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J Thorac Cardiovasc Surg 1996;111:556-566
© 1996 Mosby, Inc.
SURGERY FOR ACQUIRED HEART DISEASE |
Received for publication June 23, 1995 Accepted for publication Oct. 3, 1995. Address for reprints: Greg H. Ribakove, MD, 530 First Ave., Suite 6D, New York University Medical Center, New York, NY 10016.
Abstract
Thoracoscopic cardiac surgery is presently under intense investigation. This study examined the feasibility and efficacy of closed chest cardiopulmonary bypass and cardioplegic arrest in comparison with standard open chest methods in a dog model. The minimally invasive closed chest group (n = 6) underwent percutaneous cardiopulmonary bypass and cardiac venting, as well as antegrade cardioplegic arrest through use of a specially designed percutaneous endovascular aortic occluder and cardioplegic solution delivery system. The control group (n = 6) underwent standard sternotomy and conventional open chest cardiopulmonary bypass, aortic crossclamping, and antegrade cardioplegia. Ischemic arrest time was 1 hour in each group. Ventricular pressures and sonomicrometer segment lengths were recorded before bypass and at 30 and 60 minutes after bypass. Left ventricular function did not differ significantly between the two groups, as demonstrated by measurements of elastance and end-diastolic stroke work. Also, the preload recruitable work area was 69% and 60% of baseline at 30 and 60 minutes after bypass in the minimally invasive group versus 65% and 62% in the conventional control group (p = not significant); the stroke work end-diastolic length relationship was 78% and 71% of baseline in the minimally invasive group at these intervals versus 77% and 74% in the conventional control group (p = not significant). Myocardial temperatures were similar throughout bypass in the two groups, and ultrastructural examination of prebypass and postbypass biopsy specimens showed no differences between groups. These results demonstrate that minimally invasive cardiopulmonary bypass with cardioplegic arrest is as feasible, safe, and effective as conventional open chest cardiopulmonary bypass. Thus current technology may allow wider clinical application of closed chest cardiac surgery. (J THORAC CARDIOVASC SURG 1996;111:556-66)
Recent enthusiasm for minimally invasive surgery has been fueled by the success of laparoscopic and thoracoscopic techniques. These methods have allowed patients to undergo increasingly complex procedures without the pain and morbidity associated with standard open surgical techniques. The benefits of such an approach are obvious. Until recently, however, minimally invasive cardiac surgery has not been feasible, mainly because of limitations in percutaneous perfusion technology, limitations in operative exposure and suturing techniques with the closed chest approach, and lack of availability of a percutaneous myocardial protection system.
As early as 1962 Dennis and associates
1 described the use of left heart bypass without thoracotomy for surgical catastrophes that could not be addressed by other means. Others subsequently reported successful application of percutaneous cardiopulmonary support systems. 2-7 These previous methods, however, were developed primarily for use in emergency situations and for temporary cardiac support. Likewise, femoral vein–femoral artery cardiopulmonary bypass (CPB) has been in use for decades, and improved percutaneous perfusion systems recently have become available. Nevertheless, until now these systems have had limited appeal as a result of certain inherent disadvantages. For example, no minimally invasive system has yet been able to simultaneously provide effective CPB and cardioplegic arrest. In addition, ventricular decompression and venting have not been possible during percutaneous perfusion. Moreover, the feasibility of percutaneous cardioplegic arrest and myocardial protection has not been well established. If minimally invasive closed chest cardiac surgery is to develop, these issues need to be resolved.
The original percutaneous myocardial protection system was proposed and developed at Stanford University. Our laboratories recently have undertaken a series of studies to examine in an animal model the feasibility of closed chest cardiac surgical techniques. These include newly developed endovascular myocardial protection systems and thoracoscopic dissection and suture methods, applied in conjunction with conventional techniques, such as diathermy-assisted dissection and percutaneous femoral vein–femoral artery bypass. The two purposes of this study were (1) to determine if percutaneous minimally invasive CPB and cardioplegic arrest are feasible with newly available technology and (2) to compare the effectiveness of the minimally invasive approach with that of conventional methods.
