Impact of Early and Delayed Stroke on In-Hospital and Long-Term Mortality After Isolated Coronary Artery Bypass Grafting

Article Outline

• Abstract
• Methods
• Results
• Discussion
• References
• Copyright

Stroke after coronary artery bypass grafting (CABG) is an infrequent, yet devastating complication with increased morbidity and mortality. We sought to determine risk factors for early (intraoperatively to 24 hours) and delayed (>24 hours to discharge) stroke and to identify their impact on long-term mortality after CABG. We studied 4,140 consecutive patients who underwent isolated CABG from 1992 to 2003. Long-term survival data (mean follow-up 7.4 years) were obtained from the National Death Index. Independent predictors for stroke and in-hospital mortality were determined by multivariate logistic regression analysis including all available preoperative, intraoperative, and postoperative risk factors. Independent predictors for long-term mortality were determined by multivariate Cox regression analysis. One hundred two patients (2.5%) developed early stroke and 36 patients (0.9%) delayed stroke. Independent predictors for early stroke were age, recent myocardial infarction, smoking, femoral vascular disease, body mass index, reoperation for bleeding, postoperative sepsis and/or endocarditis, and respiratory failure, whereas those for delayed stroke were female gender, white race, preoperative renal failure, respiratory failure, and postoperative renal failure. Early stroke was an independent predictor for in-hospital (odds ratio 3.49, 95% confidence interval [CI] 1.56 to 7.80, p = 0.002) and long-term (hazard ratio 1.70, 95% CI 1.30 to 2.21, p <0.001) mortalities. Delayed stroke was not an independent predictor for in-hospital (odds ratio 0.90, 95% CI 0.23 to 3.51, p = 0.878) or long-term (hazard ratio 0.66, 95% CI 0.38 to 1.17, p = 0.156) mortality. In conclusion, risk factors for early in-hospital stroke differ from those of delayed in-hospital stroke after CABG. Early stroke is an independent predictor for in-hospital and long-term mortalities, suggesting the need for a more frequent follow-up and appropriate pharmacologic therapy after discharge.

Although independent predictors for stroke after coronary artery bypass grafting (CABG) have been extensively studied, few published data exist with respect to long-term survival and a few studies have taken into consideration the timing of stroke occurrence after CABG. The primary purpose of the present study was to determine the impact of early and delayed stroke on long-term mortality after CABG. We also reported early outcome of these types of stroke and identified their independent predictors.

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Methods 

Our study included 4,140 consecutive patients who underwent isolated CABG from January 1992 to December 2003 at St. Luke's–Roosevelt Hospital Center, a university hospital of Columbia University (New York, New York). Data were prospectively collected during admission as part of routine clinical practice and entered into the New York State adult cardiac surgery report for the variables listed in Table 1. The definitions of the used variables were derived from the New York State adult cardiac surgery report and we have mentioned some of them in our previous publications including postoperative complications.¹, ², ³ Stroke was defined as early stroke when a permanent new focal neurologic deficit occurred intraoperatively to 24 hours postoperatively, whereas delayed stroke was defined as the neurologic deficit occurred >24 hours postoperatively until discharge from the hospital. In the clinical setting patients who awoke with stroke were considered to have early stroke and patients who awoke and had normal neurologic recovery but developed stroke afterward were considered to have delayed stroke. Stroke diagnosis was made by the surgeon and/or neurologist. Neurologic consult was obtained to confirm diagnosis, and in most cases brain computer tomographic imaging was performed. Risk stratification was performed according to the European System for Cardiac Operative Risk Evaluation.⁴

Table 1. Patient characteristics after coronary artery bypass grafting without stroke, with early stroke, and with delayed stroke

