(Stroke. 1995;26:84-89.)
© 1995 American Heart Association, Inc.
Articles |
Hemodynamic Effects of Carotid Endarterectomy by Magnetic Resonance Flow Quantification
From the Departments of Clinical Radiology (R.V., H.M., K.P.), Neurology (K.K.), and Surgery (H.T.), Kuopio University Hospital, Kuopio, Finland.
Correspondence to Ritva Vanninen, MD, Department of Clinical Radiology, Kuopio University Hospital, Puijonlaaksontie 2, SF-70210, Kuopio, Finland.
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Abstract |
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Background and Purpose Blood flow can be evaluated noninvasively using magnetic resonance phase-contrast flow quantification. The purpose of this prospective study was to assess the feasibility of this method and to evaluate the hemodynamic effects of carotid endarterectomy.
Methods Volumetric flow rates and peak systolic velocities of the internal and common carotid and the vertebral arteries were measured by magnetic resonance flow quantification. Sixteen patients undergoing 18 endarterectomies had complete flow data recorded preoperatively and 3 days after surgery.
Results The inverse correlation between the angiographic stenosis degree and the preoperative flow rate in the corresponding internal carotid artery was highly significant (r=-.69, P<.001). After endarterectomy, the mean flow in the ipsilateral internal carotid artery improved from 143 to 233 mL/min (P<.001). The mean peak systolic velocity increased from 23 to 37 cm/s (P<.001). No significant changes were seen in the contralateral carotid or the vertebral arteries. The mean total blood flow improved by 81 mL/min (P=.08). In the severely stenosed bifurcations (70% to 99%, n=11), the flow rate improved by 106 mL/min and in the moderately (30% to 69%, n=4) or mildly (<30%, n=3) stenosed bifurcations by 63 mL/min. If the contralateral carotid artery was occluded or severely stenosed, the improvement was 164 mL/min.
Conclusions Magnetic resonance flow quantification provides a useful tool for the follow-up of the hemodynamic effects of carotid endarterectomy. Our results indicate that surgery is followed by a significant increase of blood flow in the ipsilateral carotid artery and that there appear to be differences in flow increase between subgroups of patients with different degrees of stenosis.
Key Words: carotid arteries • carotid endarterectomy • hemodynamics • magnetic resonance imaging
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Carotid endarterectomy (CEA) of severe stenosis has proven to be highly beneficial in the secondary prevention of stroke.1 2 The more severe the stenosis, the more prominent the risk reduction seems to be.1 The favorable effect of surgery is assumed to be based on the removal of the atheromatous plaque, which can be a source of cerebral emboli. Another explanation is the improvement of blood flow, although the importance of hemodynamic factors in the pathogenesis and treatment of focal cerebral ischemia remains unclear.3 The hemodynamic effects of carotid surgery on both the surgically treated carotid and the collateral artery blood flow, as well as on cerebral perfusion, have been previously evaluated by various radionuclide techniques and by transcranial Doppler ultrasonography.4 5 6
Magnetic resonance (MR) flow quantification with the phase-contrast method has proven to be accurate both in vitro and in vivo in the assessment of flow velocities and volumetric flow rates (VFRs).7 8 9 10 11 12 Previous studies have shown that this totally noninvasive method can provide useful information about the hemodynamic significance of a carotid stenosis.13 Flow quantification easily can be combined with carotid magnetic resonance angiography (MRA) or imaging (MRI) of the brain. Both the VFR and the peak systolic velocity, measured in the diseased internal carotid artery (ICA) distal to the stenosis, seem to have a significant inverse correlation with the degree of angiographic stenosis.14 MR flow quantification now offers a new noninvasive supplement for the follow-up of patients undergoing CEA.
