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J Thorac Cardiovasc Surg 2003;126:1504-1512
© 2003 The American Association for Thoracic Surgery

Cardiopulmonary support and physiology

Physiological coagulation can be maintained in extracorporeal circulation by means of shed blood separation and coating

^a Department of Cardiothoracic and Vascular Surgery,^a Friedrich-Schiller-University-Hospital, Jena, Germany
^b Department of Internal Medicine,^b Leipzig University, Leipzig, Germany
^c Department of Clinical Chemistry,^c Friedrich-Schiller-University-Hospital, Jena, Germany
^d Department of Medical Statistics, Informatics, and Documentation,^d Friedrich-Schiller-University Hospital, Jena, Germany

Received for publication September 26, 2002; revisions received February 10, 2003; revisions received June 16, 2003; accepted for publication June 18, 2003.

^* Address for reprints: Johannes M. Albes, MD, Department of Cardiovascular Surgery, Heart Center Brandenburg, Ladeburger Str 17, 16321 Bernau-Berlin, Germany
j.albes{at}immanuel.de

	Abstract

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OBJECTIVE: Conventional extracorporeal circulation results in an activation of coagulation cascades. Coating of extracorporeal circulation tubes as well as avoidance of shed blood recirculation have been shown to reduce these phenomena. We evaluated a new shed blood separation system (AVANT D 970) utilizing a coated cardiopulmonary bypass tube system (PHISIO).

METHODS: Forty patients (62 ± 10 years) underwent isolated coronary revascularization. Four groups (n = 10/group) were defined: no extracorporeal circulation, conventional uncoated extracorporeal circulation, uncoated extracorporeal circulation with shed blood separation, and coated extracorporeal circulation with shed blood separation. Thrombin-antithrombin complex and free Hb were analyzed and statistically compared.

RESULTS: Conventional extracorporeal circulation exhibited the highest intraoperative activation of coagulation (thrombin-antithrombin complex: extracorporeal circulation, 31.1 ± 15.8 µg/L; uncoated extracorporeal circulation with shed blood separation, 15.3 ± 7.8 µg/L; coated extracorporeal circulation with shed blood separation, 8.1 ± 4.8 µg/L; no extracorporeal circulation, 2.4 ± 0.6 µg/L; P < .05 extracorporeal circulation vs all others) and red blood cell damage (free Hb: extracorporeal circulation, 16.8 ± 11.4 µmol/L; uncoated extracorporeal circulation with shed blood separation, 10.3 ± 3.5 µmol/L; coated extracorporeal circulation with shed blood separation, 6.8 ± 2.9 µmol/L; no extracorporeal circulation, 3.4 ± 1.1 µmol/L; P < .05 extracorporeal circulation vs no extracorporeal circulation, coated extracorporeal circulation with shed blood separation). Coated extracorporeal circulation with shed blood separation showed only slight activation and cell trauma, which did not differ significantly from no extracorporeal circulation.

CONCLUSIONS: Combination of coating and avoidance of shed blood recirculation maintained physiological coagulation levels and markedly reduced red blood cell trauma in extracorporeal circulation procedures. These combined modalities may therefore offer an alternative for off-pump procedures in patients with contraindications for conventional extracorporeal circulation.

	Material and methods

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Demographic data
Forty patients (62 ± 10 years) underwent isolated elective coronary revascularization for single-, double-, or triple-vessel disease. All patients had sinus rhythm and a preoperative ejection fraction of more than 35% and all exhibited normal renal and hepatic function (serum creatinine < 100 µmol/L; prothrombin time > 70%). None of the patients was on anticoagulatory medication with coumarin, and all patients received chronic medication with acetylsalicylic acid until 7 days preoperatively (100 mg daily dose).

