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1 NUMBER 1 OF 1 AUTHOR QUERIES DATE 5/22/2013 JOB NAME MAJ ARTICLE QUERIES FOR AUTHORS Mansour et al THIS QUERY FORM MUST BE RETURNED WITH ALL PROOFS FOR CORRECTIONS AU1) Please provide manufacturer details (city, state [if USA], and country [other than USA]) for the manufacturer Kodak Dental Imaging Soft Ware KDIS. AU2) Please update the reference 1. AU3) Please provide the accessed date for reference 2. AU4) Please note that as per the journal style, if there are more than 3 authors, the first 3 author names are listed followed by et al. If the author group consists of 3 authors or fewer, all author names should be listed. Therefore, in reference 25; please list all names for up to 3 authors. For more than 3 authors, use et al. after the first 3 authors.

2 CLINICAL INVESTIGATION Panoramic Radiomorphometric Indices as Reliable Parameters in Predicting Osteoporosis Soad Mansour, PhD, Ali S.T. AlGhamdi, BDS, MS, FRCD(C), Fawad Javed, PhD, Hazem Marzouk, PhD and Emad A. Khan, PhD Abstract: Background: The purpose was to evaluate the significance of panoramic radiomorphometric indices (mandibular cortical index [MCI], mental index [MI] and panoramic mandibular index [PMI]) as useful tools for identifying osteoporosis. Methods: One hundred healthy women aged $ 30 years were included. Digital panoramic images and bone mineral density (BMD) of the lumbar spines were recorded. Radiomorphometric indices (MCI, MI and PMI) were measured and categorized. Results: Interobserver agreements were kappa fortheMCIandalpha and for the PMI and MI, respectively. The indices MI, PMI and BMD showed a statistically significant positive correlation with the t score (r , 0.36 and 0.96, respectively). The MI showed a statistically significant positive correlation with the PMI (r ). Sensitivity, specificity and diagnostic accuracy of the MI at a cutoff point of 4.5 mm were 76.9%, 54.1% and 63%, respectively, whereas for the MCI were 66.7%, 75.4% and 72%, respectively. Conclusions: Panoramic indices (MI, PMI and MCI) were positively correlated with the t score and BMD of the lumbar spines. The MCI was found to be the most reproducible index. Key Indexing Terms: Panoramic radiograph; Radiomorphometric indices; Bone mineral density; Osteoporosis; Lumbar spines. [Am J Med Sci 2013;0(0):1 6.] Osteoporosis is a skeletal disorder characterized by bone architectural disorientation and low bone mineral density (BMD) and micro-architectural deterioration, thereby resulting in increased bone fragility and/or susceptibility to fracture. 1 According to the Surgeon General of the United States, nearly 50% of all American citizens older than 50 years will be at a greater risk for fractures from osteoporosis and low BMD when compared with younger Americans. 2 A direct association between osteoporosis and architectural alterations in the inferior border of the mandible has been reported. 3,4 In addition, patients with a history of osteoporotic fractures have been shown to have increased resorption and thinning of the mandibular lower cortex when compared with their respective healthy controls. 5 Nevertheless, a large number of populations with increased risk of osteoporotic fractures remain underdiagnosed and/or untreated. 6 From the Department of Oral Basic and Clinical Sciences (SM, EAK) and Postgraduate Studies and Scientific Research (ASTA), Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia; and Engineer Abdullah Bugshan Research Chair for Growth Factors and Bone Regeneration, College of Applied Medical Sciences, (FJ) and Department of Diagnostic Oral Sciences Department, Faculty of Dentistry (HM), King Saud University, Riyadh, Saudi Arabia. Submitted March 7, 2013; accepted in revised form April 15, This study was supported by the Deanship of Scientific Research at King Abdulaziz University, Jeddah, Saudi Arabia Grant 430/ The authors have no financial or other conflicts of interest to disclose. Correspondence: Ali S.T. AlGhamdi, BDS, MS, FRCD(C), Postgraduate Studies and Scientific Research, Faculty of Dentistry, King Abdulaziz University, P.O. Box , Jeddah 21351, Saudi Arabia ( asalghamdi2@kau.edu.sa). Panoramic radiographs are routinely taken for the assessment of oral diseases including dental caries and periodontal disease 7 9 ; however, other features of panoramic radiography such as the cortical width below the mental foramen (or mental index [MI]) may also be a useful tool in identifying patients with undetected low skeletal BMD. 10,11 Studies 12,13 have reported that patients with a thin MI of 3 mm or less may have latent osteoporosis and that a cortical width of 4.5 mm or less may be considered as a high risk indicator of osteoporosis. Furthermore, results by Taguchi et al 13 showed that the diagnostic performance of dental panoramic radiography measures for identifying postmenopausal women with suspected spinal osteoporosis was similar to that of the osteoporosis self-assessment tool. From these results, panoramic radiography seems to be a cost-effective means for screening latent