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Rapid Musculoskeletal MRI with Phase-Sensitive Steady-State Free Precession: Comparison with Routine Knee MRI

¹ Department of Radiology, Stanford University School of Medicine, 300 Pasteur Dr., Stanford, CA 94305-5105.
² Department of Electrical Engineering, Stanford University School of Medicine, Stanford, CA.

Received April 11, 2004; accepted after revision September 13, 2004.

 
Residents in Radiology 2004 President's Award

Address correspondence to S. S. Vasanawala (vasanawala{at}stanford.edu).

Abstract

Top Abstract Introduction Subjects and Materials Results Discussion References

 
OBJECTIVE. The aim of this work was to show the potential utility of a novel rapid 3D fat-suppressed MRI method for joint imaging.

CONCLUSION. Phase-sensitive steady-state free precession provides rapid 3D joint imaging with robust fat suppression and excellent cartilage delineation.

Introduction

Top Abstract Introduction Subjects and Materials Results Discussion References

 
Articular cartilage may be evaluated with fat-suppressed T2-weighted 2D fast spin-echo [1] or proton density fast spin-echo with fat saturation [2, 3]. Alternatively, the volume of articular cartilage may be assessed with 3D spoiled gradient-recalled echo (SPGR) imaging [4–7]. However, SPGR is not used routinely because of lengthy scanning times. Thus, a technique enabling rapid 3D morphologic assessment of joints is desirable. Moreover, because high resolution is required for cartilage assessment [8], and resolution limits ultimately are governed by image signal-to-noise ratio (SNR), the technique must have a high SNR efficiency. Finally, to maximize contrast between non–lipid- and lipid-containing tissues, fat suppression is required. This article presents initial experience in musculoskeletal imaging with a novel technique that offers speed, high SNR efficiency, and fat–water separation.

Steady-state free precession (SSFP) imaging is a 3D high-SNR method [9–11]. The method has also been termed "true fast imaging with SSFP," "balanced fast field echo," and "fast imaging employing steady-state acquisition" and produces contrast based on the ratio of T1 to T2 in tissues [12]. The result is a bright signal from fluid with preservation of signal from cartilage. Improved gradient hardware, by permitting lower TRs, has decreased the sensitivity of balanced SSFP imaging to banding artifacts caused by field inhomogeneity. A shorter TR also increases the relative T2 image contrast [12]. Thus, the method has been of increasing utility, particularly in cardiac imaging.

However, despite optimal SNR efficiency, balanced SSFP is hindered by a bright signal from fat [13]. Several SSFP modifications incorporate fat suppression by novel radiofrequency phase cycles (fluctuating equilibrium MRI, linear combination SSFP, and multipoint Dixon) [13–15] and may be useful for cartilage imaging [16]. Although these modifications still provide rapid imaging, scanning time is increased relative to balanced SSFP by a factor of 2–4. An alternative approach, fat-suppressed SSFP [17], is based on interleaved fat-suppression pulses; this method also lengthens scanning time, and the images show artifacts from deviations in the steady-state signal. However, we have recently described a novel method, termed "phase-sensitive SSFP," that permits steady-state imaging with fat–water separation without any time penalty relative to SSFP [18]. The purpose of this work was to explore the potential utility of phase-sensitive SSFP for joint imaging.

Subjects and Materials

Top Abstract Introduction Subjects and Materials Results Discussion References

 
Phase-sensitive SSFP uses an SSFP sequence with TE restricted to half the TR. The spectral response of the signal with respect to resonance frequency is periodic (Fig. 1A, 1B). The periodicity decreases with decreasing TR, resulting in a lower sensitivity to field inhomogeneity. With TR less than 7 msec, and a center frequency set between that of fat and water, both fat and water resonance frequencies are in high-signal-intensity regions of the spectral response. The MRI signal phase has a sharp transition at the center frequency. If TE is half the TR, then the signal phase profile is nearly constant aside from the transition. Thus, fat has a phase of –/2 + and water has a phase of /2 + , where is a slowly varying phase independent of resonance frequency. Thus, water and fat signals are out of phase, as seen in Figure 2A, 2B, 2C.

