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Head and Neck Imaging |
1 From the Departments of Neuroradiology (N.A., F.S., L.S., C.R., L.S.P., G.S.) and Vascular Surgery (R. Castellano, R. Chiesa), Scientific Institute, Ospedale San Raffaele, Milan 20132, Italy; and Worldwide Medical Affairs, Bracco Imaging, Milan, Italy (M.A.K.). Received December 17, 2003; revision requested February 24, 2004; final revision received September 1, 2004; accepted September 29. Address correspondence to N.A. (e-mail: anzalone.nicoletta{at}hsr.it).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: The study had Ethics Committee approval, and each patient gave written informed consent. Forty-nine patients (18 women, mean age, 67.2 years ± 9.1 [± standard deviation], and 31 men, mean age, 63.1 years ± 8.0) with symptomatic stenosis of internal carotid artery (ICA) diagnosed at duplex ultrasonography underwent transverse 3D TOF MR angiography with sliding interleaved kY acquisition and coronal contrast-enhanced MR angiography, followed by DSA and rotational angiography within 48 hours. MR angiography was performed at 1.5-T with a cervical coil. Contrast-enhanced MR angiograms were obtained after a bolus injection of 20 mL of gadobenate dimeglumine. Maximum ICA stenosis on maximum intensity projection and source images was quantified according to NASCET criteria. Correlations for 3D TOF MR angiography, contrast-enhanced MR angiography, DSA, and rotational angiography were determined by means of cross tabulation, and accuracy for detection and grading of stenoses were calculated. Data were evaluated with analysis of variance, Wilcoxon signed rank test, and McNemar test, all at significance of P < .05.
RESULTS: Ninety-eight ICAs were evaluated at contrast-enhanced MR angiography, DSA, and rotational angiography, and 97 were evaluated at 3D TOF MR angiography. Correlations for contrast-enhanced MR angiography, 3D TOF MR angiography, and DSA relative to rotational angiography were r2 = 0.9332, r2 = 0.9048, and r2 = 0.9255, respectively. Lower correlation (r2 = 0.8593) was noted for contrast-enhanced MR angiography and DSA. Respective sensitivity and specificity for detection of hemodynamically relevant stenosis relative to rotational angiography were 100% and 90% for contrast-enhanced MR angiography, 95.5% and 87.2% for 3D TOF MR angiography, and 88.6% and 100% for DSA. Four of 31 severe stenoses were underestimated at DSA, and three were underestimated at contrast-enhanced MR angiography. Three severe stenoses were underestimated at 3D TOF MR angiography, and one was misclassified as occluded. Of 13 moderate (50%–69%) stenoses, one was overestimated at contrast-enhanced MR angiography, two were underestimated and three overestimated at 3D TOF MR angiography, and two were underestimated at DSA.
CONCLUSION: DSA results in an underestimation of ICA stenosis compared with rotational angiography. Contrast-enhanced MR angiography correlates best with rotational angiography.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The limitations inherent to conventional DSA in two or three projections may, in part, explain the apparent overestimation of ICA stenosis, which is sometimes seen at both unenhanced (19–21) and contrast-enhanced (9–12) MR angiography of the carotid artery for which multiple projections are available. Accordingly, the present study was conducted to compare prospectively the correlations between unenhanced three-dimensional (3D) time-of-flight (TOF) MR angiography, contrast-enhanced MR angiography, conventional DSA, and rotational angiography for the depiction of stenosis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Imaging Procedures
All MR angiographic examinations were performed with a 1.5-T imager (Eclipse; Marconi, Cleveland, Ohio) equipped with a gradient of 27 mT/m and a standard cervical coil. The carotid bifurcation was localized through the acquisition of a fast gradient-echo sequence (repetition time msec/echo time msec, 16/3.7; flip angle, 20°; field of view, 300 x 300 mm; matrix, 128 x 128) in three planes. Unenhanced 3D TOF MR angiography was then performed in the transverse plane by using a sliding interleaved kY acquisition sequence comprising eight overlapping slabs of 11 sections, each with a section thickness of 1 mm, a superior saturation band, 30/6.7, 35° flip angle, 200 x 200 mm field of view, 160 x 256 matrix, and one signal acquired. The final pixel size was 0.8 x 1.25 mm, and the entire imaging time was approximately 8 minutes. Twelve maximum intensity projection images were generated during postprocessing for each isolated carotid artery.
