(Circulation. 2001;103:2133.)
© 2001 American Heart Association, Inc.
Special Report |
Sex Differences in Neurological Outcomes and Mortality After Cardiac Surgery
A Society of Thoracic Surgery National Database Report
From the Department of Anesthesiology (C.W.H., V.G.D.-R.) and the Cardiovascular Division, Department of Medicine (B.B., V.G.D.-R.), Washington University School of Medicine, St Louis, Mo; Duke Clinical Research Institute, Duke University School of Medicine, Durham, NC (K.S.P., L.P.C., E.R.D.); and Missouri Baptist Medical Center, BJC Health System, St Louis, Mo (N.T.K.).
Correspondence to Víctor G. Dávila-Román, MD, Cardiovascular Division, Box 8086, Washington University School of Medicine, 660 S Euclid Ave, St Louis, MO 63110. E-mail vdavila{at}im.wustl.edu
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Abstract |
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Background—The purpose of this study was to evaluate whether women undergoing cardiac surgery are more likely to suffer neurological complications than men and whether these complications could explain, at least in part, their higher perioperative mortality.
Methods and Results—The Society of Thoracic Surgery National Cardiac Surgery Database was examined for the years 1996 and 1997 to determine the frequency of new neurological events (stroke, transient ischemic attack, or coma) occurring after cardiac surgery. We reviewed clinical information on 416 347 patients (32% women) for whom complete neurological outcome data were available. New neurological events after surgery were higher for women than for men (3.8% versus 2.4%, P=0.001). For the whole group, the 30-day mortality was higher for women than for men (5.7% versus 3.5%, P=0.001), and among those patients who suffered a perioperative neurological event, mortality was also significantly higher for women than men (32% versus 28%, P=0.001). After adjustment for other risk factors (eg, age, history of hypertension and/or diabetes, duration of cardiopulmonary bypass, and other comorbid conditions) by multivariable logistic regression, female sex was independently associated with significantly higher risk of suffering new neurological events after cardiac surgery (OR 1.21, 95% CI 1.14 to 1.28, P=0.001).
Conclusions—Women undergoing cardiac surgery are more likely than men to suffer new perioperative neurological events, and they have higher 30-day mortality when these complications occur. The higher incidence of perioperative neurological complications in women cannot be explained by currently known risk factors.
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Introduction |
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Heart disease is the leading cause of death for women in the United States, accounting for >50% of all deaths (more than one half million deaths per year).1 Cardiac surgery is being used with increasing frequency in women to effectively treat heart disease, and it is well documented that women have higher morbidity and mortality after cardiac surgery than men.2 3 4 5 6 7 8 Possible explanations for these findings include the fact that, compared with men, women undergoing cardiac surgery are older, are more likely to have unstable angina, have higher rates of comorbid conditions, have smaller coronary arteries (technically compromising surgical anastomoses), and are referred late for myocardial revascularization procedures.2 3 4 5 6 7 8 9 For the most part, the importance of perioperative complications for surgical outcomes in women have not been closely examined, despite the growing appreciation of their importance for mortality.2 3 4 5 6 7 10 11 Because women represent a growing segment of patients undergoing cardiac surgery, an understanding of the causes for higher operative mortality is important for its prevention.
A recent study from a single institution found that female sex was independently associated with increased risk of neurological events and higher mortality after cardiac surgery compared with men.12 To evaluate whether women undergoing cardiac surgery are more likely to suffer neurological complications than men and whether these complications could explain, at least in part, their higher operative mortality, we reviewed the Society of Thoracic Surgery (STS) National Cardiac Surgery Database. The STS database contains information about patient risk factors and operative outcomes from voluntarily participating cardiac surgery centers throughout North America.7 This large database is especially useful for this purpose because the data are derived from multiple institutions (both academic and private practice settings), thus providing a relevant benchmark for a wide array of surgical practices.
