(Circulation. 1999;100:642-647.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
Risk Factors for Early or Delayed Stroke After Cardiac Surgery
From the Department of Anesthesiology (C.W.H., V.G.D.-R.); the Cardiovascular Division, Department of Internal Medicine (V.G.D.-R.); and the Department of Biostatistics (K.B.S.), Washington University School of Medicine and Barnes-Jewish Hospital, St Louis, Mo.
Correspondence to Charles W. Hogue, Jr, MD, Department of Anesthesiology, Washington University School of Medicine, 660 S Euclid Ave, Box 8054, St Louis, MO 63110. E-mail hoguec{at}notes.wustl.edu
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Abstract |
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Background—Stroke after cardiac surgery is a devastating complication that leads to excess mortality and health resource utilization. The purpose of this study was to identify risk factors for perioperative stroke, including strokes detected early after cardiac surgery or postoperatively.
Methods and Results—Data were obtained from 2972 patients
undergoing coronary artery bypass graft and/or valve surgery.
Patients 
65 years old and those with a history of
symptomatic neurological disease underwent preoperative
carotid artery ultrasound scanning. Intraoperative epiaortic ultrasound
to assess for ascending aorta atherosclerosis was
performed in all patients. New strokes were considered as a single end
point and were categorized with respect to whether they were detected
immediately after surgery (early stroke) or after an initial,
uneventful neurological recovery from surgery (delayed stroke). Strokes
occurred in 48 patients (1.6%); 31 (65%) were delayed strokes. By
multivariate analysis, prior neurological
event, aortic atherosclerosis, and duration of
cardiopulmonary bypass were independently associated with early
stroke, whereas predictors of delayed stroke were prior neurological
event, diabetes, aortic atherosclerosis, and the
combined end points of low cardiac output and atrial fibrillation.
Female sex was associated with a 6.9-fold increased risk of early
stroke and a 1.7-fold increased risk of delayed stroke. In-hospital
mortality of patients with early (41%) and delayed (13%) strokes was
higher than that of other patients (3%, P=0.0001).
Conclusions—Most strokes after cardiac surgery occurred after initial uneventful recovery from surgery. Women were at higher risk to suffer early and delayed perioperative strokes. Atrial fibrillation had no impact on postoperative stroke rate unless it was accompanied by low cardiac output syndrome.
Key Words: stroke • surgery • atherosclerosis
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Introduction |
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Stroke is one of the most devastating complications of cardiac surgery, and it can lead to a decreased quality of life and excess mortality.1 2 3 4 5 6 7 8 9 10 The frequency of this complication is reported to be as high as 5% in patients undergoing coronary artery bypass graft (CABG) surgery, almost 9% in CABG patients
75 years of age, and nearly 16% in patients undergoing
valve surgery or those with preexisting cerebrovascular
disease.1 2 3 4 5 6 7 8 9 10 Adverse neurological events also have
important economic consequences, with estimated costs that exceed $2 to
$4 billion annually worldwide for patients with stroke after CABG
surgery.7 Moreover, the impact of stroke on patient
outcome is likely to remain substantial in light of the predicted
increase in elderly patients, who often suffer from comorbidity
predisposing to stroke and who will require cardiac surgery in the next
century.11 12 Therefore, identification of individuals at
risk for perioperative stroke is increasingly important
not only to accurately assess patient risk for surgery but also to
foster the development of new strategies to reduce the frequency of
this complication. Investigations have identified multiple risk factors for stroke after cardiac surgery, but the clinical applicability of these findings has been restricted by methodological limitations, including the frequent failure to include in the analysis an accurate assessment for important stroke predictors, such as atherosclerosis of the ascending aorta and carotid arteries.1 2 3 4 5 6 7 8 9 10 13 14 15 Previous studies have also in most cases considered strokes occurring during and after surgery as a single end point, despite reports suggesting that many strokes occur after an initial uneventful neurological recovery from surgery.1 2 3 4 5 6 7 8 9 10 The causes of these "delayed" postoperative strokes may differ from the causes of those that occur during surgery. Furthermore, the consideration of all strokes as a single end point, regardless of timing of the event, could lead to underestimation of the importance of variables specific to a particular perioperative period.
