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J Thorac Cardiovasc Surg 2000;119:132-137
© 2000 Mosby, Inc.

CARDIOPULMONARY SUPPORT AND PHYSIOLOGY

IS THERE A RELATIONSHIP BETWEEN SERUM S-100ß PROTEIN AND NEUROPSYCHOLOGIC DYSFUNCTION AFTER CARDIOPULMONARY BYPASS?

Stephen Westaby, FRCSa, Kjell Saatvedt, MD, PhDa, Samantha White, MAa, Takahiro Katsumata, MD, PhDa, Willem van Oeveren, PhDb, Narendra K. Bhatnagar, FRCSa, Stuart Brown, MBBSa, Peter W. Halligan, PhDc

From Oxford Heart Centre, John Radcliffe Hospital,a Oxford, United Kingdom, Department of Biomedical Engineering, University of Groningen, The Netherlands,b and University Department of Experimental Psychology, Oxford, United Kingdom.c

Financial support was received from Cobe Cardiovascular, Inc, Arvada, Colo. Haemoprobe, Groningen, The Netherlands, performed the S-100ß analysis.

Address for reprints: S. Westaby, BSc, FRCS, MS, Oxford Heart Centre, John Radcliffe Hospital, Oxford OX3 9DU, England.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objectives: Over the past decade, the glial protein S-100ß has been used to detect cerebral injury in a number of clinical settings including cardiac surgery. Previous investigations suggest that S-100ß is capable of identifying patients with cerebral dysfunction after cardiopulmonary bypass. Whether detection of elevated levels S-100ß reflects long-term cognitive impairment remains to be shown. The present study evaluated whether perioperative release of S-100ß after coronary artery operations with cardiopulmonary bypass could predict early or late neuropsychologic impairment.
Methods: A total of 100 patients undergoing elective coronary bypass without a previous history of neurologic events were prospectively studied. To exclude noncerebral sources of S-100ß, we did not use cardiotomy suction or retransfusion of shed mediastinal blood. Serial perioperative measurements of S-100ß were performed with the use of a new sensitive immunoluminometric assay up to 8 hours after the operation. Patients underwent cognitive testing on a battery of 11 tests before the operation, before discharge from the hospital, and 3 months later.
Results: No significant correlation was found between S-100ß release and neuropsychologic measures either 5 days or 3 months after the operation.
Conclusion: Despite using a sensitive immunoluminometric assay of S-100ß, we found no evidence to support the suggestion that early release of S-100ß may reflect long-term neurologic injury capable of producing cognitive impairment.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Surgery with cardiopulmonary bypass (CPB) is assumed to cause subtle cerebral injury that may be detectable on neuropsychologic measures in 30% to 70% of patients.Go Go 1,2 Elevation of serum S-100ß levels has been shown to be a sensitive, although nonspecific, indicator of central nervous system damage (eg, stroke, head injury).Go Go 3-5 S-100ß protein leaks from structurally damaged nerve cells into cerebrospinal fluid and secondarily across the blood-brain barrier.Go 6

In recent years S-100ß has been used, in a research context, to identify cerebral injury after cardiac surgery in preference to the more labor-intensive neuropsychologic evaluations.Go Go 7,8 Several studies suggest that transient elevations in levels of serum S-100ß protein reflect subclinical cerebral damage in the absence of frank neurologic signs.Go Go 9,10 To date, however, no study has demonstrated that S-100ß levels reflect neuropsychologic performance. The aim of the present study was to determine whether S-100ß could predict early or late neuropsychologic and functional impairment after coronary bypass surgery with CPB. We attempted to avoid noncerebral sources of S-100ß by discarding cardiotomy suction blood.Go 11


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Study patients
With ethics committee approval we prospectively studied 100 patients undergoing elective first-time coronary bypass without a previous history of neurologic events or psychiatric illness. Those with acute coronary syndromes were excluded to eliminate the added anxiety of a recent illness. We also excluded patients with renal or hepatic dysfunction and diabetes. All patients required between 2 and 5 bypass grafts. Patients were part of a randomized clinical trial of a new coating agent of the CPB circuit (50 patients in each group), the results of which showed no statistically significant difference in S-100ß and neuropsychologic measures. Each patient consented to a detailed 11-part neuropsychologic examination, which was administered by a psychologist(Table I).


