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Ann Thorac Surg 1997;63:1262-1267
© 1997 The Society of Thoracic Surgeons

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Original Article: Cardiovascular

Determination of Size of Aortic Emboli and Embolic Load During Coronary Artery Bypass Grafting

Departments of Neurology, Cardiothoracic Anesthesiology, Ophthalmology and Cardiothoracic Surgery, Cornell University Medical College, New York, New York

Accepted for publication November 7, 1996.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
Background. Embolic signals have been detected within both the aortic lumen and the intracranial vasculature during coronary artery bypass grafting. Total numbers of these emboli have been reported. The present study examined the size of individual emboli and the total volume of embolization.

Methods. Using transesophageal echocardiography, we continuously monitored the aortic lumen of 10 patients undergoing isolated coronary artery bypass grafting. We manually analyzed 720,000 individual echo frames over a 4-minute period after the release of aortic clamps to track and to calculate the volume of 657 individual particles. The embolic load for the entire procedure was calculated from mean volume based on analysis of 1,508 particles. We simultaneously monitored the middle cerebral artery using transcranial Doppler ultrasonography and compared numbers of emboli detected by the two techniques.

Results. Particle diameter ranged from 0.3 to 2.9 mm (mean, 0.8 mm), and particle volume from 0.01 to 12.5 mm³ (mean, 0.8 mm³). Twenty-eight percent of particles measured 1 mm or more, 44% measured 0.6 to 1.0 mm, and only 27% measured 0.6 mm or less in diameter. Aortic embolic load for the procedure ranged from 0.6 cm³ to 11.2 cm³ (mean, 3.7 cm³). Estimated cerebral embolic load for the procedure ranged from 60 to 510 mm³ (mean, 276 mm³). The fraction of aortic emboli entering the cerebral circulation was very variable (3.9% to 18.1%). Seventy-six percent of the embolic volume after the release of clamps occurred over a 20-second period. Only 1 patient was encephalopathic perioperatively. This patient had the largest estimated cerebral embolic load (510 mm³) and the second largest aortic embolic load (8.4 cm³).

Conclusions. We determined the size of individual intraaortic embolic particles and the total volume of embolization during coronary artery bypass grafting, and found the proportion entering the cerebral circulation to be very variable. The constitution of these particles and the neurologic impairment resulting from such embolization remains to be determined.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
Neurologic morbidity is the leading complication after coronary artery bypass grafting [1]. Stroke complicates the procedure in 4.7% to 5.2% of cases, and cognitive impairment occurs in up to 30% of patients [1–3]. The etiology of this dysfunction is multifactorial and includes cerebral hypoperfusion [4] as well as embolization [5–8].

Using Doppler ultrasonography, embolic signals were first noted in the extracorporeal circuit of patients undergoing coronary bypass [9]. With the advent of transcranial Doppler ultrasonography (TCD), embolic signals have been detected within the middle cerebral artery (MCA) of a majority of these patients intraoperatively [8–12]. An association between emboli and specific surgical events such as aortic cannulation, the onset of bypass [8], and the release of aortic clamps has been reported [7, 10]. Several authors have hypothesized that the emboli are gaseous and have shown a reduction in numbers with the use of membrane rather than bubble oxygenators [8] and arterial filters [12]. An association between numbers of emboli and postoperative neuropsychological dysfunction has recently been reported as well [11, 13].

In animal models, Doppler signal analysis has provided some information about embolus size and constitution [14, 15]. Particle size has been shown to correlate with signal duration and intensity [14–16], and air has been shown to produce the most intense signals [15]. However, in vivo, the size and constitution of embolic material cannot be determined by analyzing Doppler signals with existing technology.

Studies using transesophageal echocardiography (TEE) have recently detected embolic signals within the aortic lumen during coronary bypass [17] and have shown them to correlate with emboli detected intracranially using TCD [18]. In this study, we have used TEE and TCD to determine particle size and volume of embolization.

	Material and Methods

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Patient Selection
Twelve patients undergoing primary, elective, isolated coronary artery bypass were monitored using TEE. Two patients were excluded because the probe was inadequately positioned and the TEE image eccentric. The protocol was approved by our institutional review board, and participating patients gave informed consent. Mean age was 73 years, with a range of 60 to 86 years. Eight patients were male, and none had prior symptomatic cerebrovascular disease.

