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Head and Neck Imaging |
1 From the Departments of Diagnostic Radiology (J.H., S.B.F., J.T.W., P.H.L., C.H.R., D.J.C., S.J.R., M.A.B.), Neurology (R.D.B.), Neurologic Surgery (F.B.M.), Vascular Surgery (T.C.B.), and Biostatistics (C.D.S.), Mayo Clinic and Foundation, 200 1st St SW, Rochester, MN 55905. Received November 15, 1999; revision requested December 29; final revision received June 12, 2000; accepted June 28. Supported in part by National Institutes of Health grants CA37993 (J.H., S.J.R.) and HL37310 (S.J.R.) and GE Medical Systems, Milwaukee, Wis (S.J.R.). Address correspondence to J.H. (e-mail: jhuston@mayo.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fifty patients were examined prospectively with contrast-enhanced MR angiography and conventional angiography. The two examinations were performed within 1 week of each other. Two patients underwent conventional angiography of only one carotid artery, which yielded 98 arteries for comparison.
RESULTS: With conventional angiography as the reference standard and by using a 70% threshold for internal carotid arterial diameter stenosis, maximum intensity projection (MIP) images had a sensitivity of 93.3%, specificity of 85.1%, and accuracy of 87.6%, whereas reformatted transverse source images had a sensitivity of 83.3%, specificity of 97.0%, and accuracy of 92.8%. Interobserver variability for conventional angiograms was 0.97, for MIP images was 0.91, and for source images was 0.90. The contrast-enhanced MR angiographic technique had a sensitivity of 88.9% and specificity of 58.1% for the presence of irregularity and/or ulceration. All 50 examinations were triggered appropriately so that minimal or no venous signal intensity was depicted.
CONCLUSION: Contrast-enhanced elliptic centric three-dimensional MR angiography offers high-spatial-resolution, venous-suppressed images of the carotid arteries that appear to be adequate to replace conventional angiography in most patients examined prior to carotid endarterectomy.
Index terms: Carotid arteries, MR, 172.12142, 172.12143 • Carotid arteries, stenosis or obstruction, 172.731 • Magnetic resonance (MR), maximum intensity projection, 172.12142, 172.12143 • Magnetic resonance (MR), three-dimensional, 172.12142, 172.12143 • Magnetic resonance (MR), vascular studies, 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 associated thromboemboli accounts for a substantial percentage of cerebral infarctions. Findings in prospective randomized trials including the North American Symptomatic Carotid Endarterectomy Trial (NASCET) (3,4), European Carotid Surgical Trial (5), and United States Department of Veterans Affairs Cooperative Studies Program (6) have demonstrated relative risk reductions of 70%–85% when endarterectomy is performed in symptomatic patients with diameter stenosis of 70% or more. Final NASCET results recently demonstrated a surgical benefit for selected patients with stenosis as low as 50% (7). As the criteria for determining candidates for carotid endarterectomy evolve into a complex consideration of multiple factors, accurate grading of the degree of carotid stenosis and depiction of ulceration increase in importance.
Conventional cerebral angiography has traditionally been the preoperative test used to determine if a high-grade carotid stenosis is present and whether consideration of surgical intervention is necessary. Improving alternative noninvasive methods of presurgical evaluation and cost considerations recently have affected patient care. Some practices have moved to surgery on the basis of ultrasonography (US) alone, whereas others use a combination of US and time-of-flight magnetic resonance (MR) angiography (8–10).
The introduction of contrast material–enhanced carotid MR angiography has increased the confidence in MR angiographic imaging because of better depiction of arterial detail (11,12). The contrast-enhanced three-dimensional (3D) MR angiographic technique is a rapid acquisition that eliminates many of the time-of-flight MR angiographic artifacts.
A contrast-enhanced 3D MR angiographic technique recently was developed by using elliptical centric view ordering. This technique offers high spatial resolution and acquires the high-contrast elements within k space prior to venous enhancement, which results in a relative suppression of venous signal intensity (13).
The purpose of this study was to evaluate elliptic centric contrast-enhanced MR angiography of the carotid arteries by using conventional angiography as the reference standard.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patients were examined with a 1.5-T unit (Signa Echospeed Superconducting Imaging System; GE Medical Systems, Milwaukee, Wis). The maximum achievable gradient amplitude was 22 mT/m, and the slew rate was 120 T/m/sec. MR angiography was performed by using a volume neck coil and included first, 2D phase-contrast scout imaging; next, 2D time-of-flight imaging; and finally, gadolinium-enhanced 3D gradient-echo imaging. The 2D phase-contrast scout imaging was performed by using a 22 x 16-cm field of view coronal volume, which was 80 mm thick with a 60 cm/sec aliasing velocity. We used 2D time-of-flight imaging with 100 transverse sections 1.5 mm thick from superior to inferior, with the first section positioned just superior to the petrous portion of the internal carotid arteries, as depicted on the 2D phase-contrast scout image. The 2D time-of-flight imaging included a moving superior saturation band, 38/8.7 (repetition time msec/echo time msec), one signal acquired, 256 x 128 matrix, 60° flip angle, and 16 x 16-cm field of view.
