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Eur J Cardiothorac Surg 2000;18:594-601
© 2000 Elsevier Science NL

Interleukin-1, interleukin-6 and myocardial enzyme response after coronary artery bypass grafting – a prospective randomized comparison of the conventional and three minimally invasive surgical techniques

^a Cardiovascular Institute, University Hospital Dresden, Fetscherstrasse 76, 01307 Dresden, Germany
^b Institute for Laboratory Medicine, University Dresden, Dresden, Germany

Received 14 December 1999; received in revised form 14 July 2000; accepted 15 August 2000.

Corresponding author. Tel.: +49-351-450-1790; fax: +49-351-450-1512
e-mail: vassilios.gulielmos.hkz_dd{at}t-online.de

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
Objective: In order to evaluate the traumatic effects of median sternotomy and cardiopulmonary bypass (CPB) in conventional and minimally invasive coronary artery bypass grafting, inflammatory response was studied in a prospective randomized trial in patients referred to single-vessel coronary artery bypass grafting. Methods: Four surgical techniques were compared: group 1, median sternotomy with CPB in ten patients (eight male, two female; aged 59.6±11.0 years (mean±SD)); group 2, median sternotomy and off-pump in ten patients (seven male, three female; aged 65.1±10.0 years); group 3, minithoracotomy with CPB in ten patients (seven male, three female, aged 61.2±10.4 years); group 4, minithoracotomy and off-pump in ten patients (nine male, one female, aged 62.9±9.8 years). All patients received a left internal mammary artery graft to the left anterior descending artery (LAD). Clinical data, perioperative values of cytokines and cardiac enzymes were monitored. Results: There were no major complications. Troponin-T and creatine kinase isoenzyme MB (CK-MB) levels were significantly higher in CPB procedures (P<0.0056; multivariate general linear model). Interleukin-6 (IL-6) levels were significantly higher in minithoracotomy procedures. Interleukin-1 (IL-1) was significantly increased in all patients compared with the preoperative values. Conclusions: The use of CPB is combined with higher levels of troponin-T and CK-MB as signs of myocardial damage. Surgical access was identified as a trigger of inflammatory response, as minithoracotomy is related to higher levels of IL-6. IL-1 increased in all procedures and this occurred independently of the surgical access or the use of CPB, which points out a potential relationship between inflammatory response and anesthesia. Neither CPB nor surgical access influenced the clinical outcome in the treatment of coronary artery single-vessel bypass grafting.

Key Words: Inflammatory response • Cardiopulmonary bypass • Off-pump coronary artery bypass grafting • Cytokines • Troponin-T

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
Blood exposure to artificial surfaces activates complement, leukocytes, coagulation, fibrinolytic and kallikrein cascades, and platelet function is impaired [1]. This inflammatory response of the organism, known as the ‘post-pump’ syndrome, consists of increased capillary permeability, leukocytosis, accumulation of interstitial fluid and organ dysfunction [2]. Proinflammatory cytokines, such as interleukin-1 (IL-1) and interleukin-6 (IL-6), contribute to postoperative myocardial ischemia and segmental wall motion abnormalities, and even hemodynamic instability, after cardiopulmonary bypass (CPB) [3]. Troponin-T and creatine kinase isoenzyme MB (CK-MB) are reliable markers for the diagnosis of perioperative myocardial infarction, and even for estimation of the severity of myocardial damage [4–6]. All of the above-mentioned comments were the results of studies which were always performed under standard conditions in cardiac surgery, such as CPB, median sternotomy and anesthesia. New less invasive techniques in cardiac surgery allow surgical treatment of single-vessel coronary artery disease (CAD), either avoiding CPB or median sternotomy, or even both [7–9]. This situation enables the combination of CPB and off-pump procedures with two different surgical accesses (median sternotomy and minithoracotomy), thus resulting in four different surgical techniques for the treatment of single-vessel CAD: (1), the conventional technique (median sternotomy and CPB); (2), off-pump coronary artery bypass (OPCAB; median sternotomy and off-pump); (3), minimally invasive pump coronary artery bypass (MIPUCAB; minithoracotomy and CPB); (4), minimally invasive direct coronary artery bypass (MIDCAB; minithoracotomy and off-pump). In a well defined patient group using these four different techniques, detection, with each factor being responsible for a certain inflammatory reaction, is feasible.

