Published online before print March 28, 2006, 10.1148/radiol.2392050574
(Radiology 2006;239:488-496.)
© RSNA, 2006
Trabecular Bone Structure of the Calcaneus: Comparison of MR Imaging at 3.0 and 1.5 T with Micro-CT as the Standard of Reference1
Catherine M. Phan, MD,
Maiko Matsuura, MSc,
Jan S. Bauer, MD,
Timothy C. Dunn, BSc,
David Newitt, PhD,
Eva M. Lochmueller, MD,
Felix Eckstein, MD,
Sharmila Majumdar, PhD and
Thomas M. Link, MD
1 From the Department of Radiology, University of California, San Francisco, 400 Parnassus Ave, A 367, Box 0628, San Francisco, CA 94143-0628 (C.M.P., J.S.B., T.C.D., D.N., S.M., T.M.L.); Institute for Anatomy, University of Munich, Munich, Germany (M.M.); 1st Gynaecology Hospital, LMU, Munich, Germany (E.M.L.); and Institute for Anatomy, Paracelsus Medical Private University, Salzburg, Austria (F.E.). Received April 7, 2005; revision requested June 6; revision received June 30; accepted August 2. Supported by the Société Française de Radiologie, Philippe Foundation, Guerbet, and the German Research Foundation grant (Lo 730/3-1 and 3-2).
Address correspondence to T.M.L. (e-mail: tmlink{at}radiology.ucsf.edu).
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ABSTRACT
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Purpose: To investigate in vitro the calcaneal trabecular bone structure in elderly human donors with high spatial resolution magnetic resonance (MR) imaging at 3.0 T and 1.5 T, to quantitatively compare MR measures of bone microarchitecture with those from microcomputed tomography (CT), and to compare the performance of 3.0-T MR imaging with that of 1.5-T MR imaging in differentiating donors with spinal fractures from those without spinal fractures.
Materials and Methods: The study was performed in line with institutional and legislative requirements; all donors had dedicated their body for educational and research purposes prior to death. Sagittal MR images of 49 human calcaneus cadaveric specimens were obtained (mean age of donors, 79.5 years ± 11 [standard deviation]; 26 male donors, 23 female donors). After the spatial coregistering of images acquired at 3.0-T and 1.5-T MR imaging, the signal-to-noise-ratios and structural parameters obtained at each magnetic field strength were compared in corresponding sections. Micro-CT was performed on calcaneus cores obtained from corresponding regions in 40 cadaveric specimens. Vertebral deformities of the thoracic and lumbar spine were radiographically classified by using the spinal fracture index. Diagnostic performance of the structural parameters in differentiating donors with vertebral fractures from those without was assessed by using receiver operator characteristic (ROC) analysis, including area under the ROC curve (Az).
Results: Correlations between structural parameters at 3.0-T MR imaging and those at micro-CT were significantly higher (P < .05) than correlations between structural parameters at 1.5-T MR imaging and those at micro-CT (trabecular thickness, r = 0.76 at 3.0 T vs r = 0.57 at 1.5 T). Trabecular dimensions were amplified at 3.0 T because of increasing susceptibility artifacts. Also, higher ROC values were found for structural parameters at 3.0 T than at 1.5 T, but differences were not significant (trabecular thickness, Az = 0.75 at 3.0 T vs Az = 0.66 at 1.5 T, P > .05).
Conclusion: MR imaging at 3.0 T provided a better measure of the trabecular bone structure than did MR imaging at 1.5 T. There was a trend for better differentiation of donors with from those without osteoporotic vertebral fractures at 3.0 T than at 1.5 T.
© RSNA, 2006
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INTRODUCTION
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Several publications have suggested that alterations in bone architecture could explain bone fragility independent of bone mass in osteoporosis (17). Evaluating bone mass with only bone mineral density (BMD) by using dual x-ray absorptiometry or quantitative computed tomography (CT) therefore may be insufficient to fully assess the biomechanical strength of the trabecular bone or the fracture risk (69). The importance of assessing the architecture of the trabecular bone in conjunction with BMD has been established in several studies (1014). Recent advances in magnetic resonance (MR) imaging, especially the improvement of spatial resolution, allow noninvasive evaluation of trabecular bone microarchitecture in the clinic under in vivo conditions. Furthermore, different in vitro studies have shown significant correlations between structural measures obtained at 1.5-T MR imaging and the true trabecular bone structure visualized with contact radiography and micro-CT (1518).
