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James S. Gammie
Marco Zenati
Robert L. Kormos
Brack G. Hattler
Lawrence M. Wei
Ronald V. Pellegrini
Bartley P. Griffith
Cornelius M. Dyke
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Ann Thorac Surg 1998;65:465-469
© 1998 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Abciximab and Excessive Bleeding in Patients Undergoing Emergency Cardiac Operations

James S. Gammie, MD, Marco Zenati, MD, Robert L. Kormos, MD, Brack G. Hattler, MD, PhD, Lawrence M. Wei, MD, Ronald V. Pellegrini, MD, Bartley P. Griffith, MD, Cornelius M. Dyke, MD

Division of Cardiothoracic Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA

Accepted for publication August 15, 1997.

Dr Gammie, Division of Cardiothoracic Surgery, University of Pittsburgh Medical Center, Suite C-700 Scaife, 200 Lothrop St, Pittsburgh, PA 15213 (e-mail: gam@med.pitt.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Abciximab (ReoPro; Eli Lilly and Co, Indianapolis, IN) is a monoclonal antibody that binds to the platelet glycoprotein IIb/IIIa receptor and produces powerful inhibition of platelet function. Clinical trials of abciximab in patients undergoing coronary angioplasty have demonstrated a reduction in thrombotic complications and have encouraged the widespread use of this agent. We have observed a substantial incidence of excessive bleeding among patients who receive abciximab and subsequently require emergency cardiac operations.

Methods. The records of 11 consecutive patients who required emergency cardiac operations after administration of abciximab and failed angioplasty or stent placement were reviewed.

Results. The interval from the cessation of abciximab administration to operation was critical in determining the degree of coagulopathy after cardiopulmonary bypass. The median values for postoperative chest drainage (1,300 versus 400 mL; p < 0.01), packed red blood cells transfused (6 versus 0 U; p = 0.02), platelets transfused (20 versus 0 packs; p = 0.02), and maximum activated clotting time (800 versus 528 seconds; p = 0.01) all were significantly greater in the early group (cardiac operation <12 hours after abciximab administration; n = 6) compared with the late (cardiac operation >12 hours after abciximab administration; n = 5) group.

Conclusions. This report suggests that the antiplatelet agent abciximab is associated with substantial bleeding when it is administered within 12 hours of operation.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Abciximab (ReoPro; Eli Lilly and Co, Indianapolis, IN) is a monoclonal antibody that causes profound inhibition of platelet aggregation and thrombus formation by binding to the platelet membrane glycoprotein IIb/IIIa (GPIIb/IIIa) receptor. Recent studies suggesting that this novel antiplatelet agent significantly reduces the incidence of abrupt vessel closure and coronary restenosis after high-risk percutaneous transluminal coronary angioplasty (PTCA) stimulated the Food and Drug Administration to approve abciximab for general use in December 1994 [1]. We have observed dramatic intraoperative and postoperative coagulopathies in patients who receive abciximab and require emergency cardiac operations. To define the risks associated with operation on these patients and to suggest management strategies, we reviewed our clinical experience.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
We reviewed the records of all patients at the University of Pittsburgh Medical Center and the Mercy Heart Institute who were administered abciximab during PTCA and subsequently required urgent cardiac operation. All patients received aspirin and heparin before PTCA. Heparin was given intravenously at an initial dose of 5,000 to 10,000 U (70 U/kg), followed by intermittent boluses to maintain an activated clotting time (ACT) between 200 and 300 seconds. Abciximab was administered as a bolus of 0.25 mg/kg 10 to 60 minutes before PTCA, followed by an infusion of 10 µg/min. No patient had a history of a bleeding diathesis, and none had undergone previous sternotomy.

In preparation for cardiopulmonary bypass, heparin was administered routinely at 300 U/kg, with incremental doses given as needed to maintain the ACT at greater than 400 seconds. Reversal with protamine followed separation from cardiopulmonary bypass at a dose of 1 mg/100 U total heparin dose. {epsilon}-Aminocaproic acid was administered in all cases at an initial dose of 5 g, followed by a constant infusion of 1 g/h (total dose, 5 to 10 g). Chest tube drainage was measured and the requirement for allogeneic blood products was recorded.

