Ann Thorac Surg 1996;61:138-142
© 1996 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Association of Latissimus Dorsi Muscle Expansion With Electrostimulation Before Cardiomyoplasty
Juan Carlos Chachques, MD, PhD,
Michel Tapia, MD,
Marc Radermercker, MD,
Michel Pellerin, MD,
Jean F. Fuzellier, MD,
Michael J. Tolan, Frcs(I),
Xavier Renard, MD,
Vladimir Mitz, MD,
Alain F. Carpentier, MD, PhD
Department of Cardiovascular Surgery, Broussais Hospital, Paris, France
Accepted for publication September 11, 1995.
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Abstract
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Background. The principle of cardiomyoplasty is chronic electrostimulation of the latissimus dorsi muscle (LDM) flap wrapped around the heart to obtain a phasic activity that can be integrated to ventricular kinetics. In clinical cardiomyoplasty procedures, a complete wrap of both ventricles by the LDM cannot always be obtained in cases of extremely dilated hearts. This is due to the limited LDM length available for wrapping. In most of these cases, benefits of cardiomyoplasty are very limited. We have investigated the feasibility of progressive LDM expansion associated with electrostimulation. The aim was to increase the muscle area before cardiomyoplasty, while preserving the electrophysiologic characteristics of muscle fibers.
Methods. In 5 goats, a silicone LDM expander with two incorporated muscular pacing electrodes was inserted deep into the LDM through a paravertebral incision along the posterior edge of the muscle. The pacing leads were connected to a myostimulator implanted in a subcutaneous pocket. The expander was progressively inflated over 8 weeks, up to 500 mL. Simultaneously the LDM was electrostimulated.
Results. At 2 months planimetric studies demonstrated an increase of the LDM surface from 175 ± 12 to 229 ± 17 cm2 (+31% ± 4%; p < 0.05). The expanded LDM showed preserved electrophysiologic characteristics. The analysis of biopsy samples revealed histologic integrity of muscle fibers and preservation of their mean diameter.
Conclusions. Potential benefits of this procedure are (1) increase of muscle surface, (2) training of muscular fibers and preservation of muscular tone, and (3) division of the distal vascular supply at implantation, which may potentiate vascularization from the LDM main pedicle. An LDM expansion could be considered before cardiomyoplasty in cases of significant heart dilatation. This device was successfully implanted in 2 patients, 2 months before cardiomyoplasty. Cardiomyoplasties were performed without difficulty, and a complete biventricular wrap was obtained in both patients in spite of massive cardiomegaly.
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Introduction
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Dynamic cardiomyoplasty, a surgical procedure that combines cardiac and plastic surgery with electrophysiology and biomedical engineering, was conceived to enhance cardiac performance by assisting ventricular contraction using an electrostimulated latissimus dorsi muscle (LDM) flap wrapped around the heart [1, 2].
The growing interest in skeletal muscle flap use in plastic and reconstructive surgery stimulated the development of the cardiomyoplasty technique. Long-term electrical activation of skeletal muscles has already been used in various other clinical situations such as chronic generation of correcting forces to reduce developing skeletal deformities (eg, scoliosis), muscle stimulation to restore functions lost as a result of trauma or disease, diaphragmatic or phrenic nerve stimulation for respiratory support, detrusor-myoplasty to restore micturation, and surgical creation of a neo-sphincter using an electrostimulated gracilis muscle in colorectal surgery [3].
Cardiomyoplasty is appropriate for patients with severe chronic heart failure refractory to optimal medical treatment. These clinical conditions include several causes: ischemic, neoplasic, dysplastic, viral, and all nonobstructive cardiomyopathies. The efficacy of cardiomyoplasty is based on the contact area between the heart and the transposed LDM. A complete myocardial wrapping, where the LDM flap surface area is sufficient to completely cover both left and right ventricles, provides maximal assistance. As demonstrated in experimental and clinical studies, a systolic augmentation during synchronous LDM flap contraction and an improved diastolic pressure-volume relationship permit reestablishment of cardiac reserve and prevent further heart dilatation [4–6].
