Dental Panoramic Radiography in the Diagnosis of Osteoporosis

Transcription

1 The Journal of International Medical Research 2008; 36: [first published online as 36 (4) 1] Dental Panoramic Radiography in the Diagnosis of Osteoporosis B ÇAKUR 1, A ŞAHIN 2, S DAGISTAN 1, O ALTUN 1, F ÇAGLAYAN 1, Ö MILOGLU 1 AND A HARORLI 1 1 Department of Oral Diagnosis and Oral Radiology, Faculty of Dentistry, and 2 Department of Nuclear Medicine, Faculty of Medicine, Atatürk University, Erzurum, Turkey Osteoporosis is common in the elderly and the dentist is often the only healthcare professional that they visit regularly. Since dental panoramic radiographs (DPRs) are widely used for routine examinations when planning treatment, this study evaluated whether the presence of osteoporosis might be apparent in a population of patients who underwent DPR. The mandibular cortical index (MCI) and a new method of measuring the mandibular radiographic density (m-rd), which used DPR that incorporated an aluminium step-wedge, were compared with the total vertebral bone mineral density (v-bmd) of the lumbar vertebrae measured using dual energy X-ray absorptiometry (DXA) in 25 osteoporotic women. Although there was only a weak correlation between m-rd and v-bmd, significant correlation was found between MCI and v-bmd. Since both m-rd and MCI were related to v- BMD, dental radiographic density and MCI may be useful in clinical dental practice to identify osteoporotic women with previously undetected low BMD. KEY WORDS: OSTEOPOROSIS; DENTAL PATIENTS; MANDIBLE; BONE DENSITOMETRY; DUAL-ENERGY X-RAY ABSORPTIOMETRY; PANORAMIC RADIOGRAPHY Introduction Osteoporosis is defined as a disease characterized by low bone mass and microarchitectural deterioration of bone tissue. 1 It is associated with an increased incidence of fractures and consequent pain and morbidity for affected patients, as well as high costs to public health services. 2 Since low bone mass is an important factor in determining fracture risk, considerable work has been carried out on developing means of detecting individuals with low bone mass at an early stage, so that therapeutic intervention may limit the disease process. 3 5 Bone status at various sites can be assessed using single-photon absorptiometry (SPA), dual-photon absorptiometry (DPA), dual-energy X-ray absorptiometry (DXA), quantitative ultrasound, or quantitative computed tomography (QCT). 3,6 Many of these techniques require specialized facilities or are expensive, time-consuming and necessitate radiography of the highest standards. 7 Furthermore, bone density can be assessed from dental radiographs, such as periapical radiographs and panoramic radiographs. 3 Radiographic assessment of bone density has applications in implantology and in research assessing the relationship between oral bone loss and 792

2 osteoporosis. 8 A large number of quantitative and qualitative measurements of the mandibular bone taken from radiographs have been devised for this purpose, including densitometry and morphometry. 9,10 These techniques include the use of a step-wedge to compensate for any variation during film exposure, processing and digitizing. 11 The step-wedge is attached directly to the bottom of the radiograph or on the film cassette to provide a reference image on the developed and digitized radiographs so that all the measurements on the images are expressed in the equivalents of the step-wedge thickness. Some researchers have addressed the question of whether dental radiographs could have a role to play in the detection of osteoporosis. 5,10,12 It has been suggested that there may be a relationship between mandibular osteopenia and osteoporosis of the remaining skeleton If that is true, evaluation of dental radiographs for osseous changes may be a way to identify women who have no awareness of their low bone mineral density (BMD) and who would benefit from bone densitometry. The earliest suggestion of an association between osteoporosis and oral bone loss was made in Moreover, a number of mandibular cortical indices (MCI) identified by thinning of the cortex at the lower border of the mandible in the dental panoramic radiograph (DPR) have been developed to allow quantification of mandibular bone mass and identification of osteoporosis. The thickness of the mandibular cortex at both the angle of the mandible (gonial index), more anterior at the antegonial region (antegonial index) and the mental index, which is the mean of the widths of the lower border cortex below the two mental foramina, are the three indices recommended for osteoporosis assessment. 16 The present study was conducted to determine whether radiographic changes can be found in the mandible of osteoporotic patients, using conventional radiographs and simple equipment, with the ultimate goal of detecting the early signs of this common disease. Patients and methods STUDY POPULATION Women with osteoporosis diagnosed in the Department of Nuclear Medicine, Faculty of Medicine, Atatürk University were included in this study. All were diagnosed with osteoporosis, based on BMD values of the lumbar spine (L 1 L 4 ) as measured by DXA and defined by WHO criteria (T-score 2.5 SD). 17 None of the subjects had undergone medical therapy for osteoporosis. Each woman had a natural menopause. No history of fractures was noted. This study was approved by the ethical committee of Atatürk University and informed consent was obtained from all patients. VERTEBRAL BONE MINERAL DENSITY MEASUREMENTS Measurement of total vertebral BMD (v- BMD) was undertaken by a single operator using DXA on a Hologic QDR-4500 scanner (Hologic, Waltham, MA, USA) in the Department of Nuclear Medicine, Faculty of Medicine, Atatürk University. The v-bmd measurements were of the lumbar vertebrae (L 1 L 4 ) and recorded as g/cm 2. DENTAL PANORAMIC RADIOGRAPHIC MEASUREMENTS All DPRs were obtained during the DXA scan using a PM 2002 CC Proline apparatus (Planmeca, Helsinki, Finland) by a single operator. Each patient underwent panoramic radiographic examination using 793

