Proceedings of the Society for Experimental Biology and Medicine 224:133-140 (2000)
© 2000 Society for Experimental Biology and Medicine
Review Article
Skeletal Muscle as a Myocardial Substitute
Louis I. Astra and
Larry W. Stephenson1,
Division of Cardiothoracic Surgery, Wayne State University School of Medicine, Detroit, Michigan 48201
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Abstract
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Skeletal muscle has long been used in the field of cardiac surgery. Its use has progressed from providing myocardial reinforcement to assisting the heart by actively pumping blood. Early experiments revealed that skeletal muscle assistance could augment pressures and blood flow; however, the results were short-lived due to muscle fatigue. It was later shown that skeletal muscle can be conditioned electrically to be fatigue resistant and therefore may be useful for performing cardiac-type work. Once the details were formed of how to stimulate and manipulate the muscle to assist the heart, several configurations were devised. Cardiomyoplasty and aortomyoplasty refer to wrapping skeletal muscle around the heart or aorta, respectively. These techniques have been applied in humans; however, the effectiveness is controversial. Although most patients improve clinically, the hemodynamic parameters have not shown consistent improvements, and survival data are unknown. Skeletal muscle ventricles offer a promising alternative to both cardiomyoplasty and aortomyoplasty. These are completely separate pumping chambers constructed from skeletal muscle and connected to the circulation in a variety of configurations. Although these have not been tried in humans, the animal data appear quite convincing. The skeletal muscle ventricles have shown the greatest improvements on hemodynamic parameters with great stability over time.
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Introduction
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Skeletal muscle was probably first used for cardiac application by DeJesus in 1931 (1). He used pectoralis muscle to repair a penetrating cardiac wound in a young man. Two years later, Leriche and Fontaine (2) applied a pectoralis muscle graft to the surface of infarcted canine myocardium to reinforce the myocardial scar. In 1935, Beck (3) demonstrated the development of collateral blood flow from muscle grafts to the canine epicardium. Both coronaries were gradually occluded after application of the muscle graft to the myocardium. Later, the muscle graft was used clinically in the treatment of ischemic heart disease. However, it was not until 1959 that attempts were made to assist the failing heart by using the contractile power of skeletal muscle. By this time, the concept of electrically pacing the heart was well known, and perhaps investigators started to think about stimulating skeletal muscle in a similar manner with hopes that the contractile tissue could enhance cardiac function.
In 1959 Kantrowitz and McKinnon (4) wrapped pedicle grafts of canine left hemi-diaphragm around the heart and stimulated the grafts via the phrenic nerve in synchrony with the cardiac systole. They observed active contraction in the muscle grafts, but no hemodynamic changes. In a later experiment, Kusaba et al. (5) showed that a stimulated diaphragmatic graft around the heart could develop an increase in left ventricular pressure, peak femoral artery pressure, and aortic blood flow in a failing heart. This effect lasted for only 16 min owing to muscle fatigue. In 1959, Kantrowitz, working on the concepts of diastolic counterpulsation, wrapped left canine diaphragm muscle around the descending aorta. The muscle graft was stimulated during cardiac diastole through the intact phrenic nerve by an external stimulator. Kantrowitz reported an increase in diastolic aortic pressure of about 26% until the muscle fatigued several seconds later. Over the next 20 years, there were numerous innovative attempts to use the contractile force of skeletal muscle to assist cardiac function in a number of different ways in the experimental laboratory. Virtually all of these experiments ended in failure because of the rapid fatigue of the skeletal muscle. Muscle fatigue seemed to be an insurmountable barrier to further progress in this field.
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Muscle Transformation
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Buller et al. (6, 7) using cross-innervation experiments found that the contractile properties of skeletal muscle were profoundly determined by the pattern of nerve activity and could be changed by switching the motor nerves to two different types of skeletal muscle. The muscle fiber–type change was from fast-twitch to slow-twitch and slow-twitch to fast-twitch. Slow-twitch muscle is a much more fatigue-resistant type of muscle than those composed predominantly of fast-twitch fibers. Salmons and Vrbova (8) subsequently showed that a similar transformation of fast to slow-type muscle could be achieved by using chronic low-frequency electrical stimulation of the motor nerve to that muscle. In the early 1980s, we suggested that it might be possible, based on the work of Salmons and Vrbova and Pette to transform skeletal muscle and make it fatigue-resistant so that it could be used in various ways to assist the failing heart and circulation (9-11). We worked with different muscles that we thought might be useful for skeletal muscle cardiac assist (12-14). The latissimus dorsi muscle seemed best because it is large, powerful, and nonessential. It has a single major blood supply and single nerve, making mobilization and stimulation of the entire muscle relatively easy. Various stimulation patterns were tested that we felt would be compatible with skeletal muscle cardiac assist. The latissimus muscle could be transformed with many different stimulation patterns from a muscle of mixed fiber types to one of a uniform population of Type I slow-twitch fibers. We also demonstrated with exercise testing that electrically conditioned muscle is much more fatigue-resistant than its contralateral control. The conditioned latissimus dorsi muscle has a higher capillary density, greater capacity for oxidative phosphorylation, more efficient use of oxygen, and greater fatigue resistance (15, 16). This knowledge revived interest in skeletal muscle–cardiac assist research.
