Viscoelastic characterization of the porcine temporomandibular joint disc under unconfined compression

Pathophysiology of the temporomandibular joint (TMJ) disc is central to many orofacial disorders; however, mechanical characterization of this tissue is incomplete. In this study, we identified surface-regional mechanical variations in the porcine TMJ disc under unconfined compression. The intermediate zone, posterior, anterior, lateral, and medial regions of eight TMJ discs were sectioned into inferior and superior surface samples. Surface-regional sections were then subjected to incremental stress relaxation tests. Single strain step (SSS) and final deformation (FD) viscoelastic models were fit to experimental data. Both models represented the experimental data with a high degree of accuracy (R(2)=0.93). The instantaneous modulus and relaxation modulus for the TMJ disc sections were approximately 500 kPa and 80 kPa, respectively; the coefficient of viscosity was approximately 3.5 MPa-s. Strain dependent material properties were observed across the disc's surface-regions. Regional variations in stiffness were observed in both models. The relaxation modulus was largest in the inferior-medial parts of the disc. The instantaneous modulus was largest in the posterior and anterior regions of the disc. Surface-to-surface variations were observed in the relaxation modulus for only the FD model; the inferior surface was found to be more resistant to compression than the superior surface. The results of this study imply the stiffness of the TMJ disc may change as strain is applied. Furthermore, the lateral region exhibited a lower viscosity and stiffness compared to other disc regions. Both findings may have important implications on the TMJ disc's role in jaw motion and function.     

Tensile properties of the mandibular condylar cartilage

Mandibular condylar cartilage plays a crucial role in temporomandibular joint (TMJ) function, which includes facilitating articulation with the temporomandibular joint disc and reducing loads on the underlying bone. The cartilage experiences considerable tensile forces due to direct compression and shear. However, only scarce information is available about its tensile properties. The present study aims to quantify the biomechanical characteristics of the mandibular condylar cartilage to aid future three-dimensional finite element modeling and tissue engineering studies. Porcine condylar cartilage was tested under uniaxial tension in two directions, anteroposterior and mediolateral, with three regions per direction. Stress relaxation behavior was modeled using the Kelvin model and a second-order generalized Kelvin model, and collagen fiber orientation was determined by polarized light microscopy. The stress relaxation behavior of the tissue was biexponential in nature. The tissue exhibited greater stiffness in the anteroposterior direction than in the mediolateral direction as reflected by higher Young's (2.4 times), instantaneous (1.9 times), and relaxed (1.9 times) moduli. No significant differences were observed among the regional properties in either direction. The predominantly anteroposterior macroscopic fiber orientation in the fibrous zone of condylar cartilage correlated well with the biomechanical findings. The condylar cartilage appears to be less stiff and less anisotropic under tension than the anatomically and functionally related TMJ disc. The anisotropy of the condylar cartilage, as evidenced by tensile behavior and collagen fiber orientation, suggests that the shear environment of the TMJ exposes the condylar cartilage to predominantly but not exclusively anteroposterior loading.     

Stress relaxation behaviors of articular cartilages in porcine temporomandibular joint

In this study, we tested the compressive stress relaxation behaviors of the mandibular condylar and temporal cartilages in the porcine temporomandibular joint (TMJ). The aim was to determine the quantitative and qualitative similarities and differences of compressive stress relaxation behaviors between the two cartilages. Ten porcine TMJs were used; the articular surface was divided into 5 regions: anterior, central, posterior, lateral and medial. Compressive relaxation test was carried out at a strain level of 5% in each region of the two cartilages. The stress relaxation was monitored over a period of 5 min. In all the regions of the two cartilages, the time-dependent stress relaxation curves showed a marked drop in stress within the initial 10 s, which can be fitted by a standard linear viscoelastic model. The instantaneous moduli in the temporal cartilage were dominantly larger than those in the condylar cartilage, while the condylar cartilage had slightly larger relaxation moduli than the temporal cartilage except for the medial region. The both cartilages showed the regional differences in the compressive stress relaxation behavior, and in the temporal cartilage the lateral and medial regions revealed the largest values for the instantaneous and relaxation moduli. The present results demonstrate that the viscoelastic properties of compressive stress relaxation in both cartilages are region-specific, which might have an important implication for stress distribution and transmission along with the TMJ disc.     