Operation
The patients were operated on according to clinical and morphological criteria. Conventional coronary revascularization with cardiopulmonary bypass (CPB) was performed for double- or triple-vessel disease. Minimally invasive arterial revascularization (MIDCAB) without CPB was performed in patients with single-vessel disease. In all CPB patients the left internal thoracic artery and a respective number of vein grafts/anastomoses were used. All patients operated on with CPB underwent total median sternotomy, preparation, and harvesting of the left internal thoracic artery after the pleura was opened, combined with conventional open venous harvesting. In all MIDCAB patients the left internal thoracic artery was prepared via a left anterior thoracotomy and was anastomosed to the LAD with mechanical stabilization while the heart was beating.

Study protocol
The study protocol was approved by the local ethical committee on human research. All patients who agreed to participate in this trial gave written informed consent. The patients with double- or triple-vessel disease were randomly allocated to 1 of the CPB groups. The patients with single-vessel disease were uniformly allocated to the MIDCAB group. Four groups (n = 10) were defined: noECC, MIDCAB; ECC, conventional extracorporeal circulation without coating and shed blood separation; ECCSBS, uncoated ECC with shed blood separation system; CECCSBS, coated ECC with shed blood separation system.

Anesthesia
All patients received general anesthesia, conventional intubation, and ventilation. MIDCAB patients received a double lumen tracheobronchial tube to perform intermittent unilateral ventilation. After premedication with benzodiazepine, general anesthesia was induced and maintained with propofol, skeletal muscle relaxation with pancuronium bromide, and volatile anasthetics (isoflurane). Standard monitoring was established. Prior to institution of CPB all patients received 400 IU/kg of body weight (BW) intravenous heparin and additional doses, if required, to maintain an activated clotting time (ACT) of over 400 seconds during CPB. ACT (automated coagulation timer ACT II; Medtronic HemoTec Inc, Englewood, NJ) was measured directly after initial heparin administration and every 20 minutes thereafter until the end of the procedure. Volatile anesthetics (Sevoflurane; Dräger AG, Bremen, Germany) were given via the heart-lung machine during extracorporeal circulation. MIDCAB patients received 100 mg/kg BW heparin intravenously after left internal thoracic artery preparation. After completion of the anastomosis heparin was partially antagonized with 50 mg/kg BW protamine.

General extracorporeal circulation modalities
Extracorporeal circulation modalities (Stöckert SIII, Stöckert Instruments, Munich, Germany) comprised 3-point pressure monitoring (pre- and postoxygenator, arterial line; x-trans; Smith Medical Inc, Kirchseeon, Germany) and online blood gas analysis (CDI 500; Terumo CVSE Inc, Borken, Germany). Priming consisted of 900 mL Ringer's solution, 400 mL HES 6% (poly(O-2-hydroxy-ethyl-starch), 250 mL mannitol, 10000 U heparin, 2 million U aprotinin, and 20 mL NaHCO₃. Extracorporeal circulation was instituted in all patients via a 24F central aortic cannula (Jostra AG, Hirrlingen, Germany), a central 2-stage venous cannula 50/36-French (Stöckert Instruments), and a main circulatory roller pump (Stöckert Instruments). The blood was drained into a cardiotomy reservoir (AVANT Reservoir D970; Dideco Inc, Mirandola, Italy), pumped through a conventional oxygenator (AVANT-Oxygenator, Dideco Inc), and filtered (D734, Dideco Inc) back into the patient at a rate of 2.5 L/min/m² body surface area. Shed blood suction was performed with a roller pump (Stöckert Instruments). Moderate hypothermia of 33° to 34°C was employed. A regular vacuum suction was additionally used to clear the operative field. The system consisted of a disposable suction cannula and tube connected with a sterile heparinized chamber. The aspirated blood was processed in a cell saver, and debris and fat were removed by an integrated 200-µm filter (Compact A 75173, Dideco Inc). Electrical fibrillation was applied and the aorta was crossclamped. Antegrade cold blood cardioplegia (blood cardioplegia "Buckberg," cardioplegia systems with "CSC14," Dideco Inc) mixed from buffer solution and autologous blood circulating in the CPB was delivered via a roller pump and a heat exchanger at 4°C. After revascularization weaning from CPB was performed in the typical fashion. Thereafter, all patients received 1:1 protamine to antagonize heparin. The thorax was closed and the patient was transferred to the intensive care unit (ICU). The erythrocytes processed in the cell saver were substituted directly after arrival on the ICU. Drainage loss was measured using the calibration of a closed evacuation system (PLEUR-EVAC Sahara; Genzyme GmbH, Neu-Isenburg, Germany).

