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Published online before print October 19, 2007, 10.1148/radiol.2453061684
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(Radiology 2008;246:205-213.)
© RSNA, 2007

Neuroradiology

Cerebral Arteriovenous Malformation: Spetzler-Martin Classification at Subsecond-Temporal-Resolution Four-dimensional MR Angiography Compared with That at DSA1

Dariusch R. Hadizadeh, MD, Marcus von Falkenhausen, MD, Jürgen Gieseke, PhD, Bernhard Meyer, MD, Horst Urbach, MD, Romhild Hoogeveen, PhD, Hans H. Schild, MD, and Winfried A. Willinek, MD

1 From the Departments of Radiology (D.R.H., M.v.F., J.G., H.U., H.H.S., W.A.W.) and Neurosurgery (B.M.), University of Bonn, Sigmund-Freud-Strasse 25, 53105 Bonn, Germany; and Philips Medical Systems, Best, the Netherlands (J.G., R.H.). From the 2005 RSNA Annual Meeting. Received September 29, 2006; revision requested December 8; revision received February 7, 2007; accepted April 2. Address correspondence to W.A.W. (e-mail: Winfried.Willinek{at}ukb.uni-bonn.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Purpose: To prospectively test the hypothesis that subsecond-temporal-resolution four-dimensional (4D) contrast material–enhanced magnetic resonance (MR) angiography at 3.0 T enables the same Spetzler-Martin classification (nidus size, venous drainage, eloquence) of cerebral arteriovenous malformation (AVM) as that at digital subtraction angiography (DSA).

Materials and Methods: Institutional ethics committee approval and written informed consent were obtained. In a prospective intraindividual comparative study, 18 consecutive patients with cerebral AVM (nine men, nine women; mean age, 41.9 years ± 14.0 [standard deviation]; range, 23–69 years) were examined with 4D contrast-enhanced MR angiography and DSA. Four-dimensional contrast-enhanced MR angiography combined randomly segmented central k-space ordering, keyhole imaging, sensitivity encoding, and half-Fourier imaging, which yielded a total acceleration factor of 60. Fifty dynamic scans were obtained every 608 msec at an acquired spatial resolution of 1.1 x 1.4 x 1.1 mm. Four-dimensional contrast-enhanced MR angiograms were independently reviewed by one neuroradiologist and one neurosurgeon according to Spetzler-Martin classification, overall diagnostic quality, and level of confidence. Kendall W coefficients of concordance (K) were computed to compare reader assessment of image quality, level of confidence, and Spetzler-Martin classification by using 4D contrast-enhanced MR angiography and to compare Spetzler-Martin classification as determined with DSA with that at 4D contrast-enhanced MR angiography.

Results: Spetzler-Martin classification of cerebral AVM at 4D contrast-enhanced MR angiography and at DSA matched in 18 of 18 patients for both readers, which yielded 100% interobserver agreement (K = 1). Image quality of 4D contrast-enhanced MR angiography was judged to be at least adequate for diagnosis in all patients by both readers. In three of 18 patients, DSA depicted additional arterial feeders of cerebral AVM.

Conclusion: Subsecond-temporal-resolution 4D contrast-enhanced MR angiography at 3.0 T had 100% agreement with DSA with regard to Spetzler-Martin classification of cerebral AVM.

Supplemental material: radiology.rsnajnls.org/cgi/content/full/2453061684/DC1

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Three-dimensional (3D) contrast material–enhanced magnetic resonance (MR) angiography is the first-line diagnostic tool in the preoperative work-up of patients with carotid stenosis (1,2). In many centers, 3D contrast-enhanced MR angiography has replaced digital subtraction angiography (DSA) for diagnostic purposes in the supraaortic arteries because of risks inherent to DSA, including bleeding, allergy, nephrotoxicity, and thromboembolism, which add up to a risk of 0.1%–1% for permanent neurologic deficits (3–10).

Cerebral arteriovenous malformations (AVMs) are developmental disorders consisting of intracerebral direct arteriovenous shunts without a normal intervening capillary bed. These vascular malformations have an overall yearly risk for hemorrhage of 1.5%–3% and a risk of death at the first bleeding of about 10% that increases with each bleeding (11,12). For adequate diagnosis and treatment of cerebral AVM, a detailed characterization of angioarchitecture and hemodynamics—including exact location, dimension of nidus, arterial feeding, and draining veins—is required (13). In 1986, Spetzler and Martin (12) introduced a grading scale for cerebral AVM that is based on nidus size, venous drainage, and eloquence of the adjacent brain region. This scale has proved to be of high clinical relevance because of its predictive value for surgical resectability and clinical outcome after resection (11,14–16). Other scales have been proposed for the prediction of the clinical outcome of other therapeutic regimens, such as radiosurgery (17–19) and embolization (20,21).

DSA currently is the standard reference procedure for diagnosis and follow-up of cerebral AVM because of its high temporal and spatial resolution (22,23). When the short mean transit times (typically 1.0–2.1 seconds or even less) of feeding arteries and draining veins in cerebral AVM (24) are taken into account, the low temporal resolution of conventional 3D contrast-enhanced MR angiography is a considerable limitation for reliable identification of feeding and draining vessels in cerebral AVM.

High-temporal-resolution four-dimensional (4D) contrast-enhanced MR angiography combines randomly segmented central k-space ordering (contrast-enhanced timing-robust angiography [CENTRA]) (25) and keyhole (26) and parallel imaging (sensitivity encoding) (27) to achieve subsecond temporal resolution while maintaining high spatial resolution. The purpose of our study was to prospectively test the hypothesis that subsecond-temporal-resolution 4D contrast-enhanced MR angiography at 3.0 T enables the same Spetzler-Martin classification of cerebral AVM as that at DSA.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Authors who are not employees of Philips Medical Systems (Best, the Netherlands) had control of inclusion of any data and information that might present a conflict of interest for the authors (J.G., R.H.) who are employees of that company.

