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Right arrow Coronary disease

Ann Thorac Surg 2006;82:597-607
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Stable Cognition After Coronary Artery Bypass Grafting: Comparisons With Percutaneous Intervention and Normal Controls

Todd K. Rosengart, MDa,b,*, Jerry J. Sweet, PhDa,b, Eileen Finnin, RNa, Penny Wolfe, PhDa, John Cashy, PhDa, Elizabeth Hahn, MAa,b, Jesse Marymont, MDa,b, Timothy Sanborn, MDa,b

a Evanston Northwestern Healthcare, Evanston, Chicago, Illinois
b Feinberg School of Medicine, Northwestern University, Chicago, Illinois

Accepted for publication March 13, 2006.

Abbreviations and Acronyms BAI = Beck Anxiety Inventory; BDI = Beck Depression Inventory; CABG = coronary artery bypass grafting; COWA = controlled oral word association; HVLT-R = Hopkins Verbal Learning Test -Revised; MAE = multilingual aphasia examination; OPCAB = off pump coronary artery bypass; OPIE = Oklahoma premorbid intelligence estimate; PCI = percutaneous coronary intervention; RCI = reliable change index; WAIS-III = Wechsler Adult Intelligence Scale–third edition

* Address correspondence to Dr Rosengart, T19-080 Health Sciences Center, Stony Brook, NY 11794-8191 (Email: todd.rosengart{at}stonybrook.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Cognitive decline has been associated with coronary artery bypass grafting (CABG), but the extent to which these findings are related to the natural history of cognitive deficits in elderly patients with cardiac disease or have been influenced by the research methods used to determine abnormalities warrants further study.

METHODS: After excluding individuals with conditions known to cause brain dysfunction, individuals referred for percutaneous coronary intervention (n = 42) or CABG (n = 35) were compared with an age-matched and education-matched control group without clinical evidence of coronary artery disease (n = 44). These subjects underwent a battery of 14 neurocognitive tests at baseline (preoperatively) and at 3 weeks and 4 months postoperatively.

RESULTS: The majority of test scores for all three cohorts were within nonimpaired ranges at baseline and 3 weeks later. Change in impairment status from baseline to 3-week assessment was not associated statistically with type of treatment as referenced to clinical norms, and was associated with type of treatment on only one measure as referenced to control group performances. A further overall improvement in impairment status from 3 weeks' to 4 months' follow-up was seen in both CABG and percutaneous coronary intervention patients. Mean test scores were significantly worse in CABG patients versus percutaneous coronary intervention patients in 4 of 13 measures at 3 weeks' follow-up, but significant de novo impairment at 3 weeks' follow-up in the CABG group compared with the percutaneous coronary intervention and control groups was present in only one test. As assessed by reliable change methodology, impairment was statistically associated with type of treatment for only 1 of 13 measures.

CONCLUSIONS: As compared with changes seen in repeat testing of healthy control subjects and individuals who underwent percutaneous coronary intervention, clinically meaningful cognitive deterioration was not observed after CABG.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Cognitive deficits have been reported in more than 50% of individuals immediately after coronary artery bypass grafting (CABG), and to persist in more than 40% of these individuals up to 5 years later [1]. Aside from its effect on quality of life, neurocognitive decline has been associated with up to a 10% increase in hospital mortality, increased lengths of stay, and prolonged, expensive rehabilitation [2].

Neurocognitive decline after CABG has most frequently been attributed to use of the heart-lung machine and manipulations of the aorta associated with the performance of cardiopulmonary bypass [3–5]. As a consequence, the performance of either off-pump CABG procedures or percutaneous coronary interventions (PCI) have been advocated as alternatives to on-pump CABG [6].

Many post-CABG neurocognitive studies have consisted of longitudinal evaluations of surgical cohorts without non-CABG controls, and without description of important intraoperative variables associated with cognitive outcomes, such as the extent of aortic atherosclerosis or the maintenance of adequate perfusion pressure during bypass [3–7]. These reports consequently could not address the occurrence of neurocognitive decline as a function of advanced age, or in accordance with the natural history of systemic (cerebrovascular) atherosclerosis, or as a result of patient or procedure-specific risk factors for cognitive decline. Further, because of the lack of age-matched and education-matched normal control subjects in these studies, it has been difficult to determine the progression of serial testing in this aged population that likely has impaired cognitive reserve. [1, 8] Finally, state-of-the-art statistical procedures used to evaluate reliable change with repeat testing in a healthy control group have generally been absent in prior research.

