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Ann Thorac Surg 1998;65:1093-1099
© 1998 The Society of Thoracic Surgeons

Temporary Luminal Arteriotomy Seal for Bypass Grafting

Robin H. Heijmen, MDa, Cornelius Borst, MD, PhDa, Rob van Dalen, MSca, Paul F. Gründeman, MD, PhDa, Cees W.J. Verlaana

a Heart Lung Institute, Department of Cardiology, Utrecht University Hospital, Utrecht, the Netherlands

Accepted for publication December 2, 1997.

Address reprint requests to Dr Borst, Department of Cardiology, Heart Lung Institute, Utrecht University Hospital, Rm G02.523, PO Box 85500, 3508 GA Utrecht, the Netherlands
e-mail: (exp.cardio{at}hli.azu.nl)

Presented at the Seventieth Scientific Sessions of the American Heart Association, Orlando, FL, Nov 9–12, 1997.


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. To enable off-pump coronary operations in a bloodless surgical field without ischemic complications, we developed and assessed a temporary luminal arteriotomy seal in a porcine carotid artery bypass graft model.

Methods. In 16 consecutive pigs (25 kg, 32 anastomoses) the arteriotomy was sealed luminally by a polyurethane elliptic convex seal. Endothelial denudation, medial necrosis, and intimal hyperplasia were measured quantitatively and compared with those seen in conventionally sutured anastomoses.

Results. The median occlusive time upon insertion or retrieval was 90 and 82 seconds, including the arteriotomy and securing the anastomosis, respectively. Once properly positioned, the seal provided a bloodless arteriotomy in all anastomoses. Microsurgical suturing was performed without leakage of the seal and with unimpeded flow. In the recipient artery, endothelial denudation was limited to one third of its circumference. No medial necrosis was found. Intimal hyperplasia at heel and toe was not significantly different from that seen in conventionally sutured anastomoses.

Conclusions. During end-to-side bypass grafting, the temporary luminal arteriotomy seal provided a bloodless surgical field without interfering with recipient artery blood flow and with minimal damage to the arterial wall.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Coronary artery bypass grafting without cardiopulmonary bypass requires temporary interruption of coronary blood flow to obtain a bloodless surgical field for precise (micro)surgical suturing. Interruption of existing residual or collateral coronary flow, however, may result in regional myocardial ischemia [1]; rate, rhythm, or conduction disturbances [2]; deterioration of pump function; and acute myocardial infarction. Furthermore, perforating septal branches located in the vicinity of the arteriotomy may produce retrograde blood flow and obscure the vessel edges.

To enable anastomotic suturing in a bloodless surgical field in combination with persistent distal perfusion, without blocking the entrance to side branches [2], we developed a temporary luminal arteriotomy seal (TLAS). The aim of this study was to assess the TLAS in a porcine carotid artery bypass graft model and to investigate quantitatively recipient artery wall injury and healing in comparison with those obtained by conventional suturing.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Animals
Sixteen consecutive Dutch landrace pigs, weighing about 25 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 and published by the National Institutes of Health (NIH publication 86-23, revised 1985). All procedures performed in this study were approved by the Animal Experimentation Committee of Utrecht University. Eleven pigs from a different series of experiments served as controls [3].

Surgical technique and study protocol
The animals were anesthetized and monitored hemodynamically as described before [4]. In each animal, the right carotid artery was excised and used as graft to bypass a ligature of the left carotid artery (internal diameter, 3.5 mm). All 32 TLAS anastomoses and the 22 conventionally sutured anastomoses were performed by one investigator (R.H.H.). The pig was heparinized intravenously with a single bolus of 150 IU/kg to obtain an activated clotting time (Hemotec, Inc, Englewood, CO) of twice the control value. After the operation, no anticoagulants were administered.

Phasic and mean blood flow rate of the left carotid artery were measured with a transit time flow probe (4S; Transonic, Ithaca, NY) connected to a flowmeter (T208) and recorded on an eight-channel recorder, together with the electrocardiogram and intraarterial blood pressure. Mean carotid blood flow was corrected for a linear decrease during the procedure, by averaging preinsertion and postretrieval flow rate (without TLAS) of both the proximal and distal anastomoses. A comparison was made with the carotid blood flow rate during suturing (with TLAS).