	Anesthesia

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Morphine (0.1 mg/kg) and lorazepam (0.04 mg/kg) or midazolam (0.05 mg/kg) served as premedication, and thiopental (1 to 2 mg/kg), fentanyl (10 µg/kg), and pancuronium (0.1 mg/kg) were used for anesthetic induction. Anesthesia before and after bypass was maintained with additional boluses of fentanyl (5 µg/kg) and midazolam (1 to 2 mg) as necessary.

	Cardiopulmonary Bypass

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Membrane oxygenators in conjunction with nonpulsatile centrifugal pumps provided cardiopulmonary bypass. A 40-µm blood filter (Pall Biomedical Products Corp, East Hills, NY) was incorporated into the arterial line. The bypass circuit was primed with 1.5 L of crystalloid solution, and bypass itself was initiated after full systemic heparinization at flows of 2.4 L•min^-1•m^-2 at body temperature of 37°C and reduced to 1.6 L•min^-1•m^-2 at 28°C. We regulated systemic blood pressure pharmacologically using fentanyl, midazolam, sodium nitroprusside, or phenylephrine to maintain mean pressures between 50 and 80 mm Hg. The alpha-stat acid-base management was used during hypothermic intervals.

	Surgical Technique

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
All patients underwent conventional multivessel coronary artery revascularization with the above-described bypass techniques in conjunction with standard aortic cross-clamping and hypothermic, hyperkalemic antegrade and retrograde intermittent cardioplegia. Distal anastomoses were constructed first under protection of aortic cross-clamping and cold cardioplegic arrest, supplemented by topical iced saline irrigation or iced slush. Proximal anastomoses were constructed during a single application of a partial occlusion vascular clamp. Gravity venting was used at the aortic root. Surgical staff were unaware of TEE and TCD findings during the operative procedure.

	Intraoperative Transcranial Doppler Monitoring

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
Seven of 10 patients were monitored continuously from aortic cannulation to bypass discontinuation using a 2-MHz pulsed-wave Medasonics CDS TCD probe (Medasonics, Fremont, CA). Embolic signals occurring within four minutes of clamp release and total numbers for the procedure were recorded as previously described [18].

	Intraoperative Transesophageal Echocardiographic Monitoring

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
We performed TEE monitoring on all patients after induction of general anesthesia. A 5-MHz TEE probe (Acuson, Mountain View, CA) with an aperture of 10 mm and an Acuson 128 X P system were used. All studies were recorded on a VHS videotape and subsequently interpreted. The probe was focused in the transverse plane at the level of the aortic arch, just before the takeoff of the left subclavian artery, and maintained in that position for continuous recording, from before aortic cannulation until 5 to 10 minutes after termination of bypass. We defined emboli as echogenic intraluminal signals of variable size that were not present in the same position on consecutive video frames. The timing of major surgical events including clamping and clamp release were recorded. Instrumental settings were similarly standardized for comparison among all operations.

	Neurologic Assessment

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Neurologic history was obtained and patients were examined by one of us blinded to the operative data (D.B.) at day 2 or 3 postoperatively and again before discharge. Encephalopathy was defined as altered sensorium not attributable to metabolic factors such as medication or metabolic alteration and included delirium, confusion, agitation, and hallucinations.

	Image Analysis

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A 4-minute period after aortic cross-clamp [7] or partial occlusion clamp [3] release was analyzed for determination of individual and mean particle sizes. A computer with a DT 2867 image-processing board was used to "frame-grab" and store individual video frames. The frame with the largest number of emboli was selected out of 30 frames for each second starting with the appearance of the first embolus after clamp release.

