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Ann Thorac Surg 1995;59:1300-1303
© 1995 The Society of Thoracic Surgeons

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Symposium: Conference on Cardiopulmonary Bypass

Macroemboli and Microemboli During Cardiopulmonary Bypass

Cardiothoracic Unit, Guy's Hospital, London, England

Abstract

Macroscopic and microscopic emboli of gas, biologic aggregates, and inorganic debris can occur during cardiac operations with cardiopulmonary bypass and may result in end-organ ischemia. In the current era pump-generated embolism is a diminishing cause of perioperative neurologic injury, which now appears to be related mostly to atheroembolism from manipulation of the atherosclerotic ascending aorta, and presents a continuing technical challenge to the surgeon.

Systemic embolism affecting the brain is a recognized complication both of cardiopulmonary bypass (CPB) and of the underlying cardiovascular diseases that require CPB for their surgical treatment. This review considers methods of detecting embolic phenomena related to cardiac surgery and examines the relationship between cerebrovascular embolism and central nervous system (CNS) dysfunction.

Macroemboli and Microemboli

We can divide emboli into macro and micro categories according to size, the former occluding flow in arteries 200 µm or greater in diameter and the latter, in smaller arteries, arterioles, and capillaries. Such a distinction may reflect different clinical manifestations: a single macroembolus might result in hemiplegia, but a solitary microembolus is unlikely to have a noticeable effect except in very susceptible tissue such as the retina. Clinical effects of microemboli should arise only when these emboli are numerous and can be expected to present a diffuse pattern of CNS injury rather than a focal deficit. Except in the context of perfusion accidents, macroemboli are unlikely to arise from the extracorporeal circuit but rather from surgical manipulation of the heart and aorta. Distinction on the basis of size is no guide to the composition of emboli.

Types of Emboli and Tissue Effects

Gas Bubbles
Gaseous emboli consist of air or anesthetic gas, particularly nitrous oxide. Air is inevitably introduced into the left side of the heart during aortic or mitral valve operations and can also reach the aorta from the bypass circuit, especially when a bubble oxygenator is used. The gas in a bubble flowing in the bloodstream is in dynamic equilibrium with the same gas dissolved in the plasma, and a bubble will therefore grow or shrink according to the partial pressure of the gas in solution, which is largely dependent on temperature. Thus, bubbles are more likely to form and grow during the rewarming phase of CPB. Because the pressure in a bubble tends to force the gas into solution and is inversely proportional to the radius, small bubbles are inherently unstable in blood and collapse when less than 10 µm in diameter [1]. Similar considerations apply when a bubble embolus occludes a blood vessel; dispersal seems to occur rapidly, although endothelial injury and end-organ damage may persist [2].

Biologic Aggregates
Emboli of biologic aggregates including thrombus, platelet aggregates, and fat are also in a dynamic state, with the blood allowing growth or dispersal according to prevailing conditions. Dispersal is dependent on biochemical as well as physical mechanisms and may be slower than for bubbles, although experimental microvascular occlusions with platelet aggregates showed reperfusion within 20 minutes [3]. Platelets contain vasoactive substances and can also cause endothelial injury. Thrombi can arise from within the heart, most commonly from the left atrial appendage or a left ventricular aneurysm, or from the CPB circuit if heparinization is inadequate. Although heparin sodium inhibits coagulation, no pharmacologic agent is normally given to inhibit contact activation of platelets by the extensive foreign surfaces presented to the blood in artificial oxygenators, and platelet activation and aggregation during CPB are well documented. Heparin may contribute to fat embolism by stimulating endothelial lipoprotein lipase, and denaturation of proteins during CPB may also precipitate plasma lipids, but the principal source of cholesterol embolism is probably from large-vessel atherosclerotic plaques [4].

Inorganic Debris
Embolization of fragments of polyvinyl chloride tubing exposed to the roller pump and of silicone antifoam have been described, but current manufacturing standards have substantially reduced these hazards. Many studies of experimental microembolism have used glass and latex microspheres of known size, and the tissue effects of these artificial microemboli are consequently well documented [5]. Solid emboli can migrate a short distance downstream after initial impact and occlusion of a vessel but cannot disperse.

