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DOI:10.2214/AJR.04.1375
AJR 2006; 186:553-555
© American Roentgen Ray Society


Technical Innovation

Visualization and Quantification of Flow and Velocity Fields in Intracranial Arteriovenous Malformations Using Phase-Contrast MR Angiography

John W. Grinstead1,2, Shantanu Sinha1, Satoshi Tateshima3,4, Yih-Lin Nien1 and Fernando Vinuela1

1 Department of Radiological Sciences, University of California at Los Angeles, Ueberroth Bldg., Suite 3371, 10945 LeConte Ave., Los Angeles, CA 90095-7206.
2 Siemens Medical Solutions, Los Angeles, CA 90095.
3 Department of Neurosurgery, Atsugi City Hospital, Atsugi-shi, Kanagawa, Japan, 243-0004.
4 Department of System Design Engineering, Keio University School of Engineering, Kohoku-ku, Yohohama, Japan, 228-8522.

Received August 31, 2004; accepted after revision April 25, 2005.

 
Address correspondence to J. W. Grinstead.


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of this study was to describe postprocessing tools for MR phase-contrast flow quantification images and apply those tools to cerebral arteriovenous malformations (AVMs) to visualize blood flow dynamics noninvasively.

CONCLUSION. Inflow and outflow zones were clearly depicted at different regions in the AVM. The processed images showed flow patterns including vortical flow and variations in velocity over the cardiac cycle. Particle tracking gave an impression of the overall flow state and of the venous drainage system in particular.

Keywords: angiography • cine MRI • congenital malformations • hemodynamics • neuroimaging


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Most risk factors that predispose arteriovenous malformations (AVMs) to hemorrhage affect the status of blood flow through the malformation. Mansmann et al. [1] raised the importance of intracranial AVM hemodynamics to predict hemorrhage risk, although the authors mentioned that it was not easily measurable in a clinical setting. Previous studies have already shown that MR phase-contrast flow quantification is able to measure through-plane flow and velocity in the cerebral arteries [2, 3]. In vivo studies of through-plane and inplane flow dynamics gated phase-contrast flow quantification have not been reported for intracranial AVM to our knowledge. The objective of this study was to develop image processing tools on a modern, flexible software platform for use with PC techniques, which will allow noninvasive measurement of the 3D velocity distribution throughout the cardiac cycle in cerebral AVMs.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Two volunteers were recruited for MRI and signed a consent form approved by our institutional review board. Subject 1 was a 55-year-old man with a left posterior frontal lobe AVM near the motor strip measuring 2 cm in greatest diameter in the nidus and draining into superficial cortical veins. Primary venous drainage of the AVM was a large varix that subsequently drained into the superior sagittal sinus. Subject 2 was a 51-year-old woman with a left occipital AVM measuring 4 cm in greatest diameter draining into both deep and superficial venous systems.

Imaging was performed at 1.5 T (Symphony Quantum, Siemens Medical Solutions). T2-weighted images were used to prescribe the phase-contrast flow quantification slice in the vicinity of the nidus. The encoding velocity (venc) was set at 100 cm/sec because maximal blood velocities within the cerebral arteries are typically below this value even with AVMs present. Other parameters were TE, 6.3 msec; TR between excitation pulses, 19 msec; flip angle, 30°; signal averages, 2; slice thickness, 3 mm; matrix, 256 x 240; field of view, 210 x 197 mm; triggered to 7 cine frames; and total scanning time, 7 min 4 sec.

This study used a routine phase-contrast flow quantification pulse sequence that has been validated in numerous studies [2-4]. Our own validation was conducted using straight, rigid 1/4-inch-diameter tubes connected to an MR-compatible pump with blood-mimicking fluid (CardioFlow 1000MR, Shelley Medical Imaging Technologies) [5] and also with a geometrically realistic in vitro aneurysm model under pulsatile flow conditions. This model compared favorably to laser Doppler velocimetry measurements even in the presence of nonlaminar and vortical flow [6].

