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Ann Thorac Surg 2002;73:1451-1456
© 2002 The Society of Thoracic Surgeons

Original article: cardiovascular

Coronary end-to-side sleeve anastomosis using adhesive in off-pump bypass grafting in the pig

Marc P. Buijsrogge, MDa, Cees W.J. Verlaana, Mattie H.P. van Rijen, BSa, Paul F. Gründeman, MD, PhD*a, Cornelius Borst, MD, PhDa

a Heart Lung Center Utrecht, University Medical Center Utrecht, Utrecht, The Netherlands

Accepted for publication January 11, 2002.

* Address reprint requests to Dr. Gründeman, Experimental Cardiology Laboratory, University Medical Center Utrecht (Room G02.523), Heart Lung Center Utrecht, P.O. Box 85500, 3508 GA Utrecht, The Netherlands
e-mail: exp.cardio{at}hli.azu.nl


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. In the exploration of facilitated coronary anastomosis strategies, we assessed a new octyl-cyanoacrylate adhesive in combination with a modified end-to-side sleeve anastomosis in off-pump bypass grafting in the pig.

Methods. Sleeve-adhesive anastomoses (n = 20) were evaluated intraoperatively, at 3 days (n = 4), and at 5 weeks (n = 16) in an off-pump, low (<=15 mL/min; n = 10) and high flow (approximately 60 mL/min; n = 10) porcine bypass model. All anastomoses were examined by flow measurement, angiography, and histology.

Results. Anastomosis construction took 8.5 minutes (6.7 to 10.2 minutes; median [15th to 85th percentile]). At 5 weeks, all anastomoses were fully patent (FitzGibbon grade A). The adhesive did not cause impaired vessel wall healing, but was surrounded by a focal acute and limited chronic (foreign body giant cells occasionally seen) inflammatory reaction at the adventitial application site.

Conclusions. Octyl-cyanoacrylate tissue adhesive combined with end-to-side internal mammary to coronary artery sleeve anastomosis construction proved to be feasible, even in low bypass graft flow conditions (<=15 mL/min; prothrombotic milieu) in the pig and deserves interest in exploration of facilitated anastomosis strategies in coronary artery bypass grafting.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
With the pursuit of beating heart bypass procedures through smaller and smaller incisions [1], a renewed interest in a simple, timesaving, and reliable coronary artery anastomosis technique emerges [2].

Several strategies facilitating bypass construction have been described: stapling or mechanical coupling [3–5], adhesive bonding [6], and laser-assisted tissue welding [7]. Anastomosis construction by adhesives has the theoretical advantage of a fast, less complex method of facilitating vessels to bond and relatively simple delivery through small incisions.

Encouraged by earlier results with the use of cyanoacrylate adhesive in arteriotomy closure [8], we assessed the applicability of the newly developed octyl-cyanoacrylate (Dermabond; Ethicon, Inc., Somerville, NJ) in a modified sleeve [9] end-to-side approach to coronary anastomosis construction. Our objective was to assess the patency and vascular wall healing of this anastomosis technique in off-pump porcine coronary bypass grafting under both reduced, ie, low-flow (prothrombotic milieu) and high-flow conditions [10, 11] in the internal mammary artery graft.


   Material and methods
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Animals
Ten Dutch female Landrace pigs (weighing 70 to 90 kg) were used. The animals were fed a normal diet and received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals." The protocol was approved by the Animal Experimentation Committee of the Utrecht University. All animals received 1 day before surgery 560 mg acetylsalicylic acid orally, which was continued in a dose of 160 mg/d until sacrifice.

Anesthesia
Anesthesia was induced by ketamine (10 mg/kg) intramuscularly, thiopental sodium (4 mg/kg), atropine (1 mg), and the antibiotic amoxicillin (500 mg) intravenously. A mixture of oxygen and air (1:1 vol/vol) with 0.5% to 1% halothane, midazolam (0.3 mg/kg per hour) intravenously, and propranolol (range, 10 to 25 mg) were administered. Analgesia was obtained by sufentanil citrate (1 µg/kg per hour) and muscle relaxation by pancuronium (0.1 mg/kg per hour).

