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Ann Thorac Surg 2000;70:2023-2028
© 2000 The Society of Thoracic Surgeons

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Original article: cardiovascular

Markers of myocardial ischemia after minimally invasive and conventional coronary operation

^a Department of Anesthesiology, Ludwig-Maximilian-University of Munich, Munich, Germany
^b Department of Cardiac Surgery, Ludwig-Maximilian-University of Munich, Munich, Germany
^c Department of Clinical Chemistry, Ludwig-Maximilian-University of Munich, Munich, Germany

Accepted for publication May 4, 2000.

Address reprint requests to Dr Kilger, Department of Anesthesiology, Ludwig-Maximilian-University of Munich, Klinikum Grosshadern, Marchioninistrasse 15, 81377 Munich, Germany
e-mail: erichkilger{at}ana.med.uni-muenchen.de

	Abstract

Top Footnotes Abstract Introduction Patients and methods Results Comment References

 
Background. The purpose of this study was to evaluate the course of serum markers of myocardial tissue damage after two different types of minimally invasive coronary surgical procedures (MICS) as compared with conventional coronary artery bypass grafting (CABG).

Methods. We enrolled 87 patients with one- or two- vessel disease scheduled for one of the three procedures: minimally invasive direct coronary artery bypass grafting (MIDCABG) by lateral thoracotomy (n = 29), the OCTOPUS method by median sternotomy (n = 27), and CABG (n = 31). Creatine kinase activity (CK), creatine kinase MB activity (CK-MB act), creatine kinase MB mass concentration (CK-MB mass), myoglobin concentration (MG), and cardiac troponin I concentration (cTnI) were measured perioperatively until the second postoperative day.

Results. Creatine kinase-MB, CK-MB mass, and cTnI were significantly higher after CABG and were nearly maintained within the normal range in MICS. Creatine kinase and MG were significantly lower in the OCTOPUS group than in the MIDCABG or CABG groups.

Conclusions. Minimally invasive coronary surgical procedures cause less myocardial injury than CABG as indicated by specific serum markers. However, higher CK and MG reflect more substantial skeletal muscle trauma during MIDCABG operation compared with Octopus procedures.

	Introduction

Top Footnotes Abstract Introduction Patients and methods Results Comment References

 
Conventional coronary bypass operation is safe, effective, and has a low mortality rate. However, there is still significant morbidity related to cardiopulmonary bypass (CPB), global cardiac arrest, hypothermia, and median sternotomy [1, 2].

Minimally invasive direct coronary artery revascularization is performed under direct vision on the beating heart. In contrast to the coronary artery bypass grafting (CABG) procedure, this method avoids CPB and cardioplegia with global cardiac arrest [3]. Nevertheless, there is a potential risk of ischemic myocardial injury resulting from normothermic, metabolically active myocardium during the temporary occlusion of the corresponding coronary arteries.

Minimally invasive coronary artery revascularization procedures enable a better investigation than before of the role of CPB for myocardial protection during coronary bypass operation. We can compare the conventional with the newer surgical procedures and their consequences: global ischemia-reperfusion associated with a CABG procedure using CPB, cardioplegia, and global cardiac arrest versus local ischemia-reperfusion due to temporary occlusion of one of the coronary arteries as performed with the minimally invasive techniques.

Therefore, the purpose of this study was to evaluate myocardial damage indicated by creatine kinase (CK) isoenzymes, troponin I, and myoglobin (MG) release in the serum after CABG and after two different minimally invasive coronary artery procedures. Furthermore we compared the two minimally invasive procedures performed at our institution: the minimally invasive direct coronary artery bypass grafting (MIDCABG) technique [4] using a small anterolateral thoracotomy and the OCTOPUS (Medtronic Inc, Minneapolis, MN) technique [5] by median sternotomy.

