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CARDIOVASCULAR ANESTHESIA

Jugular Bulb Oxyhemoglobin Desaturation, S100ß, and Neurologic and Cognitive Outcomes After Coronary Artery Surgery

Michael J. A. Robson, MB ChB, FRCA^*, R. Peter Alston, MD FRCA, Ian J. Deary, PhD FRCPE, Peter J. D. Andrews, MD FRCA^||, and Michael J. Souter, MB ChB, FRCA^¶

*Department of Anaesthesia, St. Vincent’s Hospital, Melbourne, Australia; Anaesthesia, Critical Care and Pain Medicine Section, Department of Clinical and Surgical Sciences, University of Edinburgh; Department of Anaesthesia, Royal Infirmary of Edinburgh, Scotland; Department of Psychology, University of Edinburgh, Scotland; ||Department of Anaesthesia, Western General Hospital, Edinburgh, Scotland; and ¶Department of Neuroanaesthesia, Southern General Hospital, Glasgow, Scotland

Address correspondence and reprint requests to M. J. A. Robson, Department of Anaesthesia, St. Vincent’s Hospital, Melbourne, 41 Victoria Parade, Fitzroy, Victoria 3065, Australia. Address e-mail to mjarobson{at}hotmail.com

	Abstract

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We reported that a decline in cognitive performance 3 mo after coronary artery bypass grafting surgery is associated with palpable aortic atheroma, but not postoperative jugular bulb oxyhemoglobin saturation (SjO₂) <50%. However, the effect of SjO₂ on clinical neurologic findings is not known. S100ß is a possible surrogate biochemical marker of brain injury, and we report here the scored clinical neurologic findings in 98 patients from our previous study in relation to SjO₂, cognitive performance, aortic atheroma, and S100ß. Patients underwent a scored neurologic examination and cognitive assessment the day before and 3 mo after coronary artery bypass grafting surgery. Intraoperatively, intermittent blood sampling was performed, and postoperatively, the area under the curve describing SjO₂ <50% in relation to time was calculated from continuous jugular bulb reflectance oximetry. Palpation was used to assess the ascending aorta for the presence of atheroma. The jugular bulb concentration of S100ß was measured 6 h after completion of surgery. The neurologic score 3 mo after surgery did not correlate with either intra- or postoperative SjO₂ (r = 0.111, P = 0.278; and r = -0.074, P = 0.467, respectively). The main determinant of neurologic score at 3 mo was the preoperative neurologic score (r² = 0.63, P < 0.001), whereas palpable atheroma of the ascending aorta made a small but significant contribution (r² = 0.034, P = 0.004). Neurologic and cognitive scores correlated before surgery (r = 0.226, P = 0.022) and at 3 mo after surgery (r = 0.348, P < 0.001). A preoperative neurologic deficit of two or more had a small but significant negative effect on cognitive performance at 3 mo (standardized ß = -0.097, P = 0.018). There was a significant univariate correlation between S100ß and the 3-mo neurologic score (r = -0.232, P < 0.05), but not a multivariate correlation (ß = -0.090, P = 0.156).

IMPLICATIONS: Intraoperative jugular bulb oxyhemoglobin saturation (SjO₂) and postoperative SjO₂ <50% do not have an important influence on long-term neurologic outcome after coronary artery bypass graft surgery. Subtle preoperative neurology is associated with long-term cognitive decline, and aortic atheroma is a risk factor for both cognitive and neurologic decline.

	Introduction

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Overt neurologic signs, such as stroke, coma, and encephalopathy, are uncommon after coronary artery bypass grafting (CABG) surgery; they occur in 0%–5% of patients (1–5). In contrast, subtle neurologic signs, such as primitive reflexes, ataxia, and visual changes, are often detected before and after CABG surgery (3). The Western Perioperative Neurologic Scale provides a reproducible method of quantifying these signs (5). Brain injury after CABG surgery may also be assessed by cognitive performance (2,5). However, it is unknown whether cognitive and neurologic outcomes after CABG surgery are related.

