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CARDIOVASCULAR ANESTHESIA

Gender Differences in Stroke Risk Among the Elderly After Coronary Artery Surgery

Tomoko Goto, MD^*, Tomoko Baba, MD^*, Asuka Ito, MD^*, Kengo Maekawa, MD^*, and Takaaki Koshiji, MD

From the Departments of *Anesthesiology and Cardiovascular Surgery, Kumamoto Chuo Hospital, Kumamoto, Japan.

Address correspondence and reprint requests to T. Goto, MD, Department of Anesthesiology, Kumamoto Chuo Hospital, 1-5-1 Tainoshima, Kumamoto 862-0965, Japan. Address e-mail to togoto{at}bronze.ocn.ne.jp.

	Abstract

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BACKGROUND: Previous studies have shown that women are at higher risk than men for stroke after coronary artery bypass graft (CABG) surgery, but gender differences in systemic atherosclerosis have not been studied adequately. We investigated gender differences in the incidence of craniocervical and ascending aortic atherosclerosis and other risk factors for stroke in elderly patients (age 60 yr) undergoing CABG surgery.

METHODS: Data were prospectively collected on 720 patients (31.8% women) undergoing CABG surgery. All patients underwent preoperative brain magnetic resonance imaging and angiography to assess for prior cerebral infarctions, carotid artery stenosis, and intracranial arterial stenosis. Epiaortic ultrasound was performed at the time of surgery to assess for atherosclerosis of the ascending aorta. Cognitive status was measured using the Hasegawa-dementia score in all patients before surgery and on the seventh postoperative day.

RESULTS: Women were older and had more hypertension and intracranial arterial stenosis than did men. Men had significantly higher rates of hyperlipidemia, peripheral vascular disease, abdominal aortic aneurysm, smoking history, severe carotid artery stenosis, and severe aortic atherosclerosis than did women. Although there were no differences in prior cerebral infarction or preoperative cognitive impairment, the rate of perioperative stroke was marginally higher in men than in women (3.9% vs 1.3%, P = 0.066). Univariate predictors of perioperative stroke were prior cerebral infarctions, ascending aortic atherosclerosis, preexisting cognitive impairment, and peripheral vascular disease. Stepwise logistic regression analysis demonstrated that significant independent predictors of perioperative stroke were prior cerebral infarctions and aortic atherosclerosis.

CONCLUSIONS: These data suggest that men are more likely than women to have risk factors for stroke, including severe carotid artery stenosis, severe aortic atherosclerosis, and peripheral vascular disease. The rates of prior cerebral infarction and preoperative cognitive impairment were similar between genders.

	Introduction

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Neurological dysfunction after cardiac surgery is a devastating complication that is associated with increased mortality and prolonged hospitalization (1). Several studies have reported higher rates of stroke after coronary artery bypass grafting (CABG) surgery in women than in men (2,3). The prevalence and causes of gender difference in the rates of stroke after CABG surgery remain controversial, but advanced age and comorbid disease may play a role. Advanced age is often associated with moderate or severe aortic atherosclerosis, a major risk factor for perioperative stroke (4–6). Hogue et al. (7) further found that prior stroke was an independent risk for stroke after CABG surgery in both women and men. In previous studies we have found that craniocervical and aortic atherosclerosis were predictive of postoperative stroke (8,9). Gender differences in systemic atherosclerosis, or in the frequency of prior cerebral infarction, have not been extensively studied in elderly patients. We (8,9) have previously reported detailed clinical data on risk factors, systemic atherosclerosis, and neurological complications in patients undergoing cardiac surgery over a period of 10 yr. The purpose of this study was to evaluate gender differences in risk factors for clinical postoperative neurologic outcomes among a cohort of Japanese patients undergoing CABG surgery.

	METHODS

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This analysis was performed on prospectively gathered data from 720 patients age 60 years or older who underwent elective isolated CABG surgery with (n = 602) or without (n = 118) cardiopulmonary bypass (CPB) by two surgeons at Kumamoto Chuo Hospital between January 1995 and December 2004. This study presents data from 56% of the entire population of patients undergoing CABG surgery at our hospital during this time period. Results of the analysis of the association between atherosclerosis of the ascending aorta and stroke after CABG surgery have been published previously in this cohort (9). "Off-pump" patients undergoing surgery without CPB were previously found to have more severe systemic atherosclerosis than "on-pump" patients (10). We thus included data for patients undergoing surgery both on-pump and off-pump in this study. The IRB approved the present study and all patients provided their informed consent to participate. We excluded seven patients who could not be evaluated for the outcomes of cognitive dysfunction and stroke: two died in the immediate postoperative period, four patients had prolonged tracheal intubation (7 days) for pulmonary complications, and one patient had multiorgan system failure. Demographic and preoperative data were recorded into an institutional database including age, sex, hypertension, diabetes mellitus, hyperlipidemia, renal insufficiency (creatinine 1.9 mg/dL), peripheral vascular disease, abdominal aortic aneurysm, smoking history, cardiac operative risk evaluation (EuroSCORE), number and extent of coronary artery disease, left ventricular ejection fraction, number of coronary artery bypass grafts, use of CPB, and history of stroke or transient ischemic attack.

