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(Radiology. 2000;216:511-516.)
© RSNA, 2000


Vascular and Interventional Radiology

Multidirectional Depiction of Internal Carotid Arterial Stenosis: Three-dimensional Time-of-Flight MR Angiography versus Rotational and Conventional Digital Subtraction Angiography1

Otto E. H. Elgersma, MD, Aloys F. J. Wüst, MD, Pieter C. Buijs, MD, Yolanda van der Graaf, MD, PhD, Bert C. Eikelboom, MD, PhD and Willem P. T. M. Mali, MD, PhD

1 From the Departments of Radiology (O.E.H.E., A.F.J.W., P.C.B., W.P.T.M.M.) and Vascular Surgery (B.C.E.) and the Julius Center for Patient Oriented Research (O.E.H.E., Y.v.d.G.), University Hospital Utrecht, Heidelberglaan 100, 3584 CX Utrecht, the Netherlands. Received March 1, 1999; revision requested April 26; final revision received October 5; accepted November 10. Address correspondence to O.E.H.E. (e-mail: o.e.h.elgersma@azu.nl).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate whether and to what extent greater number of projection images obtained at three-dimensional (3D) time-of-flight (TOF) magnetic resonance (MR) angiography versus conventional digital subtraction angiography (DSA) causes overestimation of internal carotid arterial (ICA) stenosis.

MATERIALS AND METHODS: DSA (two or three projections), rotational angiography (16 or 32 projections), and 3D TOF MR angiography (12 projections) were performed in 47 stenotic ICAs of 38 symptomatic patients. Two observers independently measured maximum stenosis, and the mean differences among MR angiography, DSA, and rotational angiography were compared.

RESULTS: Three rotational and five MR angiograms were nondiagnostic. Seven MR angiograms of ICA stenoses showed a signal void and were excluded from analysis. On the remaining 32 angiograms, mean differences in maximum stenosis for observers 1 and 2, respectively, were 7% (95% CI: 3%, 12%) and 8% (95% CI: 3%, 13%) at MR angiography versus DSA and 2% (95% CI: -2%, 7%) and -1% (95% CI: -5%, 3%) at MR angiography versus rotational angiography. ICA stenosis was graded significantly higher at MR angiography versus DSA, whereas, it was not overestimated at MR angiography versus rotational angiography. The difference in maximum stenosis at MR angiography versus DSA was significantly different from that of MR angiography versus rotational angiography.

CONCLUSION: Apparent overestimation of ICA stenosis at 3D TOF MR angiography versus conventional DSA may be partly explained by the greater number of projection images available at 3D TOF MR angiography.

Index terms: Angiography, comparative studies, 172.12142, 172.12143, 172.12473 • Carotid arteries, stenosis or obstruction, 172.721, 172.781 • Digital subtraction angiography, 172.12473 • 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


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Findings from the North American Symptomatic Carotid Endarterectomy Trial (NASCET) and the European Carotid Surgery Trial (13) established that carotid endarterectomy is beneficial to patients with symptoms of cerebral ischemia and with severe internal carotid arterial (ICA) stenosis, as depicted on angiograms. In both trials, ICA stenosis was visualized in two or three directions at angiography; the projection that showed maximum stenosis was used for an assessment of the percentage of ICA stenosis. The residual stenotic lumen, however, may not have been circular (48). In a previous study (9), we demonstrated that if only two or three projections are obtained at intraarterial digital subtraction angiography (DSA), the narrowest residual lumen is not always revealed. Hence, the maximum degree of ICA stenosis is not always assessed.

Three-dimensional (3D) time-of-flight (TOF) magnetic resonance (MR) angiography, which allows multidirectional visualization of the ICA, is a widely studied technique that could replace the potentially harmful angiographic technique used in the examination and selection of patients for carotid endarterectomy (1014). Studies in which the depiction of maximum ICA stenosis at 3D TOF MR angiography and conventional angiography is compared often reveal that 3D TOF MR angiography tends to cause overestimation of the degree of stenosis (12,15,16).