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  		Table I. The neuropsychologic tests performed and a brief description of the cognitive domains evaluated
 
Anesthesia
On the day of the operation, patients were premedicated with morphine (10-15 mg) and scopolamine (0.3-0.4 mg). Anesthesia was induced with fentanyl (1 mg), pancuronium (8 mg), and etomidate (4-10 mg). Before CPB, anesthesia was maintained with a combination of oxygen, nitrous oxide, and halothane and during CPB with propofol (6 mg · kg–1 · h–1).

Conduct of the operation
All operations were performed with Cobe flat sheet membrane oxygenators and bypass circuits (COBE Cardiovascular Inc, Denver, Colo) and a pump flow of 2.4 L · m–2 · min–1 at between 32°C and 36°C. Vent suction was not used. The mean arterial pressure was maintained between 50 and 80 mm Hg and alpha-stat arterial carbon dioxide management was used. Myocardial protection was achieved with antegrade crystalloid cardioplegia. Shed mediastinal blood was minimized by careful surgery and was discarded to avoid noncerebral sources of S-100ß. Anticoagulation during CPB was monitored with the activated clotting time (Hemochron 800; International Technidyne Corp, Edison, NJ). Additional heparin was administered if the activated clotting time was shorter than 400 seconds. Heparin was neutralized by means of protamine chloride infusion (3 mg/kg) after the completion of CPB.

S-100ß analysis
Serum was analyzed for S-100ß protein concentration 24 hours before the operation (T1), 5 minutes before beginning CPB but after heparin injection (T2), immediately after termination of CPB but before protamine injection (T3), and 8 hours after the operation (T4). The serum or heparinized plasma samples were stored at –80°C until analyzed. S-100ß protein concentration was determined with the use of a new, more sensitive monoclonal immunoluminometric method (sensitivity 0.02 µ/L) (Sangtec LIA 100, Sangtec Medical AB, Bromma, Sweden). This assay method uses 3 monoclonal antibodies, SMST 12, SMSK 25, and SMSK 28, to detect the beta chains in the betabeta and the alphabeta dimers of S-100. Since S-100ß is a calcium-binding protein, plasma treated with ethylenediaminetetraacetic acid cannot be used, but heparin does not affect the results, as we showed in a separate unpublished validation study. The test is based on sandwich formation of immobilized ant-S-100ß antibody, S-100ß from the test sample and luminescence-labeled S-100ß antibody. The assay was performed according to the manufacturer’s instructions and label was measured by means of flash luminescence (Lumat LB 9507, EG & G, Berthold, Germany).

Neuropsychologic and functional assessment
Each patient underwent a comprehensive neuropsychologic examination administered by a research psychologist (S. White). The National Adult Reading Test (NART) was used to estimate pre-morbid intelligence. Tests were carried out preoperatively (1 day before the operation), before hospital discharge (5 days after the operation), and again at 3 months after the operation. All tests have been described in detail elsewhere.Go Go 12-16Table IGo lists the neuropsychologic tests and provides a brief description of the cognitive domains evaluated.

In addition to neuropsychologic performance, functional and emotional measures were also measured before the operation and at 3 months’ follow-up. These tests were as follows:

  1. Short Form-36 (multidimensional measure of subjective health status)Go 14
  2. Health Complaints Scale (measures on somatic and cognitive complaints)Go 15
  3. BADs Dysexecutive Questionnaire (measures a range of problems commonly associated with dysexecutive impairment)Go 16
  4. Hospital Anxiety and Depression ScaleGo 14

Statistical analysis
Clinical data were expressed as mean and standard deviation. Blood test values were described as mean and standard error of the mean. Neuropsychologic performance was assessed by calculating the change scores (preoperative minus predischarge and preoperative minus follow-up) for each patient on every test. Likewise, change scores (preoperative minus follow-up) were also calculated for each of the 4 functional measures. Change scores were then correlated with the S-100ß measures taken at each of the 4 different time points. Computerized statistical analysis was undertaken with the use of the SPSS for Windows (version 7) statistical program (SPSS, Inc, Chicago, Ill). Comparisons between groups were done with the Mann-Whitney test for unpaired data. Correlations between each of the mean S-100ß time points and age, CPB time, crossclamp time, blood loss, blood transfusions, ventilatory times, and neuropsychologic performance were calculated by means of the Pearson correlation coefficient and, unless specified, adopted the .01 level as significant given the large number of comparisons. Because the distribution of S-100ß values was generally skewed, these data are presented as median, 25th, and 75th percentiles.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
Patient characteristics and operative data are presented inTable II. One patient required re-entry for excessive postoperative bleeding and 1 had a stroke. After initial recovery, 1 patient had bowel necrosis develop and eventually died of multiple system failure (1% mortality).


