Micromechanical response of mineral and collagen phases in bone

Almer, J. D.; Stock, S. R.

Affiliations

¹Advanced Photon Source, Argonne National Laboratory, Argonne, IL 60439, USA

²Department of Molecular Pharmacology and Biological Chemistry, Mail Code S215, Northwestern University, 303E Chicago Avenue, Chicago, IL 60611-3008, USA

Abstract and keywords

We report the first simultaneous quantification of Young’s modulus in the separate material phases of bone: collagen and carbonated hydroxyapatite. High-energy X-ray scattering andin situ loading revealed macroscopic, mineral, and collagen Young’s moduli (90% confidence limit) for a canine fibula equaled 24.7(0.2) GPa, 38.2(0.5) GPa {for 00.4 and 43.6(1.4) GPa for 22.2}, and 18(1.2) GPa, respectively. The mineral contained compressive residual stresses on the order of −60 to −80 MPa before loading and had a stress enhancement (ratio of internal to applied stress) between 2.0 and 2.3. The diffraction peak width increased with increasing applied stress, mainly along the bone’s longitudinal direction, and peak widths returned to pre-deformation values when load was removed. In a second fibula section from the same animal, the mineral’s internal stress changed from −50 MPa (22.2 reflection) to −75 MPa (00.4) just after removal from formalin to −10 MPa after eight hours immersion in phosphate-buffered saline; the corresponding change in collagen D-spacing ΔD/D equaled 4.2 × 10⁻³.

Keywords: High-energy X-ray scattering; Bone; Synchrotron X-radiation; Stress; Strain; Young’s modulus

Links

DOI: 10.1016/j.jsb.2006.09.001

PubMed: 17055741

WoS: 000243951800008

History

Received: 2006-05-11

Revised: 2006-08-30

Accepted: 2006-09-7

Online: 2006-09-16

Cited Works (21)

Year	Entry
1999	Rinnerthaler S, Roschger P, Jakob HF, Nader A, Klaushofer K, Fratzl P. Scanning small angle X-ray scattering analysis of human bone sections. Calcif Tiss Int. May 1999;64(5):422-429.
2005	Borah B, Ritman EL, Dufresne TE, Jorgensen SM, Liu S, Sacha J, Phipps RJ, Turner RT. The effect of risedronate on bone mineralization as measured by micro-computed tomography with synchrotron radiation: correlation to histomorphometric indices of turnover. Bone. July 2005;37(1):1-9.
2001	Martin RB, Sharkey NA. Mechanical effects of postmortem changes, preservation, and allograft bone treatments. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:20-1–20-24.
1998	Weiner S, Wagner HD. The material bone: structure-mechanical function relations. Ann Rev Mater Sci. August 1998;28:271-298.
1959	Smith JW, Walmsley R. Factors affecting the elasticity of bone. J Anat. 1959;93(pt 4):503-523.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
1988	Currey JD. The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone. J Biomech. 1988;21(2):131-139.
1999	Currey JD. The design of mineralised hard tissues for their mechanical functions. J Exp Biol. December 1999;202(23):3285-3294.
1990	Schaffler MB, Radin EL, Burr DB. Long-term fatigue behavior of compact bone at low strain magnitude and rate. Bone. 1990;11(5):321-326.
2004	Fratzl P, Gupta HS, Paschalis EP, Roschger P. Structure and mechanical quality of the collagen–mineral nano-composite in bone. J Mater Chem. 2004;14(14):2115-2123.
2005	Gupta HS, Wagermaier W, Zickler GA, Aroush DR-B, Funari SS, Roschger P, Wagner HD, Fratzl P. Nanoscale deformation mechanisms in bone. Nano Lett. October 2005;5(10):2108-2111.
1996	Sasaki N, Odajima S. Stress-strain curve and Young’s modulus of a collagen molecule as determined by the x-ray diffraction technique. J Biomech. May 1996;29(5):655-658.
2006	Gupta HS, Wagermaier W, Zickler GA, Hartmann J, Funari SS, Roschger P, Wagner HD, Fratzl P. Fibrillar level fracture in bone beyond the yield point. Int J Fract. June 2006;139(3-4):425-436.
1999	Reilly GC, Currey JD. The development of microcracking and failure in bone depends on the loading mode to which it is adapted. J Exp Biol. 1999;202(5):543-552.
1982	Gilmore RS, Katz JL. Elastic properties of apatites. J Mater Sci. 1982;17:1131-1141.
2003	Heaney RP. Is the paradigm shifting? Bone. October 2003;33(4):457-465.
2000	Jäger I, Fratzl P. Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys J. October 2000;79(4):1737-1746.
1997	Currey JD, Foreman J, Laketić I, Mitchell J, Pegg DE, Reilly GC. Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res. January 1997;15(1):111-117.
1988	Currey JD. The effects of drying and re-wetting on some mechanical properties of cortical bone. J Biomech. 1988;21(5):439-441.
2005	Almer JD, Stock SR. Internal strains and stresses measured in cortical bone via high-energy X-ray diffraction. J Struct Biol. October 2005;152(1):14-27.
2001	Lucchinetti E. Composite models of bone properties. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:12-1–12-19.

