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DOI:10.2214/AJR.07.2066
AJR 2007; 189:240-245
© American Roentgen Ray Society


Original Research

Fast High-Spatial-Resolution MRI of the Ankle with Parallel Imaging Using GRAPPA at 3 T

Jan Stefan Bauer1,2, Suchandrima Banerjee1,3, Tobias D. Henning1, Roland Krug1, Sharmilla Majumdar1,3 and Thomas M. Link1

1 Department of Radiology, University of California at San Francisco, San Francisco, CA.
2 Present address: Department of Radiology, Institut für Röntgendiagnostik, Technische Universität München, Ismaninger Str. 22, 81675 München, Germany.
3 UCSF & UCB Joint Graduate Group in Bioengineering, Berkeley, CA.

Received February 19, 2007; accepted after revision March 26, 2007.

 
J. S. Bauer and S. Banerjee equally contributed to this study.

Address correspondence to J. S. Bauer (jansbauer{at}gmail.com).


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of our study was to compare an autocalibrating parallel imaging technique at 3 T with standard acquisitions at 3 and 1.5 T for small-field-of-view imaging of the ankle.

MATERIALS AND METHODS. MRI of the ankle was performed in three fresh human cadaver specimens and three healthy volunteers. Axial and sagittal T1-weighted, axial fat-saturated T2-weighted, and coronal intermediate-weighted fast spin-echo sequences, as well as a fat-saturated spoiled gradient-echo sequence, were acquired at 1.5 and 3 T. At 3 T, reduced data sets were reconstructed using a generalized autocalibrating partially parallel acquisition (GRAPPA) technique, with a scan time reduction of approximately 44%. All images were assessed by two radiologists independently concerning image quality. The signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR) were measured in every data set. In the cadaver specimens, macroscopic findings after dissection served as a reference for the pathologic evaluation.

RESULTS. SNR and CNR in the GRAPPA images were comparable to the standard acquisition at 3 T. The image quality was rated significantly higher at 3 T with both normal and parallel acquisition compared with 1.5 T. There was no significant difference in ligament and cartilage visualization or in image quality between standard and GRAPPA reconstruction at 3 T. Ankle abnormalities were better seen at 3 T than at 1.5 T for both normal and parallel acquisitions.

CONCLUSION. Using higher field strength combined with parallel technique, MR images of the ankle were obtained with excellent diagnostic quality and a scan time reduction of about 44%. In addition, parallel imaging can provide more flexibility in protocol design.

Keywords: ankle pathology • cartilage pathology • GRAPPA • high-field 3-T MRI • ligament pathology • parallel imaging • scan time reduction • tendon pathology


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
High-field imaging—in particular, imaging at 3 T—has been shown to improve musculoskeletal imaging compared with imaging at 1.5 T [1, 2]. Improvements in the signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR) are useful for high-spatial-resolution imaging of cartilage at the knee [1, 2]. Although high-spatial-resolution imaging is important for research studies, overall imaging time is a major consideration for routine clinical examinations. The additional SNR at 3 T can also be used to reduce acquisition time. Other traditional techniques for scanning time reduction are the acquisition of a rectangular field of view (FOV) and the use of a long echo-train length in fast spin-echo sequences.

In contrast, parallel imaging reduces scanning time not by changing either the k-space bandwidth or the trajectory but by increasing the sampling interval along the phase-encoding axis. When the MR signal is received by an array of coils, the scan can be accelerated by acquiring fewer phase-encoding data points, and the missing data can be synthesized after the acquisition using the spatial-encoding information of all the coil elements, which is the underlying principle of parallel imaging. Because scanning time is directly proportional to the number of phase encodes, R-folds undersampling in the phase-encoding direction reduces scanning time by the same factor, although a penalty is paid in terms of the SNR [3].

Especially in standard clinical musculoskeletal protocols, scanning time reduction using parallel imaging can prevent motion artifacts and allows more flexibility in protocol design. Several different reconstruction algorithms have been proposed for parallel imaging, such as SENSE (sensitivity encoding) [3]; SMASH (simultaneous acquisition of spatial harmonics) [4]; and, more recently, mSENSE (modified SENSE) and GRAPPA (generalized autocalibrating partially parallel acquisition) [5].

