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Yasuhiko Iryo, MD Toshinori Hirai, MD Yutaka Kai, MD Masanobu Nakamura, RT Yoshinori Shigematsu, MD Mika Kitajima, MD Minako Azuma, MD Masanori Komi, RT Kosuke Morita, RT Yasuyuki Yamashita, MD
Purpose:
To evaluate whether 3-T four-dimensional (4D) arterial spin-labeling (ASL)–based magnetic resonance (MR) angiography is useful for the evaluation of shunt lesions in patients with intracranial dural arteriovenous fistulas (AVFs).
Materials and Methods:
Institutional review board approval and prior written informed consent from all patients were obtained. Nine patients with intracranial dural AVF (seven men, two women; age range, 52–77 years; mean age, 63 years) underwent 4D ASL MR angiography at 3 T and digital subtraction angiography (DSA). Spin tagging was with flow-sensitive alternating inversion recovery with Look-Locker sampling. At 300-millisecond intervals, seven dynamic images with a spatial resolution of 0.5 3 0.5 3 0.6 mm3 were obtained. The 4D ASL MR angiographic and DSA images were read by two sets of two independent readers each. Interobserver and intermodality agreement was assessed with the k statistic.
Results:
On all 4D ASL MR angiographic images, the major intracranial arteries were demonstrated at a temporal resolution of 300 milliseconds. Interobserver agreement was excellent for the fistula site (k = 1.00; 95% confidence interval [CI]: 1.00, 1.00), moderate for the main arterial feeders (k = 0.53; 95% CI: 0.08, 0.98), and good for venous drainage (k = 0.77; 95% CI: 0.35, 1.00). Intermodality agreement was excellent for the fistula site and venous drainage (k = 1.00; 95% CI: 1.00, 1.00) and good for the main arterial feeders (k = 0.80; 95% CI: 0.58, 1.00).
Conclusion:
The good-to-excellent agreement between 3-T 4D ASL MR angiographic and DSA findings suggests that 3-T 4D ASL MR angiography is a useful tool for the evaluation of intracranial dural AVFs. RSNA, 2013
q
1
From the Departments of Diagnostic Radiology (Y.I., T.H., Y.S., M. Kitajima, M.A., Y.Y.), and Neurosurgery (Y.K.), Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Kumamoto 860-8556 Japan; Medical Satellite Yaesu Clinic, Tokyo, Japan (M.N.); and Kumamoto University Hospital, Kumamoto, Japan (M. Komi, K.M.). Received December 4, 2012; revision requested January 9, 2013; final revision received June 24; accepted July 8; final version accepted September 27. Address correspondence to Y.I. (e-mail: [email protected]). RSNA, 2013
q
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Original Research n Neuroradiology
Intracranial Dural Arteriovenous Fistulas: Evaluation with 3-T Four-dimensional MR Angiography Using Arterial Spin Labeling1
NEURORADIOLOGY: Evaluation of Intracranial Dural Arteriovenous Fistulas
T
he high spatial and temporal resolution of intraarterial digital subtraction angiography (DSA) facilitates the accurate assessment of intracranial dural arteriovenous fistulas (AVFs) and their location, as well as the identification of their feeders and drainers. DSA, however, is an invasive method that involves exposure to radiation and requires the injection of iodinated contrast medium. Therefore, a noninvasive method is required to diagnose AVFs and follow up patients with intracranial dural AVFs. Three-dimensional (3D) time-offlight magnetic resonance (MR) angiography and its source images are widely used for the assessment of intracranial dural AVFs (1,2). The lack of hemodynamic information, however, limits their clinical usefulness (2–4). While four-dimensional (4D) contrast material–enhanced MR angiography at 3 T appears to be reliable and provides hemodynamic information on intracranial dural AVFs (5), it poses risks associated with contrast agents (6). Although various techniques for time-resolved arterial spin-labeling (ASL)–based MR angiography have been reported (7–10), limitations such as low spatial resolution, short imaging coverage, and long acquisition times hamper their clinical application. Nakamura et al (11) developed a 3D volumetric nonenhanced time-resolved MR
Advances in Knowledge nn On 3-T four-dimensional (4D) arterial spin-labeling (ASL)– based MR angiographic images, the intracranial arteries are visualized at high spatial (0.5 3 0.5 3 0.6 mm3) and temporal (300 milliseconds) resolution without exogenous contrast agents. nn In the evaluation of intracranial dural arteriovenous fistulas (AVFs), intermodality agreement between 4D ASL MR angiographic and DSA findings was excellent for the fistula site and venous drainage (k = 1.00) and good for the main arterial feeders (k = 0.80). 194
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angiographic technique termed contrast inherent inflow-enhanced multiphase angiography combining multiple-phase flow-sensitive alternating inversion recovery (CINEMA-FAIR). This 4D ASLbased MR angiographic technique makes possible the sequential observation of hemodynamics similar to DSA and facilitates large 3D volume acquisition. To date, no systematic studies with the use of the 4D ASL MR angiographic technique in healthy subjects and patients with intracranial dural AVFs have been reported. The aim of our study was to compare prospectively the agreement between 3-T 4D ASL MR angiography and DSA for the characterization of intracranial dural AVFs.
Materials and Methods Study Population Our institutional review board approved this study; prior informed consent for the imaging studies was obtained from all patients. Patients were searched and recruited from our local database from May 2011 to June 2013 in Kumamoto University Hospital (Kumamoto, Japan). The inclusion criteria were that the patients had intracranial dural AVFs and underwent both 4D ASL MR angiography and DSA. The exclusion criteria were that the patients had a history of surgery in the brain, had an allergy for iodinated contrast agents or renal dysfunction, and had emergency cases. Nine patients (seven men, two women; age range, 52–77 years; mean age, 63.4 years) with intracranial dural AVFs fulfilled the selection criteria. Their primary presenting symptoms were visual disturbance in five patients, Implication for Patient Care nn Four-dimensional ASL-based magnetic resonance MR angiographic imaging at 3 T may be used as the primary diagnostic tool in patients who are suspected of having an intracranial dural AVF and in subsequent follow-up examinations.
tinnitus in two, and headache and disorientation in one each.
