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Intracranial Aneurysms: Detection with Gadolinium-enhanced Dynamic Three-dimensional MR Angiography-Initial Results¹

¹ From the Department of Radiology, Unité de RMN, Hôpital Erasme, Université Libre de Bruxelles, 808 route de Lennik, B-1070, Brussels, Belgium. Received July 7, 1999; revision requested August 17; final revision received November 29; accepted December 7. Address correspondence to T.M. (e-mail: tmetens@ulb.ac.be).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To assess the clinical utility and accuracy of contrast material–enhanced dynamic three-dimensional (3D) T1-weighted magnetic resonance (MR) angiography in the detection of unruptured intracranial aneurysms.

MATERIALS AND METHODS: A prospective blinded comparison of 3D contrast-enhanced T1-weighted MR angiography with 3D inflow magnetization transfer and tilted optimized nonsaturating excitation (MT TONE) imaging, phase-contrast MR angiography, and conventional digital subtraction angiography (DSA) was performed in 32 consecutive patients. The first dynamic 3D contrast-enhanced T1-weighted acquisition was individually timed after injection of a bolus of gadolinium-based contrast agent to obtain an arterial phase image followed by two sequential venous phase images (three 18-second acquisitions). Two readers independently interpreted and graded the MR images for diagnostic confidence and depiction of aneurysms and subsequently compared them with DSA images.

RESULTS: Three-dimensional contrast-enhanced T1-weighted MR angiograms depicted all 23 aneurysms detected in 17 patients at DSA (mean size, 6 mm; range, 2–21 mm) with one false-positive result by one reader (sensitivity, 100%; specificity, 94%). MT TONE and phase-contrast images failed to depict one and seven aneurysms, respectively (MT TONE sensitivity of 96% and specificity of 100%, phase-contrast sensitivity of 70% and specificity of 100%). Aneurysm depiction at 3D contrast-enhanced T1-weighted MR angiography was significantly better than that at MT TONE imaging (P < .012), and that with both was significantly superior to that of phase-contrast imaging (P < .001). Differences in diagnostic confidence in the presence of an aneurysm were not significant between 3D contrast-enhanced T1-weighted and MT TONE imaging (P = .076).

CONCLUSION: Dynamic 3D contrast-enhanced T1-weighted MR angiography is a fast, efficient, and minimally invasive imaging method with which to diagnose intracranial aneurysms.

Index terms: Aneurysm, intracranial, 17.73 • Aneurysm, MR, 17.12142 • Cerebral blood vessels, MR, 17.12142 • Magnetic resonance (MR), angiography, 17.12142 • Magnetic resonance (MR), three-dimensional, 17.12142

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The efficiency of magnetic resonance (MR) angiography in the detection of cerebral aneurysms has considerably improved, equaling that of conventional digital subtraction angiography (DSA) for aneurysms larger than 3–5 mm (1–4). Weakness of the vascular endothelium or damage to it as a result of hemodynamic features such as shear stress or local flow alteration after vascular treatment constitute risk factors for aneurysm formation and rupture (5,6). The relation between aneurysm size and rupture rate remains uncertain (7), but rupture of asymptomatic aneurysms smaller than 5 mm have been repeatedly reported (8–13). Even if this subject remains controversial, detection of asymptomatic aneurysms between 3 and 5 mm represents a real concern. At MR imaging, a recent study emphasized the atypical appearances of small patent aneurysms (14), and other investigations reported the efficiency of high-spatial-resolution time-of-flight MR angiography combined with multiplanar reconstruction in the detection of aneurysms as small as 2 mm (15). The same technique, in a comparison with conventional cerebral angiography in the follow-up of cerebral aneurysms treated with Guglielmi detachable coils, was improved by using a short echo time (16,17). In these studies, however, the MR acquisition time remains between 4 and 12 minutes, a period that might be considered too long for some patients with unstable acute subarachnoid hemorrhage due to aneurysmal rupture. As an alternative to MR angiography, helical computed tomography (CT) with postprocessing based on volume rendering (18,19) seems to have a relatively good sensitivity for the detection of aneurysms as small as 3 mm (mean sensitivity among four observers, 83% [19]). Helical CT, however, requires the injection of 80–100 mL of iodinated contrast material and an amount of radiation greater than that at conventional CT. All these MR and CT approaches necessitate a lot of postprocessing. In this context, there is definitely a need for a fast, noninvasive, easily interpretable method able to depict small intracranial aneurysms.

Dynamic three-dimensional (3D) contrast material–enhanced T1-weighted MR angiography combines high spatial resolution and fast acquisition with a very short echo time to provide excellent arterial phase angiograms in thoracoabdominal and neck studies (20), but to date to our knowledge, this method has not been applied to the study of intracranial vessels. The objective of our study was to evaluate prospectively the accuracy of fast dynamic 3D contrast-enhanced T1-weighted MR angiography in the diagnosis of intracranial aneurysms and compare findings with those at conventional DSA, 3D inflow MR imaging, and 3D phase-contrast MR angiography.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Study Design
To evaluate their respective value for the detection of intracranial aneurysms, we performed a prospective blinded comparison of dynamic 3D contrast-enhanced T1-weighted MR angiography, 3D inflow MR imaging, and phase-contrast MR angiography with conventional DSA. The final diagnosis was obtained at DSA.

