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  • 1. ORIGINAL CONTRIBUTIONStrokes After Cardiac Surgery and Relationshipto Carotid StenosisYuebing Li, MD, PhD; Debra Walicki, MT; Claranne Mathiesen, RN; Donna Jenny, RN;Qiang Li, MD; Yevgeniy Isayev, MD; James F. Reed III, PhD; John E. Castaldo, MDObjective: To critically examine the role of significant significant carotid stenosis. In 60.0% of cases, strokes iden-carotid stenosis in the pathogenesis of postoperative stroke tified via computed tomographic head scans were not con-following cardiac operations. fined to a single carotid artery territory. According to clini- cal data, in 94.7% of patients, stroke occurred withoutDesign: Retrospective cohort study. direct correlation to significant carotid stenosis. Under- going combined carotid and cardiac operations in-Setting: Single tertiary care hospital. creases the risk of postoperative stroke compared with patients with a similar degree of carotid stenosis but whoParticipants: A total of 4335 patients undergoing coro- underwent cardiac surgery alone (15.1% vs 0%; P=.004).nary artery bypass grafting, aortic valve replacement, orboth. Conclusions: There is no direct causal relationship be- tween significant carotid stenosis and postoperative strokeMain Outcome Measures: Incidence, subtype, and in patients undergoing cardiac operations. Combining ca-arterial distribution of stroke. rotid and cardiac procedures is neither necessary nor ef-Results: Clinically definite stroke was detected in 1.8% fective in reducing postoperative stroke in patients withof patients undergoing cardiac operations during the same asymptomatic carotid stenosis.admission. Only 5.3% of these strokes were of the large-vessel type, and most strokes (76.3%) occurred without Arch Neurol. 2009;66(9):1091-1096 C EREBROVASCULAR COMPLI- Despite this lack of evidence, com- cations following car- bined carotid and cardiac surgical proce- diac surgical procedures dures are performed frequently in an ef- are a major source of mor- fort to reduce the incidence of postoperative bidity and mortality. The stroke. It is estimated that approximately etiology for postoperative stroke is mul- 5000 such procedures were performed in tifactorial and may include carotid artery the United States in 2001 alone.6 More re- stenosis, hypotension, cardiac arrhyth- cent analyses, however, have consistently mia, aortic atherosclerosis, and transient revealed an increased incidence of ad- hypercoagulable state.1-3 The presence of verse events, including stroke or death, fol- multiple coexisting causes makes study- lowing combined procedures.6,7 ing the mechanism of stroke challenging. Significant carotid stenosis has been rec- For editorial comment ognized as a positive predictor of postop- erative stroke in patients receiving car- see page 1062 diac surgical procedures.2 However, studies directly addressing the role of severe ca- This retrospective analysis was under- rotid stenosis are lacking. To date, no ran- taken to analyze the relationship be-Author Affiliations: Division of domized clinical trials have addressed this tween stroke and carotid stenosis in pa-Neurology, Department of important topic,4 and few retrospective tients after cardiac operation. This studyMedicine (Drs Y. Li, Isayev, and trials have investigated the lateralization aimed to answer 2 simple but critical ques-Castaldo and Mss Walicki, tions: Does severe carotid stenosis in- and territorial distribution of postopera-Mathiesen, and Jenny), and tive stroke to determine whether there is crease the risk of ipsilateral anterior cir-Departments of Radiology(Dr Q. Li) and Health Studies a correlation between stroke distribution culation stroke in patients undergoing(Dr Reed), Lehigh Valley and carotid stenosis. Therefore, the evi- cardiac surgical procedures? Conversely,Hospital and Health Network, dence for carotid stenosis as a cause for does concomitant carotid repair reduce theAllentown, Pennsylvania. postoperative stroke is mostly indirect.5 risk of perioperative stroke? (REPRINTED) ARCH NEUROL / VOL 66 (NO. 9), SEP 2009 WWW.ARCHNEUROL.COM 1091 Downloaded from at Vanderbilt University, on September 29, 2009 ©2009 American Medical Association. All rights reserved.
