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J Thorac Cardiovasc Surg 1995;109:249-258
© 1995 Mosby, Inc.
CARDIOPULMONARY BYPASS, |
Pittsburgh, Pa.
Supported in part by the Allegeny-Singer Reseach Institue, the Departments of Surgery and Psychiarty and the Division of Neurulogy, Allegheny General Hospital, Pittsburgh, Pa.
Address for reprints: Richard E. Clark, MD, Cardiovascular and Pulmonary Research Center, Allegheny-Singer Research Institute, 320 E. North Ave., Pittsburgh, PA 15212.
Abstract
Cerebral dysfunction after coronary artery bypass operations represents some to the most serious and costly complications of cardiac surgery, We used transcranial Doppler ultrasonography to detect and quantify the number of microemboli in the right middle cerebral artery of patients undergoing elective first coronary bypass operations (n = 117) and second coronary bypass operations (n = 10). We hypothesized that total microemboli were related to clinical outcome. A 2 MHz transducer was positioned in front of the ear above the zygomatic arch and depth gated to 50 mm. Microemboli were recorded as perturbations of the blood flow velocity in the middle cerebral artery and aurally monitored. Each episode of mircroembolism was specified both by clock time and as perfusion or surgical event. Forty-one patients (32%) completed neurophysiologic evaluation with a battery of tests for cognitive function. Anxiety states and traits were also assessed. The distribution of microembolism showed that there were three groups of patients <30 microemboli (n = 83); 30 to 59 (n = 24) >60 (n = 24). Seven of 10 patients with cerebral complications (stroke, coma delirium, aberrant behavior) were in the >60 microemboli group. Those with cerebral complications had 20.7 ± 4.5 from perfusion and system symptoms had 95.5 ± 19.5 microemboli from perfusion and 36.0 ± 6.9 from surgical events. Neuropsychological scores were most often depressed for memory (73%), comprehension (49%) , attention (46%), and constructional ability (44%). The greatest change was in total score in the >60 microemboli group (-3.3 ± 0.6) compared with -1.1 ± 0.2 and 1.1 ± 0.2 for the 30 to 59 and <30 groups, respectively. The incidences of cardiac and pulmonary complications and mortality were different between those patients with <60 microemboli versus those with >60 microemboli group. We concluded that transcranial Doppler ultrasonography is a useful technique to quantify and detect the source of microemboli during coronary artery bypass operations and may be useful in assesing new operative stragteies, the quality of the perfusion, and poentially as an indicator for pharmacologic therapy in the operationg room in patients with high microemboli counts. (J THORACCARDIOVASCSURG1995;109:249-58)
Cerebral dysfunction after cardiac operations in which cardiopulmonary bypass (CPB) is used is one of the most serious and costly complications. In the early years of CPB, this problem was largely attributed to use of the pump-oxygenator itself. During the past three decades, however, advanced knowledge and improvements in operative and perfusion techniques have resulted in a marked decrease in cerebral complications to current low levels in the range of 1% to 4% for all types of cardiac surgery in adult patients. 
1
These technologic advances have also made it increasingly possible over the past decade for older patients (>70 years) to undergo coronary artery bypass (CABG) operations with low morbidity. The downside of this trend is that the atherosclerotic disease process in these older patients is farther advanced, which has caused an increase in the prevalence of cerebral dysfunction in the elderly. This increase, coupled with the devastating patient and family consequences of stroke and encephalopathy and the subsequent costs of care, has initiated a series of studies to prevent or decrease the risk of this major complication. Wareing, 2 Barzilai, 3 Wareing, 4 Barzilai, 5 Marshall, 6 and their associates have published postmortem, echocardiographic, and operative data in several papers showing that careful assessment of preoperative and intraoperative findings can enable the surgeon to tailor surgical techniques for a particular patient requiring CABG in such a way as to minimize permanent or transient postoperative cerebral dysfunction.
Three years ago, we began to use color-encoded transcranial Doppler ultrasonography to assess the presence of microemboli (ME) encountered during CABG procedures. After an initial demonstration in which ME were detected more frequently than expected, we designed a prospective clinical study in which preoperative and postoperative neuropsychologic testing was performed along with the transcranial Doppler monitoring. Transcranial Doppler ultrasonography was used to continuously record the velocity of blood flow in the right middle cerebral artery from the onset of the induction of general anesthesia until the patient left the operating room.
We hypothesized that ME generation was a function of both the CPB equipment and the operation and that patient outcomes were related to total ME counts
MATERIALS AND METHODS
Patient population
A total of 127 patients (111 men, 16 women, mean age 56.4 ± 0.9 years), who were scheduled at least 24 hours in advance of their CABG operation, were entered into this study. Ten of these patients were having reoperations. Men were predominant because of the difficulty in sonicating the middle cerebral artery in women older than 50 years of age. Cortical thickness of the pre-aural sphenoidal-temporal area increases in women as they age, whereas in men the bone thickness remains thin.
Patients had to be at least 18 years of age and free of known carotid or atheromatous disease as determined on physical examination. Patients were excluded if they had a history of head trauma, seizures, stroke, other serious neurologic disease, or were unable to be scored as alert on the preoperative Neurobehaviorial Cognitive Status Examination. Additionally, no patients requiring emergency or urgent treatment were accepted because there would be insufficient time to administer the neuropsychologic testing, and no patients undergoing valve repair were entered into the study. Each patient who qualified for the study signed an informed consent document that had been approved by our institutional review board.
Transcranial Doppler technique
Before the baseline neuropsychologic test was given, our neurovascular nurse specialist evaluated each patient for hyperostosis frontalis internia of the temporal bone above the zygomatic arch. The middle cerebral artery was identified at a range-gated depth of 45 mm and the skin surface was marked with a surgical highlighter for ease of intraoperative probe mount placement.
A Nicolet (formerly EME) TC 2000 transcranial Doppler unit (Nicolet Instruments, Madison, Wis) with a 2 MHz intraoperative probe attachment was used during the operation to continuously measure the patient's middle cerebral artery blood flow velocities. The transducer was held in place by a head band, positioned in front of the right ear above the zygomatic arch, and angled until a clear velocity, color-encoded signal was viewed with the depth set at 50 mm. All emboli, whether solid or gaseous, demonstrate a high audible frequency response (> 40 dB) with a harmonic quality similar to a chirping or whistling sound. An ME is shown on the color-encoded spectral display of middle cerebral artery velocity as an instant bright-red, high-velocity signal. These data were continuously stored by the computer for later review.
