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Ann Thorac Surg 2004;78:1564-1571
© 2004 The Society of Thoracic Surgeons

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Original article: cardiovascular

The Impact of Aortic Manipulation on Neurologic Outcomes After Coronary Artery Bypass Surgery: A Risk-Adjusted Study

^a Department of Surgery, Section of Cardiac Surgery, Washington Hospital Center, Washington, DC, USA
^b Department of Epidemiology and Statistics, MedStar Research Institute, Washington, DC, USA

Accepted for publication May 7, 2004.

^* Address reprint requests to Dr Corso, Section of Cardiac Surgery, Department of Surgery, Washington Hospital Center, 106 Irving St NW, Suite 316, Washington, DC 20010–2975, USA
paul.j.corso{at}medstar.net

	Abstract

Top Abstract Introduction Patients and Methods Results Comment References

 
BACKGROUND: Cerebral embolization of atherosclerotic plaque debris caused by aortic manipulation during conventional coronary artery bypass grafting (CABG) is a major mechanism of postoperative cerebrovascular accidents (CVA). Off-pump CABG (OPCABG) reduces stroke rates by minimizing aortic manipulation. Consequently, the effect of different levels of aortic manipulation on neurologic outcomes after CABG surgery was examined.

METHODS: From January 1998 to June 2002, 7,272 patients underwent isolated CABG surgery through three levels of aortic manipulation: full plus tangential (side-biting) aortic clamp application (on-pump surgery; n = 4,269), only tangential aortic clamp application (OPCABG surgery; n = 2,527) or an "aortic no-touch" technique (OPCABG surgery; n = 476). A risk-adjusted logistic regression analysis was performed to establish the likelihood of postoperative stroke with each technique. Preoperative risk factors for stroke from the literature, and those found significant in a univariable model were used.

RESULTS: A significant association for postoperative stroke correspondingly increasing with the extent of aortic manipulation was demonstrated by the univariable analysis (CVA incidence respectively increasing from 0.8% to 1.6% to a maximum of 2.2%, p < 0.01). In the logistic regression model, patients who had a full and a tangential aortic clamp applied were 1.8 times more likely to have a stroke versus those without any aortic manipulation (95% confidence interval: 1.15 to 2.74, p < 0.01) and 1.7 times more likely to develop a postoperative stroke than those with only a tangential aortic clamp applied (95% confidence interval: 1.11 to 2.48, p < 0.01).

CONCLUSIONS: Aortic manipulation during CABG is a contributing mechanism for postoperative stroke. The incidence of postoperative stroke increases with increased levels of aortic manipulation.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment References

 
Despite refinements in cardiopulmonary bypass (CPB) technology such as improved arterial filtration and membrane oxygenators, the incidence of cerebrovascular accidents (CVA) after surgical coronary revascularization remains significant, ranging from 1.0% to 2.5% [1–3]. Although numerous pathophysiologic mechanisms for stroke after coronary artery bypass graft (CABG) surgery have been suggested, the most probable cause is cerebral embolization of atherosclerotic plaque debris from the ascending aorta, released during the maneuvers of cannulation and occlusion [3–5]. Atherosclerotic disease of the ascending aorta has been thought to contribute significantly to the release of emboli during aortic manipulation and clamp application during conventional cardiac operations [4, 6]. Accordingly, in a number of recent studies, preoperative variables related to the development of atherosclerotic disease, such as hypertension, advanced age, and carotid artery disease, have been identified as risk factors for the development of postoperative CVA [2, 7].

Off-pump CABG (OPCABG) decreases or can eliminate aortic manipulation during surgery [8, 9]. The differences in the degree of aortic manipulation, with the elimination of total aortic occlusion, may be responsible for the reduction in the postoperative rate of stroke observed with OPCABG over conventional CABG [6, 10, 11]. When saphenous vein or free arterial aortocoronary grafts are used, however, there is still risk of CVA due to the tangential (side-biting) clamp, which is applied during the construction of the proximal anastomoses [12, 13]. Therefore, a number of authors have suggested implementing a strategy of eliminating CPB and operating through an "aortic no-touch" technique, which produces a significantly reduced stroke rate [8, 9, 13, 14].

