The bovine patella as a model of early osteoarthritis.

The bovine patella model has been used extensively for studying important structure-function aspects of articular cartilage, including its degeneration. However, the degeneration seen in this model has, to our knowledge, never been adequately compared with human osteoarthritis (OA). In this study, bovine patellae displaying normal to severely degenerate states were compared with human tissue displaying intact cartilage to severe OA. Comparisons of normal and OA features were made with histological scoring, morphometric measurements, and qualitative observations. Differential interference contrast microscopy was used to image early OA changes in the articular cartilage matrix and to investigate whether this method provided comparable quality of visualisation of key structural features with standard histology. The intact bovine cartilage was found to be similar to healthy human cartilage and the degenerate bovine cartilage resembled the human OA tissues with regard to structural disruption, cellularity changes, and staining loss. The extent of degeneration in the bovine tissues matched the mild to moderate range of human OA tissues; however, no bovine samples exhibited late-stage OA. Additionally, in both bovine and human tissues, cartilage degeneration was accompanied by calcified cartilage thickening, tidemark duplication, and the advancement of the cement line by protrusions of bony spicules into the calcified cartilage. This comparison of degeneration in the bovine and human tissues suggests a common pathway for the progression of OA and thus the bovine patella is proposed to be an appropriate model for investigating the structural changes associated with early OA.

New insights into the role of the superficial tangential zone in influencing the microstructural response of articular cartilage to compression.

OBJECTIVE: The purpose of this study was to characterize the microstructural response of healthy cartilage in a perturbed physical environment to compressive loading with a novel channel indentation device. Manipulation of the cartilage physical environment was achieved through (1) removal of the superficial tangential zone (STZ) and (2) varying the saline bathing solution concentration. DESIGN: Cartilage-on-bone blocks were subjected to creep loading under a nominal stress of 4.5 MPa via an indenter consisting of two rectangular platens separated by a narrow channel relief space to create a specific region where cartilage would not be directly loaded. Each sample was fixed in its near-equilibrium deformed state, after which the cartilage microstructure was examined using differential interference contrast (DIC) optical microscopy and scanning electron microscopy (SEM). The cartilage bulge in the channel relief space was studied in detail. RESULTS: STZ removal altered the indentation response at the macro- and microstructural levels. Specifically, the strain in the directly compressed regions was reduced (P=0.012) and the bulge height in the channel relief space was greater (P<0.0001) in the STZ-removed compared with the surface-intact samples. The bulge height in the STZ-removed group was always less than the preloaded cartilage thickness. There was intense shear in the non-directly-loaded regions of intact-cartilage but not in STZ-removed cartilage. Bathing solution concentration influenced only the STZ-removed group, where lower concentrations produced significantly abrupt transitions in matrix continuity between the directly compressed and adjacent non-directly-loaded cartilage (P=0.012). CONCLUSIONS: This study showed that while the surface layer was important in distributing loads away from directly-loaded regions, so were other factors such as the matrix fibrillar interconnectivity, swelling potential, and tissue anisotropy.

Influence of an initiating microsplit on the resistance to compression-induced rupture of the articular surface.

Cartilage-on-bone samples from bovine patellae containing a defined stellar or linear initiating split in the articular surface were incrementally loaded in direct compression with intervening rehydration, until articular surface rupture occurred. All patellae were either normal or exhibited a mild level of surface fibrillation. In all cases the actual loading site was free of disruption. The average rupture stress of the healthy cartilage was significantly higher than that of the mildly degenerate cartilage, and in both tissue categories average rupture stresses were lower for the linear split morphology than for the stellar. We propose that this contrasting rupture behavior is explained by differences in both secondary lineal surface strains associated with the depth of compressive indentation and in the ability of the fibrillar network within the surface layer to re-arrange itself in the localized regions of stress concentration around the initiating split.

Compression of the intervertebral disc with combined flexion and torsion

Bovine caudal motion segments were used to investigate the loss of load-bearing ability under both quasi-static and cyclic loading. 80 motion segments dissected from 41 bovine tails were subjected to quasi-static and cyclic compression...

