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(Stroke. 1997;28:1988-1992.)
© 1997 American Heart Association, Inc.

Articles

Cerebral Microembolic Signals During Cardiopulmonary Bypass Surgery

Frequency, Time of Occurrence, and Association With Patient and Surgical Characteristics

Sigrun K. Brækken, MD; David Russell, MD, PhD, FRCPE; Rainer Brucher, PhD; Michel Abdelnoor, MPH, PhD; Jan L. Svennevig, MD, PhD

From the Departments of Neurology (S.K.B., D.R., R.B.) and Surgery (M.A., J.L.S.), Rikshospitalet, The National Hospital, University of Oslo (Norway).

Correspondence to S.K. Brækken, MD, Department of Neurology, Ullevål Hospital, University of Oslo, N-0407 Oslo, Norway.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose We sought to determine the number of cerebral microembolic signals (MES) and their time of occurrence during the two most frequent types of cardiopulmonary bypass (CPB) surgery: coronary artery bypass grafting (CABG) and cardiac valve replacement (VR). Furthermore, we sought to examine the association between MES, patient characteristics, and intraoperative parameters.

Methods Forty-two patients were studied, 15 of whom had CABG and 27 VR. Cerebral MES were detected with the use of transcranial Doppler monitoring of the right middle cerebral artery.

Results Cerebral MES were detected in all patients. The number was significantly higher during VR (median, 1048) than during CABG (median, 82) (P<.001). In VR patients, 85% of the MES were detected when the heart regained effective ejection. During CABG, the highest number was detected when the aorta was cross-clamped (18%) and on release of the side clamp (13%). The numbers of MES during the period when the aorta was cross-clamped and in association with surgical procedures were not significantly different in the two patient groups. The total number of MES was inversely correlated to nasopharyngeal temperature (P<.01).

Conclusions A significantly higher number of cerebral MES were detected during VR than during CABG. The highest number occurred in VR patients when effective heart ejection was regained and in CABG patients when the aorta was cross-clamped and on release of the side clamp. The total number of MES increased at lower nasopharyngeal temperatures. Transcranial Doppler monitoring may alert the surgical team when emboli enter the cerebral circulation during CPB surgery, thus allowing preventive measures to be taken.

Key Words: cardiopulmonary bypass • embolism • ultrasonics

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Major advances in technique and equipment used during CPB surgery have led to a decrease in mortality and morbidity after open heart operations. Neuropsychological impairment has, however, been reported in up to 79% of patients.¹ Microemboli entering the cerebral circulation is one hypothesis that has been proposed to explain the decline in neuropsychological performance after open heart operations. Advances in Doppler technology have recently made it possible to test this hypothesis. Doppler ultrasound may now be used to detect not only gaseous microemboli^{2 3 4 5} but also microemboli composed of solid elements.^{2 3 4} The majority of previous studies have been performed during CABG and have shown a reduction in the number of ultrasound-detected MES with membrane oxygenators compared with bubble oxygenators.⁶ Furthermore, a lower number of MES were detected with a filter than with no filter^{7 8} and when the vent for removal of air was located in the apex of the heart instead of the proximal aorta.⁹

Two recent studies have reported a positive association between the number of intraoperative cerebral MES detected by transcranial Doppler and postoperative neuropsychological^{9 10} and neurological outcome.¹¹ This suggests that surgical techniques should be improved to reduce the number of cerebral microemboli entering the brain during open heart surgery.

The aim of this study was to determine the occurrence and frequency of cerebral MES during the two most frequent types of CPB surgery, CABG and VR, and to determine the association of MES with the various operative stages and procedures and with patient characteristics.

	Subjects and Methods

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Patient Selection
A total of 42 patients (35 men and 7 women) were included in the study after they gave informed consent. They were randomly selected among patients admitted to the Department of Surgery A for CABG or VR. Patients were excluded if they had the following: (1) unstable angina pectoris; (2) age >70 years; (3) a history or clinical findings suggesting cerebrovascular or other neurological disease; (4) >50% stenosis or occlusion of a precerebral carotid, vertebral, or major intracranial artery assessed by Doppler examination; or (5) metabolic or immunologic disease. They were divided into two groups: the VR group and the CABG group.

