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AJR 2000; 174:371-375
© American Roentgen Ray Society


Software-Triggered Contrast-Enhanced Three-Dimensional MR Angiography of the Intracranial Arteries

Haruo Isoda1, Yasuo Takehara1, Satoshi Isogai1, Hiroyasu Takeda1, Tokutaro Tanaka2, Motoichiro Takahashi1, Atsushi Nozaki3 and Yi Sun4

1 Department of Radiology, Hamamatsu University School of Medicine, 3600 Handa-cho, Hamamatsu 431-3192, Japan.
2 Department of Neurosurgery, Hamamatsu University School of Medicine, Hamamatsu 431-3192, Japan.
3 General Electric Yokogawa Medical Systems, Ltd., 4-7-127 Asahigaoka, Hino Tokyo 191-8503, Japan.
4 General Electric Medical Systems, W-801, 3200 N. Grandview Blvd., Waukesha, WI 53188.

Received January 19, 1999; accepted after revision July 8, 1999.

 
Address correspondence to H. Isoda.


Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. We investigated the effectiveness of software-triggered contrast-enhanced three-dimensional (3D) MR angiography in evaluating intracranial arteries.

SUBJECTS AND METHODS. We studied 38 patients with suspected brain lesions. Imaging was performed using a 1.5-T superconducting MR system with a commercially available head coil. To monitor signal intensity changes we used software to place a tracker volume at the basilar artery or the internal carotid artery. A 20-ml bolus of gadodiamide hydrate was administered through the antecubital vein at a rate of 2-4 ml/sec, followed by a saline flush. Three-dimensional MR angiography using a spoiled gradient-echo sequence with centric K-space ordering was triggered by the arrival of the contrast bolus in the tracker volume. Imaging times ranged from 12 to 20 sec. We used MR images to assess the effectiveness of contrast-enhanced 3D MR angiography in revealing intracranial arteries with minimal venous overlap.

RESULTS. The software triggered imaging on the arrival of the contrast bolus in 81.6% of examinations. In 77.6% of examinations, the resulting MR angiograms revealed intracranial arteries with minimal venous overlap.

CONCLUSION. Software-triggered contrast-enhanced 3D MR angiography with centric K-space ordering is a promising technique for viewing intracranial arteries.


Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Contrast-enhanced three-dimensional (3D) MR angiography enables the acquisition of data sets with a higher signal-to-noise ratio and a shorter acquisition time than those acquired with conventional MR angiography [1, 2, 3]. The T1 shortening effect of contrast media reduces spin saturation even for short TR acquisitions, thus providing images with high signal-to-noise ratios. Recent technical advances further reduce TR and TE times, enabling the acquisition of 3D data sets within 15 sec of imaging time, with minimal phase dispersion. Consequently, 3D data sets with strong signals from the intracranial vasculature can be obtained in less time, making 3D MR angiography an ideal method for visualizing vasculature.

Selective arterial phase MR angiography of the intracranial, carotid, and vertebral arteries has been very difficult [4]. Difficulties are caused by the rapid transit time through the cerebral vasculature. Also, because the blood-brain barrier prevents extraction of contrast material, there is less difference between artery and vein signal intensity compared with that of other tissues; therefore, the imaging time frame is narrow.

The quality of image contrast in a contrast-enhanced MR angiography study depends on the concentration of the contrast material in the blood at the time of acquisition. To acquire a clear arterial phase image it is critical to initiate imaging at the correct time after the injection of the contrast bolus [1, 2, 3, 4, 5]. Also, the center of the K-space should coincide with the period of maximum effect during the first-pass bolus of contrast medium for arteries [6, 7].

Smartprep software (General Electric Medical Systems, Milwaukee, WI) can be used to detect the contrast bolus arrival by monitoring the signal intensity from the tracking volume placed on the vessel of interest; Smartprep automatically initiates acquisition of contrast-enhanced studies [1, 2, 3]. Currently, this technique is applied to the aorta and carotid arteries; there is less application to the intracranial arteries.

In this study, we evaluated contrast-enhanced 3D MR angiography using the Smartprep technique to obtain arterial phase MR angiograms of intracranial arteries.


Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Imaging was performed using a 1.5-T superconducting MR system (Signa Horizon; General Electric Medical Systems) with a commercially available head coil. This study included 38 patients with suspected brain lesions (20 men; 18 women; mean age, 54 years). Before starting the procedure, informed consent was obtained from all patients.

