Review

Continuing Medical EducationNature Clinical Practice Cardiovascular Medicine (2005) 2, 246-251
doi:10.1038/ncpcardio0192  
Received 22 December 2004 | Accepted 21 March 2005

Atherosclerosis of the ascending aorta as a major determinant of the outcome of cardiac surgery

Per Bergman* and Jan van der Linden  About the authors

Correspondence *Department of Cardiothoracic Surgery & Anesthesiology, Karolinska University Hospital, Karolinska Institute, Stockholm, Sweden

Email per.bergman@karolinska.se

Summary

Epiaortic ultrasonography has high sensitivity for the detection of atherosclerosis. In several studies, the technique has identified atherosclerosis of the ascending aorta as the major risk factor for stroke after cardiac surgery. The level of risk depends on the presence, location and extent of disease when the ascending aorta is surgically manipulated. This knowledge enables clinicians to focus on the diagnostic and surgical technique and to consider the various options. Routine use of intraoperative epiaortic ultrasonography should be applied so that surgical manipulation of the ascending aorta can be reduced or, if possible, avoided in patients with atherosclerosis of the ascending aorta. Alternatively, if major manipulation such as clamping must be performed in the presence of severe atherosclerosis, the use of intra-aortic filters could be considered.

Review criteria

All articles were identified by searching the MEDLINE and PubMed databases. The search keywords, used in different combinations were "stroke", "cardiac surgery", "epiaortic ultrasound", "atherosclerosis", and "aorta". All referenced articles were full-text, English-language papers, published between the years 1989 and February 2005. We searched the articles' bibliographies and our own database for further relevant papers.

Keywords:

arterial disease, ascending aorta, atherosclerosis, stroke, surgical complication

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Introduction

The incidence of early stroke after coronary artery bypass grafting (CABG) surgery—that is, within 30 days of the operation—is reported to be 2–4%.1, 2, 3 This complication can be difficult to prevent and manage, and can lead to a substantial deficit in patients' quality of life. The financial burden has been estimated to be US$2–4 billion worldwide per year.1 The magnitude of this problem was well illustrated in a large prospective study by Roach et al.1 involving 24 centers, which has attracted worldwide attention. They reported a 3.1% incidence of TYPE I NEUROLOGIC INJURY after CABG. Affected patients had a higher in-hospital mortality rate than patients without neurologic complications (21% vs 2%), as well as a longer hospital stay (25 days vs 10 days). Predictors of type I outcomes were palpable proximal aortic atherosclerosis, a history of neurologic disease and older age.

John et al.4 reported a study that included almost 20,000 patients undergoing CABG in whom preoperative risk factors were assessed. Multivariate logistic regression identified nine variables that were significantly associated with postoperative stroke: calcified aorta, prior stroke, age, carotid arterial disease, duration of cardiopulmonary bypass, renal failure, peripheral vascular disease, cigarette smoking and diabetes mellitus. When risk ratios were considered, age was the most important risk factor for postoperative stroke, followed by palpable calcification in the aorta. Other reported risk factors for postoperative stroke are: pre-existing cerebrovascular disease, prior CABG, unstable angina, hypertension, combined valve and coronary surgery, severe perioperative hypotension, history of pulmonary disease, sustained cardiopulmonary bypass time and supraventricular arrhythmia.4, 5, 6, 7

Several studies using multivariate analysis have added weight to the importance of atherosclerosis of the ascending aorta as a risk factor for postoperative stroke in cardiac surgery.1, 3, 8, 9, 10 The routine use of EPIAORTIC ULTRASONOGRAPHY, which has high sensitivity (the ability to avoid false negatives) in the detection of atherosclerosis, has enabled the reliable estimation of stroke risk related to this factor. Thus, many reported risk factors for stroke after cardiac surgery, such as age, lose their independent status when epiaortic ultrasonography rather than digital palpation is used to diagnose atherosclerosis of the ascending aorta.3 The presence of atherosclerosis alone in this region in patients undergoing cardiac surgery increased the risk of early postoperative stroke from 1.8% to 8.7%.3 In this review, we look briefly at the ways in which atherosclerosis can be assessed in the ascending aorta, and provide a more in-depth discussion of how to take this risk factor into account when performing CABG.

