Ann Thorac Surg 1997;64:64-69
© 1997 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Development of a Minimally Invasive Technique for Coronary Revascularization in a Porcine Model
M. Clive Robinson, MD,
David R. Gross, DVM, PhD,
Kenneth A. Thielmeier, MD,
Bradley B. Hill, MD,
William F. Zeman, MD
Division of Cardiovascular and Thoracic Surgery and Department of Anesthesiology, College of Medicine, University of Kentucky, Lexington, Kentucky
Accepted for publication January 6, 1997.
 |
Abstract
|
|---|
Background. This porcine model was designed to develop a minimally invasive method for internal mammary artery (IMA) grafting using an anterior mediastinal approach and without routine use of cardiopulmonary bypass.
Methods. Assessment was made of IMA mobilization through a small parasternal incision, the feasibility of coronary artery grafting with cardiopulmonary bypass using this approach, and conditions for off-pump bypass grafting.
Results. In group 1, 6 pigs underwent IMA mobilization through a 5-cm horizontal midparasternal incision. Of the 2 group 2 pigs, 1 underwent IMA grafting to the left anterior descending coronary artery and the other, bilateral IMA grafting to the left anterior descending and right coronary arteries using femoral-vessel cardiopulmonary bypass. In group 3, 4 of 10 pigs had successful off-pump grafting during retrograde regional coronary venous perfusion of arterial blood. Retrograde coronary venous perfusion could not be established in the other 6 pigs, and attempts at off-pump grafting failed.
Conclusions. The study demonstrates that coronary artery grafting with the IMA by this minimally invasive off-pump method is feasible, although it draws attention to areas of concern and potential methods of correction. The model provides a realistic and important learning platform for the surgical issues involved with this minimally invasive technique.
|
Introduction
|
|---|
During the last 10 years, multiple clinical reports have shown that coronary artery bypass grafting (CABG) has long-term advantages over percutaneous transluminal coronary angioplasty (PTCA) and other catheter-based therapies used to treat coronary artery disease. In a large randomized study, Hamm and associates [1] found that although patients with coronary disease show equal improvement in angina at 1 year after PTCA or CABG, those undergoing PTCA have a substantially higher requirement of additional interventions and antianginal drugs. King and colleagues [2] reported the results of another randomized, prospective trial comparing CABG and PTCA. They found no significant differences in death as the result of myocardial infarction at 3 years after either procedure, but a significantly higher percentage of PTCA patients had angina during the 3-year period. Many studies [3–7] have shown that angioplasty and atherectomy have significant short-term and medium-term recurrence rates. Other series [8–12] have demonstrated the superiority of internal mammary artery (IMA) grafting over the use of both saphenous vein grafting and PTCA.
The offsetting aspect of conventional CABG includes the noncardiac-related morbidity associated with median sternotomy and cardiopulmonary bypass (CPB). Knowing the advantages of the IMA conduit and the limitations of catheter-based methods, we undertook to design a less-invasive method of CABG to address this problem. The purpose of this animal study was to develop the techniques and skills necessary to accomplish CABG with IMA pedicle grafts through a minimally invasive incision and without routine use of CPB as a preliminary experience to use of the procedure in patients.
|
Material and Methods
|
|---|
The project commenced in June 1993. The porcine model was selected largely because the basic chest wall structure and coronary anatomy are similar to those of humans and because of the poorly developed coronary collateral system that provides a sensitive "worst-case" model for acute ischemia. Animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals (NIH publication 85-23, revised 1985), and all protocols were approved by the University of Kentucky Animal Care and Use Committee. All pigs were young farm-bred species and weighed 40 to 50 kg each.