View larger version (19K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Spectrum of balanced steady-state free precession sequence when TE is one half TR. Signal magnitude (A) and phase (B) are shown as function of resonance frequency. Water and fat each fall in one high-magnitude region of spectrum but have phase difference of 180°. This phase difference is exploited in phase-sensitive SSFP.

View larger version (10K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Spectrum of balanced steady-state free precession sequence when TE is one half TR. Signal magnitude (A) and phase (B) are shown as function of resonance frequency. Water and fat each fall in one high-magnitude region of spectrum but have phase difference of 180°. This phase difference is exploited in phase-sensitive SSFP.

View larger version (18K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Images showing that water and fat signals are out of phase. Imag = imaginary. Scatterplot of complex image voxels, with real component along horizontal axis and imaginary component along vertical axis. Signal is primarily along a line, which can be determined by regression. Data may be rotated so that this line falls along vertical axis.

View larger version (33K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Images showing that water and fat signals are out of phase. Imag = imaginary. Rotation of data with voxels having positive imaginary component gives voxels dominated by water. Inset shows phase-sensitive steady-state free precession (SSFP) image produced by these voxels.

View larger version (42K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —Images showing that water and fat signals are out of phase. Imag = imaginary. Rotation of data with voxels having negative imaginary component gives voxels dominated by fat. Inset shows phase-sensitive SSFP image produced by these voxels.

For practical implementation, images are first reconstructed using the standard Fourier transform algorithm. Then, using regression techniques, can be estimated for each image slice and the data can be rotated in the complex plane to align the data optimally with the imaginary axis. The sign of the imaginary component of a voxel then may be used to determine if the voxel signal is predominantly from fat or water. Voxels are thus binned to form two separate images (Fig. 2A, 2B, 2C). Alternatively, simply displaying the imaginary component can form an extended dynamic range image. As shown below, viewing the extended dynamic range image with a broad window and low level improves visualization of bone marrow, whereas displaying the image with a higher level and narrower window delineates cartilage.

To determine the feasibility of fat–water separation and the contrast between various tissues, we scanned six knees from healthy volunteers, using phase-sensitive SSFP at 1.5 T (TR, 4–7 msec; flip angle, 25–45°; field of view, 16 cm; matrix, 256 x 256; sagittal slice thickness, 1–2 mm). After reviewing images from volunteers to determine the most promising scan parameters, we imaged 14 symptomatic knees, using a 1.5-T Signa scanner (GE Healthcare) with phase-sensitive SSFP (TR, 5.4 msec; flip angle, 28°; slice thickness, 2 mm; number of slices, 64; scanning time, 1 min 30 sec). Both symptomatic and healthy volunteers were scanned under an institutional review board–approved protocol.

The symptomatic knees were also scanned in accordance with the sagittal-sequence protocol of our institution: fat-suppressed T2-weighted fast spin-echo (TR/TE, 5,850/54; echo-train length, 8; field of view, 16 cm; matrix, 512 x 192; slice width, 3 mm; scanning time, approximately 3 min 13 sec) and proton density fast spin-echo (3,325/15; echo-train length, 6; field of view, 16 cm; matrix, 512 x 224; slice width, 3.5 mm; scanning time, approximately 4 min 18 sec). A musculoskeletal radiologist with 5 years' experience after fellowship and a senior radiology resident reviewed the phase-sensitive SSFP and fast spin-echo images, reaching a consensus on pathologic findings. Phase-sensitive SSFP and T2-weighted fat-suppressed fast spin-echo images were scored for image quality; fat suppression; and cartilage conspicuity, uniformity, and surface evaluation on a 4-point scale (1, nondiagnostic; 2, poor; 3, fair; 4, excellent).