Patients
From June 1998 through March 1999, 32 consecutive patients (13 men and 19 women; mean age, 49 years; age range, 19–78 years) underwent imaging to evaluate possible intracranial aneurysm. At clinical presentation, these patients had symptoms including severe headache, visual disturbance (oculomotor nerve palsy of sudden onset), and vertigo. Four of the patients had a history of unexplained subarachnoid hemorrhage, and six with a previous aneurysm surgery (clip placement) were referred to rule out development of new aneurysms. Three patients had CT images suggestive of an aneurysm.

The study was performed in accordance with the recommendations of our institutional review board. The whole procedure was explained to all patients, and they gave their informed consent. To be included, a patient could not have an acute aneurysmal hemorrhage at the time of the study. DSA was not always performed before MR angiography. Five patients were examined before and after intravascular treatment of an aneurysm.

MR Angiography
MR angiography was performed with a 1.5-T system (CompactPlus, PowerTrak 6000; Philips Medical Systems, Best, the Netherlands). The receiver coil was a standard head coil. High-spatial-resolution, intermediate-weighted (proton-density–weighted) images were acquired first with a turbo spin-echo sequence: repetition time msec/echo time msec of 2,900/14, turbo spin-echo factor of 10, 170 x 260-mm field of view, 354 x 512 acquisition matrix, 36 transverse 2.7-mm-thick sections, no intersection gap, 67.5% half-Fourier acquisition, imaging duration of 3 minutes 6 seconds.

Simultaneously with the injection of a test bolus of 2 mL of gadodiamide (Omniscan; Nycomed, Oslo, Norway), gradient-echo T1-weighted transverse imaging (15/2.8 with 60° flip angle) at the level of the carotid bifurcation was performed at a rate of one image every 1.3 seconds during 40 seconds.

With use of an electronic region of interest within the internal carotid artery, the individual time delay T between the beginning of contrast agent administration and the maximum arterial enhanced signal intensity was determined. Then, a double dose of gadodiamide (0.2 mmoL per kilogram of body weight) was injected, and a dynamic 3D contrast-enhanced T1-weighted gradient-echo acquisition was started after a time delay D chosen such that data collection of the central third of k space of the first acquisition began when maximum contrast agent concentration occurred in the intracranial arteries. With use of a linear gradient profile order (sequential mapping of k space) and an acquisition duration of 18 seconds for each dynamic 3D image, the delay D was given by T minus 6 seconds. During the central 6 seconds of the first dynamic acquisition, minimal venous enhancement occurred in the brain and an almost pure arterial image resulted. Three dynamic images were acquired subsequently with no interimage delay. An MR power injector (Spectris, model SSM 200; MedRad, Pittsburgh, Pa) was used for both injections, which were performed via a 20-gauge catheter placed in the left antecubital vein at a rate of 2.5 mL/sec and followed immediately with a 20-mL saline solution flush.

The parameters of the dynamic 3D contrast-enhanced T1-weighted sequence were as follows: 3D spoiled gradient-echo sequence, with phase cycling, 5.8/1.6, no flow compensation, 35° flip angle, 220 Hz per pixel bandwidth, 165 x 300-mm field of view, 228 x 512 acquisition matrix, 51 1.8-mm-thick coronal sections with 0.9-mm overlap, total imaging duration for three dynamic images of 54 seconds. The coronal 3D slabs were positioned from transverse intermediate-weighted, turbo spin-echo images and multisection survey images to include the middle cerebral artery, the circle of Willis, both carotid arteries from the bifurcation, and the vertebrobasilar system.

The protocol was modified slightly for the last eight patients to allow consecutive acquisition of two volumes: the coronal arterial volume was followed in the venous phase by a transverse volume encompassing the circle of Willis and the posterior fossa, including the posterior cerebral and superior cerebellar arteries. After the dynamic 3D contrast-enhanced T1-weighted acquisition, a transverse flow-compensated 3D inflow sequence with magnetization transfer and tilted optimized nonsaturating excitation (MT TONE) was acquired with three volumes. Acquisition was performed in descending order to avoid partial saturation of the arterial flow; the volume at the top was acquired first, followed by the central volume, and the volume at the bottom (31/3.4, starting flip angle of 14° and increasing in the feet-to-head direction, mean flip angle of 28°, 110 Hz per pixel bandwidth, magnetization transfer off-resonance prepulse, 160 x 200-mm field of view, 260 x 512 acquisition matrix, 96 contiguous 1.6-mm-thick sections with 0.8-mm overlap, total imaging duration of 7 minutes 44 seconds). The 3D MT TONE volume included the circle of Willis and the intracerebral arteries from the cervical segment of the carotid artery.

A 3D phase-contrast acquisition (14/6.7, 15° flip angle, 95 Hz per pixel bandwidth, phase-contrast encoding velocity of 30 cm/sec, 190 x 250-mm field of view, 260 x 512 acquisition matrix, 51 1.8-mm-thick coronal sections with 0.9-mm overlap, total imaging duration of 4 minutes 24 seconds) was then performed in the same orientation as the dynamic 3D contrast-enhanced T1-weighted acquisition.

