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(Stroke. 1996;27:87-90.)
© 1996 American Heart Association, Inc.


Articles

Comparison of Transcranial Doppler Ultrasonography and Transesophageal Echocardiography to Monitor Emboli During Coronary Artery Bypass Surgery

D. Barbut, MD, MRCP; F.S. Yao, MD; D.N. Hager, BA; P. Kavanaugh, MBA; R.R. Trifiletti, MD, PhD J.P. Gold, MD

From the Departments of Neurology (D.B., P.K., R.T., D.H.), Cardiothoracic Anesthesia (F.Y.), and Cardiothoracic Surgery (J.G.), Cornell University Medical College, New York, NY.

Correspondence to Denise Barbut, MD, MRCP, Starr-607, 520 E 70th St, New York, NY 10021.


*    Abstract
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*Abstract
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Background and Purpose Transcranial Doppler ultrasonography (TCD) is the standard technique for monitoring emboli in the cerebral circulation. Embolic signals have been detected with the use of this technique in most patients undergoing coronary artery bypass surgery. We previously reported that the majority of emboli are detected after release of aortic cross-clamps and partial occlusion clamps. In this study we compare the intraoperative use of TCD with transesophageal echocardiography (TEE) to monitor cerebral emboli.

Methods We simultaneously monitored 20 patients undergoing coronary bypass surgery with TCD and TEE. All patients also underwent routine TEE examination of the aorta.

Results Embolic signals were detected in all patients by both techniques. Mean total number of emboli was 535±109 by TEE compared with 133±28 by TCD. We found correlation between numbers of emboli detected by the two techniques at clamp placement and release (r=.65, P=.002). Clamp placement and release accounted for 84% of all emboli by TEE and 83% by TCD. By TEE, large, highly echogenic particles were detected after clamp release compared with small, barely echo-dense particles at the onset of bypass. No such distinction was apparent by TCD. We found correlation between severity of aortic atheroma and both TEE- (P=.003) and TCD-detected (P=.009) emboli.

Conclusions TEE and TCD can both be used to continuously monitor emboli during coronary artery bypass surgery. However, TEE is invasive and justified only if it is being performed for intraoperative assessment of aortic atheromatosis or cardiac function.


Key Words: aorta • bypass surgery • echocardiography • embolism


*    Introduction
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Coronary artery bypass surgery is an effective treatment for patients with multivessel and left main coronary artery disease. However, it is complicated by stroke in 4.7% to 5.2% of cases1 2 3 4 and by cognitive impairment in up to 30% of cases.5 6 Cerebral emboli have been detected intraoperatively with the use of transcranial Doppler ultrasonography (TCD),7 8 9 10 and a correlation between numbers of emboli and neuropsychological outcome has been reported.10 11 We previously showed that a majority of emboli occur after release of aortic clamps.12 Embolic signals (ES) have also been detected intraoperatively in the descending aorta with the use of a TCD probe.13

In this study we monitored 20 patients intraoperatively using TCD and transesophageal echocardiography (TEE) with the goal of comparing the two techniques for detection of emboli.


*    Subjects and Methods
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*Subjects and Methods
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Patient Selection
We monitored 20 patients undergoing elective isolated coronary artery bypass using TCD and TEE. The protocol was approved by our institutional review board, and participating patients gave signed informed consent. Standard TEE was performed in all patients.

Anesthesia
Morphine and lorazepam or midazolam served as premedication, and thiopental, fentanyl, and pancuronium were used for induction. Anesthesia before and after bypass was maintained with additional boluses of fentanyl and midazolam.

Cardiopulmonary Bypass
We used membrane oxygenators in conjunction with nonpulsatile centrifugal pumps. A 40-µm Pall filter was incorporated into the arterial line. Bypass was initiated at flows of 2.4 L/min per square meter at a body temperature of 37.5°C and reduced to 1.6 L/min per square meter at 28°C. We regulated systemic blood pressure pharmacologically to maintain mean pressures between 50 and 80 mm Hg. Surgical staff members were blinded to TCD and TEE findings during the operative procedure.

Standard TEE
We performed biplanar or monoplanar TEE on all patients after induction of general anesthesia and endotracheal intubation and again at the end of the surgical procedure. A 5-MHz TEE probe (Acuson) and an Acuson 128 XP system were used. All studies were recorded on standard VHS videotape and subsequently interpreted. We assessed the severity of ascending, arch, and descending aortic atheroma individually and graded each segment as follows: grade I, normal to mild intimal thickening; grade II, severe intimal thickening; grade III, atheroma protruding less than 5 mm into the lumen; grade IV, atheroma protruding 5 mm or more into the lumen; and grade V, atheroma with a mobile component.14

Intraoperative TCD Monitoring
We monitored the middle cerebral artery of patients from aortic cannulation to bypass discontinuation using a 2-MHz pulsed-wave TCD probe (Medasonics-CDS) placed on the patient's temple at a depth of 4.5 to 6.0 cm. ES were defined as high-amplitude, unidirectional, transient signals less than 0.1 second in duration and associated with a characteristic chirping sound. We recorded the timing of all major events and numbers of ES occurring within 4 minutes of the following events: aortic cannulation, inception and termination of bypass, aortic cross clamping, and aortic cross-clamp release.