The purpose of this prospective study was to assess the feasibility of MR phase-contrast flow quantification in the evaluation of the hemodynamic effects of CEA. With this aim we measured the VFRs and peak systolic velocities of both the ICAs and vertebral arteries before and after surgery in 16 patients undergoing 18 CEAs.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Patients
Twenty-five patients underwent 27 CEAs during the study period. The decision to perform CEA was based on neurological symptoms and the findings in conventional angiography. The degree of stenosis in the angiographic images was measured according to the North American Symptomatic Carotid Endarterectomy Trial (NASCET) measurement criteria.1 Based on the findings in preoperative angiography, there were no cases of retrograde flow in the ophthalmic artery on the side to be operated on, and there were no cases of subclavian steal. A standard CEA was performed with the patient under general anesthesia. A patch closure was used in two operations, and the artery was closed directly in the other operations.
Twenty-three of these patients underwent MR flow quantification preoperatively within 2 months of conventional angiography. In one case, MR measurement could not be performed because the morbidly obese patient could not fit into the MRI tube (diameter, 60 cm). One patient refused the attempted measurement because of severe back pain. In three cases, the results of at least one of the two measurements were considered unreliable because of movement artifacts in one and technical failure in two cases.
MR flow quantification was repeated after CEA before patients were discharged from the hospital, usually 3 days after surgery. Two patients refused the postoperative flow measurements, and in one case the postoperative measurements were unsuccessful because of patient movement. One patient developed transient ischemic symptoms after CEA, and the subsequent Doppler sonography and contrast angiography revealed an intimal flap causing flow restriction. This patient was excluded from the statistical analysis.
Therefore, 16 patients undergoing 18 CEAs had complete flow data
recorded before and after surgery and were included in the statistical
analysis. Of the operated arteries, 11 were severely (70% to
99%), 4 were moderately (30% to 69%), and 3 were mildly (<30%)
stenosed. No significant tandem lesions were seen. Nine of the CEAs
were performed on the right, and 9 were on the left side. The patency
of the carotid artery after surgery was confirmed by MRA (14
operations) or both MRA and duplex-Doppler (4 operations). The
demographic data of the patients are given in Table 1
.
Informed consent was obtained from all patients, and the study was
approved by the ethics committee of the hospital.
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Magnetic Resonance Flow Quantification
All MR flow measurements of the patients were performed with a
1.5-T whole-body imaging system (Siemens Magnetom) using commercially
available neck and head coils. The two-dimensional phase-contrast
measurements were performed with a fast low-angle shot (FLASH)–type
gradient-echo sequence at two levels and with electrocardiographic
triggering. Flow perpendicular to the imaging plane creates phase
shifts that can be converted into velocity values. Two views are
acquired at each phase-encoding step, and the phase difference between
these two images for any given pixel is related directly to the flow
velocity along the axis of the applied bipolar pulse. The other factors
that affect the phase portion (magnetic field inhomogeneity, eddy
currents, radio frequency penetration, pulse sequence timing) can be
subtracted by acquiring two images that differ only in the first moment
of the gradient waveform.7
The direction of the corresponding artery was first assessed by an
anatomic localizer image. The first measurement, using the neck coil,
was performed approximately 3 cm below the carotid bifurcation (Fig 1). The VFRs and peak systolic velocities of the common
carotid artery (CCA) and vertebral artery were assessed. To measure the
velocity parameters of the ICA, using the head coil, the second
measurement was performed at the level of the skull base, distal to the
stenosed part of the vessel to avoid the turbulent flow and velocity
jets associated with tight stenoses that cause potential errors in the
measured flow values.13 Both imaging planes were placed
perpendicular to the direction of the vessel. The following parameters
were used: repetition time, depending on the RR interval with a minimum
of 30 milliseconds; echo time, 6 milliseconds; flip angle, 20°; field
of view, 220 mm; matrix, 192x256; and slice thickness, 6 mm. Velocity
encoding (VENC) was 120 cm/s for arterial flow to avoid
aliasing.7 A maximum of 32 two-dimensional
velocity-encoded phase images per cardiac cycle was achieved. The
examination time was approximately 15 to 20 minutes for the two
measurements.
