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RESEARCH REPORT |
1 Division of Oral and Maxillofacial Surgery, University of Texas Southwestern, Dallas, TX; and
2 Department of Biomedical Sciences, Baylor College of Dentistry, Texas A&M University System Health Science Center, 3302 Gaston Ave., Dallas, TX 75246, USA;
* corresponding author, pdechow{at}tambcd.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: ultrasound • cortical bone • biomechanics • function
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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In general, material properties and their variation, which are important indicators of bone quality, have not received much systematic analysis in individual bone organs. A recent study (Schwartz-Dabney and Dechow, in press) demonstrates significant regional material property variation in human dentate mandibles, some of which is associated with function. Although geometry changes are reported following edentulation, nothing is known about changes in other material properties, such as elastic and shear moduli. The two previous studies that measured material properties in both dentate and edentulous mandibles had sample sizes insufficient for statistical evaluation (Carter, 1989; Arendts and Sigolotto, 1990). Some information is available for bone density, but these data are largely derived from radiographs and other scans that do not allow density to be calculated as a true volumetric measurement.
Our aim was to examine regional material property differences of edentulous mandibular cortical bone and to compare these with known properties of dentate mandibles. We hypothesized that edentulous mandibles, like dentate mandibles, differ regionally.
Regarding the potential differences between dentate and edentulous mandibles in material properties, our null hypothesis was that there were no differences. An alternate hypothesis was difficult to formulate, given the lack of information in the literature on differences in material properties resulting from bone adaptation. In experimental studies of post-cranial bone, it is widely recognized that loss of or reduction in function may lead to loss of bone mass (for review, see Martin et al., 1998). However, little is known about changes in elastic properties, especially if their three-dimensional characteristics are considered. Likewise, most studies of density are radiographic and fail to separate differences due to apparent bone density from those due to thickness. Nevertheless, the important issue of bone quality in the edentulous mandible, especially given the increasingly widespread use of implants for dental restoration, led us to test whether edentulation results not only in alveolar bone loss, but also in changes in the material properties of the remaining basal bone.
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MATERIALS & METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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All mandibles had intact alveolar ridges with no evidence of open or healing sockets. Residual ridge height was significantly reduced in all mandibles, averaging between 14 and 15 mm along the corpus. Age at death ranged from 58 to 88 yrs and was not significantly different between three males (69.7 yrs, SD = 10.4) and seven females (72.1 yrs, SD = 12.6). Mandibles (1) were from Caucasian donors, (2) did not have a documented history of bone disease, and (3) possessed an indication of denture use by the presence of dentures with most cadaver remains. Craniometric dimensions of the mandibles are given in the Appendix, Table 1 (www.dentalresearch.org).
All bone preparation was carried out under a hood, with a sterile technique and continuous water drip for coolant. Specimens from 22 sites were harvested on both facial and lingual cortices (Fig. 1
). (Numbering is not sequential, to maintain labeling consistent with that in our dentate study [Schwartz-Dabney and Dechow, in press].) Sites were marked with a graphite line parallel to the superior surface of the alveolar ridge in the molar region and with an arrowhead indicating the anterior. Bone cylinders were harvested by means of a slow-speed dental handpiece and trephine burs (inner diameter, 4.0 mm). Endosteal cancellous bone was removed with a miniature lathe equipped with grinding wheels until there was no visible porosity perpendicular to the endosteum. Samples were stored in equal proportions of 95% ethanol and isotonic saline, which maintained the elastic properties over time (Ashman et al., 1984; Zioupos et al., 2000).
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The principal axes of each specimen were identified by an ultrasonic technique (Schwartz-Dabney and Dechow, in press) with a Hewlett-Packard (Hewlett-Packard, Palo Alto, CA, USA) pulse generator, 2 mounted piezoelectric transducers (2.25 MHz longitudinal, Panametrics V323-SU, and 5.0 MHz shear, Panametrics V156-RM, Panametrics, Inc., Waltham, MA, USA), and an oscilloscope (Tektronix TDS-420, Tektronix, Inc., Beaverton, OR, USA). The arrowhead served as the origin for 9 measurements at rotations of 22.5°. The direction with the highest longitudinal velocity corresponded to the direction of maximum stiffness (D3), since ultrasonic velocity increases linearly with stiffness (Ashman et al., 1984; Kohles et al., 1997). The direction of minimum stiffness in the plane of the cortical plate (D2) corresponded to the slowest velocity and was 90° to the direction of maximum stiffness.
Material property testing used the pulse transmission technique (Ashman et al., 1984; Ashman and van Buskirk, 1987; Schwartz-Dabey and Dechow, in press). Both longitudinal and transverse ultrasonic waves were passed through the principal axes (D2 and D3) and the cortical thickness (D1) of each specimen. We measured time delays to make a phase comparison of the signals before and after transmission. We calculated ultrasonic velocities by dividing the thickness or diameter by the time delay. Elastic properties were calculated from ultrasonic velocities according to standard techniques (Ashman et al., 1984; Dechow et al., 1993; Kohles et al., 1997). Young’s elastic modulus (E) measures a structure’s ability to resist deformation along an axis, indicated by subscripts as in E1, E2, or E3. Shear modulus (G) measures a structure’s ability to resist angular shear stresses in a plane between 2 axes indicated by subscripts as in G12, G31, or G32.
