Individualized surgical strategy for the reduction of stroke risk in patients undergoing coronary...

1999;67:1246-1253 Ann Thorac SurgClaudio Pragliola, Rocco Schiavello and Gianfederico Possati

Mario Gaudino, Franco Glieca, Francesco Alessandrini, Carlo Cellini, Nicola Luciani, undergoing coronary artery bypass grafting

Individualized surgical strategy for the reduction of stroke risk in patients

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Individualized Surgical Strategy for the Reductionof Stroke Risk in Patients Undergoing CoronaryArtery Bypass GraftingMario Gaudino, MD, Franco Glieca, MD, Francesco Alessandrini, MD,Carlo Cellini, MD, Nicola Luciani, MD, Claudio Pragliola, MD, Rocco Schiavello, MD,and Gianfederico Possati, MD,Departments of Cardiac Surgery and Anesthesiology, Catholic University, Rome, Italy

Background. This study was designed to evaluate theefficacy of a protocol of systematic screening of theascending aorta and internal carotid arteries and individ-ualization of the surgical strategy to the ascending aortaand internal carotid arteries status in reducing the strokeincidence among patients undergoing coronary arterybypass grafting.

Methods. On the basis of a pre- and intraoperativescreening of the ascending aorta and internal carotid arter-ies, 2,326 consecutive patients undergoing coronary arterybypass grafting were divided in low, moderate, and highneurologic risk groups. In the high-risk group dedicatedsurgical techniques were always adopted and the reductionof the neurologic risk was considered more important thanthe achievement of total revascularization.

Results. The incidence of perioperative stroke in thehigh-risk group was similar to those of the other twogroups (1.1 versus 1.3 and 1.1%, respectively; p 5 notsignificant); however, angina recurrence was significantlymore frequent in the high-risk group.

Conclusions. The described strategy allows a low rateof perioperative stroke in high-risk patients undergoingcoronary artery bypass grafting. Whether the reductionof the neurologic risk outweighs the benefits of completerevascularization remains to be determined.

(Ann Thorac Surg 1999;67:1246–53)© 1999 by The Society of Thoracic Surgeons

Postoperative stroke represents one of the most severecomplications of coronary artery operations and, as

a result of the progressive aging of the population re-ferred for cardiac operations, it will probably tend toincrease in frequency in the near future. For this reason,the identification of the surgical strategies that can allowa reduction of postoperative neurologic events in thehigh-risk population is a priority objective of clinicalresearch in cardiac surgery.

In this report we analyze our 4 years of prospectiveexperience with the use of an integrated protocol aimedat reducing the incidence of cerebrovascular events inpatients undergoing coronary artery bypass proceduresby means of the systematic screening of the aorta andinternal carotid arteries and adoption of dedicated sur-gical strategies in case of atherosclerotic disease of one orboth vascular districts.

Patients and Methods

Patient PopulationThis study was prospectively started in October 1993 toevaluate the possibility of reducing the incidence of

cerebrovascular complications in patients undergoingcoronary artery bypass grafting by means of a protocol ofsystematic screening of the ascending aorta and theinternal carotid arteries and modification of the surgicalstrategy on the basis of the status of these two vasculardistricts.

For the purpose of this report, data collection ended inJanuary 1997. All cases submitted to isolated coronaryartery bypass (ie, not associated with any other cardiacprocedures) on elective or urgent basis at our institutionin this time frame were considered.

Emergency cases were not included due to the impos-sibility of performing a complete preoperative evaluationof the carotid arteries. Twenty-one elective or urgentpatients who could not complete this evaluation werealso excluded from the data analysis. Overall, 2,326patients were included.

During the study period no major modifications in thesurgical and anesthesiologic technique were adopted.

Preoperative and Intraoperative EvaluationFollowing a protocol in use at our Institution since 1990,all the 2,326 patients were submitted to the following tests:

Accepted for publication Oct 16, 1998.

Address reprint requests to Dr Gaudino, Divisione di Cardiochirurgia,Policlinico Universitario A. Gemelli, Largo A. Gemelli 8, 00168 Rome,Italy; e-mail: [email protected].

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© 1999 by The Society of Thoracic Surgeons 0003-4975/99/$20.00Published by Elsevier Science Inc PII S0003-4975(99)00151-4



ECHO-DOPPLER EVALUATION OF THE INTERNAL CAROTID ARTERIES.

Extracranic carotid arteries were evaluated by color flowduplex scanning study; B-mode and color flow images ofthe common, external, and internal carotid arteries wereobtained in longitudinal and transverse planes. Presenceof plaques was noted and reduction in the cross-sectionalarea of the lumen was calculated. Doppler velocity spec-tra were recorded from each of these vessels, maintainingthe angle of insonation as close to 60 degrees as possible.The highest peak systolic velocity and end-diastolic ve-locity were calculated. According to the flow velocitycriteria, severity of internal carotid artery stenosis wasgraded as # 50% when the peak systolic velocity was #120 cm/s, between 50% and 80% when the peak systolicvelocity was . 120 cm/s, and $ 80% when the peaksystolic velocity was . 120 cm/s and the end-diastolicvelocity was . 120 cm/s [1].

