Ann Thorac Surg 1995;59:313-319
© 1995 The Society of Thoracic Surgeons
Efficacy of a Skeletal Muscle–Powered Dynamic Patch: Part 2. Right Ventricular Assistance
Go Watanabe, MD,
Takuro Misaki, MD,
Masao Takahashi, MD,
Hiroshi Ohtake, MD,
Yoshio Tsunezuka, MD,
Masanari Wada, MD,
Yoh Watanabe, MD
Department of Surgery (1), Toyama Medical and Pharmaceutical University, Toyama, and Department of Surgery (1), Kanazawa University School of Medicine, Kanazawa, Japan
Accepted for publication November 18, 1994.
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Abstract
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The purpose of this study was to assess the feasibility of using a skeletal muscle-powered dynamic patch to assist the failing right ventricle. Seven adult mongrel dogs were used in the study. The proximal portion of the left latissimus dorsi muscle was harvested and reattached to the actuator to serve as a skeletal muscle energy convertor. The right ventricular free wall was fully excised and the dynamic patch was implanted under cardiopulmonary bypass. After weaning from cardiopulmonary bypass, the latissimus dorsi muscle was stimulated using a burst frequency of 33 Hz, a burst duration of 200 ms, and 1:2 synchronous mode stimulation with the native R wave. Latissimus dorsi muscle stimulation increased systolic aortic pressure (78 versus 91 mm Hg; p < 0.01), mean aortic pressure (56 versus 62 mm Hg; p < 0.05), aortic blood flow (0.73 versus 0.97 mL; p < 0.01), and systolic right ventricular pressure (41 versus 56 mm Hg; p < 0.01). The mean right atrial pressure decreased from 14 to 9.6 mm Hg (p < 0.01). Our results demonstrate that the use of a right ventricular dynamic patch powered by a skeletal muscle linear-type actuator can not only function as a right ventricular free wall substitute but also lead to the augmentation of right ventricular and global cardiac function.
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Introduction
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Right ventricular failure is associated with a number of cardiac and pulmonary diseases and may be seen after surgical correction of congenital heart disease. Although there are extensive data regarding mechanical assistance of left ventricular dysfunction, only a few recent reports have described the utility of mechanical support for right ventricular dysfunction [1–3].
The use of skeletal muscle for circulatory assistance has made tremendous progress since the procedure was first described by Kantrowitz and McKinnon in 1959 [4]. During the past several years, there has been a resurgence of interest in the use of skeletal muscle for cardiac augmentation. Experiments involving dynamic cardiomyoplasty [5, 6], aortomyoplasty [7], and skeletal muscle ventricle [8–10] to assist left ventricular function have been performed. However, these methods have been limited by the lack of significant improvement in hemodynamics and satisfactory thromboresistance.
Elsewhere in this issue we report on the use of a skeletal muscle-powered left ventricular dynamic patch for the improvement of hemodynamics in left ventricular dysfunction [11]. The purpose of the present study was to determine the feasibility of using a similar patch for improving right ventricular function and augment pulmonary and systemic circulation.
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Material and Methods
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Seven adult mongrel dogs weighing between 12 and 23.5 kg (mean, 15.6 ± 1.7 kg) were used in this study. 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 (NIH publication 85-23, revised 1985).
Preparation of the Latissimus Dorsi Muscle
The animals were premedicated with an intramuscular injection of ketamine chloride (5 mg/kg) and sedated with intravenous pentobarbital sodium (10 mg/kg). No muscle relaxants were used. A cuffed endothoracheal tube was inserted, and the animals were ventilated by a volume-controlled respirator (Harvard Apparatus). A longitudinal skin incision was made and the proximal portion of the left latissimus dorsi muscle (LDM) was carefully harvested to avoid injuring the thoracodorsal nerve, artery, and vein. The distal segment of the LDM and collateral vessels arising from intercostal arteries were left intact. The insertion of the LDM at the humerus was then dissected free and reattached to the actuator (described below). Two pacing electrodes were placed near the motor nerve branches slightly distal to their penetration into the LDM and 6 to 8 cm more distally (Fig 1
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Fig 1. . Canine model of the dynamic patch. The actuator is sutured to the proximal portion of the latissimus dorsi muscle (LDM) at one end and to the anchoring pole at the other end. It is connected to a dynamic patch, which is implanted in the right ventricle (RV).