Contrast-enhanced MR angiography was performed in the coronal plane immediately after 3D TOF MR angiography. After a preliminary mask image was acquired, patients were administered a 2-mL test bolus of gadobenate dimeglumine (MultiHance; Bracco Imaging, Milan, Italy) to determine the contrast agent arrival time. A standard 20-mL volume of gadobenate dimeglumine was subsequently injected into each patient. All injections were performed at a rate of 2 mL/sec by means of an MR-compatible power injector (Spectris; Medrad, Indianola, Pa) and were followed by a 20-mL flush of 0.9% saline that was injected at the same rate. A 3D radiofrequency spoiled gradient-echo MR imaging sequence was used with the following parameters: 4.8/1.9, flip angle of 40°, field of view of 240 x 320 mm, matrix of 128 x 256, one signal acquired, and a final pixel size of 1.25 x 1.8 mm. Two consecutive acquisitions of 44 coronal sections, each with a section thickness of 1.8 mm, were performed, which resulted in an overall imaging time of 40 seconds. Image postprocessing involved subtraction of the initial mask image and elaboration of the 12 maximum intensity projection images of isolated carotid arteries, which were radially projected at 12° increments. MR angiography was performed by one of three authors (N.A., 16 years experience; L.S., 7 years experience; or L.S.P., 5 years experience).
Conventional intraarterial DSA and rotational angiography were performed during the same session by one of two interventional radiologists (F.S., 10 years experience, or C.R., 20 years experience) within 48 hours of MR angiography. Both conventional DSA and rotational angiography were performed in each patient by the same interventionalist. A biplanar rotational angiography unit (AdvantiX; GE Medical Systems, Milwaukee, Wis) was used with an image intensifier matrix of 1024 x 1024 and a final pixel size of 0.21 mm. For catheter placement, a femoral artery approach was employed in which the tip of a 5-F catheter (Boston Scientific, Natick, Mass) was guided from the right or left common femoral artery to the ascending aorta and positioned in the right and left common carotid arteries. Two projections (posteroanterior and either lateral or ipsilateral oblique) were typically acquired at each carotid bifurcation. A third projection was acquired in patients who had overlapping vessels that were noted on the original two projections. For each projection, 10 mL of nonionic iodinated contrast material (iopamidol, Iopamiro 300; Bracco Imaging) was injected intraarterially at a flow rate of 4 mL/sec by means of an automatic injector (Mark V; Medrad).
The two MR angiographic examinations and the conventional DSA examination were considered to be of adequate diagnostic quality when artifact-free images were acquired that permitted accurate measurements of the distal ICA diameter and the minimal residual lumen.
Rotational angiography was performed in addition to conventional DSA in both the left and right carotid arteries in all patients. While the catheter from the conventional DSA examination was still in position, the angiographic unit began imaging in the lateral position and then rotated 220° around the carotid bifurcation in 5 seconds to acquire 44 projections. A 512 x 512 image intensifier matrix was used, with a final pixel size of 0.42 mm. A total volume of 20 mL of iopamidol was injected at a flow rate of 4 mL/sec. The total time needed to perform rotational angiography was 15 seconds (5 seconds to obtain the series of rotational mask images, 5 seconds to reverse the x-ray unit back to its starting position, and 5 seconds to obtain the series of contrast-enhanced images). The rotational angiograms were considered to be of diagnostic quality when contrast material sufficiently filled the ICA for the full 5-second duration of the series so as to allow reliable measurements of the distal ICA diameter and the minimal residual lumen.