Statistical analyses were carried out using JMP software (SAS Institute, Cary, NC). Differences between group means were compared using an unpaired t test. Differences between group medians were compared with the Mann-Whitney U test.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Precatheterization Characteristics
Between November 1995 and December 1996, 175 patients received abciximab before undergoing high-risk PTCA. Of these, 11 (6.3%, 9 men and 2 women) required urgent cardiac operations because of failed PTCA or intracoronary stent placement. The patients ranged in age from 43 to 80 years. Coronary artery bypass grafting (CABG) was required in 7 patients for failed stent placement and in 3 patients for unsuccessful PTCA. One patient underwent the placement of a left ventricular assist device for cardiogenic shock. Table 1 outlines the clinical characteristics of these 11 patients.


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  		Clinical Characteristics of Abciximab-Treated Patients Who Required Urgent Cardiac Operations

 
Pharmacodynamic studies have demonstrated near-normalization of platelet function by 12 hours after abciximab infusion. We therefore divided our patients into an early group (cardiac operation <12 hours after abciximab administration) and a late group (cardiac operation >12 hours after abciximab administration) [2]. Precatheterization hematologic values were similar for both groups, as was the amount of heparin given in the catheterization laboratory (Table 2). Among the 5 patients who had delays of greater than 12 hours between abciximab administration and operation, the delay was related directly to a second catheterization 24 hours after the initial procedure in 3 patients. In 1 patient, operation was delayed 8 days by the development of Staphylococcus aureus bacteremia and a large retroperitoneal hematoma that necessitated the transfusion of 9 U of packed red blood cells, 6 U of fresh frozen plasma, and a 10-pack of platelets. No other patients received blood transfusions between PTCA and operation. A final patient received abciximab at the time that two stents were placed in the left anterior descending (LAD) coronary artery and two additional stents were placed in a diagonal branch. He was readmitted to the hospital 10 days later with unstable angina and found to have an occluded LAD and thrombus in the diagonal branch, which prompted his referral for CABG.


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  		Precatheterization Hematologic Characteristics of Patients Who Underwent Cardiac Operations Early (<12 h) and Late (>12 h) After Abciximab Infusion and Unsuccessful Percutaneous Revascularization1

 
Clinical Outcome
Ten of the 11 patients survived and were discharged from the hospital. The mean length of stay for the survivors was 6.9 days. The only nonsurvivor (patient 5) was a 40-year-old man who presented with an acute anterior wall myocardial infarction and a proximally occluded (LAD). Seven stents were deployed in the LAD and left circumflex arteries, but a refractory low output state necessitated the placement of a left ventricular assist device without cardiopulmonary bypass. He recovered and did well until postoperative day 11, when he suffered a massive cerebrovascular accident.

Intraoperative and Postoperative Bleeding
There was a strong relation between the interval from the administration of abciximab to operation and the degree of intraoperative and postoperative coagulopathy. The 5 patients who were operated on more than 12 hours after receiving abciximab had minimal bleeding and modest transfusion requirements. In contrast, the 6 patients who were operated on early after they received abciximab had substantial transfusion requirements and, at times, massive coagulopathies (Table 3). There was a threefold greater mediastinal blood loss in the first 24 postoperative hours in the early group compared with the late group. The contribution of abciximab to the development of coagulopathy after cardiopulmonary bypass is demonstrated by the sharp increase in the requirement for blood product transfusions among the early group. These patients required significantly more packed red blood cells, fresh frozen plasma, and platelets than did those in the late group. The recent administration of abciximab also was associated with significantly higher ACTs during cardiopulmonary bypass. The median maximum ACT was 528 seconds in the late group compared with 800 seconds in the early group (p = 0.01).


