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Ann Thorac Surg 1996;61:420-425
© 1996 The Society of Thoracic Surgeons
Department of Cardiovascular Surgery, Broussais Hospital, Paris, France
Abstract
Background. Presently the only clinical method of skeletal muscle augmentation of the heart is achieved by wrapping muscle around the cardiac ventricles and then stimulating the muscle to contract synchronously with cardiac systole. Intraaortic balloon counterpulsation provides diastolic counterpulsation in the short-term with the known benefits of increasing diastolic pressure and reducing ventricular afterload. Using protocols already in existence for dynamic cardiomyoplasty we have investigated the long-term use of extraaortic skeletal muscle-powered counterpulsation.
Methods. In five alpine goats the right latissimus dorsi muscle (LDM) was used to achieve a wrap around the ascending aorta, which had been augmented with an elliptic pericardial patch. Electrostimulation protocols were commenced after 2 weeks and continued for 12 to 24 months. At this time baseline hemodynamic measurements were made with and without stimulation of the LDM. Acute cardiac depression was induced and further measurements were made, again with and without stimulation of the LDM.
Results. Results in the basal state demonstrated improvement in all parameters with stimulation and a 23% increase of the subendocardial viability index. After induction of cardiac depression there was a 52% increase in cardiac output, 39% decrease in systemic vascular resistance, and 27% increase in subendocardial viability index. Histologic studies demonstrated tight adhesion between the aortic wall and the LDM, no dilatation of the aortic wall, and no deleterious effects in the aortic wall of the chronic intermittent constriction. Histochemical staining demonstrated transformation of the muscle fibers of the LDM flap into type 1 oxidative muscle fibers.
Conclusions. In conclusion, our present study demonstrates that in this animal model aortomyoplasty produces a chronic counterpulsation with preservation of aortic architecture. With induction of heart failure aortomyoplasty provided an effective means of cardiac assistance. The use of the ascending aorta to achieve diastolic counterpulsation may be an efficient use of skeletal muscle energy to augment the heart in selected clinical cases. Early clinical experience is described in this article.
Intraaortic balloon counterpulsation is widely used in clinical practice to ameliorate severely depressed cardiac function. The described benefits are an increase in coronary artery perfusion pressure and a decrease in left ventricular wall tension, thus respectively optimizing myocardial perfusion and myocardial oxygen consumption. However, intraaortic balloon counterpulsation can only be used for short-term circulatory assistance [1]. We have reinvestigated the concept of extraaortic muscle-powered counterpulsation introduced 25 years ago. The original descriptions reported moderate diastolic pressure augmentation after the use of paced diaphragm muscle flaps wrapped around the descending aorta. Investigators were hindered at that time by insufficient knowledge of muscle biology and myostimulation [2].
Based on experimental data that led us to develop the concept of dynamic cardiomyoplasty at Broussais Hospital [3, 4] we have applied the newly gained fundamental knowledge of muscle-powered cardiac assistance to perform aortomyoplasty. The surgical procedure consists of wrapping of an electrostimulated latissimus dorsi muscle (LDM) pedicled autograft around the ascending aorta to generate a synchronized diastolic compression. Preliminary work in our laboratory has shown that in the experimental animal model that we have chosen, aortomyoplasty necessitates a patch enlargement of the ascending aorta to optimize its efficacy. A biocompatible reservoir is thus created, allowing the powered muscle to act on a larger blood volume [5]. In clinical practice it is hoped that with a large and long ascending aorta in humans it will not be necessary to use patch enlargement of the aorta (Fig 1
).
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Material and Methods
Five alpine goats (mean weight, 47 kg) were used in this chronic experiment. Anesthesia was induced with an intravenous injection of propofol (5 mg/kg). The animals were intubated and mechanically ventilated with a Servo Ventilator (Siemens 900C, Elema, Sweden). Anesthesia was maintained with isoflurane 2% inhalation. Curariform drugs were not used at any stage.