Variable	CABG Without Stroke	CABG With Early Stroke	CABG With Delayed Stroke	pValue
	(n = 4,002)	(n = 102)	(n = 36)
Preoperative characteristics
EuroSCORE	6.18 ± 3.40	7.95 ± 3.52	7.31 ± 4.03	<0.001
Age (yrs)	64.1 ± 10.4	69.4 ± 10.0	68.3 ± 10.1	<0.001
Women	1,239(31.0)	39(38.2%)	19(52.8)	0.006
White race	2,639(66.0%)	64(62.7%)	10(27.8%)	<0.001
Black race	710(17.7%)	25(24.5%)	17(47.2%)	<0.001
Other race	653(16.3%)	13(12.7%)	9(25.0%)	0.230
No. of coronary arteries occluded >50%
1	283(7.1%)	4(3.9%)	2(5.6%)	0.442
2	860(21.5%)	21(20.6%)	5(13.9%)	0.531
3	2,859(71.4%)	77(75.5%)	29(80.6%)	0.328
Unstable angina	2,608(65.2%)	71(69.6%)	22(61.1%)	0.569
Previous myocardial infarction (most recent)	1,876(46.9%)	61(59.8%)	12(33.3%)	0.009
Transmural myocardial infarction	1,294(32.3%)	34(33.3%)	7(19.4%)	0.250
More previous myocardial infarctions	673(16.8%)	12(11.8%)	4(11.1%)	0.268
Previous cardiac operation	273(6.8%)	6(5.9%)	1(2.8%)	0.590
Canadian Cardiovascular Society angina class	3.55 ± 0.69	3.64 ± 0.61	3.47 ± 0.81	0.498
Urgency operation
Emergency	321(8.0%)	4(3.9%)	7(19.4%)	0.013
Urgent	2,461(61.5%)	73(71.6%)	20(55.6%)	0.088
Elective	1,220(30.5%)	25(24.5%)	9(25.0%)	0.339
Hemodynamic instability	86(2.1%)	4(3.9%)	2(5.6%)	0.192
Shock	14(0.3%)	1(1.0%)	0	0.541
Ejection fraction categories
>50%	1,167(29.2%)	29(28.4%)	10(27.8%)	0.972
30–50%	2,242(56.0%)	47(46.1%)	19(52.8%)	0.128
<30%	593(14.8%)	26(25.5%)	7(19.4%)	0.009
Current heart failure	582(14.5%)	28(27.5%)	13(36.1%)	<0.001
Previous heart failure	412(10.3%)	16(15.7%)	4(11.1%)	0.211
Peripheral vascular disease
Previous stroke	261(6.5%)	9(8.8%)	2(5.6%)	0.631
Carotid disease	235(5.9%)	11(10.8%)	5(13.9%)	0.017
Aortoiliac disease	188(4.7%)	11(10.8%)	2(5.6%)	0.018
Femoral disease	369(9.2%)	21(20.6%)	4(11.1%)	0.001
Calcified aorta	320(8.0%)	15(14.7%)	3(8.3%)	0.050
Body surface area (m2)	1.90±0.22	1.82±0.23	1.84±0.20	<0.001
Body mass index (kg/m2)
<25	1,167(29.2%)	42(41.2%)	10(27.8%)	0.031
25–30	1,723(43.0%)	45(44.1%)	11(30.5%)	0.312
>30	1,112(27.8%)	15(14.7%)	15(41.7%)	0.002
Hypertension	2,824(70.6%)	83(81.4%)	29(80.6%)	0.026
Chronic obstructive pulmonary disease	535(13.4%)	18(17.6%)	5(13.9%)	0.457
Diabetes mellitus	1,372(34.3%)	40(39.2%)	20(55.6%)	0.017
Renal failure	93(2.3%)	6(5.9%)	5(13.9%)	<0.001
Preoperative dialysis	53(1.3%)	4(3.9%)	3(8.3%)	<0.001
Hepatic failure	6(0.1%)	0	1(2.8%)	0.001
Immune deficiency	44(1.1%)	0	0	0.465
Preoperative intra-aortic balloon pump	227(5.7%)	9(8.8%)	4(11.1%)	0.158
Intravenous nitroglycerin	645(16.1%)	23(22.5%)	6(16.7%)	0.221
Left ventricular hypertrophy	931(23.3%)	35(34.3%)	11(30.6%)	0.021
Malignant ventricular arrhythmia	99(2.5%)	4(3.9%)	2(5.6%)	0.336
Infective endocarditis	0	0	1(2.8%)	<0.001
Pulmonary hypertension	3(0.1%)	0	0	0.950
Previous thrombolysis surgery	200(5.0%)	3(2.9%)	1(2.8%)	0.534
Myocardial rupture	5(0.1%)	0	0	0.917
Stent thrombosis	17(0.4%)	1(1.0%)	0	0.648
Transfer to operating room after catheterization	51(1.3%)	2(2.0%)	1(2.8%)	0.614
Transfer to operating room after percutaneous coronary intervention	23(0.6%)	1(1.0%)	0	0.780
Previous percutaneous coronary intervention, this admission	86(2.1%)	2(2.0%)	1(2.8%)	0.958
Previous percutaneous coronary intervention, before this admission	485(12.1%)	7(6.9%)	3(8.3%)	0.216
Smoker in previous 2 wk	599(15.0%)	10(9.8%)	5(13.9%)	0.346
Smoker in previous year	571(14.3%)	28(27.5%)	5(13.9%)	0.001
Intraoperative characteristics
Total bypass time (min)	110 ± 52	124 ± 61	134 ± 44	0.001
Off-pump coronary artery bypass	295(7.4%)	3(2.9%)	7(19.4%)	0.005
Microscope use	1,706(42.6%)	36(35.3%)	19(52.8%)	0.154
≥2 arterial grafts	2,302(57.5%)	50(49.0%)	24(66.7%)	0.121
Anastomoses	3.4 ± 1.0	3.5 ± 1.0	3.5 ± 0.9	0.512
Postoperative characteristics
In-hospital mortality	98(2.4%)	18(17.6%)	6(16.7%)	<0.001
Postoperative complications
Postoperative myocardial infarction	21(0.5%)	2(2.0%)	0	0.141
Bleeding/reoperation	67(1.7%)	7(6.9%)	2(5.6%)	<0.001
Deep sternal wound infection	45(1.1%)	3(2.9%)	1(2.8%)	0.166
Gastrointestinal complications	53(1.3%)	1(1.0%)	3(8.3%)	0.001
Renal failure/dialysis	27(0.7%)	3(2.9%)	5(13.9%)	<0.001
Sepsis/endocarditis	25(0.6%)	9(8.8%)	4(11.1%)	<0.001
Respiratory failure	161(4.0%)	18(17.6%)	15(41.7%)	<0.001