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The lumen of each vessel was carefully evaluated at the peak systolic phase image, and the area of the lumen was used as the region of interest (ROI) for the volumetric flow and velocity quantification program. This ROI was applied throughout the whole series of the 32 two-dimensional velocity-encoded phase images, yielding values that represent the average VFR within the vessel over the cardiac cycle. To measure the maximal peak systolic velocity, an ROI of only one pixel was selected in the area of the maximal intraluminal signal intensity, usually in the middle of the vessel lumen in laminar flow.
Statistical Analysis
The Pearson correlation coefficient was first calculated between
the angiographic stenosis degree and the preoperative VFR and peak
systolic velocity in the ICA. Because there was no statistically
significant correlation between the degrees of stenosis of the right
and left carotid bifurcations of each individual patient, all
bifurcations (n=32) were included in this analysis. The Pearson
correlation coefficient was also calculated between the stenosis degree
of the operated artery and the measured flow increment. All MR flow
variables were tested for normal distribution by the Kolmogorov-Smirnov
one-sample test. Based on acceptable normality, the differences between
the preoperative and postoperative flow values were tested using the
paired t test. For the purposes of this analysis, data
on the carotid arteries were divided into operated and contralateral
sides, and data on the right and left sides were not analyzed
separately. The differences were considered statistically significant
if the probability value was <.05. All data were analyzed using the
SPSS/PC+5.01 (SPSS) statistical package.
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Results |
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There was a highly significant inverse correlation of r=-.69 (P<.001) between the angiographic stenosis degree and the preoperative VFR in the corresponding ICA distal to the stenosis. The correlation coefficient was r=-.51 (P<.001) between the stenosis degree and the peak systolic velocity in the ICA.
The preoperative and postoperative VFRs in the ICAs, CCAs, and
vertebral arteries are shown in Table 2, and the
alterations in the carotid flow rates are shown graphically in Fig 2. The flow values improved significantly from 143 to
233 mL/min after endarterectomy in the ipsilateral ICAs; the mean
improvement was 90 mL/min (95% confidence interval [CI], 54 to 124
mL/min), representing a 63% increase in the preoperative flow rate
(P<.001). In the ipsilateral CCAs, the mean improvements
were 76 mL/min (95% CI, -8 to 160 mL/min) and 28%
(P=.07), respectively. No significant changes were seen in
the contralateral ICAs or CCAs or in the vertebral arteries. The total
blood flow (TBF) was calculated as the sum of the VFRs in the right and
left ICAs and the vertebral arteries. The mean TBF improved on the
average by 81 mL/min (95% CI, -11 to 173 mL/min) after CEA, which was
a 14% increase from the value measured before surgery
(P=.08).
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The operated carotid bifurcations were then divided into two subgroups, the severely stenosed (70% to 99%) and moderately stenosed (<70%), according to the angiographic stenosis degree. The mean preoperative VFR was 120 mL/min in the severely stenosed ICAs (n=11) and 181 mL/min in the moderately stenosed group (n=7). The flow rate in the ICA improved after CEA more clearly in the group of severely stenosed bifurcations, the mean improvement being 106 mL/min (95% CI, 68 to 144 mL/min). If the bifurcation was not severely stenosed, the mean improvement was 63 mL/min (95% CI, -17 to 141 mL/min). The ratio of operated ICA to TBF increased after CEA from 0.22 to 0.36 in the severely stenosed group; this was clearly more than in the moderately stenosed group, which showed an increase from 0.31 to 0.36. The correlation coefficient was .51 (P=.03) between the percentage of stenosis degree of the operated artery and the measured flow increment in the ipsilateral ICA, and .69 (P<.01) between the stenosis degree and the increase in the ratio of operated ICA to TBF, respectively.
