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We investigated whether mandibular cortical measures on dental panoramic radiographs are associated with biochemical markers of bone turnover in 82 postmenopausal women. Mandibular cortical shape was significantly associated with biochemical markers and spinal BMD. Our results suggest that dentists may be able to identify postmenopausal women with low BMD by using dental panoramic radiographs.
Introduction: Recent studies suggest that mandibular inferior cortical shape and width on dental panoramic radiographs may be useful screening tools for low skeletal bone mineral density (BMD) or increased risk of osteoporotic fracture. However, little is known as to whether these measures are associated with bone turnover. We investigated relationships among dental panoramic radiographic findings, spine BMD, and biochemical markers of bone turnover in postmenopausal women.
Materials and Methods: Of 609 women who visited our clinic for BMD assessment between 1996 and 2002, 82 Japanese postmenopausal women, 46–68 years of age (54.1 ± 4.9 years), were recruited for this study. Mandibular inferior cortical shape (normal, mild/moderate erosion, severe erosion) and width were evaluated on dental panoramic radiographs. BMD at the lumbar spine (L2–L4) was measured by DXA and categorized as normal (T-score > −1.0), osteopenia (T-score, −1.0 to −2.5), or osteoporosis (T-score < −2.5). Bone turnover was estimated by serum total alkaline phosphatase (ALP) and urinary N-telopeptide cross-links of type I collagen (NTx), corrected for creatinine.
Results: The odds of low spine BMD in subjects with any cortical erosion were 3.8 (95% CI, 1.2–12.5). Mandibular cortical erosion was significantly associated with increased NTx (p < 0.001) and ALP (p < 0.05) levels. The associations of spine BMD with NTx and ALP were similar. Mandibular cortical width was significantly associated with spine BMD but not with NTx and ALP levels.
Conclusions: Our results suggest that mandibular inferior cortical shape on dental panoramic radiographs may be an indicator of bone turnover and spine BMD in postmenopausal women. Dentists may be able to identify postmenopausal women with increased risk of osteopenia and osteoporosis on routine dental panoramic radiographs.
Osteoporosis, a worldwide common disease, is characterized by low bone mass and microarchitectural deterioration of bone tissue, leading to enhanced bone fragility and a consequent increase in fracture risk.(1) Osteoporotic fractures contribute to substantial morbidity, medical costs, and mortality.(2) Identification of low bone mineral density (BMD) at any skeletal site by densitometry is a common strategy to predict future risk of osteoporotic fracture.(3) Recent studies indicate that biochemical markers of bone turnover alone, or in combination with BMD, may also be useful in predicting future bone loss and risk of fracture in elderly women.(4–8) However, it is not practical to refer all postmenopausal women for one or both of these measures when one considers the lack of cost-effectiveness and limited number of facilities and trained personnel.
Recent studies in Finland,(9) Japan,(10) and in the United Kingdom(11) offer differing opinions on the usefulness of mandibular inferior cortical shape and width on dental panoramic radiograph for identifying women with low skeletal BMD. Morphological changes of the mandibular inferior cortex in women with postmenopausal osteoporosis are similar to those of metacarpal cortical bone.(12) A recent study in the United States also suggested that mandibular cortical measures on dental panoramic radiographs were associated with an increased risk of osteoporotic fracture.(13) However, little is known about the associations of mandibular shape and width with markers of bone turnover.
The purpose of this study was to examine relationships among dental panoramic radiographic findings and spine BMD in postmenopausal women and extend prior investigations by also examining biochemical markers of bone turnover.
MATERIALS AND METHODS
Of 609 women who visited our clinic for BMD assessment between 1996 and 2002, 82 Japanese women, 46–68 years of age (54.1 ± 4.9 years), were recruited for this study. All subjects were postmenopausal (no menstruation for at least 1 year). Twenty-four women had hysterectomy, 7 had unilateral oophorectomy, and 12 had bilateral oophorectomy. Exclusion criteria were no consent given for panoramic radiographs and questionnaire, tobacco use, use of medications that affect bone metabolism, metabolic bone disease, cancers with bone metastasis, significant renal impairment, liver disorder, bone destructive lesions in the mandible, nonvertebral osteoporotic fractures, and vertebral osteoporotic fracture on X-ray at BMD assessment.
Measurements of BMD, biochemical markers, and mandibular inferior cortex
BMD at the lumbar spine (L2-L4) was measured by DXA (DPX-alpha; Lunar Co., Madison, WI, USA). The in vivo short-term precision error for spine BMD in our clinic is 1.0%. Spine BMD was categorized as normal (T-score > −1.0), osteopenia (T-score, −1.0 to −2.5), or osteoporosis (T-score < −2.5). Height and weight were measured at DXA measurement, and body mass index (BMI) was calculated as weight divided by the square of height (kg/m2).
