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Ann Thorac Surg 1995;59:639-643
© 1995 The Society of Thoracic Surgeons

Latissimus Dorsi and Serratus Anterior Dynamic Descending Aortomyoplasty for Ischemic Cardiac Failure

Aurel C. Cernaianu, MD, Teimouraz V. Vassilidze, MD, PhD, David R. Flum, MD, John G. Gallucci, MD, Andreas Olah, MD, Jonathan H. Cilley, Jr, MD, Michael A. Grosso, MD, Anthony J. DelRossi, MD

Division of Cardiothoracic Surgery, Department of Surgery, Cooper Hospital/University Medical Center, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School at Camden, Camden, New Jersey

Accepted for publication December 6, 1994.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Dynamic descending aortomyoplasty for cardiac assistance is a form of extraaortic, skeletal muscle-driven counterpulsation. Controversy exists regarding its clinical applicability and the most suitable muscle autograft for the procedure. Specifically, the ligation of intercostal vessels required for descending aortomyoplasty may not be tolerated clinically. This study compared the hemodynamic profiles and long-term function of latissimus dorsi (LD) aortomyoplasty to a split serratus anterior (SA) descending aortomyoplasty in which all intercostal vessels were preserved. Descending aortomyoplasty was performed in 11 goats. In 5, the SA was harvested and its distal end divided, facilitating a wrap of the aorta without ligation of intercostal arteries. In 6, the LD was used as a circumferential aortic wrap. At 90 days, an occluder placed on the left anterior descending artery created an ischemic event. Hemodynamic studies with and without assistance were performed in the ischemic and nonischemic states. Latissimus dorsi aortomyoplasty improved cardiac output 24% and 5.6%, stroke volume 29% and 66%, left ventricular stroke work index 30% and 166%, and coronary flow 4% and 3% in the normal and ischemic heart, respectively. Serratus anterior aortomyoplasty improved cardiac output 36% and 10%, stroke volume 42.8% and 13.5%, left ventricular stroke work index 64% and 21%, and coronary flow 8% and 4.3%, in the normal and ischemic heart, respectively. Two of the SA autografts were fibrotic and nonfunctional at 3 months. Aortomyoplasty with either SA or LD muscle improves cardiac function in the normal and ischemic heart. However, divided SA is associated with a higher rate of fibrosis and may be less suitable for the procedure.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
There are currently 2.3 million patients with chronic heart failure in the United States. Medical therapy for these patients is associated with a 5-year mortality of 50% [1, 2]. Unfortunately, cardiac transplantation is available to only a small percentage because of a shortage of donor hearts. While the search continues for implantable cardiac assist devices, the use of skeletal muscle for cardiac assistance has been successful in animal and human models [3]. Cardiomyoplasty and ascending aortomyoplasty have been offered as therapeutic alternatives for cardiac assistance in end-stage heart disease.

Successful cardiomyoplasty has been reported in animal and human subjects [4]. The degree of its clinical benefit and the physiologic mechanism of its assistance have been debated. Moreover, cardiomyoplasty may be contraindicated in those patients with morbidly dilated or hypertrophic cardiomyopathy. In addition, although subsequent cardiac transplantation after cardimyoplasty has been reported, the operation becomes more technically challenging.

Ascending aortomyoplasty has been advocated as a form of biomechanichal assistance [5]. The procedure, as described by Chachques and colleagues [6], includes an aortotomy and aortic patch (neo-ventricle) to facilitate the displacement of sufficient blood volume during counterpulsation. The morbidity of such a procedure may be unacceptable in clinical use. However, descending aortomyoplasty may be a more attractive alternative because it does not require an aortotomy or significantly manipulate the heart. Descending aortomyoplasty has been performed in animal models with success [7]. The descending portion of the thoracic aorta allows a longer free segment for myoplasty and therefore, may provide more effective counterpulsation.

