Ann Thorac Surg 2005;80:910-916
© 2005 The Society of Thoracic Surgeons
Original article: Cardiovascular
Examination of the Use of Cognitive Domains in Postoperative Cognitive Dysfunction After Coronary Artery Bypass Graft Surgery
Matthew S. Lewis, BAppSc Hons
a
,
b
,
*
,
Paul T. Maruff, PhD
a
,
b
,
Brendan S. Silbert, MBBS, FANZCA
a
a Centre for Anaesthesia and Cognitive Function, Department of Anaesthesia, St. Vincent’s Hospital, Victoria Parade
b School of Psychological Science, La Trobe University, Melbourne, Australia
Accepted for publication March 23, 2005.
* Address reprint requests to Mr Lewis, Department of Anaesthesia, St. Vincent’s Hospital, Victoria Parade, Melbourne, Australia 3065 (Email: m.lewis{at}latrobe.edu.au).
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Abstract
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BACKGROUND: Cognitive domain summary scores have been used to examine postoperative cognitive dysfunction in a number of influential studies. To successfully examine cognitive dysfunction in this way, the domains need to be consistent during the assessment time points or the results are distorted. The current study examines two methods of determining cognitive domains and examines their temporal stability during serial cognitive assessments after coronary artery bypass graft surgery.
METHODS: Two hundred and four coronary artery bypass graft patients and 80 matched healthy control subjects 55 years or older completed a battery of neuropsychological assessments at baseline and at 7 days and 3 months. Domains were determined in two ways. The first was based on precedence, and neuropsychological tests were allocated to commonly attributed cognitive domains. The second method was to conduct principal components analysis to statistically determine the domains at each time. The stability of these factors was then assessed over time by conducting repeated analysis.
RESULTS: There were discrepancies between the two methods used to determine decline, and among the factors in the control and surgical groups. Stability with time was not evident as the factors varied within the groups.
CONCLUSIONS: The assessment of postoperative cognitive dysfunction would be best served by the use of individual test results with efforts made to minimize false-positive classification as the extracted cognitive domains do not appear to be temporally consistent, and were sample specific.
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Introduction
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Postoperative cognitive dysfunction (POCD) is a subtle disorder of cognition that can affect up to 42% of coronary artery bypass graft (CABG) patients for up to 5 years after surgery [1], and has been observed to occur to a lesser degree after both major and minor noncardiac surgery [2, 3]. Postoperative cognitive dysfunction is believed to reflect that some change in brain function has arisen perioperatively, and although this has been related to microemboli, hypoperfusion, and other surgical factors [4–7], the specific cause remains unknown. Importantly, the incidence of POCD has varied with the different methodologies used across studies of CABG [8, 9]. Therefore, although the existence and importance of POCD has been demonstrated, it is now important to develop theoretically sound methods to increase the reliability of estimates of the incidence of POCD.
Postoperative cognitive dysfunction is classified when there is a decline in cognitive function detected from the repeated administration of neuropsychological tests before and after surgery. The neuropsychological tests are selected so that they measure a range of cognitive functions consistent with recommendations from consensus groups [10]. Neuropsychological tests are classified as measuring a specific aspect of cognition, according to the dominant cognitive strength believed necessary for successful completion of the test [11]. In neuropsychological studies, data from different neuropsychological tests that assess similar cognitive functions are often organized into single cognitive domains for analysis and interpretation. For example, data from word recall tasks and word recognition tasks may be organized to yield a memory domain score, whereas data from peg placement and finger tapping tasks may be organized to yield a motor domain score. Studies of POCD have generally focused on measuring the domains of memory, attention, manual dexterity, and executive function [12].
In studies of POCD, two methods have been used to group data from individual neuropsychological tests to form cognitive domains; factor extraction from baseline neuropsychological test performance assessment [13] and the application of theoretical models [14]. For the factor extraction method, the baseline data from all of the neuropsychological tests are submitted to principal components analysis, which searches for commonalities in the data and derives underlying factors that can more readily explain the pattern of results [15]. This technique allows for the simplification of complex data sets by reducing the number of variables to a set of fewer underlying factors to explain performance. The theoretical method classifies neuropsychological test data into cognitive domains based on standard neuropsychological brain behavior models (see Lezak [11] for a more thorough discussion of neuropsychological assessment and methods). These theoretical models are typically based on studies of patterns of cognitive strengths and weaknesses in patients with focal brain lesions. These derived domains are then applied to the data drawn from subsequent assessments. Ideally, the two different classification methods should identify the same cognitive domains.