Several factors have been suggested to explain this undesirable aspect. Large velocity gradients, acceleration, and complex flow patterns in the stenotic and poststenotic ICA cause intravoxel dephasing, which leads to local loss of signal intensity (17). Furthermore, the maximum intensity projection (MIP) algorithm used to reconstruct 3D angiographic images may cause the loss of faint signal intensity on images of stenotic areas, leading to artifactual narrowing of the apparent lumen of the ICA (15,18,19). However, since ICA stenosis is often noncircular, the greater number of projection images obtained at MR angiography could contribute to the overestimation of stenosis at MR angiography compared with DSA performed in two or three directions.

We recently reported on rotational angiography as a DSA technique that allows reliable visualization of the ICAs in many directions during one injection of contrast material (9). This technique may allow better comparison of the maximum percentage of ICA stenosis at angiography versus MR angiography.

The objective of this study was to evaluate whether possible overestimation of ICA stenosis at 3D TOF MR angiography can be attributed to its multidirectional depiction of the carotid bifurcation, as compared with DSA performed in two or three directions. Therefore, the results of MR angiography and conventional two- or three-directional angiography and the results of MR angiography and rotational angiography were compared by calculating the mean difference in measured percentages of maximum ICA stenosis.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
From March 1997 to February 1998, we included 38 patients with symptoms of carotid disease (transient ischemic attack, stroke, or amaurosis fugax) in the preceding 6 months. Thirty-three patients were men, and five were women (mean age, 65 years; age range, 45–82 years).

In our hospital, all symptomatic patients are first screened with carotid duplex ultrasonography. If peak systolic velocity values in the ICA are 150 cm/sec or higher, patients are suspected of having carotid disease (20). Patients with this finding were subsequently referred for DSA and additional MR angiographic examinations, which were performed after we obtained written informed consent. MR angiography was always performed within 2 days of DSA. The study was approved by the hospital ethics committee. All patients also participated in a previous study (9) in which rotational angiography was validated (with conventional DSA as the standard), in which ICA stenosis was compared with rotational angiography and DSA, and in which the consequences of treatment were discussed.

DSA was performed by using an Integris V3000 angiographic unit (Philips Medical Systems, Best, the Netherlands) with an image intensifier matrix of 1,024 x 1,024. By using the Seldinger technique, the tip of a 5-F catheter was guided from the common femoral artery to the ascending aorta and was positioned in the right and, subsequently, left common carotid arteries. Two or three projections (lateral, posteroanterior, and/or ipsilateral oblique) were acquired in each carotid bifurcation. For each projection, 6 mL of contrast agent (Ultravist [300 mg of iodine per milliliter]; Schering, Berlin, Germany) was intraarterially injected with a flow rate of 3 mL/sec. An additional rotational angiographic examination was performed if ICA stenosis was visible, according to NASCET criteria, on one of the conventional DSA projections and if the radiologist anticipated that the patient could remain motionless for at least 24 seconds (the time required to perform the rotational angiography—8 seconds to obtain the rotational mask series of images, 8 seconds to reverse the x-ray unit back into its starting position, and 8 seconds to obtain the rotational contrast material–enhanced series of images). In the first 20 patients, rotational angiography was performed in each symptomatic or asymptomatic ICA; whereas, in the last 18 patients, only the symptomatic ICA was selected for additional rotational angiographic examination.

The rotational angiographic technique has been described before (9). The x-ray unit started in a lateral position and rotated 180° in 8 seconds around the carotid bifurcation to acquire 32 projections in all but four patients in whom 16 projections were obtained in six carotid arteries. A 512 x 512 image intensifier matrix was used. In most patients, a delay of 2 seconds and a flow rate of 3 mL/sec were used, with a total of 27 mL of contrast material in each injection. A rotational angiogram was considered to be of diagnostic quality when contrast material filled the ICA with sufficient density to allow reliable measurements of the distal ICA diameter and minimal residual lumen to be made.

