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Original Articles: Adult Cardiac

Do Management Strategies for Coronary Artery Disease Influence 6-Year Cognitive Outcomes?

^a Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, Maryland
^b Department of Surgery, The Johns Hopkins University School of Medicine, Baltimore, Maryland
^c Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Maryland
^d Department of Biostatistics, The Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
^e Zanvyl Krieger Mind/Brain Institute, Baltimore, Maryland

Accepted for publication April 16, 2009.

^_* Address correspondence to Dr Selnes, 2206 Reed Hall, 1620 McElderry St, Baltimore, MD 21205 (Email: oselnes{at}jhmi.edu).

ADULT CARDIAC SURGERY: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 
Background: Previous uncontrolled studies have suggested that there is late cognitive decline after coronary artery bypass grafting that may be attributable to use of the cardiopulmonary bypass pump.

Methods: In this prospective, nonrandomized, longitudinal study, we compared cognitive outcomes after on-pump coronary artery bypass surgery (n = 152) with off-pump bypass surgery patients (n = 75); nonsurgical cardiac comparison subjects (n = 99); and 69 heart-healthy comparison (HHC) subjects. The primary outcome measure was change from baseline to 72 months in the following cognitive domains: verbal memory, visual memory, visuoconstruction, language, motor speed, psychomotor speed, attention, executive function, and a composite global score.

Results: There were no consistent differences in 72-month cognitive outcomes among the three groups with coronary artery disease (CAD). The CAD groups had lower baseline performance, and a greater degree of decline compared with HHC. The degree of change was small, with none of the groups having more than 0.5 SD decline. None of the groups was substantially worse at 72 months compared with baseline.

Conclusions: Compared with subjects with no vascular disease risk factors, the CAD patients had lower baseline cognitive performance and greater degrees of decline over 72 months, suggesting that in these patients, vascular disease may have an impact on cognitive performance. We found no significant differences in the long-term cognitive outcomes among patients with various CAD therapies, indicating that management strategy for CAD is not an important determinant of long-term cognitive outcomes.

Coronary artery bypass graft (CABG) surgery is effective for the treatment of angina, but the prospect of postoperative cognitive decline associated with the use of cardiopulmonary bypass has become a significant concern for many patients.

Short-term cognitive changes have been documented in some patients after CABG, but these changes are generally mild and reversible by 3 to 6 months after surgery [1]. It has been suggested, however, that these short-term changes set the stage for a "late decline" several years after surgery. One study found that compared with their preoperative baseline performance, 42% of patients had lower cognitive performance 5 years after surgery [2]. Although the etiology of these late cognitive changes was unclear in that report, since there was no control group, it was hypothesized that it might be related to the use of cardiopulmonary bypass.

Off-pump CABG surgery (OPCABG) was developed to avoid or reduce the presumptive adverse neurocognitive outcomes associated with the use of cardiopulmonary bypass. Although some early observational studies reported lower incidence of cognitive decline after OPCABG, more recent randomized controlled trials have not found significant differences between on- and off-pump surgeries in the degree of early or late cognitive outcomes [3–5]. These findings indicate that long-term cognitive changes may not be specific to a CABG population.

The interpretation of most studies of cognitive outcomes after CABG has been difficult because of the lack of comparison groups either with or without coronary artery disease. In the present study, we compared the 72-month longitudinal cognitive test performance of patients undergoing CABG with that of patients having off-pump surgery and two other groups: patients with diagnosed coronary artery disease but no surgery, and a group of heart-healthy subjects with no known risk factors for coronary artery or cerebrovascular disease. The principal goal of our study was to determine if CAD patients treated surgically had long-term cognitive decline and if there was evidence of disproportionate decline relative to patients treated with nonsurgical medical therapy.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 
Study Design
This prospective, nonrandomized study was approved by the Johns Hopkins Institutional Review Board (IRB) committee on July 14, 1997. We compared four groups: conventional on-pump CABG patients (CABG group); off-pump CABG patients (OPCABG group); medically treated patients with diagnosed coronary artery disease but no surgery (nonsurgical cardiac comparison [NSCC] group); and heart-healthy comparison patients (HHC group).

Inclusion criteria required that subjects be able to undergo neuropsychological testing, able to give written informed consent, able to sit upright, native English speaking, and not mechanically ventilated. Patients were not excluded for medical reasons. All participants underwent a standardized neuropsychological test battery, assessment of depressive symptoms, and medical history review at baseline (preoperatively for the surgical groups), and at 3, 12, 36, and 72 months. The 72-month data collection was completed in August 2008. The primary outcome measures for this study were within-subject cognitive change over time.