The region-dependent biphasic viscoelastic properties of human temporomandibular joint discs under confined compression

The objective of this study was to determine the biphasic viscoelastic properties of human temporomandibular joint (TMJ) discs, correlate these properties with disc biochemical composition, and examine the relationship between these properties and disc dynamic behavior in confined compression. The equilibrium aggregate modulus (H_A), hydraulic permeability (k), and dynamic modulus were examined between five disc regions. Biochemical assays were conducted to quantify the amount of water, collagen, and glycosaminoglycan (GAG) content in each region. The creep tests showed that the average equilibrium moduli of the intermediate, lateral, and medial regions were significantly higher than for the anterior and posterior regions (69.75±11.47 kPa compared to 22.0±5.15 kPa). Permeability showed the inverse trend with the largest values in the anterior and posterior regions (8.51±1.36×10^?15 m⁴/Ns compared with 3.75±0.72×10^?15 m⁴/Ns). Discs were 74.5% water by wet weight, 62% collagen, and 3.2% GAG by dry weight. Regional variations were only observed for water content which likely results in the regional variation in biphasic mechanical properties. The dynamic modulus of samples during confined compression is related to the aggregate modulus and hydraulic permeability of the tissue. The anterior and posterior regions displayed lower complex moduli over all frequencies (0.01–3 Hz) with average moduli of 171.8–609.3 kPa compared with 454.6–1613.0 kPa for the 3 central regions. The region of the TMJ disc with higher aggregate modulus and lower permeability had higher dynamic modulus. Our results suggested that fluid pressurization plays a significant role in the load support of the TMJ disc under dynamic loading conditions.     

An accurate finite element model of the cervical spine under quasi-static loading

Cervical disc injury due to impact has been observed in clinical and biomechanical investigations; however, there is a lack of data that helps to elucidate the mechanisms of disc injury during these collisions. Therefore, it is necessary to understand the behavior of the cervical spine under different types of loading situations. A three dimensional finite element (FE) model for the multi-level cervical spine segment (C0-C7) was developed using computed tomography (CT) data and applied to study the internal stresses and strains of the intervertebral discs under quasi-static loading conditions. The intervertebral discs were treated as nonlinear, anisotropic and incompressible subjected to large deformations. The model accuracy was validated by comparing it with previously published experimental and numerical results for different movements. It was shown that the use of a fiber reinforced model to describe the behavior of the annulus of the discs would predict higher maximum shear strains than an isotropic one, being therefore important the use of complex constitutive models in order to be able to detect the appearance of injured zones, since those strains and stresses are supposed to be related with damage to soft tissues. Several movements were analyzed: flexion, extension and axial rotation, obtaining that the maximum shear stresses in the disc were higher for a flexo-extension movement.     

Regional and disease-related differences in properties of the equine temporomandibular joint disc

Temporomandibular joint (TMJ) disorders affect up to 12% of the human population, and naturally occurring TMJ diseases are increasingly recognized in animals. The TMJ disc plays a major role in TMJ disorders in people, but little is known about its role in TMJ pathology in animals. This study characterizes differences in properties of equine TMJ discs associated with age, disc region, and presence of TMJ osteoarthritis (OA). Discs were dissected from both TMJ’s of sixteen horses euthanized for reasons unrelated to this study. Each joint was grossly evaluated and scored as normal, mild OA, or severe OA. Samples from the rostral, caudal, lateral, central, and medial regions of the disc were subject to compressive testing, quantitative biochemistry, and histology. Samples from the lateral, central, and medial region were tested for tensile properties in the rostrocaudal and mediolateral directions. We found that the equine TMJ disc is highly anisotropic, and its glycosaminoglycan (GAG) content and compressive stiffness vary between disc regions. The disc also exhibits increasing GAG content and compressive stiffness with increasing age. While equine TMJ disc properties are generally similar to other herbivores, greater compressive stiffness throughout the disc and greater GAG content in its rostral region suggest that mechanical demands on the TMJ disc differ between horses and other species. Importantly, a region-specific decrease in compressive stiffness was observed associated with joint disease and corresponded to cartilage erosions in the underlying condylar surface.     