The practice of organizing data from different neuropsychological tests into cognitive domains is derived from conventional clinical neuropsychological assessment in which patients generally complete many tests in a single assessment session. Conclusions about the nature of any cognitive impairment are based on the profile of strengths and weakness in cognitive performance on the different tests. In research settings in which one group is compared with another, performance measures from multiple tests of the same cognitive domain are often expressed as composite scores, thereby reducing the number of end points and the possibility of falsely classifying an individual as abnormal when in reality they are not (ie, reduced Type I error). In some POCD studies, researchers have also sought to reduce study end points by comparing neuropsychological performance over time using composite scores reflecting cognitive domains [14]. However, the extent to which cognitive domains defined on the basis of covaration in performance at one point in time are stable and reliable as a function of time is not really known. Furthermore, once the structure of the cognitive domains measured by any test battery has been determined using either the statistical or theoretical method, performance across subsequent assessments is then fitted to the domain model creating domain summary scores for each time point [14]. However, decisions about POCD based on change in cognitive domain scores assume that the relationship among data from each of the neuropsychological tests given to patients and the cognitive domains computed from the performance data remains constant over time. As far as we can determine this assumption has not be tested in CABG studies.
Therefore the current study had two aims. First we compared the cognitive domains that resulted from classification of neuropsychological data using the theoretical and principal components methods. We performed this analysis both in patients undergoing CABG and in healthy control subjects. The second aim was to determine the stability of the cognitive domains with time in both the CABG and control groups. The usefulness of the cognitive domains for identifying POCD was then determined by the extent to which the domain structure was consistent between methods of definition and to which it remained stable with time in both patients undergoing CABG and in age-, education-, and sex-matched control subjects tested during the same intervals.
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Patients and Methods
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Participants
Coronary artery bypass graft patients
Subjects were 204 patients who were scheduled to undergo first-time elective CABG surgery and were drawn from two sites involved in the larger prospective, randomized, Australian Trial Investigating Postoperative Deficit, Early Extubation, and Survival (ANTIPODES). All participants were older than 55 years. Exclusion criteria were poor ventricular function (ejection fraction <0.30), associated major systemic illness, preexisting neurologic disease, or anticipated difficulty with neuropsychological assessment (eg, difficulty with eyesight or hearing, poor English comprehension, hemiparesis). The demographic details are included in Table 1.
Anesthesia consisted of temazepam premedication, midazolam, fentanyl (either 10 or 50 µg/kg), propofol, and rocuronium. Arrest of the heart was managed using a combination of antegrade and retrograde warm blood cardioplegia without active cooling. Proximal anastomoses were performed under aortic cross-clamping, and cardiopulmonary bypass was undertaken with a membrane oxygenator and roller or centrifugal pump with continuous flow of 2.0 to 2.4 L · min–1
· m–2, moderate hypothermia (32° to 34°C), and mean systemic pressures maintained at 60 to 80 mm Hg. The mean bypass time was 100.9 minutes (standard deviation, 24.9) and cross-clamp time was 79.9 minutes (standard deviation, 20.7). Other surgical details such as mortality and the incidence of stroke can be viewed in Table 2.
Control subjects
Eighty people recruited through general advertisements agreed to complete the neuropsychological test battery on three consecutive occasions: at baseline, 1 week later (mean, 7 days; range, 5 to 15 days), and 90 days later (mean, 90 days; range, 81 to 103 days). All individuals underwent psychiatric and neurologic assessment at entry to the study, and a full medical history was taken to assess each person’s health status. The exclusion criteria included a history of respiratory, circulatory, or endocrine disease, personal or family history of psychiatric illness, head injury or substance abuse, mini mental status examination less than 27, and English as not the primary language (Table 1).
Procedure
After institutional ethics approval (March 2001) and informed consent, each participant completed a comprehensive neuropsychological assessment at three times: the CABG patients were assessed 1 day preoperatively and 6 days after surgery in the hospital and at 3 months postoperatively in the patients’ homes (to improve retention rates). The control group was assessed at the same times at a research institute. The cognitive test battery used, the resulting variables, and associated cognitive domains as recommended by Lezak [11] are shown in Table 3.
