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(Stroke. 2001;32:94.)
© 2001 American Heart Association, Inc.

Original Contributions

Intracranial Cerebral Artery Disease as a Risk Factor for Central Nervous System Complications of Coronary Artery Bypass Graft Surgery

Presented at the 24th American Heart Association International Conference on Stroke and Cerebral Circulation, Nashville, Tenn, February 4–6, 1999.

Byung-Woo Yoon, MD; Hee-Joon Bae, MD; Dong-Wha Kang, MD; Seung-Hoon Lee, MD; Keun-Sik Hong, MD; Ki-Bong Kim, MD; Byung Joo Park, MD, PhD Jae-Kyu Roh, MD

From the Departments of Neurology, Seoul National University (B.W.Y., D.W.K., S.H.L., K.S.H., J.K.R.) and Eulji General Hospital, Eulji University School of Medicine (H.J.B.); the Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital (K.B.K.); the Department of Preventive Medicine, Seoul National University College of Medicine (B.J.P.); and Neuroscience Research Institute, SNUMRC and Clinical Research Institute, SNUH (B.W.Y., J.K.R.).

Correspondence to Hee-Joon Bae, MD, Department of Neurology, Eulji General Hospital, 280-1, Hagye 1 Dong, Nowon Gu, Seoul, Korea 139-711. E-mail bhj1405{at}eulji.or.kr

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose—Although extracranial carotid artery disease (ECAD) is accepted as a risk factor for central nervous system (CNS) complications after coronary artery bypass graft (CABG) surgery, it remains to be clarified whether intracranial cerebral artery disease (ICAD) may also increase the risk. We conducted a prospective study to elucidate the relation between ICAD and CNS complications after CABG surgery.

Methods—We prospectively studied 201 patients undergoing nonemergency isolated CABG surgery during a 39-month period (from March 1995 to June 1998). Each patient was evaluated before surgery with neurological examination, transcranial Doppler, and carotid duplex ultrasonography. Magnetic resonance angiography was used to determine the presence and severity of ECAD and ICAD in patients with abnormal findings on clinical examination, carotid duplex ultrasonography, or transcranial Doppler. Patients were followed after surgery and evaluated for the development of CNS complications. Association between CNS complications and their potential predictors was analyzed.

Results—One hundred nine patients (54.2%) were found to have ECAD and/or ICAD. ECAD alone was found in 48 patients (23.9%), ICAD alone in 33 (16.4%), and both ECAD and ICAD in 28 (13.9%). Fifty-one patients (25.4%) had single or multiple CNS complications: 23 (11.4%) had delirium; 18 (9.0%) had hypoxic-metabolic encephalopathy; 7 (3.5%) had stroke; and 7 (3.5%) had seizure. In multivariate analysis, ICAD was found to have an independent association with the development of CNS complications (prevalence OR, 2.28; 95% CI, 1.04 to 5.01) after controlling for covariates including age, occurrence of intraoperative events, and reoperation. The joint effect of ECAD and ICAD was also statistically significant and stronger than ICAD alone (prevalence OR, 3.87; 95% CI, 1.80 to 6.52).

Conclusions—Our results suggest that ICAD may be an independent risk factor for CNS complications after CABG surgery. These results support pre-CABG evaluation of the intracranial arteries for the risk assessment of CABG surgery, at least in black and Asian patients, in whom there may be a higher prevalence of intracranial arterial stenosis.

Key Words: bypass surgery • cerebrovascular disorders • risk factors

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Coronary artery bypass graft (CABG) surgery is one of the most common operative procedures performed around the world, and central nervous system (CNS) complications account for a major source of adverse sequelae. The incidence of cerebral complications after CABG and their risk factors have been rigorously investigated.^{1 2 3 4 5} Extracranial carotid artery disease (ECAD) is well known to increase the operative risk of CNS complications, especially stroke,^{6 7 8 9 10} although there are still some controversies surrounding prophylactic carotid endarterectomy.^{11 12} The majority of studies, however, have been done in white or mixed populations. Although there have been a few reports on CABG in the Asian population, none have investigated CNS complications of CABG surgery in this patient group.^{13 14 15}

It is known that intracranial cerebral artery disease (ICAD) can lead to strokes. However, in contrast to a large number of reports on ECAD, no studies have, to date, systematically investigated the role of ICAD as a risk factor for CNS complications in patients undergoing CABG surgery. ICAD is known to be more common in blacks and Asians than in whites,^{16 17 18 19} and CABG is increasingly becoming a more frequent procedure in these populations. In this prospective study, the significance of ICAD as a predictor of CNS complications after CABG surgery in Asian patients was investigated.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
A consecutive series of 201 patients undergoing CABG surgery was enrolled in the study during a 39-month period (from March 1995 to June 1998). They all received elective CABG surgery performed by a single heart surgeon at Seoul National University Hospital, a 1500-bed, third-referral institute. Patients undergoing emergency CABG or CABG combined with other surgical procedures such as valve replacement or carotid endarterectomy were excluded from the study. Our study was approved by the institutional review committee, and informed consent was obtained from each patient.

