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Cognitive Changes 5 Years After Coronary Artery Bypass Grafting
Is There Evidence of Late Decline?
Ola A. Selnes, PhD;
Richard M. Royall, PhD;
Maura A. Grega, MSN;
Louis M. Borowicz, Jr, MS;
Shirley Quaskey, BS;
Guy M. McKhann, MD
Arch Neurol. 2001;58:598-604.
ABSTRACT
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Objective To determine the long-term (preoperative to 5 years postoperative) and
late (1-5 years postoperative) changes in cognitive test performance in patients
after coronary artery bypass grafting.
Setting The departments of surgery and neurology at The Johns Hopkins University
School of Medicine, Baltimore, Md.
Patients A group of 102 patients who completed preoperative and follow-up cognitive
testing up to 5 years after coronary artery bypass grafting.
Main Outcome Measures A battery of neuropsychological tests, assessing 8 cognitive domains
(attention, language, verbal and visual memory, visuoconstruction, executive
function, and psychomotor and motor speed), was administered preoperatively
and at 1 month, 1 year, and 5 years postoperatively.
Results Significant changes in neuropsychological test scores from baseline
to 5 years were observed in only 3 of the 8 domains: there were declines in
visuoconstruction and psychomotor speed and an improvement in executive function.
When the period from baseline to 5 years was divided into 2 intervals, we
found that cognitive test scores generally improved from baseline to 1 year.
By contrast, between 1 and 5 years, there was significant decline in all cognitive
domains except for attention and executive function. Some potential explanatory
covariates (demographic, medical history, and surgery variables) were associated
with changes from baseline to 5 years in some cognitive domains, but few covariates
were statistically significant in more than 1 cognitive domain.
Conclusions The change in cognitive test performance between baseline and 5 years
is likely related to several factors, including low baseline performance and
practice effects. The significant decline in performance between 1 and 5 years,
however, raises the possibility that a late cognitive decline may be occurring
in this population. Additional studies, with the use of a nonsurgical control
group, are needed to determine if the observed cognitive decline is related
to bypass surgery itself, normal aging in a population with cardiovascular
risk factors, or some combination of these and other factors.
INTRODUCTION
COGNITIVE CHANGE during the first several weeks after coronary artery
bypass grafting (CABG) has been extensively investigated,1
but relatively few studies2, 3, 4
have examined longer-term outcomes. In one study5
in which patients were followed up for 2 years after surgery, the investigators
concluded that there was no evidence of late cognitive decline. In 2 studies6, 7 in which patients were followed up
for up to 5 years after surgery, however, a decline in cognitive performance
from 1 to 5 years was noted. Moreover, this delayed decline appeared to be
more frequent in some cognitive domains than in others.7
Individual case studies8 of late cognitive
decline have also been reported.
To explore this observation further, we obtained long-term follow-up
on a cohort of patients enrolled in a prospective study of cognitive outcomes
after CABG. Patients had been previously examined preoperatively, at 1 month,
and at 1 year.9 In this report, we describe
the longer-term cognitive outcomes in those patients from our original study
who were available for follow-up testing 5 years after CABG. As before, individual
neuropsychological test scores were combined to represent the major cognitive
domains (attention, language, verbal and visual memory, visuoconstruction,
executive function, and motor and psychomotor speed).9
The use of cognitive domains allowed us to relate changes in cognitive performance
to possible underlying brain mechanisms.
We examined changes in mean cognitive test scores both in the period
from baseline (before surgery) to 1 year after surgery and between 1 and 5
years after surgery, and compared them with the changes from baseline to 5
years after surgery. We also examined various patient characteristics (demographic,
medical history, and surgical variables) as covariates that might help to
explain how changes in individual patients' scores vary within this group.
PATIENTS AND METHODS
PATIENTS
Patients who underwent CABG between February 20, 1992, and April 1,
1993 (N = 172), were contacted 4 to 5 years after surgery. These patients
had been prospectively evaluated with neuropsychological tests before and
up to 1 year after surgery, as described elsewhere.9
Patients who agreed to further cognitive testing completed informed consent
forms and were interviewed in the clinic or in their homes.
