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Ann Thorac Surg 2002;73:849-854
© 2002 The Society of Thoracic Surgeons

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Original article: cardiovascular

Functional recovery of the native heart after cardiomyoplasty in sheep with heart failure: passive and dynamic effects of volume loading

^a Cardiac Technology Centre, Department of Cardiology, Royal North Shore Hospital, Sydney, New South Wales, Australia
^b Department of Cardiothoracic Surgery, Nagoya University of Medicine, Nagoya, Japan
^c Department of Cardiothoracic Surgery, Royal North Shore Hospital, Sydney, New South Wales, Australia

Accepted for publication October 25, 2001.

* Address reprint requests to Dr Shirota, c/o Dr Hunyor, Cardiac Technology Centre, Block 4, Level 3, Royal North Shore Hospital, St. Leonards, Sydney, New South Wales 2065, Australia
e-mail: stephenh{at}med.usyd.edu.au

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
Background. Dynamic cardiomyoplasty (d-CMP) encourages reverse remodeling and improved contractility and stroke work (SW) efficiency of the failing native heart. This contrasts with passive cardiomyoplasty (p-CMP), which provides "passive girdling." To further evaluate pump recovery we assessed native left ventricular performance (without assist) 6 months after dynamic and passive CMP in sheep with heart failure with acute volume loading.

Methods. Heart failure (left ventricular ejection fraction 26% ± 8%) induced by coronary microembolization was followed by CMP in 11 sheep. After 8 weeks of muscle "training," paced cardiac assist was undertaken in the d-CMP group (n = 6). Five sheep with heart failure served as controls. Six months later the pressure-volume relationship was derived before and after volume loading by colloid solution. Latissimus dorsi muscle pacing was previously ceased in the d-CMP group.

Results. Volume loading increased left ventricular end-diastolic volume and pressure in all groups. After volume loading in d-CMP, the SW and pressure-volume area were increased, and SW efficiency remained unchanged. In p-CMP neither variable changed, whereas in control heart failure SW efficiency decreased due to a rise in pressure-volume area with stable SW.

Conclusions. Based on response to volume loading, the failing native heart after 6 months of d-CMP showed functional recovery from "active girdling," whereas p-CMP prevented functional deterioration through passive girdling. The failing control heart progressively deteriorated.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
In assisting the failing heart, dynamic cardiomyoplasty (d-CMP) has the advantage, when compared with in-line mechanical support devices, of being non-blood contacting and using a biological power source. Current opinion regards the principal mechanism of action to be a "passive girdling" effect that prevents left ventricular dilatation, rather than a boost to systolic ejection from active squeezing [1–3]. However, in a previous study we reported that d-CMP after 6 months of support induces reverse left ventricular chamber remodeling, leading to improvement in native heart contractility (E_es) and stroke work efficiency (stroke work/pressure-volume area), whereas passive CMP only has a girdling effect [4]. From this we concluded that dynamic CMP, through a combination of dynamic compression (squeezing effect) and long-term elastic constraint (girdling effect), achieved a reduction in myocardial oxygen consumption (MVO₂) that allowed reverse chamber remodeling of the dilated failing heart, leading to improved left ventricular contractility. This outcome was not shared by passively wrapped control heart-failure hearts. Despite the apparent long-term benefits of d-CMP, it remains unclear whether the improvements are still evident in the volume loaded native heart. We investigated the hypothesis that although d-CMP (ie, electrostimulated) does not significantly increase stroke volume or cardiac output in chronic stable heart failure, it does have a dynamic girdling effect that will be highlighted under the additional strain of acute volume loading, in contrast to the passive girdling of adynamic cardiomyoplasty. We therefore assessed native left ventricular performance by volume loading the heart in three groups of sheep with heart failure after 6 months of follow-up. The three groups consisted of the following: animals with passive (adynamic) CMP; those with dynamic (paced) CMP (with "myostimulator off" during the study); and a group with heart failure that served as controls. Left ventricular mechanics and energetics were evaluated by assessing pressure-volume relationships before and after volume loading in a stable model of chronic heart failure in sheep created by repeated coronary microembolization [5].

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
The 16 Merino-Wether sheep (52 ± 5 kg) used in this study received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and the "Guide For the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animals Research and published by the National Institutes of Health (NIH publication 86-23, revised 1985).

For each assessment procedure, the animals were anesthetized with 20 mg/kg of thiopental sodium as induction, intubated, and ventilated with 1.5 L/min of oxygen, 2 L/min of nitrous oxide, and isoflurane (1.5% to 1.8%) using a Bird model 8 respirator (Bird Australia, Pty, Ltd, Chatswood, NSW, Australia). Maintenance fluid was provided through peripheral venous access with Hartmann’s solution (at a rate of 1 mL/kg of body weight per hour). The electrocardiograph was monitored with electrodes clipped to the extremities. All assessments commenced 30 minutes after intubation, allowing stabilization of heart rate.

