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Ann Thorac Surg 1998;66:1705-1708
© 1998 The Society of Thoracic Surgeons

Nonpenetrating stapling: A valuable alternative for coronary anastomoses?

Gianfranco Lisi, MDa, Louis P. Perrault, MD, PhDc, Philippe Menasché, MD, PhDa, Alain Bel, MDa, Michel Wassef, MDb, Jean-Paul Vilaine, MDc, Paul M. Vanhoutte, MD, PhDc

a Department of Cardiovascular Surgery, Hôpital Lariboisière, Paris, France
b Department of Pathology, Hôpital Lariboisière, Paris,, France
c Cardiovascular Division, Institut de Recherches Servier, Suresnes, France

Accepted for publication June 16, 1998.

Address reprint requests to Dr Menasché, Department of Cardiovascular Surgery, Hôpital Lariboisière, 75475 Paris cedex, France


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. The safe development of minimally invasive coronary artery bypass operations might require alternatives to conventional suture-based anastomotic techniques. In this setting, nonpenetrating stapling is an attractive option because of its simplicity of use and potential for improved endothelial preservation.

Methods and Results. In the experimental part of this study, porcine internal mammary arteries were anastomosed to left anterior descending coronary arteries using either an 8-0 polypropylene running suture or nonpenetrating microclips (7 anastomoses in each group). The endothelium-dependent relaxations to bradykinin of the arterial rings bearing the anastomosis and of noninstrumented rings were compared in organ chamber experiments. There were no significant differences in maximal relaxations (mean ± SEM) between the microclipped and sutured anastomoses (81% ± 7% versus 74% ± 10%), which were both significantly lower than those of control coronary rings (98% ± 2%, p = 0.001 versus the two anastomosed groups). Histologic examination showed a comparable preservation of the coronary and graft endothelium with both techniques. The clinical part of the study comprised 7 patients in whom the left internal mammary artery was conventionally sutured to the left anterior descending whereas 13 saphenous vein grafts were anastomosed to their target vessels by nonpenetrating staples. There were no clip-related complications. An angiographic assessment of the venous grafts was performed within 10 days postoperatively in all patients. One graft is presumably occluded. The 12 remaining conduits were patent with stapled anastomoses featuring a widely open "shark-mouth" configuration.

Conclusions. These preliminary data suggest that nonpenetrating stapling is an easy-to-use technique that competes well with conventional suturing, at least in terms of immediate results. Further studies are warranted to better define its potential place within the armamentarium of minimally invasive coronary artery bypass techniques.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
There is unequivocal agreement that the technical quality of coronary anastomoses should not be compromised by the performance of revascularization procedures without cardiopulmonary bypass (CPB) support. This concern has motivated a rapidly expanding, largely industry-driven development of various instruments designed to facilitate coronary bypass grafting on a beating heart and consists primarily of stabilizers, hemostatic systems and anastomotic devices. In this setting, nonpenetrating stapling is an attractive option because the avoidance of transmural stitches could enhance intimal preservation [1] and, through this mechanism, favorably affect graft patency. The present study was therefore designed (1) to experimentally assess the endothelial response to nonpenetrating stapling in comparison with conventional suturing, and (2) to determine the short-term angiographic appearance of stapled anastomoses in patients undergoing coronary artery bypass operations.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Experimental study
Surgical technique
All experiments were performed using Large White swine of either sex aged 8 ± 1 weeks, weighing 23 ± 2 kg, in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication no. 85-23, revised 1985). After anesthesia with a mixture of tiletamine and zolazepam (15 mg/kg) injected intramuscularly, the hearts were removed rapidly through a left thoracotomy, placed in modified Krebs-bicarbonate solution (composition in mmol/L: NaCl 118.3, KCl 4.7, MgSO4 1.2, KH2PO4 1.2, glucose 11.1, CaCl2 2.5, NaHCO3 25 and calcium ethylenediaminotetraacetic acid 0.026: control solution). Oxygenation was insured using a carbogen mixture (95% O2 and 5% CO2). After removal of the heart, the left internal mammary artery (LIMA) was surgically dissected without electrocautery. The coronary arteries were dissected from the myocardium and placed with the left internal mammary artery in a silicone dish irrigated with the carbogen-oxygenated modified Krebs-bicarbonate solution. Proximal epicardial segments of the left anterior descending, circumflex and right coronary arteries were used randomly.

Experimental groups
Nonpenetrating stapling group. An end-to-side anastomosis of the left internal mammary artery to a coronary segment was performed on the silicone dish with the clipping device (VCS, Autosuture, United States Surgical Corporation, Norwalk, CT). After placement of two 8-0 polypropylene stitches on the heel and toe to approximate the two vessels, 12 to 14 clips were fired to complete the anastomosis. The coronary ring bearing the anastomosis and a coronary ring taken 2 centimeters from it (control) were then processed for assessment of endothelial function in standard organ chambers.