Postoperatively, amoxicillin trihydrate (15 mg/kg) and buprenorphine (0.6 mg) as analgesic were administered intramuscularly for 3 days.

Euthanasia
Pentobarbital sodium (200 mg/kg) was given intravenously after heparinization to obtain an activated clotting time (Hemotec, Inc., Englewood, CO) of at least four times the control value.

Surgery and experimental model
Left and right internal mammary arteries (LIMA/RIMA) were harvested in a skeletonized fashion. After heparinization intravenously to obtain an activated clotting time (determined at 10 and 60 minutes and every 30 minutes afterwards after injection until the end of the procedure) of twice the control value, both distal internal mammary arteries (IMA) were dissected. First, the distal segment of the left anterior descending artery (LAD) was immobilized by the Octopus3 Tissue Stabilizer (Medtronic, Inc., Minneapolis, MN). Loose periadventitial tissue of both IMA and LAD was removed, and the half circumference of the IMA and the outer vessel diameter of the LAD were measured with a caliper.

Anastomotic procedure
Under the microscope (magnification x6.25; Wild M680; Leica AG, Heerburg, Switzerland), first the distal end of the RIMA was cut at an angle of approximately 45 degrees. Preischemic conditioning was used before coronary artery occlusion, which was performed with two microvascular Acland clamps (B-3V; S&T Marketing Ltd, Neuhausen, Switzerland).

A longitudinal arteriotomy with a length of half the IMA circumference was performed by a diamond knife. First, a modified mattress stitch using polypropylene 8-0 suture (Ethicon, Inc.) was placed at the toe and heel of the mammary and coronary artery, slightly sleeving the IMA into the LAD (approximately 0.4 mm). Next, two mattress stitches were placed at the lateral walls of the anastomosis (Figs 1A, 1B). While traction was placed manually on two adjacent sutures to stretch the intervening anastomotic segment (Fig 1C), an air blower (Clear View Blower/Mister, Medtronic, Inc.) was used that was controlled to avoid air entry but allow gentle removal of any excessive moisture over the overlapping segment. Next, approximately 0.5 µL of octyl-cyanoacrylate (temperature, -4°C; high viscosity) was applied over the anastomotic line between the sutures under traction (Fig 1C) by a pipette (Proline Pipette, Biohit OY, Helsinki, Finland) and pipette tip (200 µL; Greiner GmbH, Frickenhausen, Germany). After adhesive polymerization, RIMA graft flow was restored by first releasing the Acland clamp on the IMA followed by the distal clamp on the coronary artery (RIMA-LAD). Subsequently, a second anastomotic procedure was performed on the proximal LAD (LIMA-LAD).



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  		Fig 1. Sleeve-adhesive anastomotic procedure. (A) Four modified mattress stitches are placed at the toe, heel, and lateral walls of the anastomosis, (B) slightly sleeving the internal mammary artery (IMA) into the left anterior descending coronary artery (LAD). (C) While traction is placed on adjacent mattress stitches to stretch the intervening anastomotic segment, approximately 0.5 µL of octyl-cyanoacrylate adhesive is applied over the anastomotic line.

 
Two anastomoses were constructed in each animal. Ligating the LAD, a distal low-flow (set at <= 15 mL/min by localization of LAD ligation) RIMA-LAD anastomosis was created, and by ligation of the left main stem, the circumflex territory was included in a proximal high-flow (approximately 60 mL/min) LIMA-LAD anastomosis [12]. All anastomoses were performed by one investigator (M.P.B.).

The animals were evaluated intraoperatively (10 animals; 10 low-flow, and 10 high-flow anastomoses), at 3 days (2 animals; 2 low-flow and 2 high-flow anastomoses), and at 5 weeks (8 animals; 8 low-flow and 8 high-flow anastomoses).