3 a cassette fitted with an aluminium stepwedge as described by Horner and Devlin. 18 DENSITOMETRY OF THE MANDIBLE The present study used a new method to measure radiographic bone density. First, the optical densities of the aluminium stepwedge and test sites on the DPR were recorded using a hand-held densitometer (Densoquick 2; Pehamed, Sulzbach, Germany). The deepest point of the antegonial notch 19 was used as a reference point (Fig. 1). The mandibular test sites were situated in a 10 x 10 mm 2 area over the reference point on each side of the mandible. In this way, the region of interest was limited to an area free of tooth elements and their roots (Fig. 1). The radiographic density was compared with the step-wedge standard to compensate for radiographic and processing variations and to provide a unit for quantifying bone mass in standard aluminium equivalents. The mean optical density measurement at both sites was expressed as equivalents of the stepwedge thickness. Secondly, the densities of each step of the aluminium step-wedge were measured by DXA and their densities at both sites were calculated for each patient. The aluminium equivalence values, recorded by a hand-held densitometer, were expressed as g/cm 2 by comparing the density of each step of the aluminium step-wedge with that calculated from DXA measurement. To the authors knowledge, this is the first time that this method has been reported in the literature. Reliability testing of this method gave a coefficient of variation of 2.28%. MANDIBULAR CORTICAL INDEX In order to determine the MCI, the appearance of the mandible on the DPR was assessed by observing it at the antegonial notch depth site distally from the mental foramen bilaterally. The appearance was categorized into one of three groups according to the classification by Klemetti et al. 10 as follows (Fig. 2): C1, the endosteal margin of the cortex was even and sharp on both sides; C2, the endosteal margin showed semilunar defects (lacunar resorption) and/or seemed to form endosteal cortical residues on one or both sides; and C3, the cortical layer formed heavy endosteal cortical residues and was clearly porous. Reliability testing of this method gave a coefficient of variation of 2.38%. The region of interest The deepest point of the antegonial notch FIGURE 1: The antegonial notch depth and the region of interest (10 10 mm 2 ) in the human mandible 794

4 C1 C2 C3 FIGURE 2: Classification of the mandibular inferior cortical appearance. 10 C1, the endosteal margin of the cortex is even and sharp on both sides; C2, the endosteal margin shows semilunar defects (lacunar resorption) and/or seems to form endosteal cortical residues on one or both sides; and C3, the cortical layer forms heavy endosteal cortical residues and is clearly porous STATISTICAL ANALYSIS Descriptive statistics (mean ± SD) and correlations were calculated using the SPSS statistics programme (SPSS version 11.0, SPSS Inc., Chicago, IL, USA). Correlations between the variables studied were assessed by calculation of Spearman s correlation coefficients. Results Twenty-five women with osteoporosis participated in this study and their ages ranged from 50 to 59 years (mean ± SD, 54.7 ± 2.9 years). Table 1 shows their age and bone-related characteristics and Table 2 shows the results of the correlation analyses. The mean ± SD for v-bmd was 0.74 ± 0.06 g/cm 2 (range g/cm 2 ) and there was a significant negative correlation between age and v-bmd (r = 0.469; P = 0.018). No correlation was observed between age and m-rd and age and MCI. The mean ± SD for m-rd was 0.95 ± 0.18 g/cm 2 (range g/cm 2 ) and m-rd was weakly correlated with v-bmd (r = 0.434; P = 0.030). The mean ± SD for MCI was 2.04 ± 0.54 TABLE 1: Age and bone-related characteristics of female patients with osteoporosis enrolled in the study (n = 25) n Mean Range SD Age (years) ± 2.92 m-rd (g/cm 2 ) ± 0.18 v-bmd (g/cm 2 ) ± 0.06 MCI ± 0.54 m-rd, mandibular radiographic density; MCI, mandibular cortical index; v-bmd, total vertebral bone mineral density. 795

