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Ann Thorac Surg 2000;70:1571-1576
© 2000 The Society of Thoracic Surgeons

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Original articles: cardiovascular

Stroke after coronary artery bypass grafting in patients with cerebrovascular disease

^a Department of Cardiovascular Surgery, Tokyo Saiseikai Central Hospital, Tokyo, Japan

Address reprint requests to Dr Hirotani, Department of Cardiovascular Surgery, Tokyo Saiseikai Central Hospital, 1-7-14 Mita, Minato-ku, Tokyo 108-0073, Japan
e-mail: hero.takashi{at}nifty.ne.jp

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Stroke has been associated with a significantly increased mortality from coronary artery bypass grafting (CABG). To determine the predictors of stroke in patients undergoing CABG, we collected data on 472 consecutive patients.

Methods. From March 1991 to March 1999, all patients undergoing CABG at our institution underwent routine duplex scanning of the extracranial carotid and vertebral arteries. Seven patients with symtomatic carotid stenosis were treated by carotid endarterectomy (CEA) before CABG.

Results. There was a 10-fold increase in mortality (12.5%) associated with postoperative stroke. Many variables were analyzed by a mutivariate technique and the severity of extracranial carotid artery stenosis was determined to be the only independent predictor of postoperative stroke (p < 0.01). None of the patients with carotid artery occlusion and none of the patients who underwent CEA before CABG experienced a stroke.

Conclusions. To reduce the stroke rate, the indications for prophylactic CEA may be extended for asymptomatic patients with carotid artery stenosis greater than 75%.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Stroke remains an important cause of morbidity and mortality after coronary artery bypass grafting (CABG) although many authors have studied countermeasures against it. The cause of stroke after CABG is believed to be a combination of cerebral hypoperfusion caused either by cerebrovascular disease or by hypotension during cardiopulmonary bypass (CPB) and embolism from the ascending aorta or carotid artery [1–3]. As a result, the causes of postoperative stroke in patients undergoing CABG are multifactorial. Among these factors, it is relatively easy to control blood pressure above an appropriate level during CPB by using vasoconstrictors, a pulsatile perfusion device, or intraaortic balloon pumping (IABP). Extracranial carotid artery occlusive disease and arteriosclerosis of the ascending aorta are important factors, as these are potentially treatable and are detectable before or during the operation. Some authors have found a significant correlation between the presence of carotid artery stenosis and postoperative stroke. However, the occurrence of stroke in patients with carotid arterial stenosis ranges widely according to previous reports [1, 4–6], probably because the degree of stenosis that was defined as a significant finding differed from 50% to 75% stenosis. Furthermore, the affect of vertebral arterial stenosis on the occurrence of postoperative stroke has not yet been studied in detail. At our institute, since 1991, all patients except for emergency cases have undergone routine duplex scanning of the extracranial carotid and vertebral arteries before CABG. In this report, the occurrence of occlusive disease in the carotid and veretebral arteries in patients undergoing CABG was analyzed by the use of a more detailed definition regarding the degree of stenosis. The purpose of this study was to determine the predictors of stroke in patients undergoing CABG, especially regarding the correlation between the presence of carotid or vertebral artery stenosis and postoperative stroke.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
From March 1991 to March 1999, the patients undergoing CABG at our institute all routinely underwent duplex scanning of the extracranial carotid and vertebral arteries as part of the preoperative examinations, except for emergency cases. The data from all of these patients (n = 472) were analyzed.

All subjects underwent screening by duplex scanning for the presence of carotid and vertebral arterial occlusive disease within 1 week of CABG. Measurements of the vessel lumen in the carotid and vertebral arteries were made and images showing the narrowest diameter were selected to define the degree of stenosis [7]. The carotid and vertebral arteries were characterized by the degree of wall thickness as none or trivial (< 50%), mild ( 50%, < 75%), moderate ( 75%, < 90%), severe ( 90%, < 100%), or occluded (100%). When the carotid artery was found to be severely stenotic by the attending neurologists, it was confirmed by cerebral angiography.