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Methods |
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STS National Database
Details of the clinical definitions and methods used for this database have been described.7 Patient data are entered locally via a uniform software program and transferred to the STS data management center. The database is scanned for missing data; records from institutions with >33% missing neurological outcome data are deleted from the analysis.
Patient Population
Data from patients whose clinical characteristics
were entered into the STS National Database from 1996 through 1997 were
analyzed. There were 487 389 available patients, but
neurological outcome data were not available for 71 042 (15%).
Outcome data were complete on the remaining 416 347, and of these,
133 231 (32%) were women. Comparison of data from patients with and
without missing data related to neurological outcomes showed no
significant differences in any of the other variables examined,
suggesting that patients with complete data were
representative of the entire data set. Demographic and
other characteristics of the patients included in the analysis
are listed in
Table 1
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Neurological Outcomes
Postoperative neurological events included stroke,
transient ischemic attack, and/or coma, defined as follows: (1)
stroke, a new, permanent, global or focal neurological deficit; (2)
transient ischemic attack, a new, transient, focal neurological
deficit; and (3) coma, a global neurological deficit lasting >24 hours
that could not be explained by other medical conditions (eg,
metabolic abnormalities, hypoxia, and/or
drugs).
Statistical Analysis
Analysis was performed with Statistical
Analysis System software (SAS Institute). The distributions of risk factors by sex were compared to
examine the degree of imbalance among risk factors. To determine the
effect of sex on the occurrence of a neurological event, the unadjusted
sex effect was considered first. Multivariable logistic regression
was then used to examine the effect of female sex after control for
confounding variables. In this analysis, only those
patients with complete outcomes and covariate data were used
(n=201 164). Covariates selected for adjustment included variables
shown to have an association with high risk for a neurological
event. To take into consideration the confounding influence of the
often smaller body size of female patients on the risk for
perioperative neurological events, weight was added to
the multivariable model so that the added effect of sex after
control for weight could be examined.
The c-index was performed to reflect the ability of the model to discriminate patients with a neurological event from those without. Specifically, the c-index considers all possible pairs of patients that can be formed such that one patient has a neurological event and the other does not. The c-index is equal to the proportion of pairs for which the patient with the neurological event has a higher predicted probability of having a neurological event than the patient without. The c-index ranges from 0.5 (no ability to discriminate) to 1.0 (full ability to discriminate). Thus, all predicted c-index values for patients who suffered a neurological event are higher than all predicted values for patients with no neurological event.
Interactions between sex and the variables associated with risk of neurological event were examined. Because of the magnitude of the data set and large number of hypothesis tests, these were considered significant only if the probability value was P<0.01.
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Results |
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Sex and Neurological Events
Women tended to be older, were more likely to have diabetes and hypertension, and were less likely to smoke or to have triple-vessel coronary artery disease than their male counterparts (Table 1
). New neurological events occurred in 13 396
patients (3.3% of the total population). The percentages of patients
who suffered a new neurological event are listed by sex in
Table 2. A significantly higher percentage of women than
men suffered a new perioperative neurological event
(3.8% versus 2.4%, P<0.001).
Patients of both sexes were divided into groups according to the type
of surgery and the age of the patient. Among both men and women, the
percentage of neurological events increased as the complexity of the
surgical procedure increased (CABG alone versus valve surgery alone
versus combined CABG and valve surgery) and as the age of the patient
increased (from <50, to 50 to 70, to >70 years). Furthermore, for all
types of surgical procedures and for all age groups, women had a
significantly higher rate of adverse neurological outcomes than
men.
