of Phalanges: Comparison of Radiographic ... centralized analysis of the image, the use of a single x-ray ... compare measurements of phalangeal. BMD with ..... fracture predictive ability of phalangeal .... phantom and analysis software used in.
Misbah Gulam, MSc Mike M. Thornton, MSc Anthony B. Hodsman, MD, FRCP David W. Holdsworth, PhD
Index terms: Bones, absorptiometry, 436.1295 Hand, 436.1295 Osteoporosis, 30.56, 40.56
Bone Mineral Measurement of Phalanges: Comparison of Radiographic Absorptiometry and Area Dual X-ray Absorptiometry1
Radiology 2000; 216:586 –591 Abbreviations: BMC ⫽ bone mineral content BMD ⫽ bone mineral density DXA ⫽ dual x-ray absorptiometry RA ⫽ radiographic absorptiometry 1
From the Departments of Medical Biophysics (M.G., D.W.H.), Medicine (A.B.H.), and Radiology (D.W.H.), University of Western Ontario, London, Ontario, Canada; the Imaging Research Laboratories, J.P. Robarts Research Institute, 100 Perth Dr, London, ON, Canada N6A 5K8 (M.G., M.M.T., D.W.H.); and the Lawson Research Institute, St Josephs Health Centre, London, Ontario, Canada (A.B.H.). Received July 13, 1999; revision requested August 30; revision received November 30; accepted December 13. Address correspondence to D.W.H. (e-mail: dholdswo@irus .rri.on.ca). © RSNA, 2000
Author contributions: Guarantors of integrity of entire study, M.G., D.W.H.; study concepts and design, A.B.H., D.W.H., M.G.; definition of intellectual content, all authors; literature research, M.G., D.W.H.; clinical studies, M.B.H.; experimental studies, M.G., M.M.T.; data acquisition, M.G.; data analysis, M.G., M.M.T.; statistical analysis, M.G., D.W.H.; manuscript preparation, M.G.; manuscript editing, M.G., D.W.H.; manuscript review, all authors
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With a standard, image-intensifier– based, digital radiographic system, high-spatial-resolution images of the hand were acquired for analysis of phalangeal bone mineral density with dual x-ray absorptiometry (DXA). Results with phalangeal DXA had precision of plus or minus 0.67% and accuracy of 4.1% and correlated well with those with radiographic absorptiometry. This phalangeal DXA technique is potentially useful for clinical diagnosis of osteoporosis.
In the assessment of osteoporosis, clinical measurement of bone mass is used to diagnose low bone mass, predict future skeletal fracture risk, and provide serial monitoring (1–3). Although dual x-ray absorptiometry (DXA) is widely available, alternative means of measuring bone mass, particularly in the peripheral skeleton (calcaneus, forearm, and phalanges), may be just as effective for the diagnosis of fracture risk (2,4,5). Radiographic absorptiometry (RA), a peripheral technique in which a hand radiograph provides an image of the middle phalangeal bones, digitizes optical absorption on the radiographic image by using a high-spatial-resolution video camera. By including an aluminum wedge in the original radiograph, to be used as a calibration device, a measure of phalangeal bone mass is generated, and the bone status can be evaluated (6,7). There are limitations to RA, however, including the time delay resulting from centralized analysis of the image, the use of a single x-ray energy, and the general limitation of calibration in arbitrary (aluminum) units. These limitations have re-
sulted in proposals that RA (with radiographic film) be replaced by digital techniques with semiautomated analysis (8). Hence, new techniques have been developed, such as digital imaging of the metacarpal bones (9), computed digital absorptiometry (10), and dual-energy computed digital absorptiometry of the middle phalanx of the middle finger (11). Despite calibrating bone mineral in arbitrary units, these techniques continue to demonstrate their usefulness in measurements of phalangeal bone mineral density (BMD) as they are precise and accurate, compare well with RA, and provide widespread screening of patients with osteoporosis (10,11). We believe that DXA of the phalanges with a two-dimensional (area) x-ray detector calibrated in hydroxyapatite is an ideal technique for measuring peripheral bone mass. DXA has been used to assess BMD at the distal radius and the calcaneus (12–14), and there have also been attempts to use DXA scanners with point and fan-beam geometry to measure total hand, phalangeal, and metacarpal BMD for the assessment of rheumatoid arthritis (15–18) and, more recently, skeletal maturity (19). But these DXA scanners are designed for central sites (spine, hip, and total body) with a large amount of surrounding tissue and may not provide the spatial resolution needed for small bones (phalanges) with little soft-tissue covering. Hence, because of the widespread availability of digital radiographic equipment, digital imaging techniques, and simple techniques for dual-energy analysis, we undertook a study to implement DXA of the phalanges, assess its precision and accuracy, and directly compare measurements of phalangeal BMD with DXA to those with RA.
