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Ann Thorac Surg 1995;60:1678-1682
© 1995 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

New Technique Measures Decreased Transmural Myocardial Pressure in Cardiomyoplasty

Division of Cardiac Surgery, Brigham and Women's Hospital, Harvard Medical School, Boston; and Division of Applied Sciences, Harvard Graduate School of the Arts and Sciences, Cambridge, Massachusetts

Accepted for publication July 14, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
Background. We introduce the use of a fluid-filled balloon, interposed between myocardium and latissimus dorsi (LD), as a new technique to measure transmural myocardial pressure in an acute goat model of dynamic cardiomyoplasty.

Methods. A half-ellipsoidal balloon, composed of polychloryl vinyl layers, was sutured to the atrioventricular groove in 5 goats, thereby completely enveloping both ventricles. Left LD dynamic cardiomyoplasty was then performed, anchoring the LD to the felt sewing skirt of the balloon so that the LD completely covered the balloon. Left ventricular pressure and balloon pressure were measured with the stimulator in the 1:2 mode as balloon volume was varied.

Results. Average transmural myocardial pressure, defined as left ventricular pressure minus balloon pressure, decreased from 34.4 mm Hg to 15.6 mm Hg during stimulator-on beats (p < 0.05).

Conclusion. These results support the conclusion that dynamic cardiomyoplasty unloads the left ventricle by decreasing wall stress. Furthermore, transmural myocardial pressure decreased more when balloon volume was increased, implying that the LD sarcomere length has an effect on wall stress. A balloon may therefore allow optimization of LD sarcomere length and thus assisted cardiac performance.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
Despite 9 years of clinical experience and more than 400 clinical cases, the mechanism of dynamic cardiomyoplasty (DCM) is still poorly understood. Since its inception in 1985 [1], several investigators have reported functional improvement but modest, inconclusive hemodynamic augmentation [2–7]. Many theories have been postulated to explain the mechanism and efficacy of cardiomyoplasty, as well as the discrepancy between the functional results and objective hemodynamic characteristics of the procedure. Several investigators have suggested that cardiomyoplasty acts by reinforcing the myocardium and preventing further pathologic dilatation of the failing ventricle [8, 9]. Others have documented increased left ventricular systolic function and contractility and have suggested that cardiomyoplasty unloads the left ventricle (LV) by decreasing wall stress, resulting in decreased myocardial oxygen consumption [10–12]. Kawaguchi and associates [13, 14] studied this issue and documented augmentation of left ventricular pump function without increased myocardial oxygen demand or compromised coronary blood flow. If indeed myocardial wall stress is decreased during DCM, precisely how much it is decreased remains unknown. To test this hypothesis, one might measure transmural myocardial pressure during cardiomyoplasty. With the latissimusdorsi (LD) actively compressing the LV and exerting additional pressure on the epicardial surface, transmural myocardial pressure (P_t), defined as the difference between LV pressure and epicardial pressure, would be expected to decrease during DCM.

In the experiments reported herein, we used a half-ellipsoidal, fluid-filled balloon, interposed between LD and myocardium, as a way to measure definitively the transmural myocardial pressure in cardiomyoplasty. Measuring transmural myocardial pressure permits direct assessment of any dynamic cardiac compression by the LD. In addition, because changes in transmural myocardial pressure imply changes in wall tension, a balloon would allow an estimation of changes in myocardial oxygen consumption during DCM.

The purpose of this study, therefore, was twofold: (1) to investigate, using a fluid-filled balloon, how transmural myocardial pressure changes during LD muscle stimulation in DCM; and (2) to understand how the volume of fluid within the balloon affects the transmural myocardial pressure.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
Five adult (Nubian) goats (20 to 40 kg) were used for this study. All animals were cared for according to the ``Guide for the Care and Use of Laboratory Animals'' published by the National Institutes of Health (NIH publication 85-23, revised 1985).

Construction of Balloon
A half-ellipsoidal balloon was constructed using four layers of polychloryl vinyl with two layers composing each wall (Fig 1). Each layer was 12 µm thick. The edges were heat sealed. An access line was placed inside the inner two layers to measure pressure inside the balloon lumen (P_b) and to allow injection or withdrawal of fluid volume. A felt sewing skirt was fastened to the top edge of the balloon. All balloons were filled with saline solution and subjected to test pressures of 200 mm Hg to ensure water tightness.

View larger version (19K): [in this window] [in a new window]   Fig 1. . A half-ellipsoidal fluid-filled balloon in cardiomyoplasty. Coronal section showing how the balloon is first sutured to the base of the heart, using the felt skirt. Left latissimus dorsi cardiomyoplasty is then performed by suturing the latissimus dorsi muscle to the balloon, again using the felt skirt.