Besides being a sensitive but not specific indicator of occlusive disease, the 2D time-of-flight sequence served as a scout for coronal 3D MR angiography performed during the administration of a bolus of contrast material. The transverse collapse maximum intensity projection (MIP) image in the section direction displayed the anterior and posterior margins of the carotid arteries. The superior-to-inferior centering for the gadolinium-enhanced sequence was established by depositing the previously determined anterior and posterior margins on the appropriate image from the 2D time-of-flight sequence.
For gadolinium-enhanced 3D MR angiography, we used a 20 x 15-cm field of view coronal slab, 5.3-cm slab thickness, 38 sections, 6.6/1.4, 45° flip angle, 256 x 168 matrix (due to three-quarter-phase field of view), and imaging time of 44 seconds. Reconstruction was performed with zero filling in all three directions, which yielded 76 sections 1.4 mm thick, with 0.7-mm overlap and a 512 x 336 matrix. The actual voxel size was 0.78 (x) x 0.89 (y) x 1.40 mm, which yielded a voxel volume of 0.97 mm3 before zero filling. Zero filling effectively improves resolution and yields a smaller effective voxel volume with reduced partial-volume signal losses (14).
In the gadolinium-enhanced 3D sequence, elliptic centric view ordering of the phase encoding was used along the y and z directions (15). This technique initially samples the center of k space, which contains the lowest spatial frequencies that determine image contrast. As the sequence progresses, the high spatial frequencies that determine spatial resolution are sampled. Since the lowest spatial frequencies that determine image contrast are acquired first, before appreciable venous enhancement has occurred, this view order suppresses subsequent venous enhancement.
Triggering of the gadolinium-enhanced 3D MR angiography was performed with MR fluoroscopy. A 2D fluoroscopic sequence was used to interactively define a double oblique monitoring plane that contained the common, internal, and external carotid arteries. The monitoring plane was then imaged continuously as the contrast material was injected. The arrival of contrast material was detected, and after a 2-second delay a click of a mouse button triggered the gadolinium-enhanced 3D MR angiography. The intrinsic hardware delay was approximately 20 msec.
Contrast material was injected with a power injector (Spectris; Medrad, Indianola, Pa). All patients received 20 mL of gadoteridol (ProHance; Bracco Diagnostics, Princeton, NJ) injected at 3 mL/sec, followed by 30 mL of a saline solution at a rate of 2 mL/sec. Arrival time of the contrast material was defined as the length of time from injection of contrast material to the point that the arterial opacification reached maximum intensity.
Selective cerebral angiography was performed in all 50 patients through a femoral arterial approach. Predominantly digital subtraction but also biplane film hard-copy techniques were used. Four projections of each carotid bifurcation typically were obtained during conventional angiography.
The contrast-enhanced MR angiograms were graded for diagnostic quality. Classification included diagnostic results, or excellent arterial opacification with minimal venous signal intensity; marginally diagnostic results, or good arterial signal intensity with moderate venous signal intensity (venous signal intensity less than arterial signal intensity); and nondiagnostic results, or poor arterial and/or venous signal intensity equal to or greater than arterial signal intensity.
Three experienced neuroradiologists (J.T.W., P.H.L., C.H.R.) blinded to clinical history and results of other diagnostic tests independently reviewed the MR and conventional angiograms. The conventional and MR angiograms were reviewed at different times. The percentage of carotid stenosis was determined by using the NASCET measurement technique and a jeweler’s eyepiece with 0.1-mm demarcations (16). When an internal carotid artery demonstrated a near occlusion with collapse of the lumen (string sign) on either the MR angiogram or the conventional angiogram, the degree of stenosis was defined as 99%.
The conventional angiograms were arranged in a randomized order, and the degree of carotid stenosis was measured. The gadolinium-enhanced studies were also arranged in a randomized order, different from that in which the conventional angiograms were reviewed. First, MIP subvolume images were measured, and subsequently transverse reformatted source images were measured. The percentage of diameter stenosis for the conventional angiographic and the gadolinium-enhanced MR angiographic MIP subvolume and source images was defined as the mean of the three independent measurements recorded by the three readers using the NASCET measurement technique (16). In addition, the mean of the MIP and source image percentage of diameter stenosis was calculated.
