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DOI: 10.1148/radiol.2363040865
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(Radiology 2005;236:1047-1052.)
© RSNA, 2005

Technical Developments

Spin-labeling Coronary MR Angiography with Steady-State Free Precession and Radial k-Space Sampling: Initial Results in Healthy Volunteers1

Marcus Katoh, MD, Matthias Stuber, PhD, Arno Buecker, MD, Rolf W. Günther, MD and Elmar Spuentrup, MD

1 From the Department of Diagnostic Radiology, University Hospital, University of Technology (RWTH), Pauwelsstrasse 30, 52057 Aachen, Germany (M.K., A.B., R.W.G., E.S.); and the Department of Radiology, Division of MRI Research, Johns Hopkins University Medical School, Baltimore, Md (M.S.). Received May 13, 2004; revision requested July 29; revision received September 15; accepted October 20. Address correspondence to M.K. (e-mail: katoh{at}rad.rwth-aachen.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
 Results
 Discussion
 References
 
The purpose of this study was to prospectively compare free-breathing navigator-gated cardiac-triggered three-dimensional steady-state free precession (SSFP) spin-labeling coronary magnetic resonance (MR) angiography performed by using Cartesian k-space sampling with that performed by using radial k-space sampling. A new dedicated placement of the two-dimensional selective labeling pulse and an individually adjusted labeling delay time approved by the institutional review board were used. In 14 volunteers (eight men, six women; mean age, 28.8 years) who gave informed consent, signal-to-noise ratio (SNR), contrast-to-noise ratio (CNR), vessel sharpness, vessel length, and subjective image quality were investigated. Differences between groups were analyzed with nonparametric tests (Wilcoxon, Pearson {chi}2). Radial imaging, as compared with Cartesian imaging, resulted in a significant reduction in the severity of motion artifacts, as well as an increase in SNR (26.9 vs 12.0, P < .05) in the coronary arteries and CNR (23.1 vs 8.8, P < .05) between the coronary arteries and the myocardium. A tendency toward improved vessel sharpness and vessel length was also found with radial imaging. Radial SSFP imaging is a promising technique for spin-labeling coronary MR angiography.

© RSNA, 2005


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 References
 
A variety of magnetic resonance (MR) angiographic techniques with different image contrast mechanisms have been implemented so far for the noninvasive visualization of the lumina of the coronary arteries. These include spin-echo (1) as well as gradient-echo techniques (1,2). More recently, steady-state free precession (SSFP) imaging has also been shown to be a promising approach for bright-blood coronary MR angiography (3–5). A consistent attribute of all these approaches is that they do not exclusively display the coronary artery lumen. With each method, the surrounding tissue, including the coronary vessel wall, the myocardium, the ventricular and atrial blood pool, and the chest wall, can be seen to same degree. To visualize the lumen of only the coronary arteries, a projection MR angiographic technique, which enables selective visualization of the coronary blood pool with high contrast (6), can be applied. In projection MR angiography, the blood pool upstream of the vascular bed of interest is labeled by using a spatially selective inversion pulse. The labeled blood (with inverted magnetization) flows into the imaging volume during a time delay between the labeling pulse and the imaging portion of the sequence. By subtracting a second data set acquired without the preceding labeling pulse, the arterial lumen can be selectively visualized on projection MR images, while the signal of the surrounding stationary tissue appears almost completely suppressed (6–8).

Recently, spin-labeling coronary MR angiography has been performed with a navigator-gated T2-prepared gradient-echo sequence and a two-dimensional (2D) selective aortic spin-labeling pulse that enabled the acquisition of high-spatial-resolution three-dimensional (3D) projection coronary MR angiograms (6). In that study, spiral k-space sampling was applied, while in more recent coronary MR angiography studies a Cartesian data acquisition scheme was preferred (2). However, the use of other nonrectilinear k-space data sampling strategies like radial imaging may also be advantageous, because radial k-space sampling is characterized by a reduced sensitivity to motion artifacts (9,10). In addition, because of the T2/T1 contrast and intrinsically high signal-to-noise ratio (SNR) it yields, use of an SSFP technique may contribute to increased signal intensity in the arterial lumen compared with the signal intensity seen with gradient-echo imaging (11). However, to our knowledge, SSFP imaging has not yet been performed in combination with radial k-space sampling.

