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Ann Thorac Surg 2003;76:765-770
© 2003 The Society of Thoracic Surgeons
a Department of Neurology, Oslo, Norway
b The Interventional Centre, Oslo, Norway
c Department of Thoracic and Cardiovascular Surgery, Oslo, Norway
d Department of Psychosomatic Medicine, Oslo, Norway
e Department of Radiology, Rikshospitalet University Hospital, Oslo, Norway
Accepted for publication April 3, 2003.
* Address reprint requests to Dr Lund, Department of Neurology, Rikshospitalet University Hospital, 0027 Oslo, Norway;
e-mail: christian.lund{at}rikshospitalet.no
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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METHODS: This was a prospective and randomized study of two comparable groups with regard to age, sex, years of education, preoperative cognitive functioning, and surgical characteristics. Fifty-two patients (29 off-pump) were monitored by the use of transcranial Doppler ultrasound for cerebral microembolization during surgery. Preoperative and postoperative clinical, cerebral magnetic resonance imaging, and neuropsychologic examinations were also carried out.
RESULTS: There was a significant reduction in the number of cerebral microemboli during off-pump compared with on-pump surgery (16.3 [range 0 to 131] versus 90.0 [range 15 to 274], p < 0.0001). No significant difference with regard to the incidence of neuropsychologic performance (decline in 29% off-pump, 35% on-pump) or neuroradiologic findings at 3 months was found, and there was no association between the number of cerebral microemboli and cognitive outcome.
CONCLUSIONS: This study clearly demonstrates that off-pump surgery leads to a reduction in intraoperative cerebral microembolization. A significant reduction in the number of off-pump patients with cognitive decline or ischemic brain lesions on cerebral magnetic resonance imaging could not be demonstrated in this relatively small patient population.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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There is a growing interest in performing coronary revascularization without the use of CPB (off-pump surgery). Furthermore, there is increasing evidence that suggests that off-pump surgery may be at least equal to on-pump surgery with regard to both in-hospital morbidity and cardiac outcome 1- to 3-years after surgery [6, 7]. It is still undecided, however, if off-pump surgery reduces the incidence of perioperative stroke and the risk for postoperative cognitive decline [8]. Preliminary studies, which have been mostly retrospective or unblinded, using transcranial Doppler (TCD) suggests that fewer microemboli may enter the brain during off-pump compared with on-pump surgery [9–12].
The main aim of this clinical study was to carry out a randomized and prospective comparison of off-pump and on-pump coronary artery bypass grafting with regard to intraoperative cerebral embolization. Preoperative and postoperative clinical neurologic and neuropsychologic tests and cerebral magnetic resonance imaging (MRI) examinations were also carried out.
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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In the off-pump group heparin (1 mg/kg per body weight) was administered during the internal mammarian artery mobilization and activated coagulation time was maintained above 250 seconds. The distal anastomoses were performed with the use of snares (Gore Tex 3-0; W.L. Gore & Associates, Flagstaff, AZ) and Octopus stabilizers (Medtronic Inc., Minneapolis, MN). In both groups, a partial aortic clamp was used for the proximal anastomoses. All patients had a coronary angiography to ascertain patency of the distal coronary anastomoses immediately after chest closure.
Doppler monitoring
Color Duplex examinations of the precerebral and major intracranial arteries were carried out preoperatively in all patients. All patients had varying degrees of carotid artery arteriosclerosis before surgery. Three patients (5.8%) had a unilateral internal carotid artery diameter reduction of 50% or more, 2 patients on the left and 1 patient on the right side. During the operation the left middle cerebral artery was insonated using TCD instrumentation (DWL, Sipplingen, Germany) and the reference gate technique. Unilateral insonation on the left side was used due to the need of an anastesiologic access on the right side. The dual-gate insonation depths were 55 and 40 mm, the sample volume 11 mm, filter setting 200 Hz, power 188 mW, and scale 150/120. A special fixation frame (DWL) was adjusted to ensure a stable probe fixation. TCD monitoring was continuously performed from incision of the pericardium until start of chest wall closing. Cerebral microemboli were identified on-line by a single observer and their time of occurrence was noted by direct visual observation of the various stages of the operation, which are illustrated in Table 2. The Doppler audio signal data were also recorded on-line with a digital audiotape (Tascam DA 38, Tokyo, Japan). When performing the off-line analysis, the Doppler audio signals were reintroduced into the Doppler system using the same instrumentation settings as those that were used during the recordings. An experienced observer who was blinded for all clinical data performed off-line identification of microembolic signals. The identification of microemboli was based upon standard criteria including only microembolic signals, which caused an increase in Doppler power of more than 6 dB above the background level [13].
