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Anesth Analg 2006;102:1602-1608
© 2006 International Anesthesia Research Society
doi: 10.1213/01.ANE.0000219591.10826.17

CARDIOVASCULAR ANESTHESIA

Section Editor:
Charles W. Hogue Jr

Preexisting Cognitive Impairment in Women Before Cardiac Surgery and Its Relationship with C-Reactive Protein Concentrations

Charles W. Hogue, Jr, MD, Tamara Hershey, PhD, David Dixon, PhD, Robert Fucetola, PhD, Abdullah Nassief, MD, Kenneth E. Freedland, PhD, Betsy Thomas, RN, and Kenneth Schechtman, PhD

Departments of Anesthesiology, Psychiatry, Neurology, Psychology, Radiology, and Biostatistics, Washington University School of Medicine, St. Louis, Missouri

Address correspondence to Charles W. Hogue, Jr., MD Department of Anesthesiology and Critical Care Med Johns Hopkins Hospital 600 N. Wolfe St, Tower 711 Baltimore, MD 21287–8711. Address e-mail to chogue2{at}jhmi.edu.


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Preoperative cognitive state is seldom considered when investigating the effects of cardiac surgery on cognition. In this study we sought to determine the prevalence of cognitive impairment in women scheduled for cardiac surgery using nonhospitalized volunteers as a reference group and to examine the relationship between C-reactive protein levels and cognitive impairment. Psychometric testing was performed in 108 postmenopausal women scheduled for cardiac surgery and in 58 nonhospitalized control women. High sensitivity C-reactive protein levels were measured in the surgical patients. Preoperative cognitive impairment was defined as >2 sd lower scores on ≥2 tests compared with the controls. Cognitive impairment was present in 49 of 108 (45%) patients. C-reactive protein levels were higher for patients with compared with those without cognitive impairment (median, 8.1 mg/L versus 4.7 mg/L; P = 0.04). Based on multivariate logistic regression analysis, patient age, lower attained level of education, type 2 diabetes mellitus, and prior myocardial infarction identified risk for cognitive impairment (P < 0.05) but C-reactive protein levels did not (P = 0.09). In conclusion, cognitive impairment is prevalent in women before cardiac surgery. C-reactive protein levels are increased in women with this condition but the relationship between this inflammatory marker and preexisting cognitive impairment is likely secondary to the acute phase reactant serving as a marker for other predisposing conditions.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Subtle neurologic complications manifest as cognitive dysfunction are reported in more than 35% of patients 1 mo after cardiac surgery (1–7). Postoperative cognitive decline is an increasing focus of investigation, in part because of its relation with increased hospital costs, diminished quality of life after hospitalization, and long-term cognitive deterioration (1–7). A limitation of many investigations, however, is the failure to include a control group for assessing baseline cognitive level. Rather, each patient often serves as their own control for comparing postoperative psychometric data. Preexisting cognitive impairment is likely to be prevalent in patients scheduled for cardiac surgery on the basis of advancing age, extensive cardiovascular disease, hypertension, and other factors (6,8–11). A low level of performance on psychometric tests before surgery makes it difficult to demonstrate further reduction after surgery, particularly of a magnitude that would meet a dichotomous definition of cognitive dysfunction (i.e., "basement effect") (12). Failure to consider baseline cognitive state may thus result in erroneous conclusions about the neurologic consequences of cardiac surgery if the methods of detection (cognitive testing) are insensitive for some patients.

There is an expanding recognition for the need to separately consider women and men in clinical trials because patient sex can influence basic biologic processes and pathophysiologic responses to disease (13–15). Women are often under-represented in clinical trials, including those involving cardiac surgical patients. Extrapolating data to women from such trials thus might lead to incorrect conclusions because they represented only a minority of studied patients. In a series of studies our group found that women are at higher risk for neurologic complications from cardiac surgery than men and that this risk could not be explained by known stroke risk factor (16–18). We have further demonstrated gender differences in the cognitive domains affected by cardiac surgery (7). Investigations of cognitive state in patients before cardiac surgery have included mostly men and younger patients and have not provided separate analysis of women (5,9–11).

