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Ann Thorac Surg 1995;60:275-282
© 1995 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Complete Atrioventricular Cardiac Transplantation: Improved Performance Compared With the Standard Technique

Department of General and Cardiothoracic Surgery, Duke University Medical Center, Durham, North Carolina

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. There has been renewed clinical interest in an alternative technique to orthotopic cardiac transplantation involving six anastomoses: left pulmonary veins, right pulmonary veins, inferior vena cava, pulmonary artery, aorta, and superior vena cava (complete technique). In this study, the results of the complete technique are compared with those of the standard operation (ventricular transplantation with atrioplasty).

Methods. Dogs were used for ten acute standard and ten acute complete atrioventricular transplantations. There were no significant differences in the baseline cardiac function (preload-independent right and left ventricular recruitable stroke work), bypass times, and cardiac ischemic times between the two groups.

Results. After transplantation, sinus rhythm was preserved after all ten complete and after only one standard transplantation but no significant hemodynamic differences were observed. The right and left ventricular preload-independent recruitable stroke work in the complete group and the left ventricular preload-independent recruitable stroke work in the standard group were conserved after transplantation, but the right ventricular preload-independent recruitable stroke work decreased by 39% ± 8% (p < 0.05) in the standard group. There was also a significant decrease in the rate of biventricular filling in the standard group after transplantation.

Conclusions. Complete atrioventricular transplantation is a feasible alternative technique and conserves normal sinus rhythm. The ischemic and bypass times are comparable for both methods. The insignificant change in the rate of biventricular filling in the dogs undergoing the complete technique indicates right and left ventricular diastolic function may be conserved after transplantation.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
See also page 282.

There has been renewed clinical interest in an alternative technique to orthotopic cardiac transplantation involving six anastomoses performed in the following order: left pulmonary veins, right pulmonary veins, inferior vena cava, pulmonary artery, ascending aorta, and superior vena cava. The standard technique, ventricular transplantation and atrioplasty, was introduced by Lower and Shumway in 1960 [1] and now has been used in more than 25,000 operations worldwide. Persistent problems associated with the standard technique include atrioventricular insufficiency, suture line thrombus and embolization, and impaired diastolic function, which may be related to distortion of the right and left atria, long anastomotic atrial suture lines, and discordant beating atria [2–4]. Limited clinical trials comparing these operations have demonstrated only minimal hemodynamic advantages to the complete technique during volume loading and exercise [5, 6]. However, transplant recipients constitute a very heterogeneous patient population, and to establish any differences between the two techniques, a large number of study subjects and the use of sophisticated analyzing tools are required. Furthermore, comparison of the two techniques also requires a detailed assessment of atrial function in combination with atrioventricular synchrony, as the primary difference between the two techniques lies at the level of atrial connection.

Therefore this study was designed to evaluate hemodynamic variables, atrial function, and biventricular performance in an experimental canine model of orthotopic complete atrioventricular and standard cardiac transplantation using objective analysis and load-insensitive measurements.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Anesthesia and Monitoring
In an acute experiment 40 adult mongrel dogs weighing 24 to 29 kg were used to study and compare biventricular cardiac function and hemodynamic variables in the settings of ten orthotopic complete atrioventricular transplantations (mean dog weight, 25.6 ± 0.5 kg) and ten orthotopic standard heart transplantations involving ventricular transplantation and atrioplasty (mean dog weight, 26.6 ± 0.6 kg). The animals were anesthetized with 5 mg/kg of intravenously administered thiopental sodium (Gensia Laboratories, Irvine, CA) and 20 mg/kg of intramuscularly administered ketamine sodium (Fort Dodge Laboratories, Fort Dodge, IA). Each animal received 1.5 mg/kg of intravenously administered gentamicin sulfate (Elkins-Sinn, Cherry Hill, NJ) and 900,000 units of penicillin G benzathine and penicillin G procaine (Fort Dodge Laboratories). All animals were intubated with a 9F endotracheal tube and mechanically ventilated with a Bear 1 ventilator (Inter Med, Bear Medical Systems, Riverside, CA). The tidal volume was set at 15 mL/kg, the fraction of inspired oxygen at 100%, and the positive end-expiratory pressure at 3 cm H₂O, and the rate-controlled ventilation mode was adjusted to maintain an arterial partial CO₂ pressure between 30 and 40 mm Hg. The arterial pH, partial O₂ and CO₂ pressures, O₂ saturation, hematocrit, and potassium levels were measured (Gem-Stat; Mallinckrodt Sensor Systems, Ann Arbor, MI) at 30-minute intervals as well as 15 minutes after any ventilator setting changes were made or medications administered. Blood samples were drawn from an external iliac artery pressure catheter (Gould, Oxnard, CA). An esophageal temperature probe was placed, and the body temperature of the donor was maintained between 36° and 37°C throughout the experiments by the application of heating pads, blankets, and heated humidified inspiration gas. Electrocardiographic monitoring was performed using three standard limb electrodes.

