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Ann Thorac Surg 2000;69:1053-1056
© 2000 The Society of Thoracic Surgeons

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ORIGINAL ARTICLES: CARDIOVASCULAR

Stroke after coronary artery operation: incidence, correlates, outcome, and cost

^a Division of Cardiothoracic Surgery, Department of Surgery, Emory University School of Medicine, Atlanta, Georgia, USA

Address reprint requests to Dr Puskas, 550 Peachtree St NE, Suite 7700, Atlanta, GA 30365

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Stroke is a major complication of coronary operation, with reported rates of postoperative cerebral dysfunction ranging from 0.4% to 13.8%. In this report, the incidence, correlates, outcomes, and costs of stroke in coronary operation were evaluated at Emory University between 1988 and 1996.

Methods. Data were entered prospectively into a dedicated computerized database at Emory University and analyzed retrospectively. Univariate and multivariate analyses were utilized where appropriate.

Results. Data from 10,860 patients undergoing primary coronary operation between 1988 and 1996 were analyzed. There were 250 patients not entered into the database. Stroke occurred in 244 (2.2%). Univariate predictors of stroke (p < 0.05) included age, female gender, hypertension, diabetes, prior stroke, prior transient ischemic attack (TIA), and carotid bruits. Multivariate correlates included age (odds ratio 1.07) previous TIA (odds ratio 2.2), and carotid bruits (odds ratio 1.9), although the area under the Receiver Operating Characteristics (ROC) curve was only 0.69, suggesting limited ability to predict stroke. One and 5 year survival rates were 64% and 44% with stroke, and 94% and 81% without stroke, respectively. Among the stroke group, 23% of the patient population died before hospital discharge. The stroke group had a significantly longer length of hospital stay, as well as higher costs.

Conclusions. Stroke is a devastating complication of coronary operation, significantly increasing morbidity, mortality, and cost. Three independent variables were identified for predicting stroke, including age, previous TIA, and carotid bruits. Patients should be carefully screened for cerebrovascular disease to help prevent stroke and its associated morbidity.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Stroke remains a major complication of coronary operation, and reported rates range from 0.4% to 13.8% [1]. Stroke is multifactorial in origin. Some recognized correlates include prior stroke, carotid bruit, hypertension, increasing age, and diabetes mellitus [2]. Possible mechanisms of stroke include arteriosclerotic emboli from the aorta, hypotension from ventricular dysfunction, and reactive thrombocytosis [3–5]. Carotid artery disease, as well as cerebral microvascular disease, have also been implicated. The purpose of this study was to identify risk factors for stroke. Stroke was defined as an acute deterioration in neurological status, and its presence or absence was determined by each individual clinician. The incidence of stroke, its attendant morbidity, length of stay, and cost were examined in 10,860 consecutive patients undergoing primary coronary operation at Emory University between 1988 and 1996. The identification of risk factors may help prevent this devastating complication of coronary operation.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
The population studied consisted of 10,860 consecutive patients undergoing primary coronary operation at Emory University between 1988 and 1996. Of these, 2800 (26%) patients were women. Patients were categorized into two groups: stroke present (stroke group) and stroke absent (nonstroke).

Surgical technique
Standard techniques were used for cardiopulmonary bypass. Perfusion was maintained at 2.0 to 2.4 L/min/m². Myocardial viability was preserved with systemic hypothermia (28 to 32°C), topical hypothermia, and cold potassium cardioplegia according to surgeon preference. After standard revascularization with internal mammary, saphenous vein and/or radial artery conduits, each patient was rewarmed and weaned from cardiopulmonary bypass, closed, and transported to the cardiovascular intensive care unit.

Data analysis
All data were entered into a computerized database in a prospective manner and analyzed retrospectively. All statistical testing was done with BMDP software (BMDP Statistical Software Inc, Chicago, IL). Results are reported as the mean ± standard deviation. Univariate analysis was performed to identify significant correlates of stroke (p < 0.05). Multivariate regression analysis was then performed on those significant correlates.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Stroke was noted in 244 (2.2%) of 10,860 patients who had primary coronary bypass operation. Table 1 presents univariate analysis of patient characteristics for the stroke and nonstroke groups. Patients who suffered stroke were older and more likely to be female, diabetic, and hypertensive than patients who did not. In addition, they were more likely to have had previous strokes, transient ischemic attack (TIAs), or carotid bruits than patients who did not suffer a perioperative stroke. Both groups had similar prevalence of class 4 angina, congestive heart failure, and emergency operation. The in-hospital morbidity, length of stay, and hospital costs were all significantly greater in the stroke population. Of patients who suffered stroke, 22.54% expired before discharge.

View larger version (37K): [in this window] [in a new window]   Fig 1. Survival curves for patients with and without stroke (X axis = years after operation; Y axis = survival).

