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American Journal of Critical Care. 2006;15: 290-298
Copyright © 2006 by the American Association of Critical-Care Nurses.
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Correlates of Neurocognitive Function of Patients After Off-Pump Coronary Artery Bypass Surgery

By Sue Sendelbach, RN, PhD, Ruth Lindquist, RN, PhD, Shigeaki Watanuki, RN, PhD and Kay Savik, MS. From Abbott Northwestern Hospital (SS) and School of Nursing, University of Minnesota (RL, KS), Minneapolis, Minn, and School of Nursing and Rehabilitations, Aino University, Osaka, Japan (SW).


   Abstract
Top
 Abstract
Review of the Literature
 Methods
 Results
 Discussion
 Conclusions
 References
 
• Background Decreases in neurocognitive function have been reported in patients who have undergone off-pump coronary artery bypass surgery; however, few investigators have examined the correlates of the decreases.

• Objectives To explore and determine the correlates of neurocognitive function at the time of discharge from the hospital in patients undergoing off-pump coronary artery bypass surgery.

• Methods Patients undergoing off-pump coronary artery bypass surgery at Abbott Northwestern Hospital, Minneapolis, Minn, were administered tests of neurocognition (cognition and motor function), anxiety, depression, and quality of life preoperatively (within 72 hours of surgery) and postoperatively (at least 72 hours after surgery but before discharge from the hospital).

• Results A total of 54 patients (79.6% men), mean age 64.5 years, completed tests both preoperatively and postoperatively. When baseline function was controlled for, increased age and new-onset atrial fibrillation (F3,40 = 42.97; P < .001) were associated with decreases in postoperative cognitive function; increased age and anxiety (F3,35 = 15.83; P < .001) were associated with decreases in postoperative motor function.

• Conclusion Older patients, anxious patients, and patients with new-onset atrial fibrillation are at risk for neurocognitive changes after off-pump coronary artery bypass surgery. Further studies with larger sample sizes should be done to examine interventions to reduce preoperative anxiety in these patients. Interventions to prevent postoperative atrial fibrillation should be explored to determine whether the interventions prevent a decline in neurocognitive function.

Despite advances in coronary artery bypass graft (CABG) surgery resulting in substantial reductions in age- and risk-adjusted mortality, the prevalence of a decline in neurocognitive function in patients after CABG surgery has changed little during the past 15 years.1 Use of the cardiopulmonary bypass pump was commonly thought to be a cause of neurocognitive decline, but adverse changes also occur in patients who have CABG surgery without use of the pump.2–6 Although on-pump or conventional CABG surgery is the more predominant surgery performed, some centers do not use cardiopulmonary bypass pumps for any coronary bypass surgeries.7

The importance of the decline in neurocognitive function is underscored by the observation that patients with even minor declines may require admission to skilled nursing facilities rather than being able to return to their homes after CABG surgery.8 The additional costs attributed to neurocognitive dysfunction are estimated to be $400 million annually; the estimate increases to $2 billion to $4 billion annually if the costs for care after discharge from the hospital are included.8,9 Moreover, neurocognitive dysfunction significantly diminishes quality of life after CABG surgery.10,11


   Review of the Literature
Top
 Abstract
 Review of the Literature
Methods
 Results
 Discussion
 Conclusions
 References
 
Conventional CABG Surgery
Neurocognitive changes after conventional CABG surgery were initially reported in the late 1950s and early 1960s.12,13 The most frequently reported deficits were decreases in concentration, memory and learning, and speed of visual-motor responses.14 In early studies,15–17 the cardiopulmonary bypass machine and intraoperative hypotension were considered potential causes of neurological events, and investigators focused on changing parts of the circuit of the bypass machine or on interventions to prevent hypotension during the surgery. Nevertheless, 31% to 73% of patients had neurocognitive decline after conventional CABG surgery.8,18–23


Neurocognitive decline following on-pump coronary artery bypass grafting occurs in 31% to 73% of patients.

 

Off-Pump CABG Surgery
Decline in neurocognitive function also occurs in patients who have off-pump CABG surgery. In the earliest published study of neurocognitive function after off-pump CABG surgery, Malheiros et al2 in Brazil found new neurocognitive abnormalities in 35.6% of patients who had conventional CABG surgery and in 38.7% of patients who had off-pump surgery. In subsequent studies4–6,24,25 of the differences between patients who had conventional CABG surgery and patients who had off-pump CABG surgery, postoperative neurocognitive declines did not differ significantly between the 2 groups or patients who had off-pump surgery had significantly less decline.