Pigs were premedicated with ketamine hydrochloride (20 mg/kg intramuscularly) and xylazine (0.05 mg/kg intramuscularly), and anesthesia was maintained with isoflurane (1.5 to 2.5 vol/100 mL) and oxygen through a cervical tracheostomy. End-tidal carbon dioxide was continuously monitored, and ventilation was adjusted to maintain arterial blood gases within normal limits. The carotid artery was cannulated for arterial blood pressure monitoring (Spectramed model P23XL pressure transducer) and blood gas determination. Body surface electrodes were applied for continuous electrocardiographic (ECG) monitoring. All transducers were connected to appropriate transducer couplers/amplifiers (Gould model 5900; Cleveland, OH). Data were collected by a videocassette recorder (TEAC XR-510) and then digitized at 500 samples per second using an IBM 386 clone (Standard Technologies) and AT/MCA-CODAS software (DATAQ Inst, Inc, Akron, OH).
Eighteen pigs were assigned to one of three consecutive groups: group 1 (n = 6) to assess the feasibility of IMA takedown through the anterior mediastinal approach; group 2 (n = 2) to assess the feasibility of IMA–CABG with CPB through the femoral vessels; and group 3 (n = 10) to assess conditions for off-pump bypass grafting using the anterior mediastinal approach. Conventional surgical principles of suturing and instrumentation were used to enable valid projection to the known long-term results of standard CABG.
|
Group 1-IMA Takedown Through Anterior Mediastinal Approach
|
|---|
A 5-cm transverse midparasternal incision was made, and the underlying third or fourth costal cartilage was either excised or disconnected from the sternum and separated (Fig 1
). Through this incision the IMA was dissected as a pedicle to close to its origin by using electrocautery and sharp dissection. In the first five procedures, video-assisted thoracoscopy through lateral chest ports was used to complete the dissection. In the pig, most of the IMA lies beneath a prominent transversus thoracis muscle that obscures the artery, and this muscle must be divided when first approached during thoracoscopic dissection.
|
Group 2-CABG Through Anterior Mediastinal Approach With CPB
|
|---|
The left IMA in 1 pig and both IMAs in the other pig were dissected through separate incisions as just described. After systemic heparinization (300 IU/kg intravenously), the left femoral artery and vein were cannulated with CPB cannulas. The pericardium underlying the anterior mediastinotomy was vertically incised, and the corresponding left anterior descending coronary artery (LAD) or right coronary artery was visualized. Use of traction sutures on the pericardial edges and, if necessary, placement of superficial left ventricular myocardial sutures or use of a mechanical lever allowed anterior and medial displacement of the heart and alignment of the respective LAD or right coronary artery in the center of the wound. Sutures of 5-0 Prolene (Ethicon, Somerville, NJ) were inserted circumferentially around the coronary artery to achieve isolation proximal and distal to the proposed anastomotic site. Cardiopulmonary bypass was initiated, and the pig was cooled to 32°C. The IMA was grafted to the coronary artery on the fibrillating heart by using standard surgical instruments and suturing techniques.
After grafting and rewarming were completed, each heart was successfully defibrillated with paddles manipulated through the incision. Straightforward weaning from bypass was achieved with return to normal ECG and hemodynamic readings. The pigs were then killed with an overdose of barbiturates (>300 mg/kg intravenously), and the anastomoses were transected and inspected.
|
Group 3-Off-Pump CABG Through Anterior Mediastinal Approach
|
|---|
In an attempt to avert the frequent hemodynamic decompensation associated with acute coronary artery isolation in the pig, we performed myocardial ischemic preconditioning along with attempts to establish retrograde regional coronary venous perfusion. For myocardial preconditioning, several 2- to 3-minute periods of LAD occlusion and reperfusion using 5-0 Prolene compressing sutures around the artery were accomplished. For regional coronary venous retroperfusion, attempts at direct retrograde anterior cardiac vein cannulation using a perfusion balloon-tipped catheter were carried out in 8 pigs (Fig 2). The entry point for the coronary vein cannula was usually at the junction of the proximal and middle thirds of the anterior interventricular septum. In the 2 other pigs, attempts were made to reach the anterior cardiac vein by direct cannulation of the coronary sinus with retrograde catheter advancement under fluoroscopy using a guide-wire through the femoral vein. Heparin sodium was given as previously described.