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Muscle Stimulation
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The concept of muscle transformation was important, but just as important was learning how to stimulate the skeletal muscle so it could do cardiac-type work. Unlike the myocardium, which can be stimulated directly and the entire heart contracts, skeletal muscle must be stimulated via its motor nerve for effective coordinated contraction.
The force of skeletal muscle contraction is modulated by the number and rate at which fibers are activated. A single electrical stimulus that results in a single muscle twitch does not normally generate sufficient force to augment cardiac function. This is different from the heart, which acts as electrical and mechanical syncytium. Rapid repetitive stimuli delivered to skeletal muscle before the fibers complete their relaxation results in mechanical summation until fusion occurs, thereby causing the muscle to generate substantial force (Figs. 1 and 2)
. Increasing the burst frequency produces more intense contraction and governs the cumulative duration of the active state of the skeletal muscle. A major early contribution to skeletal muscle cardiac assist research was made by Chiu et al. (17, 18) in Montreal, who first reported on burst stimulation for skeletal muscle cardiac assist and who stressed its importance.
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Figure 2. The upper panel shows an electrocardiography (ECG) with superimposed electrical stimuli to the skeletal muscle's nerve. The lower panel shows the tension created by the muscle stimulation. Note the difference in tension created by a single electrical impulse as compared with a burst of electrical stimuli.
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Vascular Delay
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A third important concept is that of vascular delay. For the latissimus dorsi muscle to be used for such procedures as cardiomyoplasty and aortomyoplasty, or used as a separate muscle pump, the muscle needs to be freed from its attachments so that it can be moved to a different location in the body. The thoracodorsal nerve is left intact, as well as the main blood supply, which is the thoracodorsal artery and vein. However, to free the muscle, one must divide numerous blood vessels coming from the intercostal arteries that supply the distal half of the muscle. As a result of this, the distal half and particularly the distal third of the muscle become ischemic. We found early on that if we stimulated the latissimus dorsi muscle immediately after dividing these vessels, which would result in an increased need for oxygen, the color of the distal portion of the muscle turned from light blue to purple. If we continued to stimulate the muscle, the distal portion of the muscle died.
In the early 1980s the concept of vascular delay was already well known to surgeons who moved myocutaneous pedicle flaps from one area of the body to another and to those who worked with muscle grafts. The idea was to free the muscle so that it still had some blood supply, then leave it (or partially move it with a vascular pedicle still intact) for several weeks before moving it to its final location so that the vascular collaterals would improve during this time, resulting in a recovery of blood flow in the graft. However, it was clear to us that we needed to take this concept one step further. It was known that tissue could be moved from one area of the body to another and remain viable. We needed to know whether the measurable recovery in blood flow after the muscle was moved would be enough to allow the muscle to function as it was intended. In fact, for our purposes, the muscle had to function in a much more vigorous and continuous manner, since we wanted the muscle to do cardiac-type work.
Our experiments in the early and middle 1980s confirmed our gross observations. When we ligated the numerous small vessels that supplied blood to the distal portion of the latissimus dorsi, the blood flow there was significantly impaired. During exercise, the blood flow in the proximal half of the muscle increased about six-fold as it had in the distal portion of the muscle before the distal blood vessels were ligated. After the distal blood vessels were ligated, the blood flow in the distal portion of the muscle hardly changed during exercise. However, if we divided the distal vessels, closed the wound, and came back three weeks later and repeated the flow studies, not only did the resting blood flow recover in the distal half of muscle, but more importantly, the exercise-induced increase in blood flow returned (19) (Fig. 3). This was an important finding because for the first time it indicated that we could move the muscle to different locations and still have an adequate blood supply for cardiac-type work (20-22). We now know that the blood supply in the distal half of the muscle, although improved dramatically during the vascular delay period, does not return to normal. This results in a relatively ischemic distal portion of the muscle in some animals and some humans. Some techniques now being studied will likely result in a further increase of the blood flow in the distal muscle where native blood vessels were interrupted.