the hand for RA and DXA acquisition and analysis. The imaging procedures were fully explained, and written informed consent was obtained from all participants in the study, which was approved by our institutional review board. RA Examinations
Figure 1. Numeric simulations of x-ray spectra used for DXA acquisition: (a) low energy (40 kVp, 318 mA) and (b) high energy (125 kVp, 28 mA, 1.7-mm copper filtration).
Materials and Methods Subjects Two groups of subjects were studied. Group 1 included 19 healthy premenopausal volunteers (age range, 31– 41 years; mean age, 36 years ⫾ 3 [SD]) with normal menstrual function and no known risk factors for metabolic bone disease. Group 2 included 18 healthy postmenopausal women (age range, 63– 81 years; mean age, 71 years ⫾ 5) referred to an outpatient clinic either for assessment of osteoporosis risk factors or management of established osteoporosis. In group 2, seven women (mean age, 70 years ⫾ 4) had no evidence of osteoporosis as assessed at spinal radiography and quantitative calcaneal ultrasonography, and 11 (mean age, 72 years ⫾ 5) were receiving ongoing therapy for the previously established diagnosis of osteoporosis. The subjects in the two groups were chosen to ensure a broad range of bone mass. Routine blood screening was performed to exclude subjects with other metabolic bone diseases or impaired renal function (serum creatinine, ⱖ120 mol/L). Subjects with radiologic evidence of degenerative changes in the interphalangeal joints of the hand were also excluded. Each subject underwent screen-film and digital radiography of Volume 216
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RA measurement of BMD of the phalanges was performed in a central reading laboratory (OsteoGram Analysis Center; OsteoGram, El Segundo, Calif) with exclusively licensed technology (CompuMed; Manhattan Beach, Calif). RA acquisition has been described previously (20). Briefly, RA measurement necessitated acquisition of standard, unscreened radiographs of the left hand, including an aluminum reference wedge for calibration. Two radiographs were obtained, first at 50 kVp and then at 60 kVp. The radiographs were optically processed and the images digitized with use of a highspatial-resolution video camera. To determine an index of BMD, the entire middle phalanges of the second to fourth digits were analyzed. The index is the average BMD for these phalanges with dimensions of mass per unit volume in arbitrary units (6). Note that the RA technique used in this study provided only an estimate of true volumetric BMD of the phalanges. A simple postprocessing algorithm was applied to the radiographic data to obtain an apparent volumetric BMD, assuming a circular cross section for each phalanx in each transverse section of the RA analysis (20). DXA Examinations Acquisition.—In all women, area DXA measurements of the left hand were performed with a clinical digital radiographic unit (Multistar; Siemens Medical Systems, Erlangen, Germany). We implemented the DXA technique for in vitro measurement of tissue composition described by Moreau et al (21) on our image-intensifier– based scanner. The digital radiographic system has an image intensifier with a 20-cm field of view coupled to a logarithmic 10-bit digitizing video camera as its detector system. The output image was digitized into an 880 ⫻ 880 image matrix with pixel size of 184 ⫻ 184 mm. All images were acquired with a 95-cm source-to-detector distance with a geometric magnification of 1.19. The x-ray source was a water-cooled, rotating tungsten anode tube with a 0.6-mm focal spot. The x-ray exposures for the dualenergy radiographs were 40 kVp, 318 mA, and 166 msec for the low-energy
image and 125 kVp, 28 mA, and 166 msec with 1.7 mm of additional copper filtration for the high-energy image. These tube voltages were the lowest and highest x-ray exposures available on the clinical digital radiographic system and were chosen to optimize the differential attenuation of two assumed components (bone and soft tissue) being measured. Figure 1 shows numeric simulations of the polyenergetic spectra with the Tucker-Barnes algorithm (22). Note that although we recommend use of the lowest and highest available exposure settings (to provide the largest separation in lowand high-energy x-ray spectra), the DXA technique works well with less spectral separation. Three image frames were acquired at the low energy during a 3-second period, after which the copper filter was introduced. Then, three image frames were acquired at the high energy during a 3-second period, resulting in a total acquisition time of approximately 25 seconds. The participants were required to keep their hand flat and maintain hand position for the entire scanning sequence. A crossed-wedge calibration phantom composed of material that is radiographically equivalent to soft tissue (polymerized methyl methacrylate, or Lucite) and compact bone (SB3; Gamex RMI, Middleton, Wis) was included in each image. These step wedges, which were superimposed in an orthogonal manner to produce the phantom, allowed 25 different material combinations for calibration of the system. The crossed-wedge calibration phantom encompassed an area of 50 ⫻ 50 mm with maximum step thickness of 11.2 and 18.1 mm for the boneand soft-tissue– equivalent materials, respectively. Figure 2 shows representative images of a hand obtained at the low- and highenergy exposure settings. The exposure for each setting was measured with an ion chamber dosimeter and converted to effective dose (23). The effective dose for the complete DXA scanning procedure was 1.1 Sv. Analysis.