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(Stroke. 1997;28:1345-1350.)
© 1997 American Heart Association, Inc.


Articles

Continuous Intraoperative Monitoring of Middle Cerebral Artery Blood Flow Velocities and Electroencephalography During Carotid Endarterectomy

A Comparison of the Two Methods to Detect Cerebral Ischemia

Marcel Arnold, MD; Matthias Sturzenegger, MD; Leonard Schäffler, MD; Rolf W. Seiler, MD

From the Departments of Neurology (M.A., M.S., L.S.) and Neurosurgery (R.W.S.), University of Berne (Switzerland).

Correspondence to M. Sturzenegger, MD, Department of Neurology, University of Berne, Inselspital, Murtenstrasse, CH-3010 Berne, Switzerland.


*    Abstract
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*Abstract
down arrowIntroduction
down arrowSubjects and Methods
down arrowResults
down arrowDiscussion
down arrowReferences
 
Background and Purpose Intraoperative monitoring of brain function may influence the outcome of carotid endarterectomy (CEA).

Methods We performed transcranial Doppler (TCD) monitoring of middle cerebral artery blood flow velocities (VMCAs) and eight-channel electroencephalographic (EEG) recording simultaneously in 82 patients undergoing CEA. Thiopental narcosis limited EEG interpretation in 11 patients, thus allowing direct comparison of both methods in 71 patients.

Results There was a significant correlation between VMCA decrease and the frequency of EEG changes after carotid clamping (P<.001). Eight patients (11%) showed a VMCA decrease exceeding 60%, accompanied by EEG changes in 7 patients. Altogether, 16 patients (22%) showed severe or moderate EEG changes. Stenosis or occlusion of the contralateral carotid artery led to an increase of abnormal findings with both monitoring methods, which was, however, significant only for TCD (P<.05). Four patients (4.8%) suffered intraoperative transient ischemic attacks. In 3 of these patients, there were no abnormal findings with either of the methods. The events were thus unpredictable and probably of embolic origin. The fourth patient showed VMCA decrease to 0 and severe EEG changes. Nine patients had severe or moderate EEG changes without significant VMCA decrease and without complications. EEG monitoring alone in these would have led to unnecessary use of a shunt with the increased risk of embolism.

Conclusion EEG and TCD monitoring are complementary techniques. Their results showed a good overall correlation but with marked differences in the individual patient. TCD monitoring alone was sensitive enough to prevent ischemic intraoperative complications. EEG findings are of limited value when barbiturates are used.


Key Words: electroencephalography • blood flow velocity • carotid endarterectomy • diagnostic imaging • ultrasonics


*    Introduction
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up arrowAbstract
*Introduction
down arrowSubjects and Methods
down arrowResults
down arrowDiscussion
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Major randomized trials of CEA for symptomatic high-grade ICA stenosis demonstrate an absolute risk reduction for stroke and death of 9.6% at 3 years and for ipsilateral stroke of 17% at 2 years.1 2 The benefit from surgery critically depends on a low perioperative complication rate that is between 1% and 6% in centers with experienced surgeons.2 3 4 5 With a perioperative morbidity and mortality exceeding 9%, the benefit is lost.6

Major complications are cerebral events due to embolization from the operation area, ischemia following carotid cross clamping when collateral circulation is insufficient, postoperative occlusive thrombosis, or postoperative hyperperfusion states. Next frequent and equally serious are cardiac complications.

To prevent hemodynamically induced strokes due to carotid cross clamping, most surgeons perform a selective shunting based on one or several monitoring methods. Methods applied include EEG monitoring,7 8 9 TCD,4 10 11 measurement of carotid stump pressure,10 12 monitoring with somatosensory evoked potentials,13 14 determination of regional cerebral blood flow,7 and clinical neurological evaluation while performing operations with patients under local anesthesia.15 16 An ideal monitoring system should provide continuous information about intraoperative cerebral circulation and/or function. It should be easy to interpret and alert the surgeon before the occurrence of irreversible structural lesions.