We consequently compared a cohort of individuals undergoing elective CABG at our institution with a matched sample of individuals undergoing PCI, and another matched cohort with no known history of coronary or neurologic disease. Analysis of the baseline data in this study demonstrated that individuals with coronary artery disease scheduled for CABG or PCI demonstrated cognitive impairment in some tests even before intervention compared with a healthy control group and as compared with normative test standards [9]. The present 3-week and 4-month postprocedure data, part of a 1-year longitudinal follow-up study, suggest that cognitive deterioration after CABG is negligible, especially when taking into account preoperative impairments, intraoperative variables, and the expected diminishment of cognitive function in an aged patient population with atherosclerotic vascular disease [1, 8].


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Enrollment
Institutional review board approval was obtained in February 2002, and fully informed written consent was obtained from individuals selected for participation in this study. Prospective participants in the two cardiac groups (CABG or PCI) were screened by project personnel subsequent to physician referral based on standard clinical indications for either CABG or PCI. Exclusion criteria for cardiac patients included those reflecting excessive risk of neurologic events, or potential inability to successfully complete neurocognitive assessments before PCI or isolated, primary CABG procedure (Table 1) [9, 10]. A cohort of control subjects free of cardiac and neurologic disease by history and similar to the cardiac patients in regard to age and education were recruited from the community.


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  		Table 1. Reasons for Exclusions Among Potential Study Participants
 
Neurocognitive Testing Battery
All consenting CABG, PCI, and control patients meeting inclusion criteria underwent neurocognitive testing and completed a set of self-report questionnaires, including the Beck Depression Inventory and Beck Anxiety Inventory. Each study subject was tested on all occasions by the same experienced psychometrician in a comfortable, well-lit environment generally free from visual and auditory distractions for approximately 1 hour. Median intervals from baseline testing to cardiac intervention were 1 day for each group, and were 21, 22, and 29 days to initial follow-up testing for the control, PCI, and CABG groups, respectively (p = 0.31).

The test battery included only examinations with age-specific normative standards that would remain valid on retesting, in the following domains: Attention: Digit Span from the Wechsler Adult Intelligence Scale–Third Edition; Fine motor dexterity: Grooved Pegboard (dominant and nondominant hands); Processing Speed: Digit Symbol from the Wechsler Adult Intelligence Scale–Third Edition, Trail-Making A, Stroop Color-Word Test (word and color pages); Language: Controlled Oral Word Association and Visual Naming of the Multilingual Aphasia Examination; Executive function: Stroop Color-Word Test (color-word page), Trail-Making B; Verbal learning and memory: Hopkins Verbal Learning Test—Revised (alternate form at second testing).

Operative Technique
Coronary artery bypass grafting was performed using standard cardiopulmonary bypass technique with moderate hypothermia (32°C.). Fentanyl and inhalation agents were administered to allow early extubation (mean, 4 hours postoperatively). Arterial cannulation was performed using a 22F right-angle or soft-flow cannula in an area seen to be devoid of plaque as determined by the epiaortic analysis. Mean arterial perfusion pressure on cardiopulmonary bypass was maintained at a pressure greater than 60 mm Hg, and hematocrit was maintained at a level greater than 18%.

Statistical Analysis
Analysis of variance was used to compare mean intelligence quotient, Beck Depression Inventory-II, and Beck Anxiety Inventory scores. Spearman correlations were computed to examine the relationship between intelligence quotient, Beck Depression Inventory-II, and Beck Anxiety Inventory scores and the 14 neurocognitive instruments.

Individual test scores were categorized as impaired in two ways: (1) a score greater than 1 standard deviation below published normative references; and (2) a score greater than 1 standard deviation below the mean of the control group at the given assessment time. The change in proportion of individuals impaired among the three groups at 3 weeks' and 4 months' follow-up were compared using generalized estimating equations for repeated measures.

