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Ann Thorac Surg 2001;72:1195-1201
© 2001 The Society of Thoracic Surgeons

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Original article: cardiovascular

Stroke after cardiac surgery: short- and long-term outcomes

^a Division of Cardiac Surgery, The Johns Hopkins University, Baltimore, Maryland, USA
^b Department of Neurology, The Johns Hopkins University, Baltimore, Maryland, USA

Accepted for publication May 29, 2001.

Address reprint requests to Dr Baumgartner, Blalock 618-Cardiac Surgery, Johns Hopkins Hospital, 600 N. Wolfe St, Baltimore, MD 21287-4618
e-mail: wbaumgar{at}csurg.jhmi.jhu.edu

	Abstract

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Background. Stroke remains a devastating complication of cardiac surgery, but stroke prevention remains elusive. Evaluation of early and long-term clinical outcomes and brain-imaging findings may provide insight into stroke prognosis, etiology, and prevention.

Methods. Five thousand nine hundred seventy-one cardiac surgery patients were prospectively studied for clinical evidence of stroke. Stroke and nonstroke patients were compared by early outcomes. Data collected for stroke patients included brain imaging results, long-term functional status, and survival. Outcome predictors were then determined.

Results. Stroke was diagnosed in 214 (3.6%) patients. Brain imaging demonstrated acute infarction in 72%; embolic in 83%, and watershed in 24%. Survival for stroke patients was 67% at 1 year and 47% at 5 years. Independent predictors of survival were cerebral infarct type, creatinine elevation, cardiopulmonary bypass time, preoperative intensive care days, postoperative awakening time, and postoperative intensive care days. Long-term disability was moderate to severe in 69%.

Conclusions. Stroke after cardiac surgery has profound repercussions that are independently related to infarct type and clinical factors. These data are essential for clinical decision making and prognosis determination.

	Introduction

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Stroke remains one of the most devastating potential complications of cardiac surgery. Many investigators have studied the incidence of stroke in this population, yielding estimates ranging from 1.6% to 5.2% [1–4]. Of the more than 400,000 adult patients in the United States [5] and 800,000 patients worldwide who undergo cardiopulmonary bypass procedures each year, up to 21,000 patients nationally and 42,000 patients worldwide will suffer stroke. The economic impact of stroke after coronary revascularization is estimated to exceed $2 to $4 billion annually worldwide [6].

Although cardiac surgeons, cardiologists, and affiliated clinicians have witnessed the profound effects of perioperative stroke in patients, few data exist to characterize both the functional impact and long-term survival for those who suffer this complication. Many attempts have been made, however, to determine the essential risk factors for perioperative stroke [1, 4, 7–9]. Although these efforts have yielded important data, it is clear that definitive prediction and prevention of these strokes remain elusive. This is likely due to the multifactorial etiology of stroke, as well as the heterogeneity of this patient population and the cardiac procedures themselves. Previous studies were limited by small sample size (with few strokes), retrospective study design, incomplete or late capture of stroke events, minimal analysis of brain-imaging findings, and lack of long-term follow-up.

A thorough understanding of outcomes and their predictors is essential to etiology determination and development of preventative strategies for stroke after cardiac surgery. The purpose of this study, therefore, was: (1) to evaluate early and late outcomes for patients who suffer stroke in terms of patient characteristics, intraoperative and perioperative variables, and the manifestations of stroke on brain imaging; and (2) to determine predictors of outcome in order to establish prognostic indicators and estimates for this complication.

	Material and methods

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Over a 5.5-year period (January 1992 to July 1997) at the Johns Hopkins Hospital, 5,971 consecutive, adult cardiac surgery patients were followed prospectively for clinical evidence of stroke by one of two research clinicians (MAG, LMB). Data collected for all patients included demographic information, operative procedure, postoperative in-hospital outcomes, discharge disposition, and hospital charges. Patients with focal neurological deficits (motor weakness, dysphagia, aphasia, cognitive deficits, seizures, or coma) within the first 9 postoperative days were evaluated by staff neurologists. The clinical diagnosis of stroke was made by the neurologist on the basis of clinical findings alone, independent of brain imaging findings. Once a clinical diagnosis of stroke was made, patients were entered into the Johns Hopkins Cardiac Surgery Stroke Database, which is used to monitor clinical practice.