Patients
In an ongoing prospective intraindividual comparative study, 18 consecutive patients with cerebral AVM (nine men, nine women; mean age, 41.9 years ± 14.0 [standard deviation]; age range, 23–69 years) were examined between September 2004 and August 2006 with both 4D contrast-enhanced MR angiography and DSA. Before enrollment of patients into this study, the study protocol was approved by the institutional ethics committee, and written informed consent was obtained from all patients. Patients older than 18 years who were scheduled for DSA because of suspected cerebral AVM were included in the study. Patients were excluded if contraindications to MR imaging (pacemaker, potentially magnetic implants, claustrophobia, etc) were present. Although an attempt was made to randomize the order of examinations, 4D contrast-enhanced MR angiography was performed first in 12 of 18 patients. The mean period between the DSA and the 4D contrast-enhanced MR angiographic examination was 8 days ± 22 (range, 0–92 days; median, 1 day).

MR Imaging
Four-dimensional contrast-enhanced MR angiography was successfully performed in 18 of 18 (100%) patients. MR imaging examinations were performed with a 3.0-T whole-body imager (Achieva; Philips Medical Systems) equipped with a high-performance gradient system offering a maximum gradient amplitude of 80 mT/m and a slew rate of 200 (T · m–1)/sec. A commercially available eight-channel sensitivity encoding–capable head coil (Philips Medical Systems) was used for imaging in all patients. A biphasic injection protocol was implemented with automatic power injection (Spectris; Medrad Europe, Beek, the Netherlands) of contrast medium: First, 10 mL of gadopentate dimeglumine (Magnevist; Schering, Berlin, Germany) was injected at a flow rate of 3 mL/sec, followed by 10 mL gadopentate dimeglumine at a flow rate of 1.5 mL/sec and by a saline flush of 25 mL. Four-dimensional contrast-enhanced MR angiographic acquisition was initiated 10 seconds after the injection of contrast medium was started.

Four-dimensional contrast-enhanced MR angiography was performed by using CENTRA (25,28), keyhole imaging (26) (keyhole diameter: 16% of total k-space, yielding an acceleration factor of six), parallel imaging (sensitivity encoding [27] with a reduction in the phase-encoding direction of four and in the section-encoding direction of two, yielding a total acceleration factor of eight), and half-Fourier imaging (skipping 25% of k-space data, yielding an acceleration factor of 1.25). With the combination of these techniques, 4D contrast-enhanced MR angiography resulted in a total acceleration of 6 x 8 x 1.25, which equals 60 times that at 3D contrast-enhanced MR angiography without acceleration. Fifty dynamic scans were acquired at a temporal resolution of 608 msec per scan. The acquisition parameters for the sagittal T1-weighted 3D gradient-echo sequence were as follows: repetition time msec/echo time msec, 2.2/0.9; flip angle, 15°; rectangular field of view, 100%; slab thickness, 154 mm; image matrix, 224 x 178 over a 256-mm field of view; and 140 thin partitions of 1.1 mm, yielding an almost isotropic voxel size of 1.1 x 1.4 x 1.1 mm. In addition, a transverse T2-weighted fast spin-echo sequence (3277/80; section thickness, 5 mm; number of sections, 24) was performed as part of the diagnostic work-up.

Conventional Angiography
DSA was performed with a biplane system (Integris V5000; Philips Medical Systems). A 5-F vertebral catheter was navigated into the internal carotid, external carotid, and vertebral arteries by using a transfemoral route in 18 of 18 patients. The vascular territories were displayed separately in at least two projections, each by using manual injections of 5–7 mL of iopromide (Ultravist; Schering). The frame rate was 3 frames per second in the arterial and 2 frames per second in the venous phase. In addition, fast angiographic series (8 frames per second) were obtained to improve the determination of the enhancement of the cerebral AVM. DSA was performed by one radiologist (M.v.F., >10 years of experience) who was not involved in the reading of either the MR angiographic or the DSA images.

Image Analysis
Four-dimensional contrast-enhanced MR angiograms were independently reviewed by one neuroradiologist (H.U., >10 years of experience) and one neurosurgeon (B.M., >10 years of experience) at a separate workstation (Viewforum; Philips Medical Systems) according to the Spetzler-Martin classification, taking into account nidus size, eloquence of the adjacent brain region, and venous drainage (Table 1). In addition, arterial feeders of the cerebral AVM were evaluated.


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  		Table 1. Spetzler-Martin Scores

 
The readers were blinded to the patients' names and clinical histories and to results of other diagnostic procedures, including DSA. None of the DSA examinations were performed by one of the readers. Conventional angiograms were reviewed separately from 4D contrast-enhanced MR angiograms in a randomized order by one radiologist (W.A.W., >6 years of experience) who was unaware of the 4D contrast-enhanced MR angiographic results. In all patients, transverse T2-weighted fast spin-echo images were available for both MR angiographic and DSA readings to enable better localization of the nidus and evaluation of the eloquence of adjacent brain. T2-weighted imaging is part of the routine diagnostic work-up of patients with cerebral AVM who are undergoing DSA in our center, and T2-weighted images were therefore also included in the 4D contrast-enhanced MR angiographic protocol. Nidus size, arterial feeders, and venous drainage were assessed only on DSA and 4D contrast-enhanced MR angiographic images and not on T2-weighted images.

