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Blood Flow Volume Quantification of Cerebral Ischemia

Comparison of Three Noninvasive Imaging Techniques of Carotid and Vertebral Arteries

¹ All authors: Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, Shatin, Hong Kong, China.

Received July 13, 2001; accepted after revision September 4, 2001.

 
Address correspondence to S. S. Y. Ho.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. Determination of blood flow volume is useful in assessing ischemic cerebrovascular disease. We compared the blood flow volume measurement of three noninvasive imaging techniques, namely color velocity imaging quantification, spectral Doppler imaging quantification, and MR phase-contrast flow quantification, to see how well the flow values determined by each technique agreed with one another.

SUBJECTS AND METHODS. Flow volume quantification was tested experimentally using a flow simulator and by the three techniques in the vertebral and internal carotid arteries of 40 patients with histories of cerebral ischemia. In the flow simulation study, the flow values in each technique were compared with the phantom flow by the Wilcoxon's signed rank test. In the patient study, the flow values between each paired technique were compared by paired t test. The significance level was taken at p less than 0.05.

RESULTS. Flow volumes were measured by color velocity imaging quantification. MR phase-contrast flow quantification agreed with the phantom flow simulation within the tested range, and spectral Doppler imaging quantification values were significantly overestimated. In patients, a large variation of the blood flow volume was obtained between each technique (p < 0.05). Among them, spectral Doppler imaging quantification showed the highest flow values in the vessels (internal carotid arteries, 312.6 mL/min; vertebral arteries, 112.0 mL/min), followed by color velocity imaging quantification (internal carotid arteries, 216.8 mL/min; vertebral arteries, 58.1 mL/min) and MR phase-contrast flow quantification (internal carotid arteries, 169.1 mL/min; vertebral arteries, 66.5 mL/min).

CONCLUSION. Blood flow volume measurements determined by the three noninvasive imaging techniques on the same vessel can differ widely, and spectral Doppler imaging quantification consistently overestimated the flow volume. It is, therefore, essential that the same technique, preferably color velocity imaging quantification or MR phase-contrast flow quantification, be used for clinical follow-up investigations in the future.

Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Accurate quantification of carotid and vertebral blood flow volume has many potential clinical applications in cerebrovascular disease, such as measuring the absolute hemodynamic effect of a carotid stenosis and the associated cerebral atherosclerosis [1, 2], monitoring of cerebral blood flow after carotid endarterectomy [3], investigating vertebrobasilar insufficiency [4], evaluating the vasomotor response of an affected cerebral territory, and determining the adequacy of collateral pathways [5,6,7].

Different noninvasive imaging techniques can quantify blood flow volume among which only sonography and MR phase-contrast flow quantification allow the assessment of individual vessels. Other techniques such as stable xenon CT, single-photon emission computed tomography, and positron emission tomography can only yield regional or total cerebral blood flow.

Our prospective study attempts to compare the flow volume quantification by color velocity imaging quantification, spectral Doppler imaging quantification, and MR phase-contrast flow quantification in a flow simulation phantom and in patients to show how well the blood flow volume measurements determined by these techniques agree with one another.

Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Equipment
The equipment used was an SD800 sonographic system (Philips Medical Systems, Best, The Netherlands) with a 7.5-MHz linear transducer. The system has standard features allowing flow volume measurement by color velocity imaging quantification or spectral Doppler imaging quantification. MR phase-contrast flow quantification and MR angiography were performed using a 1.5-T whole-body MR imaging scanner (Gyroscan, ACSNT; Philips Medical Systems) with a standard head—neck coil.

Phantom Simulation Study
The accuracy of flow volume quantification by the three imaging techniques was validated against an MR-compatible computer-controlled flow simulator (Shelley Medical Imaging Technologies, Ontario, Canada). This flow system can produce simulated physiologic carotid waveforms with a claimed volume flow accuracy of ±1.0%. A tissue-mimicking vascular flow phantom (Shelley Medical Imaging Technologies) with an inner vessel diameter of 4.8 mm was used on sonography. A normal carotid anthropomorphic vascular phantom (Shelley Medical Imaging Technologies) with inner common carotid artery—vessel diameter of 6.4 mm embedded in a rigid transparent acrylic was used in MR phase-contrast flow quantification. Two different vascular phantoms were used because a single phantom is not suitable for both sonography and MR imaging. The vascular phantoms were connected to the flow simulator and loaded with the blood-mimicking fluid, which was a mixture of machine tool—cutting fluid and distilled water. In the sonographic fluid, cellulose particles of 10 mm in diameter were added to provide backscatter signals similar to those of human blood.

