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Neuroradiology |
1 From the Department of Diagnostic Radiology, Mayo Clinic and Foundation, 200 First St SW, Rochester, MN 55905. Received June 18, 1998; revision requested August 5; revision received August 24; accepted October 6. Supported in part by National Institutes of Health grants HL 37310 and CA 37993, GE Medical Systems, and Bracco Diagnostics. Address reprint requests to J.H.
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Abstract |
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MATERIALS AND METHODS: Forty consecutive patients with cerebrovascular disease in the differential diagnosis were evaluated with fluoroscopically triggered 3D MR angiography (gadoteridol dose range, 0.1–0.3 mmol per kilogram of body weight; mean acquisition time, 40 seconds ± 8 [SD]). The contrast-enhanced 3D MR angiograms were evaluated for overall quality, vascular signal intensity, venous suppression, and motion artifact. Twenty patients also underwent two-dimensional (2D) time-of-flight (TOF) MR angiography. The overall quality of the 2D TOF MR angiograms and comparative quality between the 2D TOF and contrast-enhanced 3D MR angiograms were determined.
RESULTS: The contrast-enhanced 3D MR angiograms were of excellent or more than adequate quality for diagnosis in 36 of the 40 studies (90%). In 35 of the 38 contrast-enhanced 3D studies in which the contrast material bolus was detected fluoroscopically, the internal jugular vein signal intensity was either not detectable or barely visible. In 18 of the 20 patients who also underwent 2D TOF MR angiography, the quality of the contrast-enhanced 3D MR angiograms was graded as markedly superior or superior.
CONCLUSION: Contrast-enhanced, elliptic centric 3D MR angiography with real-time MR fluoroscopic triggering offers high-spatial-resolution images of the carotid arteries and aortic arch with reliable venous suppression.
Index terms: Carotid arteries, MR, 172.121412, 172.121416, 172.143 • Magnetic resonance (MR), three-dimensional • Magnetic resonance (MR), vascular studies, 172.121412, 172.121416, 172.12142, 172.12143
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Atherosclerotic disease involving the carotid bifurcation with thromboemboli accounts for a substantial percentage of ischemic infarcts. Findings in prospective randomized trials including the North American Symptomatic Carotid Endarterectomy Trial (NASCET) (1,2), European Carotid Surgical Trial (3), and Department of Veterans Affairs Symptomatic Carotid Stenosis Trial (4) have demonstrated relative risk reductions ranging from 70% to 85% when endarterectomy is performed in patients with diameter stenosis of 70% or more. Recently, final results in the NASCET have demonstrated surgical benefit for selected patients with stenoses as low as 50% (5). As the criteria for determining candidates for surgery moves from a single threshold to a more complex consideration of multiple factors, accurate grading of the degree of carotid artery stenosis increases in importance.
Conventional cerebral angiography has been the accepted preoperative test to determine if a high-grade carotid artery stenosis is present that necessitates consideration of surgical intervention. Recently, emphasis has been directed toward use of noninvasive imaging techniques including duplex color flow ultrasonography (US) (6,7), nonenhanced magnetic resonance (MR) angiography (8,9), and computed tomographic (CT) angiography (10,11) for identifying surgical candidates. These techniques all work to some degree but are still limited by one or more of the factors of limited field of view (US), dephasing artifacts, signal dropout due to saturation and long acquisition time (MR angiography), and radiation exposure with extensive image processing (CT).
