|
|
||||||||
RESEARCH REPORT |
1 Department of Orthodontics and Oral Biology, University Medical Centre Nijmegen, University of Nijmegen, PO Box 9101, 6500 HB Nijmegen, the Netherlands;
2 Department of Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), Amsterdam, the Netherlands;
3 Orthopaedic Research Laboratory, Department of Orthopaedic Surgery, Aarhus University Hospital, Aarhus, Denmark; and
4 Orthodontic Department, Royal Dental College, Aarhus University, Aarhus, Denmark;
* corresponding author, e.giesen{at}dent.umcn.nl
| ABSTRACT |
|---|
|
|
|---|
KEY WORDS: cancellous bone architecture edentate mandibular condyle
| INTRODUCTION |
|---|
|
|
|---|
In previous studies, it has been shown that the cancellous bone of the mandibular condyle is adaptive, i.e., in edentate subjects, the apparent density and bone volume fraction were found to be lower than in dentate subjects (Hongo et al., 1989a; Kawashima et al., 1997; Giesen et al., 2003b). The mechanical consequence is a reduction (2030%) in stiffness and strength (Giesen et al., 2003b). Thus far, however, there is no information available on the nature of the morphological bone changes in edentate subjects. It has been demonstrated, for example, that the apparent density of the cancellous bone in the human tibia decreases during aging (Ding et al., 1997), and that this decrease is accompanied by a change in bone structure type, from plate-like toward more rod-like (Ding and Hvid, 2000). Furthermore, the anisotropy of the bone and the bone surface-to-volume ratio has been demonstrated to increase with age (Ding et al., 2002). In patients with hip fractures, a lower bone density has been found, accompanied by a higher degree of anisotropy (Ciarelli et al., 2000).
For the mandibular condyles of dentate subjects, a close relationship between bone density and the type of trabecular structure has been shown (Giesen et al., 2003a), i.e., a higher apparent density is associated with more plate-like trabeculae, whereas a lower apparent density is associated with more rod-like trabeculae. It can be questioned whether the cancellous bone of edentate subjects exhibits the same kind of relationship. If the bone adapts similarly in dentate and edentate subjects, we would expect that, in edentate subjects, the changes in density are similarly accompanied by changes in the trabecular structure type and not by changes in, for instance, trabecular thickness or connectivity density.
In the present study, we investigated whether the stiffness of the bone of dentate and edentate subjects depended differently on the amount of bone and trabecular orientation. These measures were applied according to Giesen et al.(2003a) and were entered into linear regression analyses so that the variance in mechanical properties could be explained. It was hypothesized that, if only the amount of bone-related morphological parameters changed in the edentate subjects, the regression models to describe these mechanical properties are more or less the same for edentate and dentate subjects.
| MATERIALS & METHODS |
|---|
|
|
|---|
To obtain their three-dimensional trabecular microstructure, we scanned the specimens in a micro-computed tomography (micro-CT) system (µCT20, Scanco Medical AG, Zürich, Switzerland). The specimens were placed in embalming fluid to avoid dehydration during scanning. The scanning was performed at a resolution of 18 µm. To distinguish bone from non-bone, we used a fixed threshold, which we had obtained experimentally by matching the bone volume fraction from the scans with the one that was measured according to a method based on Archimedes principle (Ding et al., 1999). Several bone morphology parameters were calculated (Software Revision 3.1, Scanco Medical AG): bone volume fraction, bone surface-to-volume ratio, trabecular thickness, trabecular separation, connectivity density, structure model index, and degree of anisotropy. The bone volume fraction is the ratio of the bone volume to the specimens volume. Bone surface-to-volume ratio was the ratio of the bone surface to the bone volume. Trabecular thickness and trabecular separation were determined with use of a model-independent method (Hildebrand and Rüegsegger, 1997a). Connectivity density is a measure for the number of trabeculae per unit volume (Odgaard and Gundersen, 1993). The structure model index quantifies the characteristic form of the cancellous bone in terms of plate-like to rod-like. For an ideal plate and rod structure, this index is 0 and 3, respectively (Hildebrand and Rüegsegger, 1997b). The principal directions of the trabecular structure were estimated by the mean intercept length (MIL) ellipsoid. The degree of anisotropy was defined as the ratio between the MILmax and MILmin. Further, the orientation of the trabeculae was expressed by the angle between the main direction of the trabecular structure (MILmax) and the axis of the cylindrical specimen (for more detail, see Giesen et al., 2003a).
