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Eur J Cardiothorac Surg 2001;19:627-632
© 2001 Elsevier Science NL

Stroke during coronary bypass surgery: principal role of cerebral macroemboli

Division of Cardiovascular Surgery, University Health Network, and Department of Surgery, University of Toronto, Toronto General Hospital, Toronto, Ontario M5G 2C4, Canada

Received 13 September 2000; received in revised form 30 January 2001; accepted 24 February 2001.

Corresponding author. Tel.: +1-416-340-4215; fax: +1-416-340-3803
e-mail: charles.peniston{at}uhn.on.ca

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
Objective: The purpose of this study was to gain insight into the etiology of stroke during coronary bypass surgery. Methods: Retrospective review of prospectively gathered data on 6682 consecutive coronary bypass patients. Patients undergoing simultaneous procedures, including carotid endarterectomy, were excluded. We performed a systematic chart review of all patients who suffered a perioperative stroke. Predictors of stroke were determined with stepwise logistic regression analysis. Results: The prevalence of stroke was 1.5% (n=98). Stroke patients had significantly increased intensive care unit and hospital length of stays, as well as increased mortality when compared to patients without stroke (all P< 0.001). Independent predictors of stroke were (in decreasing order of magnitude): age >70 years, left ventricular ejection fraction <40%, previous stroke or transient ischemic attack, normothermic cardiopulmonary bypass, diabetes, and peripheral vascular disease. Chart review revealed that the probable cause of stroke was macroemboli, likely from ascending aorta atherosclerosis, in 37% of patients and unknown in 38% of patients. Computerized tomography (CT) scans were obtained in 79 patients (81%). Lesions detected by CT were consistent with a macroembolic etiology: nearly all lesions were ischemic in nature and located in the distribution of major cerebral arteries, particularly the middle cerebral artery. Conclusions: Stroke is a devastating complication of coronary bypass surgery. Our multivariable risk factors for stroke, chart review, and CT findings all suggest that macroemboli, presumably from the ascending aorta, are the predominant cause of stroke during coronary bypass surgery. Future studies should be directed at minimizing the risk of embolization during cardiac surgery.

Key Words: Stroke • Coronary bypass surgery • Cardiopulmonary bypass • Aortic atherosclerosis • Emboli

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
It has long been recognized that neurological complications are an important cause of morbidity and mortality in cardiac surgery [1]. Such complications range from subtle neuropsychological deficits to overt stroke and brain death. Cardiopulmonary bypass (CPB) is thought to play a major role in the etiology of these complications [2]. CPB may cause cerebral injury by microembolization, macroembolization, hypoperfusion, and/or induction of the inflammatory cascade. Experts have implicated each of these mechanisms as possible causative agents for stroke during cardiac surgery.

We have previously demonstrated that stroke during valvular surgery is predominantly caused by atherosclerotic emboli, shock, and septic emboli [3]. Information about the causes of stroke is important in order to determine methods of minimizing this catastrophic complication. The purpose of this study was to gain insight into the etiology of stroke during coronary bypass surgery.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
We investigated all patients undergoing isolated coronary bypass graft surgery (CABG) at the Toronto General Hospital from 1990 to 1995 (n=6682). Preoperative, perioperative, and postoperative data were collected prospectively on all patients. Our computerized surgical database was surveyed for those patients with a diagnosis of perioperative stroke (n=98), then a manual chart review was performed on these patients. The study protocol was approved by our institutional ethics review board.

Stroke was defined as a persistent (lasting longer than 1 week) neurologic deficit, consistent with a central nervous system lesion, that occurred within 30 days of operation. This definition of stroke is the same as that recommended by an international consensus conference on the reporting of complications of cardiac surgery [4]. In patients with a previous history of stroke or transient ischemic attack (TIA), a new stroke was diagnosed if they developed new neurologic findings or marked, prolonged worsening of their pre-existing neurologic deficits. Cardiac surgery and intensive care unit staff screened all patients for stroke postoperatively, and patients with suspected stroke were examined by an attending neurologist in order to confirm the diagnosis. Radiologic imaging by computerized tomography (CT) was obtained in all suspected stroke patients, with the exception of those who were too hemodynamically unstable and who subsequently died before imaging was possible.

