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Ann Thorac Surg 2005;80:2126-2131
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Cerebral Ischemic Injury and Cognitive Impairment After Off-Pump and On-Pump Coronary Artery Bypass Grafting Surgery

Christian Lund, MD a , * , Kjetil Sundet, PhD b , Bjørn Tennøe, MD c , Per K. Hol, MD d , Kjell A. Rein, MD, PhD e , Erik Fosse, MD, PhD d , David Russell, MD, PhD a

a Department of Neurology, Oslo, Norway
c Department of Radiology, Oslo, Norway
e Department of Thoracic and Cardiovascular Surgery, Oslo, Norway
d The Interventional Centre, Rikshospitalet University Hospital, Oslo, Norway
b Department of Psychology, University of Oslo, Oslo, Norway

Accepted for publication June 7, 2003.

* Address correspondence to Dr Lund, Department of Neurology, Rikshospitalet University Hospital, 0027 Oslo, Norway (Email: christian.lund{at}rikshospitalet.no).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Off-pump coronary artery bypass grafting surgery reduces the intraoperative cerebral embolic load and may therefore cause less brain injury. The main aim of this study was to compare off-pump and on-pump surgery with regard to the frequency of new postoperative cerebral ischemic lesions and the prevalence of postoperative cognitive impairment. We also assessed whether preoperative cerebral ischemic injury predicts the risk for cognitive dysfunction after surgery.

METHODS: One hundred twenty patients with ischemic coronary artery disease were prospectively randomized to undergo off-pump or on-pump surgery. A detailed neuropsychological assessment and a cerebral magnetic resonance imaging examination were performed on the day before and at 3 months postoperatively. The neuropsychological assessment was repeated at 12 months.

RESULTS: There was no significant (p = 0.17) difference between off-pump (8.2%) and on-pump (17.3%) surgery with regard to new postoperative cerebral lesions. The prevalence of cognitive impairment after surgery was also similar in the two groups (3 months: off-pump 20.4%, on-pump 23.1%, p = 0.74; 12 months: off-pump 24.1%, on-pump 23.1%, p = 0.90). The degree of preoperative cerebral ischemic injury was significantly associated with cognitive dysfunction after on-pump (p = 0.02) but not after off-pump (p = 0.22) surgery. None of the patients with normal preoperative radiologic findings were found to have cognitive impairment at 3 months postoperatively (p = 0.04).

CONCLUSIONS: Long-term cognitive function and magnetic resonance imaging evidence of brain injury were similar after off-pump and on-pump coronary artery bypass grafting surgery. Preoperative cerebral magnetic resonance imaging can be used to predict the risk for cognitive dysfunction after coronary artery bypass grafting surgery.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
The main clinical manifestations of cerebral injury after coronary artery bypass grafting surgery with cardiopulmonary bypass (on-pump surgery) are ischemic stroke and postoperative cognitive impairment [1, 2]. Approximately 22% of on-pump patients show cognitive decline at 2 months postoperatively [3]. There is still, however, discussion regarding the extent, duration, and pathophysiology of postoperative cognitive impairment after cardiopulmonary bypass surgery [4, 5].

Coronary artery bypass grafting surgery without cardiopulmonary bypass (off-pump surgery) reduces the intraoperative cerebral embolic load [6, 7], and may therefore be preferable for the brain [8, 9]. Although some prospective randomized studies have reported that immediate postoperative cognitive outcome is better after off-pump compared with on-pump surgery [6, 10], it is uncertain whether there is a difference with regard to long-term cognitive outcome [11, 12].

The presence and degree of postoperative cerebral ischemic injury may be assessed using magnetic resonance imaging (MRI). Magnetic resonance imaging studies after on-pump and off-pump surgery have shown new focal cerebral lesions with a frequency of 21% to 45% [13–17]. It has not been determined, however, whether off-pump surgery results in a relative reduction of postoperative cerebral ischemic lesions. Assessment of cerebral ischemic injury before surgery may help predict the risk for postoperative neurologic dysfunction after on-pump surgery [18, 19], but this has not been studied for off-pump surgery.

