Ann Thorac Surg 2003;76:828-835
© 2003 The Society of Thoracic Surgeons
Original article: cardiovascular
Skeletal muscle ventricle pressure-volume properties conform to dynamic and static conditioning
Kenneth J. Gustafson, PhDa*,
James D. Sweeney, PhDa,
John Gibney, MDa,
Lee Ann Fiebig-Mathine, PhDa
a Bioengineering Program, Arizona State University, Tempe, Arizona, USA
Accepted for publication March 4, 2003.
* Address reprint requests to Dr Gustafson, Case Western Reserve University, Department of Biomedical Engineering, Wickenden Bldg, Room 108, 10900 Euclid Ave, Cleveland, OH, USA 44106-4912
e-mail: kjg{at}po.cwru.edu
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Abstract
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BACKGROUND: Chronic changes in skeletal muscle ventricle (SMV) size and strength can directly affect performance and stability. These changes may depend on the conditioning protocol or implant system. Therefore the effects of conditioning protocols on SMV geometry and contractility must be identified for optimal SMV design and application.
METHODS: Skeletal muscle ventricles were constructed in 14 goats using the left latissimus dorsi muscle. The SMVs were conditioned with a 40 mL constant-volume isovolumetric implant (n = 5, IsoVol group) or a compliant pneumatic system that allowed dynamic shortening and direct exposure to resting pressures. Dynamic SMV resting pressure was either progressively increased from 40 to 100 to 120 mm Hg (n = 5, high pressure [HiP] group) or maintained at 40 mm Hg (n = 4, low pressure [LowP] group) during conditioning. The SMV pressure and volume characteristics were monitored daily.
RESULTS: All HiP SMVs expanded in volume during conditioning after exposure to physiologic pressures. Three of 4 LowP SMVs decreased in volume during conditioning. Skeletal muscle ventricle passive and active (isovolumetric evoked pressure) pressure-volume curves shifted toward the increasing, stable, and decreasing volumes in HiP, IsoVol, and LowP SMVs respectively.
CONCLUSIONS: Frequent monitoring of SMV characteristics during conditioning enabled progressive pressure training and is a valuable tool to evaluate SMV conformation. Chronic SMV adaptation is dependent on the conditioning protocol or implant system utilized. Demonstration of SMV expansion at physiologic pressures suggests that clinical sized SMVs may be chronically unstable unless a supporting implant system is utilized or SMV compliance is reduced. Therefore the mechanisms effecting chronic expansion should be further defined to optimally design SMVs for clinical implementation.
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Introduction
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Skeletal muscle ventricles (SMVs) may be utilized to augment cardiac output after being chronically electrically conditioned to be fatigue resistant; however conditioning can result in decreased muscle mass and performance [1]. The loss of resting tension can have damaging effects on chronic muscle viability [2]. Maintenance of skeletal muscle stretch or "mechanical conditioning" potentially results in a number of anabolic effects that include muscle lengthening [3, 4], hypertrophy [4], prevention of connective tissue accumulation [6], and increased muscle mass and blood flow [6]. In SMVs resting pressure provides muscle loading. Compliant pneumatic implant systems allow dynamic muscle shortening and control of SMV pressure. However initial exposure to aortic-level pressures may interfere with capillary perfusion or overstretch the muscle and cause muscle damage.
A SMV conditioning approach able to monitor and respond to changes in muscle performance during conditioning may prevent muscle overstress or damage and allow modification of conditioning parameters. Skeletal muscle ventricle pressure generation performance adapts to a static resting pressure and to increases in SMV resting pressure in a compliant implant system [7]. Therefore, mechanical conditioning by progressive increases of SMV pressure to just beyond that needed for peak performance, instead of immediate exposure to aortic-level pressures, may reduce muscle overstretch and damage by allowing the muscle to incrementally adapt to aortic-level pressures.