Translation of these principles to clinical practice may be limited by inability to completely wrap the heart with muscle due to both lack of available LDM flap surface area and cardiomegaly. This situation is a constant finding in patients with cardiothoracic ratio greater than 0.60 and left ventricular end-diastolic diameter greater than 75 mm. In these cases the cardiomyoplasty procedure can be performed using an autologous pericardial patch or flap to complete the cardiac wrapping (Fig 1
). However, the long-term benefits of cardiomyoplasty in most of these patients have been very limited [2, 7, 8].
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Fig 1. . Technique of cardiomyoplasty. First the latissimus dorsi muscle (LDM) is positioned between the ventricles and the diaphragm and fixed to the pericardium, using two mattress U sutures placed at the vicinity of the main pulmonary artery (A) and the inferior vena cava (B). (B) The wrapping is completed by suturing the LDM itself and by fixing the anterior part of the LDM to a pericardial flap tailored from the right edge of pericardiotomy. This technique avoids heart manipulation, thus reducing the risk of hemodynamic deterioration and arrhythmias.
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Use of balloon expanders to increase the surface of subcutaneous and cutaneous layer has been widely used in plastic and reconstructive surgery. This technique has been reliable and effective [9–11]. We have adapted this principle with specific technical modifications to potentiate the LDM surface area and contractility in a cardiomyoplasty model.
The purpose of this experimental study was to analyze the qualitative and quantitative effects on an LDM flap resulting from prior balloon expansion associated with electrostimulation of muscle fibers. Evaluation was made of the surface of the LDM with respect to area, and also a histologic examination was made of the contact area with the expander. The effects of preoperative electrostimulation were studied, as were the effects of division of the distal blood supply to the LDM flap. Preliminary results of our first clinical applications and surgical experience are provided.
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Material and Methods
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The experimental data were obtained from the study of 5 adult goats implanted with LDM expanders. The balloon expanders were triangular and were made of silicone (Sigma Medical, Nanterre, France). The size and shape were specially designed according to the LDM anatomy [12]. The maximal inflation volume was 900 mL. The device was connected to a valved chamber allowing progressive percutaneous inflation of the balloon. The thoracic surface of the expander was fitted with suturing areas to avoid any displacement after implantation. Two electrodes (model SP 5528; Medtronic, Maastricht, the Netherlands) were located on the external surface of the expander to deliver bipolar electrostimulation to the LDM (Fig 2).
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Fig 2. . Graphic representation of the balloon implanted beneath the latissiumus dorsi muscle, including a valved chamber (arrow) for progressive percutaneous inflation, and two pacing leads connected to an Itrel myostimulator (MYOST).
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Surgical Procedures
Five alpine goats (mean weight, 52 kg) were used. General anesthesia was induced by intravenous administration of propofol (5 mg/kg) and maintained by inhalation of isoflurane (2.5%). Operation was performed on animals in the right lateral decubitus position. A 10- to 15-cm left paravertebral incision was made to provide direct access to the LDM thoracolumbar aponeurosis. This fascia was opened longitudinally and the dissection was carried out beneath the distal half of the LDM. At this time, collaterals from the intercostal arteries to the latissimus dorsi were divided. Thereafter, blunt dissection was continued to the tip of the scapula.
In this manner, a space was created underneath the LDM to introduce and place the expander, which was secured to the chest wall with four simple (3-0) polypropylene sutures. The thoracolumbar aponeurosis was carefully closed and a subcutaneous pocket was created to allow the implantation of an Itrel myostimulator (Medtronic), which was connected to the LDM pacing leads.
The postoperative filling of the expander was started 1 week after operation, and by progressive injection of saline solution it was inflated to 500 mL at 8 weeks (Fig 3). This limit of 500 mL avoided overstretching of LDM fibers and skin. This was assessed by palpation at every infusion of fluid.
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Fig 3. . The latissimus dorsi expander is filled with saline solution. The pacing electrodes, located on the external surface of the expander, are coupled to an Itrel Medtronic pulse generator.