Four-dimensional ASL MR Angiographic Technique All MR studies were performed with a 3-T MR imaging system (Achieva; Philips Medical Systems, Best, the Netherlands) and a commercially available 32-channel head coil. The MR imaging unit featured a gradient system with a maximal achievable gradient amplitude of 40 mT/m and a slew rate of 200 T/m/sec. Four-dimensional ASL MR angiography was performed with the CINEMA-FAIR technique that combines ASL with a 3D segmented T1-weighted turbo field-echo sequence (11). The flow-sensitive alternating inversion-recovery method with Look-Locker sampling was used for spin tagging (12). The pulse sequence diagram of the CINEMA-FAIR technique is shown in Figure 1. The sequence was composed of two acquisitions with identical readout and different magnetization preparation schemes; measurements were in two consecutive acquisitions preceded by nonselective (global) and spatially selective inversion pulses (11). Prior Published online before print 10.1148/radiol.13122670 Content codes: Radiology 2014; 271:193–199 Abbreviations: ASL = arterial spin labeling AVF = arteriovenous fistula CI = confidence interval CINEMA-FAIR = contrast inherent inflow-enhanced multiphase angiography combining multiple-phase flowsensitive alternating inversion recovery DSA = digital substraction angiography 4D = four-dimensional 3D = three-dimensional TI = inversion time Author contributions: Guarantor of integrity of entire study, T.H.; study concepts/ study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, Y.I., M.A.; clinical studies, Y.I., T.H., Y.K., M.N., Y.S., M. Kitajima, M.A., M. Komi, K.M.; statistical analysis, Y.I., M.A.; and manuscript editing, Y.I., T.H., M.A., Y.Y. Conflicts of interest are listed at the end of this article.
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Figure 1
Figure 1: (a) Pulse sequence diagram of the CINEMA-FAIR technique. It consists of a flow-sensitive alternating inversion-recovery– based ASL sequence: global and spatially selective 180° pulses. A segmented 3D T1-weighted (T1) gradient-echo sequence (3D T1-weighted turbo field echo [TFE]) is acquired after global or selective 180° pulses. This cycle is repeated for the number of shots of the gradient-echo sequence. Look-Locker sampling with multiple inversion times (TIs) was used after each 180° pulse to obtain timeresolved MR angiographic images. This makes possible the visualization of virtual dynamic filling by flowing blood. After completion of the two acquisitions, the corresponding temporal phases with identical inversion delays were subtracted. a = Excitation pulse, N = arbitrary number. (b) Schematic labeling geometry shows global (acquisition 1) and selective (acquisition 2) labeling regions and their subtraction images.
to the T1-weighted turbo field-echo readout of the first acquisition, a nonselective inversion pulse was applied. For the second acquisition, a spatially selective inversion pulse was applied to the selectively labeled imaging volume. After completion of the two acquisitions, corresponding temporal phases of the two acquisitions with identical inversion delays were subtracted (11). Maximum intensity projection was then performed for each temporal phase of the subtracted data sets. Since multiple measurements with different TIs were conducted, sequential angiographic images were obtained. The parameters for the CINEMAFAIR sequence were as follows: repetition time msec/echo time msec, 4.5/2.2; flip angle, 10°; field of view, 200 3 200 mm2; matrix, 192 3 192;
section thickness, 1 mm; slab thickness, 100 mm; reconstructed spatial resolution, 0.5 3 0.5 3 0.6 mm3; sensitivity encoding factor, 3.0; TI, DTI, and final TI, 80 milliseconds, 300 milliseconds, and 2.0 seconds, respectively; number of acquisition phases, seven; and acquisition time, 8 minutes 26 seconds.
DSA Technique An experienced neuroradiologist and neurosurgeon performed diagnostic biplanar intraarterial DSA (Allura Xper FD; Philips Medical Systems, Best, the Netherlands). Vascular access was acquired by using the transfemoral approach and the Seldinger technique. The vascular anatomy was evaluated by using DSA combined with the manual injection (6–10 mL) of iodinated contrast medium (iopamidol, Iopamiron
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300; Bayer-Schering, Berlin, Germany) into the external and internal carotid arteries and the vertebral arteries. The image matrix and field of view were 1024 3 1024 and 170 3 170 mm2, respectively; the temporal resolution was 3 frames per second. DSA was performed within 7 days of 4D ASL MR angiography, as a rule.
Image Analysis At a picture archiving and communication system workstation, two neuroradiologists (Y.S. and M. Kitajima, with 17 and 19 years of experience in neuroradiology, respectively) independently assessed the entire sets of DSA images. Two other observers (Y.I. and T.H., with 7 and 22 years of experience in neuroradiology, respectively) independently assessed the 4D ASL MR 195
NEURORADIOLOGY: Evaluation of Intracranial Dural Arteriovenous Fistulas
angiographic images at a picture archiving and communication system workstation. They used a four-point grading system to score the overall image quality, as follows: grade 1, nondiagnostic quality due to severe artifacts; grade 2, quality with artifacts that may interfere with the diagnosis; grade 3, quality with artifacts that do not interfere with the diagnosis; and grade 4, diagnostic quality without artifacts. Then they independently evaluated the 4D ASL MR angiographic findings in regard to dural AVFs; they were blinded to clinical information and the DSA findings. On the 3D data display, all regions were visible. The observers were allowed to enlarge regions of special interest in any direction. The observers looked for the dural AVF site, the main arterial feeder, and the venous drainage on 4D ASL MR angiographic and DSA images (5). The site of the dural AVF was identified as the transverse-sigmoid sinus, the cavernous sinus, the superior sagittal sinus, or as other; the main feeders were identified as originating at the internal maxillary artery and/or the middle meningeal artery, at the ascending pharyngeal artery, at the occipital artery, at the internal carotid artery, or as at other arteries. On the basis of the classification of Borden et al (13), dural AVF drainage was recorded as type 1 (drainage directly into the dural venous sinus), type 2 (drainage into the dural venous sinus with cortical venous reflux), or type 3 (drainage directly into the subarachnoid veins [cortical venous reflux only]). Differences in their assessments were resolved in consensus.