Left Latissimus Dorsi Dissection
The animal was placed in the right lateral decubitus position, and an oblique incision from the left axilla to the left iliac crest was made. The left LD muscle was identified and carefully dissected free from its insertion and surrounding fascial attachments. The neurovascular pedicle was identified and handled carefully during the procedure. Major collaterals were ligated and divided. The humeral insertion was then transected and the thoracodorsal nerve isolated. A cuffed nerve electrode was placed around the nerve. The muscle was then tested for gross contractile strength with a Medtronic SP1005 Cardiomyostimulator (Medtronic Inc, Minneapolis, MN). The third rib was identified, and a 5- to 6-cm lateral section was resected. The free edge of the humeral tendon was then attached to the second rib. The LD and nerve cuff electrode were then placed in the thoracic cavity.

Median Sternotomy and Instrumentation
The goat was then placed in the supine position. A median sternotomy was performed, followed by a pericardiotomy. The aortic root was dissected free, and an electromagnetic aortic flow probe (Carolina Medical Electronics, King, NC) was placed to measure aortic flow. Both venae cavae were dissected free, and umbilical tapes with Rommel snares were placed around both for caval occlusion. The femoral arterial pressure transducer placed previously was then connected to the balloon access port to measure balloon luminal pressure. A dynamic testing procedure performed earlier (Appendix 1) verified that the frequency response of the Statham transducer plus cannula was adequate to measure fluctuations in P_b to the required accuracy. Catheter-tip micromanometers (Millar Instruments Inc, Houston, TX) were then positioned in the LV and aortic root through both femoral arteries. All electronic signals were sampled at 200 Hz by a 12-bit analog-to-digital converter, displayed in real time by a Simultrace Physiologic Monitoring System (PPG Biomedical Systems, Pleasantville, NY), and sent to a Unix-based microcomputer.

Left Latissimus Dorsi Cardiomyoplasty With Balloon
A Medtronic SP2083 sensing lead (Medtronic Inc) was placed on the right ventricular free wall. The balloon was then placed over the heart to envelop both ventricles completely. To secure this position, we sutured the felt sewing skirt of the balloon, using 2-0 interrupted Ethibond (Johnson and Johnson, Somerville, NJ) sutures, to the epicardium of the heart along the atrioventricular (AV) groove in a horizontal mattress fashion. Care was taken to avoid the coronary arteries. Left LD cardiomyoplasty was then performed in the standard posteroanterior fashion by suturing the spinal edge of the muscle to the felt skirt of the balloon at the AV groove, again using interrupted 2-0 Ethibond stitches. All sutures were placed carefully at regular 1.5-cm intervals completely around the AV groove in an effort to avoid balloon herniation between the sutures during muscle stimulation. The right ventricular sensing and muscle stimulator leads were then connected to a Medtronic SP1005 Cardiomyostimulator, programmed with the following stimulator variables: amplitude 5 V, burst frequency 30 Hz, pulse width 210 microseconds, pulse train duration 185 milliseconds, AV delay 50 milliseconds, and synchronization 1:2 mode.

Experimental Protocol
To define the maximum volume of fluid (V_max) that could be injected inside the balloon without causing severe tamponade and constrictive effects, we increased the balloon volume (V_b), using saline solution, from zero until mean systolic pressure decreased by 10 mm Hg. We defined such a volume of fluid as V_max for that experimental preparation. The average thickness of the balloon at V_max was calculated to be 0.27 cm (Appendix 2).

We measured balloon pressure, left ventricular pressure, aortic pressure, and aortic flow at one-third V_max, two-thirds V_max, and V_max. Approximately 20 beats were recorded at each balloon volume with the simulator in the 1:2 mode. All data were collected with the ventilator off to avoid respiratory variations. A 5-minute rest period was allowed between each data run to prevent muscle fatigue. We varied V_b in a ``mirror'' fashion, from zero to V_max and back to zero again, for a total of seven data runs. Muscle fatigue was assessed by comparing balloon pressure at a particular volume during the downward series (V_b decreasing between runs) with that measured previously at the same volume during the upward series.

Data Analysis
All data were analyzed on an Intel 486DX2-66-based microcomputer using the computational program MATLAB (The Mathworks, Natick, MA).

MARKING BEATS.
The beginning of ejection was defined as the point at which aortic flow first became non-zero after end-diastole. The end of ejection was defined as the point at which aortic flow fell to zero after the beginning of ejection. End-diastole was defined as the point at which LV pressure began to rise after diastole. End-systole was defined at the same point as end-ejection.

SEPARATING ON AND OFF BEATS.
Data runs were conducted with the stimulator in the 1:2 mode so that the LD muscle was stimulated every other heartbeat. For every different V_b, five typical on beats and five off beats were ensemble averaged for future data analysis.