Rupture of intervertebral disc under internal pressurization

Bovine caudal motion segments were used to investigate the intrinsic failure strenght of the intect intervertebral disc under internal hydrostatic pressure...

Biomechanical factors influencing nuclear disruption of the intervertebral disc.

STUDY DESIGN: A disc model with full anular division was used to investigate how different biomechanical parameters influence the severity of nuclear disruption during compressive loading. OBJECTIVE: To quantify the manner in which flexion, hydration, and loading rate contribute to the breakdown in the intrinsic cohesive structure of the nucleus pulposus. SUMMARY OF BACKGROUND DATA: The risk of disc herniation is known to increase when the disc is loaded in flexed positions. However, there is a lack of experimental data showing how a combination of flexion with different loading rates and hydration levels affects the extent of nuclear disruption. METHODS: A reproducible state of full hydration was established for isolated bovine caudal discs. A period of static preloading at an applied stress of 1 MPa was used to obtain a consistent state of partial hydration. Then 96 discs were subjected to a full-thickness division of the anulus fibrosus and compressed while hydration level, degree of flexion, and rate of loading were varied systematically. RESULTS: A full spectrum of nuclear damage was observed in the tests, ranging from no detectable disruption to sudden sequestration of the entire nucleus. These results were quantified, and a general correlation was established between the severity of disruption and the different loading parameters. CONCLUSIONS: The degree of flexion and the level of hydration were shown to play an important role in influencing the tendency of the nucleus to break loose and extrude through a preexisting anular division. Interestingly, the rate of loading appeared to have only a minor effect on the severity of damage induced in discs that incorporated a full depth anular division.

Deformation and rupture of the articular surface under dynamic and static compression.

Cartilage-on-bone samples were dynamically and statically compressed at various stress levels to determine the deformation and rupture behaviour of the articular surface (AS). Instantaneous deformations were captured photographically by using a transparent indenter in combination with a ultra high speed flash. Principal strains (PS) were evaluated using large deformation theory. The tensile strains induced indirectly in the AS were a function of the rate at which the direct compressive force was applied. At the same compressive stress the tensile strains induced statically were approximately twice those induced dynamically. Rupture of the AS occurred in about 60% of those specimens tested statically at 15 MPa and followed approximately the split-line direction. By contrast, no rupture was observed dynamically even at stresses as high as 28 MPa. In terms of joint function the research demonstrates that the AS is considerably more resistant to rupture under dynamic than under static loading. The biomechanical parameter governing rupture appears to be the level of indirectly induced surface strain rather than the directly applied compressive stress. The very different mechanisms controlling the compressive deformation of articular cartilage (AC) at high vs low rates of loading clearly influence the levels of in-plane strain induced in the AS.

Why is the adolescent joint particularly susceptible to osteochondral shear fracture?

A biomechanical investigation of the dynamic shear failure of the osteochondral region of immature, adolescent, and mature bovine cartilage bone laminates was performed. The osteochondral junction was loaded in pure shear under impact conditions through the cartilage layer only. The results indicate the adolescent tissue fails at a nominal shear stress of 2.0 MPa, whereas the immature and the mature tissues fail at 3.8 MPa and 2.6 MPa, respectively. The adolescent tissue had a significant reduction in the fracture toughness of its osteochondral junction compared with that of the immature or mature tissues. The fracture toughness, describing the energy required to initiate and propagate a crack to failure, was 3.6 kN/m, 2.3 kN/m, and 10.2 kN/m for the immature, adolescent, and mature bovine tissues, respectively. This significant reduction associated with the adolescent osteochondral junction is explained in terms of the structural changes occurring within this important anchoring region during maturation. These findings question the wisdom of subjecting the adolescent joint to high levels and rates of loading.

Effect of loading rate and hydration on the mechanical properties of the disc.