After the procedure, the data were reviewed and hard copy color recordings were made with a Hewlett-Packard color jet printer (Hewlett-Packard Co, Palo Alto, Calif.). Recording intervals were specifically related to the events of the procedure: before cannulation, aortotomy, insertion of aortic cannula, insertion of a vent line before CPB, onset of partial CPB, insertion of the cardioplegia aortic needle, insertion of the coronary sinus cardioplegia cannula, aortic crossclamping, changes in CPB flow during the grafting maneuvers, rewarming, removal of aortic crossclamp, partial crossclamp on and off, defibrillation, removal of cardioplegic needles and cannula, lifting of the heart to inspect posterior anastomosis, removal of the vent, aortic and atrial cannulas, arrhythmias, and other nonroutine maneuvers or events.
Neuropsychologic testing
Forty-one patients (32%) completed neuropsychologic evaluation. Approximately one half of the study patients had transcranial Doppler ultrasonography during CABG without neuropsychologic testing because no psychometrist was available in the late afternoon or early morning hours before the patient's operation. Our high-volume, cardiac surgery, managed-care system for patients having elective CABG has mandated minimal preoperative intervals. Additional patients were lost to follow-up who refused a first or second examination, had a stroke, or died. Standardized neuropsychologic tests* were selected to assess cognitive function by means of a battery of examinations for orientation, attention, language comprehension, repetition and naming, constructional ability, memory, calculations, reasoning similarities and judgment, and anxiety. These same methods have been used in this institution for many clinical studies.
After informed consent was obtained, the same skilled, experienced psychometrist administered the neuropsychologic tests to all patients between 2 and 12 hours before the operation and again 5 to 10 days thereafter. Testing was administered in three sections, which together lasted approximately 1 hour. The immediate postoperative interval was chosen because most reported studies show a return to preoperative status 6 weeks to 6 months after operation. The purpose was to discover if the expected decrement in cognitive function was greater than expected in those with high ME counts.
The patient was always seated on his or her hospital bed, with a movable table positioned in front of him or her for the testing The curtains were drawn for privacy and to prevent external interaction during the session. Room and individual reading lights were kept consistent among all subjects. Testing commenced only after a clear verbal indication that all instructions were understood. Timed sections were signaled with "Begin" after the patient was manually positioned for the task.
Both individual test scores and total scores were used for correlation to total ME counts, and paired comparisons were used for change in cognitive function as a consequence of a major surgical experience.
Anesthetic and cardiopulmonary management
All patients had general anesthesia induced by fentanyl and midazolam. Neuromuscular blockade was achieved with vecuronium or pancuronium. Anesthesia was maintained with fentanyl, midazolam, and isoflurane until the patient was transferred to the intensive care unit, at which time 100% oxygen was used as the insufflation agent.
Throughout the course of all operations the alpha-stat method of acid-base balance was used. The perfusion circuit consisted of a Bentley custom pack containing a BCR-3500 cardiotomy reservoir with filter (Bentley Laboratories Division, Irvine, Calif.), a Bio-Medicus blood pump model BP-80 (Medtronic Bio-Medicus, Eden Prairie, Minn.), a Bentley Univox membrane oxygenator, and a Pall Stat Prime 40 µu m blood arterial line filter (SP 3840; Pall Biomedical Products Corp., East Hills, N.J.). An RF-10 recirculation filter (Bentley Laboratories Division, Irvine, Calif.) was used before the onset of perfusion for the crystalloid prime. Total bypass and aortic crossclamp times were 80 ± 5 and 42 ± 2 minutes, respectively. Mild hypothermia was used (26 degrees to 28 degrees C) until the distal anastomoses were completed, at which time temperature was gradually increased at the average rate of 0.5 degrees to 0.7 degrees C/min. Flow rates were maintained at 2.0 to 2.2 L/min per square meter, and the minimal mean perfusion pressure was 60 mm Hg.
Postoperative clinical status
Each patient was observed after the operation for arousal threshold, orientation, behavioral appropriateness, and motor functioning. Any patient demonstrating a neurologic deficit or behavioral abnormality was examined by the study neurologist. Patients in whom stroke was a primary diagnosis received computed tomographic scans as soon as the hemodynamic status permitted transportation to the radiology department.
Cardiac complications were defined as hypotension with decreased cardiac output necessitating inotropic agents, intraaortic balloon pumping, or extracorporeal membrane oxygenation, and atrial or ventricular arrhythmias, or both. Pulmonary complications were defined as ventilator dependence, inability to maintain normal blood gases in the absence of low cardiac output, decreased work of breathing manifested by inability to wean, tracheostomy requirement, pneumothorax, or severe bronchitis.
Statistical analyses
The strength of the association between total ME and postoperative outcome (encephalopathy, stroke, and cardiopulmonary complications) was assessed by 
2 analysis. Changes in variables measured during the various stages of CPB were evaluated by repeated-measures analysis of variance. Differences between preoperative and postoperative neuropsychologic test scores were assessed by either the paired t test or the nonparametric sign test. The correlation coefficient was used to quantify the relationship between change in neuropsychologic test scores and total ME.
All continuous variables are expressed as mean values ± standard error of the mean Categoric variables are expressed as rates. All p values are two-tailed. A p value 
0.05 was considered to indicate statistical significance. Statistical analysis was performed with the Statistical Package for the Social Sciences software (SPSS/PC+, Chicago, Ill.).
RESULTS
Total ME per patient were plotted by deciles versus the number of patients (Fig. 1). This skewed distribution pattern clearly demonstrated three generic populations: those with < 30 ME, those with 30 to 59 ME, and those > 60 ME. We then determined the relationship of total ME counts to incidence of central nervous system (CNS) symptoms. Of the > 60 ME group (mean 118 ± 11.9), 35% (7/20) had symptoms. In contrast, only 4.2% (1/24) and 2.4% (2/83) of patients in the 30 to 59 ME and < 30 ME groups, respectively, had symptoms. In all, 10 of the 127 patients (7.9%) had symptoms. When grouped by type of CNS abnormality, all abnormality types had > 70 ME per category (Fig. 2). These data clearly demonstrate a relationship between total ME count and clinical outcome that was nonlinear and more of a threshold type.
