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Ann Thorac Surg 1996;61:93-98
© 1996 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Descending Thoracic Aortomyoplasty: A Technique for Clinical Application

Division of Cardiothoracic Surgery, Department of Surgery, University of Medicine and Dentistry of New Jersey, Cooper Hospital/University Medical Center, Camden, New Jersey

Accepted for publication August 18, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. Descending thoracic aortomyoplasty is a form of skeletal muscle-powered cardiac assistance. Its use in clinical settings has been limited by the ligation of intercostal arteries necessary to complete a circumferential wrap of the aorta with the latissimus dorsi.

Methods. This study assessed the feasibility and the efficacy of aortomyoplasty constructed with a modified latissimus dorsi. A pericardial patch was attached to the latissimus dorsi and divided around the preserved intercostal arteries. Nine alpine goats (37 ± 2 kg) underwent descending aortomyoplasty using this technique. All intercostal arteries were preserved. After a 6-week recovery period, the animals underwent a 6-week, incremental electrical conditioning program. After 90 postoperative days, animals were examined under anesthesia with the myostimulator on and off.

Results. Aortomyoplasty activation resulted in augmentation of mean diastolic aortic pressure by 16.0 ± 0.9 mm Hg (23%). Significant improvements in cardiac index (40%), stroke volume index (37%), left ventricular stroke work index (49%), and mean arterial pressure (19%) were noted. An intravascular sonographic probe placed in the descending aorta revealed circumferential compression of the aorta during counterpulsation. Mean cross-sectional aortic area was reduced by 51.8%, from 210.1 ± 7.1 to 108.9 ± 6.7 mm² during aortomyoplasty activation (p < 0.05). Histologic analysis confirmed the long-term patency of intercostal arteries.

Conclusions. Descending aortomyoplasty, modified with an interposing patch of pericardium, effectively transfers skeletal muscle force across the aortic wall and assists cardiac function. This technique allows preservation of all aortic branches, and with this novel approach, the clinical utility of aortomyoplasty can now be explored.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The use of autologous skeletal muscle in cardiac assistance has been under investigation for at least three decades. However, clinical application of this concept was not reported until 1985, when latissimus dorsi (LD) cardiomyoplasty was first attempted in humans. The limited success of cardiomyoplasty in clinical trials has encouraged the development of ascending and descending thoracic aortomyoplasty. Both aortomyoplasty techniques have been reported in acute [1, 2] and chronic [3, 4] experimental settings. Aortomyoplasty is associated with effective augmentation of cardiac function in animals with normal and impaired cardiac function.

The theoretical model of descending thoracic aortomyoplasty is based on the principle of aortic counterpulsation. In animal studies of heart failure [5], descending thoracic aortomyoplasty has demonstrated hemodynamic effects comparable to those achieved with an intraaortic balloon pump (IABP). However, the consistent limitation of descending aortomyoplasty has been the ligation of intercostal arteries, which branch from the descending aorta. Interruption of the vascular supply to the spinal cord is not a practical clinical maneuver because of the risk of neurologic compromise. This drawback has been the primary barrier to the clinical application of descending thoracic aortomyoplasty.

Although modifications of descending aortomyoplasty that would preclude the need for ligation of intercostal arteries have been theorized [4] and attempted [3] in experimental models, none have achieved sufficient success to progress to a clinical trial. This study was designed to assess a novel approach to descending aortomyoplasty using pericardial patch-modified LD. This may make aortomyoplasty suitable for clinical use because all intercostal arteries are preserved. The objectives of this study were to confirm that (1) skeletal muscle force is sufficiently transferred across the aortic wall during long-term counterpulsation despite an interposing band of pericardium and (2) that effective cardiac assistance can be generated with pericardial patch-modified aortomyoplasty.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Nine adult, male alpine goats weighing 37 ± 2 kg were anesthetized with intravenous ketamine (25 mg/kg) and thiopental (10 mg/kg) after a 72-hour fast of solid food and 12 hours of no oral intake. After endotracheal intubation and nasogastric suction, anesthesia was maintained with an inhaled mixture of 100% oxygen and 2% halothane (Halocarbon Labs, River Edge, NJ) and placed in the right lateral decubitus position. Continuous measurements of electrocardiogram, arterial oxygen saturation, and end-tidal CO₂ were recorded (SpaceLabs Computer Analysis System; Spacelabs, Redmond, WA) and periodic arterial blood gas analysis was performed with a blood gas analyzer (Stat 7; Nova Biomedical, Newton, MA). The left carotid artery was isolated surgically and an 8F, 12-cm fluid-filled catheter was positioned in the aortic root for pressure analysis and blood sampling.

