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Head and Neck Imaging |
1 From the Departments of Radiology (O.E.H.E., W.P.T.M.M.), Surgery (B.C.E.), and Neurology (L.J.K.), and the Julius Center for Health Sciences and Primary Care (P.J.N., Y.G.), University Medical Center Utrecht, Heidelberglaan 100, Rm E 01.132, 3508 GA Utrecht, the Netherlands. Received July 2, 2002; revision requested August 28; revision received October 16; accepted January 3, 2003. Supported in part by grant OG/030 from the Dutch Ministry of Health, Welfare, and Sports. Address correspondence to W.P.T.M.M. (e-mail: w.mali@azu.nl).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Enhanced and 3D TOF MR angiography and DSA were performed in 51 consecutive patients suspected of having carotid artery stenosis at duplex ultrasonography. Stenoses were measured by two independent observers blinded to clinical information and other test results. Pearson correlation coefficients were used, and 
for interobserver variabilities was estimated. Sensitivity and specificity of enhanced and 3D TOF MR angiography were calculated and compared with those of DSA.
RESULTS: Pearson correlation coefficients were 0.94 (P < .01) for enhanced angiography versus DSA, 0.92 (P < .01) for 3D TOF angiography versus DSA, and 0.93 (P < .01) for enhanced versus 3D TOF angiography for observer 1 and 0.94 (P < .01), 0.95 (P < .01), and 0.94 (P < .01), respectively, for observer 2. statistics were 0.81 for enhanced angiography, 0.79 for 3D TOF angiography, and 0.78 for DSA. Stenosis measurements of observer 1 at enhanced MR angiography, with inclusion of carotid arteries on the symptomatic side only, compared with those of DSA yielded a sensitivity of 90% (95% CI: 68%, 99%) and a specificity of 77% (95% CI: 55%, 92%). 3D TOF angiography yielded a sensitivity of 86% (95% CI: 67%, 97%) and a specificity of 73% (95% CI: 50%, 89%) compared with those of DSA. For observer 2, sensitivity and specificity for enhanced angiography were 91% (95% CI: 70%, 99%) and 76% (95% CI: 52%, 91%), respectively, and 90% (95% CI: 68%, 99%) and 77% (95% CI: 51%, 92%), respectively, for 3D TOF angiography.
CONCLUSION: Accuracy of enhanced MR angiography in diagnosis of severe stenosis is similar to that of 3D TOF MR angiography.
© RSNA, 2003
Index terms: Angiography, comparative studies, 172.12142, 172.12143, 172.1247 • Carotid arteries, stenosis or obstruction, 172.721 • Digital subtraction angiography, 172.1247 • Magnetic resonance (MR), contrast enhancement, 172.12143 • Magnetic resonance (MR), three-dimensional, 172.12142, 172.12143 • Magnetic resonance (MR), time of flight, 172.12142, 172.12143
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The degree of stenosis in the endarterectomy trials was established with conventional intraarterial digital subtraction angiography (DSA), which has become the standard of reference for selecting patients for carotid surgery. DSA in patients with atherosclerosis, however, has a relatively high risk of morbidity and mortality. A 4% risk of transient ischemic attack or minor stroke, a 1% risk of major stroke, and even a small (<1%) risk of death have been reported (5,6). Even patients without apparent neurologic complications after DSA have been shown to develop minor asymptomatic infarctions due to microembolisms (7).
Therefore, noninvasive or minimally invasive techniques such as three-dimensional (3D) time-of-flight (TOF) magnetic resonance (MR) angiography and contrast material–enhanced MR angiography are increasingly used supplementary to duplex ultrasonography (US) in the diagnosis of carotid artery stenosis. In the past decade, 3D TOF MR angiography was the most commonly applied angiographic technique. Findings of several studies have proved good diagnostic performance in the selection of patients for carotid artery surgery (8–13). More recently, contrast-enhanced MR angiography has been introduced, which enables visualization of a longer tract of the carotid artery, including origin and intracranial parts, compared with visualization at 3D TOF MR angiography (14–16). Furthermore, enhanced MR angiography diminishes the possibility of flow-related artifacts, one of the drawbacks of the TOF technique. To date, however, only few study findings have been published reporting the results of enhanced MR angiography that validated against the reference standard DSA (17). A recently published systematic review concluded that MR angiography is highly sensitive and specific in helping to diagnose severe carotid artery stenosis (70%–99%); however, studies of poor and heterogeneous quality were included (18). More important, the authors concluded that further research is essential to assess the diagnostic value of enhanced MR angiography. We recently developed a 3D enhanced MR angiographic technique that depicts the complete tract of the carotid artery, from the origin to the siphon, within 10 seconds before venous return. The high spatial resolution of 0.75 x 0.75 x 1.0 mm should potentially allow good visualization of near occlusions with high flow velocities in the internal carotid artery (ICA) and decrease the effect of flow-related artifacts (19–21).
