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RESEARCH |
ar*Selcuk Universitesi Dis Hekimligi Fakultesi, Oral Diagnoz ve Radyoloji Anabilim Dali, 42079 Konya Turkey
*Correspondence to: Füsun Ya
ar, Selcuk Universitesi Dis Hekimligi Fakultesi, Oral Diagnoz ve Radyoloji Anabilim Dali, 42079 Konya Turkey; E-mail: drfyasar{at}hotmail.com
Received 1 October 2004; revised 12 April 2005; accepted 12 May 2005
| Abstract |
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Methods: Forty-eight post-menopausal women between the ages of 40 years and 64 years were evaluated. Mandibular indices and the number of mandibular teeth were measured and evaluated from panoramic radiographs and fractal dimension was calculated from the direct digital periapical radiographs of the mandibular premolar-molar region in box-counting method. Weight, height, menopausal status and age of the patients were recorded by questionnaire. Bone mineral densities of the patients were measured with dual energy X-ray absorptiometry.
Results: In this study there were no statistically significant differences between the osteoporotic and non-osteoporotic patients for cortical width, panoramic mandibular index, alveolar crest resorption degree, fractal dimension and the number of mandibular teeth, but there was a difference for cortical index. Binary logistic regression analyses demonstrated that age (P=0.015) was an important risk factor for osteoporosis.
Conclusion: The results of this study demonstrated that osteoporotic patients were more likely to have altered inferior cortex morphology than non-osteoporotic patients and age is an important risk factor for osteoporosis.
Keywords: osteoporosis;; panoramic radiography;; digital radiography;; fractal dimension
| Introduction |
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Fractal analysis is a mathematical technique that can aid in the quantification of complex structures.17 In general, the higher the dimension, the more complex the shape.17,18 This technique has been evaluated with varying degrees of success in different imaging modalities such as plain film radiography,10,19 mammography,20,21 CT and MRI.22 Bone is a natural material which is designed to resist gravitational and mechanical forces and thus, has an internal structure that is highly oriented (anisotropic).23 Various investigators have evaluated this anisotropic structure of trabecular bone on dental radiographs, by using different FD methods in order to discriminate individuals with osteoporosis from those without osteoporosis. While some reported a decrease in FD,11 others reported an increase in FD in osteoporotic patients.15,16
The aims of this study were to evaluate the relationship between various oral signs and osteoporosis and to develop an equation that might be applied in assessing the probability of this relationship existing in certain patients.
| Materials and methods |
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For the examination of the bone mineral density status of the patients, anteroposterior dual X-ray absorptiometry (DXA) scans were performed using a Hologic QDR-4500 bone densitometer (Hologic Inc., Waltham, MA). The patients were classified as normal (T-score>1.0) or osteoporotic (T-score of <2.5) based on the BMD data of the lumbar spine.24 Osteopenic patients were not included the study. In order to determine the presence of thoracic spine fractures, lateral chest radiographs were evaluated by a radiologist according to the radiographic criteria of Pacifici et al.25
The spinal height of the anterior, central, and posterior third at each vertebra from the 5th thoracic spine to 12th thoracic spine was measured with a vernier calliper. Compression fracture was defined as a loss of posterior height greater than 15% compared with the mean of the posterior height of the nearest (inferior and superior) intact vertebrae. When the posterior height was within the normal range, wedging and biconcave fractures were defined as a loss of anterior and central height greater than 20% compared with the posterior height of the same vertebra. The patients who did not have thoracic fractures were included the study.
The data regarding menopausal status, age, weight and height were obtained by questionnaire. The patients did not have menstruation for at least the last year. The body mass index (BMI) was computed as weight divided by the square of height (BMI; kg m2). The number of mandibular teeth, excluding third molars was recorded from panoramic radiographs. Root remnants were counted as teeth except the ones which were totally imbedded in bone. The time and cause of tooth loss were unknown.
One panoramic radiograph (2002 CC Proline; PlanMeca, Helsinki, Finland) and two direct digital periapical radiographs in bisecting angle technique were exposed from the mandibular premolar-molar region. An intraoral X-ray unit (Trophy CCX Digital Periapical X-ray machine, France) and Dimaxis (1.52) (PlanMeca, Helsinki, Finland) intraoral computed radiography system were used to capture the images. Direct digital radiographs were exposed with 65 kV, 10 mA and 2.5 mm equivalent total filtration. Direct digital and panoramic radiographs were clinically acceptable.
ImageJ (1.28)26 was used for image processing and analysis.