The purpose of this study was to identify risk factors for early and delayed stroke in a cohort of cardiac surgical patients to whom an aggressive strategy was applied to identify atherosclerosis of the carotid arteries and ascending aorta.
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Methods |
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Patient Population
The population consisted of 2972 of 3321 consecutive patients (1900 men and 1072 women)
50 years old who underwent cardiac surgery
at Barnes-Jewish Hospital from January 1990 through August 1996.
Patients were excluded (n=349) if aortic root replacement was planned
before surgery, if emergency procedures were necessary, or if epiaortic
ultrasound equipment was unavailable (see below). This study was
approved by the Human Studies Committee at Washington University.
Preoperative Data
Patient data were analyzed as previously reported,
including the recording of information on previous neurological
events, such as stroke.8 16 17 18 19 Documentation of a prior
stroke required verification by each patient's primary care physician,
review of medical records, and review of results of CT and/or MRI
when available. Left ventricular function was assessed
angiographically and graded by use of criteria of the Coronary
Artery Surgery Study.20 Carotid artery duplex scanning was
performed as previously described in patients 65 years old and in
younger patients with carotid artery bruits and/or symptoms or history
of neurological events, including transient ischemic
episodes.15 Carotid artery stenosis was graded as
follows: insignificant or no disease (luminal narrowing 
50%);
moderate disease (narrowing >50% but <80%); severe disease
(narrowing 80 but 99%); and complete occlusion. For the
analysis, severe disease and complete occlusion were
combined.
Intraoperative Data
Epiaortic ultrasound of the ascending aorta was performed to
evaluate for atheromatous disease, and the information
was used at the time of surgery to avoid atheroma during
aortic manipulations.8 16 17 18 19 Changes in surgical
technique based on epiaortic ultrasound results were classified as
minor and major alterations. Minor alterations included a change in any
of the following: site of aortic cannulations, aortic cross-clamping,
or proximal bypass graft anastomosis. Major alterations included
replacement of a portion of the severely atherosclerotic ascending
aorta with a Dacron graft under hypothermic circulatory arrest, as
previously described.8 The severity of
atherosclerosis was graded independently by 2 blinded
investigators as follows: insignificant or no
atherosclerosis; mild atherosclerosis
(intimal thickening <3.0 mm without intimal irregularities); or
moderate to severe atherosclerosis (3.0 mm
thickening with diffuse irregularities, large mobile or protruding
atheromata, ulcerated plaques, and/or
thrombi).8 16 17 18 19
Postoperative Data
Complications documented included myocardial infarction (new Q
waves on the 12-lead ECG or ratio of fractionated lactic dehydrogenase
[LDH1/LDH2] >1 during
the first 72 hours), low cardiac output syndrome (cardiac index of
<2.0 L · min-1 ·
m-2 for >24 hours after surgery regardless of
treatment), renal failure (requiring dialysis), and death. Continuous
telemetry ECG monitoring was performed until the time of hospital
discharge to document atrial fibrillation.
Neurological Complications
Stroke was defined as any new permanent global or focal
neurological deficit that could not be attributed to other neurological
(eg, dementia) and/or medical (ie, metabolic abnormalities,
hypoxia, or drugs) processes. Reversible cerebral
ischemic events were not included in the analysis
because evidence of these events cannot be identified under general
anesthesia and their detection is hindered postoperatively
owing to residual anesthetics, analgesics, and sedative drugs. Strokes
were diagnosed by a neurologist, and in the majority of patients they
were confirmed by CT head scan. All stroke data were reviewed by 3
investigators, and the temporal onset of the deficits was classified by
consensus as either an early stroke, if the neurological deficit was
present after emergence from anesthesia, or a delayed
stroke, if the patient developed the neurological deficit after first
awaking from surgery without a neurological deficit.