All subjects also underwent computed tomography (CT) routinely and, when a cerebral infarct was observed by CT scanning of the brain, further magnetic resonance imaging (MRI) and MRI angiography were performed. In addition, when carotid endarterectomy (CEA) was performed before CABG, the absence of residual stenosis was ensured by duplex scanning after CEA.

Preoperative evaluation
The age, gender, any remote history of stroke, the prevalence of risk factors for arteriosclerosis (diabetes mellitus, hypertension, smoking history, hypercholesterolemia), history of CEA, history of myocardial infarction, and extent of coronary artery disease were noted. The degree of carotid and vertebral arterial occlusive disease was defined as described above.

Operative technique
When a patient had a stenosis greater than 75% at the extracranial carotid artery and also experienced neurologic events in the ipsilateral hemisphere, CEA was planned and was usually performed at least 1 week before CABG. Concomitant coronary and carotid artery operation was planned only when both the coronary and carotid artery lesions were considered to be unstable. When a patient had carotid artery occlusion, CEA was not planned.

When a patient had a cerebral arterial stenosis greater than 75%, the mean blood pressure during CPB was maintained at greater than 90 mm Hg by using vasoconstrictors such as phenylephrine hydrochloride or counterpulsation produced by IABP.

After a median sternotomy, single or bilateral internal thoracic arteries were dissected and the pericardium was divided; the ascending aorta and the proximal aortic arch were then palpated to identify the area of calcification. Ultrasonographic scanning of the ascending aorta was not yet available at our institution at the time of the study. The ascending aorta and right atrium were cannulated and CPB was established as usual, but when severe calcification existed on the ascending aorta the femoral artery was cannulated for arterial access. Cardiopulmonay bypass was performed under moderate hypothermia. Myocardial protection was performed with antegrade crystalloid cardioplegia. Since 1993, proximal and distal anastomoses have been performed during a single period of aortic occlusion, thus avoiding the need to partially clamp the atherosclerotic ascending aorta. When circumferential calcification of the ascending aorta was present, the aortic no-touch technique that avoided any manipulation of the ascending aorta was performed. Since 1997, after the complete construction of proximal and distal anastomoses, the cross-clamp was removed with brachiocephalic vessels being compressed at their origins by the surgeon (using his fingers) to avoid cerebral embolization of atheromatous plaques detached from the ascending aorta.

Regarding intraoperative variables, the prevalence of severe arteriosclerosis of the ascending aorta, use of IABP, avoidance of partial clamping of the ascending aorta, and use of the compression technique for the braciocephalic arteries were noted.

Postoperative evaluation
All patients with any potential for postoperative neurologic deficit were evaluated by the attending neurologists and underwent CT scanning of the brain. Furthermore, all patients who were considered to be at high risk for developing postoperative stroke, including patients who had atherosclerotic cerebrovascular lesions, any remote history of neurologic events, or severe arteriosclerosis on the ascending aorta, were evaluated by the neurologists and underwent CT scanning of the brain after CABG.

Statistical analysis
Data are represented as the mean ± standard deviation. The predictors of stroke were determined by both univariate and multivariate analyses. For the univariate analysis, all discrete data were analyzed with either ² or Fisher’s exact test as appropriate, and all continuous data were evaluated by the unpaired t test. All ordered categorical data were compared by Wilcoxon’s test. The selected variables, including all those with a p value of less than 0.20 by univariate analysis, were entered into a multivariate analysis using the stepwise logistic regression technique to determine any independent predictors of stroke. Statistical significance was set at a p value of less than 0.05.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Patient characteristics
The demographic characteristics of the patient populations with and without postoperative stroke are presented in Table 1. The distribution of carotid and vertebral artery disease is presented in Table 2. All 167 patients who had a remote history of cerebral infarction underwent MRI and MRI angiography preoperatively; 13 patients had severe stenosis greater than 75% at the intracranial carotid artery or vertebral artery. Extracranial carotid artery stenosis equal to or greater than 50% was observed in 62 patients (13%); among these patients, carotid artery occlusion was observed in 16. Moderate to severe carotid stenosis ( 75%, < 100%) was observed in 28 patients, 12 of whom had severe carotid stenosis and underwent cerebral angiography. The accuracy of duplex scanning in detecting severe carotid stenosis was 83% (10 of 12). Prophylactic CEA was performed in 7 patients because of previous neurologic events in the ipsilateral hemisphere. Prophylactic CEA was not performed in the other 21 patients for asymptomatic lesions. No concomitant coronary or carotid artery operation was performed. Vertebral artery stenosis equal to or greater than 50% was observed in 12 patients and vertebral artery occlusion was observed in 9.