MR angiography was performed with a 1.5-T MR imaging system (Gyroscan ACSNT; Philips Medical Systems) equipped with a gradient system, a maximum gradient strength of 10 mT · m-1, and a slew rate of 17 mT · m-1 · msec-1. After the head of the patient was secured in an open quadrature neck coil with soft pads, a sagittal scout two-dimensional phase-contrast image with 30 cm · sec-1 velocity encoding and two-dimensional TOF images (30 consecutive 4-mm-thick transverse sections) were acquired to localize the carotid arterial bifurcation and to plan the 3D TOF acquisition. Carefully planned 3D TOF MR angiograms were acquired by using a radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections (interpolated to 100 sections), a superior saturation band, 37/6.9 (repetition time msec/echo time msec), a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired. Imaging time was approximately 9 minutes. Postprocessing subvolumes were generated to isolate each carotid artery and to create 12 MIP images that were radially projected at 15° increments (rotation about the long axis of the body).

Images obtained at conventional DSA, rotational angiography, and MR angiography were evaluated by two independent observers (P.C.B. and A.F.J.W.) on different occasions, with at least a 1-week interval between each occasion. Observers were blinded to patient data and each other’s findings. ICA stenosis was measured on printed hard-copy images according to the following NASCET method by using a mechanical caliper with a digital display (Prezition Apparatenbau, Vaduz, Liechtenstein; resolution, 0.01 mm): stenosis = [1 - (minimal residual lumen/distal ICA lumen diameter)] x 100%.

One observer (P.C.B.) selected the rotational angiograms that were considered to be of diagnostic quality. Subsequently, both observers individually evaluated these angiograms by selecting two images (from among those with adequate contrast material filling and without overlapping vessels) on which maximum ICA stenosis was depicted; they measured the percentage ICA stenosis on these two images. One observer (P.C.B.) counted the number of images with adequate contrast material filling that did not depict overlapping vessels to assess the mean number of images that could be used to evaluate of the ICA. Furthermore, on conventional DSA images, the percentage of ICA stenosis was measured on all available projections that showed the ICA without overlapping vessels.

From the 12 projections acquired with MR angiographic MIP reconstruction, the percentage of ICA stenosis was assessed on the two images that showed the most severe ICA stenosis. Stenosis was measured by using the NASCET method. The measured degree of stenosis could vary from 0% to 99%. At MR angiography, images of some stenoses will show a signal void with distal reconstitution of the signal. These ICA images were excluded from analysis because the exact percentage of ICA stenosis could not be assessed.

By using measurements obtained on conventional DSA images, rotational angiograms, and MR angiograms, the images with the highest degree of ICA stenosis were selected for each modality. MR angiography was compared with conventional DSA and with rotational angiography for separate measurements of the two observers. The mean differences in maximum ICA stenosis with 95% CIs were calculated for MR angiography versus conventional DSA and for MR angiography versus rotational angiography. Subsequently, the mean difference between MR angiography and conventional DSA and between MR angiography and rotational angiography were calculated with 95% CIs for measurements of both observers. Values were significantly different if the 95% CI did not include zero (21).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Forty-seven carotid arteries were depicted with conventional DSA, rotational angiography, and MR angiography. The quality of three rotational and five MR angiograms was considered to be inadequate for an estimation of the degree of stenosis because of patient movement. Seven MR angiograms of ICA stenoses showed a signal void and were excluded from analysis. Therefore, 32 carotid arteries (27 symptomatic and five asymptomatic) remained for comparison. Of the 44 rotational angiograms that were considered to be of diagnostic quality, the mean number of images on which measurements of ICA stenosis could be performed (ie, images that showed sufficient contrast material filling of the ICA and that fully revealed the stenosis without an overlapping external carotid artery) was 13 (median, 12; range, four to 25).

Figure 1 shows the scatter plots of the maximum percentage of ICA stenosis at MR angiography versus conventional DSA for both observers. Figure 2 shows scatter plots of the maximum percentage ICA stenosis at MR angiography versus rotational angiography. Comparison of Figures 1a and 2a and of Figures 1b and 2b demonstrates that the agreement between MR angiography and rotational angiography is better than that between MR angiography and conventional DSA. Table 1 shows the mean differences in maximum ICA stenosis (with 95% CIs) between MR angiography and conventional DSA and between MR angiography and rotational angiography for measurements obtained by both observers.



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Figure 1a. Scatterplots show measurements of maximum ICA stenosis obtained at MR angiography versus those obtained at conventional DSA by observers (a) 1 and (b) 2. For both observers, a substantial number of measurements are above the line of equality, indicating that MR angiography results in more severe estimates of ICA stenoses than conventional DSA.

