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Ann Thorac Surg 1998;66:1674-1678
© 1998 The Society of Thoracic Surgeons

Pattern and significance of cerebral microemboli during coronary artery bypass grafting

^a Department of Cardiology, Austin and Repatriation Medical Centre, Heidelberg, Australia
^b Department of Neurology, Austin and Repatriation Medical Centre, Heidelberg, Australia
^c Department of Cardiac Surgery, Austin and Repatriation Medical Centre, Heidelberg, Australia
^d Department of Radiology, Austin and Repatriation Medical Centre, Heidelberg, Australia
^e Department of Neuropsychology, Austin and Repatriation Medical Centre, Heidelberg, Victoria, Australia

Accepted for publication May 26, 1998.

Address reprint requests to Dr Sylivris, Austin and Repatriation Medical Center, Studley Road, Heidelberg 3084, Victoria, Australia

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Strokes that occur during coronary artery bypass grafting are often caused by embolism. Intraoperative transcranial Doppler monitoring can detect cerebral microemboli. The aims of this study were to identify the pattern of microembolic phenomena during various stages of coronary artery bypass grafting, to verify whether numbers of high-intensity transient signals correlated with early neuropsychologic deficits, and to identify, using magnetic resonance imaging scans, whether radiologic evidence of cerebral infarction correlated with microembolic numbers during the bypass period.

Methods. Forty-one consecutive patients undergoing coronary bypass grafting with transcranial Doppler monitoring were enrolled in this study. All had preoperative and postoperative magnetic resonance imaging brain scans. A subgroup of 32 patients were studied by comparing microembolic load and early neuropsychological outcomes.

Results. Transcranial Doppler monitoring confirmed that most microemboli occurred during cardiopulmonary bypass. A significant early neuropsychological deficit after coronary artery bypass grafting did correspond to the total microembolic load during bypass (p = 0.008). However, patients with cerebral infarction on magnetic resonance imaging had significantly more microembolic signal during the preincision phases and not during the bypass period.

Conclusions. Microembolic load during bypass is associated with early neuropsychologic deficits. In contrast, patients who show evidence of strokes during coronary artery bypass grafting have a higher microembolic load during the preincision phase than those without cerebral infarction. Differing mechanisms may be responsible for these different outcomes.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Strokes are a major cause of perioperative morbidity and mortality in coronary artery bypass patients [1, 2] and might manifest as a variety of clinical syndromes, including paresis, seizures, confusion, and memory loss. Approximately 70% of strokes associated with open heart operations occur intraoperatively [3], and the evidence that embolic infarction is one of the major causes is increasing [4]. Numerous studies have shown that ascending aortic atheroma is an independent and significant risk factor for stroke [5, 6], and it has been postulated that stroke is caused by embolized atheromatous debris.

As a result of recent developments in transcranial Doppler (TCD) monitoring not only can flow in the middle cerebral arteries by monitored but also microemboli can be detected. In small studies, microemboli, which appear as high-intensity transient signals in the Doppler spectrum, have been shown to occur during various stages of the coronary bypass operation [7, 8]. It has been suggested that neuropsychologic deficits might be related to the number of microembolic signals (MES) during coronary bypass [7, 9].

The most sensitive radiologic method for assessment of cerebral infarction appears to be magnetic resonance imaging (MRI) scanning. A recent study has shown that MRI scanning is more accurate than computed tomographic scanning [10]. It enables even very small ischemic lesions to be detected and consequently allows for detection of silent cerebral infarction. Its role in evaluating the impact of microemboli is increasing, and perioperative MRI scanning has been used to evaluate stroke complicating carotid endarterectomy [11]. There have also been studies with small numbers of patients which have used MRI scans perioperatively during cardiac valve replacement [12] and coronary artery bypass grafting (CABG) [13].