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Figure 3. Blood flow in the distal latissimus dorsi muscle as measured by radio labelled microspheres. Open squares show the blood flow at rest and exercise in the contralateral control muscle. Open diamonds show the blood flow in the muscle after acute ligation of the collateral feeding vessels to the distal end. Open inverted triangles show blood flow in the mobilized muscle after a 3-week vascular delay. One can see that the vascular delay allows most, but not all, of blood flow recovery.
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Understanding these three important concepts—muscle transformation, techniques for skeletal muscle stimulation, and vascular delay—were necessary for the field of skeletal muscle cardiac assist to go forward.
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Cardiomyoplasty
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Cardiomyoplasty refers to wrapping skeletal muscle, in this case the latissimus dorsi, around the cardiac ventricles and stimulating the muscle graft to contract in synchrony with cardiac systole (Fig. 4). The first clinical application of this technique was in 1985 by Carpentier and Chachques (23). Since then, the technique has been performed worldwide in over 1000 patients.
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Figure 4. Schematic of cardiomyoplasty in which the latissimus dorsi muscle is wrapped around the cardiac ventricles.
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The technique usually involves a single operation. The left latissimus muscle is usually used, although sometimes the right one. Once the muscle is mobilized and detached from the humerus, it is placed inside the chest and wrapped around the cardiac ventricles. A special type of stimulator, somewhat like a pacemaker, is used to stimulate the muscle. One lead is also placed on the cardiac ventricle as a sensing lead. The muscle is first electrically conditioned for several weeks after wrapping it around the heart. This allows for muscle transformation resulting in greater fatigue resistance. The pacemaker is then programmed to deliver appropriately timed stimuli so that the skeletal muscle contracts in synchrony with cardiac systole, usually every other heartbeat. Instead of delivering a single electrical impulse like a heart pacemaker, a burst of stimuli is delivered so that a more effective and forceful contraction of the skeletal muscle will occur.
The effectiveness of cardiomyoplasty is somewhat controversial. It is clear that the majority of patients having this procedure improve clinically, sometimes very dramatically. Typically, patients improve about one and one-half New York Heart Association functional classes for heart failure. The problem has been that there has not been consistent objective improvements in hemodynamics, such as cardiac output, cardiac ejection fraction, and other parameters indicating that the overall hemodynamics have improved. If one temporarily turns the stimulator off, in most cases the changes in hemodynamics are negligible. Interestingly, in some cases of malfunction of the stimulator system, there has been a worsening of the patient's symptoms over several hours to several days. Sometimes there has also been measured deterioration in cardiac function. When the stimulator system is repaired, usually the patient's symptoms improve, and measurements in cardiac function may also improve.
Initially, it was thought that the mechanism of action of cardiomyoplasty was the skeletal muscle compressing the heart ventricles during cardiac systole. This has not been a consistent finding in most patients, despite their improvement in symptoms, leading many to believe that the mechanism of action of cardiomyoplasty is more complex. Lee et al. (24) and Bellotti et al. (25) have shown independently that cardiomyoplasty results in decreased left ventricular wall stress, which in turn results in lower oxygen demand. Our laboratory confirmed this in an ischemic heart failure model in sheep (26). Cardiomyoplasty is probably able to decrease wall stress by reducing the amount of ventricular dilatation seen in heart failure and by increasing the effective wall thickness of the ventricle by adding the skeletal muscle layer.
The effect of cardiomyoplasty on survival is still unknown. Initially, hospital mortality from the procedure was very high, ranging from 19%–31%. However, as experience was gained with the technique, the operative mortality has come down. During the Phase II trials in the United States, hospital mortality was 12% (27), and during the Phase III trials there was only one hospital death in 38 patients (2.6%).
The Phase III clinical trial that started in 1995 was to randomize 400 patients: 200 to cardiomyoplasty and 200 to medical management. However, the recruitment was slow and by November 1998, only slightly over 100 patients had been recruited; therefore, the trials were terminated. The Phase III trial did show that the patients in the cardiomyoplasty limb of the study were much improved over those that were medically managed from a symptoms standpoint. The data for survival at 12 months are about 10% better in the treatment group as compared with the controls, but due to the small sample size, the difference is not statistically significant. Since the Phase III trials were terminated in this country, it may never be known whether patients who have had this procedure live longer than their medically treated counterparts.