After the introduction of several less invasive surgical techniques for the treatment of CAD at the Cardiovascular Institute in Dresden and having already experienced the learning curve, we initiated a study using the four above-mentioned techniques, prospectively and randomly, to define the right trigger for various parameters possibly responsible for the phenomenon known as inflammatory response.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
The study protocol exactly defined the number of patients and exclusion criteria, in addition to an exact description of each technique planned to be used, with published experience in this field. The volume of blood samples and sampling times were also exactly defined.

After review, board approval was admitted by the ethics committee of the University of Dresden and the series was started. Informed consent was obtained from every patient included in this study. All patients were referred to our institution for single left internal mammary artery (LIMA) bypass to the left anterior descending artery (LAD), due to CAD. Patients also suffering from coronary artery double-vessel or multivessel disease, with only the LAD being amenable for surgery, were also included in this study. Patients with impaired left ventricular ejection fraction (LVEF, <30%), with impaired lung and renal function were excluded from the study. Further exclusion criteria were: unstable angina, major calcification of the ascending aorta and obesity (body mass index (BMI) of >30 kg/m²). In the patients included in the study, salicylate therapy was stopped 10 days before operation. Patients receiving dipyridamole, anticoagulants or immunosuppression were excluded from the study, as were patients with previous cardiac operations or previous myocardial infarction in a period of less than 2 weeks.

2.1. Anesthesia protocol
All patients received 1–2 mg Lormetacepam p.o., depending on body weight, at an exact time on the evening before operation. Morphine–HCL (0.1–0.2 mg/kg body weight s.c.), in addition to 2.5 mg dehydrobenzperidol s.c., was given 1 h before operation. In order to achieve maximal standardization of conditions, skin incision was always performed at 08:00 h. Anesthesia was inducted using methohexital (1 mg/kg body weight i.v.), fentanyl (0.03 mg/kg body weight i.v.), succinylcholin (1 mg/kg body weight i.v.) and vecuronium (0.1 mg/kg body weight i.v.). A single lumen endotracheal tube was inserted and enflurane was used to maintain anesthesia in a clinically related concentration. Two million KIU aprotinin were given i.v. at a standard time. After harvesting the internal mammary artery (IMA), 500 IU/kg heparin was injected i.v. in all cases. In procedures using CPB, normothermia was used, also avoiding topical cooling. At the end of the procedure, heparin was always reversed using 400 int. IU/kg protamine. Invasive arterial pressure, central venous pressure and 6-led ECG monitoring were performed during the procedure. For temperature monitoring, an intravesical catheter was used.

2.2. Extracorporal circuit
The oxygenator used in the extracorporal perfusion circuit in patients receiving CPB procedures was Highlight 7000 (MEDOS GmbH, Stolberg, Germany). A single hard-shell non-collapsible reservoir was used for active venous drainage (MEDOS GmbH). The arterial return cannula used was a 24 F (MEDOS GmbH). For venous drainage in median sternotomy procedures, a dual stage venous cannula (MEDOS GmbH) was used, and in minithoracotomy procedures, a percutaneous transfemoral 28 F catheter (MEDOS GmbH) was used. The priming volume for the circuit was 1800 ml electrolyte solution (Ringer's lactate solution, Fresenius, Bad Homburg, Germany) with 10 000 IU heparin. After heparin was given and until protamine reverse, the anti-clotting time (ACT) was controlled every 15 min in order to prolong the ACT above 480 s (ACT; Medtronic, Duesseldorf, Germany). If necessary, additional heparin was administered to maintain the initial prolongation of the ACT. The flow initiated for extracorporal circulation was always 2.5 l/m² per min. Cardiac arrest was inducted by antegrade crystalloid cardioplegic solution (500 ml ‘Eppendorf solution’; Fresenius, Germany).