Overall diagnostic quality of 4D contrast-enhanced MR angiograms was scored according to the following five-point grading system:

Score of 5, excellent (feeding and draining vessels could clearly be depicted, no contrast enhancement was visible on the first dynamic image, and image quality was not impaired by artifacts).

Score of 4, good (sharp depiction of feeding arteries and draining veins was possible, but minor contrast enhancement was visible on the first dynamic image or minor artifacts were present but did not interfere with image interpretation).

Score of 3, adequate for diagnosis (depiction of feeding arteries and draining veins was possible, but contrast enhancement was visible on the first dynamic image and minor artifacts were present but did not interfere with image interpretation).

Score of 2, questionable for diagnosis (depiction of feeding arteries and draining veins was impaired by contrast enhancement on the first dynamic image and/or by artifacts).

Score of 1, nondiagnostic (image quality was not sufficient for diagnosing feeding arteries and draining veins because of contrast enhancement on the first dynamic image and/or because of artifacts).

In a second step, both readers were asked to indicate their level of confidence in determining the Spetzler-Martin classification of the cerebral AVM with 4D contrast-enhanced MR angiography by using a three-point scale: score of 3, confident; 2, questionable; 1, not confident. The level of confidence was determined separately before and after T2-weighted images were provided.

Statistical Analysis
The Kendall W coefficient of concordance was computed to compare the two readers in their assessment of image quality, level of confidence, and Spetzler-Martin classification with 4D contrast-enhanced MR angiography and to compare Spetzler-Martin classification as determined at DSA with that at 4D contrast-enhanced MR angiography. Kendall W coefficients (K) of 0.5–0.8 were considered to indicate good agreement, and coefficients higher than 0.8 were considered to indicate excellent agreement. A P value of less than .05 was considered to indicate a significant difference. All statistical analyses were performed with software (SPSS, version 11.0; SPSS, Chicago, Ill).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Image Quality and Level of Confidence
Four-dimensional contrast-enhanced MR angiography enabled clear depiction of arterial feeders and draining veins of cerebral AVM in accordance with DSA results (Figs 1, 2). Image quality of 4D contrast-enhanced MR angiography was judged by both readers to be excellent (score of 5), good (score of 4), or adequate for diagnosis (score of 3) in all patients. Image quality was not impaired by artifacts, such as ghosting, periodic artifacts inherent to parallel imaging, or areas of limited signal-to-noise ratio in any study. The average image quality score as judged by reader 1 (the neuroradiologist) was 3.5 ± 0.7 (range, 3–5) and that as judged by reader 2 (the neurosurgeon) was 3.5 ± 0.7 (range, 3–5), which yielded excellent interobserver agreement (K = 0.91, P = .020). On average, the level of confidence in grading cerebral AVM according to the Spetzler-Martin classification system was high for both readers, with an average level of confidence of 2.8 ± 0.4 (range, 2–3) for reader 1 and 2.7 ± 0.6 (range, 1–3) for reader 2. In 15 of 18 patients, the levels of confidence of Spetzler-Martin classifications as determined with 4D contrast-enhanced MR angiography by both readers matched, which yielded excellent interobserver agreement (K = 0.846, P = .037). In 17 of 18 (94%) patients, the inclusion of T2-weighted images with 4D contrast-enhanced MR angiograms had no effect on the level of confidence of the readers.


Figure 1A
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  		Figure 1a: Patient 1. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.3s = 7.3 seconds). (b,c,d) Transverse T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at selective DSA of left internal carotid artery. Images depict left parasagittal cerebral AVM (Spetzler-Martin grade, 2) with 2.7-cm nidus (black arrowheads), arterial feeder from pericallosal artery (white arrowheads), and venous drainage into superior sagittal sinus (white arrows) and straight sinus (black arrows).

 

Figure 1B
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  		Figure 1b: Patient 1. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.3s = 7.3 seconds). (b,c,d) Transverse T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at selective DSA of left internal carotid artery. Images depict left parasagittal cerebral AVM (Spetzler-Martin grade, 2) with 2.7-cm nidus (black arrowheads), arterial feeder from pericallosal artery (white arrowheads), and venous drainage into superior sagittal sinus (white arrows) and straight sinus (black arrows).

 

Figure 1C
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  		Figure 1c: Patient 1. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.3s = 7.3 seconds). (b,c,d) Transverse T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at selective DSA of left internal carotid artery. Images depict left parasagittal cerebral AVM (Spetzler-Martin grade, 2) with 2.7-cm nidus (black arrowheads), arterial feeder from pericallosal artery (white arrowheads), and venous drainage into superior sagittal sinus (white arrows) and straight sinus (black arrows).

 

Figure 1D
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  		Figure 1d: Patient 1. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.3s = 7.3 seconds). (b,c,d) Transverse T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at selective DSA of left internal carotid artery. Images depict left parasagittal cerebral AVM (Spetzler-Martin grade, 2) with 2.7-cm nidus (black arrowheads), arterial feeder from pericallosal artery (white arrowheads), and venous drainage into superior sagittal sinus (white arrows) and straight sinus (black arrows).

 

Figure 2A
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  		Figure 2a: Patient 3. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.9s = 7.9 seconds). (b) Transverse (left) and coronal (right) T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at DSA (selective catheterization of right vertebral artery). Images depict right occipital cerebral AVM (Spetzler-Martin grade, 2) with 2.0-cm nidus (black arrowheads), arterial feeders from calcarine and temporo-occipital artery (white arrowheads), and superficial venous drainage into transverse sinus (white arrows).

