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MR Digital Subtraction Angiography for the Assessment of Cranial Arteriovenous Malformations and Fistulas

¹ Department of Radiology, Yamanashi Medical University, 1110 Shimokato, Tamaho-cho, Nakakoma-gun, Yamanashi, 409-3898, Japan.
² Department of Neurosurgery, Yamanashi Medical University, Tamaho-cho, Nakakoma-gun, Yamanashi, 409-3898, Japan.

Received August 2, 1998; accepted after revision January 13, 2000.

 
Address correspondence to S. Aoki.

Introduction

Top Introduction Subjects and Methods Results Discussion References

 
High temporal resolution imaging has been essential in the diagnosis of arteriovenous malformations and fistulas. Early venous filling during conventional catheter angiography may be the only diagnostic clue to detect the presence of small hemorrhagic arteriovenous malformations and postoperative, embolized, or irradiated arteriovenous malformations or fistulas with slow flow. Conventional catheter angiography (intraarterial digital subtraction angiography) has been the only available technique for this hemodynamic evaluation; however, this is an invasive procedure with a complication rate of approximately 0.5%. Unenhanced three-dimensional (3D) time-of-flight MR angiography is relatively insensitive to slow flow because flow-related enhancement (inflow effect) may not persist in the venous system or in the distal portion of the slow-flow vessels [1, 2]. With contrast agents, a more sensitive detection of slow flow in vessels is possible because of marked shortening of intravascular T1 relaxation times [3]. Compared with unenhanced flow-dependent MR angiography, 3D contrast-enhanced MR angiography is useful for the visualization of slow flow, especially in the distal portion of a severely stenotic or occluded lesion [3,4,5]. On the other hand, only a few studies have reported the use of a two-dimensional (2D) technique to reduce the scan time (increase frame rate) of contrast-enhanced MR angiography [6, 7], and to our knowledge, no researchers have applied this technique to the evaluation of cranial arteriovenous shunts. By using the 2D technique, we can easily reduce the scan time to 0.5 sec and obtain hemodynamic information similar to that obtained with invasive catheter angiography, including the separation of the arterial and venous phases. We evaluated the clinical applicability of 2D thick-slice ultrafast contrast-enhanced subtraction MR angiography (2D MR digital subtraction angiography) in the evaluation of cerebral arteriovenous malformations and fistulas.

Subjects and Methods

Top Introduction Subjects and Methods Results Discussion References

 
Twenty-one consecutive brain MR imaging examinations of 13 patients with angiographically proven arteriovenous malformations or arteriovenous fistulas (five patients had dural arteriovenous fistulas and eight patients had arteriovenous malformations) were prospectively studied. Unenhanced 3D time-of-flight MR angiography, routine unenhanced and contrast-enhanced MR imaging, and MR digital subtraction angiography were performed on a Signa 1.5-T scanner (Signa Horizon Echo Speed, version 5.52-5.7; General Electric Medical Systems, Milwaukee, WI). Two patients underwent three successive examinations, four patients underwent two, and seven patients underwent one. All patients underwent imaging before treatment. Intraarterial digital subtraction angiograms of arteriovenous shunts obtained within 1 week of the MR imaging examinations showed that the arteriovenous shunts (arteriovenous malformation or arteriovenous fistula) were patent in 18 examinations and obliterated in three. T1-weighted MR images revealed hyperintense hematomas surrounding the patent nidus in two examinations. Therefore, 18 active arteriovenous shunts (two with hematomas) and three occluded shunts were assessed.

Two-dimensional thick-slice ultrafast continuous scanning with a bolus injection of contrast material (MR digital subtraction angiography) was performed with a fast spoiled gradient-recalled sequence (TR/TE, 6.5/1.7; flip angle, 60°; field of view, 30 x 22 cm; matrix size, 512 x 192; band-width, 62 kHz; single slice thickness, 5-10 cm). MR digital subtraction angiography was performed every 0.975 sec after the initiation of a bolus injection of 15 mL of gadolinium chelates (generally at 8 mL/sec, although a slower rate was used when the placement of a large needle was difficult) for a duration of up to 40 sec on mainly sagittal planes (of the hemisphere). The last image before contrast arrival (mask image, mostly around the 10th frame) was selected on the cinematic display and subtracted from the later images. Subtraction images (simple subtraction) were generated with commercially available software (Advantage Windows; General Electric Medical Systems). Approximately 30 subtracted images were reconstructed within 1 min. Twelve of 30 subtracted images were filmed for evaluation.

