Ann Thorac Surg 1997;63:676-682
© 1997 The Society of Thoracic Surgeons
Original Article: Cardiovascular
Configuration of Linear Dynamic Cardiomyoplasty for Hypoplastic Right Ventricle
Kiyozo Morita, MD,
Hiromi Kurosawa, MD,
Shinichi Ishii, MD,
Michio Yoshitake, MD,
Makoto Hanai, MD
Department of Cardiovascular Surgery, Jikei University School of Medicine, Tokyo, Japan
Accepted for publication October 4, 1996.
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Abstract
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Background. The purpose of this study is to determine feasibility of linear dynamic cardiomyoplasty with a briefly preconditioned latissimus dorsi in the experimental model simulating patch enlargement of the hypoplastic right ventricle.
Methods. In 8 mongrel dogs, a diminished right ventricular chamber was reconstructed with an extended pericardial patch. A left latissimus dorsi, preconditioned for 2 weeks (2 Hz) after a previous 2-week vascular delay period, was placed on the patch, with the muscle fiber oriented in parallel to the right ventricular long axis.
Results. Graft pacing with trained-pulses of 25 Hz at a 1:1 ratio showed significant augmentation of pulmonary flow and pressure (158% ± 21%, 156% ± 14%, respectively), contributing to restoring right ventricular function comparable with preoperative control, which was also confirmed by the right ventricular function curve and pressure–volume relationship analyzes. Continuous pacing was performed in 4 animals for 7 hours without evidence of muscle fatigue, implying feasibility of "working conditioning" after minimum preconditioning for this type of right heart assist.
Conclusions. Linear latissimus dorsi myoplasty can restore normal right ventricular performance at a physiologic preload, and may provide a surgical option for the hypoplastic right ventricle.
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Introduction
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Dynamic cardiomyoplasty (DCMP) is currently undergoing worldwide clinical trial almost exclusively for left heart assistance in patients with cardiomyopathy [1–3].
Although there have been several experimental investigations [4–8] to extend the concept of DCMP or skeletal muscle ventricles to right ventricular (RV) assistance, clinically feasible approaches of DCMP to treat congenital heart diseases have not yet been established. Our research is, therefore, tracking toward development of new operative techniques of RV DCMP in the reparative operation for congenital heart diseases and establishment of the concept of minimum muscle preconditioning protocol followed by subsequent "working conditioning," specialized for the right heart assistance by the skeletal muscles. The purpose of the present study is to determine feasibility of linear dynamic cardiomyoplasty with a briefly preconditioned latissimus dorsi (LD) in the setting of an experimental model of patch enlargement of RV cavity after resection of the entire free wall and diminishing RV cavity to obtain a possible proxy for hypoplastic RV. The configuration was designed with the LD muscle fiber orientation in parallel to the RV long axis to use linear contraction of the entire muscle flap for compression of a patch-enlarged RV chamber and traction of the diaphragmatic surface of RV toward the outflow tract.
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Material and Methods
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Electrical Preconditioning
All animals received 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 86-23, revised 1985).
Eight adult mongrel dogs weighing between 8 and 13 kg were anesthetized with intravenous sodium thiopental (25 mg/kg) and intubated. A pair of intramuscular leads was inserted into a left LD muscle after dividing all collateral vessels to the muscle and the leads were connected to a conventional cardiac stimulator (Pacesetter Bilog VII 2050L; Solna, Sweden). After a period of 2 weeks of vascular delay, electrical stimulation was initiated 2 weeks after the operation with 2-Hz single pulses and was continued for 2 weeks. Preoperative and postoperative antibiotic prophylaxis (cefazolin sodium, 1 g daily) was administered.
Surgical Procedure
MODEL OF PATCH ENLARGEMENT OF HYPOPLASTIC RIGHT VENTRICLE.
The model is shown in Figure 1
. At the last experiment, anesthesia was induced with thiopental and maintained with isoflurane (1% to 2%). A left LD was mobilized as a pedicle flap based on the thoracodorsal neurovascular bundle. Under cardiopulmonary bypass and cardioplegic arrest, the RV free wall was totally excised and the septal trabeculation, including a body of the trabeculoseptomarginalis, was resected as extensively as possible. The anteroinferior edge of the RV free wall was plicated to the septal muscular edge to diminish the RV cavity. Refixation of papillary muscle to the remnant of interventricular septum using horizontal mattress sutures with Teflon pledgets was often required to avoid tricuspid regurgitation. The defect was repaired with a large (approximately 200% of resected free wall area) elliptical patch of glutaraldehyde-preserved bovine pericardium, sutured to the edge of the myocardium with running 4-0 Prolene (Ethicon, Somerville, NJ) sutures. Before complete closure of the RV, horizontal mattress sutures of 2-0 Tevdek with Teflon pledgets were placed inside the RV cavity at the site of the right atrioventricular junction and diaphragmatic surface to fix the LD flap later on. A sensing lead was placed on the left ventricular apex.