Studies that focus on the application of parallel imaging in clinical musculoskeletal MRI at 1.5 T have been reported in the literature [69]. Among those, GRAPPA proved to be a reliable technique with the highest effective SNR while being robust to artifacts. However, a paucity of data exists regarding parallel imaging at 3 T [10, 11] and parallel imaging for small-FOV, high-spatial-resolution MRI [12]. Thus, for this study, we focused on small-FOV imaging of the ankle at 3 T with an autocalibrating parallel technique, and we compared the quality of the resulting images with that of standard acquisitions at 3 and 1.5 T. The comparison was performed in terms of SNR; CNR; image quality; ligament, tendon, and cartilage visualization; and assessment of ankle abnormalities.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Specimens and Volunteers
MRI was performed in three fresh human cadaver ankle specimens (age of the cadavers at patients' death, 60–96 years) with abnormalities of the ligaments, tendons, and cartilage. Specimen examination was performed in accordance with legal requirements and institutional guidelines. In addition, three healthy human volunteers (age range, 23–31 years) without clinical findings suggesting ankle abnormalities were examined. These examinations were performed after institutional review board approval was granted, and informed consent was obtained from each of the volunteers.

Imaging
All imaging procedures were performed on a 1.5-T scanner and a 3-T scanner (Signa, GE Healthcare). Both MR systems were equipped with gradients, having a maximum gradient strength of 4 x 10–4 T/cm. For imaging of the specimens, a four-channel receiver coil (NMSC-001, Nova Medical) was used; for imaging of the volunteers, an eight-channel receiver coil (SHc-Head, Medical Devices) was used. A standard ankle protocol that had been previously optimized at our institution for an acquisition time of approximately 6 minutes for each sequence at 1.5 and 3 T was applied.

The protocol consisted of axial and sagittal T1-weighted, axial fat-saturated T2-weighted, and coronal fat-saturated intermediate-weighted fast spin-echo sequences and a fat-saturated spoiled gradient-recalled acquisition in the steady state (SPGR) for dedicated cartilage imaging (Table 1). In addition, at 3 T, parallel imaging acquisitions were obtained for 3D SPGR sequences and simulated for fast spin-echo sequences by decimating fully acquired data sets. The parallel acquisitions had to be simulated for the fast spin-echo sequences because the they were implemented only for gradient-echo sequences in the scanner at the time that this study was performed.


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TABLE 1: Parameters for MRI Sequences

 

Partial parallel imaging was used with a reduction factor (R) of 2 and 16 calibration lines. Thus, the parallel imaging data sets consisted of 144 phase encodes compared with 256 in a conventional acquisition. This difference resulted in an acquisition time reduction of approximately 44% for the parallel scans compared with the acquisition time for the conventional scans at 1.5 T and at 3 T. The scanning times of the conventional acquisitions at 1.5 and 3 T were in the same range, as shown in Table 1.

All images were reconstructed offline on a workstation (Sun Workstation, Solaris) using reconstruction software programmed in Matlab (MathWorks). For the partially parallel imaging data sets, images were reconstructed using a GRAPPA-based algorithm [12, 13], whereas full imaging data sets were reconstructed using a standard Fourier reconstruction.

Image Analysis
SNR was measured in every sequence, and CNR was calculated for the SPGR sequences. Images obtained from parallel imaging acquisition have a spatially varying distribution of noise. In those images, SNR calculations, which are based on mean signal intensity in a region of interest (ROI) and the background noise, are not valid. Therefore, SNR and CNR were calculated from twice-repeated acquisitions. An ROI was placed in the identical location on each of the two images, and the average SNR in the ROI was determined as the ratio of the average signal in the ROI in the mean image and the SD of the signal in the difference image [14]:

Formula
where Ix,y (A) is the signal intensity of the pixel x,y in image A, and Ix,y (B) is the signal intensity of the pixel x,y in the image B. The CNR was calculated for the SPGR sequences and was defined as the SNR of the cartilage minus the SNR of the bone marrow.

All the images were assessed by two radiologists independently concerning image quality and visualization of anatomic structures and abnormalities. The radiologists were blinded to all information about the specimens and volunteers and to the field strength and type of reconstruction.

