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of Orthodontics and Craniofacial Developmental Biology, Hiroshima University Graduate School of Biomedical Sciences, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8553, Japan; and of Functional Anatomy, Academic Center for Dentistry Amsterdam, Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands; *corresponding author, etanaka@hiroshima-u.ac.jp ABSTRACT: The temporomandibular joint (TMJ) disc consists mainly of collagen fibers and proteoglycans constrained in the interstices of the collagen fiber mesh. This construction results in a viscoelastic response of the disc to loading and enables the disc to play an important role as a stress absorber during function. The viscoelastic properties depend on the direction (tension, compression, and shear) and the type of the applied loading (static and dynamic). The compressive elastic modulus of the disc is smaller than its tensile one because the elasticity of the disc is more dependent on the collagen fibers than on the proteoglycans. When dynamic loading occurs, the disc is likely to behave less stiffly than under static loading because of the difference of fluid flow through and out of the disc during loading. In addition, the mechanical properties change as a result of various intrinsic and extrinsic factors in life such as aging, trauma, and pathology. Information about the viscoelastic behavior of the disc is required for its function to be understood and, for instance, for a suitable TMJ replacement device to be constructed. In this review, the biomechanical behavior of the disc in response to different loading conditions is discussed. Key words. Stress and strain, viscoelasticity, elastic modulus.
Introduction
ince 1980, numerous studies have been conducted to assist investigators in comprehending the biomechanics of the temporomandibular joint (TMJ). Experimental and model studies have verified that the TMJ is loaded during function (macaqueHylander and Bays, 1978, 1979; Brehnan et al., 1981; Boyd et al., 1990; humanHatcher et al., 1986; Smith et al., 1986; Throckmorton and Dechow, 1994). However, detailed data about the distribution of the loads are still lacking. Mathematical models of the human masticatory system, including the TMJ, have served as powerful tools to predict the loads acting on this joint. These models have yielded valuable information on, for example, the role of the disc and that of other tissues of the TMJ in its functioning. Many studies, however, have oversimplified the geometry of the articular surfaces and assumed them to be rigid (e.g., Koolstra et al., 1988; Ferrario and Sforza, 1994). Therefore, the deformations and the distribution of loads inside the joint could not be analyzed. The articular surfaces of the TMJ are highly incongruent. Due to this incongruence, the contact areas of the opposing articular surfaces are very small. When joint loading occurs, this may lead to large peak loads, which may cause damage to the cartilage layers on the articular surfaces. The presence of a fibro-cartilaginous disc in the joint is believed to prevent these peak loads (Tanne et al., 1991; Scapino et al., 1996), since it is capable of deforming and adapting its shape to that of the articular surfaces. These deformations ensure that loads are absorbed and spread over larger contact areas. In addition, the shape of the disc and the area and location of its contact areas with the articular surfaces change continuously during jaw movement to adapt to the changing geometry of the articular surfaces of the mandible and temporal bone. As a result, there will be a continuous change in the magnitude and location of the deformations that occur. For example, according to the
work of Beek et al. (2001b), when loading occurs in the jawclosed position, the deformations in the disc are spread throughout the entire intermediate zone, while translation of the condyle in the forward direction to obtain a protrusive or open jaw position leads to a concentration of the deformation in the lateral part of the disc. This suggests that certain areas of the disc are more heavily loaded than other areas. The magnitude of the deformation and resulting stress of the disc is primarily determined by the nature of the applied loads and by the biomechanical properties of the disc, such as stiffness and strength. An understanding of these properties is important for several reasons. First, they determine the role of the disc as a stress-distributing and load-absorbing structure (Nickel and McLachlan, 1994; Beek et al., 2001a). Therefore, the properties of the disc will also influence the stresses and strains that occur in the cartilage layers on the bone surfaces. These stresses and strains are of critical importance for adaptation and wear. For example, mechanical stress affects the proteoglycan synthesis in the disc (Carvalho et al., 1995), resulting in an adaptation of stiffness. Second, precise information on the biomechanical properties of the disc is required to develop