I bypass (CPB) circuit causes platelet damage and impairment

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1 Aprotinin Reduces Intraoperative and Postoperative Blood Loss in Membrane Oxygenator Cardiopulmonary Bypass Marcel P. Harder, MD, Leon Eijsman, MD, Klaas J. Roozendaal, MD, Willem van Oeveren, PhD, and Charles R. H. Wildevuur, MD, PhD Department of Cardiopulmonary Surgery, Research Division, University Hospital, Groningen; Department of Hematology, Onze Lieve Vrouwe Gasthuis, Amsterdam; and Department of Cardiopulmonary Surgery, Onze Lieve Vrouwe Gasthuis, Amsterdam, the Netherlands To determine whether aprotinin can provide a significant improvement of hemostasis in cardiopulmonary bypass using a membrane oxygenator, we tested this drug in a prospective, randomized, double-blind, placebo-controlled clinical trial. The subjects were 80 male patients undergoing cardiopulmonary bypass for coronary artery bypass grafting. Forty patients received aprotinin and 40 patients served as placebo controls. Aprotinin (4 x lo6 KIU) was given as a continuous infusion, starting before operation and continuing until after cardiopulmonary bypass; additionally, 2 X lo6 KIU aprotinin was added to the pump prime. Intraoperative and postoperative bleeding, respectively two thirds and one third of the total perioperative blood loss, were both significantly reduced in the aprotinin-treated group (p < 0.01). The total average perioperative blood loss, corrected to a hemoglo- bin concentration of 7 mmol/l, was 550 ml in the aprotinin-treated patients versus 900 ml in the control patients. This reduction in blood loss, furthermore, significantly decreased the amount of postoperative blood transfusions (p c 0.05) and increased the percentage of patients who did not receive postoperative donor blood from 42% to 68%. Aprotinin increased the activated clotting time significantly during cardiopulmonary bypass, which led to a reduction in heparin usage. The improved hemostasis during operation, despite the prolonged activated clotting time, might even abolish the need for heparin conversion with protamine at the end of cardiopulmonary bypass, thus allowing retransfusion through cardiotomy suction to be continued, which saves the blood that is currently lost with vacuum suction. (Ann Thorac Surg 1991;51:93641) ntensive contact of blood with the cardiopulmonary I bypass (CPB) circuit causes platelet damage and impairment of normal hemostasis [l]. Improvements made in the design of the various parts of the CPB equipment, and particularly the introduction of membrane oxygenators, have contributed to reduce platelet damage. Membrane oxygenators currently do not reduce platelet number or adenosine diphosphate-induced platelet aggregation during CPB [2]. Platelets are, however, still activated, and their function is affected during CPB as shown by the release of Pthromboglobulin from platelets and the prolonged postoperative bleeding times [3]. To protect platelets from activation during CPB, platelet inhibitors such as prostaglandin E, [4], prostacyclin [5, 61, and iloprost (ZK 36374) [7] have been used. The major drawback of all these drugs was their strong vasodilating side effect, which prevented the use of sufficiently high dosages to effectively inhibit platelet activation during CPB. Aprotinin, a proteinase inhibitor, effectively inhibits fibrinolysis [8] and improves perioperative hemostasis in bubble oxygenator perfusion [9]. This study evaluates Accepted for publication Jan 21, Address reprint requests to Dr Wildevuur, Department of Cardiopulmonary Surgery, Research Division, University Hospital, Oostersingel 59, Postbus , 9700 RB Croningen, the Netherlands. whether aprotinin treatment will also result in improved perioperative hemostasis with less of an effect on platelets in membrane oxygenator perfusion. We specifically quantified intraoperative blood loss because we observed in our previous study [ 101 that aprotinin provided improved intraoperative hemostasis during full heparinization. Material and Methods Signed informed consent was obtained from all 80 participating, otherwise healthy, male patients scheduled for elective coronary artery bypass grafting. The study protocol was reviewed and approved by the ethical committee of the Onze Lieve Vrouwe Gasthuis. Put ient Exclusion Criteria The following exclusion criteria were used: a history of allergy, acute pancreatitis and possible previous exposure to aprotinin, thromboembolic disease that required treatment with anticoagulant therapy, severe kidney and liver function disturbances as reflected in an elevated serum creatinine level (>lo0 mmol/l), and elevated prothrombin time. Patients who were preoperatively treated with acetylsalicylic acid or dipyridamole were excluded from the study by The society of Thoracic Surgeons