STUDY DESIGN: The mechanical response of bovine intervertebral discs to axial compression at different loading rates and hydration levels was quantified. OBJECTIVES: To quantify the effects of hydration and loading rate on the mechanical response of the intervertebral disc to compressive axial load. SUMMARY OF BACKGROUND DATA: The disc is known to be viscoelastic, but there are few experimental data showing the effect of loading rate and hydration on its response to compression. METHODS: Hydration level reduced by creep-loading from a fully hydrated starting point. Four groups were tested: Group A: fully hydrated (n = 5), six loading rates, from 0.3 kPa/sec to 30 MPa/sec; Group B: after 30 minutes of creep (n = 4); and Group C: after 2 hours of creep (n = 4) under a static load of 1 MPa, loading rates 3 MPa/sec, 30 kPa/sec, and 0.3 kPa/sec; Group D: at 5-minute intervals, during an 8-hour period of creep (n = 3) under a static load of 1 MPa, loading rate 3 MPa/sec. Data normalized by disc area and height: nominal stress, strain, and modulus calculated. RESULTS: Group A: Modulus increased with load and rate of loading, with significant differences among the lower three loading rates. The highest three loading rates were significantly different from the lower rates, but not from each other. Group B: At the two higher loading rates, modulus was greater than in group A. At the lowest loading rate the modulus was similar to that in Group A. Group C: At the highest loading rate, the modulus was less than that of Groups A and B. At the lower two loading rates, the modulus was similar to that in Group A. Group D: The modulus increased in the first 30 minutes and decreased in the interval from 60 to 480 minutes. CONCLUSIONS: Intervertebral disc compressive mechanical properties are significantly dependent on loading rate and hydration.

Concerning the ultrastructural origin of large-scale swelling in articular cartilage.

The swelling behaviour of the general matrix of both normal and abnormally softened articular cartilage was investigated in the context of its relationship to the underlying subchondral bone, the articular surface, and with respect to the primary structural directions represented in its strongly anisotropic collagenous architecture. Swelling behaviours were compared by subjecting tissue specimens under different modes of constraint to a high swelling bathing solution of distilled water and comparing structural changes imaged at the macroscopic, microscopic and ultrastructural levels of resolution. Near zero swelling was observed in the isolated normal general matrix with minimal structural change. By contrast the similarly isolated softened general matrix exhibited large-scale swelling in both the transverse and radial directions. This difference in dimensional stability was attributed to fundamentally different levels of fibril interconnectivity between the 2 matrices. A model of structural transformation is proposed to accommodate fibrillar rearrangements associated with the large-scale swelling in the radial and transverse directions in the softened general matrix.

The importance of physicochemical swelling in cartilage illustrated with a model hydrogel system.

The physicochemically derived swelling stress in articular cartilage plays a crucial role in determining the pattern of stress sharing between the exudable fluid and the 'solid' components comprising its matrix. This pattern of stress sharing in turn influences the manner in which cartilage consolidates or deforms in compression via the outflow of fluid. Synthetic hydrogels exposed to a variety of cationic blocking solutions provide simplified model systems for exploring quantitatively the influence of the intrinsic swelling parameter on consolidation behaviour, thus yielding further insights into the fundamental parameters controlling the biomechanical properties of complex tissues such as articular cartilage.

Experimental factors governing the internal stress state of the intervertebral disc.

This paper presents an experimental study of the response of the intervertebral disc to short-term static-axial loading within the conceptual framework of mechanical consolidation as applied to swelling materials. An experimental technique developed previously for articular cartilage was used to load the disc in compression and measure simultaneously the matrix internal excess pore pressure under both radially constrained and radially unconstrained conditions. Specifically the short-term pattern of development of the hydrostatic excess pore pressure was investigated. The average ratio of the maximum excess pore pressure u(i) to the nominal applied stress for unconstrained loading was approximately 1.9 while for constrained loading it was about 1.4. This behaviour is interpreted in terms of the generation of a pore pressure in the nucleus which reflects a non-uniform partitioning of the applied load across the inhomogeneous structure of the disc. These results provide a quantitative insight into the role that physico-chemically generated swelling plays in determining the internal mechanical response of the disc to an externally applied load and suggest a quantitative means of investigating the important influence of degenerative changes on the internal stress state of the disc without needing to pierce the annular wall in order to insert a pressure sensing device.