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The neuroradiologist was blinded with regard to the patient’s clinical status and the operative procedure carried out. The cerebral MRI examinations were carried out on a 1.5 Tesla Siemens Magnetom Vision scanner (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 2200 ms, and the echo time was 14 ms for proton and 85 ms for T2. Coronal fluid attenuated inversion recovery was performed with 5-mm slice thickness and 1.5-mm slice intergap, the repetition time was 9000 ms, and the echo time was 110 ms.
Neuropsychologic tests
All 52 TCD monitored patients, apart from 1 patient who withdrew before the second examination, were assessed with an extensive neuropsychologic test battery 1-day before surgery (t1) and 3-months postoperatively (t2). The test battery included assessment of motor coordination (grooved pegboard test dominant and nondominant hand), psychomotor speed (digit symbol substitution test from the Wechsler Adult Intelligence Scale [WAIS-R], trail making test [parts A and B]), attention (digit span forward and backward from the WAIS-R, stroop color-word interference test), verbal learning and delayed recall (rey auditory verbal learning test [RAVLT]), verbal abstraction and fluency (similarities and vocabulary from the WAIS-R, controlled oral association test [COWAT]), and visuoconstructive abilities (picture completion and block design from the WAIS-R) [14], comprising a total of 12 measures. More than 20% reduction in score from t1 to t2 on at least 2 of the 12 variables was defined as cognitive impairment. A standardized total sum score assessing cognitive function across the selected 12 measures was computed.
Statistical methods
Comparison of group proportions for categoric data within fourfold tables were calculated with the Fisher’s exact test. Continuous nonparametric distributed variables were compared using the Mann-Whitney test and the Spearman r correlation coefficient, and continuous parametric data using the Student’s t test. The level of statistical significance was p 
0.05. The statistical analyses were performed using the SPSS program (Chicago, IL). The data are presented as mean values ± standard deviation (SD) or range.
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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There was no mortality. One ischemic stroke occurred in the on-pump group, this patient had a slight right-sided hemiparesis and dysphasia when he awoke after surgery. The preoperative color duplex had demonstrated an approximately 50% internal carotid artery diameter reduction on the left side and the postoperative MRI revealed a brain infarction in the left hemisphere. One hundred forty-nine microemboli were detected during this operation, which was performed without specific complications. The patient had completely recovered at 3 months. Four patients had a peripheral nerve injury postoperatively: the ulnar nerve in 3 patients, and an inguinal nerve in 1 patient.
Neuroradiologic findings
In the off-pump group all 24 patients had similar radiologic findings at t1 and t2, whereas in the on-pump group 2 patients had new white matter lesions and 1 patient a brain infarction at t2 (p = 0.09).
Neuropsychologic findings
Eight patients (29%) in the off-pump group and 8 patients (35%) in the on-pump group had a significant decline in their neuropsychologic test score from t1 to t2 (not significant [NS]). There was no significant correlation between the number of cerebral microemboli and the degree of neuropsychologic impairment in the two groups (r = 0.12). The 3 on-pump patients who had new cerebral MRI lesions did not differ from the total patient population with regard to neuropsychologic performance.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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Traditional on-pump surgery introduces several potential embolic sources and maneuvers that may cause microemboli [15–18]. During on-pump surgery aortic arch cannulation is performed before the CPB start with a sharp incision through the ascending aorta, which may contain considerable amounts of atherosclerosis. We found that there were always clusters of microemboli associated with cannulation. Aortic clamping and partial aortic clamping entail the use of firm mechanical force to the aorta that leads to microembolization to the cerebral circulation in the following few seconds. During CPB there were always cerebral microemboli that probably had their origin within the CPB circuit [19].
In contrast, off-pump surgery is performed without CPB and this limits the use of forceful surgical procedures on the aorta. Cerebral microemboli were normally infrequent during off-pump surgery except in close association with partial aortic declamping. However, in some patients, both during off-pump and on-pump surgery, numerous microemboli were detected at other times inbetween the main procedures. This occurred most often when the surgeons pushed or pulled at the aorta, which probably led to the detachment of atherosclerotic material.
Although there were significantly fewer emboli during off-pump surgery we could not, in this relatively small study population, demonstrate any significant difference in the incidence of neuropsychologic deficits 3-months postoperative. Neuropsychologic deficits were found in approximately 30% of patients in both the on-pump and the off-pump groups. There was also in the two groups no association between the number of microemboli and evidence of cognitive decline. Our study may, however, be too small to detect significant differences in neuropsychologic outcome. The benefit with regard to cognitive outcome using off-pump surgery is undecided. Taggart and coworkers [8] reported a pattern of early decline in cognitive function at discharge from hospital followed by some late recovery 3-months postoperatively, both for patients undergoing CABG with and without CPB. On the other hand, both Diegler and colleagues [11] and BhaskerRhao and associates [12] found evidence for better cognitive outcome during the first few days after off-pump compared with on-pump surgery. The neuropsychologic assessments in these studies were, however, limited and follow-up after discharge from hospital was not carried out.
