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Ann Thorac Surg 1998;65:1676-1679
© 1998 The Society of Thoracic Surgeons

Original articles: cardiovascular

Effects of Cardiomyoplasty on Right Ventricular Filling During Volume Loading

Yoshiya Toyoda, MDa, Masayoshi Okada, MDa, Mohammed Abul Kashem, MDa, Tomoichiro Mukai, MDa

a Division II, Department of Surgery, Kobe University School of Medicine, Kobe, Japan

Accepted for publication January 31, 1998.

Address reprint requests to Dr Toyoda, Division II, Department of Surgery, Kobe University School of Medicine, 7-5-2 Kusunoki-cho, Chuo-ku, Kobe, Japan 650


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Although cardiomyoplasty (CMP) is thought to improve ventricular systolic function, its effects on ventricular diastolic function are not clear. Especially the effects on right ventricular diastolic filling have not been fully investigated. Because pericardial influences are more pronounced in the right ventricle than in the left ventricle, CMP with its external constraint may substantially impair right ventricular diastolic filling.

Methods. Fourteen purebred adult beagles were used in this study. Seven underwent left posterior CMP, and 7 underwent a sham operation with a pericardiotomy and served as controls. Four weeks later, the hemodynamic effects of CMP were evaluated by heart catheterization before and after volume loading (central venous infusion of 10 mg/kg of 4.5% albumin solution for 5 minutes).

Results. In the CMP group, mean right atrial pressure and right ventricular end-diastolic pressure increased significantly from 3.1 ± 1.2 mm Hg to 6.1 ± 2.0 mm Hg (p < 0.001) and from 4.0 ± 1.8 mm Hg to 9.6 ± 2.5 mm Hg (p < 0.001), respectively. Volume loading in the control group did not significantly increase either variable. Right ventricular end-diastolic volume and stroke volume did not change significantly (from 53 ± 9.3 mL to 60 ± 9.0 mL and from 20 ± 2.3 mL to 21 ± 3.2 mL, respectively) in the CMP group. In the control group, however, right ventricular end-diastolic volume and stroke volume increased significantly from 45 ± 7.7 mL to 63 ± 14 mL (p < 0.05) and from 18 ± 4.3 mL to 22 ± 4.2 mL (p < 0.05), respectively.

Conclusions. These results suggest that CMP may reduce right ventricular compliance and restrict right ventricular diastolic filling in response to rapid volume loading because of its external constraint.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Cardiomyoplasty (CMP) is emerging as a promising surgical treatment for patients with end-stage heart disease who may not be candidates for heart transplantation. Cardiomyoplasty has been performed in more than 700 patients worldwide. Despite symptomatic improvement, objective beneficial hemodynamic effects or improved rates of survival have not been demonstrated consistently [1]. Although clinical and experimental studies have shown improved systolic function [2–6], the effects of CMP on diastolic function are still unclear [7, 8]. Of note, the effects on right ventricular diastolic function have not been investigated. Ventricular distensibility is influenced by a variety of factors that can be considered either extrinsic or intrinsic to the ventricular chamber [9]. One of these factors, pericardial constraint, may be important in CMP. The purpose of the present study is to evaluate the effects of CMP on right ventricular diastolic filling, one aspect of various diastolic functions of the right ventricle [10, 11].


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Fourteen purebred adult beagles (mean weight, 10.8 ± 1.4 kg) were used in this study. All animals were kept in clean cages with free access to food and sterile water. The beagles received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the Institute of Laboratory Animal Resources and the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985).

Surgical techniques
Seven beagles were anesthetized and prepared for sterile surgical procedures. General anesthesia was induced with ketamine hydrochloride (5 mg/kg) and thiamylal sodium (30 mg/kg) and maintained with sodium pentobarbital given intravenously as needed. Endotracheal intubation and positive-pressure ventilation (MA-1; Acoma Inc, Tokyo, Japan) were used. Perioperative antibiotics were administered routinely.

The beagles were placed in a right decubitus position, and a longitudinal skin incision was made from the left axilla toward the costovertebral angle. The left latissimus dorsi muscle was dissected free from all attachments except the neurovascular pedicle, which was carefully preserved for good circulation and nerve response. A 3-cm portion of the lateral aspect of the second rib was resected to permit passage of the dissected muscle flap into the thoracic cavity. The proximal tendinous humeral insertion of the latissimus dorsi muscle was secured to the second rib to prevent tension on the neurovascular bundle.