The purpose of the exploratory study reported here was to identify preoperative, intraoperative, and postoperative correlates of neurocognitive functioning of patients after off-pump CABG surgery.


Neurocognitive decline was less in off-pump versus on-pump coronary bypass grafting in some studies, but no difference was found in others.

 


   Methods
Top
 Abstract
 Review of the Literature
 Methods
Results
 Discussion
 Conclusions
 References
 
This study was a part of a larger study of neurocognition in patients after off-pump CABG surgery.26 Approval for the study was obtained from the institutional review boards of the health system and the affiliated university.

Design
A prospective, descriptive, correlational design was used to document neurocognitive functioning at baseline preoperatively (within 72 hours of surgery) and at least 72 hours postoperatively (but before discharge from the hospital). Demographic data; measures of anxiety, depression, and quality of life; and patients’ characteristics were also collected.

Setting and Patients
Data were collected in cardiovascular units at Abbott Northwestern Hospital, a large urban, metropolitan, tertiary care hospital in Minneapolis, Minn, licensed for 926 beds. More than 550 patients have CABG surgery each year at the hospital; 60% to 70% of the surgeries are performed off-pump.

All patients who were scheduled for an off-pump CABG surgery procedure were screened for eligibility for participation in the study. Patients were included if they were 21 years or older, fluent in English, living within the defined geographic area, and scheduled for elective off-pump CABG surgery. Criteria for exclusion were other concurrent surgical procedures, physical impairment that precluded being able to write, neurocognitive impairment, current substance abuse, concurrent psychiatric diagnosis, pulmonary artery systolic pressure 80 mm Hg or more, inability to give consent, and physician’s objection.

Procedure
Eligible patients were identified from the surgical roster by a research assistant or by the nurse clinicians and/or physician assistants (see FigureGo). For each patient, after receipt of informed consent, the Standardized Mini-Mental State Examination (SMMSE)27 was administered, and if the score was greater than 23, the neurocognitive testing battery was administered in a consistent order. Patients with scores of 23 or less on the SMMSE were excluded, because these scores have generally been considered indicative of cognitive impairment.27


Figure 1
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  		Flow chart of patients, eligibility, and recruitment status.

Reprinted from Sendelbach et al.26 copyright2005, with permission from Elsevier.

Abbreviation: CCAB, conventional coronary artery bypass.

 
All testing was performed by research nurses and/or research assistants who were trained by a neuropsychologist or by one of the research nurses trained by the neuropsychologist. Efforts were made to ensure that preoperative and postoperative testing sessions were conducted in quiet and distraction-free environments in the patient’s hospital room or in the room where the patient received preoperative education.

Measures
Demographic data and data on preoperative, intra-operative, and postoperative cardiac and medical variables were collected to describe the sample. Data on variables reported in the literature as correlates or risk factors of neurocognitive decline after conventional CABG surgery were also collected.

A self-administered questionnaire was given pre-operatively to obtain demographic data, including age, sex, educational level, income, employment status, marital status, and ethnicity. After each patient’s discharge from the hospital, clinical characteristics were obtained from the patient’s medical record by 2 trained abstractors who used the Society of Thoracic Surgeons Database Core Data Elements, version 2.41.28 This well-established national database, which has been in existence since 1989, consists of a core data set with variables abstracted by using uniform and standard definitions.

Instruments
Tools for measurement of neurocognitive function were based on the recommendation of the Statement of Consensus on Assessment of Neurobehavioral Outcomes After Cardiac Surgery.29 Criteria for measures included the cognitive domain of the test, the sensitivity and reliability of the test, and the overall balance of the cognitive domains assessed in the battery.29 Core measures recommended were the Rey Auditory Verbal Learning Test (AVLT), the Trail Making Test parts A and B, and the Grooved Pegboard test. These were used along with the Symbol Digit Modalities and the Controlled Oral Word Association (COWA) tests. In order to reduce the number of variables, 2 composite scores, 1 reflecting motor function and 1 reflecting cognitive function, were created. Cognitive function was measured by using the AVLT, parts A and B of the Trail Making Test, and the COWA test; motor function was tested by using the Grooved Pegboard test and the Symbol Digit Modalities test.