 

Figure 2B
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  		Figure 2b: Patient 3. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.9s = 7.9 seconds). (b) Transverse (left) and coronal (right) T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at DSA (selective catheterization of right vertebral artery). Images depict right occipital cerebral AVM (Spetzler-Martin grade, 2) with 2.0-cm nidus (black arrowheads), arterial feeders from calcarine and temporo-occipital artery (white arrowheads), and superficial venous drainage into transverse sinus (white arrows).

 

Figure 2C
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  		Figure 2c: Patient 3. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.9s = 7.9 seconds). (b) Transverse (left) and coronal (right) T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at DSA (selective catheterization of right vertebral artery). Images depict right occipital cerebral AVM (Spetzler-Martin grade, 2) with 2.0-cm nidus (black arrowheads), arterial feeders from calcarine and temporo-occipital artery (white arrowheads), and superficial venous drainage into transverse sinus (white arrows).

 

Figure 2D
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  		Figure 2d: Patient 3. (a) Three of 50 dynamic phases (with transverse [top], coronal [middle], and sagittal [bottom] maximum intensity projections) from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. Times refer to start of sequence (6.1s = 6.1 seconds, 6.7s = 6.7 seconds, 7.9s = 7.9 seconds). (b) Transverse (left) and coronal (right) T2-weighted fast spin-echo images (3277/80) and lateral views of (c) arterial phase and (d) venous phase at DSA (selective catheterization of right vertebral artery). Images depict right occipital cerebral AVM (Spetzler-Martin grade, 2) with 2.0-cm nidus (black arrowheads), arterial feeders from calcarine and temporo-occipital artery (white arrowheads), and superficial venous drainage into transverse sinus (white arrows).

 
Spetzler-Martin Classification
Average nidus size of cerebral AVM at 4D contrast-enhanced MR angiography was 2.5 cm ± 1.2 (range, 0.5–5.3 cm) for reader 1 and 2.3 cm ± 1.2 (range, 0.6–4.9 cm) for reader 2. Interobserver agreement of nidus size measurement was excellent (K = 0.955, P < .013).

Deep venous drainage was present in five of 18 patients, whereas in 13 of 18 patients, only superficial veins were involved in the drainage of the cerebral AVM (Table E1, radiology.rsnajnls.org/cgi/content/full/2453061684/DC1). The identification of venous drainage patterns of cerebral AVM (deep or superficial) at 4D contrast-enhanced MR angiography matched with that at DSA in 18 of 18 (100%) patients for both readers, which yielded 100% interobserver agreement (K = 1). In three patients (patients 9–11), additional superficially draining veins into the superior sagittal sinus and into the transverse sinus were identified at DSA. Depiction of an additional draining vein at DSA did not change the general interpretation of venous drainage pattern (superficial or deep) in any patient.

In 10 of 18 patients, both readers classified the cerebral AVM to be situated in eloquent brain areas. Judgment of the eloquence of adjacent brain regions matched in 18 of 18 (100%) patients with that at DSA for both readers, which yielded 100% interobserver agreement (K = 1). In two patients, the cerebral AVM was located in the area of language production (Broca area). According to the relevance of handedness with regard to eloquence, these patients were right handed, with the cerebral AVM in the left frontal gyrus ("left dominant").

Spetzler-Martin classifications (Table 2) of cerebral AVM with 4D contrast-enhanced MR angiography and those with DSA were as follows: grade of I, four patients; II, 11 patients; III, two patients; IV, one patient. Classification matched in 18 of 18 (100%) patients for both readers, which yielded 100% interobserver agreement (K = 1). There was 100% agreement between classifications based on 4D contrast-enhanced MR angiography and those based on DSA (K = 1).


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  		Table 2. Spetzler-Martin Scores at 4D Contrast-enhanced MR Angiography and DSA

 
In three of 18 patients, selective DSA led to the identification of additional small arterial feeders of the cerebral AVM that were retrospectively seen only on 4D contrast-enhanced MR angiograms (Figs 3, 4; Table E2, radiology.rsnajnls.org/cgi/content/full/2453061684/DC1). In one patient, an additional small aneurysm in the course of the feeding artery of a left cerebellar parasagittal cerebral AVM was visualized at 4D contrast-enhanced MR angiography and confirmed with DSA (Fig 3).


Figure 3A
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  		Figure 3a: Patient 2. (a) Anterior and (b) lateral views from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. (c) Sagittal T2-weighted fast spin-echo image (3277/80) and (d) anterior and (e) lateral DSA images (selective catheterization of left vertebral artery). Images show discrete left cerebellar parasagittal cerebral AVM (arrowheads) with additional aneurysm in posterior inferior cerebellar artery (arrows).

 

Figure 3B
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  		Figure 3b: Patient 2. (a) Anterior and (b) lateral views from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. (c) Sagittal T2-weighted fast spin-echo image (3277/80) and (d) anterior and (e) lateral DSA images (selective catheterization of left vertebral artery). Images show discrete left cerebellar parasagittal cerebral AVM (arrowheads) with additional aneurysm in posterior inferior cerebellar artery (arrows).

 

Figure 3C
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  		Figure 3c: Patient 2. (a) Anterior and (b) lateral views from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. (c) Sagittal T2-weighted fast spin-echo image (3277/80) and (d) anterior and (e) lateral DSA images (selective catheterization of left vertebral artery). Images show discrete left cerebellar parasagittal cerebral AVM (arrowheads) with additional aneurysm in posterior inferior cerebellar artery (arrows).

 

Figure 3D
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  		Figure 3d: Patient 2. (a) Anterior and (b) lateral views from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. (c) Sagittal T2-weighted fast spin-echo image (3277/80) and (d) anterior and (e) lateral DSA images (selective catheterization of left vertebral artery). Images show discrete left cerebellar parasagittal cerebral AVM (arrowheads) with additional aneurysm in posterior inferior cerebellar artery (arrows).