The animals were evaluated at 2 days (n = 8) or 4 weeks (n = 8) postoperatively.

Temporary luminal arteriotomy seal
The TLAS was made from a polyurethane balloon skin material, which was obtained from a commercially available coronary sinus cannula for retrograde delivery of cardioplegic solution (thickness, 200 µm; Retroplegia, RC-014; Research Medical, Inc, Midvale, UT) (Fig 1A). The seal’s oval shape (length, 12 mm; width, 7 mm) conformed to the elliptic arteriotomy that resulted from a linear incision in the pressurized carotid artery. The TLAS was straight in the length direction and slightly curved (radius of curvature, 9 mm) in the width direction. A polypropylene 9-0 suture loop (Ethicon, Somerville, NJ) at the toe side of the TLAS was used as umbilical cord to manipulate the seal during insertion and retrieval (Fig 1B–G).



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  		Fig 1. Schematic representation of the temporary luminal arteriotomy seal and its application. The temporary luminal arteriotomy seal was made from a polyurethane balloon skin material (A). The seal was prefolded in a small cannula segment (B) and inserted into the artery (C), where it unfolded owing to the flexibility of the material (D). The suture loop at the toe side was used to position the temporary luminal arteriotomy seal correctly inside the artery (E), after which blood flow was restored. During suturing, the flimsy seal gave way when a needle was inserted between the seal and the arterial wall, without producing a leak (F). After the suturing was finished, the temporary luminal arteriotomy seal was taken hold of, slid toward the heel (see D), and withdrawn in the axial direction from the artery past the suture (G), which subsequently was tightened to complete the anastomosis.

 
Anastomotic technique
After occlusion with two single bulldog clamps proximally and distally across the left carotid artery, the TLAS, which was prefolded in a small cannula segment (inner diameter, 3.0 mm), was inserted through a standardized arteriotomy of 5 mm in length. Once in the lumen, it unfolded. The suture loop was used to position the TLAS correctly inside the artery, after which blood flow was restored. The anastomosis was performed with a continuous 8-0 polypropylene suture, beginning and finishing with a mattress stitch at heel and toe, respectively. At the toe, the suture was loosely applied, creating a funnel-shaped exit in the axial direction. After carotid reocclusion, the TLAS was taken hold of at its umbilical cord, slid toward the heel to free the edge of the seal, and withdrawn from the artery past the suture, which subsequently was tightened to complete the anastomosis (seeFigs 1B–G). The anastomotic procedure was performed under the operating microscope (Opmi-6; Zeiss, Oberkochen, Germany).

Histologic analysis
To preserve anastomotic geometry, all arteries were pressure-fixed at 80 mm Hg. After overnight fixation in formalin 4%, they were divided into three segments: reference, proximal anastomosis, and distal anastomosis. The proximal anastomoses were sectioned transversely to study the extent of arterial wall damage along the circumference of the recipient artery, whereas all distal anastomoses were sectioned in the longitudinal plane to study heel and toe. Standard procedures for histologic processing were followed. Sections were stained with hematoxylin and eosin, and with elastin van Gieson for morphometric analysis of intimal hyperplasia.

Endothelial injury
At 400x magnification, the absence of endothelial cell nuclei (endothelial denudation) along the circumference of the recipient artery was determined in hematoxylin and eosin-stained cross-sections at 2-mm intervals throughout the proximal anastomotic segment (Fig 2). Endothelial denudation was expressed as percentage of the circumference not covered by an endothelial cell layer.



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  		Fig 2. Percentage circumference of recipient artery not covered by endothelium. The schematic drawing shows the temporary luminal arteriotomy seal (TLAS) (light gray) inside the recipient artery. The arteriotomy (dark gray) measures 2 mm in width. Data are presented as mean ± standard deviation. (*One anastomosis sectioned in the longitudinal plane and excluded from analysis; {dagger}estimated circumferential coverage [%] by the TLAS. {ddagger}Constriction of the artery because of the ligature close to the proximal anastomosis and excluded from analysis.)

