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J Thorac Cardiovasc Surg 2004;127:498-503
© 2004 The American Association for Thoracic Surgery

Evolving technology

Stapled coronary anastomosis with minimal intraluminal artifact: The S2 Anastomotic System in the off-pump porcine model

Willem J. L. Suyker, MDa,c,*, Marc P. Buijsrogge, MD, PhDb, Paul T. W. Suyker, MSc, MBAc, Cees W. J. Verlaanb, Cornelius Borst, MD, PhDb, Paul F. Gründeman, MD, PhDb

a Isala Clinics, Zwolle, The Netherlands
b Heart Lung Center Utrecht, University Medical Center Utrecht, Utrecht, The Netherlands
c iiTech BV, Amsterdam, The Netherlands

Received for publication December 19, 2002; revisions received April 2, 2003; accepted for publication April 14, 2003.

* Address for reprints: Willem J. L. Suyker, MD, Cardiothoracic Surgeon, Isala Clinics (Weezenlanden, Groot Wezenland 20), PO Box 10500, 8000 GM Zwolle, The Netherlands
WSuyker{at}xs4all.nl


   Abstract
Top
 Abstract
Material and methods
 Results
 Discussion
 Conclusions
 References
 
OBJECTIVE: A reliable, easy-to-use, 1-shot anastomotic device will significantly push the barrier for less invasive coronary bypass surgery. The current study was designed to test the safety, efficacy, and early patency of a novel distal anastomotic device.

METHODS: The S2 Anastomotic System (iiTech BV, Amsterdam, The Netherlands) was used in 10 consecutive pigs (73 kg) on a mild antiplatelet regimen. In each animal, the device was used to create an internal thoracic artery to left anterior descending bypass on the beating heart. The anastomoses were evaluated intraoperatively (n = 10), at 2 days (n = 2), and at 5 weeks (n = 8) by functional flow measurements, postmortem angiography, and histomorphologic examination.

RESULTS: In all pigs, the S2Anastomic System rapidly created successful anastomoses at the first attempt (graft loading and coronary ischemia time: 1.2 ± 0.3 minutes and 3.0 ± 0.6 minutes) on target vessels of 1.6 to 2 mm inner diameter. There were no technical failures or anastomotic leaks requiring additional sutures. Both intraoperatively and at the time of death, ischemically induced peak hyperemic flow responses demonstrated widely patent bypasses, which were confirmed by postmortem angiography (FitzGibbon grade A, n = 10) and macroscopic evaluation (anastomotic orifice: 2 mm). Histomorphologic evaluation showed a normal healing response with negligible neointima covering the connector and limited streamlining repair tissue formation between the staple-like elements of the connector.

CONCLUSIONS: The S2 Anastomotic System consistently created automated, fast, and reliable internal thoracic to coronary artery anastomoses on the porcine beating heart with excellent graft patency and healing characteristics at the 5-week follow-up.


Dr Suyker


The current interest in achieving coronary artery bypass surgery through ever-shrinking incisions has prompted us to reconsider previously established techniques for creating vascular anastomoses. For example, manual suturing of the anastomosis in video-assisted port access surgery on the beating heart, even with the aid of a master-slave robotic surgery system, has proved to be prohibitively difficult.1,2 To facilitate minimal access coronary surgery, therefore, new techniques to replace the current "gold standard" of manual suturing have to be developed.

One way to achieve both facilitated and predictable tissue bonding is the use of stapling techniques.3 Although many types of devices based on a broad range of principles have been proposed, only a few are beginning to become available to the market today.4-7 The reason is that the small vessel sizes encountered in coronary surgery (1.3-3.5 mm inner diameter [ID]) have proved to pose enormous technical difficulties.

With a strong emphasis on the preservation of basic surgical principles (eg, minimizing vessel wall trauma, foreign material, and non-endothelialized surfaces exposed to the blood), a novel mechanical vessel coupling system capable of handling small vessel sizes was developed: the S2 Anastomotic System (S2AS; iiTech BV, Amsterdam, The Netherlands). This study evaluates the consistency and reliability of the system during internal thoracic to anterior descending bypass grafting on the porcine beating heart and assesses the early patency and 5-week healing response of the constructed anastomoses.