Contrast material–enhanced, three-dimensional (3D) MR angiography offers the opportunity for rapid imaging of the carotid arteries and aortic arch while addressing some of the flow-related shortcomings of nonenhanced MR angiography. Previous contrast-enhanced MR angiograms were acquired with acquisition times of several minutes or more and were degraded by the dilution of the contrast material and the presence of noticeable venous signal in the adjacent venous structures (12,13). Use of more rapid acquisition techniques in an attempt to image the first pass of contrast material in the arterial vasculature potentially offers venous suppression. However, this approach requires synchronization of the MR acquisition with the subject-dependent delay time between intravenous injection and arrival of the contrast material bolus in the carotid arteries. Among the techniques that have been used to address this in carotid and other vasculature are estimation of arrival time, separate measurement of circulation time by using a test injection of contrast material or magnesium sulfate (14), use of multiple short (eg, 10-second) 3D acquisitions (15), use of a 3D acquisition with more frequent updating of the central k-space views (16), and real-time triggering with either line scanning (17) or two-dimensional (2D) MR fluoroscopy (18,19). These techniques have all been successful to some degree. The need remains, however, for a method that reliably provides high-spatial-resolution 3D MR images of the carotid arteries with a high degree of venous suppression.
The purpose of this study was to apply the technique of fluoroscopically triggered contrast-enhanced 3D MR angiography with use of an elliptic centric view ordering in patients referred for imaging of the carotid arteries. A secondary purpose was to compare findings on contrast-enhanced 3D and 2D time-of-flight (TOF) MR angiograms obtained at the carotid bifurcation.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MR Fluoroscopic Pulse Sequence
MR fluoroscopy was used for two specific purposes: first, to interactively select the monitoring plane prior to the contrast material injection, and, second, to image the monitoring plane during the actual contrast-enhanced acquisition to detect arrival of the bolus. The same pulse sequence was used for both purposes: a gradient-echo sequence with repetition and echo times of 9 and 2.4 msec, respectively, spatial resolution of 256 (x) x 128 (y), and first-order gradient moment nulling along the section-select (z) and frequency-encoding (x) directions. A partial echo readout was used in which 160 points were sampled (32 at negative and 128 at positive kx values) by using a signal bandwidth of plus or minus 16 kHz. All fluoroscopic MR images were reconstructed with a custom system (20) that was interfaced with the commercial 1.5-T MR imager (Signa, version 5.6; GE Medical Systems, Milwaukee, Wis). Reconstruction time for each 256 x 256 displayed image for data from a single coil was approximately 300 msec and for data from a four-channel multicoil was approximately 600 msec. Partial image updating was used so images were reconstructed at rates imposed by the above array-processor reconstruction times and not by the intrinsic temporal resolution (repetition time x 128 phase encodes) of the pulse sequence. The central k-space views were sampled more frequently than were the higher spatial frequency views (21), resulting in fluoroscopic sequence rates of 3.5 images per second for single coil reception and 1.6 images per second for multicoil reception.
Interactive graphic tools were used to facilitate selection of the monitoring plane. Among those found useful was a "three-point tool" with which the operator interactively identified three separate points in potentially different image sections. Since three points define a plane, the coordinates of these points were then used to immediately image the defined oblique section. For accurate bolus detection, it is desirable to image a blood vessel longitudinally so the effects of TOF enhancement in the vessel are reduced by means of radio-frequency saturation, and high vascular signal intensity is thus primarily attributable to the presence of contrast agent. For studies of the carotid bifurcation, the monitoring plane was typically a longitudinal image of the left or right bifurcation itself. This was easily selected with the three-point tool by selecting points in the external and internal carotid branches in an axial section 2 cm distal to the bifurcation and a third point in the common carotid artery in a second axial section 2–3 cm proximal to the bifurcation. For studies of the origins of the carotid and vertebral arteries, a monitoring plane containing the aortic arch was selected by identifying points in the ascending and descending aorta in an axial section near the top of the arch and a third point in the more distal descending aorta in a second axial section typically 4–6 cm inferior to the first. Typical elapsed time for continuous fluoroscopy to select the monitoring plane for any study was about 1 minute.
After the monitoring plane was chosen, the actual contrast-enhanced acquisition was performed. The monitoring plane was imaged continuously at the rate dictated by the coil (single or multicoil). On detection of the contrast material bolus, the operator triggered the 3D sequence with a simple mouse click. The flip angle for the fluoroscopic sequence was 12° for interactive selection of the monitoring plane and 30° for the contrast material detection; the larger value was better tuned to the Ernst angle of the markedly reduced T1 of the contrast-enhanced blood.
