Ann Thorac Surg 2002;73:825-829
© 2002 The Society of Thoracic Surgeons
Original article: cardiovascular
Robotically assisted versus conventional freehand technique during beating heart anastomoses of left internal thoracic artery to left anterior descending artery
Luis H. Diodato, MDa,
John E. Scarborough, MDa,
Patrick W. Domkowski, MD, PhDa,
Monica L. Smith, BSa,
Shankha S. Biswas, MDa,
Ted Schwartz, MDa,1,
Kevin P. Landolfo, MD*a
a Department of Surgery, Duke University Medical Center, Durham, North Carolina, USA
Accepted for publication November 15, 2001.
* Address reprint requests to Dr Landolfo, Duke University Medical Center, DUMC-3675, Durham, NC 27710, USA
e-mail: lando001{at}mc.duke.edu
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Abstract
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Background. Although robotically assisted coronary arterial anastomoses are being performed clinically, the short-term and long-term quality and integrity of the left internal thoracic artery (LITA) to left anterior descending artery (LAD) anastomosis remains unknown. The goal of this study was to perform a histologic and angiographic assessment of porcine beating heart LITA to LAD anastomoses using either robotic assistance or a conventional freehand technique.
Methods. Twelve pigs underwent beating heart LITA to LAD anastomoses using either the robotically assisted (n = 6) or conventional freehand techniques (n = 6). Quantitative histologic analysis was performed in all animals in order to determine the degree of vascular wall damage. Selective coronary arteriography was performed in all animals immediately after the procedure in order to evaluate anastomotic patency. The unpaired Student’s t test was used for all comparisons between groups.
Results. There were no differences in vascular wall damage between the robotically assisted and freehand techniques. Postoperative angiography revealed no stenoses in either group.
Conclusions. Use of the robotically assisted technique for creation of a LITA to LAD anastomosis was not associated with increased histologic damage when compared with the freehand technique in a beating heart porcine model. Furthermore, there was no difference between the two techniques in postoperative patency rate. These results support further clinical investigation of robotically assisted coronary bypass surgery.
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Introduction
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Robotically assisted coronary artery bypass grafting (CABG) surgery is emerging as a novel technique in the armamentarium of heart surgeons. In recent years several groups have reported successful CABG procedures using various computer-assisted surgical systems for both arrested heart and beating heart cases [1–4]. However, few data exist concerning the efficacy of this technology especially with respect to endothelial and vessel wall injury. The purpose of our study was to compare the histologic, morphologic, and angiographic outcomes in coronary artery anastomoses using a voice-controlled and computer-assisted surgical system (Zeus; Computer Motion Inc, Goleta, CA) versus the traditional freehand technique in a porcine beating heart model.
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Material and methods
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Twelve swine (60 to 75 kg) underwent beating heart left internal thoracic artery (LITA) to left anterior descending artery (LAD) CABG procedure. The Institutional Animal Care and Use Committee at Duke University approved all the procedures performed in this study. The animals 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 Institutes of Health publication 85-23, revised 1985). The animals were randomly assigned to either the freehand or robotically assisted technique.
Preparation of the animals
The animals were sedated using 4 to 6 mg/kg intramuscular tilimetamina/zolazepan (Telazol; Wildlife Pharmaceuticals, Inc, Fort Collins, CO). An ear vein was cannulated using an 18-gauge catheter for fluid and drug administration. The animals were endotracheally intubated and mechanically ventilated. Isofluorane anesthesia was initiated at a rate of 2% and adjusted as needed. Intravenous lidocaine was administered as a bolus (0.5 mg/kg) followed by a continuous infusion (80 mg/h) in order to prevent arrhythmias. The animals were then placed on the operating table in a supine position. A right femoral arterial cutdown was performed for cannulation with a 9F hemostasis introducer (Fast-Cath Daig Corp, Minnetonka, MN), which was used for blood pressure monitoring and further access to LITA catheterization. Both blood pressure and continuous telemetry were displayed (Sirecust 404; Siemens Medical Systems, Danvers, MA) throughout the operation.