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Fig 1. . Diagrammatic representation of linear right ventricular ( RV) dynamic cardiomyoplasty in a setting of patch enlargement of hypoplastic RV. Under cardiopulmonary bypass, the diminished RV chamber through resection of the right ventricular free wall and plication was reconstructed with a large pericardial patch. A pedicled left latissimus dorsi (LD) was anchored to the third rib and placed onto the RV patch. The configuration was designed with the latissimus dorsi muscle fiber orientation parallel to the right ventricular long axis to use linear contraction of the latissimus dorsi.
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RIGHT VENTRICULAR CARDIOMYOPLASTY.
The muscle flap was passed into the left chest through a defect created by resection of the lateral arc of the second rib and the humeral tendon of the LD flap was sutured to the periosteum of the third rib. The LD flap, mainly its transverse segment, was positioned over the pericardial patch with the fibers oriented parallel to the long axis of the RV (from the diaphragmatic surface to the pulmonary trunk). The extremity of the flap was secured to the patch at the inferior right atrioventricular junction and the diaphragmatic surface, but not fixed at the superior border of the patch. The lateral segment of flap was fixed to the pericardium to the left so as to maintain sufficient tension on the muscle flap. This configuration allows the linear shortening of the LD fiber along the long axis of the RV, contributing to traction of the bottom of the RV toward the pulmonary trunk and sufficient compression of the RV chamber.
Experimental Model
A conductance catheter and a microtransducer-tipped catheter were placed into the RV apex; other pressure catheters were inserted into the right atrium, pulmonary artery, and the aorta. A transit time flowmeter (T101; Transonic Systems, Ithaca, NY) was placed around the pulmonary artery. After the termination of cardiopulmonary bypass, an external trained-pulse stimulator (SEC-2102; Nihon Koden, Tokyo, Japan) was used to provide R-wave synchronous graft stimulation. Stimulation parameters were a burst frequency of 10 to 66 Hz, an amplitude of 10 V, and a synchronization ratio of 1:1.
Evaluation
The pulmonary arterial pressure, central venous pressure (CVP), aortic pressure, electrocardiogram, and pulmonary flow were simultaneously recorded on a Fufuda-densi model eight-channel recorder system, and stroke volume and RV stroke work were calculated.
HEMODYNAMIC STUDY AND RIGHT VENTRICULAR FUNCTION.
The effects of graft stimulation on hemodynamic parameters with muscle stimulation at the varied stimulation parameters and preload (ie, CVP) were tested during repeated on and off tests. The RV function was evaluated preoperatively and postoperatively by the analysis of RV function curve, which is the relationship between CVP and RV stroke work during serial volume loading.
RIGHT VENTRICULAR PRESSURE-VOLUME RELATIONSHIP.
The RV performance with graft stimulation was tested by inscribing RV pressure–volume loops. An eight-electrode equipped conductance catheter (Webster Laboratories, Baldwin Park, CA) was inserted through the RV apex and connected to a Sigma-5-DF signal conditioner processor (Leycom, the Netherlands). Right ventricular pressure and conductance catheter signals were amplified and digitized to inscribe pressure–volume loops. After the procedure for correction of parallel conductance, a series of pressure–volume loops under variable loading conditions was generated by rapid transient occlusion of the inferior vena cava during a 7-second period of apnea with and without graft stimulation at 25 Hz. The end-systolic pressure volume relationship was analyzed by a user interactive program on a Macintosh computer, and the RV performance was described as the slope of linear regression (end-systolic elastance), as described previously [9].
ECHOCARDIOGRAPHIC STUDY.
The effect of graft stimulation (25 or 50 Hz) was evaluated by echocardiography and assessed by values of shortening fraction of the RV chamber at the site of the inlet portion. Hemodynamic evaluation including measurement of the RV pressure–volume relationships and echocardiographic study was accomplished in all 8 animals.
FUNCTIONAL DURABILITY.
After functional studies, the grafts were continuously driven with trained-pulse stimulation at 25 Hz, 10 V, 1:1 ratio in 4 animals and the on-off tests were repeated every hour to assess the percentage of augmentation in hemodynamic parameters.
Statistical Analysis
All data are expressed as mean ± standard deviation. Values of functional parameters before and after the graft stimulation were compared with paired t tests. Effects of graft stimulation on the hemodynamic parameters with varied stimulation variables were compared with one-factor repeated-measures analysis of variance (block design). Two-factor repeated-measures analysis of variance (block design) was used to analyze the RV function. Where significant F values were detected, Tukey's two-tailed tests of significance were used for multiple comparisons. Statistical significance was accepted at a p value of less than 0.05.