The sickest patients, those that are New York Heart Association functional class IV, who are either bedridden or symptomatic at rest, are considered at too high risk for cardiomyoplasty and are usually considered for heart transplants. Currently, cardiomyoplasty is no longer being performed in the United States. It continues to be an accepted treatment for heart failure in Europe and other areas of the world.
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Aortomyoplasty
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Aortomyoplasty is analogous to cardiomyoplasty, but the latissimus dorsi muscle is wrapped around the aorta instead of around the heart (Fig. 5). Again, Carpentier and Chachques (28) were the first to perform an aortomyoplasty in a human in 1992. Since then, at least 28 aortomyoplasties have been performed worldwide. In some cases, the ascending aorta has been wrapped and in others, the descending. Some surgeons have enlarged the aorta by inserting a patch of pericardium or other material so that when the latissimus muscle contracts, a larger volume of blood is displaced thus increasing the amount of diastolic aortic augmentation. The muscle wrap is usually stimulated every other heartbeat and is stimulated during cardiac diastole instead of during cardiac systole, like with cardiomyoplasty.
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Figure 5. Schematic of aortomyoplasty in which the latissimus dorsi muscle is wrapped around the descending aorta. The right side illustrates the use of a pericardial patch to create an aortic aneurysm to allow for displacing a larger volume of blood upon each skeletal muscle contraction.
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The advantages of aortomyoplasty include the technical ease and the lack of manipulations of an enlarged, failing heart. Most patients who have had the procedure report improvement. The disadvantages to the procedure include the potential for the muscle to be wrapped around a potentially diseased aorta, thus causing atherosclerotic material to break loose and embolize. Also if the descending thoracic aorta is wrapped, intercostals have to be divided, which could result in paraplegia. When the ascending aorta is wrapped, it needs to be wrapped where the aorta is adjacent, in fact touching the pulmonary artery. This could result in partial obstruction of the pulmonary artery. Also, in cases where the aorta is surgically enlarged, this is actually similar to putting an aortic aneurysm in the system, and it is unclear how this might be tolerated over time.
Aortomyoplasty at this point should be considered clinical research and although the reports have been promising, more information and longer followup is needed before this procedure can be recommended to the general public.
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Skeletal Muscle Ventricles
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Skeletal muscle ventricles (SMVs) are different from cardiomyoplasty or aortomyoplasty. They are separate pumping chambers constructed from skeletal muscle. The latissimus dorsi is usually the muscle of choice. After the latissimus dorsi is mobilized, it is wrapped around a mandrel, usually in the shape of a multilayered conical spiral. The internal cavity is about the size of the animal's own left ventricle. The skeletal muscle ventricle is then electrically conditioned for about 6 weeks to transform it into a more fatigue-resistant muscle. After this, the mandrel is removed, and the muscle pump is ready to function.
Skeletal muscle ventricles have been connected to the circulation in a number of different configurations (29-35). Some of them have been used to totally replace or bypass the right heart. However, it has been found that the skeletal muscle ventricles are not quite as compliant as the right ventricle and therefore require somewhat higher filling pressures. Because of this, most of the research using skeletal muscle ventricles has focused on assisting the left heart. Skeletal muscle ventricles have been used with valved conduits from the left atrium to the skeletal muscle ventricle to the aorta. In other cases, they have been connected from the left ventricular apex to the skeletal muscle ventricle and then to the aorta. In some cases they are connected to the aorta with either a single-limb conduit or double-limb conduits with the aorta ligated between the two limbs.
Although skeletal muscle ventricles have not been used clinically, in the laboratory they have been found to be a very effective means of cardiac assist over relatively long periods. In the past few years, our laboratory has focused on two configurations of skeletal muscle ventricle for left heart assist. One form is simpler and is referred to as the skeletal muscle aortic counterpulsator. In this configuration, the skeletal muscle ventricle is connected to the descending aorta with two polytetrafluoroethylene (PTFE) conduits. The aorta is ligated between the two conduits so that there is obligatory blood flow through the SMV even if it is not contracting (Fig. 6). The cardiomyostimulator is programmed so that the SMV contracts every other heartbeat during cardiac diastole. We have followed animals with this type of assist device for a number of years (36, 37). Our longest surviving animal was electively sacrificed after the SMV had been functioning effectively in the circulation for more than 4 years. This is probably at least 2 years longer than any other form of skeletal muscle assist or form of mechanical assist has functioned in the circulation. Skeletal muscle ventricles are lined with autogenous pericardium. This is fairly thromboresistant and also prevents the SMVs from rupturing (37).