  • 2. METHODS festation of pure motor, pure sensory, ataxic hemiparesis, clumsy-hand, or sensorimotor syndrome. Analyses were completed using the Pearson 2 or Fisher ex-The study was approved by the institutional review board of act test for categorical variables and the t test for continuousLehigh Valley Hospital and Health Network, and individual con- variables. Significance was set at .05.sent was waived. Two complementary computerized hospitaldatabases were compared and combined. Patients receiving non- RESULTSurgent coronary artery bypass grafting and/or valve replace-ment were included. Urgent cardiac surgical procedures (ie,those performed within 24 hours of admission) were ex- DEMOGRAPHIC AND OPERATIVEcluded because there was insufficient time for carotid evalua- CHARACTERISTICStion and preoperative consultation by vascular or neurology ser-vices. Members of the Division of Cardiothoracic Surgeryperformed the cardiac procedures for recognized indications. From July 1, 2001, to December 31, 2006, 4924 patientsPatients with carotid stenosis of more than 70% in diameter underwent cardiac procedures at our institution; 589 pa-were evaluated by members of the divisions of Vascular Sur- tients were excluded because of urgent operational sta-gery and Neurology to determine the need for prophylactic ca- tus or the rarity of the procedure performed, such as aor-rotid endarterectomy based on clinical presentation. When com- tic dissection repair or myxoma removal. A cohort of 4335bined carotid and cardiac procedures were recommended, patients was identified for this retrospective analysis. Ofmembers of the Division of Vascular Surgery performed ca- this cohort, 3196 patients had coronary artery bypass graft-rotid endarterectomy as the initial procedure under the same ing, 557 had aortic valve replacement, and 582 had both.general anesthesia. The mean (SD) age of the patients studied was 67.5 Carotid arteries were initially assessed with high- (11.0) years. The study included 2930 men and 4232resolution carotid duplex sonography, mostly performed withinthe month preceding the surgical date. More than 90% of the white participants. A total of 3942 patients (90.9%) un-studies were performed in our facility, where unified criteria derwent preoperative carotid evaluation with noninva-for interpretation have been in place with 96% sensitivity for sive ultrasonography. In addition, 133 patients (3.1%)detecting severe carotid stenosis when compared with percu- underwent magnetic resonance angiography, CT angi-taneous cerebral arteriography.8 Significant carotid disease was ography, or conventional percutaneous angiography.defined as 50% stenosis or greater, including carotid occlu-sion. For patients with stenosis of more than 70% on carotid POSTOPERATIVE EVENTSduplex scanning, a second type of imaging such as magneticresonance angiography, computed tomographic (CT) angiog-raphy, or conventional percutaneous angiography was usu- A total of 76 patients (1.8%) developed postoperativeally performed to verify the degree of stenosis. stroke (n=75) or retinal ischemia (n=1) (the single pa- Postoperative stroke was defined as persistent ( 24 hours) tient with retinal ischemia was considered to have a strokefocal or multifocal neurological deficits that were best ex- in subsequent analysis). Among these, 55 cases of strokesplained by ischemia involving the brain or retina from the sur- (72.4%) were detected within 24 hours of operation andgical procedure until hospital discharge. All patients with stroke 68 (89.5%) within the first 72 hours. The time period forwere evaluated by a board-certified neurologist. Patients with initial recognition of stroke ranged from postoperativenonfocal results from neurological examination, such as en- day 1 through day 9. All strokes were ischemic, and 1cephalopathy, memory deficit, or unsteadiness, were ex- was associated with hemorrhagic transformation. A totalcluded from the study if their examination results continuedto be nonfocal and a second CT scan of the brain showed no of 65 patients died, among whom 8 deaths were be-evidence of ischemia. lieved to be secondary to stroke. All brain CT and magnetic resonance imaging scans were Applying modified TOAST criteria, 57 patients (75.0%)reviewed by a neuroradiologist (Q.L.) who was blind to all clini- were classified as having cardioembolic stroke (new on-cal information except the date of symptom