Assessment of Donor and Recipient Cardiac Function
A standard median sternotomy and an anterior pericardiotomy were performed to expose the heart. A transonic flowmeter (T208X; Transonic Systems, Ithaca, NY) was placed around the pulmonary trunk to measure right ventricular output. Hemispheric ultrasonic dimension transducers (1.5-mm outer diameter, No. 1-1015-5A; Vernitron, Bedford, OH) were positioned across the base–apex major axis, the anteroposterior minor-axis diameter of the left ventricle, and the septal free wall–minor axis diameters of both the left and right ventricles to measure the left and right ventricular cavitary volumes. Pressure-sensitive catheters (MPC-500; Millar Instruments, Houston, TX) were placed into the left and right ventricles, left atrium, and pulmonary artery for continuous recording of the right and left ventricular pressures, including the end-diastolic ventricular pressures, left atrial pressure, and pulmonary artery pressure. The dynamic right ventricular volume was measured using the ellipsoidal shell subtraction method [7]. The relationship of the left and right ventricular end-systolic pressure to the volume as well as that of stroke work to end-diastolic volume (as measured by the end-diastolic segment length or chamber volume) was then evaluated. The relationship between stroke work and either the end-diastolic segment length or chamber volume was quantified by the highly linear relationship of the slope and X-intercept during vena caval occlusion [8]. The slope (preload-independent recruitable stroke work [PRSW]) and X-intercept (volume) of these linear regressions represent load-independent indices of left and right ventricular systolic function and myocardial contractility. Left and right ventricular filling pressures were measured directly at end-diastole after the a wave and were termed the right and left ventricular end-diastolic pressure, respectively. Systemic and pulmonary vascular resistances were calculated by standard formulas applying mean pulmonary and aortic pressures, cardiac output, as well as end-diastolic left and right ventricular pressures. Intraoperative echocardiography of the donor heart was performed before and after transplantation to evaluate the left ventricular wall diameter and to estimate wall volume.

Data Acquisition and Analysis
Data were collected at baseline in every donor animal as well as 60 minutes after cardiac transplantation and at the termination of cardiopulmonary bypass (CPB). At each data point, files of 500 Hz (steady-state data, 6 seconds each) and files of 200 Hz (caval occlusion, 16 seconds each) were taken. These data were acquired over a period of 30 minutes with the ventilator disconnected during the acquisition of each file. Functional and hemodynamic data were digitized on-line, collected, and stored on a microprocessor (PDP 11/23; Digital Equipment, Maynard, MA). Pressure data and cardiac output were analyzed with software developed in our laboratory, and this method is described elsewhere [8]. Briefly, all data were digitized at 500 Hz and filtered by a 50-Hz low-pass filter, stored on magnetic media, and analyzed on a Zenith Z-386/20 (Zenith Data Systems, St. Joseph, MI).