The flow rate of the flow simulation system was increased gradually in equal increments of 5 mL/sec peak flow, from 5 mL/sec to 30 mL/sec equivalent to an output of average flow volume of 91.6 mL/min to 549.9 mL/min. For each technique, three flow measurements were made, and the average value was obtained for data analysis.

Any significant deviation of the flow values from the phantom flow in each technique was tested against the Wilcoxon's signed rank test. The significance level was taken at p less than 0.05.

Patient Study
The internal carotid and vertebral arteries of 40 patients with recent cerebral ischemia were investigated by the three techniques within 2 hr. All the patients were referred for sonography of the carotid arteries and MR angiography of the intracranial arteries because of suspected stenosis. The study was approved by the ethics committee of our institution. Informed consent was obtained from each patient before blood flow volume measurement. The order of performing sonography or MR phase-contrast flow quantification was not fixed and depended on the availability of each apparatus. Patients were allowed to rest on the examination table for 10 min before the first blood flow volume measurement. A triple-blinded approach was used in the investigations.

For both spectral Doppler imaging quantification and color velocity imaging quantification, a straight segment of a vessel was selected at least 2 cm above the bifurcation of the internal carotid artery and at any straight interforaminal segment of the vertebral artery. The angle of insonation was fixed at 60°. The sample volume was made large enough to cover the entire vessel diameter. Blood flow quantification was made with at least three cardiac cycles. The blood flow volume was the average of three measurements.

For spectral Doppler imaging quantification, flow volume was calculated manually after the examination using the recorded time-averaged mean velocity and the vessel diameter taken from the same static gray-scale image at the site of interrogation (Fig. 1A). For color velocity imaging quantification, color setting was optimized to avoid aliasing and color-bleed over the vessel wall. Quantification of blood flow volume was computed on the color M-mode automatically by the system software after the image was frozen (Fig. 1B).

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Blood flow volume measurement of internal carotid artery by different techniques in 58-year-old man who recently had minor stroke. Spectral Doppler imaging quantification shows proximal segment of internal carotid artery (ICA). Angle-corrected mean velocity (48.9 cm/sec) and perpendicular vessel diameter (0.43 cm) at site of interrogation were used in calculation of blood flow volume. Obtained value was 426.1 mL/min.

View larger version (109K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Blood flow volume measurement of internal carotid artery by different techniques in 58-year-old man who recently had minor stroke. Color velocity imaging quantification shows blood flow volume measurement of same segment (A). Flow volume of 198 mL/min was computed in this vessel on colour M-mode. Note discrepancy of values between two techniques.

MR angiography of the carotid arteries of the neck was obtained by two-dimensional time-of-flight fast-field echo images in the axial plane with the following parameters: slices, 60; thickness, 3 mm; overlap, 0.6 mm; excitation, 1; field of view, 32 cm; TR/TE, 18/6.7; flip angle, 60°; matrix, 256x256.

MR phase-contrast flow quantification of the internal carotid artery was obtained with a two-dimensional nontriggered phase-contrast pulse sequence. The velocity images were acquired perpendicular to the vessel of interest by adjusting the imaging plane according to the course of the vessels shown on the maximum-intensity-projection MR imaging of the two-dimensional time-of-flight MR angiography. Flow measurement of the internal carotid artery was made at the straight portion of the artery between the bifurcation and the petrous segment at the skull base. The MR phase-contrast flow quantification for the vertebral artery was made at any extracranial straight segment. The phase-contrast flow sequence parameters were the following: slice thickness, 5 mm; excitations, 8; field of view, 26 cm; 30/9.7; flip angle, 150°; matrix, 512x512; velocity encoding, 120 cm/sec. The image acquisition time was 1 min 32 sec for each flow measurement.

Volumetric flow rate was calculated by manually tracing the perimeter of the artery that encompassed all pixels of the vessel on the magnitude image and by transposing this region of interest onto the velocity image (Fig. 1C). The product of time-averaged mean velocity and area on the velocity image in the region of interest gives the volumetric blood flow rate during the acquisition time. The procedures were repeated at three different times by the same operator, and the flow values were averaged.

View larger version (120K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —Blood flow volume measurement of internal carotid artery by different techniques in 58-year-old man who recently had minor stroke. MR phase-contrast flow quantification on high-resolution nontriggered two-dimensional phase-contrast axial images (TR/TE, 30/9.7; flip angle, 150°) shows same internal carotid artery (A) with flow data display. Image was at plane perpendicular to left internal carotid artery on MR angiography. Left upper image is magnitude image on which region of interest (ROI) at left internal carotid artery was drawn. Right upper image is phase image on which ROI drawn at left internal carotid artery on magnitude image was transposed. Respective flow information (3.49 mL/sec) was displayed on lower table corresponding to 209.4 mL/min.

