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Eur J Cardiothorac Surg 2006;29:74-81
© 2006 Elsevier Science NL

Short-term and long-term cognitive function and cerebral perfusion in off-pump and on-pump coronary artery bypass patients

Vladimir I. Chernov a , * , Nataliya Yu. Efimova b , Irina Yu. Efimova a , Shamil D. Akhmedov c , Yuri B. Lishmanov a

a Department of Nuclear Medicine, Institute of Cardiology, Kievskaya street, 111A, 634012 Tomsk, Russia
b Department of Ambulatory Cardiology, Institute of Cardiology Tomsk Research Center, 634012 Tomsk, Russia
c Department of Cardiac Surgery, Institute of Cardiology Tomsk Research Center, 634012 Tomsk, Russia

Received 20 March 2005; received in revised form 22 August 2005; accepted 3 October 2005.

* Corresponding author. Tel.: +7 3822 558298; fax: +7 3822 555057. (Email: nuclear{at}cardio.tsu.ru).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 
Objective: The aim of this study was to evaluate cognitive function, as measured by serial neuropsychological testing, and cerebral perfusion, as measured by brain SPECT scanning in patients with coronary artery diseases (CAD) following off-pump and on-pump coronary artery bypass graft surgery. Besides, the relationship between cerebral blood flow, cognitive functions, surgery parameters, and cardiac function in these patients were estimated. Also, brain-protective effects of instenon were studied. Methods: Brain SPECT and comprehensive neuropsychological testing were performed 1 day before, 10–14 days and 6 months after coronary artery bypass graft surgery (CABG). The study involved 65 patients (62 males and 3 females, mean age 55 ± 2) who underwent CABG with cardiopulmonary bypass (CPB) (43 pts) and off-pump coronary revascularization (OPCAB) using the Octopus stabilization system (22 pts). In 21 cases employing CPB, for prevention of the impairments of cerebral perfusion and cognitive deficit instenon was administered. Results: CABG with the use of extracorporeal circulation is complicated by short-term and long-term neurocognitive dysfunction (in 96 and 55% cases, correspondingly). Also, in the early period after CABG, in 68% patients, decrease in regional cerebral blood flow (rCBF) was found, and after 6 months brain perfusion was lower than the baseline in 55% cases. Relationship between postoperative rCBF changes and the dynamics of cognitive function was found in early period and after 6 months following CABG. Conclusion: The coronary revascularization on beating heart or preventive administration of instenon in CPB patients helps significantly to diminish the risk of cerebrovascular complication.

Key Words: Coronary artery bypass graft surgery • Cardiopulmonary bypass • Off-pump coronary revascularization • Cognitive function • Cerebrovascular complications • Brain SPECT


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 References
 
Despite many technological developments in cardiac surgical procedures, open-heart surgery is still a significant risk for cerebral injury. There is a high incidence of cognitive dysfunction, variously reported to occur in between 48 and 79% of patients, who had undergone coronary artery bypass graft surgery (CABG) employing cardiopulmonary bypass (CPB) [1,2]. The etiology remains unclear; at the same time, determination of reasons of cognitive dysfunction after CABG may become the base for investigation of methods for the prevention of postoperative cognitive dysfunction. Alterations in cerebral perfusion during CPB may be causative of cerebral complication [3]. Brain SPECT with 99mTc-HMPAO is widely used for noninvasive cerebral blood flow estimation.

The aim of this study was to evaluate cognitive function, as measured by serial neuropsychological testing, and cerebral perfusion, as measured by brain SPECT scanning in patients with coronary artery diseases (CAD) following off-pump and on-pump coronary artery bypass graft surgery. Besides, we estimated the relationship between cerebral blood flow, cognitive functions, surgery parameters and cardiac function in these patients. Also brain-protective effects of instenon were studied.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 References
 
2.1 Patients
The study involved 65 patients (62 males and 3 females, mean age 55 ± 2) with stable angina of the III and IV NYHA classes were included in the study, 44 of them had a history of previous transmural myocardial infarction. All patients were studied by coronary angiography using standard Judkin's protocol. All patients had CAD ranging from 1 to 5 (3.5 ± 1.2) with degree of stenosis of more than 75% of lumen. Five patients had aneurysms of left ventricular. Heart failure of I and II classes was observed in all patients.

