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Ann Thorac Surg 2002;73:1387-1393
© 2002 The Society of Thoracic Surgeons
a Department of Cardiology and Cardiac Surgery, "G. D’Annunzio" University, Chieti, Italy
Accepted for publication January 22, 2002.
* Address reprint requests to Dr Calafiore, "G. D’Annunzio" University, Department of Cardiac Surgery, S. Camillo de’Lellis Hospital, via C. Forlanini, 50, 66100 Chieti, Italy
e-mail: calafiore{at}unich.it
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Abstract |
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Methods. From January 1988 to December 2000, 4,875 patients had coronary operations; 33 who survived less than 24 hours and 19 who had aortic cannulation without cross-clamping were excluded. According to the degree of aortic manipulation, patients were divided into two groups: group A, aortic cannulation, cross-clamping, with (A1, n = 597) or without (A2, n = 2,233) side-clamping, and group B, with (B1, n = 460) or without (B2, n = 1,533) side-clamping. Patients in group A (n = 2,830) were operated on with and patients in group B (n = 1,993) were operated on without cardiopulmonary bypass (CPB). Univariate and multivariate analyses were applied to identify independent predictors of higher incidence of CVAs.
Results. Forty-nine patients (1.0%) had a postoperative CVA, 24 early and 25 delayed, with a 30-day mortality of 34.7%. Independent CVA predictors were low output syndrome, presence of extracoronary vasculopathy, conversion from off to on pump, and any aortic manipulation. This latter risk factor was significant in patients with extracoronary vasculopathy, but not in patients without. Side-clamping was not a risk factor in patients operated on with CPB, but it was in no-CPB cases. Patients in group B1 had the same CVA incidence as patients in group A2. Therefore CPB, per se, was not a risk factor for higher CVA incidence.
Conclusions. Aortic manipulation must be avoided in patients with extracoronary vasculopathy. Maintenance of a good hemodynamic status is crucial for any patient to reduce CVA incidence. Patients with extracoronary vasculopathy are at higher risk, and a correct surgical strategy should be tailored for each case. In no-CPB cases use of side-clamping provides the same CVA risk as in patients in whom CPB, aortic cannulation, and cross-clamping were used.
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Introduction |
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Many reports focus on the relationship between the ascending aorta and postoperative CVA [4, 12–14]. In the last 13 years different surgical strategies for myocardial revascularization were used in our institution. In some of these procedures the ascending aorta was either not touched or touched only to a limited extent. The effects of different degrees of aortic manipulation in determining this complication, which has devastating consequences early and late for any patient, were analyzed.
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Material and methods |
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Preoperative data
Patient data were taken from our database, which was assembled from the medical records. Prior CVA was documented on the basis of previous medical records and reviewing the computed tomographic scan or nuclear magnetic resonance images related to the episode.
Carotid endarterectomy: indication and timing
Carotid endarterectomy (CEA) was indicated in patients (1) with soft carotid plaque (defined as nonechogenic plaque, made by noncalcific atheroma), symptomatic or asymptomatic, (2) with any plaque for which computed tomographic scan demonstrated previous embolization, (3) with bilateral fibrocalcific plaques with luminal narrowing of at least 70%, and (4) with occlusion of a carotid artery and luminal narrowing in the other artery of at least 50%. Isolated carotid artery narrowing to any degree, without previous embolization, was never an indication for CEA. Single CEA was performed simultaneously with CABG if the patient had unstable angina or was considered at risk for a cardiac-related event, such as left main coronary artery disease; it was performed before CABG if the patient was stable. If the patient needed bilateral CEA, the carotid artery with the most dangerous lesion was operated on before CABG and the second lesion at the same operation as CABG.
Perioperative data
Until December 1994 all the patients except 23 (2.1%) were operated on with the aid of cardiopulmonary bypass (CPB), with hypothermic or normothermic body perfusion. Since then, the number of patients operated on without CPB through median sternotomy or left thoracotomy increased.