onset. After re- set atrial fibrillation, n=20; previously existent and per-view of the scans, the neuroradiologist (Q.L.) provided an in- sistent atrial fibrillation, n=14; acute myocardial infarc-terpretation, including the presence, size, and arterial distribution tion, n=11; stroke in multiple artery territories, n=20;of infarction. multiorgan embolism, n=4), 4 patients (5.3%) had large- Stroke subtypes were classified with modified TOAST (Trial vessel stroke (carotid artery, n=1; basilar artery, n=3),of Org 10172 in Acute Stroke Treatment) criteria.9 Cardioem- and 10 patients (13.2%) had small-vessel stroke. In 5 pa-bolism was defined based on the following criteria: (1) corti-cal or cerebellar lesions, subcortical or brainstem lesions of more tients, stroke could not be categorized owing to mul-than 1.5 cm; (2) lack of large-vessel disease in the correspond- tiple coexisting territory (carotid or basilar artery); and (3) lesions in mul-tiple vessel territories (bilateral or anterior and posterior cir- DISTRIBUTION OF INFARCTS ON IMAGINGculation) or at least 1 of the following: atrial fibrillation, acutemyocardial infarction, or dilated cardiomyopathy. Large- Of 76 patients with stroke, 75 patients underwent non-artery atherosclerosis was defined based on the following cri- contrast CT scanning of the head; 70 patients had a sec-teria: (1) cortical or cerebellar lesions, subcortical or brain-stem lesions of more than 1.5 cm; and (2) 50% stenosis or greater ond brain CT scan after 24 hours, and 2 patients also un-or occlusion in the internal carotid or basilar artery. Small- derwent magnetic resonance imaging. A total of 60vessel occlusion was defined as the following: (1) no symp- patients had evidence of acute infarction, whereas 15 pa-toms suggestive of cortical dysfunction, such as visual loss or tients had normal results on scanning. Table 1 de-aphasia; (2) isolated subcortical or brainstem lesion of less than scribes the distribution of stroke on imaging. Of 60 pa-1.5 cm or normal results on a CT scan; and (3) clinical mani- tients with abnormal imaging results, 22 had stroke in (REPRINTED) ARCH NEUROL / VOL 66 (NO. 9), SEP 2009 WWW.ARCHNEUROL.COM 1092 Downloaded from at Vanderbilt University, on September 29, 2009 ©2009 American Medical Association. All rights reserved.
  • 3. Table 1. Arterial Distribution of Stroke on Brain Imaging Table 3. Significant Carotid Stenosis and Stroke in 3942 Patients Undergoing Preoperative Carotid Evaluation Arterial Distribution No. of Patients Degree of No. of No. (%) of Unilateral anterior circulation a 22 Carotid Stenosis Patients Patients With Stroke Bilateral anterior circulation a 4 Posterior circulation b 16 50% 239 18 (7.5) Anterior and posterior circulation a,b 16 50%-79% 123 6 (4.9) Watershed c 1 80%, Nonocclusive 71 5 (7.0) Unable to determine 1 Occlusion 45 7 (15.6) Total 60 a Anterior circulation includes anterior and middle cerebral artery territorylesions. b Posterior circulation includes infarction in the vertebrobasilar artery Table 4. Incidence of Postoperative Stroke by Categoriesterritory. of Carotid Intervention c Watershed refers to infarctions found in the vascular border zone. No. (%) of No. of 9 Patients Intervention Type Patients With Stroke Table 2. Distribution of Postoperative Stroke in Patients With Significant Carotid Stenosis Combined CE and cardiac 53 8 (15) operation Staged CE, then cardiac 16 0 Category No. of Patients operation No. of patients with 50% stenosis and 18 Carotid stenting, then cardiac 5 1 (20) postoperative stroke operation Strokes in stenotic/occluded artery 4 Stenosis, nonocclusive, no Stenotic a 1 intervention Occluded 3 80% 16 0 Strokes outside the stenotic/occluded artery 14 70% 51 0 Contralateral 3 Posterior circulation 10 Abbreviation: CE, carotid endarterectomy. Watershed 1 a Patient had an ipsilateral 60% stenosis. Compared with the entire cohort, the subgroup of pa- tients with significant carotid stenosis had a higher in- cidence of postoperative stroke (7.5% vs 1.8%; P=.001).unilateral carotid distribution, 1 had a watershed pat- Table 3 summarizes the incidence of postoperative stroketern, and 36 had infarctions in the bilateral anterior dis- based on the severity of carotid stenosis. The stroke risktribution or posterior circulation that were not confined was higher (15.6%) among