EEG permits noninvasive continuous monitoring of bioelectrical activity of the superficial hemispheric cortex. It is the most widely used and best documented method.7 8 9 Many surgeons base their decisions to use an intraluminal shunt on EEG results alone.8 17 18 The striking difference between the high incidence of EEG changes and the rare occurrence of neurological complications when patients are operated on without a shunt suggests the oversensitivity of this method.18 19 20 21

TCD allows continuous noninvasive measurement of VMCA.22

Several studies have reported a close correlation between measurements of stump pressure and TCD monitoring.10 11 12 23 Only a few studies have compared the two continuous monitoring methods, TCD and EEG, and their results are conflicting.11 12 24 25 26 The disparity of the results from the literature are certainly due to methodological differences, such as not considering the influence of anesthesia, definition and grading of EEG changes, numbers of EEG channels recorded, and method of analysis (computerized versus visual analysis by an experienced neurologist). Therefore, we decided to compare retrospectively the results of both methods in our patients. We considered the following criteria: (1) degree of changes in both methods and their correlation, (2) influence of contralateral carotid lesions, (3) shunt rates, and (4) ability to predict complications. The comparison focused on findings relevant for patient management.


*    Subjects and Methods
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up arrowAbstract
up arrowIntroduction
*Subjects and Methods
down arrowResults
down arrowDiscussion
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We analyzed the findings in 82 of 87 CEAs performed on 77 patients at the Department of Neurosurgery, University of Berne (Switzerland), during a 3-year period. Five patients had staged operations on both carotid arteries. Five patients were excluded for different reasons: impossibility of finding a temporal "bone window" (3 patients), incomplete data (1 patient), and erroneous insonation of posterior cerebral artery with a definite increase of flow velocity after cross clamping (1 patient). None of these 5 patients suffered a complication. Sixteen operations (20%) were performed in women (age range, 56 to 80 years), and 66 were performed in men (age range, 60 to 80 years). The average age of all patients at the time of surgery was 65 years.

For the analysis of EEG findings, we reviewed the anesthesia recordings for possible influence of the applied anesthetics and blood pressure variations. Indications for operation were TIA in 26 patients, minor stroke in 21 patients, prolonged reversible ischemic neurological deficit in 15 patients, amaurosis fugax in 15 patients, and asymptomatic high-grade stenosis in 5 patients.

Eleven patients had brain protection with thiopental at a dosage inducing burst suppression activity on EEG monitoring. These patients had either an occlusion or a high-grade stenosis of the contralateral carotid artery or local anatomic conditions preventing easy shunt placement, such as high carotid bifurcation, long atheromatous plaque, or severe kinking or coiling.

All 82 patients were continuously monitored by eight-channel EEG, and the recordings were supervised by an experienced neurologist in the operating room.

Continuous TCD monitoring was started before carotid cross clamping and performed at least 10 minutes beyond clamp release. We used a 2-MHz pulsed Doppler transducer fixed with a head strap over the temporal bone. The mean maximal VMCA was continuously measured at an insonation depth of 45 to 55 mm. After induction of anesthesia, we usually observed a mild drop of VMCA. The subsequently stable values during at least 5 minutes were taken for baseline. The patients were divided into four groups according to the percent decrease of VMCA from baseline values: (1) 0% to 20%, (2) 20% to 40%, (3) 40% to 60%, and (4) 60% to 100%. A temporary intraluminal shunt was used when VMCA decrease exceeded 60% after cross clamping.

EEG changes occurring during the first 4 minutes after cross clamping were graded into four categories: (1) none, (2) mild (increase of theta waves <25% and/or decrease of amplitude >50% compared with the EEG before clamping), (3) moderate (increase of theta waves >25% or increase of delta waves <25% compared with preclamp EEG), and (4) severe (increase of delta waves >25% or severe flattening of amplitude or isoelectric curve). In the patient group with thiopental-induced burst suppression activity, we could only consider asymmetries between the hemispheres.

