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Eur J Cardiothorac Surg 2001;19:834-839
© 2001 Elsevier Science NL

Coronary endothelial damage during off-pump CABG related to coronary-clamping and gas insufflation

Yukio Okazaki, Kyomi Takarabe, Jun-ichi Murayama, Etsuro Suenaga, Kojiro Furukawa, Kazuhisa Rikitake, Masafumi Natsuaki, Tsuyoshi Itoh

Department of Thoracic and Cardiovascular Surgery, Saga Medical School, 5-1-1 Nabeshima, Saga City, Saga 849-8501, Japan

Received 10 October 2000; received in revised form 14 February 2001; accepted 26 March 2001.

Corresponding author. Tel.: +81-952-34-2345; fax: +81-952-34-2061
e-mail: okazaki{at}post.saga-med.ac.jp


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Objective: Although off-pump coronary artery bypass grafting (CABG) has been recognized less invasive than conventional CABG on cardiopulmonary bypass, off-pump CABG may be partly invasive especially to the coronary endothelium. The present study was designed to evaluate the adverse effects of coronary snaring with looped sutures and gas insufflation on the coronary endothelium. The protective efficacies on the coronary endothelium of coronary snaring with elastic sutures or humidified gas insufflation with/without heparin and dipyridamole-added were also tested. Methods: Thirty-six mongrel dogs were used. After systemic heparinization (150 U/kg), a 5 mm longitudinal coronary incision was made with looped non-elastic monofilament sutures or elastic sutures applied proximally and distally. The incised coronary artery was exposed to non-humidified carbon dioxide, humidified carbon dioxide with lactated Ringer solution, or humidified carbon dioxide with heparin and dipyridamole-added lactated Ringer solution for 10 or 20 min in each group. After gas insufflation, the incised coronary artery was repaired, then, the coronary was reperfused. Perfusion-fixation was done for observation of the coronary endothelium by scanning electron microscopy. The adverse effect on the endothelium was graded as follows: grade 1, appeared normal; grade 2, few blood cells deposited; grade 3, many blood cells deposited; grade 4, few endothelial cells delaminated with blood cells deposited; grade 5, many endothelial cells delaminated with blood cells deposited. Results: Non-elastic looping caused much more endothelial tears than elastic looping (P<0.00001). Non-humidified gas blowing for 20 min caused more endothelial cell damage than humidified gas blowing (P=0.00005). Non-humidified gas blowing for 10 min caused less damage than for 20 min (P=0.00326), but still caused more damage than humidified gas blowing (P=0.00253). Heparin and dipyridamole-added humidification reduced coronary endothelial area mottled by the deposited cells when compared with simple humidification (P=0.00120). Conclusions: Coronary snaring resulted in coronary endothelial injury, which was ameliorated by using elastic sutures instead of non-elastic sutures. Non-humidified gas insufflation made blood cells deposited and endothelial cells delaminated with time. Humidified gas insufflation attenuated these adverse effects. Heparin and dipyridamole-added humidification had potential advantage in terms of reducing deposited blood cells on the endothelium over simple humidification.

Key Words: Off-pump coronary artery bypass grafting • Coronary endothelial injury • Less invasive cardiac surgery


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Off-pump coronary artery bypass grafting (CABG) has been recognized to be less invasive [1–5]. However, there may be possibility of the coronary endothelial injury related to the coronary snaring and gas insufflation during coronary anastomosis in off-pump CABG.

In the present study, the coronary endothelial injuries related to coronary snaring and gas insufflation were observed using scanning electron microscopy (SEM) in dogs. Protective effects of coronary snaring with elastic sutures, humidified gas insufflation, and heparin and dipyridamole-added humidification were also evaluated morphologically.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
2.1. Animal care
All of the animals involved in this study received humane care in compliance with the Guide for the Care and Use of Laboratory Animals published by the National Institute of Health (NIH Publication No.86-23, Revised 1985) and with the European Convention on Animal Care. All procedures were approved by the Animal Research Committee of the Saga Medical School.

2.2. Animal surgeries
Thirty-six adult mongrel dogs, weighing 20–30 kg, were anesthetized with an intravenous injection of pentobarbital sodium (15 mg/kg body weight) then endotracheally intubated. General anesthesia was maintained by inhalation of isoflurane under mechanical ventilation. The animal was placed in the right lateral position. The chest was entered through the fifth intercostal space and the pericardium was incised and retracted to expose the left coronary arteries. After systemic heparinization (150 U/kg), the first diagonal branch was snared with non-elastic monofilament (3-0 Prolene, Ethicon Inc., Somerville, NJ, USA) or elastic sutures (Elastic, Matsuda Medical Inc., Tokyo, Japan) proximally and distally. A 5 mm longitudinal coronary incision was made between snares. The coronary arteriotomy was exposed to non-humidified carbon dioxide gas (5 l/min), humidified carbon dioxide gas (5 l/min) with lactated Ringer solution, or humidified carbon dioxide gas (5 l/min) with heparin (1000 U/100 ml) and dipyridamole (10 mg/100 ml) added lactate Ringer solution for 10 or 20 min in each group using Visuflo Surgical Site Visualization System (Baxter Research Medical Inc., Midvale, UT, USA). After 10 or 20 min gas insufflation completed, the coronary arteriotomy was repaired with 8-0 monofilament sutures. Both of proximal and distal coronary snarings were released, then, the coronary artery was reperfused for 1 h.

