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Ann Thorac Surg 2003;76:1119-1125
© 2003 The Society of Thoracic Surgeons

Original article: cardiovascular

Gender influence on cognitive function after cardiac operation

Charles W. Hogue, Jr, MDa*, Rema Lilliea, Tamara Hershey, PhDb, Stanley Birge, MDc, Abdullah M. Nassief, MDd, Betsy Thomas, RNa, Kenneth E. Freedland, PhDb

a Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri, USA
b Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri, USA
c Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri, USA
d Department of Neurology, Washington University School of Medicine,St. Louis, Missouri, USA

Accepted for publication April 8, 2003.

* Address reprint requests to Dr Hogue, Department of Anesthesiology, Washington University School of Medicine, 660 South Euclid Ave, Box 8054, St. Louis, MO, USA 63110
e-mail: hoguec{at}notes.wustl.edu


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Women are at higher risk than men for stroke after cardiac operation. The purpose of this study was to evaluate for gender influences on the more common postoperative neurologic complication, cognitive dysfunction.

METHODS: A standard battery of neuropsychological tests was administered to 117 patients (79 men and 38 women) the day before and again 4 to 6 weeks after cardiac operation. The battery assessed a broad array of cognitive domains, including attention, memory, executive function, and psychomotor processing speed. Analysis was performed only on patients with data from both testing sessions. Data were analyzed to assess for a dichotomous definition of postoperative cognitive impairment and to evaluate for factors influencing test results for specific cognitive domains.

RESULTS: The frequency of one standard deviation decline on two or more cognitive tests compared with preoperative results (women, 10.7 % versus men, 9.9 %; p = 0.527), no decline, or one standard deviation improvement on each test postoperatively was no different between genders. After adjusting for age, gender, preexisting medical conditions, level of attained education, preoperative cognitive tests results, type of operation, and duration of cardiopulmonary bypass, female gender was independently associated with poorer performance postoperatively on visuospatial tasks. Other variables significantly related to postoperative cognitive function varied among the specific cognitive domains.

CONCLUSIONS: These data suggest that, although the frequency of cognitive dysfunction after cardiac operation is similar for women and men, women appear more likely to suffer injury to brain areas subserving visuospatial processing. Risk factors for postoperative cognitive impairment vary depending on cognitive domain, suggesting multiple etiologies for this form of perioperative neurologic injury.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Women are widely reported to have higher morbidity and mortality rates after cardiac operation compared with men [1–5]. Explanations for this finding have focused on gender differences in patient age, coexisting medical conditions, coronary artery size, and diagnostic test utilization [1, 2]. In an analysis of single- and multi-institutional data, our group found that women are at higher risk for perioperative neurologic deficits than men and that these events are an important cause of their poorer surgical outcomes [3–5]. Whereas stroke is reported in 2% to 4% of patients, postoperative cognitive dysfunction is a more common type of neurologic complication occurring in 10% to 50% of patients 6 to 8 weeks postoperatively [3–18]. Postoperative cognitive dysfunction is associated with higher mortality, longer hospitalization, higher hospital costs, long-term impairment in quality of life, and long-term cognitive decline [6, 9, 15, 16]. The influence of patient gender on cognitive dysfunction after cardiac operation has not been extensively evaluated. Insofar as the number of women who have cardiac operations continues to increase, understanding gender-specific risk is an important first step in formulating strategies to improve patient outcomes [19]. The purpose of this study was to evaluate for gender influences on cognitive function after cardiac operation.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Using a protocol approved by the Human Studies Committee of Washington University School of Medicine, and after receiving individual informed consent, 70 women and 118 men over 50 years of age who had elective cardiac operation using cardiopulmonary bypass at Barnes-Jewish Hospital, St. Louis, Missouri, were enrolled. Exclusion criteria for the study included reoperation or cardiac operation combined with carotid endarterectomy, renal failure requiring dialysis, emergency operation, clinically evident cognitive impairment preoperatively, current treatment for any axis I or II psychiatric disorder, inability to attend outpatient visits, and inability to speak or read English.

Research nurses prospectively collected clinical data by daily review of the medical records, review of hospital-wide computerized patient information, and by direct contact with attending medical staff or family when information was not otherwise available. Routine institutional operative care was employed, including standard patient monitoring and an opioid-based anesthetic supplemented with volatile anesthetics and skeletal muscle relaxants. The cardiopulmonary bypass (CPB) circuit was primed with a crystalloid solution, and the apparatus included a membrane oxygenator (Terumo Cardiovascular Systems Corporation, Elkton, MD) and 40-µm arterial catheter filters (Terumo Cardiovascular Systems Corporation). Nonpulsatile perfusion was used during CPB with blood flows between 2.0 and 2.4 L/m2 per minute using an ascending aorta cannula. The patients were managed during CPB with the {alpha}-stat pH method with arterial carbon dioxide tension maintained between 35 and 40 mm Hg. The patient's body temperature ranged from 28°C to 33°C during CPB measured by a bladder temperature probe. During patient rewarming the gradient between the water of the heat exchanger and body temperature was kept below 5°C but did not exceed 39°C. During the operation, aspirated pericardial blood was returned to the CPB reservoir without additional filtering.