   Material and methods
Top
 Abstract
 Material and methods
Results
 Discussion
 Conclusions
 References
 
Design of the connector and delivery system
The S2AS is a micro-stapler designed to create a side-to-side anastomosis. It consists of a stainless steel 1-piece microconnector and an applicator (Figure 1). The connector consists of a thin, expandable meandering ring (thickness 0.07 mm) and 8 marginally broader, initially straight staples. The surface of the connector has not been treated. After expansion, the connector creates a rounded octagonal anastomotic orifice of slightly more than 2 mm diameter. The staples are deformed to a circular shape of 0.5 mm diameter. The connector is suitable for target coronary arteries of 1.6 to 2.1 mm ID, with a graft size of at least 2 mm ID. The applicator securely covers all staple points until firing-off the device, allowing safe intravascular manipulation, positioning, and removal without firing-off, if necessary. The key feature of the applicator is the sequence of actions that control device deployment. The first is radial expansion of the "meandering ring" followed by closure of all staples. This sequence provides an unhindered introduction of the device into the vessels and helps to reliably position the vessel walls between the anvils before stapling. Smooth introduction into the target vessel is supported by a shoe-like structure at the tip of the device. Preloading consists of passing the device through the free distal end of the graft and out through an arteriotomy (Figure 1). Subsequently, the device is introduced into the arteriotomy of the targeted coronary artery in a position perpendicular to the epicardium by first inserting the toe of the shoe in a way comparable to the introduction of an aortic punch. As a result, any contact between the back wall of the coronary artery and the staples is avoided. The applicator is activated by remote control using a hydraulic pressure unit connected to the applicator with flexible tubing to avoid transmitting any undue forces to the vessel tissue. When the pressure is released, the device returns to the unexpanded state for controlled withdrawal from the anastomosis site and the distal stump of the internal thoracic artery (ITA) graft. The anastomosis is completed with a clip closing the distal free end of the left ITA (LITA) (Figure 2).



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  		Figure 1. S2 Anastomotic system preloaded with graft.

 


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  		Figure 2. Completed anastomosis.

 
Animals
Ten female Dutch Landrace pigs (60-80 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," prepared by the Institute of Laboratory Animal Resources, National Research Council, and published by the National Academy Press (revised 1996). The protocol was approved by the animal experimentation committee of the Utrecht University. All animals received 560 mg of acetylsalicylic acid orally 1 day before the operation. This was continued at a dose of 160 mg/day until the time of death.

Anesthesia and euthanasia
Anesthesia was induced with ketamine (10 mg/kg) intramuscularly. Each animal received thiopentalnatrium (4 mg/kg), atropine (1 mg), and antibiotic prophylaxis (500 mg of amoxicillin) through an intravenous line. The animals were intubated and ventilated. Anesthesia was maintained by a continuous intravenous infusion of midazolam (0.7 mg · kg-1 · h-1). Analgesia was obtained with an infusion of sufentanilcitrate (2 µg · kg-1 · h-1) and muscle relaxation with pancuronium (0.1 mg · kg-1 · h-1). During the operation, each animal received a continuous infusion of saline solution (300 mL/h). Propanolol was administered intravenously (range 10-25 mg) to reduce the mechanical irritability of the heart. Postoperatively, amoxicillin trihydrate (15 mg/kg) was administered, and analgesia was obtained with buprenorphine (0.6 mg) intramuscularly for 3 days. Animals were put to death with pentobarbitalnatrium (200 mg/kg) intravenously after having been heparinized to obtain an activated clotting time (ACT) (Hemotec, Inc, Englewood, Colo) of at least 4 times the control value.

