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Ann Thorac Surg 1997;63:1613-1617
© 1997 The Society of Thoracic Surgeons

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Original Article: Cardiovascular

Risk Factors and Solutions for the Development of Neurobehavioral Changes After Coronary Artery Bypass Grafting

Departments of Cardiothoracic Surgery, Anesthesiology, and Neurology, The Bowman Gray School of Medicine of Wake Forest University, Winston-Salem, North Carolina

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Background. As operative mortality for coronary artery bypass grafting has decreased, greater attention has focused on neurobehavioral complications of coronary artery bypass grafting and cardiopulmonary bypass.

Methods. To assess risk factors and to evaluate changes in surgical technique, between 1991 and 1994 we evaluated 395 patients undergoing coronary artery bypass grafting with an 11-part neurobehavioral battery administered preoperatively and at 1 and 6 weeks postoperatively. Patients were instrumented with 5-MHz focused continuous-wave carotid Doppler transducers intraoperatively to estimate cerebral microembolism as an instantaneous perturbation of the velocity signal. Microembolism data were quantitated and compared with surgical technical maneuvers during operation and with neurobehavioral deficit (20% decline from preoperative performance on two or more neurobehavioral tests) postoperatively. These data and patient demographics were statistically analyzed (², t test) and the results at 2 years (1991 and 1992; group A) were used to influence surgical technique in 1993 and 1994 (group B).

Results. Significantly associated with new neurobehavioral deficits were increasing patient age (p < 0.05), more than 100 emboli per case (p < 0.04), and palpable aortic plaque (p < 0.02). Group B patients had a significant decline in the neurobehavioral event rate (group A, 69%, 140/203; versus group B, 60%, 115/192; p < 0.05) of postoperative neurobehavioral deficits at 1 week and at 1 month (group A, 29%, 52/180; versus group B, 18%, 35/198; p < 0.01). The stroke rate was less than 2% in both groups (p = not significant). Modifications of surgical technique used in group B patients included increased use of single cross-clamp technique, increased venting of the left ventricle, and application of transesophageal and epiaortic ultrasound scanning to locate and avoid trauma to aortic atherosclerotic plaques.

Conclusions. Neurobehavioral changes after coronary artery bypass grafting are common and associated with cerebral microembolization. Surgical technical maneuvers designed to reduce emboli production may improve neurobehavioral outcome.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
See also page 1617.

Although risk factors and potential methods to reduce cerebral injury after cardiopulmonary bypass and coronary artery bypass grafting have been previously studied and reported, most of the literature to date is primarily descriptive [1–3]. Difficulties in interpreting previously published data primarily are attributable to the use of stroke rates to evaluate cerebral injury. It is now widely known that frank ischemic stroke is relatively uncommon (<6%) and appears to be the tip of the iceberg in terms of overall cerebral injury. Several studies have suggested alternative techniques in the management of patients on cardiopulmonary bypass but have not applied these in a large enough group of patients to achieve statistical significance. New sensitive methods to measure subtle changes in brain function postoperatively and to scan the ascending aorta to determine the incidence and location of aortic atheroma have recently been developed [4]. Discussions of alternative methods of dealing with ascending aortic atherosclerosis and myocardial protection techniques to avoid cerebral microembolism are now the focus of many surgeons and anesthesiologists around the world. With these factors in mind we report on an extensive 4-year evaluation of a large number of patients undergoing coronary artery bypass grafting with accurate assessments of intraoperative emboli, preoperative and postoperative neurobehavioral changes, and the results of surgical technical modifications designed to reduce cerebral injury.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
From January 1991 to December 1994, 395 patients undergoing isolated coronary artery bypass grafting using cardiopulmonary bypass were evaluated in our medical center. After giving informed consent and signing a permission form approved by the Institution Review Board the patients underwent a standard preoperative workup with the addition of several specialized studies. Each patient underwent a comprehensive neurologic history and physical examination, including a visual examination. A previous history of stroke, known asymptomatic bruits, previous endarterectomy, or other neurologic deficits were recorded and analyzed separately as a risk factor. Each patient underwent an 11-part neuropsychological examination, which was administered by a psychologist. The elements of this test and the results in large numbers of patients have previously been published [5–8]. This battery of tests is a sensitive measure of attention, concentration, memory, and language and includes higher cortical function (vocabulary-Wechsler Adult Intelligence Scale-Revised); memory (auditory verbal memory [Rey], nonverbal memory); attention, concentration, psychomotor (trailmaking A&B, grooved peg board, letter cancellation, digit symbol, finger tapping, visual reaction time). The tests have been carefully structured to avoid the confounding variables of IQ and amount of secondary education. Exclusion criteria were patients with neurodegenerative disease, major depressive disorder within the past 5 years, class IV congestive heart failure, cirrhosis, renal failure, or other serious life-threatening diseases. Patients undergoing emergency operation and those who could not for physical or mental status reasons perform the neurologic and neuropsychologic tests were excluded.