Among the recent advances in MR imaging, the increase of the magnetic field strength is one of the most important. The recent development of clinical 3.0-T MR imaging has been stimulated by promise of increased signal-to-noise ratio (SNR). Higher magnetic field strength may be used to improve image quality, decrease the length of total imaging time, and increase spatial resolution. Disadvantages of imaging at 3.0 T, however, have to be considered; these include potential reduction of contrast in anatomic imaging due to lengthening of T1 and increased susceptibility effects at high field strengths.
The purpose of our study was to investigate in vitro the calcaneal trabecular bone structure in elderly human donors with high spatial resolution MR imaging at 3.0 T and 1.5 T, to quantitatively compare MR measures of bone microarchitecture with those from micro-CT, and to compare the performance of 3.0-T MR imaging with that of 1.5-T MR imaging in differentiating donors with spinal fractures from those without spinal fractures.
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MATERIALS AND METHODS
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Specimens
For this study, calcaneus, femur, and spine specimens were obtained from 49 formalin-fixed human cadavers. All specimen procedures were performed in accordance with legislative and institutional guidelines. The cadaveric specimens originated from the Institute of Anatomy at the University of Munich. The donors had dedicated their body for educational and research purposes to the Institute of Anatomy prior to death, in line with the local legislative requirements. Donors with a history of metastatic hematologic disease or metabolic bone disorders other than osteoporosis had been excluded.
From each cadaver, the left calcaneus specimen was used for this study. The specimens were examined macroscopically and tagged with a numeric and color scheme to ensure anonymity. They were embedded in paraffin plates with markers filled with gadodiamide-doped (Omniscan; GE Healthcare, Waukesha, Wis) saline as landmarks to obtain identical slice positioning. From the same cadavers, the entire thoracic and lumbar spine and ipsilateral femur specimens were obtained for vertebral fracture assessment and BMD measurements. The mean age of the study population was 79.5 years ± 11 (standard deviation)(age range, 5598 years), and the study included 26 male (mean age, 76 years ± 10.5) and 23 female (mean age, 83.2 years ± 10.5) donors.
MR Imaging
Sagittal high spatial resolution MR imaging of the calcaneus specimens was performed with a two-element phased-array wrist coil and a clinical 1.5-T and a 3.0-T imager (Signa; GE Healthcare, Milwaukee, Wis), both equipped with 44 mT/m gradients. At the two field strengths, a series of sagittal, transverse, and coronal gradient-echo MR sequences were used as localizers for the calcaneus. A set of 64 sagittal images of the calcaneus was obtained by using a three-dimensional fast gradient recalled echo sequence. At 1.5 T, parameters were as follows: repetition time, 20.0 msec; echo time, 5.1 msec; and acquisition time, 8 minutes 10 seconds. At 3.0 T, parameters were as follows: repetition time, 18.5 msec; echo time, 4.3 msec; and acquisition time, 7 minutes 34 seconds. At both 1.5 T and 3.0 T, parameters were as follows: flip angle, 20°; bandwidth, 12.5 kHz; field of view, 100 x 75 mm; section thickness, 0.5 mm; and matrix, 512 x 384 pixels with one signal acquired. Thus an in-plane spatial resolution of 156 x 156 µm at 1.5 and 3.0 T was obtained. SNRs were calculated from MR images by using the equation SNR = SIbm/SDbg, where SIbm is the signal intensity of bone marrow, and SDbg is the standard deviation of the background. SNR was determined in corresponding sections for each specimen at 1.5 and at 3.0 T. For the SNR measurements, one author (C.M.P., 5 years of experience with musculoskeletal MR imaging) placed circular regions of interest (ROIs) with a diameter of at least 10 pixels on the bone marrowcarefully avoiding areas of trabecular boneand in the background in the superior left part of the image with the largest possible diameter. These measurements were intended to compare SNR determined in the fatty bone marrow at 1.5 T with that at 3 T.
Micro-CT Scanning
After MR imaging, micro-CT was performed on trabecular bone cores obtained from 40 available calcaneus specimens (µCT 20 scanner; Scanco Medical, Bassersdorf, Switzerland). These cylindrical cores had a diameter of 8 mm and a length of 12 mm; they were retrieved perpendicular to the long axis of the calcaneus from the superior part of the inferior half of the calcaneus at the intersection of a vertical line from the posterior border of the talar cartilage. All specimens were scanned with medium scan mode, which for this device is defined as a spatial resolution of 26 µm isotropic.
