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Ann Thorac Surg 2004;77:1560-1566
© 2004 The Society of Thoracic Surgeons

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Original article: cardiovascular

Off-Pump coronary artery bypass operation does not increase procoagulant and fibrinolytic activity: preliminary results

^a Department of Cardiovascular Surgery, University Hospital Berne (Inselspital), Berne, Switzerland
^b Department of Clinical Research, University Hospital Berne (Inselspital), Berne, Switzerland

Accepted for publication October 8, 2003.

^* Address reprint requests to Dr Englberger, Department of Cardiovascular Surgery, Inselspital, University Hospital, Freiburgstrasse, 3010 Berne, Switzerland
e-mail: lars.englberger{at}insel.ch

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
BACKGROUND: This study analyzes the effects on coagulation and fibrinolysis comparing off-pump coronary artery bypass (OPCAB) and on-pump CABG operations.

METHODS: In a prospective, nonrandomized, comparative evaluation, patients scheduled for elective myocardial revascularization were studied. Due to possible confounding factors patients with postoperative retransfusion of mediastinal shed blood were excluded. Nine patients underwent OPCAB operation and 16 underwent on-pump CABG. Activated clotting time (ACT) was adjusted to 250 seconds in OPCAB (81 ± 18 [mean ± SD] IU/kg heparin) and to more than 480 seconds in on-pump CABG (400 IU/kg heparin, additional 10,000 IU in pump prime). Perioperatively blood samples were collected and hematologic and hemostatic variables including fibrinopeptide A (FPA), fibrin monomer (FM), thrombin-antithrombin complex (TAT), and D-dimer were analyzed.

RESULTS: Both groups showed comparable demographic variables. Number of grafts per patient was slightly higher in the on-pump group (3.6 ± 0.6 versus 3.0 ± 1.1, p = 0.23). The FPA levels did not differ significantly between the groups. The FM, TAT, and D-dimer values were significantly higher in on-pump CABG (p < 0.0001, p < 0.01, and p < 0.0001, respectively), reflecting increased coagulant and fibrinolytic activity. This was also the case when values were corrected for hemodilution.

CONCLUSIONS: Despite lower systemic anticoagulation activation of coagulation and fibrinolysis is reduced in OPCAB compared with on-pump CABG. Reduced thrombin generation and reduced fibrinolytic activity in OPCAB indicates better preservation of hemostasis. We suggest the term "preserved hemostasis" instead of "hypercoagulant activity" with respect to OPCAB.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Coronary artery bypass grafting (CABG) without cardiopulmonary bypass (CPB) has gained increasing popularity and is introduced in routine daily practice with proven short and midterm efficacy and safety. Owing to refinements in surgical techniques allowing improved target vessels exposure without hemodynamic compromise and stabilization combined with an aggressive surgical approach, the majority of CABG patients are eligible for off-pump coronary artery bypass (OPCAB) operations that include full midline sternotomy. However, compared with our understanding of pathophysiologic consequences initiated by extracorporeal circulation [1, 2] only a limited number of studies focus on molecular markers of inflammation and coagulation-fibrinolysis during and early after OPCAB procedures. Recently, concerns have been raised about procoagulant/hypercoagulant activity associated with OPCAB, which may increase the risk of perioperative venous thrombosis and potentially endanger the patency of coronary anastomoses [3, 4]. In addition, dose regimens of intraoperative heparinization and strategies of perioperative prophylaxis (antiplatelet therapy/application of low molecular weight heparin) are highly variable and standard protocols have not yet been developed [5].