The hemodynamic improvement after CEA also depended on the degree of stenosis of the contralateral ICA. One patient undergoing bilateral CEA had severe stenoses on both sides, one patient had an occlusion on the contralateral side, and in one patient the contralateral bifurcation was virtually occluded, with only hairline patency in the preoperative angiography. In these three cases, the mean flow rate in the operated ICA increased from the preoperative 198 mL/min (35% of the TBF) to 362 mL/min (56% of the TBF) after surgery. Thus, the increment was 164 mL/min (standard error, 7 mL/min), clearly more than in the group of patients with less severely stenosed contralateral bifurcations, who showed an increment of 80 mL/min (standard error, 19 mL/min).
The peak systolic velocities in the ICAs distal to the stenosis were also measured. On the operated side, the mean peak systolic velocity was 23 cm/s preoperatively and increased to 37 cm/s postoperatively (P<.001). On the contralateral side, the corresponding velocities were 30 cm/s and 28 cm/s (NS). The ipsilateral improvement was again more prominent in the severely stenosed arteries (from 21 to 37 cm/s; P=.003) than in the less severely stenosed bifurcations (from 26 to 37 cm/s; P=.05).
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Discussion |
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MR phase-contrast flow quantification seems to be a promising new method for carotid flow measurement. It is totally noninvasive and safe and does not require the use of ionizing radiation or radionuclide injections. Unlike Doppler sonography, MR flow measurements can be performed at any desired level of a vessel and are not affected by anatomic limitations caused by bone or gas or by pathological conditions such as calcified plaques in the arterial wall. In addition, it can be used for VFR measurements, unlike Doppler sonography, which is not considered to be a reliable method for volumetric flow measurements at present and is used mainly to measure blood velocity in clinical work.15 MR flow quantification also provides a potentially useful tool for the postoperative follow-up of the hemodynamic effects of CEA. To our knowledge, MR flow quantification has not been used previously in the postoperative evaluation of these patients.
The limitations of MR quantification are its limited availability and its vulnerability to patient movement during the measurement. Two patients in the present study were excluded because of movement artifacts. In addition, there were two software-related technical failures in the early phase of our experience, and in one case the examination failed because of morbid obesity. Preoperatively, 4 of the attempted 24 examinations (17%) failed. In addition, 1 of the remaining 20 postoperative measurements (5%) failed. In general, the feasibility of the method was relatively good.
In theory, the evaluation of the velocity images resulting from cine phase-contrast imaging should not require exact vessel-edge detection for accurate flow measurements. However, a recent report by Burkart et al16 has shown that differences in user-specified ROIs can lead to variability of VFRs between users. They have developed an automated method of vessel-edge detection that shows promise for improving the precision of cine phase-contrast flow measurements. In the present study, all measurements were performed by the same observer. The VENC for the phase-contrast flow measurements is selected so that it is a little higher than the highest expected peak velocity in the corresponding artery. Our previous study in 10 normal volunteers has shown mean CCA velocities of 77±14 cm/s,14 and a VENC of 120 cm/s was selected. The same VENC was used in the two measurements. However, a VENC of 80 cm/s would have been more appropriate for the ICAs and vertebral arteries in the present study.
Another possible source of error in the absolute flow values is associated with the "eddy current" effect. Ideally, the observed phase shifts are due only to motioninduced effects. However, eddy current effects are often observable as non–zero velocities in structures known to be static. Velocity data can be corrected using background ROIs in regions known to be static. These background-noise suppression techniques were not used in this study.