The purpose of this study was to (1) develop an implant system that enabled frequent monitoring of muscle characteristics during SMV conditioning and allowed progressive pressure conditioning and (2) determine the effects of progressive SMV pressure expansion and dynamic muscle training on chronic SMV pressure and volume. A control group was chosen based on the work of Larry Stephenson’s group, in which SMV conditioning protocols utilizing a constant volume (isovolumetric) implant have been shown to be effective [8–11]. A preliminary report of a component of this study has appeared previously [12].
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Material and methods
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Skeletal muscle ventricle construction
Skeletal muscle ventricles were constructed in 14 goats (26 to 49 kg). All animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" (National Institutes of Health publication 85-23, revised 1985).
Each animal was anesthetized with Telezol (AH Robins, Richmond, VA) and maintained with isoflurane. The left latissimus dorsi muscle was surgically exposed and mobilized from its distal tendinous origin leaving the neurovascular pedicle and proximal insertion at the humerus intact. Two intramuscular electrodes (custom designed, or Medtronic, Minneapolis, MN) were woven transversely across the fiber and nerve orientation, the cathode adjacent to the site of thoracodorsal nerve branch entrance and the anode 2 cm distal. The electrodes were connected to a subcutaneously placed externally programmable stimulator (Itrel II, Medtronic).
The SMVs in each group were formed by wrapping the internal surface of the muscle around a modified tissue expander (ISLE; Mentor Corp, Santa Barbara, CA) toward the proximal insertion to within 1 cm of the anode. The silicone rubber expander had a 7-cm fixed cylindrical axis, a 100-mL maximal volume, and a diameter of approximately 3.3 cm at a volume of 40 mL. The expander was compliant in the range of volumes investigated and therefore did not substantially insulate the muscle from SMV resting pressure. The long axis of the expander was maintained perpendicular to the muscle fiber orientation. In 2 LowP animals, similar implants (Artificial Heart Center, University of Utah) were implanted having a larger maximum volume. Isovolumetric (IsoVol) SMV first wrap circumference was set to 10.5 cm of in situ muscle length to maintain muscle stretch near the in situ level. The first wrap of dynamic SMVs had an inner circumference of approximately 3 to 4 cm; therefore a partial second wrap was obtained in each SMV. Roughly half of the total muscle mass was included in the SMV owing to the fixed implant length and the use of intramuscular electrodes that limited the proximal border. Silicone rubber tubing exited the expander laterally and was connected to a percutaneous exit site that enabled external monitoring of SMV performance.
Chronic monitoring
The resting pressure of dynamic and isovolumetric SMVs were measured and maintained daily and at least biweekly respectively. All SMV pressures were recorded using a pressure transducer (Cobe, Lakewood, CO) and amplifier (Gould Universal, Englewood, CO). Two to seven times a week each SMV was emptied and isovolumetric twitches at 2 Hz were elicited as saline was incrementally infused into the expander until just past the volume for peak evoked pressure generation (peak of the active pressure-volume curve). This volume (Vo) is the optimum volume (or muscle length) for isovolumetric pressure generation. Resting and evoked (peak minus resting) pressures at each volume were recorded to obtain passive and active pressure-volume curves.
Conditioning
The conditioning protocols for each group are shown in Table 1. Isovolumetric SMVs were filled with 40 mL of saline, forming an incompressible implant. The implant system is shown in Figure 1. The fixed longitudinal axis of the implant restricted variations in the compliant implant shape during conditioning. Therefore IsoVol implant geometry was considered constant. Dynamic SMVs were linked to a 600-mL fixed geometry external air reservoir. Pneumatic compliance allowed dynamic muscle shortening. The external location prevented implant erosion and provided access and control.
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Fig 1. Skeletal muscle ventricle (SMV) implant system. The SMV implants had a rigid longitudinal axis and expanded radially (dashed line). Dynamic SMVs were connected to an external pneumatic compliance chamber to allow dynamic shortening. An access port was used for pressure monitoring and daily testing sessions.
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High pressure (HiP) SMV resting pressures were incrementally increased in 10 mm Hg steps. If the resting pressure increase resulted in a resting volume increase, resting pressure was not increased again until Vo (the volume for peak active pressure generation) increased to the new resting volume. Therefore each resting pressure increment occurred after the SMV "adapted" to the previous increase, preventing muscle overstretch.