2 Ann Thorac Surg 1991;51: HARDERETAL 937 APROTlNlN REDUCES BLOOD LOSS DURING CPB Study Drug Administration Aprotinin (Trasylol) and placebo solution were supplied by Bayer AG (Leverkusen, Germany) in bottles containing 50 ml of saline solution without any other additives or preservatives. Each milliliter of aprotinin solution contained 10,OOO kallikrein inactivator units (KIU). The randomization code was only known to the pharmacy of the hospital. We collected the coded vials containing either placebo or aprotinin from the hospital pharmacy in the morning before the operation. We started the infusion of placebo or aprotinin with a bolus of 200 ml (2 x lo6 KIU) just after the Swan-Ganz catheter was introduced; thereafter we kept the infusion rate at 50 ml (0.5 x lo6 KIU) per hour with an infusion pump (WAC, San Diego, CA). The total amount of aprotinin delivered by infusion was 4 x 106 KIU before and during bypass. Cardiopulmonary Bypass The extracorporeal circuit contained either a William- Harvey membrane oxygenator (model HF-4000, Bard Cardiosurgery Division, Tustin, CA) or a Sci-Med 2 spiral coil membrane oxygenator (model SM 25/system; Sci-med Live Systems Inc, Minneapolis, MN). Both types of oxygenators were randomly used in the two study groups. Polyvinyl chloride tubing was used throughout the extracorporeal circuit, except for the pump tubing, which was made of silicone rubber. The prime of the extracorporeal circuit consisted of 1.5 L Haemacell (Hoechst Holland N.V., Amsterdam, the Netherlands) and 1.0 L Hartmann solution containing 5,000 IU heparin (Leo, Emmen, the Netherlands). To this priming solution we added either saline solution (placebo) or aprotinin (2 x lo6 KIU). Heparin (300 IU/kg) was given intravenously before cannulation of the ascending aorta and the right atrial appendage. During CPB we repeated heparin administration (100 IU/kg; intravenous) whenever the activated clotting time (ACT) was shorter than 400 seconds. After CPB the starting dose of heparin was neutralized with protamine sulfate on a 1:l ratio. The perfusion flow rate during moderate hypothermia was 2.5 WmZ * min. During suturing of the distal coronary anastomoses, the aorta was clamped and cardioplegia was achieved with an ice-cold isotonic solution containing 15 mmol K+, 15 mmol Mg+, and 1.5 g albumin per liter. Cardioplegia was repeated every 30 minutes. An average of 1.5 L of cardioplegic solution was used and returned to the circulation. Anesthesia Premedication was given with lorazepam (Temesta; Wyeth, Hoofddorp, the Netherlands), 4 to 5 mg, 2 hours before induction of anesthesia. Anesthesia was induced with a bolus of alfentanil (Rapifen; Janssen, Tilburg, the Netherlands) (50 pg * kg-' - min-') and etomidate (Hypnomidate; Janssen) (0.1 mg/kg) followed by pancuronium bromide (Pavulon; Organon, Oss, the Netherlands) (0.1 mgkg). Anesthesia was maintained with a continuous infusion of 10 pg - kg-' - min-' etomidate and 3 pg - kg-' - min-' alfentanil before CPB; during and after CPB the dose was, respectively, 5 pg * kg-' * min-' and 1.5 pg * kg-' * min-'. When blood pressure increased the alfentanil concentration was changed and a nitroglycerin infusion was started. At termination of CPB inotropic drugs were given if necessary. All patients were ventilated to normocapnia (arterial carbon dioxide tension, 4.5 to 5 kpa) with an aidoxygen mixture (inspired oxygen fraction, 0.5). Criteria for Transfusion of Banked Donor Blood Products During the operation red blood cell concentrates were transfused when the hematocrit value decreased to less than In the intensive care unit, red blood cell concentrates were used when the hemoglobin concentration decreased to less than 6 mmol/l, corresponding to a hematocrit value of about Hematology Preoperatively, typically the day before the operation, the bleeding time was determined according to the method of Mielke and associates [ll] with a bleeding time testing device (B.T.T. International Medical Products bv, Zutphen, the Netherlands); in addition, the activated prothromboplastin time, prothrombin time, normotest, and thrombotest were determined. These variables were determined again when the patients arrived at the intensive care unit. During operation, blood samples were taken from the radial artery