MR Angiographic Pulse Sequence
To acquire the MR angiograms, a 3D gradient-echo sequence was used that incorporated radio-frequency spoiling and rewinding of both phase-encoding gradients. Repetition time and echo time were 6.6 and 1.4 msec, respectively. A partial echo readout was used, with the 160 sampled points further synthesized to 256 points. Prior to acquisition of actual data for the 3D data set, 200 "dummy" repetitions were played out to allow the magnetization to reach a steady state. The typical matrix size was 256 (x) x 128–224 (y) x 32–48 (z). The mean acquisition time for the 3D sequence was 40.3 seconds ± 8.0 (SD) (range, 27–56 seconds). Typical fields of view were 20–24 cm in the superior-inferior (x) direction, 15–24 cm in the right-left (y) direction, and 3.2–4.4 cm in the anteroposterior (z) slab-select direction with a typical partition thickness of 1.0–1.4 mm. In the sequence, elliptic centric ordering of the phase encodings was used along the y and z directions. This has been discussed in detail previously (22). Briefly, the ordering samples the lowest spatial frequency, high-signal views at the beginning of the acquisition and samples views with higher spatial frequencies as the acquisition progresses. When properly triggered at the arrival of contrast material in the targeted anatomy, the low-order, central phase-encoding views are thus sampled during the arterial phase and prior to the venous phase. This view order thus intrinsically provides venous suppression. The elliptic nature of the view order accounts explicitly for the possible difference between the fields of view in the y and z directions.
Different parameters were evaluated to provide the best venous suppression and highest spatial resolution. Zero filling, which was implemented with the last eight patients, allowed use of a thicker imaging volume and, at the same time, finer sampling of the partition (23). This allowed complete coverage of both the cervical carotid and vertebral arteries with the volume neck coil. These eight patients were studied with a 20 (x) x 15 (y)-cm field of view and a 256 (x) x 168 (y) matrix, with 38 1.4-mm-thick sections, resulting in an acquisition time of 44 seconds. (Note the y matrix value of 168 represents the product of the prescribed value of 224 multiplied by the field-of-view factor of 15/20.) The reconstruction employed zero filling in all three directions to yield 76 1.4-mm-thick sections, with 0.7-mm overlap, and a 512 x 336 matrix. Thus, actual voxel size was 0.78 (x) x 0.89 (y) x 1.4 mm, yielding a voxel volume of 0.98 mm3. Zero filling effectively improves the resolution (23), and, allowing for an approximate improvement factor of the square root of 2 in each direction, the effective voxel volume is approximately 0.35 mm3. For arch imaging, a custom torso array multicoil was used. The imaging parameters were a 24 x 24-cm field of view and a 256 (x) x 192 (y) matrix, with 38 2.0-mm-thick sections, resulting in an acquisition time of 49 seconds. The reconstruction employed zero filling to yield 76 2.0-mm-thick sections, with 1.0-mm overlap, and a 512 x 512 matrix. The actual voxel volume of 2.34 mm3 was effectively reduced to 0.83 mm3 by means of the zero-filled reconstruction. This technique allowed visualization of the entire extracranial carotid and vertebral arteries. Higher spatial resolution of the carotid arteries could have been obtained if the entire course of the vertebral arteries had not been included.
Patient Studies
Fort consecutive patients (22 men, 18 women; age range, 18–84 years; mean age, 57 years) with cerebrovascular disease in the differential diagnosis of presenting symptoms were included in the study. The study was approved by our institutional review board, and all patients gave their informed consent to participate.
Five different coils were used to determine the extent to which different radio-frequency coils could be used in conjunction with the fluoroscopic triggering technique. A receive-only volume neck coil was used in 19 patients, a transmit-receive neurovascular coil that covered the head and neck in three, a receive-only phased-array torso coil in 16, the standard birdcage head coil in one, and the standard body coil in one. Seven of the 19 patients studied with the volume neck coil subsequently underwent contrast-enhanced 3D MR angiography of the aortic arch by using the phased-array coil in conjunction with a second injection of contrast material. The phased-array torso coil was an arrangement of four coils with one coil pair placed anterior and one pair placed posterior to the upper thorax and neck.
