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Ann Thorac Surg 1997;63:510-515
© 1997 The Society of Thoracic Surgeons
Zanvyl Krieger Mind/Brain Institute and Departments of Neurology, Surgery, and Oncology, Johns Hopkins University, Baltimore, Maryland
Accepted for publication September 26, 1996.
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Methods. Cognitive testing was done preoperatively and 1 month and 1 year postoperatively in 127 patients undergoing coronary artery bypass grafting. Tests were grouped into eight cognitive domains. A change of 0.5 standard deviation or more at 1 month and 1 year from patient's preoperative Z score was the outcome measure.
Results. We identified four main outcomes for each cognitive domain: no decline; decline and improvement; persistent decline; and late decline. Only 12% of patients showed no decline across all domains tested; 82% to 90% of patients had no decline in visual memory, psychomotor speed, motor speed, and executive function; 21% and 26% had decline and improvement in verbal memory and language; approximately 10% had persistent decline in the domains of verbal memory, visual memory, attention, and visuoconstruction; and 24% had late decline (between 1 month and 1 year) in visuoconstruction.
Conclusions. This study establishes that the incidence of cognitive decline varies according to the cognitive domain studied and that some patients have persistent and late cognitive changes in specific domains after coronary artery bypass grafting.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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For editorial comment, see 322.
The prevalence of cognitive decline assumes considerable importance today when CABG has become a routine procedure for patients with coronary artery disease: indeed, in the United States alone, 485,000 CABG procedures were performed in 1993 [6]. Thus, a potentially large population of patients may be at risk for cognitive decline after CABG, and the problem becomes even greater if these declines persist over a prolonged period.
To evaluate these longer term declines, we designed a prospective, longitudinal study of patients undergoing CABG and tested them preoperatively and 1 month and 1 year postoperatively. We devised a test battery that included eight cognitive domains (verbal memory, visual memory, language, attention, visuoconstruction, psychomotor speed, motor speed, and executive function) to determine whether specific cognitive functions were changed postoperatively. We investigated two issues: first, the incidence of cognitive change for this population within each specific cognitive domain and second, whether the cognitive changes persisted over time.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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All 172 patients tested preoperatively completed institutional review board consent (approved January 28, 1992). Because of death or refusal to continue participation, 45 of the 172 patients did not complete the study (mean education level = 11.3 years and mean national adult reading test score Wechsler Adult Intelligence Scale-Revised intelligence quotient equivalent = 103). The final sample included 127 patients who completed testing at all three times (mean education level = 13.3 years and mean national adult reading test score Wechsler Adult Intelligence Scale-Revised intelligence quotient equivalent = 107). The characteristics of these patients compared with all others are shown in Table 1
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At the time of preoperative testing, demographic data and medical history were also obtained by study investigators. Because many patients underwent cardiac catheterization at other institutions, data such as cardiac ejection fraction were not available for all patients. Therefore, a cardiac sickness index was created to quantify the severity of symptoms of coronary artery disease. The patient's preoperative location (home, hospital, or intensive care unit) and preoperative anticoagulation status were combined to classify the patient into one of four cardiac sickness index groups (see Table 1
). Postoperative complications including stroke or death were recorded.
Surgical Procedure
The surgical procedures were similar among the four surgeons. All patients had hypothermic (mean temperature, 26.7°C; range, 20.1° to 34.2°C) cardiopulmonary bypass support (mean cardiopulmonary bypass time, 102 minutes) with Sarns/3M roller-head pumps (Ann Arbor, MI), Bentley 1040D heparin-coated arterial line filters, and either a Bentley Univox membrane oxygenator or a Bentley B10-Plus bubble oxygenator (Irvine, CA). Pulsatile perfusion (20% of patients) was applied according to surgeon preference. Crystalloid cardioplegia was used in all patients, and anesthesia management consisted of a combination of benzodiazepines (midazolam hydrochloride, diazepam, and lorazepam), inhalation agents, and opiates (fentanyl citrate and sufentanil citrate). Intraarterial and pulmonary artery catheters were used for intraoperative monitoring. Temperatures were monitored with rectal and esophageal probes. Arterial blood gas samples were obtained at 15-minute intervals while patients were on cardiopulmonary bypass. Alpha-stat blood gas management was used during hypothermic cardiopulmonary bypass. A cell-saving device (Haemonetics, Braintree, MA) provided intraoperative blood conservation (cardiac surgical protocol).