All patients underwent CABG, of these 22 patients with cardiopulmonary bypass without pharmacological brain protection (group 1). In 21 randomly assigned cases employing CPB, for the prevention of the impairments of cerebral perfusion and cognitive deficit instenon ("Nycomed") was administered (group 2). The drug was injected intravenously by leaving (2 ml of instenon was soluted in 250 ml 0.9% solution of NaCl) 1 day before surgery, during CABG (before start CPB) and for 4 days after surgical intervention once a day. Then, for 10 days the patients continued taking instenon orally (one tablet three times a day). In 22 patients off-pump coronary revascularization (OPCAB) using the Octopus stabilization system "Medtronic" (USA) was carried out (group 3) [4]. Patient demographics are provided in Table 1 . The groups of patients had no differences by age, sex, education, CAD duration and extensiveness, but index of coronary arteries bypass (bypass/patients) was higher in group 2 in comparison to group 3 (3.3 vs 1.9, p < 0.05).


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  		Table 1. Patient characteristics (demographical, pre-, peri- and postoperative variables)
 
Criterions of excluding patients from the study were as follows: previous cardiac surgery, a history of surgery with a general anesthetic within the previous 2 years, surgery of carotid arteries, congenital heart disorders, valvular diseases, arrhythmia, neurological disorders (including stroke), psychiatric illness (including drug abuse and chronic alcoholism), major visual or hearing deficit, old age below 75 years, carotid artery stenosis of more than 30% of lumen by preoperative duplex examination.

Informed consent was obtained from each patient. The study was approved by Ethics Committee of human research of the Tomsk Institute of Cardiology.

2.2 Anesthesia and surgical procedure
The patients who underwent CABG were operated on with standard anesthesia techniques and surgical procedures. The anesthetic protocol consisted of premedication with relanium 10 mg, morphine 10 mg and atropine 0.5 mg. Muscle relaxation was provided by arduan 0.1 mg/kg. Anesthesia was maintained with an infusion of fentanyl bolus doses of up to 10 µg/kg x min. For the conventional CABG, all patients underwent a midline sternotomy. CPB using the heart lung machine (Jostra, Germany) was applied. Cardiopulmonary bypass was under normothermia (arterial blood temperature 36 °C). The cardiopulmonary bypass circuit was primed with isoosmolar solution with calculated hemotocritis above 25%. The mean arterial pressure was kept above 70 mmHg. Myocardial protection during aortic cross-clamping was accomplished with antegrade blood warm cardioplegia. In patients of group 1, the mean cardiopulmonary bypass time was 106 ± 8 min, the mean aortic cross-clamp time 72 ± 5 min, the mean extubation time –20 ± 4.5 h and index of coronary anastamoses (bypass/patient) –2.8. In patients of group 2, the mean cardiopulmonary bypass time was 112 ± 9 min, the mean aortic cross-clamp time 68 ± 6 min, the mean extubation time –19 ± 3.5 h and index of coronary anastamoses (bypass/patient) –3.3 (Table 1).

For the off-pump CABG (group 3), midline sternotomy was performed in all patients. The Octopus II system (Medtronic Inc., USA) was used in all patients to stabilize the suture site. In beating heart surgery patients, the mean extubation time was –17 ± 3 h and index of coronary anastamoses (bypass/patient) –1.9 (Table 1).

2.3 Protocol
All patients underwent brain SPECT scanning and comprehensive neuropsychological testing 1 day before, 10–14 days and 6 months after surgery. To reduce the "test–retest" effects different versions of neuropsychological tests were used.