This was repeated for each of the first 5 subsequent seconds and for the first second of each 3- or 5-second interval thereafter to a maximum of 240 seconds or cessation of emboli. Each image was thresholded and enhanced (Figs 1, 2), and the number of particles and mean number of pixels per particle in the intraluminal space were determined automatically by the image-analysis software (Global Lab Image, Data Translation, Marlboro, MA; and Microsoft Excel, Redmond, WA). A scaling constant was then used to compute the mean area of particles in square millimeters. From this, the mean particle radii were determined and the mean particle volume computed (1,508 particles over 233 frames). The embolic load for one frame was determined as the product of the number of particles and their mean volume. Each particle is traceable over a mean of four frames or 4/30 (0.133) second. Embolic loading rate, in cubic millimeters per second, was therefore calculated as frame volume divided by 0.133. The embolic load was calculated as the product of embolic loading rate and the duration of the interval. Clamp-related aortic embolic load was calculated as the total volume of particles over a 4-minute period after the release of aortic clamps. Decay rates of embolization after clamp release were calculated by superimposing the frame with the largest numbers of particles for each patient. Individual particle diameters and volumes were also calculated using the same software for categorization by size. The fraction of aortic particles entering the brain was calculated as twice the number of emboli detected in one MCA by TCD and another 20% based on the fact that MCAs carry approximately 80% of total cerebral blood flow. This entire process required an average of 20 hours per patient.

View larger version (52K): [in this window] [in a new window]   Fig 1. . Transesophageal echocardiographic frame showing echogenic signals within aortic lumen. (EMB = embolus.)

View larger version (27K): [in this window] [in a new window]   Fig 2. . Same picture as in Figure 1, but thresholded for analysis. (EMB = same embolus as in Figure 1.)

	Results

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

View larger version (19K): [in this window] [in a new window]   Fig 3. . Embolic particle diameters and their relation to cerebral arterial caliber. (Aa = arteriole; AcA = anterior cerebral artery; ICA = internal cerebral artery; LMV = leptomeningeal vessel; MCA = middle cerebral artery; PCA = posterior cerebral artery.)

View larger version (14K): [in this window] [in a new window]   Fig 4. . Particle volumes.

Rates of embolization as a function of time after clamp release are shown in Figure 5. Mean embolic rate at the time the maximum volume of particles was present was 130 mm³/s, falling by 90% to 13.5 mm³/s within 10 seconds. Seventy-six percent of the total volume of embolization after release of aortic clamps occurred over a 20-second period.

View larger version (13K): [in this window] [in a new window]   Fig 5. . Embolic load as a function of time after release of aortic clamps. (CX- = cross-clamp release; Tmax = time at which maximum volume of particles was present.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
Using TEE, we have determined the volume of individual intraaortic embolic particles in patients undergoing coronary artery bypass grafting, and have estimated both aortic and cerebral embolic loads. All particles, the largest of which was 2.8 mm in diameter, are small enough to enter the cerebral circulation, although as seen by simultaneous monitoring with TCD, only a small fraction of intraaortic particles reach the MCA [18]. Assuming particles of all sizes enter the cerebral vasculature in proportion to their presence in the aorta, 28% of the total (those greater than 1 mm in diameter) would be arrested in large-caliber vessels such as the MCA (see Fig 3). Atheromatous particles this size have been recovered from such major cerebral arteries, usually adjacent to territorial infarcts in patients succumbing to coronary bypass operations [19]. Another 44% of particles (0.6 to 1 mm in diameter) would lodge in intermediate-sized arterioles. Only one quarter of the total number of emboli, those less than 0.6 mm, match the internal diameter of terminal cortical arterioles and leptomeningeal vessels.

These findings are inconsistent with pathologic evidence [6, 19–23]. Most atheroemboli are located adjacent to border-zone infarcts within leptomeningeal vessels, which range from 0.01 to 0.6 mm in diameter (mean, 0.1 mm) [19–22]. Focal arteriolar dilatations observed in brains of patients and dogs undergoing cardiopulmonary bypass and thought to represent sites of atheromatous or gaseous embolization rarely measure more than 0.04 mm [32].