patients with carotid occlu-to 1 carotid artery. The remaining patient had a basal gan- sion when compared with those patients with signifi-glia stroke, the territory of which could not be precisely cant carotid stenosis, but this did not reach statistical sig-determined. nificance (P=.22). Table 4 summarizes the incidence of postoperative INFARCTS AND stroke by categories of carotid intervention. Eight strokes SIGNIFICANT CAROTID DISEASE occurred in subgroups of 53 patients (15.1%) who un- derwent combined procedures. No postoperative strokeAll 76 patients with stroke had preoperative carotid evalu- occurred in the group of 51 patients with an equal de-ation. Of these, 18 patients (23.7%) had significant ca- gree of carotid stenosis ( 70%) who underwent cardiacrotid stenosis. Two patients had bilateral significant ca- surgical procedures without any preoperative carotid re-rotid stenosis, and both had an infarction in the posterior vasculization. Table 5 shows a comparison of multiplecirculation. Table 2 shows the incidence and distribu- risk factors between these 2 groups. No significant dif-tion of stroke in these patients based on clinical and ra- ference was found other than the incidence of postop-diographic data. In 14 of 18 patients (77.8%), stroke oc- erative stroke (0% vs 15.1%; P =.004).curred outside the territory of diseased carotid artery. Of4 patients with infarcts found exclusively within the dis-eased carotid artery, 3 had ipsilateral occlusion and 1 pa- COMMENTtient had an ipsilateral 60% stenosis. A randomized trial to explore the relationship between INCIDENCE OF carotid stenosis and postoperative stroke following car- SIGNIFICANT CAROTID STENOSIS diac operations was proposed many years ago but has never been attempted because of the extraordinarily largeOf 3942 patients who received preoperative carotid evalu- number of patients needed for statistical power and theation, 239 (6.1%) had significant carotid stenosis prohibitively high cost of completing such a study.11 Using(Table 3). Based on North American Symptomatic Ca- carotid duplex and CT scanning as the major detectionrotid Endarterectomy Trial criteria, 5 were sympto- methods, this retrospective study provided a detailedmatic and 234 asymptomatic.10 analysis of the distribution of stroke and its relationship (REPRINTED) ARCH NEUROL / VOL 66 (NO. 9), SEP 2009 WWW.ARCHNEUROL.COM 1093 Downloaded from at Vanderbilt University, on September 29, 2009 ©2009 American Medical Association. All rights reserved.
  • 4. Table 5. Risk Factor Comparison in Patients With Severe Carotid Stenosis Undergoing Combined Carotid and Cardiac vs Cardiac Operations Alonea Cardiac Operation Alone Combined Operations Risk Factor (n = 51) (n = 53) P Value Female sex 17 (33) 18 (34) .95 Age, mean (SD), y 72.0 (8.8) 71.8 (9.1) .92 Hypertension 43 (84) 48 (91) .34 Hyperlipidemia 46 (90) 44 (83) .28 Peripheral vascular disease 23 (45) 19 (36) .34 Diabetes mellitus 18 (35) 19 (36) .95 Smoking Previous 27 (53) 34 (64) .25 Active 7 (14) 10 (19) .48 History of preoperative stroke or TIA 12 (24) 8 (15) .28 Cardiomyopathy 12 (24) 9 (17) .41 Atrial fibrillation Chronic 6 (12) 4 (8) .47 Postoperative 21 (41) 16 (30) .24 Aortic sclerosis 23 (45) 21 (40) .57 Bilateral carotid stenosis 50% 8 (16) 13 (25) .26 Preoperative renal failure 4 (8) 1 (2) .16 CABG/VR combined 10 (20) 6 (11) .09 Second CABG 3 (6) 1 (2) .29 Bypass time, mean (SD), min 125 (63) 122 (48) .82 Clamp time, mean (SD), min 97 (52) 94 (43) .72 Postoperative ventricular arrhythmia 14 (28) 9 (17) .20 Use of intra-aortic balloon pump 5 (10) 2 (4) .22 Severe hypotension during surgery 1 (2) 2 (4) .58 Use of inotropic agent 20 (39) 16 (30) .33 Postoperative stroke 0 8 (15) .004 Abbreviations: CABG, coronary artery bypass grafting; TIA, transient ischemic attack; VR, valve replacement. a Data are given as number (percentage) of patients unless otherwise indicated.with significant carotid disease at the bifurcation in pa- tebrobasilar artery, contralateral carotid artery, or mul-tients undergoing routine cardiac procedures.10,12 Only tivessel territory. Only 4 patients with significant carotidclinically significant strokes were considered, and pa- stenosis developed stroke in the diseased carotid terri-tients who had transient ischemic attacks were ex- tory (Table 2). Of 76 strokes, 