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Ann Thorac Surg 2009;87:1839-1844. doi:10.1016/j.athoracsur.2009.02.061
© 2009 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Temporal Pattern of Strokes After On-Pump and Off-Pump Coronary Artery Bypass Graft Surgery

Kei Nishiyama, MDa,*, Masahito Horiguchi, MD, PhDa, Satoshi Shizuta, MDa, Takahiro Doi, MDa, Natsuhiko Ehara, MD, PhDb, Ryoji Tanuguchi, MD, PhDc, Yoshizumi Haruna, MD, PhDd, Yoshihisa Nakagawa, MD, PhDe, Yutaka Furukawa, MD, PhDb, Masanori Fukushima, MD, PhDf, Toru Kita, MD, PhDb, Takeshi Kimura, MD, PhDa

a Department of Cardiovascular Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
b Kobe City Medical Center General Hospital, Kobe, Japan
c Hyogo Prefectural Amagasaki Hospital, Amagasaki, Japan
d Hirakata Kousai Hospital, Hirakata, Japan
e Tenri Hospital, Tenri, Japan
f Translational Research Center, Kyoto University Hospital, Kyoto University Graduate School of Medicine, Kyoto, Japan

Accepted for publication February 20, 2009.

* Address correspondence to Dr Nishiyama, Department of Cardiovascular Medicine, Kyoto University Graduate School of Medicine, 54 Kawahara-chou, Shogoin, Sakyo-ku, Kyoto, 606-8397, Japan (Email: keinishi{at}kuhp.kyoto-u.ac.jp).


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   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: The incidence of strokes has not decreased after coronary artery bypass graft surgery (CABG). The purpose of this study is to identify incidence, risk factors, and temporal pattern of strokes after on-pump and off-pump CABG.

Methods: We analyzed 2,516 consecutive patients who underwent first elective isolated CABG. The primary endpoint was strokes within 30 days. The temporal onset of the deficits was classified by consensus as either an "early stroke," which is present just after emergence from anesthesia, or a "delayed stroke," which is present after first awaking from surgery without a neurologic deficit.

Results: More than half of strokes (29 of 46; 63%) were delayed strokes. Patients undergoing off-pump CABG had significantly lower risk of early stroke (0.1% versus 1.1%, p = 0.0009), whereas the incidence of delayed strokes was not different significantly (0.9% versus 1.4%, p = 0.3484) between patients undergoing on-pump and off-pump CABG. In multivariate analyses, undergoing off-pump CABG was an independent protective factor for all strokes (relative risk 0.29, 95% confidence interval: 0.14 to 0.56, p = 0.0005) and early strokes (relative risk 0.05, 95% confidence interval: 0.003 to 0.24, p < 0.0001), but it was not an independent protective factor for delayed strokes (relative risk 0.54, 95% confidence interval: 0.24 to 1.17, p = 0.1210).

Conclusions: Undergoing off-pump CABG reduces the incidence of perioperative stroke mainly by minimizing early strokes; however, the risk of delayed strokes is not different between patients undergoing on-pump and off-pump CABG.

Despite advances in surgical techniques and improvements in perioperative care, the incidence of perioperative strokes after cardiac surgery has not decreased, and observation that reflects the aging of the population and an increase in the number of elderly patients with coexisting conditions who undergo cardiac surgery. Perioperative strokes result in prolonged hospital stay, increased disability rates, discharge to long-term care facilities, and death after surgery [1]. Many studies have previously compared off-pump coronary artery bypass graft surgery (CABG) with on-pump CABG surgery, and many of these studies have revealed that off-pump CABG has superior outcomes, particularly with regard to short-term mortality and complication rates, including strokes [2–15]. However, how off-pump CABG reduces the incidence of strokes is unclear.

Previous studies have demonstrated that perioperative strokes are predominantly ischemic and embolic, and the timing of embolic strokes after surgery shows a bimodal distribution. Approximately half of the perioperative strokes are identified within the first day after surgery [16, 17]; these events result from manipulations of the heart and aorta or from the release of particulate matter from the cardiopulmonary bypass pump [1, 16, 18]. The remaining half occur after uneventful recovery from anesthesia [16, 17]; these strokes are often attributed to postoperative atrial fibrillation, myocardial infarction, and coagulopathy [18]. Therefore, an investigation into the temporal pattern of strokes has important implications for risk stratification and modification of strokes after CABG.

The purpose of this study is to identify the incidence and risk factors of strokes, including strokes detected early and those detected at a later stage after CABG, and to examine the temporal pattern of strokes according to the type of surgical procedure.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
The Coronary Revascularization Demonstrating Outcome Study in Kyoto (CREDO-Kyoto) registry has collected in-hospital and long-term data (median follow-up period, 42.8 months) on the potential risk factors and outcomes in 2,516 consecutive patients who underwent their first isolated CABG at 21 institutions between 2000 and 2002 in Japan. Patients who had had an acute myocardial infarction within 1 week before the index procedure were excluded. The details of the CREDO-Kyoto registry design and main outcomes have been published [19]. The study protocol is concordant with the guidelines for epidemiologic studies issued by the Ministry of Health, Labor, and Welfare of Japan. The relevant review boards or ethics committees in all 21 participating centers approved the research protocol.