After a 2-week vascular delay period each muscle was stimulated every 4 seconds with a 130 msec duration pulse train of 210 µsec pulse width balanced charge biphasic stimuli at a frequency of 15 Hz for 2 weeks, resulting in 2 pulses per burst. During weeks 4 to 8 the frequency was increased to a 25 Hz burst, resulting in 4 pulses per burst. Stimulation voltage was monitored weekly and adjusted to result in maximum muscle activation. The electrical conditioning protocol was chosen to maintain fast fiber type properties that are preferred for muscle powered cardiac assistance, as a compromise between protocols typically used during cardiac assistance and the 2 Hz continuous stimulation protocol used by Stephenson’s group during isovolumetric training and to potentially limit conditioning damage that could be exaggerated by progressive pressure training.
Terminal procedure
After conditioning, 8 to 10 weeks after the initial surgery muscle biopsies were taken from the middle of the lateral subcutaneous section of the SMV, representing mainly the oblique muscle segment, and from the corresponding site of the contralateral control (right) muscle. Biopsies were stained with hematoxylin-eosin and myosin adenosine triphosphatase at pHs of 4.3 and 9.8. Muscle fibers were categorized as type I, II, or IIC fiber types. Not all biopsy samples demonstrated sufficient staining contrast across all sections to allow precise quantification of fiber types; therefore semiquantitative estimates were determined for those sections. When two muscle layers were at the biopsy site, data were averaged. The degree of muscle damage was determined by evaluation of the hematoxylin-eosin slides. Random sections of the muscle cross section were sampled and counted. Muscle damage consisted of ghost fibers, selected whole fascicle dissolution, areas of necrosis, fascicle degeneration, and capsule formation at the inner muscle wall. The presence and intensity of damaged areas, inflammation and reductions in fiber diameter (compared with controls) were semiquantitatively evaluated (ranked 0 to 4) based upon the percentage of total affected area (0% to 20%, to 80% to 100% respectively). The nonparametric Mann-Whitney U test was utilized to test directly between samples. The null hypothesis was that there was no difference between the means. Data are presented as mean ± SD.
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Results
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Chronic SMV pressures
An example of the progression of SMV resting pressure for a HiP SMV is shown in Figure 2.
Dynamic (HiP and LowP) SMV resting pressures varied and typically decreased daily due to pneumatic system air loss, temperature variations, and SMV volume expansion. Changes in dynamic SMV pressure and volume during postoperative day 0 to 14 are shown in Table 2.
The average measured resting pressure was 36% ± 9.0% less than the previous set resting pressure. Two HiP SMVs developed pinhole leaks that limited resting pressures to approximately 60 mm Hg for the last week of conditioning. Each dynamic SMV had instances of complete pressure loss due to animal interference with the external loading system. IsoVol SMV resting pressures were typically 10 to 40 mm Hg during conditioning except for one SMV in which pressures were 60 to 80 mm Hg after postoperative day 30.
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Fig 2. Resting pressure progression for a high pressure skeletal muscle ventricle (SMV). The SMV resting pressure was increased after the SMV had adapted to the previous increase in pressure. The end pressure is the pressure that the SMV was set to at the end of the daily testing session. The open pressure is the initial SMV resting pressure at the time of testing, typically 24 hours later. Pneumatic (high pressure and low pressure) SMV pressures varied and decreased 36% ± 9.0% daily owing to pneumatic system air loss, temperature variations, and SMV volume expansion. Squares = end pressure; circles = open pressure. (PO = postoperative.)
