Relationship Between Body Mass Index and Local Quality of Mandibular Bone Structure in Elderly Individuals

Journal of Gerontology: MEDICAL SCIENCES 2002, Vol. 57A, No. 9, M588 M593 Copyright 2002 by The Gerontological Society of America Relationship Between Body Mass Index and Local Quality of Mandibular Bone Structure in Elderly Individuals D. Knezovi ć Zlatari ć, 1 A. Čelebi ć, 1 and P. Kobler 2 Departments of 1 Prosthodontics and 2 Oral Surgery, School of Dental Medicine, University of Zagreb, Croatia. I Background. Human bones decrease in density and increase in porosity beginning at about the third decade of life. The objective of this study was to determine whether mandibular bone mineral density (BMD) and some linear radiomorphometric measurements on dental panoramic radiograph (DPR) are correlated with different categories of body mass index (BMI) in elderly individuals. Methods. Cortical width at gonion (GI), at antegonion (AI), and below mental foramen (MI) and the appearance of the cortex of the lower border of the mandible distal to the mental foramina due to resorptive changes (mandibular cortical index [MCI]) were measured bilaterally on the mandible on 136 DPRs of elderly individuals. Using DPRs and copper stepwedge, mandibular BMD was investigated densitometrically. All BMD values were expressed in equivalents of the actual stepwedge thickness. The patients with BMIs from 20 to 25 kg/m 2 were classified as category 1 (the generally accepted range of normal BMI), and the patients with BMIs higher than 25 were classified as category 2 (heavy individuals with a heavy skeleton and a large amount of fat in the body). Results. The results revealed statistically significant differences in all measured indices between different BMI categories (p.05 for MI; p.001 for GI and AI). Statistically significant differences were also found in BMD values between different BMI categories (p.05); the differences were more pronounced in women. The patients with MCI category 3 had significantly lower BMD values in comparison to MCI category 2 (p.01). Intraobserver agreement in GI, AI, MI measurement, and MCI assessments was excellent. Conclusions. Heavy people have higher BMD and higher values in linear radiomorphometric measurements than lighter people. N human beings, the loss of bone mass with increasing age is a universally observed phenomenon. Human bones decrease in density and increase in porosity beginning at about the third decade of life (1). In the adult human skeleton, 5% to 10% of the existing bone is replaced every year. The turnover of cortical bone in most areas is close to 5% per year, whereas the turnover of cancellous bone reaches levels up to 20% (2). Oral signs of the mineral bone loss might be manifested by excessive alveolar ridge resorption, tooth loss, chronic destructive periodontal disease, referred maxillary sinus pain, or fracture (3 6). The results of a number of studies suggest a correlation between residual ridge resorption (RRR) and osteoporosis (7 14). Severe RRR may also occur in individuals with good mineral status in the skeleton, and the height of the ridge does not seem to be related to the bone mineral density (BMD) of the ridge (9). According to some authors, heavy individuals with heavy skeletons and a large amount of fat in the body are less predisposed to osteoporosis than small individuals (15). While a large number of methods for the assessment of the amount of bone loss have been proposed, such as absorptiometry (16 25), quantitative computed tomography (26 28), and neutron activation analysis (4,5), one of the simplest methods in the dental evaluation of the mandibular bone loss is dental panoramic radiograph (DPR). Linear measurements (10) and even clinical bone densitometry (4,5) are often used on dental radiographs to assess the bone quality and to find the signs of resorption and osteoporosis. The aim of this study, therefore, was to determine whether the BMD of the mandible, measured using clinical bone densitometric method, and some linear morphometric indices are correlated with different categories of patients body mass index. METHODS Sample The patient sample was selected from a group of complete and removable partial denture wearers at the Department of Prosthodontics, School of Dental Medicine, University of Zagreb. The total of 150 patients was routinely screened by DPR prior to the treatment. The Ethics Committee of the Dental School approved this study, as the patients were exposed to x-rays for diagnostic purposes and future prosthodontic treatment planning. Voluntary written informed consent was obtained from each patient. Only 136 DPRs were included in the final statistical analysis. Four- M588

