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Head and Neck Imaging |
1 From the Department of Neuroradiology of Pr Marsault, Groupe Hospitalier Pitié-Salpêtrière, Bâtiment Babinski, 47-83 Boulevard de lHôpital, 75651 Paris Cedex 13, France. Received May 23, 2000; revision requested July 12; final revision received November 27; accepted December 21. Address correspondence to B.R. (e-mail: bruno.randoux@caramail.com).
| ABSTRACT |
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MATERIALS AND METHODS: Forty-four carotid arteries (in 22 patients) were analyzed by using CT angiography, enhanced MR angiography, and DSA. CT and enhanced MR angiograms were reconstructed with maximum intensity projection and multiplanar volume reconstruction. The following four features were analyzed: degree of stenosis on the basis of North American Symptomatic Carotid Endarterectomy Trial criteria, length of stenosis, luminal surface, and presence of ulcers.
RESULTS: There was significant correlation between CT angiography, enhanced MR angiography, and DSA for degree and length of stenosis. With enhanced MR angiography and CT angiography, degree of stenosis was underestimated in two of 44 cases. No case of overestimation with CT angiography was found. Severe internal carotid artery stenoses were detected with high sensitivity and specificity: 100% and 100%, respectively, with CT angiography; 93% and 100%, respectively, with enhanced MR angiography. Luminal surface irregularities were most frequently seen at CT angiography. With CT angiography and enhanced MR angiography, more ulceration was detected than with DSA.
CONCLUSION: There was a significant correlation between CT angiography, enhanced MR angiography, and DSA in evaluation of carotid artery stenosis. Enhanced MR angiography or CT angiography can be used to adequately evaluate carotid stenosis.
Index terms: Angiography, comparative studies, 172.124 Carotid arteries, stenosis or obstruction, 172.721 Computed tomography (CT), angiography, 172.12116 Magnetic resonance (MR), contrast enhancement, 172.121419 Magnetic resonance (MR), vascular studies, 172.12142, 172.12143
| INTRODUCTION |
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Investigators (3,4) concluded that the risk of stroke could be reduced by performing carotid endarterectomy in symptomatic patients with a stenosis of more than 70%. Furthermore, endarterectomy in patients with a symptomatic moderate carotid stenosis of 50%69% produced a moderate reduction in the risk of stroke (5). Investigators in the Asymptomatic Carotid Atherosclerosis Study (6) suggested that asymptomatic patients could benefit from carotid endarterectomy, even with a stenosis of 60%. Other factors are also important in determining whether a carotid lesion will remain clinically silent. Plaques that are more prone to disruption, fracture, or fissuring may be associated with a higher risk of embolization, occlusion, and consequent ischemic neurologic events (7,8). These study findings emphasize the importance of accurate delineation of the morphology of the carotid bifurcation, as well as the degree of stenosis.
The purpose of this study was to prospectively compare gadolinium-enhanced MR angiography and CT angiography with DSA for use in detecting stenosis at the carotid bifurcation, in terms of degree of stenosis and plaque morphology.
| MATERIALS AND METHODS |
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Imaging
DSA was performed with femoral artery catheterization by using the digital subtraction technique (Easyvision; Philips, Best, the Netherlands). Arch aortograms were obtained, followed by selective catheterization of the common carotid arteries. Images were obtained in anteroposterior, lateral, and two oblique projections (-45° and +45°) for each catheterization. The injected volume of nonionic contrast medium was 8 mL for each injection (iohexol, Omnipaque 300; Nycomed, Oslo, Norway). DSA was performed with a 33-cm field of view (FOV) and a 1,024 x 1,024 matrix. The spatial resolution was 0.32 x 0.32 mm.