All goats underwent a lateral thoracic incision to provide optimal exposure for careful dissection of the right LDM flap. Two pacing electrodes (model SP 5528; Medtronic, Maastricht, the Netherlands) were implanted into the proximal part of the LDM, which was brought into the right chest after a 5-cm resection of the second rib. Great care was taken to preserve the integrity of the thoracodorsal neurovascular bundle. After closure of the right incision a standard median sternotomy was performed and the ascending aorta, the aortic arch, and collateral vessels were dissected. There are some unfavorable variations in the aortic anatomy of the goat animal model. It is short and of small diameter and the branching pattern of the main arteries differ. To overcome these problems the ascending aorta was enlarged with an elliptic autologous pericardial patch treated intraoperatively with 0.6% glutaraldehyde solution. After side clamping of the ascending aorta the patch was implanted using a 5/0 polypropylene running suture. The mean surface area of the pericardial patch was 253 +/- 24 mm2 (Fig 2
). In all animals the LDM flap was positioned posteriorly with wrapping of the ascending aorta and the aortic arch counterclockwise and thus orientation of the LDM fibers perpendicularly to the longitudinal axis of the aorta (Fig 3
). In the clinical situation it will probably be more suitable to wrap the aorta clockwise, ie, anterior to posterior, and thus avoid compression of the superior vena cava by the LDM (Fig 4
).
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The hemodynamic effects were evaluated at 12 months in 3 goats and at 24 months in the other 2 goats. Hemodynamic data analyzed included left ventricular, aortic, and pulmonary artery pressures and rate of rise of left ventricular pressure (Gould transducer; Gould Inc, Instruments Division, Cleveland, OH). Cardiac output evaluation was performed by the thermodilution technique. The extent of diastolic augmentation was measured by the subendocardial viability index (diastolic pressure time index/systolic tension time index). This was calculated from superimposed tracings of aortic arch and left ventricular pressures [7]. The variation of this ratio (%) was calculated during assisted cardiac cycles (pulse generator functioning in the 1:1 stimulation mode) and 5 minutes after the device was switched off (basal values). Hemodynamic measurements were performed on healthy animals at baseline conditions and after acute pharmacologically induced heart failure using high-dose propranolol hydrochloride (3 mg/kg intravenously). Tracings were recorded for periods of 60 minutes to demonstrate stabilization of results and also to investigate fatigue resistance in the LDM flap.
Samples of the LDM flap, aortic wall, and aortic valve were processed for histologic studies. Anatomopathologic analysis of the kidneys, lungs, liver, and spleen was also performed to eliminate the occurrence of thromboembolic events. Statistical analysis was performed using one-way analysis of variance for repeated measurements to determine differences between or within groups. The 95% confidence limit was chosen as the indicator of significance (p < 0.05).
Results
All hemodynamic data were collected in chronic experimental conditions and after induction of cardiac failure. After 12 to 24 months of chronic diastolic counterpulsation a significant increase of diastolic pressure time index/systolic tension time index persisted at basal state conditions (from 1.13 +/- 0.13 with stimulator off to 1.39 +/- 0.18 with stimulator on; p < 0.05) and after induction of heart failure (from 1.10 +/- 0.10 to 1.40 +/- 0.11; p < 0.05) (Fig 5
). During heart failure aortomyoplasty increased cardiac output from 3.6 +/- 0.5 to 5.5 +/- 1.04 L/min (p < 0.05) and decreased systemic vascular resistance from 1,575 +/- 212 to 1,135 +/- 249 dynescm-5 (p < 0.05).
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Dynamic cardiomyoplasty techniques have shown promising results in humans, and the gain in fundamental knowledge of muscle biomechanics in the development of protocols of use have provoked a surge of interest in other clinical applications of the techniques [812]. The potential benefits of diastolic counterpulsation in circulatory assistance have been long recognized and have gained wide clinical application intravascularly in the form of intraaortic balloon counterpulsation. Interest in dynamic aortomyoplasty was stimulated by its possible use as a complementary technique in extraaortic counterpulsation.