Intraoperative TEE Monitoring
After completion of the aortic examination, we positioned the probe in transverse plane at the level of the aortic arch, just before the origins of the left subclavian artery, for continuous recording from aortic cannulation until 5 to 10 minutes after termination of bypass. Monitoring was started after aortic cannulation in 11 patients. Other specific events were occasionally missed because of "freezing" of the TEE equipment (TableDown). We recorded data on standard VHS videotape for subsequent analysis by two examiners. ES were defined as echogenic intraluminal signals not present in the same position on consecutive frames.


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Table 1. Comparison of Embolic Signals Detected by Transcranial Doppler Ultrasonography and Transesophageal Echocardiography

The recorded images were displayed with the use of the Data Translation DT 2867 frame grabber. Since each particle appears on several consecutive frames, only three frames with large numbers of emboli were selected of 30 frames for each second and numbers of particles in each frame counted. In this way we avoided recounting the same particle more than once. The means of these three frames were obtained for each of the first 5 seconds after the event and were summed. Only the first of each 5-second interval thereafter to a maximum of 240 seconds or cessation of emboli was similarly counted. This mean for the first of each 5-second period was then multiplied by the number of seconds in the interval to arrive at the maximum number for the 240 seconds. Emboli occurring outside these 4-minute time frames were classified as interim signals.

Statistical Analysis
Statistical analyses were performed on a Gateway P5-90 computer with the use of S-PLUS for Windows. Statistical comparison between groups and significance of correlations were performed with the use of ANOVA.

We performed multivariate linear modeling for the clamp-related numbers of emboli by TEE or TCD using the grade of severity of atheroma (as defined above) in the ascending aorta, aortic arch, and descending aorta as predictors. The "best" model was selected on the basis of minimization of Aikaike information criteria and was used to compute the "expected" number of emboli for a given patient and to test correlation with observed values.


*    Results
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*Results
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We detected ES intraoperatively by TCD and TEE in all 20 patients monitored (15 men, 5 women; mean age, 69 years [range, 50 to 78 years]). The mean number of emboli for the entire procedure was 535±109 by TEE compared with only 133±28 for TCD, although counting methods are not directly comparable. The largest number of ES occurred in the 4-minute period after aortic cross-clamp release (903 for TEE, 279 for TCD). Both techniques detected the majority of emboli after seven specific operative events: aortic cross clamp and partial occlusion clamping and release, bypass onset and discontinuation, and aortic cannulation. ES were distributed unevenly across these specific time points (Fig 1Down) (two-way ANOVA: TEE, P=.00014; TCD, P=.000009). Aortic cross clamp release accounted for 42% and 41% of the total number of emboli for TEE and TCD, respectively. Partial occlusion clamp release accounted for another 24% by TEE and 21% by TCD. Combined aortic cross-clamp and partial occlusion clamp placement and release accounted for 84% of all ES by TEE and 83% by TCD. Numbers of ES detected by the two techniques correlated for aortic cross-clamp placement (r=.66, P=.003) and release (r=.70, P=.0005), partial occlusion clamp placement (r=.77, P=.0008) and release (r=.88, P=1.86x10-6), and bypass discontinuation (r=.98, P=8.4x10-14) (Fig 1Down).



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Figure 1. Bar graph shows distribution of embolic signals (ES) across specific operative events, including aortic cannulation (AC+), bypass on (BP+), aortic cross clamp on (CX+), aortic cross clamp release (CX-), aortic partial occlusion clamp on (POC+), aortic partial occlusion clamp release (POC-), and bypass off (BP-). TCD indicates transcranial Doppler ultrasonography; TEE, transesophageal echocardiography.

The largest numbers of ES per frame were detected during the first 10 seconds after clamp release (mean, 13) and tapered down to 0 to 5 ES per frame by 20 seconds (mean, 1.57). A second smaller flurry was apparent between 150 and 200 seconds.

The difference between signals generated by the onset of bypass and clamp release was easily and consistently noticeable by TEE. Intensely echogenic, large particles followed clamp release (Fig 2Down), whereas those detected at the onset of bypass were poorly echogenic, less distinct, and smaller. TCD-detected ES generated by these two events were not distinguishable on the basis of amplitude or duration.