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Electrostimulation Protocol
After a 5-day recovery period animals underwent a 7-week incremental conditioning program. The voltage, pulse frequency, and rate of electric stimulation were gradually increased. Target stimulation was 8 to 10 V, pulse width was 300 microseconds, and burst frequency was 30 Hz, with 6 pulses per burst and 40 bursts per minute (asynchronous with the heart). The LDM surface area was measured by planimetry at implantation of the balloon expander and after 10 weeks. The electrophysiologic data included LDM thresholds of contraction and muscle impedance.
Histologic and Histochemical Studies
Biopsy samples of the cross-sectional area of the LDM were obtained in the proximal and distal parts of the muscles 10 weeks after balloon implantation. These specimens were submitted to routine pathologic analysis including hematoxylin-eosin and hematein-phloxin-saffron histologic staining. Histochemical studies of the LDM fibers were also performed.
Statistical Analysis
Results are expressed as mean ± standard error of the mean. Repeated-measures analysis of variance was used to analyze the data. A p value less than 0.05 was considered significant.
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Results
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The inflation of the expander was well tolerated and achieved in an 8-week interval. The position of the expander remained stable throughout the study, and no surgical wound complications were encountered. The evaluation of the LDM surface area after 10 weeks demonstrated a significant increase of the LDM surface from 175 ± 12 to 229 ± 17 cm2 (+31% ± 4%; p < 0.05) (Table 1).
After complete dissection, the LDM flap looked healthy and thicker. At the expander-muscle interface a thin fibrous tissue layer had developed, which did not interfere with muscle contractility. The electrophysiologic values remained stable as far as first-twitch threshold and full recruitment threshold were concerned (see Table 1
). Muscle impedance decreased at 10 weeks (from 1,526 ± 78 to 342 ± 62 ohms; p < 0.05). The reduction of impedance between the leads can be explained by an increased contract area between the pacing electrodes (fixed on the external surface of the balloon) and the LDM after inflation of the expander.
The analysis of biopsy samples revealed histologic integrity of muscle fibers, which had maintained their mean diameter. There was no change in the muscular and neurovascular anatomy (Fig 4). A thin layer of connective fibrous tissue was found in the deep surface of the LDM flap (Fig 5).
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Fig 4. . Histologic study of the latissimus dorsi muscle expansion associated with electrostimulation, showing preserved myofibrillar structure and normal fiber diameter. (Hematein-phloxin-saffron stain; x320 before 47% reduction.)
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Fig 5. . A thin layer of connective tissue developed between the expander and the latissimus dorsi. Latissimus dorsi muscle fibers in contact with the balloon have a reduced diameter. (Hematein-phloxin-saffron stain; x320 before 47% reduction.)
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The adenosine triphosphatase stain demonstrated a high rate of transformation of latissimus dorsi glycolytic type II fibers into fatigue-resistant type I oxydative fibers. The fiber distribution in the LDM after expansion and electrostimulation showed 78% ± 6% type I oxidative fibers (versus 34% ± 4% of oxidative fibers in control LDMs). The mean LDM fiber diameter after expansion and electrostimulation was 16 ± 2 µm for type I fibers (versus 14 ± 3 µm before expansion; p = not significant) and 21 ± 4 µm for type II fibers (versus 18 ± 3 µm before expansion; p = not significant).
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Comment
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Concept and Experimental Study
The clinical experience in reconstructive surgery with balloon expanders has already shown the efficacy of this technique to progressively increase the surface area of soft tissues and muscles. This process is safe and reversible [9–11]. This phenomenon is quite similar to the abdominal wall overdistention during pregnancy, which does not demonstrate late functional damage.
Anthropologists have reported numerous examples of induced tissue expansion among primitive tribes. Amazonian indians enlarge their lips by placing spacers between their gums and lips. This is also customary in Africa (Kenya and Chad), where women enlarge earlobes.
It was therefore thought that the use of tissue expansion techniques could be used to augment LDM surface area and would enhance cardiac wrapping in cardiomyoplasty procedures. This study has shown that using a silicone expander inflated with 500 mL of saline solution, a 31% increase in LDM surface area can be obtained.