or arterial line of the extracorporeal circuit 5 minutes before CPB, at 5 and 30 minutes of CPB, at the end of CPB, and 30 minutes after protamine sulfate administration. Cell Counts Two milliliters of blood containing 0.01 mom ethylenediaminetetraacetic acid was collected for platelet counts using a fully automated hematology analyzer (E 5o00, Toa Medical Electronics Co, Kobe, Japan). Activated Clotting Time Two milliliters of blood was collected in a glass vacuum tube containing 12 mg of diatomaceous earth for determination of the ACT. All ACTS were measured with a Hemochron 400 automated timing system (International Technidyne Corp, Edison, NJ). Activated clotting times exceeding 1,OOO seconds were interrupted. PThrornboglobulin PThromboglobulin concentrations were determined by means of a radioimmunoassay (Amersham, Amersham, UK). Samples were collected in chilled tubes containing platelet inhibitors (Amersham). Determination of Perioperative Bleeding During operation, particularly at the end of CPB, the surgeon and the first assistant scored the "dryness" of the operative field on a scale ranging from 1 to 5. A score of 1 was associated with a "bone dry" operative field, whereas a score of 5 was associated with a "very wet" operative field. To assess blood loss during the operation, all used

3 938 HARDERETAL APROTININ REDUCES BLOOD LOSS DURING CPB Ann Thorac surg 1991;51:93641 Table 1. Characteristics of the Study Population Characteristic Aprotinin Angina (NYHA class) Age (Y) BSA (m2) Preop Hb (mmol/l) CPB time (min) Crossclamp time (min) Cardioplegia (ml) Urine output (ml) Infusion fluids (ml) 2.70 f f f f f f f f f 187 Placebo 2.97 f f f f f f f f loo 3215 f 168 BSA = body surface area; CPB = cardiopulmonary bypass; Hb = hemoglobin; NYHA = New York Heart Association. gauzes were weighed and washed in water to achieve lysis of the red blood cells; thereafter the hemoglobin concentration of the washing fluid was measured. In addition, the volume and hemoglobin concentration of the fluid in the vacuum suction canisters were measured. This blood loss was expressed in milliliters of blood with a hemoglobin concentration of 7 mmoyl. After operation we checked the volume of the shed mediastinal blood loss collected in the Pleur-Evac (Code no: A-4000; Howmedica, International, Dublin, Republic of Ireland) hourly. The Pleur-Evac was removed on the first postoperative day. The contents of the Pleur-Evac were anticoagulated with 5 ml of 0.4 moyl ethylenediaminetetraacetic acid so that we could measure the total hemoglobin concentration. Again, we expressed this blood loss in milliliters with a hemoglobin concentration of 7 mmovl. Stat is tics All values are expressed as mean * standard error of the mean. Statistical analysis was done with a nonparametric statistical test for independent samples, in this case the Mann-Whitney test. A p value smaller than 0.05 was considered significant. Results There were no significant differences in patient population, cardiopulmonary bypass duration, aortic clamp time, volume of cardioplegic solution, intraoperative urine output, and volume of infusion fluids (Table 1). We did not observe any adverse effect during or after operation that could be related to the use of aprotinin. Patients from both groups invariably did well after operation. There were no electrocardiographic or enzymatic indications of perioperative myocardial infarction; furthermore, there was no difference between the two groups in postoperative hemodynamics or duration of intensive care treatment and total hospitalization. Dryness of the Operative Field The dryness score issued by the first assistant and surgeon showed a significantly dryer operative field in the Table 2. Dryness of the Operative Field Measurement Aprotinin Placebo pvalue Surgeon 2.17 f f 0.15 C0.05 First assistant 2.20 f f 0.14 CO.05 Closing time (min) f f 2.7 NS * Possible score ranging from 1 to 5 1 = bone dry, 5 = very wet. NS = not significant. aprotinin-treated patients (Table 2). This subjective difference in dryness resulted in a shorter so-called closing time, ie, the time interval between the end of extracorporeal circulation and the end of skin closure. In the aprotinin-treated group the closing time was about 6 minutes, 14% shorter than in the placebo group, although this difference in closing time was not significant. Blood Loss The intraoperative blood loss accounted for two thirds, the postoperative blood loss for one third of the total perioperative blood loss (Table 3). Intraoperative blood loss was significantly