Serum total non-bone-specific alkaline phosphatase (ALP), a marker of bone formation, was measured in 76 subjects. Urinary N-telopeptide cross-links of the type I collagen corrected for creatinine (NTx), a marker of bone resorption, was measured with the Osteomark enzyme-linked immunoassay (Osteomark Mochida Pharmaceutical Co. Ltd., Tokyo, Japan) in the morning second spot urine in all the subjects.
Dental panoramic radiographs were taken for all subjects who gave informed consent at the time of DXA measurement. All dental panoramic radiographs were obtained with AZ-3000 (Asahi Co., Kyoto, Japan) at 12 mA and 15 s; the voltage varied between 70 and 80 kV. Screens of speed group 200 (HG-M; Fuji Photo Film Co., Tokyo, Japan) and film (UR-2; Fuji Photo film Co.) were used. Mandibular cortical shape on dental panoramic radiograph was determined by observing the mandible distally from the mental foramen bilaterally and categorized into one of three groups according the method of Klemetti et al.(9) as follows (Fig. 1).
1. Normal cortex: the endosteal margin of the cortex is even and sharp on both sides
2. Mildly to moderately eroded cortex: the endosteal margin shows semilunar defects (lacunar resorption) or appears to form endosteal cortical residues
3. Severely eroded cortex: the cortical layer forms heavy endosteal cortical residues and is clearly porous
Overall agreements for intra- and interobserver performances were 92% and 82%, respectively.(10)
Measurement of mandibular cortical width was made bilaterally on the radiographs at the site of the mental foramen, according to our previous study.(10) A line parallel to the long axis of the mandible and tangential to the inferior border of the mandible was drawn. A line perpendicular to this tangent intersecting inferior border of mental foramen was constructed, along which mandibular cortical width was measured by calipers. Mean cortical width on both sides of the jaw was used in this study. The CV caused by positioning error and operator error in cortical width measure was less than 2%. Intraobserver variation in cortical width measure was 0.1 mm, which was similar to interobserver variation. Mandibular cortical width was categorized by quartile of its distribution.
Analysis of covariance, adjusting for years since menopause and BMI, was used to investigate relationships of biochemical markers of bone turnover (NTx and ALP) among cortical erosion category, spine BMD category, and cortical width quartiles. Comparisons among means of individual groups were made if the overall F value was significant at 0.05. Logistic regression analysis was used to estimate odds ratio for low spine BMD (osteopenia or osteoporosis) in women with any mandibular cortical erosion. Crude cortical width was compared among three spine BMD categories after adjustment of years since menopause and BMI. Findings of erosion (mild/moderate or severe) on dental panoramic radiographs were evaluated against the diagnosis at the spine by calculating positive predictive value (percentage of subjects with mandibular erosion who had osteopenia or osteoporosis) and negative predictive value (percentage of subjects with normal mandibular findings who had normal spine BMD). p values less than 0.05 were considered statistically significant.
Characteristics of 82 Japanese postmenopausal women are shown in Table 1 by mandibular cortical erosion categories. Four subjects with normal cortex and two with mild to moderate cortical erosion had no ALP data. Thirty-four subjects had normal BMD, 31 had osteopenia, and 17 had osteoporosis in the lumbar spine.
Table Table 1. Characteristics of Study Subjects (Mean ± SD or %)
The odds of low spine BMD (osteopenia or osteoporosis) in subjects with any cortical erosion was 3.8 (95% CI, 1.2–12.5). Subjects with osteoporosis had significantly less mandibular cortical width (mean ± SE, 3.11 ± 0.25 mm) than those with osteopenia (4.00 ± 0.15, p = 0.003) or normal spine BMD (4.30 ± 0.16, p < 0.001).
The positive predictive value of a finding of any cortical erosion on the mandibular radiograph was 83% in this group of women, and the negative predictive value was 60%. That is, based on dental panoramic radiograph, the finding of mandibular cortical erosion correctly identified a case of osteopenia/osteoporosis 83% of the time and a normal finding on the dental radiograph correctly identified normal spine BMD 60% of the time. When women with severe erosion (all of whom had osteoporosis) were excluded, the positive predictive value of a finding of mild/moderate cortical erosion on the mandibular radiograph remained high at 80%, and the negative predictive value remained at 60%.
Mandibular cortical erosion category was significantly associated with NTx (p < 0.001) and ALP (p < 0.05) levels (Figs. 2 and 3). Spine BMD category was also significantly associated with NTx (p < 0.05) and ALP (p < 0.01) levels (Figs. 4 and 5). Mild to moderate cortical erosion was associated with higher mean levels of NTx (adjusted for BMI and years postmenopausal) compared with normal mandibular cortex in the 34 women with normal spine BMD status (NTx = 79 ± 10 versus 55 ± 5 nmol BCE/mmol Cr, p = 0.04) and in the 31 women with osteopenia at the spine (NTx = 77 ± 8 versus 50 ± 7 nmol BCE/mmol Cr, p = 0.02). The mean levels of NTx in women with osteoporosis, regardless of mandibular erosion, were above 70 nmol BCE/mmol Cr.
