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J Thorac Cardiovasc Surg 2001;121:1150-1160
© 2001 The American Association for Thoracic Surgery
Cardiopulmonary Support and Physiology |
From the Department of Surgery, South Manchester University Hospitals, Manchester, United Kingdom.
This work was funded by the British Heart Foundation.
Received for publication April 4, 2000. Revisions requested Aug 24, 2000; revisions received Nov 1, 2000. Accepted for publication Jan 5, 2001. Address for reprints: S. J. Fearn, PhD, FRCS, Research Fellow, Department of Surgery, University Hospital of South Manchester, Nell Lane, West Didsbury, Manchester, M20 2LR, United Kingdom (E-mail: cnmcc{at}fs1.with.man.ac.uk).
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsDiscussionConclusionReferences |
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsDiscussionConclusionReferences |
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1,2 Although most deficits resolve within 6 weeks to 6 months, up to 35% persist as a source of disability for at least 12 months, with important social and economic implications. 2,3
The debate over etiology has raged for years, with intraoperative emboli arising from the cardiopulmonary bypass circuit and cerebral hypoperfusion both being implicated. 4,5 The influence of cerebral vascular disease is suggested to be important. 6,7 Emboli have been demonstrated in the retina of survivors and in the brain at postmortem examination. 8,9 Larger numbers of emboli detected by ultrasound of the carotid arteries or transcranial Doppler (TCD) studies are associated with neurologic and cognitive complications and longer inpatient stay. 10-12
The synchronous measurement of cerebral flow and emboli to the brain in patients undergoing cardiac surgery has not been attempted before, and the role of impaired cerebrovascular reserve is unclear. Our aim was to investigate the influence of preoperative cerebrovascular reserve and intraoperative cerebral perfusion and embolization on cognitive function after CABG.
We used TCD to measure blood flow velocity bilaterally in the middle cerebral arteries (MCAs) because it is the only continuous means of measuring changes in cerebral hemodynamics noninvasively and has become an essential part of neurologic monitoring. 13 A close relationship between changes in cerebral blood flow and changes in blood flow velocity as measured by TCD has been demonstrated in patients with symptoms suggesting cerebrovascular disease and in patients during cardiac surgery. 14-16 TCD can also be used to monitor embolization to the cerebral circulation using software that distinguishes between Doppler signal, noise, probe artifact, and embolic or high-intensity transient signals.
"Embolic signals" must fulfil the following criteria 17:
We used near-infrared oxygen spectroscopy to measure regional oxygen saturation noninvasively because systemic saturation is a poor indicator of cerebral saturation. 18 The use of near-infrared oxygen spectroscopy during cardiopulmonary bypass has been criticized because of factors that may differentially influence the extracranial circulation. For this reason we used probe separation distances of 30 and 40 mm from the light source to enable subtraction of the extracranial component from that reflecting saturation predominantly in the brain. When the probe is sited over MCA territory, regional changes in oxygen extraction correlate well with TCD of MCA blood flow velocity as well as jugular venous saturation but are not subject to interindividual differences in cerebral venous anatomy. 19,20 The other advantage of near-infrared oxygen spectroscopy is that it does not require a pulse wave and therefore is the only means of monitoring during nonpulsatile perfusion.
In this study, we wanted to compare the change in MCA blood flow velocity and regional cerebral oxygen saturation (CsO2) with the change in cognitive function and also to investigate the influence of embolization on cognitive change.
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsDiscussionConclusionReferences |
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Urology control subjects
Nineteen patients admitted for urologic procedures formed a control group of elderly patients undergoing general anesthesia without cardiopulmonary bypass. Exclusion criteria were a diagnosis of cancer, previous stroke or neurologic disease, or an inability to perform the cognitive test battery.
Cerebrovascular disease
Duplex Doppler imaging of the carotid arteries was carried out by an experienced vascular technologist using spectral waveform analysis to measure the severity of common or internal carotid stenosis. TCD insonation of right and left MCAs was used to determine cerebrovascular reactivity to inhaled carbon dioxide preoperatively using a standard technique that measures the change in mean MCA blood flow velocity before and after a standard period of carbon dioxide inhalation for each side. 21 A normal cerebrovascular reactivity was more than 0.86.
