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J Dent Res 86(1):52-57, 2007
© 2007 International and American Associations for Dental Research

RESEARCH REPORT
Biological

Relationship between Porotic Changes in Alveolar Bone and Spinal Osteoporosis

R. Binte Anwar1, M. Tanaka1,*, S. Kohno1, M. Ikegame2, N. Watanabe3, M. Nowazesh Ali4, and S. Ejiri2

1 Div. of Removable Prosthodontics,
2 Div. of Anatomy and Cell Biology of the Hard Tissue,
3 Div. of Orthodontics, and
4 Div. of Reconstructive Surgery for Oral & Maxillofacial Region, Niigata University Graduate School of Medical and Dental Sciences, 5274, 2-Bancho, Gakkocho-dori, Niigata 951-8514, Japan

* corresponding author, mikako{at}dent.niigata-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Epidemiological studies have shown that post-menopausal women who do not use an estrogen supplement have fewer teeth than those who do. We hypothesized that changes in the dentition of post-menopausal women might be due to alveolar bone alterations by estrogen deficiency. To clarify this, we analyzed the microstructural alveolar bone changes in ovariectomized monkeys and compared these with their lumbar bone mineral density. The % of baseline bone mineral density showed a significant decrease in the ovariectomized group as compared with the controls. The second-molar interradicular septa in ovariectomized monkeys showed a significantly decreased nodes number, cortices number, and an increased structural model index value. More pores were seen in the ovariectomized group at the top of the septa. This study demonstrated that, in such monkeys, estrogen deficiency led to fragility of the trabecular structure of the molar alveolar bone, and such fragility was inversely correlated with lumbar bone mineral density.

KEY WORDS: bone histomorphometry • non-human primates • ovariectomy • osteoporosis • alveolar bone


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Post-menopausal osteoporosis, caused by a drop in estrogen levels after menopause, is a world-wide common problem inducing low bone mass and micro-architectural deterioration of the bone scaffolding in vertebrae and long bones. This disease often leads to osteoporotic fractures, which contribute to substantial morbidity, increased medical costs, and remarkably poor quality of life in the elderly. Consequently, their mortality risk also becomes higher (Melton, 2003).

In the dental field, post-menopausal osteoporosis has also drawn attention, with some studies suggesting that estrogen influences tooth retention by preventing resorption of the alveolar bone (Krall et al., 1997). According to epidemiological research (McGrath and Bedi, 2004), the oral health status of the aged has a dramatic impact on their quality of life in a variety of physical, social, and psychological ways. Tooth loss is associated with deterioration of the systemic health of the elderly through changes in their dietary intake (Ritchie et al., 2002). Thus, it is essential for dentists to take active steps to preserve older patients’ teeth, and to help them maintain their masticatory function.

While the systemic effect of estrogen deficiency has been known for years, its relationship to alveolar bone loss and subsequent tooth loss has been examined only recently, with mixed results. A significant association was first reported between post-menopausal tooth loss and metacarpal bone mass (Daniell, 1983), and some investigators have also linked tooth loss to low general skeletal bone mineral densities and high bone-loss rates in post-menopausal women (Krall et al., 1996; Taguchi et al., 1999). However, others have failed to find such an association between tooth loss and skeletal bone mineral density in post-menopausal women (Mohammad et al., 1997; Earnshaw et al., 1998). Moreover, any relationship between periodontitis, a major factor in tooth loss in the elderly, and the condition of systemic bone mass is denied by some reports (Elders et al., 1992; Klemetti and Vainio, 1993). In contrast, positive associations among periodontitis, estrogen deficiency, and tooth loss have also been reported in other studies (Payne et al., 1999; Taguchi et al., 2004). Thus, the relationship between osteoporosis and tooth loss remains a matter of contention. It is likely that variance in the size and age range of study populations, together with the wide variety of conditions associated with mechanical stress on their jaw bones, such as differences in dentition and history of dental treatment (Lockington and Bennett, 1994), may have contributed to this controversy. From such obstacles in the assessment of human subjects, investigations with ovariectomized animals have been recently proposed.