  Cognitive Function.   The AVLT is a test of memory. Subjects repeat 15 unrelated words that have been read to them in a series of trials. In trials 1 through 5, subjects repeat the same list of words; in trial 6, they repeat a new list of 15 words, and in trial 7, they recall as many words as possible from the first 5 trials. In the final trial, trial 8, subjects are required to remember the words read to them 20 to 30 minutes previously.30–32 The end point is the number of words correctly remembered. Criterion-related validity of the test has been demonstrated; the AVLT is a sensitive measure of neurological impairment and verbal memory deficits in different populations of patients.32 Test-retest reliability was demonstrated by comparing alternative forms of the test.31

In the COWA test, subjects are given 60 seconds (for each letter) to verbalize as many words as they can remember that start with the letters F, A, and S.32 The sum of the number of correct words for all 3 letters is the score. Test-retest reliability has ranged from .70 to .88 in adults. Criterion-related validity was demonstrated in studies in which the COWA test was a highly sensitive measure of frontal lobe damage, regardless of which side the lesion occurred on, and in studies in which the COWA score indicated more impairment in patients with bilateral frontal lesions than in patients with unilateral lesions.32

Parts A and B of the Trail Making Test are tests of attention, mental flexibility, and motor function.30 Subjects are required to connect, as quickly as possible, a series of numbers and letters in alternating sequence.30 When an error is made, the subject is stopped and returned to the last correct position. The score is the time of completion, in seconds, and the number of errors. Reported interrater reliability is .94 for part A and .90 for part B.30,32 Test-retest reliability was .78 for part A and .67 for part B for patients with diffuse cerebral vascular disease with a mean age of 60 years.30,32 In a study32 of differences between healthy subjects and different groups of patients, scores on part A could be use to correctly classify healthy subjects 80% of the time, patients with diffuse neurological lesions 26% of the time, and patients with focal neurological lesions 95% of the time. In the same study, scores on part B could be used to classify healthy subjects 74% of the time, patients with diffuse lesions 20% of the time, and patients with focal lesions 94% of the time.

  Motor Function.   The Symbol Digit Modalities test is a measure of information-processing speeds, complex scanning, and visual tracking.30,33 It requires subjects to reproduce in 90 seconds as many coded symbols as possible according to a coding scheme for pairing digits with symbols. The score is the number of correct matches within the time limit. In a study33 of 80 healthy adults, the test-retest reliability was .80. Scores on the Symbol Digit Modalities test could be used to correctly identify 86% of patients who had confirmed, chronic brain lesions and 92% of healthy subjects when administered to a group of 100 subjects and patients.30

The Grooved Pegboard test is a measure of speed and dexterity.30 Subjects place 25 key-shaped pegs into a board as fast as they can, first with the dominant hand and then with the nondominant hand.30 The score is the time taken to place all pegs, with a cutoff of 300 seconds for completion of the task. Reliability coefficients have ranged from .69 to .76 for the dominant hand and from .68 to .78 for the nondominant hand during a 6-month period in a sample of 360 healthy subjects 16 to 70 years old.31

  Additional Measures.   The additional assessment battery included the following instruments: the SMMSE (mental state),27 the State Trait Anxiety Inventory (anxiety),34 the Center for Epidemiological Studies Depression Scale (depression),35 the Medical Outcomes Study 12-Item Short Form (mental and physical health components),36 and the Ladder of Life (life satisfaction).37 The reliability and validity of these tests have been well established. Subjective physical symptoms were also measured but are beyond the scope of this article.

Data Analysis
Data were analyzed by using the SPSS statistical program, version 11.0.1 (SPSS Inc, Chicago, Ill). Descriptive statistics (means, medians, SDs, and ranges) were computed for age, anxiety, depression, and health-related quality-of-life measures. Normality was assessed by using histograms.

A total of 16 different variables of neurocognitive function were used as outcomes. Two composite scores were created according to the method of O’Brien38 to guard against an inflated type I error. The scores included a cognitive composite score for memory, attention and language and a motor composite score for information-processing speed and motor speed. The values (scores) were ordered within each outcome from worst to best by replacing each value with its corresponding rank. For each subject, a mean of his or her ranks across all outcomes was calculated. A mean ranking across all variables within the 2 categories was computed for each subject. After significant changes in the composite scores were determined, individual differences between preoperative and postoperative measures were assessed by using Wilcoxon matched-pairs signed-ranks tests appropriate for assessing differences in ranked data.

Covariates possibly related to postoperative composite scores were screened by using the appropriate bivariate test for ordinal data, that is, the Spearman correlation. The baseline measures and those variables that were associated at a P ≤ .10 level were included as candidates in a multivariate analysis of the postoperative score for the composite with multivariate regression. Appropriate regression diagnostics were performed to assess any violation of assumptions. Variables significantly associated with outcome postoperative scores but not normally distributed (hours of mechanical ventilation and creatinine level) were categorized. Hours of mechanical ventilation were dichotomized to on ventilator, yes or no; creatinine levels were dichotomized by using a value, based on the standard of the hospital, at which the creatinine level was considered high (>115 µamol/L [>1.3 mg/dL]).