 

Figure 3E
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  		Figure 3e: Patient 2. (a) Anterior and (b) lateral views from T1-weighted 3D gradient-echo (2.2/0.9) sequence at 4D contrast-enhanced MR angiography. (c) Sagittal T2-weighted fast spin-echo image (3277/80) and (d) anterior and (e) lateral DSA images (selective catheterization of left vertebral artery). Images show discrete left cerebellar parasagittal cerebral AVM (arrowheads) with additional aneurysm in posterior inferior cerebellar artery (arrows).

 

Figure 4A
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  		Figure 4a: Patient 10. Lateral views from (a) T1-weighted 3D gradient-echo sequence at 4D contrast-enhanced MR angiography, (b) selective catheterization of left internal carotid artery at DSA, and (c) selective catheterization of left vertebral artery at DSA. Additional small arterial feeder from posterior cerebral artery (arrows) of left parasagittal cerebral AVM was depicted at DSA but not at 4D contrast-enhanced MR angiography. Main arterial feeder from middle cerebral artery (arrowheads) was depicted at 4D contrast-enhanced MR angiography and at DSA.

 

Figure 4B
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  		Figure 4b: Patient 10. Lateral views from (a) T1-weighted 3D gradient-echo sequence at 4D contrast-enhanced MR angiography, (b) selective catheterization of left internal carotid artery at DSA, and (c) selective catheterization of left vertebral artery at DSA. Additional small arterial feeder from posterior cerebral artery (arrows) of left parasagittal cerebral AVM was depicted at DSA but not at 4D contrast-enhanced MR angiography. Main arterial feeder from middle cerebral artery (arrowheads) was depicted at 4D contrast-enhanced MR angiography and at DSA.

 

Figure 4C
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  		Figure 4c: Patient 10. Lateral views from (a) T1-weighted 3D gradient-echo sequence at 4D contrast-enhanced MR angiography, (b) selective catheterization of left internal carotid artery at DSA, and (c) selective catheterization of left vertebral artery at DSA. Additional small arterial feeder from posterior cerebral artery (arrows) of left parasagittal cerebral AVM was depicted at DSA but not at 4D contrast-enhanced MR angiography. Main arterial feeder from middle cerebral artery (arrowheads) was depicted at 4D contrast-enhanced MR angiography and at DSA.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Several techniques for contrast-enhanced MR angiography of the brain-supplying vessels with a maximum temporal resolution of 1.5 seconds per dynamic image and 3D acquisition have been published (13,29–33). In our study, 4D contrast-enhanced MR angiography enabled 3D acquisition with a temporal resolution of 608 msec per dynamic image and a spatial resolution of 1.1 x 1.4 x 1.1 mm. To our knowledge, ours is the first study on 4D contrast-enhanced MR angiography and Spetzler-Martin classification that was performed with subsecond temporal and high spatial resolution in patients with cerebral AVM.

Two-dimensional single-thick-section techniques for time-resolved contrast-enhanced MR angiography have been reported to achieve high temporal resolution (34–38) at the expense of spatial resolution. Furthermore, postprocessing potentials inherent to acquisition of a full 3D data set are no longer available by using these methods. Summers et al (37) described a technique of two-dimensional contrast-enhanced MR angiography that achieved subsecond temporal resolution at 3.0 T by using parallel imaging (ie, sensitivity encoding). We agree that parallel imaging and high-field-strength imaging seem to be a good combination to accelerate temporal resolution at contrast-enhanced MR angiography. However, in the article by Summers and colleagues, spatial resolution was only 1.0 x 1.8 x 50–80 mm, and DSA correlation was not available. The authors concluded that two-dimensional projectional-view imaging might be sufficient because conventional angiography is usually also only a projectional technique. Although biplane DSA is still considered to be the reference standard in the diagnosis of cerebral AVM, its limits might be compensated by the selectivity of this imaging method when compared with that of noninvasive MR angiography. Three-dimensional rotational angiography has gained increasing interest as the new reference standard because it has been shown to be superior to two-dimensional DSA in many applications (39,40). However, the risks inherent to invasive conventional angiography remain at 3D rotational angiography.

In our study on noninvasive 4D contrast-enhanced MR angiography, the high temporal and high spatial resolution enabled 100% agreement with DSA with regard to the determination of the Spetzler-Martin grade of cerebral AVM. With regard to the Spetzler-Martin classification, the interobserver agreement achieved by using 4D contrast-enhanced MR angiography was excellent. The excellent interobserver agreement is particularly remarkable because some interobserver disagreement in Spetzler-Martin classification of cerebral AVM has been described at DSA (41). Even a small arterial aneurysm was correctly identified by both readers in our study. The detection of small aneurysms in the course of arterial feeders is known to be a limitation of contrast-enhanced MR angiography (38,42).

Nevertheless, the full number of arterial feeders was missed in three of 18 (17%) patients, while the correct Spetzler-Martin score was still preserved. There was no definable cutoff point for the depiction of arterial feeders because of limitations in spatial resolution. The depiction of arterial feeders was predominantly limited by the nonselectivity of the imaging technique (43). One way to further improve the selectivity of noninvasive MR angiography might be combining it with unenhanced methods, such as the arterial spin labeling with selective labeling pulses proposed by Golay et al (44).

