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Ann Thorac Surg 2000;69:834-840
© 2000 The Society of Thoracic Surgeons

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Original Articles

Craniocervical and aortic atherosclerosis as neurologic risk factors in coronary surgery

^a Department of Anesthesiology, Kumamoto Chuo Hospital, Kumamoto, Japan
^b Department of Cardiovascular Surgery, Kumamoto Chuo Hospital, Kumamoto, Japan

Address reprint requests to Dr Goto, Department of Anesthesiology, Kumamoto Chuo Hospital, 96 Tainoshima Tamukaemachi, Kumamoto 862-0965, Japan
e-mail: togoto{at}bronze.ocn.ne.jp

	Abstract

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Background. Advanced age is associated with increased systemic atherosclerosis and is a consistent neurologic risk factor after coronary artery bypass grafting (CABG).

Methods. We studied prospectively whether varying degrees of a total atherosclerotic score derived from the brain, carotid arteries, and ascending aorta predicted postoperative neuropsychologic (NP) dysfunction and stroke in 177 elderly patients ( 60 years) undergoing CABG.

Results. Group L (low total atherosclerotic score) had rates of NP dysfunction of 25% and 4%, group I (intermediate) had rates of 33% and 22%, and group H (high) had rates of 79% and 43% on postoperative days 1 and 7, respectively (p < 0.001). The incidence of stroke was higher in group H (14.3%) than in groups I and L (7.8% and 0.9%; p = 0.013). Stepwise logistic regression analysis demonstrated the significant predictors of NP dysfunction on postoperative day 7 to be total atherosclerotic score, peripheral vascular disease, and diabetes mellitus, and those of stroke to be total atherosclerotic score, peripheral vascular disease, and hyperlipidemia.

Conclusions. Perioperative evaluation of craniocervical and aortic atherosclerosis is useful to identify a high-risk patient at postoperative NP dysfunction and stroke after CABG.

	Introduction

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Elderly patients have an increased risk of neurologic dysfunction after coronary artery bypass grafting (CABG) [1]. Given their higher prevalence of systemic atherosclerosis, cerebrovascular disease, and underlying cognitive dysfunction, elderly patients are at increased risk of cerebral injury. Our previous study reported that small cerebral infarctions were common in elderly patients undergoing CABG [2]. Cerebral ischemic disorders and carotid stenosis tend to impair cerebral autoregulation mechanisms [3, 4], which may cause hypoperfusion during cardiopulmonary bypass (CPB). Advanced atheromatous disease of the ascending aorta is a major risk factor for perioperative stroke [5–7]. However, there are no data to relate severity of craniocervical and aortic atherosclerosis to postoperative neuropsychologic (NP) dysfunction and stroke after CPB in combination in a predictive model.

We focused on those three major risk factors for perioperative cerebral ischemia in elective CABG, which is performed in patients older than 60 years. Thus we studied prospectively whether varying degrees of the total atherosclerotic score of the brain, carotid arteries, and ascending aorta by using magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), and echocardiography predicted postoperative NP dysfunction and stroke in patients undergoing CABG.

	Material and methods

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After institutional review board approval, we obtained written informed consent from 177 Japanese patients older than 60 years who underwent elective CABG between January 1995 and April 1997 at Kumamoto Chuo Hospital. There were 148 asymptomatic patients and 29 with preexisting cerebrovascular disease (CVD) who had had strokes or transient ischemic attack (TIA). Patients who underwent cardiac valve replacement or ventricular aneurysmectomy were excluded to eliminate the effects of intracardiac air embolism and left ventricular thrombus. Four patients who had had postoperative prolonged intubation ( 24 hours) induced by respiratory complications were removed from the study. Demographic and historic data were defined as follows: age, sex, history of hypertension requiring treatment with antihypertensive medication, history of diabetes mellitus (insulin or oral hypoglycemic therapy or a carbohydrate-restricted diet), hyperlipidemia (total cholesterol 240 mg/dL or triglyceride 150 mg/dL or antihyperlipidemic therapy), history of peripheral vascular disease (PVD), and history of CVD with strokes or TIA.