Owing to the specific design of the expander (for the purpose of cardiomyoplasty) not only did this technique increase the muscle flap surface area, but also there were qualitative improvements. The positioning of the expander required ligation of collaterals from intercostal and lumbar arteries. The subsequent interval before the myoplasty procedure may induce improved supply from the principal thoracodorsal vascular bundle. It is known that natural anastomoses exist between the proximal thoracodorsal blood supply and the peripheral blood vessels from intercostal and lumbar arteries [9]. In the acute setting, the distal border of the LDM flap is usually cyanotic, suggesting reduced blood flow. The positioning of the expander underneath the LDM may therefore prepare the muscle for exclusive vascularization from the thoracodorsal pedicle and development of collaterals to the distal aspect of the LDM flap [13, 14].
The progressive increase of the balloon expander volume slowly stretches the LDM and consequently increases its tension. It has been shown [15] that stretching not only promotes the transformation of type II glycolitic to type I oxidative fatigue-resistant muscle fibers, but also results in physical reinforcement of the muscle due to a better actin myosin length-tension relationship. Furthermore, it was also demonstrated that when combined, stretching and electrical stimulation induce rapid and marked growth of muscles [16]. Stretch by itself is also anabolic, causing useful lengthening of muscles and preventing collagen accumulation. In contrast, muscle inactivity leads to rapid atrophy, fiber shortening, and reduced muscle compliance.
In our experimental study, the LDM was stimulated with a progressive protocol. This was done to avoid overdistention of the muscle and to acquire fatigue resistance from electrical stimulation. Preconditioning ``in situ'' of LDM flap preoperatively results in not only metabolic muscle transformation but also optimal bioenergetic profile and preserved muscle physiology [17]. These considerations support the concept of in situ muscle preparation with balloon expander and associated myostimulation protocol. This management may provide the LDM flap with improved biomechanical performance and therefore improved cardiac assistance [18].
Benefits of cardiomyoplasty in patients with advanced heart disease are now being documented. Long-term improvement of physical activity and work performance was observed in most of the patients operated on. The experimental work [3, 4] has allowed us to progress to clinical application of the cardiomyoplasty technique in the human (January 1985). Presently (September 1995) our clinical experience involves 82 patients. Current worldwide experience with this technique involves more than 600 cases. Long-term results after cardiomyoplasty are very encouraging. The Broussais Hospital series shows at 7 years an actuarial survival of 52% (hospital mortality included). Recent basic and clinical data have shown that cardiomyoplasty effects on ventricular performance are due to (1) augmentation of pump function, (2) limitation of cardiac dilatation, (3) reduction of ventricular wall stress, and (4) reverse remodeling of the left ventricular geometry [5, 6, 19–22].
Latissimus Dorsi Expansion-Electrostimulation: Clinical Experience
We have recently implanted 900-mL balloon expanders in 2 patients 10 weeks before cardiomyoplasty. Both patients had refractory congestive cardiac failure (one ischemic and one idiopathic cause) with extremely dilated hearts (cardiothoracic ratio > 0.60) (Fig 6). The progressive inflation of the device was well tolerated and effectively resulted in muscle augmentation as well as an increased vascular supply of the distal margin of the LDM flap. The vascularization was excellent, without any signs of distal ischemia.
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Fig 6. . (A) Muscle expander implanted before cardiomyoplasty in a patient with severe biventricular heart failure and an extremely dilated heart. (B) A paravertebral incision was used to insert the expander.
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This muscle was used to perform a complete myocardial wrap in both patients, in spite of massive cardiomegaly. The postoperative course was uneventful, and there were no complications related to balloon expansion.
Conclusion
In conclusion, potential benefits of LDM expansion associated with electrostimulation 2 months before cardiomyoplasty are (1) increase in muscle surface area, (2) training of muscular fibers and preservation of muscular tone, and (3) division of the distal vascular supply at implantation, which may potentiate better myocyte vascularization from the LDM main pedicle. An LDM expansion can be considered before cardiomyoplasty in cases of extreme heart dilatation. The association of expansion with electrostimulation of other skeletal muscles may be useful for the development of new techniques in the field of plastic and reconstructive surgery.
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Footnotes
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Address reprint requests to Dr Chachques, Department of Cardiovascular Surgery, Broussais Hospital, 96 rue Didot, 75014 Paris, France.
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Abstract
Introduction