A left anterolateral thoracotomy was performed in the fifth intercostal space, and the pericardium was opened. The latissimus dorsi muscle flap was passed into the left chest cavity and wrapped around both ventricles in a clockwise fashion. The muscle was sutured to the myocardium with six to eight horizontal mattress sutures of 3-0 Prolene (Ethicon, Somerville, NJ), tied over Teflon pledgets. The operative pneumothorax was evacuated with a chest tube, and all incisions were closed in layers. A 4-week recovery period was allowed for adhesion formation between the latissimus dorsi muscle and the myocardium. The effects of CMP were then studied.

Seven purebred beagles underwent a sham operation with a pericardiotomy through a left anterolateral thoracotomy in the fifth intercostal space under the same anesthesia regimen and served as controls.

Hemodynamic measurements
For each hemodynamic measurement, the beagles were anesthetized with pentobarbital (30 mg/kg intravenously) and permitted to breathe spontaneously with diminished eyelash reflex. Each study took place after the beagles had rested supine in a quiet laboratory for a minimum of 20 minutes at room temperature (20° to 24°C). Under sterile conditions, a 7.5-F Swan-Ganz catheter (Baxter Healthcare, Irvine, CA) was advanced from the femoral vein to the pulmonary artery under fluoroscopic guidance. Another catheter was placed in the femoral artery. Pressures were monitored continuously on an oscillograph (model 363; NEC San-ei Instruments Ltd). Systemic arterial pressure, central venous pressure, right ventricular pressure, pulmonary artery pressure, and pulmonary capillary wedge pressure were measured before and after volume loading. To volume load, a 4.5% albumin solution was infused into the central vein at a dose of 10 mL/kg for 5 minutes.

Cardiac output, right ventricular ejection fraction, and right ventricular end-diastolic volume were measured by the thermodilution technique using five 3-mL injections of 0.9% saline solution (1° to 5°C). The thermodilution technique with this catheter has shown good results in the measurement of cardiac output, right ventricular ejection fraction, and right ventricular volume in dogs and has been described in detail elsewhere [12]. Briefly, after intraatrial injection of cold saline solution, a computer-aided algorithm determines right ventricular residual fraction from the logarithmic temperature decay recorded by a fast-response thermistor in the pulmonary artery. Right ventricular ejection fraction is then calculated by the computer as . Thereafter right ventricular end-diastolic volume and end-systolic volume are calculated as follows: and . All hemodynamic variables were monitored by a polygraph (model 363; NEC San-ei Instruments Ltd) and continuously recorded (model 8M14; NEC San-ei Instruments Ltd).

Statistical analysis
All data are presented as the mean ± the standard deviation. Data were compared using two-way analysis of variance to determine the effects of surgical treatment and volume loading. When analysis of variance demonstrated significant differences, each difference was tested using the Scheffé F test. Any value of p less than 0.05 was accepted as significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Cardiomyoplasty
There were no operative deaths. After the experimental protocol, hearts with a latissimus dorsi muscle flap were fixed in formalin and cut vertically along the long axis of the left ventricle at the level of the papillary muscle of the mitral valve. The dense adhesion between the myocardium and the latissimus dorsi muscle flap was observed (Fig 1).



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  		Fig 1. Macroscopic findings in heart with latissimus dorsi muscle flap. The muscle flap is wrapped around both ventricles in a clockwise fashion. The dense adhesion between the myocardium and the latissimus dorsi muscle flap is shown.

 
Control group
The effects of volume loading on hemodynamic variables in the control group are shown in Table 1. Rapid infusion of the 4.5% albumin solution produced a significant increase in stroke volume and cardiac output compared with the values seen before infusion (from 18 ± 4.3 mL to 22 ± 4.2 mL and from 2.6 ± 0.8 L/min to 3.8 ± 1.1 L/min, respectively). Right ventricular end-diastolic and end-systolic volumes increased significantly from 45 ± 7.7 mL to 63 ± 14 mL, and from 27 ± 6.1 mL to 40 ± 9.8 mL, respectively. Heart rate, pulmonary artery systolic pressure, and mean pulmonary artery pressure also increased significantly. Mean right atrial pressure and right ventricular end-diastolic pressure did not change significantly.