The CT angiographic images were obtained with a scanner (HiSpeed system; GE Medical Systems, Milwaukee, Wis). Patients were placed in the supine position with the head tilted back as far as possible to avoid inclusion of dental hardware. Patients were instructed to breathe quietly without swallowing during the scanning period. Spiral data were acquired with a 3-mm collimation and a table speed of 3 mm/sec for 60 seconds starting at the seventh cervical vertebra and proceeding as far cephalad as possible. CT parameters included an FOV of 15 x 15 cm, a section thickness of 1 mm, and an imaging time of 60 seconds. With a power injector, 140 mL of nonionic contrast medium (iobitridol, Xenetix 250; Guerbet, Roissy, France) was injected at a rate of 2.5 mL/sec into an antecubital vein. Administration of each bolus was followed immediately by a 20-mL saline flush. The helical acquisition was initiated after the start of the bolus administration of contrast medium, which was determined by a test of circulation time (Smart Prep; GE Medical Systems).
Transverse source images were reconstructed in 1-mm increments by using a small FOV (15 cm). These parameters allowed a spatial resolution of 1.0 x 0.3 x 0.3 mm. Total coverage was 18 cm for a total of 178 reconstructed transverse sections. The reconstructed images were then processed with a Windows (Microsoft, Redmond, Wash) workstation (Advantage; GE Medical Systems) by using both the raw data and multiplanar volume reconstruction (VOXTOOL software; GE Medical Systems). Total postprocessing time was approximately 5 minutes per carotid artery.
Three-dimensional gadolinium-enhanced MR angiography was performed with a 1.5-T unit (Signa; GE Medical Systems) with a neurovascular head and neck coil. Gadolinium-enhanced MR angiography was performed coronally from the arch to the skull base, by using fast imaging, with the following parameters: relaxation time msec/echo time msec, 6/2; signal acquired, 0.5; flip angle, 35°; number of sections, 5256; section thickness, 1.61.8 mm; FOV, 28 x 22 cm; matrix, 256 x 192; imaging time, 32 seconds. The spatial resolution was 1.1 x 1.1 x 1.6 mm. No breath hold was used. Zero filling interpolation was used. The centric phase-ordering scheme was used for k-space filling, which is most sensitive to early image contrast enhancement produced by the arrival of the bolus of contrast material.
The contrast material (gadoterate meglumine, Dotarem; Guerbet; 0.5 mmol/mL) was infused through a 22-gauge venous angiographic catheter in the antecubital fossa, by using a power injector (Spectris; Medrad, Pittsburgh, Pa). Twenty milliliters of contrast material was injected at a rate of 2.5 mL/sec. Administration of each bolus was immediately followed by a 20-mL saline flush. An MR preparation technique (Smart Prep; GE Medical Systems) was used with the tracker placed in the aortic arch.
The images obtained were postprocessed with the workstation (Advantage; GE Medical Systems). MR angiograms were generated in lateral rotations by using a maximum intensity projection algorithm and projections every 10° from -90° to +90°. We also used raw data and multiplanar volume reconstruction to allow better analysis of plaque morphology. All views were evaluated.
Image Analysis
A neuroradiologist (B.M.) retrospectively reviewed image quality of CT angiography, contrast-enhanced MR angiography, and DSA. Image quality was evaluated for overall quality, including vascular signal intensity, venous suppression, and presence of artifacts. The evaluation criteria for overall quality were as follows: 1, excellent; 2, more than adequate for diagnosis; 3, adequate for diagnosis; 4, less than adequate for diagnosis; and 5, nondiagnostic.
For evaluating the degree of carotid artery stenosis, the order of examination was random. The patients name was hidden. Two neuroradiologists (B.M., B.R.) independently interpreted each CT and gadolinium-enhanced MR angiogram. A highly experienced neuroradiologist (A.Z.) reviewed the DSA studies. Each neuroradiologist was blinded to the findings at other examinations. DSA was considered the standard. Evaluation was performed with the computer workstation.
In each case, the projection that demonstrated the most severe stenosis was used. The diameter of the most severe stenosis was divided by the diameter of the distal cervical internal carotid artery (ICA) beyond the stenosis. The resulting value was subtracted from one and then multiplied by 100 to yield the percentage of stenosis according to diameter of the vessel. The stenosis of each ICA was graded according to the following North American Symptomatic Carotid Endarterectomy Trial criteria (3): I, normal; II (1%29%), mildly stenosed; III (30%49%) and IV (50% 69%), moderately stenosed; V (70%99%), severely stenosed; and VI, occluded. For each examination, the measurements of the exact degree of stenosis were made at the level of maximum stenosis by using high magnification and a computer caliper.