Patients were then classified in four groups: no disease,slight, moderate, or severe carotid artery disease (seeAppendix). In patients with severe stenosis a preopera-tive carotid angiography was always performed.

EVALUATION OF THE ASCENDING AORTA. To identify the pres-ence of atherosclerotic lesions of the ascending aorta thepreoperative chest roeutgengram and the coronary an-giography were carefully evaluated. In addition, intraop-erative digital palpation of the aorta was always per-formed following a described methodology [2] and thepatients were classified in four groups according to thescale proposed by Mills and Everson [2] (see Appendix):no disease, mild, moderate, or severe ascending aortaatherosclerosis. In 715 patients operated during the lastpart of the series intraoperative ultrasonographic exam-ination of the ascending aorta was also performed andthe atherosclerotic lesions were classified according tothe criteria described by Wareing and coauthors [3] (seeAppendix).

ECHO-DOPPLER EVALUATION OF THE ILIAC AND FEMORAL ARTERY.

Patients with a clinical history of peripheral vasculopathywere also submitted to examination of the iliac andcommon femoral arteries following the described Echo-Doppler methodology.

On the basis of this preoperative assessment patientswere divided in three categories of neurologic risk (incase of concomitant aortic and carotid disease of differentgravity, classification was based on the most severelesion): Patients at low risk: patients with no or slightinternal carotid artery disease and with no or slightdisease of the ascending aorta. Overall, this group in-cluded 1,602 of the 2,326 patients (68.8%). Patients atmoderate risk: patients with moderate internal carotidartery stenosis or moderate atherosclerosis of the ascend-ing aorta. In total 380 patients were assigned to this group(16.3% of the overall population). In particular, moderatecarotid artery stenosis was present in 239 patients (10.2%of the total) and moderate ascending aorta atherosclero-sis in 116 (4.9%); in 25 patients (1.0%) the two pathologiescoexisted. Patients at high risk: patients with severeinternal carotid artery stenosis (either asymptomatic or

symptomatic) or severely atherosclerotic ascendingaorta. Globally 344 patients (14.7% of the total popula-tion) were assigned to this category. In particular, severecarotid disease was present in 196 patients (8.4%), severeaortic disease in 137 (5.8%), and the two conditionscoexisted in 11 patients (0.4%).

The preoperative clinical and angiographic character-istics of the patients of the three categories are shown inTable 1.

The moderate and high-risk patients were significantlyolder than low-risk patients. In the high-risk group therewas also a greater incidence of diabetes, smoking history,unstable angina, peripheral vasculopathy, and previouscerebrovascular accidents. The incidence of severe aorticand internal carotid artery disease in relation to the ageof patients is summarized in Figure 1. As expected, olderpatients had a significantly higher incidence of severeatherosclerosis of both the ascending aorta and thecarotid arteries.

Surgical StrategyAll the operations were performed by five surgeons usingstandardized techniques. Patients of the different catego-ries were treated using different surgical strategies.

PATIENTS AT LOW RISK. After median sternotomy and peri-cardiotomy, cardiopulmonary bypass was established bycannulating the right atrium and the ascending aorta.Normothermic systemic perfusion was used and myocar-dial protection was achieved by intermittent isothermicanteretrograde blood cardioplegia; patients were activelyrewarmed if their nasopharingeal temperature fell below34°C and mean nasopharingeal temperature in thisgroup was 36.3 6 0.8°C. Mean arterial pressure duringcardiopulmonary bypass was maintained between 50 and

Table 1. Preoperative Characteristics of Patients of the ThreeRisk Groups

CharacteristicsLow-Risk

GroupModerate-Risk

GroupHigh-Risk

Group

No. of patients 1,602 380 344Mean age (y) 59.6 6 4.1 68.9 6 5.3a 79.3 6 4.6a,b

Male/female 4.5/1 5/1 4.4/1Cardiac risk factors

Diabetes 299 (18.6%) 75 (21.8%) 111 (32.2%)a,b

Smoking 972 (60.6%) 238 (62.6%) 246 (71.5%)a,b

Dyslipidemia 911 (56.8%) 214 (56.3%) 189 (54.9%)Hypertension 311 (19.4%) 81 (21.3%) 81 (23.5%)

Unstable angina 307 (19.1%) 69 (18.1%) 131 (38.0%)a,b

Previous AMI 1001 (62.4%) 257 (67.6%) 228 (66.2%)No. of diseased

vessels2.93 6 0.8 2.88 6 0.9 2.91 6 0.8

Peripheralvasculopathy

59 (3.6%) 31 (8.1%)a 68 (19.7%)a,b

Previous CVA 174 (10.8%) 47 (12.3%) 99 (28.7%)a,b

a p # 0.01 versus low-risk group; b p # 0.01 versus moderate-riskgroup.

