Abstract
Many soft tissues, such as the intervertebral disc (IVD), have a hierarchical fibrous composite structure which suffers from regional damage. We hypothesise that these tissue regions have distinct, inherent fibre structure and structural response upon loading. Here we used synchrotron computed tomography (sCT) to resolve collagen fibre bundles (∼5μm width) in 3D throughout an intact native rat lumbar IVD under increasing compressive load. Using intact samples meant that tissue boundaries (such as endplate-disc or nucleus-annulus) and residual strain were preserved; this is vital for characterising both the inherent structure and structural changes upon loading in tissue regions functioning in a near-native environment. Nano-scale displacement measurements along >10,000 individual fibres were tracked, and fibre orientation, curvature and strain changes were compared between the posterior-lateral region and the anterior region. These methods can be widely applied to other soft tissues, to identify fibre structures which cause tissue regions to be more susceptible to injury and degeneration. Our results demonstrate for the first time that highly-localised changes in fibre orientation, curvature and strain indicate differences in regional strain transfer and mechanical function (e.g. tissue compliance). This included decreased fibre reorientation at higher loads, specific tissue morphology which reduced capacity for flexibility and high strain at the disc-endplate boundary. Statement of significanceThe analyses presented here are applicable to many collagenous soft tissues which suffer from regional damage. We aimed to investigate regional intervertebral disc (IVD) structural and functional differences by characterising collagen fibre architecture and linking specific fibre- and tissue-level deformation behaviours. Synchrotron CT provided the first demonstration of tracking discrete fibres in 3D within an intact IVD. Detailed analysis of regions was performed using over 200k points, spaced every 8 μm along 10k individual fibres. Such comprehensive structural characterisation is significant in informing future computational models. Morphological indicators of tissue compliance (change in fibre curvature and orientation) and fibre strain measurements revealed localised and regional differences in tissue behaviour.
Highlights
Many soft tissues contain a hierarchical fibrous composite microstructure that is vital for their functional competence
Characterisation has been limited by methodology, for example tracking deformations as residual strain was released by dissection is a surface measurement and does not include pressurisation from NP or inherent strains related to endplate attachment [11]
Modelling approaches have attempted to determine the residual strain as a result of swelling pressure and would benefit from the detailed structural characterisation in our results [17]
Summary
Many soft tissues contain a hierarchical fibrous composite microstructure that is vital for their functional competence. The non-linear and anisotropic mechanical properties of these composites allow flexibility as fibres reorganise at low loads, and high stiffness as fibres are strained at high loads. Collagen fibres in tendon are aligned and prestressed to support rapid uptake of tensile loads [1]; whereas alternating layers of angulated fibres engender a controlled compliance ahead of peak load and pressurisation in arteries and intervertebral discs [2, 3] These fibrous tissues, are known to exhibit profound regional susceptibility to failure; with patellar tendinopathy mostly localised to the proximal and posterior portion [4], aneurysms targeted to the abdominal section of the aorta [5] and degeneration in the intervertebral disc – the focus – concentrated to its posterior-lateral region [6, 7]. Despite this wealth of clinical evidence, it remains unknown whether there is a regional distinction in collagen fibre architecture and whether there is region specific fibreand tissue-level deformation behaviours when subjected to mechanical load
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