Materials and methods
Study groups
Twelve heartworm-free mongrel dogs (25 to 30 kg) were divided into two groups. In the minimally invasive group (n = 6) CPB was established with an endovascular aortic clamp (Endoclamp device; Heartport, Inc., Redwood City, Calif.) used for aortic occlusion and endovascular delivery of cardioplegic solution and an endovascular pulmonary artery venting catheter (Heartport) for pulmonary artery venting. In the conventional group (n = 6) CPB was established by opening the chest and using a standard aortic crossclamp with antegrade delivery of cardioplegic solution into the aortic root via an aortic root catheter and a standard pulmonary artery vent. All animals were given humane care 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. 86-23, revised 1985).
Surgical preparation
In all animals anesthesia was initiated with a 4% solution of thiamylal (0.5 mg/kg) and maintained with metocurine iodide (0.5 mg/kg) and 
-chloralose (100 mg/kg) after endotracheal intubation. The animals were supported with a mechanical ventilator (Harvard Apparatus Co., Dover, Mass.) and their lungs were ventilated with 100% oxygen. All animals were monitored throughout the entire procedure with electrocardiography and measurement of carotid arterial pressure with a micromanometer (Koenigsberg Instruments Inc., Pasadena, Calif.), pulmonary artery and central venous pressures with a pulmonary artery catheter (Arrow International, Inc., Reading, Pa.), and oxygen saturation via an external pulse oximeter. Arterial blood gases and pH were kept in the normal range by adjusting inspired oxygen concentration and minute ventilation or by administering sodium bicarbonate. Electrolyte and hematocrit levels were also monitored at appropriate intervals throughout the procedure. No transfusions were given to either group.
Surgical technique
Minimally invasive CPB group
The technique of minimally invasive CPB was accomplished as shown in Fig. 1. A femoral venous catheter (17F cannula, model 58517, DLP, Inc., Grand Rapids, Mich.) was placed through a cutdown in the left femoral vein and guided by means of a fluoroscope (MCA 30, Ratheon, Tokyo, Japan) over a guide wire to a position just within the superior vena cava. A femoral arterial cannula (14F, model 57414, DLP) was placed into the left femoral artery. These catheters were connected to the bypass pump (Shiley S-100A Bubble Oxygenator, Shiley Inc., Irvine, Calif., and Pemco roller pump, model 5745, Pemco Inc., Cleveland, Ohio) in a standard fashion. Next, an endovascular pulmonary artery venting catheter (Heartport) was inserted into the external jugular vein and guided into position over a flow-directed pulmonary artery balloon catheter by means of fluoroscopy. The pulmonary artery venting catheter served the dual purpose of monitoring pulmonary artery pressure while in line with a pressure manometer or decompressing the left ventricle during CPB.
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CPB and delivery of cardioplegic solution
All animals underwent total CPB after systemic delivery of heparin (100 U/kg). They were cooled to a temperature of 28° C and subjected to CPB at flow rates of approximately 100 ml/kg per minute. Arterial oxygen tension was maintained at greater than 70 mm Hg, and the mean arterial pressure during CPB was maintained at greater than 60 mm Hg by adjusting CPB flow. Venous return was aided in both groups by attachment of the venous return cannula to a centrifugal pump (Bio-pump, Medtronic Bio-Medicus, Eden Prairie, Minn.). The ascending aorta was occluded with a vascular clamp or by inflation of the balloon of the Endoclamp device. Multiple doses of cardioplegic solution were given antegradely either through the distal end of the Endoclamp device or through the aortic root catheter. Both groups received Freme's cardioplegic solution, 8 and oxygenated blood cardioplegic solution was cooled to 6° C in a BCD Plus Heat Exchanger (Shiley). A high potassium dose of 20 ml/kg (20 to 24 mEq/L final concentration) was given initially to arrest the heart, followed by a potassium mixture of 10 ml/kg (8 to 12 mEq/L final concentration) given at 15-minute intervals. All doses were given at a rate of 75 ml/min with blood mixed with cardioplegic solution in a ratio of four to one. The hematocrit value during CPB remained above 25% in all cases. The pulmonary artery and the aortic root were vented throughout CPB and drained into the oxygenator reservoir. After 1 hour of CPB, the blood temperature was warmed to more than 35° C and the aorta was unclamped. If necessary, the heart was defibrillated. The heart was then allowed to rewarm to 37° C. Data acquisition was continued for 60 minutes after the completion of CPB.
