Strain-induced optical changes in demineralized bone

Abstract. Bone “stress-whitens,” becoming visibly white during mechanical loading, immediately prior to failure. Stress-whitening is known to make materials tougher by dissipating mechanical energy. A greater understanding of stress-whitening, both an optical and mechanical phenomenon, may help explain age-related increases in fracture risk that occur without changes in bone mineralization. In this work, we directly measure the optical properties of demineralized bone as a function of deformation and immersing fluid (with different hydrogen-bonding potentials, water, and ethanol). The change in refractive index of demineralized bone was linear: with deformation and not applied force. Changes in refractive index were likely due to pushing low-refractive-index fluid out of specimens and secondarily due to changes in the refractive index of the collagenous phase. Results were consistent with stress-whitening of demineralized bone previously observed. In ethanol, the refractive index values were lower and less sensitive to deformation compared with deionized water, corroborating the sensitivity to fluid hydration. Differences in refractive index were consistent with structural changes in the collagenous phase such as densification that may also occur under mechanical loading. Understanding bone quality, particularly stress-whitening investigated here, may lead to new therapeutic targets and noninvasive methods to assess bone quality.

[1]  C. M. Agrawal,et al.  Effects of Collagen Unwinding and Cleavage on the Mechanical Integrity of the Collagen Network in Bone , 2002, Calcified Tissue International.

[2]  R. Ritchie,et al.  Effects of polar solvents on the fracture resistance of dentin: role of water hydration. , 2004, Acta biomaterialia.

[3]  Paul K. Hansma,et al.  Plasticity and toughness in bone , 2009 .

[4]  A Heinonen,et al.  Epidemiology of hip fractures. , 1996, Bone.

[5]  Bernard Choi,et al.  Collagen solubility correlates with skin optical clearing. , 2006, Journal of biomedical optics.

[6]  I. S. Saidi,et al.  Mie and Rayleigh modeling of visible-light scattering in neonatal skin. , 1995, Applied optics.

[7]  T. Kuhl,et al.  Interaction forces between DPPC bilayers on glass. , 2013, Langmuir : the ACS journal of surfaces and colloids.

[8]  P Zioupos,et al.  Mechanical properties and the hierarchical structure of bone. , 1998, Medical engineering & physics.

[9]  D. Fyhrie,et al.  Prestress Due to Dimensional Changes Caused by Demineralization: A Potential Mechanism for Microcracking in Bone , 2002, Annals of Biomedical Engineering.

[10]  G. Schitter,et al.  High-speed photography of the development of microdamage in trabecular bone during compression , 2006 .

[11]  M. Hardisty,et al.  Stress-whitening occurs in demineralized bone. , 2013, Bone.

[12]  M. Hardisty,et al.  Do stress-whitening and optical clearing of collagenous tissue occur by the same mechanism? , 2013, Journal of biomechanics.

[13]  J. Israelachvili,et al.  Measurement of forces between two mica surfaces in aqueous electrolyte solutions in the range 0–100 nm , 1978 .

[14]  J. J. Mecholsky,et al.  Fracture toughness and work of fracture of hydrated, dehydrated, and ashed bovine bone. , 2008, Journal of biomechanics.

[15]  P. Fratzl,et al.  Spatial and temporal variations of mechanical properties and mineral content of the external callus during bone healing. , 2009, Bone.

[16]  M. Heuberger The extended surface forces apparatus. Part I. Fast spectral correlation interferometry , 2001 .

[17]  S. Stover,et al.  Relating micromechanical properties and mineral densities in severely suppressed bone turnover patients, osteoporotic patients, and normal subjects. , 2012, Bone.

[18]  A. Ascenzi,et al.  Technique for Dissection and Measurement of Refractive Index of Osteones , 1959, The Journal of biophysical and biochemical cytology.

[19]  J. Israelachvili,et al.  Topographic Information from Multiple Beam Interferometry in the Surface Forces Apparatus , 1997 .

[20]  A. Boskey,et al.  Dilatational band formation in bone , 2012, Proceedings of the National Academy of Sciences.

[21]  M. R. Dodge,et al.  Stress-strain experiments on individual collagen fibrils. , 2008, Biophysical journal.

[22]  Valery V. Tuchin Optical Properties of Tissues with Strong (Multiple) Scattering , 2015 .

[23]  É. Lalor A note on the Lorentz-Lorenz formula and the Ewald-Oseen extinction theorem☆ , 1969 .

[24]  M. Clarkson Multiple-beam interferometry with thin metal films and unsymmetrical systems , 1989 .

[25]  P. Meunier,et al.  The Degree of Mineralization of Bone Tissue Measured by Computerized Quantitative Contact Microradiography , 2002, Calcified Tissue International.

[26]  S. Leikin,et al.  Sugars and polyols inhibit fibrillogenesis of type I collagen by disrupting hydrogen-bonded water bridges between the helices. , 1998, Biochemistry.

[27]  B Chance,et al.  Dependence of tissue optical properties on solute-induced changes in refractive index and osmolarity. , 1996, Journal of biomedical optics.

[28]  Valery V. Tuchin,et al.  Optical Clearing of Cranial Bone , 2008 .

[29]  Xuanhao Sun,et al.  Visualization of a phantom post-yield deformation process in cortical bone. , 2010, Journal of biomechanics.

[30]  D T Delpy,et al.  Measurement of the optical properties of the skull in the wavelength range 650-950 nm , 1993, Physics in medicine and biology.

[31]  Zhengbin Xu,et al.  Spectroscopic visualization of nanoscale deformation in bone: interaction of light with partially disordered nanostructure. , 2010, Journal of biomedical optics.

[32]  S Lees,et al.  Studies of compact hard tissues and collagen by means of Brillouin light scattering. , 1990, Connective tissue research.

[33]  W. Walsh,et al.  Demineralized bone matrix as a template for mineral--organic composites. , 1995, Biomaterials.

[34]  J. Behari,et al.  Absorption spectra of bone , 1977, Calcified Tissue Research.

[35]  K. Meek,et al.  Changes in the refractive index of the stroma and its extrafibrillar matrix when the cornea swells. , 2003, Biophysical journal.

[36]  Valery V. Tuchin,et al.  Optical properties of human cranial bone in the spectral range from 800 to 2000 nm , 2006, Saratov Fall Meeting.

[37]  Christopher G. Rylander,et al.  Dehydration mechanism of optical clearing in tissue. , 2006, Journal of biomedical optics.

[38]  J. H. Koolstra,et al.  The Influence of Mineralization on Intratrabecular Stress and Strain Distribution in Developing Trabecular Bone , 2007, Annals of Biomedical Engineering.

[39]  N Kuznetsova,et al.  Sugars and polyols inhibit fibrillogenesis of type I collagen by disrupting hydrogen-bonded water bridges between the helices. , 1998 .

[40]  Michael D Morris,et al.  Raman Assessment of Bone Quality , 2011, Clinical orthopaedics and related research.

[41]  A. Boskey,et al.  FT-IR imaging of native and tissue-engineered bone and cartilage. , 2007, Biomaterials.

[42]  D. Maurice The structure and transparency of the cornea , 1957, The Journal of physiology.