Inflammation plays a pivotal role in the pathogenesis of cardiovascular disease, including transformation from its stable to unstable disease forms. Blood levels of C-reactive protein, a nonspecific marker of inflammation, have been shown to identify risk for cardiac events and stroke (19,20). Underlying inflammatory processes are thought to contribute to cognitive impairment in the general population, but whether this relationship applies to patients with advanced cardiovascular disease, such as those undergoing cardiac surgery, is not clear (21,22). Understanding the relationship between inflammatory processes and cognitive state in cardiac surgical patients could provide insight into the pathogenesis of these disorders and could also provide a potential means of risk stratification or therapeutic intervention.

The purpose of the study was to assess the prevalence of baseline cognitive impairment in women scheduled for cardiac surgery compared with a group of nonhospitalized control individuals. We further sought to test the hypothesis that there is an association between baseline C-reactive protein levels and cognitive impairment.


   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
All procedures were approved by Washington University’s Human Studies Committee and individual written informed consent was obtained. The patients consisted of 142 females scheduled for elective cardiac surgery. Women were either ≥55 yr of age or had undergone hysterectomy with oophorectomy >6 mo before surgery. Participants were part of a prospectively randomized, double-blind, placebo-controlled study of perioperative 17ß-estradiol replacement for women undergoing cardiac surgery. All data were obtained before receiving study treatment. Exclusion criteria included estrogen use within 6 mo of enrollment, re-operations or cardiac surgery combined with carotid endarterectomy, renal failure requiring dialysis, emergency surgery, history of dementia or clinically evident cognitive impairment before surgery, inability to attend outpatient visits, and inability to speak or read English. Controls consisted of 58 female nonhospitalized volunteers ≥55 yr of age not receiving estrogen replacement for at least 6 mo meeting the same inclusion and exclusion criteria as the surgical patients. Control patients were identified through several sources, including a University registry of individuals willing to participate in clinical research, advertising within our hospital, and personal contacts within the community. Volunteers were paid $25 for participation.

A standard neuropsychological test battery was administered to the patients 1 to 2 days before surgery. The same cognitive testing battery was administered to the controls. The battery is in accordance with Consensus Conference recommendations and provides an assessment of a broad array of cognitive domains including memory, psychomotor speed, mental flexibility, fine motor skill, and visual perception (23). Specific tests included the Rey Auditory Verbal Learning Test, in which a 15-word-list is presented over multiple trials and recall is tested after 30 min; the Digit Symbol subtest of the Wechsler Adult Intelligence Scale, in which participants transcribe number-symbol pairs under timed conditions; Trail-Making Test A and B, in which participants connect numbered and then alternately numbered and lettered dots in order under timed conditions; the Grooved Peg Board Test, in which notched pegs are rapidly placed into fitted holes on a shallow box; and the Benton Visual Form Discrimination Test, in which subjects match target shapes visually (24–30). The Beck Anxiety Inventory and the Beck Depression Inventory were used to assess depressed and anxious mood states (31,32). For the former tests, scores of 10 to 15 and >16 are considered mild and severe anxiety, respectively. For the Beck Depression Inventory, scores of 10 to 15, 16 to 23, and 24 to 63 are considered as mild, moderate, and severe depression, respectively. The Short Blessed Test was used as a screening test for dementia to ensure that patients could provide a fully informed consent (33). The latter is a brief test of cognitive functioning that correlates with clinical dementia staging and with postmortem pathological findings (34). Healthy, neurologically normal subjects average 13 (range, 0–13) on the Short Blessed Test, compared with 15.4 (range, 2–28) for mildly demented and 18.5 for moderately demented patients. The standard cutoff score of 10 is highly sensitive to clinical dementia, but it is also moderately sensitive to subclinical cognitive impairment. Because presurgical anxiety may affect test scores in some cases, a slightly higher cutoff score of >12 was used to exclude patients from further study. Patients scoring between 10 to 12 on the Short Blessed Test were asked to explain the consent form back to the recruiter to ensure that they were capable of providing informed consent.