Stiffness and strength were determined by destructive mechanical compression tests, carried out with a materials testing machine (858 Mini Bionix, MTS Systems Corporation, Minneapolis, MN, USA) equipped with a 1-kN load cell. The cylindrical specimens were compressed between parallel plates at a constant strain rate of 0.2% s-1 until a strain of 3% was reached. The E-modulus (or stiffness) is defined as the maximum slope of the stress-strain curve. The ultimate stress (or strength) is defined as the maximal stress during the test. For more details about the mechanical tests, refer to Giesen et al.(2001).
After the micro-CT scanning and mechanical testing, we applied Archimedes principle to determine cancellous bone density parameters (Ding et al., 1997). The marrow was removed from the specimens. Apparent density was defined as the ratio of the mass of specimen to its total volume. Bone volume fraction is the space occupied by mineral tissue relative to the specimens volume. Tissue density was taken as the ratio between the mass of specimen and the space occupied by mineral tissue.
We applied Students t tests to detect differences between dentate and edentate subjects. A p-value of less than 0.05 was considered statistically significant. To determine whether bone of dentate and edentate subjects had different relationships between bone morphology (bone volume fraction and the angle of the principal trabecular orientation) and mechanical properties (E-modulus and ultimate stress), we conducted linear regression analyses. The effects of age and number of absent teeth on the morphological parameters were investigated by multivariate analyses and correlation coefficients. SPSS 10.1.0 software (SPSS Inc., Chicago, IL, USA) was used for all statistical analyses.
| RESULTS |
|---|
|
|
|---|
|
|
|
|
| DISCUSSION |
|---|
|
|
|---|
The degree of anisotropy did not differ between the edentate and the dentate subjects, although in aging bone an increase in the degree of anisotropy has been reported (Ding et al., 2002). Also, in patients with hip fractures, the degree of anisotropy increased with proportionally fewer trabecular elements transverse to the primary loading axis (Ciarelli et al., 2000). In a previous study, we found an unchanged mechanical anisotropy in the edentate subjects (Giesen et al., 2003b). This is consistent with the unchanged morphological anisotropy in the present study. It indicates that the changes in bone structure occurred equally in all directions.
The regression models to describe E-modulus and ultimate stress from the angle of the trabeculae relative to the testing direction and the bone volume fraction were very similar for both the dentate and the edentate groups. Since, in edentate subjects, the volume fraction was lower, the cancellous bone of the condyle was not as stiff and strong as in dentate subjects. The similar regression models indicate a similar dependence of mechanical properties on the trabecular structure. This is in line with the changes in morphology, i.e., in edentate subjects the amount of bone was reduced, and this reduction was associated with a change toward more rod-like trabeculae. If the degree of anisotropy had changed, the mechanical properties would have depended differently on the trabecular orientation, which was not the case.
Some remarks have to be made about the material used. First, we did not know at what age the edentate subjects had lost their teeth, and whether they had worn dentures. Therefore, the time-period and the level of reduced mechanical loading were unknown. Further, we did not know if they had lost their teeth as a result of general osteoporosis, generating an overall lower bone density. Nevertheless, since it has been reported that edentate subjects have lower masticatory function (Boretti et al., 1995) and produce lower bite forces (Helkimo et al., 1977), we can safely assume that the mandibles of our edentate group had been subjected to a reduced mechanical loading. Second, the edentate subjects were significantly older than the dentate subjects. Therefore, an age-related decrease of density and E-modulus (Ding et al., 1997) could be expected in the edentate group. However, no age-related changes in density of the human mandibular condyle were previously found (Hongo et al., 1989b). Also, in the present study, we found no correlations of aging and any of the morphological parameters for both the edentate and the dentate group. In addition, in the dentate group, no correlations were found between the number of absent teeth and any of these parameters. Third, the embalming procedure could have changed the mechanical properties, i.e., a slight increase in stiffness (Linde, 1994). However, the major findings of this studythat is, the differences between dentate and edentate subjectsare not invalidated.