A biochemical marker that is released only by injured brain cells would be valuable and less resource intensive for investigating patients who are unwilling or unable to complete neurologic examinations and cognitive testing. The S100ß protein, which is prognostic of outcome after stroke, head injury, and global cerebral ischemia, has the potential to be such a marker (6,7). The appropriate time to measure S100ß after CABG surgery for prognostic value has not been established but is probably >5 h after surgery (8). However, the relationship between long-term neurologic outcome, such as a scored neurologic examination 3 mo after CABG surgery, and postoperative concentrations of S100ß is unknown.

The etiology of brain injury after CABG surgery is most likely to be multifactorial and to include cerebral hypoperfusion (9,10). Jugular bulb oxyhemoglobin desaturation (SjO₂) <50% is an estimate of cerebral hypoperfusion, and its occurrence during the rewarming phase of cardiopulmonary bypass (CPB) is associated with early cognitive decline when it is assessed 4–8 days after CABG surgery (11). We have found that SjO₂ <50% occurs frequently and often for more prolonged periods during the early postoperative period than during surgery (12,13). Therefore, if some brain damage results from SjO₂ <50% during CPB (11), then the greater intensity after surgery may consequently cause more damage. Although we have been unable to find an association with long-term cognition, the influence of postoperative SjO₂ <50% on long-term neurologic outcome is unknown (14).

We have found evidence of cerebral hypoperfusion not only with aerobic estimates, but also with anaerobic and combination estimates (13,15). However, these compounded estimates are error prone and mathematically coupled to, and not statistically independent from, potential predictor variables (14). In contrast, SjO₂ <50% and jugular bulb lactate concentration reflect aerobic and anaerobic estimates of the adequacy of cerebral perfusion, and they are both robust and independent (14).

The primary aim of this study was to determine the influence of SjO₂ <50% and jugular bulb lactate concentration on neurologic outcome 3 mo after CABG surgery in a subgroup of patients from a previously reported study (14). The subsidiary aims were to investigate the associations among neurologic outcome, cognitive performance, and palpable atheroma of the ascending aorta and jugular venous S100ß concentration 6 h after surgery.

	Methods

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The Lothian Health Ethics Committee approved the study, and patients gave written, informed consent. Of the 102 patients in our original report (14), we present additional neurologic and S100ß data on 98 of those patients. The loss of four patients arose from failure to collect serum for S100ß analysis. We elected not to present all of the data in our first report of this study because our approach to the analysis of the cognitive data was novel to this field, so it required a detailed explanation of the methodology (14). Patients underwent a structured clinical neurologic examination that was performed by the same investigator (MJAR) on the day before, and 3 mo after, surgery. The examination was performed and scored according to the Western Perioperative Neurological Scale (5). The following elements were examined: level of consciousness; speech; cranial nerves, including vision, motor function of limbs, sensation, and cerebellar function; reflexes; primitive reflexes; and gait. Each of the 14 elements was graded on a four-point scale: 0 represented a severe dysfunction, 1 a moderate dysfunction, 2 a mild dysfunction, and 3, no dysfunction. The maximum possible score was 42. Patients with a neurologic score 40 before surgery were defined as having a neurologic deficit and at 3 mo, a reduction of two or more points from the preoperative score represented a new neurologic deficit (5). A battery of 11 cognitive tests was also performed at the same time points. The tests and method used to calculate a General Cognitive Score have been described previously (14).

Anesthetic technique and management of the jugular bulb oximetric catheters have been previously described (14). Aprotinin was administered at the discretion of the surgeon and anesthetist. The surgeon performing the operation assessed the ascending aorta by palpation for the presence or absence of atheroma. Cold, anterograde St. Thomas’s solution was used as cardioplegia. Distal anastomoses of coronary grafts were performed during single application of an aortic cross-clamp, and proximal anastomoses to the aorta were undertaken by using a side-biting technique.

