Journal of Cardiothoracic and Vascular Anesthesia
Volume 17, Issue 1 , Pages 4-9, February 2003

Are serum S100β proteins and neuron-specific enolase predictors of cerebral damage in cardiovascular surgery?☆☆☆

Department of Anesthesiology-Resuscitology, Yamaguchi University School of Medicine, Yamaguchi, Japan

Article Outline

Abstract 

Objective: To examine whether serum concentrations of S100β protein and neuron-specific enolase (NSE) are predictors of cerebral damage in cardiovascular surgery. Design: Prospective clinical study. Setting: University hospital. Participants: Eighteen patients with conventional cardiopulmonary bypass (CPB), 7 with selective cerebral perfusion (SCP), and 3 volunteers (blood samples). Interventions: None. Measurements and Main Results: S100β and NSE were measured in the blood obtained at 7 time points during and after operation. The concentrations of these markers in the blood from the surgical field and the cell-saver device, and the influence of graded hemolysis (in vitro) on the concentrations of these proteins were also examined. The mean values of S100β in the CPB group (2.08 ± 2.00 ng/mL) and the SCP group (1.46 ±0.77 ng/mL) were highest after aortic declamping and after termination of SCP, respectively. The mean values of NSE in the CPB group (29.1 ± 14.0 ng/mL) and the SCP group (31.2 ± 13.6 ng/mL) were highest after termination of CPB and at the end of the operation, respectively. Three patients suffered from cerebral complications, but the elevation of these markers during operation was indistinguishable from those in the other patients. Peak concentrations of S100β protein in the CPB group and NSE in the SCP group were correlated with the duration of aortic cross-clamping and CPB, respectively. S100β protein and NSE concentrations in the blood from the surgical field were significantly larger than those in arterial blood, whereas the concentrations in the blood in the cell-saving device were not elevated. The concentration of S100β protein was not influenced by the extent of hemolysis, whereas NSE concentration was markedly elevated by hemolysis. Conclusion: A large part of the increases in S100β protein and NSE during CPB and SCP is not attributed to neuronal damage, but to contamination with the blood from the surgical field. To determine whether these markers are useful to predict neurologic complications, it will be necessary to exclude contamination from the surgical field as observed in the present study. Copyright 2003, Elsevier Science (USA). All rights reserved.

Keywords:  S100β protein, neuron-specific enolase, cardiovascular surgery, neurologic complication

 

The incidence of neurologic complications such as stroke after cardiac surgery is 1% to 5%,1, 2 and these complications represent some of the leading causes of morbidity and disability after cardiac surgery.

Biochemical markers such as S100β protein and neuron-specific enolase (NSE) have been reported to be increased in serum after several kinds of cerebral injuries such as stroke,3, 4 subarachnoid hemorrhage,3, 5 trauma,6 and cardiac arrest.7 The increase of these markers is caused by a leakage into the peripheral blood after brain injury.3, 4, 5, 6, 7 In recent years, the increases in these markers have also been reported in cardiac surgery8, 9, 10, 11, 12, 13, 14, 15 and suggested as predictors of neurologic complications.9, 10, 11, 12, 13, 14 However, Derkach et al15 recently reported that S100β protein and NSE increased only in those who had operations with cardiopulmonary bypass (CPB) but not in the patients whose operation was performed without CPB.15 In addition, there was no significant difference of S100β protein and NSE concentrations between the patients with or without perioperative neurologic complications.

Regarding the surgical procedure, the incidence of neurologic complications is higher in cases of aortic surgery with selective cerebral perfusion (SCP) than conventional CABG surgery because of the limitation of cerebral blood flow and high incidence of embolization associated with complicated cannulation in SCP cases.16 Procedures without returning cardiotomy suction blood to the patients during CABG with CPB significantly attenuated the increase in serum S100β protein.17 The blood suctioned from the surgical field may therefore influence the serum concentration of this protein during cardiac surgery. Furthermore, most patients develop some degree of hemolysis during CPB, and it is known that serum concentration of NSE is influenced by hemolysis.18 However, the influence of the extent of hemolysis on S100β protein and NSE has not been systematically evaluated.