NEUROPSYCHOLOGICAL TESTS
The cognitive test battery included the same tests that had been used
in the earlier assessments, and in most instances, each patient was tested
by the same interviewer (M.A.G. or L.M.B.) as previously.9, 10
Details of the neuropsychological test battery and the rationale for use of
composite cognitive domain scores were described previously. The following
cognitive domains and tests were included: (1) verbal memory: Rey Auditory
Verbal Learning Test; (2) visual memory: Rey Complex Figure (delayed recall)
and Symbol Digit (paired recall); (3) language: Boston Naming Test; (4) attention:
Digit Span (forward and backward); (5) visuoconstruction: Rey Complex Figure
(copy); (6) psychomotor speed: Symbol Digit and written alphabet; (7) motor
speed: Grooved Pegboard (dominant and nondominant hand); and (8) executive
function: Stroop Test. Patients were also administered the Mini-Mental State
Examination (MMSE).11 Additional information
on the psychometric characteristics of these measures has been published elsewhere.12
The Center for Epidemiological Studies Depression Scale, a 20-item self-report
questionnaire, was administered as a screening instrument for depression.13
GENETIC TESTING
For patients who completed their 5-year follow-up, a blood sample was
collected for apolipoprotein E (ApoE) genotype analysis. To identify ApoE
alleles, genomic DNA was amplified using polymerase chain reaction, as described
previously.14 Apolipoprotein E status was examined
because of a previous report15 of greater likelihood
of cognitive decline after CABG in patients with the ApoE epsilon 4 allele.
STATISTICAL METHODS
All analyses were performed using z scores
based on the mean and SD of the preoperative cognitive scores of patients
(n = 127) who completed the 1-month and 1-year follow-up evaluation.16 For cognitive domains with more than 1 test, each
patient received a composite score consisting of his or her z scores on the individual tests. The statistical significance of changes
from baseline to 1 year, from 1 to 5 years, and from baseline to 5 years was
assessed by 1-sample t tests on the average of the
within-subject z score differences (later score minus
earlier score) for each cognitive domain.
REGRESSION ANALYSES
To examine how the changes in cognitive test z
scores over time might be related to patient-specific covariates, we used
linear regression analyses. The response variable was the difference in a
patient's test scores on 2 occasions. The covariates were of several types:
demographic (eg, age and sex), medical history, and operative and postoperative
variables, as described previously.10 Because
many potentially important covariates were measured, they were divided into
2 groups: (1) preoperative covariates (including the demographic and medical
history variables) and (2) variables associated with surgery and the postsurgical
period. Separate multiple regression analyses were performed for each of these
2 groups of covariates.
RESULTS
Of the original 172 patients seen before surgery, 102 completed cognitive
testing at 5 years. Demographic characteristics for these patients are shown
in Table 1. There were 22 deaths
(13%) since surgery. In addition, 48 patients (28%) either refused or were
unable to return for follow-up. For the 23 patients who were unable to continue
participation in the study, demographic and medical data were collected by
telephone. The patients who completed the 5-year follow-up testing were more
highly educated than those who did not (P = .002),
but did not differ significantly in other demographic characteristics. The
actual interval between baseline and the last follow-up visit varied somewhat,
with a range from 47 to 74 months (mean, 53.7 months; SD, 3.9 months). Group
mean neuropsychological test scores at baseline, 1 year, and 5 years are shown
in Table 2.
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Table 1. Preoperative Demographic Characteristics of the Patient Population
Tested at 5 Years
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Table 2. Scores by Cognitive Domain Before and After Coronary Artery
Bypass Grafting
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FROM BASELINE TO 1 YEAR
Between baseline (presurgery) and 1 year (postsurgery), cognitive test
scores generally improved (Table 3).
There were statistically significant gains in 5 of the 8 domains (verbal memory,
visual memory, executive function, motor speed, and psychomotor speed), with
nonsignificant gains in language and attention and virtually no change in
visuoconstruction.
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Table 3. Mean Changes in z Scores for 8 Cognitive
Domains*
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FROM 1 TO 5 YEARS
By contrast, between 1 and 5 years, test scores showed significant decline,
on average, in 6 of the 8 domains (verbal memory, visuoconstruction, visual
memory, language, motor speed, and psychomotor speed). In the remaining 2
domains (attention and executive function), changes were slight and nonsignificant.