The aim of this study was to assess the accuracy of enhanced MR angiography compared with that of 3D TOF MR angiography and of the reference standard DSA in the diagnosis of carotid artery stenosis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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For the TOF protocol, a sagittal two-dimensional phase-contrast scout image with 30-cm-1 velocity encoding and two-dimensional TOF images (30 consecutive 4-mm-thick transverse sections) were acquired for localization of the carotid arterial bifurcation and for planning the 3D TOF acquisition. Carefully planned 3D TOF MR angiography was performed by using a radiofrequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections (interpolated to 100 sections), a superior saturation band, 31/6.9, 15° flip angle, flow compensation, 120 x 80-mm field of view, 256 x 256 matrix, and three signals acquired. Imaging time was approximately 9 minutes.
TOF MR angiography was always performed prior to enhanced MR angiography to avoid image disturbances due to the remaining contrast material. In both, 3D TOF and enhanced MR angiography, postprocessing subvolumes were generated to isolate each carotid artery and create 12 maximum intensity projections that were radially projected at 15° increments (rotation about the long axis of the body).
Intraarterial DSA was performed with an angiographic unit (Integris V3000; Philips Medical Systems) with an image intensifier matrix of 1,024 x 1,024. With use of the Seldinger technique, the tip of a 5-F catheter was guided from the common femoral artery to the ascending aorta and positioned in the right and, subsequently, in the left common carotid artery. Two or three projections (lateral, posteroanterior, and/or ipsilateral oblique) were acquired from each carotid bifurcation. For each projection, 6 mL of contrast agent (Ultravist, 300 mg of iodine per milliliter; Schering) was injected at a flow rate of 3 mL/sec.
Results of 3D TOF MR angiography, enhanced MR angiography, and DSA were read independently by two observers (O.E.H.E., P.J.N.), with at least 1 month between the readings. The tests were read with the observers blinded to patient names, clinical information, and results of the other tests. ICA stenosis was measured on printed hard copies according to the following NASCET method: Stenosis = 1 - (Minimal Residual Lumen/ Distal ICA Lumen Diameter) x 100%, by using a mechanical caliper with a digital display. At DSA, the percentage of ICA stenosis was measured on all available projections, which showed the ICA without overlapping the vessels. From the 12 MR angiographic maximum intensity projections, the percentage of ICA stenosis was assessed on three projections, which coincided with the majority of the intraarterial DSA projections used (lateral, posteroanterior, and 45° ipsilateral oblique). Flow void artifacts at 3D TOF MR angiography were defined as 85% stenosis.
Studies Excluded
Enhanced MR angiography was of nondiagnostic quality in five patients. These patients were excluded from the analyses. Reasons for nondiagnostic quality were failure in the timing of contrast material arrival and the start of imaging, which caused too much venous overprojection of the jugular vein for an adequate assessment of the degree of ICA stenosis. The five nondiagnostic enhanced MR angiographic procedures were performed in the first phase of the study. After the first phase of our study, failure in timing no longer occurred. The test results of the remaining 46 patients (92 arteries) were included in the analyses.
Image Analysis
First, the data were analyzed, including two arteries per patient (ie, both carotid arteries), to compare all stenosis measurements from enhanced and 3D TOF MR angiography with the reference standard DSA and to compare those from enhanced and 3D TOF MR angiography. Scatterplots were constructed, and Pearson correlation coefficients were calculated for both observers. Subsequently, for all three imaging tests, the interobserver variabilities were calculated by using statistics with the following categorized stenosis: 0%–29%, 30%–49%, 50%–69%, 70%–99%, and 100% (occlusion).