The animal after the simulation of off-pump CABG with coronary snaring and gas insufflation was euthanized with a lethal dose of intravenous pentobarbital and potassium after additional heparinization (additional 150 U/kg) to prevent post-mortem thrombus formation. The heart was excised with the ascending aorta and was perfused with lactated Ringer solution for rinsing. Perfusion fixation of the heart was then performed to preserve the ultrastructures of the coronary endothelium using 2.5% glutaraldehyde in 0.1 M cacodylate buffer with 3% sucrose at a perfusion pressure of 120 cmH2O. The tissue specimens including damaged coronaries with snaring or gas insufflation were stored in the same fixative until it was studied.

2.3. Observation of the coronary endothelium by scanning electron microscopy
After rinsing with 0.1 M cacodylate buffer, the tissue specimens were dehydrated through an ethanol series and freeze-dried. The tissue specimens including the coronary endothelial surfaces were coated with gold (IB-3 ion coater, Eiko Ltd., Mito, Japan), and then observed by SEM (JSM-5200LV, JEOL Ltd, Tokyo, Japan).

To achieve semi-quantitative analysis of the coronary endothelial damage, the adverse effect on the endothelium, which was mainly located at the opposite side to the arteriotomy, was graded as follows: grade 1, appeared normal; grade 2, few blood cells deposited; grade 3, many blood cells deposited; grade 4, few endothelial cells delaminated with blood cells deposited; grade 5, many endothelial cells delaminated with blood cells deposited.

To detect the differences between simple and heparin-dipyridamole-added humidified gas insufflation, the percent endothelial surface area covered by deposited blood cells was calculated using a computer image analysis system (MacSCOPE, Mitani Co. Ltd., Fukui, Japan) on the SEM specimens.

2.4. Statistical analysis
Results are expressed as the mean±standard deviation (SD). Statistical analyses were performed by the Mann–Whitney test to compare the data between the groups. Differences were considered significant at the level of P<0.05. Multiple comparisons were done using single Mann–Whitney tests with Bonferroni-correction as post-hoc comparisons if applicable.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 Appendix A. Conference...
 References
 
3.1. Coronary snaring
Coronary endothelial damage scores in the different settings of coronary snaring are summarized in Table 1. Coronary snaring by monofilament (non-elastic) sutures usually resulted in the coronary endothelial tear, where collagen fibers were exposed and blood cells and fibrin clots were likely to be deposited, not only in case of 20 min exposure (Fig. 1) but also in case of 10 min exposure. These adverse effects caused by coronary snaring were attenuated by using elastic sutures instead of non-elastic sutures both 10 and 20 min (Fig. 2) exposures significantly in terms of coronary endothelial damage scoring (P<0.00001).


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  		Table 1. Coronary endothelial damage scores associated with coronary snaringa

 


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  		Fig. 1. Scanning electron micrograph (x75) of the coronary endothelium after coronary snaring for 20 min by non-elastic suture followed by 60 min blood reperfusion. Torn endothelium was revealed.

 


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  		Fig. 2. Scanning electron micrograph (x350) of the coronary endothelium after coronary snaring for 20 min by elastic suture followed by 60 min blood reperfusion. The adverse effects caused by coronary snaring were attenuated without coronary endothelial tear, but with deposited blood cells on the endothelium.

 
3.2. Gas blowing to the coronary endothelium
Coronary endothelial damage scores in the different settings of gas blowing are summarized in Table 2. Non-humidified gas blowing for 20 min caused remarkable endothelial damages with endothelial cells partly delaminated and blood cells deposited (Fig. 3). Mean endothelial damage score after 20 min non-humidified gas insufflation was 3.67±0.52. Coronary endothelial delaminations related to 20 min humidified gas insufflation were much less observed (Fig. 4) with significantly decreased coronary endothelial damage score (1.50±0.55) than in case of 20 min non-humidified gas insufflation (P=0.00005). Non-humidified gas blowing for 10 min (Fig. 5) caused some coronary endothelial damages mainly with blood cells deposited rarely with endothelial cells delaminated. Mean endothelial damage score after 10 min non-humidified gas insufflation was 2.50±0.35, which was significantly lower than that of 20 min non-humidified gas blowing (P=0.00326). However, it was higher than that of humidified gas blowing for 10 min (Fig. 6) significantly (P=0.00253). In case of humidified gas blowing, coronary endothelial damage score did not increased with exposure time up to 20 min significantly (P=0.28969).