Patient-reported outcome
Subjective outcome was assessed with the use of the Short Form 36 (SF-36) produced and validated by the Medical Outcomes Trust. 22,23 This was completed by each patient before the operation and 2 and 6 months after the operation.
Neurologic examination
Neurologic examination according to the National Institutes of Health Stroke Scale (NIHSS) was also performed before the operation and 1 week and 2 and 6 months postoperatively. 24
Anesthesia
Drugs used and their doses per kilogram of body weight were standardized for premedication, induction, maintenance, during and after bypass, and during intensive care. Alpha-stat management of pH was used in all patients. Heart rate, mean arterial blood pressure (MAP), nasopharyngeal temperature, and end-tidal carbon dioxide were recorded every 5 minutes during the entire procedure. Hematocrit values and arterial blood gases were analyzed every 30 minutes during the operations.
Cardiopulmonary bypass
CABG was performed with the use of 32°C hypothermia, with full-flow nonpulsatile bypass (2.4 L · min–1 · m–2 multiplied by the surface area of the patient) and a standardized circuit incorporating a membrane oxygenator and 40-µm arterial filter. Aortic root palpation was not performed and cannulas were inserted in standard locations.
Cerebral perfusion
TCD
MCA blood flow velocity was recorded bilaterally with TCD (Neuroguard CDS; Nicolet Biomedical Inc, Madison, Wis) at the following settings: gain of 8 dB, a range of 10 dB, and high-pass filter 75 kHz. Transducers were immobilized throughout the operations with a head ring.
CsO2
Regional CsO2 was measured with reflected near-infrared light spectroscopy (Somanetics Corporation, Troy, Mich). 19 So that extracranial contribution could be eliminated, the oximeter comprised two detectors separated from the near-infrared emitter by 30 and 40 mm. Light entering the nearer receiver was subtracted from that entering the farther receiver to give a saturation predominantly reflecting that in the brain. Because cerebral blood is 75% to 80% venous, CsO2 is a measure of oxygen saturation. The sensors were positioned over the parietal scalp after patches of hair had been shaved to improve correspondence between flow and saturation in the MCA territory. 19,20
Measures of cerebral perfusion were recorded manually for each side at 5-minute intervals during the operation for each patient. Extra recordings were taken for each operative event (seeTable II) if the event did not fall at a recording time point.
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Cognitive function testing
As much as possible, we based the measurement of cognitive function on the criteria set down in The Statement of Consensus on Assessment of Neurobehavioral Outcomes After Cardiac Surgery. 25 A standardized, comprehensive, and computerized battery of tests produced and validated by Cognitive Drug Research Ltd (Reading, United Kingdom) was used. 26,27 Patients were examined in a controlled environment free from distractions and were supervised by a trained assessor. They were asked to respond to visual stimuli on a screen by pressing either a "yes" or a "no" button. To minimize the practice effect, patients were allowed to familiarize themselves with the equipment in a practice test. The following cognitive function tests were performed in all patients and control subjects:
Parallel forms of words and pictures were used so that new stimuli were presented at each sitting. The results were analyzed in terms of both reaction time and accuracy except for simple reaction time, which has no accuracy component. An improvement in a reaction time variable would be manifest as a shorter time (a decrease), whereas an improvement in an accuracy variable would be manifest as an increase in sensitivity. Data were recorded directly onto a floppy disk and then manipulated by computerized statistics software (SPSS for Windows; SPSS, Inc, Chicago, Ill). The majority of the data were not normally distributed. Therefore, nonparametric analysis was used: Mann-Whitney U test, Wilcoxon signed ranks, and Spearman correlation. By analyzing the change in cognitive function over time, we standardized for the influence of intelligence and education. There is no accepted standard for the analysis of cognitive function variables. We avoided using an absolute change as a definition of significant decline in cognitive function for the following reasons:
Cognitive function was assessed preoperatively and then postoperatively at 1, 8, and 24 weeks.