 
Medial necrosis
Medial necrosis was defined as the absence of smooth muscle cell nuclei caused by karyolysis during the past 48 hours. Hematoxylin and eosin-stained sections were digitized and analyzed using the software package AnalySIS (Soft-Imaging Software GmbH, Münster, Germany). Medial necrosis was expressed as the percentage of smooth muscle cell nuclei in an area of interest, relative to the average number of smooth muscle cell nuclei in a corresponding reference (ie, the most proximal part of the left carotid artery).

Areas of interest, 300 x 250 µm, in cross-sections of the proximal and distal anastomoses were located at 2, 6, and 10 o’clock, and at the top and floor of the recipient artery, respectively, at 2-mm intervals throughout the anastomotic segments (Fig. 3).



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  		Fig 3. Percentage of medial smooth muscle cell nuclei, relative to a proximal reference. Data are presented as mean ± standard deviation. (CONV = conventional anastomoses; TLAS = temporary luminal arteriotomy seal anastomoses. (*one anastomosis sectioned in the longitudinal plane and excluded from analysis; {dagger}constriction of the artery due to the ligature close to the proximal anastomosis and excluded from analysis.)

 
Intimal hyperplasia
The area enclosed by the endothelium and internal elastic lamina adjacent to the suture line in the donor and recipient artery was defined as intimal hyperplasia. Three adjacent midline longitudinal sections of each distal anastomosis were analyzed morphometrically. Mean values of intimal hyperplasia (mm2) at toe or heel were calculated for each distal anastomosis.

Previously performed conventionally sutured distal anastomoses from a different series of comparable experiments [3] were analyzed identically and served as controls for both medial necrosis (n = 6) and intimal hyperplasia (n = 5).

Statistical analysis
Data are presented as mean ± standard deviation or as median and range. The unpaired Student’s t test (two tailed) was used to compare data. A p value less than 0.05 was regarded as statistically significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Surgical procedure
Insertion of the seal required about 20 seconds. The median occlusive time required to create a standardized arteriotomy and insert the seal was 90 seconds (range, 60 to 146; outlier, 313). Retrieval of the seal required about 5 seconds. Together with tightening the suture and securing the anastomosis, 82 seconds of occlusion time (range, 54 to 154; outliers, 211 and 243) was required. Both outliers were caused by breakage of the umbilical cord (9-0 suture loop) during retrieval. After insertion, instantaneous complete sealing of the arteriotomy was obtained in 21 of 32 anastomoses (66%). In 5 anastomoses (16%), the seal was successfully repositioned intravascularly, whereas in another 5 anastomoses the seal needed to be reinserted. In 1 anastomosis, suturing was started despite initial leakage of the seal. An attempt to reposition the seal during suturing resulted in inadvertent expulsion. Insertion of a second seal resulted instantaneously in a bloodless arteriotomy. Remarkably, 10 of 11 anastomoses that showed initial leakage after insertion were located distally.

During suturing, the flimsy seal gave way when a needle was inserted carefully between the seal and the arterial wall, while maintaining a dry operative field in all cases. No intraluminal thrombus formation was observed. In none of the animals was the seal inadvertently transferred downstream.

The intraluminal seal did not change phasic and mean carotid artery blood flow: 323 ± 55 mL/min with seal versus 322 ± 44 mL/min without seal (Fig 4).



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  		Fig 4. Representative recording from a pig carotid artery during insertion of the temporary luminal arteriotomy seal. The intraluminal seal did not change phasic and mean blood flow.

 
Anastomotic suturing was successfully accomplished in 22 ± 3 minutes and required 17 ± 1 bites. An additional stitch to obtain complete hemostasis was required at three anastomosis sites.

Histology
At sacrifice, 2 days or 4 weeks postoperatively, 15 of 16 left carotid arteries bypassed with the seal were patent. All 11 conventionally sutured grafts were patent [3].

