JOURNAL OF BONE AND MINERAL RESEARCH Volume 7, Number 4, 1992 Mary Ann Liebert. Inc., Publishers
Bone Mass Measurements in the Distal Forearm Using Dual-Energy X-ray Absorptiometry and y-Ray Computed Tomography: A Longitudinal, In Vivo Comparative Study THOMAS R. OVERTON and GARRY D. WHEELER
ABSTRACT Indices of bone mass were measured in 23 volunteers weekly over 14-16 weeks using dual-energy x-ray absorptiometry (DEXA) and special-purpose computed tomography (y-CT). In vitro, the precision for both systems was excellent (coefficient of variation < 0.5%). Over 4 months, the precision in vivo (average CV for all subjects) for DEXA measures (BMD, g/cmZ, and BMC, g/cm) varied between 0.6 and 1.1%; with y-CT it varied from 1.1% for TBD (g/cm3) to 2.2% for CBD (g/cm3). Correlation between the indices of bone mass measured using DEXA and y C T at the ultradistal site was moderate, but these indices were not correlated at the distal third site. When BMD and BMC were derived from the CT index IBD, however, the correlation between these y-CT indices and the corresponding DEXA indices was high for both ultradistal and proximal radial sites.
INTRODUCTION
using computed tomography (CT) were pioneered by Ruegsegger and his colleagues.(121This technique has now been developed to permit the separate evaluation of traINGLE-PHOTON ABSORPTIOMETRY (SPA) has been widely used for more than 20 years to measure bone mineral becular (TBD), cortical (CBD), and total (IBD) bone denFor clinically ac- sities (g/cm3), in the distal forearm and in the proximal content (BMC, g/cm) in the ceptable performance, SPA has generally been limited to tibia, with a precision in vivo between 0.3 and 0.6% for recortical bone measurements in the distal third of the ra- peated measurements in healthy subjects over periods of dius, where a precision of between 2 and 3% can be ob- up t o 50 day^.('^-'^) Although currently available in only a tained routinely in longitudinal in vivo studies in young few research centers, the peripheral C T technology is an healthy subjects. Bone mineral density (BMD, g/cmZ) mea- important research tool that has facilitated monitoring of surements in the ultradistal radius using rectilinear SPA short-term transients in bone mineral distributions in scanning techniques are now also widely available and vivo(16)and has also been used to show that the rate of aphave a reported precision in vivo between 1 and 3 v 0 . ' ~ ) pendicular bone loss in individual subjects changes over Dual-energy x-ray absorptiometry (DEXA), a newly de- time. ( 1 The purposes of this study were threefold: veloped technology for BMD measurements in the spine and proximal femur, is also easily adapted for BMD measure1. T o determine in vivo precision for BMD and BMC ments at sites in the peripheral skeleton. For bone mass mea- measurements in the ultradistal and distal third radius surements in the lumbar spine and proximal femur, DEXA using DEXA (Hologic QDR 1000 system) 2 . To determine in vivo precision for TBD, CBD, and has significantly better precision than dual-photon absorptiometry (DPA).('-II) Given the demonstrated superior perfor- IBD measurements in the ultradistal and distal third radius mance of DEXA in axial skeleton measurements, we antici- using y-ray C T (7-CT) pated that DEXA could also be used for routine, high-preci3. To correlate the indices of bone mass measured in the sion bone mass measurements in the appendicular skeleton. distal forearm using DEXA with those measured using Bone mass measurements in the peripheral skeleton Y-CT
S
Department of Applied Sciences in Medicine, University of Alberta, Edmonton, Canada.
375
OVERTON A N D WHEELER
376
MATERIALS A N D METHODS In response to requests for volunteers from staff fitness classes, 23 healthy subjects (18 men and 5 women) aged 27-61 years (mean 48 years; standard deviation, SD 14 years) were entered into this study. Written informed consent was obtained from all participants in a manner approved by an institutional ethics review committee. Brief questionnaires concerning medical, dietary, physical activity, and life-style histories were completed by all subjects before acceptance into the study. No study participant had any disease known or suspected of skeletal effect or had taken medication that might have had a skeletal effect within 6 months immediately preceding this study. All were nonsmokers, no more than social consumers of alcohol, and participants in organized, 1 h long fitness classes at least thrice per week. Anthropometric data for study subjects are shown in Table I . Both y-CT and DEXA measurements were made on the same day each week over 14-16 consecutive weeks for 21 subjects; for 1 subject there was a 4 week break in the protocol for vacation. One subject dropped out of the study after 8 weeks upon confirmation of pregnancy. All available subject data at each time point are included in the analysis. Using y-CT, bone density measurements were made for the ultradistal and distal third radius employing well-established Briefly, the subject was positioned for each measurement with a preliminary C T scout view to precisely locate the distal surfaces of the radial and ulnar condyles using an interactive, semiautomatic image analysis program. For each subject, both measurement sites were defined relative to these anatomic landmarks. At the ultradistal site CT measurements were started 2 mm proximal to the lowest part of the radial end plate and extended 14-16 mm proximally from that position. The most distal part of the distal third radial site was located individually for each subject at one-third of the ulnar length measured from the radial condyle and extended 6-8 mm proximal to that location. The location of the ultradistal site and of the volumes used for evaluation of the bone mass indices are shown schematically in Fig. 1. Using y-CT, the repositioning precision was better than +0.2 mm. The measurement time for each transaxial slice was 90 s, and six to eight C T slices were obtained at the ultradistal site and three to four slices at the distal third site for each subject visit. The y-CT system was calibrated daily using a cylindrical radius phantom made of plexiglass (soft tissue, Teflon (fat), and aluminum (bone); a cylindrical, stepped-thickness (0.5-4 mm) aluminum tube phantom was also used to calibrate for the thicker cortical bone measurement at the distal third site. ( I 5 ) A two-component tissue model was assumed for the measured bone volume(1a)and C T variables (TBD, CBD, and IBD) expressed as physical densities (g/cm3). To emphasize the similarities in indices of bone mass measured by y-CT and DEXA, we also derived BMD (g/cm*) and BMC (g/cm) from the C T index IBD (g/cm3). This conversion was made as follows. For each C T slice the volume was determined from the measured slice area (number of pixels) and the fixed slice thickness (2 mm). Since the
TABLt 1 .
CHARACTERISTICS OF STUDYPOPULATION
*\\THROPOMETRIC
THE
~~~~
Subject
Age (years)
Se.v
Height (cm) ~~
F M M M F M
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
M M M M M F 11
r \I \I \I hl
M M M F M
The trabecrj' volume wrthin tt m e SLI numb f
48 45 32 31 25 45 55 51 46 56 45 46 52 45 72 52 54 29 60 49 58 46 34
I.
Weight (kg)
~
161.3 185.5 169.5 171.6 159.0 181.5 174.8 177.0 176.2 174.5 161.5 160.0 177.5 175.2 173.9 172.4 167.0 186.0 180.5 178.5 176.5 156.5 177.8
60.2 84.2 67.0 68.8 57.0 74.8 71.8 97.3 79.3 65.9 54.9 60.0 71.5 72.9 77.9 92.0 59.6 70.2 83.2 81.2 70.0 62.3 74.0
hme space (TBS) 1 by the area jr
of each slice. n). and the ir averaging
~
Average p x r l V~IIIIC hctween the 75% and 95% area conloiirs determines CBD
.