Specific extracorporeal circulation modalities
Shed blood separation used in the ECCSBS group as well as in the CECCSBS group was performed with the aforementioned cardiotomy reservoir (AVANT D970). The simple system consists of a reservoir with a separation chamber positioned on top of the main chamber. Sucked blood is drained into the separation chamber and runs freely through it into the main chamber as long as separation is not desired. If separation is indicated, the connecting tube is mechanically closed so that the blood remains in the separation chamber (Figure 1). In case of an acute volume demand the connecting tube can be reopened at any time, which was not necessary in the study. After weaning from CPB the separated shed blood was processed in a cell saver together with conventionally aspirated blood from the operating field. In the CECCSBS group a tip-to-tip coating of all components was used comprising a phosphorylcholine (PHISIO, Dideco, Inc) coating of all tubes as well as the cannulas, oxygenator, and filter.

View larger version (81K): [in this window] [in a new window]   Figure 1. Shed blood separation system: schematic view of the shed blood separation system integrated in the reservoir of the extracorporeal circulation. Note the switch (insert) provided to guarantee direct recirculation in case of urgent volume demand. Upward movement of the column results in drainage of separated blood accumulated in the upper chamber into the conventional reservoir (lower chamber).

Laboratory assessment
In all extracorporeal circulation groups arterial blood was drawn at 5 time points: preoperatively, intraoperatively (after institution of CPB, after crossclamp release, directly after decannulation), and postoperatively (first postoperative day). In the noECC group blood was drawn at 3 time points (preoperatively, intraoperatively, and first postoperative day). Free hemoglobin was determined photometrically. Hemoglobin, erythrocyte count, and platelet count were analyzed with the automated Hematology Analyser K-500 (Sysmex, Norderstedt, Germany). For verification of platelet function von Willebrand factor in the plasma of the patients was tested against lyophilized donor platelets while ristocetin was added as an activator. Ristocetin-cofactor activity was analyzed with a commercially available agglutination test (Behring Coagulation Timer; Dade Behring, Marburg, Germany). The activity was described as percentage of normal activity obtained with pooled donor plasma.^10,11 The coagulation parameters thrombin-antithrombin complex (TATc) and prothrombin fragments 1 and 2 (F1+2) and the fibrinolysis parameter plasmin-antiplasmin complex (PAPc) were analyzed by means of commercially available standard enzyme-linked immunosorbent assay techniques (TATc: Enzygnost thrombin-antithrombin complex micro; PAPc: Enzygnost plasmin/2-antiplasmin complex micro, F1+2: Enzygnost prothrombin fragment 1 and 2, Dade Behring, Marburg, Germany).

Statistical analysis
Statistical analysis was performed using SPSS statistical package for Windows (Version 9.0, SPSS Inc, Chicago, Ill). Numeric variables with normal distribution were analyzed by means of analysis of variance (ANOVA) and post hoc comparisons with Tukey honestly significant difference adjustment. Non-normally distributed variables were analyzed by means of Kruskal-Wallis test and subsequent Mann-Whitney test. Categorical variables were analyzed by means of Pearson chi-square test and subsequent adjustment. Data are shown as mean percentages or means ± standard deviation (SD). Significance was assumed if P < .05. ANOVA/Kruskal-Wallis test P values are shown or t test/Mann-Whitney test P values between specific groups are presented, respectively.