The use of MR phase-contrast velocity and flow techniques is relatively well established in normal vessels, but studies concerning stenosed vessels are limited. Artifacts caused by turbulence just distal to the stenosis must be considered. In the present study, the ICA flow measurement was placed as far away from the stenosis as possible. Previous studies concerning carotid artery MR flow measurements have shown that the measured VFRs in the ICAs are proportional to the inverse of the measured percentage of stenosis.14 A correlation coefficient of r=.84 (P<.01) has been recently reported between conventional angiography and MR flow quantification in a study involving 11 symptomatic patients.13 The corresponding correlation coefficient in the present sample of 32 bifurcations was r=.69 (P<.001). Several studies have also reported a significant correlation between the measured carotid peak systolic velocities by Doppler sonography and MR velocity measurements.13 17 18 In addition, VFRs and peak systolic velocities measured by MR have been reported to be significantly elevated in patients with arteriovenous malformations.19
Conflicting results have been published about the effects of CEA on cerebral blood flow (CBF), reporting either no change or an increased CBF.3 4 5 These discrepancies can be explained in part by the use of different measurement methods and different timing after CEA. Accurate evaluation of the hemodynamic effects of a carotid stenosis and its surgical treatment on the cerebral circulation can be made only by taking into account the contribution of the collateral circulatory pathways to the circle of Willis (the contralateral ICA and vertebral arteries) as well as the possible collateral vessels developed from the branches of the external carotid artery.
Boysen et al5 have previously performed preoperative and
postoperative carotid flow measurements in a series of 17 patients. In
their work, mean blood flow in the ICA increased from 133 to 212 mL/min
postoperatively, which is comparable to the results of the present
study demonstrating an increase from 143 to 233 mL/min postoperatively.
Their work, using a square-wave electromagnetic flowmeter for the ICA
flow measurements and the 133Xe-injection technique for the
regional CBF measurements, also indicated that surgery is followed by a
redistribution of the blood supply from previously adequate collateral
pathways back to the ipsilateral ICA. In the early postoperative
measurements of the present study, the mean flow in the operated
ICA increased by 90 mL/min, whereas the collateral flow decreased only
slightly by 5 mL/min in the contralateral ICA and by 3 mL/min in the
vertebral arteries. The increase in the TBF, calculated as the sum of
the VFRs in the ICAs and vertebral arteries, was 81 mL/min. Thus, our
data exhibit a good correlation between the flow increase in the
operated artery and the overall CBF, even if the last data are not
statistically significant (Table 2
).
Cerebrovascular hemodynamic changes associated with CEA seem to be dependent on the interval between the operation and the control measurement. In studies using intracarotid injection of 133Xe during surgery, CBF has been shown to increase after the removal of a tight stenosis.20 21 Bishop et al4 measured CBF before and after CEA in 14 patients using the intravenous 133Xe technique. They detected significantly increased flow in both hemispheres 3 hours postoperatively, and the CBF was still elevated 2 days after surgery, although the increase was no longer significant statistically in concordance with the results of the present study.
In addition to the differences in the short- and long-term hemodynamic
effects, there also seem to be differences between subgroups of
patients with different degrees of stenosis. Araki et al6
have used transcranial Doppler measurements of flow velocities in the
anterior and middle cerebral arteries before and after CEA. They
reported a significant ipsilateral increase in the velocities of both
arteries in the immediate postoperative period. Furthermore, the
velocity in the middle cerebral artery remained elevated on the second
follow-up study 
30 days after surgery. However, in patients with
moderate stenosis (<75%), no significant changes as measured by
transcranial Doppler were found. These results are in concordance with
the present study, in which the improvement of VFR in the ICA after
CEA was less significant in the subgroup of mildly or moderately
stenosed ICAs than in the subgroup of patients with severe stenosis.
The present study also indicates that the flow improvement achieved
by CEA in a severely stenosed ICA is dependent on the patency of the
contralateral ICA.