Neurologic and cerebral evaluation
Preoperative cerebrovascular evaluation was made by cerebral MRI and cervical MRA (0.5 T Superconductive MR unit, Philips, Amsterdam, The Netherlands) as described previously [2]. The scatter representing ischemic changes or infarctions in the brain on MRI was classified as 0 (almost normal); 1 (leukoaraiosis); 2 (some small infarctions); and 3 (multiple small infarctions or broad infarctions). The degree of stenosis in the carotid arteries was graded by MRA as 0 (almost normal); 1 (mild narrowing of < 50%); 2 (moderate narrowing of 50% to 75%); and 3 (severe narrowing of > 75% or obstruction). The lesions on MRI and MRA were evaluated independently by two radiologists who were blinded from preoperative risk factors and symptoms.

Cognitive status was measured using the Hasegawa dementia score (HDS; score 0 to 30, with 30 best), a modification of the Mini-Mental Status (MMS) Examination, an NP test widely utilized in Japan. Scores less than 24 on the HDS are indicative of cognitive impairment (equivalent to 24 on the MMS). The HDS consists of nine questions that test three orientations, three recall memory functions, attention, common knowledge and calculations.

All patients received neurologic and NP examinations before operation by one of three investigators (T.G., T.B., Y.S.) and on the 1st and 7th postoperative days by the same investigator (T.B.). NP examiners were blinded to patients’ preoperative neurologic findings and atherosclerotic score. NP dysfunction for each postoperative assessment was defined as a decrease in performance from baseline greater than or equal to 4 (equal to 2 standard deviations in baseline). Postoperative MRI or computed tomography (CT) was performed only on patients with neurologic deficits lasting more than 24 hours or the decrement of HDS from baseline greater than or equal to 8 on postoperative day 7. Patients with new postoperative neurologic symptoms and positive findings on postoperative MRI or CT of the brain were examined by a staff neurologist to confirm intraoperative and postoperative stroke. Total stroke was the sum of intraoperative stroke and postoperative stroke.

Patient management
Anesthesia and patient management during CPB were conducted as described previously [2]. Distal coronary anastomoses and proximal anastomoses were performed during a single aortic cross-clamp. To limit release of atherosclerotic emboli from the ascending aorta, we changed the standard site for clamp and cannulation if there was greater than or equal to 3 mm intimal thickening of the aorta. All operations were performed by the same operator (R.S.). No attempt was made to standardize the sedative or analgesic agents in the postoperative period.

Evaluation of atherosclerotic lesions in the ascending aorta
We evaluated atherosclerotic lesions in the ascending aorta by echocardiography (Sonolayer SSA-260A, Toshiba, Tokyo, Japan) using an epiaortic probe (linear, 7.5 MHz, IOE 702V). Grading of the degree of atherosclerosis in the ascending aorta was done according to the modified Wareing and associates [5] method: 0 (almost normal); 1 (mild, < 3 mm intimal thickening); 2 (moderate, 3 mm intimal thickening involving one segment of the ascending aorta); 3 (severe or diffuse, 3 mm intimal thickening involving two or all three segments).

Statistical analyses
To relate combined severity of the three atherosclerotic scores derived from the brain, carotid arteries, and ascending aorta to postoperative NP dysfunction and stroke, the 177 patients were divided into three groups according to complications with grade 3 scores. Group L was low grade score (no grade 3 atherosclerotic scores, n = 112). Groups I and H consisted of patients with intermediate and high grade scores (one grade 3 atherosclerotic score, n = 51; two or three grade 3 atherosclerotic scores, n = 14, respectively). Statistical comparison between the three groups was performed using the ² test and one-way analysis of variance (ANOVA). Pearson’s correlation coefficient was calculated to determine associations between atherosclerotic diseases in the ascending aorta, brain, carotid arteries, and peripheral arteries.

To assess the risk of NP dysfunction on postoperative day 7 and total stroke, we used univariate analysis (² test or unpaired t test, significance level, p < 0.05) and stepwise logistic regression analysis by keeping predictors with p values no greater than 0.15. We included hypertension, diabetes mellitus, hyperlipidemia, PVD, CVD (absence = 0, presence = 1), age, aortic clamp time, CPB time, the three atherosclerotic scores (MRI, MRA, and aorta), the preoperative value of HDS as ordinal value, and total atherosclerotic score (none of grade 3 = 1, one of grade 3 = 2, two or three of grade 3 = 3) into the regression model to select the best set. Odds ratios were calculated for each factor in the presence of the others in the final model. All statistical analyses were completed using the SAS Institute Inc (Cary, NC) statistical package, version 6.12.