Statistical Analysis Interobserver agreement for 4D ASL MR angiography with respect to overall image quality was determined by calculating the k coefficient (k , 0.20, poor agreement; k = 0.21–0.40, fair agreement; k = 0.41–0.60, moderate agreement; k = 0.61–0.80, good agreement; k = 0.81–0.90, very good agreement; and k . 0.90, excellent agreement) (5). Interobserver and intermodality agreement for dural AVF assessments 196
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was determined by calculating the k coefficient. We also recorded the number and percentage of times when interobserver and intermodality assessments were in exact agreement. A software package (Med-Calc for Windows; MedCalc Software, Mariakerke, Belgium) was used for all analyses.
Results Both observers judged the overall image quality on 4D ASL MR angiographic images of the nine dural AVFs to be without artifacts and of diagnostic quality (grade 4) (Fig 2). In the qualitative evaluation of DSA images, interobserver agreement was excellent for all items (k = 1.00; 95% confidence interval [CI]: 1.00, 1.00). The Table summarizes the 4D ASL MR angiographic and DSA findings in the nine dural AVFs; four were transversesigmoid sinus fistulas, three were cavernous sinus fistulas, and one was a superior sagittal sinus fistula; the other was located at the sphenoparietal sinus. On DSA images, four dural AVFs were primarily supplied by the occipital artery, three were supplied by the internal carotid artery, and one each was supplied by the internal maxillary artery and/or middle meningeal artery and by the ascending pharyngeal artery. Venous drainage on DSA images was type 1 in five patients and type 2 in four patients. There were no patients with type 3 drainage. With respect to the fistula site, the two observers reviewing 4D ASL MR angiographic images agreed in all nine assessment studies; interobserver agreement was excellent (k = 1.00; 95% CI: 1.00, 1.00). The observers of 4D ASL MR angiographic and DSA images agreed with respect to the site of all nine fistulas (Fig 2). Intermodality agreement was excellent (k = 1.00; 95% CI: 1.00, 1.00) (Table). In the analysis of the main arterial feeders, the two readers reviewing 4D ASL MR angiographic images agreed in seven of nine dural AVFs (78%); interobserver agreement was moderate (k = 0.53; 95% CI: 0.08, 0.98). Similarly, in seven of nine dural AVFs (78%), 4D
ASL MR angiographic (consensus readings) and DSA agreed on the main arterial feeders; intermodality agreement was good (k = 0.80; 95% CI: 0.58, 1.00) (Table, Fig 2). In eight of nine patients (89%) both observers reviewing 4D ASL MR angiographic images agreed in their assessment of venous drainage. Interobserver agreement was good (k = 0.77; 95% CI: 0.35, 1.00) (Table, Fig 2). With both imaging modalities, there was agreement on the drainage pattern in all nine patients (Fig 2); intermodality agreement was therefore recorded as excellent (k = 1.00; 95% CI: 1.00, 1.00) (Table).
Discussion Our study findings indicated that 4D ASL MR angiography at 3 T was a useful diagnostic tool for the characterization of intracranial dural AVFs. Agreement between 4D ASL MR angiographic and DSA findings was excellent for the fistula site and the type of venous drainage and good for the main arterial feeders. We attribute this result to the combined effect of several factors: the long T1-weighted relaxation times and the high signal-to-noise ratio on 3-T MR images and our use of a 32-channel head coil. With these techniques, we were able to obtain high spatial and temporal resolution of 0.5 3 0.5 3 0.6 mm3 and 0.3 second per volume, respectively. With regard to 4D MR angiography, there are two different techniques (ie, 4D contrast-enhanced MR angiographic and 4D ASL MR angiographic methods. Although 4D contrast-enhanced MR angiography at 3 T has been reported to be a reliable technique that provides hemodynamic information on intracranial dural AVFs (5), it poses risks associated with contrast agents (6). Because 4D ASL MR angiography is based on ASL techniques, it does not require the use of gadolinium-based contrast agents, thereby avoiding the risk for nephrogenic systemic fibrosis. Therefore, 4D ASL MR angiography may be especially useful in patients with renal dysfunction and in children in whom the rapid
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Figure 2 Figure 2: MR images in a 75-year-old man with dural AVF at the left transverse-sigmoid sinus. (a) Anteroposterior (top), lateral (middle), and axial (bottom) maximum intensity projections of 4D ASLbased MR angiographic images (4.5/2.2, 10° flip angle). The temporal resolution is 300 milliseconds. The left transverse-sigmoid sinus is depicted early in the early arterial to the arterial phase. The site of the dural AVF (thick arrows) appears to be the left transverse-sigmoid sinus. The left occipital artery has a large caliber and is well visualized from the early arterial phase (arrowheads). The posterior meningeal artery is also depicted (thin arrows). Retrograde cortical venous drainage is seen from the left transverse sinus (dotted circle). On the basis of these findings, both observers judged that the left transverse-sigmoid sinus was the fistula site, that this dural AVF was primarily fed by the occipital artery, and that venous drainage was type 2. (b) Anteroposterior (top) and lateral (bottom) projections of DSA images of the left external carotid artery in the same patient. DSA shows an arteriovenous shunt (arrows) at the left transverse-sigmoid sinus. It is supplied by branches from the left occipital artery (arrowheads). Retrograde cortical venous drainage is from the left transverse sinus (dotted circles).