In the present study, the changes in serum concentration of S100β protein and NSE in the patients whose cardiovascular operation was performed with 2 different procedures for extracorporeal circulation, namely conventional CPB or CPB with SCP were examined. To explore the possibility of contamination, if any, from other sources, S100β protein and NSE in cardiotomy suction blood and blood collected into the cell-saving device were measured. In addition, the influence of graded hemolysis on the concentrations of these proteins was examined in vitro using the blood obtained from normal volunteers.

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Methods 

After obtaining approval from the Hospital Ethics Committee and written informed consent, 25 patients who underwent elective cardiovascular surgery using CPB were enrolled in this study. Patients were grouped on the basis of surgical treatment: a CPB group and an SCP group. The CPB group consisted of 18 patients who received either CABG (16) or valvular surgery (2). One patient in the CPB group had carotid endarterectomy (CEA) together with CABG. The SCP group consisted of 7 patients who received thoracic vascular surgery under SCP.

Most patients were premedicated with morphine (3-10 mg) and scopolamine (0.1-0.4 mg). Eight patients were premedicated with hydroxyzine (25 or 50 mg) or midazolam (1 or 2 mg) instead of morphine. Anesthesia was induced with midazolam and fentanyl and maintained with midazolam, fentanyl, and isoflurane (0.5%-1%). Pancuronium was used during induction of anesthesia, and, thereafter, vecuronium was used. The target doses of fentanyl and midazolam were 40 μg/kg and 0.4 mg/kg, but the doses used varied slightly depending on the duration of operation. Propofol (2-6 mg/kg/h) was used in 1 patient, and diazepam (10 mg) was used in combination with midazolam in 1 patient in the CPB group. Intra-aortic balloon pumping was used after induction of anesthesia in 1 patient in the CPB group because of a low ejection fraction (20%) evaluated before operation.

After heparinization (300 U/Kg), CPB was established with arterial cannulation through the ascending aorta and venous cannulation through the right atrium to the superior and inferior vena cava and with pump flow of 2.2 to 2.4 L/min/m2 at 32°C of esophageal temperature. The mean perfusion pressure was maintained pharmacologically between 50 and 70 mmHg. A membrane oxygenator and a roller pump were used with an arterial filter. CPB with pulsatile flow perfusion was performed in 3 patients with carotid artery stenosis and 1 patient with low creatinine clearance. In the SCP group, CPB was established in the same fashion as in the CPB group except that the arterial cannulation was done through the right or left femoral artery. Arterial cannulation from both axillary arteries and the left common carotid artery was added except in 1 patient, in whom SCP was performed with the aortic arch only through the right subclavian artery for a short period of time during distal graft anastomosis because the aneurysm was situated only in the ascending aorta. SCP was started at a rate of 10 mL/kg/min by a single roller pump with the same CPB reservoir at 21°C. Alpha-stat management was used in both groups. During CPB, blood from the surgical field was suctioned into the CPB circuits. Before and after CPB, the blood suctioned from the surgical field, as well as the blood remaining in the CPB circuit, was collected into a cell-saver device and centrifuged and washed with 1,000 mL of 0.9% NaCl in each process, then returned to the patient. Discontinuation of CPB was carried out with administration of both dopamine and dobutamine to maintain the cardiac index greater than 3 L/min/m2, mixed venous oxygen saturation greater than 70%, and systemic blood pressure greater than 90 mmHg.

Arterial blood samples were obtained at 7 time points: (1) after anesthetic induction, (2) after heparinization, (3) after aortic declamping or termination of SCP, (4) after termination of CPB, (5) at the end of operation, (6) 1 day after operation, and (7) 2 days after operation. S100β protein was analyzed in all patient samples, whereas NSE was analyzed in 11 and 6 patient samples in the CPB and SCP groups, respectively. Blood from the surgical field was also obtained in 5 patients in the CPB group at 2 time points (after heparinization and aortic declamping), and S100β protein and NSE were analyzed. Blood collected into the cell-saving device (3 patients in CPB group) was also analyzed for S100β protein and NSE.