Results

Top Abstract Introduction Subjects and Materials Results Discussion References

 
Phase-sensitive SSFP can image the entire knee with 0.625 x 0.625 x 2.0 mm resolution in 90 sec. Excellent fat–water separation was observed in all symptomatic knees (Table 1). Because of the short TE, tissues such as menisci and ligaments that have no signal on standard musculoskeletal imaging sequences were found to have signal intensity greater than background levels on phase-sensitive SSFP (Figs. 3A, 3B, 3C and 4A, 4B, 4C).

View larger version (160K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —30-year-old patient with normal knees. Proton density (A), fat-suppressed T2-weighted fast spin-echo (B), and phase-sensitive steady-state free precession (SSFP) (C) images show normal anterior and posterior cruciate ligaments. Signal intensity of ligament on phase-sensitive SSFP images is higher than background level. Articular cartilage is clearly delineated.

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —30-year-old patient with normal knees. Proton density (A), fat-suppressed T2-weighted fast spin-echo (B), and phase-sensitive steady-state free precession (SSFP) (C) images show normal anterior and posterior cruciate ligaments. Signal intensity of ligament on phase-sensitive SSFP images is higher than background level. Articular cartilage is clearly delineated.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —30-year-old patient with normal knees. Proton density (A), fat-suppressed T2-weighted fast spin-echo (B), and phase-sensitive steady-state free precession (SSFP) (C) images show normal anterior and posterior cruciate ligaments. Signal intensity of ligament on phase-sensitive SSFP images is higher than background level. Articular cartilage is clearly delineated.

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —46-year-old man with medial knee pain. Proton density (A), fat-suppressed T2-weighted fast spin-echo (B), and phase-sensitive steady-state free precession (SSFP) (C) images show normal anterior horn of meniscus. Signal intensity in anterior horn of meniscus on phase-sensitive SSFP images is higher than background level. However, despite this normal finding, meniscal tear (arrow) is seen clearly in posterior horn.

View larger version (96K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —46-year-old man with medial knee pain. Proton density (A), fat-suppressed T2-weighted fast spin-echo (B), and phase-sensitive steady-state free precession (SSFP) (C) images show normal anterior horn of meniscus. Signal intensity in anterior horn of meniscus on phase-sensitive SSFP images is higher than background level. However, despite this normal finding, meniscal tear (arrow) is seen clearly in posterior horn.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —46-year-old man with medial knee pain. Proton density (A), fat-suppressed T2-weighted fast spin-echo (B), and phase-sensitive steady-state free precession (SSFP) (C) images show normal anterior horn of meniscus. Signal intensity in anterior horn of meniscus on phase-sensitive SSFP images is higher than background level. However, despite this normal finding, meniscal tear (arrow) is seen clearly in posterior horn.

Fast spin-echo and phase-sensitive SSFP images were equivalent in quality and fat suppression (Wilcoxon's signed rank test, p = 0.317). Of note, in a knee with a cruciate ligament repair, phase-sensitive SSFP showed excellent fat–water separation with no failure from inhomogeneity induced by hardware (Fig. 5A, 5B). Contrast between cartilage and synovial fluid was similar to that seen on T2-weighted fast spin-echo images. Phase-sensitive SSFP gave results for superior cartilage conspicuity, uniformity, and surface delineation (Wilcoxon's signed rank test, p < 0.02 for each criterion) (Figs. 3A, 3B, 3C and 5A, 5B).

View larger version (166K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —36-year-old man with prior repair to anterior cruciate ligament. Fat-suppressed T2-weighted fast spin-echo (A) and phase-sensitive steady-state free precession (SSFP) (B) images show normal cartilage. Cartilage is delineated sharply on phase-sensitive SSFP images. Repair of anterior cruciate ligament is seen on fat-suppressed fast spin-echo and phase-sensitive SSFP images (arrowhead), demonstrating robustness of phase-sensitive SSFP fat–water separation technique to field inhomogeneity.

View larger version (142K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —36-year-old man with prior repair to anterior cruciate ligament. Fat-suppressed T2-weighted fast spin-echo (A) and phase-sensitive steady-state free precession (SSFP) (B) images show normal cartilage. Cartilage is delineated sharply on phase-sensitive SSFP images. Repair of anterior cruciate ligament is seen on fat-suppressed fast spin-echo and phase-sensitive SSFP images (arrowhead), demonstrating robustness of phase-sensitive SSFP fat–water separation technique to field inhomogeneity.