There were 16 patients (3.4%) in whom a stroke was observed based on either the clinical or CT scan findings. In 3 patients, a new small infarct was accidentally observed in the postoperative CT scans, whereas these patients had no neurologic symptoms. Among the 13 symptomatic strokes, four were transient and nine were permanent. There were two global and 14 hemispheric strokes, which included eight infarcts occurring in the carotid artery region and six in the vertebral artery region (Table 4). Five patients with extracranial carotid artery stenosis had cerebral infarcts after CABG, and the side of the carotid lesion was consistent with that of postoperative infarcts in all these patients.

The findings of duplex scanning in the 16 patients with postoperative stroke are shown in Table 4.

Predictors of postoperative stroke
Table 1 compares the characteristic and Table 2 compares the degree of various cerebrovascular diseases in patients with and without postoperative stroke. Table 3 shows the intraoperative variables in patients with and without postoperative strokes. According to univariate analysis, a history of stroke, the presence of intracranial cerebrovascular disease, severity of extracranial carotid artery stenosis, laterality of extracranial carotid artery lesion, and laterality of extracranial vertebral artery lesion were determined to be significant risk factors for postoperative stroke.

According to multivariate logistic regression analysis, the severity of extracranial carotid artery stenosis was identified as an independent predictor of postoperative stroke (p = 0.0068, odds ratio = 6.59) (Table 6).

	Comment

Top Abstract Introduction Patients and methods Results Comment References

The cause of postoperative stroke in patients undergoing CABG is multifactorial. Numerous preoperative and intraoperative variables were analyzed to determine the risk factors for stroke after CABG in many previous studies [1, 3–6]. Among these variables, extracranial carotid stenosis was considered to be an important factor because it is potentially treatable and is detectable before or during operation. In our institution, all patients undergoing CABG (except for emergency cases) undergo duplex scanning to identify the presence of carotid and vertebral arterial occlusive disease within 1 week of CABG.

Extracranial carotid artery stenosis
The duplex scanning of the extracranial carotid artery is considered to be one of the most reliable methods to detect the presence of stenosis [9].

One factor complicating the results of correlation analysis between carotid artery stenosis and postoperative stroke is the indication of CEA. In our institution, asymptomatic carotid artery stenosis was not a proven indication for CEA according to the guidelines for CEA developed by the American Heart Association [10]. In the present study, all patients who required CEA because of symptomatic carotid artery stenosis underwent CEA before CABG, and the absence of residual stenosis was ensured by duplex scanning before CABG; in these patients, the degree of carotid artery stenosis at CABG was defined as none. In patients undergoing CEA and CABG simultaneously, it is unclear that postoperative stroke was attributable to CEA or CABG [5]. In the present study, such patients were not included. Thus, we considered our study to be suitable for analyzing the relationship between the carotid artery stenosis and the occurrence of postoperative stroke.

Risk factors for postoperative stroke
According to univariate analysis, a history of stroke, the presence of intracranial cerebrovascular disease, severity of extracranial carotid artery stenosis, laterality of extracranial carotid artery lesion, and laterality of extracranial vertebral artery lesion were determined to be significant risk factors for postoperative stroke. According to multivariate analysis, the severity of carotid artery stenosis was determined to be the only significant independent predictor of postoperative stroke (Table 6). Because of the small number of events and the limited statistical power, only one variable was identified to be an independent predictor; however, variables other than the severity of carotid artery stenosis was considered to be clinically important as predictors.