~
Average pixel value wrthin the 100% area conlour determines IBD ~
~~
Average pixel value wlthin m e 45% area contour determines TBD ~
FIG. 1. Radial ultradistal measurement site used in y-CT. The particular bone volumes averaged for determinations of TBD, CBD, and 1BD are shown. Both ultradistal and distal third measurement sites are located relative to the radial styloid. At the ultradistal site the bone volumes evaluated by y-CT and DEXA are similar; at the distal third site the DEXA analysis is for approximately twice the volume evaluated using y-CT.
377
DEXA AND y-CT MEASURES OF RADIAL BONE MASS measured slice volume and the average IBD are invariant with respect to rotation of the arm, the projected area of each slice can then be approximated as a product of the diameter of the circle with the same area as the slice and the slice thickness. The total measurement volume and projected area are the respective sums for all slices included in the evaluation. Using DEXA (Hologic QDR 1O00), forearm BMD and BMC measurements were made with the subject’s right arm placed palm down on the scanning table with the lateral forearm pressed lightly against the edge of a dense foam block. A single scan (120-150 contiguous translations of an approximately 1 mm wide beam) was then made, beginning distal to the radial condyle and covering both the ultradistal and distal third radius and ulna. A high-resolution scan and analysis software supplied by the manufacturer were used to obtain values for BMD and BMC at ultradistal and distal third sites for radius and ulna combined and for the radius alone. For the ultradistal site the distal limit of the analysis region was 2 mm proximal to the lowest part of the radial end plate and extended I5 mm proximally from that location. For the distal third site the distal limit of the analysis region was at one third of the ulnar length measured from the radial condyle and extended 15 mm proximally from that location. The total measurement time was between 7 and 8 minutes for all subjects. The DEXA system was calibrated daily using the calcium hydroxyapatite spine phantom supplied with the instrument. Correspondence between the longitudinal positions of the bone volumes evaluated using y-CT and DEXA was good (*0.5 mm). At the ultradistal site the estimated maximum difference between the volumes of bone evaluated by the two instruments is 7%. At the distal third site the bone volume evaluated using y-CT was about one-third of that for DEXA and was completely within the DEXA analysis volume. However, it is not necessary to measure exactly the same bone volume with both methods unless absolute comparisons of bone mass are to be made. For both y-CT and DEXA, bone mass indices are averaged over volumes of several milliliters. Small, local heterogeneities in mineral distribution are therefore relatively unimportant when comparisons are made between the indices of bone mass obtained with the two methods.
RESULTS
In vivo studies y-Ray CT: For ultradistal and distal third radius, regressions of TBD, CBD, and IBD with time were calculated; the regression line slope was not significantly different from zero @ < 0.001) for any variable in any subject. For each bone index an average coefficient of variation was calculated from the 14-16 measurements in each of 22 subjects, and 8 measurements in 1 subject, to be used to indicate in vivo performance of the y-CT method (Table 2). The correlation coefficient r and SEE (standard error of the estimate, determined from the regression and expressed as a percentage of the mean index value) between CT indices of bone mass measured at the ultradistal and distal third radius are given in Table 3. A source change (1251)was made for the y-CT system 8 weeks into this study. T o investigate the possible effects of the source change on measured bone mass indices, we separately analyzed data for the first 8 weeks and the last 6 weeks for each subject. There was no influence of source change on the regressions of bone mass indices with time, but there was a small (NS, not significant) increase in mean values for these indices after the source change. D E X A (QDR 1000): Using standard software supplied by Hologic Inc., BMD and BMC were evaluated for the ultradistal and distal third regions and for the total scan area of the forearm; the analysis was made for radius and ulna together and for radius aone. For each subject and for each bone mass index, linear regressions with time were calculated; the regression line slope was not significantly different from zero @ < 0.001) for any index in any subject. The average coefficient of variation (CVVo) and standard deviation of this coefficient for BMD and BMC at these sites are given in Table 4. Correlations between DEXA measures of BMD and BMC at different sites for the radius alone are shown in Table 5 as correlation coefficient r and SEE (determined from the regression and expressed as a percentage of the mean index value). In this report, the results for the analysis of the radius alone are presented since this bone was also measured using y-CT. However, the results for the radius and ulna combined were also obtained; these were almost identical to the results for radius alone and generally had a slightly better measurement precision. Correlation Between y-CT and DEXA Indices of Bone Muss: Correlation between y-CT and DEXA bone mass
In vitro studies Long-term, in vitro precision for y-CT and DEXA was determined from regressions with time of phantom TBD and BMD measurements, respectively. Using y-CT, the measurement precision for the linear attenuation coefficient of plexiglass within a cylindrical aluminum annulus was 0.46% (CV) over 5 years and, for the most recent year, which includes the period of this study, was 0.37%. Using DEXA, the precision over 1.5 years was 0.44% (CV) for a BMD measurement of calcium hydroxyapatite vertebral sections embedded in Lucite; for a 6 month period encompassing the present study the CV was 0.43%.
TABLE2. AVERAGE COEFFICIENT OF VARIATION(qo) AND SD FOR y-CT INDICESOF BONEMASSIN THE ULTRADISTAL A N D DISTAL THIRD RADIUS~
Radius Ultradistal Distal third
TBD, CV% (SD) 1.1 (0.5)
CBD, C V % (SD)
IBD, C V % (SD)
1.8 (0.7)
I .4 (0.6) 2.0 (1.5)
2.2 (1.1)
aThere were 14-16 measurements in each of 22 subjects and 8 measurements in 1 subject over 4 months.
OVERTON A N D WHEELER
378
(SEE) TABLE3. CORRELATION COEFFICIENT AND STANDARD ERROROF THE ESTIMATE FROM THE REGRESSION AND EXPRESSED AS A PERCENTAGE OF THE APPROPRIATE MEAN DETERMINED I N D E X VALUE BETWEEN y-CT INDICES OF BONEMASSAT ULTRADISTAL AND DISTAL THIRD RADIUS
Ultradistal radius r (SEE%) TBD UD radius CBD IBD BMD BMC D 1/3 radius CBD I BD BMD BMC
CBD
IBLI
0.63 0.84 0.75 0.58
(14) (10) (13) (15)
0.95 (3.8) 0.74 (8.0) 0.49 (10)
0.82 (7.0) 0.58 (10)
0.94 (5.2)
0.10 0.20 0.39 0.33
(17) (17) (17) (16)
0.43 (9.0) 0.44 (10.7) 0.46 (10.6) 0.30 (11.8)
0.34 (10.2) 0.39 (11.5) 0.47 (10.9) 0.34 (11.8)
0.01 (-) 0.02 ( - ) 0.74 (10) 0.74 (10)
TABLE4. AVERAGE CV (vo) A N D SD FOR DEXA INDICESOF BONEMASSIN DISTALFOREARM^
Site Ultradistal radius Distal third radius Ultradistal radius and ulna Distal third radius and ulna Total scan area
BMD
BMD, CV% (SO)
BMC, CV% (SO)
0.8 (0.3) 1 . 1 (0.4) 0.8 (0.3) 0.7 (0.3) 0.6 (0.3)
1 .O (0.6) 1 .O (0.5) 0.8 (0.4) 0.7 (0.3) 0.6 (0.3)
~
dThere were 14-16 measurements in each of 22 subjects and 8 measurements in 1 5ubject over 4 months.