 


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Figure 1b. Scatterplots show measurements of maximum ICA stenosis obtained at MR angiography versus those obtained at conventional DSA by observers (a) 1 and (b) 2. For both observers, a substantial number of measurements are above the line of equality, indicating that MR angiography results in more severe estimates of ICA stenoses than conventional DSA.

 


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Figure 2a. Scatterplots show measurements of maximum ICA stenosis obtained at MR angiography versus those obtained at rotational angiography by observers (a) 1 and (b) 2. For both observers, most measurements are at or around the line of equality, indicating that MR angiography and rotational angiography result in similar estimates of ICA stenosis.

 


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Figure 2b. Scatterplots show measurements of maximum ICA stenosis obtained at MR angiography versus those obtained at rotational angiography by observers (a) 1 and (b) 2. For both observers, most measurements are at or around the line of equality, indicating that MR angiography and rotational angiography result in similar estimates of ICA stenosis.

 

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TABLE 1. Mean Differences in Maximum ICA Stenosis
 
Compared with DSA, MR angiography caused ICA stenoses to be graded significantly higher, since the 95% CI did not include zero (Fig 3). Compared with rotational angiography, MR angiography did not cause overestimation of ICA stenoses (95% CI included zero) (Fig 4). In addition, the mean difference between MR angiography and conventional DSA and between MR angiography and rotational angiography were 5% (95% CI: 2%, 8%) for measurements of observer 1 (7% minus 2%) and 9% (95% CI: 6%, 12%) for measurements of observer 2 (8% minus -1%). Since the 95% CIs did not include zero, the difference in maximum stenosis between MR angiography and conventional DSA was significantly different from the difference in maximum stenosis between MR angiography and rotational angiography for measurements of both observers.



