Ann Thorac Surg 1995;59:305-312
© 1995 The Society of Thoracic Surgeons
Efficacy of a Skeletal Muscle–Powered Dynamic Patch: Part 1. Left Ventricular Assistance
Masao Takahashi, MD,
Takuro Misaki, MD,
Go Watanabe, MD,
Hiroshi Ohtake, MD,
Yoshio Tsunezuka, MD,
Masanari Wada, MD,
Naoki Sakakibara, MD,
Yasuhiro Matsunaga, MD,
Michio Kawasuji, MD,
Yoh Watanabe, MD
Department of Surgery (1), Kanazawa University School of Medicine, Kanazawa, and Department of Surgery (1), Toyama Medical and Pharmaceutical University, Toyama, Japan
Accepted for publication June 15, 1994.
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Abstract
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In this study, we examined the capability of a skeletal muscle–powered, dynamic patch to provide left ventricular assistance. An actuator was developed that used linear traction power furnished by the latissimus dorsi muscle and liquid as the medium for power transfer. The proximal portion of the muscle was dissected and was reattached to the actuator. The left ventricular apex was excised, and the dynamic patch lined with autologous pericardium was implanted during cardiopulmonary bypass. Hemodynamic studies were performed in 8 dogs after weaning from cardiopulmonary bypass. Muscle stimulation was found to significantly increase the systolic aortic pressure (91.6 versus 112.1 mm Hg; p < 0.01), the mean aortic pressure (65.2 versus 73.0 mm Hg; p < 0.01), and aortic blood flow (0.77 versus 0.92 L/min; p < 0.01). The left atrial pressure decreased from 17.9 to 16.6 mm Hg (p < 0.01). This ``hybrid'' left ventricular assist device possesses notable clinical advantages because of its remarkable efficacy in assisting circulation. Further experimental studies using preconditioned skeletal muscle are necessary to assess the long-term effects of this technique.
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Introduction
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The use of skeletal muscle to assist circulation has made startling progress since the technique was first described by Kantrowitz and McKinnon in 1959 [1]. This progress is attributable to the fact that the fatigue phenomenon of skeletal muscle has been overcome [2–5] and the electrostimulation method has been dramatically improved [6–10] during the past decade. In an effort to find ways to assist left ventricular function, experiments involving cardiomyoplasty [10–14], aortomyoplasty [15, 16], and circulatory assistance with skeletal muscle ventricle [17–21] have been carried out. However, all of these methods have failed in terms of both significantly improving the hemodynamics and conferring satisfactory thromboresistance.
In 1969, Schupbach and associates [22] reported on their use of a left ventricular dynamic patch actuated by a driving machine, and it was subsequently observed to remarkably improve hemodynamics [23]. Kyo and colleagues reported that the left ventricular dynamic patch was associated with a significant decrease in myocardial oxygen consumption [24] and caused increased segmental shortening of the left ventricular wall [25]. Moreover, Liapis and co-workers [26] discovered that the coronary blood flow during left ventricular support provided by the dynamic patch was significantly increased.
We describe here a left ventricular dynamic patch driven by skeletal muscle. The technique has the potential to confer a significant increase in circulatory function and to be applied clinically. The purpose of the present study was to examine the efficacy of left ventricular assistance using this newly designed ``hybrid'' left ventricular assist device.
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Material and Methods
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Eight adult mongrel dogs weighing 13 to 22.5 kg (mean, 15.8 ± 3.5 kg) were used in this study. All the 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 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 pentobarbital sodium (5 mg/kg), given intravenously. No muscle relaxants were used. A cuffed endotracheal tube was inserted, and the dog was ventilated through a volume-controlled respirator (Harvard Apparatus, South Natick, MA) with about 50% oxygen, administered at a rate of 20 to 30 respirations per minute and a tidal volume of 400 to 600 mL.
