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Ann Thorac Surg 1999;68:838-843
© 1999 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Computer-assisted endoscopic coronary artery bypass anastomoses: a chronic animal study

^a Section of Cardiothoracic and Vascular Surgery, Department of Surgery, The Milton S. Hershey Medical Center, Penn State Geisinger Health System, Hershey, Pennsylvania, USA and
^b Computer Motion, Inc, Goleta, California, USA

Address reprint requests to Dr Damiano, Section of Cardiothoracic and Vascular Surgery, The Milton S. Hershey Medical Center, Penn State Geisinger Health System, PO Box 850, Hershey, PA 17033
e-mail: rdamiano{at}psghs.edu

Presented at the Poster Session of the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 25–27, 1999.

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. With traditional instruments, endoscopic coronary artery bypass grafting (ECABG) has not been possible. This study was designed to determine the feasibility of using a robotically-assisted microsurgical system to perform ECABG in a chronic animal model.

Methods. Nine calves were placed on cardiopulmonary bypass after harvesting the left internal mammary artery (LIMA). Subxiphoid endoscopic ports (2 instrument, 1 camera) were placed, and a robotic system was used to perform ECABG between the LIMA and left anterior descending coronary artery. LIMA graft flow (LIMA_Q) was measured. Animals were sacrificed at 1 month, and hearts underwent angiographic and histologic analyses.

Results. Acute graft patency was 89% (8/9). Two animals died suddenly within the first 48 hours. There was no significant difference in mean acute and chronic (n = 6) LIMA_Q (40.9 ± 4.7 and 38.5 ± 5.0 ml/min, respectively). Survivors had an angiographic patency rate of 100% (6/6), confirmed by histology.

Conclusions. This study shows that ECABG is feasible in a chronic animal model with excellent results.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
The introduction and widespread acceptance of minimally invasive techniques have revolutionized surgical practice in many disciplines over the last two decades. Endoscopic operations have been shown to reduce patient morbidity and provide a more rapid return to work. Until recently, these new endoscopic approaches have had little impact on the field of cardiac surgery. Over the past few years, minimally invasive direct coronary artery bypass (MID-CAB) procedures have been introduced and are rapidly gaining acceptance [1]. The MID-CAB procedure typically is done on the beating heart through a small incision (left thoracotomy or partial sternotomy) without cardiopulmonary bypass. With improved techniques and instrumentation, results have been favorable [2–6]. However, several shortcomings have become apparent. Access to target vessels is limited and performance of the anastomosis is somewhat more technically challenging. Despite respectable patency rates, it has been suggested that the anastomoses may be less precise as a result of cardiac motion and limited visualization [7]. This has led many surgeons to return to the median sternotomy incision for beating heart surgery.

Port-access cardiac surgery was introduced to overcome some of these shortcomings [8–11]. Using specialized instruments and percutaneous cardiopulmonary bypass, port-access surgery provides improved exposure of target vessels in a quiescent operative field and thereby allows for multiple vessel bypass grafting [11, 12]. However, this approach still requires an incision. At the present time, endoscopically-sutured anastomoses have not been possible with either approach. The length and imprecision of standard endoscopic instruments have contributed to this failure [13].

Recently, surgical robotic systems have been developed to assist in endoscopic suturing [14, 15]. These systems consist of three main components: a surgeon interface device, a computer controller, and specially designed instruments attached to robotic arms. The surgeon manipulates traditional surgical instrument handles at the interface device. His movements are relayed in real-time by a computer to robotic arms which are attached to the operating room table. These robotic arms hold specially designed endoscopic instruments which are placed through small ports. By the use of computer elimination of tremor and motion-scaling, robotics provide the precision necessary to perform endoscopic coronary anastomoses. These robotic devices have been demonstrated to enhance surgical dexterity during a microvascular anastomosis in in vitro models [16, 17]. Our laboratory has recently completed work in an in vivo model, demonstrating the plausibility of robotic assistance in an acute large animal study [15]. The purpose of the current study was to determine both the feasibility and efficacy of using a robotically-assisted microsurgical system to perform coronary anastomoses in a chronic large animal model.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Nine Holstein calves weighing 75 to 100 kg were used in the study. All animals received humane care in Association for Accreditation for Laboratory Animal Care (AA-LAC), US Department of Agriculture (USDA) registered (#23-R-02) facilities in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and 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 No. 85-23, revised 1985).

Experimental preparation
Preparation of the animal
Calves were weighed and taken to the preoperative preparation room. Anesthesia was induced with 8 mg/kg of intravenous methahexital (Brevital, Jones Medical Industries, St. Louis, MO). The calves were intubated and begun on mechanical ventilation. Isoflurane anesthesia was initiated at a rate of 2.5% and adjusted as needed. Two 14-gauge catheters (Angiocath, Becton Dickinson Infusion Therapy Systems, Inc, Sandy, UT) were placed in the external jugular vein for administration of intravenous fluid. The calves were then placed on the operating table in a supine position.