2.4 Brain SPECT
99mTc-PAO (Amersham, UK) was prepared according to instruction and used within 5 min after labeling. Perfusion brain SPECT was performed 10–12 min after the injection of 99mTc-HMPAO in dose 25 mCi. SPECT examinations were performed using a rotating gamma-camera ("Omega 500", Technicare Corp.) equipped with a high-resolution low-energy collimator (140 keV) and interfaced with a dedicated computer system for scintigraphic data processing ("Scinti", Gelmos). Sixty-four projections in 64 x 64 matrix, of 20 s each, were acquired over 360°. Tomographic sections were obtained using Parzen smoothing filter as a series transverse 2 pixel slices.

2.5 Data analysis
SPECT brain images were divided into 14 symmetrical (right and left) regions of interest per patients: inferior and superior frontal lobes, temporal, anterior and posterior parietal, occipital lobes and cerebellar hemispheres. To calculate regional cerebral blood flow (rCBF, ml/100 g/min), a three-component model of kinetics 99mTc-HMPAO by Lassen et al. [5], modified by Yonecura et al. [6], was used. A 5% or more decrease in postoperative rCBF in comparison to preoperative rCBF was defined as significant.

2.6 Neuropsychological testing
We assessed the patients’ cognitive status by means of seven neuropsychological tests that were most sensitive to cerebral damage resulting from cardiac surgery and CPB (Table 2 ) [7]. A 20% decrease in postoperative test scores in comparison with preoperative baseline on two or more tests was defined as "cognitive dysfunction".


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  		Table 2. Neuropsychological tests used to assess cognitive deficits after cardiac surgery
 
2.7 Statistical analysis
The data received were processed by the method of variation statistics using "STATGRAF" numeric package using t-Student parametric paired and non-paired criteria. Between-group comparisons were done by using the Wilcoxon rank-sum test. Linear regression analysis was performed to calculate the relationship between rCBF, cognitive tests scores, heart functions, parameters of surgery and CPB.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 References
 
We observed no in-hospital psychiatric complications (delirium) and none of the beating heart surgery patients and patients with preventive administration of instenon suffered from postoperative neurological complications such as transient ischemic attacks or strokes. One patient of the group 1 had a stroke.

Measures of immediate verbal memory, delayed verbal memory and learning showed a significant decrease after surgery with CPB on an average of 25.6% (p = 0.022), 43.3% (p = 0.000003) and 23.1% (p = 0.00000), respectively, by the Rey Auditory Verbal Learning Test (AVLT), for delayed memory and learning that remained for 6 months (Fig. 1 ). Also, the patients of group 1 demonstrated a significantly postoperative psychomotor slowing by Trail Making Test (TMT) (B) on 13.5% (p = 0.03), decrease in immediate visual memory by CFT (early) on 26.3% (p = 0.04) and delayed visual memory by the Complex Figure Test (CFT) (delayed) on 36% (p = 0.025) (Fig. 1), for delayed visual memory that remained for 6 months. Thus, 21 (96%) patients following coronary revascularization using CPB showed a cognitive deficit, which was 12 (55%) in 6 months after surgery (Fig. 2 ).


Figure 1
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  		Fig. 1. Scores by cognitive domain before and after coronary artery bypass grafting. TMT: the Trail Making Test, AVLT: the Rey Auditory Verbal Learning Test, DCT: the Bourdon–Wiersma Dot Cancellation Test, CFT: the Complex Figure Test, * p < 0.05, ** p < 0.01, *** p < 0.001 (in comparison with the preoperative score), p < 0.05 (in comparison with group 1).

 

Figure 2
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  		Fig. 2. Neurocognitive deficit in the early and the late period after CABG.

 
CABG with CPB was followed by the decrease in regional cerebral blood flow relative to baseline in frontal and in parietal cortex of right hemisphere (p < 0.01), that remained also in inferior part of frontal cortex and in posterior part of parietal cortex in the late postoperative period (Table 3 ).


