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.
Similar content being viewed by others
References
Silva, M. J. (2006). Biomechanics of osteoporotic fractures. Injury,38(Suppl 3), S69–S76.
Bouxsein, M. L. (2006). Biomechanics of osteoporotic fractures. Clinical Reviews in Bone and Mineral Metabolism,4, 143–154.
Turber, C. H. (2005). The biomechanics of hip fracture. The Lancet,366, 98–99.
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.
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.
Helgason, B., Perilli, E., et al. (2008). Mathematical relationships between bone density and mechanical properties: A literature review. Clinical Biomechanics,23, 135–146.
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.
Evans, F. G., & Lissner, H. R. (1957). Tensile and compressive strength of human parietal bone. Journal of Applied Physiology,10, 493–497.
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.
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.
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.
Santos, L., Elliott-Sale, K. J., & Sale, C. (2017). Exercise and bone health across the lifespan. Biogerontology,18, 931–946.
Cefalu, C. A. (2004). Is bone mineral density predictive of fracture risk reduction? Current Medical Research and Opinion,20, 341–349.
Wilkin, T. J. (2001). For and against: Bone densitometry is not a good predictor of hip fracture. BMJ,323, 795–799.
McClung, M. R. (2012). To FRAX or Not To FRAX. Journal of Bone and Mineral Research,27, 1240–1242.
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.
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.
Small, R. E. (2005). Uses and limitations of bone mineral density measurements in the management of osteoporosis. Medscape General Medicine,7, 3.
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.
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.
Sievänen, H., Kannus, P., & Järvinen, T. L. N. (2007). Bone quality: An empty term. PLoS Medicine,4, e27.
Licata, A. (2009). Bone density vs bone quality: What’s a clinician to do? Cleveland Clinic Journal of Medicine,76, 331–336.
Compston, J. (2006). Bone quality: what is it and how is it measured? Arquivos Brasileiros de Endocrinologia & Metabologia,50, 579–585.
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.
Boskey, A. L. (2013). Bone composition: relationship to bone fragility and antiosteoporotic drug effects. BoneKey Reports,2, 447.
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.
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.
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.
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.
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.
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.
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.
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.
Wolfram, U., & Schwiedrzik, J. (2016). Post-yield and failure properties of cortical bone. Bonekey Report,5, 829.
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.
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.
Seber, G. A. F., & Wild, C. J. (2003). Nonlinear Regression. Hoboken, NJ: Wiley-Interscience.
Christensen, R. M. (1990). A critical evaluation for a class of micromechanics models. Journal of the Mechanics and Physics of Solids,38, 379–404.
An, Y.-H., & Draughn, R. A. (2000). Mechanical testing of bone and the bone-implant interface. New York: CRC Press.
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.
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.
Pal, S. (2014). Design of artificial human joints & organs. US: Springer.
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.
L.E.Craig, K.E. Dittmer, and K.G. Thompson. Bones and joints, chapter 2. Saunders Ltd, 6 edition, 2016.
A.L. Boskey and P.G. Robey. The regulatory role of matrix proteins in mineralization of bone, chapter 11. Academic Press, 4 edition, 2013.
Ching, W. Y., Rulis, P., & Misra, A. (2009). Ab initio elastic properties and tensile strength of crystalline hydroxyapatite. Acta Biomaterialia,5, 3067–3075.
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.
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.
Blanton, P. L., & Biggs, N. L. (1970). Ultimate tensile strength of fetal and adult human tendons. Journal of Biomechanics,3, 181–184.
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.
Bailey, A. J. (2002). Changes in bone collagen with age and disease. Journal of Musculoskeletal and Neuronal Interactions,2, 529–531.
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.
Viguet-Carrin, S., Garnero, P., & Delmas, P. D. (2006). The role of collagen in bone strength. Osteoporos International,17, 319–336.
Sroga, G. E., & Vashishth, D. (2012). Effects of bone matrix proteins on fracture and fragility in osteoporosis. Current Osteoporosis Reports,10, 141–150.
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.
Augat, P., & Schorlemmer, S. (2006). The role of cortical bone and its microstructure in bone strength. Age and Ageing,35(s2), 27–31.
Haynes, R. (1971). Effect of porosity content on the tensile strength of porous materials. Powder Metallurgy,14, 64–70.
Li, L., & Aubertin, M. (2011). A general relationship between porosity and uniaxial strength of engineering materials. Canadian Journal of Civil Engineering,30, 644–658.
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.
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.
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
Corresponding author
Ethics declarations
Conflict of interest
The authors declare there is no conflict of interest involved in the reported research.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40846-020-00506-x