Asian Cardiovasc Thorac Ann 2002;10:293-297
© 2002 Asia Publishing EXchange Pte Ltd
Experimental Coronary Artery Occlusion: Relevance to Off-Pump Cardiac Surgery
Charles Hsi, MD,
Henri Cuenoud, MD1,
Babs R Soller, PhD,
Hun Kim, MD,
Janice Favreau, BS,
Thomas J Vander Salm, MD,
John M Moran, MD
Division of Cardiothoracic Surgery
1 Department of Pathology University of Massachusetts Medical School Worcester, Massachusetts, USA
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For reprint information contact: Charles Hsi, MD Tel: 1 508 856 2587 Fax: 1 508 856 7520 email: charles.hsi{at}umassmed.edu Department of Surgery, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA 01655, USA.
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ABSTRACT
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Mechanical coronary artery occlusion is required for minimally invasive direct coronary artery bypass and off-pump coronary artery bypass surgery. It is important that the method of occlusion be minimally traumatic. Chronic effects of these methods have never been studied. Temporary occlusion of coronaries utilizing suture snare, silastic loop snare, and bulldog clamp was carried out in 12 Yucatan pigs. Three animals each were sacrificed acutely and at 3, 6, and 12 months. The area of occlusion of each vessel was examined by light microscopy and the degree of damage recorded. In the animals sacrificed acutely, there was more damage using the suture snare than with the other 2 methods, but there was minimal damage at longer intervals. There was slight damage acutely and chronically with the bulldog technique. No damage was seen acutely with the silastic loop technique, but some late damage was found. The techniques of coronary artery dissection and occlusion used for minimally invasive and off-pump bypass surgery may contribute to early postoperative graft occlusion.
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INTRODUCTION
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Currently, most coronary artery bypass graft (CABG) operations are performed on cardiopulmonary bypass (CPB). Using CPB allows coronary anastomosis to be performed in a quiet and bloodless field, which yields an excellent patency rate in the long term. Nevertheless, CPB is associated with several adverse effects, such as bleeding, neurologic complications, tissue edema, myocardial injury, and potential failure to wean the patient from the pump.1,2 Many of these complications can be attributed to mechanical and immunologic alterations of blood components.3 In addition, the use of an aortic crossclamp adds to the risk of myocardial, aortic, and neurologic complications.4
Consequently, there has been a revival of interest in performing CABG on the beating heart without using CPB or aortic occlusion. A number of series using off-pump coronary artery bypass (OPCAB) have been reported.5,6 Establishing simple and safe surgical techniques that provide a quiet and bloodless anastomotic field is essential for successful OPCAB. Minimally invasive direct coronary artery bypass (MIDCAB) without CPB has become widespread in the past 5 years. It can be performed with or without thoracoscopic assistance.7,8 Most cases are done through an anterior small thoracotomy, using mechanical and pharmacologic methods to stabilize the anastomotic area and local coronary artery (CA) occlusion to provide a bloodless field for anastomosis. Recent clinical reports documented relatively low operative mortality in patients who underwent OPCAB through a standard sternotomy for multivessel coronary artery disease.6,9 Complete multivessel revascularization can be achieved with good early clinical and angiographic results in most patients with appropriate positioning of the heart and adequate mechanical stabilization.10 Application of these techniques has allowed shorter hospitalization and reduced costs.11
Although the mortality rates of standard CABG and MIDCAB are reported to be similar,12 some reports documented a high rate of graft occlusion with MIDCAB because of technical difficulties.13–15 As it is necessary to provide mechanical occlusion of the CA in order to allow good visualization in a dry field, it is possible that trauma to the CAs contributes significantly to a higher rate of stenosis or occlusion of the graft or native CA or both. The purpose of this study was to evaluate the degree of coronary vascular damage, both acutely and chronically, caused by 3 commonly used methods of coronary occlusion using a swine model.
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MATERIALS AND METHODS
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Twelve Yucatan micro-swine weighing 30 to 40 kg were used. All animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23). The animals were sedated with intramuscular telazol-ketamine-xylazine mixture (2.2/1.1/0.2 mg.kg-1) and atropine (0.05 mg.kg-1). They were intubated and maintained under general anesthesia using 1% to 2% isoflurane with oxygen and placed on a heating pad to maintain body temperature at approximately 37ºC. The ear vein was cannulated for administration of Ringer’s lactate. Electrocardiographic leads were placed for monitoring heart rate and rhythm, and a 7F catheter was introduced into the right femoral artery to obtain blood gas samples and for placement of a blood pressure transducer (Miller Instruments, Houston, TX, USA).
