Association of sex with perioperative mortality and morbidity after carotid endarterectomy for asymptomatic carotid stenosis☆

Article Outline

• Abstract
• Methods
• Results
• Discussion
• References
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Abstract 

Objective: To examine whether perioperative morbidity and mortality after carotid endarterectomy depend on the sex and the presence of symptoms on presentation. Design: Retrospective review of quality assurance database prospectively collected. Setting: A university teaching hospital. Participants: One thousand two hundred eighty-seven patients who had 1,503 carotid endarterectomies from 1990 to 1999 from a quality assurance database. Interventions: None. Measurements and Main Results: The cases were divided into 4 groups by sex and symptoms on presentation: male-symptomatic (MS), male-asymptomatic (MA), female-symptomatic (FS), and female-asymptomatic (FA). The 4 groups were compared for preoperative demographic and comorbidity profiles, carotid plaque characteristics, and outcome. Outcome measures included in-hospital stroke, myocardial infarction (MI), congestive heart failure (CHF), and death. There were 496 cases in the MS group, 407 in the MA group, 315 in the FS group, and 285 in the FA group. Women were less likely to have a history of coronary artery disease, prior MI, or smoking, and their carotid plaques were less likely to be ulcerated or contain intraplaque hemorrhage. Even when controlling for the comorbidities and plaque characteristics, the incidence of each of the complications examined was low and not significantly different between the sexes in both the symptomatic and asymptomatic groups. The rate of stroke or death was 3.0% (MS) versus 1.9% (FS) (p = NS) and 1.2% (MA) versus 1.8% (FA) (p = NS). Conclusion: There is no significant sex difference in perioperative cardiac or cerebrovascular complications. Women with symptomatic or asymptomatic carotid stenosis can have acceptably low complication rates from carotid endarterectomy and may benefit from the surgery as much as men. Copyright 2003, Elsevier Science (USA). All rights reserved.

Keywords:  Carotid surgery, sex, morbidity and mortality

Carotid endarterectomy (CEA) was introduced as a stroke-preventing measure in 1954.¹ In the 1980s, the effectiveness of this operation in reducing the incidence of strokes in patients with carotid stenosis (CS) was brought into question,² and several prospective, randomized studies have since been performed to address this question. Regarding patients with symptomatic CS, 3 large randomized trials have shown that CEA in addition to medical optimization confers significant protection against subsequent ipsilateral stroke in patients with high-grade (>70%) stenosis compared with medical optimization alone.³, ⁴, ⁵ In the North American Symptomatic Carotid Endarterectomy Trial (NASCET), patients with symptomatic CS of >70% derived an absolute risk reduction of 16.5% of stroke or death over 2 years.³ For patients with asymptomatic CS, the results of multicenter studies have been less conclusive. The Asymptomatic Carotid Atherosclerosis Study (ACAS) concluded that the 5-year risk of stroke and death was reduced by CEA, but the magnitude of absolute risk reduction was only 5.9% over 5 years.⁶ This slim margin depends on having a low perioperative rate of stroke or death, so that for each 2% rise in the perioperative complication rate, the benefit of CEA in asymptomatic patients would be reduced by >30%.⁷

In the ACAS study, although the perioperative and 5-year complication rates of stroke or death after CEA were 1.7% and 4.1%, respectively, for men, the corresponding numbers for women were 3.6% and 7.3%.⁶ Because of the higher perioperative complication rate, the benefit of surgical therapy for CS in women did not achieve statistical significance in the study. However, in an earlier report from this institution, the authors did not find any gender differences in the rates of stroke, death, or cardiac morbidity after CEA.⁸ However, the report did not stratify the patients according to the presence of symptoms on presentation. Before it is concluded that CEA in asymptomatic women can confer a long-term stroke-free survival benefit, it is important to determine whether CEA may be performed in asymptomatic women with an acceptably low complication rate as in asymptomatic men. Therefore, the present study was undertaken to examine whether any gender difference in morbidity and mortality exists when patients are stratified for symptoms (nondisabling stroke or transient ischemic attack [TIA]) on presentation for CEA.

