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Ann Thorac Surg 2001;71:1512-1517
© 2001 The Society of Thoracic Surgeons

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Original article: cardiovascular

Increase in serum S100A1-B and S100BB during cardiac surgery arises from extracerebral sources

^a Department of Cardiothoracic Anaesthetics and Intensive Care, Karolinska Hospital, Stockholm, Sweden
^b Department of Clinical Chemistry, Karolinska Hospital, Stockholm, Sweden
^c Department of Thoracic Surgery, Karolinska Hospital, Stockholm, Sweden
^d CanAg Diagnostics AB, Gothenburg, Sweden

Accepted for publication December 13, 2000.

Address reprint requests to Dr Anderson, Department of Cardiothoracic Anaesthetics and Intensive Care, Karolinska Hospital, S-171 76 Stockholm, Sweden
e-mail: russell.anderson{at}kirurgi.ki.se

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Elevated levels of serum S100B after coronary artery bypass grafting may arise from extracerebral contamination. Serum S100B content was analyzed in several tissues, and the two dimers S100A1-B and S100BB were analyzed separately in blood.

Methods. Serum, shed blood, marrow, fat, and muscle were studied in patients undergoing coronary artery bypass grafting with cardiopulmonary bypass using suction either to the cardiotomy reservoir (group 1, n = 10) or to a cell-saving device (group 2, n = 10), or operated on off-pump (group 3, n = 10).

Results. Serum S100B was sixfold higher in group 1 than in groups 2 and 3, which were identical. The same ratio between S100A1-B and S100BB was found in all groups. When compared with serum, S100B was 10² to 10⁴ times higher in marrow, fat, muscle tissue, and shed blood.

Conclusions. Separate analysis of S100A1-B and S100BB did not distinguish between S100B of cerebral and extracerebral origin. The concept that S100B only originates in astroglial and Schwann cells is wrong. Fat, muscle, and marrow in mediastinal blood contain high levels of S100B. Cardiopulmonary bypass caused no increase in S100B.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
When cardiac operations are performed on older and sicker patients, neurologic complications occur more often. In a multicenter, prospective, randomized study, Roach and colleagues [1] found neurologic injury in 6.1% of patients undergoing coronary artery bypass grafting (CABG). Postoperative cognitive and intellectual dysfunction is even more frequent, occurring in almost 50% of patients when carefully examined by neuropsychological tests [2]. An easy biochemical test that could quantify both the severe and the more subtle neurologic injury, a "troponin T of the brain," would be a major step forward in evaluating the cerebral injuries of cardiac operations. Various serum biochemical markers of brain damage have been investigated [3], among which S100B has been among the most promising. The 50- to 100-fold increase in serum S100B observed after cardiac operations [4–7] correlates with duration of cardiopulmonary bypass (CPB) and aortic occlusion [4, 6], the number of coronary anastomoses [6], and the number of emboli counted by transcranial Doppler during the period between aortic cannulation and cross-clamp onset [8]. These and other findings have supported the association between CPB, microembolization, and brain damage. Additional support comes from observations that this increase is attenuated with the use of an arterial filter [9] and virtually eliminated in off-pump CABG [6]. S100B release is prolonged after perioperative strokes [5] and elevated after strokes in general outside the surgical setting [10]. However, correlation with postoperative cognitive deficits is unclear [11, 12].

With the improved sensitivity of the commercial S100B immunoassay, evidence began to accumulate that implicated the presence in serum of an extracerebral S100B contaminant. A small and previously undetectable increase in serum S100B was observed shortly after the start of CABG procedures, even before aortic cannulation [6]. In addition, after off-pump CABG, a similar increase in serum S100B was seen that remained relatively unchanged for 2 days after the operation and was not quite normalized after 6 days [6]. At the same time there were reports of high S100B immunoreactivity in blood shed through chest drains, first detected as postoperative peaks in serum S100B when autotransfusion was used [11]. Finally, blood from the midline incision, sternal bone marrow, and in a cell-saving reservoir when it replaced the standard cardiotomy suction [7, 11] were shown to contain 5 to 50 times more S100B than serum. Although a minimal contribution from cerebral sources to the serum S100B concentration seen after cardiac operation cannot be excluded, the dominating contribution is extracerebral [7, 11].

S100B is not a unique protein, but rather denotes collectively all S100 dimers that contain at least one ß monomer subunit [13]. The commercial immunoassay detects the ß-subunit and thereby determines the summed concentrations of at least two constituent subtypes included in S100B. These subtypes are denoted as S100BB and S100A1-B, depending on whether they are ßß-homodimers or ß-heterodimers.