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Atherosclerosis in the ascending aorta

Aortic atherosclerosis is characterized by the formation of intimal plaques with the usual morphologic features of atherosclerosis, including cellular proliferation, lipid accumulation, inflammation, necrosis, fibrosis and calcifications. Ulceration of these plaques can result in embolization of plaque elements or thrombus formation, which can lead to neurologic deficit, stroke and death.

Cardiac surgery usually involves manipulation of the ascending aorta by arterial cannulation, cross clamping and side clamping, all of which can increase the risk of embolization of atherosclerotic material to the brain. The findings from several studies1, 3, 4, 8, 9, 10 have suggested a correlation between the presence of atherosclerosis in the ascending aorta and postoperative neurologic events.

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Quantification of atherosclerosis

Ordinary chest radiography for the preoperative identification of atherosclerosis of the thoracic aorta visualizes only large calcified areas, and thus underestimates the frequency of atherosclerosis.11 Transesophageal echocardiography visualizes calcified as well as noncalcified areas, and has made grading of the extent of disease possible. The interposition of the trachea, however, makes clear evaluation of the middle and distal part of the ascending aorta impossible.12 Thus, this method significantly underestimates the severity of ascending aortic atherosclerosis, particularly in the distal ascending aorta.13, 14 This limitation is of particular importance since surgical manipulation of the ascending aorta usually takes place in this area. In contrast to transesophageal echocardiography and epiaortic ultrasonography, palpation fails to identify plaques in the ascending aorta in 50–60% of cases.3, 13 A second limitation is the lack of a uniform classification system for quantification of atherosclerosis of the ascending aorta. Various cut-off values have been used to define atheromatosis in the aortic wall as pathologic: 0.5 mm,3 1.0 mm,15, 16 and 3.0 mm.17, 18, 19, 20 Moreover, the number of grades used to classify intimal thickening has varied, being expressed in two categories (mild or severe15, 16), three categories (mild, moderate or severe17, 19, 20), or even in four categories (mild, moderate, severe I and severe II21).

Epiaortic ultrasonography

Intraoperative epiaortic ultrasonographic assessment was introduced by Marshall et al.13 for patients undergoing cardiac surgery. Atherosclerosis of the ascending aorta was diagnosed by this method in 58% of a selected series of patients, which led to the surgical technique being changed in 24% of patients overall. Several subsequent studies have confirmed epiaortic ultrasonography to be superior to transesophageal echocardiography and palpation for evaluation of the ascending aorta.12, 14, 22 Multiple views of the distal ascending aorta can be obtained by use of a high-frequency transducer, preferably 7 MHz or higher, and a probe with a built-in HARD-SHELL STANDOFF.23 The probe's advantage is that the built-in hard shell standoff, which is approximately 6 cm long, results in good resolution when the surface of the aorta is in contact with the probe, directly on the aorta, providing much better resolution than with transesophageal echocardiography.

With use of epiaortic ultrasonography, atherosclerotic disease can be identified in 20–25% of patients, most often in the cranial part of the ascending aorta.3, 9, 13 Details of the topography of the ascending aorta can be easily obtained, but whether topographic pathology can have an impact on the incidence of postoperative neurologic deficits has only just started to be studied in detail. The findings of one study, however, have shown that if the ascending aorta is divided into 12 segments (N.B. three transverse and four longitudinal), the distal anterior segment tends to be affected more often than any other segment.3 This area is where surgeons usually place the aortic cannula. Furthermore, apart from the extent of disease, the middle-right segment is associated with a high rate (26%) of early postoperative stroke. One explanation for this finding could be that the blood flow pattern at the level of the aortic valve is asymmetric, with the highest flow velocities occurring along the noncoronary leaflet, with a counter-clockwise rotation of 90° between commissures during systole.24 This pattern results in higher blood velocity along the right aspect of the ascending aorta during systole. Moreover, the blood jet through the aortic valve can strike the middle-right segment of the ascending aorta, which could dislodge atherosclerotic material that has been partly mobilized by earlier surgical maneuvers, (particularly during clamping, proximal anastomoses, cardioplegia-needle insertion etc.), and thus cause embolization into the brain vessels. This view that new lesions caused by cannulation or clamping, especially those with mobile components, are more often complicated by postoperative stroke than other types of lesions is supported by the findings of Ura and co-workers.21 The maximum thickness of atheroma near the aorta manipulation site was also identified as a predictor of new lesions.

