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Ann Thorac Surg 2001;71:122-127
© 2001 The Society of Thoracic Surgeons
a Department of Cardiac Surgery, Leopold-Franzens-University, Innsbruck, Austria
b Institute of Anatomy and Histology, Leopold-Franzens-University, Innsbruck, Austria
c Städtische Kliniken, Oldenburg, Germany
Accepted for publication July 11, 2000.
Address reprint requests to Dr Hangler, Department of Cardiac Surgery, Leopold-Franzens-University Innsbruck, Anichstrasse 35, 6020 Innsbruck, Austria
e-mail: herbert.hangler{at}uibk.ac.at
| Abstract |
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Methods. Coronary arteries of patients with dilated cardiomyopathy (n = 7) or ischemic heart disease (n = 10) undergoing heart transplantation were locally occluded after starting cardiopulmonary bypass. Immediately after excision of the diseased heart, the vessels were fixed. Unoccluded segments served as controls. Integrity of endothelial lining was observed with scanning electron microscopy.
Results. Scanning electron microscopy revealed significantly more severe endothelial injury in the area of occlusion than in the adjacent, not manipulated control segments. In the region of local occlusion, plaque rupture was noted in three of 34 atherosclerotic vessel specimens, injury to side branches was evident in two of 44, and local microthrombus formation was evident in six of 44 samples.
Conclusions. Local occlusion of human coronary arteries during beating heart coronary surgery may cause focal endothelial denudation, local microthrombosis, atherosclerotic plaque rupture, and injury to target vessel side branches.
| Introduction |
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| Material and methods |
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Procurement of tissue
Instantly after excision of the diseased recipient heart, the coronary arteries were perfused for 10 minutes with 2.5% glutaraldehyde in 0.1 mol/L cacodylate buffer (pH 7.4) at a controlled pressure of 120 mm Hg through a perfusion cannula (P616; Stöckert, Munich, Germany) inserted into the left or right coronary ostium. In this way, the endothelium was fixed in situ at physiologic pressure before being further processed for scanning electron microscopy. Subsequently, the vessels were carefully dissected free from the adherent epicardial tissue in a no-touch technique under 12x magnification and cut transverse 5 mm apart from the occlusion area on each side. Control samples were taken from the adjacent not-instrumented areas of the same coronary artery.
Preparation of the coronary arteries for scanning electron microscopy (SEM)
The coronary artery cylinders were cut longitudinally, pinned on cork plates, and postfixed in 1% Osmiumtetroxide (OsO4), further dehydrated in a graded ethanol series, and subjected to critical-point drying (CPD 030; Bal Tec, Balzers, Lichtenstein). After drying, samples were mounted on specimen stubs using colloidal silver and coated with 15 nm gold (MED 020; Bal Tec). The entire endothelial surface of each specimen was examined with a Zeiss DSM 982 Gemini scanning electron microscope, operated at 5 kV.
Histomorphology of the endothelial layer was classified into three grades
In grade I, the entire surface was covered by intact endothelial cells with a tight intercellular attachment (intact endothelial layer). In grade II, there were dehiscent intercellular junctions with isolated detachment of endothelial cells (minor endothelial injury). In grade III, there was an expanse of local endothelial denudation with the subendothelial tissue exposed (severe endothelial injury). Figure 1 depicts the three different categories of endothelial lining.
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2 test or Fishers exact test where appropriate. A p value less than 0.05 was considered to be significant. Continuous data are given as mean ± standard deviation. | Results |
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None of the control coronary artery segments exhibited endothelial damage greater than grade II. These minor changes of the coronary endothelial layer in atherosclerotic human coronary arteries have already been reported [3]. In contrast, 24 of 44 manipulated segments from both patient groups (DCMP and ICHD) showed grade III endothelial injury (p < 0.001). There was no significant difference in regard to grade III injury between instrumented coronary segments from patients with DCMP (14 of 23) and ICHD (10 of 21) (p = NS). Table 1 lists the incidence of endothelial injury according to the five different occlusion methods applied. There was a trend towards a lesser occurrence of grade III injury when occlusion was performed with elastic silicone loops and the MyOcclude device. Occlusion of coronary arteries led to local micro-thrombus formation in six of 44 samples (Fig 2). In three specimens of patients with ICHD after local occlusion, rupture of an atherosclerotic plaque was encountered (Fig 3).