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  		Table 3. The regional cerebral blood flow in CABG patients (ml/100 g/min)
 
Individual analysis of brain SPECT has shown that in 15 (68%) patients of group 1, significant decrease (more than 5%) in rCBF was found in early period after CABG and in 7 (32%) patients cerebral perfusion has not changed. After 6 months rCBF has returned to baseline only in three patients (Fig. 3 ).


Figure 3
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  		Fig. 3. The changes of regional cerebral blood flow in the early and the late period after CABG.

 
Relationship between postoperative rCBF changes and dynamics of cognitive function was found by linear regression analysis. Deterioration of delayed visual memory correlated well with the decrease in rCBF in right posterior parietal regions (R 2 = 0.612; p = 0.035) in early postoperative period. Significant correlation was shown between improvement of immediate verbal memory and increase in rCBF in right inferior frontal region (R 2 = 0.665; p = 0.048) in 6 months after surgery.

Also, the relationship between duration of CPB and immediate verbal memory in early postoperative period (R 2 = 0.255; p = 0.033) was found, as well as duration of mechanical lung ventilation correlated with early postoperative decrease in psychomotor speed and attention by Trail Making Test (Part B) (R 2 = 0.316; p = 0.024).

Patients of the group 2 have shown deterioration of delayed verbal memory in 23% (p = 0.0004) and learning on 11.6% (p = 0.0001). These parameters returned to baseline in 6 months after surgery (Fig. 1). In the group of patients with preventive administration of instenon, cognitive dysfunction was noted only in 11 (61%) and was less than in group 1 (p < 0.05). After 6 months the number of such patients decreased twice (Fig. 2).

In the patients of group 2, no significant declines of cerebral perfusion in the early postoperative measurements were found. Moreover, after 6 months in this group of patients we observed the increase in cerebral perfusion in superior frontal and right occipital regions (Table 3). In early postoperative period only 5 (24%) patients of group 2 demonstrated deterioration in cortical perfusion; moreover, in 8 (38%) cases even the increase in rCBF took place. During 6 months of follow-up the number of such patients reached 11 (52%) (Fig. 3).

Linear regression analysis was performed to evaluate the relationship between rCBF, cognitive tests scores and parameters of surgery in such group of patients. Prolongation of mechanical lung ventilation negatively influenced the immediate visual memory (R 2 = 0.295; p = 0.024) and increased the number of bypassed coronary arteries with deteriorated rCBF in left superior frontal region in early period of surgery (R 2 = 0.589; p = 0.016).

Improvement of cerebral perfusion in 6 months after CABG was connected with the improvement of cardiac function after surgery. Increase in left ventricular ejection fraction related with the rising of rCBF in right temporal and left occipital regions (R 2 = 0.901; p = 0.014 and R 2 = 0.826; p = 0.033, correspondingly).

In patients of group 3, cognitive deficit in early period after surgery was found only in 54% of cases (Fig. 2). Measures of immediate verbal memory, delayed verbal memory and learning showed a significant decrease in the early period after surgery on an average of 20.3% (p = 0.0004), 23% (p = 0.0005) and 11.3% (p = 0.003), respectively (Fig. 1). Also the patients of group 3 demonstrated a significant postoperative improvement of psychomotor speed by TMT (B) on 9.6% (p = 0.03) and attention by The Bourdon–Wiersma Dot Cancellation Test (DCT) on 66.7% (p = 0.01) (Fig. 1).

Only three (14%) of the patients following coronary revascularization on beating heart showed a cognitive deficit in 6 months after surgery, which was significantly less than in early postoperative period and in comparison to group 1 (p < 0.05) (Fig. 2).

The operations on beating heart were accompanied by the increase in cerebral perfusion in superior frontal regions in 8.9% (p < 0.05), in inferior parietal regions in 9.8% (p < 0.01) and in right occipital regions in 8.4% (p < 0.01) in the early postoperative period (Table 3). Significant improvement of rCBF in such regions remained for 6 months after CABG (Table 3).