The plots of the difference between the blood flow volume measurements against their mean obtained in any two techniques were drawn to show how well a given pair of the techniques agreed. Limits of agreement were chosen at the 95% difference level. The difference between the blood flow volume measurements in any two techniques was checked by a paired t test at a level of significance of p less than 0.05.

Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Phantom Simulation Study
The flow volume obtained by both color velocity imaging quantification and MR phase-contrast flow quantification agreed with the phantom flow in the tested flow range (Fig. 2) with no significant deviation from the phantom flow (p = 0.075 for color velocity imaging quantification; p = 0.116 for MR phase-contrast flow quantification), although MR phase-contrast flow quantification appeared to under-estimate the actual flow at higher flow rates greater than 275 mL/min. In spectral Doppler imaging quantification, the flow values were consistently higher than those in the phantom flow, more at higher levels, with significant difference shown (p=0.028).

View larger version (12K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —Line graph shows variation of flow volume by different techniques in phantom simulation study. [UNK] = ideal, x = color velocity imaging quantification, = spectral Doppler imaging quantification, = MR phase-contrast flow quantification.

Patient Study
In 40 patients, the blood flow volume of 72 internal carotid arteries and 68 vertebral arteries was successfully measured by the three techniques. Eight internal carotid arteries could not be measured because of three occlusions, three stenoses with considerable poststenotic flow disturbance, and two arteries with tortuous proximal segments. Twelve vertebral arteries could not be measured because of poor flow signals either in a small vessel or in suspected occlusions.

Among the three techniques, color velocity imaging quantification and MR phase-contrast flow quantification showed better agreement in the internal carotid artery and vertebral artery blood flow volume measurements with a smaller mean and range of difference within the 95% limit of agreement (Table 1, Figs. 3A,3B,3C and 4A,4B,4C). However, there was significant difference between the blood flow volume in the internal carotid artery and in the vertebral artery obtained in each paired technique (p<0.05) (Table 2).

View larger version (13K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —Plots show differences between blood flow volume measurements in internal carotid arteries in paired techniques against their mean. Plot shows color velocity imaging quantification versus MR phase-contrast flow quantification.

View larger version (13K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —Plots show differences between blood flow volume measurements in internal carotid arteries in paired techniques against their mean. Plot shows MR phase-contrast flow quantification versus spectral Doppler imaging quantification.

View larger version (14K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —Plots show differences between blood flow volume measurements in internal carotid arteries in paired techniques against their mean. Plot shows color velocity imaging quantification versus spectral Doppler imaging quantification.

View larger version (11K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —Plots of differences between blood flow volume measurements in vertebral arteries in paired techniques against their mean. Plot shows color velocity imaging quantification versus MR phase-contrast flow quantification.

View larger version (11K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —Plots of differences between blood flow volume measurements in vertebral arteries in paired techniques against their mean. Plot shows MR phase-contrast flow quantification versus spectral Doppler imaging quantification.

View larger version (12K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —Plots of differences between blood flow volume measurements in vertebral arteries in paired techniques against their mean. Plot shows color velocity imaging quantification versus spectral Doppler imaging quantification.

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Accurate quantification of blood flow volume in patients is difficult because of many well-documented errors inherent in each measurement technique [8, 9]. Although electromagnetic flowmeter is considered to be a gold standard, it has a reported error of approximately 10% caused by inaccuracies in measuring volume and time intervals [10]. In addition, its applications are limited to intraoperative procedures or animal studies because of its invasiveness. In contrast, both sonography and MR phase-contrast flow quantification are better techniques to use in clinical settings because of their noninvasiveness and their involving no ionizing radiation.

Blood flow volume measurement is commonly estimated by spectral Doppler imaging quantification using the uniform insonation method described by Gill [8], but conflicting results have been documented in the literature concerning its accuracy in blood flow volume quantification both in vitro and in vivo [5, 10,11,12]. In our study, we have also found that spectral Doppler imaging quantification was inaccurate in the measurement of flow volumes in phantom experiments and that its flow values were in poor agreement with the other two techniques in examinations of patients.