Principal axes could be calculated for all specimens (N = 440). However, ultrasonic velocities in the D1 direction could not be obtained in 25 specimens, which were too thin (< 0.1 mm) for repeatable measurements to be obtained, and thus elastic properties could not be calculated. Half of these specimens came from 3 sites on the lingual ramus (#14, 15, 26). Differences between sides could not be tested at some sites (#27, 30) on the coronoid process, due to confluence of the cortical plates.
Analysis
Data from 10 dentate mandibles, previously described (Schwartz-Dabney and Dechow, in press), were used as a comparison with data from the edentulous group in relevant statistical tests. Average mandibular height (inferior border to alveolar crest) along the corpus averaged between 25 mm (symphysis) and 33 mm (molars) and was approximately double the residual ridge height in the edentulous sample (difference was significant at F = 45.6, p < 0.001). Analysis of variance indicated that the dentate sample was not significantly different in age, although mean values (males = 64.2, SD = 11.7; females = 62.0, SD = 17.1) and range (48-81) were slightly less. The proportion of males (seven) and females (three) was also different in the dentate sample, but tests of differences in material properties by gender for both groups did not show significant differences.
Minitab Software (Minitab Software, Pittsburgh, PA, USA) (release 13.3) was used for most statistical calculations. Data were checked for normality and hypotheses were tested with a balanced, unrestricted ANOVA with a repeated-measures design and mandible as the repeating factor. The repeated-measures design accounts for the lack of independence between multiple samples taken from a single mandible (Zar, 1996; Minitab User’s Guide 2, Release 13, pps. 3-31–3-33, Minitab, Inc., 2000). Statistical p-values were presented where differences existed between (1) sites, (2) facial and lingual cortices, or (3) dentate and edentulous mandibles.
Directions of maximum stiffness, because of their unique angular distribution, required circular statistics (Zar, 1996), which we calculated with Oriana for Windows Version 1 (Kovach Computing Services, Anglesey, Wales, UK). We used Raleigh’s uniformity test (Zar, 1996) to determine whether the means themselves were significant, meaning the distribution of orientations was different from a random collection of angles. If angular means were significant, we tested differences between them with a generalization of the Watson-Williams test adapted for circular distributions (Zar, 1996).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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and Appendix, Table 2 [www.dentalresearch.org]). Sites with the least variation were at the inferior corpus and posterior ramus on both cortices. Sites with the most variation were near the coronoid and condylar processes and sigmoid notch area. There were 5 paired edentulous sites with significant differences (p < 0.04) between facial and lingual sides (#3, 12, 25, 27, 31).
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Cortical Thickness
Cortical thickness in edentulous mandibles was not significantly different between facial and lingual sides, but was significantly different among sites within each cortex (p < 0.001). Cortical bone was thicker in the corpus than ramus (Fig. 3 and Appendix, Table 2 [www.dentalresearch.org]). Except for one anterior border site, the thickest ramus sites were along the posterior border.
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Density
Edentulous cortical density was not significantly different between facial and lingual sides, but was significantly different among sites within each cortex (p < 0.01) (Appendix, Table 2 [www.dentalresearch.org]). Lingual ramus sites and facial masseteric and condylar sites were the least dense. There were no significant differences between edentulous and dentate mandibles.
Elastic Moduli
Edentulous elastic moduli were not significantly different between facial and lingual sides, but were significantly different among sites on each cortex (p < 0.01) (Appendix, Table 3 [www.dentalresearch.org]) and between directions (E1, E2, and E3) (p < 0.001). The grand mean elastic moduli for edentulous mandibles were 12.5 GPa (SD = 2.3) for E1, 17.9 GPa (SD = 3.3) for E2, and 26.6 GPa (SD = 5.9) for E3.
E3 values in edentulous mandibles were, on average, significantly stiffer (p < 0.04) than in dentate mandibles (22.8 GPa, SD = 5.4). Only 6 sites, all in the ramus (facial #13, 14, 21 and lingual #16, 24, 27) (Fig. 4), were, on average, less stiff. Average dentate E1 values (12.7 GPa, SD = 1.8) and E2 values (17.9, SD = 2.5) were essentially identical to those of edentulous mandibles, and no significant differences were found.
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G12 values in edentulous mandibles were, on average, modestly but significantly less stiff (10%, p < 0.01) than in dentate mandibles (5.0 GPa, SD = 0.6). Only 2 sites (#1, 2) on the facial cortex were stiffer. Average dentate G23 values (7.4 GPa, SD = 0.8) and G31 values (5.5 GPa, SD = 0.7) were not significantly different from those of the edentulous mandible.