At CT angiography, measurements were made on oblique images obtained in a scanning plane strictly perpendicular to the ICA axis. This method could not be used for contrast-enhanced MR angiography because of blurring of the vascular lumen edge due to the lack of spatial resolution. Consequently, measurement at gadolinium-enhanced MR angiography was made on reconstructed images. At contrast-enhanced MR angiography, the lack of luminal visualization at the level of the stenosis, with flow visible distal to the stenosis, was arbitrarily considered as a severe stenosis.
At DSA, gadolinium-enhanced MR angiography, and CT angiography, the length of stenosis was measured on multiplanar reconstruction images. The appearance of the plaque surface was assessed on reconstructed images by studying the interface between the plaque and the vascular lumen. No surgical correlation was available. A plaque was classified as ulcerated if it fulfilled the radiographic criteria of an ulcer niche, seen in profile as a crater penetrating a stenotic plaque. The irregular plaque category was used for wall irregularity or multiple small possible craters (9).
Statistical Assessment
The relationship between CT angiography, contrast-enhanced MR angiography, and DSA in terms of categories of stenosis was analyzed first by using the Spearman rank correlation coefficient (Rs) and second by using the bootstrapping technique (Rb), including the standard error of the correlation. For each gadolinium-enhanced MR and CT angiogram, the degree of agreement between observers in the interpretation of the degree of stenosis was determined by using the
coefficient. Agreements were classified as mild (
> 0.400.69), good (
> 0.700.89), or excellent (
> 0.901.00). The relationship between CT angiography, contrast-enhanced MR angiography, and DSA in terms of length of stenosis was analyzed by using the intraclass correlation coefficient.
| RESULTS |
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The overall quality of all CT angiographic studies was characterized as either excellent (17 studies with grade 1) or more than adequate for diagnosis (five studies with grade 2 because of deglutition artifacts (four studies) and respiratory artifacts (one study).
The overall quality of gadolinium-enhanced MR angiographic studies was characterized as follows: 13 studies were excellent (grade 1); five studies were more than adequate for diagnosis (grade 2) because of venous enhancement, which was less than arterial enhancement; two studies were adequate for diagnosis (grade 3) because of a limited signal-to-noise ratio; and two studies were less than adequate for diagnosis (grade 4) because of lack of luminal visualization at the level of the stenosis. Nevertheless, flow was visible distal to the stenosis, allowing differentiation from occlusion.
Degree of Stenosis
There was a significant correlation between CT angiography and DSA (Rs = 0.93, P < .001; Rb = 0.94, standard error = 0.008, P < .001) and between contrast-enhanced MR angiography and DSA (Rs = 0.92, P < .001; Rb = 0.91, standard error = 0.002, P < .001) for degree of stenosis (Fig 1, Table 1).
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Interobserver agreement for classification of degree of stenosis was judged as excellent for CT angiography (
= 0.92) and good for contrast-enhanced MR angiography (
= 0.87). Discrepancies were observed with two cases of stenosis less than 50%.
Length of Stenosis
We observed a significant correlation in the appreciation of the length of stenosis among the three techniques. The best correlation was observed between gadolinium-enhanced MR angiography and DSA: The intraclass correlation coefficient was 0.84 (P < .001) between contrast-enhanced MR angiography and DSA, 0.79 (P < .001) between CT angiography and gadolinium-enhanced MR angiography, and 0.70 (P < .001) between CT angiography and DSA.
Plaque Irregularities
Plaque irregularities were more frequent at CT angiography (16 cases) than at DSA (11 cases) or contrast-enhanced MR angiography (nine cases) (Table 2). All plaque irregularities assessed at DSA were also visualized at CT angiography. In seven cases, the vascular lumen appeared regular at gadolinium-enhanced MR angiography and irregular at CT angiography.
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| DISCUSSION |
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Good image quality is essential. All CT angiographic images obtained in our study were of diagnostic quality. A CT angiographic image of good quality is easily obtained if the patient does not move or swallow for 1 minute. A breath-hold acquisition is not necessary. Two contrast-enhanced MR angiographic studies were less than adequate for diagnosis (grade 4) because of lack of luminal visualization. Compared with DSA, a major limitation of gadolinium-enhanced MR angiography is spatial resolution. We attempted to optimize spatial resolution by decreasing FOV and section thickness. Although this also resulted in a reduction of the signal-to-noise ratio, no coverage error was made.