An esophageal temperature monitor was inserted (Model BAT 8, Bailey Instruments, Saddle Brook, NJ) and the animals were prepped and draped in a routine sterile fashion. A superficial branch of the right femoral artery was cannulated with a 20-gauge catheter and connected to a pressure transducer (Model 041-500-503A, Maxxim Medical, Athens, TX). The blood pressure and the electrocardiogram (recorded from limb leads) were continuously displayed (Sirecust 404, Siemens Medical Systems, Inc, Danvers, MA). The animals were given an intravenous injection of methylprednisolone (1 g). Following an intravenous lidocaine bolus (80 mg), a continuous infusion (80 mg/hr) was started for dysrhythmia prophylaxis. A longitudinal incision was made in the right neck, and the carotid artery isolated, in preparation for arterial cannulation for cardiopulmonary bypass.

Internal mammary artery harvesting
A right fourth intercostal space thoracotomy was performed. The right internal mammary artery (RIMA) was exposed at the anterior limit of the thoracotomy for subsequent flow measurements. The pericardium was dissected free from the sternum and the mediastinal pleural opened to expose the left internal mammary artery (LIMA). The internal mammary vessels were dissected from the first intercostal space to the level of the diaphragm using standard instruments, electrocautery and ligature clips (Ligaclip 20/20, Ethicon, Somerville, NJ). The animal was systemically heparinized (300 U/kg) and additional boluses were given as needed to maintain an activated clotting time of greater than 500 seconds (Hemochron 801, Technidyne International Corp, Edison, NJ). The distal internal mammary vessels were then ligated and divided. Free flow in the LIMA was measured and the vessel was occluded with an atraumatic vascular clamp. The distal end of the artery was prepared for anastomosis using standard coronary instruments.

Cardiopulmonary bypass
A conventional perfusion circuit was assembled (Pump Model 5000, Sarns3M, Ann Arbor, MI) and flushed with carbon dioxide. The bypass circuit was primed with 2 liters of Plasma-Lyte (Baxter Healthcare Corp, Deerfield, IL), 50 mEq sodium bicarbonate, 25 mg mannitol, and 10,000 U of heparin. Arterial blood gases, electrolytes, and serum hematocrits were measured prior to initiating cardiopulmonary bypass and at regular intervals thereafter. These values were maintained within the physiological range throughout the study.

The right carotid artery was cannulated with a metal tip cannula (6.4 mm ID) for arterial inflow, and a two-stage (34/48 Fr) venous cannula (Medtronic DLP, Grand Rapids, MI) was inserted into the right atrium through the thoracotomy. Cardiopulmonary bypass was instituted at a perfusion flow rate of 2.0 to 2.4 L/min/m². Mean arterial blood pressure was maintained between 60 to 80 mm Hg with the administration of phenylephrine and fluids as needed.

After the initiation of bypass, the hemiazygos vein was ligated within the pericardium. A 16F vent (Medtronic DLP) was placed into the apex of the left ventricle. The ascending aorta was encircled with an umbilical tape. A cannula (Model 24009, Medtronic DLP) was inserted into the proximal ascending aorta for cardioplegia delivery.

Preparation of the robotic system
A 10 mm endoscopic port (Endopath, Ethicon) was placed just to the right of the xiphoid process and passed into the chest. A 0° endoscope (Karl Storz, Culver City, CA) was placed through this port and attached to a video camera (Tricam SL, Karl Storz) and light source (Zenon 300, Karl Storz). The video image was displayed on a 21'' color monitor (Trinitron, Sony Corp, Tokyo, Japan). The endoscope was connected to a voice-controlled robotic camera holder (Aesop 3000, Computer Motion, Inc, Goleta, CA), which provided a steady video image and allowed for smooth, precise camera movements. Two 5 mm endoscopic ports (Endopath, Ethicon) were then placed subcostally, 7 cm on either side of the endoscope port (Fig 1).

View larger version (142K): [in this window] [in a new window]   Fig 1. Intraoperative photograph demonstrating endoscopic port placement.

Cardioplegic arrest
The calves were systemically cooled to 30 to 32°C. Myocardial temperature was monitored in the ventricular septum with a needle probe (Model TM147T, Electromedics, Inc, Parker, CO). The aorta was crossclamped and cold crystalloid cardioplegia was delivered in antegrade fashion at a pressure of 60 to 90 mm Hg. The composition of the cardioplegia used for induction was (in mEq/L): Na⁺, 130; K⁺, 40; Cl^-, 109; Ca⁺⁺, 2.7; lactate, 28; and NaHCO₃, 10. Maintenance cardioplegia was similar in composition with the exception of a lower K⁺ concentration, 20 mEq/L. Cardioplegia (10 cc/kg) was administered every 20 to 30 minutes during the crossclamp period. Systemic rewarming was initiated at the completion of the anastomosis.

