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Technical Developments |
1 From the Department of Medical Imaging, Division of Neuroradiology (R.I.F., C.M., J.K.K., R.A.W., P.W.C., D.G.W., G.C.), the Department of Surgery, Division of Neurosurgery (M.L.S.), and the Department of Medical Biophysics (G.A.W.), University of Toronto, University Health Network, Toronto Western Hospital, Fell Pavilion 3-404, 300 Bathurst St, Toronto, Ontario, Canada M5T 2S8; the Department of Imaging Research, Sunnybrook and Women’s College Health Science Centre, Toronto, Ontario, Canada (J.K.K., M.L., J.A.S., G.A.W.); and the Laboratory of Cardiac Energetics, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md (J.A.D.). Received July 26, 2000; revision requested September 8; revision received November 13; accepted December 4. Supported in part by a research grant (no. A3048) from the Heart and Stroke Foundation of Ontario and the Canadian Heads of Academic Radiology/Nycomed Research Development Program, 1999. Address correspondence to R.I.F. (e-mail: richard.farb@utoronto.ca).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMaterials and Methods ResultsDiscussionREFERENCES |
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Index terms: Arteriovenous malformations, 10.75 • Cerebral blood vessels, abnormalities, 10.75 • Cerebral blood vessels, MR, 17.12142, 17.12143 • Magnetic resonance (MR), technology • Magnetic resonance (MR), time of flight, 17.12142, 17.12143
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMaterials and Methods ResultsDiscussionREFERENCES |
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Clear consistent depiction of all AVM components is a requirement of any imaging modality advocated as a potential replacement for DSA in the pretreatment evaluation and follow-up of AVMs. Several investigators (1–5) have suggested time-of-flight (TOF) magnetic resonance (MR) angiography as a noninvasive method for evaluating intracranial AVMs. More specifically, TOF MR angiography has been advocated as the sole imaging tool required during planning and follow-up for patients undergoing stereotactic irradiation for AVMs (6). However, in general, the application of MR angiography for the evaluation of AVMs has remained of supplemental value because of a lack of consistent and complete demonstration of all components of an AVM (ie, feeding arteries, nidus, and draining veins) (2,3,7–9).
Conventional catheter angiography, with its routine two-dimensional planar technique, is also limited in its depiction of the three-dimensional (3D) anatomy of an AVM (10). The use of MR angiography, with its multiplanar functions, has the potential to substantially improve depiction of specific AVM components and may lead to improved radiosurgical targeting of the AVM nidus.
Results of recent preliminary studies (11–13) suggest that first-pass 3D gadolinium-enhanced MR angiography may be useful and perhaps superior to TOF MR angiography for the evaluation of intracranial AVMs. The techniques used in these preliminary studies consisted of obtaining a serial set of relatively low-resolution small-volume images with imaging times of 0.5–9.0 seconds. Use of these techniques sacrificed spatial resolution for a gain in temporal resolution; the intention was that several of these serial acquisitions would capture the transitory enhancement of the feeding arteries, nidus, and draining veins. In their study of four patients, Klisch et al (11) showed that AVM component delineation was possible with a subsecond MR angiographic projection technique. In imaging AVMs, however, we believe that a single centric-ordered high-spatial-resolution acquisition initiated at precisely the appropriate moment is a superior alternative to the previously described rapid-acquisition low-resolution techniques.
The purpose of this study was to compare this highly optimized form of MR angiography with a conventional TOF MR angiographic technique—namely, the popular multiple overlapping thin-slab acquisition sequence (hereafter, TOF) in the evaluation of AVMs.
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Materials and Methods |
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TOPABSTRACTINTRODUCTIONMaterials and Methods ResultsDiscussionREFERENCES |
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All MR imaging was performed with a superconducting 1.5-T system (Signa cv/i; GE Medical Systems, Milwaukee, Wis) running 8.2.5 software by using a standard head.
DSA Examination
Patients arrived in the angiographic suite with an externally applied cranial stereotactic frame (O.B.T. Frame; Tipal Instruments, Montreal, Quebec, Canada). In keeping with the standard practice at the Sunnybrook and Women’s College Health Science Centre, the frame was applied such that the radiolucent portion was positioned over the cranium; thus, the frame did not degrade the angiograms. DSA consisted of standard anteroposterior and lateral projections of injections of arteries known to supply the AVM, which were known from multiple previous diagnostic catheter angiographic examinations and embolization procedures. All DSA (Integris V-3000; Philips Medical Systems, Best, the Netherlands) was performed by using a 17- or 20-cm image intensifier. Subtracted images from the sequences, including the arterial and venous phase, were recorded. All DSA was performed without complication or technical difficulty.