Intraoperative and postoperative measurements
Either intraoperatively or at sacrifice, IMA flow and coronary peak hyperemic response were measured and recorded with a calibrated transit time flow probe (3S) connected to a flowmeter (model T208, Transonic Systems, Inc., Ithaca, NY) at a mean blood pressure of 70 mm Hg, as described before [12]. Before chest closure, the IMA flow was monitored continuously for up to 2 hours.

Angiography
After sacrifice, the anastomoses were visualized by IMA angiography at 80 mm Hg (C-arm BV27, Philips, Eindhoven, The Netherlands) and graded by an independent observer according to FitzGibbon and associates [13].

Histology
After angiography, the heart was perfused for 30 seconds with a papaverine-saline solution (5 mg/mL) and perfusion-fixed more than 30 minutes at 80 mm Hg with 4% formalin at a low perfusion rate. Subsequently, the anastomotic and reference segments (proximal LAD and IMAs) were excised, formalin fixated overnight, longitudinally cut open (3-day group), and inspected under the dissecting microscope to detect any intraluminal thrombus formation. One half of the anastomosis was sectioned in the longitudinal plane, the other half and reference segments in the transversal plane (three adjacent midline sections at ±100-µm intervals). The sections were stained with hematoxylin-eosin, van Gieson’s elastin, Weigert’s fibrin, and Oil Red O stains (Merck KGaA, Darmstadt, Germany), the latter to stain the adhesive.

Light microscopy was used to identify mural thrombus formation, intimal hyperplasia [12], medial necrosis, vessel wall inflammation, and adhesive localization.

Statistical analysis
Data are presented as mean ± standard deviation (SD) or as median and 15th to 85th percentile. Repeated measurement analysis of variance by General Linear Model was used to compare means with use of software package SPSS (SPSS, Inc., Chicago, IL) and Bonferroni correction to adjust for multiple comparisons.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Surgical results
The operative data are given in Table 1. The median anastomosis surgery time was 8.5 minutes (15th to 85th percentile, 6.7 to 10.2 minutes; from arteriotomy until completion of adhesive polymerization). Symmetric sleeving of the IMA into the LAD, including placement of the four mattress stitches, required 72% of total anastomosis time. Adhesive application (including preparation and drying of vessel wall, and application and polymerization of the adhesive) required 19% (1.6 minutes [1.2 to 2.6 minutes]).


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  		Table 1. Operative Dataa

 
Immediate complete hemostasis was obtained in 13 of 20 anastomoses. In five cases, initial oozing stopped after 1 minute. Owing to bleeding, in two cases, the IMA had to be briefly clamped again. The adhesive was peeled off from the LAD at one anastomotic quadrant and was reapplied locally, which resulted in complete hemostasis. In the last two cases, adhesive application was complicated in one because of asymmetric IMA sleeving and in the other owing to active bleeding at the application site.

The activated clotting time before heparin administration, during the anastomotic procedure, and at 240 minutes after heparinization was 100 ± 9, 224 ± 19, and 139 ± 25 seconds, respectively.

Follow-up
The scheduled follow-up was completed by all animals, and their weight had increased from 76 ± 7 kg to 80 ± 6 kg.

Intraoperative and postoperative measurements
Internal mammary artery flow measurements are given in Table 2. The flow over the low-flow and high-flow anastomoses at 5 weeks was comparable to the flow intraoperatively (p = 0.586), but different from the (increased) flow after 2 hours of anesthesia (p = 0.023; Table 2) [12].


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  		Table 2. Intraoperative and Postoperative Measurements

 
All anastomoses, either at 5 weeks or intraoperatively, were hemodynamically fully patent (Table 2). No (cyclic) flow reductions were observed during 2 hours of flow monitoring after anastomosis construction.