Ovariectomized rats have been considered a suitable model for human post-menopausal osteoporosis (Wronski et al., 1988). However, rat experiments have shown both positive (Tanaka et al., 2002, 2003; Irie et al., 2004) and negative (Moriya et al., 1998) results in relation to osteoporosis and its effect on the jawbone. Though recent experiments on rats may show a positive relationship between osteoporosis and oral bone loss, they have many limitations when it comes to mimicking human menopause. Rodents do not experience natural menopause (Frost and Jee, 1992), and also have a different remodeling status (Wronski and Yen, 1991). Non-human primates, which experience human-like menopausal processes, have always been promising models with other obvious anatomical and physiological similarities, such as their endocrine and sex steroid metabolisms (Thorndike and Turner, 1998). However, to date, no reports have concerned the effect of estrogen deficiency on the alveolar trabecular bone of monkey mandibles. Therefore, to obtain the closest result that may be reflected in human alveolar bone, we investigated the microstructural alveolar bone changes occurring in ovariectomized monkeys. In addition, we compared these alveolar bone changes with changes in the monkeys’ lumbar bone mineral density, to clarify the possible relationship between tooth loss and osteoporosis.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects and Experimental Design
Twelve female adult wild-type cynomolgus monkeys, estimated to be over 9 yrs of age, were selected for this study. All animal procedures were performed, in accordance with institutional and NIH guidelines, at Shin Nippon Biomedical Laboratories (Kagoshima, Japan). The animals were housed in individual metal cages (630W x 700D x 770H mm3), where the temperature was kept at 26 ± 4°C, with 50 ± 10% humidity and a 12-hour light (08:00–20:00)/12-hour dark cycle. The 12 animals were randomly divided into 2 groups of 6. The test group was bilaterally ovariectomized under surgical anesthesia (chloride ketamine, 6 mg/kg body wt, intramuscularly), and the remainder received sham surgery (Sham). Sham animals had both ovaries exteriorized and replaced. To prevent possible infection, each animal was injected with 0.5 mL ampicillin thihydrate (Kela Laboratoria NV, Hoogstraten, Belgium) intramuscularly every day for 1 wk after surgery.

All animals were fed Teklad Global 25% Protein Primate Diet (Harlan Sprague-Dawley Inc., Indianapolis, IN, USA) containing 0.97% Ca. Water was supplied through automatic water dispensers. Finally, all animals were killed for analysis 76 wks after surgery, after being anesthetized with ketamine (6 mg/kg body wt, i/v) and pentobarbital (1 mL/1.4 kg body wt, i/v).

Estrogen Analysis
Serum estradiol concentrations were determined from serum samples collected just before surgery and 4, 25, and 76 wks after surgery.

Lumbar Bone Mineral Density
Bone mineral density of the lumbar vertebrae (L2–L4) was measured with dual-energy x-ray absorptiometry (Lunar DPX Alpha, Madison, WI, USA) just before surgery [either Sham or ovariectomized group] and 4, 8, 13, 25, 39, 52, and 76 wks after surgery.

CT Imaging and Trabecular Bone Morphometry
All mandibles obtained from both Sham and ovariectomized monkeys were scanned by micro-CT (Elescan; Nittetsu Elex, Osaka, Japan), with the following CT settings: voxel pitch, 54 µm; pixel size, 54 µm; projection number, 600; magnification, 1.91; voltage, 80 kV; and electrical current, 20 mA. We used 256 slices of 2D images to reconstruct 3D images of the right second molar (M2) region, with the TRI/3D-BON software (RATOC, Tokyo, Japan), and the M2 was then virtually removed on each image (Figs. 1A, 1BGo). We chose the M2 region to assess the microarchitectural changes, because the first molar is small and the third molar is located in the most distal part of the jaws, close to the compact bone.