From any set of 3D images, coronal, transverse, and sagittal maximum intensity projection (MIP) images were automatically reconstructed by the system computer. For all 3D images, a set of 12-18 radial MIP images were reconstructed around the left-to-right axis (increment, 15°–10°) and targeted on the middle cerebral artery, including the circle of Willis but excluding the horizontal segment of the carotid arteries. Postprocessing included reconstruction of additional targeted MIP images whenever an abnormal structure was suspected on one of the previous MIP or 3D source images.

Conventional DSA
All patients underwent MR angiography and DSA in the same week. The intracranial vessels were selectively opacified after injection in each vessel of 8 mL of contrast material (Hexabrix; Guerbet, Roissy, France) at an injection rate of 4 mL/sec. At DSA with a high-spatial-resolution matrix (1,024 x 1,024), we always acquired conventional Town and lateral views, which we completed by acquiring various oblique projections to delineate precisely the vascular anatomy and the possible existence of an underlying aneurysm.

Endovascular treatments of aneurysms have been performed by inserting Guglielmi detachable coils (Target Therapeutics/Boston Scientific, Fremont, Calif) with general anesthesia into the aneurysmal sac itself, leading to exclusion of the aneurysm with respect to the parent artery. In two patients, the internal right carotid artery was sacrificed. All the DSA images were reviewed in consensus by three experienced neuroradiologists (G.R., T.R., P.D.). The interventional procedures in five patients were all performed by one radiologist (G.R.).

Image Analysis
MR images were interpreted by two readers with different expertise in interpreting MR angiograms (F.R., more than 10 years; T.M., 4 years), who were unaware of clinical data and blinded to DSA results. After independent interpretations, discrepancies were immediately resolved by consensus to establish the final interpretation. Intermediate-weighted images were reviewed first and any enlargement that could correspond to an aneurysm was recorded and its size measured. Then, automatic MIP images, radial MIP images, and 3D MR source images were analyzed. When relevant, additional MIP images were processed and analyzed.

The observers were asked to grade the quality of aneurysm depiction and to grade the diagnostic confidence in the presence of an aneurysm on dynamic 3D contrast-enhanced T1-weighted, MT TONE, and 3D phase-contrast images. Aneurysms were described in terms of location, orientation, shape, and size; the presence of an intraluminal thrombus was sought. In the five patients treated with intravascular detachable coils, possible residual aneurysmal flow was also sought. When present, other vascular lesions or variants were also described.

Aneurysmal depiction was graded on a four-point scale: grade 3, excellent depiction of the lesion with good analysis of the relationships between the aneurysm and the parent vessel; grade 2, lesion visible but no clear relationship with parent vessel assessed; grade 1, lesion scarcely visible or visible retrospectively after comparison of images obtained with different MR sequences; grade 0, lesion not visible. Diagnostic confidence about the presence of an aneurysm was grade 2 when the presence or absence of a lesion was diagnosed with full confidence, grade 1 when there was a serious suspicion, grade 0 when a lesion was not diagnosed or when a false-positive result was diagnosed. Grade 0 was attributed at the end of the procedure, by means of comparison with results at DSA. Small suspected structures depicted on targeted MIP images were localized on source images, and we verified whether they were or were not in continuity with small vessels, to differentiate true aneurysm from addition artifacts from vessels. We also investigated the complementarity of intermediate-weighted images with dynamic 3D contrast-enhanced T1-weighted images.

Statistical Analysis
Grades for images obtained with the three MR angiographic 3D sequences were compared with a Wilcoxon matched pairs test. Differences were considered statistically significant if the P value was less than .05. Sensitivity and specificity were calculated by using the aneurysm as the unit of analysis in the calculation (19). The mean, median, minimum, and maximum sizes of the observed aneurysms were calculated.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Twenty-three aneurysms were detected in 17 of the 32 patients included in this study. A single aneurysm was detected in 13 patients, two patients had two aneurysms, and two had three aneurysms. In three of the 17 patients, other vascular abnormalities were described: a giant arteriovenous malformation in one patient, enlargement of the basilar artery at the level of the anterior inferior cerebellar artery in another patient, and severe bilateral stenosis of the internal carotid artery at the bifurcation and caliber irregularities (dolichoectasia) of the basilar and right posterior cerebral arteries in the third. Among the remaining 15 patients, eight had no vascular abnormalities, four with an aneurysm clip had no new aneurysm, and vascular dissection was discovered in three (one of the intrapetrous internal left carotid artery and two of the vertebral artery).

Aneurysm size had the following characteristics: spherical minimum diameter, 2 mm; spherical maximum diameter, 21 mm; elliptical mean size (short and long axes, respectively), 6.2 x 7.2 mm (SD, 5.5 x 5.7 mm); elliptical median size, 4 x 6.2 mm. The location and size distribution of the aneurysms are given in Table 1. One aneurysm of the basilar artery was partially thrombosed, and one giant aneurysm (diameter, 21 mm) of the left middle cerebral artery was completely thrombosed. The treated aneurysms were located in the basilar artery (n = 1), the right posterior communicating artery (n = 1), and the siphon of the right carotid artery (n = 3). At MR angiography and DSA, all embolization procedures were verified as successful, with no residual flow into the treated aneurysms. After sacrifice of the right internal carotid artery in one patient, a good blood supply was verified via reperfusion through the circle of Willis (Fig 1).