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Construction and Mechanism of the Actuator
The actuator was designed to serve as a skeletal muscle energy convertor and make optimal use of skeletal muscle contractions. The actuator consisted of bellows equipped with a driving port and supported by two cylinders, which converted traction force from both ends of the actuator into the compression of the bellows. The bellows were made of polyurethane in a semistretched configuration and retained their characteristics after passive compression or stretching. As shown in Figure 2, the self-retaining bellows (total volume of 80 mL, maximum stroke volume of 60 mL) were capable of sliding smoothly by expansion of the actuator. The actuator was fixed to the anchoring pole at one end and attached to the proximal portion of the LDM with felt strips at the other end. The stretching and retaining of the actuator was synchronized with LDM contraction and relaxation.
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Fig 2. . Schema of the linear-type actuator. Compressions of the actuator were synchronized with latissimus dorsi muscle (LDM) contractions. During the diastolic phase, the LDM is relaxed and the bellows self-expand. During the systolic phase, the bellows contract with LDM contraction.
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Dynamic Patch
The dynamic patch consisted of an elastic hard outer shell with a polyvinyl chloride tube and a flexible latex balloon. The optimal shape of the dynamic patch was obtained using cadaveric custom-made molds. The shape of the plastic shell was oval and hemispheric to fit over an excised right ventricular free wall. According to the animal size, we have constructed two different dynamic patches. The sizes of the dynamic patches were 80 mm x 35 mm and 75 mm x 35 mm, and the pumping chambers had a stroke volume of 6.3 mL and 5.5 mL, respectively. It was covered with a woven Dacron prosthesis and lined with glutaraldehyde-pretreated autologous pericardium (Fig 3).
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Fig 3. . Photographs of the right ventricular dynamic patch. The dynamic patch was covered with a woven Dacron prosthesis and lined with autologus pericardium.
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Operative Procedure
The chest was opened using a left parasternal longitudinal thoracotomy. After heparinization (300 IE/kg), the animals were prepared for extracorporeal circulation. An arterial cannula was inserted into the ascending aorta, and drainage tubes were placed into the superior and inferior venae cavae. A left atrial venting tube was inserted into the left atrial appendage. The extracorporeal circulation consisted of a Bio-Pump (Medtronic Bio-Medicus Inc, Minneapolis, MN) and membranous oxygenator (Menox AL 2000; Kuraray, Osaka, Japan). The entire circuit (total volume, 300 mL) was primed with lactated Ringer's solution, 25% albumin, and substitute plasma (hydroxyethyl starch). Catheters were inserted and positioned to measure aortic, right ventricular, right atrial, and left atrial pressures. The blood flow through the ascending aorta was measured using a transit-time ultrasonic flow-meter (T101, Transonic Systems, Ithaca, NY).
After total cardiopulmonary bypass was initiated, the ascending aorta was cross-clamped and cold crystalloid cardioplegic solution (15 mL/kg) was administered into the aortic root. The heart was then arrested and the right ventricular free wall, including its diaphragmatic surface, was excised fully. The papillary muscle of the tricuspid valve was preserved to avoid tricuspid valve insufficiency. The dynamic patch was implanted using 12 to 14 interrupted mattress sutures that passed through an encircling Teflon felt, thus reinforcing the myocardial edge (Fig 4).
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Fig 4. . Implantation of the right ventricular dynamic patch. The right ventricular free wall was excised under cardiopulmonary bypass. The dynamic patch was implanted with interrupted mattress sutures.
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After implantation of the dynamic patch, air was evacuated and the aortic clamp was released. All animals were weaned from cardiopulmonary bypass after cardiac arrest for 29.3 ± 2.7 minutes and were able to adequately maintain their own circulation. The aortic and vena caval cannulas were removed and protamine was administered.
The driving port of the dynamic patch was connected to the actuator with a polyvinyl chloride tube. The LDM stimulation then was started. During the systolic phase, the bellows contracted by LDM stimulation and induced dynamic patch dilatation, thereby causing pulmonary blood flow to increase. When the LDM relaxed during the diastolic phase, the bellows expanded by itself and the dynamic patch volume declined to help blood fill the right ventricle (Fig 5).
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Fig 5. . Mechanism of the assist device (the dynamic patch and the actuator). (a) Diastolic phase. (b) Systolic phase. (LDM = latissimus dorsi muscle; LV = left ventricle; RV = right ventricle).
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Skeletal Muscle-Powered Dynamic Patch Stimulation
After the skeletal muscle-powered dynamic patch (SMPDP) to the circulation, the LDM was stimulated using a burst frequency of 33 Hz, a burst duration of 200 ms, an amplitude of 5 volts, and a pulse width of 1 ms. Stimulation in a 1:2 synchronous mode was used. The native R wave was detected by two sensing electrodes that were sutured to the left ventricle. A multiprogrammable stimulator was employed (SEC-2102; Nihon Koden, Tokyo, Japan).