The MR Smartprep triggering technique can be used to optimize the acquisition of arterial phase images on the basis of the arrival of the contrast bolus in the region of interest [1, 2, 3]. The MR Smartprep technique enables users to place a tracker volume to monitor the arrival of the contrast bolus. The tracker volume is independent of the imaging volume.

After obtaining sagittal and axial T1-weighted images, a Smartprep tracker volume ranging in size from 1 x 1 x 2 cm to 4 x 4 x 2 cm was placed either at the basilar artery or at the petrous segment of the internal carotid artery. The tracker was used to continuously monitor the signal intensity within the region of interest. Two thresholds were used to set the triggering of the imaging volume. One threshold was set at 1 or 2 standard deviations from the mean and the other at a 5% or 10% signal intensity increase over the baseline. Once the tracking volume signal surpassed these thresholds, caused by the arrival of the contrast bolus, data acquisition from the imaging volume was automatically triggered and a 3D MR angiogram was obtained. When the trigger failed, the acquisition of the imaging volume was set to start 30 sec after the injection of contrast medium.

In our study, MR angiographic images were obtained using a 3D spoiled gradient-echo sequence (TR range/TE range, 7.2-8.4/1.4-2.5 msec; number of excitations, 0.75-1; flip angle, 30°; number of sections, 16-24; interpolated sections, 32-64; section thickness, 2.0-4.0 mm; spacing between interpolated slices, 0.5-2.0 mm; matrix, 256 x 128; field of view, 19-21 x 9.5-15 cm; rectangular field of view, 0.75-1; bandwidth, 31.3 kHz; zero-filled interpolation processing; K-space ordering, centric; delay time from trigger to acquisition, 1 sec; imaging time, 12-20 sec). Zero-filled interpolation processing was applied in the section direction to double the number of reconstructed partitions and in the inplane direction to increase the apparent spatial resolution by appending zeros on each side of the data before Fourier transformation [8]. The imaging volume was prescribed in a coronal or axial direction and included the circle of Willis.

In our preliminary phantom study, we obtained MR images of gadolinium contrast material ranging from 1/1000 to its original concentration (0.0005-0.5 mmol/ml). We used the same imaging sequence and manually measured signal intensities. These data showed that gadolinium contrast material at 1/100-1/10 (0.005-0.05 mmol/ml) its original concentration had strong signal intensity (Fig. 1). Therefore, the optimal venous infusion rate of the contrast media was calculated to be 0.6-12 ml/sec, on the basis of a healthy cardiac output of 61.5-118.8 ml/sec [9]. We manually infused 20 ml of gadodiamide hydrate (Omniscan; Daiichi Pharmaceutical, Tokyo, Japan) through the antecubital vein at a rate of 2-4 ml/sec, immediately followed by a 20- to 50-ml manual saline flush at 2-4 ml/sec. All injections were performed by an experienced radiologist. The blood pumped out of the heart was calculated to contain 1/60-1/15 the original concentration of gadodiamide hydrate (0.0083-0.033 mmol/ml). A power injector is an ideal tool for contrast injection; however, none was available for this study.



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Fig. 1. —Graph shows signal intensity versus concentration of gadolinium chelate in three-dimensional spoiled gradient-echo sequence. Note that gadolinium contrast at 1/100-1/10 its original concentration (0.005-0.05 mmol/ml) had strong signal intensity. X-axis is log transformed.

 

MR angiograms were reconstructed with maximum intensity projection by rotating the viewing angle every 10° from perpendicular to the imaging plane along the head-foot axis, right-left axis, or ventrodorsal axis of the head.

We evaluated the success of triggered imaging acquisition for intracranial arteries using Smartprep software. Without knowledge of the clinical information, two radiologists independently evaluated intracranial arteries around the circle of Willis. The radiologists assigned the arteries to two categories. The first category included arteries that could be clinically evaluated during the arterial phase when MR angiography selectively delineated the arteries or when arteries had stronger signal intensities than venous structures. The second category included arteries that could not be clinically evaluated because of a significant coincidental venous enhancement. Without knowledge of clinical information, the radiologists independently retrospectively evaluated the MR angiograms of three patients with aneurysms and one patient with a carotid cavernous fistula diagnosed on conventional angiography. Comparisons of MR angiography with conventional angiography were performed.