In spectral Doppler imaging quantification, the velocity measurement by the uniform insonation technique in which a large sample volume is used to encompass the entire cross section of a vessel depends on the uniformity of the sample volume. Unfortunately, sufficient uniformity of the sample volume is difficult to achieve because most pulsed Doppler systems are designed to achieve high spatial resolution rather than uniformity of insonation [8]. Velocity within a sample volume is not uniform and is affected by the spectral broadening produced by beam focusing [11]. Therefore, the mean flow velocity obtained may not be a true reflection of the average Doppler shift of blood traveling the plane of the sample volume. In addition, the higher ultrasonic intensity on the axis of the beam leads to over-weighting of the higher velocity components at the center of the vessel, resulting in flow overestimation [8]. Another possible source of error comes from inaccurate diameter measurement. Spectral Doppler imaging quantification measures a static vessel diameter to yield the volume flow by ignoring the variation in vessel diameter. A large error in the flow volume measurement is likely to occur because during the cardiac cycle, the vessel diameter changes by approximately 10%. This change implies a 20% error in flow volume measurement if diameter variations are not taken into account [10]. The error is likely to be aggravated in pulsatile vessels in which the flow diameter may be much smaller than the anatomic diameter.

Both color velocity imaging quantification and MR phase-contrast flow quantification were shown to be accurate in vitro. The distinct advantage of color velocity imaging quantification in the acquisition of simultaneous information of mean flow velocity and functional diameter with use of time domain processing may account for the observation. Time domain processing differs from frequency domain processing (autocorrelation) used in the Doppler technique in which the phase shift of echoes is detected; time domain processing uses cross-correlation in which the time shift of the characteristic signals of a group of scatterers is measured [13]. Because the same scan lines are used to produce gray-scale image and flow velocity detection, simultaneous information of mean flow velocity and functional diameter is possible.

Two-dimensional MR phase-contrast flow quantification enables the measurement of time-averaged blood flow and vessel area from a nongated two-dimensional phase-contrast slice with flow encoding perpendicular to the vessel of interest. Total flow across the slice is estimated by integrating the intravascular flow velocity signal over the number of cardiac cycles during data acquisition. As the flow velocity determined in MR phase-contrast flow quantification does not have nonuniformity problems as it does in spectral Doppler imaging quantification, flow volume in conformity with the phantom flow could better be achieved by MR phase-contrast flow quantification.

Flow quantification in patients, however, is more challenging because of technical difficulties compounded by individual physiologic variation, diseased arteries, anatomic variation, and the general condition of patients. Only in ideal conditions are the flow values estimated by the imaging techniques consistent. Therefore, blood flow volume values of the three techniques do not totally agree with one another in measurements of patients.

In color velocity imaging quantification, errors in the blood flow volume quantification may arise from the inaccurate estimation of flow velocity and diameter measurement caused by off-axis sampling, tortuous vessels, turbulent or nonaxial flow, poor color setting, and great respiratory vessel movement [9]. Among all the possible sources of error, patients' respiratory vessel movement, both horizontally and vertically, was difficult to control and could lead to significant off-axis sampling resulting in erroneous diameter and velocity measurement. This source of error is also believed to affect the accuracy of MR phase-contrast flow quantification.

The accuracy of MR phase-contrast flow quantification can also be affected by the effects of acceleration and eddy currents and by partial volume effects, including the effects of finite slice thickness and resolution, pulsatile waveforms, motion, and chemical shift. The reproducibility depends on the signal-to-noise ratio of the data and the strength of the flow encoding and can be degraded by inconsistent definition of the vessel boundary [14]. Among all the possible sources of error, poor resolution of the vessel edge and partial volume effects have been suggested to be the major obstacles to accurate flow measurement [15]. The use of a high-resolution matrix (512 x 512) with an in-plane resolution of 0.5 mm in our study was to improve vessel-edge definition and to reduce the effects of intravoxel dephasing and partial volume averaging.

To minimize error in the assessment of blood flow volume, in particular in the clinical environment, standardized techniques should be applied, and the imaging parameters should be carefully selected to minimize the impact of the potential sources of error discussed previously. However, no matter how careful one is in the choice of imaging parameters, the results obtained from one technique are still in poor agreement with those of another and should not be directly compared. Furthermore, consistent overestimation of volume flow rate in spectral Doppler imaging quantification makes this technique unacceptable in clinical examinations. Therefore, it is recommended that the same imaging technique, preferably color velocity imaging quantification or MR phase-contrast flow quantification, should be considered for clinical follow-up investigations in the future.

References

Top Abstract Introduction Subjects and Methods Results Discussion References

 

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ho, S. S. Y. Articles by Metreweli, C. Search for Related Content PubMed PubMed Citation Articles by Ho, S. S. Y. Articles by Metreweli, C. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?