2.3. Patient groups and surgical techniques
One out of four techniques was prospectively chosen for each patient at random.

2.3.1. Conventional group
Two female patients and eight male patients (n=10) were evaluated for single LIMA bypass to the LAD using median sternotomy and CPB. The age ranged from 47 to 77 years (mean±SD, 59.6±11.0 years). The LVEF was 71.3±12.6% and the BMI was 26.7±2.9 kg/m². All patients were referred for single LIMA bypass to the LAD, but four patients were suffering from coronary artery multivessel disease, the other coronary vessels not being amenable for surgery. Seven patients had a previous myocardial infarction and two patients had previous percutaneous transluminal coronary angioplasty (PTCA) and/or stenting.

At surgery over a median sternotomy on CPB and after cross-clamping, the LIMA to LAD anastomosis was performed in a standard fashion.

2.3.2. OPCAB
Three female patients and seven male patients (n=10) were evaluated for OPCAB surgery using median sternotomy and off-pump. The age ranged from 44 to 88 years (65.1±10.0 years). The LVEF was 58.2±21.9% and the BMI was 26.3±3.7 kg/m². All patients were referred for single LIMA bypass to the LAD, but six patients suffered from multivessel CAD, five had a previous myocardial infarction and one patient had received a previous PTCA and stenting.

At surgery over a median sternotomy using stay sutures between the left half of the pericardium and the soft tissue, the heart was rotated to the right, resulting in medialization of the LAD, thus providing better access to this coronary vessel. Using the ‘Octopus’ (Octopus; Medtronic, Inc.), the coronary artery was occluded using a snare (4.0 Prolene; Ethicon, Norderstedt, Germany). After preconditioning (2' min temporary occlusion of the coronary vessel, reperfusion 2', and again occlusion for the anastomosis), the anastomosis was performed with the aid of an air blower to keep the operative sites free from blood.

2.3.3. MIPUCAB
Three female and seven male patients (n=10) were evaluated for single coronary artery bypass grafting through a minithoracotomy using CPB. The age ranged from 46 to 76 years (61.2±10.4 years), LVEF was 76.5±9.1% and the BMI was 26.4±2.4 kg/m². All patients were referred for single LIMA bypass to the LAD, but two patients were suffering from multivessel CAD. Four patients had a previous myocardial infarction and no patient had previous PTCA or stenting.

The LIMA was harvested via a minithoracotomy. The right atrium was cannulated transfemoral percutaneously for venous drainage for CPB. The ascending aorta was cannulated and dissected from the pulmonary trunk on pump. A conventional aortic clamp was used for external cross-clamping and cardioplegia was applied via the ascending aorta. During cardioplegic arrest, the relaxed heart was rotated for exposure of the LAD. Anastomosis of the LIMA to the LAD was performed. The procedure was performed as described by Gulielmos et al.[10].

2.3.4. MIDCAB
One female patient and nine male patients (n=10) were evaluated for MIDCAB surgery through a minithoracotomy off-pump. The age ranged from 45 to 77 years (62.9±9.8 years), LVEF was 60.1±12.8% and the BMI was 25.4±1.4 kg/m². All patients were referred to single LIMA bypass grafting, but three patients suffered from multivessel CAD. Three patients had a previous myocardial infarction and two patients had received previous PTCA and stenting.

The LIMA was harvested via a minithoracotomy. The ‘CTS’ LAD stabilizer of CTS (CTS, Cupertino, CA) was used for stabilization of the coronary vessel. Anastomosis between LIMA and LAD was performed in a standard manner as described by Boonstra et al. [11].