Biomechanics of load-bearing of the intervertebral disc: an experimental and finite element model.

This paper presents an experimental and finite element study of the biomechanical response of the intervertebral disc to static-axial loading in which classical consolidation theory was used to analyse its time-dependent response. A newly developed experimental technique was employed to load the disc in compression and measure simultaneously the matrix internal pressure and creep strain for the full consolidation process. It is shown that, upon loading, the disc develops a maximum hydrostatic excess pore pressure which gradually decays as water is exuded from the matrix. During this decay process, the applied load is progressively transferred to the solid components of the matrix until the load is borne in full by the solid at the end of consolidation. Material properties for the tissue were then obtained from the experimental stress-strain data and used in the finite element study in the development of a finite element solution based on Biot's theory of coupled solid-fluid interaction. An axisymmetric formulation was employed and the disc modelled as an anisotropic, non-linear poroelastic solid. A sensitivity analysis of the material properties for the structural components of the disc was carried out and the biomechanical response to compressive loading evaluated and compared to experimental data. The results show that the matrix permeability plays a significant role in determining the transient response of the tissue. Annular disruptions of the disc were shown to result in an increase in the nuclear principal stresses suggesting that disrupted regions of the annulus fibrosus play a reduced role in load bearing.

Dynamic fracture characteristics of the osteochondral junction undergoing shear deformation.

This paper presents a biomechanical study of the dynamic fracture response of the osteochondral regions of both immature and mature cartilage-bone laminates induced through shear loading. An instrumental impact machine, providing both mechanical and real-time macro-photographic fracture data, was used to load the osteochondral region in shear by means of a direct compressive force applied to the cartilage layer only, and in a direction parallel to the plane of the osteochondral junction. This force was applied at a known velocity of 2500 mm/s. Our results show that under these conditions of shear loading the dynamic mode II fracture toughness of the osteochondral region of the mature tissue is approximately 1.5 times that of its immature counterpart, and that the derived dynamic shear stiffness of the immature tissue is about 4 times that of the mature. The structural studies demonstrated that the mature tissue delaminates within a well-defined tidemark region whilst the immature fractures through the subchondral bone into which fingers of articular cartilage penetrate. We suggest that this pseudo-brittleness of the immature tissue could explain why there is an increased susceptibility to osteochondral failure in the younger human joint. Finally, we note that the strength-to-toughness relationship, in which stiffer engineering materials are known to exhibit lower fracture toughness, also applies to the cartilage-bone system.

A biomechanical investigation of unconstrained shear failure of the osteochondral region under impact loading.

This paper presents an investigation into the biomechanics of failure of the osteochondral region under conditions in which the cartilage/bone system was subjected to impact loading in shear through the cartilage layer only. The relationships between the nature of structural integration of the osteochondral region, its mechanism of failure in shear, and its dynamic fracture toughness were examined. The exact mechanism of osteochondral failure was found to be dependent on skeletal maturity. Shear fracture in the immature tissue always occurred subchondrally as a discontinuous propagation of a relatively large, fast moving crack. By contrast, failure in the skeletally mature tissue occurred by the rapid advance of a smaller crack which propagated within the well-defined tidemark region. RELEVANCE: The junction between the compliant articular cartilage and the rigid bone, because it represents an abrupt change in mechanical properties, is a region of potential weakness in the joint system. Clinical findings confirm that failure can occur in the osteochondral region when there is a substantial component of shear loading, and that the immature junction is more susceptible to mechanically induced failure than the mature. This study provides a quantitative assessment of the failure characteristic of the immature and mature osteochondral region under high rates of loading.

The generalized consolidation of articular cartilage: an investigation of its near-physiological response to static load.