Values are means ± SDs or numbers of patients (percentages).

EuroSCORE = European System for Cardiac Operative Risk Evaluation.

Long-term patient mortality data were obtained from the United States Social Security Death Index database.⁵ The sensitivity of the National Death Index to identify deaths is 92% to 99% depending on which identifiers are available.⁶ Social Security number alone has the best accuracy of any combination of other identifiers (first initial, last name, day of birth, month of birth, year of birth, etc.) with a sensitivity of 97% and a specificity of 99%.⁶ In this study we used only Social Security numbers, which were available in most patients (99.1%) and this allowed avoiding utilization of patients' names. In addition, patients without a Social Security number (n = 39) were censored at time of discharge from the hospital. The death index was queried in June 2006 and patients not found in the index were assumed to be alive at that date.

No informed consent was obtained, because the data used in this study had already been collected for clinical purposes. Furthermore, the present study did not interfere with the treatment of patients and the database was organized in a way that makes the identification of an individual patient impossible.

Numerical variables were presented as mean ± SD and compared with 1-way analysis of variance or the Kruskal-Wallis test where appropriate. Discrete variables were summarized by percentages and compared with chi-square test. Kaplan-Meier survival curves were compared with the log-rank test.⁷

The impact of early and delayed strokes on in-hospital mortality after CABG was determined using multivariate logistic regression analysis.⁸ All available preoperative, intraoperative, and postoperative variables were entered into the model. Variables were evaluated first using univariate and then multivariate analysis. Model selection was done with backward stepwise method starting from all variables with a p value <0.05 in univariate analyses. Early and delayed strokes were forced to remain in the multivariate model and odds ratios (ORs) and 95% confidence intervals (CIs) were calculated.