FROM BASELINE TO 5 YEARS
When the 2 intervals, baseline to 1 year and 1 to 5 years, are combined,
the changes in scores on cognitive tests (5 years minus baseline) showed mixed
results, with statistically significant changes in group mean scores appearing
in only 3 of the 8 domains. There were declines in visuoconstruction and psychomotor
speed and a gain in executive function.
REGRESSION ANALYSES
None of the covariates was found to be statistically significant across
many cognitive domains. This, together with the fact that many covariates
were examined (n = 49), suggests that the instances of statistical significance
should be interpreted cautiously. For this reason, we included in the summary
of these results only the cases in which covariates had regression coefficients
with P values of .001 or less (Table 4). Conversely, because there may not have been adequate power
to detect an effect even if one existed in this population, caution should
be used in concluding that there is no relation between the covariates and
the outcome measures.
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Table 4. Summary of Multivariate Analysis*
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With this criterion (P .001), the only demographic
variable that was associated with change in cognitive test performance was
race, and the association appeared in only 1 cognitive domain. (Race had a
significant positive coefficient in the regression for 5 years minus baseline
differences in visuoconstruction, indicating a smaller average decline for
nonwhites than for whites in our sample.) Among medical history variables,
only 1 was associated with cognitive change. (Previous history of stroke was
associated with decline in language scores, from baseline to 5 years and from
1 to 5 years.) Of the operative and postoperative variables included in this
analysis, the lowest esophageal temperature was associated with worse performance
in verbal memory, postoperative neurological event with worse performance
in visual memory, and longer time to awaken after surgery with worse performance
on tests of language.
Including the baseline neuropsychological test scores as a covariate
did not change the basic pattern of results shown in Table 3. Patients with lower baseline scores tended to improve more
between baseline and 1 year than those with higher baseline scores, consistent
with possible regression toward the mean. However, this pattern was not observed
between 1 and 5 years. For the domains of visuoconstruction, motor speed,
and psychomotor speed, patients with lower scores at baseline tended to decline
more between 1 and 5 years.
INTERIM MEDICAL EVENTS
The interim medical events since surgery included stroke (8%), myocardial
infarction (4%), percutaneous transluminal coronary angioplasty (14%), redo
CABG (3%), surgery with the use of general anesthesia (24%), and head trauma
with loss of consciousness for longer than one-half hour (3%). None of these
interim events was statistically associated with cognitive decline at 5 years
in any of the cognitive domains. Depressed mood, as measured by the Center
for Epidemiological Studies Depression Scale scores at 5 years, was not associated
with change in cognitive test scores from baseline to 5 years or from 1 to
5 years.
DEMENTIA
Change in neuropsychological test performance between baseline and up
to 5 years or between 1 and 5 years was not associated with specific ApoE
subtypes. Only 2 patients had an MMSE score in a range consistent with possible
dementia (score, <24) at 5 years, but 1 of these patients also had an abnormal
MMSE score at baseline. None of the patients had a family history or clinical
diagnosis of dementia.
COMMENT
The results of our prospective long-term follow-up study show that cognitive
test performance between baseline (preoperatively) and 5 years (postoperatively)
has a 2-stage course. Except for visuoconstruction, performance from baseline
to 1 year tended to improve for most cognitive domains. By contrast, from
1 to 5 years, performance declined for most cognitive domains. Thus, when
comparing preoperative performance and 5-year follow-up, there was no significant
change for most cognitive domains. The only domains for which performance
at 5 years was significantly worse than that at baseline were visuoconstruction
and psychomotor speed.
Although there were some medical and surgical factors that showed a
statistically significant association with change in cognitive test performance,
there was little consistency in these factors across cognitive domains or
across follow-up intervals. For example, lowest esophageal temperature during
surgery was strongly associated with worse performance in verbal memory at
5 years, but not in any other cognitive domains. Therefore, these associations
were not particularly helpful in determining who is at risk for cognitive
decline after CABG or for discerning possible underlying pathophysiological
mechanisms of late cognitive decline. Previous studies3, 10, 17
have also found it difficult to identify consistent demographic, surgical,
or medical predictors of cognitive decline after CABG.