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Results |
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TopAbstractIntroductionPatients and methodsResultsDiscussionConclusionReferences |
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Patients
Seventy patients were studied, but 5 were excluded from analysis because monitoring equipment was not available or could not be applied at the time of the operation. One patient was excluded from subsequent cognitive function analysis because he underwent combined carotid endarterectomy and CABG for symptomatic internal carotid artery stenosis (>70%). The mean age of the study patients was 60 years (range 43-77 years), and 53 (81.5%) were men. The median left ventricular ejection fraction was 60% (interquartile range [IQR] 50%-69.5%), and 88% were right-handed.
Nine patients had symptoms of cerebrovascular disease (transient ischemic attack, stroke, amaurosis fugax) and 10 had more than 70% stenosis or occlusion of one or both internal carotid arteries. The only patient with symptoms and more than 70% carotid stenosis was the one offered simultaneous carotid endarterectomy and CABG.
Cerebrovascular reactivity to inhaled carbon dioxide could not be measured in 3 patients who were unable to tolerate the nose clip and mouthpiece. Only 30% of patients had bilateral normal cerebrovascular reactivity(Fig 1), indicating a high incidence of occult cerebrovascular disease.
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Immediate postoperative outcome
Median (IQR) duration of ventilation was 9 hours (5-17 hours), duration of intensive treatment unit stay 22 hours (19-25 hours), and inpatient stay 9 days (8-10 days). Two patients died of multiorgan failure, 1 had a frontal stroke, 2 had transient neurologic deficits, and the patient who had combined carotid and CABG surgery had diffuse embolic brain injury on declamping after carotid endarterectomy.
Cerebral perfusion
MCA blood flow
Mean values for MAP, MCA blood flow velocity, and CsO2 bilaterally were calculated before and during bypass for each patient by means of an area-under-the-curve method(Table I, Figs 2 and 3).
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) and then tended to rise as a consequence of progressive systemic vasoconstriction during nonpulsatile perfusion. Peak MCA blood flow velocity fell to mean flow levels as nonpulsatile perfusion was established. Despite the fall in MAP, however, mean MCA flow velocity rose significantly by a median of 6 cm/s on bypass compared with prebypass levels (P < .0001, Wilcoxon,Fig 2). Like MAP, mean MCA blood flow velocity increased with temperature as the patient was rewarmed. In 49 (75%) patients, blood flow velocities to each cerebral hemisphere were within 5 cm/s of each other during bypass.
Asymmetry of flow in the other 16 patients was not related to significant internal carotid artery stenosis.
CsO2
During bypass, regional CsO2 fell significantly by a median (IQR) of 10% to 11% (6%-15%), depending on hemisphere, suggesting an increase in oxygen extraction despite cooling (P < .0001, Wilcoxon,Fig 3). It also tended to recover with rewarming. The falls in CsO2 were large and at the threshold for shunting after crossclamping of the internal carotid artery during carotid endarterectomy. 18
Cerebral emboli
More than half (57%) the patients had more than 200 emboli entering the cerebral circulation during surgery as detected by TCD. Most occurred when bypass was initiated and when the heart was defibrillated at the end of bypass, although readjustment of clamps and aortic cannulation also caused large numbers(Table II). Six patients were predisposed to thrombosis on preoperative serum sampling: two heterozygous for prothrombin gene variant alone, two heterozygous for factor V Leiden alone, one heterozygous for factor V Leiden with low protein C and S, and one with only a low protein C. These patients had more emboli than those with no increased tendency to thrombosis (median of 225 compared with median of 136), although the difference was not statistically significant. The patient who had multiple emboli during combined CABG/carotid surgery had factor V Leiden and deficiencies in both protein C and S.
NIHSS scores
The left-handed patient who had a left frontal stroke had no focal signs but an NIHSS of 3. The patient having combined carotid/coronary surgery had an NIHSS of 6 on the 20th postoperative day when he could be assessed neurologically as sedation was discontinued. NIHSS was normal in both these patients by 6 months.
Patient-reported outcome
SF-36 scores for all measures of vitality, physical health, and emotional role were low before the operation(Table III). All patient-reported outcome scores were significantly improved 2 months after the operation. By 6 months most scores had improved from the 2-month assessment except the mental health and general health scores, which showed little change. When compared with preoperative responses, the improvement at 6 months was statistically significant for all measures.