We divided our subjects into four groups according to imaging time. We evaluated differences in artery visibility using the Kruskal-Wallis test, a nonparametric analysis for more than three unpaired groups.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
The MR Smartprep triggered imaging in 81.6% of examinations (31 of 38 patients). Table 1 shows the results of 31 successfully triggered examinations. Observer 1 was able to evaluate arteries in 27 examinations and was unable to evaluate arteries in four examinations because of venous overlapping (Figs. 2, 3 4). Observer 2 had similar results. No significant difference was noted in the interobserver variability using Wilcoxon's rank sum test. Imaging times were 12-14 sec for four examinations, 15 sec for 10 examinations, 16 sec for nine examinations, and 18-20 sec for eight examinations. Artery visibility was independent of imaging time from 12 to 20 sec according to the evaluation criteria used in this study. No significant difference in the artery visibility was seen among the four groups with different acquisition times according to the Kruskal-Wallis test.


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TABLE 1 Smartprepa Triggering of Three-Dimensional MR Angiography: Results of 31 Examinations

 


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Fig. 2. —54-year-old man with suspected cerebrovascular disease. Arterial phase contrast-enhanced MR angiogram (inferior to superior view) in which software trigger succeeded shows arteries clearly. Resource MR angiographic images were in axial plane. Note that arteries around circle of Willis are seen well except for anterior cerebral arteries distal to anterior communicating artery because they are outside of imaging slab. Also note right and left internal carotid arteries (large straight arrows), right and left middle cerebral arteries (small straight arrows), and right and left posterior cerebral arteries (curved arrows).

 


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Fig. 3. —66-year-old man with vertigo. Arterial phase contrast-enhanced MR angiogram (anteroposterior view) in which software trigger succeeded shows arteries around circle of Willis. Resource MR angiographic images were in coronal plane. Note right and left internal carotid arteries (large straight arrows), right and left middle cerebral arteries (small straight arrows), right and left vertebral arteries (small curved arrows), and anterior cerebral arteries (large curved arrow).

 


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Fig. 4. —49-year-old man with suspected cerebrovascular disease. Contrast-enhanced MR angiogram (inferior to superior view) in which software trigger succeeded does not show parts of arteries around circle of Willis because of venous overlapping. Segmentation is useful for eliminating peripheral veins; however, it is difficult to eliminate veins near circle of Willis, especially cavernous sinuses. Resource MR angiographic images were in axial plane.

 

The trigger failed in seven examinations. When this happened, image acquisition automatically started 30 sec after the injection of contrast medium. In three of these seven examinations, minimal venous overlapping allowed arteries to be evaluated by both observers. In four examinations, arteries were not evaluated because of venous overlapping (Fig. 5).



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Fig. 5. —49-year-old woman with suspected vertebrobasilar insufficiency. Contrast-enhanced MR angiogram (anteroposterior view) in which software trigger failed shows that venous overlapping prevents evaluation of arteries around circle of Willis.

 

Overall, contrast-enhanced 3D MR angiography using Smartprep software revealed the arterial phase of intracranial arteries in 30 of 38 examinations for observer 1 and 29 of 38 examinations for observer 2, a viewing average off 77.6%. Both observers detected lesions in the three patients with intracranial aneurysms (Figs. 6A, 6B, 6C and 7A, 7B, 7C) and in the one patient with a carotid cavernous fistula.



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Fig. 6A. —65-year-old man with anterior communicating artery aneurysm. Conventional catheter angiogram of left internal carotid artery (oblique view) shows anterior communicating artery aneurysm (arrow).

 


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Fig. 6B. —65-year-old man with anterior communicating artery aneurysm. Conventional three dimensional time-of-flight MR angiogram (TR/TE, 40/7; flip angle, 30°) in oblique plane shows anterior communicating artery aneurysm (arrow).

 


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Fig. 6C. —65-year-old man with anterior communicating artery aneurysm. Contrast-enhanced MR angiogram shows anterior communicating artery aneurysm (arrow) with poor spatial resolution compared with time-of-flight technique.

 


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Fig. 7A. —54-year-old man with left internal carotid artery aneurysm. Conventional catheter angiogram of left internal carotid artery (lateral view) shows left internal carotid artery aneurysm (arrow).

 


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Fig. 7B. —54-year-old man with left internal carotid artery aneurysm. Conventional three-dimensional time-of-flight MR angiogram (TR/TE, 40/7; flip angle, 30°; left anterior oblique view) shows left internal carotid artery aneurysm (arrow). Signal intensities of aneurysm and surrounding internal carotid artery are weaker than those on contrast-enhanced MR angiogram (C). Causes of decreased signal intensity are thought to be slow or disturbed flow.