—The image data sets were transferred from the digital radiographic system to an image-processing workstation (Silicon Graphics, Mountainview, Calif) for analysis. To improve the signalto-noise ratio, each image was obtained as an average of the three acquired frames. The images were corrected and normalized to account for pixel-to-pixel nonuniformity (fixed pattern mottle), which occurs when image intensifiers are used (21). For each low- and high-energy image pair, the Bone Mineral Measurement of Phalanges
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Figure 2. Digital DXA images of hand including the calibration step wedge (sw): a, low energy and b, high energy. Photon energies provide large separation of bone mineral and soft-tissue components in the region of interest. Note that the RA aluminum reference wedge (aw) is not used in DXA analysis.
low- and high-energy log signals of beam attenuation (corresponding to each of the 25 thickness combinations of the crossedwedge calibration phantom) determined the thickness of the basis material. Radiographic images were converted to quantitative material thickness in a manner similar to that described by Moreau et al (21). Log signal values from both low- and highenergy images were measured in a 4-mm2 region of interest within each of the 25 thickness combinations. The nonlinear transformation between radiographic signal and material thickness for polyenergetic x-ray beams has been described by Johns and Beauregard (24). Parameterization of the image data in this manner allows the calculation of basis material thickness (bone or soft tissue) at any pixel location on the image. The low- and high-energy images for each hand were analyzed to obtain softtissue– and bone-equivalent (thickness) images. The bone-equivalent images were subsequently analyzed (Fig 3). The high spatial resolution of these thickness maps allowed accurate semiautomated edge determination of individual phalanges. The edge detection algorithm for segmentation is an implementation of an active contour that deforms an initial estimate contour, which is represented as a series of weights connected by a thin narrow plate of adjustable stiffness. The contour is deformed by two forces: an external force (analogous to gravity), which is calculated as the negative inverse of the gradient of image intensity values, and an internal force, which is modeled as a bending stiffness (25). This process involved two steps: manual selection of the boundary with a small number of control points followed by automated refinement of the boundary area determination (Fig 4). Standard algorithms were 588
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then used to calculate the bone mineral content (BMC) (in grams) and determine area BMD (in grams per square centimeter) of each phalanx. Data were analyzed for the second to fourth middle phalanges (chosen as analogous to analysis with RA) and the second to fourth proximal phalanges. The middle and proximal phalangeal BMD measurements were then averaged. The BMC of the middle and proximal phalanges was also taken as the average BMC for the individual phalanges. The area DXA technique estimated the BMD of the phalanges in cortical-bone– equivalent units. The bone mineral (hydroxyapatite) component, however, was calculated by correcting for the known fraction of bone mineral in compact bone (0.58) (26). This approach results in area BMD measurement (in grams of hydroxyapatite per square centimeter) that is consistent with other clinical DXA measurements. Precision and Accuracy To evaluate the precision of this DXA technique, three frozen cadaver specimens were analyzed. The cadaver hands were thawed overnight, and DXA was performed the next day. Each specimen was imaged 15 times without repositioning between acquisitions and 10 times with repositioning between acquisitions to evaluate machine precision and operator repositioning precision, respectively. BMC and BMD of the middle and proximal phalanges were determined with DXA analysis. The means and SDs for these measurements were obtained, and the coefficient of variation (percentage) was calculated by means of the method of Gluer et al (27). The accuracy of BMC and BMD measurements was determined by scanning
Figure 3. Digital DXA image shows analysis of bone-equivalent material and segmentation of regions of interest (middle and proximal phalangeal bones). Brightness of a pixel indicates greater thickness of material.