Each task was administered according to standard protocol, and the overall assessment battery required approximately 30 minutes to complete. Tasks were chosen based on their sensitivity to change, their ability to be presented in alternative forms (as appropriate), and as they met the consensus guidelines proposed by Murkin and associates [10].
All neuropsychological assessments were conducted by trained assessors and were conducted under the supervision of a neuropsychologist (P.M.). The neuropsychological tasks included in the current study were all pen and paper tests and were presented in the same order at each time. Attempts were made to keep the environment and times consistent when assessing patients, but this was extremely difficult to achieve in the hospital setting as admission was conducted in the afternoon, and discharge was typically in the morning. This necessitated that there be some variation in procedure. Similarly, attempts were made to have the same staff assess each patient, but given that a large proportion of the assessments required overnight travel, this was not always possible.
Data Analysis
The data were analyzed in three stages. First, to allow comparison with previous studies, performance on each of the neuropsychological tests at the 7-day and 90-day assessments was compared with the baseline within each group separately using a series of paired Student’s t tests. Second, cognitive domains were derived from the baseline data using theoretical precedence (Table 3).
Third, the neuropsychological data from the baseline, day 7, and day 90 in the CABG and control groups were subjected to a principal component analysis with Varimax rotation using SPSS (SPSS Inc, Chicago, IL). Principal component analysis is an exploratory, multivariate data analysis technique that is used to simplify complex data sets to more manageable numbers of components (commonly referred to as factors). This technique identified correlated data that best explained the results and grouped them as factors. Often it is necessary to rotate the data so that the factors are more easily interpretable, and this has been done using the Varimax technique as it is acknowledged to be the most suitable method for this task [15]. Data were examined for suitability of inclusion in the principal component analysis using the Kaiser-Meyer-Oklin and Bartlett’s tests for sphericity. Analysis progressed if these tests indicated that the principal component analysis was suitable. Factors were extracted if eigenvalues were greater than one. This method of factor extraction is commonly applied and indicates, in an easily replicable manner, the variables that explain the greatest proportion of the variance. Loadings on factors less than 0.3 were deleted from the tables so that the factors were more readily identifiable.
Missing Data
To minimize the possible impact that variations in the composition of the sample would have on the domain structure, participants who had data missing at any time were excluded from the analysis. This reduced the number of participants available for analysis from 204 to 148. There were no missing data for the control group. Reasons for the missing data include physical ailment (ie, arthritis), impaired mobility or sensation as a result of the surgery (ie, nerve damage from radial graft site), and time constraints (ie, discharge procedures impacting on day 7 assessment in the CABG group).
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Results
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Average Group Data With Time
Table 4
shows the group performance of the control and CABG groups at each assessment. For the control group, the Student’s t tests indicated that significant improvement occurred during the 90 days for all tests except the WLTREG. For the CABG group, performance generally deteriorated across the sample at the day 6 assessment on all tasks and an improvement in performance was seen at 3 months postoperatively. Group Student’s t tests indicated significant deterioration in performance on all neuropsychological tasks at day 6, and improvement from baseline at 90 days for all tests with the exception of the COWAT.
Equivalence of Cognitive Domains Between Groups Assessed at Baseline
Table 2 shows the baseline neuropsychological tests organized into cognitive domains according to their theoretical basis [11]. Four domains were identified; manual dexterity (grooved pegboard dominant and nondominant condition), complex attention (trails A, trails B, and DSST), verbal fluency (COWAT), and memory (three variables yielded by the WLT). For the CABG group, principal component analysis of the same baseline neuropsychological data organized the test results into three cognitive domains (ie, gave three factors) that were qualitatively similar to those defined using the theoretical method (Table 5). For example, this analysis yielded factors consistent with a memory domain (variables from the WLT) and a motor domain (grooved pegboard dominant and nondominant conditions). The third factor was consistent with the complex attention (trails A, trails B, and DSST) and verbal fluency (COWAT) domains. Together the three factors explained 69% of the variance in the results with the first contributing most strongly to the model.
