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J Thorac Cardiovasc Surg 1997;114:1097-1106
© 1997 Mosby, Inc.
CARDIOPULMONARY BYPASS, |
Supported by Bakken Research Center, Division of Medtronic, Maastricht, The Netherlands, Telectronics Pacing Systems Inc., Englewood, Colo., and A.D. Krauth GmbH, Hamburg, Germany.
Received for publication March 3, 1997 Revisions requested May 8, 1997 Revisions received June 6, 1997 Accepted for publication July 30, 1997 Address for reprints: Norbert W. Guldner, MD, Klinik für Herzchirurgie, Medizinische Universität zu Lübeck, Ratzeburgerallee 160, D-23538 Lübeck, Germany.
Abstract
Objective: To assess the impact of a dynamic cardiomyoplasty on failing hearts, it is essential to estimate the contraction force of the skeletal muscle and how its contraction is synchronized with the heart cycle. Methods: In a 6-month study a small fluid-filled, balloon-mounted catheter was placed between the myocardium and the muscular wrap in five adult female Boor goats and two female domestic pigs. The catheter was connected to a subcutaneous measuring chamber whereby pressure monitoring could be accomplished. Distinct pressure signals as a result of function of the dynamic cardiomyoplasty and the heart were detected initially in all animals. Results: Maximal relative pressure from the dynamic cardiomyoplasty was calculated as 336.2% ± 69.4% on day 24 ± 6.1 (n = 7) and end-stage pressure as 59.8% ± 9.7% on day 174.6 ± 13.1 (n = 4). A functional loss of pressure signals from the dynamic cardiomyoplasty was correlated to severe histologic muscle damage (n = 3). Pressure signals transferred from the contracting myocardium to the catheter showed defined segments of contraction, ejection, and filling periods, allowing a mechanical synchronization of the dynamic cardiomyoplasty to the heart cycle. Conclusions: This monitoring catheter enabled the assessment of the functional state of the dynamic cardiomyoplasty and allowed a synchronization to the heart cycle. It will promote understanding and might help to avoid muscle damage in dynamic cardiomyoplasty for an improved outcome of the surgical treatment of end-stage heart failure.
The first application of dynamic cardiomyoplasty (DCMP) was performed in 1985.
1 Although more than 600 procedures have been performed worldwide since then, the fundamental mechanics of the method are still not understood. Generally the patients seem to have improved physical capacity but objective measures do not always reflect this improvement. 2-6 In some clinical cases stroke work and left ventricular volume evaluation by the conductance catheter method disclosed functional improvement. 7,8 This technique only allows occasional assessment and cannot be used for a frequently applied routine examination of the training procedure. Thus a monitoring tool for evaluating and eventually optimizing the training procedure is not available today.
We hypothesize that measuring the pressure between the skeletal muscle and the myocardium could be an important tool for evaluation of the skeletal muscle contraction force and the timing of the myostimulator-induced muscle contraction in relation to the myocardial contraction. Therefore the purpose of this study was to evaluate a newly designed pressure registration system in two established DCMP animal models.
Material and methods
The implantable DCMP-monitoring double-lumen catheter (Fig. 1), constructed of polyurethane, was about 45 cm in length and 1.3 mm in diameter. At the tip, a nonextensible polyurethane balloon was mounted. Its diameter was 4 mm and its length 30 mm. The other end of the catheter was bifurcated: one branch entered a small vascular access port (Access Technologies, Skokie, Ill.) measuring chamber and the second branch a flexible tube that could be closed after filling. The balloon was filled with hypertonic saline solution to its maximal extent and then adjusted to atmospheric pressure. This procedure was repeated before each measurement to standardize measuring conditions.
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Xylazine hydrochloride 2% (Rompun), 0.2 mg/kg, and ketamine (Ketanest), 5 mg/kg, were used to induce general anesthesia. After endotracheal intubation, the lungs of the animals were ventilated with oxygen, and anesthesia was maintained with continuous delivery of propofol (Disoprivane), 4 to 6 mg/hr, through a central intravenous line via the internal jugular vein. Intermittent intravenous bolus delivery of a 1 to 2 mg/kg dose of ketamine was also done. There was no need to administer a muscle relaxant.