In this report we describe descending aortomyoplasty in the ischemic animal model and offer it as an option for cardiac assistance based on the principles of the intraaortic balloon pump. A technical barrier to clinical trials remains the fact that a complete wrap of the descending aorta requires ligation of intercostal arteries. In human subjects it is likely that interrupting the vascular supply to the spinal cord to facilitate aortomyoplasty may result in paralysis. It has been suggested that dividing the fibers of a serratus anterior (SA) muscle flap and interdigitating them around the intercostal arteries may preserve the spinal cord's vascular supply. This study compared aortomyoplasty with latissimus dorsi (LD) and split SA muscle flaps to assess the utility of a spinal cord preserving aortomyoplasty.


    Material and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Eleven adult alpine goats weighing 42 ± 8 kg were anesthetized with thiopental and halothane. In all animals a longitudinal left chest incision was created. Either the LD or SA was harvested by sharp dissection preserving the neurovascular pedicle. In each case the muscle was dissected free of its bony insertions and left intact at its origin. A bipolar pacing electrode was placed adjacent to the proximal neurovascular bundle (Medtronic model 4003; Medtronic, Minneapolis, MN). The second rib was partially resected to facilitate transfer of the muscle flap into the chest. Through a fifth interspace left lateral thoracotomy, a single, clockwise wrap of the descending aorta adjacent to the origin of left subclavian artery was completed. Latissimus dorsi aortomyoplasty required ligation of several pairs of intercostal vessels (Fig 1Go). In 5 animals the SA muscle was transferred into the chest in a similar fashion. The distal end of the SA muscle was divided longitudinally into several muscular bands allowing the muscle to interdigitate with the aorta while preserving the intercostal arteries (Fig 2Go). A single, circumferential wrap was performed in all cases. A unipolar, epicardial screw-in sensing lead (Medtronic model 6917A-53T) was placed on the right ventricle and a cardiomyostimulator (Medtronic model 1005) was inserted into a subcutaneous pocket.



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Fig 1. . Schematic representation of latissimus dorsi descending aortomyoplasty with ligated intercostal arteries.

 


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Fig 2. . Serratus anterior descending aortomyoplasty with distal end divided to allow for preservation of intercostal arteries.

 
After a 6-week ``vascular healing'' period, the cardiomyostimulator was programmed (Medtronic model 9710) to condition the muscle flap. The voltage, pulse frequency, and rate of the electrical stimulation were gradually increased (Table 1Go). The muscle stimulation was obtained with six-pulse bursts, pulse amplitude 4 to 6 V, pulse width 1.5 ms, burst rate 10 Hz. Diastolic counterpulsation was delayed 400 ms from the R wave of the electrocardiogram.


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Table 1. . Muscle Conditioning Schedule
 
At 3 months postoperatively the animals were evaluated under general anesthesia. Baseline hemodynamic measurements were made with a pulmonary artery catheter and a femoral artery cannula. Through a median sternotomy the pericardium was incised and the left anterior descending (LAD) artery was isolated. After prophylactic administration of intravenous lidocaine for arrhythmia, an occlusion of the LAD greater than 50% was created with an external vascular occluder (model OC5; In Vivo Metric, Healdsburg, CA). Diminished flow was confirmed with an extravascular sonographic flow-probe (Transonic Systems Inc, Ithaca, NY) distal to the occluder. After baseline data were obtained, the cardiomyostimulator was activated to compare assisted and nonassisted hemodynamic profiles. Measurements included left ventricular stroke work index (LVSWI), stroke volume (SV), left ventricular end-diastolic pressure (LVEDP), cardiac output, mean arterial pressure (MAP), and coronary blood flow. Thermodilution cardiac outputs in triplicate were computed and indirect measurements of cardiac function were assessed with a SpaceLabs Computer Analysis System (Spacelabs, Seattle, WA).

Statistical analysis was performed using an IBM SPSS PC PLUS (Version 3.0) statistical analysis package. Paired t test and {chi}2 test were used for statistical comparison between groups. Each animal served as its own control. A p value of less than 0.05 was considered statistically significant. Data are presented as mean ± standard deviation where appropriate.