Morphometric measurements
All measurements were made in millimetres by the same investigator with a calliper and plastic millimetre ruler. The same viewing box, magnifier (x2), calliper and ruler were used all in the measurements. When the mental foramen was visible bilaterally, the measurements were done bilaterally and their mean was used as the exposure measure in the analysis; when only one foramen was visible, the measurements were done only on that side. To evaluate the intraexaminer reliability, 48 panoramic radiographs were re-analysed for CW, PMI, M/M ratio, CI and the number of mandibular teeth with a period of 6 months interval by the same examiner. The information on age and BMD status of the patients was blinded to the examiner in order to eliminate information bias.
The inferior edge of the mental foramen was traced, and 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 the inferior border of the mental foramen was constructed. CW, PMI and M/M ratio were measured along this line (Figure 1
).
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PMI is the ratio of the thickness of the mandibular cortex to the distance between the mental foramen and the inferior mandibular cortex.7 The thickness of the cortex was divided by the distance from the inferior margin of the mental foramen to the inferior border of the mandible (a/b).
The total mandibular height was divided by the height from the centre of the mental foramen to the inferior border of the mandible to obtain the M/M ratio. This was an index of the mandibular alveolar bone resorption degree (M/M ratio) (d/c).8
In order to evaluate the CI of the mandible, the morphology of mandibular inferior cortex was visually examined distally from the mental foramen bilaterally using Klemetti's classification.9
Fractal dimension analysis
First, the 16-bit direct digital radiographs were converted to 8-bit images with ImageJ (1.28).26 Rectangular regions of interest (ROI), whose dimensions were the same (23 x 155 pixels) for all radiographs, were created between second premolar and first molar teeth (Figure 2a
). ROIs were created distally to mental foramen in edentate patients (Figure 2b
). When creating ROIs, great care was shown not to include lamina dura, periodontal ligament space and anatomical structures and they were created apically as far as possible from the crestal bone, because it has been stated that beyond 2.5 mm there is no effect of bacterial plaque on alveolar process bone.27 Digital images were segmented to binary image in a similar way described by White and Rudolph.5,14 To remove large scale variations in brightness on the image, the ROI was blurred through use of a Gaussian filter with radius of 35 pixels (Figure 2c
). The causes of these variations are differences in thickness of the object or the presence of partially overlapping soft tissue. This step removed all fine-scale and medium-scale structure and retained only large variations in density (low-pass filtering). The resulting heavily blurred image was then subtracted from the original, and 128 was added to the result at each pixel location. This generated an image with a mean value of 128, regardless of the initial intensity of the image. The idea was that individual variations in this image (brightness levels) then reflect particular types of features, in this case trabeculae and marrow spaces. The image was then made binary, thresholding on a brightness value of 128 and thus segmenting the image into components that visually (radiographically) approximate the trabeculae and marrow (Figure 2d
). The image of the trabeculae was then inverted to make the trabeculae black and then boundary description was applied to the binary image and outlines of the trabeculae were obtained (Figure 2e
). FD was calculated in box counting method with ImageJ (1.28).26 As two direct digital images were exposed from both right and left sides of the mandible in the premolar-molar region, two separate FD values were calculated. The mean of these two values was used in the study.
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) index was used as a measure of intraexaminer agreement for CI evaluation and chi-squared test was performed to evaluate the relation between osteoporosis and CI. Kolmogorov-Smirnov and Levene's tests were used, respectively, to check for the normality and homogeneity of the data. Independent samples t-test was used to evaluate the differences of oral signs (CW, PMI, M/M ratio, the number of mandibular teeth present and FD, age and BMI), in patients with osteoporosis from those without osteoporosis. A probability equation for osteoporosis was calculated by applying binary logistic regression analysis to the age, oral signs and BMI. SPSS 10.0 for Windows (SPSS, Inc., Chicago, IL) was used in the statistical analysis. | Results |
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Eight different variables were evaluated in this study for their relation with osteoporosis. Seven of the variables were continuous (CW, PMI, M/M ratio, FD, the number of mandibular teeth present, age and BMI) and one of them, CI, was categorical data. Table 1
shows the mean values and standard deviations of the continuous variables for the osteoporotic and non-osteoporotic groups. Normal distribution of the data was controlled with Kolmogorov-Smirnov test (Table 1
) and homogeneity of variances was checked with the Levene's Test for equality of variances (Table 2
). Independent samples t-test was used in comparing the differences of CW, PMI, M/M ratio, FD, the number of teeth, age and BMI for each BMD category (osteoporotic and non-osteoporotic) (Table 2
). CW, PMI, M/M ratio, and the number of mandibular teeth were evaluated twice by one of the investigators, and the mean of the two evaluations was used in the independent samples t-test. Bonferroni criteria with significance set at P<0.007 level was used in the independent samples t-test (Table 2
). None of the parameters evaluated were found to differ significantly between the osteoporotic and non-osteoporotic group.