MR digital subtraction angiography and time-of-flight MR angiography were independently evaluated by two observers who were unaware of the patency and location of vascular lesions. First, the observers were asked whether a patent arteriovenous malformation or arteriovenous fistula was present. When any possible component of an arteriovenous shunt was detected, the answer to this question was yes. After the observers answered yes, we recorded abnormal findings, such as abnormalities that indicated feeding vessels or the visualization of early venous filling. After the initial review, each MR digital subtraction angiogram was paired and compared with the corresponding sites on intraarterial digital subtraction angiography, and reassessment was performed in terms of the vascular visualization. On MR digital subtraction angiography, vessels were rated on a three-point scale (1 = not visible [including segments outside the field of view], 2 = some segments visible, 3 = all segments visible). Feeding and draining vessels were also evaluated on a three-point scale (1 = not visible, 2 = partially visible, 3 = clearly visible). Observers evaluated the following vascular structures: feeding vessels, arteriovenous shunts, draining vessels, internal carotid artery, A1 segment of the anterior cerebral artery, A2 and A3 segments of the anterior cerebral artery, M1-M3 segments of the middle cerebral artery, distal vertebral artery, basilar artery, posterior cerebral artery, superior sagittal sinus, straight sinus, deep cerebral veins, transverse and sigmoid sinus, and jugular vein. Kappa values were calculated to determine interobserver variance.

Results

Top Introduction Subjects and Methods Results Discussion References

 
On MR digital subtraction angiography, all of the patent arteriovenous shunts (18/18) were detected; however, on 3D time-of-flight MR angiography, only 14 patent arteriovenous malformations or fistulas were detected by both observers. Slow blood flow in the remaining four malformations or fistulas was diagnosed with intraarterial digital subtraction angiography. In the remaining three examinations, MR digital subtraction angiography and 3D time-of-flight MR angiography correctly indicated no definite lesions caused by occlusion or resection of the arteriovenous malformations or fistulas.

The mean vascular visualization ratings of feeding vessels, arteriovenous shunts, and draining vessels on MR digital subtraction angiography were 1.8 ( = 0.38), 2.6 ( = 1), and 2.5 ( = 0.32), respectively. In large cerebral arteries (internal carotid, vertebral, and basilar arteries) and A2 and A3 segments of the anterior cerebral artery, the mean visualization rates (2.8, 2.1, 2.7, and 2.3, respectively) and the interobserver agreement (0.58, 0.82, 0.7, and 0.77, respectively) were relatively high. In small arterial branches (A1 segment of the anterior cerebral artery and M1-M3 segments of the middle cerebral artery), the mean visualization rate (1.9, 1.9, and 2.0, respectively) and the interobserver agreement (0.32, 0.3, and 0.5, respectively) were relatively low. All the venous sinuses and tributaries were rated higher (2.7-3.0; = 1) compared with most other arterial structures.

On MR digital subtraction angiography, early venous filling was mainly used to detect arteriovenous malformations or fistulas; however, on time-of-flight MR angiography, abnormalities indicating feeding vessels were mainly assessed to detect lesions (Figs. 1A,1B,1C,1D and 2A,2B,2C,2D). One arteriovenous malformation with hematoma was diagnosed on time-of-flight MR angiography by the presence of abnormalities, which were considered to represent feeding vessels; however, nidus and draining vessles were not visible because of the hyperintense signal of hematoma. On MR digital subtraction angiography, the nidus and draining vessel were easily recognized because of the missing signal of hematoma, resulting from the subtraction technique. When large feeding vessels were visible on MR digital subtraction angiography, feeding vessels and draining vessels sometimes could be separated on different frames of MR digital subtraction angiography. No complications were observed during MR digital subtraction angiography.

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —21-year-old man with small residual subsplenic arteriovenous malformation. Patient is in postoperative residual state. Serial MR digital subtraction angiographic images in sagittal plane show arteriovenous malformation nidus (arrow) on early arterial phase (A) image. Note early venous filling in straight sinus (arrowheads) on late arterial phase (B) image.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —21-year-old man with small residual subsplenic arteriovenous malformation. Patient is in postoperative residual state. Serial MR digital subtraction angiographic images in sagittal plane show arteriovenous malformation nidus (arrow) on early arterial phase (A) image. Note early venous filling in straight sinus (arrowheads) on late arterial phase (B) image.