indices for the ultradistal and distal third radius, respectively, are shown in Tables 6 and 7 as correlation coefficient r and SEE (determined from the regression and expressed as a percentage of the average index value). For the ultradistal radius, correlations between the y-CT bone mass indices TBD, BMD, and BMC and DEXA indices BMD and BMC are shown graphically in Fig. 2a through d; for the distal third radius these relationships are shown in Fig. 2e and f . For each comparison the least-squares regression line is shown. Since the estimations of mean index values made before and after the 1251 source change in the y-CT system are independent, we combined both data sets for determinations of correlations between y-CT and DEXA, and thus 46 mean values (for 23 subjects) are plotted in the several correlations shown in Fig. 2.
DISCUSSION In vitro, the precision of y-CT and of DEXA during the 4 months of this study were similar (CV better than 0.5%) to their respective longer term precisions. Both y-CT and DEXA also showed excellent in vivo precision for repeated bone mass measurements at ultradistal
BMC
-
0.22 0.20 0.78 0.85
(15) (18) (1 3) (10.8)
and distal third sites in the radius over a 4 month period. Using y-CT, 330 TBD measurements of the ultradistal radius, made in 23 subjects over 4 months, had an average error (CV) of 1.1% (range 0.3-1.6%). This error is larger than the 0.6% previously reported from this laboratory for five subjects over 50 days.'L6'However, the present result is probably a better indicator of the average, long-term clinical performance of the y-CT system since it reflects the combined effects of a change to a '"I source in the middle of this study, of three different machine oeprators, and of normal, individual biologic variation in mineral distribution in the forearm over time in a heterogeneous group of subjects. In addition to our routine TBD analysis, we also evaluated cortical and integral bone densities in the ultradistal radius in this study. Errors in CBD and IBD values are higher than for TBD (1.8 and 1.4%, respectively) since the additional steps required in the analysis process and the differences in the volume evaluated (particularly for CBD) contribute to the overall precision error. At the ultradistal radius, the correlation between TBD, CBD, and IBD is moderate ( r = 0.63 and 0.84, respectively) but not predictive (SEE = 14 and lo%, respectively) since different proportions of cortical and trabecular bone are compared in these indices. CBD and IBD were highly correlated ( r = 0.95, SEE = 3.8%), however, indicating a relatively large cortical bone contribution to integral bone measurements in the ultradistal radius (Table 3). At the distal third radius site, errors in CBD and IBD measurements are higher than at the ultradistal site (2.2 and 2.09'0, respectively), and these indices are highly correlated ( r = 0.94, SEE = l.8%), since a transaxial section at this site generally contains only cortical bone and marrow. The increased errors in CBD and IBD measurements at the distal third site are principally due to the much smaller bone volume used in the evaluation process and to the increased number of steps in the data analysis. Using DEXA, both BMC and BMD were calculated for radius and ulna combined and for the radius alone. Over the 4 month period of this study the average CV for radius and ulna combined at the ultradistal site in 330 measure-
379
DEXA AND 7-CT MEASURES OF RADIAL BONE MASS TABLE5 . CORRELATION COEFFICIENT r A N D SEE DETERMINED FROM 'THE REGRESSION AND EXPRESSED AS A PERCENTAGE OF THE APPROPRIATE MEANINDEXVALUEBETWEENDEXA INDICES OF BONEMASSAT ULTRADISTAL AND DISTALTHIRDSITESAND FOR T H E TOTAL SCANAREAIN THE RADIUS
Ultradistal r (SEE%) BMD Ultradistal BMC Distal third BMD Distal third BMC Total scan area BMD Total scan area BMC
0.92 0.75 0.75 0.90 0.74
Distal third r (SEE%)
BMC
(5.1) (6.5) (8.4) (5.6) (8.7)
BMD
BMC
Total BMD, r (SEE%)
-
0.80 (11.6) 0.89 (7.9) 0.90 (8.3) 0.90 (8.7)
-
0.93 (3.5) 0.93 (3.7) 0.88 (4.6)
-
0.90 (7.6) 0.97 (4.2)
-
0.89 (4.5)
TABLE 6. CORRELATION COEFFICIENT r A N D SEE DETERMINED FROM 'THE REGRESSION AND EXPRESSED AS A PERCENTAGE OF THE APPROPRIATE MEANI N D E X V A L U E BETWEEN INDICES OF BONEMASSMEASURED BY y-CT A N D DEXA IN THE ULTRADISTAL RADIUS
y - C T r (SEE%) DEXA
TBD
CBD ~
BMD
BMC Total BMD Total BMC
0.734 (12) 0.527 (16) 0.528 (16) 0.527 (19)
~
0.721 0.455 0.592 0.248
(8.3) (10) (10) (11)
TABLE 7. CORRELATION COEFFICIENT r A N D SEE DETERMINED FROM THE REGRESSION A N D EXPRESSED AS A PERCENTAGE OF APPROPRIATE MEANVALUE BETWEEN INDICES OF BONEMASSMEASURED BY y-CT AND DEXA IN THE DISTAL THIRDR A D I U S ~ y-CT r (SEE%)
DEXA BMD BMC Total BMD Total BMC
BMD 0.924 (3.4) 0.898 (7.4) 0.891 (4.1) 0.856 (1 1)
IBD
BMD
BMC
0.778 (7.9) 0.509 (1 1) 0.621 (10) 0.304 (12)
0.958 (3.4) 0.902 (7.9) 0.884 (4.2) 0.741 (14)
0.900 (5.2) 0.978 (3.9) 0.892 (4.1) 0.879 (10)
~~
BMC 0.929 0.980 0.879 0.948
(3.3) (3.3) (4.3) (6.9)
aOnly the derived indices (BMD and BMC) for y-CT are shown since both cortical (CBD) and integral (IBD) bone densities (g/ cm') are constant in the distal third radius and thus are not correlated with DEXA measures of bone mass.