Detection and Quantification

A number of different methodologies have evolved to detect and quantify embolism in relation to CPB. These can be divided into in vivo methods and in vitro methods. In vitro methods include processing of blood samples and end-organ histopathology; in vivo methods use either ultrasound or observation and imaging of the microcirculation.

Blood Sampling
Studies by Swank [6] in the 1950s on the filtration of stored blood in relation to blood transfusion led to the development of the screen filtration method for the detection of microaggregates in blood. The pressure required to force blood at a given flow rate through a screen filter of given pore size was measured. Although this was not a direct method for the detection of microemboli, the residual debris on the filter was found to consist of microaggregates. The Coulter counter provides another effective method for the detection and sizing of particles in blood, although it cannot distinguish solid particles from microaggregates and cannot detect microbubbles [7]. It should be noted that both microaggregates and gaseous microbubbles are inherently unstable entities in the blood and can be altered by foreign surfaces; hence, any manipulation of blood samples for measurement has a high probability of altering such emboli.

Histopathology
In early studies, Hill and colleagues [8, 9] in San Francisco examined the brains of 133 patients who died after an open heart operation. Fat embolism was the most common finding and occurred in nearly all patients. Nonfat emboli, the majority of which were composed of platelets and fibrin, were found in 31% of patients who had cardiac operations but in only 8% of patients who died of cardiac-related causes but did not have a surgical operation. Focal hemorrhages and neuronal degeneration were also reported. Details of the CPB circuits used are unclear, but disk oxygenators and donor whole blood primes were in common use at the time. These findings have not been confirmed in the current era. It is likely that improvements in CPB techniques have virtually eliminated cerebrovascular microembolism on this scale of severity, and these data are now largely historical.

More recent studies [10] have identified platelet-fibrin microaggregates in canine retinal vessels after CPB, and these microaggregates have been associated with microfocal ischemic neuronal injury. Use of a specialized histochemical technique has revealed cerebral arteriolar and capillary lesions after CPB and is the subject of a separate presentation at this symposium by Dr Dixon Moody. More impressive cerebral pathology after CPB has been reported in a recent autopsy study from the Cleveland Clinic [4] in which evidence of atheroembolism was found in 16.3% of brains examined. Careful histopathology still provides evidence of embolic problems in the CNS after cardiac surgical interventions.

Ultrasound
On-line detection of echogenic material in the tubing of the extracorporeal circuit was first reported by Austen and Howry [11] in 1965. This technique was further developed, and to date, three modes of ultrasonic detection have been described. The pulsed-echo mode originally described was found to be poor at detecting material near the walls of the tubing [12]. Ultrasound used in the Doppler mode has greater accuracy but is poor at detecting microaggregates or solid microparticles [13]. Doppler ultrasound has also been used to detect emboli in the carotid arteries [14] and the middle cerebral arteries [15]. Continuous standing-wave (non-Doppler) ultrasound has a very high detection rate for solid microparticles [12].

Ultrasonic methods have the advantage of on-line analysis and generate electronically processed data with an appealing aura of high precision and accurate quantification. This tends to conceal a number of limitations in their application, which are seldom addressed in detail. Although it is technically possible for ultrasonic methods to differentiate between gaseous and solid emboli by spectral analysis, this has not been feasible as an on-line technique [1]. Therefore, in most reports of clinical and experimental studies, such distinctions cannot be made. More importantly, calibration of ultrasound for quantitative studies presents serious difficulties, particularly in blood. Conversion of detected signals into ``counts'' depends on software programming variables, and it is unclear whether an increase in signal amplitude reflects an increase in the number or the size of emboli. Therefore, the number of ``counts'' may not represent the exact number of particles traversing the electronic gate [16, 17]. Further considerations that might introduce quantification errors with ultrasonic detection of gaseous emboli are attenuation of the signal by blood components on their surface, scattering of signals from clusters of bubbles, and shielding of some bubbles by others [18].