On the day of operation patients were premedicated with valium (2.5 to 5 mg orally) and morphine (0.1 mg/kg intramuscularly). A standard anesthetic technique of moderate-dose narcotic supplemented as necessary with volatile agents sufficient to maintain stable hemodynamics. Neuromuscular blockade was established with pancuronium (0.1 mg/kg intravenously) and all patients were intubated orotracheally and ventilated with 100% oxygen.

Before sterile preparation each patient was instrumented over the left carotid artery with a 5-MHz focused continuous wave Doppler transducer to estimate cerebral microembolism as an instantaneous pertubation of the velocity signal (Fig 1). Carotid ultrasound data were placed on magnetic tape and microembolism estimates for each patient were performed using an automated system previously described [6, 9].

View larger version (44K): [in this window] [in a new window]   Fig 1. . Ultrasonic perturbations detected by a 5-MHz continuous-wave Doppler device are associated with both gaseous and particulate emboli. In this view, a 5-second monitoring period was captured immediately after cross-clamp release and an embolic shower was detected in the left carotid artery.

Patients had standard postoperative care with the exception that all patients received a full neurologic and neuropsychological testing at 5 to 7 days postoperatively before discharge. All patients returned at 1 month for a standard postoperative visit when both examinations were repeated. Patients were classified as having a postoperative neurobehavioral deficit if one of the following criteria were recorded: (1) a new neurologic deficit, including (a) a new postoperative deficit on comprehensive examination at 5 days or 1 month, (b) an exacerbation (worsening) of a preoperative deficit, present at 5 days or 1 month, or (c) death before 1 month, if associated with a neurologic deficit; or (2) a new neuropsychologic deficit, defined as a 20% decline in two or more neuropsychologic tests at 1 week or 1 month.

At the end of 2 years in our testing period there was general information that increasing aortic atherosclerosis was associated with increased emboli detected in the carotid artery. For that reason, in the latter 2 years of our study increased scanning of the ascending aorta with ultrasound and increased use of specific techniques designed to reduce emboli were carried out. The primary techniques were more frequent avoidance of atherosclerotic areas on the aorta during aortic cannulation directed by epiaortic ultrasound scanning, the use of single aortic cross-clamp techniques, and avoidance of a partial occlusion clamp on the ascending aorta to reduce manipulation of the aorta and accompanying arteriosclerotic plaques. In addition, previous studies from our institution performed during the 1991 to 1992 time period had identified the use of a left ventricular vent with reduced carotid emboli. Therefore, left ventricular venting was used during the second time period [10].

For the purposes of comparison the 203 patients studied between 1991 and 1992 were identified as group A and 192 patients studied between 1993 and 1994 were identified as group B. All data were compiled and statistically analyzed. Differences in the number of emboli were compared using a paired t test using each patient as his or her own control. Comparison of emboli and the results of neurobehavioral testing were performed using ² contingency tables and standard statistical analysis.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Patient demographic data from the two time periods are presented in Table 1. There were no significant differences in demographics between the two groups. In addition, the stroke rates and hospital mortality were less than 2% in both groups and were not significantly different. On the basis of group data analysis we determined that new neurobehavioral deficits were significantly associated with increasing patient age (p < 0.05). The influence of patient age on new deficits is noted in Figure 2. Another variable associated with a significant number of new neurobehavioral deficits were the presence of more than 100 emboli per case (p < 0.04), the relationship between emboli and new deficits is illustrated in Table 2. The presence or absence of aortic atherosclerosis was an important determinant of carotid embolization. In 199 patients the surgeon graded the ascending aorta. The surgeon believed the aorta was abnormal (grades 2 and 3) in 44 patients and the median number of emboli recorded in those patients was 137, whereas in 155 patients with normal aortas, the median emboli count was 88 (p < 0.03). The median number of emboli decreased from a median 103 in group A to 90 in group B and were associated with improved documentation of aortic atherosclerosis (Fig 3) and modifications of surgical technique. Group B patients had a significant decline in the neurobehavioral event rate (group A 69%, 140 of 203 versus group B 60%, 115 of 192, p < 0.05) of postoperative neurobehavioral deficits at 1 week and at 1 month (group A, 29%, 52/180; versus group B, 18%, 35/198; p < 0.01). These data are presented in Figure 4. Group B patients had modifications of surgical technique including increased use of left ventricular venting (group A, 41%; group B, 68%) and increased use of single cross-clamp technique (group A, 5.3%; group, B 11.7%). Epiaortic and transesophageal ultrasound scanning was extensively used during the second time period but was not available in the first time period for coronary patients.

View larger version (27K): [in this window] [in a new window]   Fig 2. . The effect of increasing age on neuropsychologic outcome at 5 to 7 days and 1 month after coronary artery bypass grafting (CABG). Patients at age 50 years with deficits on two or more tests have a 67% chance of becoming normal at 1 month. By age 70 years that chance drops to less than 60%.