AMI 5 acute myocardial infarction; CVA 5 cerebrovascular accident.

1247Ann Thorac Surg GAUDINO ET AL1999;67:1246–53 REDUCTION OF STROKE RISK IN CABG PATIENTS



70 mm Hg; volume infusion or vasopressors (phenyleph-rine) were used in case of hypotension. Proximal anddistal anastomoses were always performed during asingle period of aortic cross-clamping.

PATIENTS AT MODERATE RISK. These patients were also oper-ated using the conventional technique described, how-ever, due to the reported concerns on the neurologicsafety of normothermic cardiopulmonary bypass andretrograde cardioplegia [4, 5], patients of this group werealways operated using mildly hypothermic systemic per-fusion (28°C) and isothermic intermittent antegradeblood cardioplegia; mean nasopharingeal temperature inthis group was 27.4 6 0.9°C. In cases with moderate aorticdisease care was paid to avoid the atherosclerotic areasduring cannulation and cross-clamp.

PATIENTS AT HIGH RISK. We adopted dedicated surgical strat-egies for these patients. In particular, in patients withsevere monolateral internal carotid artery stenosis simul-taneous carotid endoarterectomy and coronary arterybypass was performed in case of unstable angina (n 591), whereas a staged strategy (carotid endoarterectomyperformed before myocardial revascularization) wasadopted in patients with stable angina (86 patients).During simultaneous operations the carotid endoarterec-tomy was always carried out before median sternotomy;for both concomitant and staged procedures an intralu-minal carotid shunt was used and myocardial revascu-larization was performed in condition of hypothermicsystemic perfusion. Among patients who underwentstaged operations the mean interval between the carotidand coronary operations was 14.9 6 8.7 days. Patientswith bilateral carotid artery stenosis and stable angina(n 5 15) were treated by carotid endoarterectomy of themost diseased site followed by combined operation onthe other carotid and the coronary arteries (performedwithin 2 to 3 weeks), whereas the patients with bilateralcarotid disease and unstable cardiac symptoms (n 5 4)were treated by simultaneous carotid endoarterectomy ofthe most severe lesion and coronary artery bypass, fol-lowed after 2 to 3 weeks by surgical treatment of the othercarotid artery.

In patients with severely atherosclerotic ascendingaorta we adopted the no-touch technique described byMills and Everson [2] and Suma [6] when an arterial

cannulation side (aortic arch or femoral artery) could befound (74 patients). In this instance hypothermic cardio-pulmonary bypass was established between the rightatrium and the aortic arch (n 5 21) or the commonfemoral artery (n 5 53) and a left ventricle vent wasinserted through the right superior pulmonary vein.Aortic cross-clamp and cardioplegic delivery wereavoided and ventricular fibrillation was induced electri-cally. The target vessels were occluded at the level of theanastomotic site using 5-0 Prolene (Ethicon Inc, Sommer-ville, NJ) or silicone elastomer stitches passed around theartery and pedicled arterial grafts were used. In 15patients myocardial revascularization had to be com-pleted with a saphenous vein proximally anastomosed tothe innominate artery. When aortic arch and femoralcannulation was impossible (63 patients) the operationwas performed without the use of cardiopulmonary by-pass, following the technique described by Buffolo andcolleagues [7]. In these patients all-arterial revasculariza-tion was performed using the in situ internal thoracic andgastroepiploic arteries and the radial artery proximallyanastomosed to an internal thoracic artery graft at Y. In 7patients an integrated approach (surgical grafting of theleft anterior descending and subsequent percutaneousangioplasty of the other target vessels) had to be useddue to the technical impossibility of using more than onearterial graft. The 11 patients in whom severe disease ofthe ascending aorta and internal carotid arteries coex-isted had all unstable angina and underwent simulta-neous carotid endoarterectomy and myocardial revascu-larization using either the no-touch or the no-pumptechnique (7 and 4 patients, respectively).

Main operative data of the different groups are re-ported in Table 2. As a direct consequence of our policyof privileging the reduction of the neurologic risk atexpense of the completeness of the myocardial revascu-larization, the high-risk patients received a significantlylower number of grafts and had an higher rate of incom-plete coronary grafting.

Evaluation of Postoperative Neurologic ComplicationsPostoperative neurologic complications were classifiedaccording to the definitions given in the Appendix; pa-tients with transient ischemic attacks were not consid-ered in the data analysis.