Both the conventional angiographic and MR angiographic MIP images were evaluated for the presence of vascular irregularity and ulcerations. The presence of these findings was defined as agreement of at least two of the readers.
Results of conventional angiography were considered to represent the true disease stage for each artery. Thresholds for disease included diameter stenoses of 70% or greater, 60% or greater, and 50% or greater. For each test, sensitivity (true-positive fraction) and specificity (one minus the false-positive fraction) were calculated. Two-sided 95% CIs at a threshold of 50%, 60%, and 70% stenosis were calculated exactly from the binomial distribution.
To estimate the interobserver variability, the intraclass correlation coefficient was used. This is a measurement of agreement between observers that is adjusted for agreement due to chance alone, with zero equalling no agreement and one equalling perfect agreement (17).
It was hoped that a linear regression model could be determined to compare the agreement between the types of MR and conventional angiograms (18). Linear regression could be used to compare the conventional angiogram with the MIP, source, and mean of the MIP and source images and the multivariate model, including both the MIP and source results. However, comparing R2 as a measurement of how well a regression model will predict accuracy for the univariate models with the R2 of the multivariate model, no improvement was demonstrated. Instead, for clarity we chose to use receiver operating characteristic analysis and calculate the area under the curve (19).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In previous MR angiographic studies (20,21) in which flow-dependent time-of-flight techniques were used, a signal void corresponding to a high-grade stenosis was a relatively frequent finding. With the bolus contrast-enhanced technique, high-grade stenosis appeared as a signal void in only two carotid arteries.
For conventional angiography, the intraclass correlation coefficient was 0.97 (0.96, 0.98); for the MIP images, it was 0.91 (0.87, 0.93), and for the source images it was 0.90 (0.88, 0.94). The 95% CIs, presented in the parentheses, for the MIP and source images overlap each other and are therefore not different. According to Landis and Koch (17), this is almost perfect agreement. The conventional angiographic CI does not overlap the CI of the other two techniques and, therefore, shows higher agreement than either the MIP or source images.
For the MIP images, the area under the curve was 0.98; for the source images, 0.96; and for the multivariate model, 0.97. Therefore, receiver operating characteristic analysis demonstrated no significant difference between the three techniques.
Arrival times of contrast material were determined for 48 of the 50 patients on the basis of the first appearance of contrast material during the 2D MR fluoroscopic portion of the examination. The arrival times of contrast material were 8–18 seconds (mean, 13 seconds).
Five of six near occlusions with distal collapse of the internal carotid artery or string signs were identified with the gadolinium-enhanced technique (Fig 2). The single case in which the carotid artery was falsely classified as occluded with contrast-enhanced MR angiography had extremely slow flow, with contrast material reaching the petrous portion at conventional angiography 15 seconds after injection. Endarterectomy was attempted; however, the artery had progressed to occlusion, and a carotid ligation was performed to prevent subsequent embolic events. One artery was classified by all three readers as nearly occluded on the contrast-enhanced MR angiogram and as occluded on the conventional angiogram (Fig 3). The MR angiogram in this patient was completed less than 1 hour before the conventional angiogram. The remaining 13 occluded internal carotid arteries were accurately characterized by means of the contrast-enhanced technique.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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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 MR acquisition with the subject-dependent delay time between intravenous injection and arrival of contrast material bolus in the carotid arteries. Among the techniques that have been used to address this in the carotid and other vasculature are estimation of arrival time, separate measurement of circulation time by using a test injection of contrast material (25) or magnesium sulfate, use of multiple short (example 10 seconds) 3D acquisitions (26), use of 3D with central k-space views, and real-time triggering (27) with either line scanning or 2D MR fluoroscopy. View sharing offers the possibility of a continuous acquisition with retrospective determination of which views to use in image creation (12,28), and it offers the opportunity to create multiple time-resolved images. All of these techniques have been successful to some degree.
The elliptic centric technique with proper triggering or bolus timing offers reliable venous suppression and extended imaging time to achieve high spatial resolution (29). The elliptic centric technique can be used with standard MR units with enhanced gradients, and no specialized postprocessing of the 3D data set is required. Although the fluoroscopic portion of this study required specialized hardware and software, test bolus timing is a successful alternative timing technique (25).
An advantage of the contrast-enhanced technique is the ability to image from the aortic arch through the intracranial circulation (30). We have chosen to implement the technique in a manner analogous to that used with conventional angiography. When conventional angiography of the carotid arteries is performed, a premium is placed on the use of a small field of view to achieve high spatial resolution.