The CPB circuit included a membrane oxygenator (I-3500-2A; AVECOR Cardiovascular, Inc., Plymouth, MN) and a roller pump (Stöckert Instruments, Munich, Germany). Pump flows were maintained at 2.4 L · min^-1 · m^-2 by using a nonpulsatile flow character. In the first 45 patients, the CPB circuit was primed with 2 L lactated Ringer’s solution and sodium bicarbonate 50 mmol. Subsequently, because of a change in the unit’s clinical practice, the circuit was primed with 2 L nonlactated Ringer’s solution and sodium bicarbonate 50 mmol (n = 53). Acid-base management was performed according to -stat principles, and moderate to mild hypothermia (25°C–36°C) was used according to surgical preference. Rewarming was achieved by setting the heat exchanger no more than 10°C above the nasopharyngeal temperature and never higher than 42°C. Hypovolemia was corrected with packed red cells (hemoglobin <7 g/dL) and Ringer’s solution (hemoglobin 7 g/dL). Mean arterial pressure (MAP) <40 mm Hg was treated with methoxamine 2 mg or a phenylephrine 0.5-mg IV bolus, and MAP >100 mm Hg was treated with trimetaphan 0.5–1.0 mg or a phentolamine 1- to 2-mg IV bolus.

Radial artery and jugular venous blood were sampled before CPB (baseline), 10 min into CPB, before rewarming, when nasopharyngeal temperature reached 36°C, on arrival at the intensive care unit (ICU), and 1, 2, and 6 h thereafter. Sampling times were based on a preliminary ranging study, which found these time points to have the most frequent incidence of SjO₂ <50% (13). Jugular venous samples were drawn at a rate of 1 mL/min into a preheparinized gas syringe. Samples were analyzed for the following: the concentration and saturation of oxyhemoglobin (on an IL 482 CO-Oximeter [Instrumentation Laboratory, Lexington, MA]), oxygen tension and PaCO₂ (on an ABL blood gas analyzer [Radiometer Ltd., Copenhagen, Denmark]), and the concentration of lactate (on a 2300 Stat [YSI, Inc., Yellow Springs, OH]). The CO-Oximeter and the lactate analyzers were calibrated and accuracy confirmed against reference standards before each study.

Systemic arterial pressure, nasopharyngeal temperature, and postoperative SjO₂ were measured with a Kolormon 7250 (Kontron Instruments, Ltd., Watford, Herts, UK). Systemic arterial pressure was measured by using a 20-gauge cannula inserted into the radial artery with the transducers zeroed to the level of the right atrium throughout the study. Data were logged onto a personal computer each minute by using the Edinburgh Monitor/Browser Program (Medical Research Council Head Injuries Clinical Research Initiative, Western General Hospital, Edinburgh, UK).

Arterial hemoglobin concentration and saturation, PaCO₂, SjO₂, and jugular venous lactate concentration measurements for the three sampling points during CPB and the four postoperative sampling points were each averaged. The assessment of MAP involved two approaches: means were determined from values of three MAP readings recorded at the time of blood sampling during CPB, and after surgery the duration with a MAP <60 mm Hg was used.

The area under the curve of SjO₂ <50% in relation to time was the primary estimate of cerebral hypoperfusion in the postoperative period. This was not used during CPB because we have previously found a poor agreement between fiberoptic and bench oximetry measurement at this time (16). For this reason, absolute CO-Oximeter values were used during CPB. No interventions were taken to treat SjO₂ <50%.

Serum was separated by centrifugation from a jugular venous blood sample taken 6 h after surgery and stored at -20°C for later measurement of S100ß. Serum was analyzed by a reference laboratory (Cambridge Life Sciences, Cambridgeshire Business Park, Ely, Cambs, UK) by using the LIA-mat Santec^® 100 immunoluminometric assay (Sangtec Medical, Bromma, Sweden). The minimum level of detection was <0.02 µg/L (17).

Statistical analysis was performed with SPSS Version 9.0 for Windows (SPSS Inc., Chicago, IL). Data were visually inspected for normality, and S100ß, area under the curve for SjO₂ <50%, and MAP <60 mm Hg were transformed by using the natural logarithm to achieve a near normal distribution. Unless stated otherwise, results are presented as mean (SD).

The Pearson correlation coefficient was used to identify significant (P < 0.05) univariate associations among neurologic scores, S100ß, and General Cognitive Scores and predictor variables. Those factors found to correlate significantly were then entered into a stepwise multiple regression analysis to find predictors of the 3-mo neurologic and cognitive scores. Criteria for entry to and removal from the model were P < 0.05 and P > 0.10, respectively. Retrospective calculation found that our study had an 80% power to detect 12% of the variance in the multiple regression model of neurologic score with five predictive variables.

