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Ann Thorac Surg 1997;63:492-496
© 1997 The Society of Thoracic Surgeons
Oxford Heart Centre and Department of Clinical Biochemistry, John Radcliffe Hospital, Oxford, England, and Department of Cardiothoracic Surgery, University Hospital of Lund, Lund, Sweden
Accepted for publication September 17, 1996.
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Abstract |
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 TopFootnotes Abstract IntroductionPatients and MethodsResultsCommentReferences |
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Methods. The level of S-100 protein was measured serially over 24 hours in 40 patients (27 undergoing aortic valve replacement, 9 mitral valve replacement, 4 closure of atrial septal defect) undergoing ICO and 20 patients undergoing CABG.
Results. The groups were similar with respect to age and cardiopulmonary bypass times. The S-100 level was not elevated before operation in any patient. Peak S-100 levels were reached at skin closure, when 35 of the ICO patients (88%) and 13 of the CABG patients (65%) had elevated S-100 levels. At skin closure peak S-100 levels were significantly greater in the ICO group (median [interquartile range], 0.76 [0.44–1.16] versus 0.3 [0–0.55] µg/L; p < 0.01). At 5 hours S-100 levels were still elevated in 22 patients in the ICO group compared with 1 patient in the CABG group (p < 0.01), and at 24 hours 17 ICO patients had persistently elevated S-100 levels in comparison with 2 in the CABG group (p < 0.01). One valve patient had a stroke 24 hours after operation accompanied by a secondary increase in the S-100 level. There was no significant difference in postoperative S-100 levels between 5 patients in the ICO group with a prior history of stroke and those without. The peak S-100 level correlated with patient age (r = 0.59; p < 0.001) but not with the duration of cardiopulmonary bypass or core temperature during the operation.
Conclusions. Intracardiac operation results in a significantly greater elevation in S-100 levels than CABG. Elevated S-100 levels correlate with increasing patient age but not with the duration of cardiopulmonary bypass or intraoperative core temperature. These findings raise the possibility that ICO patients may be more vulnerable to even subtle levels of cerebral injury than CABG patients.
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Introduction |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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The S-100 protein is an acidic, dimeric protein consisting of three isomers; 
, ß, and ßß, with the latter being present in high concentrations in glial and Schwann cells [4]. S-100 protein has been used as a diagnostic and prognostic tool in central nervous tumors, and increases in serum levels have been noted after stroke and cerebral injury [5, 6]. More recently, elevated serum levels have been detected after adult cardiac operations complicated by neurologic injury [7–11].
The purpose of the present study was to characterize serum levels of S-100 protein after intracardiac operation (ICO) and compare them with levels in a group of patients undergoing CABG.
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Patients and Methods |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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Patients
Forty consecutive adult patients undergoing ICO and 20 patients undergoing CABG at the Oxford Heart Centre were studied.
Anesthesia
Premedication was achieved with morphine (10 to 15 mg) and scopolamine (0.3 to 0.4 mg). Anesthesia was induced with fentanyl (1 mg), pancuronium (8 mg), and etomidate (4 to 10 mg). Anesthesia was maintained before CPB with a combination of oxygen, nitrous oxide, and halothane and during CPB with propofol (6 mg•kg-1•h-1). Benzodiazepines were not used.
Operation
All operations were performed with a pump flow of 2.4 L•m-2•min-1 at normothermia, reducing to a flow rate of 1.6 L•m-2•min-1 at 28°C. The ICOs were performed between 28°C and 37°C, whereas the CABG operations were performed at 34°C. The mean arterial pressure was pharmacologically maintained between 50 and 80 mm Hg. A Cobe CML membrane oxygenator (Cobe Cardiovascular, Inc, Arvada, CO) and a roller pump producing nonpulsatile flow were used without the use of an arterial line filter. Alpha-arterial stat CO2 tension management was employed. Myocardial protection was achieved with nonfiltered antegrade crystalloid cardioplegia (1 L St. Thomas' cardioplegic solution at 4°C repeated every 40 minutes as necessary) in the ICO group. In the CABG group the distal anastomoses were performed during brief periods (approximately 10 minutes) of aortic clamping and induced fibrillation. No topical cooling was employed, and there was no direct or indirect left ventricular venting. On completion of the distal anastomosis the aortic clamp was released and the proximal anastomosis was constructed after isolation of a portion of the ascending aorta in a side-biting clamp. If the heart did not defibrillate spontaneously, this was achieved with 10 to 20 joules of direct current.