S100β protein was measured by a monoclonal immunoluminometric assay (Sangtec 100; Sangtec Medical, Bromma, Sweden). NSE was analyzed using an enzyme immunoassay system consisting of purified antibodies specific for the α subunit of NSE (EIA-NSE; Amano P, Amano Enzyme CO, Nagoya, Japan). The coefficient of variation is 5.8% and 5.4% in the measurements of S100β and NSE, respectively.

To examine the influence of hemolysis on S100β protein or NSE concentrations, venous blood samples were obtained from 3 normal volunteers. Blood was hemolyzed with distilled water to obtain free hemoglobin at concentrations of 50, 100, 200, 300, 400, and 500 mg/dL in the serum and then S100β and NSE were measured.

The data are expressed as mean ± SD. Statistical analysis was performed using unpaired t-test and X2 test to compare the patient characteristics, risk factors for stroke, and intraoperative data between CPB and SCP groups. Repeated measurements analysis of variance was used to evaluate the time course and hemolysis effect of S100β protein and NSE concentration followed by Fisher Protected Least Significant Difference (PLSD) test. A Mann-Whitney U test was used to compare the S100β protein and NSE concentration between the serum of arterial blood and the blood from the surgical field or the cell-saving device. Simple regression analysis was used to examine the correlation between peak concentration of S100β protein or NSE and aortic cross-clamping time, CPB time, and age. A p value < 0.05 was considered statistically significant.

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Results 

Patients' characteristics, risk factors for stroke,19 and intraoperative data are presented in Table 1.

Table 1. Patients' characteristics, risk factors for stroke, and intraoperative data
CPB (n = 18)SCP (n = 7)
Age64 ± 1467 ± 12
Age > 7532
Male (female)7 (11)2 (5)
Unstable angina10
Diabetes mellitus40
History of neurologic disease20
History of vascular disease5 (3)†3
History of pulmonary disease34
Fentanyl dose (μg/kg)44 ± 1139 ± 8
Midazolam dose (mg/kg)0.45 ± 0.190.45 ± 0.14
Operation time (min)369 ± 83447 ± 80*
CPB time (min)175 ± 41205 ± 39
Ao clamp time (min)122 ± 35
SCP time (min) 92 ± 37
Neurologic complications21
*p < 0.05 compared with CPB group. †The number in the parenthesis indicates the patients with internal carotid artery stenosis.

NOTE. Values are mean ± SD.

Abbreviations: CPB, cardiopulmonary bypass; SCP, selective cerebral perfusion; Ao, aortic.

Two patients in the CPB group had a history of cerebral vascular disease and underwent valvular surgery. Three patients in the CPB group including one who received a CEA (having carotid bruit preoperatively) had internal carotid artery stenosis (greater than 50%) diagnosed by magnetic resonance angiography before operation, but they had no symptoms of cerebral ischemia. No patient had prior coronary artery bypass surgery.

The operation time in the SCP group was longer than that of the CPB group, but there was no significant difference in CPB time between the 2 groups. Postoperative neurologic complications were observed in 3 patients, 2 in the CPB group and 1 in the SCP group. In the CPB group, 1 patient had temporary left-sided hemiplegia lasting 24 hours and the other had a cerebral infarction (diagnosed by computer tomography 1 day after operation) with left-side hemiplegia after CABG with CEA (Glasgow Coma Scale [GCS 8]). In the SCP group, 1 patient had a temporary disturbance of consciousness (GCS 8) lasting 24 hours.

The changes in serum concentrations of S100β protein and NSE are shown in Figs 1 and 2, respectively.

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  • Fig. 1. 