suitable joint simulation models, with which the distribution of stress and strain in the structures of the joint can be estimated. In the last decade, several three-dimensional finite element models of the joint have been developed (Korioth et al., 1992; Tanaka et al., 1994, 2001c; Nagahara et al., 1999; Beek et al., 2000). However, thus far, the available models do not include all relevant properties, such as the shock-absorbing capabilities of the disc. Finally, information on the biomechanical properties of the disc is indispensable for the development of replacement materials for TMJ prostheses. In this paper, the fundamental concepts of the biomechanical behavior of the TMJ disc are reviewed. The review is divided into four parts. The first part introduces some basic definitions and the general physical properties of soft tissues, to facil14(2):138-150 (2003)
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itate comprehension of the later parts, in which the biomechanical behavior of the TMJ disc is discussed. Part 2 relates this behavior to the composition and organization of the disc, such as its collagen fiber and proteoglycan contents. In part 3, the biomechanical properties of the disc, including elastic modulus and viscoelasticity, are summarized. Finally, in part 4, adaptive changes of the disc in relation to its biomechanics are discussed.
(I) Nature of Loading Applied to the TMJ Disc (A) ELASTICITY UNDER VARIOUS LOADINGS
The disc is subject to a multitude of different loading regimens during mandibular movements. Basically, three types of loading can be distinguished: compression, tension, and shear (Fig. 1). Obviously, during natural loading of the joint, combinations of these basic types of the disc loading do occur. During compressive loading, the disc becomes shorter in the loading direction; during tensile loading, it is stretched in the loading direction; and during shear loading, one boundary surface of the disc moves parallel to an adjacent surface. During every type of loading, the disc undergoes a deformation, while internal forces are produced within the tissue. The amount of deformation is quantified by the amount of strain, which is defined as the change in length per unit of original length. The internal forces are quantified by the amount of stress, which is defined as force per unit area in Pa (1 Pa = 1 N/m2). The relationship between stress and strain of an elastic material can be described by a stress-strain curve (Fig. 2). The curve has both elastic and plastic deformation regions. If the structure is not loaded beyond the elastic region, it will return to its original shape once the load is released. If the structure is loaded up to its plastic region, it will not return to its original shape when the load is released. After plastic deformation, the stress will cause permanent damage of the tissue. In the elastic region, a toe region and a transition zone can be distinguished (Fung, 1981; Li et al., 1983), which are more or less arbitrarily divided by the so-called critical point (Tanne et al., 1991; Tanaka et al., 2000). The toe region can be considered as the physiologic range of stress and strain in which the tissue normally functions (Fung, 1981). Beyond the toe region, in the transition zone, the tissue usually will have a large reserve of strength before it ruptures and fails. The physiologic range can be very different for various connective tissues (mesentery, 100-200%; skin, 40%; tendon, 2-5%; Fung, 1981). The physiologic range of the disc is reported to be approximately 4% (canine, tensile strain; Teng et al., 1991). Another important feature is the strength of a tissue. The yield strength is defined as the stress at the yield point, beyond which deformation causes tissue damage. This point separates the elastic strain region and the plastic region of the stress-strain curve. The ultimate strength is the stress that the tissue can maximally sustain; the breaking strength is the stress at which the tissue will break. The value of the ultimate strength of the disc depends on the direction of the applied stress and the region where it is applied. For example, the ultimate strength of the intermediate zone of the disc is 37.4 MPa (1 MPa = 106 N/m2) when a tensile stress is applied antero-posteriorly, while it is 1.6 MPa when the stress application is medio-lateral (porcine disc; Beatty et al., 2001); the ultimate strength is significantly larger in the anterior and posterior regions of the disc (46.7 MPa and 69.7 MPa) than in its central region (14.7 MPa) (canine disc; Teng et al., 1991). For evaluation of the basic biomechanical characteristic of
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Figure 1. Diagram showing the different types of strain for three directions of loading. During compressive loading, the disc becomes shorter in the loading direction; during tensile loading, it is stretched in the loading direction; and during shear loading, one boundary surface of the disc moves parallel to an adjacent surface.