View larger version (128K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Cavernous giant aneurysm (18-mm diameter, arrowhead in a) of the right carotid artery in a 42-year-old man treated by means of sacrifice of the right internal carotid artery. MIP images in the coronal plane from dynamic contrast-enhanced coronal MR angiograms (5.8/1.6) (a, b) before and (c, d) 48 hours after endovascular treatment were obtained at (a, c) the arterial phase and (b, d) the first venous phase. The caliber of the A1 segment of the right anterior cerebral artery (straight arrow) and the anterior communicating artery (curved arrow) are clearly enlarged after sacrifice of the right carotid artery, demonstrating the excellent patency of the circle of Willis. Before embolization, the right A1 segment and the anterior communicating artery are completely depicted in only b, which is less sensitive to injection timing. After embolization, the increased diameter of the anterior communicating artery visible in c is confirmed in d.

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Cavernous giant aneurysm (18-mm diameter, arrowhead in a) of the right carotid artery in a 42-year-old man treated by means of sacrifice of the right internal carotid artery. MIP images in the coronal plane from dynamic contrast-enhanced coronal MR angiograms (5.8/1.6) (a, b) before and (c, d) 48 hours after endovascular treatment were obtained at (a, c) the arterial phase and (b, d) the first venous phase. The caliber of the A1 segment of the right anterior cerebral artery (straight arrow) and the anterior communicating artery (curved arrow) are clearly enlarged after sacrifice of the right carotid artery, demonstrating the excellent patency of the circle of Willis. Before embolization, the right A1 segment and the anterior communicating artery are completely depicted in only b, which is less sensitive to injection timing. After embolization, the increased diameter of the anterior communicating artery visible in c is confirmed in d.

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Cavernous giant aneurysm (18-mm diameter, arrowhead in a) of the right carotid artery in a 42-year-old man treated by means of sacrifice of the right internal carotid artery. MIP images in the coronal plane from dynamic contrast-enhanced coronal MR angiograms (5.8/1.6) (a, b) before and (c, d) 48 hours after endovascular treatment were obtained at (a, c) the arterial phase and (b, d) the first venous phase. The caliber of the A1 segment of the right anterior cerebral artery (straight arrow) and the anterior communicating artery (curved arrow) are clearly enlarged after sacrifice of the right carotid artery, demonstrating the excellent patency of the circle of Willis. Before embolization, the right A1 segment and the anterior communicating artery are completely depicted in only b, which is less sensitive to injection timing. After embolization, the increased diameter of the anterior communicating artery visible in c is confirmed in d.

View larger version (130K): [in this window] [in a new window] [Download PPT slide]   Figure 1d. Cavernous giant aneurysm (18-mm diameter, arrowhead in a) of the right carotid artery in a 42-year-old man treated by means of sacrifice of the right internal carotid artery. MIP images in the coronal plane from dynamic contrast-enhanced coronal MR angiograms (5.8/1.6) (a, b) before and (c, d) 48 hours after endovascular treatment were obtained at (a, c) the arterial phase and (b, d) the first venous phase. The caliber of the A1 segment of the right anterior cerebral artery (straight arrow) and the anterior communicating artery (curved arrow) are clearly enlarged after sacrifice of the right carotid artery, demonstrating the excellent patency of the circle of Willis. Before embolization, the right A1 segment and the anterior communicating artery are completely depicted in only b, which is less sensitive to injection timing. After embolization, the increased diameter of the anterior communicating artery visible in c is confirmed in d.

Considering MT TONE imaging alone or the combination of intermediate-weighted turbo spin-echo with 3D contrast-enhanced T1-weighted MR angiography, all thrombosed aneurysms were correctly detected at MR angiography, with no false-positive results.

Results of the qualitative analysis are summarized in Table 2. The mean grade for aneurysm depiction with 3D contrast-enhanced T1-weighted MR angiography was significantly greater than that with MT TONE angiography (P = .012), and the mean grades for both were significantly better than that for phase-contrast angiography (P < .001). The grade of diagnostic confidence about the presence of an aneurysm was significantly different between phase-contrast imaging and either 3D contrast-enhanced T1-weighted or MT TONE MR angiography (P < .001) but not between 3D contrast-enhanced T1-weighted and MT TONE angiography (P = .076). Considering all lesions, the quality of 3D contrast-enhanced T1-weighted images was evaluated as superior to that of MT TONE images in the depiction of 12 aneurysms and four other vascular lesions, but the converse was true for one patent aneurysm and a partial thrombosis of another aneurysm. Diagnostic confidence in the 3D contrast-enhanced T1-weighted images was superior to that in MT TONE images for four aneurysms (size, between 2 and 3.5 mm), and the converse was true in the depiction of one aneurysm pointing in the anteroposterior direction (size, 3 mm). The phase-contrast images never provided better depiction or superior diagnostic confidence than did the 3D contrast-enhanced T1-weighted or MT TONE images.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
To obtain an intracranial arterial image, individual accurate timing is crucial because the delay between arterial and venous maximal enhancement is much shorter in the brain than in extracranial locations (8 seconds at the level of the carotid bifurcation corresponds to 5–6 seconds between the middle cerebral artery and the sinus rectus or longitudinal sinus). Injection of a double dose of contrast agent lasted 8–16 seconds; thus, the central third of k space was acquired during a constant concentration of contrast agent, and no ghost artifacts occurred. Vascular caliber was sometimes different on arterial and venous images, as in Figure 1 where filling of the anterior communicating artery with contrast agent was incomplete at the time the first-pass image was acquired.

