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Ann Thorac Surg 1999;68:89-93
© 1999 The Society of Thoracic Surgeons

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Original Articles

Cerebral microemboli during cardiopulmonary bypass: increased emboli during perfusionist interventions

^a Division of Cardiovascular Surgery, The Toronto Hospital, Toronto, Ontario, Canada
^b Division of Cardiac Anesthesia, The Toronto Hospital, Toronto, Ontario, Canada

Address reprint requests to Dr Feindel, Division of Cardiovascular Surgery, The Toronto Hospital, Room EN 14-222, 200 Elizabeth St, Toronto, ON, M5G 2C4 Canada

	Abstract

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Background. Microemboli to the cerebral circulation occur during cardiopulmonary bypass (CPB) and can contribute to postoperative neurologic dysfunction. Cerebral microemboli are known to occur during specific surgical interventions, but the source of a large proportion of emboli remains unexplained. We investigated whether interventions by the perfusionist could account for the appearance of cerebral microemboli.

Methods. Transcranial Doppler ultrasonography was used to continuously monitor the middle cerebral artery of 18 patients undergoing coronary artery bypass grafting. The CPB circuit consisted of a softshell venous reservoir, a hollow-fiber membrane oxygenator, and a 32-µm arterial filter. The mean embolic rate was calculated for three time periods: (1) during surgical interventions (aortic cannulation and decannulation, cross-clamp application and removal, CPB start and end, and start of cardiac ejection); (2) during perfusionist interventions (blood sampling and drug administration into the venous reservoir); and (3) during baseline (all other time periods during CPB).

Results. Microemboli were detected in all patients (mean ± standard deviation, 207 ± 142 per patient, median, 132). The number of emboli per minute was significantly (p < 0.001) higher during perfusionist interventions (6.9 ± 4.5) than during surgical interventions (1.5 ± 1.5) or during baseline (0.4 ± 0.5). Drug administration resulted in a higher embolic rate than blood sampling.

Conclusions. Interventions by the perfusionist account for a large proportion of previously unexplained cerebral microemboli during CPB. These emboli likely represent air bubbles that are not eliminated by the arterial line filter. Although further studies of additional types of CPB circuits are required, we believe that air in the venous reservoir should be avoided whenever possible to minimize the risk of neurologic injury.

	Introduction

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Advances in surgical technique, anesthesia management, and cardiopulmonary bypass (CPB) have all contributed to reductions in morbidity and mortality during cardiac surgical procedures. However, the incidence of neurologic injury, in particular neuropsychologic impairment, remains high after CPB. Several studies have reported that 50% to 70% of patients exhibit cognitive deficits 1 week after coronary bypass operations [1, 2] and that approximately 30% of patients exhibit long-term neuropsychologic impairment [3]. Cerebral microemboli have been implicated in the etiology of neuropsychologic dysfunction with several investigators demonstrating worse cognitive outcomes for patients with greater numbers of emboli [4–7].

Microemboli are known to occur in association with specific surgical events such as aortic cannulation, initiation of CPB, and cross-clamp removal [8–11]. It has been demonstrated that once given appropriate feedback, surgeons are able to modify their technique to minimize microemboli occurrence [6]. However, up to 50% of cerebral emboli observed during CPB are not directly associated with surgical manipulations, and the source of these is currently unclear [8, 10, 12]. We hypothesized that the majority of unexplained microemboli occur as a result of perfusionist interventions and undertook this study to determine if acquisition of blood samples and injection of drugs into the venous reservoir by the perfusionist result in the production of cerebral microemboli.

	Material and methods

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From November 1997 to April 1998, a total of 18 patients (14 men and 4 women with a mean age of 64 ± 11 years) undergoing isolated coronary artery bypass grafting by a single surgeon (C.M.F.) were included in the study. Exclusion criteria included a history of carotid stenosis, atherosclerosis of the ascending aorta, reoperation, and concomitant surgical procedures. The protocol was approved by our institutional ethics review board, and participating patients gave signed informed consent.