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  		Table II. Patient characteristics including operative data
 
The serum S-100ß protein concentration at each time point is shown inTable III. In 90% of the patients the preoperative (T1) S-100ß concentration was below the detection limit of the test (0.02 µ/L). The maximum value (0.140 µ/L [0.060/0.273 µ/L]) was detected at T4. There were 9 patients at this time point without detectable S-100ß levels, and in 7 patients the S-100ß protein could not be detected at any of the 4 time points. The 1 patient who had a stroke had S-100ß levels as follows: T1, less than 0.02 µ/L; T2, 0.06 µL; T3, 0.25 µ/L; and T4, 0.09 µ/L. These levels were not significantly different from those of the other patients. Patients with undetectable levels of S-100ß at T2 had significant lower levels of S-100ß at T3 (0.06 µ/L [0/0.110 µ/L] vs 0.240 µ/L [0.120/0.330 µ/L]; P < .0001) and at T4 (0.090 µ/L [0.030/0.152 µ/L] vs 0.220 µ/L [0.115/0.355 µ/L]; P < .0001).


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  		Table III. S-100 levels at the different time points (µg/L)
 
We found no correlation between maximum S-100ß levels and crossclamp time (r = 0.024), perfusion time (r = 0.025), ventilatory times (r = 0.065), blood transfusions (r = 0.09), or total amount of fluid transfused (r = 0.041). However, the prebypass levels of S-100ß (T2) correlated significantly with the postbypass level (T3) (P < .0001, r = 0.57) and postoperative level (T4) (P = .0001, r = 0.4). The postoperative S-100ß (T4) values also correlated with age (P = .017, r = 0.26). Interestingly, those patients intubated for more than 5 hours had a significantly higher maximum serum value of S-100ß than the others (0.240 µ/L [0.090/0.480 µ/L] vs 0.125 µ/L [0.060/0.240 µ/L]; P = .04).

Neuropsychologic performance
A total of 95 patients completed the preoperative assessment. The remaining 5 were eliminated from follow-up. The mean estimated IQ for the group was 108. Before hospital discharge (5 days after the operation), 79 patients could be assessed. Two patients were excluded because of stroke and multiple organ failure. The remaining 14 patients declined for reasons of ill health. However, 3 months after the operation, 89 patients had completed all tests. Pearson correlation coefficients for all serial time points for S-100ß versus neuropsychologic and functional change scores are presented inTables IV and V.


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  		Table IV. Preoperative versus hospital discharge neuropsychologic change scores correlated against S-100 levels at the different time points
 

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  		Table V. Preoperative versus 3 months’ follow-up neuropsychologic change scores correlated against S-100 levels at the different time points
 
No significant correlations were found between the S-100ß level at any time point and neuropsychologic change scores for any test. This was true even when the level of significance was dropped to the .05 level. Similarly, no significant correlations were found between S-100ß measures at any time point and functional change scores. The correlation coefficients for the functional measures are reported inTable VI.


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  		Table VI. Preoperative versus 3 months’ follow-up functional change scores correlated against S-100 levels at the different time points
 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
It has been claimed that S-100ß protein assay may be a useful method of detecting cerebral injury after cardiac surgery.Go Go Go Go 8-10,17-19 However, to date no study has formally shown a relationship between serum S-100ß levels and late neuropsychologic performance, the gold standard for subtle cerebral injury. The results of the present study did not show any relationship between S-100ß (at any of the serial time points) and early (5 days after the operation) or late (3 months after the operation) neuropsychologic outcome. This was also true for the functional measures at 3 months’ follow-up.