Heart failure induction
Staged coronary microembolization was performed to induce heart failure with a left ventricular ejection fraction of less than 35%, as previously described [4, 5]. In brief, coronary embolization was repeated every 2 weeks until left ventricular ejection fraction decreased to target and remained stable for more than 4 weeks as assessed by echocardiogram (Opus 1; Ausonics Pty Ltd, Sydney, NSW, Australia). On average, 4 ± 2 embolizations were required. When heart failure had been established (left ventricular ejection fraction 26% ± 8%), 11 sheep underwent cardiomyoplasty (CMP), and 5 others served as a heart failure control group.

Cardiomyoplasty and muscle training protocol
The CMP procedure and latissimus dorsi muscle (LDM) training protocol are detailed in our previous publication [4]. In 6 of the 11 sheep undergoing CMP, active cardiac assist was continued with a 1:2 synchronous ratio for 6 months (dynamic CMP [d-CMP]), whereas in the remaining 5 sheep only nonpaced, passive CMP was provided (passive CMP [p-CMP]).

Hemodynamic assessment and response to volume loading
Thirty weeks after heart failure had been induced, all sheep (d-CMP, p-CMP, control heart failure) underwent hemodynamic assessment under stable light anesthesia. The carotid artery and jugular vein were isolated through a cut-down in the left side neck. Millar (5F) and 12-electrode conductance (6F; CardioDynamics, Rijinsberg, The Netherlands) catheters were placed longitudinally in the left ventricular cavity. The conductance catheter was connected to a Sigma 5 signal conditioner-processor (CardioDynamics). We corrected our volume measurements using a standard procedure that involves measurement of blood resistivity after injection of 5 mL hypertonic saline solution while the myostimulator is turned off. The jugular vein was cannulated with an inferior vena caval occlusion catheter (Fogarty 22F; Baxter International Inc, Irvine, CA). Instantaneous left ventricular pressure, volume, and electrocardiogram were displayed and digitized at 200 Hz on a personal computer during steady-state conditions and again during transient inferior vena cava occlusion. Ventilation was held at end-expiration during the measurements. Data were stored on hard disk and analyzed offline with custom software.

Volume loading of the left ventricle was performed by infusion of colloid solution (Hemaccel, Hoechst Marion Roussel Australia Pty Ltd, Lane Cove, NSW, Australia), composed of Polygeline 35 g/L, 293 mOsm/kg, at a rate of 20 mL per minute, for 10 minutes (total 200 mL) through a pulmonary artery line. In the setting of stimulator-off (assist-off), all hemodynamic variables during steady state were calculated as the average of 5 to 6 beats. The end-systolic pressure-volume relationship was assessed from each set of pressure-volume data.

Myocardial energetics were evaluated according to Suga’s method (see Appendix). In brief, the total mechanical energy generated by an ejecting contraction is regarded as equivalent to the systolic pressure-volume area. Stroke work is defined as the area within the pressure-volume loop and is the work performed by the heart on the blood. Pressure-volume area consists of both stroke work (SW) and potential energy and is directly related to left ventricular myocardial oxygen consumption. The work efficiency of cardiac contraction is the proportion of SW extracted from the total mechanical energy generated during contraction and, hence, is calculated as the ratio of SW to pressure-volume area.

Statistical analysis
A paired t test was used to compare the response of each experimental group to volume loading. Two-way repeated measures analysis of variance (ANOVA) was performed with the assumption of no interaction between time and the three study groups. Data are presented as mean ± standard deviation unless otherwise indicated. Statistical significance was set at a p value of less than 0.05.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
Left ventricular volume and pressure: effect of volume loading
As shown in Table 1, left ventricular end-diastolic volume was lower before volume loading in the d-CMP group than in the controls (one-way ANOVA; p < 0.05), whereas left ventricular end-diastolic pressure was no different in the three groups. Volume loading significantly increased both diastolic values in all three groups. In contrast volume loading led to a decrease in left ventricular end-systolic pressure in the control heart failure group, an increase in the d-CMP group and no change in the p-CMP group.

View larger version (16K): [in this window] [in a new window]   Fig 1. Changes in left ventricular end-diastolic volume (LVEDV) and stroke work (SW) caused by acute volume loading in three groups of sheep in which heart failure had been established 6 months earlier. (A) Dynamic cardiomyoplasty (n = 6), (B) passive CMP (n = 5) and (C) control heart failure (n = 5). Values before volume loading are shown by squares, whereas circles identify the response to volume loading. (*p < 0.05, **p < 0.01, NS = not significant.)