The purpose of our study, therefore, was to prospectively compare free-breathing navigator-gated cardiac-triggered 3D SSFP spin-labeling coronary MR angiography performed by using radial k-space sampling with that performed by using Cartesian k-space sampling in healthy adult volunteers.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 References
 
Volunteers
Spin-labeling MR angiography of the right coronary artery (RCA) (n = 10) or the left anterior descending (LAD) coronary artery (n = 4) was performed in 14 consecutive healthy adult volunteers (eight men and six women; mean age, 28.8 years ± 8.7 [standard deviation]) who did not have a history of cardiovascular disease. In three subjects, the left circumflex artery was included in the same imaging volume used for imaging the RCA. All subjects were in sinus rhythm (mean heart rate, 67 beats per minute ± 12). The study protocol was approved by the institutional board of clinical investigation, and written informed consent was obtained from each participating subject. M.S. is compensated as a consultant by Philips Medical Systems, Best, the Netherlands, manufacturer of the equipment described in this manuscript. The terms of this arrangement have been approved by Johns Hopkins University in accordance with its conflict of interest policies.

MR Imaging
All examinations were performed with a commercial 1.5-T whole-body MR system (Gyroscan Intera; Philips Medical Systems, Best, the Netherlands) with a gradient strength of 23 mT/m, a rise time of 219 µsec, and vector electrocardiographic technology (12). A five-element cardiac Synergy coil was used for signal reception.

A transverse cardiac-triggered breath-hold gradient-echo echo-planar imaging (fast-field-echo echo-planar imaging) cine sequence (echo time, 9.7 msec; number of echo-planar imaging readouts, seven; heart phases, 40) was performed so that we could visually determine the quiescent period during diastole (13). On the basis of the results of this sequence, the trigger delay for the subsequent fast navigator-gated cardiac-triggered 3D localizer SSFP sequence was identified (14). In addition, a breath-hold 2D SSFP cine sequence (repetition time msec/echo time msec, 2.7/1.4; flip angle, 60°; field of view, 350 mm; matrix, 160 x 160 reconstructed to 256 x 256; acceleration factor, two with sensitivity encoding [15]) was performed parallel to the left ventricular outflow tract to determine the time of aortic valve closure (Tao).

Coronary MR angiography was performed by using two high-spatial-resolution free-breathing navigator-gated cardiac-triggered 3D SSFP imaging sequences (6.1/3.0; excitation angle, 120°) (16) (Fig 1). The same sequence was performed with Cartesian (field of view, 360 x 360 mm; matrix, 384 x 384) and radial (field of view, 360 x 360 mm; number of radial trajectories, 384) k-space sampling and similar spatial resolutions (in-plane resolution, 0.9 x 0.9 mm reconstructed to 0.7 x 0.7 mm; 12 3-mm-thick sections interpolated to 24 1.5-mm-thick sections). Image data were acquired in mid-diastole by using the subject-specific trigger delay determined with the scout image (13). Sixteen radiofrequency excitations were performed during each R-R interval, resulting in an acquisition window of 97 msec. An initial {alpha}/2 preparation pulse followed by a train of five preparatory radiofrequency excitations without signal sampling was applied before the imaging portion of the sequence, enabling a smooth and rapid approach toward the steady-state conditions (17,18). To enhance the contrast between coronary blood and myocardium, and for presaturation of the myocardium and chest, a T2 preparation pulse was used (19). In addition, a spectral inversion-recovery (excitation angle, 120°) fat saturation prepulse was applied for suppression of the fat signal.



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  		Figure 1. Schematic of sequence elements for spin-labeling coronary MR angiography. Data acquisition is performed in mid-diastole with a heart rate–dependent trigger delay (TD). The labeling delay (TL) was calculated as TL = TD – Tao, where Tao is the time of aortic valve closure. The T2 preparation pulse (T2 Prep) is used for suppression of "unwanted" signal in projection MR angiography. The navigator allows data acquisition during free breathing. A spectral inversion-recovery (SPIR) pulse was applied to suppress the signal of the fatty tissue, and preparatory pulses were then performed to achieve steady-state conditions. ECG = electrocardiogram, ms = msec.