After off-pump coronary revascularization, the improvement of cerebral perfusion was found in 13 (59%) patients, and only in 2 (9%) a decrease in rCABG was revealed (Fig. 3). In the 6 months after CABG, an increase in rCABG in comparison to baseline was found in 14 (63.6%) patients and in two cases postoperative deterioration of brain perfusion was remained.

A significant association between postoperative rCBF changes and dynamics of cognitive function was found in group 3 by linear regression analysis. In early postoperative period, increase in cortical perfusion in right superior frontal region correlated well with the improvement of attention by DCT (R 2 = 0.444; p = 0.035). Improvement of perfusion in right occipital region positive influenced on psychomotor speed by TMT (Part B) (R 2 = 0.519; p = 0.018) and attention by DCT (R 2 = 0.526; p = 0.019). In the 6 months after CABG on beating heart, significant relationship between increase in rCBF in left superior frontal region and improvement in immediate verbal memory (R 2 = 0.375; p = 0.034) was found. Also, increase in rCBF in right superior frontal region positive improved attention by DCT (R 2 = 0.489; p = 0.011). Growing of perfusion in left posterior parietal region in the 6 months after CABG had relationship with the improvement in immediate and delayed verbal memory (R 2 = 0.549; p = 0.006 and R 2 = 0.410; p = 0.025, correspondingly). Increase in rCBF in right posterior parietal region correlated well with the improvement in immediate verbal memory (R 2 = 0.660; p = 0.042), and growing of perfusion in right occipital region improved psychomotor speed by TMT (Part B) (R 2 = 0.809; p = 0.038) and attention by DCT (R 2 = 0.410; p = 0.003). Improvement in psychomotor speed by TMT (Part B) (R 2 = 0.618; p = 0.021) and attention by DCT (R 2 = 0.911; p = 0.044) also related with the increase in left ventricular ejection fraction in the early period after surgery.

In early postoperative period, prolongation of mechanical lung ventilation negatively influenced immediate verbal memory (R 2 = 0.305; p = 0.040) and increased the number of bypassed coronary arteries with deteriorated rCBF in left posterior parietal region (R 2 = 0.824; p = 0.001) in group 3.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
References
 
As it is well known, the use of CPB in cardiac surgery is connected with the high risk for neurocognitive dysfunction [1,2]. The results of the present study indicated that CABG using extracorporeal circulation in 96% of cases is complicated by cognitive decline in the early postoperative period. The three variables that showed significant impairment shortly after cardiac surgery were the Trail Making Test, the Rey Auditory Verbal Learning Test and the Complex Figure Test. All of these tests characterize memory and attention of the patient. Our findings agree with previous research that found measures of memory and attention the most likely to be affected after CABG [8]. After 6 months the incidence of neurocognitive dysfunction dropped to 55%. This finding agrees with other research reporting a reduced incidence of cognitive impairment in the months and years following open-heart surgery compared with the early postoperative period [9–12].

In spite of widely using the neuropsychological tests for neurocognitive function evaluation after CABG, the neuropsychological test studies have several limitations. As such, the influence on neuropsychological test scores of test–retest effects, normal test variability, and the effects of other factors such as general anesthesia or medication, could not be determined. In addition, patients may be anxious, depressed, or fatigue, conditions limiting their ability to undergo extensive testing.

On the other hand, brain SPECT with 99mTc-HMPAO occupies a prominent place in cerebral blood flow estimation [5,6]. Brain SPECT test–retest reliability has been established for patients tested under similar environmental and hemodynamic condition [13]. Brain SPECT has been employed in the functional imaging of cognitive processes, and has been shown to be responsive to the internal cognitive state [14]. In our study in the early period after CABG, in 68% patients, a decrease in rCBF was found, and after 6 months brain perfusion was lower than the baseline in 55% cases. Our findings agree with previous research that found significantly reduced cerebral perfusion after the operation in on-pump CABG patients [15]. On the other hand, in the study by Hall et al. only 15 of the 35 on-pump CABG patients showed worsening of perfusion during cardiopulmonary bypass [3].