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Figure 3a. Conventional digital subtraction angiograms with ipsilateral (a) oblique and (b) posteroanterior projections of the carotid bifurcation do not clearly reveal the minimal residual ICA lumen. (c, d) Projections obtained at rotational angiography between the ipsilateral oblique and lateral planes clearly show a severe stenosis (arrow in d) that is not depicted in a or b because of an overlapping ulcer (arrowhead in d). (e) Ipsilateral oblique projection of the 3D TOF MR angiographic MIP reconstruction does not show the severe stenosis, since this projection is nearly identical to that in a. (f) However, a more lateral projection, similar to the image in d, shows the severe ICA stenosis (arrow) and ulcer (arrowhead). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, 37/6.9, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 3b. Conventional digital subtraction angiograms with ipsilateral (a) oblique and (b) posteroanterior projections of the carotid bifurcation do not clearly reveal the minimal residual ICA lumen. (c, d) Projections obtained at rotational angiography between the ipsilateral oblique and lateral planes clearly show a severe stenosis (arrow in d) that is not depicted in a or b because of an overlapping ulcer (arrowhead in d). (e) Ipsilateral oblique projection of the 3D TOF MR angiographic MIP reconstruction does not show the severe stenosis, since this projection is nearly identical to that in a. (f) However, a more lateral projection, similar to the image in d, shows the severe ICA stenosis (arrow) and ulcer (arrowhead). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, 37/6.9, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 3c. Conventional digital subtraction angiograms with ipsilateral (a) oblique and (b) posteroanterior projections of the carotid bifurcation do not clearly reveal the minimal residual ICA lumen. (c, d) Projections obtained at rotational angiography between the ipsilateral oblique and lateral planes clearly show a severe stenosis (arrow in d) that is not depicted in a or b because of an overlapping ulcer (arrowhead in d). (e) Ipsilateral oblique projection of the 3D TOF MR angiographic MIP reconstruction does not show the severe stenosis, since this projection is nearly identical to that in a. (f) However, a more lateral projection, similar to the image in d, shows the severe ICA stenosis (arrow) and ulcer (arrowhead). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, 37/6.9, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 3d. Conventional digital subtraction angiograms with ipsilateral (a) oblique and (b) posteroanterior projections of the carotid bifurcation do not clearly reveal the minimal residual ICA lumen. (c, d) Projections obtained at rotational angiography between the ipsilateral oblique and lateral planes clearly show a severe stenosis (arrow in d) that is not depicted in a or b because of an overlapping ulcer (arrowhead in d). (e) Ipsilateral oblique projection of the 3D TOF MR angiographic MIP reconstruction does not show the severe stenosis, since this projection is nearly identical to that in a. (f) However, a more lateral projection, similar to the image in d, shows the severe ICA stenosis (arrow) and ulcer (arrowhead). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, 37/6.9, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 3e. Conventional digital subtraction angiograms with ipsilateral (a) oblique and (b) posteroanterior projections of the carotid bifurcation do not clearly reveal the minimal residual ICA lumen. (c, d) Projections obtained at rotational angiography between the ipsilateral oblique and lateral planes clearly show a severe stenosis (arrow in d) that is not depicted in a or b because of an overlapping ulcer (arrowhead in d). (e) Ipsilateral oblique projection of the 3D TOF MR angiographic MIP reconstruction does not show the severe stenosis, since this projection is nearly identical to that in a. (f) However, a more lateral projection, similar to the image in d, shows the severe ICA stenosis (arrow) and ulcer (arrowhead). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, 37/6.9, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 3f. Conventional digital subtraction angiograms with ipsilateral (a) oblique and (b) posteroanterior projections of the carotid bifurcation do not clearly reveal the minimal residual ICA lumen. (c, d) Projections obtained at rotational angiography between the ipsilateral oblique and lateral planes clearly show a severe stenosis (arrow in d) that is not depicted in a or b because of an overlapping ulcer (arrowhead in d). (e) Ipsilateral oblique projection of the 3D TOF MR angiographic MIP reconstruction does not show the severe stenosis, since this projection is nearly identical to that in a. (f) However, a more lateral projection, similar to the image in d, shows the severe ICA stenosis (arrow) and ulcer (arrowhead). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, 37/6.9, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 4a. Rotational angiograms obtained (a, b) between the posteroanterior and ipsilateral oblique planes show only a moderate ICA stenosis (arrow in a), whereas (c, d) the projections obtained between the ipsilateral oblique and lateral planes reveal a severe stenosis (arrow in d). (e, f) Projections of the 3D TOF MR angiographic MIP reconstruction do not reveal the severe stenosis in e, whereas the projection in f, similar to the image in d, shows the stenosis (arrow). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 4b. Rotational angiograms obtained (a, b) between the posteroanterior and ipsilateral oblique planes show only a moderate ICA stenosis (arrow in a), whereas (c, d) the projections obtained between the ipsilateral oblique and lateral planes reveal a severe stenosis (arrow in d). (e, f) Projections of the 3D TOF MR angiographic MIP reconstruction do not reveal the severe stenosis in e, whereas the projection in f, similar to the image in d, shows the stenosis (arrow). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 4c. Rotational angiograms obtained (a, b) between the posteroanterior and ipsilateral oblique planes show only a moderate ICA stenosis (arrow in a), whereas (c, d) the projections obtained between the ipsilateral oblique and lateral planes reveal a severe stenosis (arrow in d). (e, f) Projections of the 3D TOF MR angiographic MIP reconstruction do not reveal the severe stenosis in e, whereas the projection in f, similar to the image in d, shows the stenosis (arrow). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 4d. Rotational angiograms obtained (a, b) between the posteroanterior and ipsilateral oblique planes show only a moderate ICA stenosis (arrow in a), whereas (c, d) the projections obtained between the ipsilateral oblique and lateral planes reveal a severe stenosis (arrow in d). (e, f) Projections of the 3D TOF MR angiographic MIP reconstruction do not reveal the severe stenosis in e, whereas the projection in f, similar to the image in d, shows the stenosis (arrow). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 4e. Rotational angiograms obtained (a, b) between the posteroanterior and ipsilateral oblique planes show only a moderate ICA stenosis (arrow in a), whereas (c, d) the projections obtained between the ipsilateral oblique and lateral planes reveal a severe stenosis (arrow in d). (e, f) Projections of the 3D TOF MR angiographic MIP reconstruction do not reveal the severe stenosis in e, whereas the projection in f, similar to the image in d, shows the stenosis (arrow). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 