CALCULATING P_t AND STROKE VOLUME.
Using the ensemble averages, we calculated transmural myocardial pressure (P_t = P_lv - P_b) for both simulator on and off beats. We found that during diastole, the magnitude of P_b was still significant with respect to P_lv, and therefore we calculated P_t over the entire cycle and not just over systole. Because peak values for P_b recorded during later data runs decreased due to LD fatigue, whereas P_lv did not change in a statistically significant manner, we averaged the transmural myocardial pressure at a particular balloon volume from the upward mirror series with that from the corresponding downward mirror series taken later. This average was then used as the P_t for that particular balloon volume. Stroke volume was calculated by integrating aortic flow with respect to time during ejection.

STATISTICS.
The means and standard deviations of transmural myocardial pressure, LV pressure, aortic pressure, and stroke volume at each V_b were calculated for both stimulator on and off beats. The means and standard deviations were also calculated for both stimulator on and off beats at each V_b. Means were compared using a paired Student's t test.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
Representative tracings for aortic flow, aortic pressure, LV pressure, balloon pressure, and calculated transmural myocardial pressure are shown in Figure 2. When the LD was stimulated, P_b increased in a sharp and smooth manner shortly thereafter. Transmural myocardial pressure, defined as P_lv - P_b, fell to a minimum value at the time P_b reached a maximum.

View larger version (29K): [in this window] [in a new window]   Fig 2. . Sample data records. Tracings were acquired at a rate of 200 samples per second. (Pao = aortic pressure; Pb = balloon pressure; Plv = left ventricular pressure; Pt = calculated transmural myocardial pressure; Qao = aortic flow.)

View larger version (28K): [in this window] [in a new window]   Fig 3. . Hemodynamic assessment. No significant changes between off and on were found for stroke volume (SV), left ventricular pressure (Plv), or aortic pressure (Pao). (NS = not significant.)

View larger version (21K): [in this window] [in a new window]   Fig 4. . Transmural myocardial pressure in cardiomyoplasty. Transmural myocardial pressure (Pt) decreased significantly at all three balloon volumes tested during latissimus dorsi muscle contraction.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

One major roadblock to understanding why patient status often improves after DCM while hemodynamic indices show no change is the difficult but necessary step of separating the mechanical contribution of the skeletal muscle from that of the native LV. In an acute model of cardiomyoplasty with no adhesions, the skeletal muscle can affect cardiac performance only by exerting a pressure perpendicular to the ventricular surface. In this study, we used a fluid-filled balloon, where the fluid within can support only normal stresses and no shear stresses [16]. By measuring balloon pressure, it is possible to separate skeletal and LV contributions to cardiac performance.

The use of such a balloon has other potential benefits as well. Controversy exists regarding which wrap configuration (anteroposterior, posteroanterior, right, or left) is most effective. Because the morphologies of each individual LD, heart, and mediastinal anatomy may vary, irregularities occur even with the same wrap configuration. The balloon may diminish the effects of wrap irregularity because any contractile force generated by the skeletal muscle is translated into inward pressure by the fluid.

The contractile force of the LD is related to the unstimulated tension of the LD muscle, reflecting the tension-length property applicable to all striated muscle. With increases in balloon volume, the LD was stretched, its length increased, and therefore its tension changed. Currently, the optimal tension for the LD wrap is unknown [17, 18]. By varying balloon fluid volume, one can manipulate in situ the heart and LD muscle interacting together in cardiomyoplasty and note the sum effect by observing P_t and P_b.

Despite the lack of significant hemodynamic change during active LD stimulation, we documented a large and statistically significant decrease in average transmural myocardial pressure at all three balloon volumes tested (see Fig 4). This benefit increased as V_b was increased, with the greatest decrease of 53% occurring at V_max (p < 0.05). As V_b was increased, mean arterial pressure decreased slightly but not significantly (see Fig 3), indicating a slight constrictive effect on the heart during filling. These results suggest that an optimal balloon volume exists at which the benefit of decreased P_t is maximized while the decrease in arterial pressure is minimized. If this is the case, then balloon-mediated cardiomyoplasty, using a balloon with an optimized fluid volume, should increase the myocardial benefit over standard cardiomyoplasty.