We wish to contribute to the discussion by presenting our conclusions regarding the influence of different degrees of aortic manipulation on neurologic outcomes after CABG surgery, drawn from a risk-adjusted analysis of a large, consistent, single-institution patient population.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment References

 
Patient Population and Data
The study population was composed of 7,272 consecutive patients undergoing primary, isolated CABG surgery between January 1998 and June 2002 who were identified from our institution's cardiac surgery research database. Patients undergoing concomitant valve repair or replacement, ventricular aneurysm resection, or other vascular surgical procedures were excluded from the study. Similarly excluded from the analysis were any patients who required emergent or salvage operations, patients who had undergone previous cardiac surgery, and patients who had a minilateral thoracotomy or ministernotomy (minimally invasive direct CABG) performed.

Preoperative, intraoperative, and postoperative patient variables were collected prospectively during the patient's hospitalization and entered into the research database as part of routine clinical practice. Patients were contacted through telephone 30 days after hospital discharge as part of routine clinical follow-up.

Study Group Creation
Patients were grouped according to the degree of aortic manipulation to which they were subjected. The group that had extensive aortic manipulation included 4,269 patients (58.7%) operated on using CPB, aortic cannulation, and complete plus tangential aortic clamp application. The moderate aortic manipulation group consisted of 2,527 patients (34.8%) who were operated on with a beating heart (OPCABG) with only a tangential aortic clamp applied, while the no aortic manipulation group included 476 OPCABG patients (6.5%) operated on with the "aortic no-touch" technique using only in situ internal mammary artery grafts and free conduits as Y or T extensions. The patients in each group were contemporaneous and not sequential cohorts.

Neurologic Complications
All patients had a postoperative neurologic examination performed when consciousness was regained, by attending medical staff. The main outcome measure for our study, new CVA, was defined as a postoperatively occurring new focal neurologic deficit, persisting for longer than 72 hours after onset, diagnosed by clinical findings, confirmed by a neurologist or brain imaging (head computed tomography or magnetic resonance imaging), and noted before discharge or death. We did not include transient neurologic events, intellectual impairment, and confusional or irritable states to avoid any subjective bias on neurologic assessments.

Aortic Disease
Gentle intraoperative digital palpation of the aorta by the operating surgeon was used for the assessment of atherosclerotic disease. Significant aortic atherosclerotic disease was defined by the presence of diffuse irregularities, large protruding atheromata, thrombi, or circumferential involvement of most of or the entire ascending aorta [15]. Intraoperative epiaortic echocardiography was not used during the period of this study.

Anesthesia and Surgical Technique
The anesthetic technique, consisting of low to intermediate dose narcotics, inhalation agents, and paralytics, and intraoperative hemodynamic monitoring (electrocardiography, plus Swan-Ganz or central venous pressure, arterial and Foley catheters) was standardized in all patients. All patients were operated on through a median sternotomy. Conduits harvested included the left, right, or both internal mammary arteries either as pedicles or free grafts, the saphenous vein, and when required the nondominant arm's radial artery. After opening the pericardium, target coronary vessels were explored and the ascending aorta was assessed for atheroma and calcification. The extensive aortic manipulation group underwent traditional extracorporeal bypass with standard anticoagulation and myocardial protection methods. The moderate and no aortic manipulation groups underwent OPCABG surgery. Selection criteria for OPCABG surgery included patients who were considered high risk for the conventional on-CPB technique because of medical comorbidities such as renal failure, diffuse cerebrovascular and peripheral vascular disease, aortic atherosclerotic disease, chronic obstructive pulmonary disease (COPD), and religious convictions that precluded blood transfusions [16]. Contraindications for OPCABG included inadequate exposure and aberrant anatomy such as poorly visualized target vessels on angiography or extensive intramyocardial coronary arteries.

Statistical Analysis
Continuous variables and ordinal categorical data were evaluated using the Spearman correlation and are expressed as mean value ± SD or as median with 25th and 75th percentiles. Dichotomous variables were compared using the Cochran-Armitage test for trends. No adjustments were made for multiple testing. The Northern New England CVA risk score was derived to access differences in the patients' preoperative stroke risk among the three study groups [17]. In all tests p values of 0.05 or less were considered significant.