Figure 1
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  		Figure 1. Steps involved in the analysis of alveolar trabecular bone. M1, M2, and M3 stand for the first, second, and third molars, respectively. (A) 3D image of the M2 region was reconstructed with micro-CT data. (B) The M2 was virtually removed on the image. The white outline represents the analyzed area. (C) Determining the region of interest (ROI): the sagittal plane passing through the mesial and distal M2 roots. Point I represents the highest point of the interradicular septum; points Mx and Dx represent the apex points of the mesial and distal roots of M2, respectively. The MxDx line served as the inferior border of the ROI. Mh and Dh represent the centers of the IMx and IDx, respectively. Two parallel lines, M and D, were perpendicularly drawn to MxDx through Mh and Dh, respectively. Finally, the ROI was established in the area between the M and D lines. (D) The M2 interseptal area was analyzed with 3D bone morphometry and 3D node-strut analysis. (E) The numbers of pores on the different alveolar socket walls were counted. Mesial wall, black line; lingual wall, dotted line; distal wall, white line; interseptal region, striped area. (F) Loss of alveolar crest height, defined as the distance between the top of the alveolar crest and the corresponding cementoenamel junction (CEJ) at the buccal area of the mandibular second molar (M2) region, was measured along the mesial root (mh) and distal root (dh), and then the average ({mh+dh}/2) was used as the final data in both groups. (G,H,I) Amano’s classification. Grade 0: no attrition on enamel, as shown in G. Grade 1: flat attrition on enamel. Grade 2: thread-like attrition on dentin. Grade 3: wide attrition on dentin, as seen in H. Grade 4: severe attrition without appearance of cusps and incisal edges, as shown in I. The degree of attrition of M2 was measured according to this classification.

 
For histomorphometry, one sampling region was determined beneath the M2 (Fig. 1CGo). To standardize the sampling region, we drew 2 straight lines from the top of the M2 interradicular septum (point I) to the mesial and distal root apex points (points Mx and Dx, respectively). Then, the midpoints of the IMx (point Mh) and IDx (point Dh) lines were determined. Finally, 2 perpendicular lines were drawn to the inferior border of the mandible (M and D lines, respectively). The area of interseptal bone obtained between the M and D lines was established as the region of interest (ROI) (Figs. 1C, 1DGo). Subsequently, the following examinations were made: From images obtained with micro-CT data, we measured bone volume, trabecular thickness, trabecular separation, trabecular number, and trabecular spacing (Uchiyama et al., 1997), assuming the parallel plate model (Parfitt et al., 1987). All the measurements were done with TRI/3D-BON software designed for 3D bone morphometry. The trabecular microstructure was also measured by node-strut analysis (Garrahan et al., 1986): The numbers of nodes, termini, and cortices were counted, and total strut length was measured and expressed per total tissue volume. The number of node-to-node struts was also counted. The alveolar bone proper was considered a kind of cortical bone, and the number of cortex-to-node struts was counted. The structural model index (Hahn et al., 1992) and trabecular bone pattern factor (Hildebrand and Ruegsegger, 1997) were also calculated.

Pores on the Alveolar Socket Walls
After the virtual removal of the dental roots from the images, we counted the number of pores on each alveolar socket wall, including the interradicular septum, using Luzex-F software (Nireco, Tokyo, Japan) (Fig. 1EGo).

Alveolar Crest Height and Attrition
The distance between the cementoenamel junction (CEJ) and the top of the alveolar crest was measured at the buccal area of the manidibular second molar (M2) region along the mesial (mh) and distal roots (dh), and then the average was defined as the loss of alveolar crest height ({mh+dh}/2) in both the Sham and ovariectomized groups (Fig. 1FGo). We also determined the degree of attrition using Amano’s classification (Amano, 1951) in both groups (Figs. 1G–1IGo). Single-regression analysis was performed to determine the relationship between alveolar crest height and attrition.

Statistical Analysis
All data are presented as the means and standard deviations for each group. Comparisons among groups were performed with Fisher’s protected least-significant-difference test [one-way analysis of variance (ANOVA)]. The statistical analysis was done with StatView J-4.5 statistical software (Abacus Concepts, Inc., Hulinks, Inc., Tokyo, Japan). We statistically analyzed all data to check their correlation with lumbar bone mineral density, using single-regression analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Systemic Condition
Before the experiment, there were no significant differences between groups with respect to their serum estradiol concentrations and lumbar bone mineral densities (Figs. 2A, 2CGo). After 4 wks, almost undetectable estradiol concentrations in ovariectomized monkeys indicated that the ovariectomies had been successful (Fig. 2AGo). Lumbar bone mineral density in ovariectomized monkeys had decreased significantly by 76 wks after surgery, and the % of baseline bone mineral density was significantly lower in the ovariectomized group than in the Sham group (Figs. 2C, 2DGo). Lumbar bone mineral density during other time-points did not show any significant differences (Data not shown).