Patients
CABG group (n = 152)
Patients scheduled to undergo isolated on-pump CABG were enrolled from all eight surgeons between September 1997 and March 1999 at our institution. There were minimal differences in the surgical and anesthetic techniques, as would be expected within a single institution; these procedures have been described elsewhere [1].

OPCABG group (n = 75)
Patients scheduled to undergo OPCABG surgery, without the use of the cardiopulmonary bypass pump, were asked to participate. As a single institution could not provide enough cases to meet our sample size needs, off-pump patients were recruited from five different area hospitals. Off-pump patients were enrolled between March 1998 and October 2003. Separate IRB approval was obtained from all participating institutions. Because multiple sites were involved, anesthetic medications and surgical techniques differed, as described elsewhere [6]. This group was used to control for the effects of the cardiopulmonary bypass pump.

NSCC group (n = 99)
Four cardiologists at our institution referred patients who were under medical management for diagnosed stable coronary artery disease (by coronary angiography) for inclusion into the study. Those who had had a cardiac surgical procedure in the past were not eligible. Patients were enrolled from September 1997 through April 2003. This group was used to control for surgical and anesthetic effects.

HHC group (n = 69)
Community-dwelling subjects were recruited through IRB-approved newspaper advertisements from November 2001 to September 2003. We enrolled heart-healthy subjects with comparable age, sex, and education profiles to match our other study groups. To exclude subjects with risk factors for heart disease, this group was screened by telephone interview for the following medical history variables: diabetes mellitus, kidney disease, hypertension, coronary artery disease (including myocardial infarction, angina, and high cholesterol), stroke/transient ischemic attack, peripheral vascular disease, and medications used to treat the above conditions. This group was added to control for the effects of vascular disease on the brain.

Neuropsychological and Mood Assessment
All participants were administered a battery of standardized neuropsychological tests on the following longitudinal schedule: baseline (preoperatively for surgical patients), 3, 12, 36, and 72 months. The scores from these 16 tests and subtests were combined as an unweighted average into the following eight cognitive domain scores: verbal memory, visual memory, visuoconstruction, language, motor speed, psychomotor speed, attention, and executive function. In addition, all the neuropsychological measures were combined into a composite global measure of cognition. The Mini-Mental State Examination (MMSE) [7], the Center for Epidemiological Studies Depression scale (CES-D) [8], and the Beth Israel Functional Status Questionnaire (FSQ) [9] were also administered at each time point.

All subjects were tested by the same team of study investigators, irrespective of the site where they were enrolled and interviewed. Over the entire course of the study, six cognitive testers were involved in this study, all of whom were trained in a standardized manner. These testers then traveled to all the sites to examine patients as needed. The same tester attempted to see the same subjects for follow-up. Previous test results were not reviewed before subsequent testing.

Statistical Methods
The primary data analysis examined the degree of improvement or decline in cognitive domain scores at 72 months relative to an individual's baseline or 12-month performance (late decline). We analyzed z-scores adjusting for age (with 2 degrees of freedom), sex, and education (with 2 degrees of freedom), and standardized with respect to the heart-healthy control group's mean and standard deviation. For timed tests, the original scores were inverted so that improved performance resulted in a higher score, as was the case for nontimed scores.

To examine how the changes in neuropsychological test z-scores over time might be related to subject-specific covariates, we used a linear mixed effects model for the z-scores from each test, estimating a separate learning effect and time trend for each group. To calculate the change scores in the eight domains, we pooled the estimates from the separate tests in each domain and used bootstrapping to quantify the statistical uncertainty of these pooled values. This methodology has been reported elsewhere [10, 11].

Power was based on the standard errors of the group differences in average change from baseline (Table 4). This study has a greater than 95%, 95%, and 98% power to detect a difference between each of the CABG, off-pump, and nonsurgical controls in the global composite score as compared with the HHC group of 0.3 population SD true differences. A 0.3 SD difference between the groups over 6 years is equivalent to a difference in the trend in cognitive decline between the two groups of 0.5 SD per year after intervention.

	Results

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

View larger version (19K): [in this window] [in a new window]   Fig 1. Boxplots showing the median distribution of baseline z-scores for each cognitive domain by study group. (Verbmem = verbal memory; vismem = visual memory; visuo = visuoconstruction; lang = language; motor = motor speed; psych = psychomotor speed; atten = attention; exec = executive function; global = global composite scores.) *These coronary artery disease groups have a difference in their baseline means compared with heart healthy controls (HHC) that are statistically significant at alpha = 0.05. (CABG = coronary artery bypass graft surgery; OPCAB = off-pump coronary artery bypass surgery (3 patients did not complete baseline testing); NSCC = nonsurgical cardiac comparison group.)