The phase-contrast flow quantification images were taken offline, sorted by image series, and imported into Matlab (MathWorks, Inc.) for further processing. Information in the DICOM header allowed the velocity encoding values, encoding direction, temporal resolution, cine frame number, pixel size, and so on to be imported automatically along with the pixel data. The visualization tools we used and developed were previously described in more detail [6, 7]. Briefly, considering an axial slice, the through-plane velocity data (superior-inferior) are plotted as contour maps with isocontour lines separating regions of differing velocity ranges.


Figure 1
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Fig. 1A —55-year-old man with left posterior frontal lobe arteriovenous malformation. Zoom-in shows phase image with through-plane velocity encoding. Average was taken over all frames having through-plane encoding to improve signal-to-noise ratio. Size of image shown is 55 x 45 mm. Points 1, 2, and 3 show locations of measurements plotted in (B). Points 1 and 2 were placed in larger draining vein (varix) and point 3 in smaller draining vein. In this gray-scale image, midgray is zero velocity, black is fluid moving out of plane (superior-inferior), and white is fluid moving into plane (inferior-superior). Particle tracking results are shown with seed points placed at every fifth pixel.

 


Figure 2
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Fig. 1B —55-year-old man with left posterior frontal lobe arteriovenous malformation. Average speed calculated over small circular region of interest (6 pixels) placed at points 1, 2, and 3. Velocity is much higher in smaller draining vein, 3, than in varix, 1 and 2. {diamondsuit} = 1, {blacksquare} = 2, {blacktriangleup} = 3.

 


Figure 3
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Fig. 1C —55-year-old man with left posterior frontal lobe arteriovenous malformation. Velocity vector field superimposed onto through-plane velocity contour map at diastole. Color bar shows velocity scale (cm/sec), with the background color (green) being zero velocity and red and blue corresponding to inferior-superior and superior-inferior motion, respectively.

 
The contour maps were colored as in Doppler sonography with blue and red signifying flow in opposite directions. In-plane velocity data (left-right and posterior-anterior) were superimposed as vector field maps where the arrow length is proportional to speed. The vessels of interest were outlined manually and only those pixels were displayed. In addition, particle paths can be superimposed instead of vector field maps. These paths were calculated from the phase-contrast flow quantification data using simple kinematic equations of motion as described elsewhere [7, 8]. Path seed points can be chosen via mouse clicks or over an automatic range. Path calculation was stopped if it moved outside the vessel of interest. Calculations took approximately 80 msec per seed point on a 2.4-GHz Pentium 4 (Intel) Windows (Microsoft) PC. Regions of interest (ROIs) at various locations throughout the AVM were selected and the average speed was plotted over the cardiac cycle. Importing the data and creating the figures and plots was completed in less than 15 min.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The phase-contrast image of the enlarged draining vessels of subject 1 is shown in Figure 1A, with particle tracking results for automatically placed seed points superimposed. Individual seed points at specific locations can be selected by a mouse click if desired. The software allows any combination of plots to be turned on or off and viewed in cine mode. Flow throughout the draining veins can be seen to follow the contours of the vessel wall. The paths connecting the varix to the smaller draining vein are shown in error because these are separate vascular structures having no anatomic connection. Care should be taken that each vessel be outlined and processed separately, which can be assisted by toggling between the anatomic and phase-contrast flow quantification images.


Figure 4
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Fig. 2 —51-year-old woman with left occipital arteriovenous malformation. Zoom-in on sagittal slice shows dilated vein of Galen with average of magnitude images from phase-contrast flow quantification cine acquisition displayed. Velocity field is shown superimposed over magnitude image at systole. Size of image shown is 35 x 35 mm.

 
Points 1, 2, and 3 in Figure 1A were selected by viewing the velocity cine images to find regions with significant flow variation over the cardiac cycle where one could visualize inflow and outflow zones. The speed at these points is plotted in Figure 1B. The maximum speed in the smaller draining vein at point 3 is approximately 58 cm/sec. The speeds in the larger draining vein (points 1 and 2) are similar throughout the cardiac cycle, and the maximum speed is a factor of 2 less than at point 3.