	Results

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Patient demographics, operative characteristics, and degrees of atherosclerosis of the three groups are summarized in Table 1. The incidence of preexisting CVD was higher in group H than the other two groups, whereas the incidence of PVD was higher in group I than the other two groups. Aortic clamp and CPB time were lower in group H than in the other two groups, as 7 patients in group H (n = 14) underwent CABG without aortic clamp. In group H (n = 14), there were 13 (93%) patients with multiple small infarctions or broad infarction; 6 (43%) patients with carotid stenosis or obstruction; and 11 (79%) patients exhibited severe or diffuse atherosclerosis of the ascending aorta.

Of the 177 patients (age, 70.3 ± 5.0 years), NP dysfunction occurred in 56 (32%) and 21 (12%) patients, respectively, on postoperative days 1 and 7. The HDS was lower in group H than in the other two groups preoperatively and on postoperative days 1 or 7 (p < 0.001; Table 2). Group L had low rates of postoperative NP dysfunction of 25% and 4%, group I had rates of 33% and 22%, and group H had rates of 79% and 43% on postoperative days 1 and 7, respectively (p < 0.001). Intraoperative stroke occurred in 4 patients of groups I and H who had severe or diffuse atherosclerosis of the ascending aorta: 2 in group I had small infarctions and PVD with aortic clamp and weakness of the upper extremities postoperatively. The remaining 2 patients in group H had multiple small infarctions without aortic clamp and induced unconsciousness postoperatively. Postoperative CT in patients with intraoperative stroke showed multiple infarctions due to emboli from the ascending aorta. In groups L and I, 3 patients developed focal deficits on the 2nd or 3rd postoperative days: 2 had hemiparesis and 1 had homonymous hemianopsia. The incidence of total stroke was higher in group H (14.3%) than in groups I and L (7.8% and 0.9%; p = 0.013). The outcome of stroke resulted in severe disability in 3 patients and mild disability in 2 patients; the remaining 2 patients had no serious functional disability. Six patients with a decrement of HDS from baseline greater than or equal to 8 on postoperative day 7 had no new findings on postoperative CT.

	Comment

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The overall incidence of postoperative NP dysfunction in our study was lower than the 69% to 79% rate reported in previous studies [7–9]. Variations in the incidence of postoperative NP dysfunction after CPB among the different studies may have been due to differences in the time of examination, methods, and definition of NP dysfunction. We determined NP dysfunction as a decrease in performance from baseline by 2 standard deviations, whereas previous studies have used the population standard deviations of baseline preoperative tests [8]. Therefore, unlike Shaw and coworkers [8], we found a lower incidence of NP dysfunction in this study. Murkin and colleagues [9] reported that 75% of CABG patients had cognitive dysfunction at 1 week and the rate was reduced to 33% at 2 months. The HDS and MMS do not require written responses and have been shown to be reliable, valid, and concise. However, NP tests have been recommended as two or more cognitive tests including attention, concentration, perceived motor speed, and memory [10]. Further studies are needed to assess the correlation between systemic atherosclerosis and postoperative NP dysfunction by long-term follow-up studies and the use of several NP tests.

Small cerebral infarctions are common in elderly patients undergoing CABG [2]. Most patients with multiple small infarctions are asymptomatic and manifest no clinical signs. However, preoperative HDS was lower in patients with a higher total score for atherosclerotic disease. Yoshitake and coworkers [11] showed that asymptomatic small infarctions were an important factor in the development of vascular dementia in a 7-year follow-up study of normal elderly residents of Hisayama town. In our study, the HDS score of group H appeared to predict the development of asymptomatic multiple small infarctions. Because NP tests such as the HDS are considered to reflect an early stage of cognitive impairment they may be useful for identifying the onset of cognitive impairment in the elderly. In addition, an NP test may serve as an indicator of neurologic and NP dysfunction after CPB.