We hypothesized that MES during CABG are associated with MRI and neuropsychologic evidence of brain injury and that MES would occur during certain stages of the operation associated with a high risk of embolism. To test these hypotheses, we aimed first to identify the pattern of microembolic phenomena during various stages of CABG and to verify whether numbers of high-intensity transient signals correlated with early neuropsychologic deficits. Second, we aimed to identify, using MRI scans, whether radiologic evidence of cerebral infarction correlated with microembolic numbers during the bypass period.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Forty-one consecutive patients undergoing isolated CABG with TCD monitoring at the Austin and Repatriation Medical Centre were enrolled in this study. We also studied a subgroup of 32 patients to compare microembolic load and early neuropsychologic outcomes. Patients who had hypertension or who were over 70 years of age were specifically targeted. This group was targeted because of their increased risk of ascending aortic atheroma [14, 15], which could be a source of embolic material. Patients were excluded if they were to have reoperation for CABG or if they did not provide informed consent. Patients undergoing any valve repair or replacement were also excluded because of the increased risk of embolic material (eg, valvular calcification) which could confound the results. In all cases the surgical and anesthetic technique was performed independent of and blinded to the trial results. Coronary bypass was achieved by a Cobe-Stockert (Lakewood, CO) roller pump with either a Dideco D703 (Milandola, Italy) or monolyth oxygenator, polyvinylchloride tubing, and 40-µm filters on the arterial line of the coronary bypass circuit. Both anterograde and retrograde cardioplegia was used in all cases. A single cross-clamp technique was use in all cases. A mean arterial blood pressure of 70 mm Hg was maintained throughout the procedure, with alpha-stat acid-base management and hypothermia to a level of 32°C.

Neuropsychological testing
On the day before the operation patients underwent a battery of neuropsychological tests that assessed cognitive functions in three major areas known to be vulnerable to ischemic damage: memory, psychomotor speed, and mental flexibility. The battery included the following verbal and performance tests from part of the Wechsler Adult Intelligence Scale—Revised [16]. Verbal tests included 1) general information questionnaire, 2) digit span test (involves patients reciting from memory a series of numbers), 3) a rey auditory verbal learning test (involves patients reciting from memory a series of words), and 4) a Controlled Oral Word Association Test (involves patients devising as many legitimate words as possible within 60 seconds after being told a starting letter). The performance test involved a digit-symbol test (patients transcribed designated symbols to a series of random numbers). Scores on the general information, digit span, and digit-symbol tests were scaled according to the patient’s age.

After the operation, the neuropsychological tests were repeated on the day immediately before discharge from the hospital. This day varied between the fifth and sixth postoperative day in our patient population. For the comparison of preoperative and postoperative tests, a decline was defined as a test score that had decreased by one grade in the scale tests or one standard deviation in the nonscale tests. A neuropsychologic deficit was defined as a significant decline in two or more test scores. This conventional definition has been widely applied in the investigation of postoperative neuropsychologic changes [17].

Transcranial Doppler monitoring
All patients underwent middle cerebral artery TCD monitoring using an EME-Nicolet TC 2020 (Pioneer, Uberlinger, Germany). The middle cerebral arteries were insonated using two 2-MHz EME probes that were fixed to the transtemporal windows by a specifically devised head brace. Microemboli were defined as short-duration, high-intensity signals that were at least 3 dB higher than background noise and had an accompanying characteristic "chirp," "pop," or "click" [18]. Embolic phenomena were counted within 1 minute of each surgical manipulation. Doppler sonogram data were monitored and analyzed online, and the time-domain audio Doppler signal was also recorded on high performance audiotape for offline verification of MES (when signals were too numerous to count). Calculations regarding agreement between online and offline counts were performed. A previous study by Levi and associates [19] showed an excellent correlation (R = 0.99) between online and offline counts. Monitoring began 30 minutes before any aortic manipulation and continued throughout the operation. Times of various surgical manipulations (eg, cannulation, application of cross-clamp, bypass time, and cross-clamp removal) were carefully noted. Other variables, such as patient age and total time on cardiopulmonary bypass, were also noted.

Magnetic resonance imaging scanning
MRI scans (Magneton 1.5 Tesla, Siemens, Erlanger, Germany) of the brain (T₁- and T₂-weighted scans) were performed 1 day preoperatively and between day 5 and 6 weeks postoperatively. Radiologic slices from the preoperative and postoperative scans were matched to identify new lesions. Two radiologists assessed the scans. Each was blinded to both the others’ assessments and to the results of the TCD microembolic numbers, the neuropsychologic tests, and other clinical outcomes.