Arterial images have the main advantage of being interpreted more easily, because they are free of venous superimposition. Moreover, the combination of a very short echo time (1.6 msec) with a high concentration of contrast agent at the first pass, which sharply reduces the T1 of blood, made these arterial images much less prone to signal intensity losses due to turbulence or flow saturation effects. Also, in comparison with the two other MR techniques in the present study, image quality with the 3D contrast-enhanced T1-weighted sequence demonstrated a relative insensitivity to artifacts in patients treated by means of detachable coils. This feature was probably related to the very short echo time, as was found in other studies (16). Thus, 3D contrast-enhanced T1-weighted images are less dependent on the flow and merely represent the blood content. These conditions made 3D contrast-enhanced T1-weighted angiography more similar to conventional DSA (Fig 2).

View larger version (157K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Aneurysm of the anterior communicating artery (6.5 x 5.5 mm [arrow]) in a 66-year-old man. The lesion is depicted on (a) a high-spatial-resolution, intermediate-weighted, transverse image (2,900/14) and (b) a coronal DSA image, which are compared with (c) a coronal maximum intensity projection image computed from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6); (d) a transverse MT TONE image (31/3.4); and (e) a coronal phase-contrast image (14/6.7). Image quality was graded as optimal in c-e. The aneurysm is displayed with a homogeneous hyperintensity in c, whereas it appears less homogeneously intense in d and e.

View larger version (142K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Aneurysm of the anterior communicating artery (6.5 x 5.5 mm [arrow]) in a 66-year-old man. The lesion is depicted on (a) a high-spatial-resolution, intermediate-weighted, transverse image (2,900/14) and (b) a coronal DSA image, which are compared with (c) a coronal maximum intensity projection image computed from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6); (d) a transverse MT TONE image (31/3.4); and (e) a coronal phase-contrast image (14/6.7). Image quality was graded as optimal in c-e. The aneurysm is displayed with a homogeneous hyperintensity in c, whereas it appears less homogeneously intense in d and e.

View larger version (118K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Aneurysm of the anterior communicating artery (6.5 x 5.5 mm [arrow]) in a 66-year-old man. The lesion is depicted on (a) a high-spatial-resolution, intermediate-weighted, transverse image (2,900/14) and (b) a coronal DSA image, which are compared with (c) a coronal maximum intensity projection image computed from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6); (d) a transverse MT TONE image (31/3.4); and (e) a coronal phase-contrast image (14/6.7). Image quality was graded as optimal in c-e. The aneurysm is displayed with a homogeneous hyperintensity in c, whereas it appears less homogeneously intense in d and e.

View larger version (130K): [in this window] [in a new window] [Download PPT slide]   Figure 2d. Aneurysm of the anterior communicating artery (6.5 x 5.5 mm [arrow]) in a 66-year-old man. The lesion is depicted on (a) a high-spatial-resolution, intermediate-weighted, transverse image (2,900/14) and (b) a coronal DSA image, which are compared with (c) a coronal maximum intensity projection image computed from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6); (d) a transverse MT TONE image (31/3.4); and (e) a coronal phase-contrast image (14/6.7). Image quality was graded as optimal in c-e. The aneurysm is displayed with a homogeneous hyperintensity in c, whereas it appears less homogeneously intense in d and e.

View larger version (125K): [in this window] [in a new window] [Download PPT slide]   Figure 2e. Aneurysm of the anterior communicating artery (6.5 x 5.5 mm [arrow]) in a 66-year-old man. The lesion is depicted on (a) a high-spatial-resolution, intermediate-weighted, transverse image (2,900/14) and (b) a coronal DSA image, which are compared with (c) a coronal maximum intensity projection image computed from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6); (d) a transverse MT TONE image (31/3.4); and (e) a coronal phase-contrast image (14/6.7). Image quality was graded as optimal in c-e. The aneurysm is displayed with a homogeneous hyperintensity in c, whereas it appears less homogeneously intense in d and e.

Interestingly, all unruptured aneurysmal lesions were hyperintense on 3D contrast-enhanced T1-weighted images, in contrast with their atypical appearance at MR imaging (14). Nevertheless, the relative orientation of aneurysms and source images should not be underestimated, especially for small aneurysms that are less visible when they point in a direction perpendicular to the native sections. One bilobate aneurysm (two spheres with 2-mm diameter each) pointing vertically was depicted more clearly on coronal 3D contrast-enhanced T1-weighted images than on transverse MT TONE images (Fig 3). The converse was true in another patient, however, for one aneurysm pointing horizontally (3-mm diameter). This difficulty could probably be circumvented by using thinner sections and thus longer acquisition time for the MT TONE and phase-contrast sequences, as was done in a recent study in which multiplanar reformatting was systematically applied in addition to MIP imaging (15).