	Patients and methods

Top Footnotes Abstract Introduction Patients and methods Results Comment References

 
After Institutional Review Board approval and written informed consent 87 consecutive patients, who were scheduled for surgical revascularization, were enrolled in this prospective, noninterventional study between April 1997 and August 1998. The CABG group comprised 31 patients with one-vessel (n = 14) or two-vessel (n = 17) coronary artery disease (CAD). The MIDCABG group included 29 patients of whom 17 were judged as having one-vessel and 12 as having two-vessel CAD. In the OCTOPUS group (n = 27) 15 patients had one-vessel and 12 patients had two-vessel CAD, respectively. The diagnosis of CAD was made by a cardiologist after standard coronary artery angiography (stenosis more than 50%). Indication for surgical treatment was influenced not only by the degree of stenosis but also by its morphologic characteristics (length of stenosis, excentric or filiform). All patients had to fulfill the following inclusion criteria: stable angina, not suitable for balloon angioplasty, not more than two vessels diseased, ejection fraction above 0.50, and no severe cerebral, pulmonary, or vascular disease. Exclusion criteria included age less than 18 years, the presence of unstable angina, myocardial infarction within the last 6 months, or skeletal muscle disease. Criteria for a later exclusion of patients were complications in the postoperative course, defined as: postoperative myocardial infarction as indicated by electrocardiogram (ECG) or significant increases in cardiac enzymes, or discharge from the intensive care unit (ICU) to the general ward later than 42 hours after admission (postoperative day 2) for clinical reasons (eg, hemodynamic instability). This design was chosen to demonstrate only the influence of the different surgical methods (CABG with the use of CPB versus the minimally invasive techniques without CPB).

The decision of which surgical method to apply was based on the following criteria. Indications for MIDCABG included an isolated proximal stenosis of the left anterior descending artery (LAD) or diagonal branch with nearly normal body weight (body mass index less than 27 kg/m²), and no history of thoracic radiation treatment. Indications for the OCTOPUS technique included an isolated LAD, right coronary artery, or diagonal branch lesion, with at most two arteries affected. For both minimally invasive procedures patients with suspected intramyocardial course of the LAD or a LAD less than 1.5 mm or calcified vessels were excluded. We excluded patients with preexisting atrial fibrillation (AF), because AF is still a relative contraindication for minimally invasive procedures. The CABG patients in the control group had to fulfill the same inclusion and exclusion criteria as defined for both minimally invasive groups.

Analysis of CK, CK-MB activity (CK-MB act), CK-MB mass concentration (CK-MB mass), MG concentration, and cardiac troponin I concentration (cTnI) was performed preoperatively (t1), after induction of anesthesia (t2), after aortic unclamping in the CABG group, after left internal mammary artery (LIMA) to LAD anastomosis in the MIDCABG and the OCTOPUS groups (t3), and every 3 hours after admission on the ICU (t4) for the first 42 hours after operation. ST-segment analysis (ST-segment elevation/depression more than 0.1 mV in lead II, more than 0.2 mV in lead V5) was registered continuously, ECGs (12 lead) were measured every 12 hours during the first 48 hours and at last before discharge from the hospital.

For the diagnosis of postoperative myocardial infarction (MI) by means of ECG, standard cardiologic criteria were applied [6]. Interpretation of the ECG was performed blinded by an independent cardiologist of the hospital. The diagnosis was confirmed by myocardial serum markers. Reference values for significant perioperative myocardial ischemia after cardiac operation were reported as CK higher than 700 U/L [7], CK-MB act above 20 U/L [8], CK-MB mass above 45 ng/mL [9], and a MG of more than 400 ng/mL for longer than 12 to 24 hours, respectively [10].

In addition, transesophageal echocardiography was performed after induction of anesthesia, after separation from CPB in the CABG group, after revascularization in the MIDCABG and OCTOPUS groups, and 4 hours postoperatively to detect new segmental wall motion abnormalities (SWMA).

The short-axis, cross-sectional image was divided into four segments using the papillary muscles as guiding structures. The wall motion of each of the four segments were graded as follows: 0 = normal, 1 = mild hypokinesis, 2 = severe hypokinesis with myocardial thickening, 3 = akinesis, and 4 = dyskinesis. An echo episode suggestive of ischemia was defined when wall motion of any segment worsened by two or more grades, lasting more than 1 minute. A persistent ischemic echo episode was defined as echocardiographic changes that persisted throughout 4 hours postoperatively [11].

For all CABG patients, the CPB apparatus used a standard roller pump (1.8 L/m²). The extracorporeal circuit included a membrane oxygenator (Maxima Forte; Medtronic Inc, Minneapolis, MN), cardiotomy reservoir (Medtronic) and an arterial filter (Pall, 40 µm; Pall Corp, East Hills, NY) placed in the arterial line. Moderate systemic hypothermia (32° ± 0.2°C) was used.