Anesthesia and surgical management
Anesthesia management consisted of induction with midazolam hydrochloride, fentanyl, and sodium thiopental, followed by maintenance with isoflurane and propofol. A Swan-Ganz catheter was inserted through the right internal jugular vein in all patients. Myocardial protection consisted of antegrade cold blood cardioplegia. The left internal thoracic artery was grafted to the left anterior descending coronary artery in all patients, and supplemental saphenous vein grafts were added as necessary. All proximal anastomoses were performed under a single cross-clamp application.

Cardiopulmonary bypass
Cardiopulmonary bypass was established with arterial inflow through either the ascending aorta or the aortic arch and venous drainage through a single two-stage right atrial cannula. The aorta was assessed prior to cannulation by digital palpation in all patients; intraoperative epiaortic ultrasonography was not employed. Hematocrit was maintained between 20% and 25% during CPB, pump flow rates were kept between 2.0 and 2.5 L · min^-1 · m^-2, and mean arterial pressure was maintained between 50 and 70 mm Hg by use of phenylephrine hydrochloride or sodium nitroprusside as required. Systemic body temperature was allowed to drift to a minimum of 34°C, with active rewarming to 37.5°C at the end of CPB.

Our CPB circuit consisted of a collapsible softshell venous reservoir (Baxter BMR 1900; Uden, Holland), a hollow-fiber membrane oxygenator (Medtronic Maxima Plus; Mississauga, ON, Canada), and nonpulsatile roller pumps (Cobe; Arvada, CO). A 32-µm filter (Abecor Affinity, Minneapolis, MN) was used in the arterial perfusion line. Perfusionists administered drugs into the bypass circuit using a manifold directly connected to the bottom of the softshell venous reservoir immediately adjacent to where the venous line enters the reservoir.

Transcranial Doppler monitoring
Using transcranial Doppler (MultiDop X4; DWL Electronic Systems, Sipplingen, Germany), we continuously monitored the middle cerebral artery from 2 minutes before cannulation of the aorta to 2 minutes after aortic decannulation. The Doppler sound was turned off during monitoring so that the surgeon and perfusionist were blinded to the number and timing of microemboli. A 2 MHz pulsed-wave transducer (diameter, 1.7 cm) was used to simultaneously monitor two depths spaced 4.97 mm apart. The mean (± the standard error) insonation depths were 49.3 ± 1.3 mm and 54.3 ± 1.3 mm. A 64-point fast Fourier transform was used. In addition, a high-pass filter set at 100 Hz and a low-pass filter at 80 kHz were employed.

Detection and analysis of microemboli
Using automated software (TCD-8 for Multi-Dop X4, version 8.00q), we discriminated between emboli and artifact according to the bigate or coincidence method [13–16]. This approach requires simultaneous monitoring of two different depths of the middle cerebral artery. If a high-intensity transient signal appears at only one depth or in both depths simultaneously, it is considered to be artifact. Conversely, if a high-intensity signal appears sequentially in the two depths in a manner that is consistent with the flow velocity and the distance between the two sample volumes, then it is classified as an embolus. Previous evaluations of the Multi-Dop X4 system during cardiac surgical procedures concluded that although the specificity is adequate, the sensitivity for microemboli detection could be improved [16]. In this study, we increased sensitivity by manually detecting artifacts during off-line analysis. We also employed a detection threshold of 12 dB to improve reproducibility while maximizing sensitivity [13, 17–19]. The algorithms for measuring signal intensity were relative to the background, which was the entire screen.

We calculated the mean embolic rate for three time periods: during surgical interventions; during perfusionist interventions; and during baseline. Surgical interventions were defined as the 2-minute period after aortic cannulation and decannulation, cross-clamp application and removal, CPB start and end, and start of cardiac ejection. Several investigators [8, 9, 11, 12] have previously demonstrated that these interventions result in microemboli production. Perfusionist interventions were defined as the 2-minute period after acquisition of blood samples and administration of drugs into a manifold directly attached to the softshell venous reservoir. (Perfusionists frequently inject blood into the manifold before acquiring blood samples to clear the manifold of stagnant blood.) Baseline was defined as all other time periods during CPB. Each of the event types just described was time-stamped on the Multi-Dop X4 computer as it happened in the operating room, thereby allowing for increased accuracy and precision in embolic detection during off-line analysis.