The proximal portion of the left latissimus dorsi muscle (LDM) was harvested through a longitudinal incision in the left axilla, taking care to not injure the feeding artery and drainage vein. Its insertion at the humerus was then dissected and was reattached to the actuator. Two pacing electrodes were placed near the motor nerve branches, one slightly distal to their penetration into the LDM and one 6 to 8 cm more distally (Fig 1
).
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Fig 1. . Schema of the experiment performed in this canine model. The actuator was sutured to the proximal side of the latissimus dorsi muscle (LDM). The other side was fixed to the pole. The actuator was connected to the dynamic patch, which was implanted in the left ventricular apex. Liquid was used to fill the device.
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The Linear Actuator for Left Ventricular Assistance
An actuator was developed that would make the most efficient use of muscle contraction. The actuator consists of a bellows supported by two cylinders. As shown in Figures 2 and 3, the self-retaining bellows (volume, 16 mL) can move unrestrictedly with linear traction of the LDM, and the configuration of the bellows can be retained on its own during muscle relaxation. The muscle power can be transmitted directly to the bellows. A hook on the actuator was sutured to the proximal portion of the LDM with felt strips, and another hook was fixed to the pole (see Fig 1
). We then confirmed that the bellows expanded and contracted smoothly as the muscle relaxed and contracted.
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Fig 3. . The actuator. The bellows expanded and contracted in concert with muscle contractions. (Upper) During the diastolic phase, the latissimus dorsi muscle is relaxed and the bellows expands by itself. (Lower) During the systolic phase, the bellows contracts as the result of latissimus dorsi stimulation.
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Dynamic Patch
The dynamic patch has a rigid plastic outer shell that consists of a flexible latex balloon with a polyvinyl chloride tube. The plastic shell was shaped like a hemisphere so that it could fit over an excised left ventricular apex. The shell was 3.5 cm in diameter and 2.0 cm in depth. The pumping chamber had a stroke volume of 7.5 mL; it was covered with a woven Dacron graft on the outside and lined with autologous pericardium treated with glutaraldehyde (Fig 4).
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Fig 4. . Dynamic patch being implanted at the left ventricular apex. (Upper) The left ventricular apex was amputated at the level of the papillary muscle to prevent mitral regurgitation. The dynamic patch was implanted with interrupted mattress sutures of 2-0 polypropylene buttressed with pledgets. (Lower) Autologous pericardium was used to reduce the incidence of thromboembolic complications and reinforce the wound edge.
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Operation
The chest was opened using a left parasternal longitudinal thoracotomy. After heparinization (0.3 mL/kg), the animals were prepared for cardiopulmonary bypass. 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 heart-lung machine consisted of a Bio-Pump (Medtronic Bio-Medicus Inc, Minneapolis, MN) and a membrane oxygenator (Menox AL2000; Kuraray, Osaka, Japan). The entire circuit (total volume, 300 mL) was primed with lactated Ringer's solution, 25% albumin, and substituted plasma (hydroxyethyl starch). Catheters were positioned to measure the aortic and left atrial pressures. Blood flow through the ascending aorta was measured with a transit-time ultrasonic flowmeter (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 administrated into the aortic root. The heart was arrested and the left ventricular apex was amputated maximally below the level of the papillary muscles to prevent mitral regurgitation. The dynamic patch was implanted with ten to twelve interrupted mattress sutures of 2-0 or 3-0 polypropylene buttressed with pledgets that passed through an encircling Teflon felt, thus reinforcing the wound edge (see Fig 4).
After implantation of the dynamic patch, the aortic clamp was released. Dogs were weaned from cardiopulmonary bypass after circulatory assist lasting 32 ± 2.7 minutes, followed by spontaneous resumption of circulation.
The tube at the center of the dynamic patch was connected to the driving actuator with a polyvinyl chloride tube (8.5 mm in a diameter). It was filled with saline solution to provide a medium for power transfer (see Fig 1). The muscle stimulation was then started. During the systolic phase, the bellows was contracted by LDM stimulation and this induced balloon dilation, thereby causing aortic blood flow to increase. When the LDM relaxed during the diastolic phase, the bellows expanded by itself and the balloon contracted, which helped draw blood into the left ventricle (Fig 5).