osteoporosis in undiagnosed individuals. In this investigation, we hypothesized that panoramic radiomorphometric indices (mandibular cortical index [MCI], MI and panoramic mandibular index [PMI]) are useful tools for identifying osteoporosis. The aim of this study was to evaluate the significance of panoramic radiomorphometric indices (MCI, MI and PMI) in identifying osteoporosis. MATERIALS AND METHODS Ethical Guidelines The study design was revised and approved by the Research Ethics Committee of the Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia. An informed consent was obtained from all individuals. It was mandatory or all study participants to have read and signed the consent form before being included in this study. Exclusion Criteria The following exclusion criteria were imposed: (1) history of systemic disorders such as diabetes and/or renal disorders, (2) hormonal replacement therapy, (3) corticosteroid use within 3 months, (4) traumatic fracture, (5) history of hysterectomy and (6) habitual smoking and/or alcohol consumption. Study Participants One hundred self-reported medically healthy females with a mean age of years (aged between 30 and 74.2 years) were included. These individuals were recruited from the Department of Oral and Maxillofacial Radiology, College of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia. Questionnaire Demographic data were collected using a self-completed questionnaire. Patients were also inquired about history of systemic diseases (including diabetes and renal disorders), drug The American Journal of the Medical Sciences Volume 0, Number 0, Month

3 Mansour et al Imaging Software KDIS ) after correcting the magnification factor. AU1 FIGURE 1. A cropped digital panoramic radiograph showing measurement lines. Line A: length between inferior cortex of mental foramen and outer cortex of mandible. Line B: length of inferior border at mental foramen. usage, alcohol/tobacco habits and bone/joint aches and menopausal status. Bone Mineral Density BMD (g/cm 2 ) measurements of lumbar spines L2 to L4 were performed using dual-energy x-ray absorptiometry (DXA) 14 (GE Lunar, Corp, Madison, WI). Height and weight were measured at the time of dual-energy x-ray absorptiometry testing. The study individuals were categorized into 3 skeletal mineral density groups based on World Health Organization criteria: normal (t score $ 21); osteopenic (t score 21 to 22.5) and osteoporotic (t score # 22.5). Digital Panoramic Radiography Digital panoramic radiographs were taken by a calibrated single operator using an Orthopantomograph 200 D (Instrumentarium Dental, Inc, Milwaukee, WI) with exposure settings of 57 to 85 peak kv and tube current of 12 to 16 ma. The position of the patient s head was standardized following the manufacturing instructions. All radiographs were assessed so that only the high-quality and correctly positioned panoramas were included. Linear measurements were made using an analytical software (Clini view 8.1; Kodak Dental Measurement of Panoramic Indices Panoramic indices (MI, PMI and MCI) were assessed twice by 2 calibrated oral radiologists within a 1-month interval wherein the data of the 1st session were masked at the 2nd session. By this, a general consensus was reached. MI, PMI and MCI The MI was measured as described elsewhere. 11 In summary, a line was drawn parallel and tangent to the inferior border of the mandible ( Figure 1). Line 1 was constructed perpendicular to the tangent, passing through the middle of the inferior cortical margin of the mental foramen. The cortical width was then measured along this perpendicular line (represented as line 2). The mean cortical width of both sides was used in this study. Osteoporosis was defined by MI cutoff points of #3 mm and #4.5 mm. The PMI was measured as the ratio between the MI and the distance between the inferior margin of the mental foramen and the inferior border of the mandibular cortex (line 2/line 1). To our knowledge from indexed literature, there is no standard threshold for a PMI value. In this regard, the mean value derived from this study was used for statistical analysis. The MCI was determined as C1 (normal), C2 (osteopenic) or C3 (osteoporotic) by examining the inferior cortex of the mandible from the mental foramen to the antegonial area on both sides. 15 The most deteriorated cortex was adopted as the diagnosis of the cortical shape. Statistical Analysis Statistical analysis was performed using a software program (SPSS, Inc, Chicago, IL). The Pearson s coefficient was used to determine the significant correlation between different variables. The Student t test was used to compare between dentate or partially dentate cases and the other variables, except for t score data, in which case, the Mann-Whitney U test was used because of the nonparametric distribution of the t score data. One-way analysis of variance (ANOVA) was used to compare between MCI classes, except for the t score, wherein the Kruskal- Wallis test was used. Tukey s post-hoc test was used for pairwise comparison between the means when the ANOVA test was significant. The Mann-Whitney U test was used for pairwise comparisons between groups for t score results. F1 FIGURE 2. Scatter diagram showing positive correlation between t score and MI. MI, mental index. 2 Volume 0, Number 0, Month 2013