Angiography
At sacrifice, all anastomoses met FitzGibbon grade A criteria, without aneurysm formation (Fig 2). Two low-flow anastomoses had a 20% anastomotic diameter narrowing.



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  		Fig 2. Representative angiogram at 5 weeks postoperatively, demonstrating a fully patent low-flow sleeve-adhesive anastomosis (arrow).

 
Histology
Vessel wall apposition
In all anastomoses, except one, the invaginated part of the graft was apposed to the intima of the LAD along its full circumference (Fig 3). In one low-flow anastomosis, a small part of the adventitial layer of the graft at the toe of the anastomosis had been exposed to blood. No dehiscence occurred, but fibroblastic fusion between vessel walls was observed. In two low-flow anastomoses, invagination of the RIMA into the LAD led to an excess of vessel wall graft at the anastomotic orifice, which compromised the lumen and resulted in a 20% anastomotic diameter narrowing. The graft was invaginated into the coronary artery over 0.41 ± 0.09 mm.



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  		Fig 3. Representative longitudinal histologic section of the toe of a sleeve-adhesive anastomosis at 5 weeks postoperatively. Note slight graft into coronary artery sleeving. Streamlining repair tissue (intimal hyperplasia) fills the anastomotic recess between the invaginated graft and coronary artery. Normal vessel wall integrity near adhesive is demonstrated. (Elastin van Gieson stain; original magnification, x100; bar = 250 µm.) (A = adhesive void; ADV LAD = adventitia of left anterior descending coronary artery; IEL LAD = internal elastic lamina of left anterior descending coronary artery; IH = intimal hyperplasia; IMA = internal mammary artery; LAD = left anterior descending coronary artery.)

 
Mural thrombus
After 3 days, the anastomotic orifices inspected under the dissecting microscope did not show intraluminal thrombus formation. A continuous thin layer of thrombus less than 40 µm was found on the intraluminally exposed media and between vessel walls.

Intimal hyperplasia
At 5 weeks, in both low-flow and high-flow conditions, streamlining intimal hyperplasia coverage with endothelial cell lining was found, which completely filled the anastomotic recess between IMA and LAD, but did not compromise the anastomotic lumen (Fig 3). In the low-flow anastomoses neointima formation was 1.25 mm2 (1.01 to 1.48 mm2), 1.15 mm2 (0.68 to 1.45 mm2), and 0.48 mm2 (0.19 to 0.60 mm2) at the heel, toe, and lateral wall of the anastomoses, respectively, and 0.72 mm2 (0.62 to 1.47 mm2), 0.75 mm2 (0.66 to 0.91 mm2), and 0.48 mm2 (0.33 to 0.80 mm2) in the high-flow anastomoses, respectively.

Medial necrosis
No medial necrosis (coronary or mammary artery) was observed in between the sutures or near the adhesive.

Adhesive
At 3 days, the adhesive application site was surrounded by a focal adventitial acute inflammatory cell reaction (polymorphonuclear cells and macrophages; >100 inflammatory cells per field; magnification: x1,000). Scattered inflammatory cells were seen between the vessel walls, but no cell reactions were observed in the media or intima adjacent to the adhesive. At 5 weeks, in both flow conditions, the adhesive was surrounded by an acute (>100 cells per field) and limited chronic inflammatory cell reaction (foreign body giant cells, occasionally seen) at the adventitial application site. In two high-flow anastomoses, inflammation (no foreign body cells) was seen focally in the outer layer of the media. In another two anastomoses (one low-flow and one high-flow), scattered acute inflammatory cells were observed in the anastomotic recess bordering the distal graft and arteriotomy. No evidence was found that adhesive had been exposed to blood.


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
The principal results of this study are (1) all adhesive end-to-side sleeve anastomoses were fully patent (FitzGibbon grade A) and showed a normal healing response, and (2) the sleeve-adhesive anastomosis technique was relatively simple and required 8.5 minutes (6.7 to 10.2 minutes).