All patients had continuous telemetry electrocardiographic monitoring postoperatively until hospital discharge. The postoperative complications that were recorded included clinically detected myocardial infarction, low cardiac output syndrome (cardiac index <2.0 L/m2 per minute for more than 8 hours postoperatively regardless of treatment), atrial fibrillation, mediastinal reexploration, allogeneic blood transfusion, tracheal intubation longer than 24 hours, renal failure requiring hemodialysis, and stroke. The definition of stroke was a nonreversible new permanent global or focal neurologic deficit not caused by metabolic abnormalities or centrally acting drugs. Postoperative physical examinations were performed daily by the attending medical staff. Clinically suspected strokes were confirmed by a neurologist based on detailed neurologic examination and usually with head computed tomography or magnetic resonance imaging. Operative death was defined as death during the same hospitalization as the operation or death within 30 days of that operation.

Cognitive testing
A standard battery of neuropsychological tests was administered to patients the day before operation and 4 to 6 weeks postoperatively. This battery assesses a broad array of cognitive domains affected by cardiac operations and is in accordance with Consensus Conference recommendations [20, 21]. The presented order of the tests was the same at both sessions. Cognitive domains tested and specific neuropsychological tests used are listed in Table 1. The Rey Auditory Verbal Learning Test involves several presentations of a 15-word list followed by a recall trial and then a 30-minute delayed recall [22]. The Facial Recognition subscale of the Wechsler Memory Scale requires the patient to discriminate between familiar and unfamiliar human faces [23]. The Paragraph Recall subscale of the Wechsler Memory Scale requires the recall of short story themes and details that were read to the patient [24]. The Digit Symbol subscale of the Wechsler Adult Intelligence Scale involves the matching of shapes and copying with numbers under time pressure [25]. The Digit Span subscale of the Wechsler Adult Intelligence Scale requires the subject to repeat lists of digits in their original order and other lists in backward order [25]. Trails A requires the timed connection of a series of circled numbers with a drawn line [26]. Trails B is similar except that the subject alternates between letters and numbers [26]. The Grooved Peg Board test involves placing notched pegs into properly fitting holes on a shallow box [27]. The pegs fit into the holes only when placed in the proper orientation. The Benton Visual Form Discrimination test requires subjects to match a target object with one of several options [28]. Parallel forms of the Rey Auditory Verbal Learning test and Wechsler Memory Paragraph Recall tests were used to minimize learning effects with repeated testing.


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  		Table 1. Cognitive Domains and Neuropsychological Tools Used For Testing

 
Statistical analysis
Analysis was performed only when cognitive test data were available from both the preoperative and 4-to-6-week postoperative testing periods. {chi}2 tests were used in univariate analyses of categorical variables to identify significant differences between male and female patients, and two-tailed t tests were used for continuous variables. Analysis of covariance with each effect adjusted for all other effects in the model was used to test the hypothesis that continuous postoperative neurocognitive test scores differ by gender, adjusting for preoperative scores, age, educational level, diabetes, hypertension, type of surgical procedure, and duration of cardiopulmonary bypass [8–13]. Logistic regression was used to determine the effects of gender on categorical neurocognitive outcomes after adjusting for the same set of covariates. Alpha was set at 0.05 per comparison.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Cognitive test results from both testing sessions were available for 38 of 70 (54.3%) women and 79 of 118 (66.9%) men (women versus men, p = 0.098). Reasons for missing data include operative death (4 women versus 8 men, p = 0.517), perioperative stroke (4 women versus 3 men, p = 0.282), or discharge from the hospital to a nursing home (16 women versus 6 men, p < 0.001). Eight women and 22 men were unable or refused to return for follow-up testing (p = 0.122). Patient characteristics for women and men included in the analysis are listed in Table 2. There was no difference in age between genders, but differences were observed in body weight, frequency of peripheral vascular disease, and preoperative use of diuretics. Compared with men, there were trends for women to have a higher frequency of hypertension and a history of congestive heart failure. Four women were receiving estrogen replacement therapy preoperatively and 5 women reported prior but not current estrogen usage. Women were less likely to have had primary coronary artery bypass grafting (CABG) than men, but they were more likely to have had isolated mitral valve operation. The duration of CPB was shorter in women than men. Women were more likely than men to receive transfusion of packed red blood cells and fresh frozen plasma. There were no differences in the frequencies of listed complications between genders.