For patients diagnosed with clinical stroke, data were collected by research clinicians for preoperative comorbidities, number of days spent preoperatively in the coronary care unit (CCU), and intraoperative indices. Postoperative data collected for stroke patients included the measured increase in serum creatinine from preoperative baseline, the number of postoperative hours until awakening, and the postoperative time until stroke presentation or detection. A total of 33 variables were collected. Stable patients underwent brain imaging with computed tomography or magnetic resonance imaging. All imaging studies were reviewed (retrospectively) for infarct type and cerebral distribution by a staff neurologist (RJW) and neuroradiologist, who were unaware of the patients’ clinical outcomes. Acute infarcts were classified radiographically as being embolic (large artery), watershed (border-zone), or lacunar (small vessel) in nature. Cerebral distribution was described according to vascular territory and the region of brain affected.

Assessment of long-term survival and functional status for stroke patients was performed by telephone interview. The modified Rankin Scale [10], a standardized questionnaire, was employed to evaluate functional status. The Rankin Scale ranges from 0 to 6; a score of 0 indicates the absence of any symptoms or functional deficits; a score of 6 indicates that the patient had died.

Comparisons of categorical and linear variables were made using the Fisher’s exact test and two-tailed Student’s t test, respectively. Survival estimates were calculated using the Kaplan-Meier method. Predictors of categorical and linear outcomes were determined by stepwise logistic and linear multivariate regression, respectively. Predictors of survival were determined using the Cox Proportional-Hazards model in a stepwise fashion. Statistical significance was defined to be present at the p equal to the 0.05 level.

	Results

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Stroke incidence and early outcomes
Of the 5,971 patients evaluated in this study, 214 (3.6%) patients showed evidence of clinical stroke within the first 9 days after their operation. The presentation of clinical stroke occurred, on average, on postoperative day 0.86 ±1.84, with 74% (158 of 214) presenting on postoperative day 0 and 91% (195 of 214) within the first 3 postoperative days. The incidence of stroke by procedure type is listed in Table 1. Isolated procedures (eg, coronary artery bypass grafting [CABG]) were associated with a lower stroke rate than combined procedures (eg, CABG/valve), p less than 0.0001. The mean age of stroke patients (68.9 ± 9.9 years) was significantly higher than that of nonstroke patients (62.2 ± 12.9 years), p less than 0.0001. Gender differences were minimal, with 136 of 214 (63.6%) male stroke patients and 3,807 of 5,757 (66.1%) male nonstroke patients. The incidence of stroke in females was no different than in males.

Only 13% of patients with a postoperative stroke had reported a history of stroke before cardiac surgery. However, on brain imaging, 42% (88 of 209) of patients had evidence of chronic infarction or ischemic changes. These findings represented lacunar infarction in 48 (55%), large vessel infarction in 30 (34%), and periventricular white matter ischemic changes in 35 (40%) patients.

Of those 151 patients who demonstrated acute infarction on brain imaging, the infarction was classified as purely embolic (large artery) in 71% (107) and purely watershed (border-zone) in 12% (18). A mixed infarction pattern (embolic + watershed) was present in 12% (18). Therefore, 125 (83%) patients demonstrated an embolic component of infarction, and 36 (24%) patients demonstrated a watershed component of infarction. Figures 1 and 2 show examples of embolic and watershed cerebral infarctions, respectively.

View larger version (111K): [in this window] [in a new window]   Fig 1. Example of embolic (large artery) cerebral infarction. Computer tomography (CT) in a patient with complete right middle cerebral artery territory infarction (within arrows). Embolic infarctions involve a well-defined vascular territory and characteristically have a triangular appearance on CT.

View larger version (74K): [in this window] [in a new window]   Fig 2. Examples of watershed (border-zone) cerebral infarction. Computed tomography in a patient with multiple watershed (border-zone) infarctions (A and B). (A) The arrow indicates a frontal lobe, middle cerebral artery-anterior cerebral artery (MCA-ACA) border-zone infarction. (B) The arrow indicates a parietal/occipital, middle cerebral artery-anterior cerebral artery, posterior cerebral artery (MCA-ACA-PCA) border-zone infarction. Watershed infarction is defined as an infarct between vascular territories. The term "watershed" infarct refers to the neuroimaging characteristics of the infarct and does not necessarily imply mechanism of stroke.