Patients undergoing coronary artery bypass grafting (CABG) and simultaneous carotid endarterectomy (n=41), a particularly high risk group for stroke [5], were excluded. Patients were also excluded if they underwent simultaneous valvular procedures (n=766), resection of a left ventricular aneurysm (n=112), repair or replacement of the ascending or transverse aorta (n=103), adult congenital procedures (n=28), or simultaneous non-cardiac procedures (n=21).

2.1. Perioperative management
Preoperative management included screening for carotid vascular disease by duplex ultrasonography in patients with a carotid bruit or a history of previous stroke, TIA, or carotid endarterectomy.

Intraoperative management consisted of median sternotomy and heparinization, followed by establishment of cardiopulmonary bypass with an ascending aorta cannula and a single two-stage right atrial cannula. Aortic cannulation was performed in areas free of atherosclerotic plaque as assessed by digital palpation. Intraoperative epiaortic ultrasonography was not employed. During CPB hematocrit was maintained between 20 and 25%, pump flow rates between 2.0 and 2.5 l/min per m², and mean arterial pressures between 50 and 70 mmHg by use of phenylephrine hydrochloride or sodium nitroprusside as required. Mean arterial pressures were kept above 60 mmHg for patients with known carotid stenosis. Myocardial protection consisted of cold antegrade blood cardioplegia, with some patients receiving warm blood cardioplegia. Systemic temperature management consisted of drifting to 34°C at the start of CPB and then active rewarming at the end of bypass to 37.5°C, in the majority of patients. Some patients were kept normothermic (>35°C) throughout CPB. All coronary anastomoses were performed under a single aortic cross-clamp technique. Partial occluding cross-clamps were not employed.

Postoperatively, low cardiac output syndrome was treated with dopamine after preload, afterload, and heart rate had been optimized. Patients who did not respond to dopamine (10 µg/kg per min) received an intra-aortic balloon pump and additional inotropes as necessary to keep the cardiac index >2.0 l/min per m² and systolic blood pressure >90 mmHg.

2.2. Chart review
We performed a systematic chart review of all patients who developed stroke (n=98) in order to attempt to determine the etiology in each patient. As previously described [3], we used a prespecified set of clinical criteria that, if present in the chart review, would determine the potential etiology of stroke. Patients were assigned an etiology of ‘atherosclerotic emboli’ if they had severe atherosclerosis of the ascending aorta, as noted by digital palpation or aortic cannulation in the operative report. Patients were assigned an etiology of ‘shock’ if they had severe hypotension, as defined by a systolic blood pressure <60 mmHg for >10 min, excluding CPB. Patients were assigned an etiology of ‘carotid vascular disease’ if they had critical carotid stenosis (>90%) with ipsilateral cerebral infarction. Patients were assigned an etiology of ‘cardiogenic thromboembolus’ if they had atrial or ventricular thrombus, as documented by transesophageal echocardiography or intraoperative visual inspection. Patients were assigned an etiology of ‘unknown’ if they had zero or more than one of the previously described clinical criteria.

We also used our chart review to determine the timing of perioperative stroke. Stroke was defined as intraoperative if the patient woke up with a deficit and postoperative if the patient was neurologically intact upon awakening from the anesthetic. All strokes that occurred within 30 days of the operation were included in our analysis, in conformance with guidelines for reporting perioperative events [4].

2.3. Statistical analysis
Comparisons of variables, as listed in Appendix A, were made between patients with (n=98) and without (n=6584) perioperative stroke. The SAS version 6.12 for Windows (SAS Institute; Cary, NC) program was used for all statistical analyses. Chi-square or Fisher's exact tests were used to evaluate categorical data univariately. Continuous variables were evaluated by Student's unpaired t-tests or Wilcoxon rank-sum tests. Stepwise multivariable logistic regression analysis was used to calculate risk-adjusted odds ratios and to determine the independent predictors of stroke. All variables suggested by the univariate analysis (P<0.25) or those judged to be clinically important were entered into the logistic regression model. Model discrimination was evaluated by the area under the Receiver Operating Characteristic (ROC) curve and model precision was evaluated by the Hosmer–Lemeshow goodness-of-fit statistic, as previously described [6].

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
The prevalence of stroke was 1.5% (n=98). Patients who had a stroke were intubated longer (median 5.9 vs. 0.9 days for stroke vs. non-stroke patients), were in the intensive care unit longer (median 8.9 vs. 2.2 days), and had longer postoperative hospital stays (median 29.3 vs. 9.6 days, all P<0.001). Stroke patients had a higher prevalence of myocardial infarction (9.2 vs. 2.8%), low cardiac output syndrome (22.4 vs. 8.6%), and mortality than patients without stroke (27.6 versus 2.6%, all P<0.001).