Patients were grouped according to the degree of aortic manipulation to which they were submitted. Group A included 2,830 patients who had CPB with aortic cannulation and cross-clamping, divided into two subgroups according to aortic side-clamping (A1, n = 597, side-clamping yes; A2, n = 2,233, side-clamping no). Group B included 1,993 patients who had no CPB, divided into two subgroups according to aortic side-clamping (B1, n = 460, side-clamping yes; B2, n = 1,533, side-clamping no). Some of the patients in this group were converted to CPB (n = 53), but they were included in group B (grouping was made according intention to treat).
Another 19 patients had CPB with aortic cannulation without cross-clamping. This group was very small and, for this reason, it was not considered. Therefore, this study included 4,823 patients. Among them, 4,012 (83.2%) had a median sternotomy, 810 (18.8%) a left thoracotomy, and 1 had a right parasternotomy.
In the statistical analysis aortic manipulation was considered as a whole and divided into two components: (1) aortic cannulation and cross-clamping and (2) side-clamping. A further analysis was performed to evaluate the risk factors when CPB was (group A) or was not (group B) used.
Disease of the ascending aorta was suspected preoperatively from the angiography or the echocardiogram, and, in selected cases, confirmed by computed tomographic scan. Intraoperatively, no routine epicardial scanning was performed. The quality of the aorta was assessed by the surgeon using his fingers.
Intraoperative hypotension (systolic blood pressure < 80 mm Hg, with electrocardiographic changes) that needed rapid institution of CPB was recorded, as well as conversion from no CPB to CPB, independently from the cause (hemodynamic or technical). Low output syndrome (LOS) at the end of the procedure was identified as a need for intraaortic balloon pump or inotropic agents (epinephrine or norepinephrine, any dose; dopamine > 10 µg · kg-1 · min-1; or dobutamine > 5 µg · kg-1 · min-1).
Postoperative data
Every patient had a neurologic examination at the moment of waking up. For the purpose of this study, incidence of death of any cause and LOS were recorded. Continuous monitoring in the intensive care unit and telemetry in the ward was used for every patient until hospital discharge, to monitor the onset of atrial fibrillation.
Definition of cerebrovascular accident
Cerebrovascular accident was defined as global or focal neurologic deficit, lasting less (transient ischemic attack) or more (stroke) than 24 hours, that could be evident after emergence from anesthesia (early CVA) or after first awaking without any neurologic deficits (delayed CVA). Cerebrovascular accident was diagnosed by a neurologist and confirmed by a brain computed tomographic scan or nuclear magnetic resonance image. Stroke was defined as a focal or global cerebral dysfunction of presumed vascular origin lasting more than 24 hours. Transient ischemic attack was defined as a focal cerebral dysfunction of presumed vascular origin that resolved completely within 24 hours.
Statistical analysis
Results are expressed as mean value ± standard deviation unless otherwise indicated. Statistical analysis comparing two groups was performed with unpaired two-tailed Student’s t test for the means or 
2 test for categorical variables. All variables included in the study are listed in the Appendix. Stepwise logistic regression was used to select the independent variables that could predict postoperative CVAs, and, as a further step, early and delayed CVAs. A similar analysis was performed to evaluate whether postoperative CVA was an independent risk factor for increased 30-day mortality. For any independent predictor odds ratio (OR), 95% confidence limit when necessary, and probability value are indicated. Actuarial survival curves were obtained with the Kaplan-Meier method. Statistical significance was calculated with the log-rank test. Cox analysis for time-dependent events was used to evaluate whether postoperative CVA was an independent risk factor for reduced late survival. All the multivariate analyses included univariate variables with p 
0.2; the final significance level for univariate and multivariate analyses was at p less than 0.05. SPSS software (Chicago, IL) was used for all the analyses in this study.
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Conversion to cardiopulmonary bypass
Fifty-three patients (1.1%) were converted to CPB, with a CVA incidence of 5.7% (3 cases; p = 0.016 versus the remaining 46 of 4,770 [1.0%]). Multivariate analysis in these patients showed no independent predictor. Nevertheless, conversion to CPB seems to be a risk factor for CVA mainly in patients with ECV. It is noteworthy that, in converted patients, all 3 CVAs occurred among the 20 patients with ECV, whereas in the remaining 33 patients no CVA occurred.