	Results

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Demographic and operative data
The majority of the patients were male (n = 38). Patients who underwent a MIDCAB procedure (noECC) tended to be younger and appeared to have less comorbidities as assessed by EuroSCORE than the other cohorts, although the differences did not gain statistical significance. All patients had an uneventful postoperative course. Rethoracotomy for bleeding was necessary in 2 patients (1 in ECC group, 1 in CECCSBS group). None of the patients developed a postoperative myocardial infarction. Sternal refixation because of dehiscence was necessary in 1 patient (ECCSBS group). Transient, mild psychosis was seen in 5 of the patients (2 in ECC group, 2 in ECCSBS group, 1 in CECCSBS group). Major neurological events such as focal deficits did not occur. Hospitalization of the noECC patients was significantly shorter than in all other groups, although differences between the 3 groups operated upon with CPB were not observed (Table 1).

View larger version (21K): [in this window] [in a new window]   Figure 2. Thrombin-antithrombin complex (µg/L) of the noECC, ECC, ECCSBS, and CECCSBS groups. Data obtained at the 5 time points: preoperatively (preop.), intraoperatively after CPB institution (at CPB), after crossclamp release (after x-clamp), after decannulation (after CPB), at the first postoperative day (PO day 1). Data are presented as mean ± SD.

PAPc exhibited corresponding findings. Although no increase was found in the noECC group as well as in the CECCSBS group, the ECC and ECCSBS groups reacted significantly with the time course of the CPB, whereas no statistical difference was found between ECC and ECCSBS groups. Postoperatively, the differences diminished (Table 4, Figure 3).

View larger version (21K): [in this window] [in a new window]   Figure 3. Plasmin-antiplasmin complex (µg/L) of the noECC, ECC, ECCSBS, and CECCSBS groups. Data obtained at the 5 time points: preoperatively (preop.), intraoperatively after CPB institution (at CPB), after crossclamp release (after x-clamp), after decannulation (after CPB), at the first postoperative day (PO day 1). Data are presented as mean ± SD.

	Discussion

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Coating
Several investigators have focused on a coating system of the CPB components to disguise the foreign surface. As a consequence, different modalities have evolved.^6,7 Heparin coating appeared to be a reasonable option, although most recent results were not entirely encouraging.^19,20 As an alternative, a phosphorylcholine coating was developed. It is considered to mimic the biological endothelial surface because phosphorylcholine is an integral component of the cell membrane.⁷ The first studies indeed showed positive effects of such a coating. Therefore, phosphorylcholine coating has been clinically introduced.⁷

Shed blood recirculation
It was observed that suction of pooled pleural blood into the cardiotomy reservoir and its recirculation resulted in a variety of detrimental effects. Liberation of prostacyclin and prostaglandin E2 in shed blood resulted in a marked decrease of the systemic blood pressure after recirculation.⁸ Other detrimental effects of shed blood have been identified as induced by lipid microembolization,²¹ activated complement,²² or cytokine release of pooled leukocytes.²³ The important clinical consequence of an increased postoperative blood loss because of an activation of fibrinolysis and platelet dysfunction in shed blood has already been demonstrated.²⁴ Therefore, avoidance of shed blood recirculation has been propagated to minimize these effects. Unfortunately, the amount of blood drained from the operating field can be high. A considerable loss of autologous blood therefore occurs. As an avenue out of this dilemma, a shed blood separation system was developed. The separated shed blood can be processed in a cell saver to retrieve the red blood cells for subsequent administration while potentially detrimental humoral factors are eliminated.^1,5,21-23

Study
In summary of the literature, both coating and shed blood separation appeared to be beneficial in terms of a reduction of cellular alteration and humoral activation. We therefore conducted a clinical study to elucidate these effects. As a control, we chose a MIDCAB instead of an off-pump coronary artery bypass (OPCAB) procedure because it represents an off-pump coronary revascularization technique with a minor operative trauma. Because a median sternotomy was not performed, liberation of bone marrow fat and subsequent activation of inflammatory parameters such as cytokines or arachidonic acid metabolites was avoided. Otherwise, MIDCAB patients exhibited sufficient similarities with the other groups because they suffered from arteriosclerosis, underwent almost identical anesthesia, and received acetylsalicylic acid as well as heparin and protamine. All ECC patients were submitted to a standard low-dose aprotinin protocol. A recent study showed that low-dose aprotinin did not inhibit the inflammatory response and coagulation caused by cardiopulmonary bypass as assessed by TATc. A reduction of fibrinolyis assessed by PAPc, however, was observed.²⁵