Surgery
After a partial median sternotomy, the LITA was harvested in a skeletonized fashion. After intravenous heparinization to obtain an ACT (determined at 10 and 60 minutes after injection and every 30 minutes afterward until the end of procedure) of twice the control value, the distal LITA was transected. Next, the LITA was sprayed with a papaverine-saline solution (5 mg/mL) to prevent spasm, after which the nonpressurized vessel's half circumference was measured with a caliper. Then, the distal segment of the left anterior descending artery (LAD) (2.0-2.5 mm outer diameter) was immobilized by the Octopus 3 Tissue Stabilizer (Medtronic, Inc, Minneapolis, Minn) and measured with a caliper in a perfused state.8 At the end of the anastomotic procedure, protamine hydrochloride (5000 IU/5 mL) was given intravenously.

Anastomotic procedure
The distal end of the LITA (cut at an angle of 90 degrees) and LAD were cleared of loose periadventitial tissue. No myocardial preischemic conditioning was used before construction of the anastomoses. Coronary artery occlusion was achieved with a single, upstream polypropylene 4-0 tourniquet (Ethicon, Inc, Somerville, NJ).

A small arteriotomy of approximately 1 mm was made in the LITA using a 15° microsurgical knife (Sharpoint; Surgical Specialties Corporation, Reading, Pa), followed by insertion of a conical tool to produce a standardized opening of approximately 2 mm in diameter. Next, the LITA was mounted onto the distal end of the S2AS applicator between the anvils of the staple-like connector. After coronary occlusion, the LAD arteriotomy was performed in a stepwise fashion. First, a small 1-mm incision was made with the 15° microsurgical knife, which was extended to approximately 2 mm using standard microscissors. A conical tool was used in an upstream direction to check the size of the arteriotomy and slightly dilate it, if necessary, to ensure subsequent smooth insertion of the device. Next, the mounted S2AS was inserted into the LAD, and after scrutinizing for proper positioning, the applicator was activated, resulting in expansion followed by closure of the staples of the vessel connector. Subsequently, the applicator was withdrawn from the distal end of the LITA. After clip placement (medium Atraumaclip; Pilling, Inc, Fort Washington, Pa) on the distal graft to convert the side-to-side anastomosis into an end-to-side configuration, perfusion through the graft was initiated, and the LAD was ligated proximal to the anastomosis.

The animals were evaluated intraoperatively (10 animals), at 2 days (2 animals), and at 5 weeks (8 animals).

Intraoperative and postoperative measurements
Both intraoperatively and at the time of death, LITA flow and coronary peak hyperemic response (after 30-second graft occlusion; ratio of peak mean graft flow after reestablishment of perfusion divided by baseline flow) were measured and recorded with a calibrated transit time flow probe (size 3S) connected to a flow meter (model T208, Transonic Systems, Inc, Ithaca, NY) at a mean blood pressure of 70 mm Hg as previously described.8

Angiography
After the animals were killed, the anastomoses were visualized by ITA angiography (C-arm BV27; Philips, Eindhoven, The Netherlands) and graded by an independent observer according to FitzGibbon and colleagues.9

Histology
After angiography, the anastomoses were perfused for 120 minutes with 4% formalin at 80 mm Hg at a low perfusion rate. After overnight fixation, the anastomotic segments were excised and longitudinally cut open (2-day follow-up) for inspection under the dissecting microscope at 10 to 20x magnification to detect any mural or intraluminal thrombus formation. The segments were subsequently embedded in methyl methacrylate and sectioned in the transversal plane at ±350-µm intervals. The sections were stained with methylenblue-basic fuchsin. The dimension of thrombus formation (2-day follow-up) and resulting anastomotic narrowing as the percentage of total anastomotic orifice were assessed with the use of the software package AnalySiS (Soft-Imaging Software GmbH, Münster, Germany). Vessel wall apposition (eg, adventitia-to-adventitia and media-to-adventitia) and the process of hyaline degeneration, fibrosis, and media necrosis (ie, complete absence or pyknosis of smooth muscle cell nuclei) were recorded. Vessel wall inflammation (presence of acute [polymorphonuclear cells and macrophages] and chronic [foreign body giant cells] inflammatory reaction10) and intimal hyperplasia (as height [millimeters] enclosed by luminal border and internal elastic laminae) were assessed with AnalySiS.