In the second part of the analysis, to assess the accuracy of enhanced and 3D TOF MR angiography compared with that of DSA in the diagnosis of severe stenosis (70%–99%), with regard to the decision making for carotid endarterectomy, we included only one carotid artery per patient (ie, the symptomatic side). In the two asymptomatic patients, that side was included for which carotid endarterectomy was considered. We calculated the sensitivity and specificity with 95% CIs at enhanced and 3D TOF MR angiography compared with those at DSA for both observers.
Finally, the frequency of flow-related artifacts at 3D TOF MR angiography and of possible tandem lesions at DSA and enhanced MR angiography (ie, stenosis >50% in the origin, in the siphon, or elsewhere in the tract of the carotid artery) were recorded.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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statistics that reflected the interobserver variability between observers 1 and 2 were very good and similar for the three tests: 0.81 for enhanced MR angiography, 0.79 for 3D TOF MR angiography, and 0.78 for DSA.
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Figure 2 represents a case in which 3D TOF MR angiography yielded a false-positive occlusion, whereas enhanced MR angiography depicted the nearly occluded lumen of the ICA similarly to the images of the reference test DSA.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MR angiography is used increasingly in imaging of carotid artery stenosis. In the past decade, findings of several studies have been published in which MR angiography was compared with DSA (8–13). The most commonly applied technique in these studies was TOF MR angiography. In the past few years, implementation of enhanced MR angiography has been repeatedly suggested in the diagnosis of carotid artery stenosis (14–16). Enhanced MR angiography of the carotid arteries is a recent development that could minimize signal loss and motion artifacts. By using an intravenous bolus of contrast material, this technique allows shorter T1 and a larger flip angle, generating a stronger signal with better background suppression and less signal saturation. Suppression of signal from the jugular vein overlapping the carotid bifurcation, however, has been one of the main drawbacks. Suppression can be achieved by imaging the carotid arteries within 10 seconds after enhancement (before venous return). Until recently, the poor resolution of 3D methods, however, even with high-gradient hardware, did not allow accurate measurements of carotid stenosis (19). Nowadays other methods for venous signal suppression that allow longer imaging time and, hence, better spatial resolution are available (22–24).
To date, however, findings of only few studies have been published in which enhanced MR angiography was compared with the reference test DSA in sufficiently large populations (17,19–21). In 1998, Slosman et al (19) introduced a non–breath-hold 3D gadolinium-enhanced MR angiographic technique, but concluded after comparison with 3D TOF MR angiography and DSA in 50 patients that the technique could not yet be recommended for the diagnosis of carotid artery stenosis. The main limitations were problems with the timing of contrast material arrival and consequently the overprojection of the jugular veins in about 30% of the carotids. Serfaty et al (17) found a sensitivity and specificity of 94% and 85%, respectively, for 3D enhanced MR angiography in a population of 48 patients. In their study, 90% of the tests yielded good image quality. They concluded, however, that enhanced MR angiography should not be used as a stand-alone examination but only in combination with duplex US instead of DSA. Randoux et al (20) compared enhanced MR angiography and DSA in 22 patients and found a sensitivity and specificity of 93% and 100%, respectively. Their conclusion was that enhanced MR angiography could be an adequate substitute for DSA. In their series, they found only two cases in which enhanced MR angiography was less than adequate for diagnosis. Recently, Remonda et al (21) compared first-pass enhanced MR angiography with DSA in 120 patients and found agreement in 93% between both tests in the detection of severe stenosis (70%–99%). The quality of enhanced MR angiographic images of all patients was graded as adequate for diagnosis.
We have recently developed a 3D enhanced MR angiographic technique that helps visualize the complete tract of the carotid artery from the origin to the siphon. The technique uses an optimized centric profile ordering of the k space, allowing data acquisition during the uptake of arterial contrast media and ensuring improved resolution by exploiting the tail of the bolus of contrast material, longer imaging time, improved venous suppression, and improved robustness to errors in timing. The high resolution of 0.75 x 0.75 x 1.0 mm and the use of optimized profile ordering should potentially allow good visualization of near occlusions with high flow velocities in the ICA and decrease the effect of flow-related artifacts. Furthermore, another advantage is the significant shorter imaging time of 44 seconds for enhanced MR angiography, compared with that of 3D TOF MR angiography, in which an imaging time of approximately 9 minutes is requested. As in other studies, the timing of the arrival of the bolus of contrast material and the start of imaging was the most crucial part in the introduction of this new procedure. With the implementation of a new technique, MR technologists, however, experience a learning curve. The five nondiagnostic enhanced MR angiographic procedures were performed in the first period of the study. After the first phase of our study, failure in timing no longer occurred.