All patients were evaluated with clinical history, neurological investigation, and cardiac investigation before surgery. The risk factors for atherosclerosis such as hypertension (previously diagnosed and treated or systolic pressure >140 mm Hg and/or diastolic pressure >90 mm Hg), diabetes (previously diagnosed and treated or fasting glucose >140 mg/dL), hyperlipidemia (previously diagnosed and treated, fasting serum cholesterol >240 mg/dL, or LDL cholesterol >160 mg/dL), and smoking (current smoker or ex-smoker who quit within 5 years) were noted. The neurological investigation consisted of an interview and neurological examination, carotid duplex ultrasonography (CD) (HDI 3000, HDI), and transcranial Doppler (TCD) (Trans-scan, EME). Absent temporal window on TCD was considered abnormal. If the patient had no history of stroke or transient ischemic attack (TIA) and no abnormal findings on neurological examination, CD, and TCD, it was determined that ECAD or ICAD was absent or negligible. Otherwise, magnetic resonance angiography (MRA) was obtained to confirm the presence and the degree of ECAD and ICAD. The degree of ECAD was classified as normal, <30%, 30% to 70%, or >70% stenosis or occlusion by North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria.²⁰ According to the involved sites, ICAD was defined as diseases of the intracranial internal carotid, middle cerebral, or basilar arteries. The most severe involvement among them was taken to represent the degree of ICAD, which was classified as normal, <50%, 50% stenosis, or occlusion based on the degree of narrowing of the luminal diameter.²¹ In the cardiac investigation, the severity of coronary artery disease was assessed according to the findings of coronary angiography by means of a method previously suggested (coronary artery disease score, CADS).²² Potential cardioembolic sources such as atrial fibrillation, intracardiac thrombus, and regional wall motion abnormality of the left ventricle were investigated on routine 12-lead ECG or on echocardiography.

Intraoperative and perioperative variables that may increase the risk of CNS complications were also evaluated. These include atherosclerotic aortic arch disease on palpation during operation; occurrence of intraoperative events such as coronary sinus rupture, intraoperative cardiac arrest, suture failure, and so on; hypotension index (HI), which was defined as the multiplication of the pressure difference between 50 mm Hg and mean arterial pressure and the length of time in minutes when mean arterial pressure is <50 mm Hg²³ ; difficulty in weaning of cardiopulmonary bypass; duration of cardiopulmonary bypass (DCPB); use of ventricular assist device; reoperation; and postoperative cardiac arrhythmia.

The patients were reevaluated 1 week after surgery, or earlier if necessary, and followed by the same neurologist who performed the initial neurological examinations. Development of any CNS complications and the final outcome at discharge were determined. CNS complications were categorized as stroke, delirium, hypoxic-metabolic encephalopathy, and seizure.² Stroke was defined as a new and sudden onset of focal neurological deficits lasting >24 hours with no apparent nonvascular causes. Delirium was defined clinically as an abnormal mental state characterized by disorientation, fear, irritability, misperception of sensory stimuli, and delusion that developed over hours to days and that fluctuated over the course of a day. Hypoxic-metabolic encephalopathy referred to either stupor or coma developing in the setting of documented hypotension, hypoxia, or multisystem metabolic dysfunction. Seizure was defined clinically according to the International Classification.²⁴ Outcome at discharge was assessed by modified Rankin scale²⁵ and categorized as good (grade 0 to 2) or poor (grade 3 or worse).