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Similarly, 15 surgical maneuvers were related to the mean numbers of ME for all patients for each of those intervals (Fig. 3). Three surgical events were prominent: cannulation (mean value 2.9 ± 0.3); partial crossclamp off (mean value 3.3 ± 0.6); and cardiac manipulations (mean value 4.9 ± 1.5). The last event was associated with lifting the heart to visualize the posterior anastomoses. When the CPB and surgical events were combined for all patients, each contributed approximately 50% of the total ME. The mean total per patient was 35.9 ± 3.7 (median 22.0; range 0 to 251; standard deviation 41.2). Variances in blood flow velocity and blood pressure were analyzed for the study interval and were small. Mean flow velocity in the right middle cerebral artery ranged from 29 to 50 cm/sec, which was entirely within the normal range, as was mean arterial blood pressure (66 to 87 mm Hg).
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Table I. The 10 patients with symptoms had 2.75-fold greater surgical ME than perfusion ME. When the three patients with < 60 ME were removed from this group that had symptoms, a threefold difference between surgical and perfusion ME remained. Comparison of the symptomatic patients to the asymptomatic ones in the > 60 ME category demonstrated an unexpected and striking finding, namely, that the surgical/perfusion source ratios were reversed. The symptom-free patients had 2.6-fold more perfusion ME than surgical ME. There were no differences in mean age in the two groups to account for this difference. The implications of these data are discussed later.
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The last aim of this study was to determine if neuropsychologic testing would reveal subtle cognitive deficits as a consequence of the ME generated during the CABG operation. Eight standardized tests measured specific abilities, and two trail-making tests, generally thought to be the most sensitive, measured general brain function. Two questionnaires measured anxiety state and traits to assist in the interpretation of any changes in the cognitive function tests.
Comparison of the preoperative total scores (75.5 ± 0.5) to postoperative total scores (73.4 ± 0.6) showed no statistical change. Comparisons of each individual test showed that four tests were decreased in the postoperative intervals, with the following incidences: memory 73%, comprehension 49%, attention 46%, and constructional ability 44% (Table II). Net change per patient was determined for the three ME groups: > 60 (n = 7) 
= -3.3 ± 0.6; for those with < 60 ME, the net changes in total scores were -1.1 ± 0.2 and -1.9 ± 0.2 for the 30 to 59 ME and the < 30 ME groups, respectively. The decrement in the >60 ME groups was strongly influenced by one symptomatic patient who had a change of -8. Even with this patient removed, the >60 ME group still had a mean decrement of 2.6 ± 0.6.
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Table III. There was a statistically significant difference for the two ME-count groups, with those with <60 ME having a low complication rate and mortality. There were four deaths (3.1%). Two were CNS-related (coma and stroke), including one patient who had the hyperperfusion phenomenon at the onset of CPB and abnormalities on the computed tomographic scan. A third patient had low cardiac output unresponsive to intraaortic balloon pumping and high-dose inotropic agents, and extracorporeal membrane oxygenation was used for ventricular assist. He awoke promptly but died on the tenth postoperative day having been successfully weaned from extracorporeal membrane oxygenation. The last patient was awaiting discharge and had sudden chest pain, cardiogenic shock, and died on the ninth day after the operation.
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Transcranial Doppler ultrasonography has been used for more than a decade to measure ME in the cerebral circulation of patients having CPB. Padayachee and colleagues 7 studied 27 patients with 2 MHz Doppler ultrasonography. Ten patients demonstrated no ME while supported by a membrane oxygenator whereas all 17 patients with a bubble oxygenator had ME, whose origin was directly related to gas flow. ME were also detected in 22 of these 27 patients during insertion of the aortic cannula. Pugsley 8 in 1989 used transcranial Doppler technology to determine the benefit of arterial line filtration with a bubble oxygenator on total ME recorded in the middle cerebral artery of 20 patients.
van der Linden and Casimir-Ahn 9 in 1991 published a small study of 10 patients having aortic or mitral valve replacement in which ME were detected during the insertion of the aortic cannula, at the initiation of CBP, after crossclamp removal, and during heart filling. The highest counts (>70 ME/min) occurred during the last interval and were shown to be the consequence of inadequate deairing procedures.
High-intensity transient signals were first observed during transcranial Doppler ultrasonography during carotid endarterectomy in 1986. 10 Thrombus, platelet aggregates, atheromatous material, and fat particles (0.5 to 5.0 mm maximum dimension) were all detected by transcranial Doppler techniques in in vitro extracorporeal experiments, which demonstrated a relation between embolus size and the maximum amplitude of the Doppler signal. 11,12 Although such relationships were obtained in highly controlled bench studies, no in vivo data exist that permit size determination or composition of any specific particle detected by transcranial Doppler techniques. Further, the specificity and sensitivity for emboli of various origins have not been determined.
The data in the present study confirm and extend the findings of previous authors, showing that strategies based on postmortem anatomic studies, epicardial echocardiography, and empiric clinical experience have relevance with respect to decreasing total ME during CABG
Outcome effects are frequently difficult to determine for low-frequency events in typical surgical series because of relatively small numbers of patients. When stroke was combined with coma and inappropriate behavior, the sum of these frequencies was related to total ME in our series. Those patients (n = 10) having > 60 ME (7.9% of the study population) had 70% of the cerebral dysfunction incidence. There was no effect of age because this variable was not related to ME counts, any CNS symptom, or stroke.
One of the major hypotheses tested in our study was that the perfusion circuit and the conduct of CPB were a major source of ME during CABG. This hypothesis was correct with respect to the overall analyses. However, for those patients with symptoms after CABG, ME from surgical events were much greater than those caused by perfusion.
Hyperperfusion at the onset of CPB occurred with few ME during the event and appears to carry a significant prognosis, with four of five patients having CNS symptoms. The perfusion and anesthesia records for these patients were thoroughly reviewed. Arterial blood gases and pH were normal as were all other measured variables. No differences were found among these five patients and the other 122 patients except for hyperperfusion. Two causes have been postulated: loss of autoregulation of the cerebral vasculature and malposition of the aortic cannula outlet toward the innominate artery. Regardless of cause, the recognition of this event by any method should be cause for immediate cessation of CPB.