Endothelial injury
At 2 days, throughout the anastomotic segment, no more than approximately one third of the circumference of the recipient artery was denuded of endothelial cells. In the midsegment of the arteriotomy, the endothelial cell layer was damaged to a smaller extent than at the toe and heel. In the longitudinally sectioned anastomoses, endothelial denudation was observed at both heel and toe, and at the floor of the anastomosis toward the heel. In none of the anastomoses was total circumferential endothelial denudation or disruption of the internal elastic lamina observed (Fig 2). At 4 weeks, all anastomoses were completely reendothelialized.

Medial necrosis
At 2 days, irrespective of the location in the anastomotic segment, the number of medial smooth muscle cell nuclei was slightly lower than in a proximal reference segment. There was no difference with the conventionally sutured anastomoses. No medial necrosis was observed(Figs 3, 5).



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  		Fig 5. Transverse cross-section of the media of the recipient artery located at the toe of the anastomosis that was covered by the temporary luminal arteriotomy seal, 2 days postoperatively. Note the absence of endothelial cells without disruption of the internal elastic lamina (arrows). Note the undisturbed medial smooth muscle cell nuclei. (Hematoxylin and eosin stain; bar = 50 µm.)

 
Intimal hyperplasia
At 4 weeks, the intimal hyperplasia area at the heel (0.26 ± 0.15 mm2) and toe (0.07 ± 0.04 mm2) was not significantly different from those of conventionally sutured anastomoses (0.25 ± 0.12 mm2 and 0.04 ± 0.02 mm2, respectively). Anastomotic intimal hyperplasia extended as a thin intimal layer of about 20 µm thickness toward the heel and toe. Except for intimal hyperplasia at the suture line, no intimal thickening was observed along the circumference of the recipient artery (Fig 6).



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  		Fig 6. Longitudinal cross-section of the heel of a temporary luminal arteriotomy seal anastomosis (A) and a conventionally sutured anastomosis (B), 4 weeks postoperatively. There was no significant difference in anastomotic intimal hyperplasia area between both groups. (IH = intimal hyperplasia.) (Elastin van Gieson stain; bar = 100 µm.)

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
The principal results of this study are as follows: (1) Insertion or retrieval of the seal required less than 30 seconds. (2) Recipient artery occlusion was limited to about 90 seconds. (3) Once properly positioned, the seal provided a bloodless arteriotomy without interfering with recipient artery blood flow and with minimal damage to the arterial wall.

Various types of catheter stents, graduated probes, or intraluminal shunts have been described to prevent blood flooding the anastomotic area after arteriotomy or to maintain recipient artery blood flow during construction of the bypass graft [1, 2, 5–8]. None of these techniques, however, has ever been widely used. This may be attributed to their inability to provide a bloodless arteriotomy without snaring the recipient artery proximally and distally, to their obstruction to residual blood flow as their size is often flow limiting, or to their cumbersome and possibly traumatic retrieval through the small residual opening in the anastomosis. Conceptually, the application of a temporary intravascular device violates the surgical "no touch" principle. The present device, however, appeared to be virtually atraumatic.

Coronary artery bypass grafting on the beating heart
Since the early 1990s, coronary artery bypass grafting on the beating heart has regained interest and is rapidly evolving as coronary motion can now be restrained adequately with mechanical stabilization devices [9, 10], enabling precise microsurgical suturing [9]. In the great majority of patients, the anastomosis is performed while native coronary flow is temporarily interrupted. Because of well-developed collateral coronary circulation in patients with high-grade proximal stenosis or occlusion, interruption of coronary flow for 10 to 20 minutes is remarkably well tolerated without an increase in cardiac troponin I level indicative of myocardial cell death [11]. In a few cases, however, flow interruption was not tolerated and hemodynamic deterioration was managed either by a conversion to a conventional procedure with cardiopulmonary bypass [10, 12] or by inserting an intraluminal shunt [13].