In each center, preoperative baseline characteristics and intraoperative data were collected from hospital charts or databases by independent clinical research coordinators according to prespecified definitions. Data in this registry include patient demographics (for example, age and sex), potential risk factors, comorbidities (for example, history of stroke, hypertension, and current smoking status), and intraoperative data (such as internal thoracic artery utilization) that have been demonstrated to be related to clinical outcomes.

To identify the incidence, risk factors, and temporal pattern of strokes, including strokes detected early after on-pump or off-pump CABG, we performed post hoc analysis. Patients were categorized into off-pump CABG and on-pump CABG groups according to the operation that they ultimately underwent. Patients undergoing surgery for cardiac valves or aortic disease simultaneously with CABG were excluded from this study. All procedural decisions and adjunctive pharmacotherapy were made at the discretion of the patient and the surgeon performing CABG, and either off-pump or on-pump CABG was performed at the discretion of the surgeons.

The primary endpoint was stroke occurrence within 30 days, and the temporal onset of the deficits was classified by consensus as follows: "early stroke," if new neurologic deficit was discovered when the patient emerged from anesthesia, and "delayed stroke," if the patient had a neurologic deficit after first awakening from surgery without a neurologic deficit.

Follow-up data after discharge were obtained from hospital charts or by contacting patients or referring physicians. An independent clinical events committee adjudicated events.

Definition of Stroke
Stroke was defined as any new permanent global or focal neurologic deficit that could not be attributed to other neurologic (for example, dementia) or medical (namely, metabolic abnormalities, hypoxia, or drugs) processes. Reversible cerebral ischemic events (transient ischemic attacks, which were defined clinically by the temporary nature of the associated neurologic symptoms that last less than 24 hours) were not included in the analysis because the occurrence of these events cannot be identified under general anesthesia, and their detection is hindered postoperatively by the residual effects of anesthetics, analgesics, and sedatives. In the majority of patients, strokes were diagnosed by neurologists and confirmed by computed tomography or magnetic resonance imaging head scans.

Diagnosis of Associated Conditions
Documentation of a prior stroke required verification by each patient's primary care physician, review of medical records, and review of the results of computed tomography and magnetic resonance imaging if available. Diabetes mellitus or hypertension was considered to be present if the patients were previously diagnosed, or if they were being treated with either insulin or oral antidiabetic drugs or antihypertensive drugs. Patients were considered to have a history of myocardial infarction if infarction had been previously diagnosed on electrocardiographs or coronary angiography. The criteria for the diagnosis of perioperative myocardial infarction were the appearance of new Q waves and an increase in creatine kinase to 2.0 times or more the upper limit of normal occurring 24 hours or less after CABG. Peripheral arterial disease was considered to be present when patients were being treated for carotid, aortic, or other peripheral vascular diseases or were scheduled for surgical or endovascular interventions. Left ventricular ejection fraction (LVEF) was measured either by contrast left ventriculography or echocardiography. Atrial fibrillation contained paroxysmal, persistent, and permanent atrial fibrillation.

Statistical Analysis
Statistical analysis of categorical variables was carried out using cross tables with the Pearson {chi}2 test. Survival curves were estimated using the Kaplan-Meier method. To determine the baseline risk factors for the incidence of all strokes, early strokes, and delayed strokes, we developed a Cox proportional hazard model for the following potential variables: off-pump CABG, emergency procedure, history of stroke, atrial fibrillation, aneurysm, peripheral arterial disease, hypertension, age, LVEF 40% or less, hyperlipidemia, serum creatinine greater than 2.0 mg/dL, history of myocardial infarction, current smoking status, diabetes mellitus, dialysis, female sex, internal thoracic artery utilization, and number of anastomoses. All statistical tests were two-tailed; a p value less than 0.05 was considered statistically significant, and a p value less than 0.1 was considered to indicate a statistical tendency. The variables for which p values were less than 0.1 in univariate analyses were included in multivariate analyses. All analyses were performed with JMP version 6.0.3 (SAS Institute, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Preoperative baseline characteristics and intraoperative variables of patients undergoing on-pump and off-pump CABG are shown in Table 1. As indicated, patients undergoing on-pump CABG appeared to have a higher prevalence of reduced left ventricular function (LVEF 40% or less) and internal thoracic artery utilization. Patients undergoing on-pump CABG had also tendency to have history of myocardial infarction more frequently. Conversely, patients undergoing off-pump CABG were older, had a history of stroke more frequently, had lower average number of anastomoses, and showed greater prevalence of hypertension, peripheral arterial disease, and hyperlipidemia. Patients undergoing off-pump CABG also had tendency to have chronic kidney disease (serum creatinine greater than 2.0 mg/dL) more frequently. The discharge medication regimens are shown in Table 2.