Tables 1 and 2 reveal the univariate associations between stroke and preoperative and intraoperative variables, respectively. Statistically significant (P<0.05) univariate predictors of stroke were: age, left ventricular dysfunction, diabetes, peripheral vascular disease, hypertension, renal failure, previous stroke or TIA, preoperative atrial fibrillation, triple vessel coronary disease, failure to use a left internal mammary artery, CPB time, and aortic cross-clamp time.

View larger version (13K): [in this window] [in a new window]   Fig. 1. Independent predictors of stroke during coronary bypass surgery as identified by multivariable logistic regression analysis. LVEF, left ventricular ejection fraction; CVA, stroke; TIA, transient ischemic attack; CPB, cardiopulmonary bypass; PVD, peripheral vascular disease.

Computerized tomography was performed in 79 patients (81%), with the remaining patients being too hemodynamically unstable to obtain imaging. Review of the patients’ charts revealed that 73 CT scans were reported as showing new ischemic lesions, five scans were reported as normal, and one scan was reported as showing a large cerebral hemorrhage. The only hemorrhagic lesion belonged to the patient who received tPA for a peripheral arterial thrombosis.

Stroke location was determined by CT scan and/or autopsy report. In those patients who did not receive a CT or an autopsy (n=9), stroke location was determined by neurologic examination. Strokes were located in the distribution of the middle cerebral artery in 47 patients (48%), the posterior cerebral artery in 10 patients (10%), the anterior cerebral artery in two patients (2%), the vertebrobasilar artery eight patients (8%), and multiple locations in 30 patients (31%). A lacunar infarct was present in one patient.

	4. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
Neurologic injury during cardiac surgery has received increasing attention in the literature as mortality rates progressively decline [7]. The most common of these complications is neuropsychological impairment, which is predominantly caused by cerebral microembolization during CPB [8,9]. Stroke is the most disabling neurologic complication, occurring in 1–8% of patients [7,10]. We have previously examined the causes of stroke during valvular surgery [3]. The current study was performed in order to gain insight into the etiology of stroke during coronary bypass surgery. The current study suggests that the majority of strokes that occur during CABG are caused by cerebral macroemboli, as opposed to cerebral hypoperfusion, induction of the inflammatory cascade, or other possible causative agents. The findings that support this conclusion are: (1) CT scans and autopsies revealed lesions in the territorial distribution of major cerebral arteries, rather than lacunar or watershed infarcts [11,12]; (2) most strokes were located in the distribution of the middle cerebral artery, a finding that would be expected for macroembolization [11–13]; and (3) nearly all CT scans showed ischemic, rather than hemorrhagic, lesions [11,12].

Possible sources of cerebral macroemboli during coronary bypass surgery may be the ascending aorta, carotid arteries, intracerebral arteries, or intracardiac cavities. We believe the most likely source is the ascending aorta, for the following reasons.

First, the ascending aorta is the site of surgical manipulations during CABG, whereas mechanical contact is not made with the other potential sources of emboli. Embolization of atherosclerotic debris is most likely to occur during aortic cannulation/decannulation, cross-clamp application/removal, and construction of proximal anastomoses [14]. However, embolization of atherosclerotic debris may also occur when the aorta is not being surgically manipulated, due to the ‘sandblast’ effect of CPB.

Second, the majority of our independent predictors of stroke – elderly age, left ventricular dysfunction, previous stroke/TIA, diabetes, and peripheral vascular disease – are strongly associated with atherosclerosis of the ascending aorta [15,16]. Several other studies have identified these same risk factors for stroke during CABG [7,10,17]. Roach et al. prospectively followed 2108 patients undergoing coronary bypass surgery at 24 institutions [7]. The strongest independent predictor of stroke was atherosclerosis of the ascending aorta with an odds ratio of 4.5. Similarly, John et al. reviewed 19 224 CABG patients operated on at 31 hospitals in New York State over 1 year [17]. Aortic calcification was the leading risk factor for stroke with an odds ratio of 3.0.

Third, our chart review suggested that the most common probable cause of stroke was atherosclerotic emboli from the ascending aorta. Palpable lesions in the ascending aorta were noted in a large proportion of stroke patients.