Mean scores on the neurocognitive instruments at baseline were compared using analysis of variance, which, when appropriate, was followed by Scheffé's test for pairwise comparisons between groups. Scores at week 3 were compared using analysis of covariance, with the baseline score as a covariate, and least-squares means and standard errors were computed. Scores for Hopkins Verbal Learning Test—Revised Recognition Discrimination were eliminated from this analysis because of statistical variability in control group measurements.

A reliable change index [11] was computed by dividing each patient's change in scores from baseline to week 3 by the standard deviation of the change in control group scores. Individuals with a reliable change index less than –1.64 were categorized as worsened, those with a reliable change index greater than 1.64 were categorized as improved, and the remainder were categorized as unchanged, as per previous recommendations regarding application of this analytic approach [11]. Proportions of patients categorized in this manner were compared using Fisher's exact test.

As compared with final enrollment numbers, a sample size of 50 patients per group was initially planned to provide 80% power, at the 0.01 significance level, to detect a difference between 10% worsening in one group and 40% worsening in a second group.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Intergroup Conformity
The three cohorts were well matched for age, and each group was relatively well educated, with well over half of each group having a college degree or advanced degree (Table 2). There were more men than women in the CABG and PCI groups, with the control group being equally divided, reflective of the distribution of sex in these populations. Patterns of comorbidities in the CABG and PCI subjects were consistent with the degree of atherosclerotic disease in these groups and the relatively limited evidence of such disease in the control group (Table 3).


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  		Table 2. Demographics and Estimated Intellectual Function at Time of Enrollment
 

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  		Table 3. Comorbidities in Subject Populations at Baseline
 
Both the Oklahoma Premorbid Intelligence Estimate and the Barona intelligence estimate indicated above-average intellectual functioning (ie, intelligence quotient greater than 109) in the enrolled subjects (Table 2). No significant differences among the three groups were found in either Oklahoma Premorbid Intelligence Estimate or Barona intelligence quotient scores; therefore, subsequent analyses were not adjusted for baseline intelligence quotient.

The Beck Depression Inventory-II and Beck Anxiety Inventory group means were all within nondepressed, nonanxious ranges, and without differences among groups at either baseline or follow-up (data not shown). Individual Beck Depression Inventory-II and Beck Anxiety Inventory correlations with each of the 14 neurocognitive outcomes were all less than 0.25.

Coronary Artery Bypass Grafting and Neurocognitive Function
Coronary artery bypass grafting patients had relatively disease-free aortas, and were maintained during cardiopulmonary bypass at relatively high mean perfusion pressures and flow rates (Table 4). Hematocrit levels and temperatures on bypass were maintained within the levels specified for this protocol. Coronary artery bypass grafting cardiopulmonary bypass duration was generally less than 2 hours.


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  		Table 4. Intraoperative Data in Coronary Artery Bypass Grafting Group (n = 35)
 
The majority of test performances in the CABG and control groups were within the nonimpaired range at baseline and 3 weeks' follow-up, although select impairments were found at both times in many cases, especially in the CABG and PCI groups (Table 5). When cognitive function was defined as deteriorated by an increase of at least 5% in the number of impaired patients at 3 weeks postoperatively versus baseline as measured by clinical standards (subject test score greater than 1 standard deviation from test norm), control and PCI patients exhibited deteriorated performance in none of the test measures. By this standard, CABG patients demonstrated worsened performance in only three measures. Using the same definition of deterioration against the control group mean standard, deterioration was noted in CABG patients in eight tests, in PCI patients in four tests, and in control patients in one test. When deterioration was defined as an increase of at least 10% in the number of patients showing impaired performance at 3 weeks' postoperatively versus baseline, deterioration was noted in only one test in CABG patients, as measured by clinical standards, and in seven tests in CABG patients and four tests in PCI patients, as measured by control group means.


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  		Table 5. Percentages of Participants Considered Neuropsychologically Impaired at Each Testing
 
The percentage of impaired CABG and PCI patients generally decreased at 4 months' follow-up compared with 3 weeks' follow-up (Table 5). For example, although the number of CABG patients defined as impaired in reference to the control group mean increased by at least 5% in two tests at 4 months compared with 3 weeks, the number of impaired CABG patients decreased by at least 5% in 12 tests, and decreased by at least 10% in 8 tests. As compared with PCI patients at 4 months' follow-up, a lesser percentage of CABG were considered impaired in almost twice as many tests as those in which a greater percentage of CABG patients were considered impaired.