View larger version (67K): [in this window] [in a new window]   Fig 3. . Epiaortic and transesophageal echocardiographic scanning provides an additional level of protection to older patients who may face higher risks of brain injury owing to a greater likelihood of embolization secondary to aortic atheroma.

View larger version (25K): [in this window] [in a new window]   Fig 4. . The percentage of patients with neuropsychologic deficits in group B at both 5 to 7 days and 1 month. (CABG = coronary artery bypass grafting.)

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

There have been three important studies that have attempted to describe changes in operative technique with reduction of emboli and cerebral damage. A recent study from the Cleveland Clinic demonstrated a stroke rate of 0.7% of patients undergoing coronary artery bypass grafting in whom a partial occlusion clamp was avoided [15]. This was a significantly lower stroke rate in a larger group of retrospectively reviewed patients in which the conventional technique, using a partial occlusion clamp, was used. The investigators speculated that the reduced manipulation of and trauma to the ascending aorta, achieved by a single application of the cross-clamp may have contributed to a significant reduction in neurologic complications. In 1993, Wareing and colleagues [16] screened patients in their institution with ultrasound techniques and identified a small group of patients with severe ascending aortic atherosclerosis. In a nonrandomized subset of this group of patients, complete replacement of the ascending aorta was performed using circulatory arrest techniques. In this small group of patients no strokes occurred and this was compared with a larger group in which standard operative procedures were performed. In this larger group, a stroke rate of 1.1% was present, which suggested that the aortic resection technique may have value in preventing embolic stroke. Many surgeons have interpreted these results with caution, as a major procedure such as ascending aortic replacement performed during circulatory arrest may markedly increase the surgical risk, especially in elderly patients. In 1994, Aranki and co-workers [17] reported on a nonrandomized study in which two groups of patients undergoing coronary bypass operations were compared. In one group, conventional aortic manipulation techniques were used, including application of a partial occlusion clamp, and in the second group a single clamp technique was used. Using multivariant logistic regression analysis for adverse outcome, the group in which a partial occlusion clamp was used had more adverse events including stroke. However, when analyzing for stroke rate alone, there was no significant difference.

This study differs from those previously published efforts in that a more sensitive method was used to detect neurobehavioral changes before and after operation and emboli counts were measured in most patients. Although it seems unreasonable to implicate microemboli as the sole cause of neurobehavioral deficit postoperatively, other researchers have reached the conclusion that microemboli are the dominant factor causing postoperative change in neuropsychological function. Shaw and co-workers [18] identified cerebral microembolism as a cause of neurologic dysfunction in a group of patients undergoing cardiopulmonary bypass, which did not occur in a similar group of patients undergoing peripheral vascular operations. Slogoff and colleagues [19] cited neuroembolism as the major factor associated with neuropsychiatric change after cardiopulmonary bypass. Blauth and associates [20] have demonstrated microemboli in the retinal circulation during cardiopulmonary bypass and linked these to intellectual dysfunction. We were able to demonstrate that minor changes in documentation of aortic atherosclerosis coupled with decreased manipulation of the ascending aorta and increased use of left ventricular vent significantly decreased emboli and improved neurobehavioral outcome in a large group of patients.

Although epiaortic ultrasound is expensive and the routine use of this modality in all coronary bypass patients is questionable, it is certainly possible to screen patients for the use of this valuable adjunctive technique. Patients who are elderly, those who have a history of previous stroke or neurologic damage, especially occurring during invasive procedures such as cardiac catheterization, and those patients in whom a surgeon palpates significant aortic plaquing might well benefit from this useful technology as suggested by others [21].

The addition of a left ventricular vent improved outcome and the explanation for this change is not straightforward. It is probable that the primary cause of this change relates to the fact that aortic vents were used while the aortic cross-clamp was in place but were removed and the entry site used for a vein graft–aortic anastomosis. Left ventricular vents were left in place until after the hearts were allowed to eject and thus may have removed both air and particulate embolic material during this critical phase of the operation. Using this combination of techniques surgeons can be expected to significantly reduce new neurobehavioral changes in their patients postoperatively, which leads to a better overall outcome and could reasonably be expected to lower length of stay and overall costs associated with coronary artery bypass grafting.

In conclusion, neurobehavioral changes after coronary artery bypass grafting are common and associated with increasing age, increasing numbers of carotid microemboli, and aortic atherosclerosis. Straightforward changes in assessment of the ascending aorta and surgical techniques designed to reduce manipulation of the ascending aorta can significantly reduce the numbers of microemboli and associated neurobehavioral changes. These techniques are reasonably expected to improve the outcome in patients undergoing coronary artery bypass grafting.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Presented at the Forty-third Annual Meeting of the Southern Thoracic Surgical Association, Cancun, Mexico, Nov 7–9, 1996.

Address reprint requests to Dr Hammon, Department of Cardiothoracic Surgery, The Bowman Gray School of Medicine, Wake Forest University, Medical Center Blvd, Winston-Salem, NC 27157.

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 

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