Fig 1. Distribution of severe carotid and ascending aorta disease inthe different age groups. (AAD 5 ascending aorta atheroscleroticdisease; ICAD 5 internal carotid artery atherosclerotic disease.)

Table 2. Operative Data in the Three Risk Groups

VariablesLow-RiskPatients

Moderate-RiskPatients

High-RiskPatients

Aortic cross-clamptime (min)

52 6 16 51 6 13 41 6 14a,c

CPB time (min) 79 6 18 78 6 16 68 6 17a,b,c

Bypass/patient 3.21 6 0.5 3.18 6 0.3 2.02 6 0.4c

Incompleterevascularization

119 (7.4%) 37 (9.7%) 96 (27.9%)c

a In the 196 patients in whom aortic cross-clamp was used; b In the 277patients in whom CPB was used; c p # 0.01 versus low and moderate-risk groups.

CPB 5 cardiopulmonary bypass.

1248 GAUDINO ET AL Ann Thorac SurgREDUCTION OF STROKE RISK IN CABG PATIENTS 1999;67:1246–53



Following a protocol in use at our institution since 1990,a neurologic evaluation was always performed by acardiac anesthesiologist (blinded to the pre- and intraop-erative evaluation) at the moment of the awakening ofthe patient from the anesthesia. In cases of neurologicabnormalities a complete neurologic examination wasperformed by a consultant neurologist immediately afterthe onset of symptoms, 24 hours later, at regular intervalof 1 or more days (depending on the clinical status), andat discharge. In case of stroke the neurologic outcomewas assessed using the Glasgow Outcome Scale [8]. TheGlasgow Outcome score was assigned in concomitancewith the neurologic evaluations by a neurologist and acardiac anesthesiologist; disagreements were resolved byconsensus after a common reevaluation. In patients withclinical evidence of neurologic complications of any typebrain computed tomographic scans were performed im-mediately after the evidence of symptoms, 24 to 48 hourslater, after any change in the neurologic status, and theday before discharge. All scans were performed prospec-tively and independently evaluated by two expert neu-

roradiologists; disagreements were resolved by commonreexamination. In case of computed tomographic evi-dence of recent stroke, lesion size was measured by aruler to the nearest half millimeter in two dimensionsand multiplied by the thickness of the slice following apreviously described methodology [9, 10]. For multiple orirregularly shaped lesions the sum of the single ischemicareas was calculated. All neurologic measurements wereprospectively entered in a computerized database.

Follow-upAll patients were regularly submitted to clinical exami-nation at our institution 1 and 6 months after operationand then every year thereafter. A stress myocardialscintigraphy was obtained in all patients 6 months post-operatively and every year thereafter. In case of clinicalor instrumental suspect of residual myocardial ischemiaor angina recurrence, reangiography was always pro-posed to the patient.

Statistical AnalysisData are expressed as mean value 6 1 standard devia-tion. For statistical analysis qualitative data were com-pared using the x2 test with Bonferroni’s correction.Parametric quantitative data were compared by two-wayanalysis of variance; for p level less than 0.05 comparisonsbetween groups were carried out using the unpaired tStudent’s test with Bonferroni’s correction. Nonparamet-ric quantitative data were compared by Friedman’s test;for p level less than 0.05 comparisons between groupswere carried out using the test Mann-Whitney U test withBonferroni’s correction. A p value less than 0.05 wasconsidered significant.

Results

Mortality and MorbidityMortality and morbidity data of the patients of thedifferent risk categories are summarized in Table 3. In the

Table 3. Postoperative Mortality and Morbidity in the ThreeRisk Groups

Variables

Low-Risk

Group

Moderate-Risk

Group

High-Risk

Group

No. of patients 1,602 380 344Operative deaths 21 (1.3%) 6 (1.5%) 9 (2.6%)Postoperative complications

Sepsis 2 (0.1%) 1 (0.2%) 2 (0.5%)IABP use 21 (1.3%) 4 (1.0%) 4 (1.1%)Perioperative AMI 17 (1.0%) 5 (1.3%) 5 (1.4%)Renal Insufficiency 13 (0.8%) 4 (1.0%) 12 (3.4%)a

Revision for bleeding 89 (5.5%) 22 (5.7%) 32 (9.3%)

a p , 0.01 versus low-risk group.

AMI 5 acute myocardial infarction; IABP 5 intraaortic balloon pump.