Other Elastic Properties
Poisson’s ratios, elastic coefficients, and anisotropy ratios are given in the Appendix (Tables 5-7) (www.dentalresearch.org).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Ogata and Satoh (1995), in a clinical study, demonstrate one functional difference between dentate and edentulous individuals that may be important. A small sample of edentulous subjects exhibited increased bilateral occlusion compared with the more prevalent unilateral chewing and biting of the dentate. Bilateral occlusion reduces the transfer of masticatory and bite forces across the symphysis and mandibular twisting moments, which would increase the relative amount of bending during chewing and biting. Since an effective way for bone to resist deformation is for the direction of maximum stiffness to be aligned with the direction of load (principal stress) (Dechow and Hylander, 2000), then the less oblique direction of maximum stiffness may be a structural adaptation to resist relatively greater amounts of bending and decreased shear in the retromolar region.
Other than our work on dentate mandibles (Schwartz-Dabney and Dechow, in press), no measurements of the direction of maximum stiffness are available for any bones. It is interesting that the direction of maximum stiffness deviates from the anatomical axes of the mandible at many sites. This may differ from diaphyses of the post-cranial skeleton, where the stiffest directions are thought to parallel the long anatomical axes.
Also of great interest is the variation in the direction of maximum stiffness between sites. Some sites have a more constant orientation, while other sites have no statistically significant mean orientation between individuals. If material orientation is functionally related, this suggests that variations in loading may correspond to individual differences in mandibular form and muscular function.
Cortical Thickness
Our results show that differences in cortical thickness between edentulous and dentate mandibles vary regionally. The most pronounced difference is the general tendency for cortical thickness to be greater in the corpus, especially lingually, and lesser in the ramus. We hypothesize that the thicker cortical bone of the edentulous corpus represents a secondary adaptation to relatively larger strains due to a reduction in alveolar height and corpus cross-section, despite overall reduced muscular and biting loads. We also hypothesize that the cortical bone of the ramus is thinner secondary to decreased muscular loading (Raustia et al., 1996). Modeling studies of function in edentulous mandibles could be used to test the mechanical effects of ridge reduction and reduced muscular load, but such information is currently unavailable.
A possible functional corollary in dentate mandibles is the relationship between mandibular cortical thickness and facial form. Cortical thickness beneath the molars varies from thicker in short-faced subjects to thinner in long-faced subjects (Masumoto et al., 2001). This difference may be directly related to masticatory loads, which are greater in short-faced individuals (Throckmorton et al., 1980).
Density
Controversy exists regarding the effects of tooth loss on mandibular density. Many of the differences among studies are methodological. Most studies assess density with two-dimensional scanning techniques (Horner and Devlin, 1992; Klemetti et al., 1994; Ulm et al., 1994), which are unable to remove the effects of thickness from material density and may be assessing primarily cortical thickness. Other studies use histological or microscopic techniques (Kingsmill and Boyde, 1998), which show cross-sectional density variations on an osteonal scale, but do not given volumetric measurements.
Our results are apparent volumetric representations of density at an intermediate tissue level, and they may differ from the results of density studies on a microscopic scale, since they are influenced by the amounts of both microporosities, such as resorption spaces, and mineralization in bone. Our results agree with those of Henrikson and Wallenius (1974), who use a technique similar to ours and find no differences in densities between dentate and edentulous individuals, or between genders. Our study extends these results to other regions of the mandible, where likewise no significant differences are found. The lack of differences suggests that cortical bone density following edentulation is maintained despite changes in structure, stiffness, and anisotropy.
Elastic Properties
The most interesting findings of this study are the significant differences in maximum stiffness (E3) between edentulous and dentate mandibles, despite the lack of significant differences in density, and other elastic moduli. The overall positive correlation between cortical bone density and stiffness is well-known. However, these correlations are generally moderate and explain only a portion of the variance in either variable. The differing results for density and maximum stiffness suggest that three-dimensional structural changes can occur within cortical bone, while density changes little.
The regional differences in maximum stiffness are also of great interest. In much of the mandible, cortical bone may partially compensate for a thinner cortex with increased stiffness. However, this increase in stiffness may come at a cost. While the mandible may deform less for a given load, the cortex may be more brittle and thus fail more quickly under the largest and most rapidly applied loads.
On average, the edentulous mandible compared with the dentate mandible has (1) greater maximum stiffness coupled with thicker bone in the lingual corpus, (2) greater maximum stiffness anteriorly in the facial corpus and at the lingual condylar neck, (3) lesser maximum stiffness and thickness in portions of the ramus, and (4) different directions of the axes of maximum stiffness at some sites, especially in the buccal retromolar region. These differences imply adaptations to altered patterns of regional loading and deformation. In the ramus, these differences correspond to decreased EMG activity, muscular atrophy, and (presumably) muscle load in edentulous individuals (Raustia et al., 1996).
An understanding of these differences and their impact on clinical restorations of the mandible and its dentition requires greater knowledge of oral function in the edentulous, as well as the links among material properties, the intermediate or microstructure of cortical bone, and the processes of bone adaptation. These findings also suggest the importance of considering the three-dimensional aspects of cortical bone structure and material properties in studies of patterns and mechanisms of bone adaptation.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Received July 25, 2001; Last revision June 14, 2002; Accepted June 17, 2002
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REFERENCES |
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) indicates a significant difference between facial and lingual cortices.