Pump flows on CPB were adjusted to maintain a mean arterial pressure above 60 mm Hg and a minimal flow rate of 2.4 L x min^-1 x m^-2 body surface area. Myocardial protection was achieved by infusion of cold hyperkalemic cardioplegia solution (Brettschneider solution) and additional topical cooling with ice-cold solution.

The MIDCABG technique consisted of a small left anterolateral thoracotomy (7 to 8 cm) followed by introduction of a specialized IMA Access Retractor and a mechanical coronary artery stabilizer (CardioThoracic System, Inc, Cupertino, CA) [3]. The Octopus technique included total median sternotomy and the use of a suction device (-400 mm Hg) to provide regional stabilization of the myocardial tissue (Octopus Tissue Stabilizer, Medtronic Inc) [3].

In all 87 patients the LIMA to LAD anastomosis was carried out routinely. In cases necessitating a second coronary artery bypass, a venous bypass graft with continuous incision along the vein course of the lower limb was used.

In both minimally invasive procedures ischemic preconditioning was performed by several brief periods (1 to 2 minutes) of clamping and declamping of the referring vessel [12].

Anesthetic management was uniform in all patients. Premedication was midazolam (0.1 mg/kg) 1 hour before induction. Anesthesia was induced with sufentanil (1.0 to 3.0 µg/kg), midazolam (0.15 to 0.25 mg/kg), and pancuronium bromide (0.1 mg/kg) and maintained as balanced anesthesia with sufentanil (1.0 to 1.5 µg/kg) and a low concentration of isoflurane (0.4 to 0.8 MAC). No additional drugs (eg, esmolol, diltiazem, or adenosine) to lower the heart rate were given. The preoperative cardiovascular medication was continued throughout the perioperative period.

Measurements of catalytic activity of CK in the serum was determined by using commercial reagents (Boehringer Mannheim, Mannheim, Germany) in an automated chemical analyzer (Hitachi 917) at 25°C. CK-MB isoenzyme activity was detected by immunoinhibition with commercial agents (Boehringer Mannheim) in the same analyzer at 25°C. CK-MB mass, cTnI, and MG concentrations were assayed by a fluorogenic sandwich enzyme immunoassay (Behring Diagnostics, Liederbach, Germany) using an Opus Magnum analyzer (Behring Diagnostics, Liederbach, Germany). The upper reference limits for the normal range were set at: CK 80 U/L; CK-MB act 8 U/L; CK-MB mass 5 ng/mL; MG 70 ng/mL; cTnI 0.5 ng/mL.

Statistical analysis was performed by use of the Friedmann, Kruskal–Wallis, Wilcoxon, or Mann–Whitney U test. A p value of less than 0.05 was considered significant. Taking into account the small number of patients Monte-Carlos correction was performed. Liljeforts modification of the Kolmogorov–Smirnov test was applied to analyze the distribution of the data. Data not normally distributed are depicted as median together with the 25th and 75th percentile (Q1/Q3).

	Results

Top Footnotes Abstract Introduction Patients and methods Results Comment References