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


    Results
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Six goats underwent LD aortomyoplasty. All animals tolerated the procedure well. On average, two to three pairs of intercostal arteries were ligated in each animal. No immediate or chronic neurologic sequelae were identified. Five goats underwent SA aortomyoplasty. No intercostal arteries were ligated in this group.

Two of five SA autografts were nonfunctional at 3 months. These muscle flaps were observed to be fibrotic and nonfunctional at autopsy. These animals were excluded from hemodynamic evaluations.

Hemodynamic profiles in the nonischemic and ischemic states are listed in Tables 2 and 3GoGo, respectively. Acute myocardial ischemia was characterized by a decrease in mean LAD flow of 57% in the LD group and 48% in the SA group. Decreases in coronary flow were associated with a 24% increase in LVEDP (9.2 ± 4.0 to 12 ± 3.1 mm Hg, p < 0.05) in the LD group and a 34% increase in LVEDP in the SA group (8.7 ± 2.7 to 13.0 ± 1.0 mm Hg, p < 0.05). The MAP and LVSWI decreased 47% and 43%, respectively, associated with nonsignificant variations in cardiac output and SV during the ischemic state in the LD group. The MAP, cardiac output, and SV decreased 13%, 12%, and 12%, respectively, in the SA group during ischemia.


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Table 2. . Hemodynamic Changes in the Normal Heart
 

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Table 3. . Hemodynamic Changes in the Ischemic Heart
 
Hemodynamic data during counterpulsation are shown in Tables 2 and 3GoGo. All cardiac variables improved with either type of aortomyoplasty when the cardiomyostimulator was activated. Improvements were significant in the ischemic and nonischemic states in the group with LD aortomyoplasty. There was a trend toward improved hemodynamics in the SA group; however, attributable to the small subgroup with functional SA autografts, the statistical significance of these results was reduced.

Two of 11 muscle wraps were considered nonfunctional at 3 months and were fibrotic on autopsy. Both failures were within the SA aortomyoplasty group. There was a statistically significant difference in failure rates between the SA group (2 of 5, 40%) and the LD group (0 of 6, 0%). No technical difficulties were noted in this group. Morbidity involved prolonged wound healing in 2 animals and the development of seroma requiring drainage in 4 animals. No functional deficit was identified as a result of muscle autografting.


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
In the United States, 35,000 patients per year require heart transplantation for chronic cardiac failure. Yearly, fewer than 2,000 donor hearts become available for transplantation [8]. This makes the search for a long-term, effective, and practical cardiac assist device essential. Skeletal muscle-driven cardiac assist devices are theoretically ideal because they are independent of external power sources and are nonimmunoreactive. The use of autologous skeletal muscle for cardiac assistance has been under investigation for cardiomyoplasty and aortomyoplasty and has achieved variable degrees of success.

In 1959, Kantrowitz and McKinnon [9] first used skeletal muscle for cardiac assistance. By wrapping a nonconditioned segment of diaphragm around the descending aorta of animals these investigators were able to demonstrate diastolic counterpulsation until muscle fatigue developed. This counterpulsation augmented MAP by 27% [10] and prompted additional research in this field, avoiding the use of hydraulic or pneumatic drives and transferring animal-driven longitudinal force into a potential cardiac assist device. Other investigators followed with similar concepts of skeletal muscle-driven assist devices; however, the barrier of muscle fatigue remained an obstacle to success [11, 12].

The ability to convert skeletal muscle into a more ``cardiac-like'' muscle was an important technical link that prompted investigators to use conditioned fatigue-resistant muscle in various models of cardiac assistance. There are significant biochemical distinctions between cardiac and skeletal muscle that account for differences in fatigability. Although cardiac muscle is composed of a syncytium of low-fatigue fibers, skeletal muscle is organized into distinct muscle units that contract separately and fatigue at variable rates. Skeletal muscle is composed of a combination of type I, slow-twitch and fatigue-resistant fibers with a variable percentage of type II, less fatigue-resistant, fast-twitch muscle fibers. Mannion and Stephenson [13] demonstrated that through chronic electrical conditioning type II muscle fibers can be converted to type I fibers, which are similar to cardiac muscle fibers in stimulation and fatigue characteristics. Macoviak and colleagues [14] used preconditioned muscle to provide several hours of effective cardiac assistance. DelRossi and co-workers [15] documented a histologic biotransformation of electrically preconditioned muscle in an animal model of descending aortomyoplasty.