Statistics
Mann-Whitney statistics were used for comparison between groups (ie, between patients with and without MRI evidence of stroke and between patients with and without neuropsychologic deficits). A proportion of agreement was performed to assess agreement for online and offline MES counting. The proportion of agreement measures the probability that the offline counts will register the same result as the online counts.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The mean age of the 41 patients enrolled in this study was 69.8 ± 6.9 years. There were 31 mean and 10 women. The mean cholesterol level was 5.6 ± 1.4 mmol/L. There were 34 previous smokers and 7 nonsmokers. Concurrent conditions included diabetes mellitus in 29%, hypertension in 56%, and peripheral vascular disease in 27%. Of these 41 patients, 36 had adequate transtemporal windows to allow perioperative bilateral TCD monitoring. The largest MES load occurred during the period of cardiopulmonary bypass. However, when the microembolic rates per minute of the operation were analyzed, the period after cross-clamp release produced the highest counts (10.4 ± 12.8 MES/min). The signal counts for other portions of the operation were as follows: palpation, 0.4 ± 1.7 MES/min; preincision, 1.0 ± 2.9 MES/min; cannulation, 3.2 ± 4.7 MES/min; cross-clamp on, 5.2 ± 7.7 MES/min; and bypass, 8.8 ± 32.4 MES/min. The total MES count during monitoring was 0.5 ± 1.9 and during bypass was 1,038 ± 4,164. Online and offline agreement was assessed by reviewing over 30 minutes of audiotape (which included 61 MES during various phases of operative manipulations), and a proportion of agreement of 0.87 was achieved.

Microembolic signals and neuropsychologic deficits
The mean age of the 32 patients used to compare embolic loads during TCD monitoring and the preoperative and postoperative neuropsychologic testing was 71.0 ± 6.5 years. There were 24 men and 8 women. Of this group, 27 were suitable for analysis. The other 5 patients had poor TCD signals resulting from an inability to obtain an adequate transtemporal window.

Seventeen (63%) of the 27 patients had a significant neuropsychologic deficit after CABG. On univariate analysis, the time duration on cardiopulmonary bypass, total microembolic load during bypass, and microembolic rates (counts per minute) during bypass were all significantly higher in the group with neuropsychologic decline (Table 1). There was no significant difference in age of patients in whom a neurologic deficit did or did not develop.

Of the 28 patients, 5 had evidence of cerebral infarction on MRI scanning and 23 had no evidence of stroke. There was complete agreement between the two radiologists. Table 2 shows the comparison between the MES load during the different surgical phases and operative factors (such as total bypass time and patient age) between patients with and without MRI evidence of cerebral infarction. Patient age was not significantly different in patients with cerebral infarction. Unlike the previous association between MES (rates and total counts) during bypass and neuropsychologic deficits, there was no relationship between these factors and radiologic evidence of cerebral infarction. However, there was a significantly higher MES load before surgical incision of the ascending aorta in patients with cerebral infarction detected by MRI scanning (p < 0.0001). This same relationship was not present in patients who had neuropsychologic deficits postoperatively.

Carotid disease and anatomic lesions
Of the 5 patients who had strokes, 4 were enrolled to have preoperative and postoperative neuropsychologic tests. All 4 had a significant decline in neuropsychologic functioning.

All patients had auscultation over the carotid arteries preoperatively, and any carotid bruit detected was investigated with a carotid duplex scan, angiography, or both. All carotid stenoses were asymptomatic and did not require surgical intervention. However, 2 of 5 patients who had radiologic evidence of cerebral infarction had carotid disease. One had an 80% stenosis in the right internal carotid artery and a 10% to 20% stenosis in the left internal carotid artery and had evidence of a right cortical lesion. The other had a 99% right internal carotid stenosis and an 80% left internal carotid stenosis and had evidence of a cerebral infarct in the right frontal lobe. Of the other 3 patients who had a cerebral infarct, none had evidence of carotid disease (2 had no carotid bruits and the other had a normal carotid duplex scan). All 4 stroke patients were in sinus rhythm with no thrombus or spontaneous echocontrast seen on perioperative transesophageal imaging. The other strokes were located in the right and left corona radiata, the right parietal and left frontal lobes (2 patients), and the right frontal lobe (2 patients).

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Recent advances in surgical and anesthetic techniques have markedly reduced the operative risks of CABG. Cerebral complications, however, are still a major cause of morbidity and mortality and consequently also have a major economic impact. The hospital stay of patients who suffer a neurologic event is significantly prolonged [20] and the latter consequences of impaired neurologic function and cognitive behavior can significantly reduce the ability to return to a full and productive lifestyle.