Group mean scores corrected for differences in baseline performances were also compared at the 3-week follow-up (Table 6, left columns). This analysis demonstrated that CABG patients performed significantly worse than PCI subjects in 4 of 13 measures at 3 weeks, but significant de novo impairment at follow-up in the CABG group compared with the PCI and control groups was present in only one test. Further, the absolute differences in group performances within the CABG patients were generally relatively small (Fig 1).


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  		Table 6. Test Mean Outcomes a and Reliable Change Index
 

Figure 1
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  		Fig 1. Coronary artery bypass grafting group performance at baseline (black bars) and at 3 weeks' follow-up (white bars), grouped according to scoring methodology specific to each testing methodology: (A) tests using t score (range, 1–100 [lower score indicates impairment]), (B) tests using percentile score (range, 1–99 [lower score indicates impairment]), and (C) tests using scaled score (range, 1–19 [lower score indicates impairment]). (COWA = Controlled Oral Word Association; HVLT-R = Hopkins Verbal Learning Test—Revised; MAE = Multilingual Aphasic Examination; WAIS III = Wechsler Adult Intelligence Scale–Third Edition.)

 
Finally, as a fourth analysis, reliable change methodology incorporating corrections for control group performances showed that CABG patients demonstrated significant deterioration of performance only on Multilingual Aphasia Examination Visual Naming at 3 weeks' follow-up (Fig 2, Table 6, right columns).


Figure 2
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  		Fig 2. Percent of patients in each group (control, white bars; percutaneous coronary intervention, striped bars; coronary artery bypass grafting, black bars) demonstrating worsening of test performance at 3 weeks' follow-up, as measured by reliable change index (please see methodology pertaining to Table 6). (COWA = Controlled Oral Word Association; HVLT-R = Hopkins Verbal Learning Test—Revised; MAE = Multilingual Aphasic Examination; WAIS III = Wechsler Adult Intelligence Scale–Third Edition.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
The present study demonstrates that the majority of neurocognitive functions measured as early as 3 weeks postoperatively are essentially unchanged compared with baseline in individuals undergoing CABG surgery. These findings are consistent with the recent review of Selnes and McKhann [7], who concluded that in current studies neurocognitive complications of CABG were mild.

Within the present study, results varied considerably depending on which of four analytic methods were used to determine impairment (ie, percentage of subjects one standard deviation beyond clinical norms, percentage of subjects one standard deviation below control group mean, comparison of group test mean outcomes, and reliable change index). This variability highlights our belief that no one analytic measure represents the gold standard for these analyses, consistent with prior discussions on this matter [1, 11, 12]. None of these measures, however, demonstrated consistently worsened performances in CABG patients compared with control subjects or PCI patients. Further, it is clear that most patients in our cardiac groups did not show great changes from baseline to follow-up. For example, mean performances for each group at baseline and 3 weeks' follow-up were generally within the range of scores considered to be normal.

The present study included tests that measured a number of distinct cognitive domains and carried age-specific normative standards, which would remain valid on retesting, as recommended by prior research [12]. Further, we examined group means and changes in individual participants' performances to ensure appropriate and comprehensive detection of potential cognitive declines. Although some similar trends were detected by both analyses, outcomes were far from identical when group means versus individual subject changes were assessed and when changes from normative standards in the CABG group were compared with changes on retesting of the PCI and healthy control groups.

Finally, we took advantage of our inclusion of control groups and used a reliable change method that essentially incorporates corrections for control group change retest effects. In this context, we believe that identifying the neurocognitive effects of CABG requires examination of the results of all four methods in concert. Taken together, consistent impairment or worsening of performance exclusive to the CABG group was demonstrated in none of the testing measures. Stated differently, the majority of measured neurocognitive outcomes did not show negative effects attributable to CABG.

A PCI group was included in the present study to allow comparisons of outcome measures that would reflect the effects of nonsurgical coronary artery disease, which can be a risk factor for cerebrovascular disease, and which in turn is well known to correlate with cognitive dysfunction [13–18]. An age-matched control group was included to correct for diminished cognitive function in the elderly and to demonstrate effects of retesting [14–17]. Although discrepancies in sex proportions exist among groups in the present study, we and others have demonstrated previously that sex did not affect neurocognitive testing [9, 18]. The relevance of such control subjects is noted in our findings of similarities between CABG and PCI group functioning, and is reflective of prior findings of comparable cognitive decline in CABG patients and non-CABG control subjects [19].