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Fig 5. . The mechanism of the assist device (the dynamic patch and the actuator). (Left) Diastolic phase. (Right) Systolic phase. (Ao = aorta; LA = left atrium; LDM = latissimus dorsi muscle; LV = left ventricle.)
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Muscle Stimulation
The LDM was stimulated periodically. During the first session, the muscle was stimulated for as long as possible in all dogs with a burst frequency of 33 Hz, a burst duration of 200 ms, an amplitude of 5 V, and a pulse width of 1 ms. Synchronous mode stimulation at 1:2 was done using a multiprogrammable stimulator (SEC-2102; Nihon Koden, Tokyo, Japan), with the native R wave detected from two sensing electrodes sutured into the right ventricle. If the dogs survived the first session of muscle stimulation, various pacing modes of stimulating the muscle for left ventricular assistance were tried after the muscle had rested for 30 minutes. In the second session, the burst duration was changed to 120, 90, or 60 ms. In the third session, a 1:4, 1:3, or 1:2 synchronous mode was tried. In the fourth session, the pacing delay from the native wave was changed from 100 to 250 ms. In the fifth session, the pacing amplitude was increased to 10 V.
Hemodynamic Study
Five hemodynamic variables were measured before and after stimulation of the LDM: heart rate, aortic pressure, mean left atrial pressure, systolic dynamic patch pressure, and aortic blood flow. To study acute feasibility, experimental results were obtained for data analysis during the first 5 minutes in the first muscle stimulation session and averaged over several beats. A 16-channel polygraph recorder (T-16; Siemens-Elema AB, Solna, Sweden) was used to record all of the data for the different variables.
Statistics
Results are expressed as the mean ± standard errors of the mean. The mean values obtained under the stimulation off and on conditions were subjected to statistical analysis using the paired t test, done in consultation with Dr Kazuo Hashimoto of Kanazawa University School of Medicine. A p value of less than 0.01 was considered statistically significant.
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Results
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All dogs survived for 3.5 ± 1.0 hours (range, 0.8 to 8.2 hours) after the termination of cardiopulmonary bypass. In 2 dogs, the hemodynamic benefits were lost after 0.8 and 0.9 hours because of muscle fatigue that reduced muscle contraction, and they died as the result of left ventricular failure. The others were euthanized by the intravenous injection of potassium after all data had been collected. The end points of this experiment were systemic hypotension, severe anemia, hypoxia due to respiratory failure or acidosis, and the like.
The weight of the excised ventricular muscle was 6.9 ± 1.0 g, and the percentage of the left ventricular mass excised was 10.3% ± 0.5%. Left ventricular function was efficiently augmented with the support provided by the dynamic patch. As shown in Figure 6, muscle stimulation significantly increased aortic pressure and aortic blood flow. The dynamic patch pressure was higher (197.3 ± 5.1 mm Hg) than the systolic aortic pressure (112.1 ± 4.8 mm Hg) when the LDM was stimulated, and declined to a negative pressure during the diastolic phase when the LDM relaxed. Moreover, the left atrial pressure significantly decreased during muscle stimulation.
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Fig 6. . Changes in the left ventricular function during stimulation and relaxation. Aortic pressure and aortic blood flow increased remarkably when the latissimus dorsi muscle was stimulated. Dynamic patch pressure was usually higher than systolic aortic pressure during the systolic phase, and negative pressure was observed during the diastolic phase. Left atrial pressure decreased significantly during stimulation. (AoF = aortic blood flow; AoP = aortic pressure; DPP = dynamic patch pressure; ECG = electrocardiogram; LAP = left atrial pressure.)