TOF MR Angiography
The TOF MR angiographic sequence parameters were as follows: repetition time msec/echo time msec, 33.3/3.0; flip angle, 20°; fractional echo acquisition; field of view, 22 x 16.5 cm; matrix, 256 x 192; bandwidth, 15.6 kHz; section thickness, 0.8 mm; and 32 sections per slab, with a six-section overlap. Three to four slabs were obtained, yielding a total imaging time of 10–14 minutes. Imaging volumes were oriented in the transverse plane. Imaging options included magnetization transfer background suppression and flow compensation. All TOF MR angiography was technically successful.
Contrast-enhanced MR Angiography
Contrast-enhanced MR angiography consisted of four integral parts: (a) initiation of a two-dimensional single-section bolus-detection sequence oriented in the transverse plane and located at the skull base; (b) intravenous power injection of contrast material; (c) automated detection of the arrival of intraarterial gadolinium-based contrast material at the skull base, resulting in automatic termination of the detection sequence; and triggering of (d) a fast MR angiographic sequence with elliptic centric-ordered phase encoding. One of two MR technologists performed the procedure for each patient. On one occasion, physician input (R.I.F.) was required when the AVM was not readily located on the conventional spin-echo images.
Interactive Two-dimensional Bolus-Detection Tool
The two-dimensional bolus-detection sequence was initiated and controlled in real time by using an interactive user-friendly computer interface on a separate workstation (Sun Microsystems, Mountain View, Calif). This workstation was connected directly to the MR imager subsystems by using a special bus adapter (Bit3, St Paul, Minn). The detection sequence consisted of a continuously refreshed two-dimensional gradient-echo acquisition of a transverse section at the level of the cavernous carotid arteries. The detection sequence parameters were as follows: 11.5/9.5; flip angle, 30°; field of view, 20 x 20 cm; matrix, 320 x 128; bandwidth, 62.5 kHz; and section thickness, 10 mm. The resultant image update rate was approximately one image every 1.5 seconds.
As a first step in the implementation of the detection sequence, interactive section positioning was performed to obtain an image at the level of the cavernous portion of the internal carotid arteries. A region of interest was then interactively placed over the basilar and carotid arteries (Fig 1). These sentinel arteries were easily identified because of the inherent flow-related enhancement of the gradient-echo image. Inferior and superior saturation bands were then sequentially applied to confirm proper placement of the regions of interest. The saturation bands were left active during the detection sequence, extinguishing signal intensity due to flow-related enhancement within the carotid arteries and thus optimizing visualization of the expectant inflow of gadolinium-enhanced arterial blood. A signal-intensity-triggering threshold was then automatically determined.
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Contrast Material Injection
As part of preparation for MR imaging, a commercially available two-cylinder MR imaging–compatible injector (Spectris; Medrad, Indianola, Pa) was loaded with 20 mL of gadodiamide (Omniscan; Nycomed Amersham, Buckinghamshire, England) in one syringe (syringe 1), and with 60 mL of normal saline in a second syringe (syringe 2). Intravenous access was obtained with a 20-gauge intravenous catheter in the right antecubital vein. A slow infusion of saline was initiated at the time of intravenous connection and continued during preliminary imaging until contrast material bolus injection. With the MR angiographic sequence prescribed and prescanned as described subsequently, and with the detection sequence armed and running as described previously, the technologist in the control room manually initiated injection. Twenty milliliters of the gadolinium-based contrast material was injected at a rate of 2 mL/sec. This was immediately followed by a 30-mL bolus of normal saline, also injected at 2 mL/sec. This injection protocol was followed for all patients.