72 are not related to sig-cluded. This study did not enroll patients at multiple cen- nificant carotid stenosis at the bifurcation. Therefore, mostters, and therefore bias toward the surgical, anesthetic, of these postoperative strokes had alternate causes.and medical practices specific to a single center could not The failure to establish carotid stenosis as a cause ofbe minimized. perioperative stroke in patients undergoing cardiac op- In this cohort, the incidence of postoperative stroke erations has been observed by others. Barbut et al25 re-(1.8%) corresponds well with most of the previously pub- ported the presence of infarction in multiple arterial ter-lished large trials, which report stroke risks from 0.9% ritories and the preponderance of infarction in theto 3.2%.1,2,13-24 The incidence appeared to be slightly higher posterior circulation in their cohort. Infarction was at-among patients undergoing combined valve replace- tributed to high-grade carotid stenosis in only 1 of 24 pa-ment and coronary artery bypass grafting, but it did not tients. In an extensive review, Naylor et al5 noted thatalter our analysis of carotid stenosis in the pathogenesis primary carotid disease alone was only responsible forof postoperative stroke (data not shown). It was ob- up to approximately 40% of postoperative strokes. Inserved that the incidence of stroke after cardiac proce- addition, Libman et al1 determined that 7 of 44 postop-dures could be as much as 4 times higher among pa- erative strokes (16%) in their series fit the criteria for clas-tients with significant carotid stenosis vs those without.5 sical lacunar syndromes.Comparably, our analysis suggested a 4-fold increased Multiple causes other than carotid stenosis could ac-relative risk (7.5% vs 1.8%). count for postoperative stroke in patients undergoing car- However, this study strongly suggests there is no di- diac procedures. For example, coexistence of aortic ath-rect causal relationship between postoperative stroke and erosclerosis has been demonstrated to be a significantsevere carotid stenosis. First, only 5.3% of postopera- determinant of postoperative stroke.26 In some studies,tive strokes were in the large-vessel category, based on clamping and manipulation of the aorta or heart couldTOAST criteria. Second, 76.3% of postoperative strokes account for more than 60% of emboli.27 Van der Lindenoccurred in the absence of significant carotid disease at and Casimir-Ahn28 reported that cerebral emboli are mostthe bifurcation. Third, 60.0% of strokes on CT scanning likely to occur during the redistribution of blood fromhad a distribution that was not confined to a single ca- the heart-lung machine to the patient, which supportsrotid artery (Table 1). Most strokes occurred in the ver- the idea that release of particles from the cardiopulmo- (REPRINTED) ARCH NEUROL / VOL 66 (NO. 9), SEP 2009 WWW.ARCHNEUROL.COM 1094 Downloaded from at Vanderbilt University, on September 29, 2009 ©2009 American Medical Association. All rights reserved.
  • 5. nary bypass pump is a major contributor to stroke. Post- rence of postoperative stroke in this subgroup is likelyoperative atrial fibrillation is seen in 30% to 50% of pa- related to the combined procedure itself, with a possibletients. 3 There is also evidence that the fibrinolytic correlation to the duration of the operation. As such, ourshutdown activates postoperatively, which may ac- findings strongly support the idea that combined ca-count for the occurrence of embolic and lacunar infarc- rotid and cardiac procedures are neither necessary nortions.29 A recent multivariate analysis by Filsoufi et al30 effective in reducing the risk of postoperative stroke insuggested that older age, female sex, and presence of dia- this population. Assuming that 5000 combined carotidbetes mellitus, cardiomyopathy, longer bypass time, and endarterectomies and cardiac operations are performedaortic calcifications are independent predictors of post- annually in the United States, avoidance of such proce-operative stroke. The apparent paradox that carotid ste- dures alone could prevent nearly 500 postoperative strokesnosis is associated with an increased incidence of stroke per year.but is not a direct cause of postoperative stroke may sug- In conclusion, we examined the relationship be-gest that it is an