Retinal and Other End-Organ Studies
The retina provides an excellent opportunity to study the cerebrovascular microcirculation in vivo. It also provides an ideal model for the study of embolic events because of the absence of arteriolar collaterals and the clear demarcation of ischemic areas. Fundoscopy is an integral part of a neurologic examination and may reveal ischemic retinal lesions. Small retinal infarcts have been reported to occur in up to 17% of patients postoperatively [19]. A systematic study of intraoperative fundoscopy was reported by Williams [20] in 1975 in which the passage of retinal emboli was described. Retinal vessels less than 30 µm in diameter, which are indistinguishable on fundoscopy, can be visualized by the photographic technique of fluorescein angiography, and this technique has been adapted for use during CPB in dogs and in patients to reveal microvascular embolic occlusions [10, 21]. Quantification of the extent of retinal ischemia was achieved by digital image analysis of the ischemic areas [22].

Direct observation of microemboli during CPB at sites other than the retina in vivo has also been reported on the surface of the cerebral hemispheres in goats after frontoparietal craniotomy [23] and in the mesentry of the dog [24].

Embolism and CNS Dysfunction

The most feared complication of cardiac surgery is stroke. Stroke is also the hardest and most important measure of CNS dysfunction after a cardiac operation. Earlier studies have correlated stroke with cerebral histologic evidence of embolism [25, 26], high screen-filtration pressure of pump blood [27], and retinal emboli [20]. More recently, stroke has been shown to correlate with cerebral atheroembolism [4]. In 129 brains examined, 21 had signs of atheroembolism. The incidence of stroke before death was significantly higher in the 21 patients with atheroembolism (52%) than in those without atheroemboli (18%) (p = 0.001) (Fig 1). It has also been suggested that middle cerebral artery emboli, detected and quantified by ultrasound Doppler, may be related to neuropsychologic deficits [28]. There appears to be no relationship between the extent of retinal ischemia and neuropsychologic deficit, and retinal microembolism does not appear to have functional consequences [10].

View larger version (11K): [in this window] [in a new window]   Fig 1. . Incidence of stroke before death in 129 consecutive patients. At postmortem examination, brain studies showed a significantly higher incidence of stroke in patients with brain atheroemboli (52%; n = 21; black bar) than in those without brain atheroemboli (18%; n = 108; white bar) (p = 0.001).

Surgical Technique
Surgical strategy has focused on avoidance of major embolism of air, intracardiac thrombus, and calcific debris from diseased heart valves. An additional consideration is avoidance of atheroembolism from the ascending aorta. A soft atheroma, which may be externally nonpalpable, is most likely to embolize. Detection of aortic atheroma depends on assessment of risk factors including age and peripheral vascular disease and may require intraoperative epiaortic echo by the surgeon. An aggressive surgical approach to aortic disease diagnosed in this way has yielded excellent results [29]. If this is not feasible, aortic trauma should be minimized in patients at risk. Transesophageal echocardiography can be a useful guide to the adequacy of deairing after valve replacement.

Cardiopulmonary Bypass
The superiority of membrane oxygenators compared with bubble oxygenators in reducing CPB–generated embolism has been demonstrated by ultrasound [15] and retinal angiography [22]. Arterial line filtration has also been shown to reduce echogenic signals in the CPB circuit [16, 30] and in the middle cerebral artery [28, 31] but it did not reduce retinal vascular occlusions, which were mostly seen in vessels smaller than the pore size of the 40-µm filter studied [10]. Pharmacologic inhibition of platelet aggregation by prostacyclin appeared promising [32] but had no discernible effect on retinal embolism [33].

Summary

In terms of clinically significant CNS dysfunction, the most important embolic hazard of cardiac surgery in the current era is atheroembolism from manipulation of the ascending aorta. Improved performance and hemocompatibility of newer extracorporeal circuits and more widespread use of membrane oxygenators have reduced the microembolic risk of CPB to the point where it is now of doubtful importance in clinical outcome after cardiac procedures. Responsibility for embolic CNS injury is back with the surgeon.

Footnotes

Presented at the Conference on CNS Dysfunction After Cardiac Surgery: Defining the Problem, Fort Lauderdale, FL, Dec 10–11, 1994.

Address reprint requests to Dr Blauth, Cardiothoracic Unit, Guy's Hospital, London SE1 9RT, England.

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