A 40-cm oblique incision was created over the medial border of the left LD muscle, extending from the apex of the left forelimb to the edge of the 12th rib. The LD was harvested by sharp dissection with preservation of the neurovascular pedicle, off all bony insertions and left intact at its origin. A bipolar, pacing electrode (model 050-003; Telectronics Corp, Englewood, CO) was placed in a woven fashion adjacent to the neurovascular bundle. The second rib was resected partially to facilitate the transfer of the LD flap into the thoracic cavity. Through a fifth interspace left anterolateral thoracotomy, dissection of the aortic adventitia was initiated just distal to the left subclavian artery, extending for 7 to 10 cm on the descending aorta. The aorta was dissected such that all intercostal arteries were preserved.

A glutaraldehyde-treated segment of bovine pericardium (Medtronic Inc, Minneapolis, MN) 7 to 10 cm in length, 1 cm in width was then fashioned as an extension to the distal aspect of the LD flap, with interrupted sutures of 2-0 Vicryl (Ethicon, Somerville, NJ) (Fig 1). Divisions of the pericardium were created to correspond to the intercostal arteries. The LD with its pericardial extension was wrapped in a clockwise circumferential manner around the aorta, and the free end of the pericardium was approximated to the proximal aspect of the LD with 2-0 Vicryl running sutures. The completed wrap was constructed such that on cross section three-quarters to seven-eighths of the circumference was covered by LD, allowing free passage of the intercostal arteries (Fig 2).

View larger version (24K): [in this window] [in a new window]   Fig 1. . Schematic representation of descending thoracic aortomyoplasty with pericardial extension (A) of the latissimus dorsi muscle (B). Extension of latissimus dorsi muscle with pericardium is completed first. The pericardium is then tapered and fashioned to the intercostal arteries. The wrap is completed with preservation of the intercostal vessels.

View larger version (38K): [in this window] [in a new window]   Fig 2. . Right lateral decubitus schematic representation of descending thoracic aortomyoplasty with pericardial extension on cross-section. (A = pericardial patch; AO = aorta; B = latissimus dorsi.)

The myostimulator was inactivated during a 6-week ``vascular healing'' period, after which it was programmed (CardioSynchronous Myostimulator Programmer CSM V3.41C; Telectronics) for incremental electrical conditioning of the muscle flap. The voltage, pulse frequency, and rate of electrical stimulation were gradually increased (Table 1). Target stimulation was 5 V, pulse width 0.65 ms, frequency 30 Hz, and 6 pulses per burst synchronized at a 3:1 ratio. The myostimulator was programmed to stimulate muscle flap counterpulsation through a 386.7-ms delay from the R wave of the electrocardiogram. This delay has been established after repeated adjustments to attain optimal diastolic augmentation.

Through a midline laparotomy incision, the abdominal aorta was isolated and a 10F, 120-cm intravascular sonographic probe (Intracardiac Catheter, model C1010; Cardiovascular Imaging Systems, Inc, Sunnyvale, CA) was placed into the descending thoracic aorta at the level of the aortomyoplasty. Sonographic images of the aorta over a 15-minute observation period were displayed on a CVIS-INSIGHT monitor and cross-sectional transverse aortic areas were computed during aortomyoplasty activation and relaxation (model I5006; Cardiovascular Imaging Systems). Images were taken at different levels of the aortic wrap to confirm consistent aortic luminal narrowing along the length of the wrap during activation of the aortomyoplasty.