VR Group
Twenty-seven patients (21 men and 6 women; age range, 34 to 69 years [median, 56 years]) had VR with mechanical bileaflet valves (Carbomedics): aortic VR (n=21), mitral VR (n=3), and double VR (n=3). Additional plastic surgery of the tricuspid valve was performed in one patient.

CABG Group
Fifteen patients (1 woman and 14 men; age range, 39 to 70 years [median, 57 years]) underwent CABG. Three patients had two-vessel disease, and 12 had three-vessel disease.

Anesthesia
After induction with diazepam, fentanyl, and pancuronium, anesthesia was maintained with nitrous oxide (40% inspired) and isoflurane (0.5% to 1.0% inspired). Nitrous oxide was stopped 10 minutes before bypass. Midazolam and fentanyl were used during CPB.

CPB
The alphastat strategy was used during the period on bypass in all patients. Preconnected, standardized tubings of fixed length and size, including a 25-µm heparin-coated (Duraflo II; Baxter Bently) arterial line filter, were used. Membrane oxygenators and nonpulsative Gambro roller pumps were used. The perfusion rate varied from 2.4 L/min per square meter of body surface area at 37°C to 1.5 L/min per square meter of body surface area in moderate hypothermia (32°C). Nasopharyngeal temperature, blood pressure, and heart rate were monitored continuously. All blood from the extracorporeal circuit was retransfused after termination of the CPB. In CABG patients the proximal anastomoses were performed after release of the aortic cross-clamp, with the use of a side clamp.

Transcranial Doppler Monitoring
Continuous Doppler examination of the right middle cerebral artery was performed from 5 minutes before cannulation of the aorta until after decannulation, when closure of the sternum was initiated. The examination was performed with a TC 2000S system (Nicolet/EME) (386 computer) with 128-point color-coded fast Fourier transform; the sample volume was fixed at 10 mm, and the sweep was kept constant and corresponded with a time window overlap between 50% and 65%. A 2-MHz flat monitoring probe was used, and a stable position was maintained with the use of a Muller and Moll probe fixation device (Nicolet/EME) at a depth of 48 to 54 mm; the angle giving the strongest Doppler signal from the middle cerebral artery was used. All Doppler findings were recorded on a videotape (Panasonic AG 7355, Matsushita Electrical Industrial) for off-line analysis.

MES
MES were counted both by an observer and automatically by means of specially designed software (RB 11).¹² The observer assessed the signals according to their sound, duration, appearance on the monitor, and the presence or absence of obvious causes of artifact during the registration. When the automatic system and the observer disagreed, the observer's assessment was used for further analysis. We have previously found a 94% sensitivity between software and observer. During periods with a very high number of MES, observer counting was impossible and only the RB 11 software was used. This program identifies an MES as an enhanced power ratio (relative power increase above the mean of the background Doppler signal from 20 ms before the embolic event until 20 ms after) of 4 dB and a duration <300 ms. When obvious artifacts occurred during the recording, their time of occurrence and duration were noted with the use of the clock display on the tape recorder. When the tapes were replayed for analysis, the audio volume was reduced until the Doppler signal was color-coded in blue/green. The number of MES was presented as the total median number of MES per operation or the number of signals during a limited period of each operation (Table 1) with range. We analyzed separately the first 5 minutes after the heart had regained effective ejection or as long as MES occurred continuously after restoration of effective ejection. MES were defined as being related to a surgical procedure if they occurred within 1 minute of the following procedures: aortic cannulation/decannulation, CPB on/off, cross-clamp on/off insertion/removal of a vent and cardioplegia cannula, respirator on, and side-clamp removal (the clamp located at the aorta where the proximal anastomoses were performed during CABG).