Elliptic Centric-ordered MR Angiographic Sequence
The intracranial arteries were imaged with a fast elliptic centric-ordered spoiled gradient-echo sequence. The view order for this MR angiographic sequence was in ascending order of radial k-space distance from the k-space origin, similar to that previously reported (15,16). Sequence parameters were as follows: 6.2/1.6; flip angle, 20°; fractional echo acquisition; field of view, 23.0 x 17.25 cm; matrix, 320 x 240; bandwidth, 62.5 kHz; section thickness, 0.8 mm; 80 sections resulting in a 6.4-cm-thick volume; and total imaging time of 126 seconds. Resultant voxel dimensions were nearly isotropic at 0.72 x 0.72 x 0.8 mm (this resolution was obtained without zero filling techniques). The imaging volume was oriented in the transverse plane in nine patients and in the sagittal plane in one patient.
All contrast material injections and subsequent automated triggering and angiographic sequences were uneventful, with 100% technical success. The mean time to trigger (the time from power injection initiation to MR angiography initiation) was 18.3 seconds, and the time to trigger range was 16–21 seconds.
Image Evaluation
Data from the MR angiographic sequences were transferred to a commercially available workstation with 3D capability (Advantage Windows 3.7; GE Medical Systems). Source and maximum-intensity projection (MIP) images were obtained for each sequence and consisted of unsegmented submentovertex, lateral, and anteroposterior projections. Segmented MIP images consisting of isolation of a cerebral hemisphere were also obtained and rotated through 180° at 15° increments. Images from each patient’s digital subtraction, TOF, and contrast-enhanced MR angiographic examinations were collected to form one image set.
Two neuroradiologists experienced in imaging and evaluating AVMs and not previously involved in the study (R.A.W., P.W.C.) independently reviewed the image sets of each of the 10 patients. Each image set assessment was recorded on a separate grading sheet.
The neuroradiologists were asked to grade the TOF MR angiograms and contrast-enhanced MR angiograms as poor, moderate, or equivalent, as compared with DSA images, for the depiction of the feeding arteries, nidus, and draining veins. A grade of "poor" was defined as a lack of depiction on MR angiograms of a structure known to exist. "Moderate" depiction was defined as incomplete but confident depiction on MR angiograms of a structure known to exist. "Equivalent" (complete) depiction was defined as depiction of a structure on MR angiograms that would allow clear localization of that structure (ie, feeding arteries, veins, or portion of nidus) and measurement similar to that which could be performed with the DSA image.
As a second assessment, readers were asked to qualitatively compare the images obtained with the two MR angiographic techniques by assigning a grade of 1–5; a grade of 1 indicated that contrast-enhanced MR angiograms were poor; 2, inferior; 3, equivalent; 4, better, or 5, far superior to TOF MR angiograms.
As a third and final assessment, readers were asked to compare contrast-enhanced MR angiograms and DSA images with respect to their depiction of the 3D spatial orientation of the arteries, nidus, and veins of a given AVM. Readers were asked to specify which modality—DSA, contrast-enhanced MR angiography, or neither (equivalence)—they perceived as providing more information regarding the spatial orientation of the AVM components.
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Results |
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TOPABSTRACTINTRODUCTIONMaterials and Methods ResultsDiscussionREFERENCES |
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Results of the comparison of TOF MR angiograms with selected DSA images are shown in the Table. In a majority of assessments, TOF MR angiograms were graded as poor in comparison with DSA images for the depiction of all three AVM components (ie, feeding arteries, nidus, and draining veins). No TOF image set was deemed equivalent to the corresponding DSA image set.
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All contrast-enhanced MR angiograms were considered superior to the corresponding TOF MR angiograms. Specifically, contrast-enhanced MR angiograms were considered "far superior" to TOF MR angiograms in 15 (75%) of 20 assessments, and "better" in the remaining five (25%) of 20 assessments.
With regard to the delineation of the spatial orientation of the AVM, in seven (35%) of 20 assessments, contrast-enhanced MR angiography was considered superior to DSA. In nine (45%) of 20 assessments, the orientation information obtained with contrast-enhanced MR angiography was considered equivalent to that obtained with DSA, and in four (20%) of 20 assessments, the spatial information provided was considered of quality inferior to that provided with DSA. Representative images are shown in Figures 2–4.
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Discussion |
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TOPABSTRACTINTRODUCTIONMaterials and Methods ResultsDiscussionREFERENCES |
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Results of our investigation indicate that the common technique of TOF MR angiography was unable to adequately depict AVM anatomy in a majority of cases. There was particular difficulty in demonstrating the correct size of the nidus (65% with poor delineation) and draining veins (90% with poor delineation), as compared with DSA. The reasons for this shortcoming of TOF MR angiography have been previously discussed in the literature and include inadequate spatial resolution, spin saturation effects, inadequate signal-to-noise ratio, inadequate background suppression, susceptibility effects, and motion artifacts (3,9,17). Particularly troublesome in AVM imaging with TOF MR angiography is inconsistent depiction of the draining veins and nidus because of overwhelming saturation effects.