View larger version (64K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —21-year-old man with small residual subsplenic arteriovenous malformation. Patient is in postoperative residual state. Partial maximum-intensity-projection image of hemisphere in lateral view of unenhanced three-dimensional time-of-flight MR angiogram fails to reveal arteriovenous malformation because of relatively slow flow in postoperative state.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —21-year-old man with small residual subsplenic arteriovenous malformation. Patient is in postoperative residual state. Lateral view of internal carotid angiogram confirms small residual arteriovenous malformation adjacent to splenium of corpus callosum.

View larger version (79K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —69-year-old woman with postembolized cavernous sinus dural arteriovenous fistula. Serial MR digital subtraction angiographic images in sagittal plane show early venous filling of posterio portion of cavernous sinus (arrows). This slow-flow abnormality was not revealed on time-of-flight MR angiog raphy (not shown).

View larger version (102K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —69-year-old woman with postembolized cavernous sinus dural arteriovenous fistula. Serial MR digital subtraction angiographic images in sagittal plane show early venous filling of posterio portion of cavernous sinus (arrows). This slow-flow abnormality was not revealed on time-of-flight MR angiog raphy (not shown).

View larger version (112K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —69-year-old woman with postembolized cavernous sinus dural arteriovenous fistula. Serial MR digital subtraction angiographic images in sagittal plane show early venous filling of posterio portion of cavernous sinus (arrows). This slow-flow abnormality was not revealed on time-of-flight MR angiog raphy (not shown).

View larger version (109K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D. —69-year-old woman with postembolized cavernous sinus dural arteriovenous fistula. Lateral view of internal carotid angiogram shows small residual arteriovenous shunt at posterior aspect o cavernous sinus (arrow) mostly filled with coils.

Discussion

Top Introduction Subjects and Methods Results Discussion References

 
Among various MR angiographic and CT angiographic techniques, contrast-enhanced 2D (or thick slice) MR angiography is considered the best technique to show cerebral hemodynamics with high temporal resolution. Additionally, it provides good imaging quality, similar to that of catheter angiography [6, 7]. Other techniques such as time-of-flight MR angiography, phase-contrast MR angiography, first-pass contrast-enhanced MR angiography, and 3D CT angiography have high spatial resolution and can provide 3D information as well. Although the delineation of anatomic structures on these techniques is excellent, temporal resolution is usually low, and the detection of early venous filling is relatively poor. Even with 3D MR digital subtraction angiography with a time-resolve technique [5] of 3-5 sec temporal resolution, it may be difficult to consistently reveal early venous filling or to differentiate feeding vessels from draining vessels. Although anatomic resolution may be limited compared with that of 3D acquisition, 2D acquisition obtained at a high speed can reveal an early draining vein.

Our 2D MR digital subtraction angiographic technique was easy to perform because complicated postprocessing techniques, such as maximum intensity projection, were not needed. In earlier articles about MR angiography, the 2D subtraction technique was probably used because of its simplicity and feasibility; however, researchers used the subtraction of a systolic image from a diastolic image [8]. Our simple, less-invasive MR digital subtraction angiography may be particularly useful for patients with iodinated contrast allergy and for those in whom multiple catheterizations should be avoided (e.g., pediatric patients). However, three limitations of our 2D MR digital subtraction angiographic technique exist: only one or two locations (usually right and left hemisphere) or planes (usually sagittal or coronal) can be obtained; small vessels may be obscured, probably because of the partial volume effect; and summation of vessels can not be eliminated by changing view angles.

In conclusion, we believe that 2D MR digital subtraction angiography with temporal resolution within 1 sec has a unique ability to reveal cerebral hemodynamics similar to that of intraarterial digital subtraction angiography and may play an important role in revealing intracranial arteriovenous malformations and fistulas.

References

Top Introduction Subjects and Methods Results Discussion References

 

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3. Prince MR. Gadolinium-enhanced MR aortography. Radiology 1994;191:155 -164[Abstract/Free Full Text]
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