The manner in which cardiopulmonary bypass is performed is another critical variable in assessing post-CABG neurocognitive outcomes. For example, the aortic cannulas used in the present study were all designed to theoretically minimize the sandblasting effect potentially associated with the use of straight, small-bore tubes that can dislodge atheromatous debris in the posterior ascending aorta or arch [3, 4]. Further, we maintained moderate hypothermia, threshold flow rates, and normalized flow pressures—factors that have also been associated with favorable neurocognitive outcomes [20]. In comparison, data regarding these variables have often not been reported in prior studies. Further, it is notable that all of our CABG patients demonstrated no worse than grade I or II aortas. This fortuitous lack of aortic atherosclerotic disease may have favored neurocognitive outcomes [3].

In comparison to the present study, Newman and colleagues [1] noted dramatic cognitive decline after CABG in their prospective trial, but did not include intraoperative data or comparison groups. Although Ahlgren and associates [21] included a PCI comparison group and Van Dijk and coworkers [22] included an off-pump CABG group to correct, respectively, for the presence of CAD and the effects of cardiopulmonary bypass, cardiopulmonary bypass methodologies were not detailed in either study. Several other studies demonstrating post-CABG cognitive decline also failed to include coronary artery disease control subjects to correct for the potential effects of atherosclerosis on cognitive decline [23–25].

In contrast, Selnes and associates [26] reported no difference between CABG and nonsurgical coronary artery disease control subjects in their study, but reported the maintenance of high pressure (60 to 80 mm Hg) during cardiopulmonary bypass and made specific reference to aortic clamp technique. A recent comparison of off-pump and on-pump CABG patients by Rankin and coworkers [27] also failed to detect a relative cognitive decline in their CABG group.

The present study focuses on outcomes at a relatively early postoperative time compared with previous reports that examine intervals up to 5 years postoperatively. With the notable exception of the report of Newman and colleagues [1], these prior studies have all generally reported improvements in post-CABG neurocognitive functions as the time after surgery increases. Thus, the present finding of relatively intact cognitive function even at an early post-CABG time would suggest that cognition will only be better at subsequent follow-up intervals. Consistent with this premise, analysis of data at 4 months postoperatively demonstrates that the majority of test scores in the CABG group were markedly improved compared with the 3-week performances. To further assess this trend, longitudinal analysis for up to 1 year in follow-up is planned.

In regard to the adequacy of the sample size in the present report, which was limited owing to difficulties in patient accrual [9], it is noteworthy that the mean postsurgery scores are not only within the normal range, the mean differences in test scores before and after CABG were not clinically meaningful (Fig 1). These means would be unlikely to change with a larger group population. Similarly, the percentage of patients demonstrating worsening of status was also generally similar among groups as measured by the reliable change index (Fig 2).

It is important to note that a great number of patients with evidence of baseline impairment were excluded from the present study (even though many patients with more subtle changes were included). It is possible that prior studies were handicapped by patients with baseline impairments and diminution in cognitive reserve, and thus at risk of subsequent impairment, compared with a relatively more intact population in the present study [5].

In conclusion, and in the context of our prior reporting of baseline impairment despite the exclusion of a considerable number of patients, it must be considered that at least for patients without overwhelming risk of cognitive impairment, CABG does not induce clinically meaningful cognitive deterioration when compared with appropriate cohorts (aged, atherosclerotic), especially if appropriate hemodynamic safeguards are applied in performing cardiopulmonary bypass. The sometimes substantial discrepancies found in identifying neurocognitive impairment and change when different analytic methods were used in the present study highlight the methodological subtleties underlying these and prior contradictory findings.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was supported by a grant from the American Heart Association. We wish to thank Milicia Vukovic, Anne Galioto, Jenna Duffecy, Lina Nayak, and Jennifer Beaumont for their assistance on this project. We wish to thank Tim Votapka, Ron Curran, Mike Frank, Edgar Chedrawy, and Glenn Murphy for their clinical contributions.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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Todd K. Rosengart
Eileen Finnin
Jesse Marymont
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