Image Analysis
To better compare images obtained at 1.5 T with those at 3.0 T, dedicated software (Analyze; Biomedical Imaging Resource Mayo Foundation, Rochester, Minn) based on an isocoordinate base volume registration was used for spatial coregistration to allow for a reliable resampling of the matched volumes during the registration. Image analysis included first the application of a low-pass filterbased coil sensitivity correction (19). The next step of image analysis was the binarization of the MR images on the basis of a dual reference model and on the assumption of a biphasic distribution previously described by Majumdar et al (20). The number of sections covering the calcaneus in the sagittal orientation was recorded, and the 20 sections (1-cm slab) located in the center of the calcaneus were chosen for image analysis. Circular ROIs with a diameter of 10 mm were placed by one author (C.M.P.) in the area where the bone cores had been removed, which was the superior part of the inferior half of the calcaneus at the intersection of a vertical line from the posterior border of the talar cartilage. The radiologist who placed the ROIs was blinded to micro-CT and BMD data, as well as to fracture status of the spine.
Histomorphologic Parameters
Structural parameters equivalent to bone histomorphometry were calculated with MR imaging and micro-CT data sets. The structural parameters included the proportion of bone volume to total volume (BV/TV), trabecular number (1/millimeter), trabecular thickness (millimeters), and trabecular separation (average distance between the individual trabeculae) (millimeters). On the MR images, these parameters were defined as "apparent" because the spatial resolution is lower than that required for standard bone histomorphometry (24,25). For MR images, structural parameters were calculated by using the mean intercept length method based on the plate model with software developed in-house by using Interactive Display Language (version 6.0; Research Systems, Boulder, Colo) (26). For the micro-CT data, structural parameters were calculated by using the model-assumption-free three-dimensional distance transformation method (2123).
BMD Measurements
Dual x-ray absorptiometry was used to determine the BMD at two sitesthe left proximal femur and the posterior part of the calcaneusby using a scanner (Lunar Prodigy; GE Healthcare). The femur specimens were positioned similar to in vivo conditions, which was mildly internally rotated, in a vessel filled with tap water up to 15 cm to simulate soft tissues. By using the manufacturer's automated software, BMD in the four standard ROIsthe femur neck, trochanter, intertrochanteric region, and the total femur ROIwas measured. The ROIs were checked for accuracy by a radiologist (T.M.L., 17 years of experience with musculoskeletal imaging). The calcaneus was placed in the scanner in a lateral position and was covered with saline-filled bags to simulate soft tissue. The heel region was scanned with a forearm algorithm by using a pencil-beam x-ray mode, and BMD (grams per square centimeter) was measured in a round ROI placed by a radiologist (C.M.P.) in the posterior region of the calcaneus, similar to ROI placement used for the MR images.
Fracture Assessment on Radiographs
Fracture status of the thoracic and lumbar spine was assessed on lateral radiographs by a radiologist (T.M.L.) and graded with the spinal fracture index, previously described by Genant et al (27): Deformities with height reductions greater than 20% are scored as fractures, grade 1 fractures are defined as deformities with a height reduction of 20%25%, grade 2 fractures have a height reduction of 25%40%, and grade 3 fractures have a height reduction larger than 40%. The spinal fracture status was defined to be the maximum grade of deformity within the spine. The radiologist who graded the radiographs was blinded to the results of all quantitative data analyses.
Statistical Analysis
The means and standard deviations of BMD measures derived from dual x-ray absorptiometry and structural parameters derived from MR imaging and micro-CT were calculated. Correlations between the individual structural parameters obtained with MR imaging, those obtained with micro-CT, and BMD measures obtained with dual x-ray absorptiometry were assessed by using linear regression analysis. Differences between parameters were evaluated by using two-tailed t tests of significance. In addition, we used the bootstrap method to compare correlations between BMD measures, micro-CTderived parameters, and MR-derived parameters (28). The statistical computations were processed with software (JMP, SAS Institute, Cary, NC; SPSS version 11.5, SPSS, Chicago, Ill). Receiver operator characteristic (ROC) analyses were performed for structural measures and BMD measures to estimate their power for differentiating fractured from nonfractured status in donors. By comparing the areas under two or more ROC curves, a nonparametric approach was applied. A level of significance of P < .05 for comparative measurements was used throughout the study.