The main aim of this study was therefore to compare off-pump and on-pump coronary artery bypass grafting surgery with regard to the frequency of new postoperative cerebral ischemic lesions and the prevalence of postoperative cognitive impairment. Second, we assessed whether preoperative cerebral ischemic injury predicts the risk for cognitive dysfunction after off-pump and on-pump surgery.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Study Population
One hundred twenty patients between 40 and 80 years of age with stable angina pectoris and moderate or good left ventricular function were included in the study. The exclusion criteria were an ejection fraction of less than 0.30 or renal failure (serum creatinine concentration > 200 mmol/L). Surgery was performed in an operation theater with integrated angiography equipment to allow intraoperative left heart catheterization with coronary angiography. In the first 40 cases patients with significant lesions of the circumflex artery were excluded from the study because the table of the angiography system could not be tilted sideways to facilitate surgery on the posterior wall. In the last 80 cases, surgery was performed on a tiltable angiography table, and the anatomic location of a coronary stenosis was no longer an exclusion criteria. Patients were randomized in blocks of 20 to undergo on-pump or off-pump surgery after induction of anesthesia. All patients gave their written informed consent before admission to the study, which was approved (May 14, 1998) by the regional human research committee. Preoperative demographic, educational, and clinical characteristics are shown in Table 1.


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  		Table 1. Preoperative Demographic, Educational, and Clinical Characteristics
 
Operative Technique and Procedures
Surgery was elective in all cases and performed with balanced anesthesia using opiates and barbiturates together with inhalation anesthesia. Propofol was given at the end of the operation to allow early extubation. Four experienced surgeons performed all of the operations, and midline sternotomy was performed in all cases. All on-pump operations were performed in moderate general hypothermia (28° to 32°C) with topical cooling using ice slush. Cold St. Thomas's cardioplegic solution was also applied at the aortic root. Off-pump surgery was performed without cooling, cardiopulmonary bypass, and aortic cannulation. A partial aortic clamp was used for the proximal vein graft anastomoses in both groups. Left heart catheterization with coronary angiography was performed in all cases to check patency of the distal coronary anastomoses immediately after chest closure, and repeated again at the 3- and 12-month postoperative controls.

Neuroradiologic Assessment
One hundred nine (90.8%) of 120 patients had a preoperative cerebral MRI examination. Magnetic resonance imaging could not be performed in 11 (9.2%) patients because of claustrophobia in 8 patients and practical nonmedical reasons in 3 patients. Three months postoperatively a second cerebral MRI was assessed in 101 (84.2%) patients. One patient had died (the additional patient who died did not have a preoperative MRI), 2 patients had withdrawn from the study, and 5 patients refused a new MRI examination.

The aim of the preoperative cerebral MRI examination was to determine the presence and degree of cerebral ischemic lesions. These preoperative MRI examinations were assessed using a modified scale [20]: (1) normal (no cerebral lesions), (2) borderline (cerebral lesions with a diameter < 5 mm), and (3) pathologic (cerebral lesions with a diameter > 5 mm). The postoperative MRI examination was carried out to detect new cerebral lesions after surgery. The MRI criteria with regard to significant change from preoperative to postoperative were one or more new visible (>2 mm) cerebral lesions. The neuroradiologist was blinded to all clinical and neuropsychological data and to the operative procedure carried out.

All MRI examinations were performed on a 1.5-T scanner (Siemens Magnetom Vision; Siemens, Erlangen, Germany), using axial proton-density and T2-weighted turbospin-echo with 5-mm slice thickness and 1.5-mm slice intergap. The repetition time was 2,200 milliseconds and the echo time was 14 milliseconds for proton and 85 milliseconds for T2. Coronal fluid–attenuated inversion recovery was performed with 5-mm slice thickness and 1.5-mm slice intergap. The repetition time was 9,000 milliseconds and the echo time was 110 milliseconds.

Neuropsychological Assessment
All 120 patients were examined with an extensive neuropsychological test battery (Table 2) before surgery. The neuropsychological examinations took approximately 90 minutes. The neuropsychologist was blinded to all clinical and neuroradiologic data and to the operative procedure carried out.