Clinical data were collected by research nurses. Data that were not available from the medical records were obtained by direct contact with attending medical staff or family. Venous blood specimens were withdrawn the day before surgery and immediately placed in glass tubes devoid of anticoagulants or preservatives. Serum was separated by centrifugation, placed in plastic tubes, and frozen at –70°C until the time of analysis. C-reactive protein concentrations were measured using a high sensitivity immunonephelometry technique (Dade Behring, Newark, DE). The lower detection limit of the assay is 0.175 mg/L.

Preexisting cognitive impairment in surgical patients was defined as >2 sd lower test scores on 2 or more tests compared with cognitive test data obtained in controls. For timed tests in which a longer time indicates decrement in performance (e.g., Peg Board and Trail tests), a score >2 sd higher than control patients was considered as "lower test score." Patients with missing data on one or more tests were not included in the analysis. Categorical data were compared using {chi}2 or Fisher’s exact test. Continuous data were compared using Student’s t-tests. Data that were not normally distributed were compared with the Wilcoxon test. C-reactive protein levels were highly skewed so the data were log-transformed for analysis. Spearman correlation coefficients were calculated between C-reactive protein levels and scores for each cognitive test. Multivariate logistic regression analysis was performed to assess for variables independently associated with cognitive impairment. Variables with a P value of <0.2 based on univariate analysis were included in the model.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Descriptive data for the control volunteers and for surgical patients are listed in Table 1. Thirty-four patients had missing data on one or more cognitive tests that precluded correct classification as having or not having cognitive impairment. Of these patients, 20 had a >2 sd lower score on one test and missing data on another test whereas 14 had missing data on 2 of the psychometric tests. There were no differences between the 34 patients excluded from analysis and the remaining surgical patients in age (70.3 ± 7.9 yr), level of attained education, Short Blessed Test scores (median, 2.0; range, 0–20), or any of the other variables listed in Table 1. Of the remaining 108 patients, 49 (45%) were categorized as having preexisting cognitive impairment. The mean age was older for the surgical patients compared with the volunteers and older for patients with compared with surgical patients without cognitive impairment. Differences were also noted between patients and volunteers in the level of attained education and, not surprisingly, items related to medical history. Patients with cognitive impairment tended to have higher scores (i.e., lower performance) on the Short Blessed Test compared with those without cognitive impairment. Four patients with cognitive impairment had Short Blessed Test scores between 10 and 12.


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  		Table 1. Volunteer/Patient Demographics and Medical History

 

Neuropsychological test results for controls and for surgical patients are listed in Table 2. Differences were noted in all psychometric test results between volunteers and patients with cognitive impairment. Compared with volunteers, surgical patients without cognitive impairment had lower scores on some, but not all, of the psychometric tests. Of note, the grooved pegboard test and Trails A and B are timed tests; a higher score indicates poorer performance.


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  		Table 2. Neuropsychological Test Results for Volunteers and for Surgical Patients With and Without Preexisting Cognitive Impairment

 

The median C-reactive protein concentration was 6.7 mg/L (mean, 15.0 ± 24.6 mg/L; range, 0.20 mg/L to 195.0 mg/L; 95% confidence interval, 11 mg/L to 19 mg/L). Seventy-four percent of surgical patients had C-reactive protein levels higher than that suggested to be associated with high risk for vascular disease (>3 mg/L) and 21% had levels >19 mg/L (35). C-reactive protein concentrations were larger for patients with cognitive impairment compared with patients without cognitive impairment (median, 8.1 mg/L versus 4.7 mg/L; P = 0.04). Significant correlations were found between C-reactive protein levels and Digit Symbol Test (r = –0.186, P = 0.042) and Trail-Making A test results (r = 0.259, P = 0.004) but not for the other psychometric measures.