ments in 23 subjects was 0.8% for both BMD and BMC; for radius alone, the average CV was 0.8 and 1070 for BMD and BMC, respectively. For the distal third site, the average CV for both BMD and BMC measurements in the radius and ulna combined was 0.7% and, in the radius alone, 1.1 and 1 .O%, respectively. Over the total scan area, the average CV was 0.6% for both indices (Table 4). The average in vivo precision for BMD and BMC measurements in the distal forearm using DEXA is generally better than that obtained for the spine (IVo), probably as a result
of a better automatic definition of the outer contours of the radius and ulna. A modest improvement in precision is obtained when averaging over the total scan area (bout 130 mm length) rather than over a local area (e.g., 15 mm length for the ultradistal site). The correlation between DEXA indices of bone mass at three sites in the forearm was high (Table 5 ) . Comparisons between the principal indices of bone mass measured by y-CT and DEXA are shown in Fig. 2 and in Tables 6 and 7. The CT index TBD (g/cm3) is moderately correlated with the DEXA indices BMD (g/cm') and BMC (g/cm) at the ultradistal radius, but the SEE is large (Fig. 2a and b). However, the lack of a predictive relationship between TBD and the DEXA indices BMD and BMC is not unexpected given the differences in the proportions of trabecular and cortical bone measured by the two technologies and the differences in the units of measurement. When BMD and BMC' are derived from the integral bone density (IBD, g/cm3) measured by CT, however, these indices are highly correlated with the corresponding DEXA indices at both ultradistal (Fig. 2c and d) and distal third sites (Fig. 2e and f). Until now, most clinical appendicular bone mass measurements in the forearm have been made using SPA at distal third sites and rectilinear scanning SPA at ultradistal sites. For research applications special-purpose CT systems have been developed for high-precision measurements of both trabecular and cortical bone densities in the appendicular skeleton. Each of these technologies, however, has
OVERTON A N D WHEELER
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total forearm scan area. The DEXA indices also correlate highly with the y-CT indices BMD and BMC (derived from IBD), and at the ultradistal site BMD is also moderately correlated with the average physical density of trabecular bone (TBD, g/crn3). For longitudinal BMD measurements in individual healthy subjects, the precision varied between 0.8 and 1.1% at the ultradistal radius site. In osteopenic subjects the measurement precision is lower, however, because of the excellent correlation between local and total BMD and BMC measures; larger scan areas, perhaps including both radius and ulna, could then be evaluated to improve performance. A Hologic QDR lo00 was used in this work, but we expect that DEXA machines from other manufacturers would have a similar performance in appendicular bone measurements.
ACKNOWLEDGMENTS
0
DEXA
1 1
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3 0,
1 0
2 5
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We particularly thank Joi Belyck, Tsylia Gorodetsky, and Nigel Gann for excellent technical support throughout this study. We greatly appreciate the generosity and cooperation of P.G. Heslip, M.D., who provided free access to the Hologic QDR lo00 in his laboratory. Finally, our biggest accolade goes to the 23 volunteers who, without complaint, attended our laboratories on a weekly basis over 4 summer months. This work was supported in part by Hologic Inc., Waltham, MA.
1
0 6
REFERENCES FIG. 2. Correlation between y-CT and DEXA indices of bone mass for the ultradistal radius (a-d) and for the distal third radius (e and f). Using y-CT, TBD, CBD, and IBD are measured indices; BMD and BMC are derived from IBD.
important practical limitations: the usefulness of SPA is limited to cortical bone measurements and usually to cross-sectional population studies; rectilinear scanning SPA, used at ultradistal sites, measures a greater proportion of trabecular bone and has an improved precision relative to SPA, but its application to longitudinal studies is still limited by poor precision; special-purpose C T systems have a high sensitivity and precision for TBD, CBD, and IBD measurements and are appropriate for both short-and long-term clinical longitudinal studies, but they are expensive, technically difficult to operate, and not widely available. In this study, using a Hologic QDR 1o00, we showed that DEXA has excellent in vivo precision for BMD and BMC measurements in the forearm. Repositioning subjects for repeated measurements using the QDR lo00 is very easy, and for the ultradistal site the scanning time is less than 3 minutes. There is a high correlation between the DEXA indices BMD and BMC measured at local sites (ultradistal, middistal, and distal third radius) and over the
I . Yano K , Wasnich R , Vogel JM. Heilbrun LK 1984 Bone mineral measurements among middle-aged and elderly Japanese residents in Hawaii. Am J Epidemiol 119:751-764. 2. Nilas L, Borg J , Gotfredsen A, Christiansen C 1986 Comparison of single- and dual photon absorptiometry in postmenopausal bone mineral loss. J Nucl Med 26:1257-1262. 3. Riggs BA, Wahner H W , Melton LJ I l l , Richelson LS, Judd H L , Offord KP 1986 Rates of bone loss in the appendicular and axial skeletons of women. Evidence of substantial vertebral bone loss before menopause. J Clin Invest 77:14871491. 4. Price RI, Barnes M P , Gutteridge D H , Baron-Hay M , Prince RL, Retallack RW, Hickling C 1989 Ultradistal and cortical
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women. A prospective study of clinical data using photon absorptiometry. Ann Intern Med 112:96-101. 6. Nilas L, Gotfredsen A, Hadberg A, Christiansen C 1988 Age-related bone loss in women evaluated by the single and dual photon technique. Bone Miner 4:95-103. 7. Wahner H W , Dunn WL, Brown ML, Morin RL, Riggs BL 1988 Comparison of dual-energy x-ray absorptiometry and dual photon absorptiometry for bone mineral measurements of the lumbar spine. Mayo Clin Proc 63:1075-1084. 8. Kelly TL, Slovik DM, Schoenfeld DA, Neer RM 1988 Quantitative digital radiography versus dual photon absorptiometry of the lumbar spine. J Clin Endocrinol Metab 67:839844.
DEXA AND Y-CTMEASURES OF RADIAL BONE MASS 9. Borders J , Kerr E, Sartoris DJ, Stein JA, Ramos E, Moscona AA, Resnick D 1989 Quantitative dual-energy radiographic absorptiometry of the lumbar spine: In vivo comparison with dual-photon absorptiometry. Radiology 170:129131. 10. Gundry CR, Miller CW, Ramos E, Moscona A, Stein JA, Mazess RB, Sartoris DJ, Resnick D 1990 Dual-energy radiographic absorptiometry of the lumbar spine: Clinical experience with two different systems. Radiology 174:539-541. II. Gliier CC, Steiger P , Selvidge R, Elliesen-Kliefoth K, Hayashi C, Genant HK 1990 Comparative assessment of dual photon absorptiometry and dual-energy radiography. Radiology 174:223-228. 12. Riiegsegger P, Elsasser U , Anliker M, Gnehm H, Kind H, Prader A 1976 Quantification of bone mineralization using computed tomography. Radiology 121:93-97. 13. Riiegsegger P 1988 Quantitative computed tomography at peripheral measuring sites. Proceedings of Kuopio International Symposium on Osteoporosis. Ann Chir Gynaecol 77: 204-207. 14. Miiller A, Ruegsegger E, Riiegsegger P 1989 Peripheral QCT: A low risk procedure to identify women predisposed to osteoporosis. Phys Med Biol 34:741-749. 15. Hangartner TN, Battista J J , Overton TR 1987 Performance
38 1 evaluation of density measurements of axial and peripheral bone with x-ray and gamma-ray computed tomography. Phys Med Biol 32: 1393- 1406. 16. Hangartner TN, Overton TR, Harley CH. van den Berg L, Crockford PM 1985 Skeletal challenge: An experimental study of pharmacologically induced changes in bone density in the distal radius, using gamma-ray computed tomography. Calcif Tissue Int 37:19-24. 17. Riiegsegger P , Dambacher MA, Riiegsegger E, Fischer JA, Anliker M 1984 Bone loss in premenopausal and postmenopausal women. J Bone Joint Surg [Am] 66:1015-1023. 18. Hangartner TN, Overton TR 1982 Quantitative measurement of bone density using gamma-ray computed tomography. J Comput Assist Tomogr 616): 1 156- 1 162.