Extracoronary vasculopathy
Nine hundred thirty-four patients (19.4%) had ECV, with a CVA incidence of 2.6% (24 cases; p < 0.001 versus the remaining 25 of 3,889 [0.6%]). Results of multivariate analysis for total CVA in patients with and without the risk factor are shown in Table 3.
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Cardiopulmonary bypass
Group B patients, who were operated on without CPB, had a global CVA incidence of 0.4% (8 of 1,993; p < 0.001 versus group A, 41 of 2,830 [1.4%]). Multivariate analysis showed that in group B, LOS (OR, 23.0; p = 0.0004), ECV (OR, 4.5; p = 0.0437), and side-clamping (OR, 4.3; p = 0.0492) were independent predictors of higher CVA incidence. In group A patients, risk factors were LOS (OR, 11.1; p < 0.0001), ECV (OR, 4.1; p < 0.001), and hypothermia (OR, 2.4; p = 0.0037).
Early and late mortality
Patients included in the study had a 30-day mortality of 1.8% (n = 87), 1.5% (n = 70) among the patients without and 34.7% (n = 17) among the patients with a postoperative CVA (p < 0.001). Mortality was similar in patients who had early (10 of 24, 41.7%) or late CVA (7 of 25, 28.0%; p = 0.315). Stepwise logistic regression showed that any postoperative CVA was an independent risk factor for higher early mortality (OR, 22.3; p < 0.0001). Global 13-year survival was 88.8% ± 0.9%, 36.7% ± 9.3% in patients who experienced a postoperative CVA and 89.5% ± 0.9% in patients who did not have this complication (p < 0.001; Fig 1).
Survival in patients with early and delayed CVA was similar (32.4% ± 12.0% versus 42.5% ± 12.8%). Cox analysis for time-dependent events showed that postoperative CVA was an important independent risk factor for reduced 13-year survival (hazards ratio, 7.0; p < 0.0001).
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The pathophysiology of this severe complication is complex and multifactorial. Different authors found different risk factors, such as arteriosclerosis of the ascending aorta [2, 3, 7, 8], previous CVA [2, 5, 7–10, 15–17], smoking [8], carotid vascular disease [11], peripheral vascular disease [3, 5, 8, 10, 17], diabetes [2, 5, 8, 10, 16, 17], CPB time [4, 7, 8, 15, 17], LOS [7], hypertension [2, 4, 16], female sex [7], chronic renal failure [4, 5, 8], unstable angina [2], and low ejection fraction [10]. Carotid occlusion was a risk factor for some authors [3], but not for others [11]. Normothermic perfusion, identified as a risk factor by some studies [17, 18] but excluded by others [19], was considered by Gaudino and associates [6] to be responsible for a superior extension of cerebral damage, but this finding was not confirmed by other reports [20]. In our study hypothermic perfusion was related to a higher CVA rate (2.4% versus 1.2%; p = 0.023); multivariate analysis confirmed this finding. Other risk factors, such as age, were constantly present in the great majority of the studies [2–5, 8–10, 15–17], but not in ours. Atrial fibrillation was a risk factor in some reports [7, 21, 22]; however, in our study no correlation between postoperative atrial fibrillation and CVA incidence was found (7 CVAs in 526 patients who experienced postoperative atrial fibrillation, 1.2%, and 43 in 4,297 patients who did not, 1.0%). None of the 68 patients with preoperative atrial fibrillation had any CVA.
Our study demonstrated that four variables were independent risk factors for higher incidence of perioperative or postoperative CVA.
Low output syndrome, present in 90 patients (1.9%), was the strongest one. Critical cerebral perfusion enhances the possibility of focal ischemia and can be at the basis of a postoperative CVA. However, a significant number of these patients (33 of 90, 36.7%) had ECV, a direct expression of diffuse vascular disease, with an incidence higher than in the remaining patients (901 of 4,733, 19.0%; p < 0.001). Multivariate analysis in patients with LOS showed that presence of ECV was the only risk factor for CVA. Indeed, maintenance of a satisfying hemodynamic status is crucial for brain integrity. The impact of LOS is constant in total, early, and delayed CVAs, but is higher in early CVAs, likely because of the direct effects of reduced cerebral perfusion.