Figure 4. Close-up digital DXA images of the middle phalanx of the third finger of a subject shows semiautomatic segmentation. (a) Software allows user to select the boundary. (b) Edge detection with active contour modeling allows automated refinement of bone boundary.
eight cylindric tissue-mimicking solids of known dimensions and BMD (CIRS, Norfolk, Va). The test samples included a range of trabecular BMD from 0 to 400 mg/cm3 and cortical BMD of 1,100 mg/ cm3 (bone-equivalent material). The true bone mineral mass of each sample was determined from measured volume and known density. These samples were placed in a plastic container and immersed in 15 mm of water, and DXA was performed to obtain the projected area, BMC, and BMD. Gulam et al
TABLE 1 Descriptive Statistics of Bone Density Measurements in Groups 1 and 2 Group 1 (Young) Data Hand RA BMD index (arbitrary units) Middle phalangeal DXA BMD (g/cm2) BMC (g) Proximal phalangeal DXA BMD (g/cm2)† BMC (g)
Mean 109.8
Group 2 (Postmenopausal) SD 9.80
Mean 84.6*
SD 11.9
0.289 0.607
0.025 0.092
0.245* 0.561
0.032 0.085
0.390 1.56
0.033 0.226
0.323* 1.39
0.043 0.226
* P ⬍ .001 compared with group 1. † P ⬍ .001 for all proximal phalangeal BMD values versus middle phalangeal BMD values.
DXA-based measurements of middle and proximal phalangeal BMD and BMC. The statistical significance of differences in these measurements between the groups were calculated with an unpaired Student t test (P ⬍ .05).
Results
Figure 5. Scatterplot shows correlation between hand BMD at RA (BMD RA ) and middle phalangeal BMD at DXA (BMD MID ). The highly significant correlation over a wide range of BMD in the 37 subjects shows that there is a linear trend allowing conversion of hand BMD measurements at RA (in arbitrary units) into phalangeal BMD measurements at DXA (area density in grams per square centimeter of calcium hydroxyapatite).
Linear regression analysis of paired results of BMC versus known bone mineral mass was then performed, yielding the equation of the line, correlation coefficient r, a standard error of the estimate about the regression line, and a P value. The accuracy of BMD measurements was also determined by means of linear regression analysis of BMD versus true area density (in grams per square centimeter), where true BMD is obtained by dividing the true bone mineral mass by the calculated projected area of the cylinder. Data Analysis The primary analysis was a comparison of middle phalangeal measurements with RA and DXA in all patients and a linear regression analysis of the two measurement techniques. For both groups of subjects, descriptive statistics were generated for RA-based measurements of BMD and Volume 216
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Descriptive statistics for hand BMD at RA and phalangeal BMC and BMD at DXA for each group are given in Table 1. Statistical analysis (unpaired t test) of the DXA results showed that the mean middle phalangeal BMD of group 1 (0.289 g/cm2 ⫾ 0.025) was significantly different (P ⬍ .001) from that of group 2 (0.245 g/cm2 ⫾ 0.032). The RA analysis also showed a significant difference in the mean BMD of the two groups (P ⬍ .001). Proximal phalangeal BMD measurements were also significantly higher than middle phalangeal BMD measurements in both age groups (P ⬍ .001). Although BMC tended to be lower in group 2, differences were not as significant as those observed with BMD. In any case, it is inappropriate to make conclusions about group differences on the basis of BMC alone as these measurements are confounded by differences in bone size. Linear regression analysis showed a strong correlation between BMD at RA and middle phalangeal BMD at DXA in all 37 subjects (Fig 5): BMDRA ⫽ (419 ⫾ 34)BMDMID ⫺ 15 (r 2 ⫽ 0.811, P ⬍ .001). Descriptive statistics for the precision analysis (studies with repositioning and those without repositioning) were generated for each cadaver specimen. Table 2 lists the coefficients of variation for measurements of BMC and BMD made with or without repositioning. For all the DXA measurements, the coefficient of varia-
tion was lower for BMC without repositioning than for BMC with repositioning. The largest difference occurred in proximal phalangeal BMD. Also, the coefficient of variation was slightly lower in proximal versus middle phalangeal measurements without repositioning. Linear regression analysis for the accuracy study in tissue- mimicking material (n ⫽ 8) is depicted in Figure 6: BMCDXA ⫽ 0.953 ⫻ BMCtrue ⫹ 0.0111 g (r2 ⫽ 0.9994, standard error of the estimate ⫽ 0.00727 g, P ⬍ .001). The accuracy error represented by the standard error of the estimate divided by the mean BMC was 4.1%. Similarly, the BMDDXA ⫽ 0.936 ⫻ BMDtrue ⫹ 0.0312 g/cm2 (r2 ⫽ 0.9991, standard error of the estimate ⫽ 0.00758 g/cm2, P ⬍ .001). The accuracy error for BMD was 3.2%.