Previous studies on aortomyoplasty have demonstrated that in short-term experimental studies this procedure can reproduce the two fundamental goals of counterpulsation, an increase in diastolic pressure and a reduction in left ventricular afterload [1318]. The results obtained in the present animal model study show that at basal state in goats, an ascending aortomyoplasty causes a 23% increase of the endocardial viability index when the stimulator is activated and a 27% increase after induction of heart failure. A 52% increase in cardiac output was noted in association with a 39% decrease of systemic vascular resistances after the induction of acute heart failure. This improvement was documented for 1 hour, suggesting that the LDM flap had acquired the functional characteristics of fatigue-resistant type 1 myocytes. We have demonstrated that the transformed LDM following a progressive electrostimulation protocol retains biomechanical characteristics allowing an effective aortic counterpulsation. These data emphasize that aortomyoplasty can be efficient chronically as a cardiac assist system.
The duration of muscle electrostimulation was adapted to permit optimal muscle contraction. Similarly, muscle relaxation occurred promptly enough not to interfere with left ventricular systole. This was confirmed by a significant drop of the arterial pressure wave after assisted diastole. The question of whether such circulatory assistance would still be efficient at higher cardiac rates is incompletely answered. It could be expected that owing to reduced speed of shortening and relaxation, characteristic of fatigue-resistant slow muscle fibers, muscles composed completely of slow fibers would be suboptimal at high cardiac frequency. However, recent data suggest that complete transformation into the slow myosin isoform is not necessary for optimal chronic performance of dynamic stimulated muscle. Thus, electrical preconditioning of muscle may be used to induce fast fatigue-resistant muscle with advantageous biomechanical characteristics for the purposes of aortomyoplasty [19].
Initial aortomyoplasty animal studies have used the descending aorta as the site of counterpulsation [2]. In our experimental approach we chose the ascending aorta instead of the descending aorta based on potential benefits. By using the ascending aorta in our experiments we hoped to gain the maximal mechanical advantage of placing a counterpulsation as close to the pulse origin as possible. Diastolic augmentation of coronary blood flow is optimized. The diameter of the ascending aorta is larger than that of the descending aorta. Use of the ascending aorta avoids the risk of iatrogenic paraplegia, as adequate wrapping of the descending aorta necessitates dissection and division of spinal artery branches of the aorta. In our experimental goat model, presenting a narrow and short ascending aorta, we have shown that patch enlargement of the aorta may improve the efficacy of the procedure. This technique has created a biocompatible autologous reservoir very close to the aortic valve and continuously washed out by the anterograde left systolic ejection volume. Important also is the avoidance of use of prosthetic chambers in using aortomyoplasty and thus the avoidance of the associated risk of thromboembolism that is prevalent in animals or patients with low cardiac output.
The histologic findings related to the aortic wall have shown an excellent tolerance of the three layers of the aortic wall layers to the continuous concentric squeezing. The patch enlargement of the ascending aorta did not lead to aneurysm formation in the long-term.
These results therefore suggest that aortomyoplasty is an effective application of muscle-powered left ventricular assistance. Long-term studies such as this one are a prerequisite to introduction of this technique as a surgical treatment for chronic left heart failure. The procedure may find an indication in patients in whom dynamic cardiomyoplasty is not possible such as extremely dilated cardiomyopathies (eg, cardiothoracic ratio >60%; left ventricular end-diastolic diameter >75 mm), or contraindicated as with mitral valve insufficiency. Routine preoperative magnetic resonance imaging to demonstrate a normal aorta free of atherosclerosis or calcification would be mandatory. The aortic valve and its function must be assessed. Aortic valve regurgitation, Marfan's syndrome, or any other dystrophic disease of the aorta would represent absolute contraindications to aortomyoplasty.
A major advantage in the clinical use of the aortomyoplasty technique is the fact that it may be performed without the use of cardiopulmonary bypass. Further developments in aortomyoplasty and its clinical application will be in conjunction with further investigation in the field of dynamic cardiomyoplasty: improving protocols of myostimulation, improvements in cardiomyostimulators, growth of knowledge on stimulation, and conditioning of muscle. We have recently performed combined aortic and pulmonary artery counterpulsation experimentally in dogs [20]. Dynamic aortomyoplasty was performed by wrapping the left LDM around the upper third of the descending aorta, and dynamic ``pulmonaromyoplasty'' was achieved by wrapping the pulmonary trunk with a right LDM muscle flap (Fig 9
). Muscle stimulation parameters such as synchronization delay, pulse amplitude, pulse width, burst rate, and burst duration were modified according to the characteristics of the hemodynamic parameters in both arteries to avoid competition with natural systole. Aortopulmonary counterpulsation resulted in an improvement in all measured hemodynamic parameters. There was a significant increase in mean aortic pressure, mean pulmonary artery pressure, and cardiac output. In addition, a significant decrease was observed in end-diastolic left ventricular pressure.