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  		Perioperative Blood Loss and Transfusion Requirements for Patients Undergoing Cardiac Operations Early (<12 h) and Late (>12 h) After Receiving Abciximab1

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
This study documents an early experience with cardiac operations in patients treated with the antiplatelet agent abciximab during percutaneous revascularization. The interval between abciximab administration and operation was critical in determining the extent of perioperative mediastinal bleeding and the necessity for blood product support. Our initial experience suggests that abciximab, when given within 12 hours of cardiac operation, is associated with significantly increased blood loss and transfusion requirements.

Platelets play a key role in the development of an arterial thrombus. Spontaneous plaque rupture within a coronary artery or mechanically induced vessel injury after balloon angioplasty result in the exposure of adhesive glycoproteins such as collagen and von Willebrand’s factor. Platelets adhere to these protein ligands through surface glycoproteins and initiate the process of thrombus formation. The major platelet surface receptor involved in platelet aggregation is the GPIIb/IIIa receptor, a member of the integrin family of platelet surface glycoproteins [3]. Once platelet adhesion to the exposed glycoprotein substrate occurs, activation produces a conformational change in the GPIIb/IIIa receptor such that it binds circulating macromolecules (predominantly fibrinogen) with high affinity. Cross-links then are formed to adjacent platelets, leading to platelet aggregation ("cohesion").

The GPIIb/IIIa receptor serves as the final common pathway for platelet activation induced by a variety of agonists and hence is a rational target for therapeutic interventions designed to prevent thrombus formation. The GPIIb/IIIa receptor is specific to platelets, and its inactivation abolishes platelet thrombus formation while leaving platelet adhesion relatively intact. Abciximab is a chimeric monoclonal antibody that strongly inhibits platelet aggregation when added to platelet-rich plasma in vitro or administered to humans and animals in vivo [4] [5]. Abciximab is far more potent than aspirin in inhibiting platelet function, and has been proven to be more effective than aspirin in preventing thrombotic complications in several animal models of arterial thrombosis [6].

Pharmacodynamic studies demonstrate gradual platelet functional recovery after the infusion of abciximab such that bleeding times and platelet aggregation return to near-normal levels 12 hours after dosing. In these studies, bleeding time was 12 minutes or less within 12 hours of infusion in 15 (75%) of 20 patients and within 24 hours of infusion in 18 (90%) of 20 patients [1]. Although platelet function largely normalizes by 12 hours, low levels of GPIIb/IIIa receptor blockade are present for up to 10 days after the cessation of abciximab infusion. A flow cytometric pharmacodynamic study of normal subjects demonstrated 27% receptor blockade by abciximab at 7 days and 11% blockade at 14 days. This analysis also found that the degree of binding was similar among all circulating platelets at times exceeding the normal 7- to 10-day platelet life span, suggesting a gradual and continuous reequilibration of abciximab among circulating platelets [7].

A multicenter, controlled, randomized trial evaluated abciximab in 2,099 patients at high risk for restenosis after PTCA [1]. The administration of abciximab as a bolus, followed by an infusion initiated just before PTCA, was associated with a decrease in the combined end points of death, myocardial infarction, and reintervention from 12.8% to 8.3% at 30 days (a 35% reduction) [1]. This reduction in thrombotic complications, however, was accompanied by a substantially increased risk of bleeding in the group that received abciximab: there was an approximately twofold increased rate of major bleeding (defined as a drop in hemoglobin of >5 g) and transfusion in the treated group. The investigators for the Evaluation of c7E3 Fab for the Prevention of Ischemic Complications (EPIC) trial reported that most of the bleeding after abciximab administration occurred either at vascular access sites or during CABG. Overall, 25 (3.6%) of 696 placebo-treated and 33 (2.4%) of 1,403 abciximab-treated patients in the EPIC trial underwent CABG. Among those patients who required CABG, the incidence of bleeding and the estimated blood loss were similar in the control and treatment groups. However, the median time to CABG was 1 day in the abciximab bolus group and 2.2 days in the bolus plus infusion group [8]. Analysis of excessive bleeding among those patients who had CABG was instructive: 7 (28%) of 25 placebo-treated patients received more than 5 U of packed red blood cells, in contrast to 19 (57%) of 33 abciximab-treated patients. Similarly, more than 5 packs of platelets were given to 11 (44%) of 25 placebo-treated patients and 23 (70%) of 33 abciximab-treated patients (Lee K, Peck S, personal communication, 1997).