Test Battery and Cognitive Domains
The neuropsychologic battery comprised the following tests [7] given in this order: written alphabet Test [8], Rey Auditory Verbal Learning Test trials 1 through 7, Rey Complex Figure copy and immediate recall, Digit Span (forward and backward), Boston Naming Test (short version), Grooved Pegboard (dominant and nondominant hands), National Adult Reading Test (done preoperatively only), Stroop Color and Word Test, Rey Auditory Verbal Learning Test trial 8, Rey Complex Figure delayed recall, and Symbol Digit Modalities Test (including paired recall). The tests and subtests from this battery were then grouped into eight cognitive domains (Table 2).
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for descriptive purposes. Preoperatively, group means were generally in the expected range for a sample of this age and educational level. However, as group measures of central tendency may obscure important changes in performance in individual patients, the p values reported in Table 2 are not central to the primary result of this study. Instead, we examined patterns of cognitive change in all patients individually (as described next), using the change in each patient's performance from preoperative testing as the outcome.
Statistical Methodology
A Z score, which is a standardized score with a mean of zero and an SD of one, was derived for each test based on the preoperative distribution of scores for the subset of the population (n = 127) with data from all three times. The raw scores are shown in Table 2. A single Z score based on the arithmetic mean of the Z scores for each of the tests within a domain was then derived. The change in score for an individual patient was calculated as the difference between the preoperative and 1-month/1-year follow-up as well as the 1-month to 1-year Z scores for each domain.
We chose a decrease of 0.5 SD or more in a Z score as the definition of decline. Because it has been shown that the expected outcome is an increase over baseline scores (from practice effects caused by repeated exposure to the same test), this should represent an actual decline of greater than 0.5 SD. There is evidence from studies of normal aging populations that repeated exposure to tests results in improved performance secondary to practice effects. The magnitude of this effect varies by test and is more pronounced in patients less than 75 years of age [9]. Epidemiologic studies have also suggested that a decline of 0.5 SD or more is of importance [10], and this end point has been used previously [11].
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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, the groups appear similar in regard to preoperative factors. However, there was a significant difference between the groups for the cardiac sickness index, which indicated that patients not completing or not enrolled in the study had more severe cardiac symptoms. Forty-five of the 172 enrolled patients did not complete 1-month testing, 1-year testing, or both. The mean preoperative Z score for these patients was -0.339 compared with 0.081 for the 127 who completed testing (p < 0.001 by Student's t test). Patients did not complete testing for the following reasons: 1 patient had a disabling stroke in the immediate postoperative period, 2 patients died of stroke, 7 additional patients died within the first year after CABG, and 35 patients refused follow-up testing at one or both postoperative times. Therefore, because patients enrolled in the study had less severe cardiac symptoms and because those completing the study performed better on preoperative testing, the incidence of cognitive decline reported here is probably underestimated.
Incidence of Cognitive Decline
The percentage of patients who showed a decline of 0.5 SD or more at 1 month and at 1 year in each cognitive domain is presented in Table 3. About 30% of patients had a decline in the verbal memory and language domains at 1 month, but performance improved in most patients at 1 year. Only a small percentage of patients (fewer than 9%) showed decline in the domains of visual memory, psychomotor speed, and motor speed at 1 month and 1 year. A slightly higher percentage of patients showed a similar decline in the attention domain at 1 month and 1 year.
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Pattern of Change Outcomes for Each Cognitive Domain
Examination of Table 3 indicated that the frequency of decline was quite different among specific cognitive domains at 1 month and 1 year. To characterize the performance of individual patients, we plotted the changes in each cognitive domain for each patient and identified the following four outcomes:
The percentage of patients showing a particular outcome within each cognitive domain is shown in Table 4. Only 12% of patients showed no decline across all domains tested. In the domains of psychomotor speed, motor speed, visual memory, and executive function more than 80% of patients had no decline over time. In contrast, a decline at 1 month followed by improvement at 1 year occurred in verbal memory, language, and visuoconstruction in 15% to 26% of patients. A late decline in visuoconstruction was seen in 24% of patients and in 11% to 13% of patients in the executive function, language, and attention domains.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Outcome Patterns
For the outcome "no decline," a patient's domain score does not decline by more than 0.5 SD from the preoperative score at 1 month or 1 year. For a variety of reasons including practice effects, improved testing circumstances, and lower emotional stress and anxiety in the postoperative period [12], this would be the expected outcome if the operation had no cognitive effects. A large percentage of patients showed no decline in the domains of visual memory, psychomotor speed, motor speed, and executive function.