Results from the multivariate logistic regression analysis are listed in Table 3. Variables independently associated with preexisting cognitive impairment included patient age, level of education, type 2 diabetes, and prior myocardial infarction (MI). A trend was noted for a relation between C-reactive protein concentrations and cognitive impairment (P = 0.09). This model identified 80% of patients with cognitive impairment. Removing the variable MI from the multivariate model resulted in C-reactive protein becoming a significant independent predictor of preexisting cognitive impairment (P = 0.04). The latter model correctly identified 77% of cases of cognitive impairment.


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  		Table 3. Variable Independently Associated with Preexisting Cognitive Impairment

 


   Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Using psychometric testing data from volunteer women for comparison, we found cognitive impairment in 49 of 108 (45%) female patients before cardiac surgery. C-reactive protein levels were higher for patients with than without cognitive impairment, but levels of this acute phase reactant were not independently associated with preexisting cognitive impairment (P = 0.09) based on multivariate logistic regression analysis.

Cognitive decline is an important source of patient morbidity after cardiac surgery (1–7). This complication is believed to result primarily from some combination of cerebral embolism and cerebral hypoperfusion occurring during surgery, particularly when cardiopulmonary bypass is used. Although some studies of the effects of cardiac surgery on cognitive outcomes have included control groups undergoing nonthoracic surgery, many investigations assess changes in psychometric testing from preoperative to postoperative periods with patients serving as their own controls (1–6). Patients undergoing cardiac surgery suffer from widespread cardiovascular disease that predispose to cognitive impairment irrespective of surgery (6,8–11). The importance of including a control group to account for the natural history of cognitive decline is emphasized by recent findings of no differences in cognitive function for patients with coronary artery disease after either coronary artery bypass grafting (CABG) surgery or percutaneous coronary artery interventions (9,10). Regardless, low baseline psychometric test scores may preclude demonstrating subsequent decline after surgery of a sufficient magnitude to meet a dichotomous definition of dysfunction (e.g., decrements of 1 or 2 sd from baseline). Even small decrements in cognition in patients with low baseline cognitive function, however, might have important implications for quality of life although the changes may not be statistically significant.

Women represent a minority of patients undergoing cardiac surgery, but they are at higher risk for complications than men, in part because of older age and a higher prevalence of comorbid medical conditions (36). Other investigations have reported cognitive deficits in candidates for cardiac surgery when compared with healthy controls. Millar et al. (6) reported that 16% of patients had cognitive impairment before CABG surgery using the Stroop screening test and published age-adjusted normative data for comparison. Using a more extensive psychometric battery, Vingerhoets et al. (11) found cognitive and motor impairment in patients before cardiac surgery compared with nonhospitalized controls. In these latter studies the data from both sexes were combined in the analysis, which limits extrapolating the results to women who comprised 18% to 21% of studied patients. Our results thus suggest that cognitive impairment may be even more frequent for women before cardiac surgery.

We selected a control group consisting of community-dwelling women without acute illness who otherwise met inclusion criteria for our 17ß-estradiol replacement study. The age and level of attained education of patients with cognitive impairment differed from volunteers and surgical patients without cognitive impairment. Because these variables were independently associated with risk for cognitive impairment, the high frequency of this condition we observed might be explained in part by the older age and lower level of education of affected patients. Nonetheless, age and level of education were also different between the controls and the surgical patients who were not categorized as having preexisting cognitive impairment. In fact, some psychometric test scores for patients without cognitive impairment were no different than for volunteers despite these differences in age and level of education. Finally, the Short Blessed Test results for patients with cognitive impairment were higher compared with non-affected surgical patients and some patients with cognitive impairment had scores >10. The latter score is highly sensitive for detecting subclinical dementia (33,34). Thus, age and level of education alone can not explain susceptibility to preexisting cognitive impairment.