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  		Table 1 Preoperative Baseline Characteristics and Intraoperative Variables of Patients Undergoing On-Pump and Off-Pump Coronary Artery Bypass Graft Surgery
 

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  		Table 2 Discharge Medication Regimens of Patients Undergoing On-Pump and Off-Pump Coronary Artery Bypass Graft Surgery
 
All patients continued to attend follow-up examinations at 30 days. Within 30 days after CABG, 46 patients (1.8%) had a stroke. Univariate analyses indicated that undergoing off-pump CABG, history of stroke, and atrial fibrillation were significant predictors of stroke (Table 3).


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  		Table 3 Univariate Relationships of Clinical Variables With All Strokes
 
The number and temporal pattern of strokes based on the type of surgical procedure is shown in Figure 1 and Table 4. The incidence of stroke was sustained for 30 days after CABG. Eighteen strokes were detected early after surgery (37% of strokes, 0.7% of the 2,516 patients); 29 strokes were delayed (63% of strokes, 1.1% of patients). Among patients who underwent off-pump CABG (n = 1,117), 1 stroke occurred early after surgery (9% of strokes, 0.1% of patients); 10 strokes were delayed (91% of strokes, 0.9% of patients). Among patients who underwent on-pump CABG (n = 1,399), 16 strokes were detected early after surgery (46% of strokes, 1.1% of patients); 19 strokes were delayed (54% of strokes, 1.4% of patients; Table 4, Fig 1). Compared with patients undergoing off-pump CABG, patients undergoing on-pump CABG more frequently had early strokes. However, the incidence of delayed strokes did not differ between patients undergoing on-pump and off-pump CABG.


Figure 1
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  		Fig 1. Cumulative incidence of stroke after coronary artery bypass graft surgery (CABG). Postoperative day 0 refers to the day of surgery. (CPB = cardiopulmonary bypass.)

 

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  		Table 4 Number and Temporal Pattern of Strokes Based on Type of Surgical Procedure
 
Multivariate analyses (considering the baseline characteristics and results of univariate analyses) indicated that undergoing off-pump CABG was an independent protective factor for stroke, and history of stroke and atrial fibrillation were independent risk factors for stroke (Table 5). Furthermore, undergoing off-pump CABG was an independent protective factor for early stroke, and history of stroke and age was an independent risk factor of early stroke. History of stroke and atrial fibrillation were independent risk factors for delayed stroke (Table 5).


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  		Table 5 Multivariate Relationships of Clinical Variables With All, Early, and Delayed Strokes
 
Within 30 days after CABG, 3 and 8 deaths occurred among patients with early and delayed strokes, respectively. This 30-day mortality rate (early strokes, 18%; delayed strokes, 28%) was higher than that observed among patients without perioperative stroke (1.9%, p < 0.0001). Perioperative Q-wave myocardial infarction incidence (on-pump 1.5% versus off-pump 1.2%, p = 0.4704) did not differ between patients undergoing on-pump and off-pump CABG.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The temporal pattern of strokes based on the type of surgical procedure was a novel finding of this study. More than half of the strokes (29 of 46; 63%) occurred after initial, uneventful neurologic recovery from cardiac surgery and were defined as delayed strokes. Patients undergoing off-pump CABG had significantly lower risk of early stroke compared with patients undergoing on-pump CABG. In contrast, the incidence of delayed stroke did not significantly differ between patients undergoing on-pump and off-pump CABG. Multivariate analyses in this study also demonstrated that undergoing off-pump CABG was an independent protective factor for all strokes and early strokes, but not for delayed strokes. From this study, we conclude that undergoing off-pump CABG may reduce the incidence of perioperative stroke mainly by minimizing early strokes; however, the risk of delayed strokes does not differ between patients undergoing on-pump and off-pump CABG.

Early strokes are mainly caused by manipulations of the heart and aorta or by the release of particulate matter from the cardiopulmonary bypass pump [1, 16, 18]. Some studies that used transcranial doppler ultrasonography demonstrated the production of aortic emboli on cannulation and application of aortic clamps [20–22] and the production of large quantities of aortic emboli during cardiopulmonary bypass without manipulation of the aorta [23]. Aortic manipulation was also reported to be an independent risk factor for postoperative stroke. Indeed, in this study, only 1 stroke (9% of strokes, 0.1% of patients) was detected early after surgery among patients who underwent off-pump CABG of this study (n = 1,117). Thus, it follows that among patients undergoing off-pump CABG, the incidence of early strokes could be reduced by avoiding cardiopulmonary bypass or by minimizing the manipulation of the aorta. Moreover, for reducing the incidence of stroke, it is important that the surgical technique is selected according to the patient's risk profile.