Since 1993, when contrast-enhanced MR angiography was first introduced by Prince et al (45), there has always been a trade-off between spatial and temporal resolution at contrast-enhanced MR angiography in clinical applications. Parallel imaging has proved to enable substantial improvement in temporal resolution, as well as spatial resolution, at contrast-enhanced MR angiography (37,46–50). Although parallel imaging acceleration factors are limited at 1.5 T because of signal-to-noise limitations, this is less of an issue at high field strengths, where parallel imaging acceleration factors of more than eight have been successfully implemented (51). Furthermore, randomly segmented central k-space ordering (ie, CENTRA) has been proved to enable robust arterial phase MR angiography of the supraaortic arteries, despite acquisition times of more than 1 minute (25,28). Keyhole imaging at MR imaging was first introduced in 1996 by van Vaals et al (26). However, it seems that this method has gained increasing interest today only with the advent of both parallel imaging and high-field-strength imagers. Despite the well-known limitations of each of the techniques, the combination of them seems to be advantageous, especially at a field strength of 3.0 T (37,52). Three-dimensional time-resolved imaging of contrast kinetics (TRICKS) (53,54) and the time-resolved echo-shared angiography technique (50) are other methods that undersample k-space to achieve high temporal resolution. However, with TRICKS, the prediction of artifacts might be much more challenging, especially with contrast material injections at flow rates of 4 mL/sec and higher (55).

The combination of 4D contrast-enhanced MR angiography and T2-weighted imaging needs to be discussed. Theoretically, flow voids in vessels on T2-weighted images will provide some information on the vascular supply of cerebral AVMs; however, this information usually is not sufficient for reliable definition of the arterial feeders and venous drainage of cerebral AVMs (35). Hence, the additional dynamic information provided at DSA is necessary in most studies (35). In our study, the additional use of T2-weighted images did not increase the level of confidence of the readers of 4D contrast-enhanced MR angiograms in 17 of 18 (94%) patients. In our clinical practice, T2-weighted images are available for DSA readings in all patients with cerebral AVM because they generally provide an overview of the cerebral AVM in relation to the brain tissue and provide information about previous bleedings. The fact that the T2-weighted images can be acquired together with 4D contrast-enhanced MR angiography at the same examination may be considered an advantage of 4D contrast-enhanced MR angiography compared with DSA.

One possible clinical application of subsecond time-resolved 4D contrast-enhanced MR angiography may be the follow-up of patients with treated cerebral AVM. Follow-up of cerebral AVM after embolization (21) or radiosurgery (17,18) requires multiple DSA examinations (34) for nidus size, degree of occlusion and revascularization, circulation time, absence of former nidus vessels, and disappearance or normalization of draining veins (56). The dynamic information and the 3D visualization of our 4D contrast-enhanced MR angiographic technique may enable the replacement of some of the DSA follow-up examinations and a reduction of the frequency of conventional angiography in cerebral AVM (57). However, larger trials are still needed to prospectively evaluate the diagnostic accuracy of 4D contrast-enhanced MR angiography for both the diagnosis and the follow-up of patients with cerebral AVM as compared with these accuracies at DSA.

In conclusion, subsecond-temporal-resolution 4D contrast-enhanced MR angiography at 3.0 T is a promising noninvasive technique in the diagnostic work-up of patients with cerebral AVM and enabled the same Spetzler-Martin classification of cerebral AVM as that at DSA.


   ADVANCE IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 


   IMPLICATION FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
References
 


   FOOTNOTES
 

Abbreviations: AVM = arteriovenous malformation • CENTRA = contrast-enhanced timing-robust angiography • DSA = digital subtraction angiography • 4D = four-dimensional • 3D = three-dimensional

Guarantors of integrity of entire study, D.R.H., H.H.S., W.A.W.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, D.R.H., H.H.S., W.A.W.; clinical studies, all authors; statistical analysis, D.R.H., W.A.W.; and manuscript editing, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCE IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 