Figure 2. Typical stress-strain curve for connective tissue. The elastic and plastic regions of the curve are divided by the yield point, beyond which deformation causes tissue failure; the elastic region is further divided into a toe region and a transition zone.
a tissue, the elastic modulus or Young's modulus E is commonly calculated. This modulus is defined as the slope of the elastic region (almost linear part) of the stress-strain curve. The tensile and compressive moduli are a measure of the ability of the tissue to resist deformation in the direction of the applied load. These are defined as E = / , where is the stress and is the strain. The shear modulus G is a measure of the ability of the tissue to resist shear stress in a particular plane. It is defined as G = / , where is the shear stress and is the shear strain. Here, the shear strain is the displacement in the direction of the applied force per original thickness (Fig. 1). In general, the shear modulus tends to be 1/3 to 1/2 of the value of the tensile or
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result of fluid flow through and out of the disc. Immediately after loading occurs, the small permeability of the collagen network impedes instantaneous fluid flow through the collagen network. With time, the load causes the fluid to be driven away from the loaded site, through pores in the collagen network (Scapino et al., 1996). This fluid flow also explains another feature of viscoelasticity, i.e., that the biomechanical behavior of the tissue is dependent on the strain rate and on the time after stress application. For instance, when the strain and stress are applied rapidly, the slope of the stress-strain curve will be steeper than when they are applied slowly.
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features (Fung, 1969). Kelvin's model is a combination of Maxwell's and Voigt's model and has been applied to characterize both creep and stress-relaxation behavior (Fung, 1969). The relationship between stress and strain at a particular time is formulated as + = ER( + ) where and are time constants, and ER is the relaxed modulus after stressrelaxation; the time constant is a measure of the relaxation time. These parameters are commonly used in studies describing the viscoelastic properties of the disc.
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straighten the crimp, and that accounts for the initial toe region of the curve (Stegenga et al., 1991; Berkovitz, 2000). Thus, the initial toe region reflects a high compliance and corresponds to the straightening of the crimping without any lengthening of the collagen fibers (Gathercole and Keller, 1991). Beyond this initial phase, the collagen fibers begin to extend and become load-bearing. Furthermore, the small permeability of the collagen network impedes interstitial fluid flow through this network (Mow et al., 1984, 1993). Therefore, the loads acting on a cartilaginous structure as the disc are initially transmitted by a pressurization of the incompressible fluid without much deformation of the collagen network (Soltz and Ateshian, 1998). Nonetheless, fluid flow through the collagen network leads to a gradual transfer of the load from the fluid to the collagen fibers. When further loaded, the collagen network deforms, and water is squeezed out of the disc while the orientation of the collagen fibers is re-arranged (Mow et al., 1986; Woo, 1986). The movement of fluid out of the disc and the re-arrangement of the collagen fibers Figure 6. Schematic illustration of the disc (antero-lateral view) with various orientations are reversible when the disc is not deformed of collagen fibers. beyond the physiologic strain range. Even application of significant long-term stresses beyond the physiologic strain range introduces E* = E + iE but minor changes in fiber waviness and alignment within the disc (Scapino et al., 1996). This enables the disc to adapt its shape where E = E* cos , E = E* sin , i = - 1, and tan = E /E is continuously to fit in the space between the opposing articular the loss tangent. E describes the elastic deformation under stress surfaces and to distribute loads suitably in the TMJ. Collagen and is directly proportional to the energy storage in a cycle of gives the disc much of its tensile stiffness and strength. deformation. E denotes the viscous deformation and is proporThe thin surface layers of the disc have an architecture different tional to the average dissipation or loss of energy as heat in a from that of the thick inner layer (Fig. 6). In the superior and infericycle of deformation. In addition, the tangent of the phase angle or surface layers, the collagen fibers are more or less perpendicular( ) between stress and strain, i.e., the loss tangent (tan ), is a mealy arranged in an antero-posterior and medio-lateral direction sure of the ratio of energy loss to energy stored during cyclic (Minarelli et al., 1997). In the inner layer, the orientation of collagen deformation. For a tissue with a high value of the loss tangent, fibers varies