Lamellar and fibre bundle mechanics of the annulus fibrosus in bovine intervertebral disc

Vergari, Claudio; Mansfield, Jessica C.; Meakin, Judith R.; Winlove, Peter

doi:10.1016/j.actbio.2016.04.002

Cited by 46 publications

(33 citation statements)

References 35 publications

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“…Similar structure and mechanics can be seen in the Online Resource 1 of a previous work, which employed a different experimental protocol (Vergari et al. 2016). In that work, large sliding occurred between bundles of fibres in cow tail samples.…”

Section: Discussionmentioning

confidence: 99%

“…This straightening within bundles of fibres, however, did not occur at 6% applied strain of larger multi-lamellar samples tested in the present work, nor did it occur in a previous study with strains up to 28% (Vergari et al. 2016). Therefore, it is unlikely that fibres can straighten in vivo under physiological loading, although it must be noted that both these works used tail discs; cow lumbar discs might have a different behaviour.…”

Section: Discussionmentioning

confidence: 99%

“…2016) was used for imaging the sample in the radial direction, with the sample orientated so that the z -axis aligned with the radius of the donor disc. The sample was illuminated with an 810-nm mode-locked femto-second Ti:Sapphire laser (Mira 900-D, Coherent Inc.) with a repetition rate of 76 MHz and a pulse width of 100 fs pumped by a 532 nm solid-state laser (Verdi V10, Coherent Inc.).…”

Section: Methodsmentioning

confidence: 99%

“…2016). Briefly, custom software was written in MATLAB 2016b (The MathWorks Inc., Natick, MA) to obtain a displacement map from each series of images and calculate instantaneous microscopic strains.…”

Section: Methodsmentioning

confidence: 99%

“…Recently, advanced imaging techniques (second harmonic generation, SHG) were used to directly observe the kinematics of bundles and lamellae in loaded annulus (Vergari et al. 2016). SHG allows visualization of the collagen network without labelling or specific preparation of the sample; it has been applied to investigate, for instance, the structure and mechanics of cartilage (Cox et al.…”

Section: Introductionmentioning

confidence: 99%

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Bovine and degenerated human annulus fibrosus: a microstructural and micromechanical comparison

Vergari

Chan

Clarke

et al. 2017

Biomech Model Mechanobiol

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The complex structure of the annulus fibrosus is strongly related to its mechanical properties. Recent work showed that it is possible to observe the relative movement of fibre bundles in loaded cow tail annulus; the aim of this work was to describe and quantify annulus fibrosus micromechanics in degenerated human disc, and compare it with cow tail annulus, an animal model often used in the literature. Second harmonic generation was used to image the collagen matrix in twenty strips of annulus fibrosus harvested from intervertebral disc of seven patients undergoing surgery. Samples were loaded to 6% tensile strain in 1% steps. Elastic modulus was calculated from loading curves, and micromechanical strains were calculated from the images using custom software. The same protocol was applied to twenty strips of annulus harvested from cow tail discs. Significant morphological differences were found between human and cow tail samples, the most striking being the lack of collagen fibre crimp in the former. Fibres were also observed bending and running from one lamella to the other, forming a strong flexible interface. Interdigitation of fibre bundles was also present at this interface. Quantitative results show complex patterns of inter-bundle and inter-lamellar behaviour, with inter-bundle sliding being the main strain mechanism. Elastic modulus was similar between species, and it was not affected by the degree of degeneration. This work gives an insight into the complex structure and mechanical function of the annulus fibrosus, which should be accounted for in disc numerical modelling.Electronic supplementary materialThe online version of this article (doi:10.1007/s10237-017-0900-z) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Bovine and degenerated human annulus fibrosus: a microstructural and micromechanical comparison

Vergari

Chan

Clarke

et al. 2017

Biomech Model Mechanobiol

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Insights into the role of water concentrations on nanomechanical behavior of type I collagen‐hyaluronan interfaces in annulus fibrosus: A molecular dynamics investigation

Bhattacharya

Dubey

2023

Numer Methods Biomed Eng

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Multi‐faceted deformation capabilities of Annulus Fibrosus (AF) results from an intricate mechanical design by nature. Wherein, organization and interactions between the constituents, collagen type I (CI), collagen type II (C2), hyaluronan, aggrecan, and water are instrumental. However, mechanisms by which such interactions influence AF mechanics at tissue‐scale is not well understood. This work investigates nanoscale interfacial interactions between CI and hyaluronan (CI‐H) and presents insights into their influence on tissue‐scale mechanics of AF. For this, three‐dimensional molecular dynamics (MD) simulations of tensile and compressive deformation are conducted on atomistic model of CI‐H interface at 0%, 65%, and 75% water concentrations (WC). Results show hyaluronan lowers local hydration around CI component of interface, owing to its hydrophilic nature. Analyses show that increase in WC from 65% to 75% leads to increased interchain sliding in hyaluronan, which further lowers tensile modulus of the interface from 2.1 GPa to 660 MPa, contributing to softening observed from outer to inner AF. Furthermore, increase in WC from 65% to 75%, shifts compressive deformation from buckling‐dominant to non‐buckling‐dominant which contributes towards lower radial bulge at inner AF. Findings provide deeper insights into mechanistic interactions and mechanisms at fundamental length‐scale which influence the AF structure‐mechanics at tissue‐scale.

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Towards engineering distinct multi‐lamellated outer and inner annulus fibrosus tissues

Santerre

Kandel

2017

Journal Orthopaedic Research

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The annulus fibrosus (AF) of the intervertebral disc (IVD) has a zonal distribution of phenotypically distinct cells. The outer AF (OAF) cells produce an extracellular matrix (ECM) rich in type I collagen with little proteoglycans, whereas the ECM of the inner AF (IAF) has abundant type II collagen and proteoglycans. The inhomogeneous distribution of the ECM in the AF may reflect the complex mechanical forces that the IVD experiences. A bioengineered AF tissue should recapitulate both the inner and outer zones in order to have proper functionality. The aim of this study is to generate multi-lamellated OAF and IAF tissues with ECM compositions that resemble their zonal origin using polycarbonate urethane (PU) scaffolds. It was observed that supplementation of the media with insulin-transferrin-selenium (ITS) and proline yielded tissues with good cellularity. However, IAF cells accumulated only type I collagen, similar to OAF cells. Addition of dexamethasone and sodium pyruvate induced the accumulation of IAF tissues rich in type II collagen and aggrecan, without altering the accumulation of type I collagen in OAF tissues. Dexamethasone stimulated mitochondrial membrane potential in both tissues in the presence of sodium pyruvate, suggesting a relationship between the mitochondrial aerobic respiratory state and dexamethasone signalling during the in vitro-tissue formation by OAF and IAF cells. Inhibition of the glucocorticoid receptor blocked the stimulation of mitochondrial membrane potentials and type II collagen accumulation. In summary, biologically distinct multi-lamellated OAF and IAF tissues can be generated, which will facilitate advancement towards the goal of engineering a biological IVD replacement. © 2017 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 36:1346-1355, 2018.

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Lamellar and fibre bundle mechanics of the annulus fibrosus in bovine intervertebral disc

Cited by 46 publications

References 35 publications

Bovine and degenerated human annulus fibrosus: a microstructural and micromechanical comparison

Bovine and degenerated human annulus fibrosus: a microstructural and micromechanical comparison

Insights into the role of water concentrations on nanomechanical behavior of type I collagen‐hyaluronan interfaces in annulus fibrosus: A molecular dynamics investigation

Towards engineering distinct multi‐lamellated outer and inner annulus fibrosus tissues

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