 
For suppression of respiratory motion artifacts, prospective real-time navigator technology, which allows for data acquisition during free breathing, as previously described (20,21), was used. The navigator was placed on the dome of the right hemidiaphragm, and the user-specified gating window was set to 5 mm. The time delay between the navigator and the imaging portion of the sequence was only 49 msec. A short time delay has been shown to be important for improved respiratory motion artifact suppression at high spatial resolution (22). A navigator efficiency of approximately 50% resulted in an overall mean imaging duration of 12 minutes for one data set in both sequences.

For accurate targeting of the coronary arteries, double-oblique section orientations were planned along the main axis of the coronary arteries by using a three-point plan-scan tool (23). To label the blood in the ascending aorta, a 2D selective (24) labeling pulse was implemented (pulse diameter, 30 mm; excitation angle, 180°) (6). The 2D labeling pulse was positioned concentric to the ascending aorta lumen at the level of the left main coronary artery with the beam axis angulated in a left posterocranial to right anterocaudal direction so that the blood above the aortic valve but not the blood in the left ventricle would be labeled. During the time delay (TD) between the aortic blood-pool labeling and imaging, the blood with inverted magnetization flows into the coronary arteries. Therefore, the labeling delay (TL) was calculated as TL = TD – Tao, where Tao is the time of aortic valve closure, so that the labeling pulse could be applied right after aortic valve closure and so that the inflow of the labeled blood into the coronary arteries could be maximized.

Two acquisitions of the same volume were performed—one with and one without the preceding spin-labeling pulse. Complex subtraction of the labeled and nonlabeled data was subsequently performed (25). Identical section orientations and positions were planned by using a three-point plan-scan tool so that both sequences could be compared. The phase-encoding direction was set to right to left for the RCA and to anterior to posterior for the LAD coronary artery. The order of the two sequences was randomized throughout the study. Coronary MR angiography was successfully completed in all volunteers.

Data Analysis
The MR imaging data were transferred to a commercially available Pentium III 550-MHz personal computer (Sinux, Karlsruhe, Germany) running Windows NT (Microsoft, Redmond, Wash) for multiplanar 3D reformatting performed by using "Soap-Bubble" analysis software (26).

Objective image analysis was performed by one of the authors (M.K., with 3 years of experience in cardiac MR imaging). The average signal intensity, or SI, of the coronary artery (SIcoro) was calculated along the center line of the vessel lumen, while user-specified regions of interest (mean size in aorta, 2.0 cm2; mean size in myocardium, 0.2 cm2) were placed so that the signal intensity in the aorta and the myocardium (SImyo) could be calculated. Identical regions of interest were copied to the images from both investigated sequences. SNRs in the coronary arteries and the aorta were calculated with the following equation: SNR = SIROI/SDair, where SIROI is the signal intensity in the region of interest and SDair is the standard deviation of the signal intensity in a region of air ventral to the chest (mean region of interest size, 31.6 cm2). Coronary-myocardial contrast-to-noise ratio (CNRcoro-myo) was calculated as CNRcoro-myo = (SIcoro – SImyo)/SDair.

In addition, vessel border definition was analyzed by calculating the magnitude of local change in signal intensity on both sides of the vessel in a Deriche image (an edge image obtained by using a first-order derivative of the input image) after the vessel path was defined by manually drawn points (19). Finally, contiguous vessel segment length was measured by using visual assessment, as previously described (26).

Subjective motion artifact level was graded on a three-point scale (on which a score of 1 indicated no visible motion artifacts; a score of 2, moderate artifacts; and a score of 3, pronounced motion artifacts preventing vessel visualization), and image quality in terms of coronary artery visualization was graded on a three-point scale (on which a score of 1 indicated good image quality with sharply defined vessel borders; a score of 2, reduced image quality although the vessel is still visible; and a score of 3, poor image quality without sufficient visualization of the coronary vessel), in consensus by two observers (A.B., with 9 years of experience in cardiac MR imaging, and E.S., with 8 years of experience in cardiac MR imaging) who were blinded to the sequence parameters.