To control for confounding variables to the main outcome measure, a multivariable logistic regression analysis was used. Variables offered into the multivariable model included those factors from the univariable analysis that were significantly or marginally significantly (p 0.15) different between the study groups plus risk factors reported in the literature as important determinants of postoperative stroke incidence. Forward stepwise selection was then used to identify significant covariates to stroke occurrence. A final logistic regression model was constructed to examine the effect of different degrees of aortic manipulation on the postoperative stroke incidence. Potential preoperative confounding factors offered to this multivariable model included advanced age, female sex, history of diabetes, hypertension, history of myocardial infarction, decreased left ventricular ejection fraction (LVEF), history of carotid artery disease, history of stroke, COPD, urgent case priority, aortic atherosclerotic disease, number of vessels grafted, and preoperative renal failure; atrial fibrillation was included as a postoperative confounder. These variables have been identified in the literature as stroke risk factors and have been utilized in the creation of widely applied stroke risk models [7, 12, 18]. Model fit was evaluated using the Hosmer and Lemeshow goodness-of-fit statistic, as well as residual diagnostics (deviance and dfBetas) analysis. The c-statistic was reported as a measure of predictive power. The presence of mulicollinearity among the independent variables was checked using diagnostics such as the variation inflation factor and tolerance.

To further reduce the effect of preoperative intergroup variability and to accurately evaluate the correlation of aortic manipulation to postoperative neurologic outcome, matched-pair analyses between the study groups were performed. Propensity scores, or the predicted probability for each patient undergoing surgery with a specific surgical technique, were computed from a logistic regression equation measuring the association of treatment selection and preoperative characteristics. Three matched-pair comparison sets were constructed, with patients who had no aortic manipulation being randomly matched on propensity score, first to patients who had extensive aortic manipulation and then to patients who had moderate aortic manipulation. Finally, patients who had extensive aortic manipulation were matched on propensity score to patients who had moderate aortic manipulation. Previous studies have shown that matching on the propensity score can control for selection bias [19, 20]. The general estimating method in a logistic regression model was used to evaluate the correlation between postoperative stroke and aortic manipulation in the three matched-pair groups [21].

Furthermore, so as to evaluate the effect of eliminating CPB in postoperative stroke incidence, a further logistic regression and matched-pair subanalyses were conducted. In this additional model, patients operated on using CPB were matched by propensity score to OPCABG surgery patients regardless of the degree of aortic manipulation they received.

All statistical analysis was performed with SAS for Windows Version 8.2 (SAS Institute, Cary, NC).

	Results

Top Abstract Introduction Patients and Methods Results Comment References

 
Patient Baseline Demographics and Stroke Risk Factors
The distribution of preoperative stroke risk factors in the three study groups and baseline patient demographics are presented in Table 1. There were significant differences between the groups in regard to age, sex, body mass index, history of hypertension and of myocardial infarction, myocardial infarction within 24 hours of surgery, unstable angina, left main stenosis, LVEF, carotid artery disease, and COPD. However, the average values of the calculated Northern New England preoperative stroke risk scores were comparable among the three groups: 1.1 (0.3 to 1.5) in the no aortic manipulation group versus 1.5 (0.9 to 2.8) for the moderate and 1.5 (0.7 to 2.8) in the extensive aortic manipulation groups (p = 0.47).

In the multivariable logistic regression model, patients who experienced extensive aortic manipulation were 1.8 times (95% confidence interval [CI]: 1.17 to 2.80, p < 0.01) more likely to develop a CVA postoperatively, compared with patients who had no aortic manipulation, and 1.7 times (95% CI: 1.13 to 2.53, p < 0.01) more likely to have a postoperative stroke compared with patients who had moderate aortic manipulation (Table 3). However, moderate aortic manipulation when compared with no aortic manipulation was not found to significantly increase the odds (odds ratio [OR] = 0.9, 95% CI: 0.62 to 1.41, p = 0.75) of developing a stroke. Other independent risk factors found significant for the development of postoperative CVA were advanced age, hypertension, decreased left ventricular ejection fraction, carotid artery and aortic atherosclerotic disease, and COPD. There was no evidence of a lack of fit and no indication of multicollinearity among the independent variables.

