Ann Thorac Surg 1996;62:109-114
© 1996 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Impact of Transfusion of Mediastinal Shed Blood on Serum Levels of Cardiac Enzymes
Dao M. Nguyen, MD,
Brian M. Gilfix, MD, PhD,
France Dennis, CCP,
David Blank, MD,
David A. Latter, MD,
Patrick L. Ergina, MD,
Jean E. Morin, MD,
Benoit de Varennes, MD
Divisions of Cardiothoracic Surgery and Clinical Biochemistry, Royal Victoria Hospital and McGill University, Montreal, Quebec, Canada
Accepted for publication March 8, 1996.
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Abstract
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Background. Infusion of shed mediastinal blood using an autotransfusion system is a widely applied technique of blood conservation in cardiac surgery. Serial determinations of serum creatine kinase (CK), its MB isoenzyme (CK-MB), and lactate hydrogenase (LDH) levels have been used to monitor perioperative myocardial injury. We investigated the impact of postoperative autotransfused blood infusion on serum levels of these enzymes.
Methods. We performed a retrospective analysis of postoperative serum CK, CK-MB, and LDH levels of 300 patients who had elective uncomplicated aortocoronary bypass grafting. Shed mediastinal blood samples from 26 patients were analyzed for CK, CK-MB (enzymatic activity and mass), and LDH levels before infusion.
Results. High postoperative serum levels of CK and LDH were observed after infusion of autotransfused blood. Shed mediastinal blood contained extremely high levels of these enzymes, particularly from patients who had internal mammary artery dissection. There was a strong correlation (r = 0.96) between measured CK-MB enzyme activities and those calculated from the CK-MB mass units.
Conclusions. Infusion of autotransfused blood containing high concentrations of CK and LDH results in elevated serum levels of these enzymes. Hemolysis, frequently present in shed blood, does not interfere with the routine biochemical assays for CK and CK-MB enzyme activities. Caution should be taken when postoperative cardiac enzyme levels are used to determine myocardial injury after aortocoronary bypass grafting if autotransfusion is used as a method of blood conservation.
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Introduction
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Aortocoronary bypass grafting (CABG) is one of the most commonly performed operative procedures in North America. It has been estimated that up to 75% of patients undergoing primary CABG receive transfusion of homologous packed red blood cells or blood products in the perioperative period [1]. Numerous methods and strategies of blood conservation have been devised and implemented in many cardiac surgery centers to minimize the risks and costs of homologous blood transfusion [2, 3]. One component of these blood conservation strategies involves infusion of shed mediastinal blood using an autotransfusion system (ATS) in the immediate postoperative period. The hematologic and biochemical effects of infusion of shed blood have previously been documented [4–7]. Wahl and associates [5] demonstrated in a small group of cardiac patients that infusion of mediastinal drainage that contained high levels of creatine kinase (CK) and lactate dehydrogenase (LDH) activities resulted in an elevation of these enzymes in the peripheral blood. Because postoperative detection of myocardial infarction depends on serial measurements of serum CK, CK-MB, and LDH activities, together with others, the impact of infusion of shed mediastinal blood on the circulating blood levels of these enzymes needs to be further defined.
The objective of our study was to document the effects of infusing shed mediastinal blood on the serum levels of CK, CK-MB, and LDH activities in the early postoperative period. Enzyme present in samples of shed blood was measured to identify the cause of elevated serum levels of these enzymes. Moreover, we also correlated CK-MB isoenzyme levels measured by the enzyme immunoinhibition method (used in the enzymatic assay) to those quantitated by the CK-MB mass concentration analysis. This was done to determine if hemolysis that is normally present in ATS blood would interfere with the biochemical assay of CK/CK-MB and be partially responsible for the elevation of CK and CK-MB activities observed after infusion of shed mediastinal blood.