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Passive and active pressure-volume properties
The progressions of passive and active pressure-volume curves during conditioning are shown for representative SMVs from each group in Figures 3 and 4 respectively to illustrate
the trends observed during conditioning in each group. Passive and active pressure-volume curves exhibited session-to-session variability and could shift in either direction depending on the resting pressure and volume at the time of testing. Therefore although SMV starting volumes were similar for HiP and LowP SMVs (Table 2), the initial pressure-volume curves for each HiP and LowP example in Figures 3 and 4 are below and above the average starting volume respectively. As shown in Figures 3 and 4 the passive and active (Vo) pressure-volume properties both shifted corresponding to the stable, increasing, and decreasing SMV volume in IsoVol, HiP, and LowP SMVs, respectively. In IsoVol SMVs the increasing slope of the passive pressure-volume curve beyond the resting volume of 40 mL during conditioning demonstrates that IsoVol SMV compliance decreased during conditioning. The decrease in compliance was approximately complete after 6 weeks. In IsoVol SMVs, Vo decreased toward the fixed implant volume of 40 mL (fixed expander circumference) during conditioning.
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Fig 3. The progression of passive pressure-volume curves for selected testing sessions are shown for representative skeletal muscle ventricles (SMVs) from each group. The passive pressure-volume properties shifted corresponding to the stable, increasing, and decreasing SMV volume in isovolumetric (Iso Vol) (top), high pressure (HiP) (middle), and low pressure (LowP) (bottom) SMVs, respectively (arraows). Postoperative dates: (top) circles = 13, squares = 18, diamonds = 28, Xs = 37, vertical dashes = 46, triangles = 56; (Middle) circles = 21, squares = 28, diamonds = 42, Xx = 49, vertical dashes = 55, triangles = 63; (bottom) circles = 15, squares = 21, diamonds = 33, Xx = 56.
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Fig 4. The progression of active pressure-volume curves for selected testing sessions are shown for representative skeletal muscle ventricles (SMVs) from each group. Pressures were evoked with single stimuli (twitches). The volume for peak pressure generation shifted toward the stable, increasing, and decreasing SMV volume in isovolumetric (IsoVol) (top), high pressure (HiP) (middle), and low pressure (LowP) (bottom) SMVs, respectively (arrows). Postoperative dates: (top) circles = 14, squares = 29, diamonds = 49, Xs = 56; (middle) circles = 18, squares = 42, diamonds = 52, Xs = 63; (bottom) circles = 15, squares = 21, diamonds = 33.
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The progressions of peak evoked isovolumetric pressures are shown in Figure 5.
Evoked pressures during testing sessions before postoperative day 21 are underestimated. Resting pressures required to reach peak-evoked pressure were not reached in all animals owing to initial concerns over SMV integrity. Initial evoked pressures were quite high when examined. For example in one SMV the peak-evoked pressure was 272 mm Hg at a volume of 26 mL on postoperative day 14.
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Fig 5. Progressions of the peak evoked (twitch) isovolumetric pressures generated during testing sessions for skeletal muscle ventricles (SMVs) in each group. Evoked pressures before postoperative (PO) date 21 are underestimated. (IsoVol = isovolumetric; HiP = high pressure; LowP = low pressure.)
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Chronic SMV volumes
Every HiP SMV significantly expanded in volume during conditioning and did not exhibit a decrease in the rate of SMV volume expansion (Fig 6).
Temporarily pressure losses resulted in substantially reduced volumes. The average rate of expansion was 0.50 ± 0.101 mL daily over the conditioning period. Based on the circumference-to-volume relationship determined before implantation, the muscles increased in length an average of just less than 1% per day. The HiP SMV resting volumes at terminal testing were slightly larger (46.4 ± 8.50 mL) than the 40-mL IsoVol SMVs.
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Fig 6. The volume expansion of each high pressure (HiP) skeletal muscle ventricle (SMV) is shown as a function of postoperative (PO) date. The SMV volumes at a pressure of 40 mm Hg are shown. Every HiP SMV expanded in volume during conditioning and did not exhibit a decrease in the rate of SMV volume expansion. A linear regression line based on the pooled data from all experiments is shown. The average rate of expansion was 0.50 ± 0.101 mL per day over the conditioning period.
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Three of four LowP SMVs decreased in volume during conditioning and one expanded in volume more rapidly than HiP SMVs and ended at the greatest SMV resting volume (approximately 80 mL). Low pressure SMV volumes were greater than HiP SMVs during postoperative days 0 to 14 but were similar on postoperative day 14 (Table 2). One LowP SMV developed an implant tubing kink on postoperative day 37 with a volume of approximately 20 mL. In two LowP SMVs volume decreased and did not recover at 40 mm Hg after a temporary pressure lost on postoperative day 21 in one and after the stimulation protocol increased on postoperative day 28 in another.