The aim of this study was to determine the effects on coagulation and fibrinolysis comparing OPCAB and on-pump CABG operations.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Thirty-two patients scheduled for elective myocardial revascularization were enrolled in this prospective, nonrandomized, comparative study. Exclusion criteria were the following: previous cardiac surgery, left ventricular ejection fraction less than 0.35, myocardial infarction less than 7 days before surgery, neurologic disorders (eg, cerebrovascular accident), severe pulmonary disorders, renal failure (elevation of creatinine and urea), liver diseases, active inflammatory disease, preoperative coagulopathies. Patients receiving preoperative aspirin or heparin were included in the study. Written informed consent was obtained from all patients. Either off-pump technique (OPCAB group) or conventional CABG utilizing CPB (on-pump group) was used depending on the surgeon's decision. Patients were operated on according to our standard routine protocol during the time of enrollment. Owing to possible confounding factors, patients with postoperative retransfusion of mediastinal shed blood were excluded from analysis [6].

Anesthesia, operation, and postoperative care
All patients had premedication with benzodiazepines. General anesthesia was induced and maintained with midazolam, fentanyl and inhalatives (isoflurane or enflurane). Muscle relaxation was achieved with pancuronium bromide. No patient in both groups received antifibrinolytics. Standard monitoring methods including electrocardiography, radial artery line, central venous catheter, two peripheral venous catheters, urinary catheter, and rectal temperature measurement were used in all patients. All patients were operated on according to a standardized surgical protocol. After full midline sternotomy, the left internal mammary artery was harvested in all patients, together with additional graft material (saphenous vein or radial artery, or both).

In OPCAB patients, stabilization of the beating heart was established with the Octopus tissue stabilizer (Medtronic, Minneapolis, MN). After harvesting of the internal mammary artery, intravenous heparin was administered to achieve systemic anticoagulation during surgery with an initial dose of 70 to 100 IU/kg to reach an activated clotting time (ACT) of 250 seconds. Standard use of protamine after the procedure was not intended. It was only given if clinically increased bleeding in the operating field was observed or if the ACT value was still above 200 seconds at the end of surgery. A cell-saving device was not used. During operation no blood was retransfused. Transfusion of packed red blood cells was performed if the hematocrit value was less than 23%.

Heparin dosage was 400 IU/kg in patients operated on with on-pump technique, given before aortic cannulation to achieve full systemic anticoagulation (ACT > 480 seconds). For cardiopulmonary bypass a roller pump (Sarns 9000; 3M Health Care Group, Ann Arbor, MI) and a cooling system (Sarns TCM II; 3M Health Care Group) were used. The extracorporeal circuit consisted of a tubing set (Jostra AG, Hirrlingen, Germany) connected to a hard-shell cardiotomy reservoir (Dideco Venocard D 774, Mirandola, Italy), a membrane oxygenator (Jostra Quadrox HMO 1000), an arterial line filter (Affinity Medtronic, Minneapolis, MN), and a blood cardioplegia system (3M Conducer 4:1). The circuits were primed with a mixture of 1,000 mL Ringer's lactate solution, 1,000 mL 4.0% gelatin preparation, mannitol, and additional heparin (10,000 IU). After cessation of CPB total amount of initial given heparin was neutralized by an equivalent dose of protamine sulfate (1 mg per 100 IU heparin). Extracorporeal circulation was performed with moderate systemic hypothermia (32°C) and nonpulsatile flow at a rate of 2.4 L/min per m² body surface. If additional volume was required macromolecular solution (4.0% gelatin preparation) was added to the circuit. Transfusion of packed red blood cells was performed at a hematocrit of less than 20%. While the patient was fully heparinized on CPB, a cardiotomy suction devise was used to return pericardial blood. After CPB unprocessed pump blood retained in the circuits was returned to the patient.

In both groups ACT was measured using a kaolin-activated system (Automated coagulation timer ACT II; Medtronic HemoTec, Englewood, NJ). Before chest closure, mediastinal and pleural drains were inserted and low-grade suction (20 cm H₂O) was performed. Blood loss was recorded at arrival on the intensive care unit (ICU), 2, 6, and 18 hours after surgery.