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Methods 

Data on all patients who underwent CEA at this institution from 1990 to 1999 were retrospectively reviewed from a quality assurance database prospectively collected. Initial data entry in the database was done by care team members and was then confirmed and, when necessary, completed by a dedicated database technician. Patients who had a simultaneous cardiac or aortic arch procedure were excluded from the review. There were 1,503 procedures performed in 1,287 patients; some patients underwent procedures on both sides. Each procedure was analyzed individually. The procedures were divided into 4 groups according to the sex and the presence of symptoms on presentation: male symptomatic (MS), male asymptomatic (MA), female symptomatic (FS), and female asymptomatic (FA). TIAs or cerebrovascular accidents (CVA) ipsilateral to the side of the operation constituted positive symptoms. Patients who had nonhemispheric symptoms such as dizzy spells or vertigo were classified as asymptomatic.

Internal carotid artery percent stenosis was derived from arteriography, duplex ultrasound scan, or magnetic resonance arteriogram. Arteriography was performed with lower frequency during the later years of the study period, consistent with other reports.⁹

The 4 groups of patients were compared for their preoperative demographic and comorbidity profiles, the characteristics of carotid plaques at the time of surgery, and outcome. Carotid plaques were characterized as to whether they were ulcerated or contained an intraplaque hemorrhage, according to the surgeon's findings. Outcome measures included in-hospital stroke, TIA, myocardial infarction (MI), congestive heart failure (CHF), and death. A stroke was defined as a neurologic deficit lasting more than 24 hours and present at the time of discharge from the hospital. A TIA was defined as a neurologic deficit lasting <24 hours or not present at the time of discharge. A new neurologic deficit was initially diagnosed by the surgical team and confirmed by a neurologist. A computed tomographic scan of the head was performed in all patients who had a new neurologic deficit after surgery. A postoperative electrocardiogram (ECG) was obtained selectively in all patients with a history of diabetes, coronary artery disease, heart failure, or arrhythmias or those with any intraoperative ECG changes suggestive of ischemia. The ECG was initially read by the surgical team and, if new changes were found, confirmed by a cardiologist. New ECG changes were defined as horizontal or down-sloping ST-segment depression of at least 0.1 mV or ST elevation of at least 0.15 mV¹⁰ and led to 3 serial cardiac isoenzymes. Postoperative myocardial infarction was defined by creatine kinase muscle-brain (MB) fraction >5% and/or troponin-I >2.0 ng/mL.

Risk profiles and outcome were compared among the groups either by Monte Carlo randomization test for categoric variables and proportions or by 2-tailed Student t-test for continuous variables. To control for different risk profiles among the groups, a multiple logistic regression was performed using age, sex, presence of symptoms on presentation, comorbidities, plaque characteristics, and a dummy variable as predictor variables and each of the cardiac or cerebrovascular morbidities and mortality as an outcome variable. The dummy variable used was the 2-year quintiles of the study period (1990-1991, 1992-1993, 1994-1995, 1996-1997, 1998-1999). A p value <0.05 was considered significant. All statistical tests were performed using True Epistat® software (Epistat Services, Richardson, TX).

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Results 

Between 1990 and 1999, there were 496 carotid endarterectomies in MS patients, 407 in MA patients, 315 in FS patients, and 285 in FA patients. Thus, surgery for asymptomatic presentation accounted for 45% of the cases in men and 48% in women (p = 0.46). As can be seen in Fig 1, the majority of cases in asymptomatic patients have been performed since 1995, when cases in asymptomatic patients started to outnumber cases in symptomatic patients.

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• Fig. 1. 