In the case of successful anterior cardiac vein cannulation, a perfusion system of arterial blood from the carotid artery line to the anterior cardiac vein was set up. This consisted of 
-inch tubing and a bubble trap primed with heparinized lactated Ringer's solution. Manual syringe perfusion was used initially at empirically derived rates of approximately 70 mL/min. In a later method, we used a precalibrated roller pump (Masterflex; Cole Parrver, Chicago, IL) with flow settings of 50 to 80 mL/min.
When satisfactory retroperfusion as evidenced by ECG and hemodynamic stability had been achieved, the off-pump CABG of the IMA to the LAD was performed. To facilitate anastomotic suturing, movement from the beating heart was limited by use of a variety of mechanical instruments. Metal rings or a pediatric aortic side-clamp was used for compression of the myocardium adjacent to the coronary arteriotomy. Also, if the coronary artery was not easily maneuvered into the center of the incision, an endoscopic lung retractor (US Surgical) was inserted through a lateral chest port and used behind the heart for medial and anterior leverage. Once the off-pump anastomosis was completed, the pigs were killed and the grafts transected to assess technical accuracy.
|
Results
|
|---|
Group 1
Mobilization of the left and right IMA pedicles from one interspace below the incision to near their origins was successful in each of the 6 pigs. Video-assisted thoracoscopy was used to facilitate the IMA dissection in 5 of these animals. The right IMA takedown was somewhat more straightforward than that of the left because on the left side, the close proximity of the heart and pericardium to the posterior surface of the ribs and sternum restricts access. An adequate IMA pedicle length was obtained in each case to allow anastomosis in the vicinity of the midpoint of the coronary artery. When cartilage was excised, the division and anterior retraction of the cartilage of the interspace above improved access. When cartilage was not excised, disconnection of cartilage from the sternum above and below the entered interspace aided access. On completion of the procedure, this transected cartilage could be sutured back to its original position.
Care was required when freeing the IMA pedicle to avoid inadvertent electrocautery injury to the IMA trunk or direct contact with the pericardium with the possibility of ventricular fibrillation. A long-handled electrocautery scalpel was useful in the proximal pedicle dissection. Hemostasis of the IMA bed was achieved by electrocautery under direct vision or with visualization assisted by a dental mirror or video-assisted thoracoscopy.
|
Group 2
|
|---|
In the 2 group 2 pigs, anastomosis of the IMA to the respective coronary artery was performed with CPB, systemic cooling to 32°C, and induced ventricular fibrillation. Avoiding sternotomy retained the pericardial suspension and maintained the anterior position of the heart. Exposure and access to the proximal portion and midportion of the LAD and the right coronary artery varied somewhat between pigs but in general were good and were facilitated by the decompressed heart on CPB.
In the situation of CPB with ventricular fibrillation, any undue left ventricular distention that may occur can be dealt with by use of a conventional transseptal left ventricular small catheter vent introduced through either the incision or the adjacent chest wall. Both pigs in this group were weaned from CPB with satisfactory ECG and hemodynamic variables. Subsequent inspection of the grafts showed them to be technically accurate.
|
Group 3
|
|---|
Satisfactory alignment of the coronary artery in the incision was less readily achieved in the full, beating heart. If there was an abnormally lateral course of the coronary artery or an abnormal axis of the heart, then the mechanical lung lever through a chest port in combination with pericardial traction sutures substantially improved access.
Myocardial ischemia was invariably a problem in the off-pump setting. Typically in the porcine model where preexisting coronary lesions are absent and coronary collateral formation is poor, acute coronary occlusion is associated with profound hemodynamic instability. Efforts at preconditioning failed to prevent these events. Usually within 3 to 5 minutes of isolating the coronary artery, a variable sequence including ischemic ECG changes, hypotension, and ventricular fibrillation occurred.