BODY MASS INDEX AND MANDIBULAR BONE QUALITY M589 teen DPRs were excluded because of cervical spine and pharyngeal air shadows overlying the image of the copper stepwedge or because of the poor quality of DPR, which disabled mandibular cortical index (MCI) assessment. There were 40 male patients (mean age, 72; range, 56 to 84 years) and 96 female patients (mean age, 69; range, 52 to 86 years). Of the 136 patients, 72 were totally edentulous (28 male patients and 44 female patients; mean age, 69; range, 56 to 86 years), and 64 had some teeth remaining only anterior to the first premolars in the mandible (12 male patients and 52 female patients; mean age, 67; range, 52 to 76 years). All the examined removable partial dentures were free-end saddles with indirect retainers and occlusal rests. Radiographic Examination DPR was performed with a constant current of 16 ma and an exposure time of 16 seconds; the kv varied between 65 and 78 kv (Siemens, Orthopos, Germany). Images were recorded using Kodak film. All films were processed together in an automatic dark chamber processor (Dürr Dental XR 24 Nova) for 12 minutes. BMD Assessment During exposure, a copper stepwedge was attached to the bottom of film cassette (trying not to cover any bone structure) to give a reference image on the radiographs. The stepwedge was composed of five steps of thickness 0.1 0.5 mm. DPRs were digitized using a Lynotype Hell (8-bit, 300 DPI) scanner. Before the measurement of gray levels (GLs), black and white colors of the images were inverted. Mean GLs were measured on each of the steps on the copper stepwedge (using Scion image, Beta 4.0.2, probe dimension 4 4 pixels). On the mandibular image, mean GLs were measured on the different regions of interest (ROIs) (Figure 1). The measurement was performed on the edentulous parts on both sides of the mandible. GLs were measured on the angle of the mandible (gonion), trying to measure the BMD of the cortical bone alone, as well as on the other ROIs, where the BMD of cortical bone and trabecular bone were measured together (Figure 1). In addition, superimpositions of the chin rest, airway, and bony shadows were avoided during the measurement. Optical densities (ODs) were calculated as follows: OD log I/255 (OD optical density and I mean measured intensity of GL). All OD values for the copper stepwedge were corrected by subtracting the OD of the immediately adjacent soft-tissue image (below the lower border of the copper stepwedge). OD values of each of the steps on the stepwedge were plotted against the related thickness of the step on the stepwedge to express all the OD values of the stepwedge in the equivalents of the actual stepwedge thickness using the third-degree polynomial. ODs of the ROIs were expressed in copper stepwedge thickness equivalents (29,30). The DenEx 2001 computer program, designed by the authors, was used for the analysis mentioned above. Linear Radiomorphometric Assessment To assess radiomorphometric indices of the mandible, DPRs were viewed using a flat view box in a room with Figure 1. Measured regions of interest on the right side of the mandible: in the projection of foramen mentale (BMD 1 upper border of the mandible, BMD 2 upper border of foramen mentale, BMD 3 lower border of the mandible), in the distal projection, in front of the anterior border of the ascending ramus (BMD 4 upper border of the mandible, BMD 5 upper border of foramen mentale, BMD 6 lower border of the mandible), and 1 mm above gonion (BMD 7). BMD bone mineral density. subdued light. Measurements were made using a 4 magnifying loupe (Getaldus, Zagreb, Croatia) and a precise caliper with the precision of 0.1 mm (MEBA, Zagreb, Croatia). The following radiomorphometric indices were measured on DPRs: cortical thickness below the mental foramen (MI), gonion index (GI), antegonial index (AI), and MCI on both sides of the mandible. The methods of measuring cortical width on gonion GI (31), antegonion AI (32), and below the mental foramen MI (33), on the lower border of the mandible, have been previously described. MCI was assessed according to the criteria defined by Klemetti (10) as described: C 1 The endosteal margin of the cortex is even and sharp on both sides of the mandible. C 2 The endosteal margin has semilunar defects (resorption cavities) with cortical residues one to three layers thick on one or both sides. C 3 The endosteal margin consists of thick cortical residues and is clearly porous. Observer Training One experienced observer and one general dental practitioner (after a thorough introductory lecture) assessed MI, GI, AI, and MCI on all DPRs, and the measurement was repeated after a week interval. No significant difference was noted between the first and the second measurements (p.89 for the general practitioner, p.93 for the experienced observer; paired samples t test). The weighted kappa statis-