BASELINE PERFORMANCE AND PRACTICE EFFECTS
We believe that in interpreting these data it is important to distinguish
between cognitive ability (or cognitive function) and neuropsychological test
performance. For a given level of ability, a subject's test performance can
be influenced by several factors. For example, repeated testing can produce
an improvement in test scores due to practice effects.16, 18, 19
The magnitude of the improvement due to practice depends on several factors,
including interval between testing, type of test, age, and educational level.20 Another possibility is that preoperative test performance
may have been adversely affected by stress, anxiety, depression, or other
factors associated with impending surgery, so that an improvement in scores
may simply have been the result of changes in testing conditions.
Alternatively, it has been suggested that in candidates for CABG, cognitive
function at baseline might be impaired because of long-standing cardiac disease,21, 22 so that postoperative improvement
in test scores might reflect a true improvement in cognitive function, perhaps
as a consequence of improved cardiovascular functioning.22
Patients with lower baseline scores tended to improve more between baseline
and 1 year, but we cannot determine if this improvement reflects true improvement
in cognitive function, as opposed to practice effects, regression toward the
mean, or the absence of preoperative conditions that may have adversely affected
test performance.
AGING EFFECTS
The cause of the decline in cognitive performance from 1 to 5 years
is also likely to be multifactorial. Cognitive changes do occur with normal
aging, and we, therefore, considered whether the observed decline from 1 to
5 years could be attributed to normal aging. In the absence of a suitable
control group for our patients, we relied on previously published estimates
of longitudinal changes in performance on specific cognitive tests. Whereas
previous reports based on cross-sectional cohort studies reported substantial
declines in cognitive performance in the later decades of life, more recent
prospective longitudinal studies have provided a more optimistic picture.23 Most studies24, 25
have concluded that although there may be mild decline in some cognitive domains
with advancing age, the magnitude of this decline is small and generally counterbalanced
by practice effects inherent in longitudinal testing. Cognitive domains reported
to show decline have included verbal fluency26
and psychomotor speed.27 Thus, longitudinal
follow-up testing for intervals from 1 to 5 years have demonstrated little
or no cognitive decline in persons without clinical evidence of dementia.
Our population of patients who underwent CABG, with a history of cardiovascular
disease and risk factors for cerebrovascular disease, may not be comparable
to "normal" controls. We are not aware of any published studies, however,
that have specifically examined the effects of aging on cognitive performance
in a population with cardiovascular disease. Several studies,21, 28, 29
on the other hand, have reported an increased risk of dementia in patients
with myocardial infarction, hypertension, and other cardiovascular risk factors.
Therefore, we cannot rule out the possibility that the late cognitive decline
observed in our population may simply be due to a combination of long-standing
cardiovascular disease and aging. Our finding that the patients with lower
baseline scores in visuoconstruction and motor and psychomotor speed showed
the greatest decline between 1 and 5 years may be consistent with this. Psychomotor
slowing and visuospatial abnormalities have been reported with subcortical
small-vessel ischemic disease,30, 31
although the specificity of the neuropsychological profile of subcortical
vascular dementia remains somewhat controversial.32
DEMENTIA
Our study population included many older subjects (>70 years), and it
is thus possible that early Alzheimer disease or other forms of dementia may
account for some of the observed cognitive decline. None of the patients in
our sample had been diagnosed as having dementia at the 5-year follow-up.
Only 3 patients had an MMSE score in the range consistent with possible dementia
at 5 years, and only 1 of these patients had an annual decline in MMSE score
greater than the 3 points reported as average for patients with dementia.33
Furthermore, Alzheimer disease is characterized by early changes in
specific cognitive domains, including memory, delayed recall, and language.34 The cognitive domains showing the greatest decline
relative to baseline in our study were psychomotor speed and visuoconstruction,
which are not among the cognitive domains showing the earliest change in Alzheimer
disease in most patients.
A previous report15 has suggested an
increased risk of cognitive decline after CABG in patients with the ApoE epsilon
4 allele. The presence or absence of the ApoE epsilon 4 allele was one of
the preoperative variables included in our regression analyses, but we found
no evidence that this variable was associated with decline in cognitive performance
in our population.