Use was made of retrograde regional coronary venous perfusion of arterial blood to correct the ischemia distal to the isolated LAD. For LAD grafting, the anterior cardiac vein was cannulated with the perfusion balloon-tipped catheter. For right coronary artery grafting, no accessible vein is available, making this alternative unsuitable. Retrograde anterior cardiac venous perfusion was successfully established in 4 pigs, and each showed impressive correction of ischemia-induced ECG and hemodynamic changes (Fig 3). Off-pump IMA grafting was completed successfully in each, and accurate anastomoses were seen at postmortem examination.
View larger version (45K):
[in this window]
[in a new window]
|
Fig 3. . (A) Baseline aortic pressure (Pao) and surface electrocardiogram (ECG). (B) Decreased Pao and ischemic ECG changes at 5 minutes of occlusion of left anterior descending coronary artery. (C) Aortic pressure and ECG at onset of retroperfusion. (D) Nearly normal Pao and ECG with 1.5 minutes of retroperfusion.
|
|
The optimal retrograde flow rate appeared to be about 70 mL/min. Slower infusions failed to adequately correct the ischemia, and faster infusions produced ventricular ectopy. However, positioning the retrograde cannula was particularly difficult through this approach. In 4 of 8 pigs, efforts at direct anterior cardiac vein cannulation failed because of tearing and disintegration of the vein wall, inability to advance the catheter beyond the isolated LAD graft segment, undue bleeding, or dislodgment after initial positioning. All attempts at grafting without retrograde perfusion support produced early and intractable ventricular fibrillation and death.
In 2 other pigs, catheter advancement was made from the femoral vein with fluoroscopic guidance into the coronary sinus and attempted positioning in the anterior cardiac vein. The pig anatomy, however, includes a large posterior azygos–coronary sinus confluence into which the disproportionately small anterior cardiac vein drains. This anatomic configuration made cannulation of that vein very difficult, and retrograde coronary perfusion could not be established in either pig. Attempts at unsupported grafting again resulted in ventricular fibrillation soon after LAD occlusion.
|
Comment
|
|---|
Our study demonstrates the technical feasibility of this minimally invasive method for IMA grafting with an anterior mediastinal approach and without CPB. This technique, although using a small incision, allows completion of the anastomosis under direct vision with standard instrumentation and sutures. It also allows direct inspection and palpation of the coronary artery for correlation with angiographic landmarks, location of stenotic disease, and selection of the correct site for the anastomosis. In addition, conventional methods can be used to deal with complications that may occur during or after CABG. Defibrillation, if required, can be performed using internal paddles placed through the incision or patches applied externally, and direct and rapid access through the incision to any site of postoperative bleeding is possible. For these reasons, extrapolation to the proven long-term results of conventional IMA grafting in humans should be valid. If necessary, sternotomy and conversion to the standard procedure can be expeditiously performed at any stage during the operation.
Once practiced, dissection of the IMA becomes relatively straightforward. Mobilization providing satisfactory length from one interspace below the incision to close to the origin is achieved. Removal of one cartilage or disconnection of the cartilages above and below the interspace improved access for direct dissection, and after the first five procedures, routine use of video-assisted thoracoscopy was abandoned. Compared with that of the human, the IMA in the pig is larger, less fragile, more widely separated from the sternum, and covered by a prominent transversus thoracis muscle. The technicalities of dissection are therefore less demanding than in humans.
Because the LAD and the right coronary artery run a parasternal rather than a retrosternal course, they are generally quite accessible through this approach. A variety of maneuvers are available to further improve access, including use of the endoscopic lung retractor as a cardiac lever.
For the animals having CABG on the pump (group 2), satisfactory myocardial protection was achieved by CPB with systemic cooling, retained coronary perfusion, and ventricular fibrillation; if required, ventricular decompression by transseptal left ventricular venting can be accomplished. These conditions provide a quiet field for placement of anastomotic sutures, and this option is a valid intermediate alternative in learning the minimally invasive technique before dispensing with CPB.