It is conceivable that expanding the indication for coronary bypass grafting without cardiopulmonary bypass to patients with three-vessel disease, lesser-grade proximal stenosis, and unstable angina will enlarge the group of patients at risk for coronary flow interruption, because of the cumulative effect of short ischemic periods and the absence of adequate collateral coronary flow. In addition, minimally invasive or endoscopic approaches are likely to prolong the anastomosis time and hence the ischemic period. Furthermore, collateral flow via perforating branches that happen to be located in the occluded coronary segment often produces retrograde flow that wells up in the arteriotomy, obscures its edges, and jeopardizes the quality of the anastomosis.

Temporary luminal arteriotomy seal
As one element in the development of coronary bypass grafting on the beating heart [12], we have developed a briefly occlusive end-to-side anastomosis technique by means of a temporary luminal arteriotomy seal. Because of its low profile (thickness, 200 µm) and the relative expansion of the artery at the arteriotomy, a minimal decrease in cross-sectional area of the recipient artery lumen is achieved and, hence, no obstruction to blood flow (Fig 7). The compliant seal nicely gives way to the suture needle without producing a leak. Before the continuous suture is tightened, the seal is retrieved in the axial direction. Thus, any damage that might be inflicted on the arterial wall by insertion or retrieval will be located proximal to the heel of the anastomosis (seeFigs 1D, 1G). Furthermore, as the seal only contacts half or less of the circumference, the limited endothelial damage is localized and reendothelialization is accelerated by spread of endothelial cells from the side of the artery opposite the arteriotomy, rather than from minute side branches (vasa vasorum) and the proximal and distal, nonoccluded segments (see Fig 2).



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  		Fig 7. Three-dimensional representation of the carotid artery with a temporary luminal arteriotomy seal in place. In 1 additional pig, the left carotid artery in which the arteriotomy was sealed with a temporary luminal arteriotomy seal was pressure-fixated at 80 mm Hg and sectioned transversely each 200 µm. In each cross-section, the lumen area was determined. Because of the relative expansion of the artery at the arteriotomy combined with the low profile of the seal, the lumen of the recipient artery, and hence the blood flow, is virtually unchanged.

 
Sealing by the TLAS is attributed to the intraarterial, transmural pressure and the elastic properties of the balloon skin material, as its radius of curvature is larger than the radius of the recipient artery. The flimsy seal caused no medial necrosis, and at 4 weeks no intimal hyperplasia was found throughout the anastomosis other than that also observed after conventional suturing in the historical control group. Corresponding to our recent findings in the rabbit [14], endothelial denudation without medial necrosis was followed by negligible intimal hyperplasia, in contrast to more intense injury, which results in medial necrosis. At sacrifice, 4 weeks postoperatively, one carotid artery bypassed with the seal was occluded. Histologic examination revealed an organized thrombus throughout the artery without apparent evidence of anastomotic failure. This may be attributed to occasional occlusion in this more thrombosis-prone model, as acetylsalicylic acid was administered in the historical control group only. Whether the TLAS effectively seals the arteriotomy in the case of atherosclerotic luminal wall surface irregularities or decreased transmural pressure remains to be established.

Coronary bypass grafting
The coronary artery lacks the large longitudinal tension of the carotid artery; hence, a linear incision in the pressurized coronary artery will widen to an almost round arteriotomy. To prevent breakage of an umbilical cord, it was replaced by a polyurethane dorsal "shark fin" in a subsequent series of experiments. Application of the seal during left internal mammary artery bypass grafting to the left anterior descending coronary artery (internal diameter, 2.5 mm) on the beating heart using the Octopus Tissue Stabilizer [9] (Medtronic, Minneapolis, MN) was successful in 18 consecutive pigs.

Potential indications
In addition to off-pump procedures, anastomosis suturing during coronary artery bypass grafting with cardiac arrest and continuous blood cardioplegia may be facilitated by the seal because it creates bloodless arteriotomy edges. Furthermore, the seal may be of help in other areas of vascular surgery where interruption of residual perfusion to the end organ is ill tolerated. Finally, a modified seal might be employed during proximal anastomosis suturing. This would obviate the need for the side-clamp on the ascending aorta and would further reduce the risk of adverse cerebral effects by particulate emboli [15].