The psychologic changes that occur with hospitalization and major life-endangering treatments have been well documented. We performed a battery of neuropsychologic tests before and after the surgical experience to determine if total ME counts could be related to decrements in testing scores out of proportion to the expected decrease in most tests as a result of traumatic experience. To determine the importance of our finding, we performed a metatype analysis on published studies of neuropsychologic testing first in patients having CABG and nonsurgical case controls (n = 3), second, in patients having CABG and noncardiac surgical case controls (n = 4), and, finally, in patients having CABG and no case controls (n = 6). 13-25 We also reviewed seven studies of patients having cardiac valve replacement without case controls and four studies on patients who had noncardiac operations without case controls. 26-36 Regardless of the type of control or lack thereof, the changes in neuropsychologic scores observed in nearly all the cognitive function studies were related to age and degree of illness before the operation and to the presence or absence of a serious noncerebral complication. The most abnormal scores occurred in those who had a cerebral complication. If we adjust for the latter, the bulk of the data demonstrated that mild to moderate depression of some cognitive tests occurred as a consequence of the illness, the operation (CABG), the intensive care unit experience, and perhaps the medications used in the immediate (<10 days) postoperative interval. The vast majority of patients in these published studies with any cognitive deficit at discharge were essentially at their preoperative status 6 weeks to 6 months after the operation.
In patients with stroke or who recover from coma, or in those who have prolonged inappropriate behavior after operation, neuropsychologic scores do not generally return to preoperative levels, and alteration of mood and personality characteristics of mood may accompany the cognitive deficits. 32
Although our data show a statistically significant change from the preoperative to postoperative interval in attention, language comprehension and repetition, and judgment, the changes were small and not clinically relevant because these were less than a whole integer, the smallest difference detectable in this type of testing
In summary, the patients with the highest surgically generated ME counts had the highest incidence of clinical CNS dysfunction after operation In contrast, those with the greatest number of ME generated by the CPB system appeared to tolerate them well, but had greater decrements in cognitive function than those with fewer ME counts. Patients with low ME counts from either surgical or perfusion events uniformly did well, with few complications and only mild cognitive function changes that could be accounted for by the major operative experience.
In our view, transcranial Doppler ultrasonography is a useful technique to monitor the ME load to the brain during CABG operations. The data presented in this study show that the consequences of various surgical maneuvers in terms of ME can be measured and used for determining alternative strategies in certain patient subsets. Further attention to the quality of perfusion is merited to explain the large variance of ME generated by the same CPB system used throughout the study interval. Finally, it may be possible to use transcranial Doppler data as an indicator for pharmacologic prophylaxis (steroids, barbiturates, adenosine-regulating agents) when high ME counts are detected.
Appendix: DISCUSSION
Dr. Robert B. Wallace (Washington, D.C.).
Dr. Clark, are you able to define a difference in ME associated with perfusion alone and those associated with surgical manipulation, and have your findings resulted in a change in the conduct of the operation?
Dr. Clark.
In response, this technology will measure certain particles down to 30 µm. Unfortunately, a piece of plaque has about the same sonic ring to it as an air bubble of the same size. Because we were not able to distinguish what the event is by a characteristic signal on spectral display, we tried to associate it with a perfusion or surgical event.
We have purposely attempted not to give feedback to the surgeons, though invariably it happens during an operation, as you know, Dr Wallace. Surgeons want to know how they are doing, especially when there is somebody present with earphones on. One important thing that has resulted from this feedback, however, has been the conclusion we made when we looked at cannulation. If a fluid-filled aortic cannula was used, about 4 1/2 ME were generated on insertion, probably because the air bubble at the tip invariably went up into the brain. Use of a dry-filled cannula, on the other hand, reduced the number to 1 ME per insertion. In that sense, the data that did feed back to the surgeons ultimately changed the operation.
Dr. Richard M. Engelman (Springfield, Mass.).
I have two questions. I assume that you placed a Doppler device over the carotid artery. Can you explain the mechanisms and the false positive results? My second question relates to the temperature of the CPB perfusate in this setting. Do you think that perfusate temperature plays a role in the outcome of patients who have ME?
Dr. Clark.
The answer to your first question is that before the operation, we locate the middle cerebral artery transonically and mark the proper location of the transducer on the skin in front of the ear. With the transducer in position, we are looking right down the middle cerebral artery, not the carotid artery, so that we know that whatever is going through the middle cerebral vessel is going to the right hemisphere.
Second, with regard to artifact, we have learned that it takes a good deal of experience to record these events. Our nurse specialist has been doing this for more than 7 years now and has been traveling the country to teach others how to do this. Not only do you have to make a recording, but you also must wear earphones to distinguish the type of change in harmonics. You then mark the event on the computer as it happens to be sure that the event is not mistaken for an artifact. We can distinguish between low-frequency artifact and the high-frequency ME that one sees with a bubble or material from the aorta.
With regard to temperature, all of the perfusions were carried out in a similar fashion in our very high-volume cardiac surgical center . The temperatures went down to about 28 ° C, which is not really very cold, and were then gradually increased. Previous ME work that I did showed that a heat exchanger could liberate bubbles when the hot water was first turned into that device and maintained a 10 ° C difference between water and blood. We did not see any increase in the number of ME with rewarming in our patients.
Dr. Robert Frater (Bronx, N.Y.).
Did you have transesophageal echo studies on these patients, and, if so, was there any correlation either with the appearance of air or the appearance of the aorta? Have you done the same test in patients undergoing valvular disease?
Dr. Clark.
We, in fact, are going to be collecting valve data. I know that the group at Bowman Gray, as well as many groups in Europe, has already done so.
To answer the last question first, the patients with valve operations have a greater number of ME. With regard to your question about transesophageal echocardiography, we used this to study the effects of triiodothyronine on left ventricular wall motion after CABG. Typically, we see a very fine, sparkling, swirling kind of picture in the left atrium after completion of all grafting, which must represent air. We noticed that the high number of ME counts occurred with the lifting of the heart, which suggests that lifting the heart allowed the bubbles to rise into the left ventricle and on the next beat these were propelled into the aorta. I think that the origin of these ME is quite different from those found earlier in the operation. We did get air into the heart during CABG in our study, which is consistent with the data of those who have really looked for it.
Dr. Nicholas T. Kouchoukos (St. Louis, Mo.).
The mean age of your patients was relatively young by current standards, at least for persons undergoing CABG operations. Did you observe any correlation between the incidence of ME and age of the patient?
Dr. Clark.
No. The age range was small, Dr. Kouchoukos. There was a trend of a relationship between age and surgical ME. None of these patients, to my knowledge, had an eggshell type of ascending aorta, nor were there any ascending aortic aneurysms in this series. I think the oldest patient was 80 years old.
Dr. L. Henry Edmunds, Jr. (Philadelphia, Pa.).