View larger version (147K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Multiple aneurysms in a 54-year-old woman. (a) Oblique DSA image of the left carotid artery depicts a 6.5-mm-diameter spherical aneurysm (arrowhead) at the trifurcation of the left middle cerebral artery. (b) Coronal DSA image of the right carotid artery demonstrates a bilobate aneurysm (two spheres with 2-mm diameter each [solid arrows]) located close to the trifurcation of the right middle cerebral artery and pointing caudally. A 3-mm-diameter spherical aneurysm (open arrow) is also depicted, on a branch of the right middle cerebral artery close to the insula. (c-e) Aneurysms are labeled as in a and b. (c) Targeted coronal MIP image from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6) depicts all three aneurysms clearly. (d) Coronal MIP image from MT TONE images (31/3.4) demonstrates the bilobate lesion, but it was depicted less accurately (as grade 1). (e) Coronal phase-contrast (14/6.7) image does not depict the bilobate lesion.

View larger version (162K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Multiple aneurysms in a 54-year-old woman. (a) Oblique DSA image of the left carotid artery depicts a 6.5-mm-diameter spherical aneurysm (arrowhead) at the trifurcation of the left middle cerebral artery. (b) Coronal DSA image of the right carotid artery demonstrates a bilobate aneurysm (two spheres with 2-mm diameter each [solid arrows]) located close to the trifurcation of the right middle cerebral artery and pointing caudally. A 3-mm-diameter spherical aneurysm (open arrow) is also depicted, on a branch of the right middle cerebral artery close to the insula. (c-e) Aneurysms are labeled as in a and b. (c) Targeted coronal MIP image from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6) depicts all three aneurysms clearly. (d) Coronal MIP image from MT TONE images (31/3.4) demonstrates the bilobate lesion, but it was depicted less accurately (as grade 1). (e) Coronal phase-contrast (14/6.7) image does not depict the bilobate lesion.

View larger version (65K): [in this window] [in a new window] [Download PPT slide]   Figure 3c. Multiple aneurysms in a 54-year-old woman. (a) Oblique DSA image of the left carotid artery depicts a 6.5-mm-diameter spherical aneurysm (arrowhead) at the trifurcation of the left middle cerebral artery. (b) Coronal DSA image of the right carotid artery demonstrates a bilobate aneurysm (two spheres with 2-mm diameter each [solid arrows]) located close to the trifurcation of the right middle cerebral artery and pointing caudally. A 3-mm-diameter spherical aneurysm (open arrow) is also depicted, on a branch of the right middle cerebral artery close to the insula. (c-e) Aneurysms are labeled as in a and b. (c) Targeted coronal MIP image from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6) depicts all three aneurysms clearly. (d) Coronal MIP image from MT TONE images (31/3.4) demonstrates the bilobate lesion, but it was depicted less accurately (as grade 1). (e) Coronal phase-contrast (14/6.7) image does not depict the bilobate lesion.

View larger version (67K): [in this window] [in a new window] [Download PPT slide]   Figure 3d. Multiple aneurysms in a 54-year-old woman. (a) Oblique DSA image of the left carotid artery depicts a 6.5-mm-diameter spherical aneurysm (arrowhead) at the trifurcation of the left middle cerebral artery. (b) Coronal DSA image of the right carotid artery demonstrates a bilobate aneurysm (two spheres with 2-mm diameter each [solid arrows]) located close to the trifurcation of the right middle cerebral artery and pointing caudally. A 3-mm-diameter spherical aneurysm (open arrow) is also depicted, on a branch of the right middle cerebral artery close to the insula. (c-e) Aneurysms are labeled as in a and b. (c) Targeted coronal MIP image from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6) depicts all three aneurysms clearly. (d) Coronal MIP image from MT TONE images (31/3.4) demonstrates the bilobate lesion, but it was depicted less accurately (as grade 1). (e) Coronal phase-contrast (14/6.7) image does not depict the bilobate lesion.

View larger version (70K): [in this window] [in a new window] [Download PPT slide]   Figure 3e. Multiple aneurysms in a 54-year-old woman. (a) Oblique DSA image of the left carotid artery depicts a 6.5-mm-diameter spherical aneurysm (arrowhead) at the trifurcation of the left middle cerebral artery. (b) Coronal DSA image of the right carotid artery demonstrates a bilobate aneurysm (two spheres with 2-mm diameter each [solid arrows]) located close to the trifurcation of the right middle cerebral artery and pointing caudally. A 3-mm-diameter spherical aneurysm (open arrow) is also depicted, on a branch of the right middle cerebral artery close to the insula. (c-e) Aneurysms are labeled as in a and b. (c) Targeted coronal MIP image from coronal 3D contrast-enhanced T1-weighted arterial phase images (5.8/1.6) depicts all three aneurysms clearly. (d) Coronal MIP image from MT TONE images (31/3.4) demonstrates the bilobate lesion, but it was depicted less accurately (as grade 1). (e) Coronal phase-contrast (14/6.7) image does not depict the bilobate lesion.