The present study was motivated by the hope that the extracerebral S100B contaminant seen after CABG procedure would be predominantly either S100A1-B or S100BB, and thus the other could be used as a specific marker for cerebral tissue damage. Specific antibodies were used to determine the individual serum concentrations of S100A1-B and S100BB in patients undergoing CABG with conventional CPB using the cardiotomy suction, with CPB using a cell-saving device, and off-pump CABG. The source of possible extracerebral contamination was also addressed by measuring the concentrations of S100 in adipose tissue, bone marrow, skeletal muscle, and blood shed from the midline incision and postoperative chest drains.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Patients population and groups
Patients undergoing elective CABG were studied after approval from the hospital’s ethics committee and patient informed consent. Only patients with normal hemoglobin content and without cerebrovascular, carotid, or other complicating diseases were included. None had a history of heart failure or severely reduced myocardial function. All patients had sinus rhythm and received their normal anti-angina medications on the morning of operation.

Patients were premedicated with morphine (7.5 to 15 mg). Anesthesia was induced with 10 µg/kg fentanyl and 70 µg/kg midazolam, and the patients were paralyzed with 0.1 mg/kg pancuronium. Mannitol (400 mg/kg) was given before CPB. Anesthesia was maintained by continuous infusion of fentanyl (5 µg/kg^-1 · h^-1) and midazolam (50 µg/kg^-1 · h^-1) until completion of the operation.

Three groups of patients (n = 10 in each group) undergoing elective CABG procedures were examined (a fourth group of thoracotomy patients was examined; see below): (1) a control group using standard CPB including cardiotomy reservoir suction; and (2) a group using CPB without cardiotomy suction, but using a cell-saving device (Shiley Therapeutic Autotransfusion System, Dideco Shiley SpA, Modena, Italy). These patients were partly described earlier [6] together with the S100B results. (3) A third group had off-pump CABG with sternotomy (7 of these were described earlier [7]). All patients received the left internal thoracic artery grafted to the left anterior descending coronary artery. Other vessels were bypassed with saphenous vein grafts.

Standard nonpulsatile CPB with centrifugal pumps was used for the first two groups. The extracorporeal system was primed with Ringer’s acetate solution, and a Maxima Forte (Medtronic Inc, Minneapolis, MN) membrane oxygenator was used with no arterial filters. Cold blood cardioplegia was used in all patients. Core temperature was cooled or was allowed to drift to 34°C. Distal anastomoses were made during cardioplegic arrest, whereas proximal anastomoses were sutured with resumed perfusion and a side-biting clamp. Norepinephrine or nitroprusside infusions were used to strive for a mean arterial pressure during CPB of 70 mm Hg. Perioperative data are given in Table 1.

All samples were immediately sent for centrifugation, freezing (-20°C), and blinded analysis.

S100 assays
A blinded batch immunoassay was performed using the commercial Sangtec 100B LIA assay (Sangtec Medical, Bromma, Sweden). This method detects the ß-subunit of S100. S100B immunoreactivity concentration represents the summed concentrations of S100A1-B and S100BB. The functional detection limit of the assay is 0.02 µg/L.

The other assays used the enzyme-labeled immunosorbent assay method [14] for measuring S100A1-B and S100BB (CanAg Diagnostics AB, Gothenburg, Sweden). Monoclonal antibodies against S100 were established by immunization with S100B, and fusion of spleen cells with Ag8 x P63 myeloma cell line. Hybridomas producing antibodies reacting with S100BB and S100A1-B, but negative for S100A1-A2, were selected, and monoclonal antibodies were produced by in vitro cultivation. The functional detection limits are similar to the Sangtec S100B assay.

After wet weights were determined, tissue samples were homogenized and diluted (NaCl 150 mM, calcium lactate 10 mM, Tris 15 mM; pH 7.4) before S100B analysis. S100A1-B and S100BB were not determined for the solid tissues as the research assays were only optimized for serum samples, and the assays showed poor dilutional behavior in buffer extracts of tissues.

Statistics
Serum concentrations are presented as mean ± standard deviation unless otherwise specified. Data with a wide range are given as median values with 25th and 75th percentiles. Data were compared using two-way analysis of variance. The criterion for significance throughout was p value less than 0.05.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The postoperative course was uncomplicated in all patients. In particular, no clinically apparent neurologic injury occurred. During conventional CABG with cardiotomy suction serum S100B concentration increased to a maximum at the end of CPB (Fig 1). Serum S100B concentration is seen to correspond approximately to the sum of S100A1-B and S100BB, and all components followed the same time course. Concentrations from all three assays increased before cannulation (p < 0.01).