Prior stroke was more frequent in patients with compared with those without cognitive impairment (23% versus 5%; P = 0.0086) but history of stroke was not independently associated with cognitive impairment. Brain imaging studies of elderly nonhospitalized individuals and cardiac surgical patients demonstrate that clinically reported stroke represents a small portion of the burden of cerebrovascular disease. For example, brain infarction detected with computed tomographic or magnetic resonance imaging is found in 31% of elderly volunteers but <15% of these individuals have a clinical history of stroke (37–39). Further, brain infarction is found with magnetic resonance imaging in >40% of cardiac surgical patients before surgery and most of these patients lack a history of stroke (40,41). Even though affected patients may not report a prior stroke, otherwise clinically "silent" brain infarction is often associated with subtle neurologic manifestations including cognitive impairment (39). Of interest, in nonhospitalized individuals C-reactive protein levels are linked to both large and small cerebral arterial brain infarctions as well as to subcortical white matter lesions associated with cognitive dysfunction (38). Regardless, these data suggest that a clinical history of stroke cannot be relied on for identifying cardiac surgical patients who have suffered cerebral infarction and are thus at higher risk for perioperative neurologic complications (3,16,17).

There are several explanations for why C-reactive protein levels were not independently associated with cognitive impairment in our study in contrast to population-based studies. Conceivably, this inflammatory protein might only serve as a marker for cognitive impairment in the absence of acute inflammatory events such as infection or acute cardiac illness. C-reactive protein levels were indeed significantly associated with cognitive impairment in the multivariate model only when eliminating previous MI. Levels of C-reactive protein in our cohort were higher than many population-based norms. The Centers for Disease Control and the American Heart Association, for example, have issued clinical guidelines suggesting that high sensitive C-reactive protein concentrations of >3 mg/L represent high vascular risk (35). In this study 74% of women had C-reactive protein levels >3 mg/L, most likely reflecting acute disease processes leading to cardiac surgery. Perhaps this should not be surprising in view of more recent findings from the Dallas Heart Study, in which median C-reactive protein levels for women were found to be higher than for men (3.3 mg/L versus 1.8 mg/L, P < 0.001) (42). In that study 51% of women had levels >3.0 mg/L. It is thus possible that the relation between C-reactive protein levels and cognitive impairment might not be as strong for women as for men.

The ultimate frequency of cognitive impairment in the surgical cohort is dependent on the characteristics of the group used for developing the normative data. Others have reported no differences in cognitive performance in patients with coronary artery disease before either CABG surgery or percutaneous coronary interventions (9,10). The number of patients with cognitive impairment might have been less if an older and less educated control group with active cardiac disease was recruited. Our aim was to develop normative data not influenced by underlying cardiovascular illness by enrolling control individuals who were otherwise free of acute illness. Regardless, our findings must be interpreted as an estimate and not as an absolute determination of the frequency of preexisting cognitive impairment. A limitation of any study using psychometric testing is selection bias of subjects consenting to the rigors of such testing. That is, individuals with cognitive impairment might not consent for testing. Although volunteers were tested either in a clinic or in their homes, surgical patients underwent psychometric testing mostly on the hospital ward, which might influence the results, particularly for timed tests (9). Patients but not volunteers would be further exposed to emotional stressors associated with pending major surgery that are difficult to measure. We did find that indicators of anxiety and depression were more frequent between surgical patients and volunteers but not between surgical patients with our without cognitive impairment. Finally, C-reactive protein concentrations were not obtained in the volunteers because normative values are available for community-dwelling adults (42–44).

In summary, these data suggest that preexisting cognitive impairment is prevalent in women about to undergo cardiac surgery. Our results further suggest that, to some extent, C-reactive protein levels are associated with susceptibility to this condition but probably only as a marker of cardiovascular disease. Because preexisting cognitive impairment is an important determinant of risk for cognitive decline after cardiac surgery, preoperative identification of susceptible patients might provide a means for risk stratification and/or focused implementation of neuroprotective strategies.


   Footnotes
 
Supported, in part, by grants from the National Heart, Lung, and Blood Institute, Bethesda, MD (RO1 64600, Charles W. Hogue, Jr., MD, Principal Investigator) and the National Institute of Mental Health (5R01MH060735, Kenneth E. Freedland, PhD, Principal Investigator).

Accepted for publication February 9, 2006.


   References
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 Introduction
 Methods
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 Discussion
 References
 

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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press