Measurement of left ventricular segment length and pressure
Instantaneous myocardial segment dimensions were measured with subepicardial pulse-transit ultrasonic dimension transducers (model CY5; Triton Technology, Inc., San Diego, Calif.). They were placed in the epicardium, via a stab incision, 5 cm apart along the left ventricle, midway between the base and apex. The piezoelectric crystals were then connected to an oscilloscope and sonomicrometer (model 100; Triton Technology) for calibration and recording of analog output.
Ventricular pressures were recorded continuously with micromanometers (models MPC-500 and SPC-450; Millar Instruments, Inc., Houston, Tex.) placed into the apices via stab incisions. All micromanometers were calibrated over a similar range and then allowed to equilibrate to 37° C. The sinus node was crushed with a clamp, and the right atrium was electronically paced (Medtronic, Inc., Minneapolis, Minn.) at a constant rate of 150 beats/min.
Myocardial contractile data acquisition and analysis
Ventricular pressure and myocardial segment dimensions were measured just before CPB (pre-CPB), 30 minutes after the completion of CPB, and 60 minutes after the completion of CPB. Five sets of data were acquired during each measurement. Each set of data acquisition lasted 30 seconds and was recorded over a range of left ventricular end-diastolic volumes produced by transient (10 seconds) bicaval occlusions. The method for measuring cardiac function was based on algorithms developed by other investigators. 9-13 The indexes of regional left ventricular systolic contractile function calculated were the slope of the end-diastolic pressure–length relationship (Mw), the x-intercept of the end-diastolic pressure–length relationship (Lw), the preload recruitable work area, the stroke work–end-diastolic length relationship, and maximal regional elastance (Emax).
Ventricular temperature measurements
Myocardial thermistors were placed into the right and left ventricular free walls and attached to a digital thermometer (Shiley). Temperature readings were made just before CPB, at 5-minute intervals throughout CPB, and after the completion of CPB. Blood temperature and cardioplegic solution temperature were also measured in series with the CPB circuit (YSI series 500; Yellow Springs Instrument Company, Yellow Springs, Ohio).
Ultrastructural and histologic examination
Ultrastructural examination was performed on transmural needle biopsy specimens taken from the apex of each ventricle before CPB and at 30 and 60 minutes after completion of CPB. Most specimens were embedded in paraffin, stained with hematoxylin and eosin, and examined with a high-power light microscope. Representative specimens were also prepared for examination by transmission electron microscopy by being rapidly immersed in fresh, cold 3% glutaraldehyde in Sorensen's phosphate buffer (0.1 mol/L, pH 7.3) for 24 hours. The specimens were then fixed in 1% osmium tetroxide, dehydrated in acetone, and embedded in Epon fixative. "Green" sections 0.5 to 1 µm thick were cut, stained with a polychrome stain, and examined by light microscopy for orientation purposes. Corresponding thin sections were cut with an LKB Ultratome III knife (LKB Instruments, Inc., Rockville, Md.), mounted on copper-coated grids, stained with uranyl acetate and lead acetate, and then examined with a Siemens transmission electron microscope (Siemens Medical Corp., Iselin, N.Y.). Specimens were qualitatively evaluated for myocyte necrosis, intercellular or intracellular edema, mitochondrial and myofilament abnormalities, cell membrane disruption, and microvascular damage.
Statistical methods
Data were analyzed by the SPSS for Windows statistical software program (SPSS, Inc., Chicago, Ill.). All results are expressed as the mean ± standard deviation. The statistical significance of changes in load-independent indexes of ventricular function were compared by repeated- measures analysis of variance. Significance was determined at the level of 5% or less.