5 TABLE 2: Correlation analyses between age, mandibular radiographic density (m-rd), mandibular cortical index (MCI), and total vertebral bone mineral density (v-bmd) in 25 female patients with osteoporosis Age m-rd MCI v-bmd Age 1 r = r = r = 0.469* NS NS (P = 0.018) n = 25 n = 25 n = 25 m-rd 1 r = r = 0.434* NS (P = 0.030) n = 25 n = 25 MCI 1 r = 0.562** (P = 0.003) n = 25 v-bmd 1 m-rd, mandibular radiographic density; MCI, mandibular cortical index; v-bmd, total vertebral bone mineral density; NS, not significant (P > 0.05). *Correlation is significant at the 0.05 level (two-tailed). **Correlation is significant at the 0.01 level (two-tailed). (range ) and there was a significant negative correlation with v-bmd (r = 0.562; P = 0.003). There was no correlation between MCI and m-rd. Discussion Measurements of BMD of the lumbar spine, proximal femur and forearm are widely used to detect osteopenia and osteoporosis, and to monitor the efficacy of treatment. Previous studies comparing bone density in the mandible with that in other bones in vivo have used a variety of methods to assess mandibular BMD. These can be divided into radiographic measurements of cortical thickness using the panoramic mandibular index, mandibular cortical index, radiographic densitometry, DPA, DXA and QCT. 9,12,20 The present study used MCI, panoramic radiographic density and lumbar v-bmd. The MCI, which is based on the appearance of the lower border of the mandibular cortex on a DPR, is a simple classification of C1 C3 based on the severity of the cortical changes. In comparison, mandibular BMD and DXA are more timeconsuming and complicated to undertake. Some workers have used densitometric evaluation of intraoral or panoramic radiographs in conjunction with SPA of the radius, and DPA and QCT of the lumbar spine. 21,22 Techniques using subjective or objective assessments of dental radiographs have given only weak, or no, correlations with skeletal BMD measurements. 23,24 Some researchers have suggested, however, that there may be a relationship between mandibular BMD, measured by microdensitometry on dental radiographs, and BMD measurements in both the femoral neck and lumbar spine measured by DXA. 18,25 27 These studies, have shown significant correlations between mandibular and skeletal BMD. 18,25 27 As a result, some authors have concluded that DPRs should not be used to assess the patient s status regarding osteoporosis, 12,28 whereas others have suggested that it could be a reliable screening tool for osteoporosis. 29,30 Kribbs et 796

6 al. 21 reported that mandibular BMD, as measured by microdensitometry, was positively correlated with total body calcium and other skeletal bone measurements in a population of osteoporotic women with vertebral compression fractures. Mohajery and Brooks 23 reported that mandibular BMD, as measured by a densitometer on a dental radiograph, was not correlated with DXA of the lumbar spine and femoral neck in populations of osteoporotic and normal women. These authors also could not determine differences in the thickness of the angle of the mandible, sinus floor or lamina dura of the tooth sockets between healthy women and those with early osteoporosis. 23 The appearance of the mandibular inferior cortex on DPRs according to the classification by Klemetti et al. 10 is also used to identify individuals with low skeletal BMD or those at high risk of osteoporosis. Previous studies have reported significant correlations between BMD measurements and the mandibular cortical thickness or the panoramic mandibular index. 9,31 33 Several groups have demonstrated that the MCI may be a useful indicator of skeletal BMD, the risk of osteoporotic fracture or bone turnover in postmenopausal women. 29,30,32,34 Bras et al. 35 reported that the cortex of the angle of the mandible was distinctly thinner on panoramic radiograms of postmenopausal women and patients with chronic kidney failure. Horner and Devlin 31 reported that both the MCI and the bone quality index were significantly correlated with the BMD of the body of the mandible as measured by DXA. Zlataric and Celebic 7 reported that patients with lower BMD values in the mandible have a much more porous cortical layer of the inferior border of the mandible. Unfortunately, because the methods used to assess oral and systemic BMD varied considerably between the different studies, it has not been possible to undertake a metaanalysis. The present study demonstrated that both the grading of the cortical bone pattern from DPRs and the radiographic density were correlated with the lumbar spine BMD measured by DXA in a population of osteoporotic women. Like those of other studies, our results suggest that DPRs could be a reliable screening tool for osteoporosis, 18,21,25 27,29 32,36,37 whereas some studies have suggested that DPRs should not be used to assess the patient s status regarding osteoporosis. 12,23,28 Our results might differ from these latter studies because of differences in a number of factors including sample size, the measured area of the mandibular bone, patient selection criteria, nature of the disease, nature of the bone, and experimental techniques and equipment. A number of other factors could also be responsible for this finding. For example, Nakamoto et al. 34 have reported that it is likely that general dental practitioners will tend to select women with a C3 cortex rather than a C1 or C2 cortex on a DPR when identifying women with a low BMD because it is easier to diagnose a C3 cortex (severely eroded or very thin cortex). Furthermore, the image quality of a DPR may influence the appearance of the mandibular inferior cortex. In addition, there might be differences in the magnification between different versions of dental panoramic equipment and the panoramic radiograph might have also contributed to differences in results through its inherently less-sharp image, wide variability in dentistry and production of ghost images. Our study has demonstrated that m-rd measurement on DPRs using a step-wedge may be clinically useful when assessing local quality of the mandibular bone structure 797