Three CA sites were identified and minimally dissected to allow precise occlusion: the left anterior descending artery (LAD) beyond the first diagonal, the proximal circumflex (CX) in the atrioventricular groove, and the first obtuse marginal (OM). In each animal, a 3/0 polypropylene suture was passed twice beneath the LAD and then through a soft silastic tourniquet, a soft bulldog clamp was placed on the CX, and a silastic tape was passed twice beneath the OM and then through a soft silastic tourniquet. In succession, as a "preconditioning" maneuver, each vessel was occluded for 3 minutes with the minimum amount of pressure that would create an obvious area of discrete cyanosis in its watershed. The initial occlusion was released for 10 minutes and then reapplied for 15 minutes, simulating the time required for anastomosis. Prophylactic intravenous lidocaine was given prior to occlusion release to prevent reperfusion arrhythmias. Each site was marked with an epicardial suture for later identification.
Three animals were sacrificed acutely; and 9 animals were closed in a routine fashion, allowed to recover, and transferred the following day to a housing facility. After intervals of 3, 6, and 12 months, 3 of the animals were sacrificed each time. The time at which each animal was sacrificed was determined before surgery, and the animals were randomized in the order of surgery and time of sacrifice. In all animals, the heart was excised and placed in 10% formalin for later dissection. At the time of dissection, approximately 2 cm of each CA, centered about the identifying suture, was removed with the surrounding epicardium and muscle. After standard fixation, multiple sections were taken and stained with hematoxylin and eosin for examination by standard light microscopy. All specimens were examined by the same experienced cardiac pathologist, who was blinded to the occlusion technique applied. The degree of injury was graded from 0 to III for each vessel. The characteristics and criteria for grading are described in Table 1
. The histologic degree of injury between the occlusion methods was compared statistically using the Student-Newman-Keuls test, with p < 0.05 being considered statistically significant. The 8 interventions in the acute group (one was abandoned because of technical difficulties) and 27 in the chronic group were analyzed separately.
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RESULTS
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All chronic animals survived and were sacrificed at the planned intervals. The degree of damage in each animal is shown in Table 2. Examples of each category of injury are illustrated in Figure 1.
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Figure 1. (A) Normal coronary artery (N), with no sign of damage to the vessel. (B) Grade I acute (Ia), with endothelial denudation (arrow). (C) Grade I acute (Ia), with endothelial denudation and luminal acute inflammatory cellular infiltrate (arrow). (D) Grade II acute (IIa), with endothelial denudation, inflammatory cellular infiltrate, and red blood cell accumulation in the media (m) and adventitia (a). (E) Grade III acute (IIIa), showing acute myocardial infarction with contraction band necrosis (arrows) and acute inflammatory cellular infiltrate. (F) Grade I chronic (Ic), with slight adventitial fibrosis (*). (G) Grade II chronic (IIc), with moderate degree of adventitial fibrosis (*). (H) Grade III chronic (IIIc), with complete vessel occlusion by proliferative organized thrombosis (*) (hematoxylin and eosin stain, original magnification x110 for all, except x80 for G and H).
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In the acutely sacrificed animals, the suture loop occlusion technique appeared to be the most damaging, with all 3 animals showing signs of injury and grade III damage in one of them, including evidence of early infarction. No damage was seen acutely with silastic loop occlusion, while a small amount of damage from the bulldog clamp was documented. However, there was no statistically significant difference.
It is evident that there were minimal, if any, lasting effects of suture loop occlusion of the LAD. Animal 10, a 12-month sacrifice, had a perfectly normal CA with acute thrombosis estimated to be about 24 hours old. The thrombosis was clearly unrelated to the original operative occlusion. Similarly, there were minimal, if any, long-term effects of bulldog clamping of the CX.