Address reprint requests to: Dr. T.R. Overton Department of Applied Sciences in Medicine University of Alberta Edmonton, Alberta, T6G 2G3, Canada Received for publication March 12, 1991; in revised form November 8, 1991; accepted Nobember 12, 1991.
Bone Mass Measurements in the Distal Forearm Using Dual-Energy X-ray Absorptiometry and y-Ray Computed Tomography: A Longitudinal, In Vivo Comparative Study THOMAS R. OVERTON and GARRY D. WHEELER
ABSTRACT Indices of bone mass were measured in 23 volunteers weekly over 14-16 weeks using dual-energy x-ray absorptiometry (DEXA) and special-purpose computed tomography (y-CT). In vitro, the precision for both systems was excellent (coefficient of variation < 0.5%). Over 4 months, the precision in vivo (average CV for all subjects) for DEXA measures (BMD, g/cmZ, and BMC, g/cm) varied between 0.6 and 1.1%; with y-CT it varied from 1.1% for TBD (g/cm3) to 2.2% for CBD (g/cm3). Correlation between the indices of bone mass measured using DEXA and y C T at the ultradistal site was moderate, but these indices were not correlated at the distal third site. When BMD and BMC were derived from the CT index IBD, however, the correlation between these y-CT indices and the corresponding DEXA indices was high for both ultradistal and proximal radial sites.
INTRODUCTION
using computed tomography (CT) were pioneered by Ruegsegger and his colleagues.(121This technique has now been developed to permit the separate evaluation of traINGLE-PHOTON ABSORPTIOMETRY (SPA) has been widely used for more than 20 years to measure bone mineral becular (TBD), cortical (CBD), and total (IBD) bone denFor clinically ac- sities (g/cm3), in the distal forearm and in the proximal content (BMC, g/cm) in the ceptable performance, SPA has generally been limited to tibia, with a precision in vivo between 0.3 and 0.6% for recortical bone measurements in the distal third of the ra- peated measurements in healthy subjects over periods of dius, where a precision of between 2 and 3% can be ob- up t o 50 day^.('^-'^) Although currently available in only a tained routinely in longitudinal in vivo studies in young few research centers, the peripheral C T technology is an healthy subjects. Bone mineral density (BMD, g/cmZ) mea- important research tool that has facilitated monitoring of surements in the ultradistal radius using rectilinear SPA short-term transients in bone mineral distributions in scanning techniques are now also widely available and vivo(16)and has also been used to show that the rate of aphave a reported precision in vivo between 1 and 3 v 0 . ' ~ ) pendicular bone loss in individual subjects changes over Dual-energy x-ray absorptiometry (DEXA), a newly de- time. ( 1 The purposes of this study were threefold: veloped technology for BMD measurements in the spine and proximal femur, is also easily adapted for BMD measure1. T o determine in vivo precision for BMD and BMC ments at sites in the peripheral skeleton. For bone mass mea- measurements in the ultradistal and distal third radius surements in the lumbar spine and proximal femur, DEXA using DEXA (Hologic QDR 1000 system) 2 . To determine in vivo precision for TBD, CBD, and has significantly better precision than dual-photon absorptiometry (DPA).('-II) Given the demonstrated superior perfor- IBD measurements in the ultradistal and distal third radius mance of DEXA in axial skeleton measurements, we antici- using y-ray C T (7-CT) pated that DEXA could also be used for routine, high-preci3. To correlate the indices of bone mass measured in the sion bone mass measurements in the appendicular skeleton. distal forearm using DEXA with those measured using Bone mass measurements in the peripheral skeleton Y-CT
S
Department of Applied Sciences in Medicine, University of Alberta, Edmonton, Canada.
375
OVERTON A N D WHEELER
376
MATERIALS A N D METHODS In response to requests for volunteers from staff fitness classes, 23 healthy subjects (18 men and 5 women) aged 27-61 years (mean 48 years; standard deviation, SD 14 years) were entered into this study. Written informed consent was obtained from all participants in a manner approved by an institutional ethics review committee. Brief questionnaires concerning medical, dietary, physical activity, and life-style histories were completed by all subjects before acceptance into the study. No study participant had any disease known or suspected of skeletal effect or had taken medication that might have had a skeletal effect within 6 months immediately preceding this study. All were nonsmokers, no more than social consumers of alcohol, and participants in organized, 1 h long fitness classes at least thrice per week. Anthropometric data for study subjects are shown in Table I . Both y-CT and DEXA measurements were made on the same day each week over 14-16 consecutive weeks for 21 subjects; for 1 subject there was a 4 week break in the protocol for vacation. One subject dropped out of the study after 8 weeks upon confirmation of pregnancy. All available subject data at each time point are included in the analysis. Using y-CT, bone density measurements were made for the ultradistal and distal third radius employing well-established Briefly, the subject was positioned for each measurement with a preliminary C T scout view to precisely locate the distal surfaces of the radial and ulnar condyles using an interactive, semiautomatic image analysis program. For each subject, both measurement sites were defined relative to these anatomic landmarks. At the ultradistal site CT measurements were started 2 mm proximal to the lowest part of the radial end plate and extended 14-16 mm proximally from that position. The most distal part of the distal third radial site was located individually for each subject at one-third of the ulnar length measured from the radial condyle and extended 6-8 mm proximal to that location. The location of the ultradistal site and of the volumes used for evaluation of the bone mass indices are shown schematically in Fig. 1. Using y-CT, the repositioning precision was better than +0.2 mm. The measurement time for each transaxial slice was 90 s, and six to eight C T slices were obtained at the ultradistal site and three to four slices at the distal third site for each subject visit. The y-CT system was calibrated daily using a cylindrical radius phantom made of plexiglass (soft tissue, Teflon (fat), and aluminum (bone); a cylindrical, stepped-thickness (0.5-4 mm) aluminum tube phantom was also used to calibrate for the thicker cortical bone measurement at the distal third site. ( I 5 ) A two-component tissue model was assumed for the measured bone volume(1a)and C T variables (TBD, CBD, and IBD) expressed as physical densities (g/cm3). To emphasize the similarities in indices of bone mass measured by y-CT and DEXA, we also derived BMD (g/cm*) and BMC (g/cm) from the C T index IBD (g/cm3). This conversion was made as follows. For each C T slice the volume was determined from the measured slice area (number of pixels) and the fixed slice thickness (2 mm). Since the
TABLt 1 .