Comparsion of volume loading effect among the three groups
As above, volume loading in the individual treatment groups achieved differing effects, with the two extremes being in the dynamic CMP and control heart failure groups. Passive CMP on the other hand gave an intermediate response. However, despite the clinical relevance of the response differential, when the effect among the three groups was analyzed by two-way repeated measures ANOVA, only a trend was detectable, without any significant interaction effect.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
A severe heart donor shortage has increasingly focused attention on the potential use of ventricular assist devices (VADs) as a possible bridge to recovery for patients with chronic heart failure. It has been argued that prolonged myocardial offloading could be effective in achieving this outcome [6]. Because myocardial oxygen consumption (MVO₂) for a given SW is increased in the failing heart [7], any therapy that can improve SW without boosting MVO₂ is likely to be beneficial. In this study we used PVA as an index of MVO₂ because of the demonstrated linear relationship between the two under steady state contraction [8].

One form of effective intervention for the failing heart would therefore be to increase the efficiency (SW efficiency: SW/PVA) of energy transfer to direct contractile work. Direct cardiac compression (DCC) assist is one intervention that achieves this, as reported by Kawaguchi and colleagues [9], who used a mechanical external compression device in the isolated heart. In a previous study, we reported that DCC assist implemented as chronic CMP (a biological form of assist) also improves this efficiency, indicating a sparing effect on myocardial oxygen consumption [10]. Direct cardiac compression systolic assist decreases wall stress, resulting in systolic unloading of the heart.

Although it has been shown that DCC assist using CMP has a myocardial offloading effect, studies that evaluate the long-term effect on the native heart have been sparse [11, 12]. Furthermore, because these studies lacked a passive CMP group, they have failed to distinguish clearly between the passive girdling and dynamic (ie, DCC) effect of CMP.

In the previous study, we described the long-term (6-month) effects of CMP on native left ventricular contractility, energetics and chamber volume by separating out active (dynamic) and passive components of the CMP effect using a chronic sheep heart failure model with appropriate control groups [4]. We showed that dynamic CMP achieves reverse chamber remodeling and improves native LV contractility (E_es) and SW efficiency. On the other hand passive CMP simply prevents ventricular dilatation. We concluded that dynamic CMP, through a combination of long-term elastic constraint, the so-called passive girdling effect, and the additional "squeezing" action of active dynamic compression, leads to decreased myocardial wall stress with a resulting decrease in oxygen consumption. This allows enhanced chamber reverse remodeling with improvement in myocardial contractility and SW efficiency.

To determine the functional recovery of the failing heart, it is important to analyze whether the native heart can increase its performance when exposed to an overload situation. In the present study, we applied a moderate acute volume load that resembles the situation that could develop in a clinical setting of deteriorating heart failure. We found that after volume loading, the native heart that had been assisted for 6 months by dynamic CMP could increase SW without loss of efficiency. This response is similar to that of a left ventricle with normal function [13], implying that the failing native left ventricle can undergo functional recovery in response to long-term dynamic CMP assist. On the other hand, volume loading did not increase SW in the native heart of either the passive CMP or control heart failure groups. Also, after 6 months follow-up, left ventricular end-diastolic volume was significantly smaller after dynamic CMP than in control heart failure hearts. This confirms our previous finding that dynamic CMP induces chamber reverse remodeling [4]. The resulting smaller left ventricle can increase stroke volume and SW more readily, consistent with the Frank-Starling mechanism.

The increase in left ventricular volume achieved by colloid infusion was quite similar in our three groups, as was the resulting SW. This indicates that in the dynamic CMP group, a smaller end-diastolic volume can generate a larger SW, implying that wall stress is less. This, in turn, leads to relatively lower required myocardial oxygen consumption. In addition, this study showed that in the volume-loaded condition SW efficiency was significantly higher in dynamic CMP than in either passive CMP or control heart failure groups. Thus, myocardial oxygen is conserved in generating a given SW. Conversely, more SW is generated for a given MVO_2. In contrast, in the control heart failure group, myocardial oxygen consumption increased and SW efficiency deteriorated in response to volume loading. Also, to maintain a given SW, the failing preload overloaded control heart only increased the energy cost of contraction, as indicated by increased potential energy generation. From the viewpoint of the Frank-Starling mechanism, stroke volume and SW were not increased despite a rise in MVO₂, because this heart had already reached a plateau on the preload-stroke-volume curve. On the other hand, in passive CMP, neither SW nor PVA changed significantly after volume loading. The end-systolic pressure-volume relationship and pressure-volume loop showed a parallel rightward shift, implying a lessened impact of volume loading on left ventricular energetics. The latissimus dorsi muscle, wrapped around the left ventricle so as to thicken effective wall thickness and diminish wall stress [14], may serve to provide a protective girdling effect against acute as well as chronic left ventricular dilation. The native heart in passive CMP did not increase either myocardial oxygen consumption or SW in response to volume loading. In the present study we demonstrated that long-term dynamic CMP assist induces functional recovery of the failing heart as well as chamber reverse remodeling. Because clinical assist with dynamic CMP tends to be continuous in the setting once it is instituted, recovery of native heart function has received little attention to date. The clinical setting is also plagued by difficulties in having valid controls and the possibility that long-term CMP effectiveness will decrease due to muscle degeneration. Our group examined the histology of the LDM in a study comparing dynamic (electrostimulated) CMP and passive (adynamic) CMP, using an LDM configuration similar to that in the present study [15]. At 0, 6, 12, 18, and 24 weeks after CMP, it was found that although transposed nonpaced LDM used in p-CMP maintained muscle fiber size and number, its paced equivalent underwent atrophy and replacement with connective tissue. The damage in paced LDM was present within 6 weeks but some recovery was seen at 6 months. This recovery in the LDM used for dynamic CMP is postulated to be necessary for functional recovery of the supported failing native heart. However, a survey of clinical results with CMP over a longer (2-year) time frame, has shown less than 60% survival, largely due to enhanced progression of heart failure [16].

