  Google Scholar 

  16. Marques, A., Lucas, R., Simoes, E., Verstappen, S. M. M., Jacobs, J. W. G., & Silva, J. A. P. (2017). Do we need bone mineral density to estimate osteoporotic fracture risk? A 10-year prospective multicentre validation study. RMD Open,3, e000509.

    Article  Google Scholar 

  17. Bonnick, S. L., & Shulman, L. (2006). Monitoring osteoporosis therapy: Bone mineral density, bone turnover markers, or both? The American Journal of Medicine,119(4A), 25S–31S.

    Article  Google Scholar 

  18. Small, R. E. (2005). Uses and limitations of bone mineral density measurements in the management of osteoporosis. Medscape General Medicine,7, 3.

    Google Scholar 

  19. Seeman, E., & Delmas, P. D. (2006). Bone quality—the material and structural basis of bone strength and fragility. New England Journal of Medicine,354, 2250–2261.

    Article  Google Scholar 

  20. Madsen, O. R., Sørensen, O. H., & Egsmose, C. (2002). Bone quality and bone mass as assessed by quantitative ultrasound and dual energy X ray absorptiometry in women with rheumatoid arthritis: Relationship with quadriceps strength. Annals of the Rheumatic Diseases,61, 325–329.

    Article  Google Scholar 

  21. Sievänen, H., Kannus, P., & Järvinen, T. L. N. (2007). Bone quality: An empty term. PLoS Medicine,4, e27.

    Article  Google Scholar 

  22. Licata, A. (2009). Bone density vs bone quality: What’s a clinician to do? Cleveland Clinic Journal of Medicine,76, 331–336.

    Article  Google Scholar 

  23. Compston, J. (2006). Bone quality: what is it and how is it measured? Arquivos Brasileiros de Endocrinologia & Metabologia,50, 579–585.

    Article  Google Scholar 

  24. Fonseca, H., Moreira-Gonçalves, D., Coriolano, H. J., & Duarte, J. A. (2014). Bone quality: The determinants of bone strength and fragility. Sports Medicine,44, 37–53.

    Article  Google Scholar 

  25. Boskey, A. L. (2013). Bone composition: relationship to bone fragility and antiosteoporotic drug effects. BoneKey Reports,2, 447.

    Article  Google Scholar 

  26. Granke, M., Does, M. D., & Nymna, J. S. (2015). The role of water compartments in the material properties of cortical bone. Calcified Tissue International,97, 292–307.

    Article  Google Scholar 

  27. M.J. Glimcher. Composition, structure, and organization of bone and other mineralized tissues and the mechanism of calcification. In R.O. Greep, E.B. Astwood, editors, Handbook of Physiology: Endocrinology. American Physiological Society, Washington, D.C., 1976.

    Google Scholar 

  28. Bala, Y., & Seeman, E. (2015). Bone’s material constituents and their contribution to bone strength in health, disease, and treatment. Calcified Tissue International,97, 308–326.

    Article  Google Scholar 

  29. Mueller, K. H., Trias, A., & Ray, R. D. (1996). Bone density and composition: Age-related and pathological changes in water and mineral content. Journal of Bone and Joint Surgery America,48, 140–148.

    Article  Google Scholar 

  30. Chen, J., Grogan, S. P., Shao, H., D’Lima, D., Bydder, G. M., Wu, Z., et al. (2015). Evaluation of bound and pore water in cortical bone using ultrashort echo time (UTE) magnetic resonance imaging. NMR in Biomedicine,28, 1754–1762.

    Article  Google Scholar 

  31. J.S. Nyman, A. Roy, X. Shen R.L. Acuna, J.H. Tyler, and X. Wang. The influence of water removal on the strength and toughness of cortical bone. Journal of Biomechanics, 39:931 – 938, 2006.

    Article  Google Scholar 

  32. Seifert, A. C., Wehrli, S. L., & Wehrli, F. W. (2015). Bi-component T2* analysis of bound and pore bone water fractions fails at high field strengths. NMR in Biomedicine,28, 861–872.

    Article  Google Scholar 

  33. Nyman, J. S., Gorochow, L. E., Horch, R. A., et al. (2013). Partial removal of pore and loosely bound water by low-energy drying decreases cortical bone toughness in young and old donors. Journal of the Mechanical Behavior of Biomedical Materials,22, 136–145.

    Article  Google Scholar 

  34. Wolfram, U., & Schwiedrzik, J. (2016). Post-yield and failure properties of cortical bone. Bonekey Report,5, 829.

    Article  Google Scholar 

  35. Mirzaali, M., Bürki, A., Schwiedrzik, J. J., Zysset, P. K., & Wolfram, U. (2015). Continuum damage interactions between tension and compression in osteonal bone. Journal of the Mechanical Behavior of Biomedical Materials,49, 355–369.

    Article  Google Scholar 

  36. Wolfram, U., Gross, T., Pahr, D. H., Schwiedrzik, J., Wilke, H. J., & Zysset, P. K. (2012). Fabric-based Tsai-Wu yield criteria for vertebral trabecular bone in stress and strain space. Journal of the Mechanical Behavior of Biomedical Materials,15, 218–228.

    Article  Google Scholar 

  37. Seber, G. A. F., & Wild, C. J. (2003). Nonlinear Regression. Hoboken, NJ: Wiley-Interscience.

    MATH  Google Scholar 

  38. Christensen, R. M. (1990). A critical evaluation for a class of micromechanics models. Journal of the Mechanics and Physics of Solids,38, 379–404.