View larger version (174K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. Partially thrombosed aneurysm in a 20-year-old man. (a) On transverse intermediate-weighted, turbo spin-echo nonenhanced image (2,900/14), the residual flow demonstrated a signal void (open arrow), whereas the thrombosed region (solid arrows) was both iso- and hyperintense and was surrounded by a hypointense hemosiderin ring (arrowheads). On (b) transverse 3D contrast-enhanced T1-weighted source image (5.8/1.6) and (c) transverse MT TONE source image (31/3.4), residual flow was markedly hyperintense (open arrow), whereas the thrombus was isointense (straight solid arrow). Peripheral contrast enhancement of the organized thrombus (curved arrows) was depicted in b and c. The hypointense hemosiderin ring (arrowheads) was also seen in c. All lesion characteristics depicted in c were also depicted in b, which was obtained with a faster sequence. Additional parenchymal information was depicted on a compared with b and c.

View larger version (179K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. Partially thrombosed aneurysm in a 20-year-old man. (a) On transverse intermediate-weighted, turbo spin-echo nonenhanced image (2,900/14), the residual flow demonstrated a signal void (open arrow), whereas the thrombosed region (solid arrows) was both iso- and hyperintense and was surrounded by a hypointense hemosiderin ring (arrowheads). On (b) transverse 3D contrast-enhanced T1-weighted source image (5.8/1.6) and (c) transverse MT TONE source image (31/3.4), residual flow was markedly hyperintense (open arrow), whereas the thrombus was isointense (straight solid arrow). Peripheral contrast enhancement of the organized thrombus (curved arrows) was depicted in b and c. The hypointense hemosiderin ring (arrowheads) was also seen in c. All lesion characteristics depicted in c were also depicted in b, which was obtained with a faster sequence. Additional parenchymal information was depicted on a compared with b and c.

View larger version (185K): [in this window] [in a new window] [Download PPT slide]   Figure 4c. Partially thrombosed aneurysm in a 20-year-old man. (a) On transverse intermediate-weighted, turbo spin-echo nonenhanced image (2,900/14), the residual flow demonstrated a signal void (open arrow), whereas the thrombosed region (solid arrows) was both iso- and hyperintense and was surrounded by a hypointense hemosiderin ring (arrowheads). On (b) transverse 3D contrast-enhanced T1-weighted source image (5.8/1.6) and (c) transverse MT TONE source image (31/3.4), residual flow was markedly hyperintense (open arrow), whereas the thrombus was isointense (straight solid arrow). Peripheral contrast enhancement of the organized thrombus (curved arrows) was depicted in b and c. The hypointense hemosiderin ring (arrowheads) was also seen in c. All lesion characteristics depicted in c were also depicted in b, which was obtained with a faster sequence. Additional parenchymal information was depicted on a compared with b and c.

The coronal arterial phase acquisition systematically provided images of the vertebral and carotid arteries from the level of the bifurcation upward. In one patient in our study, a severe bilateral stenosis of the carotid arteries at the level of the bifurcation was discovered on the coronal arterial phase images, and in all patients with dissection, the availability of a comprehensive view of the vertebral and carotid arteries from the bifurcation represented valuable additional information. Intermediate-weighted images obtained up to the pericallosal artery should be further considered as a complement to 3D contrast-enhanced T1-weighted images. In our three patients with dissection, intermediate-weighted images provided useful information, depicting clearly a hyperintense and enlarged arterial wall, peripheral to the central flow void.

The very short acquisition time of the 3D contrast-enhanced T1-weighted sequence represents another striking feature of this method, making it more suitable for use in uncooperative patients and potentially attractive in emergency conditions. Additionally, it allows dynamic studies. Interestingly, progressive contrast agent uptake was demonstrated around thrombosed aneurysms in two cases. A salient feature of dynamic 3D contrast-enhanced T1-weighted imaging is that a thrombus was never hyperintense on arterial images, whereas even very slow flow remained hyperintense. This contrasted with turbo spin-echo, intermediate-weighted MR images, on which all thrombosed aneurysms were clearly depicted with hyperintensity that, however, could not be differentiated from slow flow. When slow flow is ruled out on 3D contrast-enhanced T1-weighted images, leaving the option of a thrombus, the precise location and size of a thrombosed region can be complementarily determined on high-spatial-resolution, intermediate-weighted, turbo spin-echo images (Fig 4).

In conclusion, this preliminary study shows the efficacy of dynamic 3D contrast-enhanced T1-weighted angiography in the detection of intracranial aneurysms, including small aneurysms. This fast MR angiographic technique provides arterial images that are easily interpreted and allows large coverage of the most important arteries above the carotid bifurcation.