Atrial Systole and Diastolic Filling
Data files of 500 Hz (steady-state data, 6 seconds each) were recorded for the analysis of atrial function and its contribution to right and left ventricular loading using volume and pressure channels and their derivatives, dV/dt and dP/dt. The period of atrial systole was then defined as starting at 0 mm Hg/s for the left atrium before the rise in pressure in atrial systole and finishing at end-diastole 20 ms before the maximum left ventricular dP/dt. The duration of atrial systole was also calculated as a percentage of the cardiac cycle to prevent the use of data from animals in first-degree heart block. Left and right ventricular volumes were analyzed for baseline and maximum values and for the rate of intraventricular volume increase. The effects of atrial pacing on atrial function and ventricular filling were evaluated postoperatively by overpacing the hearts of the complete transplantation group with a higher atrial rate.

Donor Management
All cardiac donors in the two groups were treated in an identical manner and the transplantation technique alternated with each experiment. The heavier animal of the pair was used as the recipient. The technique of explantation was identical in both groups. The micromanometers and flow probes were removed after data collection, and the ultrasonic dimension transducers were left attached to the epicardium but disconnected from the sonomicrometer and protected from immersion. The animals were fully anticoagulated with a systemic injection of 350 IU/kg of heparin (Elkins-Sinn). The inferior vena cava was ligated distally at its site of emergence from the diaphragm, followed promptly by cross-clamping of the ascending aorta at the origin of the brachiocephalic artery. One liter of St. Thomas' cardioplegia (Plegisol; Abbott Laboratories, North Chicago, IL) at 4°C was infused into the aortic root through a 16-gauge cannula, and the heart was vented by incising the superior vena cava and right pulmonary veins distally. Topical normal saline solution at 4°C was applied to immerse the surface of the heart. The superior and inferior venae cavae were transected as distally as possible, and the ascending aorta was transected just proximal to the aortic cross-clamp. The left and right pulmonary veins were transected at their pleural aspects outside the pericardium. The heart was then stored in 4°C normal saline solution.

Preparation of the Recipient
Each recipient received triple immunosuppression therapy consisting of 10 mg/kg of orally administered cyclosporine (Sandoz Pharmaceutical, East Hannover, NJ), 2 mg/kg of orally administered azathioprine (Burroughs Welcome, Research Triangle Park, NC), and 25 mg/kg of intravenously administered methylprednisolone (Upjohn Company, Kalamazoo, MI) given 2 hours before transplantation. After anticoagulation with 350 IU/kg of heparin, a 16F arterial cannula was inserted into the femoral artery and venous drainage was performed by means of bicaval cannulation using a 28F cannula for the inferior vena cava and a right-angled 24F cannula for the superior vena cava, both inserted as distally as possible in preparation for CPB (Sarns 5000 heart-lung machine; Sarns, Ann Arbor, MI; and Cobe VPCML membrane oxygenator; Cobe Laboratories, Lakewood, CO). Once the animal was on CPB, the core temperature was reduced to 32°C before rewarming was initiated during anastomosis of the pulmonary artery. The flow rate was kept between 80 and 100 mL • kg^-1 • min^-1 and mean arterial pressure maintained between 60 and 70 mm Hg. Throughout CPB, the lungs were ventilated continuously to prevent atelectasis.

Complete Orthotopic Cardiac Transplantation Technique
A complete orthotopic cardiac transplantation technique was used, as described previously [9]. The superior and inferior venae cavae together with the ascending aorta and pulmonary artery were transected at their most proximal portion in the recipient. The anatomic characteristics of the pulmonary veins were delineated before the posterior wall of the left atrium was divided into two Carrel patches containing the left and right pulmonary veins. The pulmonary vein orifices in the donor heart were identified, and the left and right orifices were fashioned for anastomosis to the pulmonary veins (Fig 1). All the anastomoses were sutured using 4-0 Prolene suture (Ethicon, Somerville, NJ) in a continuous fashion and executed in the following order: left pulmonary veins, right pulmonary veins, inferior vena cava, pulmonary artery, aorta, and superior vena cava. The last anastomosis was performed after the removal of air from the heart and after release of the aortic cross-clamp.