Histologic analysis
Every SMV demonstrated an increase in either type I or type IIC oxidative-staining fibers (Table 3).
Each group increased from approximately 30% to 50% type I fibers and demonstrated a significant increase in the population of type IIC fibers to approximately one third of the total population. Only one control sample exhibited type IIC fibers (<5%). Muscle damage was focused in the inner layer of the SMV wall (7 of 8 SMVs) and in the inner muscle wrap if two were present (4 SMVs). Qualitatively there was some degree of damage or inflammatory response observed at the inner layer of the muscle wall of almost every SMV, with relatively less damage observed in IsoVol SMVs.
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Comment
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SMV conformation
In all 14 SMVs pressure-volume properties conformed to the implant during conditioning. The SMV volume-pressure data yield information on muscle length-tension properties. The passive and active pressure-volume properties adapted to the fixed resting volume in IsoVol SMVs and the progressively increasing or decreasing resting volume in HiP and LowP SMVs, respectively (Figs 3 and 4). These SMV conformations or muscle length-tension adaptations are consistent with studies investigating conformational adaptations of SMVs [7] and skeletal muscle fixed at reduced and increased lengths [3]. In mouse soleus muscle fixed in shortened or lengthened positions for 3 weeks, passive length-tension curves demonstrated shifts toward a reduced muscle length or no shift respectively [3]. The peak of active length-tension curves demonstrated shifts toward a reduced muscle length and reduced peak tension and a shift toward an increased muscle length and slightly increased peak tension respectively [3]. The muscles were shown to reduce or add sarcomeres when fixed in a shortened or lengthened position respectively [3].
Peak evoked isovolumic pressures in all groups decreased during the first 4 weeks of conditioning, as may be expected due to muscle fiber type conversion and damage [3]. Volume expansion (HiP SMVs and 1 LowP SMV) and decrease (LowP SMVs) should result in reduced and increased pressures respectively as predicted by Laplace’s Law. The lack of an observed increase in evoked pressures in LowP SMVs suggests that the damaging effects of a reduced resting tension [2] were greater than the increase predicted by Laplace’s Law.
Isovolumetric SMVs demonstrated a progressive decrease in compliance above the 40-mL resting volume. That may be due to increased muscle stiffness, which increases with conditioning [13], or to the implant capsule. Dynamically trained (HiP and LowP) SMVs did not demonstrate a decrease in compliance above the inflection point of the pressure-volume curve; however the changing SMV volume may have prevented observation of this effect. A reduced SMV compliance above a fixed volume limits SMV expansion with increases in pressure and results in a more stable SMV volume. Conformation of Vo or optimal muscle length in IsoVol SMVs was complete after approximately 4 weeks depending on the level of initial stretch. This timecourse is less than the 9-week isovolumetric conditioning phase used by Stephenson’s group [8–11]. These data support Stephenson’s use of an initial isovolumetric SMV training phase, which may result in more volume-stable SMVs with a greater resistance to expansion than SMVs directly connected to the circulation.
Volume expansion
One of the most striking results of this study was the observation that every HiP SMV and one LowP SMV continuously expanded in volume during conditioning at physiologic pressures (40 to 120 mm Hg) near or below those expected clinically. Chronic SMV expansion effects pumping performance and is likely dynamically unstable because expansion at a constant pressure will result in an increasing wall tension. Clinical application of SMVs would likely utilize larger SMVs with similar wall thicknesses. Therefore these results suggest that clinically sized SMVs would be chronically unstable at physiologic pressures without the use of a supporting implant to reduce SMV wall stress or a reduction in SMV compliance. These results have a greater impact on SMV clinical implementation using Stephenson’s approach [8–11], which does not use a limiting implant, rather than those of Guldner [14, 15] and Whalen [16], which use stress-limiting implant designs. SMV wall hypertrophy would also reduce wall stress; therefore the use of androgenic drugs which increase the power and hypertrophy of dynamically conditioned SMVs [15] may also limit SMV expansion. Similarly, the collapse of LowP SMVs suggests that right-heart SMV applications will require a minimum wall stress or chamber size to maintain chronic stability. The potential impact of these results suggests that the threshold wall stresses for chronic SMV expansion and collapse be examined in greater detail before SMVs are implemented clinically.