By using automatic triggering with detection of the contrast material bolus, we were able to selectively obtain an arterial phase image. Previous studies (11) have shown that a combination of optimal tracking volume placement and adjustment of tracking volume size ensures optimal sensitivity to the contrast material bolus. By choosing a 5 x 20-mm tracker volume placed in the aortic arch, bolus arrival was always detected.
Degree and Length of Stenosis
CT angiography is a highly accurate and precise technique for determining the percentage of stenosis. The rate of agreement in our study was 42 (95%) of 44, which is similar to the rates in other articles (1214) in the literature in which the rate of agreement ranged from 82% to 92%. Precision is reported (15) to depend more on measurement technique than on acquisition parameters. The accuracy of stenosis measurement depends on the scanning plane, which ideally should be perpendicular to the carotid artery, used to obtain magnified transverse oblique images (14).
Some authors (12,14) consider that calcified plaque could be a limitation of CT angiography. This limitation can be avoided when multiplanar volume reconstruction is used, even when circumferential calcified plaques are present. With this technique, we initially visualized the whole bifurcation, including calcifications. Then, decreasing the volume reconstruction, we clearly visualized the residual lumen at the maximal part of the stenosis, even if it was located near intramural calcifications. If multiplanar volume reconstruction is not available, transverse oblique reconstruction can be used. Calcifications should not, therefore, be considered limitations of CT angiography.
Gadolinium-enhanced MR angiography was appropriate for evaluating ICA stenosis, which confirms the results of previous studies (1618). Clinically relevant stenosis and occlusions of the ICA were correctly detected with good sensitivity and specificity and good interobserver agreement. With contrast-enhanced MR angiography, underestimation occurred in two cases of stenosis. Only one case of severe stenosis seen at DSA was judged as moderate at gadolinium-enhanced MR angiography, and this might have led to a nonsurgical treatment if contrast-enhanced MR angiography had been the sole technique used for imaging the carotid arteries. Some studies (17,18) showed that, with gadolinium-enhanced MR angiography, overestimation of the degree of stenosis tends to occur.
In our study, with contrast-enhanced MR angiography, overestimation occurred in two cases of stenosis of greater than 70% with lack of luminal visualization, which was arbitrarily considered as a severe stenosis (19). These artifacts can be due to excessive section thickness, causing a partial volume effect (20,21). Concerning stenosis greater than 70%, the residual lumen is smaller than pixel size. Despite a short echo time, intravoxel dephasing can occur. The signal loss can also be explained by the presence of hemodynamic modifications: The decreased flow caused by stenosis leads to a reduced concentration of contrast agent in the distal arterial lumen, which may also explain why overestimation of stenosis with gadolinium-enhanced MR angiography can occur (22), especially for evaluating the degree of stenosis in small-vessel lumens.
Plaque Irregularities and Ulcerations
Irregularities were more frequent at CT angiography than at DSA or contrast-enhanced MR angiography. Gadolinium-enhanced MR angiography is not sufficiently sensitive for the detection of irregularities due to its lack of spatial resolution. Further studies of contrast-enhanced MR angiography with higher resolution techniques and hardware should improve its accuracy. Our study findings suggest that CT angiography is the best modality for analyzing plaque morphology because it allows visualization of the atheromatous plaque. Nevertheless, its spatial resolution is inferior to DSA, even if spatial resolution may improve in the z axis with the future use of multidetector row CT.