    Time course changes of S100β protein. Mean ± SD (A), individual changes in the CPB group (B) and in the SCP group (C). Horizontal scale indicates the time points of sampling: 1= after anesthetic induction, 2=after heparinization, 3=after aortic declamp or termination of SCP, 4=after termination of CPB, 5=at the end of operation, 6=1 day after operation, 7=2 days after operation. At time point 7, n=5 and n=3 in the CPB group and SCP group, respectively. Solid symbols represent the patients with hemoglobinurina. Arrows represent the peak S100β protein concentrations of the patients who received valvular surgery. # P < 0.05 versus after anesthetic induction phase.

  • View full-size image.
  • Fig. 2. 

    Time course changes of NSE. Mean ± SD (A), individual changes in the CPB group (B) and in the SCP group (C). Horizontal scale indicates the time points of sampling: 1= after anesthetic induction, 2=after heparinization, 3=after aortic declamp or termination of SCP, 4=after termination of CPB, 5=at the end of operation, 6=1 day after operation, 7=2 days after operation. At time point 7, n=4 and n=3 in the CPB group and SCP group, respectively. Solid symbols represent the patients with hemoglobinurina. Arrow represents the peak NSE concentrations of the patient who received valvular surgery. # P < 0.05 versus after anesthetic induction phase.

In both groups, the mean values of S100β and NSE increased significantly at the time of aortic declamping or termination of SCP (time point 3), the termination of CPB (time point 4), and the end of operation (time point 5) compared with the values after anesthetic induction (time point 1). The mean values of S100β in the CPB group (2.08 ± 2.00 ng/mL, n = 18) and the SCP group (1.46 ± 0.77 ng/mL, n = 7) were largest after aortic declamp and after termination of SCP, respectively. The mean values of NSE in the CPB group (29.1 ± 14.0 ng/mL, n = 11) and the SCP group (31.2 ± 13.6 ng/mL, n = 6) were largest after the termination of CPB and at the end of operation, respectively. There was no significant difference between the 2 groups.

Individual changes in S100β protein and NSE in the CPB group are shown in Fig. 1, Fig. 2. The peak concentration of these proteins varied from 0.24 to 7.05 ng/mL or from 16.0 to 62.0 ng/mL, respectively. The concentration of S100β protein in 1 patient in the CPB group who exhibited cerebral infarction was slightly increased during operation (0.89 ng/mL) but decreased to normal concentration 1 day after operation. In this patient, S100β protein was elevated (2.46 ng/mL) 2 days after operation (NSE was not measured). In another patient in the CPB group who had temporary left-side hemiplegia lasting 24 hours after operation, S100β protein increased and reached its peak after aortic declamping (4.76 ng/mL), but decreased to a normal concentration (0.46 ng/mL) 1 day after operation when he was still hemiplegic. NSE also increased during operation (23.0 ng/mL, time point 3) and decreased to normal concentration 1 day after operation, but this value was indistinguishable from those in the other patients who had no neurologic complication.

In another 16 patients in the CPB group, no neurologic complications were observed even though many patients showed marked elevations of S100β protein and NSE, exceeding 0.50 and 20.0 ng/mL during operation. Their S100β protein and NSE decreased to a normal concentration 1 day after operation except in 1 patient in whom NSE concentration was still elevated 2 days after operation, but no neurologic deficit was observed.

Individual changes in S100β protein and NSE in the SCP group are shown in Fig. 1, Fig. 2, the peak values varying from 0.05 to 2.45 ng/mL and from 17.0 to 46.0 ng/mL, respectively. One patient in this group had a consciousness disturbance (GCS 8) lasting 24 hours, but the concentration of S100β protein was indistinguishable from those in the other patients. The concentration of NSE in this patient was 36.0 ng/mL at peak (time point 5) but returned to a normal concentration (14.0 ng/mL, time point 7) when he still had the consciousness disturbance. Some patients exhibited similar elevations of NSE but did not have any neurologic complication. There was a weak but significant correlation between peak concentrations of S100β protein and aortic clamping time in the CPB group (r = 0.57) and between NSE and CPB time in the SCP group (r = 0.8).