 


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Fig. 7C. —54-year-old man with left internal carotid artery aneurysm. Contrast-enhanced MR angiogram (left anterior oblique view) shows left internal carotid artery aneurysm (arrow). Postprocessing to eliminate skull base, used in CT angiography, is unnecessary.

 


Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Several studies have described contrast-enhanced MR angiography for intracranial vascular abnormalities [10, 11, 12, 13]. These techniques are useful in the visualization of small vasculature and vessels with slow flow. However, in instances of a longer imaging time because of a longer TR, venous enhancement has been reported to obscure arterial anatomy [11, 13].

Contrast-enhanced MR angiography enabled us to obtain images of arterial phase intracranial vasculature in 20 sec compared with 5-10 min for conventional 3D time-of-flight MR angiography. Reduction of the spin saturation caused by T1 shortening and diminution of spin dispersion caused by a short TE played important roles in the visualization of intracranial arteries during shorter imaging times (Figs. 2 and 3). Also, contrast-enhanced MR angiography combined the MR Smartprep with centric K-space ordering allowed maximized contrast for intracranial arteries with minimal venous overlapping.

We assessed whether four different acquisition times would affect image quality. Because intracranial circulation takes approximately 6 sec [14], we predicted that the shortest acquisition time (12-14 sec) would have the highest image quality. Contrary to this prediction, there was no difference in image quality among the four groups (Table 1).

We used centric K-space ordering in our MR angiography sequence. Therefore, the rows of K-space were filled from the middle to the periphery. The center of K-space contains the low-spatial-frequency data that give images their overall shape and contrast [6]. The MR Smartprep technique, which triggers scanning upon detecting the contrast bolus, was used to match the center of K-space to the period of maximum effect during the first-pass bolus for the intracranial arteries. The combination of MR Smartprep and centric K-space ordering allows 3D MR angiography data sets to be obtained within 20 sec. However, the duration of imaging with signal differences between carotid arteries and jugular veins is expected to be approximately 6 see because of cerebral circulation time [14].

Five factors are believed to affect the success rate of triggering when using Smartprep software. First, the MR scanner requires adjusting. A stable signal should be obtained from the tracker volume during signal monitoring. Second, tracker volume size must be selected. When a tracker volume is smaller, the standard deviation of its signal intensity is expected to increase. Thus, the signal intensity change caused by the arrival of contrast medium may not surpass the preset threshold. Third, the threshold levels must be set. A lower threshold is preferable when using smaller tracker volumes. Fourth, the location of the tracker volume is important. The tracker volume should be accurately placed at the vessels of interest, avoiding tortuous vessels because of signal fluctuations caused by disturbed or turbulent flow. A stable signal can be obtained from a tracker volume placed near the isocenter of the magnet. Fifth, patients should be requested to limit their movement because smaller tracker volumes may be affected by patient movement.

There were differences in the success rate of triggering between our data regarding evaluation of intracranial arteries and a previous study by Isoda et al. [3]. We believe that our lower triggering success rate depends on the smaller size of tracker volumes used in our experiment. Because the standard deviation of tracker volume signal was thought to increase with smaller size, the signal intensity change caused by the arrival of contrast medium did not surpass the preset threshold and triggering failed. In this study, we used a tracker volume ranging in size from 1 x 1 x 2 cm to 4 x 4 x 2 cm, thresholds of 1 or 2 standard deviations from the mean, and 5% or 10% signal intensity increase over the baseline. In the study performed by Isoda et al., researchers used a tracker volume ranging in size from 2 x 2 x 2 cm to 20 x 4 x 4 cm, thresholds of 2 or 3 standard deviations, and 15% or 20% signal intensity increase over the baseline. Furthermore, patient movement may have caused vessels to shift outside the smaller volume. Another cause of our lower triggering success may be the location of the tracker volume. Signal intensity of the tracker volume might have fluctuated because of turbulent and pulsatile flow.

Contrast-enhanced MR angiography is similar to CT angiography because both techniques require short imaging time and the use of contrast material. However, postprocedural elimination of the skull base is not necessary when using contrast-enhanced MR angiography (Fig. 7A, 7B, 7C). Also, venous overlapping obscures arterial structures around the circle of Willis in CT angiography. Gadolinium contrast materials are less nephrotoxic than iodinated contrast materials [15]; therefore, contrast-enhanced MR angiography is preferable, although it has the limitation of lower spatial resolution.

