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Dynamic Properties of Bovine Temporomandibular Joint Disks Change with Age
Department of Orthodontics, Hiroshima University Faculty of Dentistry, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8553, Japan; Correspondence: * corresponding author, etanaka{at}hiroshima-u.ac.jp
The temporomandibular joint disk exhibits morphological and biochemical age-related changes. However, the possible age-related changes of the dynamic viscoelasticity in the disk are unclear. We tested the hypothesis that the dynamic viscoelastic properties of the disk change with age. Thirty-six disks from young-adult, adult, and mature-adult cattle were used for dynamic tensile tests. In all disks, the magnitudes of the complex modulus, the storage modulus, and the loss modulus increased as the frequency increased. The mature-adult disks had higher values of these moduli than did the younger disks. The loss tangent ranged from 0.1 to 0.3, which means that the disk has relatively large elasticity and relatively small viscosity. It was concluded that both the elasticity and viscosity of the disk increase with age. This may reflect age-related changes in biochemical composition.
Key Words: temporomandibular joint disk • dynamic viscoelasticity • aging
The disk of the temporomandibular joint (TMJ), located between the temporal bone and the mandibular condyle, plays an important role as a stress absorber during function (Osborn, 1985; Tanne et al., 1991; Chin et al., 1996; Scapino et al., 1996; Kuboki et al., 1997; Tanaka et al., 1999). The TMJ disk consists mainly of type I collagen fibers and proteoglycans which are constrained in the interstices of the collagen fiber mesh (Scapino et al., 1996). Because of the composition and organization of its collagen fibers and glycosaminoglycans (GAGs), the TMJ disk exhibits viscoelastic characteristics (Nickel and McLachlan, 1994; Scapino et al., 1996; Kuboki et al., 1997; Tanaka et al., 1999). Studies of biomechanical responses to various loadings have provided useful information on the mechanical properties of various tissues and on their changes due to diseases or injuries (Oloyede et al., 1992; Iatridis et al., 1996; Ker et al., 2000; Tanaka et al., 2000). Concerning the TMJ disk, several tests—tensile, compressive, creep, and stress relaxation—have provided valuable information on the viscoelastic properties, residual strain, and strain energy dissipation associated with time (Teng et al., 1991; Scapino et al., 1996; Kuboki et al., 1997; Tanaka et al., 1999, 2002). These methods, however, are not sufficient for a rigorous evaluation of the rheological characteristics of the TMJ disk under a cyclic application of stress reflecting masticatory function (Beek et al., 2001). The automatic dynamic viscoelastometer, which is based on a principle of non-resonance-forced vibration, is a suitable instrument for evaluation of the viscoelastic properties of various materials (Clarke, 1989; Murata et al., 2000). The disk undergoes biochemical and morphological changes throughout life. These changes may be caused by changes of the loading condition in the TMJ. The calcium content of the disk increases progressively with aging (Takano et al., 1999); it has been suggested that the increase in calcifications is caused by aging or mechanical stress (Jibiki et al., 1999). Nakano and Scott (1996), using bovine TMJ disks, investigated the age-related changes in chemical composition and reported marked increases in total and sulfated GAGs in the inner tissues from mature fetuses to mature adults. Therefore, an age-related change in the viscoelastic properties can be expected. It is still unclear, however, whether the dynamic viscoelastic properties of the disk change with age. Such information may shed light on the age-related changes of the response of the TMJ disk to the applied mechanical stresses. In this in vitro study, we investigated the dynamic viscoelastic properties of the bovine TMJ disk over a wide range of frequencies. The aim was to evaluate the age-related effect on the biomechanical responses of TMJ disks, using a dynamic viscoelastometer.