markedly in different regions of the disc. The fibers run the viscous behavior is stronger than the elastic behavior. In such primarily antero-posteriorly in the intermediate zone and medioa tissue, the energy used for its deformation is dissipated as heat laterally in the anterior and posterior bands. The antero-posterior and causes changes in the inner structure by movement of fluid. fibers from the intermediate zone are interlaced with the medio-lateral fibers in both bands (Teng and Xu, 1991). In the central region (II) Biomechanical Properties of the Disc of the bands, the fibers from the intermediate zone flare superiorly Related to its Composition and Organization and inferiorly and turn medially and laterally, merging structurally The disc is composed of variable amounts of cells and an extrawith those of the bands (Mills et al., 1994; Scapino et al., 1996). In the cellular matrix. The matrix consists of macromolecules and fluid. medial and lateral regions of the disc, near the condylar poles, the The macromolecules constitute about 15-35% of the wet weight of antero-posterior fibers of the intermediate zone are attached tightly the disc, while the tissue fluid constitutes about 65-85%. These to the poles of the condyle (Teng and Xu, 1991). As a result of these macromolecules consist mainly of collagen (85-90%) and proteodifferences in collagen fiber orientation, regional differences and glycans (10-15%) (Nakano and Scott, 1989a; Sindelar et al., 2000). anisotropy in the mechanical properties of the disc can be expected. The mechanical properties of the disc are largely dependent on its (B) PROTEOGLYCANS collagen fiber and proteoglycan composition and organization Proteoglycans consist of a core protein to which glycosaminoglyand on their interaction with the tissue fluid. can (GAG) sulfate side-chains are attached (Iozzo, 1998). In the (A) COLLAGEN disc, there are several proteoglycans. Biglycan and decorin belong The collagen fibers maintain the shape of the disc, while elastin to the group of small proteoglycans, consisting of a core protein of restores shape during unloading (Scapino et al., 1996). Collagen approximately 38 kDa to which either one (decorin) or two (biglyfibers commonly exhibit waviness ("crimping"). The functional can) chondroitin/dermatan sulfate side-chains are attached significance of this crimping can be seen in the stress-strain curve (Chopra et al., 1985; Fisher et al., 1989). Aggrecan is a large proteo(Fig. 2). When a tension is applied to the disc, the first effect is to glycan containing both chondroitin sulfate and keratan sulfate
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(Nakano and Scott, 1989b). Sulfated GAGs such as chondroitin sulfate, dermatan sulfate, and keratan sulfate are synthesized as proteoglycan in the Golgi apparatus. Hyaluronic acid, another GAG, is not attached to a core protein and is synthesized as a free GAG molecule in the cell membrane (Iozzo, 1998). Proteoglycans are enmeshed in the network of collagen fibers and are virtually immobile. Proteoglycan molecules possess a high viscosity and a large molecular size that reduce their capacity to diffuse through the collagen network, thus resulting in the retention of large amounts of water (Muir, 1973). The result is a stiff viscoelastic material surrounding the collagen fibers. Because of their molecular structure, proteoglycans are ideally suited to resist compressive loadings. Proteoglycans can indirectly modulate the stiffness of the collagen network, since an increase in proteoglycan concentration leads to an increase in the osmotic pressure, which in turn affects the synthesis of collagen (Muir, 1981). In the disc, the large proteoglycans and the related chondroitin sulfate are preferentially localized in the central area of the intermediate zone and in the anterior and posterior bands (Mills et al., 1988; Nakano et al., 1993; Nakano and Scott, 1996; Mizoguchi et al., 1998). It has therefore been suggested that these parts of the disc encounter heavy compressive loading during function and may be responsible for maintaining the resilience of the disc (Nakano and Scott, 1996). The small proteoglycans, decorin and biglycan, are mainly found in the lateral and medial parts of the intermediate zone and are present in lesser amounts in the central part of the intermediate zone and in the anterior and posterior bands (Scott et al., 1995; Mizoguchi et al., 1998). The expression of decorin mRNA in tendon is promoted by tensile stress (Robbins and Vogel, 1994). Consequently, the distribution of decorin may reflect the distribution of tensile stress in the disc. Decorin can also interact with type I collagen and cause small increases in fibrillar diameter (Scott et al., 1995). This is in line with the observation that the collagen fibrils in the decorin-rich peripheral region of the disc are the thickest (Kuc and Scott, 1994). These biochemical findings for the proteoglycan concentration in different areas of the disc are consistent with results obtained from mechanical tests (see Part III).