Image Evaluation
All examinations were evaluated in randomized order. An experienced neuroradiologist (N.A.) separately and independently evaluated all source images and maximum intensity projections at unenhanced and contrast-enhanced MR angiography without knowledge of the conventional DSA or rotational angiography findings. A second neuroradiologist (F.S.) separately and independently determined the degree of carotid artery stenosis at conventional DSA and rotational angiography without knowledge of the unenhanced and contrast-enhanced MR angiography findings. Images from all available projections from all techniques were made available for assessment. The stenosis of each ICA was graded according to the North American Symptomatic Carotid Endarterectomy Trial criteria (15): percentage stenosis equals one minus the quotient of minimal residual lumen divided by distal ICA lumen diameter, all multiplied by 100. Stenoses demonstrated at each imaging procedure were graded according to the five-point North American Symptomatic Carotid Endarterectomy Trial classification scheme: 0%–29%, 30%–49%, 50%–69%, 70%–99%, and 100% stenosis (complete occlusion).
Statistical Analysis
Correlation coefficients for comparisons among the techniques were computed from scatter plots. The overall level of under- or overestimation of stenosis at contrast-enhanced MR angiography, 3D TOF MR angiography, and conventional DSA was determined according to the differences between these techniques and rotational angiography and was tested by means of a two-factor analysis of variance performed on ranks within each ICA. The Wilcoxon signed rank test was used to perform an additional analysis for each technique to determine whether the overall level of under- or overestimation of stenosis was significantly different from zero. Further comparisons were performed by using a two-factor analysis of variance to determine possible differences between contrast-enhanced MR angiography and 3D TOF MR angiography and between the two MR angiography techniques combined and conventional DSA. To investigate the possibility of dependency between the left and right ICAs in each patient, we additionally analyzed the data by using a general estimating equation.
Sensitivity, specificity, positive predictive value, and negative predictive value, together with the 95% confidence intervals for each, were determined for contrast-enhanced MR angiography, 3D TOF MR angiography, and conventional DSA by using rotational angiography as the reference standard and for contrast-enhanced MR angiography and 3D TOF MR angiography by using conventional DSA as the reference standard. Values were calculated both for the detection of hemodynamically relevant (50%–99%) stenoses and for the detection of severe (70%–99%) stenoses. On the basis of these data, the overall accuracy was calculated for contrast-enhanced MR angiography, 3D TOF MR angiography, and conventional DSA versus rotational angiography and for contrast-enhanced MR angiography and 3D TOF MR angiography versus conventional DSA. TheMcNemar test was used to determine possible significant differences in overall accuracy between each of the different imaging techniques and rotational angiography.
All statistical analyses were performed by using a commercially available statistical software package (SAS, version 8.2; SAS Institute, Cary, NC). For all tests, a P value of <.05 was considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Overall Agreement for Imaging Techniques
The overall agreement for contrast-enhanced MR angiography, 3D TOF MR angiography, and conventional DSA relative to rotational angiography and for contrast-enhanced MR angiography relative to conventional angiography is represented in the scatter plots shown in Figure 1. The greatest overall agreement, as judged from evaluations of correlation, was between contrast-enhanced MR angiography and rotational angiography (r2 = 0.9332) and between conventional DSA and rotational angiography (r2 = 0.9255). Notably, the lowest correlation was for the comparison between contrast-enhanced MR angiography and conventional DSA (r2 = 0.8593). For both contrast-enhanced MR angiography and 3D TOF MR angiography, the scatter plots revealed similar overall patterns, with discordant points evenly distributed above and below the lines of correlation. For the comparison between conventional DSA and rotational angiography, however, the discordant points were generally below the line of correlation, indicating an overall underestimation of the degree of stenosis at conventional DSA compared with rotational angiography. For the comparison between contrast-enhanced MR angiography and conventional DSA, the majority of discordant points were above the line of correlation, indicating an overall overestimation of stenosis at contrast-enhanced MR angiography compared with conventional DSA.