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| Comment |
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Integrity of the endothelial lining is an essential part in the equilibrium of the nonthrombogenic properties of the endothelial surface by inhibiting platelet function and coagulation [10]. When the subendothelial matrix is exposed to circulating blood elements, thrombosis may occur and result in early coronary artery or bypass graft closure. Higher postoperative platelet counts and a minor impaired platelet function, as well as a smaller decrease of circulating coagulation factors in off-pump coronary surgery than in on-pump surgery, with a procoagulant activity could boost local coronary artery thrombosis [11]. Therefore, platelet aggregation and thrombus formation in coronary artery areas denuded of endothelial cell coverage after external occlusion, as detected in this investigation, could be more at risk for thrombosis in off-pump than in on-pump surgery. We were surprised that in this series, despite full heparinization for cardiopulmonary bypass, six cases of local micro-thrombus formation were diagnosed. Because of this finding, we propose to routinely administer full heparin loading in off-pump procedures, keeping the activated coagulation time above 400 seconds with checks at 30-minute intervals. Other authors have suggested lower heparin doses [12]. At present, discussions are ongoing as to whether platelet-inhibiting drugs such as clopidogrel should be administered in the early postoperative period to counteract the procoagulant state in off-pump coronary artery bypass grafting. Perhaps a more vigorous postoperative anticoagulation and platelet-inhibiting pharmacotherapy could be effective. Adequate prospective randomized trials are needed to bring insight into these questions [13].
Furthermore, in the "response to injury hypothesis" [14], endothelial cell injury such as focal denudation or dysfunction of endothelium is considered to be a key event in the evolution of atherosclerosis by inducing growth factor secretion, and attachment of macrophages and monocytes. The loss of endothelial cell coverage because of external instrumentation, as demonstrated by our group, may be healed by regenerating endothelium. Nevertheless, regenerated endothelium is also dysfunctional, as these endothelial cells have lost some of their ability to release endothelium-dependent relaxing factors and are no longer able to prevent aggregating platelet-induced contraction [15]. Occurrence of vasospasm and atherosclerosis may be accelerated in these areas covered by regenerated endothelial cells. Up to now, experiments investigating the effects of coronary occlusion techniques have been preferably performed in normal pig coronary arteries [16] not burdened with preexisting atherosclerosis and chronic endothelial injury with vasomotor dysfunction [17] that could be aggravated by endothelial cell loss from mechanical manipulation. Perrault and colleagues found that intravascular devices create a significantly higher degree of functional damage compared with extravascular occlusion techniques. In regard to these animal experiments, one has to keep in mind the fact that there is already a difference in behavior between vessels of comparable size in the same individual, for instance, very little natural atherosclerotic disease in the internal thoracic arteries in contrast to a much higher degree in coronary arteries or the comparative rarity of naturally occurring atherosclerosis in many species [18].
Moreover, when snare sutures are placed in areas of coronary arteries with severe atherosclerotic disease and the circumferential tension on lipid-laden plaques exceeds its tensile strength, it possibly will rupture at its weakest point and expose atheromatous gruel, the most thrombogenic component of a plaque, to the blood stream. Acute coronary syndromes, depending on the extent of thrombus formation or embolization of atheromatous debris, may occur [19].
Another tool that facilitates constructing anastomosis in off-pump coronary surgery are intracoronary shunts that are carefully advanced into the proximal coronary lumen using a thumb forceps. Flow through the device affirms proper insertion and deairing. The opposite side of the shunt is then advanced into the distal part of the coronary artery so that at least partial blood flow is preserved and may prevent potential intraoperative ischemia with arrhythmias, ST segment elevations, or regional systolic dysfunction that occurs in as much as 40% of off-pump procedures [20]. On the other hand, introducing a device into the coronary lumen can be the cause of dissection or harm endothelial integrity with functional impairment of the coronary artery. Thus, intracoronary shunts could be a useful adjunct in beating heart revascularization. However, further research is required to investigate the impact of shunt insertion on coronary artery endothelial structure and function.
In the current study, a trend towards a lesser incidence regarding denuding endothelial injury was found when coronary arteries were occluded using elastic silicone loops or the MyOcclude device. We therefore propose to use these tools rather than polypropylene sutures. Another advantage of the MyOcclude device is that there is no need to underpass the target coronary artery with the potential for septal branch injury of left anterior descending coronary artery.
Limitations of the study
Limitations of our study are the differences in the techniques of occlusion between the two patient groups and the relatively small number of specimens with respect to the occluding methods.
Conclusions
From this study, we conclude that local occlusion of human coronary arteries by snaring sutures during beating heart coronary surgery can lead to injury of target coronary artery side branches, focal endothelial denudation, plaque rupture, and local micro-thrombus formation. Snaring of the target coronary artery distal to the arteriotomy should not be used. We recommend full heparin loading in off-pump coronary artery bypass procedures until there is sufficient data that lower heparin doses are safe and effective.
| Acknowledgments |
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| Footnotes |
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| References |
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