Statistical Analysis
The results are given as geometric mean values ± 1 standard deviation. For statistical comparison, nonparametric methods were applied by using Discovery Software, version 5.0.1.2 (JMP, Cary, NC). Objective image quality parameters (SNR, contrast-to-noise ratio, vessel sharpness, vessel length) were analyzed with the Wilcoxon test, while for the analysis of the ordinal data (motion artifacts, image quality), the Pearson {chi}2 test was applied. Differences between groups with at least P < .05 were considered statistically significant.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
Discussion
 References
 
In all cases, multiplanar reformatted images for the right or left coronary artery could be generated and subjective and objective image quality parameters could be assessed. Quantitative measurements are summarized in Figure 2.



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  		Figure 2. Bar graph shows values for SNR, contrast-to-noise ratio, vessel sharpness, and length obtained in the 14 volunteers. With radial (rad) SSFP, SNR in the coronary artery (SNR coro) and the aorta (SNR ao), as well as the contrast-to-noise ratio between the coronaries and the myocardium (CNR coro-myo) were significantly increased compared with these parameters in Cartesian k-space sampling (cart SSFP). Vessel sharpness and length were also increased with radial SSFP; these differences, however, did not reach statistical significance.

 
Representative double-oblique coronary MR angiograms acquired parallel to the main axis of the RCA or the LAD coronary artery are shown in Figures 3–5. Aortic spin labeling in conjunction with SSFP coronary MR angiography enabled selective and high-contrast visualization of the coronary lumen and the blood in the aortic root, while surrounding tissue was almost completely suppressed. In some cases, the blood in the right ventricle and in the pulmonary trunk appeared with high signal intensity, depending on the heart shape and the orientation of the 2D labeling pulse (Figs 3, 5).



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  		Figure 3a. Double-oblique coronary projection 3D SSFP MR angiogram (6.1/3.0; flip angle, 120°; field of view, 360 mm; matrix, 384 x 384; T2 and spectral inversion-recovery preparation pulse) acquired parallel to main axis of the LAD coronary artery (short arrow) in 26-year-old female volunteer with (a) Cartesian and (b) radial k-space sampling. The LAD coronary artery and a diagonal branch are depicted with high signal intensity, while the blood in the right ventricle also appears bright owing to the orientation of the 2D labeling pulse. Note the pronounced motion artifacts (long arrows) in a.

 


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  		Figure 3b. Double-oblique coronary projection 3D SSFP MR angiogram (6.1/3.0; flip angle, 120°; field of view, 360 mm; matrix, 384 x 384; T2 and spectral inversion-recovery preparation pulse) acquired parallel to main axis of the LAD coronary artery (short arrow) in 26-year-old female volunteer with (a) Cartesian and (b) radial k-space sampling. The LAD coronary artery and a diagonal branch are depicted with high signal intensity, while the blood in the right ventricle also appears bright owing to the orientation of the 2D labeling pulse. Note the pronounced motion artifacts (long arrows) in a.

 


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  		Figure 4a. Double-oblique coronary projection MR angiogram (6.1/3.0; flip angle, 120°; field of view, 360 mm; matrix, 384 x 384; T2 and spectral inversion-recovery preparation pulse) acquired parallel to main axis of RCA in 24-year-old female volunteer with (a) Cartesian and (b) radial k-space sampling. In a, the very distal portion of the RCA cannot be delineated owing to motion artifact superimposition, while in radial imaging, the vessel (arrow) is nicely depicted up to the myocardial septum.

 


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  		Figure 4b. Double-oblique coronary projection MR angiogram (6.1/3.0; flip angle, 120°; field of view, 360 mm; matrix, 384 x 384; T2 and spectral inversion-recovery preparation pulse) acquired parallel to main axis of RCA in 24-year-old female volunteer with (a) Cartesian and (b) radial k-space sampling. In a, the very distal portion of the RCA cannot be delineated owing to motion artifact superimposition, while in radial imaging, the vessel (arrow) is nicely depicted up to the myocardial septum.