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Cognitive function
Control subjects
One week after the operation, the urology control subjects were significantly faster at all tests, although accuracy was unchanged. There was little change in most cognitive tests at 2 months compared with preoperative results, although accuracy of picture recognition was significantly worse (P = .02) and overall memory and reaction times were significantly better (P = .02 and .008,Table IV).
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For the CABG group as a whole, the patients' performance deteriorated significantly in most tests of cognitive function 1 week postoperatively; reaction times were slower and accuracy was reduced(Table V). The exceptions were memory tests, accuracy of choice reaction time, and word recognition reaction time. These deteriorations in memory may not be statistically significant, but the results are poor when compared with those of the urology control patients, who showed a significant improvement in memory at 1 week as a consequence of learning.
CABG group—two months postoperatively
When questioned directly, 18 patients reported having difficulties with memory, concentration, or attention. However, on formal testing there was a significant improvement in 11 cognitive variables compared with preoperative values(Table V).
CABG group—six months postoperatively
One patient died of intracranial hemorrhage before the 6-month assessment. On direct questioning, 17 patients were still having difficulty with memory, attention, and concentration. On cognitive testing, however, there was still a general trend toward improvement(Table V). Patients were significantly better than preoperatively at 7 cognitive tests but were still worse than preoperatively in the following tests: choice reaction time, accuracy of word, speed of picture recognition, and overall accuracy.
Relationships between flow and emboli and specific cognitive dysfunction
Attention, flow, and pressure
We examined the relationship between cerebrovascular reactivity (as a measure of the ability to increase flow in times of stress), MAP during bypass, MCA blood flow velocity, and changes in sustained attention as measured by number vigilance.
We found a significant positive correlation between the accuracy of number vigilance and cerebrovascular reactivity, suggesting that the worse the cerebrovascular reactivity preoperatively, the larger the deterioration in accuracy with more false positive errors being made (r = 0.3, P = .01 for both right- and left-sided cerebrovascular reactivity,Fig 4).
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Low flow in both MCAs during bypass caused greater deteriorations in accuracy of sustained attention and a higher number of false positive errors (r = 0.3) for both cerebral hemispheres separately (P < .05, Spearman).
Memory and emboli
We examined the relationship between the number of embolic signals detected in the MCA during surgery and memory tests. We found a direct correlation between the number of emboli and the deterioration in accuracy of memory (r = 0.3, P < .005 for the right hemisphere and r = 0.4, P = .001 for the left, Spearman,Fig 5).
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Those patients with more emboli to the left (and probably dominant) hemisphere did worse in 9 of 14 cognitive tests than did those with more emboli to the right MCA territory. The differences were greatest for memory tests and overall reaction time, although none of the differences was statistically significant.
Likewise, those patients with relatively greater flow to the left MCA territory than the right during bypass had greater deteriorations in a greater number of tests than those with equal hemispheric flow or more flow to the right, although these differences did not reach statistical significance.
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Discussion |
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TopAbstractIntroductionPatients and methodsResultsDiscussionConclusionReferences |
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6,28,29 The incidence of stroke in this study was low, and NIHSS scores did not prove useful. However, cognitive deficits were almost universal after CABG surgery and were emphasized when compared with the improvements seen 1 week after urologic surgery, which suggests a practice effect. It was unfortunate that we were unable to age- and education-match our control population selected to represent an elderly population undergoing general anesthesia without the risk of cerebrovascular injury, as occurs in patients undergoing orthopedic or vascular procedures, where cerebral embolization is recognized.