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Multivariable Analysis
The results of the multivariable
analysis are listed in
Table 3. After adjustment for the covariates listed, female
sex was independently associated with increased risk for a new
postoperative neurological event (OR versus men 1.31,
P<0.001). Analysis of
body weight demonstrated that higher body weight for both sexes was
significantly associated with lower risk for a
perioperative neurological event (OR 0.93,
P<0.001). Nonetheless, after
control for weight, female sex remained an independent predictor of
postoperative neurological events (OR 1.21, 95% CI 1.14 to 1.28). The
c-index for the model with adjustment for covariates (including weight)
and sex was 0.73. Interactions between sex and other variables
previously identified to indicate high risk for postoperative
neurological events (age, cardiogenic shock, diabetes mellitus, renal
failure, and congestive heart failure) were examined but were not
significant. There was a marginally significant interaction between sex
and cerebrovascular disease
(P=0.0178). The nature of the
interaction was such that the OR for women relative to men was higher
for patients without cerebrovascular disease than for patients with
cerebrovascular disease (OR 1.25 versus 1.09).
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Length of Stay and 30-Day Mortality
The median postoperative length of stay for women was 6
days and for men 5 days
(P<0.001). Among those with a
new postoperative neurological event, the duration of hospitalization
after surgery was similar for both sexes (median 11 days). The overall
30-day mortality
(Table 4) was significantly higher for women than for men
(5.7% versus 3.5%, P<0.001).
For both sexes, the 30-day mortality increased as the complexity of the
surgical procedure increased (CABG versus valve surgery versus combined
CABG and valve surgery) and as the age of the patients increased (from
<50, to 50 to 70, to >70 years). For all types of surgical procedures
and in all age groups, women had a significantly higher 30-day
mortality than men. In the group as a whole, 30-day mortality for
patients with a new neurological event was 7-fold higher than for
patients not detected as having this complication (30% versus 4.2%,
P<0.001). The 30-day mortality
for women who suffered a postoperative neurological event was
significantly higher than for men who suffered this complication (33%
versus 28%,
P<0.001).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Results from this large, multi-institutional STS National Cardiac Surgery Database show that women undergoing cardiac surgery have a higher frequency of new perioperative neurological events and have higher 30-day mortality than men after suffering this complication. These differences remain significant for all types of surgical procedures studied and in all age groups. After multivariable analysis was used to adjust for risk factors that have traditionally been associated with adverse neurological outcomes and after adjustment for body weight, female sex remained independently associated with a higher risk of new neurological events. The findings of the present study confirm results of other studies that show an overall higher 30-day mortality and longer hospitalization after cardiac surgery for women than for men. The present study shows that the increased mortality can be explained, at least in part, by a higher incidence of postoperative neurological events in women.
Importance of Age and Sex in Cardiac
Surgery
Individuals >65 years old are the
fastest-growing segment of the American population. It is projected
that this elderly population will increase from 35 million in 2000 to
>78 million by the year
2050.13 An increase has also
been noted in the number of elderly women undergoing cardiac surgery,
who now account for 
30% of the 700 000 patients undergoing this
surgery in the United States every
year.7 8 This
number is likely to continue to increase for elderly women,
particularly because they experience a delayed onset of cardiac
disease, compared with men, until the onset of menopause, presumably
because of the protective effects of estrogen on the
cardiovascular
system.14 The higher
morbidity and mortality of women undergoing cardiac surgery thus have
important public health implications. Our findings corroborate other
studies showing the important relationship between new neurological
events and increased risk for operative
mortality.10 11 12
This complication is second only to low cardiac output syndrome as the
most important cause of death after cardiac
surgery.10 The results of
the present study extend these findings that women are at higher
risk for new neurological events after cardiac surgery and suggest that
the excess 30-day mortality in women undergoing cardiac surgery may be
explained, at least in part, by the higher incidence of new
perioperative neurological
events.12
Female Sex and Risk for Stroke
Compared with men, women undergoing cardiac
surgery tend to be older and to have more comorbid conditions, which
alone predispose to neurological injury from cardiac
surgery.2 3 4 5 6 7
After adjusting for these factors by multivariable logistic
regression analysis, however, we found that female sex was
independently associated with increased risk of neurological events
after cardiac surgery (OR 1.21, 95% CI 1.14 to 1.28,
P<0.001). Mortality does not
compensate for this sex difference, because women also have higher
30-day mortality. The results of this study thus focus attention on
causes of operative mortality for women other than those traditionally
used to explain sex differences in outcomes (eg, greater age, small
coronary artery size, more frequent
comorbidities).2 3 4 5 6 7
Because the increased susceptibility for neurological events in women
undergoing cardiac surgery cannot be explained by these traditional
risk factors, the question of whether low circulating estrogen
concentrations could have played a role is raised. A large number of
studies have shown that estrogen limits the extent of neuronal injury
in a variety of in vitro and in vivo experimental
models.15 16 17 18 19 20
Whether estrogen replacement therapy results in a reduction in
perioperative strokes is not
known.