The fourth reason we believe the ascending aorta is the likely source of macroemboli is because of ancillary autopsy data. Blauth et al. analyzed 221 consecutive autopsies in cardiac surgery patients [18]. These investigators found systemic atheroemboli in 26% of CABG patients, compared with 9% of valvular patients. Systemic atheroemboli were present in 37% of patients with atherosclerosis of the ascending aorta versus 2% of patients without ascending aortic disease. For all of the above reasons, we believe that atherosclerotic macroemboli from the ascending aorta are the predominant cause of stroke during CABG.

The discernment of macroemboli as the principal cause of stroke is important for several reasons. First, it enables identification of high risk patients. Diffuse atherosclerosis of the ascending aorta can be identified by CT, transesophageal echocardiography, or intraoperative epiaortic ultrasonography. The identification of high risk patients may help predict resource allocation and costs, as well as provide a target population for trials of neuroprotective agents.

The second reason this observation is important is because it creates a focus for the development of novel surgical techniques. Methods of decreasing embolization that have already been studied include the use of intra-aortic filters [19] and alternative aortic cannulation techniques [20]. In a prospective randomized clinical trial, we found that cannulation of the distal aortic arch resulted in a 50% reduction in cerebral emboli during coronary bypass surgery [20]. Although this technique is more technically demanding than standard cannulation of the ascending aorta, it may be an important method of reducing embolization in patients with atherosclerosis of the ascending aorta.

Another method of decreasing the risk of embolization is by minimizing aortic manipulation. Such techniques include avoiding the use of partial occluding aortic clamps [21], using multiple arterial grafts to decrease the number of proximal anastomoses [22], and performing off-pump CABG [23,24]. The benefits of beating heart surgery may be mitigated, however, if multiple applications of the partial occluding clamp are employed.

The routine use of epiaortic ultrasonography, already employed in some cardiac surgery centers, may also play an important role in decreasing the risk of embolization [25]. Epiaortic ultrasonography is the most accurate method of assessing atherosclerosis of the ascending aorta, and can be used to guide surgeons to cannulate and instrument those areas of the aorta that are relatively disease-free.

4.1. Study limitations
One limitation of the current study is our method of assessment of the ascending aorta. We assessed atherosclerosis of the ascending aorta with digital palpation, which is known to be inferior to epiaortic ultrasonography. Unfortunately, we did not have an epiaortic probe at the time of this study, leaving digital palpation as our only available method. Digital palpation is currently the most common method of aortic assessment in cardiac surgery patients. However, as evidence of the beneficial effects of epiaortic ultrasonography begin to accrue [15,25], an argument may be made supporting its routine clinical use.

Another limitation of our study is that we did not have detailed information on the severity of carotid stenosis in our patient population, which may have resulted in underestimation of its effects on stroke. However, the previously mentioned studies by Roach et al. [7] and John et al. [17] revealed that atherosclerosis of the ascending aorta is a much stronger predictor of stroke during CABG than carotid stenosis.

	5. Summary

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
Stroke is a devastating complication of coronary bypass surgery. Our multivariable analysis, chart review, and CT findings strongly suggest that macroemboli are the principal cause of stroke during CABG. The most likely source of these macroemboli is ascending aortic atherosclerosis. Future studies should be directed at minimizing the risk of embolization during cardiac surgery.

	Acknowledgments

 
M.A.B., V.R. and J.I. are Research Fellows of the Heart and Stroke Foundation of Ontario. R.D.W. is a Career Investigator for the Heart and Stroke Foundation of Ontario.

	Appendix

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 
Appendix A. Variables assessed in predictive models

Age Sex Left ventricular ejection fraction Assessed by angiography or 2D echocardiography Urgent timing Operation during same hospitalization, including emergency procedures Reoperation Any previous cardiac operative procedure Renal failure Serum creatinine >200 mmol/l or history of renal failure Diabetes mellitus History of diabetes treated with diet, oral hypoglycemics, or insulin Hypertension Patient taking antihypertensive medication preoperatively Smoking Previous or present Previous TIA or stroke Peripheral vascular disease History of peripheral or carotid vascular disease Congestive heart failure History of hospital admission for heart failure Preoperative myocardial infarction Myocardial infarction within 30 days of surgery Atrial fibrillation History of preoperative atrial fibrillation Triple vessel coronary artery disease Left main coronary artery disease Angina class Canadian Cardiovascular Society angina class Normothermic CPB Minimum systemic temperature >35°C, as measured by nasopharyngeal probe Cardioplegia temperature Cold (<28°C) or warm (28°C) blood cardioplegia Retrograde cardioplegia Use of LIMA Coronary endarterectomy CPB time Aortic cross-clamp time