4 Panoramic Indices and Osteoporosis FIGURE 3. Scatter diagram showing positive correlation between t score and PMI. PMI, panoramic mandibular index. F2 F3 The interobserver agreement for numerical data was performed with Cronbach s alpha reliability coefficient. The kappa statistic was used to measure interobserver agreement for qualitative data. The x 2 test was used to measure the association between the dentition and MCI. The level of significance was set at P, RESULTS Lumbar Spine Bone Density The mean t score of lumbar spine bone density was , with a minimum of and a maximum of Sixty-one percent of the study sample had a t score of $21 (classified as normal); 34% had a t score of 21 and $22.5 (classified as osteopenic); and 5% had a t score of #2.5, indicating osteoporosis. Radiomorphometric Indices The mean MI and PMI were (range, mm) and (range, mm), respectively. According to the MCI, 59 subjects (59%) were C1, 38 (38%) were C2 and 3 (3%) were C3. In addition, the dental statuses of the subjects were 84 (84%) dentate, 1 (1%) edentulous and 15 (15%) partially edentulous. Correlation Between the t Score and Each of BMD, MI and PMI Pearson s correlation coefficient showed a statistically significant positive correlation between the t score and each of BMD, MI and PMI (r , 0.47 and 0.36, respectively) (Figures 2 and 3). The BMD showed a statistically significant positive correlation with MI and PMI (r and 0.41, respectively). The MI also showed a statistically significant positive correlation with PMI (r ), as shown in Table 1. Mandibular Cortical Index The significant differences between the MCI (C1, C2 and C3) and other variables are presented in Table 2. The C1 cases T2 showed the statistically significant highest mean t score (or lowest negative value) followed by C2, whereas the C3 cases showed the statistically significant lowest mean t score, with a statistically significant difference between them (P ) (Figure 4). F4 The C1 cases showed the highest mean BMD, with a statistically significant difference compared with the C2 and C3 cases (P ). However, there was no statistically significant difference between the C2 and C3 cases showing the lowest means BMD. For the MI, there was no statistically significant difference between the C1 and C2 cases, which showed the statistically significant highest mean MI, whereas the C3 cases showed the statistically significant lowest mean MI, with a significant difference between C1 andc2(p50.001). C1 cases showed statistically significant highest mean PMI, with a statistically significant difference between the C2 and C3 cases (P ), whereas there was no statistically significant difference between the C2 and C3 cases, which showed the statistically significant lowest mean PMI. The dental status data of the study subjects and different variables are presented in Table 3. The edentulous case was T3 T1 TABLE 1. Results of Pearson s correlation coefficient for correlating between different variables t score BMD MI PMI t score Pearson s correlation P,0.001 a,0.001 a,0.001 a BMD Pearson s correlation P,0.001 a,0.001 a MI Pearson s correlation P,0.001 a a Significant at P, BMD, bone mineral density; MI, mental index; PMI, panoramic mandibular index. Ó 2013 Lippincott Williams & Wilkins 3

5 Mansour et al TABLE 2. ANOVA and Kruskal-Wallis results for comparing between different variables in cases classified as C1, C2 and C3 C1 C2 C3 t score (mean 6 SD) BMD (mean 6 SD) MI (mean 6 SD) PMI (mean 6 SD) Mean SD Mean SD Mean SD P a b c 0.002* a b b,0.001* a a b 0.001* a b b 0.010* * Significant at P, Means with different letters are statistically significantly different. ANOVA, analysis of variance; SD, standard deviation. FIGURE 4. Bar chart showing comparison between t scores with different MCI classes. MCI, mandibular cortical index. merged with the partially dentate group for statistical purposes. There was no statistically significant difference between the dentate and partially dentate cases regarding all variables (P $ 0.05). Interobserver Agreement, Sensitivity, Specificity and Diagnostic Accuracy Interobserver agreement of the 3 radiomorphometric indices was found to be the highest for MCI (kappa 5 TABLE 3. Results of Mann-Whitney U test, Student t test and x 2 test for comparison between different variables in dentate and partially dentate cases Dentate Partially dentate P t score (mean 6 SD) BMD (mean 6 SD) MI (mean 6 SD) PMI (mean 6 SD) MCI (frequency, %) C1 53 (63.1) 6 (37.5) C2 29 (34.5) 9 (56.3) C3 2 (2.4) 1 (6.3) Significant at P, BMD, bone mineral density; MI, mental index; PMI, panoramic mandibular index; MCI, mandibular cortical index ) and PMI (alpha ), whereas MI showed strong agreement (alpha ). The sensitivity and specificity of the MI were calculated. When we used an MI with a cutoff point of 3 mm, individuals with an MI. 3mm were considered normal. Sensitivity, specificity and diagnostic accuracy were found to be 10.3%, 98.4% and 64%, respectively. However, when the MI cutoff point was changed to 4.5 mm, all individuals. 