In this study, a 20 x 15-cm field of view with a volume neck coil was used to achieve 0.97-mm3 voxel volume before zero filling. As this technique is now used routinely in our clinical practice, we have increased the field of view to 22 x 15 cm and increased the number sections to 44, which allows depiction of the vertebral artery origins in virtually every patient. The acquisition time for this sequence is 52 seconds; however, venous suppression is still achieved. Therefore, with a single technique, high-spatial-resolution imaging of the entire vertebral basilar and nearly the entire carotid circulation can be performed. This practice is based on the finding that the presence of a tandem lesion involving the proximal common carotid arteries does not prevent the performance of carotid endarterectomy (31). If imaging of the arch is indicated, a second 24 x 24-cm contrast-enhanced MR angiogram of the aortic arch is obtained.
Because the contrast of the image is determined primarily in the first views of the elliptical centric acquisition, timing is crucial. Excellent results were achieved with all 50 examinations with the fluoroscopic timing technique. This approach allows direct depiction of the contrast material as soon as it appears within the carotid artery. With the first appearance of contrast material, a 2-second delay was included to allow maximum carotid opacification at the initiation of imaging.
As this technique has spread to our clinical practice, a test bolus timing sequence has also been used. The technique includes injection of 2 mL of contrast material at 3 mL/sec followed by 25 mL of normal saline solution at 2 mL/sec. Consistent results have been achieved with strong arterial opacification and venous suppression by using the test bolus in more than 600 clinical examinations. Whether timing is performed with the fluoroscopic technique or a bolus timing sequence, it is critical that imaging be initiated so that the first views correspond to the peak of the arterial opacification. If triggering is performed prior to the arrival of contrast material, marked edge enhancement is present, and there is little signal intensity in the center of the artery.
The elliptic centric contrast-enhanced technique is superior to previous MR angiographic techniques (Fig 5). The 2D time-of-flight and multisection time-of-flight sequences are flow dependent and therefore analogous to US. Signal loss occurs with these techniques in the presence of slow flow such as in ulcers or in the carotid bulb. Also, loss of signal can occur in complex or high flow states such as those that occur with intravoxel dephasing through a high-grade stenosis. Contrast-enhanced MR angiography is physiologically more analogous to conventional angiography. This lumen-filling characteristic allows depiction of slow or stagnant flow, including that in ulcers (Fig 4). The presence of ulceration can have an important effect on patient care (32).
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Because the contrast-enhanced portion of the image is determined during the first seconds of the sequence, there was concern that the elliptical centric technique would not be sensitive to slow flow. However, results of this study indicate that the technique is sensitive to slow flow. Five of six near occlusions with distal collapse of the internal carotid artery were depicted with the technique. One of these five arteries had been imaged with duplex color flow US that characterized the artery as occluded (Fig 2). There was a single vessel for which angiography showed filling of the lumen on images delayed up to 15 seconds that the contrast-enhanced technique did not depict. However, this artery was found to be occluded at attempted endarterectomy. In addition, there was an example of an apparent occlusion at conventional angiography in which the contrast-enhanced technique opacified the internal carotid artery. In this case, conventional angiography was performed less than 1 hour after MR angiography, and it is possible that the vessel occluded between the two examinations. A further study could help delineate the precise accuracy of elliptic centric MR angiography to slow flow; however, these results are encouraging, since the elliptic centric technique depicted slow flow states.
Elliptic centric gadolinium-enhanced MR angiography offers high spatial resolution and reliable venous suppression despite imaging times approaching 1 minute. The use of contrast material provides an examination physiologically analogous to conventional angiography and allows depiction of subtle vascular irregularities and ulceration. The performance and accuracy of elliptic centric contrast-enhanced MR angiography appears to be adequate to replace conventional angiography in the preoperative evaluation of patients prior to carotid endarterectomy.
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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.B.F., S.J.R.; study concepts, J.H., S.B.F., S.J.R., M.A.B.; study design, J.H., S.B.F., S.J.R.; definition of intellectual content, J.H., S.B.F., S.J.R., M.A.B.; literature research, J.H.; clinical studies, J.T.W., C.H.R., P.H.L., R.D.B.; data acquisition, J.H., S.B.F., D.J.C., F.B.M., T.C.B.; data analysis, C.H.R., J.T.W., P.H.L.; statistical analysis, C.D.S.; manuscript preparation, J.H., S.B.F., S.J.R., M.A.B.; manuscript editing, review, and final version approval, J.H., S.B.F., P.H.L., C.H.R., D.J.C., S.J.R., M.A.B., R.D.B., C.D.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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