View larger version (15K): [in this window] [in a new window]   Fig 1. Serum S100B, S100A1-B, and S100BB concentrations before, during, and after operation with cardiopulmonary bypass (CPB) with cardiotomy suction. Further sampling indicates the number of hours after operation. All values are mean ± standard deviation (n = 10). (Pre-op = after anesthesia, before start of operation; ACT = 5 minutes after heparin administration; End CPB and End op = at the end of CPB and operation, respectively.)

View larger version (13K): [in this window] [in a new window]   Fig 2. Serum S100B, S100A1-B, and S100BB concentrations before, during, and after operation with cardiopulmonary bypass without a cardiotomy suction, but with the use of a cell-saving device. Further sampling indicates the number of hours after operation. All values are mean ± standard deviation (n = 10). (Pre-op = after anesthesia, before start of operation; ACT = 5 minutes after heparin administration; End op = at the end of operation.)

View larger version (21K): [in this window] [in a new window]   Fig 3. Serum concentration of (a) S100B, (b) S100BB, and (c) S100A1-B after operation with cardiopulmonary bypass and cell-saving device suction (solid diamonds) and without cardiopulmonary bypass (solid squares). Further sampling indicates the number of hours after operation. All values are mean ± standard deviation (n = 10). (Pre-op = after anesthesia, before start of operation; ACT = 5 minutes after heparin administration; End op = at the end of operation.)

View larger version (13K): [in this window] [in a new window]   Fig 4. Serum concentrations of S100B, S100A1-B, and S100BB in chest drain blood after operation with cardiopulmonary bypass. Further sampling indicates the number of hours after operation. All values are mean ± standard deviation (n = 7). (End op = end of operation.)

View larger version (24K): [in this window] [in a new window]   Fig 5. S100B concentrations in tissues (µg/g) and blood (µg/L) during coronary bypass grafting. (1 = skeletal muscle; 2 = sternal bone marrow aspirate; 3 = mediastinal fat; 4 = blood in cell-saving reservoir; 5 = drain blood 6 hours after operation; 6 = serum at end of conventional coronary artery bypass grafting; 7 = serum at end of conventional coronary artery bypass grafting using cell-saving device; 8 = serum at end of off-pump coronary artery bypass grafting.)

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

Although there are several types of monomer subunits comprising the 17 different dimeric proteins included in the S100 family [13], the ß-subunit has received the greatest attention because it is reportedly found mainly in Schwann and astroglial cells. It has also been found in melanocytes, adipocytes, chondrocytes, and epidermal Langerhans cells. An -subunit is found in astroglial cells together with a ß-subunit (denoted S100A1-B) and as a homodimer (S100A1-A2) in striated muscle, heart, and kidney. The commercial immunoassay used in all recent studies uses several different monoclonal antibodies directed against the ß-subunit of these dimeric proteins, and any members of the S100 family that do not contain at least one ß-subunit should not be detected [13]. No ß-containing dimer other than S100A1-B or S100BB is known. The present study used monoclonal antibodies specific for either the - or ß-subunit, and the two-stage analysis specifically quantitates the S100A1-B and S100BB dimers separately [14]. As recently reported [7], the increase in serum S100B immunoreactivity after cardiac procedures with CPB is an artifact caused by an overwhelming contamination of extracerebral S100. Blood shed from the surgical wound contains very high concentrations of S100, which is introduced into the circulation through the cardiotomy suction [7, 11], and can account for all of the extra serum S100B seen at the end of conventional CABG. Jönsson and coworkers [11] calculated a correction factor for this contamination on the basis of the assumptions that extracerebral contribution would decay postoperatively with a 1-hour half-life and that the contamination process ended with the operation. When a cell-saving device replaced the cardiotomy suction, serum S100B immunoreactivity, measured at the end and 6 hours and a day after CABG, was no higher than after off-pump operation [6, 7]. Thus, the use of CPB did not make a detectable increase in serum S100.

The extracerebral contamination of serum S100 does not end with cessation of the cardiotomy suction, but is an ongoing process that lasts for days after the operation, as seen after off-pump CABG [6]. Separate assay of S100A1-B and S100BB did not discriminate between S100 from cerebral and extracerebral sources. The high concentrations of S100A1-B and S100BB in the cell-saving reservoir explain the high serum concentrations observed when cardiotomy suction blood is returned to the patient. Serum S100A1-B and S100BB did not differ after off-pump CABG and CABG with CPB but without cardiotomy suction. Thus, the present study supports the hypothesis that CPB does not contribute a detectable amount of S100 to serum.