The temporomandibular joint disc of Asian elephant (Elephas maximus) and African elephant (Loxodonta africana)

The temporomandibular joint (TMJ) is a synovial articulation between the mandibular head of the condylar process of the mandible and the mandibular fossa of the squamous temporal bone. Extensions of the fibrous capsule into the joint space form a biconcave disc that functions as an articulating surface and divides the joint into dorsal and ventral compartments. The TMJ disc plays a crucial role in normal functioning of the joint, and differences in cranial morphology, mastication patterns, and diet are reflected in the material and biochemical properties of the disc. The purpose of the present case study was to compare the regional histologic differences between two elephant genera and quantify the biochemical and biomechanical properties of the African elephant disc. This study provides a unique insight into the elephant TMJ disc and also provides a comparison between the African and the Asian elephant genera. The results demonstrate several remarkable findings. First, structure–function relationships exist within the elephant TMJ disc. Second, regional variations exist in the elephant TMJ disc, and these are likely to correlate with its functional requirement. Additionally, it is apparent that some properties of the disc vary with the specific anatomy, diet requirement, and jaw motion. Finally, in comparison with the TMJ disc of other species, it is clear that, although the elephant disc is unique, it has properties that transcend and are preserved among the species.     

Finite element analysis of the temporomandibular joint during lateral excursions of the mandible

One of the most significant characteristics of the temporomandibular joint (TMJ) is that it is in fact composed of two joints. Several finite element simulations of the TMJ have been developed but none of them analysed the different responses of its two sides during nonsymmetrical movement. In this paper, a lateral excursion of the mandible was introduced and the biomechanical behaviour of both sides was studied. A three-dimensional finite element model of the joint comprising the bone components, both articular discs, and the temporomandibular ligaments was used. A fibre-reinforced porohyperelastic model was introduced to simulate the behaviour of the articular discs, taking into account the orientation of the fibres in each zone of these cartilage components. The mandible movement during its lateral excursion was introduced as the loading condition in the analysis. As a consequence of the movement asymmetry, the discs were subjected to different load distributions. It was observed that the maximal shear stresses were located in the lateral zone of both discs and that the lateral attachment of the ipsilateral condyle-disc complex suffered a large distortion, due to the compression of this disc against the inferior surface of the temporal bone. These results may be related with possible consequences of a common disorder called bruxism. Although it would be necessary to perform an exhaustive analysis of this disorder, including the contact forces between the teeth during grinding, it could be suggested that a continuous lateral movement of the jaw may lead to perforations of both discs in their lateral part and may damage the lateral attachments of the disc to the condyle.     

Measurement of geometric deformation of lumbar intervertebral discs under in-vivo weightbearing condition

Quantitative data of spinal intervertebral disc deformation is instrumental for investigation of spinal disc pathology. In this study, we employed a combined dual fluoroscopic imaging system and the MR imaging technique to determine the lumbar disc deformation in living human subjects. Discs at L2-3, L3-4 and L4-5 levels were investigated in 8 normal subjects. The geometric deformation of the discs under full body weight loading condition (upright standing) was determined using the supine, non-weightbearing condition as a reference. The average maximum tensile deformation was ?21% in compression and 24% in tension, and maximum shear deformation on the disc surface reached 26%. The data indicated that different portions of the disc are under different tensile and shear deformation. Further, discs of L2-3, L3-4 and L4-5 have different deformation behavior under the physiological weightbearing condition. In general, the higher level discs have higher deformation values. The technique used in this study can be used to investigate the deformation behaviors of diseased discs as well as the efficacy of different surgical modalities at restoring normal disc deformation patterns.     