View larger version (55K): [in this window] [in a new window]   Fig 1. . Preparation of the recipient's mediastinum for orthotopic cardiac transplantation. The main differences in the method of recipient heart explantation are displayed. In the standard technique of heart transplantation, biventricular transplantation with atrioplasty (Previous), two recipient atrial cuffs remain for the anastomosis with the left and right donor heart atria. On the right side (New) left and right pulmonary vein Carrel patches in the recipient are prepared for complete atrioventricular transplantation. This requires six anastomoses performed in the following order: left pulmonary veins, right pulmonary veins, inferior vena cava, pulmonary artery, aorta, and superior vena cava.

Experimental Approval and Animal Rights
The experimental setup and procedures conformed to the guidelines established by the American Physiological Society and the National Institute of Health (Guide for the Care and Use of Laboratory Animals, NIH Publication 85-23, revised 1985). The experiments were approved by the Duke University Institutional Animal Care and Use Committee (DUIACUC Assigned Registry #A477-93-10R3).

Statistical Analysis
Statistical analysis of data obtained before and after transplantation was performed on an IBM personal computer using commercially available software (Statistical Software Package; SAS Institute, Cary, NC). Two-tailed paired Student's t tests were used to compare baseline values with posttransplantation data in every group. Two-tailed unpaired Student's t tests were used to compare baseline and posttransplantation data between the two groups. Fisher's exact test was applied for the comparison of two relative frequencies. The Mantel-Haenszel ² test was used to evaluate the differences in nonparametric data between the groups. The results are expressed as the mean ± standard error of the mean. A difference was considered statistically significant at a p value of less than 0.05.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The hemodynamic data at baseline and after transplantation for the two experimental groups are summarized in Table 1. There were no significant differences between the two groups in terms of body weight, baseline hemodynamic data, and cardiac function. Each animal was weaned gradually from CPB while the left atrial and systemic pressures were monitored. Mean systemic pressures greater than 50 mm Hg in combination with a mean left atrial pressure of 5 to 12 mm Hg were acceptable. None of the animals received any inotropic support.

Right and Left Ventricular Function
Highly linear relationships (r > 0.92) were obtained between the calculated right and left ventricular volume and pressure-volume loops during transient vena caval occlusion. Baseline PRSW data for both the right and left ventricles did not differ significantly between the two experimental groups. There was no significant change in the left ventricular PRSW after transplantation compared with the baseline values in either group, nor were there any significant differences between the groups. The right ventricular PRSW decreased significantly by 39% ± 8% compared with the baseline value after transplantation in the standard group, but no significant posttransplantation change was observed in the complete group. Left and right ventricular posttransplantation cardiac function in the complete and standard groups is shown in Figures 2 and 3.

View larger version (12K): [in this window] [in a new window]   Fig 2. . Left ventricular preload-independent recruitable stroke work (PRSW) before and after complete orthotopic atrioventricular transplantation (Complete Technique) and biventricular transplantation and atrioplasty (Standard Technique). There were no significant changes before and after transplantation.

View larger version (12K): [in this window] [in a new window]   Fig 3. . Right ventricular preload-independent recruitable stroke work (PRSW) before and after complete orthotopic atrioventricular transplantation (Complete Technique) and biventricular transplantation and atrioplasty (Standard Technique). Right ventricular function decreased significantly by 39% after standard transplantation. No significant changes were observed in the dogs undergoing the complete technique.