Figure 2
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  		Figure 2. Comparison between Sham and ovariectomized groups. (A) Serum estradiol concentrations at different time-points. Values are presented as means ± standard deviations (SDs) of 6 monkeys in each group. aSignificantly different from the baseline value of the same operational group (P < 0.05). bSignificantly different from the Sham value (P < 0.05). (B) Body weight at different time-points. Values are presented as means ± standard deviations (SDs) of 6 monkeys in each group. No significant differences were found between groups. (C) Changes in lumbar bone mineral density. aSignificantly different from the baseline bone mineral density of the same operational group (P < 0.05). bSignificantly different from the Sham value at the same time-point (P < 0.05). (D) % of baseline lumbar bone mineral densities which were calculated by the following equation: ({Final lumbar bone mineral density /baseline lumbar bone mineral density} X 100). The coefficient of variation of dual-energy x-ray absorptiometry measurement was less than 2%. bSignificantly different from the Sham value (P < 0.05). (E) Results of 3D morphometric analysis of the alveolar bone. Values are presented as means ± SDs of 6 monkeys in each group. No significant differences were found between groups. (F) Results of node-strut analysis of the alveolar bone. Values are presented as means ± SDs of 6 monkeys in each group. bSignificantly different from the Sham value (P < 0.05). (G) Results of trabecular architectural morphometry of the alveolar bone. Values are presented as means ± SDs of 6 monkeys in each group. bSignificantly different from the Sham value (P < 0.05). (H) Number of pores in the different walls of the alveolar socket. Significant difference was found between the Sham and the ovariectomized groups at the top of the interradicular septum. Values are presented as means ± SDs of 6 monkeys in each group. bSignificantly different from the Sham value (P < 0.05). (I) Loss of buccal alveolar crest height. Values are presented as means ± SDs of 6 monkeys in each group. No significant differences were found between groups. (J) Attrition degree according to Amano’s classification. Values are presented as means ± SDs of 6 monkeys in each group. No significant differences were found between groups.

 
Oral Condition
    Morphometric Analysis of Alveolar Bone
Although no significant differences were found in bone volume between the Sham and ovariectomized groups (Fig. 2EGo), some micro-CT images showed greater bone volume in the Sham than in the ovariectomized group, with less marrow space in the interradicular septum of the M2 alveolar bone (Figs. 3A–3CGo). In the Sham group, the trabeculae were connected and formed network structures; by contrast, the trabeculae of the ovariectomized group became fragmented and seemed to form isolated islands in the large bone marrow (Figs. 3A, 3BGo). Node-strut analysis revealed significant decreases in the ovariectomized group with respect to node numbers as well as the number of cortices (Fig. 2FGo), and total strut length/total tissue volume showed similar changes in bone volume.


Figure 3
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  		Figure 3. Micro-CT findings of the M2 alveolar bone. The tooth was virtually removed on the images. (A) 2D sagittal view at the center of M2. The Sham group showed larger bone volume with less bone marrow space. By contrast, the ovariectomized group showed less bone volume and increased marrow space. (B) 2D frontal view at the center of M2. The Sham group displayed normal trabecular network structure; the ovariectomized group featured disconnected trabeculae. (C) 3D images of the M2 interradicular septum showing an abundance of rod-like trabeculae in the ovariectomized group, whereas those in the Sham group are principally plate-like. (D) Buccal view of the alveolar socket. The buccal wall was virtually removed on the images. Significantly more pores are visible in the alveolar socket at the top of the interradicular septum (arrow) in the ovariectomized group than in the Sham group.

 
Trabecular architectural morphometry results showed a significantly higher structural model index in the ovariectomized group than in the Sham group (Fig. 2GGo), and was supported by micro-CT images, which revealed rod-like trabeculae in the ovariectomized group and plate-like trabeculae in the Sham group (Fig. 3CGo). Trabecular bone pattern factor results were also similar to the structural model index; however, these differences were not statistically significant (Fig. 2GGo). During observation of the internal surface of the alveolar socket, significantly more pores were present in the ovariectomized group than in the Sham group at the top of the interradicular septum (Figs. 2HGo, 3DGo). In the other regions of the alveolar walls, however, no significant differences were found between the Sham and the ovariectomized groups in terms of the number of pores.