 


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  		Figure 5a. Double-oblique coronary projection MR angiogram (6.1/3.0; flip angle, 120°; field of view, 360 mm; matrix, 384 x 384; T2 and spectral inversion-recovery preparation pulse) acquired parallel to main axis of RCA (double arrows) in 26-year-old female volunteer with (a) Cartesian and (b) radial k-space sampling. The left circumflex coronary artery (single arrow) is included in the same imaging volume. As compared with Cartesian SSFP, radial SSFP enables clear visualization of the left circumflex artery owing to a reduction in motion artifacts.

 


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  		Figure 5b. Double-oblique coronary projection MR angiogram (6.1/3.0; flip angle, 120°; field of view, 360 mm; matrix, 384 x 384; T2 and spectral inversion-recovery preparation pulse) acquired parallel to main axis of RCA (double arrows) in 26-year-old female volunteer with (a) Cartesian and (b) radial k-space sampling. The left circumflex coronary artery (single arrow) is included in the same imaging volume. As compared with Cartesian SSFP, radial SSFP enables clear visualization of the left circumflex artery owing to a reduction in motion artifacts.

 
When we compared Cartesian and radial SSFP imaging, we observed that a significantly higher signal intensity was present in the ascending aorta, as well as in the coronary arteries, with radial SSFP (P < .05). Contrast-to-noise ratio was also increased with radial k-space sampling (P < .05), which resulted in a display of longer vessel lengths (Cartesian SSFP yielded a mean vessel length of 64.2 mm for the LAD coronary artery, while radial SSFP yielded 76.4 mm; Cartesian SSFP yielded 49.0 mm for the left circumflex artery, while radial SSFP yielded 106.3 mm; and Cartesian SSFP yielded 79.2 mm for the RCA, while radial SSFP yielded 86.3 mm; P = .099) (Figs 2, 4, 5).

Measuring vessel border definition also yielded higher values with radial imaging. This difference, however, did not reach statistical significance (62.9% vs 58.5%, P = .105).

Motion artifact suppression was found to be superior with radial k-space sampling (P < .05, Table). With Cartesian k-space sampling, pronounced motion artifacts in the phase-encoding direction were observed (Fig 3). Overall image quality was also considered to be better in radial imaging, because the visualization of the more distal portions of the coronary arteries in particular was impaired in Cartesian imaging. The difference with respect to subjective image quality, however, did not reach statistical significance.


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  		Distribution of Subjective Image Quality Parameters

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
References
 
In a relatively recent study (6), 3D projection MR angiography performed with a 2D labeling pulse enabled the selective visualization of the coronary artery lumen while suppressing signal from the surrounding tissue. In that study, spiral k-space sampling, which provided a time- and signal-efficient readout during a short acquisition window (50 msec), was performed. In the present study, we sought to improve vessel visualization by reducing motion artifacts with a radial data acquisition scheme. Compared with previous projection MR angiographic techniques (7,8,27–30), in our technique, further technical refinements, including a modified orientation of the 2D labeling pulse, an individually adapted trigger delay, and the use of an SSFP sequence, were implemented.

Spatially selective labeling of the aortic blood with subsequent entry into the coronary system enables high-contrast visualization of the coronary arteries with both Cartesian and radial SSFP imaging. Originally, the 2D selective labeling pulse was typically aligned along the ascending aorta. However, the use of such an orientation may invert the blood in the left ventricle and thereby reduce the MZ magnetization that enters the coronaries in the next R-R interval. This subsequently may lead to a reduced SNR and contrast-to-noise ratio in the coronary arterial blood pool. Therefore, we used an orientation of the labeling pulse that was angulated nearly orthogonal to the long axis of the heart to maintain the full magnetization of the blood in the left ventricle (8). When this technique is used, the inverted blood in the right ventricle may appear with high signal intensity. However, this will not affect the visualization of the coronary arteries because the longitudinal magnetization will approach equilibrium magnetization during circulation through the lung. In addition, we corrected the position of the labeling pulse by using the 2D cine SSFP sequence. In this way the center of the 2D labeling beam was adjusted to the center of the ascending aorta at Tao. Considering the movement of the aortic root during the heart phase may lead to optimized labeling efficiency. Furthermore, Tao was determined so that we could calculate the maximal labeling delay in each subject. The prolonged labeling delay allows for a wash-in of the labeled aortic blood into more distal portions of the coronary arteries (6).