Surgical procedure
After median sternotomy the LITA was mobilized and harvested as a pedicle using standard instruments, electrocautery, and ligature clips. After heparinization (150 IU/kg), the LITA was transected and the distal end was prepared using standard coronary instruments. The chest retractor was then positioned and the pericardium opened. A pericardial cradle was not created so that the heart was left in situ. Atraumatic silastic snares (Retract-O-Tape; Quest Medical, Allen, TX) were placed underneath the middle third of the LAD, avoiding the inclusion within that segment of a large diagonal branch. The Genzyme OPCAB immobilizer device (Genzyme Biosurgery, Cambridge, MA) was then attached to the retractor and the immobilizer stabilization platform positioned on the anastomotic target. Subsequently the LAD was occluded and a 7-mm to 8-mm arteriotomy was performed using conventional instruments. A 2.0-mm diameter double-end intravascular shunt (IVS2030; Baxter, Irvine, CA) was then inserted through the arteriotomy to provide blood flow through the LAD during anastomosis. The silastic snares were then integrated into the slits provided by the stabilization platform to achieve a bloodless surgical field.
For the freehand beating heart anastomoses the parachute technique was used with a single-armed 7-0 polypropylene suture, conventional instruments, and standard 3.5 magnifying loops. For the robotically assisted procedures a 5-mm right instrument port was placed at the midline subxiphoid position, a 10-mm camera port was placed in the left fifth intercostal space 6-cm lateral to the midline, and a 5-mm left instrument port was placed in the left sixth intercostal space at the anterior axillary line. A 0-degree two-dimensional endoscope (Stryker, Santa Clara, CA) was attached to the video camera (882TE, Stryker) and light source (Quantum 4000, Stryker). Two specialized curved needle drivers were used for creation of the robotically assisted anastomosis. An assistant followed the surgical procedure by either direct vision or on a 21-inch monitor positioned at the side of the operating table. After the anastomosis was performed, saline was injected at low pressure in order to test for leakage. Additional sutures were placed if a leak was discovered. The septal branches were then identified and ligated with 7-0 polypropylene sutures. The shunting, stabilization, and anastomotic times in addition to the number of sutures used were collected for each animal.
Upon completing the anastomosis, the chest was closed and the animals were transported to our research catheterization laboratory where they underwent a LITA catheterization. During the procedure the animals were kept under inhalational anesthesia. A 9F guiding catheter (AR 1; Cordis, Miami, FL) was advanced from the right groin to the orifice of the LITA. The anastomosis was visualized with frontal and right anterior oblique projections (OEC-Diasonics, Salt Lake City, UT). The animals were then taken back to the operating room where they were sacrificed and the hearts harvested. To preserve the geometry of the anastomoses and to prevent elastic retraction after transecting the bypassed LAD, 2% agarose at 38°C was injected through the graft at low pressure [5]. The hearts were then placed in iced saline in order to allow the agarose to gel. The anastomoses were subsequently excised en bloc and fixed in 4% formaldehyde overnight.
Tissue processing and histologic stains
After overnight fixation in 4% formaldehyde the anastomoses were sectioned symmetrically in a transverse plane at the middle segment. The divided anastomoses were then paraffin embedded and sectioned in 4-µm slices, which were then mounted on charged glass slides. Twenty slides were mounted per anastomosis and of these, two were randomly chosen for application of each of three different types of stains. Hematoxylin and eosin (H&E) staining was used in order to assess the histologic viability of the vascular endothelium. Similarly, elastin van Gieson staining was used to identify viability of the internal elastic lamina of the anastomosed vessels. Finally, factor VIII related antigen immunostaining was performed on each anastomosis in order to assess the integrity of the endothelium at the time of study. Selection of these three stains was based on their compatibility with formaldehyde-fixed tissue and their ability to cross react with porcine tissue.