The primary area of contention was in the off-pump CABG group (group 3). When off-pump CABG is contemplated, concerns relating to distal coronary artery ischemia, possible local arterial wall injury from methods of vessel control, and technical accuracy of the graft must be addressed. These issues are of added concern when a small incision is used. As a measure to offset distal ischemia, our primary focus was on the use of regional retrograde coronary venous perfusion of autologous arterial blood. In our experience, the technicalities of establishing this were a problem. The fragile wall of the anterior cardiac vein split readily, and bleeding often obscured the anastomotic area. Even with a Seldinger wire, advancing and retaining the catheter was a problem. Also, because of the anatomy of the azygos vein and coronary sinus in the pig, successful cannulation through this route could not be achieved.
Although the off-pump method was proved feasible in our model, the experience did identify the expected concerns with the off-pump technique in general and with the pig model in particular. Reassuring results were seen in 4 of 4 pigs when successful retrograde perfusion was completed. The method was cumbersome, and for the purposes of more reliably maintaining heart function in this model, consideration could be given to alternative systems, such as combined ischemic and pharmacologic preconditioning or direct intraluminal catheter placement and perfusion of arterial blood through the arteriotomy. In comparison with this animal model, the situation in patients differs because of chronic ischemic lesions and established coronary collateral formation, and with both ischemic and pharmacologic preconditioning, coronary artery isolation is usually well tolerated. An effective retrograde regional venous or coronary sinus perfusion system, however, may offset ischemia or further improve ischemic tolerance for grafting, thus increasing the safety of off-pump grafting. Such a system has been used widely in other experimental animal studies [13, 14] and in clinical cardiac situations [15–18], including during PTCA [19, 20], and a commercially available diastolic retroperfusion system with a specialized catheter advanced through the coronary sinus (RSI Inc, Irvine, CA) is available.
Beyond the question of ischemia during grafting, and again relevant to our porcine model, are other concerns with off-pump grafting. Although the anastomoses from the grafts examined in these pigs appeared accurate, the impression was that conditions are considerably less optimal than when grafting with an arrested heart. Large patient series and quite widespread experiences with off-pump CABG have been reported, but technicalities of grafting, ischemia, and possibly vessel wall injury remain areas for improvement. Nonetheless, routinely dispensing with CPB where possible is an important component of the minimally invasive CABG technique. Besides identifying and addressing the issues of technical feasibility and areas for improvement of this minimally invasive method, the porcine model provides a very suitable and important learning platform for experience with both the anterior mediastinal surgical access and off-pump grafting.
|
Footnotes
|
|---|
Address reprint requests to Dr Robinson, Division of Cardiovascular and Thoracic Surgery, University of Kentucky Chandler Medical Center, 800 Rose St, Rm MN276, Lexington, KY 40536-0084.
|
References
|
|---|
- Hamm CW, Reimers J, Ischinger T, Rupprecht HJ, Berger J, Bleifeld W. A randomized study of coronary angioplasty compared with bypass surgery in patients with symptomatic multivessel coronary disease. German Angioplasty Bypass Surgery Investigation (GABI). N Engl J Med 1994;331:1037–43.[Abstract/Free Full Text]
- King SB III, Lembo NJ, Weintraub WS, et al. A randomized trial comparing coronary angioplasty with coronary bypass surgery. Emory Angioplasty versus Surgery Trial (EAST). N Engl J Med 1994;331:1044–50.[Abstract/Free Full Text]
- Kramer JR, Proudfit WL, Loop FD, et al. Late follow-up of 781 patients undergoing percutaneous transluminal coronary angioplasty or coronary artery bypass grafting for an isolated obstruction in the left anterior descending coronary artery. Am Heart J 1989;118:1144–53.[Medline]
- Schwartz L, Lesperance J, Bourassa MG, et al. The role of antiplatelet agents in modifying the extent of restenosis following percutaneous transluminal coronary angioplasty. Am Heart J 1990;119:232–6.[Medline]
- Topol EJ, Leya F, Pinkerton CA, et al. A comparison of directional atherectomy with coronary angioplasty in patients with coronary artery disease. The CAVEAT Study Group. N Engl J Med 1993;329:227.