   Results
Top
 Abstract
 Review of the Literature
 Methods
 Results
Discussion
 Conclusions
 References
 
The mean age of the sample (n = 54) was 64.5 years; 66.7% had some college to a bachelor’s degree or higher; 44.2% were retired; 50% earned at least $55 000. The majority were white (92.5%) and were married (84.9%).

The medical characteristics of the sample were recorded from a review of the patients’ medical records. A majority of patients had class III angina according to the Canadian Cardiovascular Society Classification (50.9%); had significant stenosis of 3 major vessels (75.9%); and had a history of hypertension (80.8%) and hypercholesterolemia (90.4%). The majority of patients (96.2%) had 4 or fewer bypass grafts. Atrial fibrillation (25.9%) was the most frequent complication experienced; 9.3% of patients experienced pneumonia; other complications were acute renal failure (1.9%), need for dialysis (1.9%), and stroke (0.9%). Most patients (94.4%) went home or to other private residences after discharge from the hospital.

Patients reported that they felt more positively about their past lives than about their present lives (P <. 001), and they felt more positively about the future than about the present (P < .001). We found no difference in anxiety measurements from preoperative to postoperative (P = .25).

Baseline measures and intraoperative and postoperative variables associated at a P ≤ .10 (Table 1Go) that were entered into the multivariate analysis as possible correlates of cognitive function were education ({rho} =.24, P=.10), age ({rho} =–.50, P<.001), ejection fraction ({rho} =.24, P = .08), cognitive composite score ({rho} = .85, P < .001), motor composite score ({rho} = .66, P < .001) hours of mechanical ventilation ({rho} = –.38, P = .007), atrial fibrillation ({rho} =.28, P=.04), and postoperative anxiety ({rho} =–.30, P = .03). The variables for motor function were age ({rho} = –.61, P < .001), creatinine level ({rho} = –.35, P = .01), cognitive composite score ({rho} = .65, P < .001), motor composite score ({rho} =.70, P<.001), hours of mechanical ventilation ({rho} = –.44, P = .002), morphine equivalents ({rho} = .34, P = .02), and postoperative anxiety ({rho} = –.35, P = .01).


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  		Table 1 Bivariate correlations of preoperative variables and intraoperative and postoperative variables to postoperative cognitive and motor composites of neurocognitive functional outcome*

 
The final model for postoperative cognitive composite (Table 2Go) accounted for 76.3% of the total variance of the dependent variable. Significant correlates in the final model were the preoperative (baseline) cognitive composite score (P < .001), age (P = .01), and atrial fibrillation (P = .02). Younger patients with better preoperative cognitive function or those who did not go into atrial fibrillation had better postoperative cognitive function. The final model for the postoperative motor composite (Table 3Go) accounted for 58% of the total variance of the dependent variable and significant correlates were motor composite score at baseline (P < .001), age (P = .04), and postoperative anxiety (P < .02). Those patients who were younger, had less anxiety, or performed better at baseline had better motor composite scores postoperatively before discharge from the hospital.


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  		Table 2 Final model of stepwise regression (cognitive composite)

 

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  		Table 3 Final model of stepwise regression (motor composite)

 

Younger patients with better preoperative cognitive function or those without atrial fibrillation had better postoperative cognitive function.

 


   Discussion
Top
 Abstract
 Review of the Literature
 Methods
 Results
 Discussion
Conclusions
 References
 
Correlates of Neurocognitive Function
Age is a major contributor to central nervous system dysfunction after cardiac surgery, and it is the most consistent and least controversial factor predictive of a decline in neurocognitive function.39–43 Our results confirmed this association. Although the mechanisms of action that place older persons at increased risk for poorer neurocognitive function after cardiac surgery are unknown, several investigators have offered explanations. Aging is associated with an increased incidence of atherosclerosis and cerebrovascular disease.21 In addition, patients who need a CABG procedure usually have extensive atherosclerosis in multiple vascular systems.44 Atherosclerosis of the aorta has often been identified as increasing the risk for neurocognitive deficits; the incidence of such aortic atheromatous disease increases with age, from 20% at age 50 years, to more than 80% in persons older than 75 years; however, the age-related effects on organ systems are variable.45–48 Therefore, if and when the aorta is manipulated during surgery, the possibilities for plaque or debris to be dislodged and to migrate into the brain during surgery are increased. Other researchers45–48 have suggested that aging may increase patients’ vulnerability to injury, because increased age has been associated with a reduction in global and regional blood flow and with alterations in the autoregulation of cerebral blood flow.