	Results

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The 98 patients had a mean age and a body mass index of 60 (9) yr and 28 (4), respectively. A median of three (range, one to four) CABGs were performed. The average duration of CPB and aortic cross-clamping were 85 (26) min and 43 (16) min, respectively. Patients reached a mean minimum nasopharyngeal temperature of 31 (2)°C. Thirty patients (31%) had palpable atheroma of the ascending aorta, 25 (26%) received aprotinin, and the CPB pump was primed with lactated Ringer’s solution for 45 (46%) patients. Tracheal extubation occurred on average 18 (29) h after arrival in the ICU, and the average length of stay in the ICU and hospital was 38 (36) h and 7 (2) days, respectively.

After surgery, the bias and limits of agreement between the catheter and CO-Oximeter measurements were 0.1% and -5.8% to 6.0%, respectively. Reflectance oximetry during this period identified 46 (47%) patients with SjO₂ <50%. The mean total duration of SjO₂ <50% was 40 (87) min. The mean PaCO₂ during CPB was 4.8 (0.5) (range, 3.7–6.2) kPa, and after surgery it was 5.6 (0.7) (range, 4.1–7.9) kPa.

Six hours after surgery, the median level of S100ß was 0.37 (range, 0.06–3.18) µg/L. S100ß correlated positively with age (r = 0.305, P = 0.002) and postoperative SjO₂ (r = 0.320, P = 0.001). Postoperative neurologic score (r = -0.232, P < 0.05), use of a lactated prime (r = -0.392, P < 0.001), and the concentration of jugular bulb lactate during CPB (r = -0.297, P = 0.003) were all negatively correlated with S100ß. The preceding five variables were entered in a stepwise fashion into a linear regression model of S100ß. Lactated prime (r² = 0.145, standardized ß [standardized regression coefficient] = -0.322, P = 0.001), age (r² = 0.094, standardized ß = 0.352, P < 0.001), and postoperative SjO₂ (r² = 0.059, standardized ß = 0.269, P = 0.004) were retained in the model, and neurologic score (ß = -0.084, P = 0.373) and jugular bulb lactate during CPB (ß = -0.107, P = 0.363) were excluded. Patients with palpable aortic atheroma had a median S100ß level that was significantly more than those without (0.46 µg/L versus 0.33 µg/L, Mann-Whitney U-test, Z = -2.19, P = 0.028). S100ß did not correlate with cognitive outcome after CABG surgery (r = 0.030, P = 0.772).

The median neurologic score before surgery was 42 (range, 38–42), and this score decreased to 40 (range, 36–42) 3 mo after surgery (Fig. 1). Fifty percent (n = 49) of patients developed new neurologic signs. Fifty-four percent (n = 24) of the 44 patients with neurologic signs before surgery subsequently developed new signs after surgery. Before surgery, 26% (n = 26) of patients had a neurologic deficit (neurologic score 40), and at the 3-mo follow-up a new neurologic deficit was detected in 23% (n = 23) of patients (Table 1). None of the patients developed major neurologic signs. One patient had mild facial weakness, and another had a peripheral visual field defect. "Primitive reflexes" were the most commonly detected findings before and after surgery; these accounted for 34% and 30% of the total neurologic signs, respectively. The individual neurologic domains accounted for similar proportions of the total neurologic score before and after surgery (Z = -0.229 to -1.57, Wilcoxon’s signed rank test).

View larger version (11K): [in this window] [in a new window]   Figure 1. Neurologic scores before 3 mo after coronary artery bypass grafting surgery.

	Discussion

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We have found an incidence of subtle neurologic signs in a low-risk group of CABG surgery patients, before surgery (45%) and three months after surgery (50%), that is similar to that previously reported by other researchers (2,3,18). Twenty-three percent of our patients showed a neurologic deficit after surgery, and this result is similar to the 17% reported by Murkin et al. (5). Although most of these neurologic signs are subtle and do not appear to interfere with daily activities, they are manifestations of brain injury, and it is therefore important to determine their etiology (2,3,18).

