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1 Department of Diagnostic Radiology and Organ Imaging, Prince of Wales
Hospital, Ngan Shing St., Shatin, New Territories, Hong Kong.
2 Department of Surgery, Prince of Wales Hospital, Shatin, New Territories, Hong
Kong.
3 Department of Anaesthesia and Intensive Care, Prince of Wales Hospital,
Shatin, New Territories, Hong Kong.
Received May 4, 2004;
accepted after revision July 20, 2004.
Address correspondence to W. W-m. Lam.
Abstract
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SUBJECTS AND METHODS. Cerebral blood flow and extracranial arterial blood flow volume of 35 patients with symptomatic carotid occlusive disease were measured before and after the administration of acetazolamide on stable xenon CT and color velocity imaging quantification, respectively. The changes in unilateral extracranial arterial blood flow volume and respective hemispheric cerebral blood flow were compared. The mean difference in the percentage of change in flow volume, the 95% limit of agreement, and Cohen's kappa coefficient were calculated.
RESULTS. A total of 64 unilateral extracranial arterial blood flow volume changes were successfully compared with the changes in the ipsilateral hemispheric cerebral blood flow. The mean difference in percentage of change in flow volume between the two techniques was 4.7%, with the 95% limit of agreement ranging from -90.2% to 99.7%. Cohen's kappa coefficent was 0.41 (95% confidence interval, 0.13–0.68; p = 0.001).
CONCLUSION. The performance of color velocity imaging quantification for evaluating cerebral vasoreactivity is comparable to that of transcranial Doppler sonography. Because color velocity imaging quantification is not as limited as transcranial Doppler sonography, it could be an ideal complementary tool to transcranial Doppler sonography. More studies are required to define its clinical value.
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Acetazolamide injection is frequently used in clinical settings to evaluate cerebral vasoreactivity. It reduces cerebral vascular resistance with no significant change on cerebral perfusion pressure. A 40% increase in blood flow velocities in the cerebral arteries and a 20–30% increase in cerebral blood flow are expected in the uncompromised brain [4]. By measuring the changes in cerebral blood flow or flow velocity using stable xenon CT (XeCT) and transcranial Doppler sonography, respectively, we may calculate cerebral vasoreactivity [5]. However, stable XeCT imposes radiation hazards, and the success of transcranial Doppler sonography is largely limited by the thickness of the temporal bone [6, 7].
Changes in cerebral blood flow may also be measured by determining the total arterial inflow to the brain from the extracranial carotid and vertebral arteries. We recently reported the successful use of color velocity imaging quantification of the blood flow volume in these arteries [8, 9]. In this study, we investigated the potential value of color velocity imaging quantification to measure acetazolamide-induced cerebral vasoreactivity in patients with cerebrovascular disease.
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Before acetazolamide injection, each patient had a baseline color velocity imaging quantification measurement of the blood flow volume in both the carotid and vertebral arteries. XeCT was then performed before and after acetazolamide administration. The color velocity imaging quantification measurement was repeated after completion of the second XeCT examination. Acetazolamide was not administered to the patients again for the color velocity imaging quantification reestimation because it was considered unethical to give a second injection for research purposes. The sonographer who analyzed the color velocity imaging quantification data and the radiologists who interpreted the XeCT findings were blinded to the results of the other investigation. The color velocity imaging quantification results were then correlated with XeCT findings.
Color Velocity Imaging Quantification
Color velocity imaging quantification, a sonographic technique using time
domain processing, has been shown to be accurate in vitro and in vivo for
estimating blood flow volume in an artery
[8,
9,
11–13].
We measured the blood flow volume in the CCA and vertebral arteries using the
7.5-MHz linear transducer of the sonographic system SD 800 (Philips Medical
Systems) based on the standard color velocity imaging quantification
technique. This technique requires examination of the straight segment of an
artery, use of a large sample volume to encompass the entire vessel wall,
fixed angle correction at 60°, and optimal color setting with no aliasing
or color "bleeding" over the vessel wall (Figs.
1A and
1B). The technique has a
reported inconsistency of 10%. Errors may arise from imprecise angle
correction, turbulent flow, off-axis sampling, and pulsatile flow
[8]. The blood flow volume of
an artery was averaged from three consecutive measurements. Each patient was
allowed to rest on the examination table for at least 10 min before the first
blood flow volume measurement.