Suture group (n = 7)
An end-to-side anastomosis of the left internal mammary artery to a coronary segment was performed on the silicone dish in a standard fashion with a 8-0 polypropylene running suture. Like in the stapling group, two coronary rings (one bearing the anastomosis and a control) were isolated for the endothelial study.

Endothelial function study
The endothelial function of rings was studied in organ chambers filled with control solution (20 mL). Responses to potassium chloride and bradykinin were compared. All studies were performed in the presence of indomethacin (10-5 mmol/L; to exclude production of endogenous prostanoids) and propranolol (10-7 mmol/L; to prevent the activation of ß-adrenergic recpetors). Each preparation was stretched to the point of its active length-curve (usually 4 g), as determined by measuring the contraction to potassium chloride (30 mmol/L) at different levels of stretch, and then stabilized for 90 min. The maximal contraction was determined with potassium chloride (60 mmol/L). After washing and stabilization for 30 min, prostaglandin F2{alpha} (range, 2 x 10-6 to 10-5 mmol/L) was added to achieve a target contraction of 50% to 70% of the maximal contraction to KCl (60 mmol/L).

Histology
After assessment of endothelial function had been completed, the rings were fixed under optimal tension with formaldehyde, 10%, for 20 min. Rings were embedded in paraffin and 5-µm segments were stained for hematoxylin-eosin safran. Each section was studied under light microscopy for the presence, extent and distribution of internal elastic lamina disruption and endothelial cell coverage. All readings were made in a blinded fashion.

Drugs
All solutions were prepared daily. Bradykinin, prostaglandin F2{alpha}, indomethacin and propranolol were purchased from Sigma Chemical Co (St. Louis, MO).

Statistical analysis
Student’s t test for paired/unpaired observations were used for statistical analysis. Dose-response curves were compared with analysis of variance with the Newman-Keuls test being used as the posthoc test. A p value of less than 0.05 was considered significant. Relaxations were expressed as a percentage of maximal contraction for each group. All data are given as mean ± standard error of the mean (mean ± SEM).

Clinical study
Seven male patients, ranging in age from 49 to 75 years, underwent triple (n = 6) or quadruple (n = 1) coronary artery bypass using normothermic cardiopulmonary bypass and continuous normothermic retrograde blood cardioplegia. In all patients the left anterior descending coronary artery was grafted with the left internal mammary artery with a standard polypropylene 8-0 running suture (as was the right internal mammary artery to the right coronary artery in the patient who had four bypass grafts). Thirteen saphenous vein grafts were distally anastomosed to obtuse marginal (n = 6), right coronary (n = 3), diagonal (n = 3), and posterior descending (n = 1) coronary arteries using 12 to 14 nonpenetrating medium-sized clips after placement of four U-shaped 8-0 stitches placed at the heel, toe, and middle of each side of the coronary arteriotomy. These everting sutures allow a proper alignment of the edges of the vein graft and its recipient coronary artery which are then approximated by a series of contiguously fired staples. In 1 patient the vein graft was conventionally sutured because the poor quality of the recipient artery precluded satisfactory eversion of the vessel walls. All patients underwent a postoperative coronary angiogram within 10 days after the operation.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Experimental study
Endothelial function
There were no differences in the amplitude of contraction to potassium chloride and prostaglandin F2{alpha} between anastomosed and control rings (Table 1). Likewise, there was no significant difference in maximal relaxations to bradykinin between the stapling and polypropylene suture groups (81% ± 7% and 74% ± 10%, respectively, p = 0.155), but overall, the maximal relaxation of all anastomosed rings was significantly lower than that of controls (98% ± 2%; p < 0.001 versus the stapled and sutured groups).


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Table 1. Contractions to Potassium Chloride (60 mmol/L) and Prostaglandin F2{alpha} of Control Rings and Rings Bearing Stapled or Sutured Anastomoses

 
Histology
In the two groups, the hematoxylin-eosin staining showed a good preservation of the endothelium. Limited disruption of endothelial cells was only evident in the polypropylene suture group at the needle insertion site whereas no anastomotic material was visible in the lumen of the stapled anastomoses, thereby confirming the absence of vessel wall penetration by the microclips.

Clinical study
The time required for stapling an anastomosis was initially in the range of 12–15 minutes and became subsequently shorter with increasing experience. There were no clip-related complications. The postoperative course of all patients was uneventful except for one re-exploration for bleeding which was unrelated to the use of the stapling technique. Postoperative angiographic evaluation showed all the conventional left internal mammary artery to left anterior descending coronary artery anastomoses to be patent. One vein graft could not be visualized and is presumably occluded. The 12 remaining saphenous conduits were widely patent (92.3%) with their distal stapled anastomoses featuring a wide "shark-mouth" configuration (Fig 1).



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Fig 1. Postoperative angiography of a stapled right coronary artery anastomosis.