the results of the various studies cannot be easily compared. Differences in experimental techniques include the size, hydration fluid and holding of the specimens, and different testing machines and protocols. Due to this variation, the reported moduli show a large range (from 1 to 100 MPa). Most information has been obtained from human and from porcine and bovine discs, because of their structural and functional similarity to the human disc. Structurally, the bovine and porcine TMJ have a more or less similar shape, and their mandibular halves are rigidly fixed, as in the human (Bermejo et al., 1987, 1993; Gonzlez et al., 1991). Functionally, the bovine and porcine TMJ exhibit lateral translatory movements (Berg, 1978; Hatton and Swann, 1986). The masticatory pattern of pigs is different from that in humans and cattle (Langenbach and Van Eijden, 2001). Pigs chew faster than humans and cattle, but the pattern of pig chewing is probably more similar to that of the human than to that of cattle; cattle have much greater excursions than humans. In addition to these species, information has been obtained from canine discs. However, functionally, the dog exhibits mainly chopping strokes during mastication. Another problem when the results of various studies are compared is that different tests (for example, compression and tension) have not been performed on the same specimen. Also, as mentioned before, the relationship between stress and strain for the disc is non-linear and time-dependent. For example, the tensile modulus of the porcine disc is about 27 MPa at a strain rate of 0.5 mm/sec, whereas it is about 83 MPa at a rate of 500 mm/sec (Beatty et al., 2001). Thus, when data on elastic moduli are evaluated, consideration should also be given to the strain rate, the magnitude of the applied strain, and the measuring time. In addition, because of structural differences within the disc, the location of the loading and its direction and type (tension, compression, shear) are major factors for determining its elastic properties.
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TABLE
Centa
Meda
Region
Anta
Posta
Nsa
Dog Dog Human Pig Cow Human Pig Human Dog Cow Human
50.2b 43.3b 101.1c 91.9c 18.4e 44.0d (29.9)de 95.7f (61.2)fe 1.2-3.2g 27.3-76.4h 21.7-24.0 20.2-22.9 24.0-25.9
30.0e
30.1e
15.5 (1.4)e
b c
Lateral (Lat), central (Cent), and medial (Med) regions of intermediate zone, anterior (Ant) and posterior (Post) bands, region not specified (Ns). Stress range, 0-1.5 MPa. Stress range, 1.5-4.0 MPa.
the tensile modulus ranged between about 22 and 26 MPa, and the compressive modulus between 14 and 17 MPa. The possible explanation for the larger tensile modulus is that the elasticity of the disc is more dependent on the collagen fibers than on the proteoglycans. During tension, the stiffness is primarily due to the resistance produced by the collagen fibers. During compression, the collagen fibers are probably slack, which makes them less effective in resisting compressive stress.
humans, which may be associated with a shift of the loading to the lateral side of the intermediate zone (Beek et al., 2000).
