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RESEARCH REPORT |
1 Dental Institute, Barts and The London Queen Mary’s School of Medicine and Dentistry, New Road, London, UK, E1 1BB;
2 Cancer Research UK, Lincoln’s Inn Fields Laboratories, London WC2A 3PX; and
3 UCL Eastman Dental Institute, London WC1X 8LD, UK
* corresponding author, v.j.kingsmill{at}qmul.ac.uk
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: cortical porosity • scanning electron microscopy • osteoporosis • age changes • bone histomorphometry
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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In support of the idea that turnover of different bones may be regulated differentially, we have previously demonstrated marked differences in the degree of mineralization between the mandible and other bones in the aged human (Kingsmill and Boyde, 1998b). Using a quantitative method for obtaining high-resolution information on the degree of mineralization of bone at the fabric level (BSE-SEM, Boyde et al., 1995), we have shown that the mandible was more highly mineralized than bones of the post-cranial skeleton (Kingsmill and Boyde, 1998b). In addition, the level of mineralization of the mandible did not correlate with the levels in other post-cranial bones (fourth lumbar vertebra, iliac crest, and femoral neck), but it did show a correlation with the level of mineralization in parietal bone. The factors influencing turnover, remodeling, and mineralization of the mandible are potentially of considerable clinical importance in prosthodontics and dental implantology.
One explanation for the differences in mineralization might be that the mandible turns over more slowly than post-cranial bone in elderly individuals, thus allowing the tissue to attain a higher level of mineralization. However, alveolar bone has, at least traditionally, been thought to have a high turnover rate. Alternatively, mandibular bone might have a higher capacity for mineralization than other bones. However, the lack of correlation between the mineralization levels in the mandible and in post-cranial bones supports the hypothesis that there are innate regional anatomical differences in the regulation of bone turnover and degree of mineralization. These observations might suggest that there are preprogrammed differences in responses in bone cells from different sites. However, it is also possible that the differences between responses in different bones are the result of structural variations between bones. Specifically, variations in vascularity between different bones might be a key factor in determining the responsiveness to local and systemic factors which may regulate bone turnover, particularly since the recruitment of osteoclasts is likely to be from blood-borne precursors of the monocyte lineage.
Therefore, the aim of this study was to investigate the hypothesis that the level of mineralization of bone correlates with the local cortical porosity of bone. We also investigated the regional variation in the vascular canals within the mandible, to determine whether there is a relationship between cortical porosity and other local (the degree of residual ridge resorption and dental status) or systemic variables (age, sex, and the cortical porosity of other bones).
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MATERIALS & METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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).
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Since the bone samples had been embedded in poly-methylmethacrylate (PMMA), which, compared with mineralized bone, has a very low electron backscattering coefficient, it was easy to threshold to separate ’bone’ from ’non-bone’ (Fig. 1a). A shape factor was used to remove features with an aspect ratio of less than 0.2, to eliminate the cracks present in some specimens. Blocks of marrow space or other extra-bony space were excluded on a size basis, to leave all osteonal canals, including those ’cutting cones’ which had yet to be filled with bone.
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): the average cross-sectional area of a canal = canals/number of canals (= c/a); and the canal volume fraction = proportion of bone tissue taken up by vascular canals (c/(b+c)).
Data Analysis
Mandible
Buccal, lingual, inferior border, and alveolar crest sites were studied in bone slices from midline, mental foramen, and third molar regions of the mandible. For the third molar region, an additional sampling site was selected on the supero-medial aspect (at the site of the insertion of mylohyoid muscle): The term ’alveolar’ is here used to denote the most superior aspect of the mandibular body, in edentulous regions being represented by the crest of the ridge.
The data were also analyzed for the effects of gender and dental status—dentate having all teeth, partially dentate having anterior teeth but no more than 1 posterior tooth, and edentate having no teeth. For the edentulous individuals, we analyzed the data further to determine whether size or number of vascular canals showed any co-variation with the mandibular height (measured from radiographs of the 2-mm-thick bone slices taken in the mental foramen region, with the specimen placed directly on the film packet, and focus-film distance of 1 m, at 50 kV, 150 mA, and 0.02 sec; Kingsmill and Boyde, 1998a).