Although jugular bulb oximetry gives a global view of the balance between cerebral oxygen demand and delivery, it does not necessarily correlate with cerebral blood flow (19). Furthermore, continuous jugular bulb reflectance oximetry is unreliable during surgery, and discrete sampling provides information on only a snapshot in time (16). It is conceivable that regional cerebral hypoperfusion may occur, for example, as a result of intracranial cerebrovascular disease despite an SjO₂ in the normal range. These limitations have been described in neurosurgery, in which direct mea-surement of brain tissue partial pressure of oxygen is feasible (20). However, such invasive monitoring of brain tissue during CABG surgery could not be ethically justified. Moreover, other noninvasive methods of assessing the adequacy of cerebral perfusion, such as near infrared spectroscopy, have other limitations (19).

Notwithstanding limitations of the measurement techniques, our data suggest that SjO₂ during CPB and SjO₂ <50% after CABG surgery does not have a meaningful affect on neurologic or cognitive outcome three months after CABG surgery. If many patients are experiencing SjO₂ <50% during the rewarming phase of CPB and in the first few hours after CABG surgery, what causes this phenomenon, and why is it not associated with long-term adverse neurologic or cognitive outcome? We have found that SjO₂ to be highly influenced by PaCO₂ (13,21) during and after CABG surgery. Moreover, as we have also found that decreases in SjO₂ are not reciprocated by an increase in cerebral lactate production (21), SjO₂ <50% in this setting probably does not represent cerebral ischemia. Rather, SjO₂ <50% appears to be largely caused by hypocapnia inducing cerebral vasoconstriction (21). This in turn decreases cerebral blood flow, and any decrement in cerebral oxygen delivery is compensated for by increased oxygen extraction. Therefore, SjO₂ <50% occurring during CPB and in the early postoperative period after CABG surgery is not a valuable predictor of long-term cerebral outcome.

Although we found significant univariate correlations among postoperative neurologic score, age, and jugular venous concentrations of S100ß sampled six hours after surgery, only age remained significant in the multiple regression model. Furthermore, there was no association between cognitive performance and S100ß. Rasmussen et al. (8) and Anderson et al. (22) have found that systemic venous concentrations of S100ß up to five hours after CPB, when cardiotomy suction is used, are of little prognostic value for cognitive and neurologic outcome. Our results are in accordance with these findings and suggest that jugular venous concentrations of S100ß six hours after CABG surgery are also not prognostic of long-term neurologic or cognitive outcome. However, its value as a prognostic indicator of cerebral outcome might be improved by measuring the arteriovenous gradient of S100ß across the brain, avoiding the use of cardiotomy suction during surgery, or both of these.

Epi-aortic scanning is a more precise method of detecting aortic atheroma than surgical palpation (23). However, because the primary aim of the study was not to investigate the influence of aortic atheroma on neurologic outcome, we used palpation. The positive correlation between palpable aortic atheroma and neurologic outcome is in keeping with the findings of other researchers (18,24,25). What remains unclear is the mechanism of this association. One reasonable hypothesis is that surgical manipulation and cannulation of an atheromatous aorta is more likely to generate particulate microemboli than with an unaffected aorta. However, Barbut et al. (26) have found that although aortic atheroma is related to outcome, the number of microemboli generated during surgery is not. An alternative hypothesis is that atheroma in the ascending aorta is a marker for cerebrovascular disease (26,27). Vascular disease is important in the etiology of cerebral injury, cognitive decline, and dementia (28,29), and these patients may be predisposed to brain injury because of previous subclinical ischemia or a failure of neuronal repair mechanisms (30,31). The mechanism that associates atheroma of the ascending aorta with cerebral outcome needs to be elucidated because it may hold a key for prevention or amelioration of the cognitive and neurologic deficits that are associated with CABG surgery.

Preoperative stroke or transient ischemic events are known risk factors for cognitive decline after CABG surgery (10,28). However, we have demonstrated that there are significant positive correlations between more subtle neurologic signs, as determined by a scored examination, and cognitive performance both before and three months after CABG surgery. Furthermore, preoperative clinical neurologic findings have a small, but significant, negative influence on cognitive performance three months after CABG surgery. Future studies examining cognition after CABG surgery should therefore include scored neurologic assessment.