intravenous injection of a bolus of contrast material may be difficult. In addition, 4D contrast-enhanced MR angiography is not a reliable tool for assessing
main arterial feeders of dural AVFs (5). On the basis of the results of our current study, agreement between 4D ASL MR angiographic findings and DSA
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findings was good for the main arterial feeders. In assessment of main arterial feeders, intermodality agreement might be better for 4D ASL MR angiography than for 4D contrast-enhanced MR angiography. This idea is probably a consequence of the difference between the spatial and temporal resolution of these techniques (ie, 0.5 3 0.5 3 0.6 mm3 and 0.3 second per volume for 4D ASL MR angiography and 1.0 3 1.0 3 1.5 mm3 and 1.9 seconds per volume for 4D contrast-enhanced MR angiography [5], respectively). While time-resolved ASL-based MR angiographic techniques (eg, true fast imaging with steady-state precession– based spin tagging with alternating radiofrequency, or True STAR; timeresolved vessel-selective digital subtraction MR angiography, or DSMRA; and time-spatial labeling inversion pulse, or Time-SLIP, MR DSA methods) have been reported (8–10), they are of limited value because of low spatial resolution, short imaging coverage, or long acquisition times (maximum, 197
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Summary of 4D ASL MR Angiographic and DSA Findings 4D ASL MR Angiography Clinical Data Fistula site Transverse-sigmoid sinus Cavernous sinus Superior sagittal sinus Others Main arterial feeder Internal mammary artery and/or middle meningeal artery Ascending pharyngeal artery Occipital artery Internal carotid artery Others Drainage pattern Type 1‡ Type 2§ Type 3||
Observer 1
Observer 2
Interobserver Agreement*
DSA
4D ASL MR Angiography†
Intermodality Agreement*
4 3 1 1
4 3 1 1
1.00 (1.00, 1.00) ... ... ...
4 3 1 1
4 3 1 1
1.00 (1.00, 1.00) ... ... ...
0
0
0.53 (0.08, 0.98)
1
0
0.80 (0.58, 1.00)
2 3 4 0
0 4 5 0
... ... ... ...
1 4 3 0
0 4 5 0
... ... ... ...
6 3 0
5 4 0
0.77 (0.35, 1.00) ... ...
5 4 0
5 4 0
1.00 (1.00, 1.00) ... ...
* Data are k statistics, and numbers in parentheses are 95% CIs. †
Consensus reading of the two observers.
‡
Venous drainage directly into the dural venous sinus.
§
Venous drainage into the dural venous sinus with cortical venous reflux.
||
Venous drainage directly into the subarachnoid veins (cortical reflux only).
45–60 minutes), or all three. These disadvantages hamper their clinical usefulness for the evaluation of dural AVFs. On the other hand, 4D ASL MR angiography with CINEMA-FAIR offers the advantage of higher spatial and temporal resolution, larger image coverage, and shorter acquisition times (approximately 7–9 minutes). In addition, image data consist of isotropic voxels that allow loss-free reformatting, an important factor in the assessment of complex vascular structures such as dural AVFs. Our study had some limitations. Because we performed a single-center study that involved a small number of patients, we were unable to determine whether 4D ASL MR angiography and DSA are of equal diagnostic value. Second, only arterial phase images were obtained and evaluated at 4D ASL MR angiographic imaging. This factor was due to the short T1 decay (approximately 2 seconds) of the magnetically labeled water. However, this limitation might be advantageous for 198
the evaluation of arteriovenous shunt lesions. Third, we did not determine the number of feeders and drainers of the nine dural AVFs. Feeders other than the main feeders were not evaluated because 4D ASL MR angiography did not fully depict small-caliber feeding vessels. Because the size of voxels on 4D ASL MR angiographic images may be larger than the diameter of the arterial dural AVF feeders, the spatial resolution of these images may not be high enough to depict small feeders. In conclusion, on 3-T 4D ASL MR angiographic images, the intracranial arteries are visualized at high spatial and temporal resolution without exogenous contrast agents. The good-toexcellent agreement between 3 T 4D ASL MR angiographic and DSA findings suggests that 3-T 4D ASL MR angiography is a useful tool for the evaluation of intracranial dural AVFs. Further studies on larger populations are needed to clarify the clinical role of 3-T 4D ASL MR angiography in patients with intracranial dural AVFs.
Disclosures of Conflicts of Interest: Y.I. No relevant conflicts of interest to disclose. T.H. No relevant conflicts of interest to disclose. Y.K. No relevant conflicts of interest to disclose. M.N. No relevant conflicts of interest to disclose. Y.S. No relevant conflicts of interest to disclose. M. Kitajima No relevant conflicts of interest to disclose. M.A. No relevant conflicts of interest to disclose. M. Komi No relevant conflicts of interest to disclose. K.M. No relevant conflicts of interest to disclose. Y.Y. No relevant conflicts of interest to disclose.
References 1. Chen JC, Tsuruda JS, Halbach VV. Suspected dural arteriovenous fistula: results with screening MR angiography in seven patients. Radiology 1992;183(1):265–271. 2. Hirai T, Korogi Y, Hamatake S, et al. Threedimensional FISP imaging in the evaluation of carotid cavernous fistula: comparison with contrast-enhanced CT and spin-echo MR. AJNR Am J Neuroradiol 1998;19(2):253– 259. 3. Ouanounou S, Tomsick TA, Heitsman C, Holland CK. Cavernous sinus and inferior petrosal sinus flow signal on three-dimensional time-of-flight MR angiography. AJNR Am J Neuroradiol 1999;20(8):1476–1481.
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4. Watanabe K, Kakeda S, Watanabe R, Ohnari N, Korogi Y. Normal flow signal of the pterygoid plexus on 3T MRA in patients without DAVF of the cavernous sinus. AJNR Am J Neuroradiol 2013;34(6):1232– 1236. 5. Nishimura S, Hirai T, Sasao A, et al. Evaluation of dural arteriovenous fistulas with 4D contrast-enhanced MR angiography at 3T. AJNR Am J Neuroradiol 2010;31(1):80– 85.
8. Yan L, Wang S, Zhuo Y, et al. Unenhanced dynamic MR angiography: high spatial and temporal resolution by using true FISPbased spin tagging with alternating radiofrequency. Radiology 2010;256(1):270–279. 9. Robson PM, Dai W, Shankaranarayanan A, Rofsky NM, Alsop DC. Time-resolved vesselselective digital subtraction MR angiography of the cerebral vasculature with arterial spin labeling. Radiology 2010;257(2):507–515.