  1. Huston J 3rd, Fain SB, Wald JT, et al. Carotid artery: elliptic centric contrast-enhanced MR angiography compared with conventional angiography. Radiology 2001;218:138–143. [Abstract/Free Full Text]
  2. Willinek WA, von Falkenhausen M, Born M, et al. Noninvasive detection of steno-occlusive disease of the supra-aortic arteries with three-dimensional contrast-enhanced magnetic resonance angiography: a prospective, intra-individual comparative analysis with digital subtraction angiography. Stroke 2005;36:38–43. [Abstract/Free Full Text]
  3. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70-99%) or with mild (0-29%) carotid stenosis. European Carotid Surgery Trialists' Collaborative Group. Lancet 1991;337:1235–1243. [CrossRef][Medline]
  4. Robless P, Halliday A. Vascular surgical society of Great Britain and Ireland: carotid angiography is used more selectively in the asymptomatic carotid surgery trial. Br J Surg 1999;86:690–691. [Medline]
  5. Johnston DC, Chapman KM, Goldstein LB. Low rate of complications of cerebral angiography in routine clinical practice. Neurology 2001;57:2012–2014. [Abstract/Free Full Text]
  6. Komiyama M, Yamanaka K, Nishikawa M, Izumi T. Prospective analysis of complications of catheter cerebral angiography in the digital subtraction angiography and magnetic resonance era. Neurol Med Chir (Tokyo) 1998;38:534–539. [Medline]
  7. Earnest F, Forbes G, Sandok BA, et al. Complications of cerebral angiography: prospective assessment of risk. AJR Am J Roentgenol 1984;142:247–253. [Abstract/Free Full Text]
  8. Dion JE, Gates PC, Fox AJ, Barnett HJ, Blom RJ. Clinical events following neuroangiography: a prospective study. Stroke 1987;18:997–1004. [Abstract/Free Full Text]
  9. Heiserman JE, Dean BL, Hodak JA, et al. Neurologic complications of cerebral angiography. AJNR Am J Neuroradiol 1994;15:1401–1407. [Abstract]
  10. Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W. Neurologic complications of cerebral angiography: prospective analysis of 2899 procedures and review of the literature. Radiology 2003;227:522–528. [Abstract/Free Full Text]
  11. Han PP, Ponce FA, Spetzler RF. Intention-to-treat analysis of Spetzler-Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg 2003;98:3–7. [CrossRef][Medline]
  12. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg 1986;65:476–483. [Medline]
  13. Duran M, Schoenberg SO, Yuh WT, Knopp MV, van Kaick G, Essig M. Cerebral arteriovenous malformations: morphologic evaluation by ultrashort 3D gadolinium-enhanced MR angiography. Eur Radiol 2002;12:2957–2964. [Medline]
  14. Hartmann A, Stapf C, Hofmeister C, et al. Determinants of neurological outcome after surgery for brain arteriovenous malformation. Stroke 2000;31:2361–2364. [Abstract/Free Full Text]
  15. Lawton MT. Spetzler-Martin Grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery 2003;52:740–748. [CrossRef][Medline]
  16. Spetzler RF, Martin NA, Carter LP, Flom RA, Raudzens PA, Wilkinson E. Surgical management of large AVM's by staged embolization and operative excision. J Neurosurg 1987;67:17–28. [Medline]
  17. Meder JF, Oppenheim C, Blustajn J, et al. Cerebral arteriovenous malformations: the value of radiologic parameters in predicting response to radiosurgery. AJNR Am J Neuroradiol 1997;18:1473–1483. [Abstract]
  18. Oppenheim C, Meder JF, Trystram D, et al. Radiosurgery of cerebral arteriovenous malformations: is an early angiogram needed? AJNR Am J Neuroradiol 1999;20:475–481.
  19. Pollock BE, Flickinger JC. A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 2002;96:79–85. [Medline]
  20. Hartmann A, Pile-Spellman J, Stapf C, et al. Risk of endovascular treatment of brain arteriovenous malformations. Stroke 2002;33:1816–1820. [Abstract/Free Full Text]
  21. Gobin YP, Laurent A, Merienne L, et al. Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 1996;85:19–28. [Medline]
  22. Fasulakis S, Andronikou S. Comparison of MR angiography and conventional angiography in the investigation of intracranial arteriovenous malformations and aneurysms in children. Pediatr Radiol 2003;33:378–384. [Medline]
  23. Wintermark M, Dillon WP. Advanced CT and MR imaging techniques: an academic whim or a clinical standard in the making? AJNR Am J Neuroradiol 2006;27:1257. [Free Full Text]
  24. Todaka T, Hamada J, Kai Y, Morioka M, Ushio Y. Analysis of mean transit time of contrast medium in ruptured and unruptured arteriovenous malformations: a digital subtraction angiographic study. Stroke 2003;34:2410–2414. [Abstract/Free Full Text]
  25. Willinek WA, Gieseke J, Conrad R, et al. Randomly segmented central k-space ordering in high-spatial-resolution contrast-enhanced MR angiography of the supraaortic arteries: initial experience. Radiology 2002;225:583–588. [Abstract/Free Full Text]
  26. van Vaals JJ, Brummer ME, Dixon WT, et al. "Keyhole" method for accelerating imaging of contrast agent uptake. J Magn Reson Imaging 1993;3:671–675. [Medline]
  27. Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P. SENSE: sensitivity encoding for fast MRI. Magn Reson Med 1999;42:952–962. [CrossRef][Medline]
  28. Willinek WA, Gieseke J, von Falkenhausen M, et al. CE-3D MRA of the supraaortic arteries at 512 and 1024 matrix: the use of randomly segmented central k-space ordering (CENTRA) [abstr]. In: Proceedings of the 10th Meeting of the International Society for Magnetic Resonance in Medicine. Berkeley, Calif: International Society for Magnetic Resonance in Medicine, 2002.
  29. Farb RI, McGregor C, Kim JK, et al. Intracranial arteriovenous malformations: real-time auto-triggered elliptic centric-ordered 3D gadolinium-enhanced MR angiography—initial assessment. Radiology 2001;220:244–251. [Abstract/Free Full Text]
  30. Gauvrit JY, Oppenheim C, Nataf F, et al. Three-dimensional dynamic magnetic resonance angiography for the evaluation of radiosurgically treated cerebral arteriovenous malformations. Eur Radiol 2006;16:583–591. [CrossRef][Medline]