The propensity for early and delayed strokes after CABG was determined using multivariable logistic regression analysis as described earlier. The final models were used to calculate propensity scores. These propensity scores represented the probability that a patient would develop early or delayed stroke. The c-statistic (equivalent to the area under the receiver operating characteristic curve) and the Lemeshow-Hosmer goodness-of-fit statistic were calculated to assess the performance and calibration of the model, respectively. A c-statistic >0.70 indicates reasonable ability to discriminate between patients who developed stroke and those who did not.⁹ For the Lemeshow-Hosmer goodness-of-fit statistic, a p value >0.05 indicates acceptable calibration of the model.

The impact of early and delayed strokes on long-term mortality after CABG was determined using multivariate Cox regression analysis.¹⁰ In the entire database all available preoperative, intraoperative, and postoperative variables were entered into the model. Variables were evaluated first using univariate and then multivariate analysis. Model selection was done with backward stepwise method starting from all variables with a p value <0.05 in univariate analyses. The model was then confirmed using forward stepwise selection. Early and delayed strokes were forced to remain in the multivariate model and hazard ratios and 95% CIs were calculated. Risk-adjusted Kaplan-Meier survival curves for patients with CABG without stroke, with early stroke, and with delayed stroke were plotted. All analyses were performed with SPSS 15.0 (SPSS, Inc, Chicago, Illinois) and all p values are 2-tailed. Risk-adjusted hazard function curves for the 3 groups were plotted and constructed using STATA/SE 9.1 (STATA Corp., College Station, Texas).

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Results 

The mean age within the study sample (n = 4,140) was 64.3 ± 10.4 years and 31.3% (n = 1,297) were women. During the 30,441 person-years of follow-up (mean follow-up 7.4 ± 4.3 years), 1,353 (32.7%) deaths were recorded. One hundred two patients (2.5%) developed early stroke and 36 (0.9%) delayed stroke. A comparison of patients with CABG without stroke, with early stroke, and with delayed stroke is presented in Table 1.

Freedom from all-cause mortality in patients with CABG without stroke at 1 year and 7 years after surgery was 93.9 ± 0.4% and 75.4 ± 0.7% respectively, compared with 68.4 ± 4.8% and 45.8 ± 5.2% for patients with early stroke and 68.6 ± 7.8% and 53.4 ± 8.6% for patients with delayed stroke (p <0.0001, Figure 1).

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• Figure 1. 

  (A) Kaplan-Meier survival plots of patients with CABG without stroke (1), with early stroke (2), and with delayed stroke (3). (B) Risk-adjusted Kaplan-Meier survival plots of the same groups (adjusted for all variables listed in Table 5). HR = hazard ratio.

Independent predictors for in-hospital mortality are listed in Table 2. The discriminatory ability of the logistic model as measured by c-statistic was 0.90 (95% CI 0.87 to 0.94) and the Lemeshow-Hosmer goodness-of-fit test was not statistically significant (p = 0.148), indicating excellent discriminative power and good calibration of the model, respectively. Independent predictors for early stroke are listed in Table 3. The discriminatory ability of the logistic model as measured by c-statistic was 0.75 (95% CI 0.70 to 0.79) and the Lemeshow-Hosmer goodness-of-fit test was not statistically significant (p = 0.273), indicating very good discriminative power and good calibration of the model, respectively. Independent predictors for delayed stroke are listed in Table 4. The discriminatory ability of the logistic model as measured by c-statistic was 0.81 (95% CI 0.73 to 0.90) and the Lemeshow-Hosmer goodness-of-fit test was not statistically significant (p = 0.456), indicating excellent discriminative power and good calibration of the model, respectively.