Dr. Clark, did you use a filter in the arterial line, and if so what was the pore size? Can the Doppler technique distinguish between types of ME? Obviously you can pick up air and atherosclerosis, but what about fat, red cell debris, and so on?
Dr. Clark.
In vitro studies show a sensitivity for detection in the 50 to 70 µm range for protein particles and down to 30 µm for highly sonicated particles of plaque or air. Unfortunately, there is no correlation of size or signal amplitude of type of ME.
The circuit consisted of a membrane oxygenator, reservoirs, a biopump, and a 40 µm filter on our arterial line filter that was used throughout the entire perfusion. A recirculation filter was used before the lines were connected.
Dr. Anthony L. Moulton (Providence, R.I.).
What method was used for venting the left ventricle, and was there any impact of the different methods for that?
Dr Clark.
There were eight surgeons operating, whose venting methods ranged from none, to venting the pulmonary artery, to occasionally venting the left atrium. It was rare to vent the left side of the heart, however.
Acknowledgments
We acknowledge the interest, cooperation, and collegiality of the cardiac surgeons who actively gave their support and enlisted patient cooperation for these studies. The surgeons were Daniel H. Benckart, John A. Burkholder, George A. Liebler, George J. Magovern, Jr., James A. Magovern, Thomas D. Maher, and Sang B. Park. We are indebted to the skill and persistence of the psychometrist, Jasmine Gulati, MS, the cerebral scrutiny and statistical treatment of the data by Diane Vido, MS, the editorial skills of Nancy Lynch, MA, RN, BSN, the literature search and bibliography assimilation of Jane Etherington, BS, and the support services of Kathleen Pater.
Footnotes
Read at the Seventy-fourth annual meeting of the American Assocation for Thoracic Surgery, New York, N.Y., April 24-27, 1994. 
*Neurobehaviorial Cognitive Status Examination. The Northern California Neurobehavioral Group, Inc,. 1988. State-Trait Anxiety Inventory. Spieleberger Consulting Psychologists, Inc. 1992.
References
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J. W. Hammon Extracorporeal Circulation: Perfusion System Card. Surg. Adult, January 1, 2008; 3(2008): 350 - 370. [Full Text]
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J. T. Gutsche, A. T. Cheung, M. L. McGarvey, W. G. Moser, W. Szeto, J. P. Carpenter, R. M. Fairman, A. Pochettino, and J. E. Bavaria Risk Factors for Perioperative Stroke After Thoracic Endovascular Aortic Repair Ann. Thorac. Surg., October 1, 2007; 84(4): 1195 - 1200. [Abstract] [Full Text] [PDF]
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J.-C. Tardif, M. Carrier, D. E. Kandzari, R. Emery, R. Cote, T. Heinonen, M. Zettler, V. Hasselblad, M.-C. Guertin, R. A. Harrington, et al. Effects of pyridoxal-5'-phosphate (MC-1) in patients undergoing high-risk coronary artery bypass surgery: Results of the MEND-CABG randomized study J. Thorac. Cardiovasc. Surg., June 1, 2007; 133(6): 1604 - 1611. [Abstract] [Full Text] [PDF]
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F. D. Rubens and H. Nathan Lessons learned on the path to a healthier brain: dispelling the myths and challenging the hypotheses Perfusion, May 1, 2007; 22(3): 153 - 160. [Abstract] [PDF]
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 M. Y. Kassab, A. Majid, M. U. Farooq, H. Azhary, L. A. Hershey, E. M. Bednarczyk, D. F. Graybeal, and M. D. Johnson Transcranial Doppler: An Introduction for Primary Care Physicians J Am Board Fam Med, January 1, 2007; 20(1): 65 - 71. [Abstract] [Full Text] [PDF]
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K. Yoshitani, F. de Lange, Q. Ma, H. P. Grocott, and G. B. Mackensen Reduction in Air Bubble Size Using Perfluorocarbons During Cardiopulmonary Bypass in the Rat Anesth. Analg., November 1, 2006; 103(5): 1089 - 1093. [Abstract] [Full Text] [PDF]
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K. G. Shann, D. S. Likosky, J. M. Murkin, R. A. Baker, Y. R. Baribeau, G. R. DeFoe, T. A. Dickinson, T. J. Gardner, H. P. Grocott, G. T. O'Connor, et al. An evidence-based review of the practice of cardiopulmonary bypass in adults: A focus on neurologic injury, glycemic control, hemodilution, and the inflammatory response. J. Thorac. Cardiovasc. Surg., August 1, 2006; 132(2): 283 - 290.e3. [Full Text] [PDF]
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D. Whitaker, J. Stygall, M. Harrison, and S. Newman Relationship between white cell count, neuropsychologic outcome, and microemboli in 161 patients undergoing coronary artery bypass surgery J. Thorac. Cardiovasc. Surg., June 1, 2006; 131(6): 1358 - 1363. [Abstract] [Full Text] [PDF]
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T.-Y. Hsia and P. J. Gruber Factors Influencing Neurologic Outcome After Neonatal Cardiopulmonary Bypass: What We Can and Cannot Control Ann. Thorac. Surg., June 1, 2006; 81(6): S2381 - S2388. [Abstract] [Full Text] [PDF]
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T. T. Laitio, H. V. Huikuri, J. Koskenvuo, J. Jalonen, T. H. Makikallio, H. Helenius, E. S.H. Kentala, J. Hartiala, and H. Scheinin Long-term alterations of heart rate dynamics after coronary artery bypass graft surgery. Anesth. Analg., April 1, 2006; 102(4): 1026 - 1031. [Abstract] [Full Text] [PDF]
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D. C Whitaker, J. Stygall, C. Hope-Wynne, R. K Walesby, M. J. Harrison, and S. P Newman A prospective clinical study of cerebral microemboli and neuropsychological outcome comparing vent-line and auto-venting arterial line filters: both filters are equally safe Perfusion, March 1, 2006; 21(2): 83 - 86. [Abstract] [PDF]
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R. A. Rodriguez, F. Rubens, D. Belway, and H. J. Nathan Residual air in the venous cannula increases cerebral embolization at the onset of cardiopulmonary bypass Eur. J. Cardiothorac. Surg., February 1, 2006; 29(2): 175 - 180. [Abstract] [Full Text] [PDF]