4.5 mm were considered normal. Sensitivity, specificity and diagnostic accuracy were found to be 76.9%, 54.1% and 63%, respectively ( Table 4). The sensitivity, specificity and diagnostic accuracy of the MCI were found to be 66.7%, 75.4% and 72%, respectively. DISCUSSION The results demonstrated that panoramic indices (MI, PMI and MCI) are positively correlated with the t score and BMD of the lumbar spines. Therefore, these indices could serve as simple and useful tools to assess latent osteoporosis. Our results are in accordance with previous studies, which reported that dental panoramic radiographs can be useful for detecting those at high risk for osteoporotic fractures. However, controversial results have also been reported. 21 Studies 16,17,22 have focused primarily on radiomorphometric measurements with reference to gender and age; however, only a limited number of studies 5,23 25 have evaluated changes in MCI, MI or PMI. The results of this study revealed that subjects classified as C3 on the MCI showed significantly T4 4 Volume 0, Number 0, Month 2013

6 Panoramic Indices and Osteoporosis TABLE 4. Results of sensitivity, specificity and diagnostic accuracy of MI using 3 and 4.5 mm as cutoff points t score t score MI, 3 mm Osteoporotic Normal Total MI, 4.5 mm Osteoporotic Normal Total Osteoporotic 4 (True +ve) 1 (False +ve) 5 Osteoporotic 30 (True +ve) 28 (False +ve) 58 Normal 35 (False ve) 60 (True ve) 95 Normal 9 (False ve) 33 (True ve) 42 Total Total MI, mental index. lowest mean t score and BMD, followed by C2 and C1 cases. This result could be attributed to the radiographic porosity of the mandibular cortex that have been detected in C3 cases and resulted in such low records. This reflects that the MCI is helpful in identifying female patients with low BMD. These findings are in agreement with the other studies. 3,12,15,16,26 28 Furthermore, our results demonstrated that the C3 group showed the lowest MI, with a statistically significant difference from C1 and C2. Similarly, C2 and C3 groups showed significantly lowest PMI when compared with C1. Thus, MCI was found to be a fairly good index in detecting osteoporosis, and it can be used as a useful screening tool. In our results, the excellent harmony between interobserver interpretations of data reflects that oral radiologists may be able to perform a more accurate diagnosis than other general clinical dental practitioners. Studies 5,16,22 have assessed the sensitivity, specificity and diagnostic accuracy of MCIs. These studies 5,16,22 concluded that measurement of MCI is a reliable method of identifying osteoporosis. Our results showed values of 66.7%, 75.4% and 72%, respectively, when compared with the study by Taguchi. 29 It is generally agreed that tests with close values of sensitivity and specificity are considered reliable, a finding that is supported by our results. The results of this study demonstrated no statistically significant difference between the dental status of the patients and their t score, BMD, MI, PMI or MCI. This could possibly be explained by the fact that the basal bone remains unaffected following exodontia when compared with alveolar bone, which ultimately resorbs after tooth extraction. This is in accordance with other studies 11,23,30 ; however, Gulsahi et al 24 and Sahyoun et al 31 concluded that dental status was the 2nd most important parameter for MCI. Further studies are warranted to assess the relationship between dental status and MCI. The results of this study showed a significant correlation between the MI and BMD. These results remarked that MI and MCI are precise indices for measuring BMD in osteoporotic female patients as reported by other investigators. 32 In addition, our results have shown that there was a statistically significant positive correlation between the MI and both the t score and the PMI. On correlating PMI with the t score, BMD and MI, it was found that there was a statistically significant positive correlation between them. This study findings supported our hypothesis, and we considered these indices valuable in predicting osteoporosis in the dental clinic. Thus, we recommend that the responsibility of oral radiologist to identify individuals at risk of osteoporosis be officially declared. Although the interobserver agreement of the PMI in this study was excellent, other studies have found that the PMI assessment has a limited repeatability that might limit its usefulness in clinical practice. 33,34 This disagreement could be owed to the differences in the observers experiences. CONCLUSIONS Panoramic indices (MI, PMI and MCI) were positively correlated with the t score and BMD of the lumbar spines. The MCI was found to be the most reproducible index. REFERENCES 1. Davis AT, Israel H, Cannada LK, et al. 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