In conclusion, neither intraoperative SjO₂ nor postoperative SjO₂ <50% has an important influence on long-term neurologic outcome after CABG surgery. Subtle preoperative neurologic abnormality is associated with a decline in long-term cognitive performance, and palpable atheroma of the ascending aorta is a risk factor for both adverse cognitive and neurologic outcome. These findings suggest that patients with aortic atheroma and subtle preoperative neurologic abnormalities have less cognitive reserve and are prone to a decline in function after CABG surgery.

	Acknowledgments

 
Supported by Welcome Trust Grant 050190.

We would like to thank Shona Yates, BSc (Hons), for undertaking the cognitive assessments and Timothy P. Howells, BA, PhD, for supplying and modifying the computer-based data collection system for use in this study.

	References

Top Abstract Introduction Methods Results Discussion References

 

1. Roach GW, Kanchuger M, Mangano CM, et al. Adverse cerebral outcomes after coronary bypass surgery. N Engl J Med 1996; 335: 1857–63.[Abstract/Free Full Text]
2. Shaw PJ, Bates D, Cartlidge NEF, et al. Neurologic and neuropsychological morbidity following major surgery: comparison of coronary artery bypass and peripheral vascular surgery. Stroke 1987; 18: 700–7.[Abstract/Free Full Text]
3. Shaw PJ, Bates D, Cartlidge NEF, et al. Early neurological complications of coronary artery bypass surgery. BMJ 1985; 291: 1384–7.
4. McKhann GM, Goldsborough MA, Borowicz LM, et al. Predictors of stroke risk in coronary artery bypass patients. Ann Thorac Surg 1997; 63: 516–21.[Abstract/Free Full Text]
5. Murkin JM, Martzke JS, Buchan AM, et al. A randomized study of the influence of perfusion technique and pH management in 316 patients undergoing coronary artery bypass surgery. II. Neurologic and cognitive outcomes. J Thorac Cardiovasc Surg 1995; 110: 349–62.[Abstract/Free Full Text]
6. Persson L, Hardemark HG, Gustafsson J, et al. S-100 protein and neuron-specific enolase in cerebrospinal fluid and serum: markers of cell damage in human central nervous system. Stroke 1987; 18: 911–8.[Abstract/Free Full Text]
7. Martens P, Raabe A, Johnsson P. Serum S-100 and neuron-specific enolase for prediction of regaining consciousness after global cerebral ischaemia. Stroke 1998; 29: 2363–6.[Abstract/Free Full Text]
8. Rasmussen LS, Christiansen M, Hansen PB, Moller JT. Do levels of neuron-specific enolase and S-100 protein reflect cognitive dysfunction after coronary artery bypass? Acta Anaesthesiol Scand 1999; 43: 495–500.[Web of Science][Medline]
9. Alston RP, Souter MJ. Cerebral sequelae of cardiac surgery. Curr Opin Crit Care 2000; 6: 92–7.
10. Selnes OA, Goldsborough MA, Borowicz LM, et al. Determinants of cognitive change after coronary artery surgery: a multifactorial problem. Ann Thorac Surg 1999; 67: 1669–76.[Abstract/Free Full Text]
11. Croughwell ND, Newman NF, Blumenthal JA, et al. Jugular bulb saturation and cognitive dysfunction after cardiopulmonary bypass. Ann Thorac Surg 1994; 58: 1702–8.[Abstract]
12. Souter MJ, Andrews PJD, Alston RP. Jugular venous desaturation following cardiac surgery. Br J Anaesth 1998; 81: 239–41.[Abstract/Free Full Text]
13. Millar SA, Alston RP, Souter MJ, Andrews PJD. Aerobic, anaerobic and combination estimates of cerebral hypoperfusion after cardiac surgery. Br J Anaesth 1999; 83: 936–9.[Abstract/Free Full Text]