Histologic evaluation
The Olympus IX70 microscope (Olympus Optical, Japan) with a x20 magnification lens (Modulation Optics, Olympus, Japan) was used. The images were developed utilizing the Spot RT digital camera with the Spot RT software (version 3.06; Diagnostics Instruments, Sterling Heights, MI), which amplified the field 10 times. Subsequently the images were captured on an Adobe Photoshop (version 5.5; Adobe Systems, San Jose, CA) and then analyzed using the NIH Image 1.62 computer program. The histologic injury was quantitatively expressed as a percentage of the total endothelial and internal elastic lamina layers.
Data analysis
Data are presented as mean ± standard error of the mean (SEM). The unpaired Student’s t test (two tailed) was used for all the comparisons. A p value less than 0.05 was considered to denote statistical significance.
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Results
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The same surgical team performed both the freehand and robotically assisted procedures. All animals survived the procedure and were able to undergo postoperative selective biplane LITA catheterization. A blinded interventional cardiologist reviewed the angiograms. All anastomoses were patent with optimal run-off (Fig 1).
Minor stenoses (20% to 25%) were observed in the distal segment in 2 cases, 1 in each group of animals. Longer operative times were observed in the robotic assisted beating heart cases (Fig 2). No differences were seen in the number of sutures, (13.8 ± 0.16 freehand versus 13.5 ± 0.22 robotic, p = 0.25). The histologic evaluation showed no significant differences in endothelial and internal elastic lamina damage using H&E, factor VIII, and elastin van Gieson on the graft or coronary side respectively (Figs 3, 4, 5).
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Fig 1. Selective left internal thoracic artery catheterization of a beating heart case performed with robotically assisted technique.
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Fig 2. The operative times required to perform the robotically assisted procedures are compared: 1 = anastomotic time; 2 = shunting time; 3 = stabilization time. Values are expressed as mean ± standard error of the mean.
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Fig 3. The histologic damage with the three different stains used in the beating heart cases (phase 2) is compared. Values are expressed as mean ± standard error of the mean. (H&E = hematoxylin & eosin; LAD = left anterior descending artery; NS = not significant.)
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Fig 4. Factor VIII stain on a left internal thoracic artery to left anterior descending artery beating heart anastomosis performed with the freehand technique. The coronary side is the upper half of the anastomosis.
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Fig 5. Elastin van Gieson stain on a robotically assisted beating heart left internal thoracic artery to left anterior descending artery anastomosis.
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Comment
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Loulmet and colleagues [1] performed the first endoscopic, computer-assisted coronary artery bypass graft on an arrested heart in 1998 and were soon followed by other groups [2, 3]. The next step in the clinical development of this new technology came 1 year later when the first totally endoscopic beating heart CABG was performed at the University of Western Ontario [4]. Despite these clinical advancements there remains a lack of information on the effects of the robotically assisted technique on the quality of coronary artery anastomoses and the integrity of vessel wall structures.
It is known that the endothelium is critical in maintaining vascular homeostasis. In addition to its role in governing membrane permeability the endothelial cell also modulates vascular tone by producing nitric oxide and other endothelial-derived relaxing factors [6]. Endothelial cells also elaborate an array of potent growth promoters and inhibitors that work both in autocrine and paracrine fashion [7]. Finally, the endothelial layer serves as a physical barrier between blood elements and procoagulants contained within the subendothelium such as tissue factor. The exposure of blood cells to these procoagulants promotes platelet adhesion, aggregation, and degranulation, predisposing to vascular thrombosis. Platelets produce mitogens such as platelet-derived growth factor that regulate smooth muscle cell proliferation and migration into the intima [8, 9]. Intimal thickening and an increased propensity for early graft failure ensue. Thus endothelial integrity after coronary anastomosis is a critical determinant of early anastomotic patency.