Statistical analysis
Data are presented as mean ± SD, median and range, or 15th through 85th percentiles.


   Results
Top
 Abstract
 Material and methods
 Results
Discussion
 Conclusions
 References
 
Surgery
All anastomoses were performed by 1 investigator (M. P. B.). The operative data are given in Table 1. Mounting of the LITA onto the S2AS lasted 1.2 ± 0.3 minutes, including making the arteriotomy but excluding complete skeletonization of the vessel wall. Construction of the anastomosis took 2.7 ± 0.5 minutes, including making the arteriotomy and clipping the distal end of the ITA graft but excluding epicardial incision.


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  		TABLE 1. Operative data

 
Immediate full hemostasis was obtained in 8 of 10 anastomoses. Two anastomoses showed some oozing, which stopped spontaneously within a few minutes before administration of protamine.

The ACT was 90 ± 12 seconds before heparin administration and 235 ± 36 seconds during the anastomotic procedure.

Follow-up
The scheduled follow-up was completed for all 10 animals. Their weights had increased from 73 ± 7 kg to 78 ± 6 kg. Before the time of death, no myocardial infarctions or wall motion disturbances were noted. All anastomoses were patent at 2 days and 5 weeks. Macroscopically, the anastomoses showed a smooth round to slightly oval orifice of approximately 2 mm ID (Figure 3).



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  		Figure 3. Gross view from the bottom of the LAD (cut open longitudinally) into the S2AS anastomosis (diameter 2.0 mm) after excision at 5 weeks.

 
Intraoperative and postoperative measurements
ITA flow measurements are given in Table 2. The median flow at unstressed resting condition over the bypasses was 15 mL/min or less and consequently classified as "low-flow bypass condition" (Table 2).8 Flow capacity was demonstrated by the mean hyperemic flow response at the time of death (5.3 and 5.6 times baseline flow at 2 days and 5 weeks [133 mL/min and 73 mL/min, respectively]), which was comparable to the intraoperative response (mean 5.9 times baseline flow [77 mL/min]), indicating hemodynamically fully patent anastomoses over time.


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  		TABLE 2. Intraoperative and postoperative measurements

 
Angiography
At the time of death, all postmortem angiograms revealed FitzGibbon grade A anastomoses with rapid distal run-off (Figure 4). No anastomotic aneurysm formations were observed.



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  		Figure 4. Representative angiogram at 5 weeks postoperatively, demonstrating patent LITA-to-LAD anastomosis (arrow).

 
Histology
Vessel wall apposition
In all anastomoses, the adventitia of the graft was apposed to the adventitia of the LAD along its full circumference (Figure 5). Thus, the medial layers of both the coronary and thoracic artery were initially exposed to blood. In 4 anastomoses, a small part of the adventitia of the LAD at the lateral walls of the connector anastomoses had been intraluminally exposed. In all anastomoses, major parts of the connector (ie, staples and interconnecting elements) were exposed. Fibroblastic tissue was observed between vessel walls and surrounding the connector frame. No dehiscence or aneurysm formation was observed.



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  		Figure 5. Representative histologic transverse cross-section of a LITA-to-LAD anastomosis at 5 weeks postoperatively. Note the internal connector covered by small layer of neointimal tissue (methylenblue-basic fuchsin stain). ITA, Internal thoracic artery; LAD, left anterior descending artery.

 
Mural thrombus
After 2 days, the anastomotic orifices inspected under the dissecting microscope did not show intraluminal thrombus formation. The clipped distal end of the thoracic artery, forming a cul-de-sac, was filled with thrombus. A continuous thin layer of thrombus less than 30 µm thick was found on the intraluminally exposed media of both graft and coronary artery. On the intraluminally exposed connector frame, small platelet depositions were found. At 5 weeks, no fresh or organized thrombus was detected.