Results
Regional myocardial contractile function
When the instantaneous left ventricular intracavitary pressure was plotted against the regional left ventricular segment length, pressure- length work loops resulted (Fig. 3). At baseline before the institution of CPB, regional myocardial function did not differ in the minimally invasive versus conventional groups. There were no significant differences in the slopes (143.2 ± 12.9 vs 131.3 ± 21.9 erg x cm-1 x 103) or the x-intercepts (4.8 ± 1.0 vs 4.3 ± 0.7 cm) (p = NS) (Table I). The mean linear correlation coefficient for the end-diastolic pressure–segment length relationship before and after CPB was 96%. There were no significant changes with respect to between- subject effects in the x-intercept at both 30 and 60 minutes after the completion of CPB (Fig. 4). There were also no significant changes in the slope after the completion of CPB (Fig. 5). The mean percentage standard deviations were 3% and 5% for the variables slope and x-intercept, respectively. Power analysis of our experimental protocol revealed that with a power of 80% and a two-tailed t test at the level of 5%, we were able to detect a difference between treatment groups if the percentage difference between the groups was more than 5% for x- intercept and more than 8% for slope. 14
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(Table I, Fig. 6) or stroke work–end-diastolic length relationships (Fig. 7) at 30 and 60 minutes. The mean linear correlation coefficient for the end-systolic pressure–segment length relationship before and after CPB was 95% in both groups. Emax remained relatively constant throughout the experiment (Table I, Fig. 8). The mean changes in Emax after CPB at 30 and 60 minutes were not statistically significant.
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Myocardial temperature
The right and left ventricular temperatures before, during, and after CPB are depicted in Fig. 9. The mean myocardial pre-CPB temperatures for the minimally invasive and conventional groups were 36.0° ± 0.8° and 36.5° ± 0.5° C, respectively. During CPB the heart was cooled in the minimally invasive and conventional groups to a mean temperature of 17.5° ± 1.4° C and 17.3° ± 1.0° C, respectively. With regard to isolated cooling of the left ventricle in the minimally invasive and conventional groups during CPB, the average temperatures were 17.2° ± 1.2° and 17.5° ± 1.5° C, respectively. The right ventricle was cooled to mean temperatures of 17.3° ± 1.0° C and 17.5° ± 1.4° C, respectively, in the two groups. At the conclusion of aortic crossclamping, the myocardium was rewarmed in the minimally invasive and conventional groups to 31.9° ± 5.5° C and 33.1° ± 1.3° C, respectively (p = not significant). The blood temperatures were all above 35° C in both groups.
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A key point in assessing the efficacy of any new CPB–myocardial protection technique is to determine the technique's potential for minimizing myocardial damage during aortic crossclamping and for promoting the recovery of myocardial performance after reperfusion. In this experiment, all measurements of regional myocardial performance, including the slope and x-intercept of the stroke work versus end-diastolic relationship, the preload recruitable work area, the stroke work–end-diastolic length relationship, and the Emax were equivalent in the minimally invasive group and the conventional open myocardial protection group. In addition, the mean percentage standard deviation for each parameter was low with the exception of Emax. Despite the small number of subjects in each group, we were able to compare the treatment groups with respect to the end-diastolic relationships to determine if a difference had occurred. 14 This was possible because of the low percentage standard deviations observed in each group. However, the variability in Emax could have resulted either from magnification of measurement error or, more likely, from the true minute-to-minute variation in cardiac performance.
With the exception of Emax, all of the contractile performance indexes measured are relatively independent of preload and afterload and are extremely sensitive to ischemia. 12 Glower and coworkers 10 previously described the variable sensitivity of Emax to ischemia and have attributed it to a reversible phenomenon called diastolic creep. Some of the variability noted in Emax in these experiments may be a creep effect.
A potential limitation of the methods used in the experiment is that measuring dynamic ventricular dimensions rather than volume assumes that regional ventricular hydrodynamic performance accurately reflects global performance. This assumption appears valid because of the consistent correlation between segment length and stroke volume and between regional and global stroke work reported by others. 13
An important goal of this study was to determine if percutaneous endovascular delivery of cardioplegic solution could cool the myocardium as well as standard open antegrade delivery of cardioplegic solution. The results showed equivalent mean temperatures (approximately 17° C) in each group during CPB. This level of hypothermia was achieved despite the absence of topical cooling in these experiments. In addition, the ability to bathe the heart in cool saline solution should be technically feasible in the minimally invasive group. Effective decompression of the heart by the endovascular aortic catheter technique and endovascular pulmonary artery vent proved to be clearly possible. This ability to unload 15 and decompress the heart is thought to be essential for adequate myocardial protection.