6. Yang L, Krefting I, Gorovets A, et al. Nephrogenic systemic fibrosis and class labeling of gadolinium-based contrast agents by the Food and Drug Administration. Radiology 2012;265(1):248–253.
10. Hori M, Aoki S, Oishi H, et al. Utility of time-resolved three-dimensional magnetic resonance digital subtraction angiography without contrast material for assessment of intracranial dural arterio-venous fistula. Acta Radiol 2011;52(7):808–812.
7. Miyazaki M, Lee VS. Nonenhanced MR angiography. Radiology 2008;248(1):20–43.
11. Nakamura M, Yoneyama M, Okuaki T, et al. Contrast 3D volumetric time-resolved MRA
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combining multiple phase FAIR (CINEMAFAIR) [abstr]. In: Proceedings of the Nineteenth Meeting of the International Society for Magnetic Resonance in Medicine. Berkeley, Calif: International Society for Magnetic Resonance in Medicine, 2011; 4036. 12. Günther M, Bock M, Schad LR. Arterial spin labeling in combination with a LookLocker sampling strategy: inflow turbosampling EPI-FAIR (ITS-FAIR). Magn Reson Med 2001;46(5):974–984. 13. Borden JA, Wu JK, Shucart WA. A pro posed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 1995;82(2):166–179.
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Yasuhiko Iryo, MD Toshinori Hirai, MD Yutaka Kai, MD Masanobu Nakamura, RT Yoshinori Shigematsu, MD Mika Kitajima, MD Minako Azuma, MD Masanori Komi, RT Kosuke Morita, RT Yasuyuki Yamashita, MD
Purpose:
To evaluate whether 3-T four-dimensional (4D) arterial spin-labeling (ASL)–based magnetic resonance (MR) angiography is useful for the evaluation of shunt lesions in patients with intracranial dural arteriovenous fistulas (AVFs).
Materials and Methods:
Institutional review board approval and prior written informed consent from all patients were obtained. Nine patients with intracranial dural AVF (seven men, two women; age range, 52–77 years; mean age, 63 years) underwent 4D ASL MR angiography at 3 T and digital subtraction angiography (DSA). Spin tagging was with flow-sensitive alternating inversion recovery with Look-Locker sampling. At 300-millisecond intervals, seven dynamic images with a spatial resolution of 0.5 3 0.5 3 0.6 mm3 were obtained. The 4D ASL MR angiographic and DSA images were read by two sets of two independent readers each. Interobserver and intermodality agreement was assessed with the k statistic.
Results:
On all 4D ASL MR angiographic images, the major intracranial arteries were demonstrated at a temporal resolution of 300 milliseconds. Interobserver agreement was excellent for the fistula site (k = 1.00; 95% confidence interval [CI]: 1.00, 1.00), moderate for the main arterial feeders (k = 0.53; 95% CI: 0.08, 0.98), and good for venous drainage (k = 0.77; 95% CI: 0.35, 1.00). Intermodality agreement was excellent for the fistula site and venous drainage (k = 1.00; 95% CI: 1.00, 1.00) and good for the main arterial feeders (k = 0.80; 95% CI: 0.58, 1.00).
Conclusion:
The good-to-excellent agreement between 3-T 4D ASL MR angiographic and DSA findings suggests that 3-T 4D ASL MR angiography is a useful tool for the evaluation of intracranial dural AVFs. RSNA, 2013
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From the Departments of Diagnostic Radiology (Y.I., T.H., Y.S., M. Kitajima, M.A., Y.Y.), and Neurosurgery (Y.K.), Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Kumamoto 860-8556 Japan; Medical Satellite Yaesu Clinic, Tokyo, Japan (M.N.); and Kumamoto University Hospital, Kumamoto, Japan (M. Komi, K.M.). Received December 4, 2012; revision requested January 9, 2013; final revision received June 24; accepted July 8; final version accepted September 27. Address correspondence to Y.I. (e-mail: [email protected]). RSNA, 2013
q
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Original Research n Neuroradiology
Intracranial Dural Arteriovenous Fistulas: Evaluation with 3-T Four-dimensional MR Angiography Using Arterial Spin Labeling1
NEURORADIOLOGY: Evaluation of Intracranial Dural Arteriovenous Fistulas
T
he high spatial and temporal resolution of intraarterial digital subtraction angiography (DSA) facilitates the accurate assessment of intracranial dural arteriovenous fistulas (AVFs) and their location, as well as the identification of their feeders and drainers. DSA, however, is an invasive method that involves exposure to radiation and requires the injection of iodinated contrast medium. Therefore, a noninvasive method is required to diagnose AVFs and follow up patients with intracranial dural AVFs. Three-dimensional (3D) time-offlight magnetic resonance (MR) angiography and its source images are widely used for the assessment of intracranial dural AVFs (1,2). The lack of hemodynamic information, however, limits their clinical usefulness (2–4). While four-dimensional (4D) contrast material–enhanced MR angiography at 3 T appears to be reliable and provides hemodynamic information on intracranial dural AVFs (5), it poses risks associated with contrast agents (6). Although various techniques for time-resolved arterial spin-labeling (ASL)–based MR angiography have been reported (7–10), limitations such as low spatial resolution, short imaging coverage, and long acquisition times hamper their clinical application. Nakamura et al (11) developed a 3D volumetric nonenhanced time-resolved MR
Advances in Knowledge nn On 3-T four-dimensional (4D) arterial spin-labeling (ASL)– based MR angiographic images, the intracranial arteries are visualized at high spatial (0.5 3 0.5 3 0.6 mm3) and temporal (300 milliseconds) resolution without exogenous contrast agents. nn In the evaluation of intracranial dural arteriovenous fistulas (AVFs), intermodality agreement between 4D ASL MR angiographic and DSA findings was excellent for the fistula site and venous drainage (k = 1.00) and good for the main arterial feeders (k = 0.80). 194
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angiographic technique termed contrast inherent inflow-enhanced multiphase angiography combining multiple-phase flow-sensitive alternating inversion recovery (CINEMA-FAIR). This 4D ASLbased MR angiographic technique makes possible the sequential observation of hemodynamics similar to DSA and facilitates large 3D volume acquisition. To date, no systematic studies with the use of the 4D ASL MR angiographic technique in healthy subjects and patients with intracranial dural AVFs have been reported. The aim of our study was to compare prospectively the agreement between 3-T 4D ASL MR angiography and DSA for the characterization of intracranial dural AVFs.