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  		Table 2. Neuropsychological Test Battery
 
We report complete longitudinal neuropsychological test results from 106 (88.3%) patients who completed all three neuropsychological assessments. Two patients died within the first postoperative month, 2 patients withdrew from the study before the 3-month control, 6 patients refused a further neuropsychological examination after the initial preoperative examination, and 4 patients attended only one of the postoperative assessments owing to various practical nonmedical reasons. The demographic, educational, and clinical characteristics of the 106 patients did not differ significantly from the data reported in Table 1.

Six neuropsychological components were assessed by 10 different tests: motor coordination (Grooved Pegboard Test), psychomotor speed (Digit Symbol [WAIS-R], Trail Making Test), attention (Digit Span [WAIS-R], Stroop Color-Word Interference Test), verbal memory (Rey Auditory Verbal Learning Test, L and R), verbal comprehension and fluency (Similarities [WAIS-R], Controlled Oral Association Test [COWAT]), and visuoconstructive abilities (Block Design [WAIS-R]) [21–23]. Patients showing a greater than 20% decrease on at least two tests at the 3- or the 12-month control compared with the preoperative assessment were defined as cognitively impaired.

Statistical Analysis
Previous studies have defined a significant change in cognitive performance from baseline to follow-up as a 20% decrease or a reduction of one standard deviation on two or more tests, which equal an effect size of approximately d = 1.0. To detect changes with effect size in the range defined as medium to large (d = 0.7), power analysis showed that 50 patients were needed in each group when the significance level was set to {alpha} = 0.01 and statistical power to ß = 0.8. To tolerate a dropout rate of 20 patients from baseline to 12 months, the study was designed to recruit 60 patients in each group.

Spearman's rank order coefficient (two-tailed) was used to analyze nonparametric data. Differences between group means were tested using one-way analysis of variance. Differences in patient characteristics, neuropsychological performance, and neuroradiologic characteristics were compared using {chi}2 analysis and Student's t test. Neuropsychological performance was analyzed at group level in terms of differences in mean scores between the two operation groups. Repeated-measure analyses of variance with time of testing (preoperative and 3 and 12 months postoperatively) as the within-factor and operation group (off-pump versus on-pump) as the between-factor variables were performed for the 10 neuropsychological tests. The statistical significance level for analyses of neuropsychological data was set to p less than 0.01 to avoid false-positive findings (type I error); otherwise p less than 0.05 was used. All data were analyzed at an intention-to-treat basis keeping intraoperatively converted patients in the off-pump group. The statistical analyses were performed using SPSS 11.0 (Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Intraoperative Results
The mean ± standard deviation for the number of distal anastomoses was equal in the two groups (2.6 ± 0.9 off-pump versus 2.8 ± 1.0 on-pump, p = 0.21), but the mean ± standard deviation for the operation time was significantly longer in the off-pump group (192 ± 56 minutes off-pump versus 162 ± 45 minutes on-pump, p = 0.001). Seven (11.7%) of 60 off-pump patients were intraoperatively converted to on-pump surgery because of hemodynamic instability or angiographic findings during surgery.

Neuroradiology
The preoperative cerebral MRI examination showed normal findings in 21 (19.3%) patients, borderline findings in 40 (36.7%) patients, and pathologic findings in 48 (44.0%) patients. There was no significant difference with regard to the preoperative MRI classification between the two groups (p = 0.22).

The 3-month postoperative cerebral MRI examination revealed one or more new cerebral ischemic lesions in 13 (12.5%) of the 101 patients assessed: 4 of 49 patients (8.2%) in the off-pump and 9 of 52 (17.3%) in the on-pump group (p = 0.17). A detailed description of postoperative cerebral MRI findings is given in Table 3. There was no significant association between the degree of preoperative cerebral lesions and presence of new cerebral lesions at the 3-month assessment (p = 0.32).