The regional contribution of glycosaminoglycans to temporomandibular joint disc compressive properties

Understanding structure-function relationships in the temporomandibular joint (TMJ) disc is a critical first step toward creating functional tissue replacements for the large population of patients suffering from TMJ disc disorders. While many of these relationships have been identified for the collagenous fraction of the disc, this same understanding is lacking for the next most abundant extracellular matrix component, sulfated glycosaminoglycans (GAGs). Though GAGs are known to play a major role in maintaining compressive integrity in GAG-rich tissues such as articular cartilage, their role in fibrocartilaginous tissues in which GAGs are much less abundant is not clearly defined. Therefore, this study investigates the contribution of GAGs to the regional viscoelastic compressive properties of the temporomandibular joint (TMJ) disc. Chondroitinase ABC (C-ABC) was used to deplete GAGs in five different disc regions, and the time course for >95% GAG removal was defined. The compressive properties of GAG depleted regional specimens were then compared to non-treated controls using an unconfined compression stress-relaxation test. Additionally, treated and non-treated specimens were assayed biochemically and histologically to confirm GAG removal. Compared to untreated controls, the only regions affected by GAG removal in terms of biomechanical properties were in the intermediate zone, the most GAG-rich portion of the disc. Without GAGs, all intermediate zone regions showed decreased tissue viscosity, and the intermediate zone lateral region also showed a 12.5% decrease in modulus of relaxation. However, in the anterior and posterior band regions, no change in compressive properties was observed following GAG depletion, though these regions showed the highest compressive properties overall. Although GAGs are not the major extracellular matrix molecule of the TMJ disc, they are responsible for some of the viscoelastic compressive properties of the tissue. Furthermore, the mechanical role of sulfated GAGs in the disc varies regionally in the tissue, and GAG abundance does not always correlate with higher compressive properties. Overall, this study found that sulfated GAGs are important to TMJ disc mechanics in the intermediate zone, an important finding for establishing design characteristics for future tissue engineering efforts.     

Ligament material behavior is nonlinear,viscoelastic and rate-independent under shear loading

The material behavior of ligament is determined by its constituents, their organization and their interaction with each other. To elucidate the origins of the multiaxial material behavior of ligaments, we investigated ligament response to shear loading under both quasi-static and rate-dependent loading conditions. Stress relaxation tests demonstrated that the tissue was highly viscoelastic in shear, with peak loads dropping over 40% during 30 min of stress relaxation. The stress relaxation response was unaffected by three decades of change in shear strain rate (1.3, 13 and 130%/s). A novel parameter estimation technique was developed to determine material coefficients that best described the experimental response of each test specimen to shear. The experimentally measured clamp displacements and reaction forces from the simple shear tests were used with a nonlinear optimization strategy based around function evaluations from a finite element program. A transversely isotropic material with an exponential matrix strain energy provided an excellent fit to experimental load-displacement curves. The shear modulus of human MCL showed a significant increase with increasing shear strain (p<0.001), reaching a maximum of 1.72+/-0.4871 MPa. The results obtained from this study suggest that viscoelasticity in shear does not likely result from fluid flow. Gradual loading of transversely oriented microstructural features such as intermolecular collagen crosslinks or collagen-proteoglycan crosslinking may be responsible for the stiffening response under shear loading.     

Viscoelastic shear properties of the corneal stroma

The cornea is a highly specialized transparent tissue which covers the front of the eye. It is a tough tissue responsible for refracting the light and protecting the sensitive internal contents of the eye. The biomechanical properties of the cornea are primarily derived from its extracellular matrix, the stroma. The majority of previous studies have used strip tensile and pressure inflation testing methods to determine material parameters of the corneal stroma. Since these techniques do not allow measurements of the shear properties, there is little information available on transverse shear modulus of the cornea. The primary objectives of the present study were to determine the viscoelastic behavior of the corneal stroma in shear and to investigate the effects of the compressive strain. A thorough knowledge of the shear properties is required for developing better material models for corneal biomechanics. In the present study, torsional shear experiments were conducted at different levels of compressive strain (0–30%) on porcine corneal buttons. First, the range of linear viscoelasticity was determined from strain sweep experiments. Then, frequency sweep experiments with a shear strain amplitude of 0.2% (which was within the region of linear viscoelasticity) were performed. The corneal stroma exhibited viscoelastic properties in shear. The shear storage modulus, G′, and shear loss modulus, G″, were reported as a function of tissue compression. It was found that although both of these parameters were dependent on frequency, shear strain amplitude, and compressive strain, the average shear storage and loss moduli varied from 2 to 8 kPa, and 0.3 to 1.2 kPa, respectively. Therefore, it can be concluded that the transverse shear modulus is of the same order of magnitude as the out-of-plane Young's modulus and is about three orders of magnitude lower than the in-plane Young's modulus.     