Discussion In this study, we used a standard, imageintensifier– based, digital radiographic system to acquire high-spatial-resolution images of the hand, including a calibration wedge for DXA analysis of phalangeal BMD. The images were postprocessed for semiautomatic analysis of the second to fourth middle and proximal phalanges. Inclusion of an epoxy-based calibration wedge in each image allowed BMD to be expressed as grams per square centimeter of bone mineral (calcium hydroxyapatite). This study also compared phalangeal BMD measurements obtained with DXA to those obtained with RA in two representative groups of subjects, and the precision and accuracy of measurements of BMC and BMD with DXA were determined. Measurements with RA have strong correlations with those obtained with other bone densitometric techniques, including measurements of BMD of the radius, hip, and spine (6,12,13,28 –30). Our results also demonstrate a strong correlation between RA and DXA measurements over a wide range of BMD; thus, the two phalangeal measurement techniques are comparable. The results show that both RA and DXA are able to help separate young women from postmenopausal women in terms of their phalangeal BMD measurement. The accuracy and precision of these bone mineral measurements indicate that the phalanges may be as clinically useful as any other body site for assessing BMD (5). Our study shows that the precision error of our DXA technique is very small, with coefficients of variation of less than 1% for BMC and BMD measurements. For examBone Mineral Measurement of Phalanges
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ple, the precision of DXA in the middle phalanges had a coefficient of variation of 0.67%, which is comparable to the 0.6% precision reported for RA (31) and lower than the 1.8% precision reported for dual-energy computed digital absorptiometry (11). Likewise, the 4.1% accuracy for BMC measurements with DXA compares well with the 4.8% accuracy for RA reported by Yang et al (31). Recently, prospective studies of the fracture predictive ability of phalangeal BMD measurements have been published. Huang et al (32) found that hand RA can predict fracture risk at either spine or nonspine sites, with phalangeal BMD showing a highly significant association with nonspine fractures. In another population-based prospective study, Mussolino et al (20) showed that RA is a significant predictor of future hip fracture. Hence, the measurement of phalangeal BMD at RA is clinically useful, as phalangeal BMD is a strong risk factor for osteoporotic fracture (5). Findings in our study indicate that measurements of phalangeal BMD with peripheral DXA should have comparable usefulness. Often the accuracy of bone densitometric measurements is assessed in cadaver specimens by weighing the amount of ash left by burned bones. In this study, the choice of test material provided an appropriate test for all aspects of DXA including edge detection and calibration in true bone mineral units. We chose cylindric bone-mimicking phantoms, which may be an appropriate model for the phalanges. The advantage of using these phantoms is that both true BMC and true BMD were known, whereas only BMC is obtained from burned bones. Steel et al (33) describe a phantom for assessing BMD of the hand with DXA that is made of aluminum in the shape of cylindric tubes embedded in polymethyl methacrylate, or Perspex. They conclude that the phantom cannot be used to assess the accuracy of BMD measurements, however, because it has not been calibrated against standards of known bone density (33). This limitation was addressed with our phantom as it incorporated cortical bone-mimicking material. DXA has become the most widely used technology to measure BMD and has been the most thoroughly studied (34). Owing to the relatively high cost and dedicated space required for this equipment, however, there continues to be interest in the development of compact densitometric applications for the peripheral skeleton, particularly since DXA at the peripheral sites may have the same 590
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TABLE 2 Precision of DXA in Repeated Measurements Coefficient of Variation (%)
Phalanges Middle BMD BMC Proximal BMD BMC
Without Repositioning (n ⫽ 15)
With Repositioning (n ⫽ 10)
0.67 0.75
0.77 0.91
0.65 0.63
0.90 0.81
Note.—Data are from n repeated measurements in each of the three cadaver hands.