	References

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Summary Appendix References

 

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				N. Hedayati, J. T. Sherwood, S. J. Schomisch, J. L. Carino, and A. H. Markowitz Axillary artery cannulation for cardiopulmonary bypass reduces cerebral microemboli J. Thorac. Cardiovasc. Surg., September 1, 2004; 128(3): 386 - 390. [Abstract] [Full Text] [PDF]

				C. Schmitz, S. Weinreich, J. White, I. Oengoeren, R. Schneider, D. Schneider, I. Speth, C. Pohl, and A. Welz Can particulate extraction from the ascending aorta reduce neurologic injury in cardiac surgery? J. Thorac. Cardiovasc. Surg., December 1, 2003; 126(6): 1829 - 1836. [Abstract] [Full Text] [PDF]

				J. E. Scarborough, W. White, F. E. Derilus, J. P. Mathew, M. F. Newman, and K. P. Landolfo Combined use of off-pump techniques and a sutureless proximal aortic anastomotic device reduces cerebral microemboli generation during coronary artery bypass grafting J. Thorac. Cardiovasc. Surg., November 1, 2003; 126(5): 1561 - 1567. [Abstract] [Full Text] [PDF]

				C. Hagl, J. D. Galla, D. Spielvogel, C. Bodian, S. L. Lansman, R. Squitieri, M. A. Ergin, and R. B. Griepp Diabetes and evidence of atherosclerosis are major risk factors for adverse outcome after elective thoracic aortic surgery J. Thorac. Cardiovasc. Surg., October 1, 2003; 126(4): 1005 - 1012. [Abstract] [Full Text] [PDF]

				R. C. Gilkeson, A. H. Markowitz, and L. Ciancibello Multisection CT Evaluation of the Reoperative Cardiac Surgery Patient RadioGraphics, October 1, 2003; 23(90001): S3 - 17. [Abstract] [Full Text] [PDF]

				P. E. Antunes, J. Ferrao de Oliveira, and M. J. Antunes Predictors of cerebrovascular events in patients subjected to isolated coronary surgery. The importance of aortic cross-clamping Eur. J. Cardiothorac. Surg., March 1, 2003; 23(3): 328 - 333. [Abstract] [Full Text] [PDF]

				J. Bucerius, J. F. Gummert, M. A. Borger, T. Walther, N. Doll, J. F. Onnasch, S. Metz, V. Falk, and F. W. Mohr Stroke after cardiac surgery: a risk factor analysis of 16,184 consecutive adult patients Ann. Thorac. Surg., February 1, 2003; 75(2): 472 - 478. [Abstract] [Full Text] [PDF]

				R. J. Frumento, C. M.N. O'Malley, and E. Bennett-Guerrero Stroke after cardiac surgery: a retrospective analysis of the effect of aprotinin dosing regimens Ann. Thorac. Surg., February 1, 2003; 75(2): 479 - 483. [Abstract] [Full Text] [PDF]

				D. J. Cook, T. A. Orszulak, K. J. Zehr, N. A. Nussmeier, J. J. Livesay, J. W. Hammon, and X. Chen Effectiveness of the Cobra aortic catheter for dual-temperature management during adult cardiac surgery J. Thorac. Cardiovasc. Surg., February 1, 2003; 125(2): 378 - 384. [Abstract] [Full Text] [PDF]

				P. W.M. Fedak, N. Mamalias, and R. D. Weisel Invited commentary Ann. Thorac. Surg., December 1, 2002; 74(6): 2160 - 2160. [Full Text] [PDF]

				D. Bainbridge and D. Cheng Initial Perioperative Care of the Cardiac Surgical Patient Seminars in Cardiothoracic and Vascular Anesthesia, September 1, 2002; 6(3): 229 - 236. [Abstract] [PDF]

G. M. McKhann, M. A. Grega, L. M. Borowicz Jr, M. Bechamps, O. A. Selnes, W. A. Baumgartner, and R. M. Royall Encephalopathy and Stroke After Coronary Artery Bypass Grafting: Incidence, Consequences, and Prediction Arch Neurol, September 1, 2002; 59(9): 1422 - 1428.