Patients were treated in the ICU according to routine protocol. In OPCAB patients up to 12 hours after surgery, shed mediastinal blood was retransfused (Autotransfusion Reservoir; Jostra Medizintechnik, Hirrlingen, Germany) if necessary (hemoglobin < 90 g/L and total drainage volume exceeded 250 mL). Identical criteria for blood transfusion were used in both study groups: packed red blood cells were transfused when hemoglobin value decreased to less than 85 g/L. Transfusion of fresh frozen plasma was indicated to correct suspected deficiency of coagulation factors when drain production was increased (> 250 mL/h).

Prophylactic measures were started at the first postoperative day with orally given aspirin (100 mg once per day) and subcutaneous injection of low-molecular-weight heparin (weight-adapted dosage once per day) in both study groups.

Laboratory analyses
Perioperatively routine hematologic measurements (hemoglobin, hematocrit [HKT], platelet count) and levels of creatinine, creatine phosphokinase (CK) including its isoenzyme MB, and troponin I were recorded in all patients. Samples were analyzed by the central laboratory of the hospital for routine analysis.

Arterial blood samples were collected at six different time points to determine fibrinopeptide A (FPA), fibrin monomer (FM), thrombin-antithrombin complex (TAT), and D-dimer: preoperatively, after induction of anesthesia (T1); during distal anastomoses (OPCAB group), or after aortic declamping (on-pump group), respectively (T2); at the end of surgery (T3); 2 hours (2H), 6 hours (6H), and 18 hours (18H) postoperatively. To determine coagulation and fibrinolysis, blood was used treated with CTADPPACK anticoagulant [7]. Immediately the corpuscular content was separated from the fluid phase by centrifugation at 2,000g for 15 minutes at 6°C. Plasma was aliquoted and stored at –70°C before being assayed. Fibrinopeptide A was measured using a radioimmunoassay (IMCO Corporation, AB, Stockholm, Sweden). Fibrin monomer, TAT, and D-dimer were analyzed employing enzyme-linked immunosorbent assay techniques (Enzymun-Test FM, Roche Diagnostics, Rotkreuz, Switzerland; Enzygnost TAT micro, Dade Behring, Marburg, Germany; Dimertest, Agen Biomedical, Acacia Ridge, Australia). All samples were assayed in duplicate and the mean value is reported.

Statistical analysis
Statistical analysis was carried out using standard software (StatView 5.0.1, SAS Institute, Cary, NC). Data are presented as mean ± SD in text and tables and as mean ± SEM in graphs. A ² analysis or Fisher's exact test was used for categorial data. Nonparametric evaluation was performed for other variables (Mann-Whitney U test). Laboratory results were tested within the groups to detect time interactions (Wilcoxon signed-rank). Differences between the groups for repeatedly measured variables (laboratory results) were analyzed with analysis of variance (ANOVA) testing. If ANOVA showed significant differences post hoc nonparametrical testing (Mann-Whitney U) between the groups at single time points was added. A p value less then 0.05 was considered statistically significant.

Since a different level of hemodilution in both study groups has been anticipated, laboratory results (platelet count, FPA, FM, TAT, and D-dimer) were analyzed without and with correction for hemodilution according to the formula: [Sample_corrected]_TX = [Sample]_TX x [HKT]_T1/[HKT]_TX.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Both groups showed comparable demographic characteristics and intraoperative variables (Table 1). No statistically significant differences were noted between the groups with respect to mean age, gender, body mass index, left ventricular function and operating time. Mean total number of grafts per patient was slightly higher in the on-pump group, but without significant difference between the groups. Twenty patients (69%) of the whole study group received aspirin within 7 days before surgery (Table 1).

Renal functional creatinine compared preoperatively and at the first and second postoperative day showed no significant differences between the groups. A trend toward lower levels of the routine myocardial markers CK, CK-MB and troponin-I at the first postoperative day was visible in the OPCAB group (Table 3).