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Table 5. Results of Factor Analysis and Loadings of Variables (> 0.3) on Factors for Coronary Artery Bypass Graft Patients
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The same analysis conducted in the control group yielded a different set of factors shown in Table 6. One factor consisted of tests defined theoretically as from the motor (grooved pegboard dominant and nondominant conditions), verbal fluency (COWAT), and memory (delayed recognition) domains. A second factor consisted of tests defined theoretically as measuring complex attention (DSST, trails A, and trails B), and a third factor consisted of tests defined theoretically as measuring the memory domain (immediate and delayed recall). Together these three factors explained 60% of the variance in the baseline data with the manual dexterity–verbal fluency–delayed recognition the strongest factor. Thus, the composition of the factors derived from the principal component analysis of the control group baseline data was qualitatively different from that derived theoretically and that derived from principal component analysis of the CABG group baseline neuropsychological data.
Stability of the Domains With Time
For the CABG group, principal components analysis of the day 7 and day 90 assessments indicated that the structure of cognitive domains at day 90 was the same as that observed at baseline. However, for day 7, the neuropsychological data were organized into only two cognitive domains. The domains on which these were based consisted of tests defined theoretically as measuring the domains of complex attention (DSST, trails A, and trails B) and manual dexterity (grooved pegboard dominant and nondominant conditions) for the initial factor. The second factor consisted of the tests defined theoretically as measuring memory (the three variables of the WLT) and verbal fluency (COWAT). At each assessment, however, the factor models explained similar proportions of the variance.
For the control group, principal component analysis of data from the day 7 and day 90 assessments indicated that the structure of cognitive domains at these two assessments was different from that observed for the baseline. For the day 7 assessment the analysis identified three cognitive domains that were based on factors that consisted of tests defined theoretically as measuring the domains of memory (delayed recall), complex attention (trails B), and motor function (grooved pegboard dominant and nondominant conditions); the domains of memory (immediate recall and delayed recognition) and complex attention (trails A); and the domains of complex attention (DSST) and verbal fluency (COWAT). At the 3-month assessment the three cognitive domains identified were different again with factors consisting of tests defined theoretically as measuring the memory (immediate and delayed recall) and complex attention domains (DSST, trails A, and trails B); the domains of motor function (grooved pegboard dominant and nondominant conditions) and verbal fluency (COWAT) domains; and the memory domain (delayed recognition).
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Comment
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The results of the study strongly suggest that cognitive domains derived from repeated neuropsychological test performance in studies of CABG are unsuitable for the classification of POCD. Cognitive domains identified from the statistical analysis of baseline neuropsychological data did not completely match those identified on the basis of neuropsychological theory. Furthermore, the domains identified statistically in the CABG patients were not the same as those identified when the same statistical analysis was applied to data from the same tests performed by healthy control subjects. These findings suggest that the error accompanying cognitive domains reduces their efficacy in the detection of POCD.
To identify POCD reliably, it is necessary to measure and compare the same aspect of cognitive function preoperatively and postoperatively. The current results suggest that the cognitive domain scores, derived from analysis of the preoperative neuropsychological data applying the methods used by Newman and colleagues [13], are not consistent with time and therefore should not form the basis for the preoperative and postoperative comparisons used to classify POCD. For this comparison to be reliably made, the contribution of the individual neuropsychological tests to a cognitive domain needs to remain constant.
In both the CABG and older healthy subject groups, the cognitive domains derived statistically from the neuropsychological data on the three assessments differed. The instability was greater for control subjects than for the patients as indicated by the inconsistent contributions of the individual neuropsychological tests to specific domains at each time. This is best illustrated with an examination of the memory tasks. Whereas the memory tasks reliably contributed to the same domains in the CABG group at each assessment, they were less consistent in the control group and actually contributed to separate domains at each time. For the CABG group, the cognitive domains identified at the preoperative and 3-month neuropsychological assessment were the same; however, the structure of the day 7 assessment differed. For the expression of change to be accurate the cognitive domains must be identical at each assessment as the chance of committing error increases as the domains become more dissimilar. We believe that this error will make the accurate detection of true change, on which POCD depends, more difficult.