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Results
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Hemodynamics
No animal could be weaned from cardiopulmonary bypass when the RV cavity was repaired without patch enlargement because of insufficient RV cavity size. In the setting of RV patch enlargement, all 8 animals were weaned from cardiopulmonary bypass without graft stimulation, showing suboptimal cardiac output (maximum cardiac index, 56 ± 9 mL · min-1 · kg-1, at a CVP of 10 mm Hg). After stimulation at 10 V, a burst frequency of 25 Hz, a burst duration of 120 ms, and at a 1:1 synchronization, marked increases in the pulmonary arterial pressure and pulmonary flow resulted in the elevation of aortic pressure as shown in Figure 2. Changes in hemodynamic parameters in the 8 animals during graft stimulation at a CVP of 5 and 10 mm Hg are summarized in Table 1.
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Fig 2. . A typical tracing of pulmonary arterial pressure ( PAP), aortic pressure (AP), central venous pressure (CVP), and pulmonary flow (PA Flow) before and after graft stimulation (a burst frequency of 25 Hz, a burst duration of 120 ms, and the synchronization ratio of 1:1). (ECG = electrocardiogram.)
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Effects of stimulation variables on hemodynamic augmentation are depicted in Table 2. The increase in burst frequency from 15 to 66 Hz caused an increase in percent assistance in all hemodynamic parameters, where maximal augmentation of pulmonary flow, aortic pressure, and pulmonary arterial pressure reached 224%, 136%, and 188%, respectively.
RIGHT VENTRICULAR FUNCTION CURVE.
The relationships between CVP and RV stroke work before operation (control), after operation without graft stimulation (off), and with stimulation at a burst frequency of 25 Hz (on) are shown in Figure 3. Without graft stimulation, profound RV dysfunction was noted, whereas RV performance was markedly restored with graft stimulation, especially at the lower range of CVP.
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Fig 3. . Right ventricular function curves showing the relationships between central venous pressure ( CVP) and right ventricular stroke work (RVSW) before operation (CONTROL), after operation without graft stimulation (OFF), and with stimulation at a burst frequency of 25 Hz (ON).
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RIGHT VENTRICULAR PRESSURE–VOLUME RELATIONSHIPS.
Figure 4 depicts a typical recording of pressure–volume loops with and without graft stimulation at a steady state (Fig 4A) and the series of pressure–volume loops generated by rapid transient occlusion of the inferior vena cava with and without graft stimulation at 25 Hz (Fig 4B) was analyzed. End-systolic elastance, the slope of the end-systolic pressure volume relationship, and percentage of external work assessed by the area within the loop were significantly increased by graft stimulation at 25 and 50 Hz (Table 3).
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Fig 4. . Typical recordings of the right ventricular ( RV) pressure–volume loops (A) in a steady state during the on-off test and (B) during transient caval occlusion with and without graft stimulation. (RVP = right ventricular pressure.)
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Table 3. . Effects of Dynamic Cardiomyoplasty on Right Ventricular Function Assessed by Right Ventricular Pressure Volume Relationships Using the Conductance Method
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ECHOCARDIOGRAPHIC FINDINGS.
Without graft stimulation, the anterior wall of the RV chamber showed slightly dyskinetic motion, whereas graft contraction caused apparent compression of the RV chamber (Fig 5), resulting in a significant increase in fractional shortening from 12.5% ± 3.2% to 39.1% ± 9.2% (Table 4).
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Fig 5. . Echocardiographic findings: left ventricular long axial view (left) and M-mode tracings (right). ( ED = end-diastole; ES = end-systole; LDMF = latissimus dorsi muscle flap; LV = left ventricle; RV = right ventricle.)
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Functional Durability
In 4 animals, the LD muscle grafts were continuously stimulated at 25 Hz and the 1:1 ratio for 7 hours until the experiment was terminated. Periodically repeated on-off tests revealed that LD grafts produced physiologically significant increases in RV function over the entire period of study without evidence of muscle fatigue, contributing to normal cardiac index sustained up to the termination of the experiment (Fig 6).
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Fig 6. . Changes in percent assistance in pulmonary flow ( PA Flow) and cardiac index over the period of continuous stimulation in 4 animals.
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Comment
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In the present study, we extended the concept of dynamic cardiomyoplasty, which has been appreciated as an effective surgical option for left ventricular assistance in patients with dilated cardiomyopathy [2, 3], to surgical correction of congenital heart diseases with hypoplastic right ventricle. Most of the previous experiments using skeletal muscle in right heart assist [5, 6] were performed without cardiopulmonary bypass. In that situation the contraction of the skeletal muscle is not necessarily essential to maintain optimal hemodynamics, thus compromising a definitive conclusion regarding its potential use in patients with hypoplastic right ventricle or univentricular hearts. Our study showed that the linear dynamic cardiomyoplasty onto a patch-enlarged RV chamber restored normal RV performance at the physiologic range of CVP in an acute setting of hypoplastic right ventricle, whereas profound RV dysfunction was noted without patch enlargement of RV and graft stimulation. Although the model itself is not totally analogous to the hypoplastic RV and the experiment was not conducted in a chronic setting, results were encouraging as a feasibility study for a surgical modification of the currently applicable technique in a reconstructive operation.