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XeCT Technique
XeCT cerebral blood flow studies were performed on a helical CT unit
(HiSpeed Advantage; GE Healthcare). A nonenhanced scan of the brain was first
obtained to locate a standardized plane before xenon inhalation. The
standardized slice selected was one that passed through the basal ganglia
(caudate and putamen), third ventricle, thalamus, and pineal body. The study
involved two baseline scans and six scans at each level of study after the
xenon inhalation started. Each scan contained three contiguous 10-mm cerebral
levels that included the standardized plane. The exposure factors used were 80
kV, 240 mA, and 2 sec. During the examination, patients inhaled 30% xenon and
25% oxygen through a tightly fitted facemask, delivered by a gas delivery
system (Enhancer 3000, XeCT System-2, Diversified Diagnostic Products) for 4
min. Subtraction of the baseline scans from the subsequent enhanced scans gave
a series of images representing the accumulation over time of xenon in the
tissue being studied. The procedure was repeated 15–20 min after IV
injection of 1 g of acetazolamide to the patient.
A computerized cerebral blood flow analysis program was synchronized with CT to calculate the mean XeCT cerebral blood flow on the standardized slice with regions of interest that approximate the vascular territories of the anterior, middle, and posterior cerebral arteries (Figs. 1C and 1D). A wash-in quantitative cerebral blood flow software protocol was used in which all gray matter data and 50% of white matter data were extracted for cerebral blood flow calculation in the first 2 min of xenon administration. With the application of the wash-in method, XeCT is estimated to have an accuracy of ± 5% in high flow and ± 10% in low flow [14].
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Data Analysis
Cerebral blood flow on XeCT was computed using a baseline scan and eight
enhanced scans of the standard slice. The percentage of change in each
hemispheric cerebral blood flow on XeCT before and after acetazolamide
administration was compared with that of the ipsilateral extracranial arterial
blood flow volume, which was equal to the total blood flow volume of the
ipsilateral CCA and two vertebral arteries. Inclusion of the vertebral
arterial blood flow volume is considered crucial because the vertebral
arteries are important collaterals to the anterior cerebral circulation in the
event of proximal carotid stenosis or occlusion
[15].
We measured the agreement of XeCT and color velocity imaging quantification on a plot of the difference in percentage of low-volume changes between XeCT and color velocity imaging quantification against the mean of their percentage of flow volume changes [16]. The mean difference in percentage of flow volume changes within the 95% limit of agreement between XeCT and color velocity imaging quantification was calculated. We also classified the data into positive and negative vasoreactivity. Positive vasoreactivity was defined as a greater than 0% change in the hemispheric cerebral blood flow or unilateral extracranial arterial blood flow volume, and negative vasoreactivity was defined as a change of 0% or less in the respective flow volume levels. Cohen's kappa coefficient was used to measure the chance-corrected agreement between the two techniques, with the level of significance set at a p value of less than 0.05.
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Technical Inaccuracy
Although XeCT is a widely accepted technique coupled with acetazolamide
injection for assessing cerebrovascular reserve in patients with occlusive
carotid disease, some inherent errors are difficult to eliminate. First,
cerebral blood flow values may be significantly affected by tissue
heterogeneity and CT noise. Tissue heterogeneity lowers the blood flow
estimates and is most pronounced in equal mixtures of gray matter and white
matter. Enhancement noise tends to overestimate the derived flow
[17]. Even though the effect
of tissue heterogeneity and CT noise may offset each other, an error in
cerebral blood flow estimation is inevitable. Second, we found that cerebral
blood flow was augmented during inhalation of xenon. A flow activation curve
showed a logarithmic increase in cerebral blood flow in patients with cerebral
disease: between 3% and 7% within the first 90 sec of xenon
"wash-in," 12% after 160 sec, and no further augmentation after
310 sec [18]. In this study,
we used the wash-in technique, which has been suggested to be effective in
minimizing the error of flow activation
[19]. Finally, flow
calculation on XeCT requires knowledge of the xenon concentration in arterial
blood as a function of time. Errors in the estimation of the xenon arrival
time to the brain in relationship to sequential CT time may introduce a
significant error in the determination of arterial blood concentration and
hence blood flow determination
[20].
Color velocity imaging quantification is a technically demanding technique because inaccurate blood flow volume measurement may result from wrong diameter estimation and imprecise angle correction. These errors inevitably occur in great respiratory vessel movement, leading to off-axis sampling, and in tortuous or stenotic segments in which nonlaminar flow is present, preventing accurate angle correction. This is why the CCA segment was sampled in this study instead of the ICA segment, because most of the ICA segments in the study subjects were stenotic or occluded. Even when one uses great caution, errors in blood flow volume measurement are hard to avoid.