Upon completion of the research protocol, animals were euthanized with Somlethal (J.A. Webster Inc, Sterling, MA). During necropsy, the aortomyoplasty and adjacent aorta were removed en-bloc and fixed in 10% buffered formalin for sectioning and histopathologic analysis. A two-dimensional computer image capturing system (Mocha Automated Image Analysis System, version 1.2; Jandell Scientific, San Raphael, CA) was used for analysis of microscopic images. Intercostal artery patency was examined using light microscopy analysis after hematoxylin and eosin staining was performed.

Statistical analysis was performed using an IBM SPSS PC PLUS (version 3.0) package. Independent t test was used for statistical comparison between groups. A p value of less than 0.05 was considered statistically significant. Data are presented as mean ± standard error of the mean where appropriate.

All animals received humane care in compliance with the ``Guide for Care and Use of Laboratory Animals'' published by the National Institutes of Health (NIH publication 85-23, revised 1985).

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Nine animals underwent successful aortomyoplasty with complete preservation of the intercostal arteries. No neurologic sequelae were identified after aortomyoplasty. Seroma formation was associated with the postoperative course in 3 of 9 animals. All were treated with prompt surgical drainage. Although limping was noted in all animals during the first postoperative week, no lasting functional deficit was identified.

Hemodynamic data during aortomyoplasty activation demonstrate augmented cardiac function (Table 2). Figure 3 displays simultaneous aortic root pressure and electrocardiographic readings in a representative sample of 90-day counterpulsation. Mean diastolic aortic pressure increased 23%, from 68 ± 1 to 84 ± 2 mm Hg (mean augmentation, 16 ± 6.9 mm Hg) during counterpulsation.

View larger version (54K): [in this window] [in a new window]   Fig 3. . Representative electrocardiogram and aortic root pressure tracing after chronic (90 days) descending thoracic aortomyoplasty. (arrowheads = aortic diastolic pressure deflection; asterisks = pulse burst.) Myostimulator set to a 1:3 ratio. Each box is equivalent to 5 mm; paper speed (A) 6.25 mm/s, (B) 25 mm/s.

View larger version (121K): [in this window] [in a new window]   Fig 4. . Intravascular two-dimensional sonographic images of the descending thoracic aorta during (A) aortomyoplasty relaxation and (B) aortomyoplasty activation.

View larger version (156K): [in this window] [in a new window]   Fig 5. . Computer-enhanced image of a representative histologic section (hematoxylin and eosin) of aortomyoplasty (original magnification, x4) with patent intercostal artery at 90 days. (A = patent intercostal artery; B = aortic wall; C = latissimus dorsi; D = pericardial patch.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

Descending thoracic aortomyoplasty has been under investigation as a cardiac assist device, and has been demonstrated to effectively alter the hemodynamics of normal and failing ventricles [2–5]. The proposed mechanism of descending aortomyoplasty cardiac assistance is modeled on the IABP. Descending aortomyoplasty and the IABP are based on effective afterload reduction and diastolic augmentation. Several investigators [3, 8, 9]Au: have renumbered references; #8 not cited in sequence have described effective descending aortomyoplasty created with a circumferential wrap of LD around the aorta. This requires ligation of two to three pairs of intercostal vessels. In these studies diastolic augmentation was noted from 12 weeks to 12 months in animals with normal cardiac function and in models of ischemic heart failure. In addition, Constance and colleagues [2] documented similar improvements in cardiac function in a model of chemically induced congestive heart failure.