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  		Table 2. Demographics and Patient Characteristics for Women and Men

 
Univariate comparisons of cognitive test results between genders are given in Table 3. Lower scores indicate worse cognitive performance on the Benton Visual Form Discrimination, Facial Recognition I and II, Rey Delayed Auditory Recognition, Digit Symbol, Digit Span, and the Paragraph Recall tests. The Trails A and B and Grooved Peg Board tests are timed tasks, so higher scores (longer time) indicate poorer performance. The mean postoperative test scores indicated that women performed significantly worse on the Trails A and B, the Benton Visual Form Discrimination, and the Grooved Peg Board (dominant hand) tests than men. With the exception of the Grooved Peg Board tests, these test scores were not different between genders preoperatively. There was no difference between genders in the frequency of a one-standard deviation (SD) decline, no decline, or one-SD improvement for each cognitive test at the 4 to 6 week postoperative testing period compared with preoperative test results. The frequency of a one-SD decline from the preoperative to the postoperative testing periods on two or more postoperative cognitive tests was no different between genders (women, 10.7 % versus men, 9.9 %; p = 0.527).


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  		Table 3. Unadjusted Cognitive Test Results From the Preoperative and Postoperative Testing Sessions by Gender

 
Table 4 lists variables that were related to performance on each postoperative cognitive test result after statistically adjusting for age, gender, preoperative test results, diabetes, hypertension, duration of CPB, level of education, and type of operation. Preoperative test score was significantly correlated with postoperative results for each test. Gender was a significant predictor of measures of visuospatial processing and visual memory (Benton Visual Form Discrimination and Facial Recognition I). Other variables that were related to the adjusted results varied depending on the specific cognitive test. Age was a significant predictor of test performance on measures of visuospatial processing, visual memory, and immediate verbal memory. Level of education was a significant predictor of performance in several cognitive domains, whereas diabetes selectively influenced the results of tests of complex attention and visuomotor processing speed. A history of hypertension and type of operation had minimal influence on postoperative cognitive performance. The duration of CPB was not a significant predictor of any postoperative test result.


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  		Table 4. Variables Related to Postoperative Cognitive Test Performance After Adjusting for Age, Gender, Medical Conditions, Preoperative Test Results, and Operative Factors

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Although mortality rates for cardiac operations have steadily declined over the past decade, neurologic complications remain a substantial source of morbidity and mortality, especially for the increasing numbers of elderly patients who are particularly susceptible to these complications [3–6, 19]. In a series of prior investigations, our group has found that women are at higher risk than men for stroke after cardiac operation and that this complication contributes significantly to a higher mortality rate [3–5]. In this study we report that the frequency of postoperative cognitive impairment using a categorical definition (one SD decline on two or more cognitive measures) was not different between women and men (women, 10.7% vs men, 9.9%; p = 0.527). These data are consistent with the findings of both Newman and colleagues [16] and Kadoi and associates [17], who reported that female gender is not a significant predictor of cognitive decline after CABG. The expected finding of repeat cognitive testing, however, is an improvement in scores due to practice effects, better testing conditions, and reduced anxiety postoperatively, leading some investigators to suggest that failure to improve postoperative test scores, and not necessarily only a decline in test scores, itself may indicate postoperative cognitive dysfunction [11, 12, 14]. We found, however, that there was no difference between genders in the frequency of patients showing no change or a one-SD improvement in postoperative test results compared with the preoperative results.

Although a dichotomous definition of cognitive impairment is useful for determining the frequency of cognitive dysfunction especially for intervention trials, it is less sensitive for assessing the effects of cardiac operation on specific cognitive domains [9–13]. Thus, we further compared the continuous score data for specific cognitive tests between women and men. Differences were found between genders on the mean scores of specific cognitive tests (Table 3). In some cases (eg, Benton Visual Form Discrimination) these differences were small and might be explained by a decrease in the test score variability (ie, standard deviation) postoperatively. Further analysis was performed on the combined data by using statistical methods to adjust for differences between genders in factors that might influence the results. After these adjustments we found that gender was significantly related to poorer performance on tests of visuospatial processing (Benton Visual Form Discrimination test and Facial Recognition test I). Trends for gender to influence executive function and mental flexibility (Trails B test) were also noted. These results are somewhat similar to those reported by Selnes and associates [11], who found that female gender was independently associated with decline in visual memory 1 month (p = 0.017) and 1 year (p = 0.018) after CABG. Together these data suggest that the frequency of cognitive dysfunction after cardiac operation is not different between genders, but the effects of cardiac operation on specific cognitive domains are different between women and men.