reduced in the aprotinin-treated patients by an equivalent of about 200 ml of blood. Aprotinin-treated patients also had significantly reduced mediastinal drainage production, particularly in the first 8 postoperative hours (Table 4). Based on the hemoglobin concentration of the fluid in the Pleur-Evac, which was 1.9 f 0.2 mmol/l in the aprotinin group and 2.6 * 0.18 mmoyl in the control group, we calculated a significantly reduced postoperative blood loss (7 mmoyl) of 126 -C 10 ml in the aprotinin group versus 250 f 20 ml in the placebo group in the fist 18 hours. Banked Donor Blood Products During operation both the control and aprotinin patients needed similar amounts of banked donor blood products. After operation, aprotinin-treated patients needed significantly less banked donor blood products. Also, the percentage of patients that received banked donor blood products was reduced by 26% (Table 5). Hematology After heparinization the ACT increased from 150 to 495 k 29 seconds in the untreated patients; it was significantly Table 3. Blood Loss Measurement Aprotinin Placebo p Value Intraoperative Gauzes 203 f f 159 <0.02 Suction 217 f f 247 <0.02 Total intraoperative 420 f f 231 <0.01 Postoperative 139 f f 139 <0.01 Total perioperative 559 f f 170 <0.01 a Values are given in milliliters of blood with a hemoglobin concentration of 7 mmovl.

4 Ann Thorac Surg 1991;51: HARDERETAL 939 APROTININ REDUCES BLOOD LOSS DURING CPB Table 4. Shed Mediastinal Blood" 1000, Postoperative Hour Aprotinin Placebo p Value 1 69 f 9 96 f 17 NS 2 35 f 4 76 f 9 < f 4 53 f 5 < f 6 42 f 4 < f 3 NS 6 14 f < f 2 26 f 4 C f 2 21 f 3 <0.05 Total volume a All values are in milliliters. NS = not significant. higher, seconds, in the aprotinin-treated patients (p < 0.001). Throughout CPB the ACT of the aprotinintreated patients remained significantly higher than the ACT of the untreated patients (Fig 1). Additionally, in contrast to patients receiving placebo, aprotinin-treated patients did not receive extra heparin during bypass to keep the ACT greater than 400 seconds. The ACTS of both groups returned to normal after protamine administration. PThromboglobul in pthromboglobulin concentrations increased similarly in both groups of patients throughout CPB. At the end of CPB a threefold increase of pthromboglobulin was measured (Fig 2). The bleeding time increased in both groups as a result of CPB. This increase in bleeding time was not significantly different between the groups, mainly because of the large interindividual spread of preoperative bleeding times. The activated prothromboplastin time, prothrombin time, and platelet and leukocyte counts on the first postoperative day did not differ significantly between groups (Table 6). Comment Our results clearly show that aprotinin treatment in CPB with membrane oxygenator perfusion significantly re- Table 5. Usane of Banked Donor Blood Products Blood Product Aprotinin Placebo p Value Intraoperative Packed cells (units) 1.5 f f 0.2 NS FFP (units) 0.2 f f 0.14 NS Patients no blood (%) Postoperative Packed cells (units) 0.4 f <0.05 FFP (units) 0.3 f f 0.20 <0.05 Patients no blood (%) FFP = fresh frozen plasma; NS = not significant. A E P Y E d CPB I, I I I time (min) Fig 1. The activated clotting time (ACT) was significantly higher after administration of heparin in the patients treated with aprotinin (squares) than in the control patients (circles). fp < 0.02 during the whole procedure of cardiopulmona y bypass [CPBI.) duces both intraoperative and postoperative blood loss, which eliminates the need for postoperative blood transfusions in 68.5% of the treated patients. This study also shows that the bulk of perioperative blood loss occurs intraoperatively. We found that intraoperative blood loss accounts for two thirds and postoperative blood loss for only one third of the total blood loss. The effect of aprotinin treatment on the reduction of intraoperative blood loss was clearly noticed by the surgeons, because they operated in a remarkably dry operative field right from the start of operation [12]. We could substantiate this subjective indication of improved intraoperative hemostasis because aprotinin treatment resulted in saving an equivalent of 200 ml of blood during operation. This improvement in intraoperative hemosta- 6oo 1 0, I CPB I I I I time (mln) Fig 2. pthromboglobulin (&TG) concentrations increased in both aprotinin-treated (squares) and control patients (circles) during cardiopulmonary bypass (CPB). No significant differences w e obserwd between the two groups.