2.4. Monitoring
Perioperative values, such as operative time, postoperative ventilation, CPB time (if used), cross-clamping time and coronary occlusion time were monitored. If, for any reason, the procedure could not be completed as planned, the patient would be excluded from the study and this would be documented as a conversion. Particular attention would be given to eventually ‘take backs‘, as this would be combined with additional anesthesia and would probably falsify the results. IL-1, IL-6, CK-MB and Troponin-T were monitored in nine different times. Venous blood samples were drawn:

1. At 5 min before induction of anesthesia.
   
2. On induction of CPB or occlusion of the LAD.
   
3. At 15 min after induction of CPB or occlusion of the LAD.
   
4. At 1 h after induction of CPB or occlusion of the LAD.
   
5. At 2 h after induction of CPB or occlusion of the LAD.
   
6. At 6 h after induction of CPB or occlusion of the LAD.
   
7. At 12 h after induction of CPB or occlusion of the LAD.
   
8. At 24 h after induction of CPB or occlusion of the LAD.
   
9. At 48 h after induction of CPB or occlusion of the LAD.
   

Twelve-led ECGs 4 h after operation, on postoperative days 1 and 6, as well as 3-month ECGs and coronary angiograms, were planned to document the quality of the anastomosis and the absence of myocardial infarction.

2.4.1. Cytokines
IL-1 and IL-6 were measured in the plasma by means of kits (Quantikine^® HS Human IL-1ß and IL-6 immunoassay) obtained from R & D Systems, Minneapolis, MI. In addition, adjustment for hemodilution.

2.4.2. CK-MB
CK-MB levels were measured in the plasma by means of kits (BM/Hitachi 705) obtained from Boehringer, Mannheim, Germany. There was an adjustment for hemodilution.

2.4.3. Troponin-T
Troponin-T levels were measured in the plasma by means of kits (Elecsys^® Troponin-T STAT immunoassay) obtained from Boehringer, Mannheim, Germany. There was an adjustment for hemodilution.

2.5. Statistical analysis
Statistical analysis was made with SPSS version 9.0 (SPSS GmbH Software, Munich, Germany). The patient and surgical data were analyzed using the Mann–Whitney U-test. Differences with P<0.05 were defined as statistically significant.

For detecting significant increases or decreases in the laboratory parameters, we used the Wilcoxon signed rank test. With Bonferroni correction, we defined P<0.00625 as statistically significant.

After log-transformation of the laboratory parameters to reach a normal distribution, we used the multivariate general linear model to analyze the influences of the surgical access and the use of CPB. After using the Bonferroni correction, we defined P<0.0056 as statistically significant.

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
Between the four groups, there were no differences in terms of age, BMI or incidence of previous infraction. Postoperative transthoracic echocardiogram (TTE) or transesophageal echocardiogram (TEE) showed same as preoperative or better LVEF. In no case was interruption of the procedure necessary, and all procedures were completed as they were planned. All patients left the operating room in sinus rhythm without signs of ischemia or necessity for inotropic support. The 3-month coronary angiogram always revealed patency of the anastomoses. The time of operation, CPB time, if used, cross-clamping time, coronary occlusion time and postoperative ventilation time are listed in Table 1. There were no major complications in all four groups. Postoperatively, CK-MB, troponin-T, 12-led ECG and echocardiography excluded a myocardial infarction.

View larger version (17K): [in this window] [in a new window]   Fig. 1. Levels of CK-MB (mean±standard error). Statistical significance, *P<0.001, multivariate general linear model.

View larger version (19K): [in this window] [in a new window]   Fig. 2. Levels of troponin-T (mean±standard error). Statistical significance, *P<0.005, multivariate general linear model; and statistical significance, **P<0.001, multivariate general linear model.

View larger version (16K): [in this window] [in a new window]   Fig. 3. Levels of IL-6 (mean±standard error). Statistical significance, *P<0.005, multivariate general linear model; and statistical significance, **P<0.001, multivariate general linear model.