Given the powerful antiplatelet effect of abciximab, it is not surprising that patients with failed PTCA or stent placement who require emergency cardiac operations would be at substantial risk for bleeding complications. Our early experience operating on patients who have been given this drug strongly supports an association between abciximab and excessive intraoperative and postoperative bleeding. Four of the 6 patients in this series who were operated on within 12 hours of abciximab administration required 5 U or more of allogeneic packed red blood cells, and all 6 had mediastinal blood loss in excess of 1,000 mL (mean, 1,543 mL), despite aggressive platelet transfusion. This contrasts with a single-center study of 5,426 patients undergoing first-time CABG in which only 29% had mediastinal blood loss exceeding 1,000 mL, as well as with a recent review of 52 studies reporting on more than 10,000 patients undergoing a variety of cardiac surgical procedures that reported a mean postoperative blood loss of 917 mL [9]. We have been struck by the large quantities of platelets that are required to effectively reverse the postabciximab coagulopathies. Among our 6 patients who underwent operation within 12 hours of abciximab administration, the mean number of platelet transfusions was 34 U.

The administration of abciximab within 12 hours of operation in the present series was associated with a substantial increase in the maximum ACT during cardiopulmonary bypass (519 versus 800 seconds in the late and early groups, respectively). This effect was seen despite the use of similar weight-adjusted heparin doses. A similar effect was reported by Moliterno and colleagues [10], who analyzed the EPIC data and found that patients who received abciximab had a 10% lower heparin requirement to achieve a target ACT between 300 and 350 seconds. Despite receiving significantly lower doses of heparin, the abciximab-treated group had higher initial and maximal ACT values than did the placebo group. These data support an independent anticoagulant effect of antiplatelet agents such as abciximab. These effects can be quantitative (decreased numbers of platelets in a thrombus reduce the amount of catalytic surface available for thrombin generation) and qualitative (inhibition of the catalytic effect of the activated platelet surface on enhancing thrombin production) [11]. Ammer and colleagues [12] have shown in vitro that abciximab, when added to heparinized blood, prolonged the ACT. Additional in vitro analysis showed that abciximab decreased thrombin generation by nearly 50% [13].

Potential strategies for managing patients who have been given abciximab and require cardiac operation include delaying operation until platelet function has returned. Because this often is not possible, our initial approach to these patients was based primarily on the administration of exogenous platelets. Freshly transfused platelets should provide a pool of unbound GPIIb/IIIa to bind abciximab and, by lowering overall levels of receptor blockade, provide a salutatory effect on platelet function. Our perception that even large quantities of exogenous platelets alone frequently are ineffective in reversing abciximab-induced coagulopathies, in addition to the data that support an anticoagulant effect of abciximab, have altered our management of these patients. We now routinely give half-dose heparin (150 U/kg) before cardiopulmonary bypass to achieve a target ACT of between 400 and 500 seconds. We believe that this reduced heparin dose may minimize perioperative bleeding while maintaining adequate levels of anticoagulation.