Endoscopic anastomosis
The heart was left in its in situ position and was not suspended in a pericardial cradle. The chest retractor was removed to allow a more normal anatomic position of the chest wall. Following cardioplegic arrest, an arteriotomy was made in the distal left anterior descending coronary artery (LAD) using the robotic system and specialized scissors. The proximal LAD was occluded with a MyOcclude clamp (United States Surgical Corp, Norwalk, CT). A continuous, end-to-side anastomosis was performed endoscopically using the robotic instruments and camera (Fig 2). No manipulation of the heart was necessary doing the anastomosis and there was excellent visualization of each stitch through the subxiphoid camera port. Exposure of the anastomotic site was enhanced with the use of a blower (Visuflo SSVW-002, Research Medical, Inc, Midvale, UT). The running anastomosis was performed with a specially designed 7 cm, double-armed 7-0 Gore-Tex suture (W.L. Gore and Associates, Flagstaff, AZ). After completion of the anastomosis, the suture was tied endoscopically. No repair stitches were required.

View larger version (159K): [in this window] [in a new window]   Fig 2. Intraoperative photograph taken from the endoscopic camera of the left internal mammary artery to left anterior descending anastomosis.

Postoperative care and termination
The animals spent the first several postoperative days under monitored care. A nitroprusside infusion was used as needed to maintain a mean arterial blood pressure of 80 to 90 mm Hg during the first 24 hours. When appropriate, the arterial catheter, chest tube, and intravenous catheters were removed. Following clearance from a veterinarian, the animals were then taken to a barn facility.

At 4 to 6 weeks postoperatively, the animals were brought back to the operating room and anesthetized. Arterial blood pressure and the electrocardiogram were monitored and a right thoracotomy was performed. After data acquisition, the animals were euthanized with a 50 cc intravenous injection of Sleepaway (Fort Dodge Laboratories, Fort Dodge, IN). The heart and a suitable length of the LIMA graft were rapidly excised for pathological fixation.

Data acquisition
Graft flow measurements
Following vessel harvest, free LIMA flow was measured using a timed collection. After the anastomosis was performed, LIMA and RIMA flow was assessed acutely, both on and 30 minutes after being weaned from cardiopulmonary bypass. Flow measurements were made using a 3 or 4 mm probe (HT311, Transonic Systems, Inc, Ithaca, NY) placed on the proximal LIMA graft and recorded using FlowTrace 32 software (Transonic Systems, Inc). Prior to termination of the animal, chronic LIMA graft flow was assessed in a similar fashion.

Transesophageal echocardiography
A single plane, 2-D probe (Model I5100, Acuson Computed Sonography, Mountain View, CA) was used to obtain transesophageal echocardiography (TEE) images with a two-chamber view in the long axis (Model 128XP/10, Acuson Computed Sonography). Anterior wall motion and left ventricular ejection fraction were assessed as a measure of ventricular function. Studies were obtained prior to and following cardiopulmonary bypass, and chronically at autopsy.

Angiography
Excised hearts were fixed via the ascending aorta with 10% buffered formalin perfused at 100 mm Hg for 1 hour. The hearts were then studied angiographically before being submitted for histologic analysis. Contrast (MD-76R, Mallinckrodt Medical, Inc, St. Louis, MO) was injected via the LIMA graft as radiographic images were obtained.

Histology
Gross descriptions of the fixed specimens were obtained following dissection and sectioning of the LIMA and LAD anastomoses. Microscopic slides were then made of the LIMA, LAD, anastomosis, left ventricular septum, and left ventricular free wall using hematoxylin and eosin staining. Additional slides were obtained using Trichrome, Verhoff’s Elastica, and Von Kossa stains.

Data analysis
Coronary blood flow was compared acutely and at 1 month follow-up using a Student’s paired t test.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Intraoperative
All animals underwent successful coronary grafting and were weaned from bypass without difficulty. The total bypass time (mean ± SEM) was 135.0 ± 7.3 minutes, with a crossclamp time of 42.1 ± 2.6 minutes. The time for completion of the anastomosis (including knot tying) was 33.2 ± 3.4 minutes. Eight animals received temporary support in the form of a low dose dopamine infusion (3–5 mcg/kg/hr) during the immediate postoperative period (< 2 hours). The graft patency rate, as measured by a flow meter, following completion of the anastomosis was 89% (8 of 9). The animal with the occluded graft was included in the intraoperative data analysis, but removed from further study of graft patency. The occluded graft was examined at autopsy 1 month later and was found to be thrombosed over its entire length.