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RESULTS
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Structural Parameters at 1.5- and 3.0-T MR Imaging
By using a two-tailed t test for the quantitative analysis, either significantly (P < .05) higher or lower structural parameters were obtained at 3.0 T than at 1.5 T (Table 1). Apparent BV/TV, apparent trabecular number, and apparent trabecular thickness were higher at 3.0 T, while apparent trabecular separation was lower at 3.0 T. The 3.0-T1.5-T measurement ratio showed that apparent BV/TV was approximately 1.4-fold higher, apparent trabecular number and apparent trabecular thickness were 1.2-fold higher, and apparent trabecular separation was 0.7-fold lower at 3.0 T than at 1.5 T (Table 1).
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Table 1. Structural Parameters Derived from 1.5-T MR Images, 3.0-T MR Images, and Micro-CT Images and MRMicro-CT Ratios of Corresponding Results
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Structural parameters were not significantly correlated with age given the relatively narrow age range in this elderly population (P > .05). Sex differences were not observed in the structural parameters obtained at 3.0 T, while at 1.5 T apparent BV/TV and apparent trabecular numbers were mildly, yet significantly (P < .05), higher in the male donors, and apparent trabecular separation was higher in the female donors.
The SNR was only 26% higher in the 3.0-T images compared with the 1.5-T images (12.9 at 1.5 T vs 16.3 at 3.0 T). Overall, however, substantially better visualization of the trabeculae at 3.0 T compared with that at 1.5 T was demonstrated (Fig 1). Differences in the dimensions of the trabeculae are also appreciated qualitatively on the images as reflected in the quantitative structure assessment. At 3.0 T, the trabeculae appeared thicker in diameter and better defined than at 1.5 T, and intertrabecular spaces appeared smaller at 3.0 T than at 1.5 T. The differences between osteoporotic and normal trabecular bone structure were qualitatively better visualized at 3.0 T than at 1.5 T (Figs 1, 2).

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Figure 1a: MR images (a, b) at 1.5 T and (c, d) at 3.0 T from calcaneus specimens acquired with fast gradient recalled echo sequence. Images b and d demonstrate specimen with scarce trabecular structure (donor had multiple osteoporotic compression deformities of spine), and a and c demonstrate specimen with dense, well-interconnected trabecular bone structure (donor had no osteoporotic deformities of spine).
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Figure 1b: MR images (a, b) at 1.5 T and (c, d) at 3.0 T from calcaneus specimens acquired with fast gradient recalled echo sequence. Images b and d demonstrate specimen with scarce trabecular structure (donor had multiple osteoporotic compression deformities of spine), and a and c demonstrate specimen with dense, well-interconnected trabecular bone structure (donor had no osteoporotic deformities of spine).
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Figure 1c: MR images (a, b) at 1.5 T and (c, d) at 3.0 T from calcaneus specimens acquired with fast gradient recalled echo sequence. Images b and d demonstrate specimen with scarce trabecular structure (donor had multiple osteoporotic compression deformities of spine), and a and c demonstrate specimen with dense, well-interconnected trabecular bone structure (donor had no osteoporotic deformities of spine).
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Figure 1d: MR images (a, b) at 1.5 T and (c, d) at 3.0 T from calcaneus specimens acquired with fast gradient recalled echo sequence. Images b and d demonstrate specimen with scarce trabecular structure (donor had multiple osteoporotic compression deformities of spine), and a and c demonstrate specimen with dense, well-interconnected trabecular bone structure (donor had no osteoporotic deformities of spine).
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Figure 2a: Representative MR images obtained at (a) 1.5 T and (b) 3.0 T. Circle indicates the corresponding region of (c) micro-CT image. Details of trabecular structure are more apparent on b.
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Figure 2b: Representative MR images obtained at (a) 1.5 T and (b) 3.0 T. Circle indicates the corresponding region of (c) micro-CT image. Details of trabecular structure are more apparent on b.
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Figure 2c: Representative MR images obtained at (a) 1.5 T and (b) 3.0 T. Circle indicates the corresponding region of (c) micro-CT image. Details of trabecular structure are more apparent on b.