Table 4. Postoperative Mortality and Morbidity in the High-Risk Group in Relation to the Surgical Strategy Used

CharacteristicsNo-TouchTechnique

No-Pumptechnique

SimultaneousCEA 1CABG

StagedCEA 1CABG

No-Touch 1Simultaneous

CEA

No-Pump 1Simultaneous

CEA

Staged CEAand CEA 1

CABG

Staged CEA1 CABG and

CEA

Patients 74 63 91 86 7 4 15 4Operative

deaths2 (2.7%) 0 2 (2.21%) 3 (3.4%) 1 (14.2%) 0 1 (6.6%) 0

PostoperativecomplicationsSepsis 1 (1.3%) 0 0 0 1 (14.2%) 0 0 0IABP use 1 (1.3%) 0 1 (1.0%) 0 1 (14.2%) 0 1 (6.6%) 0Perioperative

AMI6 (8.1%) 1 (1.5%) 1 (1.0%) 1 (1.1%) 0 0 1 (6.6%) 0

Renalinsufficiency

7 (9.4%) 0 6 (6.5%) 2 (2.3%) 1 (14.2%) 1 (25.0%) 0 0

Revision forbleeding

6 (8.1%) 7 (11.1%) 17 (18.6%) 0 1 (14.2%) 1 (25.0%) 0 0

AMI 5 acute myocardial infarction; CABG 5 coronary artery bypass grafting; CEA 5 carotid endoarterectomy; IABP 5 intraaortic balloonpump.




low-risk group the causes of death were stroke (8 pa-tients), myocardial infarction (9), multiorgan failure (2),gastrointestinal complications and pulmonary embolism(1 patient each).

In the moderate-risk category the 6 deaths were due tostroke (2 patients), perioperative myocardial infarction,renal failure, untractable coagulopathy, and massive in-testinal infarction (1 patient each), whereas among thehigh-risk patients the 9 deaths were due to myocardialinfarction (3 patients), stroke (1), multiorgan failure (2),sepsis, hepatic insufficiency, and intestinal infarction (1patient each).

No significant difference in mortality was found be-tween the three groups; renal insufficiency was the onlypostoperative complications significantly more frequentin the high-risk population. Postoperative mortality andmorbidity of patients of the high-risk group in relation tothe different surgical strategy used are shown in Table 4.

Neurologic ComplicationsOverall, 27 patients suffered a perioperative stroke(1.1%). Twenty-one of the 27 strokes occurred intraoper-atively and 6 (22.2%) in the postoperative period. Thestroke incidence was not significantly different betweenthe three risk groups (Table 5); in fact, 18 events werereported in the low-risk group (1.1%; 15 intraoperativeand 3 postoperative), five in the moderate-risk group(1.3%; 4 intraoperative and 1 postoperative), and four inthe high-risk group (1.1%; 2 intra- and 2 postoperative).

The mean Glasgow Outcome Scale score and thecomputed tomographic extension of the brain lesionwere similar in the three risk categories ( p 5 notsignificant).

In the moderate-risk group all four episodes of intra-operative stroke occurred in patients with moderateaortic disease (4 of 116, 3.4%; Fig 2), whereas the onlypostoperative stroke was reported in 1 of the 25 patientsof concomitant carotid and aortic disease (1 of 25, 4.0%);there were no case of perioperative stroke among pa-tients with moderate carotid stenosis (n 5 239).

The difference in incidence of intraoperative strokebetween patients with aortic and carotid disease wasstatistically significant ( p , 0.01), whereas no differenceswas found with regard to the postoperative events.

In the high-risk group the two intraoperative strokeoccurred in 1 of the 137 patients with severe ascendingaorta atherosclerosis (0.7%) and in 1 of the 196 patientswith severe carotid stenosis (0.5%), whereas the twopostoperative events were reported in 1 patients withsevere carotid disease (again 0.5%) and in 1 patients withsevere aortic atherosclerosis (again 0.7%); there were nocase of perioperative stroke among patients with con-comitant carotid and aortic disease (n 5 11). In this groupno significant difference in the incidence of intra- andpostoperative events between patients with carotid andaortic disease could be demonstrated (Fig 3).

In the high-risk series the four strokes occurred in 1patient with simultaneous carotid endoarterectomy andmyocardial revascularization (1 of 95, 1.0%; intraopera-tively), in 1 patient who underwent no-pump revascular-ization (1 of 63, 1.5%; postoperatively), in 1 patient oper-ated using the no-touch technique (1 of 74, 1.3%;intraoperatively), and in one case of staged carotid endo-arterectomy and myocardial revascularization (1 of 101,0.9%; postoperatively) (Table 6).

No cases of perioperative stroke were reported amongpatients who underwent simultaneous no-pump or no-touch and carotid procedures, carotid endoarterectomyfollowed by carotid and coronary operation, or stagedcarotid and coronary procedure followed by endoarter-ectomy of the other carotid artery.

Follow-upClinical follow-up was 98.3% complete (2,253 of 2,290patients). Mean follow-up time for the overall populationwas 35 6 11 months without significant differences inlength between the three groups (38 6 12 months in thelow, 39 6 8 in the moderate, and 38 6 10 in the high-riskgroup).