Statistical Analysis
Data were analyzed by version 6.12 of SAS.
Univariate comparisons between subjects with and without
stroke were performed with 
2 tests for
dichotomous variables and ANOVA for ordered categorical and
continuous variables. The latter analyses were performed
nonparametrically when regression residuals suggested that
the model fit was poor. Stepwise logistic regression was used to select
a best set of independent predictors of both early and delayed stroke.
Variables entered into the initial logistic models were those with
a univariate probability value of P<0.2. The
final model included all variables with an independent significance
level of P<0.1. The quality of the fit of the logistic
model was tested with the Hosmer and Lemeshow goodness-of-fit test.
Data for continuous variables are presented as mean±SD. A
significant difference was considered to exist when
P<0.05.
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Results |
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Strokes
Demographic and other characteristics of all patients are listed in Table 1
. Stroke occurred in 48
patients (1.6%). Seventeen strokes (35% of strokes, 0.6% of
patients) were detected early after surgery; 31 (65% of strokes, 1.0%
of patients) were delayed (Figure).
Fourteen early strokes (82%) and 22 delayed strokes (71%) occurred in
patients 65 years old. The frequency of stroke after the different
surgical procedures that the study patients underwent (Table 2) was significantly different for all
strokes (P=0.006) and early strokes (P=0.02) but
not for delayed strokes (P=0.2). The number of strokes that
occurred in patients in whom alterations in the surgical technique was
made for ascending aorta atherosclerosis is shown in
Table 3. Brain CT examinations were
performed in 93% of patients suffering a stroke. On the basis of
clinical interpretations of the results, the cause of early strokes was
believed to be embolic in 11 patients and due to cerebral hypoperfusion
in 5 patients. The cause of delayed strokes was believed to be embolic
in 18 patients and due to hypoperfusion in 11.
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Predictors of Stroke
The characteristics of patients who suffered strokes and
univariate predictors of these events are listed in Table 4. Further analysis demonstrated
that female patients were significantly older than male patients (70±8
years versus 67±9 years, P<0.05) and were more likely to
have diabetes, hypertension, and low cardiac output syndrome
(P<0.05). Atrial fibrillation after surgery was prevalent
in patients with and those without stroke. Because of the relationship
between atrial fibrillation and stroke in the general population and in
cardiac surgical patients, the data were examined to evaluate for
covariates that, when present with atrial fibrillation, increased
the risk of stroke.21 22 Because this
analysis suggested that postoperative atrial fibrillation is a
risk factor for delayed stroke only in the presence of low cardiac
output syndrome (Table 5), all
multivariate analyses of data on delayed stroke
included a variable that combined low cardiac output and
postoperative atrial fibrillation.
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Results from the multivariate logistic regression
analysis are listed in Table 6.
History of stroke was the strongest independent predictor of
perioperative stroke, regardless of whether strokes
were considered as a single end point or whether early and delayed
strokes were considered separately. Female sex was also independently
associated with stroke, regardless of the timing of the event, as was
ascending aorta atherosclerosis. Other independent risk
factors for stroke, however, were dependent on the timing of the
neurological event: duration of cardiopulmonary bypass was an
independent predictor of early stroke, whereas diabetes and the
combined variable of low cardiac output and atrial fibrillation
were additional independent predictors of delayed stroke. The presence
of significant carotid artery stenosis was an independent
predictor of early stroke only when prior stroke was excluded from the
multivariate analysis.
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Because women were found to have a higher risk of stroke, we evaluated the covariate-adjusted role of sex in greater detail. Multivariate logistic analysis was repeated by including variables that differed between the sexes (P value of <0.2) as well as stroke risk factors such as prior stroke, atrial fibrillation, ascending aortic atherosclerosis, carotid artery stenosis, and hypertension. After correction for these potentially confounding factors, female sex was still independently associated with a >3-fold increased risk of perioperative stroke.