	4. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
Today, in coronary artery single-vessel disease, where the LAD is the target vessel, the surgical treatment of choice, although older than 30 years, is still LIMA bypass [12] for better long-term results [13], and is always combined with median sternotomy and CPB, presenting the golden standard of cardiac surgery for many decades now. In the beginning of the 1980’s, perioperative morbidity led cardiac surgeons to seek the sources which were responsible. CPB was accused of initiating the ‘post-pump’ syndrome, stimulating a serious number of scientists to try and explain this inflammatory reaction of the body in order to find a way to avoid it [1,2]. Even if some cytokines reveal a cytoprotective characteristic [14], some are damaging and involved in septic shock [15]. Several proinflammatory cytokines (IL-1 and IL-6), as endogenous proteins, influence the immune response to injury in general [16]. Proinflammatory cytokines also show cardiovascular activity[17]. IL-6 is more a marker than a mediator of injury[3], which also shows inflammatory properties, synergistically with IL-1, being implicated in the pathophysiology of autoimmune diseases [18]. In estimating such sensitive markers, maximum standardization is required in order to avoid false results. When assessing cytokines in coronary artery bypass surgery, a major source of error is technical failure in myocardial infarction [19]. We were therefore very precise in the diagnosis of eventual myocardial infarction for any reason, and above all, reasons related to technical failure. Apart from 12-led ECGs, cardiac muscle specific enzymes (CK-MB and troponin-T), hemodynamics, ECG, 3-month echocardiographies and 3-month angiograms were performed in order to detect patients with poor surgical results and exclude them from this evaluation. We were very fortunate to find all grafts patent after 3 months of operation with no postoperative decrease in the LVEF. In addition, ischemia signs were completely absent in the ECGs, thus excluding the case of myocardial infarction.

As patients with impaired renal function were excluded from this series, there was no influence upon troponin-T levels. The rise of troponin-T levels in all procedures, can be explained as a different degree of myocardial damage related to the surgical trauma itself [6]. Higher rates of troponin-T were found in CPB groups as soon as 2 h after the start of CPB/LAD-occlusion with a high statistical significance (P=0.0001; Wilcoxon signed rank test) versus beating heart procedures remaining at the same level even 48 h after the start of CPB/LAD-occlusion. This suggests that the use of CBP is involved in myocardial damage despite the protective properties of cardioplegia, which is in agreement with other groups [4]. However, these higher rates never reached levels indicating myocardial infarction. CK-MB levels revealed an equal course to that of troponin-T, with an earlier fall after 24 h, almost reaching normal levels at 48 h, also indicating that CPB is involved in myocardial damage.

A temporary decease of IL-1 with recovery up to the ‘normal’ range within the next 2 h, followed by a further increase in the next 48 h, was found in all patients. There was no dependence, either to the use of CPB or to the surgical access.

The main goal of this study was to isolate the use of CPB and the surgical access as different parameters by choosing different combinations among those in order to identify the real trigger of several reactions. The fact that a rise in IL-1 was detected in all groups, independent of the surgical access and the use of CPB, leads us rather to the thought that anesthesia and/or operative trauma, in general, might be triggers as yet not well identified. Higher levels of IL-1 related to the use of CPB admitted by others might find their explanation in the use of aprotinin, or even in our short CPB times, as we only included single bypass procedures [20].

IL-6 levels increased in all groups within the first 2 h after the start of CPB/LAD-occlusion and reached a maximum after about 12 h. It is very interesting that higher levels were already found at 6 h in minithoracotomy rather than median sternotomy procedures with a statistical significance (P<0.001; Mann–Whitney U-test), showing no relation to the use of CPB. Patients with impaired LVEF often reveal perioperative high levels of IL-6 [21]. Impaired LVEF was an exclusion criterion in this series, thus resulting in the elimination of this source of error.

This difference lasted up to 48 h when levels started decreasing in all groups. This phenomenon suggests that IL-6 in procedures with short CPB times is more related to muscle damage (minithoracotomy) than to the use of CPB or bone injury, which confirms the hypothesis already made [22]. Our findings reveal that the lower IL-6 levels in CPB rather than others, are probably due to the fact that the CPB times for a single graft in our series were significantly shorter than those described by others [17,22].

	5. Conclusions

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
As the use of CPB is associated with higher levels of troponin-T and CK-MB, there is a relationship between myocardial damage and the use of CPB. The rise in IL-1 in all procedures, independently of the use of CPB or the surgical access, suggests that anesthesia and/or operative trauma play a role not yet fully identified. The surgical access (minithoracotomy) was detected as a trigger of inflammatory response (IL-6), even when the skin incision was smaller than in median sternotomy and bone injury was not involved.