M590 KNEZOVI Ć ZLATARI Ć ET AL. tics showed excellent agreement between the observers ( 0.81). As the reliability of the measurements and the agreement were satisfactory, the assessment of the experienced observer was considered for statistical analysis, as she was more consistent between the first and the second measurements. Body Mass Index The body mass index (BMI) of each subject was calculated by dividing the weight (kg) of the subject by the square of his or her height (m 2 ). The patients with BMIs from 20 to 25 kg/m 2 were classified as category 1 (the generally accepted range of normal BMI) and the patients with BMIs higher than 25 were classified as category 2 (heavy individuals with a heavy skeleton and a large amount of fat in the body). Statistical Analysis The data were analyzed using the SPSS 10.0 statistical package (SPSS, Inc., Chicago, IL) (descriptive statistics, analysis of variance, and chi square). Analysis of variance was used to compare mean values of the calculated equivalents of stepwedge thickness on seven different ROIs on the mandible and mean values of the three measured indices (GI, AI, and MI) within the different categories of BMI and to compare the mean values of BMD within different categories of MCI. Cross tabulations were performed to investigate the distribution of MCI within each category of BMI. RESULTS All measurements were made on both left and right sides of the mandible. Correlation between the right and left sides was high for all variables (r 0.8 0.9; p.001). Therefore, the means of the right and left sides were used in all further statistical analyses. The distributions of the BMD measurements, radiomorphometric measurements, and BMI values in this study were normal (one-way Kolmogorov Smirnov test, p.05). There were 60 patients classified in category 1 according to the calculated BMI values, and the rest of the patients (76 of them) were classified in category 2. In BMI category 1, there were 16 male and 44 female patients, and in BMI category 2, there were 24 male and 52 female patients. There was no statistically significant difference between the gender depending on two different BMI categories ( 2 0.390, 1 df, p.532). Statistically significant differences between gender (with men having higher values) were recorded for BMD values (p.01) and MI, AI, and GI values (p.05). The significant difference was also recorded for MCI categories; men had less MCI category 3 ( 2 8.290, 1 df, p.05). Therefore, these variables were separately analyzed for each gender in the further statistical analysis. The mean measured radiomorphometric values (x), together with their standard deviations (SD), for each category Figure 2. Diagram for the values of the measured radiomorphometric indices (gonion [GI], antegonion [AI], and mental foramen index [MI]) dependent on the body mass index (BMI) categories in women and men (BMI 1 20 25 kg/m 2, BMI 2 25 kg/m 2 ). Figure 3. Diagram for the calculated bone mineral density (BMD) values dependent on the body mass index (BMI) categories in women and men (BMI 1 20 25 kg/m 2, BMI 2 25 kg/m 2 ).

BODY MASS INDEX AND MANDIBULAR BONE QUALITY M591 Table 1. Significance of the Differences Between Measured Radiomorphometric Indices and Body Mass Index in Women and Men Women Men Index df F value p F value p MI 1 4.101 0.045* 4.173.049* GI 1 7.405.001 20.357.001 AI 1 13.532.001 5.49.024* Note: MI mental foramen; GI gonion; AI antegonion. *p.05. p.001. of BMI in women and men are shown in Figure 2, and the mean BMD values for each category of BMI, together with their standard deviations, in women and men are shown in Figure 3. All the mean values for the radiomorphometric measures (GI, AI, and MI) in both genders with BMI category 2 were higher than the same values in both genders with BMI category 1 (p.05 for MI, p.001 for GI and AI, Table 1) (Figure 2). For all mean BMD values, higher BMDs were recorded in both genders with BMI category 2 than category 1. The difference was significant in female patients for all seven BMD values (p.001, Table 2; Figure 3), but in male patients, the difference was significant only for BMD 4 and BMD 5 ( p.05) and for BMD 