Atherosclerosis Assessments
All patients underwent preoperative brain magnetic resonance imaging and angiography (MRI, MRA) to assess for prior cerebral infarctions, carotid artery stenosis, and intracranial arterial stenosis as previously described (8). MRI finding were classified as: almost normal or leukoaraiosis; some small infarctions with a diameter <15 mm; or multiple small infarctions or large infarctions >15 mm or those that included the cortical area. The degree of stenosis of intracranial arteries was graded bilateraly by MRA as: almost normal; moderate narrowing of >50%; or occluded. The degree of stenosis in the carotid arteries was graded based on MRA as: normal or mild narrowing of <50%; moderate narrowing of 50%–75%; or severe narrowing >75% or obstruction. All patients underwent epiaortic ultrasound scans at the time of surgery to assess for atherosclerosis of the ascending aorta. The ultrasound scans were recorded on VHS tape for subsequent off-line analysis. We divided the ascending aorta from the aortic valve to the innominate artery into three segments and assessed intimal thickening by off-line on videotape records. The degree of atherosclerosis in the ascending aorta was graded as: normal or mild, <3 mm intimal thickening; moderate, 3mm intimal thickening involving at least one segment of the ascending aorta; or severe, 3 mm intimal thickening involving two or all three segments, often with protruding, ulcer of surface or mobile components. Based on the findings from real-time imaging, the need for modification of cannulation, clamping, proximal CABG anastomotic sites and/or cardioplegia cannula sites were determined by the cardiac surgeons as previously described (9). One examiner measured the intimal thickening of the three segments of the ascending aorta in all patients. Two observers assessed plaque-surface morphology without being aware of the clinical details and modifications to operative technique.

Neurologic Evaluation
Cognitive status was measured using the Hasegawa-dementia score (HDS) in all patients before surgery and on the seventh postoperative day. The HDS is a modification of the Mini-Mental State Examination with a range of score from 0 to 30 with higher scores representing better cognitive state (11). Preoperative cognitive impairment was defined as a HDS <24, which is indicative of cognitive impairment (equivalent to 24 on the Mini-Mental State Examination). Postoperative cognitive dysfunction was defined as a decrease in performance from baseline of at least 4 (equal to two standard deviations in baseline on preliminary study) on the HDS tests. Postoperative brain MRI or computed tomography (CT) were performed only on patients with a clinically detected neurological deficit lasting >24 h or with a decrement of HDS from baseline of at least eight points on postoperative day 7. Stroke was defined as a new motor or sensory deficit that was confirmed by postoperative MRI or CT of the brain. To assign the stroke subtype, we used a diagnostic algorithm that classified patients as having infarction caused by embolism, infarction caused by hypoperfusion (watershed infarctions or diffuse hypoxia), or infarction from thrombosis caused by large-vessel atherosclerosis (atherothrombotic stroke) (12). All stroke classifications were reviewed by two independent neurologists who were unaware of the intraoperative findings or modification in operative technique due to epiaortic scan results.

Patient Management
Surgery with CPB was performed using a membrane oxygenator and roller pump under alpha-stat pH management and moderate hypothermia (28°C–34°C), as described previously (8). For patients with prior cerebral infarction or severe carotid stenosis, mean arterial blood pressure was maintained >70 mm Hg during CPB and rewarming was at a rate of speed to maintain no more than a 3°C difference between rectal and CPB perfuse temperatures. In other patients mean arterial blood pressure was maintained between 50 and 70 mm Hg and the difference between rectal and CPB perfuse temperature was restricted to 5°C–6°C during rewarming. Off-pump CABG surgery were performed using Medtronic Octopus II or IV devices and deep pericardial traction sutures were applied for cardiac displacement. A cell-saving device was used for intraoperative blood conservation.