	Comment

Top Abstract Introduction Patients and methods Results Comment References

Several studies have evaluated risk factors for stroke during coronary operation [2, 6, 8, 10]. McKhann and colleagues [2] reported that hypertension, increasing age, diabetes, and prior stroke all correlated with higher risk of stroke. Prolonged cardiopulmonary pump time was associated with a higher risk of stroke [2]. This finding has been supported in another study, suggesting that a longer pump time increased the risk of poor neurologic outcome [12].

Univariate analysis revealed that age, previous TIA, previous stroke, female gender, hypertension, and diabetes were all associated with higher risk of stroke. Logistic regression analysis was used to identify independent risk factors and odds ratios for variables associated with stroke. The three preoperative variables shown to be statistically significant independent predictors of stroke included age, prior TIA, and carotid bruits. These data support the work of Rao and colleagues [8] who identified triple vessel disease, normothermic systemic perfusion, age greater than 70 years, history of TIA or prior stroke, peripheral vascular disease, and diabetes as independent risk factors.

Age showed a strong correlation with stroke by univariate and multivariate analysis. An odds ratio of 1.9 per decade (CI 1.73 to 2.09) was calculated. This is consistent with data from a recent prospective multicenter study that showed older age correlated with a higher risk of stroke [1]. Other studies have shown a correlation of increasing age with stroke [2, 13], including a previous study from this institution that found older age to be a multivariate correlate of both stroke and death after coronary operation [12]. A history of previous TIA correlated with stroke after coronary artery bypass grafting (CABG) by both univariate and multivariate analysis. The odds ratio was 2.2 with a 95% CI of 1.32 to 3.68. Transient ischemic attacks have been shown to be predictors of carotid disease, as well as independent predictors of stroke [14]. Previous injury to the brain is thought to increase susceptibility to subsequent adverse effects of coronary operation [7]. Redmond and colleagues [7] showed that patients with a prior history of stroke not only had a greater risk of stroke, but were also extubated later and had a greater incidence of reintubation. Berens and colleagues [15] identified female sex, peripheral vascular disease, history of stroke or TIA, smoking, and left main coronary disease as risk factors for carotid disease in the elderly. Consistent with the present study, several centers have shown that prior stroke correlates with a greater risk of neurologic complications on univariate analysis [6, 8, 16, 17]. In the present study, prior stroke was not an independent predictor after multivariate analysis.

In this analysis, carotid bruits showed a statistically significant correlation after both univariate and multivariate analysis, supporting the previous report of Mickleborough and colleagues [6]. The odds ratio was 1.9, but the area under the ROC curve was only 0.69. This suggests that the ability to predict stroke is somewhat limited. At this institution, all carotid bruits are evaluated by carotid ultrasound prior to elective CABG. Selective use of carotid ultrasound can help identify those patients at risk for neurological complications [14]. With only minor variation between surgeons, the institutional policy has been to perform carotid endarterectomy under local anesthesia, 48 hours before elective CABG for any symptomatic stenosis greater than 70%, or for any asymptomatic stenosis greater than 80%. In the case of compelling carotid stenosis with truly unstable angina or tight left main coronary stenosis, a combined carotid endarterectomy is performed with coronary bypass. Preoperative carotid duplex ultrasound was performed for patients over age 65, or those with left main coronary disease, and for those with carotid bruits, significant peripheral vascular disease, or previous stroke. Preoperative identification of carotid stenosis by noninvasive duplex ultrasound allows for individualization of surgical treatment plans to achieve optimal outcomes.

Diabetes was a univariate correlate of stroke in this study. This is consistent with other published reports [2, 8, 18]. Patients in the present study had multiple risk factors for stroke. They were known to have macro and microvascular diseases. Coronary artery disease in diabetic patients may be more severe, predisposing patients to ventricular dysfunction, leading to postoperative hypotension and hypoperfusion syndrome with neurologic sequelae [8].

Preoperative hypertension was a univariate, but not a multivariate, correlate of stroke in this study. Cernaianu and colleagues [17] have shown that preoperative hypertension was an independent risk factor for postoperative cerebrovascular accident [16]. McKhann and colleagues [2] reported that hypertension was an independent predicator of stroke. Female gender was a univariate correlate of stroke in this study, but not a significant independent predictor of stroke: 37.7% of patients who suffered perioperative strokes were female, while 20% of patients who did not were female (p < 0.0001). Some authors have found no correlation between gender and stroke incidence.

Cost, length of stay, and morbidity were assessed in patients suffering stroke during coronary operation. As expected, all of these variables were significantly increased in the stroke population. On average, each preoperative stroke increased hospital costs (not charges) by $15,972.00. Rao and colleagues [8] found that patients suffering neurologic complications had prolonged length of stay in intensive care.

Vigilance in evaluating preoperative history of TIA stroke or carotid bruits is important, particularly in elderly patients. Left main coronary artery disease is a marker for carotid stenosis [8]. Advanced age, tobacco abuse, left main coronary stenosis, extensive peripheral vascular disease, and history of previous cerebrovascular accident or TIA are correlates of carotid disease, which is an important cause of preoperative stroke. Selected use of epiaortic ultrasound and transesophageal echocardiograph before aortic cannulation for cardiopulmonary bypass may allow the surgeon to appropriately individualize surgical technique to reduce incidence of stroke due to embolism of debris from the ascending aorta in high risk patients [12]. Adjustments in technique may range from use of a single cross-clamp, to ultrasound guided choice of cross-clamp site, to complete avoidance of aortic clamping and alternative sites of arterial cannulation.