Mortality
Seven and 4 deaths occurred in patients with early and delayed
strokes, respectively. This in-hospital mortality (early strokes, 41%;
delayed strokes, 13%) was higher than that observed in the control
group (3%, P=0.0001). The mortality rate for women (5.4%)
was higher (P=0.0008) than that for men (2.9%).
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Discussion |
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In this study, we sought to evaluate risk factors for perioperative stroke in a cohort of cardiac surgical patients in whom an aggressive strategy was implemented to identify atherosclerotic disease of the carotid arteries and the ascending aorta. We found that the majority of strokes occurred after an initial, uneventful neurological recovery from cardiac surgery. A new finding of this study was that women were at a higher risk for both early and delayed stroke. Also, postoperative atrial fibrillation was associated with increased risk of delayed stroke only when associated with low cardiac output syndrome, and diabetes was associated with increased risk of delayed but not early stroke. A history of previous stroke and ascending aorta atherosclerosis were independent predictors of either early or delayed stroke. Results of the present study confirm that perioperative stroke is associated with a significantly higher in-hospital mortality, regardless of when the event occurs.
The stroke rate observed (1.6%) is lower than that reported from other studies (3% to 5.6%).1 2 3 4 5 6 7 8 9 10 Despite this fact, the percentage of delayed strokes that occurred in the present study (nearly 66% of strokes) is similar to that previously reported, suggesting that the number of strokes that occur after initial recovery from surgery has not changed in more than a decade.2 3 5 An understanding of the mechanisms for early and delayed stroke and whether they differ has important implications for potential preventive strategies and thus requires further investigation. Moreover, these data suggest that future clinical trials should consider temporal onset of stroke to accurately judge the efficacy of strategies aimed at specifically preventing early and/or delayed strokes. The finding that ascending aorta atherosclerosis was an independent predictor of delayed strokes suggests that risk of stroke associated with this condition may result from mechanisms other than direct atheroembolism. In addition to being a potential cause of cerebral embolism, ascending aorta atherosclerosis may be a marker of widespread atherosclerosis of the aortic arch and cerebral vessels.8 16 17 18 19 23 24 25 26
Prior neurological event, carotid artery stenosis, diabetes mellitus, and advanced age have been found in many studies to increase susceptibility to perioperative stroke, possibly by identifying individuals with widespread cerebrovascular disease, impaired cerebral blood flow, and/or increased susceptibility to atheroembolism or thromboembolism.1 2 3 4 5 6 7 8 9 10 27 28 29 The relative importance of these risk factors for stroke in the present study in comparison with previous reports might result from the aggressive detection of atherosclerosis of the carotid arteries and ascending aorta. These findings support the notion that many of these previously identified risk factors for stroke may represent surrogate markers for risk factors not previously evaluated, such as atherosclerosis of the ascending aorta. The lack of an independent association between age and perioperative stroke in this study suggests that the relationship between these variables may be associated with age-related risk factors and not age per se.
The identification of female sex as an independent risk factor for stroke is new.1 2 3 4 5 6 7 8 9 10 In this study, women were more likely to have comorbid conditions and were more likely to have undergone valve surgery. However, after adjustment for potential confounding variables by use of multivariate analysis, female sex remained an independent predictor of stroke. It is possible that female sex has not been identified as a risk factor in previous studies because of the small number of women included in these studies or because of the failure to account for atherosclerosis of the ascending aorta and/or carotid arteries. It is also possible that the sex-related stroke risk that we observed represents an emerging phenomenon arising from the changing characteristics and general aging of cardiac surgical patients.
Atrial fibrillation is a frequent complication of cardiac surgery that
has been reported to increase the risk of perioperative
stroke in some, but not all, studies.1 2 3 4 5 6 7 8 9 10 22 The
contribution of postoperative atrial fibrillation to stroke risk may
have been underestimated in previous investigations because the timing
of the neurological event was not taken into consideration. Indeed,
because early strokes precede the onset of postoperative atrial
fibrillation, this arrhythmia cannot be a predictor of these
events. An equally important explanation may be the strong interaction
we observed between postoperative atrial fibrillation combined with low
cardiac output syndrome and delayed stroke, an interaction that has not
been reported previously (Table 5
). Because both complications
are associated with cardiac thrombus formation and cerebral
hypoperfusion, aggressive therapy may be beneficial for patients with
both conditions.