No significant changes were observed in the systemic hemodynamic variables during pacing in the complete group when the same animals were atrially overpaced. There were insignificant changes in left and right ventricular filling and atrial systole as a result of atrial overpacing of the complete transplantation hearts, and the duration of atrial systole in the paced hearts remained constant compared with that in the hearts in normal sinus rhythm. There were no significant changes in left ventricular volume stemming from atrial pacing; however, right ventricular filling was significantly increased from 2.4 ± 0.5 to 6.2 ± 0.1 mL compared with that in the hearts in normal sinus rhythm. The right ventricular dV/dt increased by a factor of nearly two, from 40.9 ± 13.8 to 78.8 ± 27.6 mL/s, as a result of pacing. The changes during atrial pacing are summarized in Table 3.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
An alternative technique of orthotopic cardiac transplantation was introduced into clinical practice by Carpentier's group in 1989 [10], primarily as a result of persistent problems with the conventional technique of heart transplantation, including sinus node injury, enlarged atria with atrioventricular insufficiency, and altered hemodynamics function [2, 3]. Known as complete atrioventricular transplantation, this technique involves the performance of separate left and right pulmonary vein anastomoses as well as separate inferior and superior vena caval anastomoses, unlike the standard technique of Lower and Shumway [1] that involves ``bilateral atrioplasty and total ventricular transplantation.'' Refinements in cardiac graft protection and preservation and the development of more advanced surgical equipment allowed for the practical application of such a technique, which requires longer CPB and ischemic times than those required by the standard technique [11]. Had such technology been available 30 years ago, Lower and Shumway in 1960 might have proceeded with research of this complete technique, as it had already been described by Neptune and associates in 1953 [12] and by various other investigators thereafter [13, 14]. Instead Lower and Shumway found that the complete method of transplantation in experimental models involved prolonged cardiac ischemic times and led to associated cardiac dysfunction. They subsequently described a technique of biatrial atrioplasty and ventricular transplantation that took significantly less time to perform [15].

Surprisingly no experimental studies were performed before this new technique was introduced into clinical practice [6, 11]. Observations from the present study comparing these two techniques of orthotopic heart transplantation support the concept that complete atrioventricular transplantation is a feasible technique and does not require significantly prolonged CPB and total ischemic times when the superior vena cava is anastomosed last after release of the aortic cross-clamp [9]. The results of this experiment demonstrate that all hearts transplanted using the new technique maintained a stable sinus rhythm after the termination of CPB without the use of external pacing. All hearts in the standard group required atrial pacing because of bradycardic supraventricular rhythms, and sinus node recovery was only observed in 1 animal in this group at the end of the study. An increased ischemic time, which is the major determinant of sinus node function after orthotopic heart transplantation [16], cannot account for this observation because the ischemic times did not differ significantly between the transplantation groups. Presumably the sinus node was injured during operation in the animals undergoing the standard technique, although particular care was taken to avoid manipulations in the vicinity of the sinoatrial junction.

Direct measurement of blood flow and cavitary pressures using high-fidelity catheters and ultrasonic flowmeters revealed no significant hemodynamic advantages to the complete technique compared with the standard technique. Both experimental groups were homogeneous in respect to body weight, and there were no significant differences in the baseline hemodynamic variables measured. The posttransplantation systemic arterial pressure, left and right ventricular filling pressures, cardiac output, and systemic and pulmonary resistance did not differ significantly between the groups, although a trend toward improved hemodynamic function was observed in the complete group. No significant hemodynamic differences were noted either in a few clinical trials comparing the standard with the complete technique. However, in these trials only a small number of transplant recipients were studied, and they were very heterogeneous with respect to their underlying diseases and donor hearts [5, 6, 17]. Long-term follow-up experiments are required to evaluate and compare the respective long-term hemodynamic variables and diastolic function associated with the two transplantation techniques, thus allowing for a more thorough appraisal of the potential functional advantages and superiority of one of these techniques.