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Figure 6. Skeletal muscle ventricle (SMV) connected to descending aorta in the aortic counterpulsator model. The SMV is connected to the aorta by two synthetic conduits. The aorta is ligated between the two conduits to allow for passive flow through the SMV. The cardiomyostimulator has two leads, a sensing lead to the heart and a motor lead to the muscle's nerve.
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We have also seeded the skeletal muscle ventricles with endothelial cells (38, 39). These SMVs pumped blood in the arterial circulation for a number of hours (40). To our knowledge, these have been the only experiments where a pump surface has been lined with autogenous endothelial cells, and the endothelial cells have stayed on the pump surface while pumping blood in the arterial circulation. Since the autogenous pericardium is much simpler to use as the lining for the SMV cavity and yields good results, we have not continued the endothelial cell experiments.
In most of our experiments, the animals have temporarily had profound heart failure induced using propranolol, and the skeletal muscle ventricles have been stimulated to function over an hour during the profound low cardiac output (41). We have found that in most cases, the degree of cardiac augmentation is actually better during the low output state than it is when the heart has not been suppressed (Fig. 7).
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Figure 7. Hemodynamic measurements from an SMV in the aortic counterpulsator model comparing the effects at baseline with those when acute heart failure is induced with propanolol. Note the increase in mean arterial pressure (MAP) every other heart beat with the contraction of the SMV. The effects are much more pronounced with the propanolol.
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The other model of skeletal muscle ventricle cardiac assist that shows promise is the model where a valved conduit connects the left ventricular apex to the SMV, and a second conduit connects the SMV to the descending aorta (Fig. 8). This is the most hemodynamically effective form of skeletal muscle cardiac assist that we have studied. Recently, 10 of these pericardial-lined SMV left ventricular apex to aorta models were tested and followed for up to 1 year while pumping blood in the circulation (Fig. 9). The SMV was stimulated during diastole at a 1:2 ratio with the heart. SMV contraction increased femoral pressure by 23% at 33 Hz and 28% at 50 Hz whereas 32% and 33% of the total systemic blood flow, respectively, was pumped by the SMV (42). Five of the animals survived from beyond 6 months to 1 year and in most cases, the SMV function remained stable.
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Figure 8. SMV left ventricular apex to aorta configuration. Note the valves in the afferent and efferent conduit that allows for unidirectional flow.
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Figure 9. Hemodynamic recordings obtained from one animal whose SMV from the LV apex-SMV-aortic position had been pumping continuously in circulation for 1 year. The burst pattern can be seen on the ECG tracing every other heart beat. Note that the aortic root flow decreases after each time the SMV contracts because blood is diverted from the ventricle through the SMV. ECG, electrocardiography; LV pressure, left ventricular pressure.
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Conclusion
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Cardiomyoplasty clearly benefits some patients suffering from heart failure for at least a couple of years. They improve at least one or more functional classes for heart failure. The muscle wrap actively augments ventricular systolic function in some patients, decreases ventricular wall stress in most patients, and prevents further ventricular dilatation in many patients. Since the Phase III trials were terminated in this country, it may never be known whether patients who have had this procedure live longer than their medically treated counterparts.
Aortomyoplasty has been performed in at least 28 patients worldwide. Early reports suggest that symptoms of heart failure have improved. Much more information is needed about the procedure, including longer term followup. This procedure should still be considered clinical research.
Skeletal muscle ventricles are a promising form of skeletal muscle cardiac assist. Measurable hemodynamic benefits can easily be made with the stimulator turned on versus off. It is possible that this form of skeletal muscle cardiac assist may be ready for clinical use within the next few years. Other innovative ways to take advantage of the contractile power of skeletal muscle are being evaluated in laboratories worldwide. For example, some groups are studying the use of skeletal muscle cells implanted into damaged myocardium as a possible way of treating heart failure.
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Footnotes
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1 To whom requests for reprints should be addressed at Division of Cardiothoracic Surgery, Harper Hospital, 2102 Harper Professional Building, 3990 John R, Detroit, MI 48201. 
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Abstract
Introduction