Limitations of the Study
We were unable to evaluate the efficacy of epiaortic ultrasound in
reducing perioperative stroke because patients were not
randomly assigned to undergo this procedure and thus there was no
control group. These same considerations also limit the utility of
comparisons of stroke rates in patients for whom no alterations, minor
alterations, or major alterations in aortic manipulations were made
(Table 3). Although the diagnosis of stroke was made by a
neurologist, a detailed preoperative neurological assessment was not
performed in our patients, and thus, paired neurological evaluations
were not available. More detailed neurological and neurocognitive
examinations might have revealed subtle neurological events, but it is
unlikely that strokes went undetected. Carotid artery ultrasound was
performed in 75% of all patients, most of whom represented
a "high-risk" group of those with the disease. It is possible that
the prevalence of carotid artery disease could have been
underestimated, but the 25% of patients who underwent carotid artery
ultrasound can be considered to be a "low-risk" group for
significant carotid artery disease on the basis of clinical
criteria.15 Because of the inherent exploratory nature of
stepwise regression analysis, we acknowledge that some
variables identified to be independently associated with stroke
risk (based on probability value close to 0.05) might not be predictors
in other studies. This limitation, however, would not apply to
predictive variables with a strong level of significance.
Conclusions
Most strokes after cardiac surgery occur after initial uneventful
neurological recovery from surgery. Previous stroke and ascending aorta
atherosclerosis were associated with increased risk for
perioperative stroke regardless of the timing of onset
of the event, but other risk factors appeared to be associated with the
time of occurrence. Women were found to be at higher risk for early and
delayed perioperative stroke and in-hospital mortality.
Atrial fibrillation was found to have no impact on postoperative stroke
rate unless accompanied by low cardiac output syndrome.
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Acknowledgments |
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We acknowledge Benico Barzilai, MD, and Nicholas T. Kouchoukos, MD, for their thoughtful review and advice regarding the manuscript.
Received December 22, 1998; revision received May 5, 1999; accepted May 19, 1999.
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R. Lee, N. Matsutani, A. C. Polimenakos, L. C. Levers, M. Lee, and R. G. Johnson Preoperative Noncontrast Chest Computed Tomography Identifies Potential Aortic Emboli Ann. Thorac. Surg., July 1, 2007; 84(1): 38 - 42. [Abstract] [Full Text] [PDF]
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 H. Tsukui, A. Abla, J. J. Teuteberg, D. M. McNamara, M. A. Mathier, L. M. Cadaret, and R. L. Kormos Cerebrovascular accidents in patients with a ventricular assist device J. Thorac. Cardiovasc. Surg., July 1, 2007; 134(1): 114 - 123. [Abstract] [Full Text] [PDF]
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 C. W. Hogue Jr, K. Freedland, T. Hershey, R. Fucetola, A. Nassief, B. Barzilai, B. Thomas, S. Birge, D. Dixon, K. B. Schechtman, et al. Neurocognitive Outcomes Are Not Improved by 17{beta}-Estradiol in Postmenopausal Women Undergoing Cardiac Surgery Stroke, July 1, 2007; 38(7): 2048 - 2054. [Abstract] [Full Text] [PDF]
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 E. Sisillo, M. R. Marino, G. Juliano, C. Beverini, L. Salvi, and F. Alamanni Comparison of on pump and off pump coronary surgery: risk factors for neurological outcome Eur. J. Cardiothorac. Surg., June 1, 2007; 31(6): 1076 - 1080. [Abstract] [Full Text] [PDF]