View larger version (22K): [in this window] [in a new window]   Fig 2. Distribution of longitudinal composite global score pattern for each study group: coronary artery bypass graft surgery group (dotted line), heart-healthy comparison group (solid line), nonsurgical cardiac comparison group (long-dashed line), and off-pump coronary artery bypass group (short-dashed line).

Change From 12 Months to 72 Months
To evaluate the degree of late cognitive decline, we compared the adjusted 12-month z-scores with the scores at 72 months for each group. Relative to the changes observed in the HHC group, the CABG group had a greater degree of late decline in several cognitive domains, with statistically significant greater decline for the domains of verbal memory (p = 0.04), visuoconstruction (p < 0.01), language (p = 0.03), executive function (p < 0.01), and the global composite domain (p < 0.01). The pattern of late decline was similar in the nonsurgical group, who showed significantly greater decline than did the HHC group for the cognitive domains of visuoconstruction (p < 0.01), motor speed (p < 0.01), executive function (p = 0.03), and the composite global domain (p = 0.04). The off-pump group did not differ from the HHC group in the degree of late decline for any of the cognitive domains. Overall, the degree of change from 12 to 72 months was greater than that from baseline to 72 months (data not shown).

Changes in Mini-Mental State Examination Scores
We also examined changes in scores on the MMSE from baseline to follow-up points for all study groups. From baseline to 72 months, the average within-patient change on the MMSE ranged from a decline of 0.4 point for the OPCABG group to an improvement of 0.02 point for the HHC group. The number of patients with an MMSE score in the clinically impaired range (< 24) at 72 months was similar for the CABG and NSCC groups (7%) and somewhat lower (2%) for the OPCABG and HHC groups (Table 2).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 
The principal finding of this study was that although there is mild cognitive decline over time in all groups with CAD, we found no evidence of disproportionate long-term decline in patients who had conventional on-pump surgery when compared with patients with off-pump surgery or nonsurgical medical management. Comparison of changes in cognitive performance in these groups from baseline to 72 months or from 12 to 72 months showed greater decline in the groups with coronary artery disease than in the HHC comparison group, but no statistically significant differences in the degree of decline among the three groups with coronary artery disease. The lack of evidence for a clinically meaningful difference among CABG, off-pump, and nonsurgically treated patients suggests that choice of management strategies for coronary artery disease does not influence the long-term cognitive performance of these patients.

Compared with the HHC group, the three groups with coronary artery disease had lower performance even at baseline. This finding is consistent with results from several other studies that have reported lower than expected cognitive performance among candidates for CABG before surgery [12, 13]. Jensen and colleagues [3] found that 20% of their CABG candidates had an MMSE score in the impaired range (< 24) before surgery, and another recent study reported that 45% of their patients met operational criteria for cognitive impairment before surgery [14]. Studies that have examined the nature of the preoperative cognitive impairment have reported that the cognitive domains most commonly impaired include executive functioning, memory, and speed of processing [15]. These are also the cognitive domains that have been found to be impaired in patients with subcortical small vessel disease [16], suggesting that patients with coronary artery disease may also have cerebrovascular disease.

Subjects in all four groups improved from baseline to 3 months, as well as from 3 to 12 months. Other studies have also shown this trend [1, 2]. We attribute this improvement to a combination of postoperative recovery and practice effects associated with greater familiarity with the neuropsychological tests. Changes in cognitive performance from 3, 6, or 12 months to 5 years has been considered as "late" decline in previous studies [2, 4, 17]. In our study, we observed decline in performance from 12 to 72 months for all groups, including the HHC group for some cognitive domains. Compared with the HHC group, there were also statistically greater, but nonetheless modest, late changes in the CABG and NSCC groups. These findings suggest to us that there is mild late decline after CABG, but because a similar degree of decline was found in the NSCC group, they are not specific to CABG patients. Previous longitudinal studies of community-dwelling persons have also reported decline in performance on some cognitive tests with longer follow-up periods [18], and attributed this decline to a combination of reduced practice effects and age-related changes in performance. Thus, although there has been considerable interest in the phenomenon of "late" cognitive decline after medical interventions, we believe that comparison with the actual baseline performance provides a clinically more useful measure of long-term cognitive changes.

We did not find evidence of clinically relevant changes over 72 months in a commonly used screening measure of cognitive performance (the MMSE), and there were no significant differences among the coronary artery disease groups in the degree of change in MMSE over time. The changes observed in the MMSE scores in our study are comparable to those that have been reported for community-dwelling older persons [19]. Some previous studies have suggested that CABG may be associated with greater risk of developing Alzheimer's disease [20]. However, we found no difference between the CABG and NSCC in the frequency of patients with an MMSE score in the clinically impaired range at 72 months.