Detection of ulcerated plaques may prove to be important, since it has been suggested (8) that the presence of plaque ulceration is a risk factor for embolism. However, the inability of DSA to depict plaque ulceration is well documented (23,24), partly because of the limited number of views that are typically obtained. In our study, ulcerations were more frequently observed at gadolinium-enhanced MR angiography (12 cases) and CT angiography (11 cases) than at DSA (eight cases). All ulcerations identified at DSA (eight cases) were also observed at CT angiography. We noted three differences between CT angiography and contrast-enhanced MR angiography. In the case in which CT angiography depicted an ulceration that was not depicted at gadolinium-enhanced MR angiography, this could be due to a lack of spatial resolution at gadolinium-enhanced MR angiography. As for the two cases in which contrast-enhanced MR angiography depicted an ulceration not depicted at CT angiography, we can assume that ulceration is not visible at CT angiography because of the calcified plaque (Fig 5). Since there was no histologic comparison in our study with regard to plaque irregularities and ulcerations, we do not think any conclusion can be drawn.
This study has some limitations. Owing to the small number of patients, the statistical power of our work is limited. DSA was considered as the standard, which can engender a standard bias. To confirm the encouraging results of this study, further studies are needed with histologic correlation to evaluate the atheromatous plaque.
In conclusion, CT angiography and gadolinium-enhanced MR angiography are reliable and fast techniques to evaluate the degree of ICA stenosis (24). CT angiography has some substantial benefits, including its accuracy and lack of invasiveness, compared with DSA (25). It is also an inexpensive and easily accessible technique. Limiting factors are a limited volume of exploration and use of an ionizing technique. Three-dimensional gadolinium-enhanced MR angiography was useful in showing the carotid artery in the arterial phase. The main limiting factor is the low spatial resolution, but by using contrast-enhanced MR angiography, the carotid arteries can be rapidly imaged from the aortic arch to the skull base, and some flow artifacts can be eliminated.
Since we found a close correlation between gadolinium-enhanced MR angiography, CT angiography, and DSA in the evaluation of the degree of carotid stenosis, we conclude that the first two techniques can be used to adequately evaluate carotid stenosis (26).
| FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, B.R., C.M.; study concepts, C.M., A.Z.; study design, B.M., A.Z.; literature research, B.R., B.M.; clinical studies, B.R., F.K.; data acquisition, B.M., M.S.; data analysis/interpretation, B.M., B.R.; statistical analysis, M.D.; manuscript preparation, B.R.; manuscript definition of intellectual content, B.R., B.M.; manuscript editing, B.R.; manuscript revision/review, B.R., C.M.; manuscript final version approval, B.M., C.M.
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J. H. Lee, C. G. Choi, D. K. Kim, G. E. Kim, H. K. Lee, and D. C. Suh Relationship Between Circle of Willis Morphology on 3D Time-of-Flight MR Angiograms and Transient Ischemia During Vascular Clamping of the Internal Carotid Artery During Carotid Endarterectomy AJNR Am. J. Neuroradiol., April 1, 2004; 25(4): 558 - 564. [Abstract] [Full Text] [PDF] |
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B. Randoux, B. Marro, C. Marsault, J. Alvarez-Linera, J. Escribano, J. Campollo, R. Gesto, and J. Benito-Leon Carotid Artery Stenosis: Competition between CT Angiography and MR Angiography AJNR Am. J. Neuroradiol., April 1, 2004; 25(4): 663 - 664. [Full Text] [PDF] |
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B. Randoux, B. Marro, F. Koskas, J. Chiras, D. Dormont, and C. Marsault Proximal Great Vessels of Aortic Arch: Comparison of Three-dimensional Gadolinium-enhanced MR Angiography and Digital Subtraction Angiography Radiology, December 1, 2003; 229(3): 697 - 702. [Abstract] [Full Text] [PDF] |