Materials and Methods Study Population Our institutional review board approved this study; prior informed consent for the imaging studies was obtained from all patients. Patients were searched and recruited from our local database from May 2011 to June 2013 in Kumamoto University Hospital (Kumamoto, Japan). The inclusion criteria were that the patients had intracranial dural AVFs and underwent both 4D ASL MR angiography and DSA. The exclusion criteria were that the patients had a history of surgery in the brain, had an allergy for iodinated contrast agents or renal dysfunction, and had emergency cases. Nine patients (seven men, two women; age range, 52–77 years; mean age, 63.4 years) with intracranial dural AVFs fulfilled the selection criteria. Their primary presenting symptoms were visual disturbance in five patients, Implication for Patient Care nn Four-dimensional ASL-based magnetic resonance MR angiographic imaging at 3 T may be used as the primary diagnostic tool in patients who are suspected of having an intracranial dural AVF and in subsequent follow-up examinations.
tinnitus in two, and headache and disorientation in one each.
Four-dimensional ASL MR Angiographic Technique All MR studies were performed with a 3-T MR imaging system (Achieva; Philips Medical Systems, Best, the Netherlands) and a commercially available 32-channel head coil. The MR imaging unit featured a gradient system with a maximal achievable gradient amplitude of 40 mT/m and a slew rate of 200 T/m/sec. Four-dimensional ASL MR angiography was performed with the CINEMA-FAIR technique that combines ASL with a 3D segmented T1-weighted turbo field-echo sequence (11). The flow-sensitive alternating inversion-recovery method with Look-Locker sampling was used for spin tagging (12). The pulse sequence diagram of the CINEMA-FAIR technique is shown in Figure 1. The sequence was composed of two acquisitions with identical readout and different magnetization preparation schemes; measurements were in two consecutive acquisitions preceded by nonselective (global) and spatially selective inversion pulses (11). Prior Published online before print 10.1148/radiol.13122670 Content codes: Radiology 2014; 271:193–199 Abbreviations: ASL = arterial spin labeling AVF = arteriovenous fistula CI = confidence interval CINEMA-FAIR = contrast inherent inflow-enhanced multiphase angiography combining multiple-phase flowsensitive alternating inversion recovery DSA = digital substraction angiography 4D = four-dimensional 3D = three-dimensional TI = inversion time Author contributions: Guarantor of integrity of entire study, T.H.; study concepts/ study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, Y.I., M.A.; clinical studies, Y.I., T.H., Y.K., M.N., Y.S., M. Kitajima, M.A., M. Komi, K.M.; statistical analysis, Y.I., M.A.; and manuscript editing, Y.I., T.H., M.A., Y.Y. Conflicts of interest are listed at the end of this article.
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Figure 1
Figure 1: (a) Pulse sequence diagram of the CINEMA-FAIR technique. It consists of a flow-sensitive alternating inversion-recovery– based ASL sequence: global and spatially selective 180° pulses. A segmented 3D T1-weighted (T1) gradient-echo sequence (3D T1-weighted turbo field echo [TFE]) is acquired after global or selective 180° pulses. This cycle is repeated for the number of shots of the gradient-echo sequence. Look-Locker sampling with multiple inversion times (TIs) was used after each 180° pulse to obtain timeresolved MR angiographic images. This makes possible the visualization of virtual dynamic filling by flowing blood. After completion of the two acquisitions, the corresponding temporal phases with identical inversion delays were subtracted. a = Excitation pulse, N = arbitrary number. (b) Schematic labeling geometry shows global (acquisition 1) and selective (acquisition 2) labeling regions and their subtraction images.
to the T1-weighted turbo field-echo readout of the first acquisition, a nonselective inversion pulse was applied. For the second acquisition, a spatially selective inversion pulse was applied to the selectively labeled imaging volume. After completion of the two acquisitions, corresponding temporal phases of the two acquisitions with identical inversion delays were subtracted (11). Maximum intensity projection was then performed for each temporal phase of the subtracted data sets. Since multiple measurements with different TIs were conducted, sequential angiographic images were obtained. The parameters for the CINEMAFAIR sequence were as follows: repetition time msec/echo time msec, 4.5/2.2; flip angle, 10°; field of view, 200 3 200 mm2; matrix, 192 3 192;
section thickness, 1 mm; slab thickness, 100 mm; reconstructed spatial resolution, 0.5 3 0.5 3 0.6 mm3; sensitivity encoding factor, 3.0; TI, DTI, and final TI, 80 milliseconds, 300 milliseconds, and 2.0 seconds, respectively; number of acquisition phases, seven; and acquisition time, 8 minutes 26 seconds.
DSA Technique An experienced neuroradiologist and neurosurgeon performed diagnostic biplanar intraarterial DSA (Allura Xper FD; Philips Medical Systems, Best, the Netherlands). Vascular access was acquired by using the transfemoral approach and the Seldinger technique. The vascular anatomy was evaluated by using DSA combined with the manual injection (6–10 mL) of iodinated contrast medium (iopamidol, Iopamiron
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300; Bayer-Schering, Berlin, Germany) into the external and internal carotid arteries and the vertebral arteries. The image matrix and field of view were 1024 3 1024 and 170 3 170 mm2, respectively; the temporal resolution was 3 frames per second. DSA was performed within 7 days of 4D ASL MR angiography, as a rule.