The serum levels of S-100ß after uncomplicated cardiac operations follow a different pattern from those after acute ischemic cerebral events, wherein peak values occur after 3 days.Go Go 20,21 Studies on S-100ß release during and after CPB have shown peak S-100ß levels soon after perfusion, presumably resulting from transient increase in permeability of the blood-brain barrier as part of the inflammatory response.Go Go Go Go 8-10,18,19 Joensson and associatesGo 9 showed that S-100ß levels immediately after CPB did not correlate with cerebral outcome although grossly elevated levels of S-100ß 48 hours after the operation were associated with clinically obvious stroke.Go 9 The early release of S-100ß after cardiac surgery may thus be a transient serum elevation without any relation to permanent neuronal damage. However, the early S-100ß studies were interpreted without the awareness that S-100ß from noncerebral sources might confuse the issue by elevating overall levels.Go 11 In the present study, extracerebral S-100ß was reduced by discarding cardiotomy blood and not retransfusing shed mediastinal blood, which has been shown to contain high levels of S-100ß.Go 11 Consequently, our S-100ß levels were lower and also peaked later than in earlier reports.Go Go Go Go 8-10,18,19 Lower levels might also be caused by other factors. We used a new, highly sensitive immunoluminometric assay test capable of detecting much lower levels of S-100ß, whereas in earlier studies levels of S-100ß below 0.2 µ/L were not detectable. Consequently, more patients in our study had detectable levels of S-100ß. As most of these were at or below the previous less-sensitive level, it is likely that they contributed to the lowering of the mean levels, since previous studies in which less-sensitive assays were used did not always include patients with undetectable S-100ß levels.

Grocott and colleaguesGo 10 described a weak but significant relationship between cerebral microemboli and S-100ß levels. In an experimental study, blood aspirated from the surgical field during CPB and reinfused into dogs generated a greater density of small capillary and arterial dilatations in the brain than CPB without cardiotomy suction.Go 23 The presence of so-called small capillary and arterial dilatations was first demonstrated by Moody and colleaguesGo 24 in autopsy specimens from patients who had undergone cardiac operations with CPB. There is evidence to suggest that lipid microembolism is the cause of these diffuse cerebral changes.Go 25 We have also shown that an arterial line filter can significantly reduce levels of S-100ß, although this early investigation was performed with cardiotomy suction and the less-sensitive S-100ß assay.Go 26

A recent study by Backstroem and associates,Go 22 using a kinetic model employing elimination rates of S-100ß during the first 5 hours after operation, found a positive correlation with early adverse cognitive outcome. The authors proposed early S-100ß elimination rate (as an expression of postbypass release) in preference to absolute levels to correct for contamination from extracerebral sources.Go 9 However, the formula to calculate elimination rate requires a progressive decrease in postoperative levels, whereas our study without cardiotomy suction shows an increase over this time frame. Consequently, for our study the calculation would have been meaningless for most patients.

Appearance of S-100ß in serum after CPB may indicate cellular damage, increased permeability of the blood-brain barrier, or both. Transient permeability of the blood-brain barrier to S-100ß protein could be caused by the inflammatory response generated by CPB itself. Since the development of inflammation is time related, we might expect a positive correlation between perfusion time and S-100ß release. In fact, correlation between perfusion time and S-100ß levels has been an inconstant finding.Go Go Go Go Go Go 8-10,18,19,27,28 Our present study found no relationship between S-100ß and perfusion time, although in general the duration of CPB was short. However, we did find a significant correlation between the prebypass value and the postbypass levels, and patients without detectable prebypass levels had significantly lower levels of S-100ß afterward, irrespective of perfusion time. These findings suggest that factors other than perfusion time may influence the release of S-100ß. Surgical injury and the anesthesia may well contribute to this release, and differences have been shown in valve, aortic aneurysm, and hypothermic circulatory arrest patients where S-100ß levels are greater and remain significantly higher for between 5 and 48 hours.Go 18 In open cardiac operations (as opposed to coronary operations), the relationship between S-100ß and neuropsychologic outcome might be different irrespective of the contribution of cardiotomy suction.

The finding of significantly higher S-100ß levels in patients requiring ventilation for more than 5 hours is interesting and consistent with a recent report claiming a relationship between postoperative S-100ß levels and prolonged intubation.Go 28 Cerebral edema has been demonstrated within an hour of CPB by magnetic resonance scanning in patients undergoing routine coronary bypass.Go 29 The swelling is variable and may similarly reflect transient change in permeability of the blood-brain barrier without injury to the brain itself. The transient increase in S100ß levels may then represent a reversible increase in the permeability of cellular and vascular membranes as opposed to structural neuronal damage. All patients having coronary operations in this study were subjected to fast track and early extubation protocols (irrespective of age), so that shorter extubation time reflected early awaking and conscious awareness.Go 30