Using a circumferential wrap of the aorta with ligation of several pairs of intercostal arteries, Lazarra and associates [4] have demonstrated augmentation of diastolic aortic root pressures, indices of left ventricular contractility, diastolic relaxation mechanics, and increases in diastolic aortic velocity in the nonfailed canine heart. Significant improvements in endocardial viability and indices of myocardial oxygenation were also identified with descending aortomyoplasty. These investigators were able to document effective counterpulsation up to 274 days.

In a study comparing IABP use and descending thoracic aortomyoplasty, Lazarra and co-workers [5] identified several unique and unexpected aspects of cardiac assistance with descending thoracic aortomyoplasty in an experimental model of dilated cardiomyopathy. Although both IABP and descending aortomyoplasty provided diastolic augmentation, aortomyoplasty activation was associated with improvement in load-insensitive aspects of systolic and diastolic function. Improved left ventricular contractility and diastolic relaxation were associated with aortomyoplasty activation, independent of effects on preload or afterload. This load-independent effect is not expected by the model, nor was it observed with IABP. These researchers speculate that stimulation of the thoracodorsal nerve or circulating catecholamines may be a component of additional nonload-dependent improvements in cardiac performance. Despite the important improvements noted, they acknowledge the significant barrier to clinical application represented by the ligation of the intercostal arteries in existing models of descending aortomyoplasty.

Although no paraplegia has been demonstrated in investigative models where the intercostal arteries were ligated [2–8 10], as a clinical option in end-stage cardiac disease, ligation of these vessels is prohibitive. As a result, investigators have searched for a technique of descending aortomyoplasty that avoids ligation of these vessels. Lazarra and colleagues [4] have suggested that by tapering the width of the muscle, the narrowed LD can be woven around the intercostal arteries, thereby preserving flow. However, in our evaluation of goat anatomy, only a 2- to 3-cm distance exists between intercostal branches. This narrow space would require excessive tapering of the LD, which at this level is 8 to 12 cm in width. Human cadaveric studies would be helpful in determining whether this short interspace precludes such an approach. More important, narrowing the LD pedicle may jeopardize the vascular supply of the autograft and unnecessarily decrease the effective contractile surface. Our group has previously evaluated the use of serratus anterior muscle strips in descending thoracic aortomyoplasty to avoid ligation of the intercostal arteries [3]. The vascular supply of the serratus anterior muscle allows subsegmental division without vascular compromise [9]. Therefore, we divided the distal aspect of the serratus anterior muscle and interdigitated the muscle strips around the aorta and its branches, thereby preserving intercostal vessels. Although effective counterpulsation was generated with serratus anterior muscle-powered aortomyoplasty, extensive division of the serratus anterior muscle was associated with significant muscle fibrosis. A 40% failure rate of aortomyoplasty constructed with the serratus anterior muscle was noted as a result of fibrosis.

The model of descending aortomyoplasty presented in this study is the first to address the practical considerations of using aortomyoplasty in clinical settings. By interposing a small segment of bovine pericardium and dividing it around the intercostal arteries, effective ``near-circumferential'' muscle wrapping of the aorta can be achieved with preservation of spinal blood supply. The amount of pericardium required for preservation of the branches is kept to a minimum and descending aortomyoplasty with pericardium interposition provides effective counterpulsation despite incomplete muscle wrapping of the aorta. Improvements in hemodynamic profiles have been identified along with significant changes in the aortic pressure tracings. Significant aortic luminal compression during extraaortic counterpulsation has been identified by intravascular sonography. Most important, long-term patency of the intercostal arteries has been confirmed by histologic analysis.

The hemodynamic benefit of pericardial patch-modified descending aortomyoplasty appears similar to that observed previously in nonmodified LD aortomyoplasty [1, 3, 11]. The interposition of a small segment of pericardium does not appear to diminish contractile force, and there is a clear transfer of mechanical energy across the aortic wall during activation. Although ischemic states were not evaluated in this study, previous work has demonstrated the utility of aortomyoplasty-derived cardiac augmentation in models of cardiac failure [3, 5].