For all sequences, image quality was graded by each of the radiologists using a 4-level confidence scale. Items subjectively assessed with this scale included sharpness of edges; amount of blurring and noise; delineation of small ligamentous structures; and contrast between different tissues, such as joint fluid, cartilage, cortical bone, ligaments, and fat. Images were given a score of 4 if subjective image quality was optimal so that ligaments and cartilage were clearly demarcated and noise and artifacts were minimal to the eye. A score of 3 was given when one or two of the previously mentioned criteria were visually less than optimal. A score of 2 corresponded to pronounced limitations in the images that affected diagnostic quality. Images scored as 1 had substantial diagnostic limitations because of extensive artifacts and noise.


Figure 1
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Fig. 1A Spoiled gradient-recalled acquisition in the steady state (SPGR) images show grade 3 cartilage defect (arrowhead) in ankle of cadaver specimen. No significant difference in visualization of abnormality was found between normal (A) and parallel (B) acquisitions at 3 T.

 


Figure 2
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Fig. 1B Spoiled gradient-recalled acquisition in the steady state (SPGR) images show grade 3 cartilage defect (arrowhead) in ankle of cadaver specimen. No significant difference in visualization of abnormality was found between normal (A) and parallel (B) acquisitions at 3 T.

 


Figure 3
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Fig. 1C Spoiled gradient-recalled acquisition in the steady state (SPGR) images show grade 3 cartilage defect (arrowhead) in ankle of cadaver specimen. Cartilage defect was not seen at 1.5 T by one of two radiologists.

 
For the fast spin-echo sequences, visualization of four ankle ligaments—that is, the anterior tibiofibular ligament, anterior talofibular ligament, anterior tibiotalar ligament, and spring ligament—was graded (4 = excellent, 1 = poor) by both radiologists subjectively.

In the cadaver specimens, abnormalities were evaluated on 1.5- and 3-T scans on and parallel scans obtained at 3 T separately. Macroscopic findings after dissection served as the standard of reference. Ligament and tendon abnormalities were assessed using the fast spin-echo sequences. Although no ligament abnormalities were present, abnormalities of eight tendons (tibialis anterior and posterior, flexor and extensor hallucis longus, flexor and extensor digitorum longus, and peroneus brevis and longus) were described on a 5-point scale. The absence of abnormalities was scored as 0; tenosynovitis, which appear as pronounced fluid around the tendon, was scored as 1; tendinosis, which showed elevated, abnormal signal, as 2; partial split or full split tear as 3; and complete rupture as 4.

Cartilage abnormalities were evaluated on the SPGR sequences. The depth of a lesion was categorized using a modified Noyes classification [15]: 1, lesion < 50% of the cartilage thickness; 2, lesion > 50% of the cartilage thickness, 3, full-thickness lesion. Similar classification systems were used for macroscopic assessments.

Statistically significant differences in image quality, SNR, and CNR were tested using a paired two-sided Student's t test with a significance level of p < 0.05. All statistical computations were processed using SPSS software (version 11.5, SPSS).


Results
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
GRAPPA imaging using a reduction factor (R) of 2 resulted in a scanning time reduction of 44% compared with conventional imaging. SNRs and CNRs calculated from repeated acquisitions were comparable between the GRAPPA images with an R of 2 and the conventional images obtained at 3 T (Table 2) for both specimen and volunteer studies. Comparing 3- and 1.5-T images, SNRs and CNRs had doubled on the SPGR sequence at 3 T (Figs. 1A, 1B, and 1C) while remaining similar on the fast spin-echo sequences (Figs. 2A, 2B, 2C, 2D, 2E, 2F, 3A, 3B, and 3C) because of the increased spatial resolution of the 3-T sequences. Line profiles plotted from conventionally acquired images and parallel images at 3 T matched closely, as shown on the 3-T SPGR images in Figure 4. These images also show comparable edge sharpness between the conventional and GRAPPA images.