  (A) Number of cases of carotid endarterectomy by year for symptomatic and asymptomatic men and women. Note the rise in the number of asymptomatic cases in both sexes in 1995. (B) Percentage of total cases of carotid endarterectomy by year for each gender-symptom subgroup. Note that before 1995, most cases were performed in symptomatic patients; whereas after 1995, the majority of cases were in asymptomatic patients.

In 1999, the men:women ratio of cases was about 1.5:1, and the asymptomatic:symptomatic ratio was about 1.2:1.

Patients' demographic and comorbidity profiles are as shown in Table 1.

Table 1. Demographic and comorbidity profiles

NOTE. Numbers in the parentheses indicate those with history of the comorbidity.

Abbreviations: MS, male symptomatic; MA, male asymptomatic; FS, female symptomatic; FA, female asymptomatic; ASA, aspirin; CAD, coronary artery disease; MI, myocardial infarction; CHF, congestive heart failure; PVD, peripheral vascular disease; CRI, chronic renal insufficiency.

There was no significant difference in age among the groups, and the patients were predominantly white. Preoperative use of aspirin was similar among the groups, but heparin, as expected, was used preoperatively mostly in the symptomatic patients. Female patients, whether symptomatic or asymptomatic, were less likely to have a history of coronary artery disease, prior MI, and a history of smoking than their male counterparts. The asymptomatic patients, whether men or women, were more likely to have a history of hyperlipidemia than their symptomatic counterparts. The FA group was more likely to have a history of peripheral vascular disease than the FS group and less likely to have contralateral carotid stenosis of ≥70% than the MA group. Otherwise, the comorbidity profile and the degree of carotid stenosis were similar among the 4 groups.

About 80% of the cases were performed under general anesthesia (Table 2). Although the asymptomatic cases were more likely to get a shunt and a patch angioplasty than their symptomatic counterparts, this finding probably reflected the fact that shunt placement and patch angioplasty became more widely used in the later years of the study period (Figs 2 and 3), when there was a relative increase in the number of asymptomatic cases (Fig 1).

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• Fig. 2. 

  Percentage of cases that had patch angioplasty by year for each gender-symptom subgroup. The percentage increased dramatically between 1994 and 1996, and patch angioplasty is now performed virtually in all cases for all the gender-symptom subgroups.

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• Fig. 3. 

  Percentage of cases with carotid shunting by year for each gender-symptom subgroup. The percentage has increased gradually over the decade, and shunting is now used in the vast majority of cases for all subgroups.

Intraoperatively, female patients were less likely to have intraplaque hemorrhage than male patients (Table 2). The FA group was also less likely to have an ulcerating plaque than the FS or MA groups.

Table 2. Operative techniques and the carotid pathology

NOTE. Numbers in the parentheses indicate those with the finding or the technique used.

Abbreviations: MS, male symptomatic; MA, male asymptomatic; FS, female symptomatic; FA, female asymptomatic.

In-hospital cerebrovascular and cardiac morbidity and mortality for the 4 groups are shown in Table 3.

Table 3. Outcome

NOTE. Numbers in the parentheses indicate those with the complication.

Abbreviations: MS, male symptomatic; MA, male asymptomatic; FS, female symptomatic; FA, female asymptomatic; LOS, length of stay; CVA, stroke; TIA, transient ischemic attack; MI, myocardial infarction; CHF, congestive heart failure.

After controlling for age, comorbidities, plaque characteristics, and year of surgery, sex or presence of symptoms did not have a significant effect on stroke (Table 4), death (Table 5), or death or stroke (Table 6).

Table 4. Multiple logistic regression of postoperative stroke as a function of sex, symptoms on presentation, risk profiles, and plaque characteristics

NOTE. For categoric variables, the following values were used. Gender: 1 = male, 0 = female. Symptom on presentation: symptomatic = 1, asymptomatic = 0, Comorbidities: 1 = present, 0 = absent.

Abbreviation: CAD, coronary artery disease.