In contrast to the results of TOF MR angiography, the results of contrast-enhanced MR angiography were more favorable. The major advantages of gadolinium-enhanced MR angiography over TOF MR angiography derive from the robust signal intensity afforded by the high intravascular concentration of gadolinium-based contrast material (18). This nonsaturating increased signal intensity allows for the use of a short repetition time, yielding better suppression of background signal intensity arising from fat and methemoglobin (Fig 4), as well as reduced relative susceptibility artifact arising from paramagnetic material such as surgical clips. The time gained by the reduced repetition time is reinvested to improve spatial resolution. Also, because of a lack of vascular saturation issues, contrast-enhanced MR angiograms can be acquired in a transverse, coronal, or sagittal orientation, whichever best fits the size of the abnormality and the available imaging volume.
The modification of gadolinium-enhanced MR angiography, which we have performed, uses a much longer imaging time, with elliptic centric encoding of k space. This type of sequence can provide high-spatial-resolution images displaying tissue contrast on the basis of the early short interval of optimal AVM enhancement. This sequence acquires the low-frequency information at the beginning of imaging (15,16). This ordering of k space has the effect of providing a snapshot of the status of the vessels during the first several seconds of imaging, which, if timed appropriately with the arrival of contrast material, would correspond to the first pass, peak arterial concentration. This produces a final angiogram with major structural signal intensity determined within the arterial phase of contrast material distribution. Contrast-enhanced gadolinium-enhanced MR angiographic sequences have been successful in depicting various target vessels, including the aorta (19), renal arteries (16), carotid arteries (20–22), and intracranial arteries (23).
As described previously, a key aspect of imaging all three major AVM components (ie, feeding arteries, nidus, and draining veins) is timing. The results of previous investigations (22,24) have indicated that the normal cranial circuit transit time typically is 5–8 seconds. This indicates a short optimal time window, likely several seconds, during which the feeding arteries, nidus, and draining veins are optimally enhanced prior to filling of the normal cerebral veins. Given this timing constraint, optimal imaging of all three AVM components requires a properly timed, efficient phase-encoding scheme such as elliptic centric ordering.
Recently, a fluoroscopically (real-time) guided manual triggering technique was described (25). This technique relies on a specially trained operator to observe the inflow of arterial gadolinium-based contrast material on the MR fluoroscopic (real-time) images. The operator is then required to rapidly judge when the level of enhancement will likely peak, factor in the time for a desired trigger delay and the inherent time delay of the image processing and pulse controller, and then manually trigger the angiographic sequence.
Observer-dependent manually triggered systems have inherent observer variability in reaction time and judgment. This will undoubtedly result in suboptimal triggering and degraded final image quality. We believe that the use of an automated triggering mechanism for the gadolinium-enhanced MR angiographic sequence is a more reliable and consistent method of first-pass arterial imaging.
Nonfluoroscopic automated detection and triggering, also known as MR Smartprep (GE Medical Systems), does not allow for direct visualization of contrast material inflow (26). This could be a problem if the monitoring plane were displaced by patient movement or initially incorrectly located. In this errant scenario, without fluoroscopic (real-time) depiction and manual override, the contrast material bolus would be missed completely (25). Isoda et al (23) described difficulties that arise when using nonfluoroscopic automated detection and triggering with small tracker volumes, as required for intracranial vascular imaging. These include threshold calculation, tracker volume placement, and patient movement issues and are likely partially responsible for the reported failure rate (18.4%) of this technique when used for intracranial arterial imaging. We also noted that premature triggering of elliptic centric-ordered angiography results in marked degradation of final images (17,19,27).
We believe that real-time depiction of contrast material inflow is desirable both to reduce the likelihood of these errors and to visually confirm proper triggering. In light of the timing constraints for imaging AVMs with gadolinium-enhanced MR angiography, we believe an automated real-time trigger is desirable. Ideal triggering would result in initiation of the elliptic centric-ordered angiographic sequence at the instant of peak intraarterial contrast material concentration. We have found it necessary to insert a nonzero trigger delay (500 msec), which, in summation with electronic system delays, approximates the rise-to-peak time for intraarterial gadolinium concentration.