Samples for S-100 Analysis
Blood samples (2 mL) were collected from central neck lines at induction of anesthesia, a half hour after the termination of bypass (equivalent to skin closure), and at 5 and 24 hours after the operation. The samples were centrifuged within an hour of collection to separate the serum, which was frozen to -20°C for batch analysis.
The Assay
The assay has been described in detail previously [9]. Briefly, the S-100 immunoradiometric assay (Sangtec 100; Sangtec Medical AB, Bromma, Sweden) is a monoclonal two-site immunoradiometric (sandwich) assay. The method is defined by the three monoclonal antibodies SMST 12, SMSK 25, and SMSK 28. The monoclonal antibodies detect the ßß and ß dimers. The sample is incubated with a plastic bead coated with monoclonal antibody to S-100. During this incubation, S-100 is bound to the antibody-coated bead. The bead is then washed to remove unbound material and incubated with iodine-125–labeled monoclonal antibody to S-100. This antibody binds to the S-100 captured by the bead antibody. After unreacted radioactivity antibody is washed off the bead, the radioactivity is measured using a gamma counter.
The amount of S-100 in the sample is then calculated using standards with known concentrations of S-100. The samples were analyzed in duplicate with the intention of rejecting any with more than 10% variation. This did not apply to any of the trial patients. A value of 0.2 µg/L in serum was the lower level of sensitivity of the assay. Levels in excess of 0.2 µg/L were considered pathologic.
Assessment of Neurologic Events
Any previous history of neurologic events was recorded. Postoperative neurologic status was assessed daily by clinical examination.
Statistics
Computerized statistical analysis was performed using the SPSS for Windows (release 6.1.1) statistical program. Clinical data are presented as means and standard deviations. Biochemical data are presented as median and interquartile range. Differences between groups were compared with the Mann-Whitney or 
2 tests. Correlations between peak S-100 levels and age, CPB time, and intraoperative temperature were calculated using the Spearman correlation coefficient.
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Results |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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. Ages and cardiopulmonary bypass times were similar in both groups.
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Serum S-100 Levels
Serial changes in S-100 levels are presented in Figure 1 and Table 2. The S-100 level was not elevated (> 0.2 µg/L) before sternotomy in any patient. Peak levels of S-100 were reached half an hour after the end of CPB (roughly equivalent to skin closure). At skin closure 35 ICO patients (87.5%) had elevated S-100 levels (median [interquartile range], 0.76 µg/L [0.44–1.16 µg/L]) in comparison with 13 patients (65%) in the CABG group (0.3 µg/L [0–0.55 µg/L). At 5 hours after the operation S-100 levels were still elevated in 22 patients in the ICO group compared with 1 in the CABG group, and the day after the operation 17 ICO patients had persistently elevated S-100 levels in comparison with 2 in the CABG group.
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Effects of Preoperative Neurologic Event
Five patients had a definite history of a previous neurologic event (transient ischemic attack or cerebrovascular accident), varying between 6 days and 20 years before the operation. None of these patients had an elevated preoperative S-100 level. All showed elevated postoperative S-100 levels, which returned toward normal the day after the operation, and none demonstrated new neurologic signs in the postoperative period. There was no significant difference in postoperative S-100 levels in patients with and without preoperative neurologic events.
Effects of Age, Duration of Cardiopulmonary Bypass, and Temperature
There was a weak but significant correlation between the peak S-100 levels and patient age (r = 0.59; p < 0.001) (Fig 2). No correlation was found between peak S-100 levels and the duration of CPB (Fig 3) or core temperature during the operation.
