The Role of Water Compartments in the Material Properties of Cortical Bone

Abstract

Comprising ~20% of the volume, water is a key determinant of the mechanical behavior of cortical bone. It essentially exists in 2 general compartments: within pores and bound to the matrix. The amount of pore water – residing in vascular-lacunar-canalicular space – primarily reflects intracortical porosity (i.e., open spaces within the matrix largely due to Haversian canals and resorption sites), and as such, is inversely proportional to most mechanical properties of bone. Movement of water according to pressure gradients generated during dynamic loading likely confers hydraulic stiffening to the bone as well. Nonetheless, bound water is a primary contributor to mechanical behavior of bone in that it is responsible for giving collagen the ability to confer ductility or plasticity to bone (i.e., allows deformation to continue once permanent damage begins to form in the matrix) and decreases with age along with fracture resistance. Thus, dehydration by air-drying or by solvents with less hydrogen bonding capacity causes bone to become brittle, but interestingly, it also increases stiffness and strength across the hierarchical levels of organization. Despite the importance of matrix hydration to fracture resistance, little is known about why bound water decreases with age in hydrated human bone. Using 1H nuclear magnetic resonance (NMR), both bound and pore water concentrations in bone can be measured ex vivo because the proton relaxation times differ between the two water compartments giving rise to two distinct signals. There are also emerging techniques to measure bound and pore water in vivo with magnetic resonance imaging (MRI). NMR/MRI-derived bound water concentration is positively correlated with both strength and toughness of hydrated bone, and may become a useful clinical marker of fracture risk.

Zoledronate treatment has different effects in mouse strains with contrasting baseline bone mechanical phenotypes

“…Post-yield properties are known to be negatively affected by several tissue-level properties including mineralization [25], microdamage [26], collagen cross-linking [27], and hydration [28]. The absence of significant change in tissue-level density (from microCT) suggest some other tissue-level change – such as microdamage, collagen, or hydration – is likely playing a significant role in these B6 mice treated with zoledronate.…”

Raman spectral classification of mineral- and collagen-bound water's associations to elastic and post-yield mechanical properties of cortical bone

“…The porosity was also used to estimate the contribution of unbound water (4) to total Raman intensity because unbound water is richly located in the microscopic pores (29) and there is about 20% unbound water contribution to the total Raman intensities of wet bone (25) . Porosity adjusted Raman intensity was calculated for each biomarker as follows: $$I^{normal\mathit{adj}}=I^{normal\mathit{tot}}(1-p)$$ where I tot was total intensity and p was the percentage of the porosity.…”

Bone Quality Assessment Techniques: Geometric, Compositional, and Mechanical Characterization from Macroscale to Nanoscale

“…Both varieties of water in bone are distinguishable through proton NMR [55]. In a study investigating water content, aging, and mechanical properties ex vivo , bound water increased with age while unbound water correlated to porosity.…”

“…Additionally, both bound and unbound water influenced mechanical properties [56]. The important roles of water in bone and the push towards its use in clinical measurements is described in a recent review [55]. Advances in NMR technology in the past several decades have also enabled ultrafast Magic Angle Spinning (MAS) NMR on solid bone samples [57], [58].…”