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Weighted Kappa statistic was used to evaluate the agreement of CI for both observations (Table 4
). Weighted
was found as 0.85 and there was almost perfect agreement between the observations for 99% confidence interval. Interpretation of the Kappa statistics was quoted from the guidelines of Landis and Koch: Less than 0.00 poor agreement, 0.000.20 slight agreement, 0.210.40 fair agreement, 0.410.60 moderate agreement, 0.610.80 substantial agreement and 0.811 almost perfect agreement.29 The frequency distribution of osteoporosis for CI classification in two observations and the Pearson chi-squared test results are shown in Table 5
(P=0.002 for the first observation and P=0.001 for the second observation with 99% confidence interval). There was a statistically significant difference between the CI classifications in osteoporotic and non-osteoporotic patients in both observations. As there was a high agreement between the first and second observations of CI, the two tables were combined (Table 6
). Later, risk ratio for osteoporosis was calculated for three CI classifications. There was a significant difference in all CI categories with 99% confidence interval (Table 7
). The risk of osteoporosis in CI 3 category was 1/0.079 (12.6) times more than CI 2, the risk of osteoporosis in CI 2 category was 1/0.083 (12) times more than CI 1, and the risk of osteoporosis in CI 3 category was 1/0.007 (142.8) times more than CI 1 (Table 8
).
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Pv=1/(1+ez)
Pv is the probability value. The numerical value was obtained from the B estimates from Table 9
. Frequently our interest is to use the logistic model to predict the outcome for a new subject. When the age of a new patient is written in the equation, a Z value can be obtained and then P can be calculated. If P<0.50 then Pv =0 and it can be said that it is very likely that this person is osteoporotic and if P
0.50; Pv =1 and the subject is more likely to be non-osteoporotic. The overall accuracy of this model to predict subjects having osteoporosis was 99% (Table 10
).
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| Discussion |
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Post-menopausal women constitute more than 15% of the population in developed countries whereas this rate is 58% in less developed regions of the world.33 By 2030, the world population of menopausal and post-menopausal women is expected to increase to 1.2 billion, with 47 million new cases each year.33,34 Osteoporosis and fractures are more difficult and costly to treat than to prevent. Therefore, several health care interventions have been proposed to identify those people who may be at risk and who could benefit from preventive interventions.35
CW, PMI, M/M ratio, CI, the number of teeth present and FD are the parameters evaluated in various studies for detecting their effectiveness in screening osteoporosis. Some of the investigators reported that they could be used in screening osteoporosis810,14,16,3638 but others reported that there was no relation between these parameters and osteoporosis.39,40 Kingsmill and Boyde41 studied the variability in the anatomy of mandibles of differing ages and differing stages of tooth loss. They studied the cross sectional slices of the dry mandibles and measured CW from the radiographs of those slices. They concluded that unlike other bones, the mandible may show an increase in apparent density with age, implying that the mandible may not be suitable for evaluating osteoporotic status and they found no relationship between radiographic cortical thickness and age. Taguchi et al42 studied the mandibular bone density of women who were in different post-menopausal stages and reported that BMD of the mandibular cortical bone had greater correlation (r=0.73) with lumbar trabecular bone mineral density in recent post-menopausal group than in long-term post-menopausal group (r=0.46). Kingsmill and Boyde's result about density is supporting the results of Taguchi et al.42 In this study we were unable to show any relation between osteoporosis and the oral signs such as CW, PMI, M/M ratio, number of teeth present and FD.
The age at menopause is between 45 years and 55 years all over the world. Cessation of menses between age 40 years and 45 years has been defined as early menopause.43,44 13 patients (27.08%) participating this study were below 45 years. The mean age of the patients participating in this study was relatively young (osteoporotic patients: 52.11 years, non-osteoporotic patients: 48.38 years). Besides this, none of the patients in this study had osteoporotic fractures. These two factors might be the limitations of the study and also they might be the reason of not finding an association between the oral signs, except CI, and osteoporosis. The other reason might be the BMI of the women. Unchangeable causes of increased bone loss are increasing age, family history of osteoporosis, being female, being in menopause, and being thin.35 The World Health Organization45 classified BMI as follows:
Normal weight 18.5
BMI< 25
overweight 25
BMI<30
obese BMI
30
It was reported that BMI significantly correlates with BMD and people with a BMI of 2025 kg m2 have a higher rate of bone loss than those who are heavier.35 The mean BMI of the women included in this study was classified as overweight according to WHO criteria (mean BMI: 27.78; SD: 4.32).