The angiographic stenosis degree, according to the NASCET measurement
criteria applied in the present study, was mild (<30%) in three
of the operated carotid bifurcations. In two of these cases, the
postoperative flow rates in the operated ICAs were actually lower than
in the preoperative ones. The VFR ratio (operated ICA/TBF) did not
increase in these three CEAs, unlike in the moderately or severely
stenosed operated ICAs (Fig 3). These patients were
included in the European Carotid Surgery Trial (ECST), and the decision
for operation was made based on the ECST measurement
criteria.2 It has been previously shown that these
measurement methods can give significantly different degrees of
stenosis and can lead to different clinical
decisions.22 23
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The average rate of flow through the adult brain is 750 mL/min.24 In healthy adults, the measured CBF values obtained by MR flow quantification have been similar to the values obtained by other methods.19 24 25 26 However, there are two reasons why the measured TBF in this study does not necessarily represent the exact total CBF. First, the VFR of the ICA was measured at the level of the skull base, which means that the possible collateral flow through the ophthalmic artery or the leptomeningeal collaterals was not included in the calculations. Second, the sum of the flow rates in both the vertebral arteries also includes the flow within spinal branches of the vertebral arteries. Marks et al19 performed MR phase-contrast flow measurements in patients with arteriovenous malformations and calculated the total CBF as the sum of the flow rates in the internal and basilar arteries. Their method does not include the flow through the posterior and anterior cerebellar arteries in the total CBF calculations. In the present cohort of neurologically symptomatic elderly patients with proven cerebrovascular disease, both the mean preoperative (583 mL/min) and postoperative TBFs (664 mL/min) were somewhat lower than the reported average values for healthy individuals. A decline in CBF with advancing age has been reported both in cross-sectional and longitudinal analyses.25 26 27 28 29 30 This decline seems to be more prominent in patients with cerebrovascular disease.28
In conclusion, MR phase-contrast flow quantification provides a new noninvasive method for the measurement of carotid hemodynamics. It can be used to monitor the effects of surgical therapy on carotid flow and the cerebral circulation and will hopefully lead to a better understanding of the hemodynamic effects of CEA. It must be realized, however, that MR flow quantification is still in its infancy and that further studies with larger patient populations are needed to evaluate this new clinical tool.
Received June 14, 1994; revision received October 10, 1994; accepted October 11, 1994.
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D. R. Rutgers, J. D. Blankensteijn, and J. van der Grond Preoperative MRA Flow Quantification in CEA Patients : Flow Differences Between Patients Who Develop Cerebral Ischemia and Patients Who Do Not Develop Cerebral Ischemia During Cross-Clamping of the Carotid Artery Stroke, December 1, 2000; 31(12): 3021 - 3028. [Abstract] [Full Text] [PDF]
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L. J. Kappelle, M. Eliasziw, A. J. Fox, B. L. Sharpe, and H. J. M. Barnett Importance of Intracranial Atherosclerotic Disease in Patients With Symptomatic Stenosis of the Internal Carotid Artery Stroke, February 1, 1999; 30(2): 282 - 286. [Abstract] [Full Text] [PDF]
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M. Kluytmans, J. van der Grond, B. C. Eikelboom, and M. A. Viergever Long-Term Hemodynamic Effects of Carotid Endarterectomy Stroke, August 1, 1998; 29(8): 1567 - 1572. [Abstract] [Full Text] [PDF]
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E. J. Heyer, D. C. Adams, R. A. Solomon, G. J. Todd, D. O. Quest, D. J. McMahon, S. D. Steneck, T. F. Choudhri, and E. S. Connolly Neuropsychometric Changes in Patients After Carotid Endarterectomy Stroke, June 1, 1998; 29(6): 1110 - 1115. [Abstract] [Full Text] [PDF]
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K. J. van Everdingen, C. J. M. Klijn, L. J. Kappelle, W. P. T. M. Mali, and J. van der Grond MRA Flow Quantification in Patients With a Symptomatic Internal Carotid Artery Occlusion Stroke, August 1, 1997; 28(8): 1595 - 1600. [Abstract] [Full Text]
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J. van der Grond, B.C. Eikelboom, and W.P.Th.M. Mali Flow-Related Anaerobic Metabolic Changes in Patients With Severe Stenosis of the Internal Carotid Artery Stroke, November 1, 1996; 27(11): 2026 - 2032. [Abstract] [Full Text]
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