After matching 64% (n = 1,915) of patients operated on a beating heart (OPCABG technique) to an equal number of on-CPB CABG patients, CPB emerged as a significant predictor for developing a postoperative stroke (OR = 1.9, 95% CI: 1.16 to 3.02, p < 0.01).

	Comment

Top Abstract Introduction Patients and Methods Results Comment References

 
The initiation of CPB involves extensive mechanical manipulation of the aorta. Placement of aortic pursestring sutures, aortic and cardioplegia cannula insertion, cross-clamping of the ascending aorta, and tangential clamp application for the performance of the proximal graft anastomoses are all integral steps of cardiac revascularization operations utilizing CPB [22]. Provided a relatively normal aortic vascular wall, the maneuvers can be performed with minimal risk. In the presence of atheromatous disease, however, the force applied can lead to cracking or rupture of an atherosclerotic plaque releasing debris, which can then cause embolization and ischemic damage to the brain [22–24].

A number of studies utilizing transcranial Doppler measurements have demonstrated substantial number of emboli production with aortic cannulation and application, readjustment, and removal of aortic cross and side clamps [4, 6, 25, 26]. Macroemboli as well as microemboli are most notably detected during application and release of the aortic cross clamp with significant neurocognitive sequelae [27, 28]. Therefore, it is not unexpected that the presence of extensive aortic atherosclerotic disease has emerged as one of the most significant risk factors for post–CABG stroke [2, 5, 12, 29, 30]. A recent study by Calafiore and colleagues [1] concluded that the maneuvers necessary to institute CPB are significant risk factors for increased CVA incidence, both early and delayed. Correspondingly, Stump and Newman [31] demonstrated a substantial embolic load produced during aortic cannulation and decannulation. During the last decade, there has been a considerable increase in the average age of the patient population presenting for surgical coronary revascularization [32]. The prevalence of atherosclerotic disease is increased in these older patients, leading to a higher overall risk for atheroembolic cerebrovascular events during and after cardiac surgery. Therefore, the effect of aortic manipulation on the postoperative stroke incidence has become a concern for many cardiac surgeons.

This study demonstrated that the considerable handling of the aorta during CPB is a significant contributing factor in the development of postoperative stroke. A correlation of the main study outcome, the incidence of focal neurologic deficit, to correspondingly increasing levels of aortic clamp application was demonstrated by the univariable analysis. Our experience included comparable study groups and a large patient sample size, but inevitably not all preoperative variables were evenly distributed among the three sets. Therefore, a logistic regression model was created to adjust for these preoperative risk factors. After risk adjustment, extensive aortic manipulation and CPB during CABG emerged as an independent predictor for postoperative stroke. Other independent predictors for stroke included aortic atherosclerotic disease and related or contributing factors to it, such as advanced age, hypertension, and carotid artery disease. These findings confirm the previous findings by Hartman and coworkers [18], Stamou and colleagues [7], and Likosky and coworkers [18].

However, aortic cross-clamp application is not exclusively responsible for the development of postoperative stroke, but rather, a synergistic effect with CPB exists. Ura and colleagues [33] used ultrasonographic studies to demonstrate that aortic cannula jets can dislodge debris from the vascular wall. More significantly, Bowles and coworkers [34], by using transcranial Doppler imaging, demonstrated large quantities of emboli occurring while on CPB but without the aorta having been manipulated. Hemodynamic fluctuations, loss of pulsatile flow during CPB, cerebral hypoperfusion, and coagulation and inflammatory cascade derangement might also be contributing or mediating factors in the development of postoperative CVA [35, 36].

Eliminating the use of CPB and the maneuvers associated with it in surgical coronary revascularization procedures should minimize emboli generation and subsequently decrease postoperative strokes. This was the driving concept behind the development of OPCABG surgery, a technique that avoids extensive aortic manipulation and reduces the physiologic dysfunction caused by CPB [12, 37–39]. Recent studies have not only demonstrated the safety and efficacy of OPCABG but also produced a reduction in mortality and morbidity, particularly in the rates of postoperative CVA [10, 37, 40]. This study also demonstrated a significant association between CPB and the incidence of postoperative neurologic dysfunction. When 1,915 pairs of patients operated on either through the use of CPB or on a beating heart were compared, on-CPB patients were twice as likely to have a stroke during their procedure. This confirms the findings of an earlier report, on a chronologically distinct patient cohort, from our institution [10].