7 before undertaking conventional or implantsupported prosthodontic treatment. If osteoporosis is suspected, we also suggest that the dentist or dental hygienist should refer the patient to a physician with extensive training in osteoporosis in order to confirm the diagnosis and initiate the most appropriate treatment strategy, because therapeutic intervention may limit the disease process. Patients with osteoporosis should be encouraged to practice good oral hygiene, to maintain regular dental checkups for frequent dental cleaning, to consume calcium and vitamin D, and to add weight training to their exercise regimen. In conclusion, we suggest that the DPR should be used in clinical dental practice to identify those women with undetected low BMD who should undergo further testing with bone densitometry. Use of the MCI with its simple three-graded classification to indicate changes in the mandibular cortex has been shown in this study to correlate significantly with DXA measurement and should be used as an indicator of skeletal status in potentially osteoporotic women. Conflicts of interest The authors had no conflicts of interest to declare in relation to this paper. Received for publication 7 January 2008 Accepted subject to revision 14 January 2008 Revised accepted 12 March 2008 Copyright 2008 Field House Publishing LLP References 1 Gillespy T, Gillespy MP: Osteoporosis. Radiol Clin N Am 1991; 29: Gabriel SE, Tosteson AN, Leibson CL, et al: Direct medical costs attributable to osteoporotic fractures. Osteoporosis Int 2002; 13: Kribbs PJ, Smith DE, Chesnut CH: Oral findings in osteoporosis. Part I: Measurement of mandibular bone density. J Prosthet Dent 1983; 50: Devlin H, Horner K: Measurement of mandibular bone mineral content using the dental panoramic tomogram. J Dent 1991; 19: Bras J, van Ooij CP, Abraham-Inpijn L, et al: Radiographic interpretation of the mandibular cortex: a diagnostic tool in metabolic bone loss. Part I. Normal state. Oral Surg Oral Med Oral Pathol 1982; 53: Klemetti E, Vainio P: Effect of bone mineral density in skeleton and mandible on extraction of teeth and clinical alveolar height. J Prosthet Dent 1993; 70: Zlataric DK, Celebic A: Clinical bone densitometric evaluation of the mandible in removable denture wearers dependent on the morphology of the mandibular cortex. J Prosthet Dent 2003; 90: Hildebolt CF: Osteoporosis and oral bone loss. Dentomaxillofac Radiol 1997; 26: Benson BW, Prihoda TJ, Glass BJ: Variations in adult cortical bone mass as measured by a panoramic mandibular index. Oral Surg Oral Med Oral Pathol 1991; 71: Klemetti E, Kolmakov S, Kroger H: Pantomography in assessment of the osteoporosis risk group. Scand J Dent Res 1994; 102: Klemetti E, Vainio P, Lassila V, et al: Cortical bone mineral density in the mandible and osteoporosis status in postmenopausal women. Scand J Dent Res 1993; 101: Kribbs PJ, Smith DE, Chesnut CH: Oral findings in osteoporosis. Part II: Relationship between residual ridge and alveolar bone resorption and generalized skeletal osteopenia. J Prosthet Dent 1983; 50: Kribbs PJ, Chesnut CH: Osteoporosis and dental osteopenia in the elderly. Gerodontology 1984; 3: von Wowern NV, Stoltze K: Comparative bone morphometric analysis of mandibles and second metacarpals. Scand J Dent Res 1979; 87: Groen JJ, Duyvensz F, Halsted JA: Diffuse alveolar atrophy of the jaw (non-inflammatory form of paradental disease) and pre-senile osteoporosis. Geront Clin (Basel) 1960; 2: Ledgerton D, Horner K, Devlin H, et al: Radiomorphometric indices of the mandible in a British female population. Dentomaxillofac Radiol 1999; 28: World Health Organization: Assessment of fracture risk and its application to screening for post-menopausal osteoporosis. Technical Report Series. Geneva: World Health Organization, 1994; p Horner K, Devlin H: Clinical bone densitometric 798

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