Eight patients showed regions of increased signal intensity in bone marrow on fat-suppressed T2-weighted fast spin-echo images, suggesting edema. In these cases, extended dynamic range phase-sensitive SSFP images delineated increased bone-marrow signal intensity similar in anatomic location and extent, whereas standard binned water phase-sensitive SSFP images showed edema over smaller anatomic regions (Fig. 6A, 6B, 6C). On the basis of the criterion of increased-intensity signal clearly extending to the articular surface, both methods showed five cases of presumed meniscal tear (Fig. 4A, 4B, 4C), and fast spin-echo showed one additional case of presumed meniscal tear. Of these cases of presumed meniscal tear, one patient has undergone arthroscopy, corroborating the assessment of meniscal tear on fast spin-echo and phase-sensitive SSFP images. On the basis of the criterion of abnormal contour, two presumed anterior cruciate ligament tears were revealed with phase-sensitive SSFP and fast spin-echo. A cartilage contour or signal abnormality corresponding to presumed damage was shown both by fast spin-echo and by phase-sensitive SSFP in eight cases, by only fast spin-echo in one case, and by only phase-sensitive SSFP in one case.

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A. —31-year-old woman after volleyball injury. Comparison of fat-suppressed T2-weighted fast spin-echo (A), phase-sensitive steady-state free precession (SSFP) binned water (B), and phase-sensitive SSFP extended dynamic range (C) images of knee injury. Binned image underestimates bone marrow edema relative to fat-suppressed fast spin-echo image, whereas extended dynamic range image displays cortical bone with same intensity as cartilage. Thus, the pair of images are complementary. Mild femoral cartilage thinning is delineated (arrow).

View larger version (124K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B. —31-year-old woman after volleyball injury. Comparison of fat-suppressed T2-weighted fast spin-echo (A), phase-sensitive steady-state free precession (SSFP) binned water (B), and phase-sensitive SSFP extended dynamic range (C) images of knee injury. Binned image underestimates bone marrow edema relative to fat-suppressed fast spin-echo image, whereas extended dynamic range image displays cortical bone with same intensity as cartilage. Thus, the pair of images are complementary. Mild femoral cartilage thinning is delineated (arrow).

View larger version (172K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6C. —31-year-old woman after volleyball injury. Comparison of fat-suppressed T2-weighted fast spin-echo (A), phase-sensitive steady-state free precession (SSFP) binned water (B), and phase-sensitive SSFP extended dynamic range (C) images of knee injury. Binned image underestimates bone marrow edema relative to fat-suppressed fast spin-echo image, whereas extended dynamic range image displays cortical bone with same intensity as cartilage. Thus, the pair of images are complementary. Mild femoral cartilage thinning is delineated (arrow).

Discussion

Top Abstract Introduction Subjects and Materials Results Discussion References

 
Phase-sensitive SSFP is a novel, fast, SNR-efficient fat–water separation method of 3D musculoskeletal imaging. In this work, excellent fat suppression and detection of joint abnormalities with phase-sensitive SSFP was shown. The method was faster than the previously described fat-suppressed steady-state methods. This 3D method may be useful for detailed examination of the volume and thickness of articular cartilage as part of a routine protocol for joint imaging [6, 19].

However, this work had several limitations. First, given the characteristic appearance of phase-sensitive SSFP images, reviewers of the images could not be unaware of the technique being assessed. Second, assessment of presumed disease was based on imaging findings alone, without confirmation by histology or arthroscopy. Thus, the validity of assessment of disease by phase-sensitive SSFP imaging was inferred from the previous work of others validating the accuracy of fast spin-echo in characterizing joint disease. Hence, in one case of a presumed meniscal tear seen on fast spin-echo but not on phase-sensitive SSFP, uncertainty remained about whether this finding was true-positive on fast spin-echo or true-negative on phase-sensitive SSFP. Another limitation of the study was the inclusion of only one comparison sequence for fat-suppressed T2 fast spin-echo to evaluate cartilage. At our institution, cartilage is evaluated with this sequence, a practice supported in the literature [1]. However, multiple other sequences have been advocated for articular cartilage evaluation, including SPGR [4–7] and fat-suppressed proton density fast spin-echo [2, 3]. Because of constraints on scanning time, these alternatives were not included for comparison. Given these limitations, the results of this work encourage investment in a larger study with arthroscopic and histologic correlation to determine the accuracy of phase-sensitive SSFP in detecting joint disease.