Investigation of shear properties in synovial joints is of particular interest, because shear stress can result in fatigue, damage, and deformation of cartilage (Spirt et al., 1989; Zhu et al., 1993, 1994). Therefore, data on the shear modulus might contribute to a better understanding of secondary tissue damage. It is very likely that shear stresses occur during loading of the disc, because the articular surfaces that compress the disc are not parallel. As a result, not all areas of the disc are deformed in the same direction, leading to local shear. Another reason why shear stress occurs in the disc is its non-homogeneous structure. Its inner layer consists mainly of antero-posterior running collagen fibers and the "leaflet-like" proteoglycans (Kuc and Scott, 1994; Nakano and Scott, 1996), whereas the superior and inferior surface layers consist mainly of anteroposteriorly and medio-laterally running collagen fibers and small proteoglycans (Nakano and Scott, 1996; Minarelli et al., 1997). Therefore, these layers are considered to have different biomechanical properties (Nakano and Scott, 1996; Mizoguchi et al., 1998), which might lead to shear stress. This is supported by the results of a finite element study, in which a relatively large shear stress was predicted in a disc consisting of three layers (Tanaka et al., 1994). With respect to the shear modulus of the disc, thus far, only one study has been published, in which the shear modulus of the intermediate zone of the human disc (strain rate, 0.02 mm/sec) was evaluated (Lai et al., 1998). It appeared that in the central region the shear modulus (about 1.0 MPa) was lower than in the lateral and medial regions (about 1.75 MPa). It has been reported that the shear stress in cartilage is very sensitive to the frequency and direction of the loading and to the amount of compressive strain (Mow et al., 1992). Therefore, the shear behavior
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of the disc should also be considered as a nonlinear, anisotropic, and time-dependent behavior. Future studies need to examine the effects of dynamic shear properties on the disc.
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generate catabolic effects (Burger et al., 1992). Therefore, information on creep time may help to assess the possible effects of permanent changes of the disc as a result of prolonged stress.
Figure 9. Measurement signals of a cyclic test with a constant frequency. Data from Beek et al. (2001a). (A) Stress vs. time. (B) Strain vs. time. (C) Stress vs. strain.
indicate that fluid flow within and out of the disc is slower during compression than during tension. Creep time appears not to be dependent on loading region (central, lateral, and medial regions of the intermediate zone; Tanaka et al., 2001a) or stress level (10 N, 20 N, and 30 N; Kuboki et al., 1997; 1.0 MPa and 1.5 MPa; Tanaka et al., 2001a). During tension, the initial response to the load is due to stretching of the collagen crimping within the toe region, and the secondary response is due to the elongation of the collagen network and the squeezing of fluid against internal stress. Fluid flow through the network is nonetheless possible, which leads to a gradual transfer of the load from the fluid to the collagen network. This finding also indicates that stress distribution occurs in the disc. Changes in the shape of the disc reduce the amount of stress concentration and probably decrease the progression of injury (Tanaka et al., 2001a). The restoration curves (Fig. 8) exhibit a marked decrease in strain during the first 5 sec, and the decrease in strain ceases after a few minutes. This feature indicates that some of the energy used to deform the disc is not released immediately after unloading occurs, and that the return of fluid from outside the disc and the recovery to its original shape are relatively slow (Beek et al., 2001a). The residual strain after creep could be an important factor for the capability for recovery and the prediction of permanent deformation in the disc. The residual strain after 20 min of creep is less than 1%, which is almost similar among the central, lateral, and medial regions of the intermediate zone (Tanaka et al., 2002a). This implies that the disc has a great capability of recovery after sustained stress. The creep time of 20 min is long when compared with in vivo loading conditions, such as sustained clenching. However, sustained stress with high magnitude is considered to