CHARACTERISTICS OF STUDYPOPULATION
*\\THROPOMETRIC
THE
~~~~
Subject
Age (years)
Se.v
Height (cm) ~~
F M M M F M
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
M M M M M F 11
r \I \I \I hl
M M M F M
The trabecrj' volume wrthin tt m e SLI numb f
48 45 32 31 25 45 55 51 46 56 45 46 52 45 72 52 54 29 60 49 58 46 34
I.
Weight (kg)
~
161.3 185.5 169.5 171.6 159.0 181.5 174.8 177.0 176.2 174.5 161.5 160.0 177.5 175.2 173.9 172.4 167.0 186.0 180.5 178.5 176.5 156.5 177.8
60.2 84.2 67.0 68.8 57.0 74.8 71.8 97.3 79.3 65.9 54.9 60.0 71.5 72.9 77.9 92.0 59.6 70.2 83.2 81.2 70.0 62.3 74.0
hme space (TBS) 1 by the area jr
of each slice. n). and the ir averaging
~
Average p x r l V~IIIIC hctween the 75% and 95% area conloiirs determines CBD
.
~
Average pixel value wrthin the 100% area conlour determines IBD ~
~~
Average pixel value wlthin m e 45% area contour determines TBD ~
FIG. 1. Radial ultradistal measurement site used in y-CT. The particular bone volumes averaged for determinations of TBD, CBD, and 1BD are shown. Both ultradistal and distal third measurement sites are located relative to the radial styloid. At the ultradistal site the bone volumes evaluated by y-CT and DEXA are similar; at the distal third site the DEXA analysis is for approximately twice the volume evaluated using y-CT.
377
DEXA AND y-CT MEASURES OF RADIAL BONE MASS measured slice volume and the average IBD are invariant with respect to rotation of the arm, the projected area of each slice can then be approximated as a product of the diameter of the circle with the same area as the slice and the slice thickness. The total measurement volume and projected area are the respective sums for all slices included in the evaluation. Using DEXA (Hologic QDR 1O00), forearm BMD and BMC measurements were made with the subject’s right arm placed palm down on the scanning table with the lateral forearm pressed lightly against the edge of a dense foam block. A single scan (120-150 contiguous translations of an approximately 1 mm wide beam) was then made, beginning distal to the radial condyle and covering both the ultradistal and distal third radius and ulna. A high-resolution scan and analysis software supplied by the manufacturer were used to obtain values for BMD and BMC at ultradistal and distal third sites for radius and ulna combined and for the radius alone. For the ultradistal site the distal limit of the analysis region was 2 mm proximal to the lowest part of the radial end plate and extended I5 mm proximally from that location. For the distal third site the distal limit of the analysis region was at one third of the ulnar length measured from the radial condyle and extended 15 mm proximally from that location. The total measurement time was between 7 and 8 minutes for all subjects. The DEXA system was calibrated daily using the calcium hydroxyapatite spine phantom supplied with the instrument. Correspondence between the longitudinal positions of the bone volumes evaluated using y-CT and DEXA was good (*0.5 mm). At the ultradistal site the estimated maximum difference between the volumes of bone evaluated by the two instruments is 7%. At the distal third site the bone volume evaluated using y-CT was about one-third of that for DEXA and was completely within the DEXA analysis volume. However, it is not necessary to measure exactly the same bone volume with both methods unless absolute comparisons of bone mass are to be made. For both y-CT and DEXA, bone mass indices are averaged over volumes of several milliliters. Small, local heterogeneities in mineral distribution are therefore relatively unimportant when comparisons are made between the indices of bone mass obtained with the two methods.
RESULTS
In vivo studies y-Ray CT: For ultradistal and distal third radius, regressions of TBD, CBD, and IBD with time were calculated; the regression line slope was not significantly different from zero @ < 0.001) for any variable in any subject. For each bone index an average coefficient of variation was calculated from the 14-16 measurements in each of 22 subjects, and 8 measurements in 1 subject, to be used to indicate in vivo performance of the y-CT method (Table 2). The correlation coefficient r and SEE (standard error of the estimate, determined from the regression and expressed as a percentage of the mean index value) between CT indices of bone mass measured at the ultradistal and distal third radius are given in Table 3. A source change (1251)was made for the y-CT system 8 weeks into this study. T o investigate the possible effects of the source change on measured bone mass indices, we separately analyzed data for the first 8 weeks and the last 6 weeks for each subject. There was no influence of source change on the regressions of bone mass indices with time, but there was a small (NS, not significant) increase in mean values for these indices after the source change. D E X A (QDR 1000): Using standard software supplied by Hologic Inc., BMD and BMC were evaluated for the ultradistal and distal third regions and for the total scan area of the forearm; the analysis was made for radius and ulna together and for radius aone. For each subject and for each bone mass index, linear regressions with time were calculated; the regression line slope was not significantly different from zero @ < 0.001) for any index in any subject. The average coefficient of variation (CVVo) and standard deviation of this coefficient for BMD and BMC at these sites are given in Table 4. Correlations between DEXA measures of BMD and BMC at different sites for the radius alone are shown in Table 5 as correlation coefficient r and SEE (determined from the regression and expressed as a percentage of the mean index value). In this report, the results for the analysis of the radius alone are presented since this bone was also measured using y-CT. However, the results for the radius and ulna combined were also obtained; these were almost identical to the results for radius alone and generally had a slightly better measurement precision. Correlation Between y-CT and DEXA Indices of Bone Muss: Correlation between y-CT and DEXA bone mass
In vitro studies Long-term, in vitro precision for y-CT and DEXA was determined from regressions with time of phantom TBD and BMD measurements, respectively. Using y-CT, the measurement precision for the linear attenuation coefficient of plexiglass within a cylindrical aluminum annulus was 0.46% (CV) over 5 years and, for the most recent year, which includes the period of this study, was 0.37%. Using DEXA, the precision over 1.5 years was 0.44% (CV) for a BMD measurement of calcium hydroxyapatite vertebral sections embedded in Lucite; for a 6 month period encompassing the present study the CV was 0.43%.
TABLE2. AVERAGE COEFFICIENT OF VARIATION(qo) AND SD FOR y-CT INDICESOF BONEMASSIN THE ULTRADISTAL A N D DISTAL THIRD RADIUS~
Radius Ultradistal Distal third
TBD, CV% (SD) 1.1 (0.5)
CBD, C V % (SD)
IBD, C V % (SD)
1.8 (0.7)
I .4 (0.6) 2.0 (1.5)
2.2 (1.1)
aThere were 14-16 measurements in each of 22 subjects and 8 measurements in 1 subject over 4 months.