Extracoronary vasculopathy was, in our study, an important risk factor. Its action is constant in early and delayed CVA, even if higher in the early phase. It is the sum of other risk factors, such as peripheral vasculopathy, carotid disease, and aortic arteriosclerosis. However, whereas each of the first two variables separately had a direct effect, the latter one had no influence on CVA incidence. Disease of the ascending aorta can, by itself, be an important risk factor [2, 3, 7, 8], but its detection forces the surgeon to consider possible strategies to avoid aortic manipulation [12, 13, 23], such as operation without CPB or arterial cannulation in peripheral sites (eg, femoral or subclavian artery) without cross-clamping. Use of arterial revascularization or proximal anastomosis of veins in nonaortic sites limits the effects of aortic disease on early outcome.
Whereas peripheral vasculopathy had influence only on early CVA, carotid disease was a risk factor for both early and delayed CVA. Both of them are markers of diffuse vasculopathy, with involvement of peripheral cerebral territory. We analyzed more deeply the risk factor carotid disease, which was divided into carotid disease without and with CEA (Table 2). The latter was the strongest one; however, the presence of carotid disease, even if without any necessity of operation, remains related to higher incidence of CVA. Whereas carotid disease can be a sign of diffuse cerebral vasculopathy, CEA of this artery can cause, both immediately and hours after operation, local clotting (perioperative and postoperative changes from hypocoagulation to hypercoagulation can be a predisposing cause) followed by cerebral embolization. Of seven CVAs in patients who had CEA, five cerebral lesions were on the same side of the CEA and two were not. Our findings are similar to those shown by others [24]. However, other authors [11], in a group of patients smaller than ours, found that extracranial carotid stenosis was a risk factor for postoperative CVA, but contemporary CEA was protective. These authors advised prophylactic CEA also in patients with asymptomatic carotid stenosis of at least 75%.
Aortic manipulation is a very strong risk factor for increased incidence of CVA, both early and delayed. When the ascending aorta is manipulated, cerebral embolization can be the consequence. Clamp removal was demonstrated to be the major source of emboli [25]; aortic cannulation gave the same incidence of microemboli as clamp application [26], lower than unclamping. Importance of perfusionist intervention in causing microemboli was also emphasized [26].
Anytime a vessel is manipulated, the possibility of plaque rupture, local intimal damage, and thrombotic phenomena related to coagulation changes during and after the procedure has to be considered. This can cause both early and delayed strokes. Moreover, Ura and colleagues [14] demonstrated that new lesions can be identified by ultrasonography after decannulation, related mainly to cannulation itself or to aortic cross-clamping or side-clamping. Some of these lesions were located opposite from the aortic cannula, suggesting that the probable cause could be the aortic cannula jet. Thus, aortic manipulation can not only act on preexisting lesions, but also cause new ones by itself.
The impact of aortic manipulation in patients with ECV was striking. Among 934 patients with ECV, 624 (66.8%) had some degree of aortic manipulation with 21 CVAs (3.4%) and 310 (33.2%) did not, with 3 CVAs (1.0%; p = 0.029). Aortic manipulation was a CVA predictor in patients with ECV (Table 3). In patients who had no ECV (n = 3,889), 2,666 had some aortic manipulation with 25 CVA (0.9%) and 1,223 did not, with no CVA (0%; p = 0.001). However, the multivariate analysis failed to confirm that in patients without ECV, aortic manipulation is a risk factor, very likely because of the small number of events.
If the different degrees of aortic manipulation are separately evaluated, each of them shows the same effects, higher for cannulation and cross-clamping, and lower for side-clamping (Table 2). Side-clamping is confirmed as a CVA predictor, mainly for the delayed ones; however, this was evident only when CPB was not used. Other authors already advocated the elimination of side-clamping, but only for technical reasons [27]; Aranki and coworkers [28] were not able to demonstrate any reduction in CVA incidence with or without side-clamping. Recently Kim and associates [29] reported that in patients operated on with CPB, single-clamp technique is not protective against CVA in coronary operation, demonstrating that the topic is still controversial. Our results support these conclusions, as in patients operated on with CPB, side-clamping did not add any further risk to CVA incidence. It was an independent predictor only when CPB was not used.