Statistical Analyses
Demographics and perioperative parameters were compared between genders with Student t-test for continuous data and the ² test or Fisher exact test for discrete variables. All probabilities were two-tailed, with a P < 0.05 regarded as significant. Spearman rank correlation coefficients were used to examine the association between craniocervical atherosclerosis, age, and risk factors. Stepwise logistic regression analysis was performed to separately assess for predictors of perioperative stroke. Variables included in the multivariate model included all variables found to be associated factors with this condition with a P < 0.20 on univariate analysis and potential risk factors for perioperative stroke. These included history of cerebrovascular disease, peripheral vascular disease, use of CPB, carotid and cerebral artery stenosis, cerebral infarctions and atherosclerosis of the ascending aorta. Odds ratios (OR) and 95% confidence interval (CI) were calculated for each variable. Goodness of fit was assessed by Hosmer-Lemeshow statistic. All statistical analyses were completed using the SAS Institute, Inc., statistical package (version 8.2, Cary, NC).

From our previous study (9), we assumed the frequency of craniocervical and aortic atherosclerosis in men and women were 10% and 4%, respectively. A power analysis with = 0.05, ß = 0.02 (power 80%) determined that a sample size of 697 should be adequate.

	RESULTS

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Of the 720 patients, 229 (31.8%) were women. Preoperative and intraoperative characteristics for men and women are summarized in Table 1. Compared to men, women were older and significantly more likely to have hypertension, and a higher Euro SCORE. Men were more likely to have common vascular risk factors such as hyperlipidemia, peripheral vascular disease, and smoking history than do women. Men were more likely than women to have an abdominal aortic aneurysm, and they had more left main coronary artery disease and more low left ventricular ejection fraction than did women.

Table 2 lists the prevalence of craniocervical and atherosclerosis of the ascending aorta, preoperative cognitive impairment, postoperative cognitive dysfunction and perioperative stroke. Men had a significantly higher rate of severe carotid artery stenosis, and severe atherosclerosis of the ascending aorta than did women. Compared to men, women were significantly more likely to have intracranial artery stenosis. The frequency of cerebral infarction on preoperative brain MRI, preoperative cognitive impairment and postoperative cognitive dysfunction were almost identical in men and women. Perioperative stroke occurred in 3.9% of men (19 of 491) and 1.3% of women (3 of 229, P = 0.066). Postoperative CT or MRI in 15 of 17 patients (88%) with intraoperative stroke revealed multiple infarctions were probably caused by emboli. In a subgroup with severe aortic atherosclerosis, the surgical technique was modified in 92 male patients and in 15 female patients (Table 2). There were no significant operative modifications between genders.

Univariate analysis demonstrated that patients with perioperative stroke had significantly more frequent peripheral vascular disease, preoperative cognitive impairment, prior cerebral infarctions, and severe aortic atherosclerosis than patients not suffering stroke (Table 3). The hospital mortality was 0.4% (3 of 720); 4.5% (1 of 22) in patients with perioperative stroke versus 0.3% (2 of 698) in patients not suffering stroke (P = 0.002). Stepwise logistic regression analysis identified prior cerebral infarctions (odds ratio [OR] per grade, 1.987: 95% CI, 1.179–3.393; P = 0.010) and atherosclerosis of the ascending aorta (OR per grade, 1.990; 95%CI, 1.222–3.333; P = 0.005) to be independently associated with perioperative stroke. The final study model had area under the receiver operating characteristic curve ("c" index) of 0.718 with an adjusted Hosmer-Lemeshow test statistic of 0.847.

Based on Spearman rank correlation, the grade of atherosclerosis of the ascending aorta increased with the grade of carotid stenosis (r = 0.199, P < 0.001), smoking history (r = 0.252, P < 0.001), renal insufficiency (r = 0.237, P < 0.001), peripheral vascular disease (r = 0.156, P < 0.001), abdominal aortic aneurysm (r = 0.119, P = 0.002), hypertension (r = 0.124, P = 0.001), age (r = 0.120, P = 0.001), and male sex (r = 0.186, P < 0.001). To further clarify the relationship between gender, age, and atherosclerosis of the ascending aorta, we stratified patients by ascending aortic grade, sex, and age. Figure 1 shows that the percentage of patients with severe atherosclerosis of the ascending aorta increases with age, from approximately 20% in the sixth to seventh decade of life to 38% at the eighth decade in men. In men, the percentage of patients with moderate and severe aortic atherosclerosis was double that of women.

View larger version (28K): [in this window] [in a new window]   Figure 1. The percentage of patients with moderate and severe aortic atherosclerosis between gender. Each bar represents sum of moderate and severe aortic atherosclerosis of subjects in a given age decade.

	DISCUSSION

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Our results show that women and men present for CABG surgery with different stroke-associated comorbidities and a different distribution of severe atherosclerosis of the arteries supplying the brain. We found that men have a higher incidence of peripheral vascular disease, abdominal aortic aneurysm, hyperlipidemia, smoking history, carotid artery stenosis, and moderate or severe atherosclerosis of the ascending aorta than do women. Women, in contrast, were older than men and they had a higher frequency of hypertension and intracranial artery stenosis. Multivariate analysis revealed that prior cerebral infarctions and atherosclerosis of the ascending aorta were independent predictors of perioperative stroke.