Several investigations [4, 6, 10] have shown the potential for total RV bypass using a skeletal muscle ventricle. Nevertheless, the disadvantages of this approach lie in the propensity for thrombus formation within the skeletal muscle ventricle cavity and subsequent thromboemboli and a need for long conduit with biologic valves. Additionally, attempts to provide right heart assist in the setting of a Fontan circulation have been frustrated by the low right atrial pressure [4, 6] that supplies an inadequate preload to allow optimal skeletal muscle ventricle function. In contrast, the present study showed that our approach with a modification of DCMP for the enlarged RV chamber with a compliant pericardial patch can avoid the use of a valved conduit and permit sufficient ventricular filling at physiologic preload.
Previous studies [4, 5, 11, 12] have shown the feasibility of full-thickness cardiomyoplasty to substitute a part of the RV wall in acute and chronic preparations, similar to the model described in the present study. Macoviak and colleagues [4, 11, 12] reported that myoventriculoplasty with a diaphragmatic muscle or a left LD muscle flap as a small trimmed island pedicle flap produced functional enlargement of the right ventricle and sustained stable hemodynamic status for several hours. In their study, however, detailed functional assessment was not included. Soberman and colleagues [5] have shown that right LD cardiomyoplasty can function as a partial RV free wall replacement in a chronic canine model without the use of cardiopulmonary bypass. In that report, a small part of the free wall was excised; the resulting functional improvement was reported as trivial (RV ejection fraction, 0.52 to 0.66; RVP, 23 to 25 mm Hg). In these previous studies of myoventriculoplasty, the limited amount of excised RV muscle might compromise a definitive conclusion about the potential of this method for patients with hypoplastic right ventricle or univentricular hearts. Also, the amount of muscle flap used as a working portion was restricted to the area implanted to the RV defect, whereas the thickest and well-perfused proximal portion of the flap is located in the left thorax as a nonworking portion. Unlike previous approaches of myoventriculoplasty, the configuration of longitudinal RV cardiomyoplasty described in the present study uses the linear contraction of the entire muscle flap to achieve compression of a patch-enlarged chamber and traction of the diaphragmatic surface of RV toward the outflow tract. In addition, this configuration without wrapping the entire LV may avoid energy loss attributable to compression of a more vigorous LV and allow more efficient augmentation of a low-pressure RV chamber.
It is of interest that despite the use of a much shorter preconditioning period with single pulses than the standard conditioning protocol [2] in the present study, optimal hemodynamic status was sustained during continuous muscle stimulation at 25 Hz 1:1 for as long as 7 hours without evidence of muscle fatigue. This finding suggests that less energy is required for this type of RV assist than for the conventional DCMP.
Two weeks of continuous stimulation in the present training protocol is apparently not long enough for the skeletal muscle to be completely transformed, and canine muscles must contain a large number of intermediate fibers and possess a certain degree of baseline fatigue resistance [13, 14]. Continuous stimulation of the unconditioned skeletal muscles with trained pulses to augment left ventricular function results in rapid muscle fatigue within several minutes [15], whereas similar stimulation under nonworking status (in situ preconditioning or skeletal muscle ventricle before connecting to the circulation) can be used for muscle conditioning without muscle fatigue even in the control unconditioned muscles. Therefore, the optimal training protocol should be determined, taking the situation in which the muscle is used into account. The present finding may imply the potential for a minimum muscle preconditioning protocol, followed by subsequent "working conditioning," for this type of RV assist.
Although the results were encouraging as a feasibility study, there are important unsolved issues, including thromboembolism resulting in chronic pulmonary embolism, changes in muscle compliance over time, which will require higher preload, and chronic changes in the skeletal muscle itself with continued electrical stimulation. These crucial issues, which are inherent to the concept of using skeletal muscle grafts for right heart assistance, are to be solved in further experimental studies before this technique can be anticipated as a promising approach for reconstructive operation in the congenital hypoplastic ventricle.
In conclusion, linear LD myoplasty after patch enlargement of the RV can restore optimal systolic performance at a physiologic preload, and may provide a surgical option for the hypoplastic RV. Functional durability of incompletely conditioned muscles in an acute phase may imply the feasibility of working conditioning after minimum preconditioning protocol for this type of right heart assist.
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Footnotes
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Address reprint requests to Dr Morita, Department of Cardiovascular Surgery, Jikei University School of Medicine, 3-25-8, Nishi-shinbashi, Minato-ku, Tokyo 102, Japan.
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References
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Abstract
Introduction