Importance of Other Risk Factors
Histories of cerebrovascular disease, diabetes
mellitus, peripheral vascular disease, previous
cerebrovascular accident, and hypertension were independent predictors
of new postoperative neurological events, as has been shown in multiple
studies.10 11
Although this study did not evaluate atherosclerosis of
the ascending aorta and of the aortic arch, other studies have shown
that it identifies patients at high risk of suffering new postoperative
neurological events from
atheroembolism.12 21 22 23 24
It has been documented that age and previous stroke are particularly
strong predictors of adverse neurological outcomes after cardiac
surgery, possibly because they identify patients at higher risk of
atheroembolism and/or those with impaired cerebral blood flow
autoregulation, predisposing to cerebral hypoperfusion during
cardiopulmonary
bypass.10 11 12 25 26
After adjustment for the presence of atherosclerosis of
the ascending aorta and the carotid arteries, it has been shown that
age is not associated with risk for stroke and that previous stroke is
the most significant risk
factor.12 The latter finding
suggests that the risk of perioperative stroke
associated with advancing age is related to other risk factors that are
more prevalent in older patients and not to age per se. The findings of
reduced risk for perioperative neurological
complications in obese patients, those with more severe angina, and
patients taking aspirin are noteworthy. Most postoperative neurological
events after cardiac surgery are due to cerebral embolism, and aspirin
use until the day of surgery may decrease the risk of thromboembolism,
but the association between obesity and risk of
perioperative neurological deficits is not
clear.10 11 12 27 28
Limitations of This Study
The STS National Cardiac Database provides data
from a large number of patients from a wide array of both academic and
private institutions, which enhances the generalizability of these
results. The most important limitation of this study is that, because
information is provided to the database on a voluntary basis, centers
with less than optimal operative results may not provide complete
reports, resulting in a bias toward lower complication rates. The STS
assures strict confidentiality, however, which guards against this
potential problem. Assuming that centers with less than optimal results
comply with full reporting, the results of this study should be widely
applicable, because the inherent bias associated with analysis
of data from a single academic institution is avoided. The rate of
neurological complications found in our study (3.3% of the whole
population) is similar to that found in a recent large
multi-institutional study.11
The neurological end points used in this study are very clearly defined
and probably represent the most severe manifestations of
neurological injury after cardiac surgery.
Conclusions
In this large, multi-institutional study of
416 347 patients undergoing cardiac surgery, we found that compared
with men, women (who composed 32% of the study population) had a
higher incidence of new postoperative neurological events and higher
30-day mortality when they suffered neurological complications. The
higher risk for postoperative neurological complications in women
cannot be fully explained by presently known risk factors.
Development of strategies to reduce neurological injury from cardiac
surgery is necessary to improve mortality associated with cardiac
surgery in both sexes, but particularly in
women.
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Acknowledgments |
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The authors wish to acknowledge Eric Peterson, MD, and T. Bruce Ferguson, MD, for their critical review of the manuscript; Mary Eiken, Society of Thoracic Surgeons, for administrative assistance; and Elizabeth Engeszer, Cardiovascular Division at Washington University, for editorial assistance.