Age is a major contributor to central nervous system dysfunction following cardiac surgery.

 


Aortic atherosclerosis, which occurs in 20% of patients at age 50 and about 80% at age 75, increases the risk of neurocognitive deficits because plaque may be dislodged as the aorta is manipulated.

 

In our study, cognitive and motor functions at baseline (individual tests and composite scores) were significantly associated with postoperative cognitive and motor performance (individual tests and composite scores). A similar association was found by Millar et al40 in a study of cognition (memory). In that study, 16% of patients who had conventional CABG surgery had indications of neurocognitive impairment in pre-operative tests. Of these patients, 85% had impairment 6 days after surgery and 39% at 6 months. These findings contrasted with those of the group (84% of patients) who had no evidence of impairment preoperatively; only 14% of these had impairment at 6 days after surgery, and only 2% remained impaired at 6 months. Although the patients in this study40 were younger (mean age 59.4 years for men and 62.4 years for women) than the patients in our study, age was also clearly established as a predictor or correlate of neurocognitive decline after CABG surgery.

Atrial fibrillation is a common condition after CABG surgery. In the first published study of the association between atrial fibrillation and neurocognitive function, Stanley et al49 found an association between atrial fibrillation and neurocognitive function at 6 weeks after surgery. Atrial fibrillation causes an increased risk for thrombus formation and decreased cardiac output. These effects could be responsible for the deficits we detected in the patients in our study.

Consistent with the recommendations of the Consensus Statement,29 we measured anxiety because mood state can influence tests of neurocognitive function. Despite the views of the authors of the Consensus Statement that performance could make a subject more anxious, the reverse was not considered, that is, that the poor motor function caused the higher anxiety. We found a correlation between postoperative anxiety and postoperative motor function. These results suggest a potentially nonorganic basis for function. Anxiety has been well documented in patients undergoing CABG surgery. Duits et al50 performed a meta-analysis of studies that predicted psychosocial outcome after CABG surgery and found that preoperative anxiety and depression were predictive of postoperative psychological maladjustment. Anxiety is a nursing diagnosis that may be amenable to nursing intervention. Further studies should examine which nursing interventions would be most effective in decreasing the anxiety of patients undergoing off-pump CABG surgery.


Preoperative anxiety and depression are predictive of postoperative psychological maladjustment.

 

Limitations
This study has several limitations. First, patients with SMMSE scores of 23 or less were excluded from the study because they may have had cognitive impairment. This exclusion may limit the generalizability to patients with initially low SMMSE scores. Second, the small sample size further limits the generalizability. With a larger sample size, we might have found other statistically significant correlates. Third, the study was conducted at a single institution where approximately 60% to 70% of all CABG surgeries are performed off-pump; nationally, approximately 20% are done off-pump.51 Last, patients undergoing off-pump CABG surgery urgently or emergently were excluded from the study; the results might have been different if these patients had been included.


   Conclusions
Top
 Abstract
 Review of the Literature
 Methods
 Results
 Discussion
 Conclusions
References
 
Age, anxiety, new-onset atrial fibrillation, and baseline cognitive and motor function were found to be correlates of neurocognitive function at the time of discharge from the hospital in patients who had off-pump CABG surgery. Future studies should include larger representative samples to determine replicability and generalizability of these findings. Interventions to reduce anxiety and reduce and/or eliminate postoperative atrial fibrillation should be studied to determine their impact on patients’ neurocognitive function. Finally, a study of neurocognition, including the course of patients after discharge from the hospital, would be of value to better understand long-term neurocognitive outcomes of patients after off-pump CABG surgery.


   ACKNOWLEDGMENTS
 
This research was funded by grants from the Minneapolis Heart Institute Foundation, the Helen Wells Nursing Research Award, and the Allina Foundation.

To purchase electronic or print reprints, contact The InnoVision Group, 101 Columbia, Aliso Viejo, CA 92656. Phone, (800) 809-2273 or (949) 362-2050 (ext 532); fax, (949) 362-2049; e-mail, reprints{at}aacn.org.


   REFERENCES
Top
 Abstract
 Review of the Literature
 Methods
 Results
 Discussion
 Conclusions
 References
 

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