An explanation for why gender might influence impairment of specific cognitive domains after cardiac operation is not forthcoming. The etiology of perioperative neurologic injury is believed to result primarily from cerebral microembolism and macroembolism with or without cerebral hypoperfusion [4, 6–8, 11, 14]. A larger embolic load to cerebral areas subserving visual tasks for women compared with men would be a possible explanation for our findings. However, this seems unlikely based on data showing that microembolism results in diffuse cerebral injury [29]. Another explanation might be higher susceptibility of women than men to regional cerebral hypoperfusion to watershed areas at the junction of major cerebral arteries subserving visuospatial processing. Women who have cardiac operations are more likely than men to have preexisting hypertension; in this study, hypertension was more prevalent in women than men (p = 0.084) [1, 3, 5]. Impaired blood pressure–blood flow autoregulation associated with hypertension and with preexisting cerebrovascular disease might predispose affected patients to cerebral hypoperfusion during CPB when blood pressure is often maintained at low levels (approximately 50 mm Hg) [8, 14, 31, 33]. Nonetheless, in this study hypertension alone had minimal influence on postoperative cognitive function. Finally, the role that the loss of the positive modulatory effects estrogens have on cognitive function and that the loss of the natural neuroprotective properties of estrogen might have on cognitive function after cardiac operation in postmenopausal women is not determinable from these data [32–38].

In addition to gender, we found that factors associated with poor performance on specific tests varied depending on the cognitive domain (Table 4). These findings are similar to those reported by Selnes and associates [11]. Those investigators found that postoperative change in cognitive function was related to medical and surgical variables and time points of the evaluation. These results suggest multiple etiologies for postoperative cognitive dysfunction, including nonspecific effects of anesthesia and prolonged operating time and convalescence interacting with the specific effects of the operation. The latter observation would have important implications on preventative and treatment strategies.

In this study, women were more likely than men to have cardiac valvular operation, whereas the frequency of isolated CABG was higher for men. There were no differences between genders in the frequency of concomitant CABG and valvular operation. Other investigations have found that the frequency of cognitive dysfunction is no different for patients who had cardiac valvular operation compared with CABG [39, 40]. In our analysis, we adjusted for type of operation, and we found that valvular operation was only weakly related to postoperative scores on tests of attention and psychomotor processing speed (Digit Span tests). Thus, differences in the type of procedure do not appear to explain our findings of higher susceptibility for decline in visuospatial processing and visual memory for women after cardiac operation.

Limitations of the current study are (1) the failure to determine the importance of the cognitive test scores for functional outcomes and quality of life and (2) the lack of long-term cognitive assessments. There is still much controversy on how to best define cognitive dysfunction after cardiac operation. The frequency of this complication varies markedly, depending on the timing of the testing and definitions used [9–12, 18]. Our findings that 10% of patients would be classified as having postoperative cognitive impairment is within the range reported by others (10% to 38% 2 months postoperatively) using a similar definition of one-SD decline on two or more tests compared with the preoperative test results [12]. This frequency is lower, though, than the rates reported by other investigations who used different methodologies (eg, 20% to 50% 6 weeks postoperatively) [8, 9, 14, 16, 17]. In some of these latter studies patients with a stroke were classified as having a neurocognitive deficit, and missing cognitive data were imputed to the score meeting the definition of decline. In this study we analyzed data only when preoperative and postoperative tests results were available, and we excluded patients who had stroke. Nevertheless, any definition of cognitive dysfunction is dependent on the fidelity of the preoperative test data as representing a true baseline for comparison of each patient's postoperative test results. In light of contemporary cardiac surgical practices that minimize preoperative hospitalization, performing cognitive testing immediately before major operations most likely does not represent a true baseline for many of the patients. This consideration undoubtedly influences the rate of cognitive decline we observed. Nonetheless, our primary emphasis was on the evaluation of specific cognitive domains and not absolute frequency of cognitive dysfunction, and the male and female patients were tested under comparable conditions.

In conclusion, these data suggest that the frequency of cognitive dysfunction is similar for women and men after cardiac operation. Women, however, appear more likely than men to suffer injury to brain areas subserving visuospatial processing and visual memory. Risk factors for postoperative cognitive impairment vary depending on cognitive domain, suggesting multiple etiologies for this form of perioperative neurologic injury. [30]


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
Supported in part by grants from the National Heart, Lung, and Blood Institute (RO1 HL64600, Dr Hogue principle investigator) and the National Institute of Mental Health (RO1MH060735, Dr Freedland, principle investigator) of the National Institutes of Health, Bethesda, Maryland.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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T. K. Rosengart, J. Sweet, E. B. Finnin, P. Wolfe, J. Cashy, E. Hahn, J. Marymont, and T. Sanborn
Neurocognitive Functioning in Patients Undergoing Coronary Artery Bypass Graft Surgery or Percutaneous Coronary Intervention: Evidence of Impairment Before Intervention Compared With Normal Controls
Ann. Thorac. Surg., October 1, 2005; 80(4): 1327 - 1335.
[Abstract] [Full Text] [PDF]

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