Table 5. Multiple logistic regression of postoperative death as a function of sex, symptoms on presentation, risk profiles, and plaque characteristics

NOTE. For categoric variables, the following values were used. Gender: 1 = male, 0 = female. Symptom on presentation: symptomatic = 1, asymptomatic = 0. Comorbidities: 1 = present, 0 = absent.

Abbreviation: CAD, coronary artery disease.

Table 6. Multiple logistic regression of death or stroke as a function of sex, symptoms on presentation, risk profiles, and plaque characteristics

NOTE. For categoric variables, the following values were used. Gender: 1 = male, 0 = female. Symptom on presentation: symptomatic = 1, asymptomatic = 0. Comorbidities: 1 = present, 0 = absent.

Abbreviation: CAD, coronary artery disease.

However, there was a trend that presence of symptoms on presentation might increase the incidence of stroke about 2-fold (p = 0.08). Similarly, after controlling for age, comorbidities, plaque characteristics, and year of surgery, sex and presence of cerebrovascular symptoms were not significantly associated with the incidence of postoperative MI or CHF (data not shown).

The length of stay was significantly greater for the symptomatic patients than the asymptomatic counterparts within each gender. Length of stay decreased over time during the study period, going from 7.0 ± 8.2 days for 1990 to 1991 and 6.9 ± 7.9 days for 1992 to 1993 to 3.9 ± 3.9 days for 1994 to 1995, 2.4 ± 2.9 days for 1996 to 1997, and 2.4 ± 2.9 days for 1998 to 1999.

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Discussion 

The main findings of this retrospective analysis of the data obtained from 1990 to 1999 in 1,503 carotid endarterectomies, including 692 performed for asymptomatic carotid stenosis, are that the perioperative rates of major cerebrovascular and cardiac morbidity and death were relatively low and similar, regardless of the sex and the presence of symptoms on presentation. Of note, in FA patients, the rate of stroke or death was 1.8%.

Whether carotid endarterectomy should be performed for patients with asymptomatic carotid stenosis has been a matter of controversy and is a matter of importance in public policy. Five percent to 10% of the general population over the age of 65,¹¹ and 20% to 30% of patients admitted for either peripheral vascular disease¹² or ischemic heart disease¹³ have >50% stenosis of a carotid artery. A recommendation for surgery for asymptomatic carotid stenosis would therefore have major implications in public policy. The population prevalence of significant carotid stenosis in women is slightly less than in men under the age of 50 but approaches the prevalence in men after age 50.¹⁴ In patients referred for carotid duplex scans for nonhemispheric symptoms such as dizziness and fainting, the likelihood of finding >50% carotid stenosis is about the same in women as in men and is >20% in smokers in their 60s and >30% in smokers in their 70s but <10% in nonsmokers in their 60s and 10% to 20% in nonsmokers in their 70s.¹⁵ Thus, if female patients with asymptomatic carotid stenosis were judged not to benefit from surgical therapy, the number of appropriate carotid surgeries would significantly decrease.

In the ACAS, patients with asymptomatic carotid stenosis of 60% or greater had a reduced 5-year risk of ipsilateral stroke if surgery was performed.⁶ But because the absolute reduction of risk was relatively small at 5.9% over 5 years, surgical therapy was considered to afford benefit only if perioperative morbidity and mortality were <3%. The expert panel of the American Heart Association likewise provided a guideline that endarterectomy should be recommended in asymptomatic patients with 60% to 99% carotid stenosis, only if the perioperative rate of stroke or death is <3% and the patient's life expectancy is at least 5 years.¹⁶ The National Stroke Association has issued a similar recommendation.¹⁷