Preoperative diagnosis of atherosclerosis

Although epiaortic ultrasonography has become the gold standard for detecting atherosclerotic changes in the ascending aorta, this method can only be used during the operation. Therefore, if the findings do not reflect the anticipated diagnosis, decisions regarding technique have to be made during surgery. Preferably, such decisions should be made preoperatively. Thus, it would be of interest to investigate whether a commonly available preoperative method such as CT can evaluate severe atherosclerosis in the ascending aorta as effectively as intraoperative epiaortic ultrasonography. Presently, however, CT cannot classify the extent and location of disease with the same accuracy as intraoperative epiaortic ultrasonographic scanning.25 Finally, as indicated by Summers et al.,26 other noninvasive diagnostic techniques, including MRI, might also be of great value in the preoperative evaluation of severe atherosclerosis in the ascending aorta.

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Surgical techniques

Most of the surgical techniques used presently to diminish the risk of stroke focus on reducing manipulation of the ascending aorta. Options range from canceling the surgery to choosing an off-pump coronary artery bypass approach, and can include one or more of the following alternatives: altering the aortic cannulation and cross-clamp sites; using only one cross clamp for proximal and distal coronary artery graft anastomoses; placing the aortic cannula in sites other than the ascending aorta; intra-aortic filtration; use of anastomotic devices for proximal anastomoses; using a no-touch approach that totally avoids the ascending aorta; using alternative sites for placement of proximal anastomoses (innominate or internal mammary arteries); and use of aortic atherectomy or aortic replacement under deep hypothermic circulatory arrest.

Intra-aortic filters

Aortic filtration is an attractive method of minimizing systemic and cerebral embolization during cardiac surgery.27, 28, 29, 30 Intra-aortic filters placed in the distal portion of the ascending aorta during unclamping in cardiac procedures reportedly capture atheromatous material in the majority of patients undergoing cardiac surgery.27, 29 A reduction of neurologic complications by intra-aortic filtration has been shown by the International Council of Emboli Management group,27 who studied patients undergoing cardiac surgery prospectively and compared their outcomes to the calculated risk for neurologic impairment. Histologic examination of intra-aortic filters has revealed that up to 85% contained atheromatous or fibrous cap.28, 31 Findings also indicate a possible protective effect of intra-aortic filters on neuropsychologic function in patients undergoing CABG.30 The first randomized study on the use of a filter, however, was not sufficiently powered to show whether there was a significant influence on stroke rate.29 Moreover, the poor acceptance rate for this technique in the cardiac-surgery community might indicate that the potential for reducing stroke in clinical practice is low, or that significant problems occur during application of these devices.

Off-pump coronary artery bypass

The findings from two nonrandomized studies, using propensity scores, showed lower rates of stroke with off-pump coronary artery bypass than with on-pump coronary artery bypass.32, 33 Conversely, however, a number of other studies showed no benefit.34, 35, 36 A reduced number of strokes was reported in two retrospective studies of octogenarians.37, 38 This advantage was probably related to raised rates of atherosclerosis in the ascending aorta among elderly patients, leading to greater differences between off-pump and on-pump groups. On the other hand, two randomized studies called into question the superiority of off-pump surgery over CABG with cardiopulmonary bypass.39, 40 Consequently, off-pump coronary artery bypass might show a reduction in the stroke rate more clearly if the avoidance of cardiopulmonary bypass is combined with other measures, listed below, that reduce manipulation of the ascending aorta.41

Single-clamp technique

A simple way of reducing manipulation of the ascending aorta is to avoid the use of side clamping, and to perform the proximal and distal anastomoses during a single-clamp period. Grega et al.42 showed that the double-clamp technique is an important operative risk factor for neurologic complications and that the single-clamp technique significantly reduced neurologic injuries in patients undergoing CABG.

Total avoidance of clamping

There are two ways to avoid clamping completely during CABG: a mechanical anastomotic graft connector is used for sutureless proximal anastomoses in off-pump coronary artery bypass;43 or the proximal anastomoses are sutured on a site other than the ascending aorta, such as the subclavian or axillary arteries,44 or as an arterial or a venous Y-graft on an internal thoracic artery.45, 46 This latter method is termed the 'no-touch' approach.