ability to predict fracture as axial DXA technologies (34). The DXA technique used in this study measures BMD of small bones with little soft-tissue covering with high spatial resolution (⬍200 m) and rapid acquisition time (⬍20 seconds) equal to or better than those of conventional clinical DXA. The entire DXA procedure could be less than 1 minute with direct digital acquisition and immediate analysis, thus providing an advantage over RA, in which the interpretation of measurements is delayed by analysis of radiographs of the hand at a central reading facility. DXA also has a distinct advantage over RA and computed digital absorptiometry as it allows soft-tissue correction with the dual-energy algorithm while also reporting true BMD rather than BMD in arbitrary (aluminum) units. This DXA technique was implemented with a clinical digital radiographic system with the large area (image intensifier) detectors commonly used for digital subtraction angiography. Although this system is highly specialized—and hence may not be available at smaller centers— this is not a serious limitation, since the technique could easily be implemented on a smaller, dedicated portable digital DXA system with a reduced range of xray energies and analysis area. With large area detectors, the high spatial resolution ensures reliable semiautomated bone detection, which is particularly important near the joints. Furthermore, the excellent performance of the active contour segmentation technique allows separate analysis on entire phalanges. Implementation of a fully automated segmentation technique may be feasible with a priori knowledge of hand and calibration material placement (35). Note that DXA systems with a fixed region of interest
Figure 6. Scatterplots show accuracy of DXA measurements in tissue-mimicking materials for (a) BMC and (b) BMD with knowledge of the true projected BMD value. Findings with the DXA technique are linear over a wide range of trabecular and cortical BMD values.
may introduce additional variability, as the analysis may include portions of adjacent bone (11). Clearly, a dedicated portable digital DXA system incorporating fully automatic BMD detection would be an invaluable tool for quick and easy diagnosis of bone mass. In conclusion, these data indicate that high-spatial-resolution area DXA accurately and precisely predicts BMD and BMC in the middle and proximal phalanges. The strong correlation between RA and DXA indicates that conversion between measurements of hand BMD at RA and phalangeal BMD at DXA will be possible in future studies. High-spatial-resolution digital measurements of BMD of entire phalanges with DXA with an area detector allows rapid acquisition and immediate analysis, making DXA a potentially useful tool for clinical diagnosis of osteoporosis. With a conventional digital radiographic system, phalangeal DXA may be performed with little extra cost; Gulam et al
this method requires only the reference phantom and analysis software used in this study. This technique has the greatest potential, however, for development as a dedicated and compact peripheral DXA unit. Acknowledgments: We thank Hanif Ladak, PhD, for help in implementing the active contour model algorithm in the software and Hristo Nikolov, MSc, for constructing the calibration wedge. We also thank James A. Johnson, PhD, for providing cadaver specimens. References 1. Kanis JA, Delmas P, Burckhardt P, Cooper C, Torgerson D. Guidelines for diagnosis and management of osteoporosis: The European Foundation for Osteoporosis and Bone Disease. Osteoporos Int 1997; 7:390 – 406. 2. Baran DT, Faulkner KG, Genant HK, Miller PD, Pacifici R. Diagnosis and management of osteoporosis: guidelines for the utilization of bone densitometry. Calcif Tissue Int 1997; 61:433– 440. 3. Marshall D, Johnell O, Wedel H. Metaanalysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 1996; 312: 1254 –1259. 4. Gluer CC, Jergas M, Hans D. Peripheral measurement techniques for the assessment of osteoporosis. Semin Nucl Med 1997; 27:229 –247. 5. Wasnich RD. Perspective on fracture risk and phalangeal bone mineral density. J Clin Densitometry 1998; 1:259 –268. 6. Cosman F, Herrington B, Himmelstein S, Lindsay R. Radiographic absorptiometry: a simple method for determination of bone mass. Osteoporos Int 1991; 2:34–38. 7. Yates AJ, Ross PD, Lydick E, Epstein RS. Radiographic absorptiometry in the diagnosis of osteoporosis. Am J Med 1995; 98:41S– 47S. 8. van Kuijk C, Genant HK. Radiogrammetry and radiographic absorptiometry. In: Genant HK, Guglielmi G, Jergas M, eds. Bone densitometry and osteoporosis. Springer-Verlag: Berlin, Germany, 1998; 291–304. 9. Hagiwara S, Engelke K, Takada M, et al. Accuracy and diagnostic sensitivity of radiographic absorptiometry of the second metacarpal. Calcif Tissue Int 1998; 62:95– 98. 10. Bouxsein ML, Michaeli DA, Plass DB, Schick DA, Melton ME. Precision and accuracy of computed digital absorptiometry for assessment of bone density of the hand. Osteoporos Int 1997; 7:444 – 449.
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