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MR-derived versus Micro-CTderived Structural Parameters
The structural parameters obtained from the micro-CT data sets were either significantly (P < .05) higher or lower than those obtained from MR imaging data sets (Table 1). The ratio of apparent BV/TV was approximately threefold higher at 3.0 T and 2.2-fold higher at 1.5 T than at micro-CT, while the ratio of apparent trabecular number was 1.6-fold higher at 3.0 T and 1.3-fold higher at 1.5 T than at micro-CT. The ratio of apparent trabecular separation was 0.5-fold lower at 3.0 T and 0.7-fold lower at 1.5 T than at micro-CT.
Significant (P < .05) correlations were obtained between all structural parameters derived from MR imaging at both field strengths and structural parameters derived from micro-CT. Micro-CT parameters were used as a standard of reference for the depiction of bone microarchitecture (Fig 2). These correlations were significantly (P < .05) higher at 3.0 T than at 1.5 T (Table 2). At 3.0 T, the highest correlations were obtained for apparent BV/TV (r = .87) and apparent trabecular separation (r = 0.87), while at 1.5 T the highest correlations were obtained for apparent trabecular number (r = 0.76) and apparent trabecular separation (r = 0.72). Figure 3 shows scatter plots and the linear regression of 1.5-T and 3.0-T MRderived versus micro-CTderived structural parameters. No significant differences in the slopes of the two regression lines were found (P > .05); however, except for apparent trabecular thickness, all intercepts were significantly different (P < .05). We also calculated the number of outliers by using a threshold of two for the standardized residual (residual divided by standard deviation) and found three outliers for BV/TV at 1.5 T and two at 3.0 T, one for trabecular separation at 1.5 and one at 3.0 T, one for trabecular number at 1.5 T and two at 3.0 T, and two for trabecular thickness at 1.5 T and one at 3.0 T. This was considered acceptable; given n = 40, we would expect approximately two outlier values, because at a standardized residual threshold of two we are looking for 95th percentile values and would get five of 100 from a perfect normal distribution.

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Figure 3a: Scatter plots demonstrate relationships between MR- and micro-CTderived measures. Linear regression was used to obtain correlation between measures. Correlations for each structural parameter are (a) apparent BV/TV: r = 0.68 at 1.5 T, r = 0.87 at 3.0 T; (b) apparent trabecular number (Tb.N): r = 0.76 at 1.5 T, r = 0.79 at 3.0 T; (c) apparent trabecular separation (Tb.Sp): r = 0.72 at 1.5 T, r = 0.87 at 3.0 T; and (d) apparent trabecular thickness (Tb.Th): r = 0.57 at 1.5 T, r = 0.76 at 3.0 T. All correlations were significant (P < .05).
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Figure 3b: Scatter plots demonstrate relationships between MR- and micro-CTderived measures. Linear regression was used to obtain correlation between measures. Correlations for each structural parameter are (a) apparent BV/TV: r = 0.68 at 1.5 T, r = 0.87 at 3.0 T; (b) apparent trabecular number (Tb.N): r = 0.76 at 1.5 T, r = 0.79 at 3.0 T; (c) apparent trabecular separation (Tb.Sp): r = 0.72 at 1.5 T, r = 0.87 at 3.0 T; and (d) apparent trabecular thickness (Tb.Th): r = 0.57 at 1.5 T, r = 0.76 at 3.0 T. All correlations were significant (P < .05).
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Figure 3c: Scatter plots demonstrate relationships between MR- and micro-CTderived measures. Linear regression was used to obtain correlation between measures. Correlations for each structural parameter are (a) apparent BV/TV: r = 0.68 at 1.5 T, r = 0.87 at 3.0 T; (b) apparent trabecular number (Tb.N): r = 0.76 at 1.5 T, r = 0.79 at 3.0 T; (c) apparent trabecular separation (Tb.Sp): r = 0.72 at 1.5 T, r = 0.87 at 3.0 T; and (d) apparent trabecular thickness (Tb.Th): r = 0.57 at 1.5 T, r = 0.76 at 3.0 T. All correlations were significant (P < .05).
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Figure 3d: Scatter plots demonstrate relationships between MR- and micro-CTderived measures. Linear regression was used to obtain correlation between measures. Correlations for each structural parameter are (a) apparent BV/TV: r = 0.68 at 1.5 T, r = 0.87 at 3.0 T; (b) apparent trabecular number (Tb.N): r = 0.76 at 1.5 T, r = 0.79 at 3.0 T; (c) apparent trabecular separation (Tb.Sp): r = 0.72 at 1.5 T, r = 0.87 at 3.0 T; and (d) apparent trabecular thickness (Tb.Th): r = 0.57 at 1.5 T, r = 0.76 at 3.0 T. All correlations were significant (P < .05).