This paper presents a study of the response of articular cartilage to compression whilst measuring simultaneously its strain and fluid excess pore pressure using a newly developed experimental apparatus for testing the tissue in its unconfined state. This has provided a comparison of the load-induced responses of the cartilage matrix under axial, radial and 3-D consolidation regimes. Our results demonstrate that the patterns of the hydrostatic excess pore pressure for axial and 3-D consolidation are similar, but differ significantly from that obtained under the more physiologically relevant condition in which the matrix exhibits radial consolidation when loaded either through a non-porous polished stainless steel indenter or an opposing cartilage disc. Based on the transient strain characteristics obtained under axial and unconfined compression we argue that consolidation is indeed the controlling mechanism of cartilage biomechanical function.

Complex nature of stress inside loaded articular cartilage.

We show that in the early stages of loading of the cartilage matrix extensive water exudation and related physicochemical and structural changes give rise to a distinctly consolidatable system. By enzymatically modifying the pre-existing osmotic condition of the normal matrix and measuring its hydrostatic excess pore pressure, we have studied the exact influence of physicochemistry on the consolidation of cartilage. We argue that the attainment of a certain minimum level of swelling stiffness of the solid skeleton, which is developed at the maximum hydrostatic excess pore pressure of the fluid, controls the effective consolidation of articular cartilage. Three related but distinct stresses are developed during cartilage deformation, namely (1) the swelling stress in the coupled proteoglycan/collagen skeleton in the early stages of deformation, (2) the hydrostatic excess pore pressure carried by the fluid component, and (3) the effective stress generated on top of the minimum value of the swelling stress in the consolidation stages following the attainment of the fluid's maximum pore pressure. The minimum value of the swelling pressure is in turn generated over and above the intrinsic osmotic pressure in the unloaded matrix. The response of the hyaluronidase-digested matrix relative to its intact state again highlights the important influence of the osmotic pressure and the coefficient of permeability, both of which are related to the volume fraction of proteoglycans on cartilage deformation, and therefore its ability to function as an effective stress-redistributing layer above the subchondral bone.

The biomechanical ambiguity of the articular surface.

A series of micromechanical tests carried out on the articular surface of cartilage have provided an accurate description of the mechanical properties of any one site with respect to the orientation framework obtained from its characteristic split-line direction. Ultrastructural studies revealed little evidence that the split-line direction correlated strongly with any preferred alignment of fibrils. This paper therefore offers a new interpretation of the biomechanical significance of the widely used split-line test for the articular surface of cartilage.

A physical model for the time-dependent deformation of articular cartilage.

A physical analogue was developed to simulate the time-dependent deformation of articular cartilage. The analogue was constructed from a matrix of water-saturated sponge material whose permeability could be varied, and was constrained so as to allow one-dimensional deformation under both static and dynamic compressive loading. Simultaneous measurements were made of the applied stress, matrix excess pore pressure and matrix strain. The results obtained reinforce the view that under static and low strain-rate loading conditions, a consolidatable system like cartilage sustains the applied stress through a stress-sharing mechanism between matrix water and the solid skeleton. However, at high strain-rates load-bearing is dominated by a mechanism in which the matrix water is immobilized and the excess pore pressure rises to almost that of the applied stress, thus suggesting that the constituents of the matrix act as a single functional entity to support the applied load. The model supports the description of cartilage as a poro-visco-hyperelastic material.

A new biomechanical approach to assessing the fragility of the internal elastic lamina of the arterial wall.

Patterns of tearing of the internal elastic lamina induced by controlled tensile extension of the arterial wall in the axial direction are similar morphologically to those induced in vivo in the anastomosed arteries of experimental arteriovenous fistulae. The mural response is modelled with a simple bi-layer analogue and it is shown that the internal elastic lamina exhibits a greater degree of strain-limiting deformation behavior in the axial direction than the medial and adventitial layers. Application of laminate theory indicates that the frequency of intimal tearing along the vessel length is directly related to the failure strength of the intimal layer.