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The changes in the hemodynamics are shown in Figure 7. The heart rate did not change significantly after stimulation of the LDM. The systolic aortic pressure increased by 22.4%, from 91.6 ± 3.2 to 112.1 ± 4.8 mm Hg (p < 0.01) and the diastolic aortic pressure did not change significantly, but the aortic pressure increased by 11.9%, from 65.2 ± 2.4 to 73.0 ± 2.9 mm Hg (p < 0.01). The left atrial pressure decreased by 7.3%, from 17.9 ± 0.3 to 16.6 ± 0.4 mm Hg (p < 0.01), and aortic blood flow increased by 19.5%, from 0.77 ± 0.1 to 0.92 ± 0.1 L/min (p < 0.01). The systolic dynamic patch pressure was 0 mm Hg before stimulation and 197.3 ± 5.1 mm Hg after stimulation. It was 1.76 times greater than the systolic aortic pressure.
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Fig 7. . Plots of the mean aortic pressure, aortic blood flow, and left atrial pressure. Latissimus dorsi stimulation significantly increased the systolic and aortic pressures and the aortic blood flow. The left atrial pressure was significantly decreased.
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In all dogs, the LDM showed no macroscopically visible signs of cyanosis, as seen in the fully dissected, nonvascular delayed LDM. Representative hemodynamic changes observed during the first session in 1 animal are presented in Figure 8. The deterioration in muscle function took place slowly during the first session, even though the muscle was not preconditioned. The power of the LDM after continuous stimulation for 30 minutes was enough to bring about an improvement in hemodynamics. The hemodynamic changes that occurred over time after the second session are presented in Figure 9. The interval between each session was about 30 minutes, and it took a relatively short time for recovery from muscle fatigue to occur in the first several sessions. However, in subsequent sessions, the contractile power tended to deteriorate and muscle stimulation could not be maintained for more than 30 minutes. In terms of the muscle power, there was considerable variation among the dogs.
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Fig 8. . Hemodynamic changes during the first stimulation session. The deterioration in function took place slowly, and the muscle power retained was enough to cause the hemodynamics to improve. The mean systolic aortic pressure decreased from 124 mm Hg just after stimulation to 112 mm Hg after 30 minutes. The mean aortic blood flow decreased from 0.97 to 0.92 L/min. (AoF = aortic blood flow; AoP = aortic pressure; ECG = electrocardiogram.)
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Fig 9. . Hemodynamic changes over time. After the first session, the LDM needed a resting time of 30 minutes for recovery from muscle fatigue to take place. Thereafter, various pacing modes to stimulate the muscle were tried. The skeletal muscle–powered dynamic patch worked effectively in any kind of pacing mode. However, a deterioration in LDM power was observed in the last session because the muscle had not been preconditioned. (AoF = aortic blood flow; AoP = aortic pressure; DPP = dynamic patch pressure; ECG = electrocardiogram; II = second session; III = third session; IV = fourth session; V = fifth session.)
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Comment
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In the present study, the skeletal muscle–powered dynamic patch provided sufficient left ventricular assistance. Hemodynamic monitoring showed a significant increase in aortic pressure and decrease in left atrial pressure. The aortic blood flow also increased significantly.
In patients undergoing dynamic cardiomyoplasty, an improved functional status has been observed: an average increase in the New York Heart Association functional class of 1.4 [12] and a reduction in the number of rehospitalizations necessitated by heart failure of from 2.4 to 0.3 times per patient per year [13]. However, the degree of left ventricular functional improvement conferred by cardiomyoplasty remains controversial. An improvement in left ventricular function was observed in experimental studies evaluating the performance characteristics of the skeletal muscle ventricle [17–21], but this technique has not been applied clinically because of the latent risks of thromboembolic complications associated with its use.