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Structural Parameters at MR Imaging and Micro-CT versus BMD
Correlations between MR-derived and micro-CTderived structural parameters and calcaneal BMD determined with dual x-ray absorptiometry were significant (P < .05) (Table 3). The highest correlations were observed for apparent BV/TV; these ranged from 0.73 for MR at 1.5 T to 0.79 for MR at 3.0 T and 0.8 for micro-CT. Correlations for calcaneal structural parameters and femoral BMD were also significant (P < .05) yet were substantially lower than those obtained with calcaneal BMD (Table 3). The highest correlations were again found for apparent BV/TV. There were no significant differences in the correlations between BMD and the structural parameters for the individual imaging modalities (P > .05).
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Table 3. Correlation between Structural Parameters Derived from MR and Micro-CT and Calcaneal and Femoral Neck BMD
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Performance in Assessing Vertebral Fracture Status
Results of the grading of the spine radiographs are presented in Table 4. The ROC analyses demonstrated that micro-CT and 3.0-T MR imaging compared with 1.5-T MR imaging and BMD were the best modalities to differentiate donors with from donors without vertebral fractures (Table 5). Among the structural parameters, apparent BV/TV and apparent trabecular thickness were most discriminative for micro-CT and 3.0-T MR imaging, while apparent trabecular number showed no significant difference at 3.0 T (P > .05). At 1.5 T, apparent trabecular number was the only parameter that showed a statistically significant difference in differentiating fracture from nonfracture subjects, while apparent BV/TV, apparent trabecular separation, and apparent trabecular thickness showed no significant difference in differentiating fracture from nonfracture subjects (P > .05). Among all the modalities, calcaneal BMD obtained the lowest area under the ROC curve. It should be noted, however, that no significant differences (P < .05) were found between the individual areas under the curve, which may be explained by the relatively low number of specimens available for the ROC analysis.
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Table 5. ROC Analysis to Quantify Performance of Modalities in Differentiating Cadaveric Donors with Vertebral Fractures from Those without
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DISCUSSION
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In this study we were able to show that trabecular bone architecture is better visualized at 3.0-T MR than at 1.5-T MR by using micro-CTderived structural measures as a standard of reference. By comparing MR images obtained from human calcaneus specimens, we observed a significantly higher SNR at 3.0-T MR than at 1.5-T MR and better correlations with micro-CTderived parameters at 3.0 T than at 1.5 T. With increasing field strength, however, an artificial amplification of the bony trabeculae is also noted. To our knowledge, this is the first study that directly compares MR imaging of trabecular bone structure at 1.5 T with that at 3.0 T.
MR imaging at 3.0 T has shown promise in musculoskeletal imaging, in particular in better depicting cartilage morphologic conditions (29,30). A previous preliminary study performed at 3.0 T in 15 human proximal femur specimens also found highly significant correlations between structural parameters derived from MR images and micro-CT data sets (31). In this study, however, the performance of different field strengths was not compared. Correlations between the individual parameters were mildly higher in that study than those obtained in our study. This could be explained by the fact that MR imaging was performed on whole calcaneus specimens in our study and micro-CT was performed on bone cores derived from these specimens with retrospectively matched ROIs, whereas in the previous study MR imaging and micro-CT were performed on the same bone cores at a higher spatial resolution. As in the current study, an amplification of the trabecular dimensions was found at 3.0 T; apparent BV/TV was overestimated by a factor of 2.44 and apparent trabecular number by a factor of 1.23, while apparent trabecular separation was underestimated by a factor of 0.62 (31). In our study, overestimations were slightly higher at 3.1 for apparent BV/TV, 1.6 for apparent trabecular number, and 0.5 for apparent trabecular separation. These results may also be explained by the lower spatial resolution used in our study.
Previous studies used 1.5-T MR imaging to assess bone architecture and also found highly significant correlations between MR-derived and micro-CTderived structural parameters (18,22,32). Laib et al (22) quantified trabecular bone microarchitecture on MR images of distal radius specimens and found correlations with the corresponding micro-CTderived parameters in the range of those that were found in our study, yet the spatial resolution used in these substantially smaller specimens was higher than the spatial resolution used in our study. On the other hand, Issever et al (18) and Link et al (32) found lower correlations in human proximal femur (up to r = 0.68) and distal radius specimens (up to r = 0.66) by using spatial resolutions more similar to those in this study.