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Figure 4f. Rotational angiograms obtained (a, b) between the posteroanterior and ipsilateral oblique planes show only a moderate ICA stenosis (arrow in a), whereas (c, d) the projections obtained between the ipsilateral oblique and lateral planes reveal a severe stenosis (arrow in d). (e, f) Projections of the 3D TOF MR angiographic MIP reconstruction do not reveal the severe stenosis in e, whereas the projection in f, similar to the image in d, shows the stenosis (arrow). (Three-dimensional TOF MR angiography was performed by using an radio-frequency spoiled gradient-echo sequence with 50 1-mm-thick transverse sections [interpolated to 100 sections], a superior saturation band, a flip angle of 15°, flow compensation, a field of view of 120 x 120 mm, an imaging matrix of 256 x 115, and three signals acquired.)

 
Categorized lumen reduction measurements of maximum ICA stenosis obtained by both observers at MR angiography versus those obtained at conventional DSA and rotational angiography are shown in Tables 2 and 3, respectively. Images of carotid arteries that showed a signal void at MR angiography were included separately. A notable finding was that three of seven carotid arteries with MR angiograms that showed a signal void (often regarded as a high-grade stenosis) were graded as being only moderately stenotic (30%–69%) at conventional DSA, while at rotational angiography, only one was graded as being moderately stenotic, and six were graded as being severely stenotic (70%–99%).


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TABLE 2. Categorized Lumen Reduction Measurements of Maximum ICA Stenosis at MR Angiography vs Conventional DSA
 

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TABLE 3. Categorized Lumen Reduction Measurements of Maximum ICA Stenosis at MR Angiography vs Rotational Angiography
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
An often reported and important limitation of 3D TOF MR angiography as a reliable and safe alternative for DSA (which is potentially harmful) is the overestimation of the degree of ICA stenosis (12,15,16). Our purpose was to assess whether possible overestimation is caused by only MR angiography–specific artifacts of local signal intensity loss in stenotic regions or if it is also substantially related to MR angiographic depiction of the ICA in a greater number of directions, as compared to two- or three-directional conventional DSA. In the case of a noncircular stenosis, conventional DSA may actually cause underestimation of the stenosis, whereas MR angiography may correctly depict the stenosis as being more severe. We have previously shown that rotational angiography, as a reliable angiographic technique for the multidirectional depiction of vessels, generally demonstrates a more severe maximum ICA stenosis than does conventional two- or three-directional DSA (9). Our hypothesis was that, because of the great number of projections, the depiction of maximum stenosis at MR angiography can be more reliably compared with that of rotational angiography than with that of conventional DSA performed in a limited number of projections.

Our study findings demonstrated that 12-directional 3D TOF MR angiography caused statistically significant overestimation of the degree of maximum ICA stenosis of approximately 8% compared with two- or three-directional conventional DSA, whereas this difference was reduced to about 1% (not significantly different from zero) when MR angiography was compared with rotational angiography. This finding demonstrates that the greater number of ICA projections obtained with MR angiography at least partly accounts for the overestimation of ICA stenosis at MR angiography, if conventional DSA is used as the standard of reference.

A potential limitation of this study is that we did not perform rotational angiography in all consecutive patients. Since rotational angiography can be performed successfully only in patients who are able to remain motionless for at least 24 seconds, the radiographer decided that six (14%) of 44 patients referred for carotid angiography were not eligible for an additional rotational angiographic examination. After this initial selection, rotational angiography still had a failure rate of 6% (three of 47 ICAs) because of patient movement. 3D TOF MR angiography had similar limitations. The scanning time was about 9 minutes during which patients were to remain motionless. Unfortunately, not all patients could comply with this condition. Therefore, the quality of five (11%) of 47 ICA MR angiograms was considered to be too poor for use in the estimation of the degree of stenosis.