All patients received gadoteridol (ProHance; Bracco Diagnostics, Princeton, NJ) with a dose range between 0.1 and 0.3 mmol per kilogram of body weight during performance of one or two contrast-enhanced 3D MR angiographic sequences. The contrast material was delivered by using a power injector (Spectris; Medrad, Indianola, Pa) at a rate between 2 and 4 mL/sec followed by a saline solution flush of 20–30 mL at a rate of 1.5–3.0 mL/sec. When multiple injections were used, 20 mL of contrast material was injected for each acquisition. During imaging of the carotid arteries, the patient was instructed to continue quiet breathing and not move. Studies of the aortic arch specifically were performed with breath holding. For all studies, the circulation time was noted from initiation of injection to arrival of the contrast material in the fluoroscopic monitoring plane. No contrast material reactions or adverse events occurred during the contrast-enhanced portion of the studies.
A rapid, sagittal, phase contrast 2D scout image was initially acquired and used to establish the volume to be imaged at contrast-enhanced 3D MR angiography. In the second set of 20 patients, 2D TOF MR angiography of the carotid bifurcation was also performed. This sequence was added primarily as a better method with which to position the 3D MR angiographic volume, but it also allowed comparison with an established MR angiographic technique. The 2D TOF sequence included imaging of 80 axial 1.5-mm-thick sections with a moving superior saturation band (repetition time, 40 msec; echo time, 8.7 msec; one signal acquired; 256 x 128 matrix; 60° flip angle; 16 x 16-cm field of view). The sequence was prescribed in a supero-inferior direction to cover the carotid arteries from the skull base to the low common carotid arteries, as determined on the 2D phase contrast scout image. The 2D TOF sequence was also performed prior to the contrast-enhanced 3D MR angiographic sequence.
Evaluation
The fluoroscopic image for each patient was evaluated to determine whether contrast material arrival was detected in the monitoring plane during the real-time acquisition.
The contrast-enhanced 3D MR angiograms were evaluated for overall quality, vascular signal intensity, venous suppression, and motion artifact. The evaluation criteria for overall quality were 1, excellent; 2, more than adequate for diagnosis; 3, adequate for diagnosis; 4, less than adequate for diagnosis; and 5, nondiagnostic. The criteria for vascular signal intensity were 1, excellent vascular image; 2, minimal signal dropout; 3, moderate signal dropout but diagnostic; 4, moderate artifact, questionable diagnostic quality; and 5, nondiagnostic. The criteria for venous suppression were 1, no internal jugular vein signal intensity; 2, barely visible internal jugular vein signal intensity; 3, noticeable internal jugular vein signal intensity but less noticeable than the internal carotid artery signal; 4, comparable internal jugular vein and internal carotid artery signal intensities; and 5, internal jugular vein signal intensity more noticeable than that of the internal carotid artery. The criteria for motion artifact were 1, no motion artifact; 2, minimal artifact; 3, moderate artifact but diagnostic study; 4, moderate artifact, questionable diagnostic quality; and 5, nondiagnostic. The criteria for the quality of depiction of the arch or carotid artery origins (if imaged) were 1, excellent; 2, more than adequate for diagnosis; 3, adequate for diagnosis; 4, less than adequate for diagnosis; and 5, nondiagnostic.
In the comparison of contrast-enhanced 3D and 2D TOF MR angiograms in 20 patients, the evaluation criteria for quality were 1, contrast-enhanced 3D image markedly superior to 2D TOF image; 2, contrast-enhanced 3D image superior to 2D TOF image; 3, comparable quality; 4, contrast-enhanced 3D image inferior to 2D TOF image; and 5, contrast-enhanced 3D image markedly inferior to 2D TOF image. The criteria for 2D TOF image quality were 1, excellent; 2, more than adequate for diagnosis; 3, adequate for diagnosis; 4, less than adequate for diagnosis; and 5, nondiagnostic. Also, the aortic arch was evaluated when either a single image included both the carotid bifurcation and aortic arch (16 cases) or when separate images included the bifurcation or arch (seven cases). The collapse image was visually inspected and the source images were reviewed to determine if venous signal intensity was detectable. The studies were reviewed in an unblinded manner by three authors ( J.H., S.B.F., S.J.R.). Evaluation was performed in a group reading, and consensus was required.