OVERTON A N D WHEELER
378
(SEE) TABLE3. CORRELATION COEFFICIENT AND STANDARD ERROROF THE ESTIMATE FROM THE REGRESSION AND EXPRESSED AS A PERCENTAGE OF THE APPROPRIATE MEAN DETERMINED I N D E X VALUE BETWEEN y-CT INDICES OF BONEMASSAT ULTRADISTAL AND DISTAL THIRD RADIUS
Ultradistal radius r (SEE%) TBD UD radius CBD IBD BMD BMC D 1/3 radius CBD I BD BMD BMC
CBD
IBLI
0.63 0.84 0.75 0.58
(14) (10) (13) (15)
0.95 (3.8) 0.74 (8.0) 0.49 (10)
0.82 (7.0) 0.58 (10)
0.94 (5.2)
0.10 0.20 0.39 0.33
(17) (17) (17) (16)
0.43 (9.0) 0.44 (10.7) 0.46 (10.6) 0.30 (11.8)
0.34 (10.2) 0.39 (11.5) 0.47 (10.9) 0.34 (11.8)
0.01 (-) 0.02 ( - ) 0.74 (10) 0.74 (10)
TABLE4. AVERAGE CV (vo) A N D SD FOR DEXA INDICESOF BONEMASSIN DISTALFOREARM^
Site Ultradistal radius Distal third radius Ultradistal radius and ulna Distal third radius and ulna Total scan area
BMD
BMD, CV% (SO)
BMC, CV% (SO)
0.8 (0.3) 1 . 1 (0.4) 0.8 (0.3) 0.7 (0.3) 0.6 (0.3)
1 .O (0.6) 1 .O (0.5) 0.8 (0.4) 0.7 (0.3) 0.6 (0.3)
~
dThere were 14-16 measurements in each of 22 subjects and 8 measurements in 1 5ubject over 4 months.
indices for the ultradistal and distal third radius, respectively, are shown in Tables 6 and 7 as correlation coefficient r and SEE (determined from the regression and expressed as a percentage of the average index value). For the ultradistal radius, correlations between the y-CT bone mass indices TBD, BMD, and BMC and DEXA indices BMD and BMC are shown graphically in Fig. 2a through d; for the distal third radius these relationships are shown in Fig. 2e and f . For each comparison the least-squares regression line is shown. Since the estimations of mean index values made before and after the 1251 source change in the y-CT system are independent, we combined both data sets for determinations of correlations between y-CT and DEXA, and thus 46 mean values (for 23 subjects) are plotted in the several correlations shown in Fig. 2.
DISCUSSION In vitro, the precision of y-CT and of DEXA during the 4 months of this study were similar (CV better than 0.5%) to their respective longer term precisions. Both y-CT and DEXA also showed excellent in vivo precision for repeated bone mass measurements at ultradistal
BMC
-
0.22 0.20 0.78 0.85
(15) (18) (1 3) (10.8)
and distal third sites in the radius over a 4 month period. Using y-CT, 330 TBD measurements of the ultradistal radius, made in 23 subjects over 4 months, had an average error (CV) of 1.1% (range 0.3-1.6%). This error is larger than the 0.6% previously reported from this laboratory for five subjects over 50 days.'L6'However, the present result is probably a better indicator of the average, long-term clinical performance of the y-CT system since it reflects the combined effects of a change to a '"I source in the middle of this study, of three different machine oeprators, and of normal, individual biologic variation in mineral distribution in the forearm over time in a heterogeneous group of subjects. In addition to our routine TBD analysis, we also evaluated cortical and integral bone densities in the ultradistal radius in this study. Errors in CBD and IBD values are higher than for TBD (1.8 and 1.4%, respectively) since the additional steps required in the analysis process and the differences in the volume evaluated (particularly for CBD) contribute to the overall precision error. At the ultradistal radius, the correlation between TBD, CBD, and IBD is moderate ( r = 0.63 and 0.84, respectively) but not predictive (SEE = 14 and lo%, respectively) since different proportions of cortical and trabecular bone are compared in these indices. CBD and IBD were highly correlated ( r = 0.95, SEE = 3.8%), however, indicating a relatively large cortical bone contribution to integral bone measurements in the ultradistal radius (Table 3). At the distal third radius site, errors in CBD and IBD measurements are higher than at the ultradistal site (2.2 and 2.09'0, respectively), and these indices are highly correlated ( r = 0.94, SEE = l.8%), since a transaxial section at this site generally contains only cortical bone and marrow. The increased errors in CBD and IBD measurements at the distal third site are principally due to the much smaller bone volume used in the evaluation process and to the increased number of steps in the data analysis. Using DEXA, both BMC and BMD were calculated for radius and ulna combined and for the radius alone. Over the 4 month period of this study the average CV for radius and ulna combined at the ultradistal site in 330 measure-
379
DEXA AND 7-CT MEASURES OF RADIAL BONE MASS TABLE5 . CORRELATION COEFFICIENT r A N D SEE DETERMINED FROM 'THE REGRESSION AND EXPRESSED AS A PERCENTAGE OF THE APPROPRIATE MEANINDEXVALUEBETWEENDEXA INDICES OF BONEMASSAT ULTRADISTAL AND DISTALTHIRDSITESAND FOR T H E TOTAL SCANAREAIN THE RADIUS
Ultradistal r (SEE%) BMD Ultradistal BMC Distal third BMD Distal third BMC Total scan area BMD Total scan area BMC
0.92 0.75 0.75 0.90 0.74
Distal third r (SEE%)
BMC
(5.1) (6.5) (8.4) (5.6) (8.7)
BMD
BMC
Total BMD, r (SEE%)
-
0.80 (11.6) 0.89 (7.9) 0.90 (8.3) 0.90 (8.7)
-
0.93 (3.5) 0.93 (3.7) 0.88 (4.6)
-
0.90 (7.6) 0.97 (4.2)
-
0.89 (4.5)
TABLE 6. CORRELATION COEFFICIENT r A N D SEE DETERMINED FROM 'THE REGRESSION AND EXPRESSED AS A PERCENTAGE OF THE APPROPRIATE MEANI N D E X V A L U E BETWEEN INDICES OF BONEMASSMEASURED BY y-CT A N D DEXA IN THE ULTRADISTAL RADIUS
y - C T r (SEE%) DEXA
TBD
CBD ~
BMD
BMC Total BMD Total BMC
0.734 (12) 0.527 (16) 0.528 (16) 0.527 (19)
~
0.721 0.455 0.592 0.248
(8.3) (10) (10) (11)
TABLE 7. CORRELATION COEFFICIENT r A N D SEE DETERMINED FROM THE REGRESSION A N D EXPRESSED AS A PERCENTAGE OF APPROPRIATE MEANVALUE BETWEEN INDICES OF BONEMASSMEASURED BY y-CT AND DEXA IN THE DISTAL THIRDR A D I U S ~ y-CT r (SEE%)
DEXA BMD BMC Total BMD Total BMC
BMD 0.924 (3.4) 0.898 (7.4) 0.891 (4.1) 0.856 (1 1)
IBD
BMD
BMC
0.778 (7.9) 0.509 (1 1) 0.621 (10) 0.304 (12)
0.958 (3.4) 0.902 (7.9) 0.884 (4.2) 0.741 (14)
0.900 (5.2) 0.978 (3.9) 0.892 (4.1) 0.879 (10)
~~
BMC 0.929 0.980 0.879 0.948
(3.3) (3.3) (4.3) (6.9)
aOnly the derived indices (BMD and BMC) for y-CT are shown since both cortical (CBD) and integral (IBD) bone densities (g/ cm') are constant in the distal third radius and thus are not correlated with DEXA measures of bone mass.