Differences in embolic rate were evaluated using one-way analysis of variance with Scheffé’s multiple-range t test. Analysis of covariance was used to test for the effect of individual perfusionists as possible covariates. We employed the SAS system (SAS Institute; Cary, NC) for all analyses.

	Results

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Patient demographics are summarized in Table 1. The average number of bypass grafts placed was 3.6 ± 0.8 (± the standard deviation), the mean duration of CPB was 85 ± 16 minutes, and the mean cross-clamp time was 63 ± 8 minutes. The microemboli data were as follows: mean number, 207 ± 142; median number; 132, and range, 57 to 531. The highest mean embolic rate (± standard deviation) was associated with perfusionist interventions (6.9 ± 4.5), which was significantly (p < 0.001) different from surgical interventions (1.5 ± 1.5) and from baseline (0.4 ± 0.5) (Fig 1). This result was consistent across the 9 perfusionists who participated in the study. Figure 2 reveals that the largest proportion of microemboli during CPB occurred during perfusionist interventions.

View larger version (12K): [in this window] [in a new window]   Fig 1. Rate of microemboli detection during surgical interventions, perfusionist interventions, and baseline (see text for definitions). Perfusionist interventions resulted in a significantly higher rate of emboli production.

View larger version (14K): [in this window] [in a new window]   Fig 2. Proportion of total microemboli detected during each event. Drug injections and blood sampling (perfusionist interventions) resulted in a higher proportion of emboli than other events. (Aorta cann, Aorta decann = aortic cannulation and decannulation; CPB = cardiopulmonary bypass; Eject = start of cardiac ejection after cross-clamp removal; XCL = cross-clamp.)

View larger version (12K): [in this window] [in a new window]   Fig 3. Rate of microemboli detection during each surgical intervention. Initiation of cardiopulmonary bypass (CPB on) and start of cardiac ejection after cross-clamp removal (Eject) resulted in higher rates of emboli production than other surgical events. Other abbreviations are the same as in Figure 2.

View larger version (15K): [in this window] [in a new window]   Fig 4. Rate of microemboli detection during perfusionist interventions. Drug injection resulted in a higher rate of emboli production than blood sampling or any other period examined.

	Comment

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Neurologic injury is a major cause of morbidity and mortality during cardiac surgical procedures [20]. Neuropsychologic impairment, in particular, is a very common complication with approximately one third of patients exhibiting long-term cognitive deficits after CPB [3]. The principal cause of neuropsychologic impairment is thought to be diffuse microischemia secondary to cerebral microemboli [21]. The introduction of intraoperative transcranial Doppler has revealed that cerebral microemboli occur in virtually all patients undergoing CPB [22]. Patients with a high number of emboli have an increased incidence of major neurologic and cardiac morbidity [23]. Further, reduction in the number of microemboli is associated with a decreased incidence of cognitive impairment [4–7].

Several previous investigators [8–12] have demonstrated the occurrence of cerebral microemboli in association with specific "surgical" events, ie, aortic cannulation and decannulation, CPB start and end, cross-clamp application and removal, and start of cardiac ejection after cross-clamp removal. However, each of these studies has a large proportion of microemboli that cannot be explained by these interventions. We hypothesized that perfusionist events, ie, blood sampling and drug injections, result in the majority of these unexplained emboli. We could find no prior studies that assessed the association of microemboli with perfusionist interventions.

The current study demonstrated an increased rate of microemboli production during perfusionist interventions compared with surgical interventions or baseline in patients undergoing coronary artery bypass grafting. We also found a significantly higher proportion of total emboli during perfusionist events, particularly during injection of drugs into the venous reservoir, than at any other time. This effect was consistent among all perfusionists who participated in this study.