	Footnotes

 
Presented at the 13th Annual Meeting of the European Association for Cardio-thoracic Surgery, Glasgow, Scotland, UK, September 5–8, 1999.

	Appendix A. Conference discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 
Dr R. Dion (Brussels, Belgium): You say that it might be beneficial to use beating heart or minimally invasive procedures in emergency patients and in those with bad LV function. Don't you think that, precisely in these situations, and for obvious practical reasons and the sake of safety, it would be preferable to go through a median sternotomy and stick to a classical CPB operation?

Dr Gulielmos: Well, first of all, we should answer the question whether a CPB procedure is of benefit in impaired myocardial function, and I think this is definitely the case, because as we found using CPB, we have myocardial damage in a situation where already there aren't as many ‘myocardial cells’, if you want to put it like that. I think that impaired LVEF is an indication for off-pump procedures, and we had a paper about this topic, proving that, indeed, it is the case.

Now, about the other issue, using median sternotomy and off-pump procedures in emergency cases, I cannot prove that, but we had, at our institution, several cases of emergency cases with myocardial infarction within the past 10 h, and we performed coronary bypass grafting, not using CPB, and these patients did very well without necessitating an intra-aortic balloon pump or inotropic support. We would never use minithoracotomy in an emergency case.

Dr V. Subramanian (New York, NY, USA): I have two questions. First, obviously the inflammatory response, the magnitude of it and its effect on clinical outcome will be dependent largely not only on the access and CP bypass, but more so on comorbid factors. Do you expect the same finding in people with higher risk comorbidity, such as renal failure, COPD and multiple other problems?

Secondly, it seems interesting to me that you use aprotinin in all of these patients. As you know, aprotinin has a decisive effect on reducing postoperative bleeding and a very strong inhibitive effect on complement activation, so you might have blunted the response of inflammatory release in CPB by using aprotinin, and if that is the case, then aprotinin is probably a very useful drug, even in off-pump cases. Can you comment on that?

Dr Gulielmos: With regard to your second question with aprotinin, there are a couple of studies implying that the use of aprotinin decreases inflammatory response, at least in a certain way. As you see, we were very happy to assess a huge amount of inflammatory parameters, and aprotinin does not decrease every inflammatory parameter, but some of those.

With regard to your first question, I think that you are totally right. I mean, Dr. Subramanian, we all know he is one of the leaders in off-pump surgery, and we saw that in a study we performed on patients at high risk for CPB procedures, they definitely benefit, whether you are dealing with impaired LVEF or impaired renal or lung function.

Mr R. Stanbridge (London, UK): One or two other studies have also confirmed the same sort of findings, that pharmacy agents are worse on bypass and markers. They also correlate with the length of time of bypass, and I wondered if you noticed any correlation with the time of bypass rather than just whether it was bypass?

Dr Gulielmos: You are absolutely right, because if we take a look at the literature, we find with regards to IL-6 levels, that if we are dealing with longer CPB times, we will find also an increase of this cytokine as well, but in this certain patient group of single-vessel disease, as you know, CPB time is always very reduced. I think the longest CPB time we had, using small access, was about 38 min, so IL-6 was never found to be increased in this particular patient group, as I said, with short CPB times.

Dr D. Saksena (Bombay, India): My question relates to the statement that you made that in sick patients and patients with recent infarct, you are better off operating on a beating heart and the LV function is less likely to suffer. My question is, do you believe that if you operate on patients with a beating heart on bypass, that means without clamping the aorta, would there be any difference, in your opinion, in the LV function whether you clamp the aorta or do it without clamping the aorta on CPB?

Dr Gulielmos: I cannot answer 100% to this question as I don't know the answer, but I have a few thoughts about that. It depends on the disease of the patient. Speaking of, for instance, chronic gastritis, we should definitely try to avoid CPB as homovanillic acid showed us, but with a patient who necessitates emergency and who is hemodynamically unstable, I think you have no other alternative.

	References

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion 5. Conclusions Appendix A. Conference... References

 

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