No-touch off-pump coronary artery bypass

Saphenous veins and radial arteries, which are the most commonly used grafts, normally require a proximal anastomosis. The preferred area to place such anastomoses is the ascending aorta. On the other hand, Y-grafts to the internal thoracic arteries avoid the necessity for such proximal anastomoses. Kim et al.45 reported the avoidance of proximal anastomoses by performing complete arterial revascularization with internal thoracic and radial artery Y-grafts during off-pump bypass. This technique might be suitable for patients with atherosclerosis in the ascending aorta. Royse et al.46 reported a reduced incidence of late neuropsychologic dysfunction, and of microemboli detected by transcranial Doppler imaging, with use of exclusive Y-grafts for CABG compared with proximal anastomoses applied to the ascending aorta, respectively. Although several risk-adjusted studies clearly indicate a reduced incidence of stroke with use of the no-touch technique,17, 18, 47, 48 randomized studies of this method are still lacking.

Aortic resection and graft replacement

In the presence of severely diseased ascending aorta, a total resection and graft replacement under deep hypothermic circulatory arrest may not decrease the postoperative stroke and mortality rate.49, 50

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Clinical implications

Despite various minor modifications in surgical technique the incidence of postoperative stroke in patients with atherosclerotic disease in the ascending aorta has been reported to be as high as 8.7%.3 Some of the surgical strategies to prevent postoperative stroke are easy to carry out, such as changing the arterial cannulation site and avoiding the aortic side clamp, but other techniques, such as off-pump CABG, require extensive surgical training. Moreover, given the diversity of options, there is a clear need for additional clinical studies to define the appropriate technique for the individual patient, in order to decrease the incidence of postoperative stroke. There are two strategies that seem to be of particular interest. The no-touch bypass technique is the ultimate surgical solution for severe disease because it does not allow mobilization of atheroma from the ascending aorta. The presence of disease might dictate the use of off-pump CABG, preferably with the no-touch technique, with which revascularization can be achieved without any manipulation of the ascending aorta. Second, intra-aortic filtration may be an option in patients with severe atherosclerosis in whom manipulation of the ascending aorta is unavoidable.

Other minor surgical modifications include altering the aortic cannulation and cross-clamp sites. Whenever disease is detected in a particular area, the surgeon automatically tries to avoid it. Clinical studies have indicated that such avoidance results in a reduction in cerebral embolization detected by transcranial Doppler imaging,51 and improves neuropsychologic outcome,52, 53 but a significant effect on clinical stroke rate has not yet been demonstrated. Almost all patients undergoing cardiac surgery, including coronary surgery, have a significant amount of particulate embolization.27, 29 Moreover, the number of captured particulates is related to the number of plaques or degree of atheroma in the ascending aorta,31 thus confirming earlier studies of stroke rate1, 3, 54 and emboli detected by transcranial Doppler imaging.55 In view of the notable risk of stroke3 and the up to 33% rate of postoperative cerebral dysfunction,1 one approach is to use intra-aortic filters in all patients in whom epiaortic ultrasound detects atheroma in the ascending aorta and aortic clamping is being used. Alternative techniques such as proximal anastomotic devices56 or preferably off-pump coronary artery bypass without manipulation of the ascending aorta46 may also prove to decrease the rate of cerebral complication to the level of or even below the competing technique of angioplasty.

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Conclusions

Atherosclerosis of the ascending aorta is the major risk factor for stroke after cardiac surgery. The level of risk depends on the presence, location and extent of disease, when the ascending aorta is surgically manipulated. Routine use of intra-operative epiaortic ultrasonography should be applied so that surgical manipulation of the ascending aorta is reduced or, if possible, avoided in patients with atherosclerosis of the ascending aorta. Alternatively, if major manipulation such as clamping must be performed in the presence of severe atherosclerosis, the use of intra-aortic filters could be considered.

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Competing interests

P Bergman and J van der Linden have been members of the International Council of Emboli Management (ICEM) Study Group, which was sponsored by EMBOL-X Inc, Mountain View, CA, who manufacture intra-aortic filters

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