During the follow-up there were 37 noncardiac death(7 in the low, 16 in the moderate, and 14 in the high-riskgroup), mainly from cancer (15 patients, 4 in the low, 6 inthe moderate, and 5 in the high-risk group) and cerebro-vascular accidents (8 patients, 3 in the low, 3 in themoderate, and 2 in the high-risk group).

Fig 2. Postoperative neurologic outcome in the moderate-risk group inrelation to the location of atherosclerotic lesions. (AAD 5 ascendingaorta atherosclerotic disease; ICAD 5 internal carotid artery athero-sclerotic disease). *p , 0.05 versus the other two groups.

Table 5. Incidence of Perioperative Stroke in the Three RiskGroups

Variables

Low-RiskPatients

(n 5 1602)

Moderate-RiskPatients

(n 5 380)

High-RiskPatients

(n 5 344)

Intraoperative stroke 15 (0.9%) 4 (1.1%) 2 (0.5%)Postoperative stroke 3 (0.1%) 1 (0.2%) 2 (0.5%)Total 18 (1.1%) 5 (1.3%) 4 (1.1%)Mean GOS score 2.50 6 1.59 2.40 6 1.34 2.50 6 1.00Mean CT extension of

the ischemic lesion(mm3)

7240 6 2016 6921 6 1842 7387 6 1959

All p values not significant.

CT 5 computed tomography; GOS 5 Glasgow Outcome Scale.




The rate of freedom from clinical or instrumentalangina recurrence and cardiac death was significantlyhigher in the low and moderate-risk categories: 98.4% inlow-risk patients (1,549 of 1,574), 98.0% in the moderate(351 of 358), and 85.3% in the high-risk cases (274 of 321)( p , 0.01).

Comment

In 1993 we started this prospective study with the aim ofevaluating the possibility of reducing the incidence ofneurologic events in patients undergoing isolated coro-nary artery bypass grafting by means of a protocol ofsystematic pre- and intraoperative evaluation of the aortaand the carotid arteries and adoption of dedicated surgi-cal strategies in cases of severe atherosclerosis of one orboth vascular districts. Using this approach we achieveda 1.0% global stroke incidence and a rate of cerebrovas-cular complications in the high-risk group not signifi-cantly superior to that of the low-risk cases (Table 5) andconsiderably inferior to that expected on the basis of thecurrent literature.

In fact, Roach and coauthors [11] in a recent largeprospective multicenter trial found that perioperativecerebrovascular accidents occurred in 7.8% of patientswith carotid disease versus 2.5% of cases without thischaracteristic and the Buffalo Cardiac Cerebral StudyGroup estimated a 6.01 odds ratio for postoperativestroke in patients with carotid stenosis $ 50% [12].Likewise, McKhann and colleagues [13] reported peri-

operative cerebrovascular accidents in 15.5% of theirpatients in whom a carotid bruit was identified preoper-atively and Reed and associates [14] showed in a case-control study that the presence of clinically diagnosedcarotid pathology increases the risk of perioperativestroke or transient ischemic attack by 3.9-fold. On theother hand, Mickleborough and colleagues [15] reportingon 1,631 consecutive patients undergoing coronary arterybypass procedures reported a stroke incidence of 10% inpatients with and 0.9% in patients without intraoperativeevidence of atherosclerotic ascending aorta ( p , 0.01).Similarly, Gardner and co-workers [16] found that peri-operative stroke occurred in 14% of patients with aorticdisease compared to 3% of cases without evidence ofdiseased aorta and Lynn and associates [17], using logis-tic regression analysis, identified aortic calcification as anhighly significant risk factor for postoperative stroke in aseries of 1,000 consecutive coronary patients. The lowincidence of cerebrovascular events in all groups of ourseries (despite the fact that our protocol did not take intoconsideration any other risk factors for perioperativestroke) suggests that atherosclerotic disease of the as-cending aorta and internal carotid arteries, besides beingthe only factors susceptible of surgical manipulation, isprobably the major determinant of the stroke incidencein patients undergoing coronary artery bypass grafting.

A limitation of our study relies in the method used toevaluate the ascending aorta. In the majority of ourpatients the assessment of the aortic status was per-formed by intraoperative palpation, a technique that hasalready been shown to be quite insensitive in the dem-onstration of ascending aorta atherosclerosis [18, 19]. Infact, when analyzing the neurologic outcome of themoderate-risk population in relation to the type andseverity of the atherosclerotic lesions, it is evident that allthe cases of intraoperative strokes of this group occurredin patients with (presumed) moderate aortic atheroscle-rosis (Fig 2). It seems likely that in these patients a moresevere disease of the ascending aorta has been unrecog-nized and the patients have been undertreated; theadoption of dedicated strategies even in these instancescould have probably led to a further reduction of the rateof perioperative neurologic complications. For this rea-son we decided to use routine intraoperative echographicexamination of the ascending aorta in the last part of ourstudy.