Red blood cells
In our study we found supporting evidence for the data published in the literature as well as both investigated strategies. The global erythrocyte count decreased only moderately in all CPB groups. Free hemoglobin, in contrast, was markedly increased in the conventional ECC group while it was much less elevated in both shed blood separation groups. The combination of coating and shed blood separation, however, exhibited the least damage.

Platelets
In our study we did not find statistical proof for an effect of shed blood separation and coating on platelet morphology and function. However, some trends were observed and can be interpreted carefully in the light of the results already demonstrated in the literature. The total number of platelets did not exhibit significant findings aside from a moderate decrease in all groups including the MIDCAB patients, although we expected a normal platelet count in our MIDCAB procedures because of the absence of CPB and the moderate blood loss. Von Willebrand factor–ristocetin cofactor correlates with platelet aggregation in high shear stress situations such as extracorporeal circulation^10,11 and was therefore chosen to assess platelet function in this study. Indeed, platelet function appeared to be less altered in the coated CPB group. One could therefore assume a beneficial effect of phosphorylcholine coating on platelet function, which has already been demonstrated by others.⁷ Heparin alone and in combination with protamine can alter platelet function and induce fibrinolysis,²⁶ although chronic pretreatment with acetylsalicylic acid may have reduced this phenomenon in our study. However, our findings supported the hypothesis that platelet consumption by activation, aggregation, and clearance can be triggered by the various drug interactions during anesthesia.¹

Coagulation and fibrinolysis
The analysis of coagulatory and fibrinolysis parameters exhibited a detrimental effect of conventional extracorporeal circulation. In conventional ECC both coagulation and fibrinolysis were markedly elevated, although shed blood separation alone was beneficial in terms of a reduction of coagulation disturbances but not fibrinolysis. The combination of coating and shed blood separation was followed by the least pronounced effects of coagulation and fibrinolysis in our study. We expected a down-regulation of fibrinolysis in all ECC groups because of the standard low-dose aprotinin protocol, which was uniformly applied.²⁵ The remaining extent of fibrinolysis in both uncoated groups, however, underlines the benefit of coating with phosphorylcholine in terms of a reduction of fibrinolysis. In this regard one can speculate that in the coated groups a reduction of circulating fibrin monomers may have contributed to a partial neutralization of plasmin activity.

Blood loss and substitution
One of the important clinical consequences of a reduced activation of coagulation cascades, as well as alteration of blood cells due to mechanical forces, may be the amount of perioperative drainage as well the necessity for blood and blood product substitution.²⁶ Our results demonstrated that drainage loss was higher in all CPB groups than in the MIDCAB patients. However, statistical evidence was not seen. Both the MIDCAB patients as well as the group with shed blood separation and coating required less substitution of blood than the other CPB groups. Again, these differences did not reach statistical significance.

Study limitations
In our study the isolated impact of phosphorylcholine coating was not investigated. Other clinical studies, however, have already been conducted and exhibited positive effects of phosphorylcholine coating on coagulation.^6,7 The specific CPB modalities investigated by us did not serve the purpose of saving blood in our study, although the observed trends may gain statistical relevance in a larger trial.

Conclusion
We conclude from this first investigation that phosphorylcholine coating in combination with shed blood separation reduced mechanical alteration of red blood cells and coagulation disturbances in routine CPB procedures to a level otherwise only seen in off-pump procedures. The separated blood can be processed in a cell saver for later substitution, thereby avoiding excessive blood loss.

	Footnotes

 
The laboratory analysis of the specific coagulation and fibrinolysis parameters TATc, PAPc, and F1+2 was financially supported by Sorin Inc, Mirandola, Italy.

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