Dataset Information

Structure-function relations and rigidity percolation in the shear properties of articular cartilage.

ABSTRACT: Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus |G(?)| and both the collagen fiber orientation and polarization. We find a much stronger correlation between |G(?)| and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction vc lead to orders-of-magnitude changes in the modulus with |G(?)| scaling as (vc - v0)(?). Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue's surface.

SUBMITTER: Silverberg JL

PROVIDER: S-EPMC4190603 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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Structure-function relations and rigidity percolation in the shear properties of articular cartilage.

Silverberg Jesse L JL Barrett Aliyah R AR Das Moumita M Petersen Poul B PB Bonassar Lawrence J LJ Cohen Itai I

Biophysical journal 20141001 7

Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet ...[more]

PMID: 25296326

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Project description:SignificanceArticular cartilage exhibits a zonal architecture, comprising three distinct zones: superficial, middle, and deep. Collagen fibers, being the main solid constituent of articular cartilage, exhibit unique angular and size distribution in articular cartilage zones. There is a gap in knowledge on how the unique properties of collagen fibers across articular cartilage zones affect the scattering properties of the tissue.AimThis study hypothesizes that the structural properties of articular cartilage zones affect its scattering parameters. We provide scattering coefficient and scattering anisotropy factor of articular cartilage zones in the spectral band of 400 to 1400 nm. We enumerate the differences and similarities of the scattering properties of articular cartilage zones and provide reasoning for these observations.ApproachWe utilized collimated transmittance and integrating sphere measurements to estimate the scattering coefficients of bovine articular cartilage zones and bulk tissue. We used the relationship between the scattering coefficients to estimate the scattering anisotropy factor. Polarized light microscopy was applied to estimate the depth-wise angular distribution of collagen fibers in bovine articular cartilage.ResultsWe report that the Rayleigh scatterers contribution to the scattering coefficients, the intensity of the light scattered by the Rayleigh and Mie scatterers, and the angular distribution of collagen fibers across tissue depth are the key parameters that affect the scattering properties of articular cartilage zones and bulk tissue. Our results indicate that in the short visible region, the superficial and middle zones of articular cartilage affect the scattering properties of the tissue, whereas in the far visible and near-infrared regions, the articular cartilage deep zone determines articular cartilage scattering properties.ConclusionThis study provides scattering properties of articular cartilage zones. Such findings support future research to utilize optical simulation to estimate the penetration depth, depth-origin, and pathlength of light in articular cartilage for optical diagnosis of the tissue.

Project description:Structural properties of articular cartilage such as proteoglycan content, collagen content and collagen alignment are known to vary over length scales as small as a few microns (Bullough and Goodfellow, 1968; Bi et al., 2006). Characterizing the resulting variation in mechanical properties is critical for understanding how the inhomogeneous architecture of this tissue gives rise to its function. Previous studies have measured the depth-dependent shear modulus of articular cartilage using methods such as particle image velocimetry (PIV) that rely on cells and cell nuclei as fiducial markers to track tissue deformation (Buckley et al., 2008; Wong et al., 2008a). However, such techniques are limited by the density of trackable markers, which may be too low to take full advantage of optical microscopy. This limitation leads to noise in the acquired data, which is often exacerbated when the data is manipulated. In this study, we report on two techniques for increasing the accuracy of tissue deformation measurements. In the first technique, deformations were tracked in a grid that was photobleached on each tissue sample (Bruehlmann et al., 2004). In the second, a numerical technique was implemented that allowed for accurate differentiation of optical displacement measurements by minimizing the propagated experimental error while ensuring that truncation error associated with local averaging of the data remained small. To test their efficacy, we employed these techniques to compare the depth-dependent shear moduli of neonatal bovine and adult human articular cartilage. Using a photobleached grid and numerical optimization to gather and analyze data led to results consistent with those reported previously (Buckley et al., 2008; Wong et al., 2008a), but with increased spatial resolution and characteristic coefficients of variation that were reduced up to a factor of 3. This increased resolution allowed us to determine that the shear modulus of neonatal bovine and adult human tissue both exhibit a global minimum at a depth z of around 100 microm and plateau at large depths. The consistency of the depth dependence of |G*|(Z) for adult human and neonatal bovine tissue suggests a functional advantage resulting from this behavior.

Dataset Information

Structure-function relations and rigidity percolation in the shear properties of articular cartilage.

Publications

Structure-function relations and rigidity percolation in the shear properties of articular cartilage.

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