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The difference between rotational angiography and each of the three imaging modalities was significantly different from zero for each technique (P = .002 for contrast-enhanced MR angiography, P = .001 for 3D TOF MR angiography, and P = .002 for conventional DSA), as determined by using the Wilcoxon signed rank test.
Detection of Hemodynamically Relevant Stenoses for Each Imaging Technique Relative to Rotational Angiography
The level of agreement for contrast-enhanced MR angiography, 3D TOF MR angiography, and conventional DSA relative to rotational angiography is shown in Table 1. Overall, hemodynamically relevant stenoses (50%–99%) were detected in 44 (45%) of 98 arteries at rotational angiography. Of these stenoses, 31 of 44 were classified as severe (grade 4, 70%–99%), whereas 13 were classified as moderate (grade 3, 50%–69%). Of the hemodynamically relevant stenoses detected at rotational angiography, all 44 (100%) were demonstrated at contrast-enhanced MR angiography. One stenosis that was classified as moderate at rotational angiography, however, was overestimated as severe at contrast-enhanced MR angiography. Three of the 31 stenoses classified as severe at rotational angiography were misclassified moderate (one grade lower, 50%–69%) at contrast-enhanced MR angiography.
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Detection of Hemodynamically Relevant Stenoses at MR Angiography Relative to Conventional DSA
An evaluation of the agreement between contrast-enhanced MR angiography and 3D TOF MR angiography by using conventional DSA as the reference standard is shown in Table 3. Of the 12 stenoses graded as moderate (50%–69%) at conventional DSA, 11 were correctly classified at contrast-enhanced MR angiography, and one was overestimated as severe. At 3D TOF MR angiography, on the other hand, one of 12 stenoses was underestimated, and two of 12 stenoses were overestimated. Of the 27 stenoses that were classified as severe at conventional DSA, 26 were correctly classified at contrast-enhanced MR angiography, but one was underestimated as one category lower. At 3D TOF MR angiography, 25 of 27 stenoses were correctly classified, one stenosis was underestimed, and the remaining stenosis was classified as occluded.
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A consequence of underestimation at conventional DSA compared with rotational angiography was an apparent reduction in the overall accuracy of both contrast-enhanced MR angiography and 3D TOF MR angiography (89.3% and 88.0%, respectively) for detection of hemodynamically relevant stenoses when conventional DSA was used as the reference standard. On the other hand, the overall accuracy of contrast-enhanced MR angiography and 3D TOF MR angiography (95.2% and 92.8%, respectively) for the detection of severe stenoses was largely unchanged, despite the fact that fewer true-positive lesions were considered.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Because there are typically a greater number of projections available for MR angiography than are available for conventional DSA, the possible implications of these findings for studies assessing the accuracy of MR angiography versus conventional DSA may be an apparent overestimation of ICA stenosis. Notably, apparent overestimations have been observed at both unenhanced (19–21) and contrast-enhanced (9–12) MR angiography when conventional DSA was used as the reference standard. In our study, fewer and less dramatic underestimations of ICA stenoses were noted at contrast-enhanced MR angiography and 3D TOF MR angiography than at conventional DSA when rotational angiography was used as the reference standard. Three of 31 severe stenoses were misclassified as one category lower at both contrast-enhanced MR angiography and 3D TOF MR angiography. One of 31 severe stenoses was additionally misclassified as occluded at 3D TOF MR angiography. Better results were noted for the depiction of moderate stenoses for contrast-enhanced MR angiography, for which just one of 13 stenoses was overestimated as severe, than for 3D TOF MR angiography, for which three of 13 stenoses were overestimated as severe and two of 13 were underestimated as not hemodynamically relevant (30%–49%). Notably, patients with moderate (50%–69%) stenoses may still benefit from carotid endarterectomy (23,24).