Another limitation of rotational angiography was that it did not provide views of the carotid bifurcation from every direction. Inadequate contrast filling in the full 180° rotation in some patients due to time variations between patients in the arrival of contrast material in the ICA and the presence of an overlapping external carotid artery on a considerable number of projections (the patient with 25 images of diagnostic quality had an external carotid arterial occlusion) were responsible for a mean of only 13 of 32 images acquired that were useful for the measurement of ICA stenosis. However, the use 3D TOF MR angiographic MIP reconstructions for the measurement ICA stenosis from any direction was limited, likewise, because the external carotid artery overlapped the ICA stenosis on certain projections. Therefore, the useful projections of the carotid bifurcation obtained at rotational angiography were essentially comparable to those obtained at MR angiography after MIP reconstruction.

The measurement of ICA stenosis on 3D TOF MR angiograms is complicated by signal intensity loss due to intravoxel dephasing and by signal voids (17,22). Gadolinium-enhanced MR angiography of the carotid arteries is a recent development that could potentially minimize signal voids. By shortening the T1 of blood, it allows a larger flip angle to be used, generates a stronger signal with better background suppression, and has less signal saturation. Unfortunately, a limitation of this new technique is that the jugular vein overlaps the carotid bifurcation on almost all projections. This problem can be avoided by imaging the carotid arteries within about 10 seconds after the start of enhancement (before venous return). In this case, however, the poor resolution of 3D methods, even with the use of high-gradient hardware, does not yet allow the accurate measurement of ICA stenosis (23,24).

Pan et al (8) studied ICA specimens removed en bloc during carotid endarterectomy and observed that lumen cross sections in the stenotic area were never circular. They compared measurements of maximum stenosis obtained from ICA specimens with those obtained at two-directional DSA and 3D TOF MR angiography with reconstruction in twelve projections. DSA caused underestimation of ICA stenosis in as many as 37% of the cases and caused overestimation of ICA stenosis in 6% of the cases. Conversely, MR angiography caused underestimation of ICA stenosis in 7% of the cases and caused overestimation of ICA stenosis in only 17% of the cases. Because their study population consisted of only patients who had undergone surgery and because all of the specimens showed severe stenoses, more or less, they could not address the reliability of conventional DSA and MR angiography in the assessment of more moderate degrees of stenosis.

Our study however, also addressed mild and moderate stenoses because we included patients who showed 0%–99% ICA stenosis by NASCET criteria at the initial two- or three-directional conventional DSA examination. Nonetheless, our results were similar to the findings of Pan et al (8). We found that, compared with conventional DSA, MR angiography caused underestimation of ICA stenosis in one to two (3%–6%) of the 32 cases and caused overestimation of ICA stenosis in as many as 10–13 (31%–41%) cases. Conversely, when compared with rotational angiography, MR angiography caused underestimation of ICA stenosis in four to seven (12%–22%) of the 32 cases and caused overestimation of ICA stenosis in only six (19%) cases.

Therefore, we conclude that the overestimation of ICA stenosis at MR angiography compared with conventional DSA cannot be attributed to local signal intensity loss in the ICA or to the use of the MIP algorithm alone, but that it is, to a large extent, caused by the greater number of projections of the ICA obtained at MR angiography. The clinical implication of these findings is that when modalities (other than conventional DSA, which allows visualization in a few directions) that offer multidirectional visualization of the ICA are used to select patients for carotid endarterectomy, inevitably, more patients will undergo surgery.


    FOOTNOTES
 
Abbreviations: DSA = digital subtraction angiography, ICA = internal carotid artery, MIP = maximum intensity projection, NASCET = North American Symptomatic Carotid Endarterectomy Trial, TOF = time of flight, 3D = three-dimensional

Author contributions: Guarantors of integrity of entire study, O.E.H.E., W.P.T.M.M.; study concepts, O.E.H.E., B.C.E., W.P.T.M.M.; study design, O.E.H.E., P.C.B., A.F.J.W.; definition of intellectual content, O.E.H.E., Y.v.d.G., B.C.E.; literature research, O.E.H.E., P.C.B.; clinical studies, O.E.H.E., A.F.J.W., P.C.B.; data acquisition, O.E.H.E., A.F.J.W., P.C.B.; data analysis, O.E.H.E.; statistical analysis, O.E.H.E., Y.v.d.G.; manuscript preparation, O.E.H.E.; manuscript editing, O.E.H.E., A.F.J.W., P.C.B.; manuscript review, Y.v.d.G., B.C.E., W.P.T.M.M.


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 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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