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TABLE 2: Signal-to-Noise Ratio (SNR) and Contrast-to-Noise Ratio (CNR) of All Sequences

 

Figure 4
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Fig. 2A T1-weighted (A–C) and fat-saturated T2-weighted (D–F) images of ankle joint in cadaver specimen. Images show superior image quality at 3 T (A, B, D, and E) as opposed to 1.5 T (C and F). No significant difference in image quality or signal-to-noise ratio (SNR) was found between normal (A and D) and parallel (B and E) acquisitions at 3 T (p > 0.05). Mean values of image quality for T1-weighted sequences were as follows: 2.8 (1.5 T), 3.5 (3 T), and 3.5 (3 T with generalized autocalibrating partially parallel acquisition [GRAPPA] algorithm). Mean values of SNR for T1-weighted sequences were as follows 43.0 (1.5 T), 49.7 (3 T), and 47.2 (3 T with GRAPPA algorithm [3.0TGR]).

 

Figure 5
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Fig. 2B T1-weighted (A–C) and fat-saturated T2-weighted (D–F) images of ankle joint in cadaver specimen. Images show superior image quality at 3 T (A, B, D, and E) as opposed to 1.5 T (C and F). No significant difference in image quality or signal-to-noise ratio (SNR) was found between normal (A and D) and parallel (B and E) acquisitions at 3 T (p > 0.05). Mean values of image quality for T1-weighted sequences were as follows: 2.8 (1.5 T), 3.5 (3 T), and 3.5 (3 T with generalized autocalibrating partially parallel acquisition [GRAPPA] algorithm). Mean values of SNR for T1-weighted sequences were as follows 43.0 (1.5 T), 49.7 (3 T), and 47.2 (3 T with GRAPPA algorithm [3.0TGR]).

 

Figure 6
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Fig. 2C T1-weighted (A–C) and fat-saturated T2-weighted (D–F) images of ankle joint in cadaver specimen. Images show superior image quality at 3 T (A, B, D, and E) as opposed to 1.5 T (C and F). No significant difference in image quality or signal-to-noise ratio (SNR) was found between normal (A and D) and parallel (B and E) acquisitions at 3 T (p > 0.05). Mean values of image quality for T1-weighted sequences were as follows: 2.8 (1.5 T), 3.5 (3 T), and 3.5 (3 T with generalized autocalibrating partially parallel acquisition [GRAPPA] algorithm). Mean values of SNR for T1-weighted sequences were as follows 43.0 (1.5 T), 49.7 (3 T), and 47.2 (3 T with GRAPPA algorithm [3.0TGR]).

 

Figure 7
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Fig. 2D T1-weighted (A–C) and fat-saturated T2-weighted (D–F) images of ankle joint in cadaver specimen. Images show superior image quality at 3 T (A, B, D, and E) as opposed to 1.5 T (C and F). No significant difference in image quality or signal-to-noise ratio (SNR) was found between normal (A and D) and parallel (B and E) acquisitions at 3 T (p > 0.05). Mean values of image quality for T1-weighted sequences were as follows: 2.8 (1.5 T), 3.5 (3 T), and 3.5 (3 T with generalized autocalibrating partially parallel acquisition [GRAPPA] algorithm). Mean values of SNR for T1-weighted sequences were as follows 43.0 (1.5 T), 49.7 (3 T), and 47.2 (3 T with GRAPPA algorithm [3.0TGR]).

 

Figure 8
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Fig. 2E T1-weighted (A–C) and fat-saturated T2-weighted (D–F) images of ankle joint in cadaver specimen. Images show superior image quality at 3 T (A, B, D, and E) as opposed to 1.5 T (C and F). No significant difference in image quality or signal-to-noise ratio (SNR) was found between normal (A and D) and parallel (B and E) acquisitions at 3 T (p > 0.05). Mean values of image quality for T1-weighted sequences were as follows: 2.8 (1.5 T), 3.5 (3 T), and 3.5 (3 T with generalized autocalibrating partially parallel acquisition [GRAPPA] algorithm). Mean values of SNR for T1-weighted sequences were as follows 43.0 (1.5 T), 49.7 (3 T), and 47.2 (3 T with GRAPPA algorithm [3.0TGR]).