Falk and colleagues [10] studied the quality of robotically created versus conventional freehand anastomoses in isolated hearts. Macroscopic and angiographic outcomes were equivalent for both techniques but no microscopic evaluation of the endothelial layer was performed. Using the Zeus telemanipulator system we were able to create LITA to LAD anastomoses in a porcine beating heart model. Because of our use of formaldehyde fixation to preserve our anastomoses we selected three histologic stains that are both compatible with this preservation technique and able to cross react with porcine tissue. Hematoxylin and eosin staining, which depicts histologic structures nonspecifically, revealed equivalent vessel integrity in the robotically assisted and freehand anastomoses. Elastin van Gieson staining, which is specific for the internal elastic lamina of medium-sized arteries, also showed a comparable degree of LAD and LITA integrity between the two anastomotic techniques. Finally, factor VIII related antigen immunostaining, in which the immunogen is located exclusively within endothelial cells, revealed adequate maintenance of endothelial architecture in both the robotically assisted and freehand anastomoses. Thus we have demonstrated that vessel wall integrity and specifically endothelial integrity are preserved after LITA to LAD anastomosis using the Zeus robotic system. These histologic findings help to explain the uniform patency of our anastomoses when assessed angiographically.
Boyd and colleagues [11] found that three-dimensional visualization with the Intuitive robotic microsurgical system reduces operating times, complexity of the anastomosis, and improves the quality of the graft when compared with endoscopic coronary anastomosis manually constructed with combined two- and three-dimensional visualization. The gold standard surgical procedure for the treatment of coronary artery disease is the conventional open chest nonbeating heart freehand technique. Any developing technology should demonstrate results that are at least equivalent to those that are already well established. In addition to demonstrating that the histologic integrity of LITA to LAD anastomoses is comparable between the two anastomotic techniques, we also were able to show angiographically that postoperative anastomotic patency was equivalent between the two groups. Furthermore the number of sutures needed to create the anastomoses was similar for both the robotically assisted and freehand techniques. The only significant difference we found between the two techniques was in the amount of time required to perform the anastomosis. The robotically assisted group required significantly greater operative times. The most likely explanation for this difference is the significant learning curve associated with use of the Zeus robotic system. Anastomotic times improved with increased use of the robotically assisted technique but even the later robotic cases took longer to perform than the freehand cases. Important components of this learning curve include the lack of force feedback, the lack of depth perception associated with two-dimensional visualization, and the availability of only four ranges of motions with the Zeus system.
Our study has several limitations. First, we used intracoronary arterial shunts during creation of the anastomoses in order to prevent ventricular arrhythmias. It has been previously shown that these shunts may have a deleterious effect on vascular endothelial function [12]. In order to minimize this potentially harmful effect we used the smallest shunt size feasible and inserted the shunt through extended arteriotomies (7 to 8 mm). Second, we performed histologic analyses on only the middle segment of each anastomosis. The use of normal caliber coronary arteries made it technically impossible to obtain adequate sections of the heel and toe segments without compromising the macrostructure of the entire anastomosis. Had we been able to analyze the peripheral segments of the anastomosis we may have observed endothelial denudation secondary to shunt insertion.
A third potential limitation was the use of silastic snares in order to occlude the coronary artery and thus create a bloodless surgical field. Previous electron micrographic studies have shown that the use of these snares causes some degree of endothelial injury [13]. However, other studies have failed to demonstrate any functional sequelae of such injury [14]. The use of the Genzyme stabilizer in beating heart surgery has not been shown to significantly affect endothelial integrity [15]. A final limitation of this study is its acute nature. A similar histologic and angiographic analysis of anastomotic integrity weeks to months after anastomosis is indeed warranted based on our early postoperative results.
In conclusion, this study demonstrates that robotically assisted LITA to LAD anastomosis in a beating heart model does not lead to increased histologic damage when compared with the conventional freehand technique. Similarly, no differences were observed in the two techniques with respect to angiographic patency. The robotically assisted anastomoses did, however, take longer to perform. These data support the continued clinical investigation of robotically assisted coronary surgery. Further investigation of the chronic effects of this technology on vessel wall integrity is clearly desirable.
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Footnotes
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1 Dr Schwartz discloses that he has a financial relationship with Computer Motion, Inc. 
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References
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Top
Abstract
Introduction