The current data also demonstrated disagreement between theoretical and statistical methods for ascribing performance on the different neuropsychological tests to specific cognitive domains. For example, in the CABG group, classification of baseline neuropsychological test performance using the theoretical procedure identified four cognitive domains: memory, complex attention, verbal fluency, and manual dexterity. Statistical classification of the same data yielded only three factors, although these had some qualitative similarity to the theoretically based classification. Whereas both classifications identified memory and manual dexterity domains, the statistical analysis classified the tests of complex attention and verbal fluency as reflecting the same underlying cognitive domain rather than the two independent domains derived theoretically. For the control group, statistical analysis of baseline performance data identified three cognitive domains although these were completely different from the four cognitive domains derived theoretically [11] and from the three cognitive domains identified in the statistical analysis of the CABG group baseline data. Taken together these data suggest that the statistical identification of cognitive domains is sample specific, and that the consistency implied in the theoretical derivation of factors is not supported.
In grouping the tasks under cognitive domains, two assumptions are operating. First is the assumption that the tests under that domain will contribute solely and consistently to that domain. The second assumption is that this will provide some descriptive value in the detection of POCD. The current results suggest that both assumptions are violated when neuropsychological test data are reduced to cognitive domain scores, defined either theoretically or statistically. The ability to complete neuropsychological tasks does not depend on a single cognitive ability. In fact, all neuropsychological tests require many cognitive systems to work in synchrony to support their successful performance [16]. As an illustration, the Trail Making Tests are broadly considered to be tasks of complex attention, but they also assess aspects of working memory, visual scanning, manual dexterity, speed of processing, and motivation in their successful completion [11] and may be best regarded as tasks of general cognition rather than of any cognitive domain [17]. Therefore, impairment in any of these cognitive processes will impact negatively on performance of the neuropsychological task. Given that individual neuropsychological tasks actually measure multiple cognitive processes, it is highly possible that the creation of cognitive domain scores based on theoretical or statistical models may unnecessarily add error to analyses and thereby complicate conclusions. This is particularly the case in studies with prospective designs in which the stability and reliability of these cognitive domain scores are paramount. A number of influential studies have based their estimates of the incidence of POCD on the comparison of cognitive domains with time. In the studies of Selnes and colleagues [14, 18] and McKhann and associates [19], the cognitive domains used were derived theoretically, whereas Newman and colleagues [13] derived their cognitive domains statistically from the baseline neuropsychological performance (using the same method as that used here). However, none of these studies demonstrated the stability of the cognitive domains with repeated assessments and have progressed in the assumption that the cognitive domains were reliable. If the cognitive domains identified in these studies possessed properties similar to those detected in the current study then it would interfere with the identification of true POCD, and would negatively impact on any attempts to describe the underlying cognitive impairment.
The use of cognitive domains is appealing as it will theoretically reduce the chances of falsely identifying POCD. As the number of tests increases, there is an increasingly likely chance of falsely classifying an individual as having POCD [20, 21]. This can impact greatly on the incidence of POCD given that neuropsychological assessment batteries used to assess patients’ cognitive function have ranged from 1 [8] to 27 individual measures [22]. The concerns highlighted here regarding the temporal instability of cognitive domains and their variability among samples suggests that the use of cognitive domains may be adding more error to the process rather than reducing it. Postoperative cognitive dysfunction would be more accurately represented by analyzing tests individually with some effort used to minimize the chances of falsely detecting POCD when using multiple tests. Ingraham and Aiken [21] provided a theoretical demonstration of the error rates associated with neuropsychological assessment batteries composed of different numbers of tests, which allows the statistical rule for POCD to be adjusted so that the error rate of the rule is kept low relative to the number of tests that make up the assessment battery. Rasmussen and colleagues [23] used a similarly accessible method to address concerns about false classification by calibrating their definition of POCD against a healthy control group. This allowed for the adjustment of their rule of POCD so that the chances of falsely classifying a healthy person as demonstrating cognitive decline was less than 5%, an acceptable level of error.
Although cognitive domains may be more applicable in clinical neuropsychological practice, in which there is a more exhaustive assessment of cognitive function than is possible in POCD research [10], in the current context the use of cognitive domains appears to complicate the analysis of change by creating artificial summary scores that may not be reflective of the data, nor of any underlying cause. This can be easily overcome by using individual test scores as opposed to domain summary scores. To protect against the false classification of decline, the calibration of the statistical rule against a control group has proven effective in the past and is recommended.
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Acknowledgments
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Funding was provided by the National Health and Medical Research Council, Australia (Project Grant No. 140510).
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Abstract
Introduction