The S100β protein and NSE data in the serum of arterial blood, blood from the surgical field, and the blood collected into the cell-saving device in the CPB group are shown in Figs 3A and B.

  • View full-size image.
  • Fig. 3. 

    S100β protein (A) and NSE (B) concentrations in the serum of blood, blood from the surgical field (Surgical) and cell-saving device (Cell saver). Data are mean ± SD. * P < 0.05 versus serum concentration.

S100β protein concentration in the serum of blood in the surgical field was significantly larger than in the serum of arterial blood (after heparinization and after aortic declamping). The concentration of S100β in the serum of blood in the surgical field (52.5 ± 56.3 ng/mL) was approximately 375 times the concentration of serum (0.14 ±0.06 ng/mL) (after heparinization). NSE concentration in the serum of blood in the surgical field (249 ± 181 ng/mL) was also significantly larger after heparinization, the concentration was approximately 17 times the serum concentration (15.0 ±12.0 ng/mL). In contrast, in the blood of the cell-saving device, the S100β protein concentration (0.16 ± 0.12 ng/mL) was not significantly elevated, and the NSE concentration was even smaller (12.0 ± 3.0 ng/mL) compared with the serum concentration of arterial blood after CPB.

The influence of hemolysis on the concentrations of S100β and NSE is shown in Fig 4.

The concentration of S100β was not influenced by increasing of the extent of hemolysis up to a serum-free hemoglobin of 500 mg/dL. In contrast, NSE concentration was markedly influenced by hemolysis; the concentration was increased with increasing hemoglobin concentration in a concentration-dependent fashion.

Hemoglobinuria was seen in 4 patients of the CPB group and 1 patient of the SCP group (Fig. 1, Fig. 2, solid symbols), and haptoglobin was used in these cases after CPB. The levels of serum-free hemoglobin were not measured in these cases.

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Discussion 

S100β protein is one of the isoforms of the S100 protein and is known to be contained in glial cells in high concentration. NSE is one of the isoforms of a glycolytic enzyme richly localized in neurons. Some reports have suggested that elevation of serum concentrations of these proteins was expected as markers of cerebral damage in cardiac surgery.9, 10, 11, 12, 13, 14 However, this issue is still controversial.

In the present study, S100β protein and NSE were increased in many patients during cardiac surgery performed using CPB, and the elevation of these proteins was correlated with the time of aortic cross-clamping and CPB. The patterns of the changes of these proteins in 3 patients who exhibited postoperative neurologic complications were indistinguishable from those with no neurologic complications. The concentrations of these proteins in the blood suctioned from the surgical field was significantly greater than that of arterial blood. Graded hemolysis (in vitro) did not influence S100β protein but increased NSE. These results indicate that the blood suctioned from the surgical field can contribute to elevation of serum S100β protein and NSE.

Johnsson et al10 first reported an association of the elevation of serum S100β protein with neurologic complications in cardiac surgery; the measurements of S100β protein were done on the second postoperative day, but not during the operation. In a report that showed larger elevations of S100β protein in patients who had carotid artery stenosis, no patient suffered from cerebral complications.11 In other reports that showed elevations of S100β protein and NSE, the surgical procedures were complicated, requiring either prolonged CPB,12 aortic cross-clamping,14 or deep hypothermic CPB and retrograde cerebral perfusion.15 Thus, it is possible that some factors other than neuronal damage may have contributed to the elevation of these proteins during cardiac surgery.

In Jönsson et al's large series,13 S100β protein elevation was associated with prolonged CPB time, advanced age, pre-existing cerebrovascular disease, or the presence of an atheromatous aorta. In the present study, the elevation was correlated with the duration of aortic cross-clamping (in the CPB group) and CPB (in the SCP group), but there was no significant correlation between age and peak concentration of S100β protein and NSE or differences in the peak concentration of S100β protein or NSE between the SCP and CPB groups. The S100β protein concentrations in 5 patients who had carotid artery stenosis or cerebral infarction diagnosed before operation (including the case with cerebral infarction perioperatively) were not large.

