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1
Department of Radiology, Northwestern University Medical School, 676 St. Clair
St., 8th Floor, Chicago, IL 60611.
2
Department of Biomedical Engineering, Northwestern University Medical School,
Chicago, IL 60611.
3
Siemens Research and Development, 448 E. Ontario St., Chicago, IL 60611.
Received July 19, 2001;
accepted after revision September 17, 2001.
Address correspondence to J. C. Carr.
Abstract
 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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MATERIALS AND METHODS. Forty patients underwent high-resolution contrast-enhanced MR angiography on a 1.5-T Magnetom Symphony. A coronal three-dimensional (3D) gradient-echo sequence (TR/TE, 4.36/1.64; flip angle, 25°) with asymmetric k-space acquisition was used. The 136 x 512 matrix yielded voxel sizes of 1.33 x 0.64 x 1.0 mm. A timing-bolus acquisition, orientated in the coronal plane to include the aortic arch, was obtained initially during free-breathing. Twenty milliliters of gadopenetate dimeglumine was injected at 2 mL/sec. Unenhanced and enhanced 3D volumes were recorded. A subtracted 3D set was calculated and subjected to a maximum-intensity-projection algorithm. Half of the patients held their breath during angiography and the other half did not. Aortic arch motion was measured on the timing-bolus acquisition as the distance moved by a single pixel in both the x and y directions. Maximum-intensity-projection MR images were assessed independently by two observers, and vessel sharpness was scored on a scale of 1-5. Sharpness was also assessed quantitatively by generating a signal intensity profile across the aortic arch vessel wall and calculating the average of the upslope and downslope at full-width half maximum. Visualization of carotid branch vessels was scored on a scale of 0-5, and venous contamination was scored on a scale of 0-3.
RESULTS. Average in-plane aortic arch movement was 10.3 mm in the x direction and 8.7 mm in the y direction. Quantitative and qualitative sharpness of the aortic arch and great vessel origins was better (p < 0.05) during breath-holding than during non—breath-holding. No difference in the sharpness of the carotid vessels was noted between the two groups. Carotid branch vessels were well visualized from the aortic arch to the intracerebral circulation. The average venous contamination score was 0.56.
CONCLUSION. Breath-holding greatly improves the sharpness of the aortic arch and great vessel origins but has no effect on visualization of the carotid vessels. High-resolution breath-hold contrast-enhanced MR angiography can produce high-quality, artifact-free images of the entire carotid circulation from the aortic arch to the intracerebral circulation.
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MR angiography has emerged as a useful technique for assessing the carotid circulation. It is noninvasive and has the advantage of providing images similar to those obtained with conventional angiography. MR angiography was initially implemented using two-dimensional (2D) and three-dimensional (3D) time-of-flight techniques, and good results for detection of arterial disease were reported [5, 6, 10,11,12,13,14,15]. Time-of-flight imaging involves long acquisition times and can result in overestimation of stenosis [16, 17]. More recently, contrast-enhanced MR angiography has become a useful technique for imaging the vasculature and is readily applied to the carotid circulation. Studies have shown contrast-enhanced MR angiography to have high sensitivities and specificities in revealing carotid artery stenosis [18,19,20,21,22]. Previous techniques have not clearly visualized the entire carotid circulation, including the circle of Willis and aortic branch vessels, on a single study. In addition, breath-holding has been used variably in MR angiography of the carotid arteries and arch vessels, the implication being that these vessels are unaffected by respiratory motion. Early venous enhancement in the carotid circulation can interfere with visualization of the arterial system unless the contrast bolus is accurately timed to the arterial phase.
The purpose of our study was to show that high-resolution breath-hold contrast-enhanced MR angiography combined with a timing-bolus technique can produce high-quality images of the entire carotid circulation and to evaluate the effect of breathing on the image quality of the aortic arch and carotid vessels.
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Imaging Technique
Before positioning the patient, a 20-gauge cannula was inserted into an
antecubital vein and connected via extendable tubing to a power injector
(Medrad, Indianola, PA) containing 20 mL of gadopenetate dimeglumine
(Magnevist; Berlex Laboratories, Montvale, NJ) and 40 mL of normal saline.
Patients were placed in a supine position on the scan table, and a circularly
polarized neck coil was connected. They were then entered head-first into the
magnet bore.