Predictors of early outcomes in stroke patients
Comorbidities in stroke patients included hypertension in 170 (79%), hypercholesterolemia in 93 (43%), diabetes mellitus in 82 (38%), history of cigarette smoking in 134 (63%), and history of stroke in 27 (13%) patients. The number of days spent preoperatively in the CCU averaged 0.58 ± 1.47, and 108 (50%) of these patients had been transferred to our institution from an outside hospital. Cardiopulmonary bypass time averaged 139.9 ± 58 minutes, and aortic cross-clamp time averaged 83.1 ± 40.5 minutes. Lowest esophageal temperature during surgery had a mean of 26.0°C ± 3.5°C. Pulsatile flow was used in 53 (25%) and cell-saver was used in 143 (67%) patients. The operative surgeon reported that there was severe ascending aortic disease (via palpation) in 82 (38%) patients.

Postoperatively, stroke patients awakened a mean of 14.8 hours (± 15.2) after operation, and stroke was diagnosed a mean of 0.86 ± 1.84 days after operation. Preoperative serum creatinine averaged 1.55 ± 1.33 mg/dL, and the stroke patients averaged a 0.37 ± 0.91 mg/dL increase in serum creatinine within the first 7 postoperative days. Twenty-seven (13%) stroke patients had an intraaortic balloon pump placed either preoperatively or intraoperatively.

Postoperative time to awakening was directly related to type of cerebral infarction. Patients with embolic infarction averaged 14.7 ± 16.2 hours to awaken, while patients with watershed infarction averaged 22.4 ± 17.3 hours, and those with mixed infarctions averaged 25.0 ± 19.4 hours. Stroke patients demonstrating any acute infarction on brain imaging averaged 16.7 ± 16.9 hours to awaken, while stroke patients who did not show acute infarction on brain imaging averaged only 10.0 ± 8.0 hours (p < 0.005).

In-hospital mortality was 19% and operative (30-day) mortality was 14%. Of the 33 variables analyzed, the statistically significant independent predictors of both types of mortality are shown in Table 3. Independent negative predictors of discharge directly to home were similarly determined. Postoperative increase in serum creatinine (per 1 mg/dL increase, Odds Ratio [OR] =0.32, p < 0.001), prior history of stroke (OR = 0.25, p = 0.013), evidence of watershed infarction on brain-imaging (OR = 0.28, p = 0.005), and number of preoperative CCU days (per day, OR = 0.73, p = 0.031) were all negative predictors of patients being discharged to home.

Predictors of late outcomes in stroke patients
Assessment of long-term survival was completed for 211 (99%) stroke patients, with a mean follow-up of 1.89 ± 1.75 years (range 0.01 to 5.99 years). Overall survival was 67% at 1 year and 47% at 5 years (see Fig 3). Statistically significant independent predictors of late mortality are shown in Table 4. Long-term survival based on infarct type is presented in Table 5.

View larger version (15K): [in this window] [in a new window]   Fig 3. Kaplan-Meier survival curve for all stroke patients. Dashed lines indicate the upper and lower limits for the 95% confidence interval.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

The profound impact of stroke after cardiac surgery is demonstrated by a nearly fivefold increase in hospital mortality (19% vs 4%) [6], a more than doubling of intensive care unit and postoperative length of stays, and a $30,000 increase in total hospital charges. Furthermore, stroke patients were only half as likely to be discharged to home, and therefore incurred much more nursing home and rehabilitation center charges. Late outcome assessment further demonstrated the severity of stroke after cardiac surgery. Many studies of long-term survival in patients aged 70 years or greater after CABG have described 5-year survival rates of 66% to 86% [12, 13]. Despite a lower average age of 68.9 years, stroke patients in this study had a 1-year survival of 67% and 5-year survival of only 47%, with median survival of 3.2 years. These data are further contrasted with the life expectancy of a 69 year old in the general population, which is 13.3 years for males and 16.2 years for females [14]. Assessment of functional status in stroke patients demonstrated marked long-term disability. Of the 81% of patients who survive to hospital discharge, only 39% lead a life with minimal disability. That is, of all patients who suffered stroke in this study, approximately two-thirds of patients will suffer early demise or lead a life of significant disability, findings that are similar to those reported by Roach and associates [6]. The personal, familial, and societal impact of stroke cannot be overstated [15, 16].