Our findings are consistent with those of previous studies that have compared cognitive outcomes after on- versus off-pump surgery. One large randomized controlled trial reported that both on- and off-pump patients had comparable incidence of decline at 5 years in the two groups. They concluded that factors other than the use of cardiopulmonary bypass were responsible for the long-term cognitive decline [4]. They hypothesized that use of general anesthesia and the systemic inflammatory response associated with major surgery could account for the late decline, but could not rule out other factors such as, for example, normal aging. We observed a similar degree of long-term cognitive change in both the nonsurgical and CABG patients, suggesting that these changes may not be attributable to anesthesia or major surgery. Rather, the changes in these two groups may be related to a combination of increasing age and cerebrovascular disease. In previous studies, one of the most consistent predictors of late cognitive decline has been older age [2, 4]. Patients with coronary artery disease have been found to have a high prevalence of cerebrovascular disease, even before surgery [21, 22]. The lower cognitive performance observed at baseline in all groups with coronary artery disease would be consistent with possible manifestations of cerebrovascular disease.

This study has limitations: it was not randomized as it was not possible at the time of inception of our study to design or implement such a study. Further, it was not ethically appropriate to randomly assign patients with triple-vessel coronary artery disease to surgical or nonsurgical treatment. The changes from baseline to 72 months observed in the composite global score in our CAD groups are of similar magnitude (ranging from –0.10 to 0.05 SD units) to that observed in previous randomized comparisons of on- and off-pump patients (ranging from –0.06 to –0.09 SD units) [4], suggesting that our findings are similar to those from the only prospective randomized study of these two populations. The majority of patients, with the exception of the off-pump group, were from a single institution. Although it is possible that these findings would not apply to a larger population, the patient demographics for this study are similar to those in many studies of CABG populations in academic medical centers in the United States. It is also possible that selective drop-out of poorly performing subjects would bias the findings from this study. Our statistical methods adjusted for differential drop-out rates that are predictable from observed variables, but not for those that cannot be observed.

The strengths of this study are in its design, with appropriate comparison groups, length of follow-up, and testing by the same closely knit, experienced team. The overall loss to follow-up in this study is similar to what has been reported in previous long-term studies of cognition after CABG. The mortality and follow-up rates were similar in the three coronary artery disease groups. Hence, comparisons of change in cognitive performance among the groups with CAD are not biased by differential mortality. There was, however, higher mortality among the CAD groups than in the HHC group, and we therefore cannot rule out some bias in these comparisons.

In contrast with many previously published studies of long-term cognitive change, we included all eligible subjects in each group with no exclusions for medical reasons. Previous studies of late cognitive decline after CABG have generally focused on the incidence of late decline [2, 4, 17]. In the absence of appropriate comparison groups, however, the choice of a criterion for what constitutes actual decline is largely arbitrary. Thus, previously reported incidences of decline have limited clinical applicability. We chose to analyze within-patient changes in performance over time using comparison patients with and without coronary artery disease, which allowed us to take into account factors associated with repeated cognitive testing such as practice effects, random variability, and regression to the mean.

In summary, this study indicates that there is mild decline in cognitive performance over the 72-month follow-up period for all three groups with coronary artery disease. The lack of significant differences in the late cognitive outcomes among the groups with coronary artery disease rules out any selective effects attributable to the surgery, anesthesia, or the use of cardiopulmonary bypass. Thus, we conclude that long-term cognitive performance should not be a factor in choice of therapy for coronary artery disease.

	Appendix 1

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 

	Appendix 2

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 

	Appendix 3

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 
This study was supported by grant 35610 from the National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD; by the Dana Foundation, New York, NY; and by the Johns Hopkins Medical Institution GCRC grant RR 00052. The authors thank the participating physicians and surgeons who contributed to patient recruitment from our institution, as well as referring off-pump surgical sites. We acknowledge the efforts of Louis M. Borowicz, Jr., who assisted in the coordination of the study and neuropsychological testing, and thank Pamela Talalay, PhD, Rebecca Gottesman, MD, and Marilyn Albert, PhD, for their assistance in manuscript preparation. Special thanks are extended to our study participants who volunteered their time and energy to make this study possible.

	Footnotes

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 
The Appendices are available only online. To access them, please visit: http://ats.ctsnetjournals.org and search for the article by Selnes, Vol. 88, pages 445–54.

^_* See note at end of article regarding e-only Appendices.

^_* See note at end of article regarding e-only Appendices.

	References

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Appendix 3 Footnotes Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): William A. Baumgartner Permission Requests Citing Articles Citing Articles via HighWire Google Scholar Articles by Selnes, O. A. Articles by McKhann, G. M. PubMed Articles by Selnes, O. A. Articles by McKhann, G. M. Related Collections Coronary disease Extracorporeal circulation Related Article