The technique of minimally invasive CPB used in this study is based on an innovative percutaneous vascular access device (the Endoclamp device) that provides for endovascular aortic occlusion, delivery of cardioplegic solution, and left ventricular decompression. The Endoclamp device is a triple-lumen catheter with an inflatable balloon at its distal end. Proper positioning of the balloon is paramount because improper placement can result in aortic valve incompetence and left ventricular distention, unequal distribution of cardioplegic solution, occlusion of the major head vessels, or an inability to adequately arrest the heart. In this study proper positioning of the balloon proved to be easily achievable by means of fluoroscopic guidance, and positioning in human beings should be easier because the ascending aorta is longer in the human being than in the dog, as has been confirmed independently in human cadaver studies. Cardioplegic solution is delivered in an antegrade fashion through a central lumen that communicates with the tip. This lumen also acts to vent the aortic root after delivery of the cardioplegic solution. A second lumen is used to monitor aortic root pressure. The third lumen is used for inflation of the balloon. The pulmonary artery venting catheter is percutaneously placed through the external jugular vein and passed into the pulmonary artery, so that the heart is vented to achieve ventricular decompression.
Use of this system in combination with percutaneous CPB perfusion allowed the hearts in these experiments to be easily arrested, cooled, and vented. The overall results demonstrate that the Endoclamp device in association with the endovascular pulmonary artery venting catheter was able to provide complete aortic occlusion, adequate cardioplegic delivery with prompt heart arrest, adequate myocardial cooling, and excellent myocardial functional recovery to an extent equivalent to that of conventional techniques.
The findings of this study demonstrate that minimally invasive CPB and endovascular cardioplegic arrest are technically feasible and effective. The technique provides myocardial protection equivalent to that obtained with open methods. The implications of these findings are significant, because effective closed chest techniques for myocardial protection are necessary if minimally invasive cardiac surgery is to become a clinical reality. The minimally invasive endovascular myocardial protection system studied here provides the foundation for development of routine methods for accomplishing many types of cardiac operations without median sternotomy or thoracotomy.
Acknowledgments
We would like to thank Manasse Decady, Francisco Rivera, and Eleones Anglade for their expert technical assistance.
Footnotes
From the Department of surgery, Division of Cardiothoracic Surgery,a New York University Medical Center, New York, N.Y., and the Departments of Cardiothoracic Surgery,b Anesthesia,c and Medicine,d Stanford University School of Medicine, Palo Alto, Calif. 
Funded in part by a grant from Heartport, Inc., Redwood City, Calif.
References
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G. Soulez, M. Gagner, E. Therasse, F. Basile, I. Prieto, P. Pibarot, C. Laflamme, L. Lamarre, and H. Shennib Catheter-Assisted Totally Thoracoscopic Coronary Artery Bypass Grafting: A Feasibility Study Ann. Thorac. Surg., October 1, 1997; 64(4): 1036 - 1040. [Abstract] [Full Text]
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A. Lange, M. Walayat, C. M Turnbull, P. Palka, P. Mankad, G. R Sutherland, and M. J Godman Assessment of atrial septal defect morphology by transthoracic three dimensional echocardiography using standard grey scale and Doppler myocardial imaging techniques: comparison with magnetic resonance imaging and intraoperative findings Heart, October 1, 1997; 78(4): 382 - 389. [Abstract] [Full Text] [PDF]