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
The development of minimally invasive coronary artery bypass operations may require new, nonsuture-based anastomotic techniques among which nonpenetrating stapling is of special interest in view of the successful results that it has already yielded in plastic surgery [1] and construction of arteriovenous fistulae [2]. The principle of this technique is to approximate the everted walls of the two vessels to be anastomosed, thereby avoiding transmural stitches and the subsequent risk of intimal hyperplasia. This concept is particularly appealing in coronary artery surgery in which hyperplasia has been implicated in the pathogenesis of graft occlusion [3]. It can be reasonably argued that a limitation of the technique is that endothelial integrity is still disrupted at the location of the transmural everting stitches. However, because of their limited number, these sutures are expected to be less damaging than a series of contiguous transendothelial bites.

The experimental results of the present study show that the endothelial responsiveness of coronary segments bearing stapled anastomoses was not different from that of segments bearing anastomoses that had been conventionally fashioned with suturing. With the caveat that this result was obtained in isolated vessel segments of normal porcine arteries, it supports the safety of the technique with regard to endothelial preservation, which is consistent with our histological findings and those previously reported in a rabbit model of carotid artery anastomosis achieved with nonpenetrating stapling [1]. Maintenance of an uninjured endothelial coverage is important because regenerated endothelium presents selective dysfunction that may predispose to spasm and atherosclerosis [46], thereby affecting both medium-term and long-term graft patency. Along with preservation of endothelial integrity, avoidance of exposure of subintimal connective tissue is important for reducing the risk of thrombosis at the anastomotic site. Interestingly, in the previously mentioned rabbit model where carotid arteries were anastomosed end-to-end with nonpenetrating staples [1], neither fibrin deposition nor wall thrombi were detected in the early postoperative period. Likewise, platelet aggregation seemed to be dramatically reduced by the absence of intraluminal foreign body [1].

Clinically, the feasibility of nonpenetrating stapling in coronary artery bypass surgery has been previously established [7], but only 3 out of the 10 patients of this series underwent postoperative angiography. Conversely, the present study was designed to systematically assess the short-term angiographic appearance of all grafts. From this standpoint, the results are encouraging. Twelve out of the 13 venous conduits were patent. The remaining graft had been branched to a distal right coronary artery with a poor run-off, which could have contributed to occlusion. All stapled anastomoses featured a widely open "shark-mouth" configuration provided by the symmetric eversion of the vessel edges. The resulting absence of lumen distortion should reduce transanastomotic turbulent flow and consequently contribute to further limit the risk of thrombosis at this site. Technically, the stapler is easy to deal with provided figure-of-eight sutures are first placed to allow proper alignment of the walls of the bypass conduit and its target vessel. Such an alignment cannot be achieved when the arterial wall is calcified, which represents a contraindication to the technique. With increasing experience, it is shorter by a few minutes to staple the anastomosis than to suture it conventionally. We believe, however, that it is a minor advantage compared with the expectedly improved preservation of endothelial integrity. Additional studies with systematic angiographic follow-up are now required to assess whether this expectation will be met in the long term. This assessment is not only important for appropriate patient care but also for evaluation of the cost/benefit ratio. Currently, it is approximately twice more expensive to use the stapler than conventional sutures for completing two distal venous anastomoses. In this era of cost containment, it is therefore critical to determine whether such extra charges are justified by superior long-term results with regard to limitation of neointimal hyperplasia and improvement in graft patency.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Dr Perrault is supported by the Clinician-Scientist program from the Medical Research Council of Canada.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Boeckx W.D., Darius O., van den Hof B., van Holder C. Scanning electron microscopic analysis of the stapled microvascular anastomosis in the rabbit. Ann Thorac Surg 1997;63:S128-S134.
  2. Schild A.F. Use of a vascular staple device for creation of AV fistulas and bridge grafts for hemodialysis. In: Henry M.L., Ferguson R.M., eds. Vascular access for hemodialysis-V. Chicago: Precept Press, 1997:95-102.
  3. Bryan A.J., Angelini G.D. The biology of saphenous vein graft occlusion: etiology and strategies for prevention. Curr Opin Cardiol 1994;9:641-649.[Medline]
  4. Shimokawa H., Aarhus L., Vanhoutte P.M. Porcine coronary arteries with regenerated endothelium have a reduced endothelium-dependent responsiveness to aggregating platelets and serotonin. Circ Res 1987;61:256-270.[Abstract/Free Full Text]
  5. Lin P.J., Pearson P.J., Cartier R., Schaff H.V. Superoxide anion mediates the endothelium-dependent contractions to serotonin by regenerated endothelium. J Thorac Cardiovasc Surg 1991;102:378-385.[Abstract]
  6. Cartier R., Pearson P.J., Lin P.J., Schaff H.V. Time course and extent of recovery of endothelium-dependent contractions and relaxations after direct arterial injury. J Thorac Cardiovasc Surg 1991;102:371-377.[Abstract]
  7. Nataf P., Kirsch W., Hill A.C., et al. Nonpenetrating clips for coronary anastomosis. Ann Thorac Surg 1997;63:S135-S137.



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Alain Bel
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