Postoperative
Two of the 8 animals died suddenly within the first 2 postoperative days (at 2 hours, and at 2 days). Neither animal had any sign of hemorrhage or graft occlusion at autopsy. In both animals, grafts were found to be patent by angiography. The cause of death remains speculative, but may have been an arrhythmia. The rest of the animals (n = 6) recovered without complication and underwent autopsy at 31 ± 2 days postoperatively.

Coronary bypass graft flow
Blood flow (mean ± SEM) in the in situ RIMA was 47.0 ± 6.7 cc/min while on bypass, and 82.5 ± 15.6 cc/min off bypass. Graft flow (measured in the proximal LIMA) was 21.1 ± 5.9 cc/min on bypass, and 40.9 ± 4.7 cc/min off bypass. Graft patency as measured by flow meter was 100% (6 of 6), with a graft flow at autopsy of 38.5 ± 5.0 cc/min. Flow tracings from all grafts showed good diastolic augmentation (Fig 3).

View larger version (25K): [in this window] [in a new window]   Fig 3. Typical blood flow tracings in the grafted (left) and in situ (right) internal mammary arteries off cardiopulmonary bypass.

View larger version (120K): [in this window] [in a new window]   Fig 4. Postmortem angiogram demonstrating the anastomosis between the left internal mammary artery (arrow) grafted to the left anterior descending coronary artery. Contrast was injected through the proximal left internal mammary artery. A MyOcclude clamp is on the proximal left anterior descending coronary artery.

Echocardiography
The only postoperative regional wall motion abnormality evident in any animal was graded as slight anterior hypokinesia in one calf in the immediate postoperative period. This had resolved at chronic follow-up. Ejection fraction was preserved intraoperatively and chronically in all animals studied.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
In the past several years, minimally invasive techniques have had a significant impact on the field of cardiac surgery. The potential benefits of these approaches include reduced costs, less blood loss, lower complication rates, and shorter hospital stay [18, 19]. The initial results of both beating heart and port-access procedures have been encouraging, with acceptable graft patency and minimal morbidity in large series of patients [2, 4, 20]. Recent reports with more intermediate follow-up also have shown satisfactory outcomes [21]. However, with the present techniques it has not been possible to achieve the ultimate goal, completely endoscopic coronary artery bypass grafting (ECABG).

Recently, robotically-assisted microsurgery systems have been introduced to increase the precision of endoscopic surgery. These computer-guided systems can control both surgical instruments [15, 16] and endoscopic cameras [22]. The advantages afforded by robotic instrumentation may help overcome some of the obstacles to endoscopic coronary artery bypass grafting. Specifically, robotic instrumentation may provide access to multiple target vessels and offer the surgeon the ability to precisely operate in very confined spaces. In the current study, the robotic microsurgical system was able to eliminate tremor by filtering high frequency motions, and smooth the surgeon’s movements through computer motion-scaling. Thus, computer assistance has the potential to overcome perhaps the most significant limitation of standard endoscopic instruments; ie, lack of precision due to instrument length and operator tremor. Endoscopic magnification of the operative site helped with the accuracy of suture placement by providing the surgeon with excellent visualization.

In our previous studies using an acute animal model, the performance of ECABG was technically feasible with excellent acute graft patency [15]. The current study analyzed the outcomes of robotically-assisted ECABG in a more clinically relevant chronic animal model. Graft patency was excellent acutely in the operating room (89%, 8/9) and remained so at 1 month (100%, 6/6), as demonstrated both by angiography and histology.

Limitations and clinical implications
The current study was performed using a bovine model, which had inherent anatomic limitations due to the configuration of the animal’s chest. The percutaneous methods of cardiopulmonary bypass and cardioplegic arrest currently available were incompatible with the short ascending aorta of the calf, which necessitated a right thoracotomy. Therefore, this was not a completely endoscopic approach. However, all anastomoses were performed endoscopically. The different chest wall anatomy of the human may require an alteration in the approach for clinical cases. Moreover, a completely endoscopic procedure remains a formidable challenge and will require the development of new instruments and techniques in order to perform a complete operation through ports. Nonetheless, the current study confirms that robotically-assisted ECABG is feasible and efficacious in a chronic large animal model with excellent anastomotic outcomes. Clinical trials are warranted in the near future.

	Acknowledgments

 
The authors gratefully acknowledge the technical assistance of Karen M. Reigle.

	Footnotes

 
The work described in this report was supported by a grant from Computer Motion Inc. Sachin Sankholkar is an employee of Computer Motion Inc.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Ralph J. Damiano, Jr Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Stephenson, E. R. Articles by Damiano, R. J. Search for Related Content PubMed PubMed Citation Articles by Stephenson, E. R., Jr Articles by Damiano, R. J., Jr