In addition to accurate bolus timing, which maximizes the signal-to-noise ratio of target AVM components, high spatial resolution is needed for adequate depiction of AVM detail. This requirement resulted in a sequence that lasted 126 seconds, far longer and with higher resolution than was previously reported for elliptic centric-ordered angiographic sequences (20,23,26); it resulted in 0.72 x 0.72 x 0.8-mm near-isotropic voxel dimensions. As expected, this longer imaging time leads to subtle increased edge enhancement of venous structures; however, in the final MIP images, venous suppression remains intact because of the considerably higher arterial signal intensity.
Our concept, therefore, has been to use a real-time-monitored 3D gadolinium-enhanced MR angiographic sequence with auto-triggered high-spatial-resolution elliptic centric-ordered enhancement for imaging intracranial AVMs. Real-time monitoring provides ease of use and assurance of proper triggering. Auto-triggering provides accurate, reliable timing. A longer imaging time provides high spatial resolution. Elliptic centric ordering of phase encoding provides more efficient acquisition of central phase-encoding views during peak arterial gadolinium concentration, resulting in robust arterial signal intensity and a modicum of temporal resolution (ie, later-filling venous anatomy exclusion from the final image). To our knowledge, this is the first description and reported implementation of a real-time prescribed and monitored contrast-material bolus detection and triggering system with full automation for gadolinium-enhanced MR angiography of intracranial AVMs. We have previously described successful use of this system in carotid arterial MR angiography (28).
Perceived disadvantages to contrast-enhanced MR angiography might include issues of cost of the contrast agent, accompanying cost of the power injector and supplies, and training of the MR technologists. These disadvantages are minor in comparison with the cost and potential morbidity of DSA (29).
The true limitation on imaging time, as well as the elucidation of T1 values of gadolinium-enhanced blood, remain two important issues requiring clarification as first-pass gadolinium-enhanced MR angiography continues to evolve. Longer imaging times will allow for larger imaging volumes, with even greater spatial resolution. Higher gadolinium-based contrast material doses may further improve signal-to-noise ratio.
In retrospect, the 20° flip angle used in the current study was probably low because of an initial underestimation of the intraarterial concentration of gadolinium. A 30°–40° flip angle approximating the true Ernst angle might have yielded slightly higher arterial signal intensities (30). Accurate calculation of the T1 of gadolinium-enhanced arterial blood and its variance with time would allow for application of the recently suggested technique of using a flip angle that varies with time (31).
Potential future intracranial applications of gadolinium-enhanced MR angiography include imaging for evaluation of ischemic disease and intraparenchymal hemorrhage, presurgical diagnosis and follow-up of intracranial aneurysms, and depiction of tumor-vessel relationships, as well as venous imaging. Each of these applications will require minor modification of the techniques described herein for optimization.
In conclusion, in this initial investigation, we have shown that real-time monitored auto-triggered elliptic centric-ordered MR angiography is superior to TOF MR angiography for evaluation of intracranial AVMs, resulting in improved depiction of the components of an AVM, in particular the nidus and draining veins. When compared with DSA, contrast-enhanced MR angiography consistently depicted AVM components and their orientation, which at times exceeded the two-dimensional planar abilities of DSA. Further refinement and clinical evaluation of this MR angiographic technique is warranted and may indeed lead to the obviation of DSA in the treatment planning and follow-up of patients with AVMs.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, R.I.F.; study concepts, R.I.F., J.K.K.; study design, R.I.F., J.K.K., M.L., G.A.W., M.L.S.; literature research, R.I.F., J.K.K.; clinical studies, R.I.F., C.M., M.L.S., D.G.W., P.W.C., G.C., J.A.S., R.A.W.; data acquisition, R.I.F., C.M., M.L., J.A.S., J.A.D., D.G.W.; data analysis/interpretation, R.I.F., P.W.C., G.C., M.L.S., R.A.W.; statistical analysis, R.I.F.; manuscript preparation, R.I.F., J.K.K.; manuscript definition of intellectual content and editing, R.I.F.; manuscript revision/review, R.I.F., J.K.K., M.L., G.A.W.; manuscript final version approval, R.I.F., G.A.W., J.K.K.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMaterials and Methods ResultsDiscussionREFERENCES |
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