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J. L Rudolph, D. Tilahun, P. R Treanor, V. E Pochay, M. A Mahendrakar, P. Sagar, and V. L Babikian Use of a large bore syringe creates significantly fewer high intensity transient signals (HITS) into a cardiopulmonary bypass system than a small bore syringe Perfusion, January 1, 2006; 21(1): 67 - 71. [Abstract] [PDF]
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J. P. Gold, K. E. Torres, W. Maldarelli, I. Zhuravlev, D. Condit, and J. Wasnick Improving Outcomes in Coronary Surgery: The Impact of Echo-Directed Aortic Cannulation and Perioperative Hemodynamic Management in 500 Patients Ann. Thorac. Surg., November 1, 2004; 78(5): 1579 - 1585. [Abstract] [Full Text] [PDF]
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D. C. Whitaker, S. P. Newman, J. Stygall, C. Hope-Wynne, M. J.G. Harrison, and R. K. Walesby The effect of leucocyte-depleting arterial line filters on cerebral microemboli and neuropsychological outcome following coronary artery bypass surgery Eur. J. Cardiothorac. Surg., February 1, 2004; 25(2): 267 - 274. [Abstract] [Full Text] [PDF]
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E. Neri, C. Sassi, L. Barabesi, M. Massetti, G. Pula, D. Buklas, R. Tassi, and P. Giomarelli Cerebral autoregulation after hypothermic circulatory arrest in operations on the aortic arch Ann. Thorac. Surg., January 1, 2004; 77(1): 72 - 79. [Abstract] [Full Text] [PDF]
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J. Bucerius, J. F. Gummert, M. A. Borger, T. Walther, N. Doll, V. Falk, D. V. Schmitt, and F. W. Mohr Predictors of delirium after cardiac surgery delirium: Effect of beating-heart (off-pump) surgery J. Thorac. Cardiovasc. Surg., January 1, 2004; 127(1): 57 - 64. [Abstract] [Full Text] [PDF]
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V. Dalinin, P. S. Lingaas, K. Hatteland, and J. L Svennevig Carotid Doppler microembolic signals in patients one year after heart valve surgery Perfusion, December 1, 2003; 18(6): 333 - 337. [Abstract] [PDF]
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M. Schoenburg, B. Kraus, A. Muehling, U. Taborski, H. Hofmann, G. Erhardt, S. Hein, M. Roth, P. R. Vogt, G. F. Karliczek, et al. The dynamic air bubble trap reduces cerebral microembolism during cardiopulmonary bypass J. Thorac. Cardiovasc. Surg., November 1, 2003; 126(5): 1455 - 1460. [Abstract] [Full Text] [PDF]
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J. E. Scarborough, W. White, F. E. Derilus, J. P. Mathew, M. F. Newman, and K. P. Landolfo Combined use of off-pump techniques and a sutureless proximal aortic anastomotic device reduces cerebral microemboli generation during coronary artery bypass grafting J. Thorac. Cardiovasc. Surg., November 1, 2003; 126(5): 1561 - 1567. [Abstract] [Full Text] [PDF]
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C. Lund, P. K. Hol, R. Lundblad, E. Fosse, K. Sundet, B. Tennoe, R. Brucher, and D. Russell Comparison of cerebral embolization during off-pump and on-pump coronary artery bypass surgery Ann. Thorac. Surg., September 1, 2003; 76(3): 765 - 770. [Abstract] [Full Text] [PDF]
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T. Goto, T. Baba, K. Matsuyama, K. Honma, M. Ura, and T. Koshiji Aortic atherosclerosis and postoperative neurological dysfunction in elderly coronary surgical patients Ann. Thorac. Surg., June 1, 2003; 75(6): 1912 - 1918. [Abstract] [Full Text] [PDF]
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R Ascione and G.D Angelini OPCAB surgery: a voyage of discovery back to the future Eur. Heart J., January 2, 2003; 24(2): 121 - 124. [Full Text] [PDF]
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J. S. Savino, T. F. Floyd, and A. T. Cheung Cardiac Anesthesia Card. Surg. Adult, January 1, 2003; 2(2003): 249 - 281. [Full Text]
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E. A. Hessel II and L. H. Edmunds Jr. Extracorporeal Circulation: Perfusion Systems Card. Surg. Adult, January 1, 2003; 2(2003): 317 - 338. [Full Text]
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R. Salenger, J. S. Gammie, and T. J. Vander Salm Postoperative Care of Cardiac Surgical Patients Card. Surg. Adult, January 1, 2003; 2(2003): 439 - 469. [Full Text]
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S. Urbanek and H.-J. Tiedtke Improved methods for measurement of gaseous microbubbles during extracorporeal circulation Perfusion, December 1, 2002; 17(6): 429 - 434. [Abstract] [PDF]
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T. J. Jones, D. D. Deal, J. C. Vernon, N. Blackburn, and D. A. Stump Does vacuum-assisted venous drainage increase gaseous microemboli during cardiopulmonary bypass? Ann. Thorac. Surg., December 1, 2002; 74(6): 2132 - 2137. [Abstract] [Full Text] [PDF]
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L. S. Rasmussen, B. Sperling, H. H. Abildstrom, and J. T. Moller Neuron loss after coronary artery bypass detected by SPECT estimation of benzodiazepine receptors Ann. Thorac. Surg., November 1, 2002; 74(5): 1576 - 1580. [Abstract] [Full Text] [PDF]
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N. Stroobant, G. Van Nooten, Y. V. Belleghem, and G. Vingerhoets Short-term and long-term neurocognitive outcome in on-pump versus off-pump CABG Eur. J. Cardiothorac. Surg., October 1, 2002; 22(4): 559 - 564. [Abstract] [Full Text] [PDF]
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D. J. Cook, K. J. Zehr, and T. A. Orszulak Reduction in brain embolization using the aegis aortic cannula during bypass in swine Ann. Thorac. Surg., September 1, 2002; 74(3): 825 - 829. [Abstract] [Full Text] [PDF]
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D. J. Cook, K. J. Zehr, T. A. Orszulak, and J. M. Slater Profound reduction in brain embolization using an endoaortic baffle during bypass in swine Ann. Thorac. Surg., January 1, 2002; 73(1): 198 - 202. [Abstract] [Full Text] [PDF]