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zone shows a great capacity of energy dissipation, especially during dynamic loading such as mastication and chewing. When one compares the results of tests with a relatively large strain (30%; Beek et al., 2001a) with those of tests with a small strain (0.5%; Tanaka et al., 2002b), all dynamic moduli become larger when a larger strain is applied. Presumably, this difference is due to differences in fluid flow. The small permeability of the collagen network (pore size of 10-60; Mow et al., 1984, 1993) impedes the fluid flow through the collagen network. Under small strains, the hydrostatic pressure in the interstitial fluid due to the hydrophilic character of the proteoglycans is in balance with the applied force (Tanaka et al., 2002b). Therefore, the load acting on the disc can be assumed to be carried by pressurization of fluid without much deformation of the collagen network (Soltz and Ateshian, 1998). This mechanism protects the collagen network against extreme local deformations during loading. Under relatively high strain, fluid flow through the collagen network is nonetheless possible, which may lead to a gradual transfer of the load from the fluid to the collagen network (Beek et al., 2001a). When loaded, the collagen network deforms. This enables the disc to adapt its shape continuously to fit the space between the opposing articular surfaces. However, the return of the fluid squeezed out of the disc under loading is relatively slow, as mentioned above. As a result, the disc cannot keep sufficient fluid in itself during cyclic loading, resulting in a higher stiffness than that under small strain. The values of dynamic viscoelastic E-moduli ( E* , E , and E ) also increase as the frequency increased from 0.1 to 100 Hz (Tanaka et al., 2002b). In dynamic tensile tests, the dynamic viscoelastic E-moduli are about 2 times larger at 100 Hz than those at 1 Hz (Tanaka et al., 2002b). This non-linear dependency on the frequency is due to fluid flow and squeezing within the matrix of the disc. At higher frequencies, the proteoglycans occupying the interfibrilar spaces interfere with smooth fluid flow, which leads to strain energy dissipation, resulting in a higher stiffness.
(A) AGE
Age-related changes in viscoelasticity have been extensively studied in connective tissues, such as skin and tendon (Walker et al., 1976; Vogel, 1980; Woo, 1986). The tensile modulus of the rat skin increases with maturation and decreases with senescence (Vogel, 1980). In canine tendon, an increased stiffness and reduced viscoelasticity were found during aging (Walker et al., 1976). Age-related changes have also been demonstrated in the disc. The calcium content of the human disc increases progressively with aging (Takano et al., 1999). The increase in calcification may be caused by an intrinsic aging process or by an altered mechanical stress (Jibiki et al., 1999). With respect to the GAG composition in the disc, the amounts of total and sulfated GAGs markedly increase from mature fetuses to mature adults (Nakano and Scott, 1996). An increase in the content of sulfated GAGs relative to the tissue fluid will elevate the osmotic swelling pressure and, hence, the compressive stiffness of the disc. Accordingly, the material properties of the disc can also be expected to be related to age. Lai et al. (1998) were the first who demonstrated that the shear modulus of the human disc increases with age and suggested that the increase of this modulus may be the result of a decrease of collagen-remodeling capacity. The elastic modulus of normal human discs has a constant value of about 45 MPa up to 50 years of age, but increases thereafter to about 65 MPa (Tanaka et al., 2001b). The elastic moduli of bovine discs increase slightly but significantly from those of the young adult (about 22 MPa) to those of the mature adult (about 25 MPa; Tanaka et al., 2001b). The ratio of collagen to water in the disc increases with age, while the water content remains constant (Nakano and Scott, 1996). Young discs contain relatively more fluid and are capable of releasing much more fluid out of the disc, resulting in a smaller elasticity. In contrast, mature discs consist of relatively abundant collagen fibers, and may exhibit less water loss after relaxation.
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and Watzke, 1991; ProplastHeffez et al., 1987; Florine et al., 1988; Valentine et al., 1989; Wagner and Mosby, 1990). The major reason for these failures is that these biomaterials were not strong enough to withstand the functional loading applied to them.
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