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  		Table 2. Coronary endothelial damage scores associated with gas blowinga

 


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  		Fig. 3. Scanning electron micrographs of the coronary endothelium after 20 min non-humidified gas blowing followed by 60 min blood reperfusion. (A) Coronary endothelial cells were partly delaminated (x500). (B) Many blood cells and fibrin clots were deposited mainly on the denuded area (x1500).

 


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  		Fig. 4. Scanning electron micrographs of the coronary endothelium after 20 min humidified gas blowing followed by 60 min blood reperfusion. Although coronary endothelial cells were quite rarely delaminated, some blood cells were deposited on the endothelial cells (x500).

 


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  		Fig. 5. Scanning electron micrographs of the coronary endothelium after 10 min non-humidified gas blowing followed by 60 min blood reperfusion. (A) Coronary endothelial cells were mottled by many blood cells without delamination (x750). (B) Leukocytes were deposited on the endothelial cells with rolling (x1500).

 


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  		Fig. 6. Scanning electron micrograph of the coronary endothelium after 10 min humidified gas blowing followed by 60 min blood reperfusion. A few blood cells were deposited on the endothelial cells (x1000).

 
The percent of the coronary endothelial surface area that was covered with deposited cells after simple or heparin and dipyridamole-added humidified gas blowing is shown in Table 3. Although heparin and dipyridamole-added humidification for 10 min or 20 min failed to show the advanced coronary endothelial protective effects over simple humidification in terms of coronary endothelial damage score, percentage of the covered endothelial surface area with deposited blood cells after dipyridamole-added humidification was significantly less than simple humidification after 10 min exposure (P=0.00028), as well as 20 min exposure (P=0.00120).


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  		Table 3. The percent of the coronary endothelial surface area that was covered with deposited cells after simple or heparin and dipyridamole-added humidified gas blowinga

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
Appendix A. Conference...
 References
 
Cardiopulmonary bypass (CPB) induces inflammatory response with leukocytes activated [6–11], which injure the myocardium and coronary endothelium during reperfusion [12]. Off-pump CABG has been, therefore, recognized to be less invasive than conventional CABG on CPB in terms of reduced inflammatory response and subsequent myocardial injury associated with CPB [1–5].

The quality of the coronary anastomosis of off-pump CABG is, however, still a great concern. Poirier and her colleagues demonstrated that the anastomoses during off-pump CABG had lesser degree of intraluminal stenosis when performed with the use of a myocardial wall stabilizer [13]. During anastomosis in off-pump CABG, how to keep bloodless surgical field without endothelial injury remains an issue. Although surgeons usually use coronary snaring for coronary occlusion and/or gas insufflation to clear the anastomotic site [14,15], these procedures may cause coronary endothelial injury [16], which may promote blood clotting and smooth muscle cell migration and proliferation at the anastomosis [17].

In the present study, the adverse effects on the coronary endothelium caused by coronary snaring using non-elastic sutures and non-humidified gas blowing were morphologically demonstrated by SEM observation with blood reperfusion after anastomosis completed. In spite of only 60 min blood-reperfusion at the anastomotic site without reverse of systemic heparinization, blood cells were remarkably deposited on the area where the coronary endothelial cells were delaminated. In the clinical settings with much longer blood perfusion and recovered coagulation system after surgery, more blood cells can be expected to be deposited on the injured area with endothelial cells denuded, which will result in thrombus formation at the anastomosis [18]. Furthermore, smooth muscle cell proliferation will be activated [17]. Endothelial injury during off-pump CABG potentially results in the post-operative graft occlusion.

The protective efficacy of elastic coronary snaring and humidified gas blowing on the coronary endothelium was also shown in the present study. However, cognizable blood cells were still deposited on the morphologically intact endothelium. Activation of cell adherences (P-selectin, ICAM-I, GP-IIbIIIa etc.) in the vicinity of anastomosis may occur in off-pump CABG with coronary endothelium functionally damaged. In case of heparin and dipyridamole-added humidification, blood cells deposited on the endothelium reduced when compared with simple humidification. Although coronary anastomosis within 10 min in off-pump CABG may be free from coronary endothelial injury related to simple humidified gas insufflation, heparin and dipyridamole-added humidification potentially have some advantages in case of technically difficult anastomosis that will take more time. Further investigation to reduce endothelial damage and to realize optimal bloodless surgical fields in off-pump CABG should be continued to achieve as reliable anastomoses in off-pump CABG as in conventional CABG.

