Introduction Understanding how annular failure might occur following increased nuclear pressurisation requires an experimental approach that avoids artefactual injury to the annulus but reveals structural disruption resulting directly from the pressurisation event. The aim of this study was to investigate the fundamental mechanisms by which both intra and inter-lamellar relationships are disrupted by nuclear pressurisation, with the development of a model that might accurately reproduce mechanisms of intervertebral disc injury secondary to events causing raised intradiscal pressure.

Methods Bovine motion segments were subjected to internal pressurisation using a novel “through vertebra” method. Intra and inter-lamellar sections were deliberately chosen so as to expose systematic patterns of structural disruption resulting from the pressurisation event. This micro-disruption was investigated using a novel method which combined microtensile manipulation and simultaneous differential contrast imaging of the fully hydrated unstained sections.

Results The inner annulus was most severely disrupted. The middle regions developed a series of regular clefts along axes of weakness within the in-plane arrays of fibres in each lamella with a slight oblique passage radially away from the centre. These annular clefts separated the pre-existing transverse or side-to-side interconnections within the longitudinal fibre arrays. Progression to the peripheral lamellae occurred when the clefts crossed lamellae with associated inter-lamellar junction separation, with progressively lesser degrees of disruption further from the central area of pressurisation.

Discussion This study demonstrates that raised intradiscal pressure creates a consistent pattern of annular failure, which may preceed clinically relevant disc lesions, and specifically annular lesions. These findings offer a possible explanation for (a) annular weakening that alters the ability of the nucleus to maintain hydration after load, (b) the initiation of paths for annular tear development, (c) pathways that may expand to allow disc prolapse and (d) pathways for ingrowth of inflammatory and neural tissue mediating disc pain.

Introduction Compressive loads applied to the disc are translated into an internal hydrostatic pressure in the nucleus which is resisted by the annulus. The anisotropic, inhomogeneous, multiply, collagenous architecture of the annulus reflects the complex pattern of mainly tensile stresses developed in this region of the disc during normal function. While many previous investigators have analysed the tensile behaviour of the annulus there still remains much to be learned about the fundamental structural relationships within the disc wall and upon which normal function depends. There is also much to be learned about how alterations in these relationships might lead to disc malfunction. Both intra and inter-lamellar structural relationships will be fundamental to the maintenance of annular wall strength. The aim of this study was to use high resolution ‘live’ imaging to explore the fundamental structural relationships governing the elasticity, intrinsic strength and rupture behaviour of intra-lamellar sections.

Methods In-plane intra-lamellar sections of nominal thickness 70–90μm were cut from the outer lamellae of bovine discs using a sledging microtome. Using a micro-mechanical technique in combination with simultaneous high resolution differential interference contrast optical microscopy (DIC) structural responses both along and transverse to the primary direction of the mono-array of collagen fibres were studied.

Results and Discussion Stretching along the primary alignment direction revealed a biomechanical response consistent with the behaviour of an array of strong fibres whose strength is governed primarily by the strength of embedding in the vertebral endplates rather than from inter-fibre cohesion along their length. The mono-aligned array, even when lacerated, is highly resistant to any further tearing across the alignment direction. Although not visible in the relaxed mono-arrays, transverse stretching revealed a highly complex set of interconnecting structures embodying a series of hierarchical relationships not previously revealed. It is suggested that these structures might play an important role in the containment under pressure of the nuclear contents. The dramatic differences in rupture behaviour observed along versus across the primary fibre direction are consistent with known clinical consequences arising from varying degrees of annular wall damage, and might also explain various types of disc herniation. The lamellar architecture of the healthy disc revealed by this ‘live’ tissue investigation provides an important reference framework for exploring structural changes associated with disc trauma and degeneration.