Intimal hyperplasia
At 5 weeks, both the intraluminally exposed medias and the connector were covered by thin neointimal repair tissue formation. Thickness of this layer ranged from 30 to 100 µm on the metal parts to 300 µm in places where anastomotic recesses, resulting from the anastomotic configuration, had been covered. No excessive, lumen-narrowing intimal hyperplasia was found in any of the anastomoses (0.14 mm ± 0.04 mm [mean ± SD]) (Figure 5). Toward the toe of the anastomosis (ie, the clipped distal end of the conduit), neointimal repair tissue reorganized the lumen of the thoracic artery.

Medial necrosis
Full-thickness medial necrosis was recorded near the penetrating staple elements of the ring frame. No medial necrosis or thinning of either the coronary or the thoracic artery was observed in between the staple elements.

Inflammation
At 2 days, the frame was surrounded by a focal, acute inflammatory cell reaction (polymorphonuclear cells and macrophages <100 inflammatory cells/field; magnification x1000). At 5 weeks, the connector was surrounded by an acute (<100 cells/field) and limited chronic inflammatory cell reaction (foreign body giant cells, occasionally seen in 5 anastomoses). No extensive or full-thickness media inflammation was seen in any of the anastomoses.


   Discussion
Top
 Abstract
 Material and methods
 Results
 Discussion
Conclusions
 References
 
The principal findings of this study are the following: (1) Using arterial grafts exclusively, we determined that the S2AS device performed as intended in all 10 pigs. Ease-of-use, expedience, and consistency were illustrated by the creation of 10 consecutive, surgically hemostatic anastomoses within 3.0 ± 0.6 minutes coronary occlusion time. (2) At 5 weeks, all S2AS anastomoses were both angiographically and hemodynamically fully patent (FitzGibbon grade A with rapid distal run-off, peak hyperemic flow response: 5.6 ± 0.9). This was achieved in deliberately chosen small-caliber peripheral target vessels under prothrombotic low base flow conditions (<=15 mL/min) using a low-dose Aspirin regimen. (3) The anastomoses showed a normal healing response with thin neointimal coverage (<=100 µm) of the internal connector and minimal inflammatory reaction.

Key features of the S2AS
Compared with other coronary anastomotic connectors4,5 (particularly the SJM distal connector,6 which has some features in common with the present device), the S2AS incorporates 4 specific features that are presumed to be useful. (1) By radial expansion of the applicator, reliable tissue positioning between the anvils was obtained before stapling took place. (2) The anvils allowed the exertion of force directly on the staples. (3) The foreign body area exposed to blood was limited to a 0.07-mm (<0.003 inch) meandering ring to avoid the necessity of aggressive anticoagulation or antiplatelet therapy. This small area approaches the standard suture material area. (4) With the staple ends covered completely by the anvils, perpendicular introduction of the S2AS applicator could be performed easily and without the risk of capturing the back wall of the coronary artery.6

Anastomotic geometry and wall apposition
For long-term reliability, it seems safe to adhere as much as possible to the basic principles of the "gold standard": the hand-sewn anastomosis. The overall geometry and wall apposition of the S2AS anastomosis was inspired by the diamond-shaped (90-degree), side-to-side, hand-sewn anastomosis, which is commonly used for sequential grafts. One of its main features is the necessity to limit the arteriotomy in the target vessel to avoid an awkward indentation resulting from transversely overstretching the graft at the anastomotic site (the "sea-gulling" effect). Despite the small arteriotomy, diamond-shaped anastomoses reveal excellent patency and functionality.11 Finishing the side-to-side anastomosis by closing the free end of the graft resulted in a smooth end-to-side configuration, as experienced by other investigators.5,6 An important additional advantage of the side-to-side approach is the favorable take-off angle and complete directional freedom of the graft that prevents kinking.

Advantages over conventional suturing
The predictable result of a standardized anastomosis, paired to speed and a reduced dexterity requirement, even in difficult to reach locations, offers an attractive alternative to suturing. In open chest procedures, therefore, these devices may stimulate surgeons to opt more often for off-pump techniques. These connectors may represent important enabling technology for more limited access procedures and, ultimately, totally endoscopic coronary artery bypass grafting in the future.