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C. W. Hogue Jr, C. A. Palin, and J. E. Arrowsmith Cardiopulmonary bypass management and neurologic outcomes: an evidence-based appraisal of current practices. Anesth. Analg., July 1, 2006; 103(1): 21 - 37. [Abstract] [Full Text] [PDF]
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C. W. Hogue Jr, T. Hershey, D. Dixon, R. Fucetola, A. Nassief, K. E. Freedland, B. Thomas, and K. Schechtman Preexisting cognitive impairment in women before cardiac surgery and its relationship with C-reactive protein concentrations. Anesth. Analg., June 1, 2006; 102(6): 1602 - 1608. [Abstract] [Full Text] [PDF]
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I. E. Konstantinov, T. Karamlou, E. H. Blackstone, R. S. Mosca, G. K. Lofland, C. A. Caldarone, W. G. Williams, A. S. Mackie, and B. W. McCrindle Truncus Arteriosus Associated with Interrupted Aortic Arch in 50 Neonates: A Congenital Heart Surgeons Society Study Ann. Thorac. Surg., January 1, 2006; 81(1): 214 - 222. [Abstract] [Full Text] [PDF]
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 M. Barak and Y. Katz Microbubbles: Pathophysiology and Clinical Implications Chest, October 1, 2005; 128(4): 2918 - 2932. [Abstract] [Full Text] [PDF]
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 A. A. Fox and N. A. Nussmeier Does Gender Influence the Likelihood or Types of Complications Following Cardiac Surgery? Seminars in Cardiothoracic and Vascular Anesthesia, December 1, 2004; 8(4): 283 - 295. [Abstract] [PDF]
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 T.C. Clayton, S.J. Pocock, R.A. Henderson, P.A. Poole-Wilson, T.R.D. Shaw, R. Knight, and K.A.A. Fox Do men benefit more than women from an interventional strategy in patients with unstable angina or non-ST-elevation myocardial infarction? The impact of gender in the RITA 3 trial Eur. Heart J., September 2, 2004; 25(18): 1641 - 1650. [Abstract] [Full Text] [PDF]
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 H. Rexius, G. Brandrup-Wognsen, A. Oden, and A. Jeppsson Gender and mortality risk on the waiting list for coronary artery bypass grafting Eur. J. Cardiothorac. Surg., September 1, 2004; 26(3): 521 - 527. [Abstract] [Full Text] [PDF]
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V. Vaccarino and C. G. Koch Long-term benefits of coronary bypass surgery: Are the gains for women less than for men? J. Thorac. Cardiovasc. Surg., December 1, 2003; 126(6): 1707 - 1711. [Full Text] [PDF]
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V. Vaccarino, Z. Q. Lin, S. V. Kasl, J. A. Mattera, S. A. Roumanis, J. L. Abramson, and H. M. Krumholz Sex Differences in Health Status After Coronary Artery Bypass Surgery Circulation, November 25, 2003; 108(21): 2642 - 2647. [Abstract] [Full Text] [PDF]
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C. W. Hogue Jr, R. Lillie, T. Hershey, S. Birge, A. M. Nassief, B. Thomas, and K. E. Freedland Gender influence on cognitive function after cardiac operation Ann. Thorac. Surg., October 1, 2003; 76(4): 1119 - 1125. [Abstract] [Full Text] [PDF]
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A. K. Jacobs Coronary Revascularization in Women in 2003: Sex Revisited Circulation, January 28, 2003; 107(3): 375 - 377. [Full Text] [PDF]
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 V. Vaccarino, Z. Q. Lin, S. V. Kasl, J. A. Mattera, S. A. Roumanis, J. L. Abramson, and H. M. Krumholz Gender differences in recovery after coronary artery bypass surgery J. Am. Coll. Cardiol., January 15, 2003; 41(2): 307 - 314. [Abstract] [Full Text] [PDF]
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V. Vaccarino, J. L. Abramson, E. Veledar, and W. S. Weintraub Sex Differences in Hospital Mortality After Coronary Artery Bypass Surgery: Evidence for a Higher Mortality in Younger Women Circulation, March 12, 2002; 105(10): 1176 - 1181. [Abstract] [Full Text] [PDF]
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