Stroke remains a devastating complication of coronary bypass operation occurring in 2.0% of these patients, and carrying a 22.5% mortality. Three significant independent risk factors for stroke were identified in 10,860 consecutive patients having primary coronary bypass operation: age, prior TIA, and carotid bruits. Stroke was associated with higher mortality, longer hospitalization, and higher cost. Identification of risk factors for stroke may allow surgeons to individualize surgical techniques to reduce the incidence of stroke after coronary operation [11].

	References

Top Abstract Introduction Patients and methods Results Comment References

 

1. Roach G., Kanchuger M., Mangano C., Newman M., et al. Adverse cerebral outcomes after coronary bypass surgery. N Engl J Med 1996;335:1857-1863.[Abstract/Free Full Text]
2. McKhann G., Goldsborough M., Borowicz L., et al. Predictors of stroke risk in coronary artery bypass patients. Ann Thorac Surg 1997;63:516-521.[Abstract/Free Full Text]
3. Hartman G., Yao F., Bruefach M., et al. Severity of aortic atheromatous disease diagnosed by transesophageal echocardiography predicts stroke and other outcomes associated with coronary artery surgery. Anesth Analg 1996;83:701-708.[Abstract]
4. Barbut D., Gold J. Aortic atheromatosis and risks of cerebral embolization. J Cardiothor Vasc Anesth 1996;10:24-30.[Medline]
5. Crowley J., Hannigan M., Daly K. Reactive thrombocytosis and stroke following cardiopulmonary bypass surgery. Eur Heart J 1994;15:1144-1146.[Abstract/Free Full Text]
6. Mickelborough L., Walker P., Takagi Y., Ohashi M., Ivanov J., Tamariz M. Risk factors for stroke in patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg 1996;112:1250-1259.[Abstract/Free Full Text]
7. Redmond J.M., Greene P.S., Goldsborough M.A., et al. Neurologic injury in cardiac surgical patients with a history of stroke. Ann Thorac Surg 1996;61:42-47.[Abstract/Free Full Text]
8. Rao V., Christakis G., Weisel R., et al. Risk factors for stroke following coronary bypass surgery. J Card Surg 1995;10(Suppl):468-474.[Medline]
9. Ricotta J., Faggioli G., Castilone A., Hassett J. Risk factors for stroke after cardiac surgery. J Vasc Surg 1995;21:359-364.[Medline]
10. Libman R., Wirkowski E., Neystat M., Barr W., Gelb S., Graver M. Stroke associated with cardiac surgery. Arch Neurol 1997;54:83-87.[Abstract/Free Full Text]
11. Salasidis G., Latter D., Steinmetz O., Blair J., Graham A. Carotid artery duplex scanning in preoperative assessment for coronary artery revascularization. J Vasc Surg 1995;21:154-162.[Medline]
12. Craver J.M., Bufkin B.L., Weintraub W.S., Guyton R.A. Neurologic events after coronary bypass grafting. Ann Thorac Surg 1995;59:1429-1434.[Abstract/Free Full Text]
13. Marshall G., Shroyer A.L.W., Grover F.L., Hammermeister K.E. Bayesian-Logit model for risk assessment in coronary artery bypass grafting. Ann Thorac Surg 1994;57:1492-1500.[Abstract]
14. D’Agostino R.S., Svensson L.G., Neumann D.J., Balkhy H.H., Williamson W.A., Shahian D.M. Screening carotid ultrasonography and risk factors for stroke in coronary artery surgery patients. Ann Thorac Surg 1996;62:1714-1723.[Abstract/Free Full Text]
15. Berens E., Kouchoukos N., Murphy S., Wareing T. Preoperative carotid artery screening in elderly patients undergoing cardiac surgery. J Vasc Surg 1992;15:313-323.[Medline]
16. Sotaniemi K.A. Long-term neurologic outcome after cardiac operation. Ann Thorac Surg 1995;59:1336-1339.[Abstract/Free Full Text]
17. Cernaianu A., Vassilidze T., Flum D., et al. Predictors of stroke after cardiac surgery. J Card Surg 1995;10:334-339.[Medline]
18. Kurki T.S., Kataja M. Preoperative prediction of postoperative morbidity in coronary artery bypass grafting. Ann Thorac Surg 1996;61:1740-1745.[Abstract/Free Full Text]

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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): John D. Puskas John Parker Gott Joseph M. Craver Ellis L. Jones Robert A. Guyton William S. Weintraub Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Puskas, J. D. Articles by Weintraub, W. S. Search for Related Content PubMed PubMed Citation Articles by Puskas, J. D. Articles by Weintraub, W. S. Related Collections Related Article