7 ( p.01; Table 2). In evaluation of MCI, only two appearance categories were observed: the majority (58.8%) demonstrated type 3 cortices whereas the remainder (41.2%) demonstrated type 2. None of the patients had category 1 of MCI. In MCI category 2, there were 24 male and 32 female patients, and in MCI category 3, there were 16 male and 64 female patients. The distribution of MCI category appearances by the calculated BMI values in women and men is shown in Figure 4 for both male and female patients. Most of the patients with type 2 MCI were heavier with heavy skeletons and a large amount of fat in the body (BMI category 2), and the patients with type 3 MCI were smaller and thinner. Cross-tabulation of MCI by BMI categories demonstrated a body massrelated pattern, which was confirmed by the chi-squared test Figure 4. The frequency of the mandibular cortical index (MCI) categories (C2 and C3) related to the body mass index (BMI) categories in men and in women (BMI 1 20 25 kg/m 2, BMI 2 25 kg/m 2 ). for trend in women ( 2 21.48, 1 df, p.001) and in men ( 2 13.61, 1 df, p.001). The mean BMD values for each category of MCI (only categories 2 and 3), together with their standard deviations for women and men, are shown in Figure 5. All BMD values for female and male patients were higher in MCI category 2 than in category 3. Female patients had significantly higher BMD 1 7 values in MCI category 2 than in category 3 (p.05) (Table 3). Male patients had significantly higher BMD 1 and BMD 2 (p.05) values (Table 3) in MCI category 2 than in MCI category 3. DISCUSSION After the age of 40, the BMD of the skeleton decreases, so that by the age of 65, about one third of the bone miner- Table 2. Significance of the Differences Between Bone Mineral Density and Body Mass Index Women Men BMD df F value F value p 1 1 24.38** 2.6.116 NS 2 1 30.38** 0.547.464 NS 3 1 12.19** 1.715.198 NS 4 1 7.97** 5.054.03* 5 1 24.05** 6.12.018* 6 1 20.89** 0.904.348 NS 7 1 53.27** 10.36.003** Note: BMD bone mineral density; NS not significant. *p.05; **p.01; NS p.05. Figure 5. Diagram for the calculated bone mineral density (BMD) values dependent of the mandibular cortical index (MCI) categories in women and men.

M592 KNEZOVI Ć ZLATARI Ć ET AL. Table 3. Significance of the Differences Between Bone Mineral Density and Mandibular Cortical Index in Women and Men Women Men BMD df F value p F value p 1 1 25.09.01** 9.18.004** 2 1 15.31.01** 4.10.05* 3 1 4.72.032* 0.025.878 NS 4 1 16.28.01** 0.665.420 NS 5 1 4.03.49* 0.080.778 NS 6 1 11.27.01** 0.002.965 NS 7 1 11.14.01** 0.830.368 NS Note: BMD bone mineral density; NS not significant. *p.05; **p.01; NS p.05. als have been lost (34). Decreased physical activity, lowered secretion of estrogen, diet, race, and heredity may all play a role in age-related bone loss (35). According to Kroger and colleagues, clinically significant osteoporosis is more common in short, lightweight nulliparous women than in tall, heavy women who have had children (15). This is because of the different amounts of bone mass to be lost, and also because of the difference in estrogen metabolism, which is affected by the amount of fat tissue in the body (36). The body skeleton status and the amount of body calcium might be correlated with the height of the mandibular alveolar ridge. Kribbs and colleagues suggested that the height of the edentulous alveolar ridge is correlated with the total amount of calcium in the body and that the bone mass of the mandible depends more on the status of the bony tissues in the whole skeleton (11,37). Some authors investigated gender- and age-related patterns with bone mineral content in the bones of the mandible. Von Wowern found that the bone mineral loss in the bones of the mandible seems to be higher in old women (1.5% per year) than in old men (0.9% per year) (38). Ulm and colleagues also reported the significant difference in the results of bone mineral content between the sexes (39), which is in agreement with the results of this study, as all BMD values, as well as MI, AI, and GI values, were significantly higher in men than in women (p.01). The relationship between the BMI and the remaining alveolar ridge has also been studied. The results revealed that the remaining height of the residual ridge in the mandible was significantly higher among the women with high BMIs (40). Those with high BMIs also had fewer difficulties with their complete denture than did the subjects with low BMI (40). Our study group of patients was not selected on the basis of any radiographic or medical criteria, which would define an