When rotational angiography was used as the reference standard, similar overall sensitivity and specificity values were obtained for the depiction of severe stenoses at contrast-enhanced MR angiography, 3D TOF MR angiography, and conventional DSA. Of particular interest was the observation of reduced overall accuracy with conventional DSA despite the higher resolution (1024 x 1024) of this technique compared with that of the rotational technique (512 x 512). This finding demonstrates the importance of projection versus spatial resolution for the depiction of eccentric stenoses and serves to emphasize further the inherent limitations of using conventional DSA as the reference standard for diagnostic procedures with multiple projections.
Whereas the sensitivity and specificity of contrast-enhanced MR angiography and 3D TOF MR angiography techniques can already be considered good, a consequence of the underestimation of several high-grade stenoses at conventional DSA was the improved sensitivity and only marginally worsened specificity when conventional DSA was used as the reference standard. These values compare favorably with those reported in the literature for unenhanced TOF MR angiography versus conventional DSA (20,21) and for contrast-enhanced MR angiography versus conventional DSA (1,3–13,25–27). These findings strongly suggest that the apparent overestimations of ICA stenoses in previous studies of unenhanced TOF MR angiography and contrast-enhanced MR angiography versus conventional DSA may result more from underestimation at conventional DSA than from overestimation at MR angiography. Such a conclusion is supported in the present study by the higher overall correlation that was seen in contrast-enhanced MR angiography versus rotational angiography (r2 = 0.9332) than in contrast-enhanced MR angiography versus conventional DSA (r2 = 0.8593).
Although the implications for individual patient care remain to be determined, the results suggest that contrast-enhanced MR angiography is a more appropriate modality for diagnostic imaging of the carotid arteries, particularly when taking into consideration the heightened safety concerns associated with the invasiveness of the DSA procedure. In this regard, early reports on the safety of intraarterial DSA revealed a procedural risk of major stroke of up to 1% and a risk of transient ischemic attack or minor stroke of up to 4% (28,29). Although findings from more recent studies suggest that the prevalence of ischemic attack or stroke after DSA may be slightly lower (30), minor asymptomatic infarctions from microemboli have been reported after DSA even in patients without apparent neurologic complications (31). Conversely, the procedural risk associated with noninvasive or minimally invasive MR angiographic approaches is negligible.
Of interest in the present study was the similar diagnostic performance of 3D TOF MR angiography and contrast-enhanced MR angiography for the depiction of ICA stenoses. The sliding interleaved kY acquisition technique for unenhanced multislab 3D MR angiography overcomes many of the boundary artifacts associated with other multiple overlapped thin-slab acquisition techniques (32,33). In common with other unenhanced TOF techniques (19,20,34,35), however, are the image acquisition times, which are long compared with those of contrast-enhanced MR angiography, particularly for comparatively large fields of view. Thus, while the carotid arteries are reasonably well suited to unenhanced TOF imaging, acquired images are nevertheless still prone to motion artifacts, as well as to the flow-related artifacts that are characteristic of TOF sequences in general (36). As a result, in routine practice, the field of view is typically limited to a volume that principally covers the area of the carotid bifurcation (19). In the present study, despite an overall examination time of approximately 8 minutes, only one ICA was considered unevaluable at 3D TOF MR angiography because of motion artifacts. Furthermore, the only discrepancy among severe stenoses at 3D TOF MR angiography compared with contrast-enhanced MR angiography was the misclassification of one stenosis of 99% as occluded. Thus, the results for unenhanced 3D TOF MR angiography in the present study largely confirm the findings from other studies (19–21,34); that is, that this technique is a valuable tool for the grading of ICA stenosis.