Chronic monitoring of SMV adaptations
Chronic monitoring of SMV pressure and volume on an almost daily basis was a valuable tool to monitor the time course of SMV performance and adaptations. Implant systems that allow monitoring of SMV performance during conditioning [14–19] provide the opportunity to predict performance and modify the conditioning protocol based on muscle performance. This study used this ability to match the rate of pressure expansion to each HiP SMV. Chronically conditioned SMVs adapt their peak pressure to changes in resting tension within a 2-week period [7]. This study demonstrated that SMV volumes could vary daily with SMV pressure changes.
Study limitations
The pressures used in this study did not effectively represent arterial pressures expected during clinical use. Maintaining steady pneumatic pressure levels inside the SMVs of conscious animals was technically challenging. Daily SMV pressure decreases are consistent with the variance of implanted, pneumatic system pressures observed in other studies [14, 17]. These problems likely resulted in the observed variability in SMV pressure and volume during conditioning. Condensation in the small diameter tubing between the SMV and the external reservoir increased airflow resistance and may have altered pressure during SMV ejection. Because experimental wall stresses in HiP SMVs were lower than expected during counter-pulsation applications, expansion was likely underestimated. Therefore our conclusions based on volume expansion are still valid. Conversely the variability in SMV volumes and pressures in LowP SMVs may have contributed to the collapse of these SMVs. Dynamic SMV conditioning may mimic physiologic conditions more accurately than isovolumetric training; therefore the results may be more predictive despite the technical challenges involved.
Histologic analysis
Although every muscle demonstrated an expected shift in fiber types, most muscles contained fast fibers, which are preferred for cardiac assistance. Although this suggests that the stimulation protocol used (4 stimuli per burst, 15 beats per minute) maintains a population of fast fibers, the stimulation level used was less than typically used during cardiac assistance that results in complete conversion. Therefore fiber type conversion may only have been slowed.
Dynamic training may result in greater damage than isovolumetric training. Dynamic SMVs were directly exposed to SMV resting pressures, resulting in greater SMV wall tensions and higher intramuscular pressures, which can interfere with muscle perfusion. These factors and chronic length changes likely contributed to the damage focused on the inner muscle layers. Although the greater damage observed in dynamic (HiP and LowP) than IsoVol SMVs (Table 3) was not statistically significant, the low p values suggest that a larger sample size would result in statistical significance.
Skeletal muscle ventricles conform to the implant system and resting pressures utilized during conditioning. The SMVs exposed to physiologic pressures near but below those expected clinically continuously expanded, which will affect pumping performance and is dynamically unstable. Clinically sized SMVs may therefore be chronically unstable unless a supporting implant is used to reduce SMV wall stress or SMV compliance is decreased. The potential impact of these results on SMV stability suggests that the mechanisms involved in chronic SMV expansion and critical wall stresses for chronic SMV expansion be further examined to optimally design SMVs for clinical implementation. (5)
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Acknowledgments
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This work was supported by the American Heart Association, Arizona Affiliate, and the Plastic Surgery Educational Foundation. Medtronic, Inc, provided stimulators and electrodes. Mentor Corporation and Willem Kolff and Dan Bishop at the Artificial Heart Center, University of Utah, provided tissue expanders. Special thanks to Tedd Brandon for assistance with the surgical procedures. Additional support was provided by National Institutes of Health K25 HD40298.