Several studies have found that women are at higher risk for stroke after cardiac surgery than men, while others report no gender difference in stroke risk. In single center and large multicenter studies, Hogue et al. (2,3) found that women were at higher risk than men for perioperative stroke and stroke-related mortality. This higher risk could not be explained by known stroke risk factors, including advanced age, hypertension, and atherosclerosis of the ascending aorta (2,3). In contrast, Koch et al. (13) in single-center study suggested that men and women with a similar risk profile were not at higher risk for stroke or high mortality based on propensity-based analysis. In this study, we found that there were no differences in the rate of stroke between genders, and if anything, there was a trend for men to have higher stroke risk than do women. However, the small number of patients in this cohort precludes drawing firm conclusions regarding gender susceptibility for stroke. Further, while our findings suggests that the pattern of atherosclerosis varies between men and women, the small number of women in this cohort does not allow for a precise assessment of the importance of this finding on stroke risk.

Small cerebral infarctions are common in elderly patients and their presence increases the risk for perioperative stroke after CABG surgery (8). Most patients with multiple infarctions do not provide a history of clinical stroke, but many may be found to have cognitive impairment (14). We found that the prevalence of prior cerebral infarctions and preoperative cognitive impairment were similar between men and women, despite our finding that men had a significantly higher rate of carotid artery stenosis and atherosclerosis of the ascending aorta, but less frequent intracranial artery stenosis than did women. Similar to our observations, several studies have shown that carotid artery stenosis is related to hyperlipidemia, coronary artery disease, and smoking history (15), whereas intracranial artery stenosis is associated with hypertension (16). It should be emphasized that gender difference of systemic atherosclerosis derived from a particular cohort subject cannot be extrapolated to a wider population. Further studies should determine, prospectively, the relationship of comorbidities and the distribution of systemic atherosclerosis in high risk patients undergoing CABG.

Atherosclerosis of the ascending aorta is an important risk factor for cerebral embolism and stroke after cardiac surgery (4–6,9,17). Increasing age is associated with a higher frequency of atherosclerosis in the ascending aorta. This study demonstrated that moderate or severe atherosclerosis of the ascending aorta was more common in elderly men than in elderly women. Di Tullio et al. (18) have also demonstrated that aortic plaques 4 mm are significantly more frequent in men than in women with ischemic stroke. Many investigators have reported that cerebral microembolization occurred during aortic cannulation, clamping and declamp during cardiac surgery (19,20). The main cause of intraoperative stroke seemed to be embolic, suggesting that macro and microemboli created by surgical maneuvers on the atherosclerotic ascending aorta might be associated with the risk factors for brain injury. This suggests that the embolic load for the brain during cardiac surgery may be greater in men than in women. Transcranial Doppler ultrasonography is a useful technique to quantify and detect the source of microemboli during CPB (21). Studies have shown that diffusion-weighted imaging MRI may provide clues on the association of new cerebral lesions and cause of stroke after CABG surgery (22). Further study is needed to determine the relationship between emboli and neurological dysfunction using Transcranial Doppler ultrasonography and diffusion-weighted imaging-MRI. This would help us determine the etiologic mechanism of stroke after CABG in high risk patients.

There are several limitations to the present analysis. Our data were derived from an analysis at a single institution. Thus, we cannot exclude the possibility that our results are biased by institutional standards or patients. The prevalence of coronary heart disease among men is about twice that among women between the ages of 49 and 82 years. In this study, the proportion of women, 31.3% was consistent with other published findings (25%–30%) (23). These small numbers decreased the statistical power for detecting the gender difference of stroke after CABG. However, our study is the first to address the distribution of craniocervical and atherosclerosis of the ascending aorta and its association with stroke between genders in elderly patients undergoing CABG surgery.

In conclusion, this study demonstrated that women and men present for CABG surgery with different stroke-associated comorbidities and a different distribution of severe atherosclerosis of the arteries supplying the brain. Although the prevalence of prior cerebral infarctions and preoperative cognitive impairment were also identical between sexes, men were more likely than women to have severe carotid artery stenosis, severe aortic atherosclerosis, and peripheral vascular disease. Perioperative evaluation, management and therapy should include a focus on underlying craniocervical and aortic atheroslerosis to reduce the incidence of stroke after CABG.

	ACKNOWLEDGMENTS

 
The authors thank Dr. Jon Moon for his editorial assistance and Dr. Akira Kitagawa for his statistical assistance.

	Footnotes

 
Accepted for publication January 23, 2007.

	REFERENCES

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Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999