Confirmation of our neuropsychologic findings in a larger patient population would strongly suggest that postoperative neuropsychologic impairment following CABG is not totally dependent on the total number of intraoperative cerebral microemboli. However, the clinical consequences of cerebral microemboli may depend more on their composition rather than on their total number. Cerebral microemboli detected during cardiac surgery may be either gaseous or solid. Solid microemboli introduced into the cerebral circulation during surgery may be composed of atherosclerotic material, platelet aggregates or soft fat-containing particles. Small gas bubbles are probably less dangerous for the brain than solid emboli. We have previously introduced air-filled ultrasound contrast agents and increasing amounts of air into the cerebral circulation in an experimental rat model without finding signs of injury to the cerebral microcirculation or cerebral microinfarction at autopsy [20]. On the other hand, a brain necropsy study in 36 patients who died within 3-weeks after cardiac valve repair surgery or traditional CPB bypass surgery revealed that thousands of microemboli were found in the cerebral arterioles and capillaries in all patients [21]. In this study, an increasing CPB time was associated with evidence of an increasing cerebral embolic load. To date TCD monitoring during cardiac surgery has not provided information regarding the composition and size of microemboli. This should be possible in the future using multifrequency Doppler, which can differentiate microemboli into solid and gaseous [22, 23]. Microemboli that cause relative increases in Doppler power of 14 dB in the middle cerebral artery are, as an example, commonly found during cardiac surgery. Theoretical calculations using an assumed middle cerebral artery diameter of 3 mm and an axial sample volume of 10 mm suggest that this Doppler power increase may be due to a gas bubble that is 4 µm in diameter or a solid microembolus of 130 µm. A 4-µm gas bubble should normally pass through the cerebral microcirculation (7 to 10 µm), whereas this may seem more difficult for a 130-µm solid microembolus [23].
Cerebral microemboli detected during cardiac surgery before any incision through any artery are most probably solid. The majority of the microembolic signals, which appear during the first seconds after aortic arch cannulation, may be due to small air bubbles, which are introduced into the arterial lumen, or solid atherosclerotic particles, which are mechanically detached by the cannula. The microemboli that are associated with aortic arch clamping are probably solid as they appear in the first seconds after a rough nonpenetrating mechanical force has been applied to the aorta.
Intraoperative cerebral microembolization is not the only pathophysiologic factor which may be implicated as a cause of brain injury during cardiac surgery. In on-pump surgery systemic inflammation is induced due to the heart-lung machine [24] and brain metabolism is changed due to anesthesia. Furthermore, the cerebral blood flow pattern may be severely changed during both on-pump and off-pump surgery. During CPB, cerebral perfusion is nonpulsatile with delivery of a fixed flow rate by the artificial bypass pump. Nonpulsatile cerebral perfusion may lead to a diffuse brain edema, which may be avoided by using the off-pump technique where cerebral perfusion is pulsatile [25].
Theoretically, the normal pulsatile cerebral blood flow pattern present during off-pump surgery should be advantageous for the brain. In off-pump surgery, however, manual cardiac manipulation during the grafting stage causes intermittent reductions in cardiac output and cerebral perfusion pressure with the risk of significant cerebral hypoxia. Intraoperative ventricular arrhythmias also represent a special danger for the brain during off-pump surgery due to lack of a "back-up" circulation system. We have previously reported that such intraoperative ventricular arrhythmias may cause complete cessation of cerebral circulation [26]. Caplan and Hennerici [27] have also suggested that cerebral microemboli may be potentially more dangerous when cerebral perfusion pressure is too low to wash microemboli through the microvasculature. Therefore, it is possible that sudden reductions and continuous variations in cerebral perfusion pressure and cerebral oxygenation during off-pump surgery may at least partly explain why we found similar cognitive outcomes after off-pump and on-pump surgery.
In this study of 52 operations we found that only 1 patient experienced an ischemic stroke in the immediate postoperative period. This on-pump patient, and 2 additional on-pump patients, were the only who had new white matter lesions on the cerebral MRI examination 3-months after the operation. The number of ischemic lesions may have been higher if diffusion-weighted MRI examinations had been performed during the first postoperative days [28].
In conclusion, this study has clearly demonstrated that there are significantly fewer cerebral microemboli during off-pump compared with on-pump CABG. This reduction is due to the fact that CPB and a number of operative procedures on the ascending aorta are avoided during off-pump surgery. We could not in this small population find a difference between the two methods with regard to cognitive outcome assessed at 3-months postoperatively.
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J. J. Ferguson If There's Smoke, Is There Fire? Circulation, March 30, 2004; 109(12): 1442 - 1444. [Full Text] [PDF]
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