In five cases judged to have barely visible internal jugular vein signal intensity (venous suppression grade 2), quantitative measurement of the degree of venous-to-arterial signal was performed. The mean venous signal for these five cases was 11% ± 6 of arterial signal. Because the venous signal was negligible in many cases, quantitative measurement was discontinued in favor of the qualitative evaluation.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Vascular signal intensity was assessed as either excellent (grade 1) or minimal signal dropout (grade 2) in 35 of the 40 patients (Fig 1c). The five remaining cases were graded as having moderate signal dropout but still diagnostic quality. In one of these cases, the carotid artery signal intensity was low due to late triggering, and this was one of the two failures of fluoroscopic detection of contrast material arrival. In three of the remaining four cases of low vascular signal intensity, the reason was primarily coil choice. In one case with the head coil and in two cases with the torso array coil, the carotid bifurcation was at the edge of the coil imaging zone. As a result, reduced signal intensity was detected at the bifurcation, but the images were still diagnostic. None of the 40 studies was graded as nondiagnostic due to absent or low signal intensity.
For the 23 cases in which the origins of the carotid arteries were depicted on contrast-enhanced 3D MR angiograms, the evaluation is presented in Figure 1d. The quality of 21 of these 23 studies (91%) was considered to be either excellent (grade 1) or more than adequate for diagnosis (grade 2).
In 20 of the 40 patients, direct comparison was possible between contrast-enhanced 3D and 2D TOF MR angiograms. In 18 of these 20 patients, the quality of the contrast-enhanced 3D MR angiograms was markedly superior (grade 1, five patients) or superior (grade 2, 13 patients) (P < .001, Wilcoxon signed rank test) (Figs 3a, 4–6). The angiograms were judged to be of comparable quality in two patients. In one of these patients, the carotid bifurcation was at the edge of the torso array coil, which resulted in a moderate dropout of signal on the contrast-enhanced 3D study. In the other patient, imaging was performed with a torso array coil, with a 32 x 32-cm field of view, which resulted in poor visualization of the carotid bifurcation in the contrast-enhanced 3D study. The contrast-enhanced 3D studies were superior to the 2D TOF studies despite the high quality of the latter. In fact, the 2D TOF study was judged to be of excellent quality in 12 patients, but, when compared with the corresponding contrast-enhanced 3D study, the latter was judged to be superior or markedly superior in 11 patients (Fig 3b).
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Although real-time fluoroscopy allows accurate and reliable triggering, it is the elliptic centric view order that allows high-spatial-resolution, venous-suppressed MR angiography (Fig 7). Many previous techniques for performing contrast-enhanced 3D MR angiography of the carotid arteries have been implemented under the premise that image acquisition should be approximately completed in the small, typically 5–8 second arterial window before the appearance of contrast material in the jugular vein. With use of a phase-encoding order that is centric along the two 3D phase-encoding directions, it is possible to obtain a high degree of venous suppression despite use of acquisition times much longer than the arterial-to-venous window. In the patients in this study, these times were typically more than 40 seconds. One may question whether contrast material persists in the arterial vasculature over this entire time and, thus, if meaningful signal is being measured throughout the entire acquisition. Findings in our study suggest that contrast material is present. For example, Figure 8 shows the signal measured in regions of interest at the carotid bifurcation and the jugular vein in a patient study in which the fluoroscopic sequence was performed continuously without triggering a 3D sequence but with the same contrast material injection technique as was used for the 3D studies. Contrast material persisted in the artery as long as 1 minute after arrival. Further study of the interplay between contrast material administration and spatial resolution is warranted.