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K. Kotoh, K. Fukahara, T. Doi, S. Nagura, and T. Misaki Predictors of Early Postoperative Cerebral Infarction After Isolated Off-Pump Coronary Artery Bypass Grafting Ann. Thorac. Surg., May 1, 2007; 83(5): 1679 - 1683. [Abstract] [Full Text] [PDF]
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 R. G. Sheiman and B. J. d'Othee Screening Carotid Sonography Before Elective Coronary Artery Bypass Graft Surgery: Who Needs It Am. J. Roentgenol., May 1, 2007; 188(5): W475 - W479. [Abstract] [Full Text] [PDF]
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C. W. Hogue, O. A. Selnes, and G. McKhann Should All Patients Undergoing Cardiac Surgery Have Preoperative Psychometric Testing: A Brain Stress Test? Anesth. Analg., May 1, 2007; 104(5): 1012 - 1014. [Full Text] [PDF]
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T. Goto, T. Baba, A. Ito, K. Maekawa, and T. Koshiji Gender Differences in Stroke Risk Among the Elderly After Coronary Artery Surgery Anesth. Analg., May 1, 2007; 104(5): 1016 - 1022. [Abstract] [Full Text] [PDF]
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 M. Selim Perioperative Stroke N. Engl. J. Med., February 15, 2007; 356(7): 706 - 713. [Full Text] [PDF]
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C. W. Hogue and M. J. London Aprotinin Use During Cardiac Surgery: A New or Continuing Controversy? Anesth. Analg., November 1, 2006; 103(5): 1067 - 1070. [Full Text] [PDF]
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A. Sedrakyan, A. W. Wu, A. Parashar, E. B. Bass, and T. Treasure Off-Pump Surgery Is Associated With Reduced Occurrence of Stroke and Other Morbidity as Compared With Traditional Coronary Artery Bypass Grafting: A Meta-Analysis of Systematically Reviewed Trials * Supplemental Appendix I Stroke, November 1, 2006; 37(11): 2759 - 2769. [Full Text] [PDF]
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 I. Kronzon and P. A. Tunick Aortic Atherosclerotic Disease and Stroke Circulation, July 4, 2006; 114(1): 63 - 75. [Full Text] [PDF]
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C. W. Hogue Jr, C. A. Palin, R. Kailasam, J. S. Lawton, A. Nassief, V. G. Davila-Roman, B. Thomas, and R. Damiano C-reactive protein levels and atrial fibrillation after cardiac surgery in women. Ann. Thorac. Surg., July 1, 2006; 82(1): 97 - 102. [Abstract] [Full Text] [PDF]
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C. W. Hogue Jr, C. A. Palin, and J. E. Arrowsmith Cardiopulmonary bypass management and neurologic outcomes: an evidence-based appraisal of current practices. Anesth. Analg., July 1, 2006; 103(1): 21 - 37. [Abstract] [Full Text] [PDF]
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Y. Kadoi, K.-i. Takahashi, S. Saito, and F. Goto The comparative effects of sevoflurane versus isoflurane on cerebrovascular carbon dioxide reactivity in patients with diabetes mellitus. Anesth. Analg., July 1, 2006; 103(1): 168 - 172. [Abstract] [Full Text] [PDF]
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L. B. Goldstein, R. Adams, M. J. Alberts, L. J. Appel, L. M. Brass, C. D. Bushnell, A. Culebras, T. J. DeGraba, P. B. Gorelick, J. R. Guyton, et al. Primary Prevention of Ischemic Stroke: A Guideline From the American Heart Association/American Stroke Association Stroke Council: Cosponsored by the Atherosclerotic Peripheral Vascular Disease Interdisciplinary Working Group; Cardiovascular Nursing Council; Clinical Cardiology Council; Nutrition, Physical Activity, and Metabolism Council; and the Quality of Care and Outcomes Research Interdisciplinary Working Group: The American Academy of Neurology affirms the value of this guideline. Circulation, June 20, 2006; 113(24): e873 - e923. [Abstract] [Full Text] [PDF]
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 G. N. Djaiani Aortic arch atheroma: stroke reduction in cardiac surgical patients. Seminars in Cardiothoracic and Vascular Anesthesia, June 1, 2006; 10(2): 143 - 157. [Abstract] [PDF]
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