A combined numerical and experimental technique for estimation of the forces and moments in the lumbar intervertebral disc

Evaluation of the loads on lumbar intervertebral discs (IVD) is critically important since it is closely related to spine biomechanics, pathology and prosthesis design. Non-invasive estimation of the loads in the discs remains a challenge. In this study, we proposed a new technique to estimate in vivo loads in the IVD using a subject-specific finite element (FE) model of the disc and the kinematics of the disc endplates as input boundary conditions. The technique was validated by comparing the forces and moments in the discs calculated from the FE analyses to the in vitro experiment measurements of three corresponding lumbar discs. The results showed that the forces and moments could be estimated within an average error of 20%. Therefore, this technique can be a promising tool for non-invasive estimation of the loads in the discs and may be extended to be used on living subjects.     

Compressive and tensile mechanical properties of the porcine nasal septum

The expanding nasal septal cartilage is believed to create a force that powers midfacial growth. In addition, the nasal septum is postulated to act as a mechanical strut that prevents the structural collapse of the face under masticatory loads. Both roles imply that the septum is subject to complex biomechanical loads during growth and mastication. The purpose of this study was to measure the mechanical properties of the nasal septum to determine (1) whether the cartilage is mechanically capable of playing an active role in midfacial growth and in maintaining facial structural integrity and (2) if regional variation in mechanical properties is present that could support any of the postulated loading regimens. Porcine septal samples were loaded along the horizontal or vertical axes in compression and tension, using different loading rates that approximate the in vivo situation. Samples were loaded in random order to predefined strain points (2–10%) and strain was held for 30 or 120 seconds while relaxation stress was measured. Subsequently, samples were loaded until failure. Stiffness, relaxation stress and ultimate stress and strain were recorded. Results showed that the septum was stiffer, stronger and displayed a greater drop in relaxation stress in compression compared to tension. Under compression, the septum displayed non-linear behavior with greater stiffness and stress relaxation under faster loading rates and higher strain levels. Under tension, stiffness was not affected by strain level. Although regional variation was present, it did not strongly support any of the suggested loading patterns. Overall, results suggest that the septum might be mechanically capable of playing an active role in midfacial growth as evidenced by increased compressive residual stress with decreased loading rates. However, the low stiffness of the septum compared to surrounding bone does not support a strut role. The relatively low stiffness combined with high stress relaxation under fast loading rates suggests that the nasal septum is a stress dampener, helping to absorb and dissipate loads generated during mastication.     

Diurnal fluid expression and activity of intervertebral disc cells

The intervertebral discs are large cartilaginous structures situated between the vertebral bodies, occupying around one third of the length of the spinal column. They act as the joints of the spine and carry mechanical load arising from body weight and muscle activity. Loads change with every alteration of posture and activity and the discs thus undergo a diurnal loading pattern with high loads on the discs during the day's activity and low loads on it at night during rest. As the disc is an osmotic system, around 25% of the disc's fluid is expressed and re-imbibed during each diurnal cycle with consequent changes in the osmotic environment of the disc cells. Here, present information on the effect of osmotic changes in disc cell metabolism is reviewed; results indicate that prevailing osmolarity is a powerful regulator of disc cell activity.     

In vivo liver tissue mechanical properties by Transient Elastography: comparison with Dynamic Mechanical Analysis

Understanding the mechanical properties of human liver is one of the most critical aspects of its numerical modeling for medical applications or impact biomechanics. Generally, model constitutive laws come from in vitro data. However, the elastic properties of liver may change significantly after death and with time. Furthermore, in vitro liver elastic properties reported in the literature have often not been compared quantitatively with in vivo liver mechanical properties on the same organ. In this study, both steps are investigated on porcine liver. The elastic property of the porcine liver, given by the shear modulus G, was measured by both Transient Elastography (TE) and Dynamic Mechanical Analysis (DMA). Shear modulus measurements were realized on in vivo and in vitro liver to compare the TE and DMA methods and to study the influence of testing conditions on the liver viscoelastic properties. In vitro results show that elastic properties obtained by TE and DMA are in agreement. Liver tissue in the frequency range from 0.1 to 4 Hz can be modeled by a two-mode relaxation model. Furthermore, results show that the liver is homogeneous, isotropic and more elastic than viscous. Finally, it is shown in this study that viscoelastic properties obtained by TE and DMA change significantly with post mortem time and with the boundary conditions.     