The timing-bolus acquisition was obtained in the coronal plane to include the aortic arch and carotid bifurcations. A 2D turbo fast low-angle shot (FLASH) sequence was used, with scanning parameters of TR/TE, 5.0/ 3.2; inversion time, 22 msec; flip angle, 15°; bandwidth, 355 Hz; matrix, 128 x 256; field of view, 300 x 350 mm; pixel size, 2.73 x 1.37 mm; and slice thickness, 20 mm. Forty measurements were acquired, each lasting 1 sec. Two milliliters of gadopenetate dimeglumine was injected at 2 mL/sec followed by a 20 mL bolus of normal saline. The MR acquisition was started simultaneously with the contrast injection, and patients were instructed to breath freely. The transit time was recorded as the time between the start of the injection and initial enhancement of the carotid bifurcation. Because the measurement was acquired in the coronal plane, the contrast material could always be seen entering the heart even when carotid enhancement was not clearly seen.
A 3D gradient-echo FLASH pulse sequence was used for high-resolution MR angiography. An asymmetric k-space scanning scheme in all three gradient axes was used; the remainder of k-space was filled with zero padding. The FLASH sequence had scanning parameters of TR/TE, 4.36/1.64; flip angle, 25°; bandwidth, 432 Hz; matrix, 136 x 512; field of view, 165 x 330 mm; slab thickness, 70 mm; partitions, 80; and voxel size, 1.21 x 0.64 x 0.88 mm. Acquisition time was approximately 19 sec per 3D slab. The 3D slab was orientated in the coronal plane in such a way that the posterior margin was level with the vertebral body pedicles. Two measurements—one after the contrast injection and one before the contrast injection—were acquired.
Half of the patients were asked to breath-hold in inspiration, and the other half were asked to breathe freely. All the patients in the breath-holding group were given specific instructions about breath-holding and were told to hyperventilate before scanning began. Twenty milliliters of gadopenetate dimeglumine was injected at 2mL/sec. A single subtracted 3D set was calculated by subtracting the unenhanced set from the enhanced one. This set was subjected to maximum-intensity-projection postprocessing. Coronal maximum-intensity-projection MR images rotated through 180° at 10° increments were produced. All postprocessing was carried out by an experienced MR imaging technologist, with a processing time of approximately 10 min per patient.
Quantitative Analysis
Movement of the aortic arch during free breathing was measured from the
timing-bolus acquisition using horizontal and vertical excursions of a single
pixel located at a fixed point on the aortic arch. The average distance moved
in both directions was calculated.
As a quantitative measure of image quality, the sharpness of the aortic arch, proximal innominate artery, proximal left common carotid artery, proximal left subclavian artery, and carotid bifurcations was measured directly from the maximum-intensity-projection MR images. A segment of the artery of interest was magnified three times using bilinear interpolation. A signal intensity profile was obtained along a user-defined line (sampling line width = 3 pixels) perpendicular to the major axis of the vessel. The profile evaluations were performed using Scion Image software (Scion, Frederick, MD). For evaluating the sharpness of a vessel, the maximal and minimal values were first noted for each side of the profile. From these measurements, A (20% maximal intensity) and B (80% maximal intensity) were calculated as A = minimum + (maximum - minimum) x 0.2 and B = minimum + (maximum - minimum) x 0.8.
Then the distances between A and B, d1 and d2, were calculated (in millimeters) for each side of the profile, and the average value, d, was obtained. The reciprocal, 1/d, was used as a measure of the sharpness in the image [23]. The higher the value of 1/d, the greater the sharpness.
Qualitative Analysis
All of the maximum-intensity-projection MR images underwent assessment by
two observers who reached agreement on ratings by consensus. Both observers
were unaware of whether the patients belonged to the breath-hold or
non—breath-hold group.
The observers rated the subjective sharpness of the aortic arch, proximal innominate artery, proximal left common carotid artery, proximal left subclavian artery, and carotid bifurcations on a scale of 1-5 (1 = very poor; 2 = poor; 3 = fair; 4 = good; or 5 = excellent). They rated the degree of visualization of the aortic arch; innominate artery; common carotid arteries; subclavian arteries; internal carotid arteries; external carotid arteries; proximal vertebral arteries; distal vertebral arteries; basilar artery; circle of Willis; and anterior, middle, and posterior cerebral arteries on a scale of 0-5 (0 = not seen; 1 = very poor; 2 = poor; 3 = fair; 4 = good; or 5 = excellent). The degree of jugular and brachiocephalic venous contamination was scored on a scale of 0-3 (0 = none; 1 = < aorta; 2 = same as aorta; or 3 = > aorta).
Statistical Analysis
A two-tailed paired Student's t test was used to compare the
differences between the breath-hold and non—breath-hold groups. A
p value of 0.05 or less was considered to be statistically
significant.
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Quantitative Analysis
The average distance that the aortic arch moved during the timing-bolus
acquisition was 10.3 mm in the horizontal direction (range, 7.7-15.9 mm) and
8.7 mm in the vertical direction (range, 3.9-15.7 mm).