Cited By (19)

Year	Entry
2008	Akhtar R, Daymond MR, Almer JD, Mummery PM. Elastic strains in antler trabecular bone determined by synchrotron x-ray diffraction. Acta Biomater. 2008;4(6):1677-1687.
2014	Gallant MA, Brown DM, Hammond M, Wallace JM, Du J, Deymier-Black AC, Almer JD, Stock SR, Allen MR, Burr DB. Bone cell-independent benefits of raloxifene on the skeleton: a novel mechanism for improving bone material properties. Bone. April 2014;61:191-200.
2020	Taylor EA, Donnelly E. Raman and Fourier transform infrared imaging for characterization of bone material properties. Bone. October 2020;139:115490.
2015	Stock SR. The mineral–collagen interface in bone. Calcif Tiss Int. September 2015;97(3):262-280.
2018	Unal M, Creecy A, Nyman JS. The role of matrix composition in the mechanical behavior of bone. Curr Osteoporos Rep. June 2018;16(3):205-215.
2011	Stock SR, Yuan F, Brinson LC, Almer JD. Internal strain gradients quantified in bone under load using high-energy x-ray scattering. J Biomech. January 11, 2011;44(2):291-296.
2011	Dong XN, Almer JD, Wang X. Post-yield nanomechanics of human cortical bone in compression using synchrotron X-ray scattering techniques. J Biomech. February 24, 2011;44(4):676-682.
2014	Yamada S, Tadano S, Fukuda S. Nanostructure and elastic modulus of single trabecula in bovine cancellous bone. J Biomech. November 7, 2014;47(14):3482-3487.
2016	Georgiadis M, Müller R, Schneider P. Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils. J R Soc Interface. June 1, 2016;13(119):20160088.
2017	Unal M. Classification of Bound Water and Collagen Denaturation Status of Cortical Bone by Raman Spectroscopy [PhD thesis]. Cleveland, OH: Case Western Reserve University; January 2017.
2020	Taylor EA. Validation and Implementation of Vibrational Spectroscopic Measures of Bone Composition [PhD thesis]. Ithaca, NY: Cornell University; December 2020.
2019	Groetsch A. Micro- and Nanomechanics of Mineralised Collagen Fibre Elasto-Plasticity [PhD thesis]. Ebinburgh, Scotland: Heriot-Watt University; November 2019.
2007	Akhtar R. Micromechanical Behaviour of Bone [PhD thesis]. University of Manchester; 2007.
2012	Deymier-Black AC. Study of the Elasto-Plastic Properties of Mineralized Biomaterials Via Synchrotron High-Energy X-Ray Diffraction [PhD thesis]. Evanston, IL: Northwestern University; June 2012.
2012	Yuan F. Finite Element Simulation of the Mechanical Properties of Mineralized Biomaterials [PhD thesis]. Evanston, IL: Northwestern University; August 2012.
2012	Sun X. Mechanically Induced Calcium Efflux from Bone Matrix Stimulates Osteoblasts [PhD thesis]. Purdue University; May 2012.
2012	Barkaoui A. Modélisation multiéchelle du comportement mécano-biologique de l’os humain: De l’ultrastructure au remodelage osseux [PhD thesis]. University of Orleans; 2012.
2018	Creecy A. Age- and Diabetes-Related Changes in the Matrix and Fracture Resistance of Bone [PhD thesis]. Nashville, TN: Vanderbilt University; August 10, 2018.
2014	Schwartz AG. Ihh Signaling and Muscle Forces Are Required for Enthesis Development [PhD thesis]. St. Louis, MO: Washington University in St. Louis; May 2014.