These deficits were transient for most cognitive tests, improving by 2 months postoperatively, although deficits were still present at 6 months. Newman and associates 2 described resolution of deficits within 6 weeks to 6 months of surgery, although others describe persistent deficits for at least 12 months. 3 In this study, the recovery of most cognitive function at 2 months was accompanied by an improvement in general well-being reported by patients using the SF-36 questionnaire. These improvements were in physical health, vitality, social functioning, and mental health, and it may be that cognitive function plays an important part in subjective outcome after surgery. The lack of correlation between cognitive outcome and patient-reported health status is not new and reflects the difficulties encountered when comparing objective and subjective measurements. 30
Cognitive deficits after cardiac surgery are similar to those occurring with aging 31: attention, concentration, memory, and speed of response were the areas most affected. 30 The right hemisphere appears to be more vulnerable than the left as the brachiocephalic artery has a more direct origin from the aortic arch, which may predispose to the capturing of emboli from the heart or CABG circuit. 32,33 However, greater cognitive disability occurs if flow is impaired or embolic load is greater to the left (and usually dominant) hemisphere.
Although lesion analysis suggests that specific areas of the brain relate to specific functions, there is still considerable overlap when cognitive pathways are being mapped. Impaired MCA flow in our study related to a subsequent inability to perform cognitive tests requiring attention. The vulnerable areas of the brain in hypoperfusion are the watershed areas at the junction of the major cerebral arterial territories. However, emboli may cause a more diffuse injury to relatively well-perfused brain and appear to relate to subsequent inability to perform memory tests. The relationship between handedness and cerebral dominance is not entirely clear but is improving with functional magnetic resonance imaging. 34 A separate analysis with respect to handedness was not possible because of the small number of left-handed patients.
During cardiopulmonary bypass, MAP was low at only 55 mm Hg. Perioperative hypotension is associated with an increased incidence of neurologic complications, especially if below 40 mm Hg. 35,36 However, a recent retrospective study failed to detect any difference between those patients receiving perfusion above 65 mm Hg or those below. 37 None of these studies has addressed changes in cognitive function. In patients with significant carotid disease, it is generally thought better to maintain MAP above 50 mm Hg during bypass 38; however, there are no controlled prospective studies to support this.
Mean MCA blood flow velocity fell with temperature as bypass was established, implying preservation of autoregulation. 39 MCA flow rose during bypass, implying increased vascular tone from nonpulsatile perfusion similar to that occurring in the systemic circulation. 40 MCA flow was not infrequently greater to one hemisphere than the other. Inasmuch as this did not relate to the side of severity of carotid artery stenosis, it may relate to directed flow from the aortic cannula during bypass.
Falls in regional CsO2 on cardiopulmonary bypass were substantially greater than those during internal carotid crossclamping for carotid endarterectomy, where a 10% fall is considered sufficient to justify the insertion of a shunt. 19,20 If cerebral perfusion was adequate during bypass, one would not expect a fall in CsO2, especially because oxygen extraction should fall due to cooling. It is generally thought that rewarming increases metabolism and hence oxygen requirements. The rise in CsO2 to above preoperative levels when CABG patients were rewarmed suggests a state of luxury perfusion that may be a response to previous hypoxia where blood flow exceeds the oxygen requirements for some hours after ischemia. 41
The prevalence of cerebrovascular symptoms was high and matched by the substantial proportion of patients (70%) with impaired cerebrovascular reactivity to inhaled carbon dioxide. These patients are less able to cope with the abnormal flow and cerebral perfusion pressures during cardiopulmonary bypass.