The quantitative sharpness of the aortic arch and great vessel origins was consistently rated higher in the images of the breath-hold group (Figs. 1,2A,2B,3) than in those of the non—breath-hold group (Fig. 4). No significant difference in the quantitative sharpness of the carotid bifurcations between the two groups was found. The quantitative sharpness of the aortic arch was 0.74 in images of the breath-hold group compared with 0.59 in the images of the non—breath-hold group (p < 0.05). The average quantitative sharpness of the great vessel origins was 0.85 in the images of the breath-hold group compared with 0.69 in the non—breath-hold group (p < 0.01). The average quantitative sharpness of the carotid bifurcations was 0.85 in both groups (p > 0.05). The results of the quantitative analysis for vessel sharpness are summarized in Figure 5.
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Qualitative Analysis
The qualitative sharpness of the aortic arch and great vessel origins was
consistently rated higher in the images of the breath-hold group (Figs.
1,2A,2B,3)
than in those of the non—breath-hold group
(Fig. 4). No significant
difference in the qualitative sharpness of the carotid bifurcations between
the two groups was found. The qualitative sharpness of the aortic arch was
4.18 in the images of the breath-hold group compared with 2.47 in the images
of the non—breath-hold group (p < 0.001). The average
quantitative sharpness of the great vessel origins was 4.34 in the images of
the breath-hold group compared with 2.61 in the images of the
non—breath-hold group (p < 0.001). The average quantitative
sharpness of the carotid bifurcations was 4.71 in the breath-hold group's
images compared with 4.41 in the non—breath-hold group's images
(p > 0.05). The results of the qualitative analysis for vessel
sharpness are summarized in Figure
6.
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The entire carotid circulation from the aortic arch to the intracerebral circulation was well visualized on all studies (Figs. 1,2A,2B,3,4). The results of the visualization scores for the branches of the carotid circulation are given in Table 1.
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The aortic arch, innominate arteries, common carotid arteries, subclavian arteries, internal carotid arteries, external carotid arteries, and proximal and distal vertebral arteries were visualized on all studies. The basilar artery was visualized in 38 (95%) of 40 patients, as was the circle of Willis. The petrous portion of the internal carotid artery was visualized in 78 (98%) of 80 images; the anterior cerebral arteries were visualized in 60 (75%) of 80 images. The middle cerebral arteries were visualized in 74 (93%) of 80 images. The posterior cerebral arteries were visualized in 75 (94%) of 80 images.
The average venous contamination score for all patients was 0.56 (range, 0-2 on a 3-point scale). Two patients had grade 2 venous contamination. No patient had grade 3 venous contamination.
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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MR angiography has evolved as a useful noninvasive technique for evaluating the vasculature. The carotid circulation is well suited to MR imaging because of its superficial location. Until recently, time-of-flight methods were used to assess the carotid vessels [5, 6, 10,11,12,13,14,15]. Time-of-flight techniques produce excellent images of the carotid bifurcations, but the long imaging times required result in motion artifacts. The anatomic coverage is limited such that the aortic arch and circle of Willis are typically not included in the same acquisition. In addition, artifactual loss of signal intensity can occur in the region of the carotid bifurcation, an occurrence thought to be related to flow incoherence and intravoxel dephasing [13]. Another limitation is the loss of signal from tortuous vessels running parallel to the scan orientation because of the complete saturation of the blood flowing in the imaging plane [14].
Contrast-enhanced MR angiography has emerged as a new technique for imaging blood vessels and has been implemented successfully in different vascular territories [24,25,26]. It relies on an IV injection of the T1-shortening contrast agent gadolinium and rapid imaging with a 3D gradient-echo pulse sequence. Typically, unenhanced and enhanced 3D sets are acquired, and a subtraction technique is used to further enhance the resulting images.
Rapid arteriovenous transit poses a particular challenge in imaging the carotid circulation. As a result, considerable venous contamination can occur, potentially obscuring the diagnostic information in the study. With recent advances in gradient technology, shorter repetition times are now available and may be used either to shorten the acquisition time (resulting in increased temporal resolution) or to acquire more phase-encoding lines (increasing the spatial resolution). In addition, different strategies, such as fluoroscopic triggering [27,28,29,30] or the timing-bolus technique [19, 31] have been used to directly time the arrival of the contrast bolus at the carotid arteries so that the arterial phase can be selectively imaged and the amount of venous contamination can be reduced.
Recent studies have used pulse sequences with a 128 x 256 matrix and acquisition times ranging from 9 to 32 sec [18,19,20,21,22]. In our study, a 3D gradient-echo pulse sequence with a short TR was used. An asymmetric k-space sampling scheme was applied in both in-plane and through-plane phase encoding directions to further reduce the acquisition time required for each 3D data set. A submatrix of k-space points was explicitly measured using a linear trajectory, and the remainder of k-space was filled using zero padding. A 136 x 512 matrix optimized spatial resolution. Using these techniques, high-resolution 3D MR angiography was successfully implemented in relatively short acquisition times of 18-19 sec, allowing imaging to be performed during the arterial phase of contrast enhancement.