 
Two patients were excluded because of MI in the postoperative course (1 patient in the CABG group and the other in the MIDCABG group). From the minimally invasive coronary surgical procedures (MICS) groups no patient had to be conversed to the CABG procedure. Demographic data and data from the surgical procedures are depicted in Table 1. The occlusion time in the OCTOPUS group for the right coronary artery or the diagonal branch was 20 minutes (25th/75th percentile, 18/34 minutes) if a second bypass graft was performed. Creatine kinase activity (Fig 1) and MG concentration (Fig 2) were not different in the MIDCABG and CABG groups, but they were significantly lower in the OCTOPUS group. The maximal CK activity reached 304 U/L (25th/75th percentile, 205/390 U/L) 27 hours postoperatively in the CABG group and 294 U/L (25th/75th percentile, 206/327 U/L) in the MIDCABG group, whereas in the OCTOPUS group a maximal CK activity of 132 U/L (25th/75th percentile, 82/186 U/L) was measured 24 hours postoperatively. After 12 hours maximal values for MG of 301 ng/mL (25th/75th percentile, 217/391 ng/mL) were recorded in the CABG group and 299 ng/mL (25th/75th percentile, 260/363 ng/mL) in the MIDCABG group. In the OCTOPUS group 200 ng/mL (25th/75th percentile, 110/291 ng/mL) were reached after 9 hours, respectively. The serum levels of specific markers of myocardial injury—CK-MB act (Fig 3), CK-MB mass (Fig 4), and cTnI (Fig 5)— were significantly higher after CABG throughout the entire measurement period (p < 0.001) compared with both minimally invasive procedures. In the patients of the MIDCABG and the OCTOPUS groups CK-MB act 8.6 (25th/75th percentile, 8.0/12.2 U/L) and 9.3 U/L (25th/75th percentile, 8.1/12.2 U/L), respectively, CK-MB mass 2.6 (25th/75th percentile, 1.5/6.5 ng/mL) and 3.1 ng/mL (25th/75th percentile, 1.7/5.8 ng/mL), respectively, and cTnI 0.5 (25th/75th percentile, 0.5/4.7 ng/mL) and 0.5 ng/mL (25th/75th percentile, 0.5/1.7 ng/mL), respectively, were nearly maintained within the normal range. In the CABG group the peak values of CK-MB act 20 U/L (25th/75th percentile, 13/25 U/L) and of CK-MB mass 31 ng/mL (25th/75th percentile, 21/40 ng/mL) were measured 3 hours postoperatively, whereas the maximum of cTnI concentration 11 ng/mL (25th/75th percentile, 6/16 ng/mL) was detected 9 hours postoperatively. Signs of myocardial ischemia indicated by 12-lead ECG or continuous ST-segment analysis could not be detected in any of the 85 patients remaining in the study. In the CABG group intra- and postoperative transesophageal echocardiography controls revealed no new SWMAs. Few patients of the MIDCABG (n = 3) and the OCTOPUS groups (n = 2) demonstrated transitory SWMA (grade 1) during temporary occlusion of one of the coronary vessels that disappeared completely after revascularization (Table 1).

View larger version (37K): [in this window] [in a new window]   Fig 1. Activity of creatine-kinase (U/L) in the serum of coronary artery bypass grafting (CABG; •), minimally invasive direct coronary artery bypass grafting (MIDCABG; ), and OCTOPUS () patients at the different time points (see text). The symbols represent medians, the bars Q1/Q3 (25%/75% percentiles). (+Significant difference between CABG and OCTOPUS; *Significant difference between MIDCABG and OCTOPUS (p < 0.05); ICU = intensive care unit; OR = operating room.)

View larger version (40K): [in this window] [in a new window]   Fig 2. Concentration of myoglobin (ng/mL) in the serum of coronary artery bypass grafting (CABG; •), minimally invasive direct coronary artery bypass grafting (MIDCABG; ), and OCTOPUS() patients at the different time points. The symbols represent medians, the bars represent the Q1/Q3 (25%/75% percentiles). (+Significant difference between CABG and OCTOPUS; *Significant difference between MIDCABG and OCTOPUS (p < 0.05); ICU = intensive care unit; OR = operating room.)

View larger version (33K): [in this window] [in a new window]   Fig 3. Activity of creatine kinase MB (U/L) in the serum of coronary artery bypass grafting (CABG; •), minimally invasive direct coronary artery bypass grafting (MIDCABG; ), and OCTOPUS () patients at the different time points. The symbols represent medians, the bars represent the Q1/Q3 (25%/75% percentiles). ( #Significant difference between CABG and MIDCABG. +Significant difference between CABG and OCTOPUS (p < 0.05);ICU = intensive care unit; OR = operating room.)

View larger version (34K): [in this window] [in a new window]   Fig 4. Concentration of creatine kinase MB mass (ng/mL) in the serum of coronary artery bypass grafting (CABG; •), minimally invasive direct coronary artery bypass grafting (MIDCABG; ), and OCTOPUS () patients at the different time points. The symbols represent medians, the bars represent the Q1/Q3 (25%/75% percentiles). (#Significant difference between CABG and MIDCABG; +Significant difference between CABG and OCTOPUS (p < 0.05); ICU = intensive care unit; OR = operating room.)