 

Figure 9
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Fig. 2F T1-weighted (A–C) and fat-saturated T2-weighted (D–F) images of ankle joint in cadaver specimen. Images show superior image quality at 3 T (A, B, D, and E) as opposed to 1.5 T (C and F). No significant difference in image quality or signal-to-noise ratio (SNR) was found between normal (A and D) and parallel (B and E) acquisitions at 3 T (p > 0.05). Mean values of image quality for T1-weighted sequences were as follows: 2.8 (1.5 T), 3.5 (3 T), and 3.5 (3 T with generalized autocalibrating partially parallel acquisition [GRAPPA] algorithm). Mean values of SNR for T1-weighted sequences were as follows 43.0 (1.5 T), 49.7 (3 T), and 47.2 (3 T with GRAPPA algorithm [3.0TGR]).

 

Figure 10
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Fig. 3A 31-year-old healthy male volunteer. Axial T1-weighted fast spin-echo images of foot show superior delineation of spring ligament (arrow) at 3 T (A and B) as opposed to 1.5 T (C); 3.0TGR = 3.0T with GRAPPA algorithm. No significant difference was found between (A) and parallel (B) acquisitions at 3 T; visualization of this ligament was rated very good at 3 T and as moderate at 1.5 T (C) by both radiologists.

 

Figure 11
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Fig. 3B 31-year-old healthy male volunteer. Axial T1-weighted fast spin-echo images of foot show superior delineation of spring ligament (arrow) at 3 T (A and B) as opposed to 1.5 T (C); 3.0TGR = 3.0T with GRAPPA algorithm. No significant difference was found between (A) and parallel (B) acquisitions at 3 T; visualization of this ligament was rated very good at 3 T and as moderate at 1.5 T (C) by both radiologists.

 

Figure 12
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Fig. 3C 31-year-old healthy male volunteer. Axial T1-weighted fast spin-echo images of foot show superior delineation of spring ligament (arrow) at 3 T (A and B) as opposed to 1.5 T (C); 3.0TGR = 3.0T with GRAPPA algorithm. No significant difference was found between (A) and parallel (B) acquisitions at 3 T; visualization of this ligament was rated very good at 3 T and as moderate at 1.5 T (C) by both radiologists.

 

Figure 13
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Fig. 4 Line profiles of spoiled gradient-recalled acquisition in the steady state (SPGR) images of cadaver specimen suggest edge sharpness of conventional images and of generalized autocalibrating partially parallel acquisition (GRAPPA) images is comparable at 3 T. Gray region corresponds to cartilage. 3.0 TGR = 3.0T imaging with GRAPPA algorithm.

 

The image quality of all sequences was rated highest at 3 T (Table 3) for both specimen and volunteer studies. The axial T1-weighted sequence obtained an average score of 3.5 of 4 points at 3 T for both parallel and normal acquisitions, compared with a score of 2.8 at 1.5 T. There was no significant difference between parallel and normal acquisitions at 3 T for all sequences (p > 0.05), whereas 3 T performed significantly better than 1.5 T in three of five sequences (p < 0.05).


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TABLE 3: Average Score for Image Quality

 

Similar trends were found for ligament visualization (Table 4). For all ligaments, visualization was rated highest for images obtained using a normal acquisition at 3 T (average score, 3.6). The average scores were slightly lower for parallel acquisition at 3 T (average score, 3.5), but this difference was not significant (p < 0.05). Both average scores were significantly higher than the average score at 1.5 T (p < 0.05); however, ligament visualization was good even at 1.5 T (average score, 3.3 of 4 points).


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TABLE 4: Average Score for Ligament Visualization

 

The pathologic examination of the three ankle specimens revealed three cartilage abnormalities that were classified as one grade 3 lesion in the lateral talus, one grade 2 lesion in the medial talus, and one grade 1 lesion in the tibia. Furthermore, in two specimens, three tendon abnormalities were found: a partial split tear of the peroneus tendon was seen in two specimens and a partial split tear associated with tenosynovitis of the peroneus longus tendon was seen in one specimen. In the third specimen, an os tibiale externum was present.

The tendon abnormalities were detected on all three sequence types. The grade 3 cartilage lesion was seen on images obtained using both parallel and standard acquisitions at 3 and 1.5 T. However, at 1.5 T, this cartilage lesion was described by only one of the two radiologists. The grade 1 and 2 cartilage lesions were missed in all three acquisitions by both radiologists.