In the present study, the concentration of S100β protein in the surgical field was markedly elevated, whereas the concentration in the blood of a cell-saving device after processing was not elevated. These results are in accordance with recent reports that showed no or only small elevation of S100β protein in off-pump CABG, where the blood from the surgical field was suctioned into the cell-saving device and returned to the patients.15, 20, 21 The elevation of S100β protein was not great even in the CABG patients under conventional CPB, when all blood from the surgical field was collected in the cell-saving device and then infused.17 The concentration of NSE in the blood suctioned from surgical fields was also markedly elevated. It is known that NSE is contained not only in cerebral tissue but also in bone marrow matrix,22, 23 red blood cells, and platelets.23, 24 Thus, the increase in NSE during operation could well be because of the contamination derived from these tissues and cells. The concentration of NSE in the blood from the cell-saving device was not elevated. This probably explains why NSE did not increase significantly in off-pump CABG in which suctioned blood from the surgical field was transfused after processing in the cell saver.15

Hemolysis itself did not influence the concentration of serum S100β protein tested in vitro. Thus, the large concentration of this protein in the blood suctioned from surgical fields is caused by some factors other than hemolysis. It has been found that S100β protein is localized mainly in glia, but it also has been detected in extracerebral tissues such as fatty tissue25 and thymus.26 Thus, the elevation of S100β after sternotomy and manipulation of the intrathoracic cavity could be attributed to the leakage from fatty tissue and thymus.

In contrast, elevation of NSE was dependent on the grade of hemolysis determined in vitro. Hemolysis with a free-hemoglobin concentration of 500 mg/dL provided NSE concentrations up to 48.0 ±5.0 ng/mL. Therefore, if the red blood cells were broken mechanically during CPB, serum NSE concentration would be substantially increased.

Hemoglobinuria, which is observed when plasma hemoglobin is 150 mg/dL or greater, is a phenomenon relatively frequently observed during CPB. The concentration of plasma hemoglobin can be 500 mg/dL in severe hemolysis cases with CPB.27 In the present clinical study, hemoglobinuria was seen in 4 patients of the CPB group and 1 patient of the SCP group. Because the levels of plasma-free hemoglobin were not measured in these cases, the extent of contribution of hemolysis cannot be quantified. However, the elevation of NSE in the patients could be caused in part by hemolysis as reported by Gao et al.18

There may be a limitation in precise evaluation of the difference between the groups and of the correlation between the serum S100β and NSE concentrations and neurologic complications because of the small and unequal sample size of the groups and of the variations in the surgical procedure. However, the present study suggests the possibility that the elevation of S100β protein and NSE during cardiovascular surgery is attributed to a contamination of non-neuronal origin.

In conclusion, the concentrations of S100β protein and NSE increased during CPB and SCP. A large part of the increases in these markers appears to be attributed to contamination of the blood from the surgical field. The results suggest that these markers are not reliable to predict cerebral complications in cardiac surgery when suctioned blood is returned to the circulation without cell-saving processing or when severe hemolysis occurs. It needs to be determined whether these markers are useful to predict neurologic complications by excluding the contamination observed in the present study.

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References 

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☆ Supported in part by the Young Researcher Project of the Venture business Laboratory, Yamaguchi University and in part by the Ministry of Education, Science, Sports and Culture (Grant No 12671474. to Kazuyoshi Ishida).

☆☆ Address reprint requests to Kazuyoshi Ishida, MD, Department of Anesthesiology-Resuscitology, Yamaguchi University School of Medicine, 1-1-1 Minami-Kogushi, Ube, Yamaguchi 755-8505, Japan. E-mail: kazuyo@yamaguchi-u.ac.jp.

PII: S1053-0770(02)47702-6

doi:10.1053/jcan.2003.2

Journal of Cardiothoracic and Vascular Anesthesia
Volume 17, Issue 1 , Pages 4-9, February 2003

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