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  		Table 1. Effects of Volume Loading on Hemodynamics in Control Groupa,b

 
Cardiomyoplasty group
Table 2 summarizes the hemodynamic changes caused by volume loading in the CMP group. There were no significant differences in the preinfusion values for the hemodynamic variables between the control and CMP groups. Volume loading significantly increased mean right atrial pressure and right ventricular end-diastolic pressure in the CMP group from 3.1 ± 1.2 mm Hg to 6.1 ± 2.0 mm Hg and from 4.0 ± 1.8 mm Hg to 9.6 ± 2.5 mm Hg, respectively. Right ventricular systolic pressure, pulmonary artery systolic pressure, and mean pulmonary artery pressure also increased. However, in contrast with findings in the control group, stroke volume, cardiac output, and right ventricular end-diastolic and end-systolic volumes did not increase significantly. In addition, heart rate and right ventricular ejection fraction did not change significantly.


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  		Table 2. Effects of Volume Loading on Hemodynamics in Cardiomyoplasty Groupa,b

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Attempts to augment cardiac pressure using skeletal muscle grafts were initially reported by Kantrowitz and McKinnon [13] and then Nakamura and Glenn [14]. However, muscle fatigue has been found to be a serious obstacle to the use of skeletal muscle for long-term cardiac assistance. With the observation by Salmons and Sreter [15] that long-term, low-frequency electric stimulation not only caused a transformation of skeletal fast muscle to slow-fiber type but also increased its resistance to fatigue, skeletal muscle cardiac assistance has been explored by many researchers [16–20]. More than 10 years have passed since clinical use of CMP was reported by Carpentier and Chachques [21]. Theoretically, CMP should have beneficial effects including augmentation of ventricular contractility [2–6], reduction of myocardial oxygen consumption [6, 22] and prevention of further dilatation of the failing heart [23]. However, improvement in survival has not been demonstrated [1, 2], and therefore, CMP has not been widely accepted.

Cardiac performance is determined by both systolic and diastolic function, and heart failure occurs when either one or both of these functions deteriorate. With respect to ventricular diastolic function, pericardial constraint is one of the most important factors influencing diastolic dysfunction [8]. Because skeletal muscle inevitably adheres to the epicardium in CMP, it may have effects similar to the pericardial constraint seen in constrictive pericarditis. Because the thin-walled right ventricle, with low end-diastolic pressures, is more vulnerable to the influence of pericardial constraint than the thicker left ventricle [10, 11], volume loading can be a useful method to detect right ventricular diastolic filling impairment [24, 25]. In this study, increases in mean right atrial pressure and right ventricular end-diastolic pressure were significant only in the CMP group, whereas right ventricular end-diastolic volume and end-systolic volume increased significantly only in the control group. Cardiac ouptut and stroke volume also increased significantly only in the control group, and these changes correlated with increases in right ventricular end-diastolic volume. This hemodynamic response to volume loading was initially described by Starling [26] and then Sarnoff and Berglund [27].

The findings of the present study suggest that the right ventricle cannot dilate sufficiently in response to increases in preload because of constriction resulting from CMP wrapping. As a result, right atrial pressure and right ventricular end-diastolic pressure are elevated. These hemodynamic findings are typical of diastolic dysfunction [24, 25]. Accordingly, it is reasonable to believe that CMP may impair the distensibility of the right ventricle during volume loading. We think that this response is caused by the external constraint resulting from CMP. In other words, it is also possible that CMP may prevent overdistention of the right ventricle in response to volume overloading.

The present evaluation has limitations related to the methodology. We studied the effects of volume loading on right ventricular function after CMP without training by electric stimulation. This study was done to clarify the effects of the wrapped skeletal muscle itself. In dynamic CMP using a conditioned skeletal muscle, which may need more time to relax than myocardium, insufficient time would be available for relaxation of the skeletal muscle, resulting in residual tension and incomplete filling [28], and the effects on diastolic filling might be more prominent. However, with latissimus dorsi muscle flap electric stimulation, right ventricular ejection might increase, leading to an increase (per beat) in right ventricular filling, even though end-diastolic volume did not increase. In other words, with electric stimulation and a decrease in right ventricular end-systolic volume, right ventricular filling would increase. To clarify the effects of dynamic CMP on right ventricular filling, further investigation will be necessary.

In conclusion, our results suggest that because of its external constraint, a latissimus dorsi muscle flap in CMP may reduce right ventricular compliance and restrict right ventricular diastolic filling in response to rapid volume loading.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. El Oakley R.M., Jarvis J.C. Cardiomyoplasty: a critical review of experimental and clinical results. Circulation 1994;90:2085-2090.[Free Full Text]
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