At the 3-month interval, 2 of the 3 OM arteries were occluded and showed impressively proliferative fibrosis, most likely indicative of trauma at the time of operation. Yet, there was minimal evidence of arterial trauma in the 6-month cohort. The level of trauma in the 12-month group was moderate. Statistical analysis of all 27 interventions in the chronic group showed a significant difference between the degree of damage to the OM compared to the LAD and CX (p < 0.05).
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DISCUSSION
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Before the current interest in MIDCAB and OPCAB surgery, there was only occasional need for mechanical CA occlusion, to control noncoronary collateral flow in a quiet, flaccid heart, or in a fibrillating heart. In off-pump procedures, unless there is total coronary occlusion with minimal, if any, collateral circulation, occlusion is necessary proximal to, and sometimes distal to, the point of arteriotomy to attain a dry field and to enable precise anastomosis. The dissection required to ensnare the vessel in the beating heart is more challenging because of cardiac contraction and motion. Current myocardial stabilization techniques reduce this challenge.
In either case, it is important that the method of occlusion is minimally traumatic to avoid the cumulative effect of dissection and occlusion. There is no consensus among surgeons on the least traumatic method of coronary occlusion. Personal preferences vary, with little data on which to base the logical use of one method over another. This study was designed to evaluate the 3 most commonly used means of occlusion, acutely and at intervals of up to 1 year. The Yucatan micro-swine was selected because of anatomic and physiologic similarities of its heart and coronary circulation to those of the human. In addition, they are adult pigs, not subject to growth-induced changes in the heart and CAs.
In the acute group, it is clear that the suture loop technique applied to the LAD was more damaging to the intima and media, but because of the small numbers it did not reach statistical significance. As little damage to the LAD was seen in the chronic group, it may be inferred that effective healing is the norm for that type and degree of injury. Conversely, the lack of signs of acute injury using the silastic loop on the OM was not borne out in the chronic studies, in which there were 2 complete occlusions and only 3 of the 9 vessels in this cohort showed no signs of chronic damage. The most probable cause of injury was the combination of dissection in muscular tunnels and the relatively small size of the OM, one of several branches of the CX. It is unlikely that the inert, soft silastic tape in itself was responsible. Since the 2 animals showing occlusion were the eighth and twelfth animals in the series, a "learning curve" phenomenon was not a factor.
Previous studies have evaluated the effects of vascular clamps and snares on peripheral vessels.16–18 Moore and colleagues17,18 compared the effect of vascular clamps and silastic vessel loops on normal canine arteries and atherosclerotic human artery segments. Vascular clamps caused injury to the endothelium of both normal and diseased arteries, while the silastic loop was atraumatic. In more recent studies of porcine CAs, Perrault’s team investigated the effect of Gore-Tex suture snare19 and the bulldog clamp20 on endothelial function. In these acute studies, the suture snare did not cause endothelial dysfunction, while the bulldog clamp impaired endothelial integrity. Chronic effects of these techniques have not been reported. Additionally, the use of light microscopy, rather than electron microscopy as was used in other vascular studies, provided information about trauma to the media and adventitia. Electron microscopic assessment reveals damage only to the endothelium, potentially underestimating the degree of vascular and myocardial injury caused by dissection and occlusion.
It should be noted that our study was performed on normal swine arteries — the effects of the occlusion methods on human atheromatous and calcified CAs may well be different, and possibly more damaging. However, we expect that the relative effects of these techniques can be extrapolated to the human condition as observed by Moore’s team.17,18
When the study was designed, we wanted to glean as much information as possible from a limited number of animals and felt that 36 interventions in 12 animals would be sufficient to provide answers to the question asked. The findings in the acute animals seemed to validate this approach, but only with analysis of the chronic groups and the unexpected findings was it appreciated that a different study design would have introduced fewer variables and possibly provided better data. For instance, applying a single randomized technique to the same large vessel and avoiding a small vessel, which is more difficult to find, may have been a preferable approach.
In conclusion, the least acute damage to the CA was caused by the silastic loop and the most by the suture snare, with the bulldog clamp in between. Significantly more damage in the chronic animals was found with the silastic loop technique than with the other methods. This study indicates that the techniques of CA dissection and occlusion unique to MIDCAB and OPCAB surgery may contribute to postoperative graft occlusion. Reduced patency and graft occlusion may be avoided by careful operative technique and proper choice of occlusion devices.
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ABSTRACT
INTRODUCTION