The overestimation of trabecular dimensions found at 3.0-T MR imaging may be explained by an increase in susceptibility artifacts, which are particularly pronounced with gradient-echo sequences. However, even though artifacts were increased, correlations with micro-CTderived parameters were still higher at 3.0-T MR than at 1.5-T MR. To reduce this effect, spin-echo sequences have been applied (3234), with the disadvantage of a lower SNR and thus longer acquisition times, which are required to achieve comparable image quality. With the inherent higher SNR of MR imaging at 3.0 T, however, these sequences may become more attractive.
Theoretically, SNR provided from MR images should be two times higher at 3.0 T than at 1.5 T. In our study the improvement in SNR was substantially smaller. This may be partially explained by limitations in current coil design, which needs to be further improved as imaging sequences are adapted to exploit the full potential of 3.0-T imaging. Another explanation may be the increase in susceptibility effects, which amplify trabecular structures. These effects may have been noticeable in areas with apparent bone marrow too and could thus have potentially reduced SNR at 3.0 T. In addition, because of factors such as changes in tissue relaxation time, sensitivity to magnetic susceptibility, and chemical shift difference between fat and water, image sequences will have to be adjusted. A potential limitation of this study is that the fast gradient recalled echo sequence used at 3.0 T was similar to the sequence used at 1.5 T and was not fully adjusted to imaging at 3.0 T. However, we wanted to compare similar sequences and evaluate the effect of field strength on the depiction of the trabecular bone structure. Even better image quality is anticipated if imaging sequences are optimized to the higher field strength.
The effect of the spatial resolution also represents an important factor in the accurate assessment of the trabecular bone microarchitecture. Because of the limited spatial resolution of in vivo MR imaging measurements, the individual trabeculae are not depicted with their true thickness, and trabecular parameters are defined as apparent because the spatial resolution is lower than that required for standard bone histomorphometry (24,25). Clinical spatial resolution in 1.5-T MR images is limited to minimal voxel sizes of approximately 150 x 150 x 500 µm. With 3.0-T MR imaging, we may increase spatial resolution for clinical imaging and thus improve the visualization of the trabeculae, which reduces overestimation of trabecular dimensions. It has been shown by Kothari et al (35) that increase in spatial resolution particularly improves accuracies of apparent trabecular separation and apparent trabecular number. This will have to be the focus of future studies.
Vertebral fracture status has a central role in the assessment of osteoporosis and is an important predictor of future fractures (36). Our study showed a trend for better fracture discrimination with bone structure measures at 3.0 T as opposed to 1.5 T. This has clinical implications, as the presented imaging protocol is applicable in vivo. Structural measures of the calcaneus, however, may be even better suited to predict hip fractures than spine fractures (12,37).
In conclusion, the feasibility of imaging trabecular bone structure with MR at 3.0 T has been demonstrated in this study. Higher correlations were found between micro-CTderived structure measures and those obtained with MR at 3.0 T compared with those obtained at 1.5 T, which suggests that 3.0-T MR imaging may be better suited to assess trabecular bone microarchitecture. It was also shown, however, that intensified susceptibility artifacts increase the overestimation of the true trabecular dimensions.
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ADVANCES IN KNOWLEDGE
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- When compared with micro-CT, MR imaging better delineates trabecular bone architecture at 3.0 T than at 1.5 T.
- With increasing MR field strength, an artificial amplification of the bony trabeculae is noted.
- Subjects with vertebral fractures may be better differentiated from those without vertebral fractures at higher MR field strength.
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ACKNOWLEDGMENTS
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The authors acknowledge Roland Krug, PhD, Ying Lu, PhD, and Suchandrima Banerjee, MSc, for their substantial contributions.
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FOOTNOTES
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Abbreviations: BMD = bone mineral density BV/TV = bone volume to total volume ROC = receiver operator characteristic ROI = region of interest SNR = signal-to-noise ratio
Author contributions: Guarantor of integrity of entire study, C.M.P., M.M., S.M., T.M.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, C.M.P., J.S.B., T.C.D., T.M.L.; experimental studies, C.M.P., M.M., D.N., E.M.L., F.E., S.M.; statistical analysis, C.M.P., J.S.B., T.C.D., T.M.L.; and manuscript editing, all authors
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