Fortunately, the inherent errors in the two techniques should not significantly affect our observations in this study because the errors can be treated as constants.
Study Limitations
In this study, cerebral blood flow measurement and extracranial arterial
blood flow volume quantification after the administration of acetazolamide
were not undertaken simultaneously. The cerebral blood flow measurement was
made 15–20 min after acetazolamide injection, whereas extracranial
arterial blood flow volume was quantified shortly after XeCT, with a 10- to
15-min delay. We believe it unethical to reinject the patients or subject them
to a further test. Although half the acetazolamide was still active after 95
min, its maximal activity on cerebral blood flow occurs at approximately 25
min [21]. These figures imply
that the XeCT measurements were performed in the optimal time range for
acetazolamide, whereas color velocity imaging quantification sampling was
undertaken later. The delay in examination after acetazolamide injection would
have affected the level of flow and therefore the comparability of the two
techniques.
Another possible explanation for the low agreement between color velocity imaging quantification and XeCT is that cerebral vasoreactivity detected on XeCT was made only at three levels of the brain and so was not a full representation of vasoreactivity in the cerebral hemisphere. A thorough study of cerebral vasoreactivity of the whole brain is limited by the speed of the CT scanner and the high radiation dose received by the patients. Conversely, the extracranial arterial blood flow volume measured on color velocity imaging quantification reflects primarily the integrity of the respective hemispheric cerebral vasoreactivity because the external carotid artery flow volume constitutes only about 20–30% of the CCA blood flow volume [22] and is unaffected by acetazolamide administration [23]. The difference analyzed with the two techniques is likely to contribute to the discrepancy in the findings.
Altered Cerebral Hemodynamics in Carotid Occlusion
In patients with severe compromise of cerebral hemodynamics in whom the
primary collaterals in the circle of Willis are involved, the cerebral
circulation increasingly depends on leptomeningeal collaterals, resulting in
negative flow reactivity after acetazolamide administration. Negative flow
vasoreactivity is believed to be caused by blood "stealing" from
the maximally dilated vessels in the circle of Willis to the leptomeningeal
collaterals [24]. Total
extracranial arterial blood flow volume can give a clue to the efficiency of
intracranial collateral circulation
[25]. When leptomeningeal
collaterals are dilated to accommodate more blood flowing through them,
extracranial arterial blood flow volume may rise, leading to false-positive
cerebral vasoreactivity.
Furthermore, because the route of collateral pathways may be on the ipsilateral or contralateral side of the carotid occlusion, depending on the prevailing pressure gradient in the anastomotic areas [25], extracranial arterial blood flow volume that includes flow of only one CCA is likely to miss the collateral flow coming from the contralateral artery and hence fails to account for the percentage of change in the respective hemispheric cerebral blood flow before and after acetazolamide administration, resulting in false-negative cerebral vasoreactivity.
Summary
The limitations of our study design and the altered cerebral hemodynamics
in carotid occlusion are probably the main contributions to the discrepancy,
whereas the potential errors associated with both techniques may be less
significant.
XeCT is an expensive and complex examination necessitating excellent patient cooperation, the presence of an anesthetist, and the use of specialized and expensive equipment. Furthermore, XeCT involves radiation and inhalation of xenon. The radiation dose for XeCT is relatively high because repeated scans are obtained at the same level. The whole-body dose that results mostly from scattered radiation is comparable to typical doses received during 133Xe blood flow studies, but the thyroid dose is likely to be higher with the CT method [26]. Unfortunately, a possible dose reduction is limited by the increase in CT noise [27]. Side effects of xenon inhalation, such as a decrease in respiratory rate, headaches, nausea, vomiting, and convulsions, may occasionally occur [28]. Lower xenon supply may reduce the side effects but also reduces the signal-to-noise ratio and lowers the flow values in all areas of the brain [29]. Optimization of each of the aforesaid parameters is critical in obtaining accurate cerebral blood flow measurements.
Compared with XeCT, sonographic techniques are simpler and radiation-free. In this study, we showed that color velocity imaging quantification measuring extracranial arterial blood flow volume changes can be used to predict cerebral vasoreactivity and has a level of agreement similar to transcranial Doppler sonography when compared with XeCT. Because color velocity imaging quantification samples extracranial arterial segments and does not have the same limitation as transcranial Doppler sonography, our findings suggest that color velocity imaging quantification can be a complementary technique to transcranial Doppler sonography in assessing cerebral vasoreactivity. However, prospective studies are required to define the clinical value of color velocity imaging quantification before it can be used as a clinical tool.
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