To conclude, the morphology of the cancellous bone in the mandibular condyles in edentate subjects was less dense than that in dentate subjects and had changed toward a more rod-like structure. The regression models of the mechanical properties built from the bone volume fraction and the trabecular orientation were similar for the two groups. Thus, mechanical properties depended similarly on morphology.
| ACKNOWLEDGMENTS |
|---|
Received July 24, 2003; Last revision December 5, 2003; Accepted December 8, 2003
| REFERENCES |
|---|
|
|
|---|
Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA (2000). Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res 15:3240.[Medline]
Ding M, Hvid I (2000). Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone 26:291295.[Medline]
Ding M, Dalstra M, Danielsen CC, Kabel J, Hvid I, Linde F (1997). Age variations in the properties of human tibial trabecular bone. J Bone Joint Surg Br 79(B):9951002.
Ding M, Odgaard A, Hvid I (1999). Accuracy of cancellous bone volume fraction measured by micro-CT scanning. J Biomech 32:323326.[Medline]
Ding M, Odgaard A, Linde F, Hvid I (2002). Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res 20:615621.[Medline]
Giesen EB, Ding M, Dalstra M, Van Eijden TM (2001). Mechanical properties of cancellous bone in the human mandibular condyle are anisotropic. J Biomech 34:799803.[ISI][Medline]
Giesen EB, Ding M, Dalstra M, Van Eijden TM (2003a). Architectural measures of the cancellous bone of the mandibular condyle identified by principal components analysis. Calcif Tissue Int, 73:225231.[ISI][Medline]
Giesen EB, Ding M, Dalstra M, Van Eijden TM (2003b). Reduced mechanical load decreases the density, stiffness, and strength of cancellous bone of the mandibular condyle. Clin Biomech 18:358363.
Helkimo E, Carlsson GE, Helkimo M (1977). Bite force and state of dentition. Acta Odontol Scand 35:297303.[ISI][Medline]
Hildebrand T, Rüegsegger P (1997a). A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc 185:6775.
Hildebrand T, Rüegsegger P (1997b). Quantification of bone microarchitecture with the Structure Model Index. Comput Methods Biomech Biomed Engin 1:1523.[Medline]
Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999). Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14:11671174.[ISI][Medline]
Hongo T, Yotsuya H, Shibuya K, Kawase M, Ide Y (1989a). Quantitative and morphological studies on the trabecular bones in the condyloid processes of the Japanese mandibles. Comparison between dentulous and edentulous specimens. Bull Tokyo Dent Coll 30:6776.[Medline]
Hongo T, Orihara K, Onoda Y, Nakajima K, Ide Y (1989b). Quantitative and morphological studies of the trabecular bones in the condyloid processes of the Japanese mandible; changes due to aging. Bull Tokyo Dent Coll 30:165174.[Medline]
Huiskes R (2000). If bone is the answer, then what is the question? J Anat 197(Pt 2):145156.
Kabel J, Odgaard A, van Rietbergen B, Huiskes R (1999). Connectivity and the elastic properties of cancellous bone. Bone 24:115120.[Medline]
Kawashima T, Abe S, Okada M, Kawada E, Saitoh C, Ide Y (1997). Internal structure of the temporomandibular joint and the circumferential bone: comparison between dentulous and edentulous specimens. Bull Tokyo Dent Coll 38:8793.[Medline]
Kinney JH, Ladd AJ (1998). The relationship between three-dimensional connectivity and the elastic properties of trabecular bone. J Bone Miner Res 13:839845.[ISI][Medline]
Linde F (1994). Elastic and viscoelastic properties of trabecular bone by a compression testing approach. Dan Med Bull 41:119138.[ISI][Medline]
Newton JP, Yemm R, Abel RW, Menhinick S (1993). Changes in human jaw muscles with age and dental state. Gerodontology 10:1622.[Medline]
Odgaard A, Gundersen HJ (1993). Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstruction. Bone 14:173182.[Medline]
Turner CH (1998). Three rules for bone adaptation to mechanical stimuli. Bone 23:399407.[Medline]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| IADR Journals | Advances in Dental Research ® |
| Journal of Dental Research ® | Critical Reviews (1990-2004) |