Contralateral ICA stenosis was graded according to the results of preoperative Doppler examination and to measurement of distal and local degree of stenosis at angiography.27 In three patients with differing results as assessed by these two methods, we gave preference to Doppler grading, which is more relevant for hemodynamic reasons.

Complications were divided into "intraoperative," encompassing those detected immediately after awakening from anesthesia, and "postoperative," ie, those occurring in the course of the first postoperative week.

Statistical analysis was performed using the SPSSX statistical package (SPSS Inc; 3rd edition). We compared (1) VMCA decrease and frequency of intraoperative EEG changes ({chi}2 test), (2) mean VMCA decrease and intraoperative EEG changes (Mann-Whitney U test), (3) VMCA decrease and degree of contralateral carotid stenosis (Mann-Whitney U test), (4) intraoperative EEG changes and degree of contralateral carotid stenosis ({chi}2 test), and (5) shunt rates and degree of contralateral carotid stenosis ({chi}2 test).


*    Results
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up arrowSubjects and Methods
*Results
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Cross clamping resulted in an average VMCA decrease of 32% (SD, 30%) in the whole group (n=82). Thirty-nine patients (47%) showed a 0% to 20% decrease, 23 patients (28%) a 20% to 40% decrease, 8 patients (10%) a 40% to 60% decrease, and 12 patients (15%) a 60% to 100% decrease. In the group without thiopental anesthesia (n=71), EEG changes occurred in 20 patients (28%): 8 were located over the hemisphere ipsilateral to the operated carotid artery, 11 were bilateral with ipsilateral predominance, and 1 was bilateral symmetrically. Four (6%) of these EEG changes were mild, 11 (15%) were moderate, and five (7%) were severe. In the thiopental group (n=11), 3 patients showed EEG asymmetries.

TCD and EEG changes were compared in the patient group without thiopental protection (n=71): EEG changes were found in 3 (8%) of 36 patients with a VMCA decrease of 0% to 20%, in 5 (36%) of 19 patients with a VMCA decrease of 20% to 40%, in 5 (63%) of 8 patients with a VMCA decrease of 40% to 60%, and in 7 (88%) of 8 patients with a VMCA decrease of >60%. There was a significant correlation between the percent decrease of VMCA and the incidence of EEG changes (P<.001). Patients without EEG changes after cross clamping (n=51) had a mean VMCA decrease of 20%, compared with 53% in the patient group with EEG changes (n=20) (P<.001). Fig 1Down shows the distribution of the graded EEG changes in the four groups according to VMCA decrease. Fig 2Down illustrates the individual variability of EEG changes and TCD findings; this variability was marked.



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Figure 1. Correlation between decrease of VMCA and EEG changes during carotid cross clamping (patient group without thiopental anesthesia). Mild, moderate, and severe indicate the graded EEG changes, and total indicates the sum of all grades of EEG changes. The numbers on the top of the bars indicate absolute patient numbers. {chi}2 analysis showed a significant (P<.001) correlation between the decrease of VMCA (%) and the incidence of EEG changes.



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Figure 2. Variation of TCD findings and EEG changes during cross clamping in the individual patients. Horizontal bars indicate the mean percentage decrease of VMCA in the four categories of EEG changes.

The mean decrease of VMCA following clamping was significantly higher (P<.01) in a contralateral stenosed or occluded carotid artery (n=25) compared with a normal contralateral carotid artery (n=57). Furthermore, stenosis or occlusion of the contralateral ICA was associated with a higher incidence of abnormal EEG findings, which was, however, not significant (P>.5). TCD and EEG findings in relation to graded contralateral carotid artery lesions are listed in Table 1Down.