    Loss of Alveolar Crest Height and Attrition
No significant differences were found with respect to loss of buccal alveolar crest height and attrition as a result of the estrogen deficiency (Figs. 2I, 2JGo). However, loss of alveolar crest height and attrition were themselves significantly correlated (Fig. 4AGo).


Figure 4
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  		Figure 4. Results of single-regression analysis. (A) Significant positive relationship between loss of buccal alveolar crest height and attrition. (B) Significant positive relationship between % of baseline bone mineral density and node number. (C) Significant negative correlation between % of baseline bone mineral density and pore count at the top of the interradicular septum. Individual data (Sham = 6, ovariectomized group = 6) and the correlation coefficient R shown in each plot.

 
Relationship between Lumbar Bone Mineral Density and Alveolar Bone
The % of baseline bone mineral density showed a significant positive correlation with the number of nodes (Fig. 4BGo), and a significant negative one with the pore count at the top of the septa (Fig. 4CGo).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Lumbar bone mineral density in ovariectomized monkeys had decreased significantly by 76 wks after ovariectomy, a result consistent with previously reported changes in the lumbar bone mineral density of ovariectomized monkeys (Jerome et al., 1997) and of post-menopausal woman (Frost et al., 2004). This is the first study to report alveolar bone changes due to estrogen deficiency in monkeys; however, our study includes the limitation of a smaller sample size. Ovariectomized rats showed significant differences in bone volume between groups (Tanaka et al., 2002; Irie et al., 2004), but ovariectomized monkeys did not. The disparity between these results might be related to experimental conditions and other variables, such as age, estrogen status, remodeling vs. modeling sites in the bone, and/or species differences. It seems that complicated masticatory movement and differences in mechanical stress (including occlusal force and food habits) also give rise to individual differences in monkeys, as shown in the high SD values.

Trabecular structural damage reflects the fragility of bone tissue more directly than does a decrease in bone volume (Recker, 1989). The significant decrease in the numbers of nodes and cortices in the ovariectomized monkeys indicates that the individual trabeculae had broken into fragments. Once the trabeculae had become fragmented and therefore decreased in number, it might have been very difficult to return to the original trabecular structure, even if increased mechanical stress were to stimulate bone formation on the remaining trabeculae. The structural model index value found in the Sham group reflected their trabecular architecture, with an abundance of plate-like trabeculae. In contrast, as a result of estrogen deficiency, those in the ovariectomized group showed a significantly higher structural model index, which was further shown by the rod-like trabeculae in their micro-CT images. The fragility of the molar alveolar bone was further evident, since significantly more pores were observed in the interseptal area of the alveolar socket in the ovariectomized group than in the Sham group. However, the pore count was not significantly different in other walls of the alveolar socket, suggesting that the interradicular septum could be the most sensitive area to be affected by estrogen deficiency. The interradicular septal area is rich in trabeculae, and it is known that estrogen acts more profoundly on trabecular-rich areas (Martin et al., 1987). No significant differences were found between the groups with respect to loss of buccal alveolar crest height and attrition. However, loss of alveolar crest height itself showed a significant correlation with attrition, indicating that aging as such seems to have the most influence on this height, apart from the effects of estrogen deficiency. Periodontal diseases may also account for this correlation, because severe periodontitis causes increased bone loss (Page and Schroeder, 1976) in the alveolar crest in elderly people.

The % of baseline bone mineral density was positively correlated with node numbers and was negatively correlated with the interseptal pore count of alveolar bone. This means that the microstructural damage found in the molar alveolar bone of the ovariectomized monkeys was linked to their spinal osteoporosis. Therefore, we must pay more attention to the alveolar bone of elderly women who are long past menopause, because they too may experience similar changes toward fragility in the alveolar bone.


   ACKNOWLEDGMENTS
 
This work was supported by grants-in-aid for scientific research from the Japan Society for the Promotion of Science (grant nos. 15209067 and 16591938). The authors thank Mr. Ian Megill for his invaluable assistance in preparing the manuscript, and also Mr. Hideshi Tsusaki, DVM, Drug Safety Research Laboratories, Shin Nippon Biomedical Laboratories, Ltd. (Kagoshima, Japan) for his support during this research.

Received September 22, 2005; Last revision September 3, 2006; Accepted September 29, 2006


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 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
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