Fig 3. Postoperative neurologic outcome in the high-risk group inrelation to the location of atherosclerotic lesions. (AAD 5 ascendingaorta atherosclerotic disease; ICAD 5 internal carotid artery athero-sclerotic disease.)

Table 6. Incidence of Perioperative Stroke in the High-Risk Group With Reference to the Surgical Strategy Used

VariablesNo-TouchTechnique

No-PumpTechnique

SimultaneousCEA 1CABG

StagedCEA 1CABG

No Touch 1Simultaneous

CEA

No-Pump 1Simultaneous

CEA

Staged CEAand CEA 1

CABG

Staged CEA1 CABGand CEA

Patients 74 63 95 101 7 4 15 4Intraoperative

stroke1 0 1 0 0 0 0 0

Postoperativestroke

0 1 0 1 0 0 0 0

Total 1 (1.3%) 1 (1.5%) 1 (1.0%) 1 (0.9%) 0 0 0 0

CABG 5 coronary artery bypass grafting; CEA 5 carotid endoarterectomy.




The technical solutions that we applied have beenextensively described and are part of the knowledge of allcardiac surgeons; however, we concentrate our effort onthe careful evaluation of each case and on the systematicindividualization of the surgical approach to the clinicaland anatomic condition of every single patient. In thisperspective some patients at high risk were treated usingintegrated techniques (surgical and percutaneous inter-ventions) and, more in general, the completeness ofsurgical revascularization (once that the left anteriordescending was protected by a mammary graft) wasjudged less important that the reduction of the neuro-logic risk. As a consequence, patients of the high-riskcategory received a significantly inferior number ofgrafts, had an higher rate of incomplete revascularization(Table 2), and an inferior degree of freedom from isch-emia at midterm follow-up. Whether the reduction of theperioperative neurologic risk outweighed the benefits ofcomplete myocardial revascularization (especially inthese older patients with reduced functional capacities)and whether an incomplete grafting limited to the mostimportant vessels can be accepted in these instances is animportant question that requires further extensive inves-tigation. In this regard, it is important to underscore thata considerable part of the cases of ischemia recurrence inthe high-risk group were detected only instrumentally(by means of stress myocardial scintigraphy) and affectedonly marginally the patients’ quality of life (whereas aperioperative stroke would probably have more severeconsequences on the patients’ physical and social status).It is possible that in a near future the no-pump grafting ofall the target vessels with pedicled arterial conduits willbecome a real possibility, and will represent the idealsurgical solution in this setting. However, at presenttechnical and technological improvements are neededbefore a safe introduction of this strategy into the every-day clinical practice.

Our policy in dealing with combined monolateral ca-rotid and coronary disease was to adopt simultaneouscarotid endoarterectomy and myocardial revasculariza-tion in patients with unstable angina and a staged pro-cedure (the carotid endoarterectomy performed beforethe coronary revascularization) in patients in more stablecardiac conditions. Patients with concomitant bilateralcarotid artery stenosis and stable angina were treated bycarotid endoarterectomy of the most diseased site fol-lowed by combined operation on the other carotid andthe coronary arteries, whereas the patients with bilateralcarotid disease and unstable cardiac symptoms weretreated by simultaneous carotid endoarterectomy of themost severe lesion and coronary artery bypass, followedby surgical treatment of the other carotid artery.

This approach allowed a safe and effective treatment ofconcomitant carotid and coronary disease, leading toacceptable rates of perioperative stroke and myocardialinfarction in all groups of patients (Tables 4 and 6).

In conclusion, our experience demonstrates that it ispossible to achieve a low rate of perioperative cerebro-vascular complications in high-risk patients undergoingisolated coronary artery bypass grafting with the use of

an integrated protocol of systematic evaluation of theascending aorta and internal carotid arteries and adop-tion of dedicated surgical strategies in case of atheroscle-rotic disease of one or both of these vascular districts. Itis likely that in the next decade the adoption of this typeof policy and a continuous effort to tailor the surgicalstrategy to the individual characteristics of the patientwill play a key role in the necessary effort of providingacceptable risk procedures to an increasingly older pop-ulation with a growing rate of associated noncardiacpathologies.

References

1. Roederer GO, Langlois YE, Jager KA, Lawrence RJ, Pri-mozich JT, Phillips DJ. A simple spectral parameter foraccurate classification of severe carotid disease. Bruit 1984;8:174–8.

2. Mills NL, Everson CT. Atherosclerosis of the ascending aortaand coronary artery bypass. J Thorac Cardiovasc Surg 1991;102:546–53.