epiphenomena indicating an increased tween postoperative stroke and carotid stenosis in a largeunderlying cardiovascular risk. group of patients undergoing common, nonurgent car- The lack of a causal relationship between carotid ste- diac procedures at a single medical center. We con-nosis and postoperative stroke raises serious doubts about firmed a higher incidence of stroke in the subgroup ofhypoperfusion as a major mechanism. This finding is in patients with significant carotid stenosis. However, mostline with data from the Northern New England Cardio- strokes have no direct causal relationship with the dis-vascular Disease Study Group suggesting that fewer than eased carotid artery. Combined carotid and cardiac pro-10% of postoperative strokes were caused by hypoperfu- cedures result in a significantly higher incidence of post-sion.2 In our study, the incidences of stroke for patient sub- operative stroke and should be avoided. Preoperativegroups with 50% to 79% stenosis, 80% to 99% stenosis, and studies such as echocardiography or CT or magnetic reso-occlusion were 4.9%, 7.0%, and 15.6%, respectively nance imaging of the heart and aorta could identify dis-(Table 3). Although higher incidence of stroke was asso- ease-free areas for manipulation and clamping to pre-ciated with more severe stenosis, this trend did not reach vent postoperative strokes.statistical significance. The most plausible explanation forsuch a trend might simply be the cardiovascular risk bur- Accepted for Publication: January 21, 2009.den, as reflected by the degree of carotid stenosis. The ob- Correspondence: John E. Castaldo, MD, Department ofservation that more postoperative strokes occur outside Medicine, Lehigh Valley Hospital and Health Network,rather than within the territory of diseased carotid arteries 1250 S Cedar Crest Blvd, Ste 405, Allentown, PA 18103was consistent among these subgroups. ( The increased incidence of stroke among patients with Author Contributions: Drs Y. Li and Castaldo had fullcarotid stenosis has led to the proposal for combining ca- access to all the data in the study and take responsibilityrotid and cardiac procedures in selected patients. How- for the integrity of the data and accuracy of the data analy-ever, recent analyses suggest that simultaneous repair of sis. Study concept and design: Y. Li and Castaldo. Acqui-carotid lesions is associated with a higher risk of post- sition of data: Y. Li, Walicki, Jenny, and Q. Li. Analysisoperative stroke and death in patients undergoing car- and interpretation of data: Y. Li, Walicki, Mathiesen, Q.diac operations.6,7,31 In this sample of 239 patients with Li, Isayev, Reed, and Castaldo. Drafting of the manu-significant carotid stenosis, 4 patients had strokes found script: Y. Li. Mathiesen, Jenny, Q. Li, and Isayev. Criticalto be caused by carotid disease, but only the patient with revision of the manuscript for important intellectual con-60% unilateral carotid stenosis would have been consid- tent: Y. Li, Walicki, Isayev, Reed, and Castaldo. Statisti-ered a candidate for endarterectomy based on results of cal analysis: Reed. Administrative, technical, and mate-the Asymptomatic Carotid Atherosclerosis Study.12 There- rial support: Jenny, Q. Li, and Isayev. Study supervision:fore, there is virtually no compelling evidence to sug- Y. Li and Castaldo.gest that repairing the diseased carotid artery prevents Financial Disclosure: None reported.postoperative stroke after cardiac procedures. Could the Additional Contributions: Karen Boutron, RN, andeffect of carotid stenosis be falsely low because a signifi- Joanne Rodgers, RN, provided substantial help in datacant portion of patients underwent carotid revascular- collection. We also thank the Department of Surgery atization procedures before cardiac operations? We do not Lehigh Valley Hospital and Health Network for allow-believe this is the explanation. Instead, the incidence of ing us access to the databases.stroke (15.1%) was significantly higher in the subgroupof patients undergoing combined carotid and cardiac pro-cedures than among patients with similar degrees of ca- REFERENCESrotid stenosis but who underwent cardiac procedures 1. Libman RB, Wirkowski E, Neystat M, Barr W, Gelb S, Graver M. Stroke associ-alone (Table 4). 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