14. Robson MJA, Alston RP, Deary IJ, et al. Cognition after coronary artery surgery is not related to postoperative jugular bulb oxyhemoglobin desaturation. Anesth Analg 2000; 91: 1317–26.[Abstract/Free Full Text]
15. Souter MJ, Andrews PJD, Alston RP. Propofol does not ameliorate cerebral venous oxyhemoglobin desaturation during hypothermic cardiopulmonary bypass. Anesth Analg 1998; 86: 926–31.[Abstract]
16. Millar SA, Alston RP, Souter MJ, Andrews PJD. Continuous monitoring of jugular bulb oxyhaemoglobin saturation using the Edslab dual lumen oximetry catheter during and after cardiac surgery. Br J Anaesth 1999; 82: 521–4.[Abstract/Free Full Text]
17. Asharaf S, Bhattacharya K, Zacharias S, et al. Serum S100ß release after coronary artery bypass grafting: roller versus centrifugal pump. Ann Thorac Surg 1998; 66: 1958–62.[Abstract/Free Full Text]
18. Carella F. Cerebral complications of coronary by-pass surgery: a prospective study. Acta Neurol Scand 1988; 77: 158–63.[Web of Science][Medline]
19. Ali MS, Harmer M, Latto IP. Jugular bulb oximetry during cardiac surgery. Anaesthesia 2001; 56: 24–37.[Web of Science][Medline]
20. Gupta AK, Hutchinson PJ, Al-Rawi P, et al. Measuring brain tissue oxygenation compared with jugular venous oxygen saturation for monitoring cerebral oxygenation after traumatic brain injury. Anesth Analg 1999; 88: 549–53.[Abstract/Free Full Text]
21. Millar SM, Alston RP, Andrews PJD, Souter MJ. Cerebral hypoperfusion in the immediate postoperative period following coronary artery bypass, heart valve and abdominal aortic surgery. Br J Anaesth 2001; 87: 229–36.[Abstract/Free Full Text]
22. Anderson RE, Hansson L-O, Liska J, et al. The effect of cardiotomy suction on the brain injury marker S100ß after cardiopulmonary bypass. Ann Thorac Surg 2000; 69: 847–50.[Abstract/Free Full Text]
23. Marshall WG, Barzilai B, Kouchoukous NT, Saffitz J. Intraoperative ultrasonic imaging of the ascending aorta. Ann Thorac Surg 1989; 48: 339–44.[Abstract]
24. John R, Choudhri AF, Weinberg AD, et al. Multicenter review of preoperative risk factors for stroke after coronary artery bypass grafting. Ann Thorac Surg 2000; 69: 30–6.[Abstract/Free Full Text]
25. Hammon JW, Stump DA, Kon ND, et al. Risk factors and solutions for the development of neurobehavioral changes after coronary artery bypass grafting. Ann Thorac Surg 1997; 63: 1613–8.[Abstract/Free Full Text]
26. Barbut D, Lo Y-W, Hartman GS, et al. Aortic atheroma is related to outcome but not numbers of emboli during coronary bypass. Ann Thorac Surg 1997; 64: 454–9.[Abstract/Free Full Text]
27. Taylor RL, Borger MA, Weisel RD, et al. Cerebral microemboli during cardiopulmonary bypass: increased emboli during perfusionist interventions. Ann Thorac Surg 1999; 68: 89–93.[Abstract/Free Full Text]
28. McKann GM, Goldsborough MA, Borowicz LM, et al. Cognitive outcome after coronary artery bypass: a one-year prospective study. Ann Thorac Surg 1997; 63: 510–5.[Abstract/Free Full Text]
29. Prince MJ. Vascular risk factors and atherosclerosis as risk factors for cognitive decline and dementia. J Psychosom Res 1995; 39: 525–30.[Web of Science][Medline]
30. Newman MF, Laskowitz DT, Saunders AM, et al. Genetic predictors of perioperative neurologic and neuropsychological injury and recovery. Semin Cardiothorac Vasc Anesth 1999; 3: 34–46.[Abstract/Free Full Text]
31. Redmond JM, Greene PS, Goldsborough MA, et al. Neurological injury in cardiac surgical patients with a history of stroke. Ann Thorac Surg 1996; 61: 42–7.[Abstract/Free Full Text]

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