Hemodynamic Study
The following hemodynamic parameters were measured before and after stimulation of the LDM: heart rate, aortic pressure, right ventricular pressure, right atrial pressure, dynamic patch pressure, and aortic blood flow. A 16-channel polygraph recorder (T-16; Siemens-Elema AB, Solna, Sweden) was used to record these parameters. The LDM was stimulated continuously for at least 30 minutes with burst stimulation during the first session. Hemodynamic data analysis was obtained during the first 5 minutes in the first session of LDM stimulation and averaged over several beats. A second session of stimulation was begun after muscle recovered again for 30 minutes. Stimulation of the LDM was terminated when muscle fatigue resulted in failure of further hemodynamic benefit after a repeated session. Progressive respiratory deterioration, metabolic acidosis, and oozing from the tissue were evident in all cases during cessation of stimulation. All animals ultimately were euthanized by an intravenous injection of potassium.
Statistic Analysis
Results were expressed as mean ± standard error of the mean. Mean values between stimulation on and off were subjected to statistical analysis with the paired t test in consultation with Dr Kazuo Hashimoto, Professor of the Department of Hygiene, Kanazawa University School of Medicine, Kanazawa, Japan. A p value of less than 0.05 was considered statistically significant.
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Results
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Experimental data were obtained in the acute phase. All animals tolerated the surgical procedure and the period over which SMPDP stimulation produced physiologically significant useful work on LDM stimulation and hemodynamic effects due to graft contraction.
The experiment was terminated 106 ± 16.8 minutes (range, 45 to 180 minutes) after weaning from cardiopulmonary bypass. In all animals, the hemodynamic effect of SMPDP stimulation persisted for more than 30 minutes despite the fact that the muscles were not preconditioned. The hemodynamic changes over the first 30 minutes are shown in Figure 6, and the hemodynamic data for the longest surviving animal (180 minutes) are shown in Figure 7. Right ventricular function significantly improved with the use of the SMPDP. Latissimus dorsi muscle stimulation significantly increased aortic pressure and aortic blood flow. Dynamic patch pressure tracings demonstrated a suprasystolic right ventricular pressure (Fig 8).
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Fig 6. . Hemodynamic changes during first 30 minutes. (AoF = aortic blood flow; AoP = aortic pressure; d = diastolic; m = mean; RVP = right ventricular pressure; s = systolic; *p < 0.05; **p < 0.01.)
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Fig 7. . Hemodynamic changes for the longest surviving animal (180 minutes) over time. (AoF = aortic blood flow; AoP = aortic pressure; ECG = electrocardiogram; DPP = dynamic patch pressure; RVP = right ventricular pressure.)
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Fig 8. . Pressure tracings recorded with right ventricular dynamic patch at a rate of 1:2. (Top) Recorded at a paper speed at 25 mm/s. (Bottom) Recorded at a paper speed of 5 mm/s to emphasize the effects of right ventricular dynamic patch assist. (AoF = aortic blood flow; AoP = aortic pressure; DPP = dynamic patch pressure; ECG = electrocardiogram; LAP = left atrial pressure; RVP = right ventricular pressure.)
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The changes in the hemodynamic parameters were as follows. The heart rate did not change significantly after stimulation of the LDM. The systolic aortic pressure increased 36% from 78.1 ± 2.0 to 91.3 ± 3.4 mm Hg (p < 0.01). The mean aortic pressure increased from 56.2 ± 2.6 to 62.2 ± 1.8 mm Hg (p < 0.05). The systolic right ventricular pressure increased 36% from 41.0 ± 1.5 to 55.6 ± 2.1 mm Hg (p < 0.01), and mean right atrial pressure decreased from 14.3 ± 0.99 to 9.57 ± 0.37 mm Hg (p < 0.01). Aortic blood flow significantly increased 33% from 0.73 ± 0.13 to 0.97 ± 0.17 L/min (Table 1). The weight of the excised ventricular muscle was 7.4 ± 1.2 g, which represented 6.79% of the entire ventricular mass.
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Comment
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Research involving the use of skeletal muscle for cardiac assistance has been directed along four major approaches: (1) dynamic cardiomyoplasty, where skeletal muscle is wrapped directly around the right or left ventricle [5, 6], (2) aortomyoplasty [7], (3) a skeletal muscle ventricle [8–10], and (4) the development of an energy source for assist devices [12, 13], the so-called hybrid biomechanical assistance. In dynamic cardiomyoplasty, skeletal muscle is wrapped around the heart and stimulated to contract synchronously with cardiac systole. Although an improvement in clinical functional status (an average increase of 1.4 New York Heart Association classes [14]) and a reduction in the number of rehospitalizations due to heart failure (from 2.4 to 0.3 times per patient per year [15]) have been observed with this technique, the degree of left ventricular functional improvement has been inconsistent [16, 17].