Independent predictors of these early and late outcomes were determined for stroke patients. The utility of these data is clear for clinical decision making and providing prognostic information to family members, who often make decisions on behalf of the patient. Our analysis reinforced the importance of acute renal dysfunction, length of cardiopulmonary bypass, postoperative time to awakening, and preoperative CCU stay in predicting outcomes. Furthermore, this analysis emphasized the significant influence of brain-imaging results (ie, acute infarct presence and type) on long-term survival and functional status. Patients without evidence of acute infarction on brain-imaging studies, despite the clinical diagnosis of stroke, fare much better. Patients with watershed infarction or a mixed infarction pattern, however, have dismal long-term outcomes.

Brain-imaging for patients diagnosed with clinical stroke revealed evidence of acute infarction in approximately 70% of patients, irrespective of the imaging modalities utilized. While the majority of acute infarcts were purely embolic in nature (71%), a significant number of infarcts demonstrated a watershed component (24%). Previous studies of acute infarcts in stroke patients after cardiac surgery have shown watershed infarcts in 14% to 27% of patients, although these were much smaller series [17, 18]. New brain-imaging technologies such as magnetic resonance imaging/angiography with diffusion and perfusion studies promise to be much more sensitive in detecting ischemic defects [19]. This technology may demonstrate that nearly all patients with clinical stroke do in fact have demonstrable defects, some of which may be reversible.

Stroke after cardiac surgery has been attributed to multiple etiologies. A significant potential cause of embolic stroke is the result of aortic manipulation (eg, clamping, cannulation) [2, 20–22] and the sandblasting effect of flow through the aortic cannula against the aortic wall [23–25]. Large emboli that escape from or through the arterial pump line filter, whether consisting of air or platelet/thrombin aggregates, have also been implicated as a potential source of embolic stroke [26]. Finally, valve and other open cardiac procedures involving the left heart carry the risk of bubble, thrombus, or particulate matter embolization to the brain with resultant embolic stroke. This study demonstrates that the majority of acute cerebral infarcts after cardiac surgery do demonstrate an embolic pattern, a finding reported by others [5, 18, 27–29]. It should be reemphasized, however, that approximately 25% of patients with acute infarction demonstrated a watershed component. Traditionally, watershed or "border-zone" infarctions have been attributed to global hypoperfusion, whether secondary to the lower perfusion pressures of cardiopulmonary bypass or distal hypoperfusion related to stenotic arch or cerebral vessels [18, 30, 31]. Recent investigators have suggested that watershed infarction may also result from fine embolic shower of atheromatous debris or cholesterol [2, 32].

Whatever the specific etiologies of these infarction patterns may be, it is clear that distinct infarct types occur after cardiac surgery and that infarct type is a major independent predictor of short-term and long-term outcomes. Given the findings of this study, the difficulty with which previous investigators have attempted to determine specific risk factors for stroke after cardiac surgery is less surprising [1, 3, 4, 7, 28, 29]. Any prediction and prevention of stroke in this population needs to be approached in light of the distinct infarct types and the corresponding potential etiologies.

Aortic manipulation appears to be a major causative factor of stroke after cardiac surgery, whether secondary to large emboli or fine embolic shower. Novel approaches to the prevention of aorta-related stroke are needed. These may include better diagnosis and management of aortic disease using epiaortic ultrasound or transesophageal echocardiography, performance of proximal coronary anastomoses without removing the aortic cross-clamp (minimizing aortic trauma), and arch vessel protective "screens" for use during aortic manipulation [33]. Furthermore, a better understanding is needed of the relative contribution of the cardiopulmonary bypass pump circuit to embolic events, especially that of the arterial line filter. Finally, cerebral hypoperfusion both intraoperatively and during the immediate postoperative period must be carefully avoided, especially in patients with previous stroke or cerebrovascular disease.

Stroke after cardiac surgery is a devastating complication that has profound economic and functional repercussions in addition to hastening patient demise. Short- and long-term outcomes are independently related to specific patient and clinical parameters, thereby establishing a realistic assessment of patient prognosis after stroke. Furthermore, patients who suffer stroke after cardiac surgery manifest distinct cerebral infarction patterns that are associated with specific outcomes. These findings facilitate a reassessment of stroke etiology and suggest that future investigations of stroke etiology and prevention need to incorporate the notion of multiple potential mechanisms.

	Acknowledgments

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We would like to thank Drs Guy M. McKhann and Pamela Talalay for their assistance in the review of this manuscript. Special thanks to the CSICU nurses and staff who care for the cardiac surgical patients and provided assistance in data collection.

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