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Figure 2. Transesophageal echocardiographic image shows transverse section of aortic arch (Ao Ar) at clamp release (AXC OFF). Arrows indicate intraluminal emboli.

Mobile atheromatous plaque (grade V) was present in four patients, mostly in the descending aorta. Severity of TEE-detected aortic atheroma correlated with numbers of TEE- and TCD-detected emboli (Fig 3Down). Atheroma severity in all three aortic segments combined significantly predicted numbers of ES by TCD (r=.63, P=.009) and TEE (r=.82, P=.003). Severity of atheroma in the aortic arch alone also had predictive value, particularly for TCD (r=.57, P=.009).



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Figure 3. Scatterplot shows value of aortic atheroma in predicting number of emboli. TCD indicates transcranial Doppler ultrasonography; TEE, transesophageal echocardiography.


*    Discussion
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
*Discussion
down arrowReferences
 
TCD is the standard technique for monitoring emboli during coronary artery bypass surgery.7 8 9 10 11 With this technique, emboli have been detected in most patients.7 11 12 We have previously shown that the bulk of embolization occurs after aortic cross clamp and partial occlusion clamp release, which suggests an association with the severity of aortic atheroma.12 The distribution of emboli in relation to specific operative events is very similar with TEE monitoring. In accordance with previous results,12 aortic cross clamp and partial occlusion clamp release accounted for 66% of TEE-detected and 62% of TCD-detected emboli. The numbers of emboli detected by TEE were substantially higher than with TCD, reflecting the fact that only a fraction of the aortic emboli enter the cerebral circulation. Rates of embolization on a second-by-second basis after clamp release are better delineated with TEE monitoring. Analysis of sequential frames reveals that the vast majority of emboli occur within the first 20 seconds after clamp release.

The difference between the large, intense emboli after clamp release and the small, indistinct particles seen at onset of bypass is quite striking with TEE. The significance of this difference in terms of pathological material is unclear. In vitro, the size of injected particles has been shown to correlate with TCD-detected signal amplitude and duration.15 Neither TCD nor TEE, however, can differentiate between particles of differing constitution in vivo. The flurry of whirling intra-aortic echo densities seen on TEE at the onset of bypass has no consistent counterpart at the level of the middle cerebral artery by TCD. It is our impression that they consist of gaseous microbubbles formed by turbulent flow, most of which are too small to detect by the time they reach the middle cerebral artery, or they are merely of variable echogenicity caused by mixing crystalloid priming solution and blood. The highly echo-dense particles detected by TEE after clamp release are accompanied by substantial numbers of high-amplitude ES on TCD. Preliminary results suggest that numbers of ES correlate with severity of aortic atheroma.16 17 This has led us to believe that these signals mostly represent atheromatous debris rather than gaseous microbubbles trapped behind the clamps. In this study we found a strong association between numbers of emboli and severity of aortic disease by both TEE and TCD. Taken individually, only the aortic arch significantly predicted numbers of emboli. The biologically most plausible association would be correlation with ascending segment disease and proximal aortic arch, since emboli originating from the distal arch or descending segment cannot enter the cerebral circulation. Unfortunately, the ascending segment and proximal arch are the least well visualized parts of the aorta by TEE, even with a biplanar probe. Atheromatous plaque in this segment is frequently missed unless the epiaortic probe is used.18 Marschall et al19 has shown a compelling association between aortic arch atheroma and stroke after bypass surgery; emboli monitoring was not performed. Much larger patient numbers are needed to establish the exact relationship between aortic atheroma, numbers of emboli, and more importantly, neurological and cognitive outcome.

TEE is increasingly being used during coronary artery bypass surgery to assess the severity of aortic atheroma. Positioning the probe at the level of the aortic arch to monitor intraluminal emboli after completion of the aortic examination is technically quite simple. The technique enables more detailed analysis of embolization after specific operative events and may yield more information regarding size and constitution of emboli. Unlike TCD, TEE is an invasive procedure, and its use cannot be justified unless examinations of the heart and aorta are being performed. The TEE equipment is considerably more expensive and bulkier than TCD, and the review of tapes is labor intensive. A fully automated emboli counting system would have to be developed to make it a useful adjunct to standard intraoperative TEE.

Received June 16, 1995; revision received September 21, 1995; accepted October 4, 1995.


*    References
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
up arrowDiscussion
*References
 
1. Shaw PJ, Bates D, Cartlidge NEF, Heaviside D, Julian DG, Shaw SA. Early neurological complications of coronary artery bypass surgery. Br Med J. 1985;291:1384-1387.