Skeletal muscle ventricles also have been coupled with the circulation either in parallel or in series using numerous methods [8–10]. A total right ventricular bypass using a skeletal muscle ventricle has been developed in our laboratories [18]. The skeletal muscle ventricle allows for more efficient transfer of muscle energy to the circulation than dynamic cardiomyoplasty. However, the disadvantage of the system lies in the propensity for thrombus formation within the skeletal muscle ventricle cavity and subsequent thromboemboli [8]. This problem persists despite lining the skeletal muscle ventricle cavity with a material with relatively low thrombogenicity such as polytetrafluoroethylene.
The hybrid biomechanical assistance model is another means of circulatory assistance that combines skeletal muscle power and an artificial assist device [12, 13]. Hybrid biomechanical assistance models are composed of skeletal muscle, an energy convertor system, and a circulatory assist device such as the ventricular assist device or the total artificial heart. The major problem with skeletal muscle as a power source is harnessing available energy and using it efficiently for maximal circulatory support. Biomechanical assistance using a ventricular assist device and a total artificial heart are thought to be feasible. However, controversy exists regarding energy losses and thromboembolic complications associated with the blood pump and mechanical valve. To obtain more cardiac assistance with fewer thrombogenic complications, we developed a new skeletal muscle-powered ventricular dynamic patch and a skeletal linear-pull energy convertor.
Dynamic Patch
The dynamic patch was designed as an implantable ventricular assist device. Previous experiments have indicated that this device not only has beneficial hemodynamic effects but also is beneficial for myocardial metabolic recovery in the ischemic failing heart [10, 19, 20]. An aortic dynamic patch has been clinically applied with good results and no thromboembolic complications [21, 22]. However, because of the difficulties of infection with percutaneous access, clinical evaluation of this system has been suspended. A new concept of hybrid implantable circulatory assistance involves the development of a skeletal muscle-powered dynamic patch. Using skeletal muscle power as an energy source, the problem of percutaneous energy access is circumvented. In our system, the inner surface of the dynamic patch was covered with autologous pericardium, thereby avoiding thromboembolic complications during chronic use.
Linear Skeletal Muscle Actuator
The linear-type actuator was developed by our group to optimize skeletal muscle contraction and minimize in situ muscle dissection. Blood flow is maintained to the LDM from collateral vessels through the chest wall. In this study we used unconditioned muscle; however, the hemodynamic effect of SMPDP stimulation persisted for more than 30 minutes. These results suggested that the fatigue rate of our linear-pull model was less than SMV model using unconditioned muscle [23, 24].
An additional advantage of this system is the effective use of skeletal muscle power. As skeletal muscle is accustomed to pulling, obtaining direct tension and power by using the muscle in a wrap-around configuration is very inefficient. Farrar and others [25, 26] have reported maximal mechanical advantages and efficiency by a linear alignment of the energy convertor. However, the development of a suitable muscle attachment system and rib fixation requires further studies. In this experiment, we used an ex situ pole for proximal fixation of the actuator. The clavicle or first rib is inadequate for this purpose because more length is required to obtain natural tension of the LDM.
In our previous study [11], we applied the SMPDP to the left ventricle after excision of the left ventricular apex. During LDM stimulation, we demonstrated sufficient left ventricular assistance using this device. In the present study, we extended these findings to a right ventricular free wall resection model. The results of this preliminary feasibility study are encouraging. Our results demonstrate that the right ventricular SMPDP can function as a right ventricular free wall substitute, augment right ventricular function, and significantly contribute to global cardiac function. In this study, aortic flow increased by 33% during activation of the dynamic patch.
Study Limitations and Clinical Implications
Our study has three limitations. First, the study did not address potential chronic thromboembolic complications. Second, the durability of the dynamic patch and the actuator were not evaluated. An advanced model designed to resolve the problem of tissue adhesion and biomaterial leak [27] is required for chronic use. Finally, we used unconditioned muscle. Transformed muscles generate less force than nontransformed muscles [24]. The hemodynamic effects of this procedure using preconditioned skeletal muscle are currently being investigated in our laboratory, and a new linear-push–type actuator is now being developed for chronic use [11].
This method has the potential for augmenting the ventricular size in hypoplastic right ventricles and for replacing diseased right ventricular segments in patients with severe right heart failure, right ventricular dysplasia including arrhythmogenic right ventricular dysplasia, and certain congenital heart diseases such as tricuspid atresia. This hybrid right ventricular assist device offers promise for long-term circulatory assistance.
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Footnotes
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Address reprint requests to Dr Watanabe, Department of Surgery (1), Toyama Medical and Pharmaceutical University, 2630 Toyama, Sugitani 930-01, Japan.
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References
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Abstract
Introduction