Description of the Sample Thirty-six bovine TMJ disks from 12 young-adult (3 yrs old), 12 adult (7 yrs old), and 12 mature-adult cattle (more than 10 yrs old) were obtained at a local abattoir (Japan Agriculture, Hiroshima, Japan). The ages of the animals were estimated from the numbers of permanent anterior teeth. The protocol of the experiment was approved by the animal care and use committee at Hiroshima University. The disks were carefully dissected soon after the animals’ death. All disks were visually normal, oval, and had thicknesses and sizes within standard range (Meister and Berg, 1972). Immediately after resection, the disks were placed in 0.9% NaCl solution and stored at 4°C; tensile tests were conducted within 8 hrs after resection. Each disk was sectioned antero-posteriorly, and a test specimen was derived from the central region (Fig. 1  ). To be able to determine the amount of applied stress (see below) for each specimen, we calculated the cross-sectional area by multiplying its thickness and its mediolateral width. Width and thickness were measured by means of digimatic calipers (CD-S20C, Mitutoyo Co., Kawasaki, Japan) and were 2.1 ± 0.3 mm (mean ± SD) and 10.0 ± 1.0 mm in the young-adult, 1.8 ± 0.2 mm and 9.1 ± 0.9 mm in the adult, and 1.8 ± 0.1 mm and 9.6 ± 0.3 mm in the mature-adult groups; cross-sectional areas were 21.3 ± 4.0, 16.3 ± 2.5, and 17.3 ± 1.1 mm2 (mean ± SD) in the young-adult, adult, and mature-adult groups, respectively. The amount of antero-posterior length of the specimens was approximately 14 mm, including the length (about 4 mm) for gripping of the specimen in the dynamic viscoelastometer (see below).
Testing Apparatus and Conditions The dynamic viscoelastic properties of the specimens were determined with the use of an automatic dynamic viscoelastometer (Rheovibron DDV-25FP, Orientec Corp., Tokyo, Japan) (Fig. 1  ). This device consists of a measurement operation block, a main unit, a power unit, a data-processing device, and testing jigs. The measurement operation block consists of a magnetic exciter, a tension control motor, an amplitude-detecting sensor and an amplifier, a load-detecting load cell, and chucks. The specimen was rigidly clamped in the two chucks; the chuck-to-chuck distance was 10 mm.
All experiments were performed in a bath with 0.9% NaCl solution at room temperature. During the test, a dynamic tension was applied to the specimen along an antero-posterior axis by a sinusoidal strain of
Dynamic Viscoelastic Parameters The magnitude of complex modulus |E*| was determined by
|E*| =
Based on the phase angle E* = E' + iE''
E' = |E*| cos
E'' = |E*| sin
where i =
The dependence of the dynamic viscoelasticity on age was statistically evaluated by use of the results at 1.0 Hz. This frequency reflects masticatory conditions (Druzinsky, 1993; Gallo et al., 2000). We performed Student’s t tests to test for the differences among mean values of E'', E', and tan
In all age groups, the values of |E*|, E', and E'' increased as the frequency increased from 0.1 to 100 Hz (Fig. 2 ). Note that the specimens from the young-adult group showed a relatively small change with frequency. The mature-adult group had higher values of |E*|, E', and E'' than did the younger groups, regardless of frequency.
In all groups, the loss tangent exhibited relatively small changes between 0.1 and 1 Hz; it increased with frequencies beyond 1 Hz (Fig. 3 ). Throughout the entire range of frequencies tested, the mature-adult group had a larger loss tangent than did the younger groups. The young-adult and adult groups showed almost the same loss tangent, regardless of frequency. The tan ranged from 0.1 to 0.3, which means that the TMJ disk has a relatively large elasticity and a relatively small, but not negligible, viscosity.
The storage modulus E', loss modulus E'', and loss tangent tan at 1.0 Hz differed among the groups (Fig. 4). The storage modulus E' was 0.69 ± 0.21 MPa (mean ± SD) in the young-adult group, 1.21 ± 0.41 MPa in the adult group, and 1.44 ± 0.31 MPa in the mature-adult group; the storage modulus of the young-adult group was significantly smaller than that of the older groups (p < 0.01). In the mature-adult group, the loss modulus E'' was 0.23 ± 0.06 MPa, which was significantly larger than E'' in the younger groups (p < 0.01). With respect to the loss tangent tan, the mature-adult group had the highest value (0.16 ± 0.03); this value was significantly larger than that in the adult group (p < 0.01). The value of tan in the adult group was almost the same as that in the young-adult group.