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The results of our study have shown that higher-field-strength (i.e., 3-T) imaging combined with parallel imaging produces MR images of the ankle that are of excellent diagnostic quality while decreasing scanning time by 44%. Images acquired using the GRAPPA algorithm with a reduction factor of 2 were visually indistinguishable from images obtained using standard acquisitions. Theoretically, for parallel imaging with low reduction factors, an SNR decrease by the square root of the acceleration factor R—and thus a similar effective SNR compared with conventional acquisition—would be expected. The calibration lines incorporated in the GRAPPA reconstruction slightly reduce the SNR loss to a lower factor than R. For fast spin-echo sequences, the reduction in T2 decay that results from performing parallel imaging also partly offsets the SNR loss.

Parallel imaging techniques such as GRAPPA are referred to as "autocalibrating" techniques because the coil calibration necessary for the parallel imaging reconstruction is built into the accelerated scan. Hence, the reconstruction is not affected by patient motion between scans or by gradient nonlinearity in the high-resolution scan. GRAPPA has several advantages over other parallel imaging techniques for our specific application. In small-FOV imaging, often, there is slight aliasing outside the ROI but within the FOV. Griswold et al. [5] showed that parallel imaging techniques that belong to the class of GRAPPA are more robust to such situations than SENSE-like parallel imaging techniques. Moreover, the quality of image reconstruction by the former class of parallel imaging techniques is not as sensitive to errors in estimation of coil sensitivities as the latter.

Figures 2B and 2E show axial GRAPPA-reconstructed images of the left ankle with slight aliasing from the right ankle. The aliasing in the FOV and difficulty of estimating the coil sensitivity in certain regions would compromise the image quality for a SENSE-like parallel imaging technique, whereas as can be seen in Figures 2B and 2E, the GRAPPA technique provided a good image quality.

The limitations for this preliminary study must be considered. First, coils optimized for musculoskeletal and parallel imaging were not available for both 3- and 1.5-T scanners. The benefit of parallel imaging is expected to be higher with optimized receiver arrays. Another potential limitation of this study is the small sample size and limited range and number of abnormalities that were analyzed. However, these factors do not affect the comparison of image quality as presented.

In conclusion, the combination of parallel and high-field MRI can provide high-spatial-resolution images with good diagnostic quality in a short scanning time. In addition to reducing scanning time, parallel imaging can provide more flexibility in protocol design—for example, with 3D sequences the technique can be used to improve volume coverage without increasing scanning time. Alternatively, if SNR permits, spatial resolution can be improved without increasing acquisition time compared with the standard acquisition. For 2D fast spin-echo sequences, a reduction of echo-train length will reduce T2 blurring and can improve the SNR compared with standard acquisitions. The reduction in the number of 180° pulses during the sequence will also decrease the radiofrequency power deposition in the subject, which can be a significant benefit at higher magnetic fields.

Although we used only a reduction factor of 2 for this study, higher reduction factors can be used with a receiver array optimized for musculoskeletal applications if the baseline SNR is sufficiently high. The results of this study showed that parallel imaging using the GRAPPA algorithm provides a robust way to further improve musculoskeletal imaging at high field strength. A large-scale clinical study evaluating different abnormalities in the ankle to determine the optimal combination of reduction factor, image quality, and time necessary for imaging each abnormality now is clearly warranted.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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J. Y. Jung, Y. C. Yoon, S.-H. Choi, J. W. Kwon, J. Yoo, and B.-K. Choe
Three-dimensional Isotropic Shoulder MR Arthrography: Comparison with Two-dimensional MR Arthrography for the Diagnosis of Labral Lesions at 3.0 T
Radiology, February 1, 2009; 250(2): 498 - 505.
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K. J. Stevens, R. F. Busse, E. Han, A. C. S. Brau, P. J. Beatty, C. F. Beaulieu, and G. E. Gold
Ankle: Isotropic MR Imaging with 3D-FSE-Cube--Initial Experience in Healthy Volunteers
Radiology, December 1, 2008; 249(3): 1026 - 1033.
[Abstract] [Full Text] [PDF]


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