The origin of the serum S100B, S100A1-B, and S100BB seen after CABG off-pump and after CPB when using a cell-saving device remains to be discussed. However, several findings make it quite unlikely that any of the serum S100B originates from the brain. First, the increase in serum S100B occurred early during the procedure, and was at the time of cannulation at the same level as the maximum concentrations seen during off-pump operation and during operation with CPB using a cell-saving device. Second, the concept that S100B only originates in astroglial and Schwann cells is wrong. Even though nonnervous tissues may have low S100B concentrations relative to nervous tissues, individual cell concentrations are less relevant than the amount of S100B freed by the surgical versus supposed embolic cerebral trauma. S100B from the traumatized tissues (muscle, fat, bone marrow) results in a large concentration gradient between mediastinal blood or injured tissue and the circulating blood. This concentration gradient may easily cause an uptake into the bloodstream through capillaries and the lymphatic system of the small (11 kd) S100 monomer. Iodine-labeled albumin, six times the molecular weight of the S100 monomer, is absorbed into serum after being applied to the eye and lacrimal system [15] and in the pericardium [16]. There is no production or release of S100B in the blood itself.

One can only speculate on the published correlation between S100B after CABG and various other variables. Duration of CPB or number of anastomoses [6] may contribute to the amount of blood in the surgical field or duration of use of cardiotomy suction. Arterial filters in the CPB could conceivably remove some particulate sources of S100 passed through the cardiotomy suction filter, whereas the lower S100B observed when using a heparinized CPB system may be related to less bleeding and less use of cardiotomy suction. Most of the observed correlations between S100B and characteristics of patients or the surgical procedure may indeed be related to use of the cardiotomy suction. A longer-lasting operation or a more difficult patient population will result in greater use of the cardiotomy suction with increased return of mediastinal blood to the circulation. The weak correlation found between cognitive deficits and S100B most probably reflects such an indirect, and not a causal, relationship.

Serum S100B increases after strokes in nonsurgical patients [17], and this study does not affect its value as a marker of brain tissue damage in such patients. Wong and Bonser [18] have shown that effluent blood from the brain contains more S100B than blood used for retrograde cerebral perfusion during deep hypothermic arrest for aortic arch surgical procedures, suggesting increased permeability of the blood–brain barrier and perhaps brain tissue injury in that setting. The present study does not address CABG patients with gross postoperative neurologic deficits in whom serum S100B is both elevated and prolonged [5]. However, for several days after operation [6], variable amounts of extracerebral S100B in serum in stroke patients will confound the interpretation of those studies and diminish the predictive value of S100.

The present study does not answer the question of whether CPB causes brain tissue damage with the release of S100B into cerebrospinal fluid. Only cerebrospinal fluid sampling will provide conclusive evidence. Van Dongen and associates [19] compared S100B in serum and cerebrospinal fluid when using partial CPB for repairing aneurysms of the descending aorta. They also compared S100B in serum and cerebrospinal fluid in thoracotomized patients undergoing repair of the descending aorta using partial, not full, CPB [19]. Using an older S100B assay (detection limit 0.2 µg/L) they observed no increase in serum S100B in these thoracotomized patients, although S100B in cerebrospinal fluid tripled, an increase they attributed to spinal cord ischemia and correlated with motor evoked potentials. Using an assay with 10-fold increased sensitivity, serum S100B in patients undergoing off-pump CABG by means of a thoracotomy was shown to increase to 0.2 µg/L, the detection limit of the earlier assay method [6].

In summary, S100B is far from brain specific, and in cardiac operations, with the use of a cardiotomy suction, there are a variety of extracerebral sources of contamination. Separate analysis of the dimers S100A1-B and S100BB does not distinguish between S100B of cerebral and extracerebral origins. No detectable contribution from the brain that is attributable to CPB was found in the absence of gross neurologic deficits. Previous studies using the early release of S100B may have investigated an artifact.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
We gratefully acknowledge the technical assistance of Gunilla Barr and Rumjana Dijlai-Merzoug. This study has been supported by the Swedish Heart Lung Foundation, the Swedish Medical Research Council (grant no. 11235), Sigurd och Elsa Goljes Minne, and Vrdalstiftelsen.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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