Table 2. Independent predictors for in-hospital mortality after coronary artery bypass grafting

Variable	OR	95% CI	pValue
Age (continuous variable)	1.037	1.012–1.063	0.003
Emergency operation	3.03	1.66–5.52	<0.001
Shock	5.16	1.21–22.03	0.027
Previous heart failure	2.34	1.35–4.06	0.002
Malignant ventricular arrhythmia	4.04	1.73–9.44	0.001
Preoperative renal failure	5.07	2.33–11.03	<0.001
Total bypass time (continuous variable)	1.008	1.003–1.012	0.001
Early stroke	3.49	1.56–7.80	0.002
Postoperative myocardial infarction	11.13	2.96–41.83	<0.001
Sepsis and/or infective endocarditis	7.19	2.65–19.46	<0.001
Gastrointestinal complications	8.13	3.56–18.60	<0.001
Postoperative renal failure	2.97	1.00–8.81	0.050
Respiratory failure	8.22	4.84–13.98	<0.001

Table 3. Independent predictors for early stroke after coronary artery bypass grafting

Variable	OR	95% CI	pValue
Age (continuous variable)	1.049	1.027–1.072	<0.001
Myocardial infarction (most recent)	1.60	1.06–2.40	0.026
Smoker in previous year	2.59	1.63–4.13	<0.001
Femoral vascular disease	1.76	1.04–2.96	0.034
Body mass index >30 kg/m2	0.51	0.29–0.90	0.019
Bleeding requiring reoperation	2.74	1.15–6.55	0.023
Sepsis and/or infective endocarditis	5.93	2.35–14.95	<0.001
Respiratory failure	2.21	1.16–4.23	0.017

Table 4. Independent predictors for delayed stroke after coronary artery bypass grafting

Variable	OR	95% CI	pValue
Female gender	1.99	1.00–3.97	0.049
White race	0.28	0.13–0.59	0.001
Preoperative renal failure	3.12	1.08–9.05	0.036
Postoperative renal failure	4.72	1.48–15.08	0.009
Respiratory failure	9.75	4.71–20.18	<0.001

The crude hazard ratio of long-term mortality for patients with CABG who developed early stroke was 2.63 (95% CI 2.04 to 3.39, p <0.001) and for those who developed delayed stroke was 2.65 (95% CI 1.62 to 4.34, p <0.001). Independent predictors for long-term mortality are listed in Table 5. Risk-adjusted Kaplan-Meier survival curves of the 3 groups are displayed in Figure 1, which shows that only patients with early stroke had decreased survival compared with patients without stroke. Similarly, patients with CABG with early stroke showed an increased hazard estimate up to 8 years postoperatively compared with patients without stroke (Figure 2).

Table 5. Independent predictors for long-term mortality after coronary artery bypass grafting

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• Figure 2. 

  Risk-adjusted hazard estimates of patients with CABG without stroke (1), with early stroke (2), and with delayed stroke (3).

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Discussion 

In the present study, we separately analyzed early and delayed strokes after CABG. We showed that early stroke had a detrimental effect on patient long-term survival in a series of 4,140 patients with CABG from a single center with a mean follow-up of 7.4 years. After multivariate adjustment for all preoperative, intraoperative, and postoperative factors, early stroke was associated overall with a 1.7-fold increase in long-term mortality. In contrast, delayed stroke was not an independent predictor for long-term mortality. To the best of our knowledge, this is the first study addressing separately the effects of these types of stroke on long-term survival after CABG.

The finding that stroke affects long-term mortality after CABG is well in accordance with previous reports.¹¹, ¹², ¹³ However, in most published studies stroke after CABG has been considered a single end point, regardless of timing of the event. In the present study we detected 138 (3.3%) strokes of which 102 (74%) were early strokes and 36 (26%) were delayed strokes occurring after an initial uneventful neurologic recovery. Similarly, Salazar et al¹³ reported the same percentage of strokes on the day of surgery, whereas Lahtinen et al¹⁴ and Likosky et al¹⁵ demonstrated that most strokes presented on the first postoperative day.