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Material and Methods
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The demographics, clinical courses, and serum biochemical values of a highly selected group of 300 patients were obtained from the Royal Victoria Hospital Cardiac Surgery Registry over a 48-month period between November 1991 and November 1993 (out of 1,100 patients). Infusion of shed mediastinal blood using the ATS (Atrium Inc, Hudson, NH) was initiated at our institution at the beginning of November 1992 as part of a blood conservation protocol for cardiac surgical patients. The patient selection criteria were elective procedure, uncomplicated primary isolated myocardial revascularization, no postoperative bleeding complication that required reoperation, absence of significant postoperative hemodynamic instability that required more than 12 hours of inotropic support or the use of intraaortic balloon cardiac assist device, and no evidence of new Q wave or ischemic changes in postoperative serial electrocardiographic examinations. One hundred ten patients had internal mammary artery (IMA) and saphenous vein grafts and postoperative mediastinal blood infusion with ATS (group I), 80 patients had saphenous vein conduits only and postoperative ATS infusion (group II), and 110 patients (group III) serving as controls for the above-mentioned two groups had IMA and vein grafts but did not have ATS (using instead mediastinal sump drains with the shed blood discarded).
All patients were operated on by the same group of surgeons employing uniform surgical techniques and postoperative care protocols. Cold blood cardioplegia (Plegisol St. Thomas; 1:4 cardioplegia to blood ratio; Abbott, North Chicago, IL) delivered through a multiple perfusion set with ventline (DLP, Grand Rapids, MI) cardioplegia catheter via the aortic root and individual vein grafts was used for myocardial protection. Mild to moderate total body hypothermia (28°C to 32°C) and bubble oxygenator (Bentley 10 plus; Bentley-Baxter, Irvine, CA) cardiopulmonary bypass were used in all patients. At the end of the cardiac procedure, mediastinal tubes were inserted (one in the anterior mediastinum, the other in the pericardial sac), connected to the ATS, and placed to -20 cm H2O suction. The blood collection chamber was primed with 50 mL of citrate-phosphate-dextrose solution as an anticoagulant. The connecting tubings were gently milked every 15 to 20 minutes to prevent clogging of the tubes. Shed mediastinal blood was infused when the collection chamber was full or after 4 hours had elapsed, whichever occurred first. Collection of shed blood for infusion was discontinued when drainage was less than 50 mL/h. Mediastinal blood was infused via blood transfusion tubing having an in-line blood filter.
Serum CK-MB and LDH activities were measured at 0, 12, 24, and 48 hours after the operation. In 26 patients who had ATS (18 in group I and 8 in group II), mediastinal blood samples were collected before infusion and the CK, CK-MB, and LDH activities were measured to determine if high concentrations of enzymes in ATS blood were responsible for the elevated serum levels of activity observed after ATS blood infusion. Mass concentrations of CK-MB in the postoperative serum and in ATS blood samples were also quantified in this group of 26 patients. Total CK activity, CK-MB activity, and LDH activity were measured on a Beckman Synchron CX-7 automatic analyzer (Beckman Instruments Inc, Brea, CA) using commercially available reagents supplied by Beckman. The upper limit of the reference range was taken to be 145 U/L for total CK activity, 24 U/L for CK-MB activity, and 210 U/L for LDH activity, based on studies on our hospital population. Creatine kinase-MB mass was measured on a Ciba-Corning ACS:180 automatic analyzer using reagents supplied by Ciba Corning Canada Ltd (Markham, Ontario, Canada). The upper limit of the reference range is, according to the manufacturer, 7.5 µg/L. The specific activity of pure CK-MB was taken to be 800 IU/mg of enzyme at 37°C based on information provided by Boehringer-Manneheim Canada (Laval, Quebec, Canada).
The results were expressed as means and standard deviations. Pearson correlation coefficient, analysis of variance with Bonferroni test, 
2 test, and Student's t test were used for statistical analysis where indicated; p less than 0.05 was considered significant.
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Results
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The demographic and operative data of the three groups of patients summarized in Table 1
were compared by the appropriate statistical test. The age, total cardiopulmonary bypass time, and total volume of shed mediastinal blood infused were similar between groups I and II. There were more female patients in group II (40%) than in groups I (11%) and III (15%). The number of bypass grafts in groups I (3.3 ± 0.9) and III (3.4 ± 0.9) were similar (p > 0.05), but greater than that in group II (2.3 ± 1.0) (p < 0.001). Groups I and III were comparable in terms of age, sex distribution, number of bypass grafts, and the total cardiopulmonary bypass time.