Mechanism of postoperative stroke
What, then, is the mechanism of the postoperative stroke in patients with carotid artery stenosis, hypoperfusion of the diseased carotid artery region, or an embolism from the atherosclerotic lesion of the carotid artery? According to the analysis of the type of stroke (Table 4), there were only two global strokes and both patients did not have either carotid or vertebral artery stenosis. All strokes, which occurred in patients with extracranial carotid artery stenosis, were hemispheric and were suspected to be embolic infarcts. Furthermore, in the present study no patients with carotid artery occlusion had stroke after CABG. In our institution, when cerebral artery occlusion or stenosis greater than 75% was observed on MRI or angiography, the mean blood pressure during CPB was maintained at greater than 90 mm Hg using vasoconstrictors or counterpulsation produced by IABP [3]. Probably because of the effects of these measures the brain was protected against hypoperfusion, and no global stroke was observed in patients with carotid artery stenosis or occlusion. We thus considered that the cause of postoperative stroke in our patients with carotid artery stenosis was embolism from the atherosclerotic lesion of the carotid artery.

The question remains as to why such embolism frequently occurs during CABG. We suppose two possible reasons. One possibility is that the hemodynamic change from pulsatile to nonpulsatale perfusion during the operation plays a role in detaching the atherosclerotic material from the carotid artery lesion. Another possibility is that high pressure jet emanating from the cannula tip may detach debris from the carotid artery lesion, as it was demonstrated to detach the debris from the aorta [11]. If so, then the placement of the arterial cannula may be better at an alternative site (such as the femoral artery) in patients with carotid artery stenosis.

Prophylactic carotid endarterectomy
Operative morbidity of CEA for isolated asymptomatic carotid artery stenosis is quite low in modern series [12], and many cardiovascular surgeons have advocated simultaneous CEA and CABG [4, 13, 14]. In our institution, asymptomatic carotid artery stenosis has not been a proven indication for CEA even in patients undergoing CABG. According to the results presented here, the postoperative stroke rate increased according to the severity of the carotid artery stenosis. Special attention should be drawn to the fact that the postoperative stroke rate in asymptomatic patients with carotid artery stenosis greater than 75% was fivefold higher than that in patients with carotid artery stenosis less than 50% (Table 5). On the other hand, symptomatic patients who underwent CEA before CABG (N = 7) experienced no strokes after CABG. Although these results do not address the feasibility of the combined procedure of CEA and CABG for all patients with asymptomatic carotid artery stenosis because of the small sample size, it appears that the indications of prophylactic CEA can be extended for asymptomatic patients with carotid artery stenosis greater than 75%.

Vertebral artery stenosis
Vertebral arteries are important arteries of the brain and their lesions are detectable by duplex scanning. However, no studies have previously analyzed the relationship between vertebral artery stenosis and the occurrence of stroke after CABG. In the present study, vertebral artery stenosis equal to or greater than 50% was observed in 21 patients (4.4%); among them, vertebral artery occlusion was observed in 9. The severity of vertebral artery stenosis was not determined based on multivariate analysis as a predictor of postoperative stroke, probably because the sample size was too small. However, among 16 postoperative strokes, six occurred in the vertebral region, and therefore further study of extracranial vertebral artery disease may help us to improve the mortality and morbidity associated with CABG.

Arteriosclerosis of the ascending aorta
Atheroemboli from the severely atherosclerotic ascending aorta are known to be related to stroke [15–17]. Intraoperative screening for the presence of ascending aortic arteriosclerosis by ultrasonic aortic scanning and its relationship to postoperative stroke have been reported [17]. In our institution, the presence of significant ascending aortic calcification or atherosclerotic plaque was assessed by palpation and a visual inspection at the site of proximal vein graft anastomoses because ultrasonic equipment was not available during the period of this study. Regarding the ascending aortic disease and its contribution to the likelihood of the postoperstive stroke, we cannot exclude the possibility that it might become a significant predictor of stroke if ultrasonic aortic scanning were used in all subjects.

Limitations
The present prospective study regarding postoperative stroke after CABG was too small to be conclusive and was not a randomized study for the ethical reasons. Larger studies will be needed to understand the pathogenesis of stroke during CABG correctly.

In conclusion, extracranial carotid artery stenosis was determined to be a predictor of stroke after CABG. To reduce the incidence of stroke after CABG, indications for prophylactic CEA may thus be extended for asymptomatic patients with carotid artery stenosis greater than 75%.

	References

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