In 1985, Neilson and colleagues [16] used a skeletal muscle-driven extraaortic pump to compress a polyurethane bulb placed in circuit with the heart. Other investigators have addressed the use of a hydraulic pouch powered by the rectus abdominis [12], latissimus dorsi [3], or serratus anterior muscles. However, thrombogenicity and foreign body reaction have been associated with these models. In the mid-1980s Carpentier and associates [3] reported the use of cardiomyoplasty in human subjects. Chronic data demonstrate effective fatigue-resistant cardiac assistance [17]. The mechanism of this augmentation has not been clarified and reproducible data are difficult to obtain [18]. Moreover, the operation may be contraindicated in many of the patients for whom it might be helpful. Specifically, patients with extremely dilated and hypertrophic cardiomyopathy are not candidates. Although technically feasible, extensive adhesions after cardiomyoplasty may complicate future heart transplantation [19].

Ascending aortomyoplasty was advocated by Chachques and colleagues [5] as a promising approach to assisted biomechanical circulation. Because the length of ascending aorta available for aortomyoplasty is limited by anatomic considerations, these investigators have suggested an enlargement of the ascending aorta through an aortotomy and the application of a pericardial patch (neo-ventricle). Acute [5] and chronic data [6] have been reported but the technical feasibility of this neo-ventricle in humans has not been addressed. Moreover, the morbidity of aortotomy may exceed the practical benefits of the procedure.

Several investigators have been involved with models of descending aortomyoplasty. The feasibility and efficacy of this procedure have been demonstrated in acute [20] and chronic [21] animal studies. The technique is modeled on the intraaortic balloon pump. In both cases, effective counterpulsation is based on (1) the generation of a force to displace blood volumes and assist systemic perfusion, (2) augmentation of coronary flow during diastole, and (3) precise timing to decrease afterload. The hemodynamic benefits of counterpulsation are an increased cardiac contractility and coronary flow.

Lazarra and colleagues [22] have evaluated the hemodynamic benefits of descending aortomyoplasty compared with those yielded by an IABP in an animal model. These investigators found that LD aortomyoplasty has a beneficial effect on left ventricular contractility that is independent of its effects on preload and afterload. The hemodynamic effects were comparable to those achieved with an IABP. An improvement in diastolic relaxation time was identified and has been advocated as an important factor in the hemodynamic changes associated with descending aortomyoplasty.

The descending aorta permits a longer length for myoplasty than the ascending aorta and therefore should provide more effective displacement of blood volume. However, the mobilization of a large segment of descending aorta may compromise spinal cord blood flow. No animals in the LD group demonstrated paraplegia after ligation of several pairs of intercostal arteries. Our animal model may have a more developed collateral circulation. It is generally considered that ligation of these vessels in humans may interrupt the vascular supply to the spinal cord.

In this study we have addressed the use of divided SA muscle fibers to achieve aortomyoplasty without division of intercostal branches. Our data demonstrate evidence of improved hemodynamic profiles with both models of aortomyoplasty. Specifically, in both the normal and ischemic heart an increase in cardiac output, SV, and LVSWI were identified. It is likely that LVSWI improved dramatically as a result of the decrease in afterload demonstrated with descending aortomyoplasty. A similar effect has been demonstrated by other authors [22].

Although the operations were technically successful in both groups, there is a statistically significant difference in failure rate between the groups. In our series, SA muscle assistance was a less effective technique. Our results may be explained by the extensive dissection required for harvest, mobilization, and splitting of the muscle fibers in the SA group. The segmental vascular anatomy of the SA has been described by Tobin and colleagues [23] who have advocated it as a theoretical alternative to the LD in aortomyoplasty. However, in practice, when the SA is harvested and divided for wrapping around the aorta additional dissection is required. Moreover, despite careful consideration of the vascular anatomy, nonanatomic splitting of the muscle fibers may be associated with ischemia and therefore fibrosis. Both LD and SA muscle flaps were otherwise treated in a similar fashion and it is unlikely that the neurovascular pedicle was compromised in either group. Although no histologic confirmation was performed, fibrosis was evident on gross examination during necropsy. The presence of fibrosis was not evident in the functional SA or the LD aortomyoplasty group, although no quantitative analysis was performed. Therefore, the benefit of SA muscle flaps in this configuration is equivocal. The procedure was tolerated well in both groups and minimal complications were noted.