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In conclusion, real-time MR fluoroscopic triggering offers a reliable method for detection of the contrast material bolus in contrast-enhanced MR angiograms of the carotid arteries and aortic arch. When combined with an elliptic centric view order, it is possible to obtain high-quality, high-spatial-resolution arterial phase images with imaging times as long as 49 seconds.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantors of integrity of entire study, J.H., S.J.R.; study concepts, J.H., S.B.F., S.J.R., A.H.W.; study design, J.H., S.J.R., A.H.W.; definition of intellectual content, J.H., S.B.F., S.J.R., A.H.W.; literature research, J.H., S.J.R.; clinical studies, J.H.; experimental studies, S.B.F., S.J.R., A.H.W., M.A.B., R.F.B.; data acquisition, J.H., S.B.F., A.H.W.; data analysis, J.H., S.B.F., S.J.R., A.H.W.; statistical analysis, S.B.F., S.J.R.; manuscript preparation, J.H., S.B.F., S.J.R.; manuscript editing, J.H., S.B.F., S.J.R., M.A.B.; manuscript review, A.H.W., R.F.B.
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J. H. III, S. B. Fain, J. T. Wald, P. H. Luetmer, C. H. Rydberg, D. J. Covarrubias, S. J. Riederer, M. A. Bernstein, R. D. Brown, F. B. Meyer, et al. Carotid Artery: Elliptic Centric Contrast-enhanced MR Angiography Compared with Conventional Angiography Radiology, January 1, 2001; 218(1): 138 - 143. [Abstract] [Full Text]
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M. A. Neimatallah, T. L. Chenevert, R. C. Carlos, F. J. Londy, Q. Dong, M. R. Prince, and H. M. Kim Subclavian MR Arteriography: Reduction of Susceptibility Artifact with Short Echo Time and Dilute Gadopentetate Dimeglumine Radiology, November 1, 2000; 217(2): 581 - 586. [Abstract] [Full Text]
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A. M. Masaryk, R. Frayne, O. Unal, A. H. Rappe, and C. M. Strother Utility of CT Angiography and MR Angiography for the Follow-up of Experimental Aneurysms Treated with Stents or Guglielmi Detachable Coils AJNR Am. J. Neuroradiol., August 1, 2000; 21(8): 1523 - 1531. [Abstract] [Full Text]
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X. Leclerc, L. Nicol, J.-Y. Gauvrit, V. L. Thuc, D. Leys, and J.-P. Pruvo Contrast-enhanced MR Angiography of Supraaortic Vessels: The Effect of Voxel Size on Image Quality AJNR Am. J. Neuroradiol., June 1, 2000; 21(6): 1021 - 1027. [Abstract] [Full Text]
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E. R. Melhem, J.-M. Serfaty, L. Jones, R. Itoh, B. S. Kuszyk, J.-B. Martin, P. Gailloud, K. P.J. Murphy, and D. A. Rufenacht Contrast-enhanced MR Angiography: The Effects of k-Space Truncation on Luminal Representation in a Carotid Artery Phantom Model AJNR Am. J. Neuroradiol., June 1, 2000; 21(6): 1028 - 1031. [Abstract] [Full Text]
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S. J. Riederer, M. A. Bernstein, J. F. Breen, R. F. Busse, R. L. Ehman, S. B. Fain, T. C. Hulshizer, J. H. III, B. F. King, D. G. Kruger, et al. Three-dimensional Contrast-enhanced MR Angiography with Real-time Fluoroscopic Triggering: Design Specifications and Technical Reliability in 330 Patient Studies Radiology, May 1, 2000; 215(2): 584 - 593. [Abstract] [Full Text]
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B. C. Bowen MR Angiography of Spinal Vascular Disease: What about Normal Vessels? AJNR Am. J. Neuroradiol., November 1, 1999; 20(10): 1773 - 1774. [Full Text]
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 I. M. Meissner Expert Commentary Perspectives in Vascular Surgery and Endovascular Therapy, January 1, 1999; 12(1): 27 - 29. [PDF]
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