A decreased P_t indicates that myocardial wall stress has decreased. In its simplest form, the Law of Laplace relates the wall stress of a sphere (_s) of uniform thickness (h) and radius (r) to the transmural pressure (P_ts) across the sphere's wall:

Assuming that the LV is a sphere of uniform thickness and radius, calculations based on Laplace's Law therefore predict that during muscle stimulation with V_b = V_max, average myocardial wall stress decreased by 53%. With an average percentage decrease in P_t of 26% and 31% at one-third V_max and two-thirds V_max, respectively, calculated myocardial wall stress decreased concomitantly by the same percentages. Recently, other results from this laboratory [10] and from Cho and associates [12] have suggested that cardiomyoplasty acts by unloading the LV through decreased wall stress and afterload. Thus, these results support our previous conclusions. Myocardial wall stress or tension is a strong correlate of myocardial oxygen consumption [19]. Therefore, this study supports the hypothesis that cardiomyoplasty decreases myocardial oxygen consumption.

The limitations of this work include the use of untrained LD muscle instead of transformed muscle. Untrained skeletal muscle is stronger and faster. Using untrained muscle therefore overestimates the effect of decreased transmural pressure in cardiomyoplasty. On the other hand, cardiomyoplasty may benefit dilated cardiomyopathic hearts more than normal hearts in terms of mechanical enhancement [14]. Because we used normal rather than cardiomyopathic hearts in this study, our results can be expected to underestimate cardiac assistance and unloading compared with the clinical situation. In addition, the effect of varying balloon volume may be diminished in a chronic study, in which sarcomeres may exhibit conformational adaptation [17]. In such a situation, periodic adjustment of the balloon volume may be necessary to achieve optimal sarcomere length. Further studies using the technique of balloon-mediated cardiomyoplasty in cardiomyopathic hearts and employing trained LD muscle are required to predict the clinical effectiveness of balloon-mediated cardiomyoplasty.

In conclusion, this study demonstrates that while conventional measures of objective hemodynamics remained the same, transmural myocardial pressure during DCM decreased greatly using untrained LD muscle applied to the normal heart of a goat. Our results suggest that cardiomyoplasty provides benefit to the cardiovascular system not by increasing standard hemodynamic indices such as aortic pressure or stroke volume, but by decreasing transmural myocardial pressure, myocardial wall stress, and thus myocardial oxygen consumption. Furthermore, we documented an increased benefit at greater balloon volumes, demonstrating that LD sarcomere length may have a determining effect on myocardial wall tension. The use of such a balloon interposed between the LD muscle and myocardium may allow an optimization of LD sarcomere length and therefore of assisted cardiac performance in DCM.

	Appendix 1. Accuracy of Balloon Pressure Measurement Technique

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
We were concerned that the frequency response of the balloon access catheter, leading from the Statham pressure transducer to the lumen of the balloon, might introduce distortions in P_b. Thus, we constructed a balloon in the standard fashion but added a port for a high-fidelity micromanometer (Millar Instruments Inc). The balloon was then placed around a wooden heart model, and manual hand compressions were made at a frequency of 100/min to simulate compressions of the LD muscle. Pressures from both the high-fidelity micromanometer, introduced directly into the balloon lumen, and from our standard cannula plus Statham pressure transducer were recorded simultaneously. Five such recordings were made. Taking the pressure recorded from the high-fidelity micromanometer as a reference, we found that the Statham system gave a signal that was within ±2% of the reference throughout the simulated heart cycle. Thus, we conclude that our cannula system plus Statham pressure transducer measures balloon luminal pressure with adequate accuracy.

	Appendix 2. Thickness of the Fluid-Filled Balloon

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
We wished to calculate the average maximal thickness between the myocardium and LD due to the four balloon layers plus the fluid within the balloon lumen. Assuming that the heart and LD wrap are perfectly spheric, we applied the following formula:

where r_o represents the distance from the center of the heart to the inside of the LD wrap and r_i the distance from the center of the heart to the epicardium. For all five experiments, average V_max was calculated to be 40 cm³ and r_i to be 3.24 cm. Solving for r_o and substituting for V_max and r_i yields a value 3.51 cm for r_o. Because the polychloryl vinyl layers of the balloon are orders of magnitude thinner than the fluid contained between them, we concluded that their thickness is negligible. Thus, the thickness of the fluid-filled balloon between the myocardium and LD wrap is calculated as follows:

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 
We gratefully acknowledge support from the Harvard-MIT Health, Sciences, and Technology Research Fund and Rhone-Poulenc Rorer. In addition, the support of Medtronic, Inc, is much appreciated.

	Footnotes

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Presented in part at the Forty-first Annual Conference of the American Society for Artificial Internal Organs, Chicago, IL, May 4–6, 1995.

Address reprint requests to Dr McMahon, Harvard University, Pierce Hall 325, Cambridge, MA 02138.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Appendix 1. Accuracy of... Appendix 2. Thickness of... Acknowledgments References

 

1. Carpentier A, Chachques JC. Myocardial substitution with a stimulated skeletal muscle: first successful clinical case. Lancet 1985;8440:1267.
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