Image Analysis At a picture archiving and communication system workstation, two neuroradiologists (Y.S. and M. Kitajima, with 17 and 19 years of experience in neuroradiology, respectively) independently assessed the entire sets of DSA images. Two other observers (Y.I. and T.H., with 7 and 22 years of experience in neuroradiology, respectively) independently assessed the 4D ASL MR 195
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angiographic images at a picture archiving and communication system workstation. They used a four-point grading system to score the overall image quality, as follows: grade 1, nondiagnostic quality due to severe artifacts; grade 2, quality with artifacts that may interfere with the diagnosis; grade 3, quality with artifacts that do not interfere with the diagnosis; and grade 4, diagnostic quality without artifacts. Then they independently evaluated the 4D ASL MR angiographic findings in regard to dural AVFs; they were blinded to clinical information and the DSA findings. On the 3D data display, all regions were visible. The observers were allowed to enlarge regions of special interest in any direction. The observers looked for the dural AVF site, the main arterial feeder, and the venous drainage on 4D ASL MR angiographic and DSA images (5). The site of the dural AVF was identified as the transverse-sigmoid sinus, the cavernous sinus, the superior sagittal sinus, or as other; the main feeders were identified as originating at the internal maxillary artery and/or the middle meningeal artery, at the ascending pharyngeal artery, at the occipital artery, at the internal carotid artery, or as at other arteries. On the basis of the classification of Borden et al (13), dural AVF drainage was recorded as type 1 (drainage directly into the dural venous sinus), type 2 (drainage into the dural venous sinus with cortical venous reflux), or type 3 (drainage directly into the subarachnoid veins [cortical venous reflux only]). Differences in their assessments were resolved in consensus.
Statistical Analysis Interobserver agreement for 4D ASL MR angiography with respect to overall image quality was determined by calculating the k coefficient (k , 0.20, poor agreement; k = 0.21–0.40, fair agreement; k = 0.41–0.60, moderate agreement; k = 0.61–0.80, good agreement; k = 0.81–0.90, very good agreement; and k . 0.90, excellent agreement) (5). Interobserver and intermodality agreement for dural AVF assessments 196
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was determined by calculating the k coefficient. We also recorded the number and percentage of times when interobserver and intermodality assessments were in exact agreement. A software package (Med-Calc for Windows; MedCalc Software, Mariakerke, Belgium) was used for all analyses.
Results Both observers judged the overall image quality on 4D ASL MR angiographic images of the nine dural AVFs to be without artifacts and of diagnostic quality (grade 4) (Fig 2). In the qualitative evaluation of DSA images, interobserver agreement was excellent for all items (k = 1.00; 95% confidence interval [CI]: 1.00, 1.00). The Table summarizes the 4D ASL MR angiographic and DSA findings in the nine dural AVFs; four were transversesigmoid sinus fistulas, three were cavernous sinus fistulas, and one was a superior sagittal sinus fistula; the other was located at the sphenoparietal sinus. On DSA images, four dural AVFs were primarily supplied by the occipital artery, three were supplied by the internal carotid artery, and one each was supplied by the internal maxillary artery and/or middle meningeal artery and by the ascending pharyngeal artery. Venous drainage on DSA images was type 1 in five patients and type 2 in four patients. There were no patients with type 3 drainage. With respect to the fistula site, the two observers reviewing 4D ASL MR angiographic images agreed in all nine assessment studies; interobserver agreement was excellent (k = 1.00; 95% CI: 1.00, 1.00). The observers of 4D ASL MR angiographic and DSA images agreed with respect to the site of all nine fistulas (Fig 2). Intermodality agreement was excellent (k = 1.00; 95% CI: 1.00, 1.00) (Table). In the analysis of the main arterial feeders, the two readers reviewing 4D ASL MR angiographic images agreed in seven of nine dural AVFs (78%); interobserver agreement was moderate (k = 0.53; 95% CI: 0.08, 0.98). Similarly, in seven of nine dural AVFs (78%), 4D
ASL MR angiographic (consensus readings) and DSA agreed on the main arterial feeders; intermodality agreement was good (k = 0.80; 95% CI: 0.58, 1.00) (Table, Fig 2). In eight of nine patients (89%) both observers reviewing 4D ASL MR angiographic images agreed in their assessment of venous drainage. Interobserver agreement was good (k = 0.77; 95% CI: 0.35, 1.00) (Table, Fig 2). With both imaging modalities, there was agreement on the drainage pattern in all nine patients (Fig 2); intermodality agreement was therefore recorded as excellent (k = 1.00; 95% CI: 1.00, 1.00) (Table).
Discussion Our study findings indicated that 4D ASL MR angiography at 3 T was a useful diagnostic tool for the characterization of intracranial dural AVFs. Agreement between 4D ASL MR angiographic and DSA findings was excellent for the fistula site and the type of venous drainage and good for the main arterial feeders. We attribute this result to the combined effect of several factors: the long T1-weighted relaxation times and the high signal-to-noise ratio on 3-T MR images and our use of a 32-channel head coil. With these techniques, we were able to obtain high spatial and temporal resolution of 0.5 3 0.5 3 0.6 mm3 and 0.3 second per volume, respectively. With regard to 4D MR angiography, there are two different techniques (ie, 4D contrast-enhanced MR angiographic and 4D ASL MR angiographic methods. Although 4D contrast-enhanced MR angiography at 3 T has been reported to be a reliable technique that provides hemodynamic information on intracranial dural AVFs (5), it poses risks associated with contrast agents (6). Because 4D ASL MR angiography is based on ASL techniques, it does not require the use of gadolinium-based contrast agents, thereby avoiding the risk for nephrogenic systemic fibrosis. Therefore, 4D ASL MR angiography may be especially useful in patients with renal dysfunction and in children in whom the rapid
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Figure 2 Figure 2: MR images in a 75-year-old man with dural AVF at the left transverse-sigmoid sinus. (a) Anteroposterior (top), lateral (middle), and axial (bottom) maximum intensity projections of 4D ASLbased MR angiographic images (4.5/2.2, 10° flip angle). The temporal resolution is 300 milliseconds. The left transverse-sigmoid sinus is depicted early in the early arterial to the arterial phase. The site of the dural AVF (thick arrows) appears to be the left transverse-sigmoid sinus. The left occipital artery has a large caliber and is well visualized from the early arterial phase (arrowheads). The posterior meningeal artery is also depicted (thin arrows). Retrograde cortical venous drainage is seen from the left transverse sinus (dotted circle). On the basis of these findings, both observers judged that the left transverse-sigmoid sinus was the fistula site, that this dural AVF was primarily fed by the occipital artery, and that venous drainage was type 2. (b) Anteroposterior (top) and lateral (bottom) projections of DSA images of the left external carotid artery in the same patient. DSA shows an arteriovenous shunt (arrows) at the left transverse-sigmoid sinus. It is supplied by branches from the left occipital artery (arrowheads). Retrograde cortical venous drainage is from the left transverse sinus (dotted circles).