2. Reed G, Singer D, Picard E. Stroke following coronary artery bypass grafting. N Engl J Med. 1988;319:1246-1250. [Abstract]

3. Turnipseed WD, Berkoff HA, Belzer FO. Postoperative stroke in cardiac and peripheral vascular disease. Ann Surg. 1980;192:365-368. [Medline] [Order article via Infotrieve]

4. Breuer AC, Furlan AJ, Manson MR, Lederman RJ, Loop FD, Cosgrove DM, Greenstreet RL, Estafanous FG. Central nervous system complications of coronary artery bypass graft surgery: prospective analysis of 421 patients. Stroke. 1983;14:682-687. [Abstract/Free Full Text]

5. Smith PLC, Treasure T, Newman SP, Joseph P, Ell P, Schneidau A, Harrison M. Cerebral consequences of cardiopulmonary bypass. Lancet. 1986;1:823-825. [Medline] [Order article via Infotrieve]

6. Savageau JA, Stanton BA, Jenkins CD, Frater WM. Neuropsychological function following elective cardiac operation: a six month reassessment. J Thorac Cardiovasc Surg. 1982;84:595-600. [Abstract]

7. Padayachee TS, Parsons S, Theobold R, Linley J, Gosling RG, Deverall PB. The detection of microemboli in the middle cerebral artery during cardiopulmonary bypass: a transcranial Doppler ultrasound investigation using membrane and bubble oxygenators. Ann Thorac Surg. 1987;44:298-302. [Abstract]

8. Bunegin L, Mitzel HC, Wahl D, Albin MD. Incidence and volume of air emboli in the middle cerebral artery during cardiopulmonary bypass. In: Program and abstracts of The Brain and Cardiac Surgery, September 23-26, 1994; Key West, Fla. Abstract.

9. Lieh H, Roach GW, Kanchuger M, Marschall K, Mangano DT. Correlation between the severity of atherosclerosis of the ascending aorta and cerebral emboli during coronary artery bypass graft surgery. In: Program and abstracts of The Brain and Cardiac Surgery, September 23-26, 1994; Key West, Fla. Abstract.

10. Pugsley W, Klinger L, Paschalis C, Treasure T, Harrison M, Newman S. The impact of microemboli during cardiopulmonary bypass on neuropsychological functioning. Stroke. 1994;25:1393-1399. [Abstract]

11. Clark RE, Brillman J, Davis DA, Lovell MR, Price TRP, Magovern GJ. Microemboli during coronary artery bypass grafting: genesis and effect on outcome. J Thorac Cardiovasc Surg. 1995;109:249-258. [Abstract/Free Full Text]

12. Barbut D, Hinton RB, Szatrowski TP, Hartman GS, Bruefach M, Williams-Russo P, Charlson ME, Gold JP. Cerebral emboli detected during bypass surgery are associated with clamp removal. Stroke. 1994;25:2398-2402. [Abstract]

13. Russel D, Madden KP, Clark WM, Sandset PM, Zivin JA. Detection of arterial emboli using Doppler ultrasound in rabbits. Stroke. 1991;22:253-258. [Abstract/Free Full Text]

14. Katz ES, Tunick PA, Rusinek H, Ribakove G, Spencer FC, Kronzon I. Protruding aortic atheromas predict stroke in elderly patients undergoing cardiopulmonary bypass: experience with intraoperative transesophageal echocardiography. J Am Coll Cardiol. 1992;20:70-77. [Abstract]

15. Markus HS, Brown MM. Differentiation between different pathological cerebral embolic materials using transcranial Doppler in an in vitro model. Stroke. 1993;24:1-5. [Abstract/Free Full Text]

16. Barbut D, Hinton RB, Hartman GS, Bruefach M, Hahn R, Szatrowski TP, Charlson ME, Gold JP. Number of emboli detected by TCD during CABG is related to aortic atheroma as assessed by TEE. In: Program and abstracts of The Brain and Cardiac Surgery, September 23-26, 1994; Key West, Fla. Abstract.

17. Lieh H, Roach GW, Kanchuger M, Marschall K, Mangano DT. Correlation between the severity of atherosclerosis of the ascending aorta and cerebral emboli during coronary artery bypass graft surgery. In: Program and abstracts of The Brain and Cardiac Surgery, September 23-26, 1994; Key West, Fla. Abstract.

18. Konstadt SN, Reich DL, Quintana C, Levy M. The ascending aorta: how much does transesophageal echocardiography see? Anesth Analg. 1994;78:240-244. [Medline] [Order article via Infotrieve]

19. Marschall K, Kanchuger M, Kessler K, Grossi E, Yarmush L, Roggen S, Tissot M, Paglia S, Nacht A, Shrem S, Turndorf H. Superiority of transesophageal echocardiography in detecting aortic arch atheromatous disease: identification of patients at increased risk of stroke during cardiac surgery. J Cardiothorac Vasc Anesth. 1994;8:5-13.[Medline] [Order article via Infotrieve]




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