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  		Table 3. Cerebral Magnetic Resonance Imaging Findings at the 3-Month Postoperative Assessment
 
Neuropsychology
Neuropsychological test performances for all neuropsychological assessments are shown in Table 4. No significant effect of the operative method used (off-pump versus on-pump) was seen for any of the measures. A significant effect of time was found for several test measures indicating improvement in performance for the three assessments. However, because no significant interaction effects between group and time were found, both off-pump and on-pump patients improved at the same rate.


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  		Table 4. Neuropsychological Test Performance With Mean and (Standard Deviation) Scores at the Preoperative (t1) and at the Three- (t2) and Twelve- (t3) Month Postoperative Assessments for On-Pump (n = 52) and Off-Pump (n = 54) Patients
 
There was no difference between off-pump and on-pump surgery with regard to postoperative cognitive impairment. At 3 months, 11 (20.4%) of 54 off-pump and 12 (23.1%) of 52 on-pump patients showed cognitive decline (p = 0.74), whereas 13 (24.1%) of 54 off-pump and 12 (23.1%) of 52 on-pump patients were impaired at 12 months (p = 0.90). The statistical consistency of this finding was of medium strength as only 10 (9.4%) patients, 5 off-pump and 5 on-pump, had by definition cognitive impairment at both postoperative controls. Thirteen patients improved from impaired status and 15 patients worsened to impaired status from the 3- to the 12-month control. Measures of psychomotor speed (Trail Making Test), verbal memory (RAVL-R), and verbal comprehension and fluency (COWAT) showed the largest incidence of impairment, but no effect with regard to operation group was seen.

There was no significant correlation between presence of new cerebral ischemic lesions at the 3-month postoperative MRI examination and change in neuropsychological performance from preoperative to 3 months postoperatively (n = 98, {rho} = 0.11, p = 0.29).

Impact of Preoperative Cerebral Magnetic Resonance Imaging Classification on Cognitive Outcome
The association between preoperative cerebral MRI classification and changes in neuropsychological performance from preoperation to 3 months postoperatively is shown in Table 5 for off-pump and in Table 6 for on-pump patients. The on-pump group showed a significant correlation between preoperative cerebral MRI findings and neuropsychological dysfunction (p = 0.02), but this was not the case for the off-pump group (p = 0.22).


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  		Table 5. Association Between Preoperative Cerebral Magnetic Resonance Imaging Classification and Neuropsychological Performance Three Months Postoperatively for Off-Pump Patients (n = 54)
 

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  		Table 6. Association Between Preoperative Cerebral Magnetic Resonance Imaging Classification and Neuropsychological Performance Three Months Postoperatively for On-Pump Patients (n = 54)
 
None of the patients with normal preoperative MRI findings were found to have cognitive impairment at 3 months postoperatively, whereas 20.0% of patients with borderline MRI findings and 27.1% of patients with pathologic MRI findings showed cognitive decline ({chi}2 = 6.6 [2 degrees of freedom], n = 108, p = 0.04).


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
This study found no difference between on-pump and off-pump coronary artery bypass grafting surgery with regard to MRI evidence of brain injury and prevalence of cognitive impairment at 3 and 12 months after surgery. The degree of cerebral ischemic injury found on the preoperative MRI examination was, however, a predictor for postoperative cognitive impairment for on-pump, but not for off-pump, patients. None of the patients with normal preoperative cerebral MRI findings were found to have cognitive impairment at 3 months postoperatively.

Cognitive dysfunction after coronary artery bypass grafting surgery has a multifactor pathophysiology including cerebral embolism, systemic inflammation, body temperature, and cerebral hemodynamics [24]. These pathophysiologic factors are, however, weighted differently for off-pump and on-pump surgery. Off-pump surgery reduces intraoperative cerebral embolization [6, 7], systemic inflammatory responses [25–27], and the degree of postoperative brain edema [28]. On the other hand, on-pump surgery is usually performed during moderate hypothermia, which may have a neuroprotective effect [29]. Cerebral blood flow is pulsatile during off-pump surgery, but cardiac output and cerebral perfusion pressure may vary significantly during some periods of off-pump surgery, which may subsequently lead to a reduction in cerebral perfusion pressure and neuronal ischemia.