View this table: [in this window] [in a new window]   Table 1. Number of Cerebral MES and Time of Their Occurrence

Statistical Analysis
All values are expressed as median and range. Since the distribution of the frequency of MES was skewed, the Mann-Whitney nonparametric test was used to compare groups of patients. The following variables were analyzed for an association with the total number of MES: age, New York Heart Association class, CPB time, minimum nasopharyngeal temperature, minimum hematocrit during CPB, and the patient's body surface area. An association between two continuous variables was estimated with Pearson's correlation coefficient.¹³ Its square value was used to estimate the attributable proportion of association between two continuous variables. Linear multivariate analysis was performed between total number of MES per operation as outcome and CPB time and lowest nasopharyngeal temperature with the linear regression model. Statistical analysis was performed with the Epi Info version 5.01A (Centers for Disease Control, Atlanta, Ga).

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Total Patient Population
Association Between Cerebral MES and Patient/Surgical Characteristics
Total number of MES. Cerebral MES were detected in all patients, with a median of 371 (range, 19 to 4541). There was no association between the number of MES per operation and patient age (P=.5) or preoperative New York Heart Association class (P=.9). There was a positive association between the median number of MES and the CPB time (r=.33, r²=.11, .03<R<.57) (P<.05) and an inverse association between number of MES and the minimum nasopharyngeal temperature (r=-.40, r²=.16, -.63<R<-.11) (P<.01) (Fig 1). Furthermore, there was an inverse association between CPB time and minimum nasopharyngeal temperature (r=-.37, r²=.14, -.61<R<-.8) (P<.01). When we performed an analysis using a multivariate model with these two variables and the total number of MES as outcome, the lowest nasopharyngeal temperature was significantly associated with the total number of MES (F=4.6555, P<.05). In this model, no significant association was found between total number of MES and CPB time (P=.2). There was no association between the total number of MES and the lowest hematocrit during CPB (P=.2) or the patient's body surface area (P=.1).

View larger version (15K): [in this window] [in a new window]   Figure 1. Regression line shows the correlation between the total number of MES on the vertical axis and minimum nasopharyngeal temperature on the horizontal axis in 42 patients during CPB surgery

Number of MES during cross-clamping. The number of MES that were detected during the period the aorta was cross-clamped (median, 11 [range, 0 to 405]) was not significantly associated with the cross-clamping time (P=.2). The number of MES was significantly higher during cooling (median, 8 [range, 0 to 304]) than during the period of rewarming (median, 1.5 [range, 0 to 41]) (P<.001). This difference was also significant when the number of MES per hour was calculated (median, 15 [range, 0 to 629] versus 6.5 [range, 0 to 189], respectively) (P=.01).

Group Comparisons
The VR patients had a significantly longer cross-clamping time and CPB time than the CABG patients. Other preoperative and intraoperative parameters between the two groups were not significantly different (Table 2).

View this table: [in this window] [in a new window]   Table 2. Preoperative and Intraoperative Parameters

Occurrence of Cerebral MES
A higher total number of MES (Table 1, Fig 2) and a higher frequency per hour (median, 607 [range, 78 to 2437] versus 46 [range, 22 to 157]) (P<.001) were detected in VR patients than in CABG patients. Within both patient groups, the total number of MES varied considerably (mean±SD: CABG, 189±213; VR, 1389±1264). The number of signals when the heart regained effective ejection was also higher in the VR group (Table 1). No difference in frequency between the two groups of patients was found in association with surgical procedures and the period the aorta was cross-clamped (Table 1). When the different stages of each operation were assessed separately, the highest number of MES during CABG was found in the period when the aorta was cross-clamped, followed by the period when the side clamp was removed (Table 1). During VR, 85% of the MES were found when the heart regained effective ejection (Table 1, Fig 3).

View larger version (30K): [in this window] [in a new window]   Figure 2. Distribution of the total number of intraoperative MES in relation to type of surgery performed (CABG, n=15; VR, n=27).