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Comment |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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The presence of a serum marker of cerebral injury would be of great benefit in both the quantification and investigation of the pathophysiology of subtle cerebral injury. S-100 protein is a dimeric protein consisting of three isomers whose ßß isomer is present in high concentrations in glial and Schwann cells [4]. Elevated serum concentration of S-100 ßß isomer correlates with proven cerebral injury [5, 6] and has recently been reported to increase after CPB [7–11]. Åberg's group [8], using a mock perfusion circuit and comparing patients undergoing cardiac and noncardiac operations, noted that peak S-100 levels were reached at the termination of CPB and concluded that elevated S-100 levels were not due to anesthesia, operation, or blood trauma but implied cerebral injury. Westaby and colleagues [9] confirmed that elevation in serum levels of S-100 did not occur in patients who underwent CABG without CPB and demonstrated a highly significant correlation of S-100 levels with the duration of CPB (r = 0.89; p < 0.01). Elevated serum levels of S-100 also correlate with the duration of total circulatory arrest during repair of the aortic arch despite the use of deep hypothermia and retrograde cerebral perfusion [10]. Most recently Johnsson and colleagues [11] have confirmed the relationship of elevated S-100 levels and neurologic injury during CPB and suggested that the magnitude of elevation in S-100 level may reflect the degree of cerebral injury.
In this study we characterized the pattern of release of S-100 during ICO (consisting of valve and atrial septal defect operation) and compared this with patients undergoing CABG. The two groups were very similar with respect to age and CPB times, but there were major differences in postoperative S-100 levels. In comparison with the levels in the CABG patients, S-100 levels in the ICS group were more frequently elevated, to a significantly greater magnitude, and remained significantly elevated for longer.
Our results imply that the brain is more susceptible to injury during ICO than during CABG. The major limitation of our study is that although significant elevations in S-100 levels have been correlated with overt cerebral injury, more modest elevations in S-100 have not been correlated with functional indices of subtle levels of cerebral damage as detected by neuropsychometric testing. Nevertheless, our findings are compatible with the generally perceived view of a higher incidence of cerebral injury in valve operations compared with CABG [12, 13] because of the greater likelihood of embolism of particulate or gaseous matter during ICO. To our knowledge, only one study has reported a higher postoperative incidence of central nervous system complications in CABG patients compared with valve patients [14]. The authors of that study suggested that their results reflected adverse epidemiologic features in the CABG patients, who were older with a higher prevalence of cerebrovascular disease and longer CPB times than valve patients [14].
Patients with a previous history of cerebrovascular accident are generally believed to be at greater risk of further cerebral injury during CPB [15]. Five of our valve patients had a previous history of neurologic injury, occurring between 6 days and 20 years before their cardiac operation. None of these patients had evidence of carotid artery disease or any overt evidence of cerebral injury in the postoperative period. As a group they did not have a higher S-100 level before or after CPB compared with patients without a prior history of cerebral insult. This implies that cerebral injury occurring long before a cardiac operation does not increase the risk of cerebral damage in patients without evidence of carotid artery disease. The patient who had suffered a stroke 6 days before the operation underwent aortic valve replacement because of gross cardiac failure. Her S-100 level was not elevated before the operation, and her peak level (0.97 µg/L) returned toward normal the next day. Only 1 patient in the ICO group suffered a stroke. This 88-year-old patient had a cerebrovascular accident the day after the operation accompanied by a secondary increase in her S-100 level, confirming the correlation between S-100 levels and obvious cerebral injury.
Our results show a weak but significant correlation between increasing age (but not intraoperative temperature or duration of CPB) and peak S-100 levels, suggesting an increased cerebral vulnerability to CPB in older patients. This would be consistent with the findings of other studies documenting advanced age as a major risk factor for postoperative central nervous system complications [16, 17]. Although there may be several mechanisms by which age increases the risk, the most likely explanation is the increasing prevalence of atherosclerosis with occult cerebrovascular disease as well as an increased risk of embolization [16].
In the ICO group we did not find a correlation between S-100 levels at skin closure and the duration of bypass. This is in contrast to the findings of Westaby and associates [9], who reported a highly significant (r = 0.89; p < 0.001) correlation between the duration of bypass and the peak S-100 levels in patients undergoing CABG. One possible explanation for this apparent discrepancy is that the effects of the duration of CPB on the brain are swamped by the effects of opening the heart in valve operations.
In summary, in comparison with CABG patients S-100 levels are more frequently elevated, to a greater level and for a significantly longer period, in ICO patients. These findings raise the possibility that ICO patients may be more vulnerable to even subtle levels of neurologic injury than CABG patients.
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Footnotes |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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References |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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