To obtain maximal possible signal in the coronary arteries, the imaging sequence also needs to be optimized. Previous investigators chose to use a reduced number of radiofrequency excitations in each acquisition, as in echo-planar imaging, or reduced excitation angles, because higher excitation angles are less signal efficient for labeling techniques in which labeling information is stored in the longitudinal magnetization. We decided to implement a SSFP coronary MR angiographic technique to take advantage of the high T2/T1 contrast and intrinsically high SNR previously demonstrated to be characteristic of this technique (10,11,31). SSFP has the added advantage of being flow compensated in all three spatial coordinates because of the symmetric shape of the gradients—that is, although the visualization of the coronary arteries depends on the inflow of labeled blood, the sequence itself does not need to be flow sensitive. Furthermore, data were acquired in a relatively short acquisition window (97 msec), which minimizes potential blurring due to residual intrinsic cardiac motion.

In general, subtraction-based MR angiographic techniques are sensitive to subtraction errors. However, although data were acquired during free breathing, successful suppression of stationary tissue was achieved in all cases by using a real-time navigator. The visibility of the small-caliber vessels seen in the figures suggests that the navigator implementation effectively suppressed breathing-related bulk motion. In addition, with free-breathing navigator technology, no breath-hold time constraints for data acquisition exist. Thus, high-spatial-resolution imaging, as well as the acquisition of multiple views, was possible.

However, phase errors in Cartesian imaging and streaking artifacts in radial imaging were still visible around the coronary arteries. These artifacts may originate from the remaining cardiac motion and probably depend on heart rate changes. Motion artifacts occur arbitrarily and hence are not subject to subtraction. In fact, they may even be amplified when subtraction techniques are used. In our study, motion artifact suppression was judged to be superior with radial k-space sampling. In Cartesian imaging, increased motion artifacts are visible in the phase-encoding direction, which was a limitation for the visualization of small-vessel branches. On the other hand, radial imaging resulted in small streaking artifacts that were spread homogeneously all over the image. These artifacts were considered to have the same origin as artifacts in Cartesian sampling—namely, motion. The modified artifact pattern not only brings about better subjective image impressions but also allows for better background suppression after subtraction and, hence, increased visualization of the distal portions of the coronary arteries.

With the present approach, two data sets are needed, which doubles the imaging duration. The prolonged imaging time in conjunction with the small imaging volume is deemed to be a major drawback limiting the examination to one or, at maximum, two vessels. The dependence of the projection MR angiographic technique on inflow may be another limitation; however, it is conceivable that this property may turn out to be another advantage that enables investigation of flow dynamics—for example, by using different labeling delay values (6).

In conclusion, an optimized labeling delay time and a modified placement of the 2D selective labeling pulse in navigator-gated cardiac-triggered 3D SSFP projection MR angiography enable a more effective targeting of the blood pool that enters the coronary arteries, resulting in high-quality coronary angiograms in which small-diameter and more distal vessels can be seen. When compared with the more conventional Cartesian k-space sampling approach, radial data acquisition minimizes motion artifacts and therefore leads to further improved image quality and vessel visualization. It may potentially be an alternative approach for assessing coronary artery stenoses, because the acquisition of a 3D data set permits the reconstruction of multiple views, thus yielding the advantage of identifying eccentric vessel narrowing. Studies including patients with coronary artery disease depicted at conventional angiography are needed for further evaluation.


   FOOTNOTES
 

Abbreviations: LAD = left anterior descending • RCA = right coronary artery • SNR = signal-to-noise ratio • SSFP = steady-state free precession • 3D = three-dimensional • 2D = two-dimensional

See Materials and Methods for pertinent disclosures.

Author contributions: Guarantor of integrity of entire study, E.S.; study concepts, all authors; study design, M.K., E.S.; literature research, M.K., E.S.; clinical and experimental studies, M.K., E.S.; data acquisition, M.K.; data analysis/interpretation, A.B., E.S.; statistical analysis, M.K., A.B.; manuscript preparation and revision/review, M.K.; manuscript definition of intellectual content, M.S.; manuscript editing and final version approval, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 References
 

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