Hematocrit and platelet count
As expected hematocrit was significantly lower in the on-pump group (Fig 1, A). Compared with baseline (T1) values were significantly lower in both study groups at all sampling points (T2 to 18H; p < 0.05 for each correlation). Minimal mean values were detected during CPB (T2) in the on-pump group (24% ± 3% versus 33% ± 4% in the OPCABG group during operation, p < 0.001) and 2 hours postoperatively in OPCAB patients (29% ± 3% versus 27% ± 4% in the on-pump group, p = 0.19).

View larger version (12K): [in this window] [in a new window]   Fig 1. (A) Hematocrit (ANOVA p < 0.001). (B) Platelet count without correction for hemodilution (ANOVA p = 0.001). (C) Platelet count with correction for hemodilution (ANOVA p < 0.05). Data are presented as mean ± SEM. Significant intergroup differences (*p < 0.05; **p < 0.01; ***p < 0.001). Circles = off-pump group; diamonds = on-pump group. (ANOVA = analysis of variance; H = hours postoperative; T1 = baseline; T2 = during operation; T3 = end of operation.)

Fibrinopeptide a
Levels of FPA did not differ significantly between the groups (Fig 2, A). Compared with baseline (T1) only at the end of operation (T3) in the on-pump group significantly elevated values were detected (p < 0.01). Statistically comparable differences within the groups and also no significant difference between the groups were detected if values were corrected for hemodilution (ANOVA between groups, p = 0.63).

View larger version (13K): [in this window] [in a new window]   Fig 2. (A) Fibrinopeptide A (FPA [ANOVA p = 0.83]). (B) Fibrin monomer (FM [ANOVA p < 0.0001]). Values shown not corrected for hemodilution. Data are presented as mean ± SEM. Significant intergroup differences (*p < 0.05; **p < 0.001). Circles = off-pump group; diamonds = on-pump group. (ANOVA = analysis of variance; H = hours postoperative; T1 = baseline; T2 = during operation; T3 = end of operation.)

Thrombin-Antithrombin complex
Levels of TAT were significantly lower in the OPCAB group (Fig 3, A). Compared with baseline (T1) values were significantly elevated at T3 to 6H in the on-pump group, whereas no significant elevated values in the OPCAB group were detected over the whole study period (T2 to 18H). Maximal mean values were detected in the on-pump group at the end of operation (32.4 ± 17.9 µg/L versus 6.3 ± 3.0 µg/L in the OPCAB group, p < 0.001). Statistically comparable differences within the groups and between the groups were detected if values were corrected for hemodilution (ANOVA between groups, p < 0.01).

View larger version (14K): [in this window] [in a new window]   Fig 3. (A) Thrombin-antithrombin complex (TAT [ANOVA p < 0.01]). (B) D-dimer (ANOVA p < 0.0001). Values shown not corrected for hemodilution. Data are presented as mean ± SEM. Significant intergroup differences (*p < 0.05; **p < 0.01; ***p < 0.001). Circles = off-pump group; diamonds = on-pump group. (ANOVA = analysis of variance; H = hours postoperative; T1 = baseline; T2 = during operation; T3 = end of operation.)

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
In this study we present some preliminary results comparing OPCAB and on-pump CABG with respect to thrombin activity (FPA, FM), thrombin formation (TAT), and fibrinolysis (D-dimer). Serum changes of these markers have been previously attributed to CPB and to ischemia-reperfusion injury during cardiac operations [8, 9]. Cardiopulmonary bypass and its negative effects on hemostasis, platelet count and function may lead to increased postoperative bleeding, substantial need for foreign blood transfusion and adverse outcome [10]. However, impaired hemostasis (on the venous as well as on the arterial site) may prevent development of deep vein thrombosis, pulmonary embolism, and postoperative graft thrombosis. In order to reduce CPB associated morbidity, OPCAB has gained popularity. Utilizing the OPCAB technique, hemostatic competence seems to be preserved and postoperative bleeding is attenuated [11, 12]. On the other hand, one area of concern is the uncertainty of an existing increased procoagulant or even hypercoagulant state in OPCAB operations.