Cardiac function was assessed in the donor animal at baseline and after transplantation using the PRSW, which permits functional analysis of intrinsic myocardial performance of the left and right ventricles independent of the atria. In the standard group right ventricular PRSW was significantly decreased after transplantation compared with the baseline value. In addition, the right ventricular volume was significantly increased, and this is due to a distortion of the right ventricular free wall relative to the interventricular septum as shown by a significant increase in the septum-to–right ventricular free wall dimension assessed by the ultrasonic transducers. The altered right ventricular geometry after transplantation brought about by the standard technique is not caused by myocardial wall edema after reperfusion, as selective right ventricular free wall edema is unlikely. Furthermore, the echocardiographic evaluation of the left ventricular wall thickness and wall volume did not show any significant changes, and the septum-to–left ventricular wall dimension remained unchanged compared with the baseline dimension. Thus, in the standard group the right ventricular–intercept stroke work relationship was shifted to the right and end-diastolic volumes were increased after transplantation (see Table 2). In the complete group no significant changes in the dimension and X-intercept were found and there was no evidence of any distortion in the ventricular geometry or of functional loss. Echocardiographic analysis of cardiac transplant recipients in whom the standard technique was used showed enlarged right ventricular cavities and dilatation immediately postoperatively [18]. The distortion of the right ventricular geometry in combination with the frequently observed abnormal diastolic interventricular septal motion in dysfunctional right ventricles [19] may be attributable to the frequently observed atrioventricular insufficiency and regurgitation that occur after standard orthotopic heart transplantation [20].

There is a significant atrial contribution to cardiac performance in patients who undergo orthotopic heart transplantation [21], and both atrial contraction and intact atrioventricular synchrony enhance ventricular filling [22]. Thus, in this study atrial function and its contribution to ventricular filling were analyzed and the effects of atrial pacing on atrial contractility were determined. After complete atrioventricular transplantation, atrial function was preserved but left and right ventricular filling were not significantly reduced compared with the results in the animals that underwent standard transplantation, in which biventricular filling was significantly impaired. The rate of left and right ventricular filling was reduced in both groups after transplantation, but more significantly in the standard group. Left atrial contractility and relaxation were also significantly reduced in the standard group. The atrial contribution to left ventricular filling was maintained in the complete group. Atrial pacing had a significant effect on atrial contractility and ventricular loading after transplantation, as observed in the animals that underwent complete transplantation when arbitrarily overpaced. Posttransplantation atrial pacing in the complete group increased the rate of left and right ventricular filling and left atrial contractility to levels comparable to baseline values.

The sustained atrial contractility and maintained right ventricular function brought about by complete atrioventricular transplantation may lead to a larger role for the technique as a preferred method in select young patients and in particular those potential transplant recipients with end-stage cardiac disease and severely elevated pulmonary vascular resistance.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Supported in part by grant HL 09315-30 awarded by the National Institutes of Health.

We appreciate the expertise of George Quick, Laboratory Coordinator, and the expert technical assistance of Kurt A. Campbell.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Presented at the Thirty-first Annual Meeting of The Society of Thoracic Surgeons, Palm Springs, CA, Jan 30–Feb 1, 1995.

Address reprint requests to Dr Bittner, Duke University Medical Center, PO Box 3333, Durham, NC 27710.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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17. Bizouarn P, Treilhaud M, Portier D, Train M, Michaud JL. Right ventricular function after early total or standard orthotopic heart transplantation. Ann Thorac Surg 1994;57:183–7.[Abstract]
18. Bhatia S, Kirshenbaum J, Shemin R, Cohn L, Collins J. Time course of resolution of pulmonary hypertension and right ventricular remodeling after orthotopic cardiac transplantation. Circulation 1987;76:819–26.[Abstract/Free Full Text]
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This Article Abstract 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): Hartmuth B. Bittner Simon W. H. Kendall Edward P. Chen Robert D. Davis Peter Van Trigt, III Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bittner, H. B. Articles by Van Trigt, P. Search for Related Content PubMed PubMed Citation Articles by Bittner, H. B. Articles by Van Trigt, P., III Related Collections Related Article