In all patients, the serum levels of CK and LDH activities within 48 hours after cardiac revascularization were greater than the upper reference limits for CK and LDH activities at our institution. Serum CK levels were similar in groups I (ATS and IMA grafts), II (ATS and no IMA), and III (no ATS, IMA grafts) immediately after the operation. Infusion of shed mediastinal blood in association with IMA dissection (group I) resulted in the greatest elevation of serum CK activity between 12 and 24 hours after operation (p < 0.0001 versus group II and group III); this activity remained elevated at 48 hours postoperatively (p < 0.0001 versus group II and p < 0.05 versus group III) (Fig 1). The serum CK-MB fraction as percentage of the total CK activity was less than 5% in all groups at 12, 24, and 48 hours after operation (group I: 3.7% ± 1.6%, 3.5% ± 1.5%, 3.3% ± 1.4%; group II: 4.3% ± 1.2%, 3.6% ± 2.1%, 3.9% ± 1.9%, group III: 3.6% ± 2.0%, 3.3% ± 2.5%, 4.9% ± 2.9%, respectively). Infusion of shed mediastinal blood either with or without IMA dissection (groups I and II) was associated with a persistent and significant elevation of LDH activity up to 48 hours after operation (Fig 2). The LDH activities in these groups were significantly higher than those of the controls (group III). The high degree of hemolysis in the shed mediastinal blood was the main cause of such an increase in the postoperative serum LDH activity. All mediastinal blood samples showed gross evidence of hemolysis; upon centrifugation, their supernatants were pinkish to red in color. Even without ATS infusion (group III), there was an increased LDH activity above the upper reference limit (210 IU/L) in the early postoperative period.
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Fig 1. . Serial serum total creatine kinase activity at 0, 12, 24, and 48 hours after aortocoronary bypass grafting. Creatine kinase activities are significantly elevated, reaching a peak level 12 hours after bypass grafting, during the entire study period in group I. The upper limit of normal serum creatine kinase activity is 145 IU/L.
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Fig 2. . Serial serum lactate dehydrogenase activity at 0, 12, 24, and 48 hours after aortocoronary bypass grafting. Infusion of shed mediastinal blood either in the presence (group I) or absence (group II) of internal mammary artery harvesting resulted in significantly higher serum levels of lactate dehydrogenase activity than those of group III in the immediate postoperative period. The upper limit of normal serum lactate dehydrogenase activity is 210 IU/L.
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Eighteen shed mediastinal blood samples from group I and 8 from group II were analyzed for CK, CK-MB, and LDH enzymatic activities before infusion. Mediastinal blood samples of group I patients contained an extremely high level of CK (7,760 ± 3,908 IU/L); only 3.8% ± 2.2% was CK-MB. This level was much higher than the CK activity detected in ATS blood of group II patients (1,496 ± 535 IU/L; p < 0.001). Similarly, ATS blood samples from group I patients contained higher levels of LDH activity (1,290 ± 569 IU/L) than those of group II (571 ± 309 IU/L; p < 0.005) (Fig 3).
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Fig 3. . Total creatine kinase (CK) and lactate dehydrogenase (LDH) activity in the samples of autotransfused blood of patients in group I (n = 18) and group II (n = 8). There are high levels of CK and LDH in autotransfused blood, significantly higher in samples of group I patients. Mean CK-MB fraction was 3.8%.
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Figure 4 demonstrates the relationship between CK-MB activity as determined by immunoinhibition assay and CK-MB activity calculated from the corresponding measured CK-MB masses using the conversion factor of 800 IU/mg of enzyme. For 121 paired determinations (both peripheral and mediastinal blood samples), there was an excellent correlation between these two entities with a correlation coefficient of r = 0.96 (95% confidence interval = 0.94 to 0.97).
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Fig 4. . Correlation of the serum creatine kinase (CK)-MB activity as measured by biochemical assay and the CK-MB activity equivalent as calculated from the concomitantly measured CM-MB mass using the conversion factor 800 IU/mg of enzyme. The correlation coefficient is 0.96.