3. Wareing TH, Davila-Roman VG, Daily BB, et al. Strategy forthe reduction of stroke incidence in cardiac surgical patients.Ann Thorac Surg 1993;55:1400–8.

4. Martin TD, Craver JM, Gott JP, et al. A prospective, random-ized trial of retrograde warm blood cardioplegia: myocardialbenefit and neurologic threat. Ann Thorac Surg 1994;57:298–304.

5. Guyton RA, Mellitt RJ, Weintraub WS. A critical assessmentof neurological risk during warm heart surgery. J Card Surg1995;10:488–92.

6. Suma H. Coronary artery bypass grafting in patients withcalcified ascending aorta: the no-touch technique. Ann Tho-rac Surg 1989;48:728–30.

7. Buffolo E, Andrade JCS, Branco JNR, et al. Myocardialrevascularization without extracorporeal circulation. EurJ Cardio-thorac Surg 1990;4:504–8.

8. Jennett J, Bond M. Assessment of outcome after severe braindamage. Lancet 1975;1:480–4.

9. Petersen P, Madsen EB, Brun B, Pedersen F, Gyldensted C,Boysen G. Silent cerebral infarction in chronic atrial fibril-lation. Stroke 1987;18:1098–100.

10. Petersen P, Pedersen P, Johnsen A, et al. Cerebral computedtomography in paroxysmal atrial fibrillation. Acta NeurolScand 1989;79:482–6.

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12. Ricotta JJ, Faggioli GL, Castilone A, Hassett JM, for theBuffalo Cardiac Cerebral Study Group. Risk factors forstroke after cardiac surgery: Buffalo Cardiac Cerebral StudyGroup. J Vasc Surg 1995;21:359–64.

13. McKhann GM, Goldsborough MA, Borowicz LM, et al.Predictors of stroke risk in coronary artery bypass patients.Ann Thorac Surg 1997;63:516–22.

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Appendix. Definitions

Neurologic Complications

Intraoperative stroke was defined as a new focal neurologicdeficit or coma associated with computed tomographic scandemonstration of recent ischemic cerebral lesion who be-came evident at the moment of the awakening of thepatient from the anesthesia and lasted more than 24 hours.

Postoperative stroke was defined as a new focal neurologicdeficit or coma lasting more than 24 hours and associatedwith computed tomographic scan evidence of recent isch-emic cerebral lesion who occurred after a normal awaken-ing from the anesthesia and a normal postoperative neuro-logic status.

Transient ischemic attack was defined as the onset (either atthe awakening of the patient or after a normal postoperativeperiod) of a new neurologic deficit lasting less than 24 hoursand associated with normal brain computed tomographicscan

Previous cerebrovascular events was defined as an anamnestichistory of either overt stroke or reversible cerebral ischemicattacks.

Internal carotid artery disease was graded on the basis of thepreoperative echo-Doppler in absent, slight (mono or bilateralstenosis #50%), moderate (mono or bilateral stenosis between50% and 80%), or severe (mono or bilateral stenosis #80%)disease. In cases of bilateral carotid artery stenoses of differentdegrees the classification was based on the most severe lesion.

Ascending aorta disease was graded according to Mills andEverson [2] in absent, mild (small diseased areas on the aorta thatcould easily be avoided with the aortic cannula and bypassgrafts), moderate (disease extensive enough to cause concern forpossible embolization, yet adequate soft, disease-free areascould be found for cannulation or placement of bypass grafts), orsevere (clearly significant circumferential disease that wouldnecessitate aortic cannulation, aortic cross-clamping and place-ment of bypass grafts into diseased ascending aorta). In patientsin whom intraoperative ultrasonographic examination was usedthe ascending aorta and the proximal aortic arch were divided inthree equal segments in the coronal plane (proximal, middle,and distal) and the atherosclerotic lesions were classified ac-cording to the criteria described by Wareing and co-workers [3]:no disease, mild (localized thickening #3 mm in the three seg-ments), moderate (intimal thickening 3 to 5 mm in one or moresegments), or severe (intimal thickening .5 mm in one or moresegments or the presence of marked calcification, protruding ormobile atheroma, ulcerated plaques, thrombi, or circumferentialinvolvement of most of all the ascending aorta) disease.

Neurologic outcome of patients who suffered a stroke wasgraded according to the Glasgow Outcome Scale [8] as follows:1, death; 2, persistent vegetative state; 3, severe disability; 4,moderate disability; and 5, good recovery.




1999;67:1246-1253 Ann Thorac SurgClaudio Pragliola, Rocco Schiavello and Gianfederico Possati

Mario Gaudino, Franco Glieca, Francesco Alessandrini, Carlo Cellini, Nicola Luciani, undergoing coronary artery bypass grafting

Individualized surgical strategy for the reduction of stroke risk in patients

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