However, the better physiologic milieu produced through the elimination of CPB did not reduce the postoperative stroke incidence to corresponding rates seen with comparable thoracic, vascular, or abdominal procedures [37, 38, 40]. A study by Kim and associates [9], while demonstrating lower incidence of postoperative stroke in patients operated on through OPCABG without any aortic manipulation, reported similar stroke rates between patients who had OPCABG with aortic manipulation and who had had conventional on-pump CABG. Therefore, tangential clamp application has been cited as an independent predictor of postoperative CVA when CPB is not used [1]. In response, a number of authors have proposed improving neurologic outcome by using an "aortic no-touch" technique, in which the surgical revascularization is performed without the use of CPB by using only in situ internal mammary artery grafts and free conduits as Y or T extensions [13, 14]. In contrast, a number of studies refute that tangential clamp application increases the incidence of postoperative stroke in OPCABG surgery [24, 41]. Patel and associates [24], utilizing a large sample size and a risk-adjusted methodology, suggested that tangential clamp application does not significantly influence neurologic outcome in OPCABG patients. A debate has therefore emerged within the cardiac surgery scientific community regarding the safety threshold of aortic manipulation during OPCABG surgery.

Our study confirmed that any time the aorta is manipulated, the risk of subsequent stroke increases. The unadjusted incidence of stroke in the no aortic manipulation group was significantly decreased compared with the CVA rate seen in the moderate aortic manipulation group. Secondary to the small number of index events, however, this twofold difference in stroke incidence was not found statistically significant in the risk-adjusted logistic regression model. Similarly, when propensity matched-pair analyses were conducted, comparing 94.7% and 98.7% of the no aortic manipulation group patients to an equal number of patients from the extensive and moderate aortic manipulation groups, the odds of developing a postoperative stroke were not found to be statistically different. That occurs frequently when the incidence of a clinical event is very low, and therefore a considerable study sample is required to demonstrate a statistical difference. The study by Patel and associates [24] also contained a small number of index events (CVA rate in OPCABG with aortic manipulation = 2 [n = 520]; CVA rate in OPCABG without aortic manipulation = 3 [n = 597]), and therefore it is difficult to accept the conclusion that application of a tangential clamp during OPCABG surgery does not significantly contribute to the incidence of postoperative CVA. On the contrary, our findings suggest that any degree of aortic manipulation increases stroke risk. When adequately large sets of extensive and moderate aortic manipulation patients, randomly matched to produce equivalent risk distributions, were compared, the odds of developing a postoperative stroke were not significantly different between them. Therefore optimal stroke prophylaxis during surgical revascularization procedures would include the complete avoidance of aortic manipulation. As previously shown, however, the elimination of CPB in itself produces such a significant reduction in the magnitude of aortic manipulation and in stroke incidence that it surpasses any risk of stroke associated with the tangential clamp application during OPCABG.

Study Limitations
Limitations of this study include all those inherent in a retrospective single-institution analysis. However, all data elements were prospectively entered into a cardiac surgery research database according to prespecified definitions. Although a prospective randomized trial would provide the most conclusive evidence, the large sample size that would be required for such a study make it difficult to conduct. Instead, we tried to adjust for selection factors by using multivariable logistic regression and propensity score matched-pair analyses. Secondarily, because the study did not possess a large enough patient sample to accurately reflect differences in the limited number of index events, the incidence of stroke both in the logistic regression model and in the matched-pair analysis failed to reach statistical significance between the moderate and no aortic manipulation groups. Furthermore, intraoperative digital palpation of the aorta, and not epiaortic echocardiography, was used for the assessment of atherosclerotic disease.

In conclusion, we have demonstrated that in our institution the magnitude of aortic manipulation is a significant contributor to postoperative stroke. Off-pump CABG surgery, regardless of tangential clamp application, reduces postoperative stroke incidence compared with conventional CABG.

	References

Top Abstract Introduction Patients and Methods Results Comment References

 

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