Conclusion
The TLAS provided a bloodless surgical field without interfering with recipient artery blood flow and with minimal damage to the arterial wall. The TLAS may expand the indications for coronary artery bypass grafting on the beating heart and may facilitate the development of porthole, closed-chest off-pump coronary surgery.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We acknowledge the assistance or advice of Yvonne J. M. van der Helm, Hendricus J. Mansvelt Beck, Chantal M. Mouës, L. Floor van der Steen, and Hans W. G. Vosmeer and colleagues from the Utrecht University Central Animal Facilities.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Franzone A.J., Wallsh E., Stertzer S.H., DePasquale N.P., Bruno M.S. Reduced incidence of intraoperative myocardial infarction during coronary bypass surgery with use of intracoronary shunt technique. Am J Cardiol 1977;39:1017-1020.[Medline]
  2. Rivetti L.A., Gandra S.M.A. Initial experience using an intraluminal shunt during revascularization of the beating heart. Ann Thorac Surg 1997;63:1742-1747.[Abstract/Free Full Text]
  3. Heijmen R.H., Gründeman P.F., Borst C. Intima–adventitia apposition in end-to-side arterial anastomosis: an experimental study in the pig. Ann Thorac Surg 1998;65:705-711.[Abstract/Free Full Text]
  4. Van Leeuwen T.G., van Erven L., Meertens J.H., Motamedi M., Post M.J., Borst C. Origin of arterial wall dissections induced by pulsed excimer and mid-infrared laser ablation in the pig. J Am Coll Cardiol 1992;19:1610-1618.[Abstract]
  5. Trapp W.G., Bisarya R. Placement of coronary artery bypass graft without pump oxygenator. Ann Thorac Surg 1975;19:1-9.[Medline]
  6. Parsonnet V., Gilbert L., Gielchinsky I. Graduated probes for coronary bypass surgery. J Thorac Cardiovasc Surg 1974;68:424-427.[Medline]
  7. Grow J.B., Sr, Brantigan C.O. Use of a Fogarty biliary catheter to create a bloodless field for saphenous vein–coronary artery anastomosis. J Thorac Cardiovasc Surg 1975;69:105-106.[Medline]
  8. Ludington L.G., Kafrouni G., Peterson M.H., Verska J.J., Mulder A., Brewer L.A., III Technique for using soft, flexible catheter stents in aortocoronary vein bypass operations. Ann Thorac Surg 1976;21:328-332.[Abstract]
  9. Borst C., Jansen E.W.L., Tulleken C.A.F., et al. Coronary artery bypass grafting without cardiopulmonary bypass and without interruption of native coronary flow using a novel anastomosis site restraining device ("Octopus"). J Am Coll Cardiol 1996;27:1356-1364.[Abstract]
  10. Shennib H., Lee A.G.L., Akin J. Safe and effective method of stabilization for coronary artery bypass grafting on the beating heart. Ann Thorac Surg 1997;63:988-992.[Abstract/Free Full Text]
  11. Vaissier E, Benarim S, Jault F, et al. Perioperative monitoring of myocardial ischemia during minimally invasive coronary artery bypass grafting [Abstract]. Presented at the World Congress on Minimally Invasive Cardiac Surgery, Paris, France, May 30–31, 1997.
  12. Borst C., Jansen E.W.L., Gründeman P.F. Less invasive coronary artery bypass grafting: without cardiopulmonary bypass and via reduced surgical access [Editorial]. Heart 1997;77:302-303.[Free Full Text]
  13. Levinson M.M., Fooks G.S. Coronary grafting using a temporary intraluminal shunt instead of heart-lung bypass. Ann Thorac Surg 1995;60:1800-1801.[Abstract/Free Full Text]
  14. Doornekamp F.N., Borst C., Post M.J. Endothelial cell recoverage and intimal hyperplasia after endothelium removal with or without smooth muscle cell necrosis in the rabbit carotid artery. J Vasc Res 1996;33:146-155.[Medline]
  15. Roach G.W., Kanchuger M., Mangano C.M., Newman M., Nussmeier N., Wolman R. Adverse cerebral outcomes after coronary bypass surgery. N Engl J Med 1996;335:1857-1863.[Abstract/Free Full Text]



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