The mechanics of diastolic augmentation created by descending aortomyoplasty are not completely understood. All models of descending aortomyoplasty are composed of circumferential wraps of the aorta with most autografts left intact at their origin. This orients the net compression of the aorta in a manner different from the effect seen with IABP. The conceptual model of aortomyoplasty counterpulsation is that the aorta undergoes a circumferential compression that mimics the IABP effect of aortic luminal reduction and pressure augmentation. However, our observation is that the net effect of descending aortomyoplasty stimulation is compression combined with aortic lifting toward the insertion of the LD. In an acute state this lifting alters normal anatomic relationships; however, once adhesions are formed the aorta appears anchored to the periaortic tissues. The summation of forces appears as a ``corkscrew'' effect. This torsion of the aorta may, in part, describe the mechanism of aortic pressure augmentation, explaining why a complete circumferential muscular wrap of the aorta is not necessary for effective descending thoracic aortomyoplasty. Aortic pressure augmentation and relaxation may be the result of more than one type of mechanical vector.

As in previous studies that use LD autografts, there is little functional deficit identified after the operation, with acute limping in the associated forelimb that appears to be related to the extent of muscle group dissection. In our series all limping resolved by postoperative day 5. Seroma formation continues to be a troublesome complication of LD harvesting. This complication may be species dependent with similar reports noted after canine cardiomyoplasty. Seroma formation in ruminants requires aggressive drainage because of the risk of infection. Other species-dependent technical issues relate to the difficulty of discriminating the different components of the electrocardiogram for timing of the muscle contraction. For this reason we used a fixed delay of 386.7 ms from the R wave, in contrast to other investigators who used a delay of 50% of the RR interval [11]. Both standard recording equipment and the telemetry of the pacemaker must be carefully regulated because of the high amplitude of the T wave in goats. It is often necessary to time muscle stimulation based on the T wave rather than the R wave in certain animals, although this was not the case in our series. Although these technical issues should not be a factor in the clinical application of aortomyoplasty, they are relevant to further research endeavors.

Descending thoracic aortomyoplasty with pericardial extension could be applied in clinical settings without affecting previous aortocoronary bypass grafts or necessitating an aortic enlargement, as is required with reported models of ascending aortomyoplasty [1]. The practical use of descending aortomyoplasty is further supported by chronic experimental studies in other models that show effective counterpulsation at lengths up to 1 year [4, 8]. Although chronic studies with this model of descending aortomyoplasty would be beneficial, the long-term results of other study models are encouraging, because they suggest chronic muscle stimulation can produce long-term effective counterpulsation. In addition, LD autografts combined with pericardial extensions have been used to extend muscle coverage since the origins of the cardiomyoplasty technique with good, chronic resultsAu: incomplete sentence [12].

A theoretical consideration of cardiac assistance with autologous muscle is the time delay required for ``vascular healing'' and muscle conditioning. However, reports of skeletal muscle autograft use with vascular healing delay periods of 2 days [13] and conditioning periods as short as 4 weeks [4] suggest that descending aortomyoplasty, like cardiomyoplasty, could be used in more acute settings. Descending aortomyoplasty would be useful in patients with New York Heart Association functional class III or early class IV who are expected to have clinical progression. Descending aortomyoplasty would be most suitably applied electively or semielectively, as a bridge to cardiac transplantation, as an adjunct to cardiomyoplasty, or in patients who are not candidates for transplant. In those ineligible for other therapeutic interventions, descending thoracic aortomyoplasty might function as a chronic, cardiac-assist device. A theoretical consideration of clinical application of descending aortomyoplasty is whether or not the compliance of the atherosclerotic aorta impedes effective counterpulsation, or adds morbidity.