In this study, we attempted to introduce selective arterial phase contrast-enhanced MR angiography of intracranial arteries; however, the image quality using this technique was poor compared with that of unenhanced time-of-flight MR angiography (Figs. 6A, 6B, 6C and 7A, 7B, 7C). Therefore, we could not replace 3D time-of-flight MR angiography with contrast-enhanced 3D MR angiography to evaluate intracranial arteries. We predict that the evolution of MR technology will soon address this problem. Contrast-enhanced MR angiography is also inferior to 3D time-of-flight MR angiography because of the cost of IV contrast material. However, we believe that contrast-enhanced MR angiography has several merits. Contrast-enhanced MR angiography is suitable for uncooperative patients with suspected intracranial main artery occlusion. Axial imaging slabs are preferable for visualization of intracranial arteries using conventional 3D time-of-flight MR angiography because signal intensity depends on time-of-flight effects. Conversely, contrast-enhanced 3D MR angiography allows us to choose a coronal imaging slab because the signal intensity depends on contrast material, not on time-of-flight. Therefore, contrast-enhanced 3D MR angiography can show arterial structures from the origin of the internal carotid artery to the intracranial arteries. This technique, with a shorter echo time, is expected to show the perfusion status of cerebral aneurysms treated with coils or aneurysm clips, and of adjacent cerebral arteries more clearly than 3D time-of-flight MR angiography with relatively longer echo time because shorter echo time can reduce susceptibility artifacts caused by metal. Contrast-enhanced 3D MR angiography is useful for patients with carotid cavernous fistula, arteriovenous malformation, and moyamoya disease, in which abnormal vessels may be overlooked using unenhanced 3D time-of-flight MR angiography because of their small caliber or slow flow. Further investigation is needed to evaluate the clinical efficacy of contrast-enhanced 3D MR angiography.

In conclusion, the Smartprep software triggered imaging of intracranial arteries in 81.6% of examinations. In 77.6% of examinations, the resulting MR angiograms revealed intracranial arteries with minimal venous overlap. Contrast-enhanced 3D MR angiography coupled with the Smartprep software is a promising method for delineating intracranial arteries and vascular lesions in less than 20 sec.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Foo TKF, Saranathan M, Prince MR, Chenevert TL. Automated detection of bolus arrival and initiation of data acquisition in fast, three-dimensional, gadolinium-enhanced MR angiography. Radiology 1997;203:275-280[Abstract/Free Full Text]
  2. Prince MR, Chenevert TL, Foo TKF, Londy FJ, Ward JS, Maki JH. Contrast-enhanced abdominal MR angiography: optimization of imaging delay time by automating the detection of contrast material arrival in the aorta. Radiology 1997;203:109-114[Abstract/Free Full Text]
  3. Isoda H, Takehara Y, Isogai S, et al. Technique for arterial-phase contrast-enhanced three-dimensional MR angiography of the carotid and vertebral arteries. AJNR 1998;19:1241-1244[Abstract]
  4. Levy RA, Prince MR. Arterial-phase three-dimensional contrast-enhanced MR angiography of the carotid arteries. AJR 1996;167:211-215[Abstract/Free Full Text]
  5. Isoda H, Ushimi T, Masui T, et al. Clinical evaluation of pulmonary 3D time-of-flight MRA with breath holding using contrast media. J Comput Assist Tomogr 1995;19:911-919[Medline]
  6. Wood ML. Fourier imaging. In: Stark DD, Bradley WG Jr., eds. Magnetic resonance imaging , 2nd ed., St. Louis: Mosby-Year Book, 1992:21-66
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  9. Trindade PT, Brown P, Puryear JV, Popylisen S, Schnittger I. Automatic cardiac output measurement (ACOM): clinical applications of a new non-invasive tool. Int J Card Imaging 1998;14:147-154[Medline]
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  11. Jung HW, Chang KH, Choi DS, Han MH, Han MC. Contrast-enhanced MR angiography for the diagnosis of intracranial vascular disease: optimal dose of gadopentetate dimeglumine. AJR 1995;165:1251-1255[Abstract/Free Full Text]
  12. Talagala SL, Jungreis CA, Kanal E, et al. Fast three-dimensional time-of-flight MR angiography of the intracranial vasculature. J Magn Reson Imaging 1995;5:317-323[Medline]
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  14. Milburn JM, Moran CJ, Cross DT III, Diringer MN, Pilgram TK, Dacey RG Jr. Effect of intraarterial papaverine on cerebral circulation time. AJNR 1997;18:1081-1085[Abstract]
  15. Prince MR, Arnoldus C, Frisoli JK. Nephrotoxicity of high-dose gadolinium compared with iodinated contrast. J Magn Reson Imaging 1996;6:162-166[Medline]

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