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D C Whitaker, J A Stygall, S P Newman, and M J. Harrison The use of leucocyte-depleting and conventional arterial line filters in cardiac surgery: a systematic review of clinical studies Perfusion, December 1, 2001; 16(6): 433 - 446. [Abstract] [PDF]
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W. Plochl, C. G. Krenn, D. J. Cook, E. Gollob, T. Pezawas, H. Schima, O. Ipsiroglu, G. Wollenek, and G. Grubhofer Can hypocapnia reduce cerebral embolization during cardiopulmonary bypass? Ann. Thorac. Surg., September 1, 2001; 72(3): 845 - 849. [Abstract] [Full Text] [PDF]
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T. Goto, T. Baba, K. Honma, Y. Shibata, Y. Arai, H. Uozumi, and T. Okuda Magnetic resonance imaging findings and postoperative neurologic dysfunction in elderly patients undergoing coronary artery bypass grafting Ann. Thorac. Surg., July 1, 2001; 72(1): 137 - 142. [Abstract] [Full Text] [PDF]
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R. W. Kim, D. C. Mariconda, G. Tellides, G. S. Kopf, M. L. Dewar, Z. Lin, and J. A. Elefteriades Single-clamp technique does not protect against cerebrovascular accident in coronary artery bypass grafting Eur. J. Cardiothorac. Surg., July 1, 2001; 20(1): 127 - 132. [Abstract] [Full Text] [PDF]
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M. I. Dar, T. Gillott, F. Ciulli, and G. J. Cooper Single aortic cross-clamp technique reduces S-100 release after coronary artery surgery Ann. Thorac. Surg., March 1, 2001; 71(3): 794 - 796. [Abstract] [Full Text] [PDF]
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L. Steed, R. Kong, J. Stygall, J. Acharya, M. Bolla, M. J.G. Harrison, S. E. Humphries, and S. P. Newman The role of apolipoprotein E in cognitive decline after cardiac operation Ann. Thorac. Surg., March 1, 2001; 71(3): 823 - 826. [Abstract] [Full Text] [PDF]
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M Schonburg, P Urbanek, G Erhardt, B Kraus, U Taborski, A Muhling, S Hein, M Roth, H J Tiedtke, and W P Klovekorn Significant reduction of air microbubbles with the dynamic bubble trap during cardiopulmonary bypass Perfusion, January 1, 2001; 16(1): 19 - 25. [Abstract] [PDF]
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B. J. Bowles, J. D. Lee, C. R. Dang, S. N. Taoka, E. W. Johnson, E. M. Lau, and K. Nekomoto Coronary Artery Bypass Performed Without the Use of Cardiopulmonary Bypass Is Associated With Reduced Cerebral Microemboli and Improved Clinical Results Chest, January 1, 2001; 119(1): 25 - 30. [Abstract] [Full Text] [PDF]
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A. G. Royse, C. F. Royse, A. E. Ajani, E. Symes, P. Maruff, S. Karagiannis, R. P. Gerraty, L. E. Grigg, and S. M. Davis Reduced neuropsychological dysfunction using epiaortic echocardiography and the exclusive Y graft Ann. Thorac. Surg., May 1, 2000; 69(5): 1431 - 1438. [Abstract] [Full Text] [PDF]
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A. Diegeler, R. Hirsch, F. Schneider, L.-O. Schilling, V. Falk, T. Rauch, and F. W. Mohr Neuromonitoring and neurocognitive outcome in off-pump versus conventional coronary bypass operation Ann. Thorac. Surg., April 1, 2000; 69(4): 1162 - 1166. [Abstract] [Full Text] [PDF]
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T. Goto, T. Baba, A. Yoshitake, Y. Shibata, M. Ura, and R. Sakata Craniocervical and aortic atherosclerosis as neurologic risk factors in coronary surgery Ann. Thorac. Surg., March 1, 2000; 69(3): 834 - 840. [Abstract] [Full Text] [PDF]
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D. J. Cook, W. Plochl, and T. A. Orszulak Effect of temperature and PaCO2 on cerebral embolization during cardiopulmonary bypass in swine Ann. Thorac. Surg., February 1, 2000; 69(2): 415 - 420. [Abstract] [Full Text] [PDF]
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J. C. K. Fitch, S. Rollins, L. Matis, B. Alford, S. Aranki, C. D. Collard, M. Dewar, J. Elefteriades, R. Hines, G. Kopf, et al. Pharmacology and Biological Efficacy of a Recombinant, Humanized, Single-Chain Antibody C5 Complement Inhibitor in Patients Undergoing Coronary Artery Bypass Graft Surgery With Cardiopulmonary Bypass Circulation, December 21, 1999; 100(25): 2499 - 2506. [Abstract] [Full Text] [PDF]
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X. M Mueller, H. T Tevaearai, D. Jegger, M. Augstburger, M. Burki, and L. K von Segesser Ex vivo testing of the Quart(R) arterial line filter Perfusion, December 1, 1999; 14(6): 481 - 487. [Abstract] [PDF]
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C. R. Wilhelm, J. Ristich, L. E. Knepper, R. Holubkov, S. R. Wisniewski, R. L. Kormos, and W. R. Wagner Measurement of Hemostatic Indexes in Conjunction With Transcranial Doppler Sonography in Patients With Ventricular Assist Devices Stroke, December 1, 1999; 30(12): 2554 - 2561. [Abstract] [Full Text] [PDF]
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M. A. Borger, R. L. Taylor, R. D. Weisel, G. Kulkarni, M. Benaroia, V. Rao, G. Cohen, L. Fedorko, and C. M. Feindel DECREASED CEREBRAL EMBOLI DURING DISTAL AORTIC ARCH CANNULATION: A RANDOMIZED CLINICAL TRIAL J. Thorac. Cardiovasc. Surg., October 1, 1999; 118(4): 740 - 745. [Abstract] [Full Text] [PDF]
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R. L. Taylor, M. A. Borger, R. D. Weisel, L. Fedorko, and C. M. Feindel Cerebral microemboli during cardiopulmonary bypass: increased emboli during perfusionist interventions Ann. Thorac. Surg., July 1, 1999; 68(1): 89 - 93. [Abstract] [Full Text] [PDF]
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F. Musumeci, M. Feccia, P. A. MacCarthy, G. R. Ellis, L. Mammana, F. Brinn, and W. J. Penny Prospective randomized trial of single clamp technique versus intermittent ischaemic arrest: myocardial and neurological outcome Eur. J. Cardiothorac. Surg., June 1, 1999; 13(6): 702 - 709. [Abstract] [Full Text] [PDF]