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Table 1. Influence of Contralateral Carotid Artery Lesions on TCD and EEG Changes

Twelve (15%) of 82 patients had a temporary intraluminal shunt implanted because of a VMCA decrease exceeding 60%. Eight of them had no thiopental protection. Shunt rates in the four groups according to VMCA decrease in relation to contralateral carotid lesions are listed in Table 2Down. A shunt was required significantly more often in patients with a contralateral stenosed or occluded carotid artery (10 [40%] of 25 patients) compared with a normal carotid artery (2 [4%] of 57 patients) (P<.001).


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Table 2. Temporary Intraoperative Shunting Depending on Contralateral Carotid Artery Lesions

Cerebral complications occurred in 7 patients: 4 suffered an intraoperative ipsilateral TIA, 1 a postoperative TIA, and 2 a postoperative stroke. Results of both monitoring methods and the influence of contralateral carotid lesions in these patients are listed in Tables 3Down and 4Down. The overall combined stroke and death rate was 3.6% (3 of 82 patients).


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Table 3. Intraoperative Complications


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Table 4. Postoperative Complications


*    Discussion
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
*Discussion
down arrowReferences
 
Main cerebral complications of CEA result from hemodynamic or embolic events due to the surgical procedure. Careful preparation of the arteries can prevent embolism from friable plaques. The risk of critical reduction of cerebral perfusion may be avoided by temporary shunting, which, however, prolongs operation time and increases the risk of embolism. Various monitoring methods intraoperatively assessing either brain function (eg, EEG, evoked potentials) or cerebral circulation (eg, TCD, regional cerebral blood flow) have been used to reduce perioperative complications. Both EEG and TCD allow for continuous monitoring. The measurements of these two methods, however, are completely different, and the benefit of each has been questioned.14 18 19 28

The present results show a significant correlation between the percent decrease of VMCAs and the incidence of EEG changes. However, when individual patients are analyzed, there are marked differences in the results of the two methods: 1 patient showed a decrease of VMCA of >60% without any EEG changes. This finding can be explained by the fact that EEG cannot assess the whole cerebral cortex in its extent or depth and that it assesses the subcortical brain structures even less reliably. Studies of patients operated on under local anesthesia document the occurrence of focal neurological deficits without any EEG changes supporting such an interpretation.15 A marked decrease of VMCA (main stem) can lead to functionally important ischemia in the basal ganglia and/or in the white matter (lenticulostriate arteries), resulting in hemiparesis. Adequate perfusion of superficial cortical areas, however, may be provided by leptomeningeal anastomoses to an extent such that no EEG changes can be registered. On the other hand, 9 patients showed severe or moderate EEG changes without a VMCA decrease exceeding 60% during cross clamping. Two of them had no VMCA decrease at all in spite of severe EEG changes. None of these 9 patients suffered an intraoperative complication, although no shunt had been inserted. This combination may again be explained by the complex arrangement of hemispheric perfusion: (1) in the case of an insufficient leptomeningeal collateral network, VMCA measured in the M1 segment may be only moderately decreased in spite of a critically reduced oxygen supply to the terminal areas of the vascular fields, with consecutive transient reduction of metabolic function and EEG changes; (2) the other and more probable explanation is an embolization to a clinically silent cortical region. In conclusion, the information provided by the two monitoring methods are obviously complementary, which is easily explained by the fact that they monitor different aspects or levels of brain function. Both techniques have a high temporal resolution; however, poor spatial resolution is a major shortcoming: EEG monitors only the function of the most superficial part of the cortex. TCD does not provide information on potential changes in collateral pathways, such as anterior and posterior cerebral arteries. In our series, EEG monitoring alone was oversensitive and would have led to unnecessary use of a temporary shunt in 9 patients if indication for shunt placement had been made on EEG results alone. Furthermore, TCD will disclose shunt malfunction, eg, malfunction due to kinking by an immediate reduction of VMCA. On the other hand, an absent "acoustic temporal bone window" may preclude the use of TCD monitoring. Three patients in the present study had to be excluded for this reason; an age-dependent prevalence of up to 15% was reported.