Emboli, whether particulate or gaseous, may in fact fragment along their course, embolizing distal to the site of initial stasis. This has previously been suggested by Masuda and associates [19], who found atheroemboli in the artery corresponding to the territorial infarct in only 3 of 6 patients. In the other 3, cholesterol emboli were present only within the terminal arterioles distal to the main vascular supply. Gaseous emboli, in addition to fragmenting, diminish in size through resorption. A gaseous bubble within the aortic lumen is thus likely to be considerably smaller intracranially. This may explain why border-zone infarcts, common accompaniments of microvascular embolic occlusions, are a more typical finding than territorial infarcts in patients succumbing to coronary operations [19, 21]. Technical limitations may also have led us to underestimate the number of small particles. The resolution of a phased-array, 5-MHz TEE transducer with an aperture of 1 cm is 0.3 mm, consistent with the smallest particle detected (0.3 mm). Smaller particles may have been missed altogether, or their size overestimated.

Embolic load, the total volume of material reaching the brain, has not been measured in vivo. In animals, the embolic load required to obstruct a given proportion of the cerebral microvasculature has been established. Thus, ten thousand 15-µm glass microspheres per gram of brain tissue are known to occlude 0.25% of dog cerebral capillary bed [24], and in dogs subjected to cardiopulmonary bypass, Moody and associates [6] estimated 2,600 SCADs per gram of brain tissue to be equivalent to a load of microspheres that would obstruct 0.065% of the capillary bed. Among patients succumbing to coronary bypass, Moody and associates [6] estimated the largest number of small capillary and arteriolar dilatations (SCADs) to be 15.3 million. Assuming mean SCAD diameter to be 20 µm, the total embolic volume in this patient would be 0.5 cm³. A second patient with mean SCAD diameter of 20 µm was estimated to have an embolic load of 0.05 cm³ (Moody DM, personal communication). In our study, the largest number of aortic particles was 16,590 and the total volume 8.4 cm³ (patient 1). The embolic load to the brain, however, was only 0.5 cm³, the same order of magnitude as the embolic load derived from analysis of SCADs in Moody and associates' first patient.

The embolic load required to produce neurologic impairment in humans is unknown. In dogs, ten thousand 15-µm glass microspheres per gram of brain tissue cause no visible neurologic damage, whereas much smaller numbers of spheres measuring 50 µm clearly do [24]. Particle size is as important a determinant of neurologic impairment as is total embolic load. In this study, marked and prolonged postoperative encephalopathy was evident in 1 patient only (patient 1). In addition to having the highest cerebral embolic load (0.5 cm³), this patient also had the largest number of emboli, and three of the four largest particles detected. Larger studies may establish the significance of this association.

Rate of embolization, like particle size and numbers, may influence the neurologic impact of a given embolic load. Nearly half the total number of emboli follow the release of aortic cross-clamps [10], and 75% of these emboli were detected over a 20-second period. Cerebrovascular compensation may be greater when a given embolic load is delivered slowly.

The constitution of intraaortic particles is unclear. Analyzing Doppler characteristics of different materials in animal models, several authors have found that air and fat produce Doppler signals of greater intensity than atheromatous particles or platelet thrombi of similar size [14, 15]. The nature of the embolic materials in vivo, however, cannot be determined with any degree of certainty by analyzing Doppler characteristics.

Neurologic impairment after embolization is determined not only by embolic material characteristics but also by the quality of brain parenchyma and vascular reserve capacity. An embolic onslaught may thus cause multiple infarcts in an elderly patient with atheropathy with little vascular and neuronal reserve, and have no visible impact, clinically or radiologically, in a younger person with healthy vessels. In the latter case, a reduction in vascular reserve would only be demonstrable pathologically or at a subsequent cerebral insult.

Despite methodologic limitations, this study demonstrates the possibility of estimating embolic volume in vivo in patients undergoing coronary artery bypass grafting. Although this method is extremely laborious and time-consuming, refinements will hopefully lead to greater precision in future studies and ease analyses, and technologic advances will help determine particle constitution. Large numbers of patients need to be studied to determine the neurologic consequences of such embolization.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Anesthesia Cardiopulmonary Bypass Surgical Technique Intraoperative Transcranial... Intraoperative Transesophageal... Neurologic Assessment Image Analysis Results Comment Acknowledgments References

 
Supported in part by a grant from the Raeburn Foundation. Additional support from Samuel and Ella Scher.

	Footnotes

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Address reprint requests to Dr Barbut, Starr 607, 520 E 70 St, New York, NY 10021.

	References

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