In conclusion, coronary snaring resulted in coronary endothelial injury, which was ameliorated by using elastic sutures instead of non-elastic sutures. Non-humidified gas insufflation made blood cells deposited and endothelial cells delaminated with time. Humidified gas insufflation attenuated these adverse effects. Heparin and dipyridamole-added humidification had potential advantage in terms of reducing deposited blood cells on the endothelium over simple humidification.


   Acknowledgments
 
The authors wish to express their profound gratitude to Dr Katsuhisa Horimoto, Laboratory of Mathematics, for his guidance on the statistical analysis; Mr Toshimi Tabata and Mr Shin-ichi Nakahara for their technical assistance.


   Footnotes
 
Presented at the 14th Annual Meeting of the European Association for Cardio-thoracic Surgery, Frankfurt, Germany, October 7–11, 2000.


   Appendix A. Conference discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
References
 
Dr D. Boehm (Munich, Germany): I wonder what the influence of your Visuflow, of this spraying device, really is. Are you planning to investigate it as well? Excessive use in off-pump surgery can cause a considerable amount of edematous swelling of the tissues.

Dr Okazaki: In the clinical setting we usually use the flow rate of 5 1/min, so in this experimental study we tested the same flow rate, but in our preliminary study, we tested more than 10 1/min. It caused much severe damage with edema on the artery. So I think it is important to us to use as low as possible a flow rate, I mean, to protect the endothelium from gas.

Mr R. Ascione (Bristol, UK): I can't really understand the rationale of doing this study when it is well known over the last 2 years that the way of doing off-pump surgery is by using an intracoronary shunt and a blower humidifier to enhance visualization. Currently the need of using a proximal snare is only for a few seconds, I mean 5–10 seconds, to open the coronary, to insert the shunt and then you release it. So you are going to have a shunt perfusing the heart during the anastomosis. The shunt is keeping the coronary site open so you can stitch it very nicely.

Also I have a small concern regarding your methodology. You didn't check the effect of your perfusate on the endothelium. You give it at 120 mmHg continuously, whereas the normal flow mostly is during the diastolic phase of the cardiac cycle with a lower pressure, and you did not take into account the effect of the surgical technique itself, like opening the coronary and stitching, on your endothelium.

Dr Okazaki: For the first question and comment you said what?

Mr Ascione: I was just saying that now we are in the era of intracoronary shunts and a blower humidifier to enhance visualization during the anastomosis. So there is no need of snaring for 20 min a coronary, which has been shown already with previous studies to make some problem on the endothelium.

Dr Okazaki: In our preliminary study, we also tested the coronary shunting system, but if we used an oversized shunt, we can see sort of damage of the coronary endothelium. So it is important for us to use a little bit smaller shunt.

Mr Ascione: That is a very good point, the sizing of the shunt is very important and indeed one should choose a shunt just a little bit smaller than the actual size of the coronary to prevent injury. One can actually accept a bit of bleeding as the blower-humidifier will enhance visualization anyway.

Dr Okazaki: And the second question?

Mr Ascione: Was regarding your methodology, as I think you didn't take into account the effect of your perfusate and of surgery itself on the endothelium. I mean the coronary incision and the stitching going through might effect the endothelium. Also you infused the perfusate at a pressure of 120 mmHg continuously, whereas we know that most of the blood perfusion to the heart happens during the diastolic phase of the cardiac cycle with lower blood pressure.

Dr Okazaki: At first I would like to explain the coronary endothelial damage associated with the surgical maneuver. By only suturing we can see severe damage around the anastomotic site, even in case of on-pump CABG.

And the second question, the reperfusion pressure of the blood you mentioned, the pressure in this experiment, we applied usually 100–150 mmHg for systolic pressure and almost 80 mmHg of diastolic pressure, because we used dog, and in case of dog, the blood pressure is usually a little bit higher than human, I think, even under general anesthesia. so the mean reperfusion pressure was almost 100 or 120 mmHg.

And I showed the perfusion pressure of 120 cmH2O was for preparation of the coronary, to view the coronary endothelium by scanning electron microscope. I mean, if coronary collapsed, we cannot see the coronary endothelium. so in tissue specimens, coronary should be wide open, similar to a living setting. So we applied 120 cmH2O pressure for perfusion fixation.

Dr S. Ener (Bursa, Turkey): I just want to make a comment because I have been doing OPCAB surgery since ‘97, and I have got experience with 400 cases. Actually this study doesn't compare with the actual practice, because we don't use continuous blowing, and for every stitch we use only a few seconds. Then the moisture or the misted blowing may be less necessary than we thought with such studies.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 

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  3. Ascione R., Lloyd C.T., Underwood M.J., Lotto A.A., Pitsis A.A., Angelini G.D. Inflammatory response after coronary revascularization with or without cardiopulmonary bypass. Ann Thorac Surg 2000;69:1198-1204.[Abstract/Free Full Text]
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