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References
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- Jarvis J.C., Mayne C.N., Salmons S. Basic studies on skeletal muscle for cardiac assistance. J Card Surg 1991;6(Suppl):204-209.[Medline]
- El Oakley R.M., Jarvis J.C., Barman D., et al. Factors affecting the integrity of latissimus dorsi muscle grafts: implications for cardiac assistance from skeletal muscle. J Heart Lung Transplant 1995;14:359-365.[Medline]
- Williams P.E., Goldspink G. Changes in sarcomere length and physiological properties in immobilized muscles. J Anat 1978;127:459-468.[Medline]
- Goldspink D.F., Easton J., Winterburn S.K., Williams P.E., Goldspink G.E. The role of passive stretch and repetitive electrical stimulation in preventing skeletal muscle atrophy while reprogramming gene expression to improve fatigue resistance. J Card Surg 1991;6:218-224.[Medline]
- Williams P.E., Catanese T., Lucey E.G., Goldspink G. The importance of stretch and contractile activity in the prevention of connective tissue accumulation in muscle. J Anat 1988;158:109-114.[Medline]
- Leighton W.D., Russell R.C., Feller A.M., Eriksson E., Mathur A., Zook E.G. Experimental pretransfer expansion of free-flap donor sites: II. Physiology, histology, and clinical correlation. Plast Reconstr Surg 1988;82:76-87.[Medline]
- Gealow K.K., Solien E.E., Bianco R.W., Chiu R.C.-J., Shumway S.J. Conformational adaptation of muscle: implications in cardiomyoplasty and skeletal muscle ventricles. Ann Thorac Surg 1993;56:520-526.[Abstract]
- Niinami H., Hooper T.L., Hammond R.L., et al. Functional evaluation of intrathoracic versus extrathoracic skeletal muscle ventricles. J Surg Res 1993;54:230-236.[Medline]
- Lu H., Fietsam R., Hammond R.L., et al. Skeletal muscle ventricles: left ventricular apex to aorta configuration. Ann Thorac Surg 1993;55:78-85.[Abstract]
- Nakajima H., Nakajima H.O., Thomas G.A., et al. Chronic morphologic changes of skeletal muscle ventricles in circulation. Ann Thorac Surg 1994;57:912-920.[Abstract]
- Thomas G.A., Lu H., Isoda S., et al. Pericardium-lined skeletal muscle ventricles in circulation up to 589 days. Ann Thorac Surg 1994;58:978-988.[Abstract]
- Gustafson K.J., Sweeney J.D., Gibney J., Brandon T.A. Progressive pressure expansion in skeletal muscle ventricle conditioning. ASAIO J 1996;42:M360-M364.[Medline]
- Trumble D.R., LaFramboise W.A., Duan C., Magovern J.A. Functional properties of conditioned skeletal muscle: implications for muscle-powered cardiac assist. Am J Physiol 1997;273:C588-C597.
- Guldner N.W., Eichstaedt H.C., Klapproth P., et al. Dynamic training of skeletal muscle ventricles. A method to increase muscular power for cardiac assistance. Circulation 1994;89:1032-1040.[Abstract/Free Full Text]
- Guldner N.W., Klapproth P., Grossherr M., et al. Biomechanical hearts: muscular blood pumps, performed in a 1-step operation, and trained under support of clenbuterol. Circulation 2001;104:717-722.[Abstract/Free Full Text]
- Whalen R.L., Richards C.L., Lim G.W., et al. A ventricular assist device powered by conditioned skeletal muscle. Ann Thorac Surg 1999;68:780-784.[Abstract/Free Full Text]
- Acker M.A., Hammond R.L., Mannion J.D., Salmons S., Stephenson L.W. An autologous biologic pump motor. J Thorac Cardiovasc Surg 1986;92:733-746.[Abstract]
- Trumble D.R., Magovern J.A. A muscle-powered energy delivery system and means for chronic in vivo testing. J Appl Physiol 1999;86:2106-2114.[Abstract/Free Full Text]
- Reichenbach S.H., Gustafson K.J., Egrie G.D., Weidman J.R., Farrar D.J., Hill J.D. Evaluation of a skeletal muscle energy convertor in a chronic animal model. ASAIO J 2000;46:482-485.[Medline]
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Abstract
Introduction