A substantial number of cerebral emboli were produced on establishing cardiopulmonary bypass and on defibrillation after bypass. Although TCD cannot clearly differentiate between gas and solid emboli, emboli produced at certain times, such as aortic clamping, are likely to be particulate. These were associated with poorer memory, especially if the left cerebral hemisphere was involved. This suggests that long-term repetitive emboli may be a cause of vascular dementia. In the Western world, vascular dementia is second only to Alzheimer disease as the leading cause of cognitive impairment and is the only preventable cause. 42,43 No systematic attempt has been made to correlate focal lesions with specific brain dysfunctions in multi-infarct dementia. 44
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Conclusion |
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TopAbstractIntroductionPatients and methodsResultsDiscussionConclusionReferences |
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Acknowledgments |
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References |
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TopAbstractIntroductionPatients and methodsResultsDiscussionConclusionReferences |
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 B. S. Silbert, P. Maruff, L. A. Evered, D. A. Scott, M. Kalpokas, K. J. Martin, M. S. Lewis, and P. S. Myles Detection of cognitive decline after coronary surgery: a comparison of computerized and conventional tests Br. J. Anaesth., June 1, 2004; 92(6): 814 - 820. [Abstract] [Full Text] [PDF]
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S. C. Knipp, N. Matatko, H. Wilhelm, M. Schlamann, P. Massoudy, M. Forsting, H. C. Diener, and H. Jakob Evaluation of brain injury after coronary artery bypass grafting. A prospective study using neuropsychological assessment and diffusion-weighted magnetic resonance imaging Eur J Cardiothorac Surg, May 1, 2004; 25(5): 791 - 800. [Abstract] [Full Text] [PDF]
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D. C. Whitaker, S. P. Newman, J. Stygall, C. Hope-Wynne, M. J. G. Harrison, and R. K. Walesby The effect of leucocyte-depleting arterial line filters on cerebral microemboli and neuropsychological outcome following coronary artery bypass surgery Eur J Cardiothorac Surg, February 1, 2004; 25(2): 267 - 274. [Abstract] [Full Text] [PDF]
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K. G. Engstrom Contaminating fat in pericardial suction blood: a clinical, technical and scientific challenge Perfusion, January 1, 2004; 19(1_suppl): S21 - S31. [Abstract] [PDF]
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C. W. Hogue Jr, R. Lillie, T. Hershey, S. Birge, A. M. Nassief, B. Thomas, and K. E. Freedland Gender influence on cognitive function after cardiac operation Ann. Thorac. Surg., October 1, 2003; 76(4): 1119 - 1125. [Abstract] [Full Text] [PDF]
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D. L. Ngaage Off-pump coronary artery bypass grafting: the myth, the logic and the science Eur J Cardiothorac Surg, October 1, 2003; 24(4): 557 - 570. [Abstract] [Full Text] [PDF]
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A. E. Jewell, E. F. Akowuah, S. K. Suvarna, P. Braidley, D. Hopkinson, and G. Cooper A prospective randomised comparison of cardiotomy suction and cell saver for recycling shed blood during cardiac surgery Eur J Cardiothorac Surg, April 1, 2003; 23(4): 633 - 636. [Abstract] [Full Text] [PDF]
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D. J. Cook, T. A. Orszulak, K. J. Zehr, N. A. Nussmeier, J. J. Livesay, J. W. Hammon, and X. Chen Effectiveness of the Cobra aortic catheter for dual-temperature management during adult cardiac surgery J. Thorac. Cardiovasc. Surg., February 1, 2003; 125(2): 378 - 384. [Abstract] [Full Text] [PDF]
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K. G. Engstrom The embolic potential of liquid fat in pericardial suction blood, and its elimination Perfusion, January 1, 2003; 18(1_suppl): 69 - 74. [Abstract] [PDF]
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F. Merkle, W. Bottcher, and R. Hetzer Prebypass filtration of cardiopulmonary bypass circuits: an outdated technique? Perfusion, January 1, 2003; 18(1_suppl): 81 - 88. [Abstract] [PDF]
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P. Bergman, L. Hadjinikolaou, and J. van der Linden Aortic atheroma is related to number of particulates captured by intra-aortic filtration in CABG Eur J Cardiothorac Surg, October 1, 2002; 22(4): 539 - 544. [Abstract] [Full Text] [PDF]
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M. Swaminathan, B. J. McCreath, B. G. Phillips-Bute, M. F. Newman, J. P. Mathew, P. K. Smith, J. A. Blumenthal, and M. Stafford-Smith Serum Creatinine Patterns in Coronary Bypass Surgery Patients With and Without Postoperative Cognitive Dysfunction Anesth. Analg., July 1, 2002; 95(1): 1 - 8. [Abstract] [Full Text] [PDF]
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S. J. Fearn, R. Pole, M. Burgess, S. G. Ray, T. L. Hooper, and C. N. McCollum Cerebral embolisation during modern cardiopulmonary bypass Eur J Cardiothorac Surg, December 1, 2001; 20(6): 1163 - 1167. [Abstract] [Full Text] [PDF]
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