5 940 HARDERETAL APROTININ REDUCES BLOOD LOSS DURING CPB Ann Thorac Surg 1991;51: Table 6. Postoperative Coagulation Variables" Variable Aprotinin Placebo Bleeding time (s) 410 f f 36 Hb (mmovl) AIJlT (4 47 f f 1.40 m-r (s) 15 f f 0.30 Platelets Preop 236 f f 16.8 Postop 141 4_ f 7.9 a There were no significant differences between the aprotinin and placebo groups. = activated partial thromboplastin time; Hb = hemoglobin; FIT = prothrombin time. sis despite full heparinization is most likely associated with a preservation of the hemostatic function of platelets. We previously demonstrated in control patients a 50% loss of the adhesive receptor from the platelet membrane (GPlb) within the first 5 minutes of CPB. In aprotinintreated patients, however, we found full preservation of this adhesive receptor throughout CPB 113). The adhesive receptor on the platelet membrane plays an important role, independent of clotting factors, in the initial platelet plug formation on damaged vascular endothelium. The preservation of this receptor by aprotinin treatment most likely explains the improved intraoperative hemostasis despite heparinization. In contrast, the a-granule release from platelets, demonstrated by pthromboglobulin, was not protected by aprotinin. This indicates that the platelets can still be activated by various agonists, such as ADP. The significantly reduced intraoperative blood loss with aprotinin treatment was not sufficient to result in a significant reduction of intraoperative packed cell usage. A large percentage of patients (75%) in both groups still needed packed cells to correct for a low hematocrit value during bypass. This low hematocrit value is mainly a result of both clear prime and the large circulating volume caused by nitroglycerin infusion, which was used routinely in all patients. It is clear that further reduction of intraoperative packed cell usage has to be obtained by adaptation of the anesthesia protocol with respect to the afterload reduction and by defining the lowest acceptable hematocrit values during and shortly after bypass. In this regard a hematocrit value of 0.28 shortly after bypass is probably sufficient [14]. Another important intraoperative observation was that the vacuum suction, started after the administration of protamine, accounted for 54% of the total intraoperative blood loss. Because the hemostasis was well maintained independent of full heparinization and anticoagulation, as witnessed by the prolonged ACT values during bypass, the use of protamine to neutralize the heparin could be abandoned and continuation of retransfusion of cardiotomy suction remained possible. Not only can this double the efficacy of saving blood intraoperatively, but it can also avoid the well-documented negative effects of prot- amine on platelet function [l] and on the cardiovascular system (151. In general, interventions seeking to reduce blood loss and, consequently, donor blood requirements will profit most by measures that reduce intraoperative blood loss because two thirds of the total blood loss occurs intraoperatively. In the postoperative period the reduction in shed mediastinal blood and donor blood requirements in the aprotinin group correlated nicely; both were approximately halved. Postoperatively donor blood was needed in 32% of the aprotinin-treated patients, whereas 57% of the placebo-treated patients needed donor blood. The routine hemostasis variables that we measured on amval in the intensive care unit were similar in both groups and did not explain the improved postoperative hemostasis in the aprotinin-treated group. In particular, platelet numbers did not differ in both groups and bleeding times were not significantly different, although they tended to be somewhat higher in the placebo group. With an improvement of platelet hemostatic function in the aprotinin group, as previously indicated by a preservation of the platelet adhesive receptors [13], one may expect an improved