Although our model of ischemia used to evaluate the hemodynamic effects of aortomyoplasty was documented by reductions of the LAD flow and global hemodynamic impairment, no direct contractility assessments, wall motion abnormalities, or laboratory evidence of ischemia were included in the study.

Our data demonstrate the efficacy of descending aortomyoplasty in the ischemic animal model. The SA aortomyoplasty, although experimentally effective, may not be a clinically practical choice based on its higher rate of fibrosis. The preservation of intercostal arteries, therefore, remains an investigational issue to advance this technique to clinical trials.

Clearly, there is a clinical demand for an effective and practical cardiac assist device. Skeletal muscle autografts demonstrate many of these important qualities. Further investigation is required to determine if descending aortomyoplasty is a potentially effective and practical cardiac assist device.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Presented at the Ninth International Congress Cardiostim 94, Nice, France, June 15–18, 1994.

Address reprint requests to Dr Cernaianu, Division of Cardiothoracic Surgery, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, Cooper Hospital/University Medical Center, 3 Cooper Plaza, Suite 411, Camden, NJ 08103.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Kannel WB, Thom TG. Incidence, prevalence and mortality of cardiovascular disease. In: Hurst JW, ed. The heart, 6th ed. New York: McGraw-Hill, 1986:562–3.
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  3. Carpentier A, Chachques JC, Grandjean PA. Cardiomyoplasty. Mount Kisco, NY: Futura, 1991.
  4. Lee KF, Wechsler AS. Dynamic cardiomyoplasty. Adv Card Surg 1993;4:207–36.[Medline]
  5. Chachques JC, Grandjean PA, Fischer EC, et al. Dynamic aortomyoplasty to assist left ventricular failure. Ann Thorac Surg 1990;49:225–30.[Abstract]
  6. Chachques JC, Haab F, Cron C, et al. Long-term effects of dynamic aortomyoplasty. Ann Thorac Surg 1994;58:128–34.[Abstract]
  7. Constance CG, Sabini G, Turi GK, et al. Descending thoracic aortomyoplasty: effect of chronically conditioned muscle on heart failure. Cardiovasc Surg 1993;1:291–5.[Medline]
  8. Kolff WJ. The artificial heart; the inevitable development: will it be the U.S. or abroad? Artif Organs 1989;13:183–4.[Medline]
  9. Kantrowitz A, McKinnon WMP. The experimental use of the diaphragm as an auxiliary myocardium. Surg Forum 1959;9:266.
  10. Kantrowitz A, Krakauer J, Rubenfine M, et al. Functioning autogenous muscle used experimentally as an auxiliary ventricle. Trans Am Soc Artif Intern Organs 1960;6:305–10.
  11. Kusserow BK, Clapp JF. A small ventricle-type pump for prolonged perfusions: construction and initial studies, including attempts to power a pump biologically with skeletal muscle. Trans Am Soc Artif Intern Organs 1964;10:74–8.
  12. Spotnitz HM, Merker C, Malm JR. Applied physiology of the canine rectus abdominis: force-length curves correlated with functional characteristics of a rectus powered ventricle-potential for cardiac assistance. Trans Am Soc Artif Intern Organs 1974;20:747–56.
  13. Mannion JD, Stephenson LW. Potential uses of skeletal muscle for myocardial assistance. Surg Clin N Am 1985;65:679–987.
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  19. Jegaden O, Delahaye F, Montagna P, et al. Cardiomyoplasty does not preclude heart transplantation. Ann Thorac Surg 1992;53:875–80.[Abstract]
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