View larger version (35K): [in this window] [in a new window]   Fig 5. Concentration of troponin I (ng/mL) in the serum of coronary artery bypass grafting (CABG; •), minimally invasive direct coronary artery bypass grafting (MIDCABG; ), and OCTOPUS () patients at the different time points. The symbols represent medians, the bars represent the Q1/Q3 (25%/75% percentiles). (#Significant difference between CABG and MIDCABG; +Significant difference between CABG and OCTOPUS (p < 0.05); ICU = intensive care unit; OR = operating room.)

	Comment

Top Footnotes Abstract Introduction Patients and methods Results Comment References

Therefore the increase of the enzymes and proteins in our study, particularly cTnI, which are reliable and highly specific markers of myocardial ischemia during cardiac operation, can be used to assess the efficacy of cardioprotective procedures [13]. Additionally it has to be considered that reversible myocardial ischemia can cause a functional dysintegrity of the cell membranes and a consecutive release of cytosolic enzymes without subsequent cellular necrosis or a relevant decrement in function [14]. The fact that no patient developed MI as indicated by ECG and echocardiography may support the following hypothesis: virtually all patients had temporary myocardial ischemia that lead to release of cytosolic molecules leaking from reversibly injured myocytes. Our study showed that this release is of a significantly greater extent in patients undergoing CABG than those in the MICS groups. Even an occlusion time of 31 minutes in 1 patient revealed no significant release of markers into the serum. This finding could be either an effect of ischemic preconditioning [12] or a result of perfusion of the myocardium distal to the occluded coronary artery by preexisting collateral vessels [15]. The consideration that the OCTOPUS technique is associated with an additional release of serum markers induced by myocardial injury due to the suction devices cannot be supported by our data.

Therefore a postoperative increase of these specific serum markers in patients after MICS without CPB seems to suggest a new myocardial ischemia. One limitation of this study might be that the number of grafts differed between the three study groups. We performed separate subgroup analysis to rule out whether this limitation indeed affected the results of our study.

Comparison of patients in the three study groups receiving a single graft only (CABG n = 14, MIDCABG n = 28, OCTOPUS n = 15) yielded the same results in terms of statistical significance, and therefore confirms our conclusion. In summary the findings of this study have demonstrated minor myocardial injury induced by minimally invasive bypass techniques avoiding CPB and cardioplegia compared with conventional CABG. These results can be confirmed by two recently published studies. Birdi and coworkers [16] demonstrated a small increase in cTnI after minimally invasive coronary artery operation, but the values were considerably lower than in conventional CABG patients. Penttilä and coworkers [17] revealed in coronary operation without CPB only minor changes in myocardial energy metabolism and no clinically relevant increase in cTnI and CK-MB mass concentration, as well.

An additional interesting aspect of our findings was that CK act and MG levels were elevated in the CABG and MIDCAB groups compared with the OCTOPUS group. Different respective causes may contribute to this observation. Inselmann and colleagues [18] reported increases in CK and MG levels in patients undergoing CABG and noncardiac thoracic operation that were comparable to the findings in our study. They explained their findings by transitory cardiac tissue hypoxia (CABG) and the transmuscular surgical access (MIDCABG), respectively. Our data showed that cardiac operation by sternotomy but without CPB (OCTOPUS) does not cause a relevant release of CK and MG. Thus CPB per se seems to induce an additional release of CK and MG. The difference between the MIDCABG and the OCTOPUS group may be explained by the transmuscular access. The exact mechanism that leads to CPB-induced CK and MG elevation cannot be derived from our data and must be the target of further investigation, using markers with more specificity to different tissues.

We conclude that the MIDCABG and OCTOPUS procedures cause significantly lower release of specific serum markers of myocardial injury than conventional CABG. These findings reflect minor myocardial injury when minimally invasive techniques are used. Therefore an increase of these specific serum markers after MICS might be highly suspect for a new myocardial ischemia. However, higher serum CK activity and MG concentration after MIDCABG procedures may be induced by the more vigorous skeletal muscle trauma compared with the OCTOPUS procedure. Despite these promising advantages of minimally invasive revascularization procedures, randomized, controlled studies are necessary to clarify the impact on patients’ outcomes compared with conventional coronary bypass operation.

	Footnotes

Top Footnotes Abstract Introduction Patients and methods Results Comment References

 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/

	References

Top Footnotes Abstract Introduction Patients and methods Results Comment References

 

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