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H. E. Garrett Jr, J. C. Gilmore, G. A. Lowdermilk, and D. McCoy Complete Direct Mammary Harvest for Minimally Invasive Coronary Artery Bypass Ann. Thorac. Surg., September 1, 1997; 64(3): 864 - 866. [Abstract] [Full Text]
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L. C. Siegel, F. G. St. Goar, J. H. Stevens, M. F. Pompili, T. A. Burdon, B. A. Reitz, and W. S. Peters Monitoring Considerations for Port-Access Cardiac Surgery Circulation, July 15, 1997; 96(2): 562 - 568. [Abstract] [Full Text]
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D. S. Schwartz, G. H. Ribakove, E. A. Grossi, J. D. Schwartz, P. M. Buttenheim, F. G. Baumann, S. B. Colvin, and A. C. Galloway SINGLE AND MULTIVESSEL PORT-ACCESS CORONARY ARTERY BYPASS GRAFTING WITH CARDIOPLEGIC ARREST: TECHNIQUE AND REPRODUCIBILITY J. Thorac. Cardiovasc. Surg., July 1, 1997; 114(1): 46 - 52. [Abstract] [Full Text]
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H. Shennib, M. J. Mack, and A. G. L. Lee A Survey on Minimally Invasive Coronary Artery Bypass Grafting Ann. Thorac. Surg., July 1, 1997; 64(1): 110 - 114. [Abstract] [Full Text]
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W. S. Peters, L. C. Siegel, J. H. Stevens, F. G. St. Goar, M. F. Pompili, and T. A. Burdon Closed-Chest Cardiopulmonary Bypass and Cardioplegia: Basis for Less Invasive Cardiac Surgery Ann. Thorac. Surg., June 1, 1997; 63(6): 1748 - 1754. [Abstract] [Full Text]
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D. S. Schwartz, G. H. Ribakove, E. A. Grossi, P. M. Buttenheim, J. D. Schwartz, R. M. Applebaum, I. Kronzon, F. G. Baumann, S. B. Colvin, and A. C. Galloway MINIMALLY INVASIVE MITRAL VALVE REPLACEMENT: PORT-ACCESS TECHNIQUE, FEASIBILITY, AND MYOCARDIAL FUNCTIONAL PRESERVATION J. Thorac. Cardiovasc. Surg., June 1, 1997; 113(6): 1022 - 1031. [Abstract] [Full Text]
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 A. Diegeler, V. Falk, T. Walther, and F. W. Mohr Minimally Invasive Coronary-Artery Bypass Surgery without Extracorporeal Circulation N. Engl. J. Med., May 15, 1997; 336(20): 1454 - 1454. [Full Text]
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W. R. Chitwood Jr, J. R. Elbeery, and J. F. Moran Minimally Invasive Mitral Valve Repair Using Transthoracic Aortic Occlusion Ann. Thorac. Surg., May 1, 1997; 63(5): 1477 - 1479. [Abstract] [Full Text]
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P. J. Lin, C.-H. Chang, J.-J. Chu, H.-P. Liu, F.-C. Tsai, F.-C. Lin, C.-W. Chiang, M.-W. Yang, and P. P. C. Tan Video-Assisted Coronary Artery Bypass Grafting During Hypothermic Fibrillatory Arrest Ann. Thorac. Surg., April 1, 1997; 63(4): 1113 - 1117. [Abstract] [Full Text]
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J. M Toomasian, W. S Peters, L. C Siegel, and J. H Stevens Extracorporeal circulation for port-access cardiac surgery Perfusion, March 1, 1997; 12(2): 83 - 91. [Abstract] [PDF]
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W. R. Chitwood Jr., J. R. Elbeery, W. H. H. Chapman, J. M. Moran, R. L. Lust, W. A. Wooden, and D. H. Deaton VIDEO-ASSISTED MINIMALLY INVASIVE MITRAL VALVE SURGERY: THE "MICRO-MITRAL" OPERATION J. Thorac. Cardiovasc. Surg., February 1, 1997; 113(2): 413 - 414. [Full Text]
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M. F. Pompili, J. H. Stevens, T. A. Burdon, L. C. Siegel, W. S. Peters, G. H. Ribakove, and B. A. Reitz PORT-ACCESS MITRAL VALVE REPLACEMENT IN DOGS J. Thorac. Cardiovasc. Surg., November 1, 1996; 112(5): 1268 - 1274. [Abstract] [Full Text]
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S. Westaby and F. J. Benetti Less Invasive Coronary Surgery: Consensus From the Oxford Meeting Ann. Thorac. Surg., September 1, 1996; 62(3): 924 - 931. [Full Text]
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