	FOOTNOTES

 
Abbreviations: DSA = digital subtraction angiography, MIP = maximum intensity projection, MT TONE = magnetization transfer and tilted optimized nonsaturating excitation, 3D = three-dimensional

Author contributions: Guarantor of integrity of entire study, T.M.; study concepts and design, T.M.; definition of intellectual content, T.M.; literature research, T.M., F.R.; clinical studies, G.R., D.B.; data acquisition, G.R., D.B., T.R., P.D.; data analysis, F.R., T.M.; statistical analysis, T.M.; manuscript preparation and editing, T.M., F.R.; manuscript review, D.B., T.R., P.D., G.R.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Korogi Y, Takahashi , Mabuchi N, et al. Intracranial aneurysms: diagnostic accuracy of three-dimensional Fourier transform, time-of-flight MR angiography. Radiology 1994; 193:181-186.[Abstract/Free Full Text]
2. Huston J, Nichols DA, Luetmer PH, et al. Blinded prospective evaluation of sensitivity of MR angiography to known intracranial aneurysms: importance of aneurysm size. AJNR Am J Neuroradiol 1994; 15:1607-1614.[Abstract]
3. Ronkainen A, Puranen MI, Hernesniemi JA, et al. Intracranial aneurysms: MR angiographic screening in 400 asymptomatic individuals with increased familial risk. Radiology 1995; 195:35-40.[Abstract/Free Full Text]
4. Grandin CB, Mathurin P, Duprez T, et al. Diagnosis of intracranial aneurysms: accuracy of MR angiography at 0.5 T. AJNR Am J Neuroradiol 1998; 19:245-252.[Abstract]
5. Redekop G, TerBrugge K, Montanera W, Willinsky R. Arterial aneurysms associated with cerebral arteriovenous malformations: classification, incidence, and risk of hemorrhage. J Neurosurg 1998; 89:539-546.[Medline]
6. Rodesch G, Van Bogaert P, Szliwowski H, Baleriaux D, Brotchi J. Post embolization flow disturbances at the basilar tip triggering the development of an arterial aneurysm: a case report. Intervent Neuroradiol 1998; 4:247-251.
7. International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: risk of rupture and risks of surgical intervention. N Engl J Med 1998; 339:1725-1733.[Abstract/Free Full Text]
8. Ronkainen A, Hernesniemi J, Tromp G. Special features of familial intracranial aneurysms: report of 215 familial aneurysms. Neurosurgery 1995; 37:43-46.[Medline]
9. Inagawa T, Hirano A. Ruptured intracranial aneurysms: an autopsy study of 133 patients. Surg Neurol 1990; 33:117-123.[Medline]
10. Inagawa T, Hirano A. Autopsy study of unruptured incidental intracranial aneurysms. Surg Neurol 1990; 34:361-365.[Medline]
11. Schievink WI, Piepgras DO, Wirth FP. Rupture of previously documented small asymptomatic saccular intracranial aneurysms: report of three cases. J Neurosurg 1992; 76:1019-1024.[Medline]
12. Asari S, Ohmoto T. Natural history and risk factors of unruptured cerebral aneurysms. Clin Neurol Neurosurg 1993; 95:205-214.[Medline]
13. Solomon RA, Correll JW. Rupture of a previously documented asymptomatic aneurysm enhances the argument for prophylactic surgical intervention. Surg Neurol 1988; 30:321-323.[Medline]
14. Rollen P, Sze G. Small patent cerebral aneurysms: atypical appearances at 1.5-T MR imaging. Radiology 1998; 208:129-136.[Abstract/Free Full Text]
15. Chung TS, Joo JY, Lee SK, Chien D, Laub G. Evaluation of cerebral aneurysms with high-resolution MR angiography using section interpolation technique: correlation with digital subtraction angiography. AJNR Am J Neuroradiol 1999; 20:229-235.[Abstract/Free Full Text]
16. Gonner F, Heid O, Remonda L, et al. MR angiography with ultrashort echo time in cerebral aneurysms treated with Guglielmi detachable coils. AJNR Am J Neuroradiol 1998; 19:1324-1328.[Abstract]
17. Brunereau L, Cottier JP, Sonier CB, et al. Prospective evaluation of time-of-flight MR angiography in the follow-up of intracranial saccular aneurysms treated with Guglielmi detachable coils. J Comput Assist Tomogr 1999; 23:216-223.[Medline]
18. Harrison MJ, Johnson BA, Gardner GM, Welling BG. Preliminary results on the management of unruptured intracranial aneurysms with magnetic resonance angiography and computed tomographic angiography. Neurosurgery 1997; 40:947-955.[Medline]
19. Korogi Y, Takahashi M, Katada K, et al. Intracranial aneurysms: detection with three-dimensional CT angiography with volume rendering—comparison with conventional angiographic and surgical findings. Radiology 1999; 211:497-506.[Abstract/Free Full Text]
20. Remonda L, Heid O, Schroth G. Carotid artery stenosis, occlusion, and pseudo-occlusion: first-pass gadolinium-enhanced three-dimensional MR angiography—preliminary study. Radiology 1998; 209:95-102.[Abstract/Free Full Text]
21. Atlas SW, Hurts RW. Intracranial vascular malformations and aneurysms. In: Atlas SW, eds. Magnetic resonance imaging of the brain and spine. 2nd ed. Philadelphia, Pa: Lippincott-Raven, 1996; 489-556.
22. Litt AW, Maltin EP. Cerebrovascular abnormalities. In: Stark BW, eds. Magnetic resonance imaging. 3rd ed. St Louis, Mo: Mosby–Year Book, 1999; 1317-1327.

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