Structure and mechanical function of the inter‐lamellar matrix of the annulus fibrosus in the disc

Abstract

The inter-lamellar matrix (ILM) has an average thickness of less than 30 mm and lies between adjacent lamellae in the annulus fibrosus (AF). The microstructure and composition of the ILM have been studied in various anatomic regions of the disc; however, their contribution to AF mechanical properties and structural integrity is unknown. It was suggested that the ILM components, mainly elastic fibers and cross-bridges, play a role in providing mechanical integrity of the AF. Therefore, the manner in which they respond to different loadings and stabilize adjacent lamellae structure will influence AF tear formation and subsequent herniation. This review paper summarizes the composition, microstructure, and potential role of the ILM in the progression of disc herniation, clarifies the micromechanical properties of the ILM, and proposes critical areas for future studies. There are a number of unknown characteristics of the ILM, such as its mechanical role, impact on AF integrity, and ultrastructure of elastic fibers at the ILM-lamella boundary. Determining these characteristics will provide important information for tissue engineering, repair strategies, and the development of more-physiological computational models to study the initiation and propagation of AF tears that lead to herniation and degeneration. Keywords: inter-lamellar matrix; cross-bridges; annulus fibrosus; elastic fibersThe inter-lamellar matrix (ILM) lies between the lamellae of the annulus fibrosus (AF) of the intervertebral disc and has a thickness of less than 30 mm. The ILM is comprised of four main components: Matrix, cross-bridges, elastic fibers, and cells; however, those components are not restricted to the ILM alone (i.e., cross-bridges are present in the ILM space and cross radially through multiple AF layers). 1-5 ILM failure results in delamination (separation of lamellae) and may be one of the initial stages of herniation and degeneration. 6-8 Knowledge of the ILM structure and mechanical function is important to determining the loading conditions under which the AF is at risk of delamination and subsequent disc disruption and herniation. This understanding of the ILM may lead to the development of improved clinical strategies for disc treatment of herniation and painful degenerative disc disorders.AF delamination and tears, and the associated disc degeneration, are directly related to the structural integrity of the ILM. 9-12 Migration of the NP propagates-under certain circumstances-circumferentially, increasing ILM localized stress and risk of delamination in deep (i.e., inner) AF layers. 8 ILM failure and associated delamination alters ovine spine segment mechanics and causes increased lamellar thickness and vertebral bone volume fraction. 7 On the other hand, delamination may also lead to increased tensile loading within the collagenous AF lamellae components. Therefore, the role of the ILM on the AF microstructural integrity 13 and strength is evident, as mechanical properties of multi-lamellae are different from single ...

Annulus fibrosus cell phenotypes in homeostasis and injury: implications for regenerative strategies

“…61,62 This angle-ply structure contributes to the nonlinear and anisotropic mechanical properties of the AF. 63 Adding to this structural complexity, individual lamellae are separated by a disorganized interlamellar tissue containing proteoglycan-rich matrix, elastic fibers, and cells, 13 and are connected by networks of interlamellar cross-bridges consisting of elastin and type VI collagen, which are thought to be important for maintaining healthy AF function. 13,64,65 Elastic fibers are also known to bridge layers, and these have been speculated to be functional tie fibers and/or remnants of vascular channels that regress following IVD development.…”

“…63 Adding to this structural complexity, individual lamellae are separated by a disorganized interlamellar tissue containing proteoglycan-rich matrix, elastic fibers, and cells, 13 and are connected by networks of interlamellar cross-bridges consisting of elastin and type VI collagen, which are thought to be important for maintaining healthy AF function. 13,64,65 Elastic fibers are also known to bridge layers, and these have been speculated to be functional tie fibers and/or remnants of vascular channels that regress following IVD development. 64,66 The organization of this complex fiber-reinforced material also exhibits excellent mechanical performance, inhibiting crack progression and maintaining excellent stiffness behaviors even after damage has accumulated.…”

“…Tissue engineering of biologic laminates demonstrated that cells both develop and respond to the unique cross‐ply fiber form of the AF . There is also a base knowledge on AF mechanical interlamellar interactions . Even with these important advances and knowledge, there remains little information on the characteristic phenotypes of different AF cell populations throughout development, maturity, and aging.…”

“…11 There is also a base knowledge on AF mechanical interlamellar interactions. [12][13][14][15][16] Even with these important advances and knowledge, there remains little information on the characteristic phenotypes of different AF cell populations throughout development, maturity, and aging. Identifying cell phenotypes is challenging since very few markers exist and consequently distinction of AF cell phenotypes is currently based on anatomic separation of cells and tissues.…”

New Horizons in Spine Research: Disc biology, spine biomechanics and pathomechanisms of back pain

“…Novel features of IVD structure and their functional roles are still being identified and the role of the inter‐lamellar matrix is clarified by Tavakoli et al Identifying early degenerative changes requires advanced imaging methods, their quantitation, and their validation in animal models . Effects of degeneration on human motion segment functional biomechanics are clarified in papers using advanced multi‐degree‐of‐freedom biomechanical testing methods, and Muruiki et al further identifies biomechanical changes with spinal level and sex .…”