RELATION TO CABG
In the absence of an appropriate control group, which would allow us
to adjust for the effect of nonsurgical variables on longitudinal changes
in cognitive performance, a specific causal relation between CABG and late
cognitive decline cannot be established. There is nevertheless some indirect
evidence of a possible link between late cognitive decline and CABG.
First, when performance at 5 years was compared with performance at
baseline, one of the cognitive domains with significant decline was visuoconstruction.
There is some indication that the changes observed in visuoconstruction after
CABG may not be coincidental. In a previous study7
that included measures to assess visuoconstructional abilities in which patients
were followed up for more than 1 year, a similar decline in visuoconstructional
performance was reported. Other recent long-term follow-up studies35, 36 that did not find evidence of late
decline had not included measures of visuoconstructional abilities.
Second, a common neuroanatomical correlate of visuoconstructional deficits
includes the posterior parietal regions of the cerebral hemispheres.37 This is also an area of the brain that is believed
to be particularly vulnerable during or after cardiac surgery. For example,
Barbut and colleagues38 reported that 53% of
patients who had strokes after cardiac surgery had posterior watershed area
infarcts. Furthermore, blood flow studies39
have also documented parietal lobe hypoperfusion after CABG, and autopsy studies40, 41 of patients with neurological complications
after cardiac surgery have reported a high incidence of posterior watershed
area infarcts.
The mechanism by which cardiopulmonary bypass surgery might cause brain
injury is generally believed to be related to hypoperfusion, microemboli,
or both,42 but there is no obvious link between
any of these mechanisms and a progressive or delayed decline in specific cognitive
domains. There is, however, accumulating evidence that certain cerebrovascular
events, such as incomplete infarction, may result in delayed neuronal necrosis.43, 44 Progressive dementia after stroke
has also been reported.45 Some investigators46, 47 have suggested that hypoperfusion
followed by reperfusion during cardiopulmonary bypass surgery in some patients
may initiate a cascade of events that eventually lead to the development of
amyloid plaques and subsequent neuronal injury.
Interpretation of the findings from our study are limited by several
factors, including the unavailability for follow-up of some patients during
the 5-year study period. The educational level of subjects who did not complete
follow-up testing was lower than that of subjects who completed the follow-up.
Therefore, the results of our study may have been biased by selective attrition
of subjects with the lowest cognitive performance at baseline. Our results
are also limited by the lack of appropriate controls. Further longitudinal
studies with appropriate nonsurgical controls are needed to determine whether
the observed late changes in cognitive test scores are the result of normal
aging in a population with cardiovascular risk factors, of the cardiopulmonary
bypass operation itself, or of some combination of these and other factors.
We have in progress a 3-arm prospective study that may help resolve these
questions. In addition to a group undergoing standard CABG, the study also
includes a nonsurgical control group of patients with cardiovascular risk
factors to control for the effects of normal aging and a group of patients
undergoing off-pump bypass surgery that will control for the possible effects
of anesthesia.
AUTHOR INFORMATION
Accepted for publication September 7, 2000.
This study was supported by grant 35610 from the National Institute
of Neurological Disorders and Stroke, National Institutes of Health, Bethesda,
Md; and by the Charles A. Dana Foundation, New York, NY.
We thank Pamela Talalay, PhD, and Marilyn Albert, PhD, for their help
during the preparation of the manuscript.
From the Departments of Neurology (Drs Selnes and McKhann, Mr Borowicz,
and Ms Quaskey) and Surgery (Ms Grega), The Johns Hopkins University School
of Medicine, Department of Biostatistics, The Johns Hopkins University, School
of Public Health (Dr Royall), and the Zanvyl Krieger Mind/Brain Institute
(Dr McKhann), Baltimore, Md.
Corresponding author and reprints: Ola A. Selnes, PhD, Division of
Cognitive Neurology, Department of Neurology, Meyer 222, The Johns Hopkins
Hospital, 600 N Wolfe St, Baltimore, MD 21287 (e-mail: Oselnes{at}jhmi.edu).
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