- Rodriguez A, Santaera O, Larribeau M, Sosa MI, Palacios IF. Early decrease in minimal luminal diameter after successful percutaneous transluminal coronary angioplasty predicts late restenosis. Am J Cardiol 1993;71:1391–5.[Medline]
- King SB 3rd, Schlumpf M. Ten-year completed follow-up of percutaneous transluminal coronary angioplasty: the early Zurich experience. J Am Coll Cardiol 1993;22:353–60.[Abstract]
- Loop FD, Lytle BW, Cosgrove DM, et al. Influence of the internal mammary artery graft on 10-year survival and other cardiac events. N Engl J Med 1986;314:1–6.[Abstract]
- Azariades M, Fessler CL, Floten HS, Starr A. Five-year results of coronary bypass grafting for patients older than 70 years: role of internal mammary artery. Ann Thorac Surg 1990;50:940–5.[Abstract]
- Boylan MJ, Lytle BW, Loop FD, et al. Surgical treatment of isolated left anterior descending coronary stenosis. Comparison of left internal mammary artery and venous autograft at 18 to 20 years of follow-up. J Thorac Cardiovasc Surg 1994;107:657–62.[Abstract/Free Full Text]
- Barner HB, Barnett MG. Fifteen- to twenty-one–year angiographic assessment of internal thoracic artery as a bypass conduit. Ann Thorac Surg 1994;57:1526–8.[Abstract]
- Edwards FH, Clark RE, Schwartz M. Impact of internal mammary artery conduits on operative mortality in coronary revascularization. Ann Thorac Surg 1994;57:27–32.[Abstract]
- Oh BH, Volpini M, Kambayashi M, et al. Myocardial function and transmural blood flow during coronary venous retroperfusion in pigs. Circulation 1992;86:1265–79.[Abstract/Free Full Text]
- Martinez-Leon J, Carbonell-Canti C, Ortega-Serrano J. Myocardial protection by retrograde cardioplegic perfusion in the presence of acute coronary artery obstruction. An experimental study. Scand J Thorac Cardiovasc Surg 1992;26:207–12.[Medline]
- Hochberg MS, Austen WG. Selective retrograde coronary venous perfusion. Ann Thorac Surg 1980;29:578–88.[Abstract]
- O'Byrne GT, Nienaber CA, Miyazaki A, et al. Positron emission tomography demonstrates that coronary sinus retroperfusion can restore regional myocardial perfusion and preserve metabolism. J Am Coll Cardiol 1991;18:257–70.[Abstract]
- Kar S, Nordlander R. Coronary veins: an alternative route to ischemic myocardium. Heart Lung 1992;21:148–57.[Medline]
- Barnett JC, Freedman RJ, Touchon RC, Mesner MR. Coronary venous retroperfusion of arterial blood for the treatment of acute myocardial ischemia. Cathet Cardiovasc Diagn 1993;28:206–13.[Medline]
- Gore JM, Weiner BH, Benotti JR, et al. Preliminary experience with synchronized coronary sinus retroperfusion in humans. Circulation 1986;74:381–8.[Abstract/Free Full Text]
- Beatt KJ, Serruys PW, de Feyter P, van den Brand M, Verdouw PD, Hugenholtz PG. Haemodynamic observations during percutaneous transluminal coronary angioplasty in the presence of synchronized diastolic coronary sinus retroperfusion. Br Heart J 1988;59:159–67.[Abstract/Free Full Text]
This article has been cited by other articles:
|
|
|
|
 
J. O. Solem, D. Boumzebra, J. Al-Buraiki, S. Nakeeb, W. Rafeh, and Z. Al-Halees
Evaluation of a new device for quick sutureless coronary artery anastomosis in surviving sheep
Eur. J. Cardiothorac. Surg.,
March 1, 2000;
17(3):
312 - 318.
[Abstract]
[Full Text]
[PDF]
|
|
|
Top
Abstract
Introduction