Recent studies have addressed the mechanism of native heart recovery after LVAD support [17, 18] and have suggested the possibility of extending mechanical left ventricular support because of the availability of new mechanical direct cardiac compression devices [19, 20]. Studies of CMP conducted to date are likely to prove valuable in the design and implementation of mechanical direct compression devices, which hold the potential of achieving cardiac assist without blood contact.

Study limitations
Left ventricular volume measurement with the conductance method involves a parallel volume component that is needed to estimate absolute volume. We therefore corrected our volume measurements using an injection of hypertonic saline solution in the steady-state control situation. Because E_es, PVA and SW are determined by relative volume from V₀, the error of analysis resulting from the conductance volume measurement is negligible.

In conclusion, based on the response to acute volume loading, the failing native heart subjected to 6 months of d-CMP shows functional recovery based on "active girdling." On the other hand, p-CMP wrapping only prevents functional deterioration through passive girdling. The non-CMP control failing heart shows a progressive deterioration of function.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
This work was performed partly under the Australian Government’s Cooperative Research Centers (CRC) Scheme in the CRC for Cardiac Technology. We acknowledge the technical assistance of Dr Xing Zheng, Dr Russell Carrington, and Ray Kearns, Gabrial Gomes, Janelle Wright, and Peter Darge.

	Fig 2. Pressure-volume area and MVO2

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 
Through their time varying elastance model, Suga and Sagawa proposed that end-systolic elastance (E_es) could be used to assess LV contractile state under acutely changing conditions and virtually independent of preload or afterload [21, 22]. E_es is the slope of the end systolic pressure-volume relationship (ESPVR), a linear regression of LVESP points from iterative P-V loops during preload reduction. The model provides a framework for measuring total mechanical energy generated by ventricular contraction, represented by the pressure-volume area (PVA) [23].

Pressure-volume area is derived from the integration of instantaneous ventricular pressure P (t), with the change in ventricular volume (dv) from the end of diastole (EDV) to the end of ejection (EEV).

((2))

where PVA = pressure-volume area, SW = stroke work, PE = potential energy, and ESPVR = end systolic pressure-volume relationship.

PVA consists of a stroke work (SW) (Fig 2) component generated by cross-bridge cycling within the LV wall, and a non-work-related potential energy (PE) component that represents the energy expenditure by the ATPases of the Na⁺-K⁺ and Ca²⁺ pumps [23]. PVA correlates linearly with MVo₂ [21, 23], whereby

((1))

This linear correlation has been confirmed in isolated and in situ hearts [23–25], and in diseased human hearts in vivo [26–28].

View larger version (18K): [in this window] [in a new window]   Pressure-volume loop diagram of ventricular contraction. (Ees = end-systolic maximal elastance; ESPVR = end-systolic pressure-volume relationship; PE = potential energy; PVA = pressure-volume area; SW = stroke work of contraction represented by the black colored loop area; Vo = volume-axis intercept of ESPVR.)

End-systolic maximal elastance (E_es, the slope of ESPVR) is derived from P_es the difference of end-systolic volume (V_es) and the volume intercept (volume-axis) of the ESPVR (V₀).

((3))

where P_es = end-systolic pressure, V_es = end-systolic volume and V₀ = intercept of ESPVR.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments Fig 2. Pressure-volume area... References

 

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This Article Abstract Full Text (PDF) 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): Peter W. Brady Yuichi Ueda Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Shirota, K. Articles by Hunyor, S. N. Search for Related Content PubMed PubMed Citation Articles by Shirota, K. Articles by Hunyor, S. N.