In this study, the risk of delayed stroke did not significantly differ between patients undergoing on-pump and off-pump CABG. Delayed stroke, which is often attributed to postoperative atrial fibrillation, myocardial infarction, and coagulopathy, remains a problem after both on-pump and off-pump CABG. Multivariate analyses of this study also indicated that atrial fibrillation was independent risk factors for delayed stroke. Atrial fibrillation, which was reported to occur in 30% to 50% of patients after cardiac surgery and to increase the risk of perioperative stroke in some studies [16, 18, 24–28], was found to be a significant predictor of delayed strokes after CABG in this study. No controlled trials have specifically addressed the use of anticoagulation therapy for new-onset postoperative atrial fibrillation; however, the American College of Chest Physicians recommends the consideration of heparin therapy for patients in whom atrial fibrillation develops after surgery, and the continuation of anticoagulation therapy for 30 days after the return of a normal sinus rhythm [29]. It was reported that the incidence of postoperative atrial fibrillation and stroke may be reduced by the prophylactic administration of amiodarone and beta-blockers before cardiac surgery [30]. Because, in this study, we do not have precise information about the in-hospital adjunctive pharmacotherapy that might affect the incidence of perioperative stroke, we excluded the information about the adjunctive pharmacotherapy from the analyses of perioperative strokes. Further studies are required to investigate whether these pharmacologic interventions reduce the incidence of delayed strokes.

Study Limitations
This study was not a randomized observational study. We had no precise information about the mechanism of the strokes, in-hospital adjunctive pharmacotherapy, and the incidence of atrial fibrillation after surgery. Previously, it was reported that delayed stroke also may be related to intimal injury to the ascending aorta due to clamping [31]; however, we also do not have precise intraoperative information (for example, use of intra-aortic balloon pump, intraoperative echocardiography of the ascending aorta, use of single or multiple applications of the aortic cross-clamp) that might affect the incidence of both early and delayed strokes. The study population was not very large, and hence, we could not properly examine the precise predictors of stroke and the protective effects of risk modification to prevent stroke and morbidity.

In conclusion, this is the first study of a large prospective cohort analyzing the temporal pattern of perioperative strokes based on the type of surgical procedure in patients undergoing CABG. We found that more than half of the perioperative strokes after CABG were delayed strokes that occurred after initial uneventful neurologic recovery from surgery. This study also demonstrated that undergoing off-pump CABG might reduce the incidence of perioperative stroke, mainly by minimizing early strokes, when neurologic deficit was detected after the patient's emergence from anesthesia; the risk of delayed strokes did not differ between patients undergoing on-pump and off-pump CABG. Delayed stroke, which is often attributed to postoperative atrial fibrillation, myocardial infarction, and coagulopathy, remains a problem after both on-pump and off-pump CABG.


   Appendix
 
List of Participating Centers and Investigators

Centers Investigators
Kyoto University Hospital Ryuzo Sakata
Kishiwada City Hospital Masahiko Onoe
Tenri Hospital Kazuo Yamanaka
Tenri Hospital Kazunobu Nishimura
Hyogo Prefectural Amagasaki Hospital Shinichi Nomoto
Kokura Memorial Hospital Hitoshi Okabayashi
Maizuru Kyosai Hospital Teruaki Ushijima
Nara Hospital, Kinki University School of Medicine Noboru Nishiwaki
Kobe City Medical Center General Hospital Yukikatsu Okada
Osaka Red Cross Hospital Kazuaki Minami
University of Fukui Hospital Kuniyoshi Tanaka
Shizuoka City Shizuoka Hospital Mitsuomi Shimamoto
Hamamatsu Rosai Hospital Masaaki Takahash
Shiga University of Medical Science Hospital Tohru Asai
Japanese Red Cross Society Wakayama Medical Center Masaki Aota
Shimabara Hospital Takafumi Tahata
Kagoshima University Medical and Dental Hospital Ryuzo Sakata
Shizuoka General Hospital Katsuhiko Matsuda
Kurashiki Central Hospital Tatsuhiko Komiya
Mitsubishi Kyoto Hospital Hiroyuki Nakajima
Kumamoto University Hospital Michio Kawasuji
Juntendo University Shizuoka Hospital Satoru Suwa


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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Related Article

Invited Commentary
Cullen D. Morris and Ulfur T. Gudjonsson
Ann. Thorac. Surg. 2009 87: 1845. [Extract] [Full Text] [PDF]



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C. D. Morris and U. T. Gudjonsson
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Ann. Thorac. Surg., June 1, 2009; 87(6): 1845 - 1845.
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