Use of phase-sensitive SSFP in the musculoskeletal system has two pitfalls related to fat–water separation. First, phase-sensitive SSFP, like all SSFP techniques and frequency-selective fat-suppression methods, is sensitive to field inhomogeneity. This pitfall can be addressed by use of a short TR. Mis-registration of fat and water will occur at 1.5 T and a TR of less than 7 msec when resonant frequency varies by more than ± 110 Hz. Second, when fat and water are within a voxel, the signals partially cancel each other and the voxel is assigned to either fat or water, whichever is predominant. Although the voxel is binned, the signal magnitude perceived on the image indicates the presence of both fat and water. Thus, in bone marrow edema, if signal from fat still predominates over signal from water in a voxel, the edema is appreciated as decreased signal intensity on the fat image. And if signal from water predominates over signal from fat in a bone marrow voxel, the edema is appreciated as increased signal intensity on the water image. Extended dynamic range images may be reviewed to assess the full extent of marrow edema. Increasing the image resolution decreases mixing of fat and water within a voxel. Except for the situation of marrow edema, mixing of water and fat in voxels in the musculoskeletal system is uncommon.

Evaluation of cartilage with T2-weighted fast spin-echo depends on a long effective TE to generate contrast between cartilage and synovial fluid. However, as TE increases, the SNR of cartilage decreases. In addition, resolution of fast spin-echo is limited by blurring induced by acquisition of echoes over a range of TEs [20, 21]. Higher scores for cartilage surface delineation with phase-sensitive SSFP were seen in this study, likely because of the thin slices of the 3D technique and perhaps because there was no blurring from sampling at various TEs. Alternatively, SPGR avoids blurring from multiple TE sampling and offers 3D imaging capability. Previous work has shown that SPGR and balanced steady-state sequences have similar SNR efficiency for cartilage [15, 22]. Although SPGR yields high signal intensity in cartilage, delineation of the cartilage surface is limited by suboptimal contrast with synovial fluid, and as previously noted, image acquisition is markedly longer with SPGR than with SSFP methods.

Because the balanced SSFP signal is a complex summation of many echoes, some of which have undergone minimal T2 decay, the SSFP signal in part comprises short T2 species that do not contribute to the MRI signal of standard sequences. It is well known that short T2 species are present in cartilage, menisci, tendons, and ligaments; these species are likely the origin of the higher-than-background signal intensity seen in these tissues on phase-sensitive SSFP images. However, it is unknown how these species are altered by disease and, in turn, how the resulting net phase-sensitive SSFP signal intensity is affected. This initial work suggested that pathologic changes in menisci might result in a higher phase-sensitive SSFP signal intensity.

Our results showed equivalent quality and fat suppression on phase-sensitive SSFP and fast spin-echo images and superior delineation of cartilage on phase-sensitive SSFP images. In a few patients, phase-sensitive SSFP and fast spin-echo depicted presumed bone marrow edema and meniscal injuries similarly. The method is faster than previously described methods, with volumetric evaluation of the knee in 90 sec, roughly half the time of fast spin-echo. The T2-like contrast and high SNR efficiency of this sequence may enable it to replace several routine sequences in a typical examination, allowing the use of techniques to examine the physiology of cartilage [23–27] in a reasonable examination time. Phase-sensitive SSFP is a promising technique to increase the speed and flexibility of musculoskeletal imaging.

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Top Abstract Introduction Subjects and Materials Results Discussion References

 

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