The different types of stroke presumably reflect different risk factors and we have confirmed this in the present study. The only common risk factor for early and delayed strokes was association with postoperative respiratory failure. Patients requiring eventually prolonged mechanical ventilation may have demonstrated decreased cerebral perfusion and oxygenation.¹⁶ Age, recent myocardial infarction, smoking in the previous year, femoral vascular disease, body mass index >30 kg/m², bleeding requiring reoperation, and sepsis and/or endocarditis were unique independent predictors in patients with early stroke. Age and recent myocardial infarction represent 2 well-recognized risk factors for stroke after CABG.¹⁷, ¹⁸, ¹⁹, ²⁰ Other reports have also determined smoking as an independent predictor.²⁰ Surprisingly, carotid vascular disease, calcified aorta, and previous stroke were not independent predictors for stroke. In the present study, we considered the various manifestations of peripheral vascular disease as single risk factors. However, only femoral vascular disease was an independent predictor. Femoral vascular disease may be reflective of an overall increase of atherosclerotic burden in patients with CABG. We recommend examination of femoral vascular disease as a more sensitive index of atherosclerotic disease in patients with CABG. Patients with obesity (body mass index >30 kg/m²) showed decreased early stroke rates. Similarly, Pan et al²¹ reported 0.7% and 2.2% stroke rates in obese nondiabetic and diabetic patients undergoing primary CABG compared with 2.6% and 4.8% stroke rates in normal-weight patients, respectively. We have also demonstrated the association of early stroke with sepsis and/or endocarditis after CABG,²² which can be also supported by the fact that early stroke is an independent predictor for respiratory failure after CABG.²³ Moreover, the association of early stroke with bleeding requiring reoperation may be explained by hypotension and subsequent cerebral hypoperfusion, although this association has also been demonstrated by others correlating transfusion requirements with stroke after CABG.²⁴, ²⁵

Female gender, white race, preoperative renal failure, and postoperative renal failure were unique independent predictors in patients with delayed stroke. Female gender has been reported as an independent predictor for stroke.¹⁹, ²⁶ This difference between men and women might be related to body size.²⁷ Preoperative renal failure is a well-recognized risk factor for stroke after CABG.¹⁷, ¹⁸, ¹⁹, ²⁰, ²⁵ Postoperative renal failure requiring dialysis was another predictor of delayed stroke, possibly due to secondary renal artery arteriosclerosis.²⁴ Further, white race was a protective risk factor (OR 0.28, p = 0.001) for delayed stroke and this finding may be largely related to the higher prevalence of intracranial cerebral disease in black and Asian patients.²⁸

The surprising finding of a lack of association between delayed stroke and long-term mortality could be the result of the paucity (only 36 patients) of such patients, indicating an underpowered study for this subgroup. In contrast, patients with delayed stroke had higher percentages of black race, emergency operation, diabetes mellitus, preoperative renal failure, and preoperative renal failure on dialysis and were associated with higher percentages of gastrointestinal complications. All these factors represent strong independent predictors for long-term mortality after CABG (Table 5). Therefore, the impact of delayed stroke on long-term mortality may be also obfuscated by these strong predictors, which were more prevalent in patients with delayed stroke.

After successful CABG surgery and discharge at home the recommendation usually given to a patient is to visit the surgeon and cardiologist after 1 month and then the cardiologist every 6 months. Figure 2 in our study clearly shows that patients with early stroke after CABG have almost double mortality rates up to 1 year to 1.5 years postoperatively and at 7 years postoperatively. Therefore, we recommend that patients who developed stroke after CABG should have a more frequent follow-up (i.e. every 2 to 3 months) to ensure appropriate monitoring and pharmacologic therapy. There are studies that have shown that in patients with stroke the use of pharmacologic therapy including statins and β blockers and strict control of glucose in diabetics can significantly decrease long-term mortality after CABG.²⁹

Our study has several limitations. This is a retrospective study. Cause of death in these patients is not documented and is not necessarily stroke-related. We had no follow-up data on readmission for stroke, which is a valuable parameter and may affect long-term mortality. Preoperative neurologic assessment was not performed in our patients, and thus paired neurologic evaluations were not available. This study refers to a single-center database, and it is likely that selection of patients for CABG and race variation may be important determinants, which differ widely among cardiac surgery units.

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