Facilitated coronary artery anastomosis
Although substantial progress is being made [5], still none of the alternative facilitated anastomosis techniques using mechanical coupling (devices) [3, 4, 14, 15], surgical adhesives [6, 16–18], or laser welding [7] has demonstrated sufficient advantages over the sutured coronary anastomosis to fully displace it as technique of choice yet.

Cyanoacrylates have been used for many years as surgical adhesives [19]. Favorable qualities are their strong bonding capacity, brief polymerization time, relatively simple application, and low costs. But so far, the use of these adhesives has been disappointing because of histotoxicity, distortion of vessel walls, and application failures [16, 17, 20, 21].

Octyl-cyanoacrylate anastomosis
The newly developed 2-octyl-cyanoacrylate adhesive, which is currently approved by the U.S. Food and Drug Administration for topical wound closure, theoretically addresses at least part of the cyanoacrylate limitations (relatively low histotoxicity and a strong, yet flexible bond). For improvement of adhesive polymerization conditions and minimizing application failures, we introduced a modified sleeve end-to-side coronary anastomosis technique. By means of IMA into LAD sleeving (approximately 0.4 mm), an overlapping vessel wall apposition without flow-limiting anastomotic narrowing was created.

After 5 weeks in the porcine model (which corresponds to 15 to 30 weeks of wall healing in the [stented] human coronary artery [22]), the use of octyl-cyanoacrylate did not cause medial necrosis or impaired anastomotic vessel wall healing [23]. At follow-up at 5 weeks, all sleeve anastomoses (even in low-flow conditions of less than 15 mL/min) were fully patent without significant stenosis (peak hyperemic flow response was 5.3 ± 1.3).

Compared with conventional anastomoses [12], more neointima formation was observed, which is attributed to the sleeve anastomosis technique itself. By means of overlapping vessel wall apposition (Fig 3), a circumferential recess between graft and coronary artery was created, which was completely filled by neointima. No excessive lumen narrowing and flow-limiting intimal hyperplasia was found in the study anastomoses.

In combination with the overlapping sleeve technique, the use of adhesive was satisfactory, relatively simple, and quick (application time, ±2 minutes). The present results support earlier findings with the use of higher homolog cyanoacrylates in the end-to-end anastomoses [23, 24] or arteriotomy closure [8]. In case of incorrect or inadvertent octyl-cyanoacrylate application, the adhesive could be peeled off (easily) from the anastomotic line and reapplied. But, a major limitation in the use of cyanoacrylate adhesive is the ineffectiveness in the presence of blood. However, our study, with its overlapping vessel margins, use of an air blower to remove excessive blood, and a minimal amount of octyl-cyanoacrylate, reports promising results.

Although the adhesive did not have a detrimental effect on the healthy porcine vessel walls (outer diameter, 3.5 mm) after 5 weeks, the long-term effect (ie, ongoing foreign body giant cell reaction) remains to be established. Additionally, it remains speculative whether the sleeve-adhesive technique is applicable to a small-caliber, atherosclerotic site for distal anastomosis in humans.

The end-to-side internal mammary to coronary artery sleeve anastomosis with octyl-cyanoacrylate adhesive proved to be feasible, even in low bypass graft flow conditions (<=15 mL/min) in the pig. The use of adhesives in the exploration of facilitated anastomosis strategies in coronary artery bypass grafting deserves renewed interest.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We acknowledge the constructive contributions of M. Schurink, Dr. A. R. T. Donders, S. van der Horst, J. W. Kouwenhoven, L. Timmers, and colleagues from the Utrecht University Central Animal Facilities.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
This research was supported by a grant from the University Medical Center Utrecht, Utrecht, The Netherlands (1995/B903).


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Reichenspurner H., Boehm D.H., Gulbins H., et al. Robotically assisted endoscopic coronary artery bypass procedures without cardiopulmonary bypass. J Thorac Cardiovasc Surg 1999;118:960-961.[Free Full Text]
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