Our reported accuracies in the diagnosis of severe stenosis (70%–99%) might seem relatively low compared with those in the literature. However, one should realize that we included only the symptomatic arteries (ie, one carotid artery per patient) in this part of our analysis, contrary to the arteries included in studies in the literature (17,19–21). Inclusion of all arteries yields a higher specificity because the asymptomatic artery often shows a stenosis far beyond the cutoff point of 70% and, therefore, often will be classified correctly with both tests in the comparisons. Inclusion of stenosis measurements of all arteries (both asymptomatic and symptomatic sides) in our data (observer 1) would result in a sensitivity of 90% and a specificity of 89% for enhanced MR angiography. These numbers are consistent with those in the literature, and we can conclude that we found a similar accuracy for enhanced MR angiography.
It is preferable to investigate a larger population. Earlier, however, we performed a diagnostic study comparing 3D TOF MR angiography with DSA in 350 patients (25). On the basis of the results of this study, we no longer routinely perform DSA in all patients in whom carotid endarterectomy is considered. Therefore, we no longer have the reference standard at our disposal in a consecutive patient series. This implies an important limitation in the validation of enhanced MR angiography and of any new technique in carotid artery imaging with regard to the endarterectomy trials.
In our relatively small study population, we could not find a significant difference in accuracy between 3D TOF MR angiography and enhanced MR angiography. However, even if a larger population was to be investigated, it remains uncertain if possible advantages of enhanced MR angiography over 3D TOF MR angiography can be reflected in a significantly different accuracy. For example, with enhanced MR angiography, the occurrence of flow void artifacts strongly diminishes. Because flow voids at 3D TOF MR angiography occur in approximately 15% of the imaged arteries and are classified correctly as severe stenosis (70%–99%) in 85% of the cases, the number of patients needed to find a significant difference between the two techniques would be more than 1,000 (26). However, there certainly is a clinical advantage in the availability of good morphology of severely stenosed arteries provided by enhanced MR angiography. Furthermore, in our study, enhanced MR angiography helped to correctly classify all occlusions.
Finally, as with DSA, enhanced MR angiography allows visualization of a long tract, from the origin to the siphon, of the carotid artery. In a preliminary evaluation, the two additional lesions diagnosed at DSA (one in the carotid origin and the other in the intracranial siphon) could be confirmed with enhanced MR angiography. The accuracy of enhanced MR angiography in depicting tandem lesions was not yet studied properly. Although the effect of additional morphologic information of tandem lesions on the results of carotid endarterectomy has not yet been entirely studied, it is certainly often taken into account in decision making regarding performance of carotid endarterectomy in individual cases (27).
In conclusion, enhanced MR angiography seems a promising new technique in the imaging of carotid arteries. First results show a similar accuracy to that of 3D TOF MR angiography in the diagnosis of severe stenosis. Our reported diagnostic accuracy is comparable with that in recent literature. Enhanced MR angiography should preferably be compared with DSA in a larger study population. To date, however, DSA is often no longer routinely performed in all patients in whom carotid endarterectomy is considered. Therefore, an exact estimate of the accuracy of enhanced MR angiography compared with that of DSA, with regard to the results of the carotid artery surgery trials, remains undetermined.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, P.J.N., Y.v.d.G., W.P.T.M.M.; study concepts, Y.v.d.G., B.C.E., W.P.T.M.M.; study design, all authors; literature research, P.J.N., O.E.H.E.; clinical studies, all authors; data acquisition, P.J.N., O.E.H.E.; data analysis/interpretation, all authors; statistical analysis, P.J.N., Y.v.d.G.; manuscript preparation, P.J.N., Y.v.d.G., B.C.E., W.P.T.M.M.; manuscript definition of intellectual content, P.J.N., Y.v.d.G., L.J.K., W.P.T.M.M.; manuscript editing, P.J.N., O.E.H.E., Y.v.d.G.; manuscript revision/review and final version approval, all authors
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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