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In conclusion, our present study demonstrates that in an animal model aortomyoplasty produces a chronic counterpulsation with preservation of aortic architecture and aortic diameter. After induction of heart failure aortomyoplasty offers an efficient circulatory support without thromboembolic risk. Present results suggest the clinical feasibility of this promising approach to biomechanical-assisted circulation.
Dynamic Aortomyoplasty: Clinical Experience
Since November 9, 1992, the date of the first clinical aortomyoplasty case performed at Broussais Hospital, 14 aortomyoplasty procedures have been performed worldwide. Patients (10 men and 4 women) have been operated on at Broussais Hospital (3), Marseille, France (2), Jeddah, Saudi Arabia (7), and Buenos Aires, Argentina (2).
The mean age of patients was 56 +/- 7 years. The cause of left ventricular failure was ischemic cardiomyopathy in 9 and idiopathic dilated cardiomyopathy in 5. An important cardiomegaly was present in most of these patients. The mean cardiothoracic ratio was 0.69 +/- 0.5, and the mean end-diastolic left ventricular diameter was 82 +/- 6 mm (measured by echocardiography). All patients possessed a normal aortic valve function and aortic wall.
The mean preoperative New York Heart Association functional class was 3.4, and the mean left ventricular ejection fraction (radioisotopic) was 0.16 +/- 0.04. Associated cardiac pathologies were mitral insufficiency in 6, atrial fibrillation in 2, pulmonary vascular hypertension (unresponsive to vasodilator drugs) in 4, severe ventricular arrhythmia in 3, and diffuse calcification of the left ventricular wall in 1. In 2 patients biventricular heart failure was present, and 1 patient had had previous myocardial revascularization (3 coronary artery bypass grafts). Associated extracardiac pathologies were insulin-dependent diabetes in 2, respiratory insufficiency in 2, gastric ulcer in 1, polycystic kidney disease in 1, and breast cancer in 1. Most of those patients presented contraindications for heart transplantation.
Aortomyoplasty techniques consisted of 11 ascending aorta wrappings (in 1 case the aorta was enlarged with a pericardial patch) and 3 descending thoracic aorta wrappings. The right LDM was used to wrap the ascending aorta, and the descending aorta was wrapped with the left LDM. Cardiopulmonary bypass was not used in any of the cases presented. In 6 patients an intraaortic balloon pump was used during the perioperative period.
The tension applied to the LDM during aortic wrapping seems to be of great importance for the effectiveness of aortomyoplasty because the aortic diameter is not very large.
In-hospital mortality (before LDM stimulation) was 14% (2 of 14 patients). Causes of perioperative mortality were heart failure in 1 patient and multiorgan failure in another. Four patients died during the follow-up period (4 of 11; 36%). Causes of death included sudden death in 3 and septicemia in 1.
Current clinical evaluation (mean follow-up, 9 months) shows a significant improvement of the functional class and the quality of life of operated patients. Hemodynamic and Doppler echocardiographic studies demonstrated diastolic augmentation and compression of the aorta during LDM electrostimulation. It seems that dynamic aortomyoplasty has the potential to be an efficient technique to assist patients with severe refractory cardiac failure. A larger clinical experience and a longer follow-up period are necessary to clearly assess the benefits of this procedure.
Footnotes
Presented at The Third International Conference on Circulatory Support Devices for Severe Cardiac Failure, Pittsburgh, PA, Oct 28-30, 1994.
Address reprint requests to Dr Chachques, Department of Cardiovascular Surgery, Hôpital Broussais, 96, Rue Didot, Paris 75014.
References
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