This series suggests that emergency cardiac operations in patients who have received abciximab frequently are associated with profound intraoperative and postoperative coagulopathies that are difficult to manage with conventional therapeutic strategies, and that the effect of abciximab is most pronounced when the operation is performed within 12 hours of abciximab administration, after which adequate clearance of the drug has occurred and platelet function largely has normalized. It is likely that the cardiac surgeon will be called on more frequently to operate on patients that have been given abciximab or other anti-GPIIb/IIIa agents. Many of these compounds are actively under investigation in clinical trials, including several phase III trials of unstable angina [14]. Two large trials of abciximab recently have been discontinued before complete patient accrual because of highly significant reductions in the study end points among treated patients, according to interim data analysis [15] [16]. The first trial included both low- and high-risk patients undergoing PTCA and showed a substantial decrease in death and myocardial infarction in the patients who were given abciximab. The second trial also showed substantial benefit of abciximab in patients who required urgent PTCA for refractory unstable angina. Details regarding bleeding complications in these trials have not yet been published. It is likely that the widespread use of powerful antiplatelet agents directed at the GPIIb/IIIa receptor will mean that in the future, more patients who come to the operating room will have profound deficits of platelet function and will be at increased risk for hemorrhagic complications after cardiopulmonary bypass.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Albert G. Marrangoni, MD, for his generous assistance with data collection.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. The EPIC Investigators. Use of a monoclonal antibody directed against the platelet glycoprotein IIb/IIIa receptor in high-risk coronary angioplasty. N Engl J Med 1994;330:956-961.[Abstract/Free Full Text] Abciximab product information, Centocor Labs, 1996.
  2. LeBreton H, Plow EF, Topol EJ Role of platelets in restenosis after percutaneous coronary revascularization. J Am Coll Cardiol 1996;28:1643-1651.[Abstract]
  3. Coller BS A new murine monoclonal antibody reports an activation-dependent change in the conformation and/or microenvironment of the platelet glycoprotein IIb/IIIa complex. J Clin Invest 1985;76:101-108.
  4. Coller BS, Scudder LE, Beer J, et al. Monoclonal antibodies to platelet GPIIb/IIIa as antithrombotic agents. Ann NY Acad Sci 1991;614:193-213.[Medline]
  5. Coller BS Inhibitors of the platelet glycoprotein IIb/IIIa receptor as conjunctive therapy for coronary artery thrombolysis. Coron Artery Dis 1992;3:1016-1029.
  6. Mascelli MA, Lance ET, Wagner CL, Weisman HF, Jordan RE Abciximab (7E3) pharmacodynamics demonstrates an extended and gradual recovery from GPIIb/IIIa blockade. Circulation 1996;94(Suppl):3008.
  7. Aguirre FV, Topol EJ, Ferguson JJ, et al. Bleeding complications with the chimeric antibody to platelet glycoprotein IIb/IIIa integrin in patients undergoing percutaneous coronary intervention. Circulation 1995;91:2882-2890.[Abstract/Free Full Text]
  8. Belisle S, Hardy JF Hemorrhage and the use of blood products after adult cardiac operations: myths and realities. Ann Thorac Surg 1996;62:1908-1917.[Abstract/Free Full Text]
  9. Moliterno DJ, Califf RM, Aguirre FV, et al. Effect of platelet glycoprotein IIb/IIIa integrin blockade on activated clotting time during percutaneous transluminal coronary angioplasty or direction atherectomy (the EPIC trial). Am J Cardiol 1995;75:559-562.[Medline]
  10. Coller BS, Anderson K, Weisman HF New antiplatelet agents: platelet GPIIb/IIIa antagonists. Thromb Haemost 1995;74:302-308.[Medline]
  11. Ammar T, Scudder LE, Coller BS In vitro effects of the platelet glycoprotein IIb/IIIa receptor antagonist c7E3 on the activated clotting time. Circulation 1997;95:614-617.[Abstract/Free Full Text]
  12. Reverter JC, Kessels H, Beguin S, et al. Platelet glycoprotein IIb/IIIa inhibition decreases thrombin generation induced by tissue factor [Abstract]. Blood 1994;84:470a. Tcheng JE, Harrington RA, Kottke-Marchant K, for the IMPACT Investigators. Multicenter, randomized, double-blind, placebo-controlled trial of the platelet integrin glycoprotein IIb/IIIa blocker integrilin in elective coronary intervention. Circulation 1995;91:2151–7.
  13. Ferguson JJ EPILOG and CAPTURE trials halted because of positive interim results. Circulation 1996;93:637.[Free Full Text]
  14. Van de Werf F More evidence for a beneficial effect of platelet glycoprotein IIb/IIIa-blockade during coronary interventions. Latest results from the EPILOG and CAPTURE trials. Eur Heart J 1996;17:325-326.[Free Full Text]



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