bleeding time postoperatively. Indeed, an improved postoperative bleeding time with the use of aprotinin was measured in earlier studies using bubble oxygenators [9]. To explain this discrepancy with our current findings one has to bear in mind that platelet function during membrane oxygenator perfusion is less impaired than during bubble oxygenator perfusion, and therefore the additional favorable effect of aprotinin on platelet function during CPB could fall within the outer limits of the sensitivity of the bleeding time determination. Electrocardiography was routinely performed in the postoperative period. Because no indications of infarctions were observed, further biochemical measurements (creatine kinase-mb) were not performed. In conclusion, aprotinin treatment reduces intraoperative and postoperative blood loss significantly even in membrane oxygenator perfusion, which maintains better platelet function, resulting in a decrease of postoperative donor blood requirements by about half. In addition, the need for postoperative blood transfusions in patients after CPB was reduced from 57% to 32%. Because the bulk of perioperative blood loss is caused by intraoperative bleeding, further efforts to reduce donor blood requirements should be concentrated particularly on reduction of intraoperative blood loss. References 1. Mannen FM, Koets MH, Washington BC, et al. Hemostasis changes during cardiopulmonary bypass surgery. Semin Thromb Hemost 1985;11: Harder MP, Leusink JA, de-nooy EH, Gerding A, Wildevuur Chl7H. Haematological characteristics of a new membrane oxygenator: the Cobe CML. J Cardiovasc Surg 1987;28: Harker LA, Malpass TW, Branson HE, et al. Mechanism of abnormal bleeding in patients undergoing cardiopulmonary

6 Ann Thorac Surg 1991;51:93641 HARDER ET AL APROTlNlN REDUCES BLOOD LOSS DURING CPB 941 bypass: acquired transient platelet dysfunction associated with selective alpha granule release. Blood 1980;56: Van den Dungen JJAM, Karliuek GF, Brenken U, Homan van der Heide JN, Wildevuur ChRH. The effect of prostaglandin El in patients undergoing clinical cardiopulmonary bypass. Ann Thorac Surg 1983;35:40& Malpass TW, Amory DW, Harker LA, Ivey TD, Williams DB. The effect of prostacyclin infusion on platelet hemostatic function in patients undergoing cardiopulmonary bypass. J Thorac Cardiovasc Surg 1984;8755&5. 6. Fish KJ, Samquist FH, van Steenns C, et al. A prospective randomized study of the effects of prostacydin on platelets and blood loss during coronary bypass operations. J Thorac Cardiovasc Surg 1986;91: Kappa JR, Horn MK, Fisher CA, et al. Efficacy of iloprost (-74) versus aspirin in preventing heparin-induced platelet activation during cardiac operations. J Thorac Cardiovasc Surg 1987;94: Fritz H, Wunderer G. Biochemistry and applications of aprotinin, the Mlikrein inhibitor from bovine organs. Arzneim Forsch Drug Res 1983;33: Bidstrup BP, Royston D, Sapsford RN, Taylor KM. Reduction in blood loss and blood use after cardiopulmonary bypass with high-dose aprotinin (Trasylol). J Thorac Cardiovasc Surg 198%9736& Van Oeveren W, Harder MP, Roozendaal KJ, Eijsman L, Wildevuur ChRH. Aprotinin protects platelets against the initial effect of cardiopulmonary bypass. J Thorac Cardiovasc Surg 1990;99: Mielke CH Jr, Kaneshiro MM, Mahler IA, Weiner JM, Rapaport SI. The standardized normal Ivy bleeding time and its prolongation by aspirin. Blood 1969;34:2& Alajmo F, Calamai G, Pema AM, et al. High-dose aprotinin: hemostatic effects in open heart operations. Ann Thorac Surg 1989;48: Van Oeveren W, Eijsman L, Roozendaal KJ, Wildevuur ChRH. Platelet preservation by aprotinin during cardiopulmonary bypass. Lancet 1988; Cosgrove DM, Loop FO, Lytle BW, et al. Determinants of blood utilization during myocardial revascularization. Ann Thorac Surg 1985;40:3Nl Frater RWM, Oka Y, Hong Y, et al. Protamine-induced circulatory changes. J Thorac Cardiovasc Surg 1984;

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