Post-cranial Bones
Only cortical regions were selected. For the fourth lumbar vertebral body, which has very thin ’cortical’ bone, a site one-third of the way down the midline of the anterior aspect was chosen. This eliminated the chance of including areas of calcified fibrocartilage from the end plates, which may attain very high levels of mineralization compared with calcified bone proper. For the iliac crest, the inner and outer cortices were chosen from the site usually selected for bone biopsies. For the cross-sections of the femoral neck, a mean value was obtained from 20 evenly spaced sites imaged around the entire cortex.
Statistical Method
For each outcome of interest, a mean value per site per individual was calculated from the multiple images processed at each site. Data were analyzed by a Generalized Estimating Equation (GEE) approach (Laing and Zeger, 1986), with the statistical software package STATA, version 7.0 (STATA Corporation, 2002, College Station, TX, USA). GEE is a regression technique that explicitly accounts for the clustered nature of the data. This was necessary since multiple data items were collected from each specimen. Where appropriate, analyses were undertaken for both unadjusted relationships (univariately) and also adjusted for the potential confounding effects of the individuals’ ages and genders (Table 2). Parameter estimates and their associated 95% confidence intervals were calculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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), with a mean cortical porosity of 16.1%.
In the mandible, the size of blood vessel canals was fairly constant. The labial aspect of the midline was the most porous site studied (mean, 10.8%), having a high number of canals (mean, 7.2 per mm2) of nearly double the cross-sectional area of the other mandibular sites (23,004 µm2, Figs. 1b, 1c, 1d). Buccal sites generally tended to have larger-diameter canals than did lingual sites, a finding in agreement with that of Atkinson and co-workers (Atkinson and Woodhead, 1968; Atkinson and Hallsworth, 1983). The third molar region of the mandible was less porous than more anterior sites, as a consequence of having canals of narrower diameter.
As seen previously (Kingsmill and Boyde, 1998b), the mandible was more highly mineralized than the other sites (Fig. 1e). The lower value seen for the supero-lingual aspect of the bone section from the third molar region resulted from the fact that many of the samples for this site came from young individuals, known to have less highly mineralized bone at a site of an erupting tooth. No correlation was found between mineralization density and cortical porosity, as measured either by canal size (r2 = 0.123 for all sites, and r2 = 0.0002 where the post-cranial bones were excluded); or where assessed by the percentage of bone occupied by canals (r2 = 0.40, and r2 = 0.006 when post-cranial bones were excluded).
Variation with Dental Status
Unexpectedly, the cortical porosity in the posterior of partially dentate mandibles was found to be significantly greater than that of either dentate or edentate mandibles, due largely to an increase in the size of the canals (Figs. 2a–2c). The mineralization density was also greater in the partially dentate (Fig. 2d).
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Variation with Gender
The mandibular cortex in females contained a greater proportion of vascular space (female mean, 8.57%, SD, 6.23; male, 6.15%, SD, 5.62, p = 0.001) than in males, being 1.6% more porous. The number of canals was the same, but they were of a significantly greater mean cross-sectional area (p = 0.026). There were no significant differences in canal number or mean mineralization density between the sexes (Table 2).
Variation with Degree of Residual Ridge Resorption
Even adjusted for age and sex, no relationship was seen between the porosity of the cortex of highly resorbed edentulous mandibles compared with those that showed less resorption (number, size, proportion of bone occupied by canals, p = 0.79, 0.71, and 0.27, respectively).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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A relationship between bone mineralization and vascularity might be expected, since, within cortical bone, the canals that contain the blood vessels are the sites of bone turnover. New cutting cones being filled with newer, less mineralized bone may have a large central canal if the bone infill is incomplete. In this study, however, no relationship between the overall degree of tissue mineralization and the number, size, or percentage of tissue occupied by canals was seen. This would suggest that differences in mandibular vascularity do not account for the very high level of tissue mineralization in the mandible.