In summary, we were unable to demonstrate any correlation between serum S-100ß protein levels and early or late neuropsychologic impairment after elective coronary operations with CPB. It is possible that the transient passage of S-100ß from cerebrospinal fluid to serum bears little relationship to the type of neuronal injury necessary to produce impairment of neuropsychologic and functional measures.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. Mahanna EP, Blumenthal JA, White WD, Croughwell ND, Clancy CP, Smith LR, et al. Defining neuropsychological dysfunction after coronary artery bypass grafting. Ann Thorac Surg 1996;61:1342-7.[Abstract/Free Full Text]
  2. Shaw PJ, Bates D, Cartlidge NEF, French JM, Heaviside D, Julian DG, 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. Rosen H, Rosengren L, Herlitz J, Blomstrand C. Increased serum levels of the S-100 protein are associated with hypoxic brain damage after cardiac arrest. Stroke 1998;29:473-7.[Abstract/Free Full Text]
  4. Aurell A, Rosengren LE, Karlsson B, Olsson JE, Zbornikova V, Haglid KG. Determination of S-100 and glial fibrillary acidic protein concentration in cerebrospinal fluid after brain infarction. Stroke 1991;22:1254-58.[Abstract/Free Full Text]
  5. Kim JS, Yoon SS, Kim YH, Ryu JS. Serial measurement of interleukin-6, transforming growth factor beta, and S-100 protein in patients with acute stroke. Stroke 1996;27:1553-7.[Abstract/Free Full Text]
  6. Ingebrigtsen T, Romner B, Kongstad P, Langbakk B. Increased serum concentrations of protein S-100 after minor head injury: A biochemical serum marker with prognostic value? J Neurol Neurosurg Psychiatry 1995;59:103-4.
  7. Johnsson P. Marker of cerebral ischemia after cardiac surgery. J Cardiothorac Vasc Anesth 1996;10:120-6.[Medline]
  8. Blomquist S, Johnsson P, Luhrs C, Malmkvist G, Solem JO, Alling C, et al. The appearance of S-100 protein in serum during and immediately after cardiopulmonary bypass surgery: a possible marker for cerebral injury. J Cardiothorac Vasc Anesth 1997;11:699-703.[Medline]
  9. Joensson H, Johnsson P, Alling C, Westaby S, Blomquist S. Significance of serum S-100 release after coronary artery bypass grafting. Ann Thorac Surg 1998;65:1639-44.[Abstract/Free Full Text]
  10. Grocott HP, Croughwell ND, Amory DW, White WD, Kirchner JL, Newman MF. Cerebral emboli and S-100 beta during cardiac operations. Ann Thorac Surg 1998;65:1645-50.[Abstract/Free Full Text]
  11. Joensson H, Blomquist S, Alling C, Jonsson P. Early release of S-100 after cardiac surgery: interference from extracerebral sources [abstract]. Ann Thorac Surg 1998;66:1493.
  12. Lezak MD. Neuropsychological assessment, 3rd ed. Oxford: Oxford University Press; 1995.
  13. Coughlan AK, Hollows SE. The adult memory and information processing battery: test manual. Leeds: AK Coughlan; 1985.
  14. Wade DT. Measurement in neurological rehabilitation. Oxford: Oxford University Press; 1992.
  15. Denollet JD. Health complaints and outcome assessment in coronary heart disease. Psychosom Med 1994;56:463-74.[Abstract/Free Full Text]
  16. Wilson BA, Alderman N, Burgess P, Enslie H, Evans JJ. Thames Valley Company. Catalogue 1997-98.
  17. Westaby S, Johnsson P, Parry A, Blomquist S, Solem JO, Alling C, et al. Serum S-100 protein: a potential marker for cerebral events during cardiopulmonary bypass. Ann Thorac Surg 1996;61:88-92.[Abstract/Free Full Text]
  18. Taggart DP, Mazel J, Bhattacharya K, Meston N, Standing SJ, Kay JDS, et al. Comparison of serum S-100B levels during CABG and intracardiac operations. Ann Thorac Surg 1997;63:492-6.[Abstract/Free Full Text]
  19. Johnsson P, Lundquist C, Lindgren A, Ferencz L, Alling C, Stahl E. Cerebral complications after cardiac surgery assessed by S-100 and NSE levels in blood. J Cardiothorac Vasc Anesth 1995;9:694-9.[Medline]
  20. Kim JS, Yoon SS, Kim YH, Ryu JS. Serial measurement of interleukin-6, transforming growth factor-beta, and serum S-100 protein in patients with acute stroke. Stroke 1996;27:1553-7.
  21. Missler U, Wiesman M, Friedrich C, Kaps M. S-100 protein and neuron-specific enolase concentrations in blood as indicators of infarction volume and prognosis in acute ischemic stroke. Stroke 1997;28:1956-60.[Abstract/Free Full Text]
  22. Backstroem M, Joensson H, Bergh C, Blomquist S, Alling C, Johnsson P. Early release of S-100 after cardiac surgery is associated with neuropsychological outcome [abstract]. Ann Thorac Surg 1998;66:1493.
  23. Brooker RF, Brown W, Moody DM, Hammon JW Jr, Reboussin DM, Deal DD, et al. Cardiotomy suction: a major source of brain lipid emboli during cardiopulmonary bypass. Ann Thorac Surg 1998;65:1651-5.[Abstract/Free Full Text]
  24. Moody DM, Bell MA, Challa VR, Stump DA, Reboussin DM, Legault C. Brain microemboli associated with cardiopulmonary bypass: a histologic and magnetic resonance imaging study. Ann Thorac Surg 1995:59:1304-7.
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  26. Taggart DP, Bhattacharya K, Meston N, Standing SJ, Kay JD, Westaby S, et al. Serum S-100 protein concentrations after cardiac surgery: a randomized trial of arterial line filtration. Eur J Cardiothorac Surg 1997;11:645-9.[Abstract]
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Received for publication April 2, 1999. Revisions requested June 11, 1999; revisions received July 21, 1999. Accepted for publication Aug 18, 1999.