Off-pump surgery may seem superior to on-pump surgery when intellectual skills are evaluated immediately after surgery [6, 10]. However, this finding may mainly be related to a transient delirium caused by reversible cerebral physiologic changes such as systemic inflammation and brain edema. Our long-term postoperative neuropsychological findings are in accordance with the multicenter study published by Van Dijk and colleagues [11], who did not find a difference in longitudinal cognitive outcome between the two methods during the first postoperative year. To date, however, studies comparing cognitive outcome after off-pump versus on-pump surgery have enrolled a middle-aged population without the highest degree of comorbidity. We can therefore not exclude the possibility that the off-pump technique may be less harmful for the brain in subgroups of patients undergoing revascularization surgery, in particular, elderly patients and those who have cerebrovascular disease or extensive generalized atherosclerosis [30].

The interpretation and comparison of neuropsychological findings from different cardiac surgery studies must be carried out with caution [31]. Divergence in methods, patient selection, and statistical criteria used for data analysis could give very different results with regard to the proportions of patients defined as cognitive impaired [32]. In our study, only 9.4% of patients were by definition cognitively impaired at both the 3- and 12-month postoperative assessments. A rather significant number of patients changed their status from impaired to nonimpaired or vice versa during this time, which demonstrates the dynamic pattern of neuropsychological test performances.

Most perioperative strokes during coronary artery bypass grafting surgery are embolic [33], and new postoperative cerebral MRI lesions most likely represent permanent ischemic brain injury caused by intraoperative emboli [34]. There was a nonsignificant trend that the patients undergoing on-pump surgery had a higher incidence and a higher number of postoperative cerebral ischemic lesions. Such lesions may be regarded as clinically silent embolic ischemic strokes, and can therefore be used as surrogate markers for assessment of stroke risk after different types of cardiovascular surgery. It is possible that a main clinical advantage of off-pump coronary artery bypass grafting surgery will be a significant reduction in the perioperative stroke incidence [35]. Our study population was, however, too small to assess stroke risk after off-pump compared with on-pump surgery.

The average age and the amount of comorbidity, cerebrovascular disease included, in patients undergoing cardiac surgery is increasing. The clear majority of preoperative cerebral MRI lesions found in these patients are probably attributable to (silent) cerebrovascular disease. Such lesions are associated with limited cognitive resources [36], which may make patients with a higher degree of lesions particularly vulnerable to further ischemic brain injury. An important finding in our study was the significant association between a normal preoperative cerebral MRI and the absence of cognitive dysfunction at 3 months postoperatively. Preoperative cerebral MRI findings may help to predict the risk for cognitive impairment, at least after on-pump surgery [18, 19].

A possible confounding factor with regard to the interpretation of this study is the fact that all patients, in addition to coronary artery bypass grafting surgery, also underwent left heart catheterization. Catheterization was performed intraoperatively, and at the 3- and 12-month postoperative controls, to assure the quality of the coronary anastomoses made and to evaluate graft patency [37]. We have recently reported that left heart catheterization may cause harm to the brain [38]. During catheterization there is a transport of both gaseous and solid microemboli to the brain, and 11.9% of patients in our recent study had new lesions on a diffusion-weighted cerebral MRI on the day after catheterization. The new postoperative cerebral MRI lesions in this present study may therefore partly be related to the catheterizations. However, the cerebral burden caused by cardiac catheterization was equal for both groups and should therefore not prevent a comparison of cerebral outcome after off-pump and on-pump surgery.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
The Norwegian Council on Cardiovascular Diseases supported Christian Lund, MD.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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M. Hamon, S. Gomes, C. Oppenheim, R. Morello, R. Sabatier, T. Lognone, G. Grollier, P. Courtheoux, and M. Hamon
Cerebral Microembolism During Cardiac Catheterization and Risk of Acute Brain Injury: A Prospective Diffusion-Weighted Magnetic Resonance Imaging Study
Stroke, August 1, 2006; 37(8): 2035 - 2038.
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