In the ACAS, it was noted that although the perioperative complication rate of stroke or death was 1.7% in men (N = 544), it was much higher at 3.6% in women (N = 281).⁶ As a result, there was found to be no significant reduction in 5-year risk of stroke or death caused by surgery in women. In addition, several large case series have identified the female sex as a significant risk factor for increased cerebrovascular morbidity and death after carotid endarterectomy.¹⁸, ¹⁹, ²⁰, ²¹ However, recent studies as well as the findings of the present study challenge this notion. An earlier report from this institution covering the period from 1990 to 1998 showed that there was no significant difference in the perioperative rate of stroke, TIA, MI, CHF, or death between the sexes and, more importantly, that the perioperative rate of stroke or death in women was <2%.⁸ This study, however, did not stratify the patients according to the presence of symptoms on presentation. Sternbach and Perler²² reported a single surgeon experience with 156 endarterectomies for asymptomatic carotid stenosis and found no significant gender difference in morbidity or mortality, with none of the female patients (N = 66) having a perioperative stroke, MI, or death. In a larger patient population (N = 1,485 men and 991 women), Rockman et al²³ reported that there was no gender difference in perioperative rate of stroke, MI, or death and that, when the female patients were subdivided according to the presence of symptoms on presentation, the FA patients (N = 332) had at least as low a perioperative stroke rate (1.2%) as the symptomatic patients. Although they did not break down the mortality according to the presence of symptoms, the perioperative mortality for all women was 0.5%, and the perioperative rate of stroke or death for asymptomatic women was likely to have been <3%, the threshold for recommending surgery according to the American Heart Association.

The present cohort of patients differed from those of Rockman et al²³ in several important aspects and yet showed similarly low perioperative event rates for asymptomatic females. In comparison to the female patients of Rockman et al, the FA patients in this study were older (71.3 v 68.6 yr); were more likely to have a history of diabetes (42% v 20%), hypertension (78% v 62%), significant contralateral carotid stenosis (18% v 10%), and smoking (66% v 36%); and had a similar incidence of coronary artery disease (41% v 38%). Although regional anesthesia was used in more than 80% of the patients of Rockman et al, the vast majority of the present patients had general anesthesia. With a preponderance of regional anesthesia, Rockman et al used selective shunting in about 30% of their patients, whereas about 75% of these patients had a shunt. In a systematic review of randomized and nonrandomized trials comparing regional and general anesthesia for CEA, Tangkanakul et al²⁴ concluded that although the nonrandomized trials suggested that regional anesthesia might be associated with clinically significant reductions in the rate of stroke, MI, or death, the randomized trials had too few patients either to confirm or refute the findings of the nonrandomized trials. Even though the present patients might be considered higher risk than those of Rockman et al and the surgical and anesthetic techniques differed between the 2 institutions, these patients had perioperative morbidity and mortality rates that were at least as satisfactory as theirs. The FA group, with a sample size comparable to that of the ACAS, had a combined stroke or death rate of 1.8%, safely below the 3% threshold of superior benefit of the surgical therapy. These findings show that FA patients of differing risks can have carotid endarterectomies under different surgical and anesthetic techniques with acceptably low perioperative morbidity and mortality.

The female patients did not necessarily represent the same risks as the male patients. The female patients had a lower incidence of history of coronary artery disease, prior MI, and smoking, and they were less likely to have an intraplaque hemorrhage. The asymptomatic female patients were also less likely to have significant contralateral carotid stenosis and an ulcerating plaque than the male counterparts. Yet, when multiple logistic regressions were performed to control for age, comorbidities, plaque characteristics, and year of surgery, sex was not associated with any of the complications examined. With such a small gender difference in any of the outcome variables as in this study, it would have taken a much larger sample size to show a statistically significant difference. For example, to show a significant difference between a mortality of 0.2% and 0.4% with an α error of 0.05 and a β error of 0.10, this study would have needed more than 25,000 patients. Yet, the main conclusion of this study that complication rates in the FA group can be acceptably low to justify surgical therapy just as in the MA group remains valid, whether or not the rates are marginally different or the same among the groups.