Stenosis or occlusion of the contralateral carotid artery led to an increase of abnormal findings with both monitoring methods, which was, however, significant only for TCD.29 30 This finding was to be expected because of the contribution of the contralateral carotid artery to the collateral circulation. The marked individual variations, independent of the degree of contralateral carotid stenosis, are due to multiple factors influencing collateral circulation: the state of the vertebrobasilar system, the carotid siphon, and the intracerebral arteries, especially the circle of Willis with its frequent variations, and the autoregulatory mechanisms. On the basis of these findings, some surgeons routinely perform shunting when the contralateral carotid artery is occluded. Because of the individual variations in both monitoring methods and the potential risks of shunt implantation, we recommend a selective shunting based on TCD monitoring also in the case of an occluded or stenosed contralateral carotid artery.

Twelve patients (15%) in our series had temporary shunt implantation based on VMCA decrease exceeding 60%. The critical value of VMCA reduction requiring a shunt insertion is still controversial. Many authors claim a VMCA decrease of 60% to 70% of preclamp value.14 31 Halsey32 proved that patients with a VMCA decrease of >85% have a clear benefit from shunt insertion, whereas shunting with a lower percentage decrease involves the risk of inducing an embolic stroke. None of our patients that were operated on without a shunt suffered intraoperative stroke. One (8.3%) of 12 operations with shunts compared with 3 (4.2%) of 70 operations without shunts were complicated by TIAs. A temporary shunt was used in 10 (40%) of 25 patients with stenosed or occluded contralateral ICAs and in 2 (4%) of 57 patients with normal contralateral ICAs. However, to conclude that monitoring patients without diseased contralateral ICA is unnecessary would be illogical. Clamping may also be risky with patent contralateral ICAs, eg, when absent or hypoplastic communicating arteries cannot provide adequate collateral blood supply.

Four patients suffered intraoperative TIA, with monitoring findings indicating a probably embolic origin. In 3 patients, findings during cross clamping with both monitoring systems were normal, and in 1 patient, EEG showed a sudden ipsilateral depression on final clamp release without VMCA change. We conclude that TCD monitoring in our series was sensitive enough to detect potential hemodynamic complications, which can be prevented by selective shunt insertion. Low combined mortality and morbidity rates in series performed with thiopental cerebral protection favor such an approach, which, however, requires EEG monitoring for dose finding.5 It is not clear whether doses high enough to provide sufficient brain protection in any case (obviating the need for shunting) without causing cardiovascular depression can be safely determined. When judgment of EEG findings is severely limited because of thiopental-induced changes, TCD monitoring might help; however, the critical VMCA decrease, again, has yet to be determined.

High-intensity transient signals were recorded occasionally during artery preparation and regularly followed clamp release.4 33 34 35 36 These data unfortunately have not been taken down in enough detail to allow correlation with intraoperative complications.

In conclusion, the information provided by the two techniques was complementary, and the results showed a significant overall correlation, but there were marked differences in the individual patient. For immediate patient management, in our study with a small sample size (n=82), EEG did not add to the information acquired by intraoperative TCD monitoring, provided that a technically satisfactory insonation was possible. We suggest that temporary shunting should be performed selectively on the basis of TCD results. The critical value of VMCA decrease is somewhere between 60% and 85% of baseline.


*    Selected Abbreviations and Acronyms
 
CEA = carotid endarterectomy
EEG = electroencephalography, electroencephalographic
ICA = internal carotid artery
TCD = transcranial Doppler ultrasonography
TIA = transient ischemic attack
VMCA = blood flow velocity in ipsilateral middle cerebral artery

Received September 9, 1996; revision received May 5, 1997; accepted May 6, 1997.


*    References
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
up arrowDiscussion
*References
 

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Stroke, April 1, 1999; 30 (4): 895 - 897.
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