Various investigators reported different levels of repeatability for CW, PMI, M/M ratio and CI.46,47 Generally authors used correlation coefficients in describing agreement between two quantitative variables but high correlation does not imply good agreement.48 Bland and Altman introduced the Bland and Altman plot to describe agreement between two quantitative measurements.48 There is no P-value available to describe this agreement but rather a quality control concept. The difference of the paired two measurements is plotted against the mean of the two measurements and they recommended that 95% of the data points should lie within the ±1.96 (approximately ±2) standard deviation of the mean difference. In this study, the strength of the relationship between repeated measurements was assessed by Pearson's correlation coefficient and the repeatability was assessed with the method of Bland and Altman.28 Making measurements from panoramic radiographs is associated with intrinsic errors and observer variability. There is a limitation in the repeatability of panoramic radiographic measurements.49,50 The number of mandibular teeth had the highest repeatability (r=1; SD: 0,000), M/M ratio (r=0.864; coefficient of repeatability: 0.65), PMI (r=0.871; coefficient of repeatability: 0.12) were following it in decreasing order and cortical width (r=0.869; coefficient of repeatability: 1.17) had the worst repeatability. Obtaining high agreement in measuring gross structures, such as counting teeth, is easier than obtaining high agreement in measuring in millimetres, because in these measurements, the visual perception of human eye and brain should also be taken into consideration. The linear measurements have greater observer dependency and another factor is to measure X-ray films by hand to better than the nearest 0.5 mm is not justifiable.41 To obtain the same results in repeated observations, the borders of the mental foramen should be determined correctly and later the necessary drawings should be made and finally these configurations should coincide with each other. That is, as the operations that must be performed for measuring an index increases, the measurement error would also increase; so it might be more effective to use simple indexes to reduce measurement error and increase agreement between the repeated measurements. The repeatability of CI was evaluated by weighted Kappa statistic. Kappa does not take into account the degree of disagreement between observers and all disagreement is treated equally as total disagreement. Therefore when the categories are ordered, it is preferable to use weighted Kappa.29 There was a very good agreement (0.851) between the two observations. This finding was unsurprising because CI is relatively simple index and it requires no measurements.
One of the most commonly studied parameters of mandibular bone in relation to osteoporosis is the porosity of the mandibular cortical bone (CI). Some of the investigators have found an association between CI and osteoporosis,9,37,38,46,47 but Drozdzowska et al40 reported that there was no relationship between osteoporosis and CI. In this study, the best performing parameter in discriminating the osteoporotic patients from non-osteoporotics was CI with a very good agreement in repeatability (0.851). The risk of osteoporosis in CI 3 category was 12.6 times more than CI 2, the risk of osteoporosis in CI 2 category was 12 times more than CI 1 and the risk of osteoporosis in CI 3 category was 142.8 times more than CI 1 with 95% confidence interval. For the other parameters, some measurements must be performed and some calculations are necessary, and as it was stated before, the complexity of an index may increase its measurement error and decrease its repeatability. CI is a simple classification based on the appearance of the lower border of mandibular cortex.13 In this study, CI showed a statistically significant difference in the osteoporotic and non-osteoporotic patients even in the younger age range and in non-fractured patients.
The structure of the trabecular bone has been analysed in relation to osteoporosis with FD in many studies and it has provided conflicting results. While some authors stated that FD decreases in osteoporosis,22,51 others reported an increase.10,15 Generally digitized forms of conventional radiographs were used in the other studies but in this study direct digital images were used. Each imaging modality may have its own non-linear artefacts such as sampling frequency and noise and this may have an affect on the results of FD.23 Geraets and van der Stelt23 have stated that most reports based on radiographs in vivo find an association between osteoporosis and increased values of FD.10,15 In this study, the mean FD in osteoporotic patients was 1.40 and it was 1.38 in non-osteoporotic patients but there was no statistically significant difference between the two groups. Relatively young mean age and high BMI might have an effect on this. The other reasons might be the method and the region that was used to calculate FD. In this study, FD was calculated from mandibular bone but BMD was measured from the lumbar spine of the patients. Maybe it would be more accurate to compare the FD and the BMD of the same bone. Osteoporosis might not be affecting all bones at the same time with the same severity.
In conclusion, the results of this study demonstrated that CW, PMI, M/M ratio, number of mandibular teeth present and FD do not lend themselves to the diagnosis of osteoporosis. CI, which has a relatively easier application, is a useful oral sign in screening the patients for osteoporosis and it might be used as a subsidiary diagnostic tool in referring the patients to bone densitometry clinics.
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