View larger version (80K): [in this window] [in a new window]   Figure 3. MES detected in the right middle cerebral artery in a patient examined with transcranial Doppler when the heart regained effective ejection. The MES (red) represented an intensity increase 15 dB greater than the background signal (blue), which is hidden by the MES. Blood flow velocities are shown on the vertical axis in centimeters per second; the time base on the horizontal was 3 seconds.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
In this study cerebral MES were detected in all patients during CPB surgery. This supports findings from the majority of previous transcranial Doppler^{9 14 15 16 17} and autopsy studies.¹⁸ The frequency differed, however, both between patients and depending on the type of surgery being performed.

The number of MES was much higher during VR than during CABG. This difference is most likely due to the entrance of a greater number of air bubbles into the cerebral circulation during VR. VR differs from CABG in that the former requires opening of the heart, which allows air to enter the cavities of the heart. All of this air may not be removed during venting,¹⁹ and some may subsequently be ejected into the arterial circulation when the heart restores effective ejection. The number of cerebral MES during VR may therefore be reduced by more effective removal of air from the heart.¹⁴

VR and CABG did not differ with regard to the absolute number of MES that occurred in relation to surgical procedures. MES were detected during aortic cannulation, the initiation of CPB, and the period the aorta was cross-clamped. Similar observations have been reported in the majority of previous reports.^{8 9 11 14 16 17} However, in two previous studies^{6 15} MES were not registered during total bypass when a filter was used. This is probably because these authors only considered Doppler intensity increases that caused overloading of the instrumentation as MES. Intensity increases within the Doppler spectrum were not counted as MES, as was the case in our study. During CABG we found a relatively high number of MES when the partial clamp was removed. However, the number associated with aortic cross-clamp release was lower than that reported by Barbut et al,¹⁶ who also found a correlation between the number of MES associated with clamp release and the degree of aortic atheroma. This difference may be due to less atherosclerosis in the aortas of our patient population. Another possibility is a methodological difference. We defined MES associated with a procedure if they occurred within 1 minute of the latter, whereas Barbut et al¹⁶ used a 4-minute interval.

The significant inverse correlation between the total number of MES and nasopharyngeal temperature and the high number of MES during cooling was unexpected. A reduction in the number of MES may be anticipated during hypothermia if they are caused by reflections from gas bubbles, since gases are more soluble in cold liquids.²⁰ Previous reports on the effect of temperature changes on bubble formation have provided conflicting results. In an experimental study with bubble oxygenators, only minor fluctuations in bubble activity were detected when the perfusate temperature varied from 20°C to 40°C.²¹ A study in dogs supported by bubble oxygenators, on the other hand, demonstrated an inverse relationship between bubble activity and perfusate temperature,²² similar to findings in our study. It is important to stress that although we found a significant association between the total number of MES and the minimal nasopharyngeal temperature, the variability of MES explained by these correlations was only 17%. It is also important to note certain methodological problems. The transcranial Doppler examinations were only performed in the right middle cerebral artery, and therefore no exact information regarding the number of MES entering the left hemisphere is known. Furthermore, during periods with frequent emboli, counting is very difficult and the number of MES is underestimated.

Several studies have demonstrated a correlation between the number of cerebral MES and the time of their occurrence during CPB surgery and postoperative neurological¹¹ and neuropsychological deficits.^{9 10} However, the clinical consequences of cerebral microemboli may be dependent not only on the number but also on the composition and size of emboli entering the microvasculature of the brain during CPB surgery. Presumably, both gaseous and solid emboli occur during CPB surgery. This problem may be solved in the near future since dual-frequency transcranial Doppler may now be used to differentiate between solid and gaseous microemboli.²³ In the meantime this method may be used to alert the surgical team when microemboli are entering the cerebral circulation so that preventive measures can be initiated.

	Selected Abbreviations and Acronyms

 

CABG = coronary artery bypass grafting CPB = cardiopulmonary bypass CPB time = the total period when patients were connected to the heart-lung machine cross-clamping time = the period when the aorta was cross-clamped and patients were supported by the heart-lung machine MES = microembolic signals VR = cardiac valve replacement

	Acknowledgments

 
This study was supported by The Norwegian Council on Cardiovascular Diseases.

Received December 3, 1996; revision received June 23, 1997; accepted June 23, 1997.

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