The contour map and velocity vector field plot are shown at diastole in Figure 1C. The inflow and outflow zones are clearly visualized at different regions of the AVM, with the pair with the maximum velocities in the inferior aspect and two vortices with two different directions of rotations in the upper part of the AVM. Velocity changes between systole and diastole were noticeable throughout the AVM but are most pronounced in the posterior portion and in the smaller draining vein (point 3 in Fig. 1A). The isocontour lines show various zones where fluid is moving into the slice (inferior-superior, colored red) and where they are moving out (superior-inferior, colored blue).

Figure 2 contains a sagittal slice showing the dilated vein of Galen in subject 2. The in-plane velocity at systole is superimposed onto the magnitude image. The vectors follow the path of the vessel as expected, even with the slow flow that is present.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Murayama et al. [9] could perform intravascular sonography velocity measurements during AVM embolotherapy because the draining vein of the animal model had a simple anatomy, making navigation of the guidewire relatively easy. This would not typically be feasible or justifiable in a clinical setting because draining veins regularly have a torturous venous anatomy and a high risk during wire navigation. Phase-contrast flow quantification can measure the flow patterns and velocity in the feeding arteries and draining veins noninvasively. Simple through-plane velocity measurements or 3D velocity studies of selected vessels as shown here are possible.

The software we developed is based on a modern, extensible, and widely used scripting platform that runs on all major operating systems. The postprocessing is not overly time consuming but does require some experience. The time and labor involved is similar to segmenting 3D volume images using a semiautomated algorithm. Some modifications may be required for interpretation in DICOM header information from different software versions because some of the DICOM fields used in phase-contrast flow quantification are not standardized across vendors.

In conclusion, software was developed that allows one to process phase-contrast flow quantification images in a reasonable time on a standard PC platform. The results show flow patterns, vortical flow features, and variations in velocity throughout the cardiac cycle in cerebral AVMs.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Mansmann U, Meisel J, Brock M, Rodesch G, Alvarez H, Lasjaunias P. Factors associated with intracranial hemorrhage in cases of cerebral arteriovenous malformation. Neurosurgery2000; 46:272 -279; discussion 279-281[CrossRef][Medline]
  2. Spilt A, Box FM, van der Geest RJ, et al. Reproducibility of total cerebral blood flow measurements using phase contrast magnetic resonance imaging. J Magn Reson Imaging 2002;16 : 1-5[CrossRef][Medline]
  3. Marks MP, Pelc NJ, Ross MR, Enzmann DR. Determination of cerebral blood flow with a phase-contrast cine MR imaging technique: evaluation of normal subjects and patients with arteriovenous malformations. Radiology 1992;182 : 467-476[Abstract/Free Full Text]
  4. Chatzimavroudis GP, Oshinski JN, Franch RH, Walker PG, Yoganathan AP, Pettigrew RI. Evaluation of the precision of magnetic resonance phase velocity mapping for blood flow measurements. J Cardiovasc Magn Reson 2001; 3:11 -19[CrossRef][Medline]
  5. Sinha S, Hodgson JA, Finni T, Lai AM, Grinstead J, Edgerton VR. Muscle kinematics during isometric contraction: development of phase contrast and spin tag techniques to study healthy and atrophied muscles. J Magn Reson Imaging 2004; 20:1008 -1019[CrossRef][Medline]
  6. Tateshima S, Grinstead J, Sinha S, et al. Intraaneurysmal flow visualization by using phase-contrast magnetic resonance imaging: feasibility study based on a geometrically realistic in vitro aneurysm model. J Neurosurg 2004; 100:1041 -1048[Medline]
  7. Grinstead J, Sinha S. In-plane velocity encoding with coherent steady-state imaging. Magn Reson Med2005; 54:138 -154[Medline]
  8. Buonocore MH. Visualizing blood flow patterns using streamlines, arrows, and particle paths. Magn Reson Med1998; 40:210 -226[Medline]
  9. Murayama Y, Massoud TF, Vinuela F. Hemodynamic changes in arterial feeders and draining veins during embolotherapy of arteriovenous malformations: an experimental study in a swine model. Neurosurgery 1998;43 : 96-104; discussion, 104-106.[CrossRef][Medline]

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