An often-suggested reason for the female patients having a higher stroke rate after carotid endarterectomy than male patients is that the internal carotid artery in women is relatively small, which may predispose to technical errors or early postoperative thrombosis.²³ Samijo et al²⁵ measured the diameter of common carotid arteries in Dutch volunteers and found that the diameter increased gradually with age, so that in those in their sixth decade, the mean diameter was 6.31 mm in women and 6.44 mm in men. A Swedish study found a greater gender difference (about 10-20%) in the size of common carotid arteries for healthy volunteers in their 50's to 70's.²⁶ If it is surmised that the diameter of the internal carotid artery would be proportional to that of the common carotid artery, then the gender difference in the diameter of the internal carotid artery would be estimated to be between <2% up to 20% or between 0.1 mm to a maximum difference of about 1 mm. This magnitude of difference appears unlikely to significantly contribute to additional surgical difficulty. In any case, increasing the use of patch angioplasty in recent years has helped overcome any difficulty with smaller sized carotid arteries.

One subgroup of female patients who have previously been identified to have a high rate of strokes after carotid endarterectomy consists of black women. Rigdon²⁷ reported that black women (N = 56) coming for carotid surgery had a very high incidence of history of hypertension (98% in his study) and often had severe acute perioperative hypertensive episodes. They had a perioperative stroke rate of 16%, a cardiac complication rate of 3.6%, and a mortality rate of 8.9%—numbers much higher than those for white women or white or black men. The present study population had very few (<4%) nonwhite patients and this might have contributed to low complication rates even among women. Whether black women indeed represent a high-risk group who may not benefit from surgical therapy of carotid stenosis will need to be tested in a larger population than Rigdon's. It should also be noted that age-adjusted death rates from cerebrovascular diseases are higher in black women than in white women; in the United States in 1982, the rates for those between 35 and 74 in age were about 110 per 100,000 in black women and about 50 per 100,000 in white women.²⁸ Therefore, even with a higher perioperative rate of stroke or death, carotid endarterectomy may prove beneficial for black women.

The experience of the institution and Rockman et al's with low perioperative stroke or death rates in female patients undergoing carotid endarterectomy cannot necessarily be extrapolated to other institutions. Both studies are limited in scope in that they each report single-institution experiences. Karp et al²⁹ reviewed all carotid endarterectomies performed on Medicare beneficiaries in Georgia in 1993 (N = 1,945).²⁹ Fifty-one percent of the patients were operated for asymptomatic carotid stenosis. The authors noted significant interinstitution variation in perioperative stroke or death rates. There was a significant relationship between the complication rates and the surgical volume, and the threshold of <3% rate of stroke or death was achieved only in those hospitals that performed >50 carotid endarterectomies per year. More than 80% of the hospitals in the Georgia review performed fewer than 50 endarterectomies per year and accounted for about 43% of the patients undergoing the surgery. In another survey, in 1995 the mean annual volume of carotid endarterectomy cases per hospital was 36 in California, 52 in New York, and 44 in Ontario.³⁰ A public policy implication of the findings of the present study and the previously quoted studies may be that although female patients with asymptomatic carotid stenosis can benefit from surgical therapy, this may or may not hold true in hospitals in which CEA is not commonly performed.

After the publication of randomized trials of the 1990s that showed the benefit of surgical therapy for carotid stenosis, there have been significant rises in the rate of carotid endarterectomy.³⁰ Even in this review, the authors note a significant rise in the number of carotid endarterectomies around 1995 (the year of publication of the ACAS), especially endarterectomies performed for asymptomatic carotid stenosis. Such a rise in the general population would be justifiable, if the rise were occurring in hospitals in which the perioperative complication rates are kept under the threshold of benefit,⁷ which is 3% at present.¹⁶, ¹⁷ Information on institutional complication rates should be made available, and education of both referring physicians and vascular surgeons should be increased so that more of the carotid surgeries are performed in institutions with greater surgical volume and lower complication rates. Only then will the benefit of carotid endarterectomy in prevention of ischemic strokes be realized in the general population, as in the clinical trials.

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