Carotid stenosis was another statistically significant risk factor for NP dysfunction. A recent study suggested that carotid disease is a predictor of perioperative stroke [12]. Although patients with severe stenosis of the carotid arteries have not been at increased risk for stroke during CABG [13], distal hemodynamic deficiencies depend, to a large degree, on the presence of collateral flow in these patients. Besides a reduced cerebral blood flow (CBF), cerebrovascular reactivity is frequently impaired distal to areas of severe stenosis or occlusion of the cervical carotid artery [4]. Several studies also reported that in patients with asymptomatic small infarctions CBF reactivity to carbon dioxide was significantly lower than in normal controls [3]. However, there are no data to define optimal mean arterial pressure (MAP) during CPB in these patients. Further studies should examine whether higher MAP may reduce the incidence of postoperative NP dysfunction and stroke after CPB in patients with multiple small infarctions and carotid stenosis.

Atherosclerotic disease of the ascending aorta was a significant factor for NP dysfunction and stroke after CPB [5–7]. Microemboli have been implicated in the cause of NP dysfunction after CPB. Many studies reported that NP deficits after routine CPB were related to the number of microemboli delivered during the surgical procedure [14, 15]. In an important pathologic study, Moody and colleagues [16] demonstrated a high percentage of small capillary and arteriolar dilatations in patients undergoing CPB. Many investigators reported that microemboli occurred during CPB, especially aortic cannulation, clamping, and declamping [14, 17]. These data suggested that microdebris from the ascending aorta induced NP dysfunction after CPB. On the other hand, those with the greatest number of microemboli generated by the CPB system appeared to tolerate them well, but had greater decrements in cognitive function than those with fewer microemboli counts [15]. Our data suggested that microemboli from the ascending aorta may have lodged in greater numbers in the arteriolar vasculature with cerebral atherosclerosis.

In our multivariate analysis, diabetes mellitus became a significant factor associated with NP dysfunction on the 7th postoperative day, whereas hyperlipidemia was a significant factor with total stroke. Although the association between hyperlipidemia and stroke is unclear, hyperlipidemia has been associated with carotid artery atherosclerosis in several studies that used ultrasonography [18]. This study used a small number of patients to identify the predictors for stroke. Thus, further study is needed to determine the relation between hyperlipidemia and stroke. On the other hand, diabetes mellitus patients are unable to compensate, when necessary, with an increased CBF during and after CPB [19]. In addition, it is conceivable that diffuse damage to the cerebral microvasculature is the mechanism of increased NP dysfunction in diabetes mellitus after CPB.

Our univariate and multivariate analyses showed that total atherosclerotic score was a significant predictive factor for NP dysfunction and total stroke after CPB. In our series of 177 patients older than 60 years who underwent CABG, 14 (group H, 7.9%) had severe systemic atherosclerosis. PVD was a significant factor associated with NP dysfunction and total stroke. We found that PVD was correlated with atherosclerotic disease of the ascending aorta and carotid stenosis. Criqui and associates [20] reported that the presence of PVD may indicate an increased probability of atherosclerosis in the coronary or cerebrovascular arteries. Patients with history of CVD and PVD, or patients with signs of vascular dementia should be referred for assessment of craniocervical and aortic atherosclerosis. We elected to discriminate patients based on the total atherosclerotic score and preoperative risk factors alone, without explicitly considering operative interventions. Further studies should validate prospectively whether the strategies of perioperative management reduce NP dysfunction and stroke in the higher risk patients. The total atherosclerotic score, a measure of illness, with a higher score representing a greater burden of comorbidity, predicted postoperative NP dysfunction and stroke after CPB.

Routine screening for postoperative NP dysfunction should be performed with prompt workup of incident cases by screening test, such as MMT or HDS, to detect underlying cognitive dysfunction and focal deficit. Given the multifactorial nature of NP dysfunction and stroke after CPB, high-risk patients may be best managed by modifications in surgical techniques and by providing stable perioperative hemodynamics. Perioperative assessment using cerebral MRI, cervical MRA, and epiaortic ultrasonography could reduce the incidence of postoperative NP dysfunction and stroke in elderly patients undergoing CABG.

	Acknowledgments

 
The authors thank Dr Yasuhiko Matsukado for his critical comments and suggestions, and Dr Jon Moon for his editorial assistance. This work was supported in part by the Okinaka Memorial Institute for Medical Research of Japan.

	References

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This Article Abstract 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 Add to Personal Folders Download to citation manager Author home page(s): Ryuzo Sakata Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Goto, T. Articles by Sakata, R. Search for Related Content PubMed PubMed Citation Articles by Goto, T. Articles by Sakata, R.