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D. J. Cook Changing Temperature Management for Cardiopulmonary Bypass Anesth. Analg., June 1, 1999; 88(6): 1254 - 1254. [Full Text] [PDF]
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D. A. Stump, W. R. Brown, D. M. Moody, K. D. Rorie, J. C. Manuel, N. D. Kon, J. B. Butterworth, and J. W. Hammon Microemboli and Neurologic Dysfunction After Cardiovascular Surgery Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 1999; 3(1): 47 - 54. [Abstract] [PDF]
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R. L. Wolman, N. A. Nussmeier, A. Aggarwal, M. S. Kanchuger, G. W. Roach, M. F. Newman, C. M. Mangano, K. E. Marschall, C. Ley, D. M. Boisvert, et al. Cerebral Injury After Cardiac Surgery : Identification of a Group at Extraordinary Risk Stroke, March 1, 1999; 30(3): 514 - 522. [Abstract] [Full Text] [PDF]
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L. R. Caplan and M. Hennerici Impaired Clearance of Emboli (Washout) Is an Important Link Between Hypoperfusion, Embolism, and Ischemic Stroke Arch Neurol, November 1, 1998; 55(11): 1475 - 1482. [Abstract] [Full Text] [PDF]
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C. F. Bladin, L. Bingham, L. Grigg, A. G. Yapanis, R. Gerraty, and S. M. Davis Transcranial Doppler Detection of Microemboli During Percutaneous Transluminal Coronary Angioplasty Stroke, November 1, 1998; 29(11): 2367 - 2370. [Abstract] [Full Text] [PDF]
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F. P. Milsom and S. J. Mitchell A dual-vent left heart deairing technique markedly reduces carotid artery microemboli Ann. Thorac. Surg., September 1, 1998; 66(3): 785 - 791. [Abstract] [Full Text] [PDF]
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N. D. Croughwell, J. G. Reves, W. D. White, H. P. Grocott, B. I. Baldwin, F. M. Clements, R. D. Davis Jr, R. H. Jones, and M. F. Newman Cardiopulmonary Bypass Time Does Not Affect Cerebral Blood Flow Ann. Thorac. Surg., May 1, 1998; 65(5): 1226 - 1230. [Abstract] [Full Text] [PDF]
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A. Jacobs, M. Neveling, M. Horst, M. Ghaemi, J. Kessler, H. Eichstaedt, J. Rudolf, P. Model, H. Bonner, E. R. de Vivie, et al. Alterations of Neuropsychological Function and Cerebral Glucose Metabolism After Cardiac Surgery Are Not Related Only to Intraoperative Microembolic Events Stroke, March 1, 1998; 29(3): 660 - 667. [Abstract] [Full Text] [PDF]
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D. Georgiadis, A. Wenzel, H. R. Zerkowski, S. Zierz, and A. Lindner Automated Intraoperative Detection of Doppler Microembolic Signals Using the Bigate Approach Stroke, January 1, 1998; 29(1): 137 - 139. [Abstract] [Full Text] [PDF]
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S. K. Brakken, D. Russell, R. Brucher, M. Abdelnoor, and J. L. Svennevig Cerebral Microembolic Signals During Cardiopulmonary Bypass Surgery : Frequency, Time of Occurrence, and Association With Patient and Surgical Characteristics Stroke, October 1, 1997; 28(10): 1988 - 1992. [Abstract] [Full Text]
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S J Mitchell, T Willcox, and D F Gorman Bubble generation and venous air filtration by hard-shell venous reservoirs: a comparative study Perfusion, September 1, 1997; 12(5): 325 - 333. [Abstract] [PDF]
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D. Barbut, F.-S. F. Yao, Y.-W. Lo, R. Silverman, D. N. Hager, R. R. Trifiletti, and J. P. Gold Determination of Size of Aortic Emboli and Embolic Load During Coronary Artery Bypass Grafting Ann. Thorac. Surg., May 1, 1997; 63(5): 1262 - 1267. [Abstract] [Full Text]
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D. Barbut, Y.-W. Lo, J. P. Gold, R. R. Trifiletti, F. S. Frank Yao, D. N. Hager, R. B. Hinton, and O. W. Isom Impact of Embolization During Coronary Artery Bypass Grafting on Outcome and Length of Stay Ann. Thorac. Surg., April 1, 1997; 63(4): 998 - 1002. [Abstract] [Full Text]
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J Johnson and J B Desai Fingertip temperature during cardiopulmonary bypass Perfusion, March 1, 1997; 12(2): 120 - 126. [Abstract] [PDF]
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J. P. Slater, E. A. Rose, H. R. Levin, O. H. Frazier, J. K. Roberts, A. D. Weinberg, and M. C. Oz Low Thromboembolic Risk Without Anticoagulation Using Advanced-Design Left Ventricular Assist Devices Ann. Thorac. Surg., November 1, 1996; 62(5): 1321 - 1327. [Abstract] [Full Text]
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C. T. Mora, M. B. Henson, W. S. Weintraub, J. M. Murkin, T. D. Martin, J. M. Craver, J. P. Gott, and R. A. Guyton THE EFFECT OF TEMPERATURE MANAGEMENT DURING CARDIOPULMONARY BYPASS ON NEUROLOGIC AND NEUROPSYCHOLOGIC OUTCOMES IN PATIENTS UNDERGOING CORONARY REVASCULARIZATION J. Thorac. Cardiovasc. Surg., August 1, 1996; 112(2): 514 - 522. [Abstract] [Full Text]
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D. A. Stump, A. T. Rogers, and J. W. Hammon Neurobehavioral Tests Are Monitoring Tools Used to Improve Cardiac Surgery Outcome Ann. Thorac. Surg., May 1, 1996; 61(5): 1295 - 1296. [Full Text]
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D. Barbut, F.S. Yao, D.N. Hager, P. Kavanaugh, R.R. Trifiletti, and J.P. Gold Comparison of Transcranial Doppler Ultrasonography and Transesophageal Echocardiography to Monitor Emboli During Coronary Artery Bypass Surgery Stroke, January 1, 1996; 27(1): 87 - 90. [Abstract] [Full Text]
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M. Kurusz, B. D Butler, J. Katz, and V. R Conti Air embolism during cardiopulmonary bypass Perfusion, November 1, 1995; 10(6): 361 - 391. [PDF]
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M. E. Lee Microembolization during coronary artery bypass grafting J. Thorac. Cardiovasc. Surg., October 1, 1995; 110(4): 1153 - 1153. [Full Text]
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