  31. Tsuchiya K, Aoki C, Fujikawa A, Hachiya J. Three-dimensional MR digital subtraction angiography using parallel imaging and keyhole data sampling in cerebrovascular diseases: initial experience. Eur Radiol 2004;14:1494–1497. [Medline]
  32. Wu Y, Goodrich KC, Buswell HR, Katzman GL, Parker DL. High-resolution time-resolved contrast-enhanced 3D MRA by combining SENSE with keyhole and SLAM strategies. Magn Reson Imaging 2004;22:1161–1168. [CrossRef][Medline]
  33. Ziyeh S, Strecker R, Berlis A, Weber J, Klisch J, Mader I. Dynamic 3D MR angiography of intra- and extracranial vascular malformations at 3T: a technical note. AJNR Am J Neuroradiol 2005;26:630–634. [Abstract/Free Full Text]
  34. Hans FJ, Reinges MH, Reipke P, Reinacher P, Krings T. Clinical applications of 2-D dynamic contrast-enhanced MR subtraction angiography in neurosurgery: preliminary results. Zentralbl Neurochir 2005;66:170–179. [CrossRef][Medline]
  35. Mori H, Aoki S, Okubo T, et al. Two-dimensional thick-slice MR digital subtraction angiography in the assessment of small to medium-size intracranial arteriovenous malformations. Neuroradiology 2003;45:27–33. [Medline]
  36. Nagaraja S, Capener D, Coley SC, et al. Brain arteriovenous malformations: measurement of nidal volume using a combination of static and dynamic magnetic resonance angiography techniques. Neuroradiology 2005;47:387–392. [CrossRef][Medline]
  37. Summers PE, Kollias SS, Valavanis A. Resolution improvement in thick-slab magnetic resonance digital subtraction angiography using SENSE at 3T. J Magn Reson Imaging 2004;20:662–673. [CrossRef][Medline]
  38. Warren DJ, Hoggard N, Walton L, et al. Cerebral arteriovenous malformations: comparison of novel magnetic resonance angiographic techniques and conventional catheter angiography. Neurosurgery 2001;48:973–982. [CrossRef][Medline]
  39. Anzalone N, Scomazzoni F, Castellano R, et al. Carotid artery stenosis: intraindividual correlations of 3D time-of-flight MR angiography, contrast-enhanced MR angiography, conventional DSA, and rotational angiography for detection and grading. Radiology 2005;236:204–213. [Abstract/Free Full Text]
  40. Elgersma OE, Wust AF, Buijs PC, van der GY, Eikelboom BC, Mali WP. Multidirectional depiction of internal carotid arterial stenosis: three-dimensional time-of-flight MR angiography versus rotational and conventional digital subtraction angiography. Radiology 2000;216:511–516. [Abstract/Free Full Text]
  41. Du R, Dowd CF, Johnston SC, Young WL, Lawton MT. Interobserver variability in grading of brain arteriovenous malformations using the Spetzler-Martin system. Neurosurgery 2005;57:668–675. [CrossRef][Medline]
  42. Griffiths PD, Hoggard N, Warren DJ, Wilkinson ID, Anderson B, Romanowski CA. Brain arteriovenous malformations: assessment with dynamic MR digital subtraction angiography. AJNR Am J Neuroradiol 2000;21:1892–1899. [Abstract/Free Full Text]
  43. Bos C, Smits HF, Bakker CJ, Viergever MA. Selective contrast-enhanced MR angiography. Magn Reson Med 2000;44:575–582. [CrossRef][Medline]
  44. Golay X, Petersen ET, Hui F. Pulsed star labeling of arterial regions (PULSAR): a robust regional perfusion technique for high field imaging. Magn Reson Med 2005;53:15–21. [CrossRef][Medline]
  45. Prince MR, Yucel EK, Kaufman JA, Harrison DC, Geller SC. Dynamic gadolinium-enhanced three-dimensional abdominal MR arteriography. J Magn Reson Imaging 1993;3:877–881. [Medline]
  46. Born M, Willinek WA, Gieseke J, von Falkenhausen M, Schild H, Kuhl CK. Sensitivity encoding (SENSE) for contrast-enhanced 3D MR angiography of the abdominal arteries. J Magn Reson Imaging 2005;22:559–565. [CrossRef][Medline]
  47. Weiger M, Pruessmann KP, Kassner A, et al. Contrast-enhanced 3D MRA using SENSE. J Magn Reson Imaging 2000;12:671–677. [CrossRef][Medline]
  48. Maki JH, Wilson GJ, Eubank WB, Hoogeveen RM. Utilizing SENSE to achieve lower station sub-millimeter isotropic resolution and minimal venous enhancement in peripheral MR angiography. J Magn Reson Imaging 2002;15:484–491. [CrossRef][Medline]
  49. Michaely HJ, Herrmann KA, Kramer H, et al. High-resolution renal MRA: comparison of image quality and vessel depiction with different parallel imaging acceleration factors. J Magn Reson Imaging 2006;24:95–100. [CrossRef][Medline]
  50. Fink C, Ley S, Kroeker R, Requardt M, Kauczor HU, Bock M. Time-resolved contrast-enhanced three-dimensional magnetic resonance angiography of the chest: combination of parallel imaging with view sharing (TREAT). Invest Radiol 2005;40:40–48. [Medline]
  51. Willinek WA, Gieseke J, Hadizadeh DR, et al. Contrast-enhanced supraaortic MRA at 3.0T using 8-channel and 16-channel neurovascular coils and parallel acquisition with acceleration factors ranging from 1 to 9 [abstr]. In: Proceedings of the 14th Meeting of the International Society for Magnetic Resonance in Medicine. Berkeley, Calif: International Society for Magnetic Resonance in Medicine, 2006; 567.
  52. Cashen TA, Carr JC, Shin W, et al. Intracranial time-resolved contrast-enhanced MR angiography at 3T. AJNR Am J Neuroradiol 2006;27:822–829. [Abstract/Free Full Text]
  53. Mazaheri Y, Carroll TJ, Du J, et al. Combined time-resolved and high-spatial-resolution 3D MRA using an extended adaptive acquisition. J Magn Reson Imaging 2002;15:291–301. [CrossRef][Medline]
  54. Korosec FR, Frayne R, Grist TM, Mistretta CA. Time-resolved contrast-enhanced 3D MR angiography. Magn Reson Med 1996;36:345–351. [Medline]
  55. Madore B, Pelc NJ. New approach to 3D time-resolved angiography. Magn Reson Med 2002;47:1022–1025. [CrossRef][Medline]
  56. Karlsson B, Lindquist C, Steiner L. Prediction of obliteration after gamma knife surgery for cerebral arteriovenous malformations. Neurosurgery 1997;40:425–430. [CrossRef][Medline]
  57. Shim YW, Chung TS, Kang WS, Joo JY, Strecker R, Hennig J. Non-invasive follow-up evaluation of post-embolized AVM with time-resolved MRA: a case report. Korean J Radiol 2002;3:271–275. [Medline]




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