Univariate analysis was performed to assess the association between the development of CNS complications and the possible risk factors including age, sex, ECAD, ICAD, hypertension, diabetes, hyperlipidemia, smoking, CADS, atrial fibrillation, regional wall motion abnormality of the left ventricle, intracardiac thrombus, atherosclerotic aortic arch disease, occurrence of intraoperative events, HI, difficulty in weaning of cardiopulmonary bypass, use of ventricular assist device, DCPB, reoperation, and postoperative cardiac arrhythmia. Because CADS, DCPB, and HI were not normally distributed on the Kolmogorov-Smirnov test (P<0.001), they were categorized by percentile. Age was normally distributed but was dichotomized in univariate analysis by 50 percentile to meet the convenience of demonstration in tabular form. All the variables were analyzed by Pearson ² test, Fisher’s exact test, or Mantel-Haenszel ² test as appropriate. A logistic regression model was constructed for assessing the independent effect of ICAD on CNS complications after CABG. We included variables with probability values <0.1 in univariate analysis in the model as confounders. The results are presented as prevalence odd ratios (PORs) and their 95% confidence intervals. Data were analyzed with SPSS version 7.5.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Among the 201 patients, 154 were men and 47 were women (mean age, 50.5±8.0 years; range, 38 to 78 years). Hypertension was found in 98 patients (48.8%), diabetes in 58 (28.9%), and hyperlipidemia in 51 (25.4%). Current or ex-smokers numbered 126 patients (62.7%). A history of stroke or TIA was found in 27 patients (13.4%), preoperative neurological examination was abnormal in 9 (4.5%), and potential cardioembolic sources such as atrial fibrillation, intracardiac thrombus, and regional wall motion abnormality of the left ventricle were detected in 134 patients (66.7%).

MRA was carried out in 116 patients (57.7%) according to prespecified indications. We found ECAD or ICAD in 109 patients (54.2%). Forty-eight patients (23.9%) had ECAD alone, 33 (16.4%) ICAD alone, and 28 (13.9%) both ECAD and ICAD. Among the 76 patients with ECAD (37.8%), 6 (3.0%) had stenosis of >70%, whereas stenosis between 30% and 70% was found in 22 patients (10.9%).

In 61 patients with ICAD (30.3%), we found 79 intracranial vessels with steno-occlusion. The intracranial internal carotid artery was the most commonly involved site (37 vessels, 46.8%), followed by the middle cerebral artery (25 vessels, 31.6%) and basilar artery (17 vessels, 21.5%). Stenosis of 50% was found in 16 patients (8.0%).

Among the 201 patients, 51 (25.4%) had CNS complications. Stroke developed in 7 patients (3.5%), delirium in 23 (11.4%), hypoxic-metabolic encephalopathy in 18 (9.0%), and seizure in 7 (3.5%). Four patients had multiple CNS complications. All strokes were cerebral infarction. Among the 7 patients who had stroke, 2 died and 1 was left with severe disability at the time of discharge. Among the 18 patients with hypoxic-metabolic encephalopathy, outcome at discharge was poor in 7 patients. On the contrary, all patients who had delirium recovered without significant sequelae.

Among the 7 patients with stroke, 4 had ICAD and 5 had ECAD (Table 1). The clinical correlation of stroke with known cerebral artery disease could be presumed in 3 patients, all with ICAD.

View this table: [in this window] [in a new window]   Table 1. Clinical Profiles of Patients With Stroke

We compared the rates of CNS complications according to the presence of ECAD or ICAD. In the patients with ECAD alone, complications occurred in 16 among 48 patients (33.3%); in those with ICAD alone, complications occurred in 13 among 33 (39.4%); and in those with both ECAD and ICAD, complications occurred in 9 among 28 (32.1%); whereas in those with neither ECAD nor ICAD, CNS complications occurred in 13 among 92 (14.1%).

In univariate analysis, age, ECAD, ICAD, occurrence of intraoperative events, DCPB, use of ventricular assist device, and reoperation appeared to increase the risk of CNS complications (P<0.1) (Tables 2 and 3).

View this table: [in this window] [in a new window]   Table 2. Preoperative Factors and Frequency of CNS Complications After CABG Surgery1

View this table: [in this window] [in a new window]   Table 3. Perioperative Factors and Frequency of CNS Complications After CABG Surgery1

Multiple logistic regression analysis showed that ICAD may independently increase the risk for the development of CNS complications after CABG (POR, 2.28; 95% CI, 1.04 to 5.01) after controlling for the effect of confounders including age, occurrence of intraoperative events, and reoperation (Table 4). We also assessed the joint effect of ICAD and ECAD on CNS complications after CABG, which was found to be more profound than the effect of ICAD alone (POR, 3.87; 95% CI, 1.80 to 6.52).

View this table: [in this window] [in a new window]   Table 4. Multiple Logistic Regression Analysis for Predictive Factors of CNS Complications

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Our results demonstrate that ICAD can increase the risk for development of CNS complications in patients undergoing CABG. To the best of our knowledge, this is the first study to reveal ICAD as an independent predictor of CNS complications of CABG. ECAD is associated with coronary heart disease^{26 27} and regarded, at least when severe, as a predictor of stroke or CNS complications in CABG.^{6 7 8 9 10} On the contrary, the correlation between ICAD and coronary heart disease has been suggested by only a few earlier autopsy-based studies.^{28 29} Virtually no attention, however, has been paid to the significance of ICAD in CABG surgery. We found ICAD in 30.3% of our patients undergoing CABG and demonstrated that it may be an independent predictor of CNS complications, increasing the risk >2-fold. Moreover, the risk would be increased further in patients with both ECAD and ICAD.