Our findings are important for two reasons. First, they suggest that the majority of microemboli that occur during CPB consist of air. Small bubbles of air within the syringe are injected into the softshell venous reservoir by way of the manifold, thus entering the reservoir at the same point of entry as the CPB venous line. These bubbles are then transported to the oxygenator before they are able to rise to the top of the collapsible venous reservoir. Acquisition of blood samples results in embolus production because of the practice of injecting blood into the venous reservoir, to clear the manifold of stagnant blood, prior to acquiring the sample. In fact, we observed that when the perfusionists had discarded the stagnant blood rather than injected it, emboli did not occur. Careful deairing of the syringe before drug administration as well as discarding stagnant blood before sampling should result in a decreased number of cerebral microemboli. Although gaseous microemboli may not cause as much cerebral injury as atherosclerotic emboli, we believe that minimizing the occurrence of emboli of any type is important.

The second important observation from this study is that gaseous emboli are able to traverse the arterial filter. We used a 32-µm filter in the arterial line for all patients, yet air was able to be transported from the venous reservoir to the aorta. On two separate occasions, we observed a massive number of cerebral microemboli occurring without obvious cause. Shortly thereafter, the surgeon realized that the venous line was sucking air from the right atrium. When the venous cannula was repositioned, the microemboli immediately stopped. The method by which air traverses the arterial filter is not entirely clear but perhaps involves distortion of the bubbles into a "sausage" shape to fit through the pores or coalescence of fragmented bubbles distal to the filter. Although arterial filters have been demonstrated to reduce the number of cerebral emboli [24] and their use is standard, it is obvious that these devices do not remove all emboli.

The main limitation of this study is that our findings may be specific to our CPB circuit, in particular to the collapsible softshell venous reservoir. The use of a hardshell reservoir, as in the majority of cardiac surgical centers in Canada and the United States, may result in less microemboli because air bubbles may be able to rise to the top of the reservoir more efficiently. In addition, the manifold we used for drug administration and blood sampling is directly attached to the bottom of the reservoir and may be more prone to embolization than one connected to the top of the reservoir. Further studies are required to determine if our findings are generalizable to other types of venous reservoirs and CPB circuits. Until the results of these studies are known, however, we think it is reasonable to suggest the minimization of air in any venous reservoir to decrease the risk of cerebral embolization.

In summary, cerebral microemboli are more likely to occur during perfusionist interventions, particularly during injection of drugs into the venous reservoir, than at any other time during CPB. These emboli presumably consist of air not removed by the arterial filter. We suggest strict avoidance of air in the venous reservoir, whether injected by the perfusionist or inadvertently by means of a leak around the venous cannula, to minimize cerebral injury associated with CPB.

	Acknowledgments

 
Supported in part by the Heart and Stroke Foundation of Ontario. Dr Borger is a Research Fellow of the HSFO, and Dr Weisel is a Career Investigator of the HSFO.

We thank The Toronto Hospital cardiovascular surgery staff, in particular the anesthetists and perfusionists, for their cooperation and support.

We also thank DWL Electronic Systems for allowing us to use their transcranial Doppler equipment.

	References

Top Abstract Introduction Material and methods Results Comment References

 

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				A. M. Calafiore, M. Di Mauro, G. Teodori, G. Di Giammarco, S. Cirmeni, M. Contini, A. L. Iaco, and M. Pano Impact of aortic manipulation on incidence of cerebrovascular accidents after surgical myocardial revascularization Ann. Thorac. Surg., May 1, 2002; 73(5): 1387 - 1393. [Abstract] [Full Text] [PDF]

				M. J. A. Robson, R. P. Alston, I. J. Deary, P. J. D. Andrews, and M. J. Souter Jugular Bulb Oxyhemoglobin Desaturation, S100{beta}, and Neurologic and Cognitive Outcomes After Coronary Artery Surgery Anesth. Analg., October 1, 2001; 93(4): 839 - 845. [Abstract] [Full Text] [PDF]
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