In our study, neurocognitive function significantly correlated with the duration of mechanical lung ventilation in early postoperative period. Relationship between postoperative rCBF changes and dynamics of cognitive function was found in early period and after 6 months following CABG. According to this we suggest an agreement with other authors [16,17] that the early postoperative cognitive deficit reflect a combination of nonspecific effects of surgery (stress of hospital admission, sleep disturbance, fatigue and new environments) and anesthesia, superimposed on the effects of microemboli and/or hypoperfusion, the most frequently postulated pathophysiological mechanisms of cognitive change after open-heart surgery.

Persistent cognitive deficit observed after 6 months following CABG can be explained, in general, by the long-term consequences of extracorporeal circulation. According to this we can suggest that one of the most important causes of cerebral dysfunction after CABG involving CPB is microembolization of the brain vessels, associated with specific surgical and perfusion manipulation (the insertion of the aortic cannula, the start of CPB and, especially, removal of the aortic cross-clamp). Other researchers mention these phenomena in their works [18,19].

The sources of cerebral microemboli in cardiac surgery have become, as a rule, platelet aggregation, air, lipid droplets and particulate debris from atherosclerotic plaque in the ascending aorta [19]. Recent studies indicate that the degree of arterosclerotic disease of the aorta and the number of emboli detected by transcranial Doppler ultrasound during CPB are correlated with the changes in cognitive function [19]. Thus, using filter for microemboli may be helpful for the prevention of brain injury after CABG [20].

The mechanism of the preventive action of instenon on cerebral perfusion and cognitive function is connected with the effect of compounds of the medicine (ethamivan, hexobendin and ethophyllin) on pathogenic steps of ischemic and hypoxic cerebral damage. Ethamivan stimulates respiratory and vasomotor centers, and activates limbic system and reticular formation. These effects improve the functioning of cortical and subcortical neurons and help to reduce neurocognitive deficit. Hexobendin stimulates anaerobic glycolysis and improves cerebral metabolism in hypoxia. Ethophyllin improves in myocardial metabolism and heart contractility and as a result increases cerebral blood flow [21].

In turn, the increase in cerebral perfusion and some improvement in test scores of cognitive function in our study after CABG on beating heart are connected with normalization of cardiac hemodynamics, in particular with the increase of left ventricular ejection fraction [22].

The observed early neurocognitive deficit after CABG without the use of CPB may be associated with general nonspecific aspects of cardiac surgery, particularly, with anesthetization supply. The prolonged deterioration of cognitive function recorded in 14% of patients can be related to microemboli releasing during partial aortic clamping [23]. However, data about the influence of beating heart surgery on occurrence of cognitive deficit are various. Our result is in contrast with the follow-up study of Taggart et al.[24], who found no difference between the off-pump and on-pump CABG patients after 3 months. Murkin et al. [25], however, found a significantly lower incidence of cognitive deficit at 5 days (66% vs 90%, respectively, p = 0.005) and 3 months postoperatively (5% vs 50%, respectively, p = 0.0011) in off-pump surgery patients compared with on-pump CABG patients. In the study by Stroobant et al. [26] was also found a significant difference between the two groups 6 months after surgery.

The main limitation of our study is the fact that on-pump groups included more patients with a higher number of grafts. At the same time groups did not differ with regard demographic variables, important risk factors and postoperative factors.

Although some selection bias cannot be excluded, we conclude that CABG with use of extracorporeal circulation in 55% of cases is complicated by long-term neurocognitive dysfunction, connected with the decrease of cerebral perfusion. The coronary revascularization on beating heart or preventive administration of instenon helps significantly to minimize the risk of cerebrovascular complication, respectively, to 1.8 and 3.9 times.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 

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S. F. Marasco, L. N. Sharwood, and M. J. Abramson
No improvement in neurocognitive outcomes after off-pump versus on-pump coronary revascularisation: a meta-analysis
Eur. J. Cardiothorac. Surg., June 1, 2008; 33(6): 961 - 970.
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