Table 2 shows that it is crucial to avoid any aortic manipulation. If we look at Table 1, CVA incidence in patients operated on with CPB and cross-clamping (Group A2), but without side-clamping, is the same as in patients operated on without CPB (no cannulation and cross-clamping) but with a side clamp used for proximal aortic anastomosis of saphenous vein or radial graft (group A2, 27 of 2,233, 1.2% and group B1, 5 of 460, 1.1%; p = 0.987). This means that CPB, per se, is not related to higher incidence of CVA, but the maneuvers necessary to institute it are. Conversely, myocardial revascularization without CPB does not reduce CVA incidence per se, as previously demonstrated [30], but only when any aortic manipulation is avoided, as in group B2.
However, if myocardial revascularization without CPB can be related to lower incidence of CVA if the aorta is not touched, conversion to CPB during a procedure scheduled without CPB can be extremely dangerous for postoperative CVA (3 of 53, 5.7%, in patients who were converted versus 3 of 1,940, 0.2%, in patients who were not converted; p < 0.001). Nevertheless, even if rapid conversion to CPB is an important risk factor for CVA incidence, the global CVA incidence when CPB is not scheduled (group B; Table 1) is still the lowest one if compared with the use of CPB (and related aortic manipulation). However, conversion to CPB seems to be a risk factor for CVA mainly in patients with ECV, as all 3 CVAs happened among the 20 with ECV, whereas in the remaining 33 no CVA occurred.
The presence of left main coronary artery disease was an independent CVA predictor in patients without ECV. Left main coronary artery disease is related to higher incidence of ECV; of 451 patients with left main coronary artery disease, in 143 (31.7%) ECV was clinically evident, whereas in the remaining 4,372 patients ECV was diagnosed in 791 cases (18.1%; p < 0.001). It is likely that even if ECV is not diagnosed, the presence of left main coronary artery disease can be an indirect sign of some degree of vasculopathy not clinically evident, at the basis of a CVA in particular situations such as during myocardial revascularization.
With regards to CVA timing, all the independent predictors shown in Table 2 for total CVA incidence were also risk factors for early CVA, except side-clamping. In all the analyses performed this risk factor, when present, was active mainly for the delayed CVA. Other risk factors, such as conversion from no CPB to CPB, had an impact only on early and not on delayed CVA, very likely because of hemodynamic instability related to this factor. Other more general risk factors, such as peripheral vasculopathy or carotid disease without need of CEA, acted more on early CVA because of expression of a diffuse vasculopathy, more sensitive to any perioperative hypotension or early hypercoagulability.
In conclusion, postoperative CVAs are a dangerous event after myocardial revascularization, related to higher early and late mortality. Its prevention is a critical feature of coronary operation. Our study reports that preventing LOS is crucial in reducing CVA incidence in any patient, with or without ECV, operated on with or without aortic manipulation and with or without CPB. Avoiding any aortic manipulation is another goal, not always easy to fulfill, but it is valid mainly for patients with ECV. Rapid conversion to CPB can increase CVA incidence, but again mainly in patients with ECV. Cardiopulmonary bypass per se is not a risk factor for higher CVA incidence. If it has to be used, side-clamping does not increase CVA incidence, but, when ECV is present, very likely it does. If CPB is not scheduled, side-clamping for proximal anastomoses is an independent predictor for higher CVA incidence and should be avoided.
In patients with ECV any of the general risk factors increases CVA incidence. Maintaining hemodynamic stability and avoiding any aortic manipulation is crucial in this cohort of patients at high risk for postoperative CVA.
A limitation of this study is that it is a retrospective study that considers 13 years of activity. During this time, surgical strategies changed and could influence directly CVA incidence. No preoperative screening of disease of the ascending aorta was made. Even if some patients had transesophageal echocardiography, epicardial scanning was never used. However, this reflects the reality of the great majority of the operating theaters and, for this reason, the conclusions of this study can be used by the great majority of surgical teams.[31]
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AMI = acute myocardial infarction; BH = beating heart; CABG = coronary artery bypass grafting; CPB = cardiopulmonary bypass;CVA = cerebrovascular accident; ECG = electrocardiograph; IABP = intraaortic balloon pump; OR = operating room.
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75 years