Although we did not include a control group in our study, other studies [13, 14] that have examined nonsurgical control groups have shown either no change or improvement in follow-up test scores. When CABG patients were compared with other surgical control groups, cognitive decline was seen in both groups, but to a larger extent in the cardiac patients [2]. Thus, currently available studies demonstrate that nonsurgical control patients tend to improve on cognitive testing, whereas patients who have had a surgical procedure other than a cardiac operation tend to show some decline on cognitive testing but to a lesser degree than do cardiac patients. Of note, none of these studies followed up control patients for longer than 7 months. Therefore, the cognitive performance of control patients for longer periods is not known. Additional study is required to establish the extent and duration of change that is specifically related to cardiac operation.
For the outcome "decline and improvement," a patient's domain score declines at 1 month but improves at 1 year. This outcome has been observed by other investigators who have examined group mean scores and has led some [14] to conclude that the cognitive effects after CABG are transient. Our results show that decline and improvement occurs, mostly in the domains of verbal memory and language and to a lesser extent in other areas of cognition.
These two outcomes (no decline and decline and improvement) demonstrate that for certain cognitive domains, patients have little change at 1 year after CABG. In contrast, in other domains, patients have persistent or late declines in specific cognitive areas at 1 year. The identification of these latter two outcomes is of particular interest, as they highlight patterns of change not previously characterized.
For the outcome "persistent decline," a patient's domain score declines and does not improve at 1 year. This includes scores that decline at 1 month and do not improve at 1 year as well as those scores that have a slow progression resulting in a decline at 1 year. Approximately 10% of patients exhibited this persistent decline in the domains of visuoconstruction, verbal memory, visual memory, and attention. Although this percentage is relatively small, because of the large number of CABG procedures being performed nationwide, it could represent a significantly large number of individuals at risk for a nonreversible neurologic injury.
For the outcome "late decline," a patient's domain score, independent of performance between the preoperative and 1 month times, declines by 0.5 SD or more from 1 month to 1 year. This unexpected result may represent a delayed response to injury. As few studies have followed patients for more than 6 months, it is likely that this late decline would have been missed in the majority of other studies.
Nevertheless, when data in studies of long-term cognitive outcomes were examined, suggestions of similar decline were found. In a study of CABG patients [15], our review of the data showed decline in the Benton Test of Visual Retention and subtle slowing in Trailmaking Test B performance at 24 months. In a group of cardiac surgical patients, Åberg and colleagues [16] reported late decline on a battery of three tests with strong visuospatial components. Sotaniemi and co-workers [17] also described a similar late decline phenomenon. However, the patients in the latter two studies are not comparable with those in our study, because those patients had had intracardiac operations and prosthesis placement. In our study, late decline was observed most frequently in the domain of visuoconstruction, where the deficit was noted in the copying of a complex figure.
Our study indicates that for more complete characterization of cognitive decline, patients should be followed for at least 1 year after CABG. For example, those with persistent decline may eventually show improvement or further decline. Whether these changes occur requires evaluation at longer intervals, which we plan in an ongoing study of this population.
Mechanisms of Injury
Two pathophysiologic mechanisms have been proposed to underlie neural injury associated with CABG, hypoperfusion, and multiple emboli [18]. Although these two mechanisms might explain the appearance of decline and improvement or of persistent decline, they may not explain the late decline seen in this study. Delayed decline in neurologic function after an acute injury to the nervous system has been reported in a number of circumstances, including radiation therapy [19] and postpoliomyelitis syndrome [20]. In addition, the delayed effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on the substantia nigra [21] in some patients suggest damage to a population of neurons, which is then manifested by clinical symptoms after an interval of months or years. This type of biphasic response to injury is not typically associated with anoxia, with the possible exception of changes that take place after carbon monoxide exposure [22]. In that situation, however, the mechanism of delayed changes in neurologic and cognitive function appears to be related to white matter pathology and not cortical neuronal loss.
Use of domains of cognition as defined here may help identify underlying neural mechanisms involved in cognitive decline. In addition, the use of patterns of cognitive change over time may provide an understanding of how the brain responds to injury.
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Acknowledgments |
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We acknowledge the contributions of Drs Pamela Talalay and Marilyn Albert for their assistance in preparation of the manuscript.
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