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N Rilinger, H Seifarth, R Sokiranski, S Kramer, F Liewald, J Goerich, A Tomzcak, and C E E Nierhoff Virtual intra-arterial angioscopy (VIA) of the carotid artery based on helical CT data Br. J. Radiol., November 1, 2003; 76(911): 792 - 797. [Abstract] [Full Text] [PDF] |
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G. M Hathout, M. J. Duh, and S. M. El-Saden Accuracy of Contrast-Enhanced MR Angiography in Predicting Angiographic Stenosis of the Internal Carotid Artery: Linear Regression Analysis AJNR Am. J. Neuroradiol., October 1, 2003; 24(9): 1747 - 1756. [Abstract] [Full Text] [PDF] |
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P. J. Nederkoorn, O. E. H. Elgersma, Y. van der Graaf, B. C. Eikelboom, L. J. Kappelle, and W. P. T. M. Mali Carotid Artery Stenosis: Accuracy of Contrast-enhanced MR Angiography for Diagnosis Radiology, September 1, 2003; 228(3): 677 - 682. [Abstract] [Full Text] [PDF] |
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F. A. Fellner, M. Requardt, W. Lang, C. Fellner, W. Bautz, and A. Cavallaro Peripheral Vessels: MR Angiography with Dedicated Phased-Array Coil with Large-Field-of-View Adapter—Feasibility Study Radiology, July 1, 2003; 228(1): 284 - 289. [Abstract] [Full Text] [PDF] |
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M. H. Lev, J. M. Romero, D. N.F. Goodman, R. Bagga, H. Y. K. Kim, N. A. Clerk, R. H. Ackerman, and R. G. Gonzalez Total Occlusion versus Hairline Residual Lumen of the Internal Carotid Arteries: Accuracy of Single Section Helical CT Angiography AJNR Am. J. Neuroradiol., June 1, 2003; 24(6): 1123 - 1129. [Abstract] [Full Text] [PDF] |
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J. Alvarez-Linera, J. Benito-Leon, J. Escribano, J. Campollo, and R. Gesto Prospective Evaluation of Carotid Artery Stenosis: Elliptic Centric Contrast-Enhanced MR Angiography and Spiral CT Angiography Compared with Digital Subtraction Angiography AJNR Am. J. Neuroradiol., May 1, 2003; 24(5): 1012 - 1019. [Abstract] [Full Text] [PDF] |
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P. J. Nederkoorn, Y. van der Graaf, and M.G. M. Hunink Duplex Ultrasound and Magnetic Resonance Angiography Compared With Digital Subtraction Angiography in Carotid Artery Stenosis: A Systematic Review Stroke, May 1, 2003; 34(5): 1324 - 1331. [Abstract] [Full Text] [PDF] |
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R. A. Willinsky, S. M. Taylor, K. terBrugge, R. I. Farb, G. Tomlinson, and W. Montanera Neurologic Complications of Cerebral Angiography: Prospective Analysis of 2,899 Procedures and Review of the Literature Radiology, May 1, 2003; 227(2): 522 - 528. [Abstract] [Full Text] [PDF] |
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D. C.C. Johnston, J. D. Eastwood, T. Nguyen, and L. B. Goldstein Contrast-Enhanced Magnetic Resonance Angiography of Carotid Arteries: Utility in Routine Clinical Practice Stroke, December 1, 2002; 33(12): 2834 - 2838. [Abstract] [Full Text] [PDF] |
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P. J. Nederkoorn, Y. van der Graaf, B. C. Eikelboom, A. van der Lugt, L. W. Bartels, and W. P.T.M. Mali Time-of-Flight MR Angiography of Carotid Artery Stenosis: Does a Flow Void Represent Severe Stenosis? AJNR Am. J. Neuroradiol., November 1, 2002; 23(10): 1779 - 1784. [Abstract] [Full Text] [PDF] |
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F. A. Fellner, W. Lang, A. I. Qureshi, S. H. Kim, M. F. K. Suri, and L. N. Hopkins The Way Out * Response Stroke, August 1, 2002; 33(8): 1948 - 1949. [Full Text] [PDF] |
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R. Wutke, W. Lang, C. Fellner, R. Janka, C. Denzel, M. Lell, W. Bautz, and F. A. Fellner High-Resolution, Contrast-Enhanced Magnetic Resonance Angiography With Elliptical Centric k-Space Ordering of Supra-aortic Arteries Compared With Selective X-Ray Angiography Stroke, June 1, 2002; 33(6): 1522 - 1529. [Abstract] [Full Text] [PDF] |
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J. H. Gillard, B. D. M. Tom, W. Hollingworth, B. Randoux, B. Marro, F. Koskas, M. Duyme, M. Sahel, A. Zouaoui, and C. Marsault Validation of the Effectiveness and Efficiency of Newer Techniques * Dr Randoux and colleagues respond: Radiology, May 1, 2002; 223(2): 586 - 587. [Full Text] |
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