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Comment
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Wahl and associates [5] reported in a preliminary study the effects of reinfusing ATS blood on the levels of "cardiac enzymes" (CK, LDH, aspartate aminotransferase) in the circulation. They demonstrated that shed mediastinal blood contained very high levels of these enzymes and that the serum levels were drastically elevated 1 hour after ATS blood infusion. In the study reported here, we demonstrated the following in uncomplicated CABG patients: (1) early postoperative serum levels of CK and LDH activities in patients with or without ATS infusion were much higher than the upper reference limits, (2) serum CK activities were highest in patients having ATS infusion in the presence of IMA dissection, (3) in the absence of IMA dissection, creatine kinase levels were similar to controls, (4) infusion of shed mediastinal blood (both groups I and II) was associated with significantly elevated serum levels of LDH activity, and (5) finally, shed mediastinal blood from patients having IMA grafting contained five times more CK and two times more LDH activity than that of patients not having IMA harvestings. Dissection of IMA pedicles with associated skeletal muscle damage, which releases a large quantity of CK into the reinfused mediastinal shed blood, appears to be the most important cause of the observed elevation of CK activities in the circulating blood volume. This was confirmed by the demonstration of an extremely high level of CK activity in the shed blood samples (see Fig 3
). Even though ATS blood of group II did contain a moderately high level (1,496 ± 535 IU/L) of CK, infusion of a relatively small volume (about 600 mL) of this ATS blood (see Table 1, group II) would not have a big impact, due to dilution of the CK activity in a much larger circulating blood volume. Lactate dehydrogenase is a ubiquitous enzyme abundantly found in various tissues including muscle (striated, smooth, cardiac), liver, and red blood cells. A high level of LDH activity in ATS blood is derived mainly from lysed red blood cells, traumatized skeletal muscles, and other tissues. Infusion of LDH-rich mediastinal shed blood leads to levels that are much higher than those of the control group. On the other hand, release of LDH into the circulation from damaged tissues at the operative site is probably the explanation for mildly elevated LDH serum levels above the upper limit of normal in the control group. Other local and systemic sources of CK, CK-MB, and LDH include myocardium at the atrial cannulation site, myocardial dissection to locate intramural coronary arteries, and their release from other tissue such as stomach, small intestine, lung, colon, and liver secondary to noncardiac-related tissue injury from inadequate tissue perfusion or systemic inflammatory response after cardiopulmonary bypass. Systemic subclinical hemolysis due to mechanical trauma to erythrocytes during cardiopulmonary bypass would further contribute to the elevation of LDH activity.
Elevated serum levels of CK, CK-MB and LDH activities have been observed after uncomplicated cardiac procedures [8, 9]. Graeber and associates [9] studied postoperative serial serum CK, CK-MB, LDH, and LDH1/LDH2 ratios in cardiac surgical patients (elective CABG, atrial septal defect closure, mitral valve replacement). Enzyme levels were elevated above the upper limit of normal in every case (especially in atrial septal defect and mitral valve replacement patients, presumably due to incision and suturing of atrial tissue) up to 4 days postoperatively. Mitral valve replacement and CABG patients having transmural postoperative myocardial infarction (MI) had the greatest elevation of CK and CK-MB (as fraction of total and absolute isoenzyme activity), and an LDH1/LDH2 ratio greater than 1.00. If CK-MB activity of greater than 50 IU/L was chosen as the upper reference limit (a cutoff point much higher than that of 10 IU/L in nonsurgical patients), then the sensitivity and specificity of CK-MB in detecting postoperative MI were 94% and 100%, respectively [9]. Creatine kinase levels reached 800 to 1000 IU/L range in those patients. Such levels are lower than those of uncomplicated CABG patients with ATS infusion in our study. A number of group I patients in our study had serum CK-MB activity higher than 50 IU/L up to 24 hours after operation, even though the CK-MB fraction was less than 5%. Similar to our finding, other investigators noted high levels of CK-MB activity in the immediate postoperative period in the absence of MI [8–10]. Reperfusion of ischemic myocardium induces complex cellular changes that are frequently associated with a rapid and excessive shedding of cytoplasmic enzymes [11].