intravenous injection of a bolus of contrast material may be difficult. In addition, 4D contrast-enhanced MR angiography is not a reliable tool for assessing
main arterial feeders of dural AVFs (5). On the basis of the results of our current study, agreement between 4D ASL MR angiographic findings and DSA
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findings was good for the main arterial feeders. In assessment of main arterial feeders, intermodality agreement might be better for 4D ASL MR angiography than for 4D contrast-enhanced MR angiography. This idea is probably a consequence of the difference between the spatial and temporal resolution of these techniques (ie, 0.5 3 0.5 3 0.6 mm3 and 0.3 second per volume for 4D ASL MR angiography and 1.0 3 1.0 3 1.5 mm3 and 1.9 seconds per volume for 4D contrast-enhanced MR angiography [5], respectively). While time-resolved ASL-based MR angiographic techniques (eg, true fast imaging with steady-state precession– based spin tagging with alternating radiofrequency, or True STAR; timeresolved vessel-selective digital subtraction MR angiography, or DSMRA; and time-spatial labeling inversion pulse, or Time-SLIP, MR DSA methods) have been reported (8–10), they are of limited value because of low spatial resolution, short imaging coverage, or long acquisition times (maximum, 197
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Summary of 4D ASL MR Angiographic and DSA Findings 4D ASL MR Angiography Clinical Data Fistula site Transverse-sigmoid sinus Cavernous sinus Superior sagittal sinus Others Main arterial feeder Internal mammary artery and/or middle meningeal artery Ascending pharyngeal artery Occipital artery Internal carotid artery Others Drainage pattern Type 1‡ Type 2§ Type 3||
Observer 1
Observer 2
Interobserver Agreement*
DSA
4D ASL MR Angiography†
Intermodality Agreement*
4 3 1 1
4 3 1 1
1.00 (1.00, 1.00) ... ... ...
4 3 1 1
4 3 1 1
1.00 (1.00, 1.00) ... ... ...
0
0
0.53 (0.08, 0.98)
1
0
0.80 (0.58, 1.00)
2 3 4 0
0 4 5 0
... ... ... ...
1 4 3 0
0 4 5 0
... ... ... ...
6 3 0
5 4 0
0.77 (0.35, 1.00) ... ...
5 4 0
5 4 0
1.00 (1.00, 1.00) ... ...
* Data are k statistics, and numbers in parentheses are 95% CIs. †
Consensus reading of the two observers.
‡
Venous drainage directly into the dural venous sinus.
§
Venous drainage into the dural venous sinus with cortical venous reflux.
||
Venous drainage directly into the subarachnoid veins (cortical reflux only).
45–60 minutes), or all three. These disadvantages hamper their clinical usefulness for the evaluation of dural AVFs. On the other hand, 4D ASL MR angiography with CINEMA-FAIR offers the advantage of higher spatial and temporal resolution, larger image coverage, and shorter acquisition times (approximately 7–9 minutes). In addition, image data consist of isotropic voxels that allow loss-free reformatting, an important factor in the assessment of complex vascular structures such as dural AVFs. Our study had some limitations. Because we performed a single-center study that involved a small number of patients, we were unable to determine whether 4D ASL MR angiography and DSA are of equal diagnostic value. Second, only arterial phase images were obtained and evaluated at 4D ASL MR angiographic imaging. This factor was due to the short T1 decay (approximately 2 seconds) of the magnetically labeled water. However, this limitation might be advantageous for 198
the evaluation of arteriovenous shunt lesions. Third, we did not determine the number of feeders and drainers of the nine dural AVFs. Feeders other than the main feeders were not evaluated because 4D ASL MR angiography did not fully depict small-caliber feeding vessels. Because the size of voxels on 4D ASL MR angiographic images may be larger than the diameter of the arterial dural AVF feeders, the spatial resolution of these images may not be high enough to depict small feeders. In conclusion, on 3-T 4D ASL MR angiographic images, the intracranial arteries are visualized at high spatial and temporal resolution without exogenous contrast agents. The good-toexcellent agreement between 3 T 4D ASL MR angiographic and DSA findings suggests that 3-T 4D ASL MR angiography is a useful tool for the evaluation of intracranial dural AVFs. Further studies on larger populations are needed to clarify the clinical role of 3-T 4D ASL MR angiography in patients with intracranial dural AVFs.
Disclosures of Conflicts of Interest: Y.I. No relevant conflicts of interest to disclose. T.H. No relevant conflicts of interest to disclose. Y.K. No relevant conflicts of interest to disclose. M.N. No relevant conflicts of interest to disclose. Y.S. No relevant conflicts of interest to disclose. M. Kitajima No relevant conflicts of interest to disclose. M.A. No relevant conflicts of interest to disclose. M. Komi No relevant conflicts of interest to disclose. K.M. No relevant conflicts of interest to disclose. Y.Y. No relevant conflicts of interest to disclose.
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4. Watanabe K, Kakeda S, Watanabe R, Ohnari N, Korogi Y. Normal flow signal of the pterygoid plexus on 3T MRA in patients without DAVF of the cavernous sinus. AJNR Am J Neuroradiol 2013;34(6):1232– 1236. 5. Nishimura S, Hirai T, Sasao A, et al. Evaluation of dural arteriovenous fistulas with 4D contrast-enhanced MR angiography at 3T. AJNR Am J Neuroradiol 2010;31(1):80– 85.
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