That unenhanced TOF MR angiography has been superceded almost entirely in routine practice by contrast-enhanced techniques can be attributed to the absence of flow-related artifacts for contrast-enhanced MR angiography and to the dramatically reduced overall acquisition times, which have largely overcome the problems associated with patient movement and have permitted image acquisition over much larger fields of view. With the more recent technologic developments, accurate diagnostic imaging with high spatial resolution is now routinely performed from the aortic arch to the circle of Willis (2,8,13).
Finally, the choice of contrast agent for the present study should be considered. Unlike the contrast agents used in previous studies to evaluate contrast-enhanced MR angiography for the depiction of ICA stenoses, gadobenate dimeglumine possesses an approximately twofold higher T1 relaxivity in blood (9.7 [mmol · L–1]/sec) owing to a capacity for weak and transient interaction with serum albumin (37,38). Findings from previous studies in other vascular territories have demonstrated not only that a dose of 0.1 mmol/kg gadobenate dimeglumine is optimal for contrast-enhanced MR angiography (39,40), but also that the signal intensity enhancement that is achieved with this dose is superior to that achieved with an identical dose of conventional gadolinium agents when administered at equivalent flow rate (41–44).
Unfortunately, a limitation of the study is that a standard volume of 20 mL of gadobenate dimeglumine was administered to each patient. Since the body weights of the individual patients were not recorded, it was not possible to determine the precise dose of gadobenate dimeglumine given to each patient. It is common practice in the clinical setting, however, to administer standard volumes of contrast agent rather than to administer a specific dose. Similar approaches have been reported on numerous occasions for studies assessing the accuracy of contrast-enhanced MR angiography in imaging the carotid arteries (2–5,12,14,25,29).
When evaluating the findings of the present study, it should also be noted that all MR angiograms were evaluated by one investigator (N.A.) and that all DSA images were evaluated by another investigator (F.S.). It is common in clinical routine, however, for two or more experienced physicians to evaluate the findings of different diagnostic procedures according to their respective areas of expertise. Therefore, the use of two independent physicians in the present study cannot be considered a source of potential bias. On the contrary, the high level of experience of the two physicians in their respective areas would tend to lend weight to the findings of the study. Of importance, for the purposes of the present study, any possible bias owing to the recall of results from one examination during evaluation of results from another examination by either physician was prevented by means of the complete randomization of images prior to assessment.
In conclusion, findings in the present study confirm the findings of Elgersma et al (17) that conventional DSA frequently causes the degree of ICA stenosis to be underestimated because of the limited number of projections available. Moreover, the better correlation between contrast-enhanced MR angiography and rotational angiography supports the suggestion that previously observed overestimations of stenoses at contrast-enhanced MR angiography compared with conventional DSA may be erroneous. Given the high level of agreement between contrast-enhanced MR angiography and rotational angiography, the safety and rapidity of the procedure, and the level of diagnostic information attainable, we believe contrast-enhanced MR angiography—rather than conventional DSA—should be considered the technique of choice.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Abbreviations: DSA = digital subtraction angiography • ICA = internal carotid artery • 3D = three-dimensional • TOF = time of flight
Author contributions: Guarantors of integrity of entire study, N.A., R. Chiesa, G.S.; study concepts, N.A., G.S.; study design, N.A., G.S., R. Chiesa; literature research, M.A.K., N.A.; clinical studies, N.A., F.S., R. Castellano, L.S., C.R., L.S.P.; data acquisition, N.A., F.S., R. Castellano, L.S., C.R., L.S.P., M.A.K.; data analysis/interpretation, N.A., L.S.P., M.A.K.; statistical analysis, N.A., C.R., M.A.K., L.S.P.; manuscript preparation, M.A.K., N.A.; manuscript definition of intellectual content, N.A., M.A.K., L.S.P.; manuscript editing, M.A.K., N.A.; manuscript revision/review, M.A.K., G.S., N.A., R. Chiesa; manuscript final version approval, N.A., M.A.K., G.S.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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