Limitations of the study
The current experiment was limited to a 5-week follow-up in the porcine model, which correlates with a 15- to 30-week healing response in the human coronary artery.12 Nevertheless, the currently presented initial results need to be further substantiated with longer term survival studies. In addition, the feasibility of the system in small-caliber, human, atherosclerotic coronary arteries remains to be established.


   Conclusions
Top
 Abstract
 Material and methods
 Results
 Discussion
 Conclusions
References
 
In the healthy pig, the S2AS consistently created automated, fast (<3 minutes), and surgically hemostatic LITA-to-LAD anastomoses of 2 mm orifice diameter in target vessels of 1.6 to 2 mm ID on the beating heart with excellent graft patency and healing characteristics with a mild antiplatelet regimen. This device may help to expand the scope of full-access off-pump coronary artery bypass grafting and encourage limited access procedures, ultimately enabling totally endoscopic multivessel myocardial revascularization.


   Acknowledgments
 
We acknowledge the constructive contributions of M. Schurink, G. Pasterkamp, MD, PhD, and colleagues from the Utrecht University Central Animal Facilities.


   References
Top
 Abstract
 Material and methods
 Results
 Discussion
 Conclusions
 References
 

  1. Mack MJ, Acuff TE, Casimir-Ahn H, Lönn UJ, Jansen EWL. Video-assisted coronary bypass grafting on the beating heart. Ann Thorac Surg. 1997;63:S100–103
  2. Falk V, Diegeler A, Walther T, Banush J, Brucerius J, Raumans J, et al. Total endoscopic computer enhanced coronary artery bypass grafting. Eur J Cardiothorac Surg. 2000;17:38–45[Abstract/Free Full Text]
  3. Werker PMN, Kon M. Review of facilitated approaches to vascular anastomosis surgery. Ann Thorac Surg. 1997;63:S122–127
  4. Solem JO, Boumzebra D, Al-Buraiki J, Nakeeb S, Rafeh W, Al-Halees Z. Evaluation of a new device for quick sutureless coronary artery anastomosis in surviving sheep. Eur J Cardiothorac Surg. 2000;17:312–318[Abstract/Free Full Text]
  5. Adams D, Filsoufi F, Farivar RS, Anderson C, Chen R, Aklog L. Sutureless distal coronary bypass using a novel magnetic coupler. Heart Surg Forum. 2001;4:S73
  6. Eckstein FS, Bonilla LF, Engelberger L, Eberli F, Windecker S, Berg TA, et al. First clinical results with a new mechanical connector for distal coronary anastomoses in CABG. Circulation. 2002;106(Suppl I):1–4[Free Full Text]
  7. Martens S, Dietrich M, Doss M, Moritz A, Wimmer-Greinecker G. The Heartflo device for distal coronary anastomoses: clinical experiences in 60 patients. Ann Thorac Surg. 2002;74:1139–1143[Abstract/Free Full Text]
  8. Buijsrogge MP, Gründeman PF, Verlaan CWJ, Borst C. Unconventional vessel wall apposition in off-pump porcine coronary bypass grafting: low versus high graft flow. J Thorac Cardiovasc Surg. 2002;123:341–347[Abstract/Free Full Text]
  9. FitzGibbon GM, Kafka HP, Leach AJ. Coronary bypass graft fate and patient outcome: angiographic follow-up of 5,065 grafts related to survival and reoperation in 1,388 patients during 25 years. J Am Coll Cardiol. 1996;28:616–626[Abstract]
  10. Hill AC, Maroney TP, Virmani R. Facilitated coronary anastomosis using a nitinol U-clip device: bovine model. J Thorac Cardiovasc Surg. 2001;121:859–870[Abstract/Free Full Text]
  11. van Sterkenburg SM, Ernst SM, Brutel de la Riviere A, Defauw JA, Hamerlynck RP, Knaepen PJ, et al. Triple sequential grafts using the internal mammary artery. An angiographic and short-term follow-up study. J Thorac Cardiovasc Surg. 1992;104:60–65[Abstract]
  12. Fishell TA, Virmani R. Intracoronary brachytherapy in the porcine model. A different animal. Circulation. 2001;104:2388–2390[Free Full Text]



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