ments in 23 subjects was 0.8% for both BMD and BMC; for radius alone, the average CV was 0.8 and 1070 for BMD and BMC, respectively. For the distal third site, the average CV for both BMD and BMC measurements in the radius and ulna combined was 0.7% and, in the radius alone, 1.1 and 1 .O%, respectively. Over the total scan area, the average CV was 0.6% for both indices (Table 4). The average in vivo precision for BMD and BMC measurements in the distal forearm using DEXA is generally better than that obtained for the spine (IVo), probably as a result
of a better automatic definition of the outer contours of the radius and ulna. A modest improvement in precision is obtained when averaging over the total scan area (bout 130 mm length) rather than over a local area (e.g., 15 mm length for the ultradistal site). The correlation between DEXA indices of bone mass at three sites in the forearm was high (Table 5 ) . Comparisons between the principal indices of bone mass measured by y-CT and DEXA are shown in Fig. 2 and in Tables 6 and 7. The CT index TBD (g/cm3) is moderately correlated with the DEXA indices BMD (g/cm') and BMC (g/cm) at the ultradistal radius, but the SEE is large (Fig. 2a and b). However, the lack of a predictive relationship between TBD and the DEXA indices BMD and BMC is not unexpected given the differences in the proportions of trabecular and cortical bone measured by the two technologies and the differences in the units of measurement. When BMD and BMC' are derived from the integral bone density (IBD, g/cm3) measured by CT, however, these indices are highly correlated with the corresponding DEXA indices at both ultradistal (Fig. 2c and d) and distal third sites (Fig. 2e and f). Until now, most clinical appendicular bone mass measurements in the forearm have been made using SPA at distal third sites and rectilinear scanning SPA at ultradistal sites. For research applications special-purpose CT systems have been developed for high-precision measurements of both trabecular and cortical bone densities in the appendicular skeleton. Each of these technologies, however, has
OVERTON A N D WHEELER
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total forearm scan area. The DEXA indices also correlate highly with the y-CT indices BMD and BMC (derived from IBD), and at the ultradistal site BMD is also moderately correlated with the average physical density of trabecular bone (TBD, g/crn3). For longitudinal BMD measurements in individual healthy subjects, the precision varied between 0.8 and 1.1% at the ultradistal radius site. In osteopenic subjects the measurement precision is lower, however, because of the excellent correlation between local and total BMD and BMC measures; larger scan areas, perhaps including both radius and ulna, could then be evaluated to improve performance. A Hologic QDR lo00 was used in this work, but we expect that DEXA machines from other manufacturers would have a similar performance in appendicular bone measurements.
ACKNOWLEDGMENTS
0
DEXA
1 1
BHC
q/cm
3 0,
1 0
2 5
; .o
9
g 2 0
3 0.8 1 5 : 0
We particularly thank Joi Belyck, Tsylia Gorodetsky, and Nigel Gann for excellent technical support throughout this study. We greatly appreciate the generosity and cooperation of P.G. Heslip, M.D., who provided free access to the Hologic QDR lo00 in his laboratory. Finally, our biggest accolade goes to the 23 volunteers who, without complaint, attended our laboratories on a weekly basis over 4 summer months. This work was supported in part by Hologic Inc., Waltham, MA.
1
0 6
REFERENCES FIG. 2. Correlation between y-CT and DEXA indices of bone mass for the ultradistal radius (a-d) and for the distal third radius (e and f). Using y-CT, TBD, CBD, and IBD are measured indices; BMD and BMC are derived from IBD.
important practical limitations: the usefulness of SPA is limited to cortical bone measurements and usually to cross-sectional population studies; rectilinear scanning SPA, used at ultradistal sites, measures a greater proportion of trabecular bone and has an improved precision relative to SPA, but its application to longitudinal studies is still limited by poor precision; special-purpose C T systems have a high sensitivity and precision for TBD, CBD, and IBD measurements and are appropriate for both short-and long-term clinical longitudinal studies, but they are expensive, technically difficult to operate, and not widely available. In this study, using a Hologic QDR 1o00, we showed that DEXA has excellent in vivo precision for BMD and BMC measurements in the forearm. Repositioning subjects for repeated measurements using the QDR lo00 is very easy, and for the ultradistal site the scanning time is less than 3 minutes. There is a high correlation between the DEXA indices BMD and BMC measured at local sites (ultradistal, middistal, and distal third radius) and over the
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DEXA AND Y-CTMEASURES OF RADIAL BONE MASS 9. Borders J , Kerr E, Sartoris DJ, Stein JA, Ramos E, Moscona AA, Resnick D 1989 Quantitative dual-energy radiographic absorptiometry of the lumbar spine: In vivo comparison with dual-photon absorptiometry. Radiology 170:129131. 10. Gundry CR, Miller CW, Ramos E, Moscona A, Stein JA, Mazess RB, Sartoris DJ, Resnick D 1990 Dual-energy radiographic absorptiometry of the lumbar spine: Clinical experience with two different systems. Radiology 174:539-541. II. Gliier CC, Steiger P , Selvidge R, Elliesen-Kliefoth K, Hayashi C, Genant HK 1990 Comparative assessment of dual photon absorptiometry and dual-energy radiography. Radiology 174:223-228. 12. Riiegsegger P, Elsasser U , Anliker M, Gnehm H, Kind H, Prader A 1976 Quantification of bone mineralization using computed tomography. Radiology 121:93-97. 13. Riiegsegger P 1988 Quantitative computed tomography at peripheral measuring sites. Proceedings of Kuopio International Symposium on Osteoporosis. Ann Chir Gynaecol 77: 204-207. 14. Miiller A, Ruegsegger E, Riiegsegger P 1989 Peripheral QCT: A low risk procedure to identify women predisposed to osteoporosis. Phys Med Biol 34:741-749. 15. Hangartner TN, Battista J J , Overton TR 1987 Performance
38 1 evaluation of density measurements of axial and peripheral bone with x-ray and gamma-ray computed tomography. Phys Med Biol 32: 1393- 1406. 16. Hangartner TN, Overton TR, Harley CH. van den Berg L, Crockford PM 1985 Skeletal challenge: An experimental study of pharmacologically induced changes in bone density in the distal radius, using gamma-ray computed tomography. Calcif Tissue Int 37:19-24. 17. Riiegsegger P , Dambacher MA, Riiegsegger E, Fischer JA, Anliker M 1984 Bone loss in premenopausal and postmenopausal women. J Bone Joint Surg [Am] 66:1015-1023. 18. Hangartner TN, Overton TR 1982 Quantitative measurement of bone density using gamma-ray computed tomography. J Comput Assist Tomogr 616): 1 156- 1 162.
Address reprint requests to: Dr. T.R. Overton Department of Applied Sciences in Medicine University of Alberta Edmonton, Alberta, T6G 2G3, Canada Received for publication March 12, 1991; in revised form November 8, 1991; accepted Nobember 12, 1991.