Hybrid Left Ventricular Assist Device
As a new approach to circulatory assistance, we developed a hybrid assist device that connects the dynamic patch with the skeletal muscle–powered actuator. This technique could eliminate the clinical problems associated with the previously described dynamic patch [22–26], which required that the patient remain in bed because of the extracorporeal mechanical power source needed to drive it. Moreover, clinical applications of the aortic dynamic patch revealed no evidence of thrombosis [27–29]. In our experiment, the autologous pericardium located at the innerside of the patch proved to be more useful than the previous dynamic patch, and we believe that there are more advantages to this device in terms of minimizing thromboembolic complications than to other methods that involve blood coming into direct contact with artificial materials.
Hydraulic Linear Actuator Driven by Skeletal Muscle
We developed a linear actuator that could optimize skeletal muscle contraction. This actuator generated efficient contraction power because only the proximal portion of the LDM was utilized without division of the collateral vessels from the intercostal arteries. The muscle fibers were oriented in the ideal direction during muscle contraction. In studies examining the acute efforts, which have previously been reported on, the unconditioned muscles rapidly fatigued after a few minutes of stimulation. In our experiment, however, the unconditioned LDM possessed a much greater contractile power and was more fatigue resistant than the contractile power and fatigue resistance seen for the previous methods. The collateral vessels from the chest wall were thought to be very important from the standpoint of muscle contraction. Potential ways in which cardiomyoplasty can fail to improve hemodynamics [12–14] include detachment of the implanted muscle on the heart as well as inadequate contractions of skeletal muscle stemming from the lack of collateral vessels.
We chose hydraulic liquid as the medium for transmitting the contraction energy of the skeletal muscle directly to the dynamic patch. This method ensures adequate assistance to left ventricular function. In our preliminary study that evaluated this device, we found that muscle energy is superior to liquid resistance (Takahashi and associates, manuscript in preparation). The diameter of the connecting tube between the actuator and the dynamic patch needs to be large enough to reduce resistance. Because systolic dynamic patch pressures were usually 1.76 times higher than systolic aortic pressures, we consider this device to be free of problems when it comes to assisting circulation. Moreover, the end-diastolic negative pressure of the actuator (see Fig 6) could help promote filling of the left ventricle. If substances with a specific gravity less than that of liquid are used (ie, silicon oil), assistance will be more efficient without a loss of energy.
We attempted to use air as the medium for power transfer, but the stroke volume obtained with the dynamic patch was inefficient when the systolic aortic pressure exceeded 60 mm Hg, because air has a large reduction rate in relation to volume and pressure. However, the pneumatic dynamic patch implanted in the right ventricular free wall brought about a significant improvement in right ventricular function [30].
Study Limitations and Clinical Implications
There were several limitations to the present study: it did not assess potential long-term thromboembolic complications; endurance tests of the dynamic patch and the actuator were not performed; an advanced device, which would eliminate the major problem of the fixation point of the device, tissue adhesion, and biomaterial leaks [31] must be developed for long-term use; and we did not use preconditioned skeletal muscle. We are currently investigating the long-term effects of this technique using preconditioned skeletal muscle. We are also developing a new linear-push actuator that is fixed to the thoracic wall (Fig 10), and we are now investigating the performance characteristics of this device as a driving power source for the dynamic patch. We believe this type of device can be applied in the clinical setting.
One of the best clinical indications for the use of this device may be a left ventricular aneurysm. About 10% of the ventricular wall was excised in the dogs in this series. However, the device may be more effective in the setting of left ventricular failure stemming from a giant ischemic aneurysm, which requires a patch that takes up as much as 20% to 30% of the left ventricular wall. This operation would be similar to the previously described left ventricular aneurysmectomy with patch replacement.
This so-called hybrid left ventricular assist device offers great clinical promise and possesses distinct advantages in terms of providing long-term circulatory assistance. The use of autologous skeletal muscle is a critical factor, and would allow the patient to leave the hospital and return home if the device is operational.
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Footnotes
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Address reprint requests to Dr Takahashi, Department of Surgery (1), Kanazawa University School of Medicine, 13-1 Takaramachi, Kanazawa 920, Japan.
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References
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Top
Abstract
Introduction