Nucleotomy reduces the effects of cyclic compressive loading with unloaded recovery on human intervertebral discs

The first objective of this study was to determine the effects of physiological cyclic loading followed by unloaded recovery on the mechanical response of human intervertebral discs. The second objective was to examine how nucleotomy alters the disc?s mechanical response to cyclic loading. To complete these objectives, 15 human L5-S1 discs were tested while intact and subsequent to nucleotomy. The testing consisted of 10,000 cycles of physiological compressive loads followed by unloaded hydrated recovery. Cyclic loading increased compression modulus (3%) and strain (33%), decreased neutral zone modulus (52%), and increased neutral zone strain (31%). Degeneration was not correlated with the effect of cyclic loading in intact discs, but was correlated with cyclic loading effects after nucleotomy, with more degenerate samples experiencing greater increases in both compressive and neutral zone strain following cyclic loading. Partial removal of the nucleus pulposus decreased the compression and neutral zone modulus while increasing strain. These changes correspond to hypermobility, which will alter overall spinal mechanics and may impact low back pain via altered motion throughout the spinal column. Nucleotomy also reduced the effects of cyclic loading on mechanical properties, likely due to altered fluid flow, which may impact cellular mechanotransduction and transport of disc nutrients and waste. Degeneration was not correlated with the acute changes of nucleotomy. Results of this study provide an ideal protocol and control data for evaluating the effectiveness of a mechanically-based disc degeneration treatment, such as a nucleus replacement.     

Dynamic shear properties of the porcine molar periodontal ligament

The role of the periodontal ligament (PDL) is to support the tooth during function and resist external forces applied to it. The dominant vertical component of these forces is associated with shear in the PDL. Little information, however, is available on the dynamic behavior of the PDL in shear. Therefore, the present study was designed to determine the dynamic shear properties of the PDL in the porcine molar (n=10). From dissected mandibles transverse sections of the mesial root of the first molar were obtained at the apical and coronal levels and used for dynamic shear tests. Shear strain (0.5%, 1.0%, and 1.5%) was applied in superoinferior direction parallel to the root axis with a wide range of frequencies (0.01-100 Hz). The dynamic complex and storage moduli increased significantly with the loading frequency, the dynamic loss modulus showed only a small increase. The dynamic elasticity was significantly larger in the coronal region than in the apical region although the dynamic viscosity was similar in both regions. The present results suggest that non-linearities, compression/shear coupling, and intrinsic viscoelasticity affect the shear material behavior of the PDL, which might have important implications for load transmission from tooth to bone and vice versa.     

Contribution of vertebral [corrected] bodies, endplates, and intervertebral discs to the compression creep of spinal motion segments

Spinal segments show non-linear behavior under axial compression. It is unclear to what extent this behavior is attributable to the different components of the segment. In this study, we quantified the separate contributions of vertebral bodies and intervertebral discs to creep of a segment. Secondly, we investigated the contribution of bone and osteochondral endplate (endplates including cartilage) to the deformation of the vertebral body. From eight porcine spines a motion segment, a disc and a vertebral body were dissected and subjected to mechanical testing. In an additional test, cylindrical samples, machined from the lowest thoracic vertebrae of 11 porcine spines, were used to compare the deformation of vertebral bone and endplate. All specimens were subjected to three loading cycles, each comprising a loading phase (2.0 MPa, 15 min) and a recovery phase (0.001 MPa, 30 min). All specimens displayed substantial time-dependent height changes. Average creep was the largest in motion segments and smallest in vertebral bodies. Bone samples with endplates displayed substantially more creep than samples without. In the early phase, behavior of the vertebra was similar to that of the disc. Visco-elastic deformation of the endplate therefore appeared dominant. In the late creep phase, behavior of the segment was similar to that of isolated discs, suggesting that in this phase the disc dominated creep behavior, possibly by fluid flow from the nucleus. We conclude that creep deformation of vertebral bodies contributes substantially to creep of motion segments and that within a vertebral body endplates play a major role.