The TMJ disk is subjected to intermittent loading during mastication and to sustained loading during clenching. In response to dynamic force conditions, the disk behaves in a viscoelastic fashion, which is different from its behavior during static conditions. It was found that the dynamic viscoelastic behavior of the bovine TMJ disks is sensitive to changes in frequency regardless of age. All of the dynamic viscoelastic parameters became larger with an increase of frequency. This implies that, at higher frequencies, a larger load is required to produce the same strain. Thus, at higher frequencies, the disk is better able to resist higher loads than at lower frequencies. This property may come from the wavy structure of the collagen fibers comprising the TMJ disk under unstrained condition. Collagen crimping in the human TMJ disk is observed at ages ranging from 4.5 to 63 yrs (Berkovitz, 2000). It should be realized that, in the current experiment, more than 10 cycles were applied for each frequency and that the measured moduli were based on a steady-state response. Under cyclic loading, a steady-state response of the disk, as in other viscoelastic tissues, is usually reached within 10 cycles (see also Beek et al., 2001). Therefore, it is not likely that the increase in the moduli with frequency observed in the present study is due to a time-dependent effect. To rule out such an effect, we carried out experiments (for each age group, n = 5) in which the moduli were also measured at several selected constant frequencies (1, 10, and 100 Hz) with increasing cycles (data not shown). Except for the above-mentioned initial response to reach a steady state, there was no effect of cycle number, and the steady-state moduli at these constant frequencies did not differ significantly from those obtained with the regular experimental protocol. In the present study, the total strain was 0.5%. Within this range of strain, the predominant increase in the resultant stress with an increase of frequency may be related to the movement of water rather than to the resilience of the collagenous portion of the matrix. Below a certain level of frequency, the morphological change of the TMJ disk may match up to the water movement within the tissue. At higher strain rates (higher frequency), the frictional resistance due to interstitial fluid flow relative to the solid matrix (collagen matrix) may increase, resulting in a higher stiffness; the dissipation due to interstitial fluid flow may also increase, resulting in a larger hysteresis loop with an increase of frequency. In the present study, the storage modulus E' of the disk was less than 2.5 MPa, regardless of frequency and age, which is smaller than the elastic moduli previously measured under static conditions (Tanne et al., 1991; Teng et al., 1991; Tanaka et al., 1999). In general, the dynamic properties are determined in cycle tests at low strain levels, as was the case in the study. Furthermore, it is known that the curves showing the experimental peak-and-valley stresses in cyclic testing match well with those obtained from the theoretical stress-relaxation curves according to the quasi-linear viscoelastic theory (Woo, 1986). Recently, we investigated the stress relaxation property of bovine TMJ disks in compression and found that the relaxed modulus ranged from 1.1 to 2.3 MPa (del Pozo et al., 2002). The values of the relaxed modulus have some resemblance to the dynamic viscoelastic parameters in the present study. This finding implies that, under dynamic conditions, the disk exhibits a biomechanical equilibrium which is similar to that after stress-relaxation.
In this study, we examined a wide range of frequencies. This range is relatively large compared with the upper limit of the chewing frequency in the cow (Druzinsky, 1993). It should be realized, however, that, during mastication, impulse loadings may occur which include high-frequency components. Within the wide frequency range examined in the present study, values of 0.5 to 1.0 Hz reflect masticatory conditions (Druzinsky, 1993; Gallo et al., 2000). These values are considered to be important for assessment of the clinical significance of the results. Therefore, in this study, the dependence of dynamic viscoelasticity on aging was evaluated by use of the results at 1.0 Hz. At this frequency, the mature-adult group had significantly higher values than the young-adult group in storage modulus E', loss modulus E'', and loss tangent tan The present finding that the values of the viscoelastic parameters of the bovine TMJ disk increase with age is consistent with the findings of previous biochemical studies (Nakano and Scott, 1996; Nishimura et al., 1998). The increase in loss tangent implies an increase of viscosity relative to elasticity. Functionally, the damping, which results from a higher value of loss tangent, is likely to produce a degree of stress relief under masticatory forces. Therefore, the mature-adult disk may have a greater capacity for stress distribution and thus may reduce stress concentration at the surfaces of the articulating bones.
This research was supported in part by a grant (No. 12771280) for Science Research from the Ministry of Education, Science and Culture, Japan. Received for publication September 7, 2001. Revision received June 14, 2002. Accepted for publication July 8, 2002.
Journal of Dental Research, Vol. 81, No. 9,
618-622 (2002) This article has been cited by other articles:
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ABSTRACT
INTRODUCTION
/2 > 
= 
), with an administrative strain of 
= 
1 and tan
Complex modulus |E*|; x Storage modulus E'; and • Loss modulus E''.
Adult, and • Mature-adult groups.