Recent studies have identified cerebral embolism as a potential causative factor in the development of cerebral infarction [3, 4, 21]. In a study by Katz and associates [22], they found a strong correlation between protruding mobile plaques in the aorta, as detected by transeosophageal echocardiography, and strokes during CABG. It has therefore been hypothesized that atheromatous debris might be the source of the embolic strokes. Several studies [7, 8] analyzed microembolic phenomena during the various stages of coronary bypass operations to determine the embolic causes of strokes during these operations. The present study clearly showed that most emboli occurred during the bypass period. However, the actual rates of emboli detected per minute were highest during release of the aortic cross-clamp. A study of 20 patients by Barbut and colleagues [8] supports our finding that most emboli occur during cross-clamp release. They postulated that cross-clamp release might represent dislodgment of fragments of atheromatous plaque; however, in the absence of any current method to differentiate air from particulate matter this remains speculation.

The sensitivity of stroke detection varies by the technique applied. Recently, in a nonsurgical population, MRI scanning was shown to be more accurate than computed tomographic scans in stroke detection [10]; consequently we used this technique. Other researchers [12, 13] also used MRI perioperatively and concluded that MRI is a sensitive measure of subclinical cerebral ischemia after valve operations. We were able to detect five perioperative strokes in 28 patients scanned. The clinical stroke rates in prospective studies can vary widely depending on stroke definitions (permanent versus transient) and detection methods. Schmidt and associates [13] detected cerebral infarction in 14.3% of patients postoperatively, which agrees with the present cerebral infarction rate of 18%. Moreover, of these 5 patients, 4 were enrolled to have neuropsychologic testing, and all 4 had a significant decline in function. Despite this, an analysis of the overall group showed that MES during bypass (rates and total counts) were not significantly higher in the MRI stroke group compared with the nonstroke group. However, we did find that neuropsychologic decline correlates with microembolic numbers during this phase. This last finding is supported by Pugsley and associates [23] who showed that during CABG both microembolic rates and neuropsychologic decline were reduced by incorporation of 40-µm filters into the bypass machine.

There are many possible explanations for the different predictors of neuropsychologic versus MRI damage. If microembolic numbers during bypass are assumed to be pathologic, then it is conceivable that neuropsychologic testing is more sensitive than radiologic detection of strokes. Certainly there is a limit to image resolution of MRI scans; consequently, very small strokes might not be detected. Another explanation is that early neuropsychologic testing is not specific for strokes and that other factors, such as sleep deprivation and pain, can result in neuropsychologic decline. This last hypothesis, however, does not explain why neuropsychologic decline is related to microembolic numbers during bypass.

The other possibility is that many of the high-intensity transient signals detected might be microbubbles of air. Small quantities of air might not be as pathologic as particulate matter [24]; consequently, the total number of microemboli (gaseous plus particulate) might not correlate well with definite stroke. Microbubbles of air could enter the cerebral circulation via the bypass system. Levi and colleagues [25] showed that microbubbles of air as small as 25 nL can be detected by TCD in in vitro models. Consequently, despite the 40-µm filters on the bypass loop, small amounts of air might be contaminating the system.

Research is currently being undertaken to differentiate gaseous and particulate microemboli [25, 26]; however, definitive criteria that can be used clinically have yet to be described. We favor the theory that many of the high-intensity transient signals during the bypass period might be microbubbles of air, as it helps explain the association between strokes and preaortic incision embolic numbers. Emboli detected before incision should be particulate in composition as they occur before possible air contamination (in the aorta or cerebral arteries). In the present study, higher microembolic loads at this time were strongly associated with subsequent stroke and suggest that particulate microemboli are strongly pathogenic. The finding of higher numbers of microemboli during aortic cannulation might support this hypothesis, as dislodgment of aortic atheroma could be a logical explanation. The major focus now must be on developing accurate criteria for differentiating air and particulate microemboli and applying these criteria to confirm that microemboli at these stages are of formed elements.

One limitation of our study is that the TCD investigator was not blinded to the results of the neuropsychologic tests. Although many of the test scores were numerically derived and not subject to bias, ideally, independent investigators should have performed each of the tests blinded to each other’s results. Additionally, although results were statistically significant, not many patients had MRI evidence of stroke.

In summary, we have shown that although most microemboli occur during bypass, the highest rates actually occur with cross-clamp release. We also showed that both the total number and rate of microemboli during bypass were strongly associated with development of neuropsychologic deficits but not with radiologic evidence of strokes. Microemboli that occurred before aortic incision (and therefore were probably of particulate composition) were associated with MRI evidence of strokes. We suggest that studies developing accurate criteria for differentiating air and particulate microemboli are needed and that such studies might help further our understanding of the mechanism and prevention of perioperative strokes.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Doctor Stephen Sylivris holds a scholarship from the National Heart Foundation of Australia.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): George Matalanis