Of the 30.3% of patients who had ICAD, 8% showed stenosis of 50%. We could not find any data in the literature on the prevalence and severity of ICAD in patients undergoing CABG, but Uehara and colleagues²¹ found ICAD in 16.4% of Japanese patients with ischemic heart disease, being severe in 4.5% of the patients. The higher prevalence and severity of ICAD in our study compared with the Japanese study may be explained by the fact that we studied patients undergoing CABG, who may have had more severe ischemic heart disease and therefore more advanced diseases of the cervicocranial arteries. Because ICAD is known to be more common in blacks and Asians than in whites,^{16 17 18 19} it is noteworthy that ICAD was not uncommon in the Japanese and in our study, both performed in Asian patient groups, although it was less common than ECAD.

Although ECAD is well known to be an important risk factor, our study did not demonstrate a significant association between ECAD and CNS complications after CABG surgery. Previous studies showing ECAD as a risk factor, however, included much larger numbers of patients.^{6 7 8 9 10} Moreover, we had a lower rate of patients with severe carotid stenosis, who are more likely to have perioperative stroke in CABG surgery.¹³ Severe ECAD was found in 3.0%, which is lower than the rates previously reported in other studies (3.8% to 12%).^{7 8 30 31} Instead of ultrasonography, as was used in most of these studies, we used MRA to determine the degree of ECAD, which may overestimate rather than underestimate the stenosis.³² Therefore, the lower rate of severe ECAD in our patients cannot be explained by a difference in evaluation methods. Although racial difference might have contributed to the results, in one Japanese study, where MRA was used for pre-CABG evaluation of the carotid artery, severe stenosis was found in 9.7% of the patients.³³ The most likely explanation of why we failed to prove an association between ECAD and CNS complications is that because of the exclusion of patients with severe stenosis who had carotid endarterectomy combined with CABG surgery, our rate may have been an underestimation of the actual prevalence of severe ECAD in this patient population.

It was not practicable in our study to obtain MRA in every patient to detect and assess ECAD or ICAD. Therefore, MRA was not undertaken in patients with no history of stroke or TIA and normal findings on neurological examination, CD, and TCD. Although CD may underestimate the stenosis, it is considered an effective diagnostic procedure for ECAD screening,³² and TCD is a valuable tool, sensitive and specific in the evaluation of the intracranial arteries, despite limitations such as operator dependency and absent temporal windows in some patients.³⁴ Therefore, the combination of clinical findings, CD, and TCD was adequate, in our opinion, to screen for patients with ECAD or ICAD, who were then further investigated with MRA.

Stroke is an important complication, significantly affecting the outcome after CABG surgery.^{3 10} In our study, almost half of the patients with stroke had poor outcome. We could not assess whether ICAD might increase the risk for stroke because stroke occurred in only 7 patients. However, we could find 3 patients with stroke presumably relevant to ICAD. A multicenter, prospective study involving a much larger sample size will be necessary to investigate the relation between ICAD and stroke after CABG surgery.

Evaluation for ECAD is recommended before CABG surgery and carotid endarterectomy or angioplasty/stenting are considered if the stenosis is significant.³⁵ Direct intervention is usually impossible in patients with ICAD, although there are a few reports on angioplasty.^{36 37} However, identification of the presence of ICAD would provide valuable information regarding the operative risk to both surgeons and patients, and more attention to avoid hypotension or dehydration during and after operation would be necessary in patients with ICAD.

In conclusion, our results suggest that ICAD may independently increase the risk of CNS complications after CABG surgery. These findings may have significant clinical implications for the increasing number of black and Asian patients undergoing CABG in the United States³⁸ and Asian countries, respectively,^{39 40} as well as any CABG patients with known ICAD. Because preoperative carotid screening has been recommended^{8 9 10} and is generally accepted as the usual practice, the results of our study suggest that evaluation of the intracranial arteries with such diagnostic tools as TCD, and MRA, if applicable, may be warranted for the risk assessment of CABG surgery, at least in black or Asian patients, in whom ICAD may be more prevalent.

	Acknowledgments

 
This study was supported by Seoul National University Hospital Research Fund (02-1995-1680). The authors wish to thank Grace Wang for her excellent assistance in preparation of the manuscript.

Received June 19, 2000; revision received September 11, 2000; accepted September 14, 2000.

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