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V. Zamvar, D. Williams, J. Hall, N. Payne, C. Cann, K. Young, S Karthikeyan, and J. Dunne
Assessment of neurocognitive impairment after off-pump and on-pump techniques for coronary artery bypass graft surgery: prospective randomised controlled trial
BMJ, November 30, 2002; 325(7375): 1268 - 1268.
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 PerfusionHome page
H. I Flom-Halvorsen, E Ovrum, F Brosstad, G Tangen, M A. Ringdal, and R Oystese
Effects of two differently heparin-coated extracorporeal circuits on markers for brain and myocardial dysfunction
Perfusion, September 1, 2002; 17(5): 339 - 345.
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 SEMIN CARDIOTHORAC VASC ANESTHHome page
D. Harrington, C. H. Wong, and R. S. Bonser
Neurological Complications of Aortic Surgery
Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2002; 6(1): 7 - 16.
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B. Krishnadasan, C. R. Hampton, J. Griscavage-Ennis, R. J. Dabal, and E. D. Verrier
Molecular Mechanisms of Neurologic Injury Following Cardiopulmonary Bypass
Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2002; 6(1): 43 - 53.
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 Ann. Thorac. Surg.Home page
D. L. Reich, S. Uysal, M. A. Ergin, and R. B. Griepp
Retrograde cerebral perfusion as a method of neuroprotection during thoracic aortic surgery
Ann. Thorac. Surg., November 1, 2001; 72(5): 1774 - 1782.
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T. Sakamoto, S.'i. Hatsuoka, U. A. Stock, L. F. Duebener, H. G. W. Lidov, G. L. Holmes, J. S. Sperling, M. Munakata, P. C. Laussen, and R. A. Jonas
Prediction of safe duration of hypothermic circulatory arrest by near-infrared spectroscopy
J. Thorac. Cardiovasc. Surg., August 1, 2001; 122(2): 339 - 350.
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S. Westaby, K. Saatvedt, S. White, T. Katsumata, W. van Oeveren, and P. W. Halligan
Is there a relationship between cognitive dysfunction and systemic inflammatory response after cardiopulmonary bypass?
Ann. Thorac. Surg., February 1, 2001; 71(2): 667 - 672.
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 ChestHome page
S. Wan and A. P. C. Yim
Is Off-Pump Cardiac Surgery Better for the Brain?
Chest, January 1, 2001; 119(1): 1 - 1.
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P. Masetti and N. T. Kouchoukos
S-100{beta} protein: Yet uncertain role as a marker of cerebral injury in cardiac surgery
J. Thorac. Cardiovasc. Surg., October 1, 2000; 120(4): 830 - 831.
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