Mariani and coworkers [3] investigated patients with off-pump single myocardial revascularization performed either with midline sternotomy or anterolateral thoracotomy. They found that 24 hours after surgery procoagulant markers were elevated compared with baseline regardless of the surgical approach. They conclude that OPCABG patients may be at increased risk of thrombotic graft occlusion and pulmonary embolism that requires adequate perioperative anticoagulation for these patients. However, this study did not include on-pump control patients. Recently, another study [13] investigated activation of coagulation and fibrinolysis comparing on-pump CABG and OPCAB. It was demonstrated, that after adjustment for hemodilution, both surgical modalities were associated with a comparable net consumption of antithrombin and fibrinogen, whereas transient decrease in platelet counts and increased D-dimer formation occurred only in the on-pump group. Twenty-four hours after surgery, the hemostatic profile was found to be similar in both groups. Nevertheless, this study was focused on indirect markers (consumption products fibrinogen and antithrombin) of the plasmatic coagulation cascade.

Despite a low level of intraoperative heparinization in our OPCAB patients we found significantly elevated molecular markers reflecting thrombin activity (FM) and thrombin formation (TAT) in on-pump CABG compared with OPCAB in the perioperative period. Since intergroup differences were found in levels of FM but not in FPA generation (both markers of thrombin activation), an explanation can be given by the different kinetics of these markers: FPA with a quite short half-life (3 to 5 minutes) is reflecting acute thrombin activity; whereas elevated values of FM are indicative for ongoing coagulation or reflect the sum of the coagulation process by accumulated molecules due to a long half-life. Well defined factors of activated coagulation in on-pump CABG are the contact of blood with the foreign surfaces of the extracorporeal circuit [8, 9], blood air contact in open venous reservoir [14], as well as the use of cardiotomy suction [15], that are all factors present in our on-pump group. These findings underline that some degree of thrombin activation may occur even with full-dose heparinization triggered by a powerful prothrombotic stimulus during surgical setting of CABG with CPB. Compared with the results in the OPCAB group, where consistently lower levels of thrombin activity (FM) and thrombin formation (TAT) have been demonstrated, one may assume attenuation of consumptive coagulopathy.

Increased activation of fibrinolysis measured by D-dimer formation was detected in the on-pump group, which is in accordance with the finding of Casati and colleagues [13]. However, activated fibrinolysis starting in the early postoperative hours was seen also in OPCABG patients. This may justify the use of antifibrinolytics in OPCAB in order to reduce postoperative blood loss [16, 17].

Differences between the two patient groups were significant in terms of the measured plasmatic markers of coagulation and fibrinolysis despite the limited number of patients investigated. Nevertheless, our results are limited on plasmatic markers of coagulation and fibrinolysis and we did not perform functional tests on platelets. We found higher platelet counts in the OPCAB group, but the differences were less pronounced after correction for hemodilution. This also indicates that the avoidance of CPB may reduce functional abnormalities and consumption of platelets. Overall the result may be a less disturbed equilibrium between procoagulant and anticoagulant activity in patients operated with OPCAB technique.

In view of this experience we would like to recommend the term "preserved hemostasis" as better than "hypercoagulant activity" in the situation after OPCAB operation. Since hemostasis is preserved thromboembolic prophylaxis is mandatory and commonplace like in other types of major surgery. Further research has to be directed to the development of perioperative anticoagulation standards and the optimal use of antiplatelet agents in OPCAB.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
We thank Marianne Stutz and Trinh Cung for laboratory help at the Thrombosis Research Laboratory, Department of Clinical Research, University Hospital Berne, Switzerland.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Friedrich S. Eckstein Thierry P. Carrel Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Englberger, L. Articles by Carrel, T. P. Search for Related Content PubMed PubMed Citation Articles by Englberger, L. Articles by Carrel, T. P. Related Collections Minimally invasive surgery