    Article  Google Scholar 

  39. An, Y.-H., & Draughn, R. A. (2000). Mechanical testing of bone and the bone-implant interface. New York: CRC Press.

    Google Scholar 

  40. Yan, J., Daga, A., Kumar, R., & Mecholsky, J. J. (2008). Fracture toughness and work of fracture of hydrated, dehydrated, and ashed bovine bone. Journal of Biomechanics,41, 1929–1936.

    Article  Google Scholar 

  41. McElhaney, J. H., Fogle, J., Byars, E., & Weaver, G. (1964). Effect of embalming on the mechanical properties of beef bone. Journal of Applied Physiology,19, 1234–1236.

    Article  Google Scholar 

  42. Pal, S. (2014). Design of artificial human joints & organs. US: Springer.

    Book  Google Scholar 

  43. Currey, J. D., & Brear, K. (1990). Hardness, Young’s modulus and yield stress in mammalian mineralized tissues. Journal of Materials Science: Materials in Medicine,1, 14–20.

    Google Scholar 

  44. L.E.Craig, K.E. Dittmer, and K.G. Thompson. Bones and joints, chapter 2. Saunders Ltd, 6 edition, 2016.

  45. A.L. Boskey and P.G. Robey. The regulatory role of matrix proteins in mineralization of bone, chapter 11. Academic Press, 4 edition, 2013.

  46. Ching, W. Y., Rulis, P., & Misra, A. (2009). Ab initio elastic properties and tensile strength of crystalline hydroxyapatite. Acta Biomaterialia,5, 3067–3075.

    Article  Google Scholar 

  47. Shen, Z. L., Dodge, M. R., Kahn, H., Ballarini, R., & Eppell, S. J. (2008). Stress-strain experiments on individual collagen fibrils. Biophysical Journal,95, 3956–3963.

    Article  Google Scholar 

  48. Wren, T. A. L., Yerby, S. A., Beaupre, G. S., & Carter, D. R. (2001). Mechanical properties of the human achilles tendon. Clinical Biomechanics,16, 245–251.

    Article  Google Scholar 

  49. Blanton, P. L., & Biggs, N. L. (1970). Ultimate tensile strength of fetal and adult human tendons. Journal of Biomechanics,3, 181–184.

    Article  Google Scholar 

  50. Matson, A., Konow, N., Miller, S., Konow, P. P., & Roberts, T. J. (2012). Tendon material properties vary and are interdependent among turkey hindlimb muscles. Journal of Experimental Biology,215, 3552–3558.

    Article  Google Scholar 

  51. Bailey, A. J. (2002). Changes in bone collagen with age and disease. Journal of Musculoskeletal and Neuronal Interactions,2, 529–531.

    Google Scholar 

  52. Panwar, P., Lamour, G., Mackenzie, N. C. W., Yang, H., Ko, F., Li, H., et al. (2015). Changes in structural-mechanical properties and degradability of collagen during aging-associated modifications. The Journal of Biological Chemistry,290, 23291–23306.

    Article  Google Scholar 

  53. Viguet-Carrin, S., Garnero, P., & Delmas, P. D. (2006). The role of collagen in bone strength. Osteoporos International,17, 319–336.

    Article  Google Scholar 

  54. Sroga, G. E., & Vashishth, D. (2012). Effects of bone matrix proteins on fracture and fragility in osteoporosis. Current Osteoporosis Reports,10, 141–150.

    Article  Google Scholar 

  55. Dong, X. N., & Guo, X. E. (2004). The dependence of transversely isotropic elasticity of human femoral cortical bone on porosity. Journal of Biomechanics,37, 1281–1287.

    Article  Google Scholar 

  56. Augat, P., & Schorlemmer, S. (2006). The role of cortical bone and its microstructure in bone strength. Age and Ageing,35(s2), 27–31.

    Article  Google Scholar 

  57. Haynes, R. (1971). Effect of porosity content on the tensile strength of porous materials. Powder Metallurgy,14, 64–70.

    Article  Google Scholar 

  58. Li, L., & Aubertin, M. (2011). A general relationship between porosity and uniaxial strength of engineering materials. Canadian Journal of Civil Engineering,30, 644–658.

    Article  Google Scholar 

  59. Wu, Y., Dai, G., Ackerman, J. L., Hrovat, M. I., Glimcher, M. J., Snyder, B. D., et al. (2007). Water- and fat-suppressed proton projection MRI (WASPI) of rat femur bone. An Official Journal of the International Society for Magnetic Resonance in Medicine,57, 554–567.

    Article  Google Scholar 

  60. Wu, Y., Hrovat, M. I., Ackerman, J. L., Reese, T. G., Cao, H., Ecklund, K., et al. (2010). Bone matrix imaged in vivo by water- and fat-suppressed proton projection MRI (WASPI) of animal and human subjects. Journal of Magnetic Resonance Imaging,31, 954–963.

    Article  Google Scholar 

Download references

Acknowledgements

The reported research has been supported by Research Manitoba and Natural Sciences and Engineering Research Council (NSERC) of Canada, which are gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yunhua Luo.

Ethics declarations

Conflict of interest

The authors declare there is no conflict of interest involved in the reported research.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, Y., Wu, X. Bone Quality is Dependent on the Quantity and Quality of Organic–Inorganic Phases. J. Med. Biol. Eng. 40, 273–281 (2020). https://doi.org/10.1007/s40846-020-00506-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40846-020-00506-x

Keywords

Navigation