To further minimize venous enhancement, we used a timing-bolus technique to directly measure the transit time to the carotid arteries. In our study, the average score for venous contamination was 0.56 on a 3-point scale. Only two patients had grade 2 venous contamination. In no case did venous overlap interfere with the diagnostic quality of the images.
Using a rapid MR imaging scheme together with a timing-bolus technique produced high-resolution images of the carotid circulation with minimal venous overlap. All pulse sequences and system hardware used in this study are now commercially available.
Contrast-enhanced MR angiography during suspended respiration has been shown to reduce the effects of physiologic motion that breathing causes in other parts of the body [25, 26]. Breath-holding is used variably in MR angiography of the carotid arteries and arch vessels, the implication being that these vessels are relatively unaffected by respiratory motion [18,19,20,21,22, 32]. However, results of imaging the origins of the great vessels using standard neck acquisition protocols have been highly variable. Some studies have shown improved visualization of the arch vessels with breath-holding during MR angiography of the thoracic aorta [33, 34]. We have observed that substantial blurring of the aortic arch and its branches is common in non-breath-hold MR angiography of the carotid arteries, and we hypothesize that this blurring is attributable to respiratory motion rather than to vascular pulsatility.
We observed considerable movement of the aortic arch during free breathing. The arch moved by as much as 16 mm in both the horizontal and vertical directions. To see if breath-holding improved image quality, we compared images of patients who held their breath during high-resolution MR angiography with images of those who did not. Studies were assessed both qualitatively and quantitatively for vessel sharpness. Quantitative and qualitative sharpness of the aortic arch and great vessel origins was rated significantly higher in the images of the breath-hold group than in those of the non—breath-hold group. No difference in sharpness of the carotid bifurcations between the two groups was evidenced. These results suggest that, although the carotid bifurcations are unaffected by respiratory motion, breath-holding is necessary to adequately visualize the aortic arch and proximal vessels during carotid MR angiography. This finding is important because treatable proximal vessel disease can commonly exist with or without carotid artery disease, necessitating clear depiction of the carotid circulation and arch vessels on a single study. To our knowledge, quantitative measurements of aortic arch movement and vessel sharpness have not previously been reported.
Evaluation of the entire carotid circulation is essential to exclude the possibility of tandem lesions before surgery. Previous studies have not captured the entire carotid circulation—from the aortic arch to the intracerebral vessels—on a single study. In our study, high-resolution carotid MR angiography consistently allowed visualization of the carotid circulation from the aortic arch to the circle of Willis. The visualization scores for the aortic arch and great vessels were lower for the images of the non—breath-hold group, reflecting the deleterious effect of breathing on image quality. The external carotid, internal carotid, and vertebral arteries were well depicted on all studies. In addition, the basilar artery, circle of Willis, and proximal intracerebral vessels were well visualized in most cases. Potentially, this finding may allow identification of intracranial circulation disease, providing an alternative explanation for symptoms in patients with a normal-appearing carotid bifurcation. In the studies of some patients, the anterior and posterior cerebral arteries were not visualized at all because the 3D slab had inadvertently been positioned too far anteriorly or too far posteriorly. The petrous portion of the internal carotid artery was well depicted on most of the patients' studies, which confirms the advantages of contrast-enhanced MR angiography over time-of-flight imaging: the tortuosity of the internal carotid artery in this area can cause variations in blood signal intensity on time-of-flight images.
Our study has limitations. No angiographic correlation was performed in any of the patients. In our institution, carotid MR angiography is used as a first-line investigation so that most patients do not undergo conventional angiography. As a result, we have not been able to address the accuracy of the technique for the common indication of carotid artery disease. However, our aim was not to assess the clinical accuracy of the technique. Further clinical studies will be required to assess this aspect.
In conclusion, high-resolution carotid MR angiography can produce high-quality images of the entire carotid circulation from the aortic arch to the circle of Willis. When used in conjunction with a timing-bolus technique, the transit time can be calculated, resulting in minimal venous contamination. Because there is significant movement of the aortic arch during free breathing, breath-holding results in greatly improved image quality, particularly of the aortic arch and great vessels. The large anatomic coverage possible with this technique has the potential to show concomitant disease of the aortic arch and great vessels as well as of the intracerebral circulation, which may have implications for treatment. Further studies are needed to assess the accuracy of this technique in detecting carotid artery disease.
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= breath-hold.