individual as normal or osteoporotic, woman or man, and was not chosen from any particular dental specialty. The group, therefore, represented a typical range of older female and male patients, who had undergone a DPR examination as part of the prosthetic treatment. In the present study, the cortical thickness (MI, AI, and GI) along the lower border of the mandible was significantly higher among the patients of both genders with high BMIs ( 25 kg/m 2 ; p.05; p.001) (Figure 2, Table 1). This could be attributed to the fact that the heavy subjects with larger and thicker jaws have more substance to lose and also often have more profitable sex-hormone metabolism. Therefore, wider supportive tissues in the mandible obviously provide better foundations for the use of the removable dentures than those provided by the jaws of small individuals. All the mandibular BMD values (BMD 1 7) were significantly higher in women with higher categories of BMI (p.01, Figure 3, Table 2). All of the BMD values were also higher in male patients, but the significant difference between BMI categories was recorded for BMD 3, BMD 4, and BMD 7 (p.05, Figure 3, Table 2). These results again support the fact that the decrease in BMD is slower in heavy individuals. It seems that the slower decrease in BMD is more pronounced in heavy women than in heavy men. These results support the results of Kroger and colleagues (15), who found that clinically significant osteoporosis is more common in short, lightweight women than in heavy women. Our results are also in accordance with the study of Von Wowern, as she found higher mineral bone loss in the mandibles in old women than in old men (38). It seems that BMI has greater influence on BMD in women than in men, as heavy women are less predisposed to osteoporosis. The results also revealed that most of the male and female patients in this study with semilunar defects (resorption cavities) on the endosteal margin and cortical residues one to three layers thick (MCI category 2) were heavier, with heavy skeletons and a large amount of fat in the body (BMI category 2), and the patients with thick cortical residues on the endosteal margin and clearly porous margin (MCI category 3) were smaller and thinner (BMI category 1). However, it was, again, more pronounced in women than in men, again underlying that light women are more predisposed to osteoporosis (Figure 4). None of the patients in the study had category 1 MCI, which was attributed to the relatively aged group of patients (the youngest was 52 years and the next youngest was 58 years), and it is well known that the first signs of bone loss start at the age of 30 years (41). This study also revealed that, in both genders, anatomical changes in the endosteal margin of the mandibular inferior cortex were found to be useful as a means of the estimating the BMD in the mandible, considering both cortical and trabecular parts of the bone as C3 had significantly lower BMD values in comparison to C2 in women, while significant differences between C2 and C3 categories were found for BMD 1 and BMD 2 in men (p.001). Our results confirm those results of Horner and Devlin, showing the same significant correlation between MCI and BMD (42). The size of the individual (weight and height) and the amount of fat and calcium in the body may play important roles in the impact of mandibular resorption during aging. The use of radiomorphometric measurements, MCI categories, and clinical bone densitometry on DPRs may be helpful in the assessment of the local quality of the mandibular bone structure.

BODY MASS INDEX AND MANDIBULAR BONE QUALITY M593 Acknowledgment Address correspondence to Dubravka Knezovi ć Zlatari ć, Department of Prosthodontics, School of Dental Medicine, University of Zagreb, Gundulićeva 5, 10000 Zagreb, Croatia. E-mail: dkz@email.hinet.hr References 1. Von Wowern N. Microradiographic and histomorphometric indices of mandibles for diagnosis of osteopenia. Scand J Dent Res. 1982;90:47 63. 2. Parfitt AM. The coupling of bone formation to bone resorption: a critical analysis of the concept and of its relevance to the pathogenesis of osteoporosis. Metab Bone Dis Relat Res. 1982;4:1 4. 3. Shapiro S, Bomberg TJ, Benson BW, Hamby C. Postmenopausal osteoporosis: dental patients at risk. Gerodontics. 1985;1:220 225. 4. Kribbs PJ, Smith DE, Chestnut CH. Oral findings in osteoporosis. Part I: measurement of mandibular bone density. J Prosthet Dent. 1983;50: 576 579. 5. Kribbs PJ, Smith DE, Chestnut CH. Oral findings in osteoporosis. 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