The results showed similarity in porosity along the body of the mandible, which would be expected, since this is the direction in which the Haversian canals are thought to run (Seipel, 1948). The midline, however, showed a higher volume density of canals, which may arise as a result of cross-over from the contralateral side, or from vessels entering the bone at this site (Fanibunda and Matthews, 2000; Saka et al., 2002). However, the vascular canal data must be interpreted with caution, since they provide only an implied indication of the vascularity of the cortex.
It is interesting that there was no significant difference in the porosity of the cortical bone between completely dentate and edentulous individuals. If porosity reflects function in any way, then both dentate and edentulous mandibles must be operating at similar levels of strain for their size and shape. However, the partially dentate mandibles showed an increased cortical porosity in the posterior mandible, with a similar numerical density of canals but of an increased cross-sectional area. Partially dentate individuals can generate reasonably high bite forces (Helkimo et al., 1977), but the bone height in the third molar region is reduced and may thus experience higher strains. The most strained part of the bone therefore appears to have the largest canals.
Larger canals may indicate more rapid turnover, and hence the Haversian canals are newer and less in-filled, but if this were the case, the mineralization levels of the surrounding newer bone would be less, whereas the opposite is the case (Fig. 2d), with these mandibles having more highly mineralized bone in the posterior region. This situation could arise if there is a failure of infilling of the canals, thus leaving only the older, hypermineralized interstitial bone. This might suggest that the posterior portion of partially dentate mandibles could be mechanically and biologically different, by being both more highly mineralized and more porous, yet possibly having a greater vascularity.
The femoral neck cortex was seen to be highly porous, mostly arising as a result of a large number of canals (Bell et al., 2001). The high porosity of the neck of the femur may again indicate a link with high functional loading.
With regard to the differences seen between the sexes, the increased cross-sectional area of canals in females represents a relative failure in osteonal closure. Whether this confers any disadvantage, such as the bone being less resistant to fracture due to its increased porosity, or advantage, due, for example, to an increased capacity for vascular penetration in implant healing, remains to be determined. The vascular canals that exist within aged mandibular bone and their variation at different sites may have implications for the rate of healing at different sites in the mandible after surgery.
Overall, there was no evidence that increased mineralization in the mandible, as we observed previously, is the result of differences in bone turnover arising from variations in vascularity of that bone compared with other bones. This raises the intriguing possibility that bone tissue at different sites may be regulated by intrinsically distinct local and systemic factors, although further studies are clearly required to pursue this idea.
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ACKNOWLEDGMENTS |
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Received December 19, 2005; Last revision November 14, 2006; Accepted November 22, 2006
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Atkinson PJ, Woodhead C (1968). Changes in human mandibular structure with age. Arch Oral Biol 13:1453–1464.[ISI][Medline]
Bell KL, Loveridge N, Reeve J, Thomas CD, Feik SA, Clement JG (2001). Super-osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec 264:378–386.[Medline]
Boyde A, Davy KWM, Jones SJ (1995). Standards for mineral quantitation of human bone by analysis of backscattered electron images. Scanning 17(Suppl V):6–7.
Fanibunda K, Matthews JN (2000). The relationship between accessory foramina and tumour spread on the medial mandibular surface. J Anat 196:23–29.
Helkimo E, Carlsson GE, Helkimo M (1977). Bite force and state of dentition. Acta Odontol Scand 35:297–303.[ISI][Medline]
Kingsmill VJ, Boyde A (1998a). Variation in the apparent density of human mandibular bone with age and dental status. J Anat 192:233–244.
Kingsmill VJ, Boyde A (1998b). Mineralisation density of human mandibular bone: quantitative backscattered electron image analysis. J Anat 192:245–256.
Laing KY, Zeger SL (1986). Longitudinal data analysis using generalized linear models. Biometrika 73:13–22.
Saka B, Wree A, Anders L, Gundlach KK (2002). Experimental and comparative study of the blood supply to the mandibular cortex in Gottingen minipigs and in man. J Craniomaxillofac Surg 30:219–225.[Medline]
Seipel CM (1948). Trajectories of the jaws. Acta Odontolog Scand 8:81–191.
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