Neither NTx nor ALP was related to mandibular cortical width (Table 2).
Table Table 2. NTx and ALP by Quartile of Mandibular Cortical Width
In this group of postmenopausal women, mandibular cortical width and the degree of mandibular cortical erosion were significantly associated with BMD status at the spine. These findings are in agreement with several previous studies.(9–11) The evaluation of mandibular cortical erosion appeared to be a better indicator of systemic bone status than cortical width, however. This is suggested by the facts that mandibular erosion was also associated with NTx levels, and the positive predictive value of a finding of erosion was high. If dental panoramic radiograph was used as the basis of identifying women with spinal osteopenia or osteoporosis in this group of women, the finding of any mandibular cortical erosion correctly identified a case of low BMD 83% of the time, and a normal finding on the dental radiograph correctly identified normal spine BMD 60% of the time. When women with severe erosion (all of whom had osteoporosis) were excluded, the positive predictive value of a finding of mild/moderate erosion on the mandibular radiograph remained high at 80%, and the negative predictive value remained at 60%.
The NTx levels, which were significantly elevated in osteoporosis, were associated with mandibular erosion but not with cortical width. However, it was interesting to note that NTx levels were already elevated in women with only mild/moderate mandibular cortical erosion compared with those with normal cortex. These elevated levels caused by mandibular erosion were seen in women with normal spine BMD and women with osteopenia. These findings suggest that mandibular cortical erosion on dental panoramic radiograph may reflect bone turnover, especially increased bone resorption, in postmenopausal women. They also suggest that NTx levels may be useful information in addition to mandibular erosion status to identify women early, before developing osteoporosis.
Subjects with osteoporosis had higher NTx and ALP levels than those with normal BMD or osteopenia. This finding agrees with previous studies.(8,14,15) Bone resorption rate after menopause is one of the important determinants of low BMD or osteoporosis in postmenopausal women.(16) There was no significant difference in ALP levels between women with normal and mildly to moderately eroded cortex, although a significant difference in ALP was observed between subjects with normal and severely eroded cortex (all osteoporotic). This discrepancy in the associations of NTx and ALP with cortical erosion may be because of urinary NTx being a more sensitive marker of bone turnover than serum total ALP.
Mandibular cortical width was significantly associated with spine BMD category but not with NTx and ALP levels. These results imply the possibility that cortical width may not reflect increased bone turnover after menopause but rather peak bone mass in younger age. Horner et al. recently report that a thinning of the mandibular cortex in a normal perimenopausal female was associated with low skeletal BMD.(17) An investigation whether cortical width reflects peak bone mass in young women is in progress.
Significant correlation was found between BMD of the spine and hip with DXA and cortical BMD of the mandible with quantitative computed tomography (QCT) in Finnish postmenopausal women.(18) We also found significant correlation between BMD of the spine with QCT and cortical BMD of the mandible with QCT in Japanese postmenopausal women.(19) However, there was no consistent finding between skeletal BMD and trabecular BMD of the mandible between both studies. One of possible causes of this controversy is that trabecular bone of the mandible may be easily influenced by dental infection. That is why we selected the cortical portion of the mandible as an indicator of bone metabolism, although it is well known that trabecular bone of the general skeletons is more sensitive against bone metabolic change than cortical bone.
It is likely that decreased mechanical stresses in occlusion caused by tooth loss may influence mandibular cortical findings. It is still unknown whether tooth loss largely influences on mandibular inferior cortex, although Elovic et al. found decreased trabecular bone area fraction of the mandible in ovariectomized rats after loss of mechanical stress.(20) In our previous study,(21) mandibular inferior cortical width started to decrease after 50 years of age, whereas number of teeth remaining started to decrease after 60 years of age in women. Mandibular cortical width became constant after 70 years of age, but number of teeth remaining continued to decrease. If tooth loss largely influences on mandibular inferior cortex, mandibular cortical width would continue to decrease after 70 years of age.
This study has limitations. All subjects of this study were not healthy volunteers, but were patients who visited our clinic for BMD assessment. Our subjects therefore are not representative of normal Japanese postmenopausal women. The small sample size and use of non-bone-specific ALP also limit the interpretation of our findings. Further investigations with other markers of bone formation, such as bone-specific ALP and osteocalcin, in a large population would be necessary to confirm our findings.
In conclusion, mandibular inferior cortical shape on dental panoramic radiographs was associated with biochemical markers of bone turnover as well as spine BMD, and was able to correctly identify more than 80% of cases of spinal osteoporosis. Combined cortical width and erosion findings need to be investigated in future studies to determine if prediction of osteoporotic fracture risk can be improved with multiple or serial screening tools. Our present results do suggest that because dental panoramic radiographs can be routinely taken as part of general dental practice, the cortical findings on such radiographs may provide dentists with a means to identify patients with undetected low BMD and refer them to medical professionals for bone densitometry.
This study was supported by a grant-in-aid for scientific research from the Japan Society for the Promotion of Science (14571786).