As the incidence of patients progressing to end-stage heart failure increases, so does the demand for development of effective, accessible cardiac assist devices. Ideal qualities are low immunoreactivity, availability despite age or concurrent disease, and technical feasibility. The use of descending thoracic aortomyoplasty addresses many of these issues; however, the technical drawback of intercostal artery preservation has acted as a barrier to its clinical application. This novel approach to descending aortomyoplasty, using pericardial extension, provides effective cardiac assistance without compromise of spinal blood flow. Further studies will be required to reinforce these findings and prepare for the clinical application of this technique.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
We thank Mark Iezzi, Elizabeth Hedrick, Michael Srulevich, Joshua D. Moss, and Gordon Jacobs for their technical assistance and support, and Martin Valdez for assistance in manuscript preparation. Myostimulators, programming software, and pacing leads have been generously provided by Telectronics, Inc, Englewood, CO.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Address reprint requests to Dr Cernaianu, 47 Cambridge Rd, Haverford, PA 19041.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

1. Chachques JC, Grandjean PA, Cabrera Fischer EC, et al. Dynamic aortomyoplasty to assist left ventricular failure. Ann Thorac Surg 1990;49:225–30.[Abstract/Free Full Text]
2. Constance CG, Sabini G, Turi GK, Hines GL. Descending thoracic aortomyoplasty: effect of chronically conditioned muscle on heart failure. Cardiovasc Surg 1993;1:291–5.[Medline]
3. Cernaianu AC, Vassilidze TV, Flum DR, et al. Latissimus dorsi and serratus anterior dynamic descending aortomyoplasty for ischemic cardiac failure. Ann Thorac Surg 1995;59:639–43.[Abstract/Free Full Text]
4. Lazarra RR, Trumble DR, Magovern JA. Autogenous cardiac assist with chronic descending thoracic aortomyoplasty. Ann Thorac Surg 1994;57:1540–4.[Abstract/Free Full Text]
5. Lazarra RR, Trumble DR, Magovern JA. Dynamic descending thoracic aortomyoplasty: comparison with intra-aortic balloon pump in a model of heart failure. Ann Thorac Surg 1994;58:366–71.[Abstract/Free Full Text]
6. Salmons S, Henriksson J. The adaptive response of skeletal muscle to increased use. Muscle Nerve 1981;4:94–105.[Medline]
7. DelRossi AJ, Cernaianu AC, Vertrees RA, Cilley JH Jr, Baldino WA, Camishion RC. Biotransformation of skeletal muscle used for long-term dynamic aortomyoplasty. BAM 1991;1:311–6.
8. Vertrees RA, Cernaianu AC, Camishion RC, Cilley JH Jr, Baldino WA, DelRossi AJ. A surgical approach to chronic aortomyoplasty in the goat model. J Invest Surg 1993;6:419–29.[Medline]
9. Tobin AE, Barker JH, Slater AD, Gray LA, Tobin GR. The anatomic basis for serratus anterior aortic counterpulsation in humans. Surg Forum 1993;44:657–60.
10. Hines GL, Mishriki Y, Williams L, Monroe K, Metwally N. Physiologic and pathologic evaluation of chronic extra-aortic counterpulsation with latissimus dorsi flap. J Cardiovasc Surg 1991;32:485–90.[Medline]
11. Chachques JC, Haab F, Cron C, et al. Long-term effects of dynamic aortomyoplasty. Ann Thorac Surg 1994;58:128–34.[Abstract/Free Full Text]
12. Carpentier A, Chachques JC. Cardiomyoplasty: surgical technique. In: Carpentier A, Chachques JC, Grandjean PA, eds. Cardiomyoplasty. Mount Kisco, NY: Futura, 1991:105-22.
13. Pattison CW, Cumming DVE, Williamson A, et al. Aortic counterpulsation for up to 28 days with autologous latissimus dorsi in sheep. J Thorac Cardiovasc Surg 1991;102:766–73.[Abstract]

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Riad Meada Laura A. Lee Michael A. Grosso Anthony J. DelRossi Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Flum, D. R. Articles by DelRossi, A. J. Search for Related Content PubMed PubMed Citation Articles by Flum, D. R. Articles by DelRossi, A. J.