Identification of perioperative MI in cardiac surgical patients has great clinical implication. Post-CABG transmural (Q-wave) MI has been shown to be associated with higher operative mortality and an overall lower long-term actuarial survival. The major impact of perioperative MI on mortality occurs before hospital discharge, as indicated by the observation that uncomplicated MI patients who survived to leave the hospital have no adverse 3- and 5-year survival rates [12–14]. A complicated perioperative MI (cardiogenic shock, congestive heart failure, arrhythmias), however, exerts a potent negative effect on long-term survival, even in hospital survivors [12]. A combination of diagnostic modalities has frequently been employed to detect perioperative MI: serial electrocardiograms, serologic myocardial enzyme markers (CK, CK-MB, LDH, and LDH1/LDH2 ratio) and more recently, CK-MB mass measurement and cardiac troponin T quantitation [15–17]. After cardiac procedures, the characteristic evolution of myocardial ischemia/non-Q infarction is frequently compromised in the presence of new bundle-branch blocks, preexisting Q wave, or cardiac pacing. The postoperative results of conventional serologic markers of myocardial injury are even more difficult to interpret, especially with infusion of shed mediastinal blood, as has been discussed here. The increase in total CK activity (the denominator of the percent MB calculation) may lower the MB fraction associated with a small non-Q MI, and potential important interventions such as extended electrocardiographic monitoring, more stringent evaluation, and follow-up may be withheld. Cardiac troponin T, the tropomyosin-binding subunit of the regulatory complex of the myofilament, has recently been evaluated as a marker even more specific for the detection of myocardial injury. Early results have demonstrated its usefulness, with specificity and sensitivity that surpass conventional CK-MB assay in detecting MI [15, 18]. The diagnostic potential of troponin T for postoperative MI in cardiac surgical patients, particularly those receiving ATS blood infusion, needs to be further studied.
Determination of CK and CK-MB levels by biochemical assay may be falsely elevated by the presence of high degrees of hemolysis [19], which may be observed in patients receiving ATS infusion. More recently, a convenient immunologic assay has become available for clinically applicable rapid measurement of CK-MB physical mass in serum. Its use has been shown to increase the clinician's ability to accurately detect a small MI with equivocal elevation of CK-MB enzyme activity and electrocardiographic changes that is otherwise not diagnosed by conventional methods [15–17]. Its measurement, moreover, is not prone to interference by hemolysis or atypical and macromolecular forms of CK. We demonstrated in our study that measurement of serum CK-MB enzymatic activity in the presence of shed mediastinal blood infusion correlated very well with that calculated from mass determination. These findings indicated that the degree of hemolysis seen in our patients did not interfere with the enzymatic method of CK-MB activity measurement. It appears that biochemical assays for serum CK and CK-MB levels remain reliable in this patient population. Elevated CK and CK-MB activity noted in the post-CABG period therefore reflected the levels of enzymes released from tissues and not an effect of hemolysis.
Infusion of shed mediastinal blood in the presence of IMA dissection is associated with high levels of CK (with normal CK-MB fraction) and LDH activities in the circulation of patients undergoing uncomplicated myocardial revascularization. Enzymatic assay is a reliable method to quantitate CK and CK-MB even in the presence of significant hemolysis. Similar studies in unselected cardiac surgical patients are clearly needed to further define the impact of ATS infusion on serum levels of cardiac enzymes. Elevation of CK and LDH levels in the peripheral blood secondary to ATS use undermines the usefulness of serial enzyme determination as a screening method for myocardial infarction. New serologic diagnostic criteria or other markers should be evaluated for an accurate detection of myocardial injury after cardiac operations.
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Acknowledgments
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We acknowledge the enthusiastic support of the Cardiac Intensive Care Unit Nursing staff for collecting numerous blood samples and the technical assistance of Ms Violet Nagy, Ms Nancy Maguigad, Ms Joan Ohashi, and Mr Tony Fascia of the Department of Clinical Biochemistry, Royal Victoria Hospital, in performing various assays. We thank Ms Manon Francoeur for her help in the preparation of the manuscript.
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Footnotes
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Doctor Nguyen's current address is Department of Thoracic and Cardiovascular Surgery, University of Texas MD Anderson Cancer Center, Houston, TX 77030. 
Address reprint requests to Dr de Varennes, Division of Cardiothoracic Surgery, Royal Victoria Hospital, Rm S8.44, 687 Pine Avenue W, Montreal, Quebec, Canada H3A 1A1.
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Abstract
Introduction