The goats and pigs were placed in the right lateral decubitus position and an oblique incision from the left axilla to the left iliac crest was made. The left latissimus dorsi muscle (LD) was dissected from its insertion and surrounding fascial attachments. Two intramuscular electrodes (Telectronics model IML-2) were inserted 6 cm apart around the branches of the thoracodorsal nerve. Five to six centimeters of the third rib was resected and the LD was transferred into the thoracic cavity. The free edge of the humeral tendon was then attached to the second rib. Animals were placed in the supine position and a median sternotomy was done. The left LD cardiomyoplasty was then performed in the standard posteroanterior fashion. The catheter was deaired by injection of saline solution. The balloon was then placed on the diaphragmatic posterior wall of the left ventricle, near the base of the ventricle. Before the DCMP wrap was completed with the use of a pericardial flap (Fig. 1, top), appropriate pressure signals of the catheter were verified. A ventricular screw-in sensing electrode (Telectronics model 033-572) and the myoelectrodes were then connected to a myostimulator (Telectronics model 7220) programmed with the following stimulation variables: amplitude 2.5 volts, burst starting with 2 pulses and a frequency of 50 Hz, a pulse width of 100 µsec, and a synchronization mode of 1 DCMP beat per 20 beats of the heart (1:20).
Stimulation was initiated immediately with no postoperative delay period. During the first 4 weeks after the operation the number of pulses per burst was increased from 2 to 10 (burst length 40 to 200 msec). In this phase the burst frequency was 1 to 20 heartbeats (1:20). In the following 8 weeks this frequency was gradually increased to 1:2 in goats 1 and 2, 1:4 in goat 3, and 1:8 in goats 4 and 5 and pigs 1 and 2 (Table I).
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Assessment of the long-term functional state of the DCMP was based on relative change in the DCMP amplitude during an assisted cardiac cycle. This amplitude was defined as the relation between the DCMP amplitude difference normalized by the heart amplitude difference as follows:
The relative change of heart amplitude over time was defined as the relation between the currently measured amplitude of the heart divided by the heart amplitude measured at the beginning of the study:
This relation is useful to document any change in signal amplitude over time, for example, change caused by encapsulation of the measuring balloon. These values were averaged from 10 cardiac cycles. Summarized results are represented by mean values and standard deviation (mean plus or minus standard deviation).
Two months after the operation, a 7F conductance catheter (Cardiodynamics, Leiden, The Netherlands) was inserted in goat 4 and pig 1. The conductance catheter was introduced by the Seldinger technique into the carotid artery and placed along the long axis of the left ventricle for real-time pressure-volume data acquisition. The mechanical signals from the cardiac cycle, as indicated by the DCMP monitoring catheter, were related to the pressure-volume data obtained by the conductance catheter to relate DCMP catheter recording to the cardiac cycle.
Histologic and histochemical examinations of the transposed skeletal muscle wrap were performed to compare functional results from the DCMP monitoring catheter with morphologic findings. Biopsy specimens were taken from the region of the LD muscle covering the posterior heart base. Three were taken for histologic evaluation and three for histochemical analyses. The pedicle of the LD muscle was not examined. Samples for the histologic examination were carefully mounted in 5 x 10 mm blocks and fixed in 4% buffered formaldehyde solution. Samples for adenosinetriphosphatase (ATPase) staining were quickly frozen in isopentane cooled in liquid nitrogen at –160° C. Microtome sectioning (8 µm thickness) was performed in a cryostat. Histologic evaluation was done after hematoxylin-eosin staining and histochemical analyses for fiber type were performed by ATPase staining at pH 4.35 according to the method of Brooke and Kaiser. 9,10
Results
High-quality pressure signals as a result of cardiac motion and DCMP contraction were obtained throughout training (Fig. 1). Pressure signals via the DCMP catheter were recorded several times during the observation period (Fig. 2). In four of seven animals, signals from the contracting DCMP were detected throughout the entire study period of 174.6 ± 13.1 days. In goats 1, 2, and 3, in all of whom a final synchronization mode of 1:2 and 1:4 was reached, no pressure signals as a result of a DCMP contraction were observable after postoperative week 8. In goats 4 and 5 and the two pigs, all of whom underwent a final synchronization mode of 1:8, no muscle failure of the examined LD muscle wrap was observed up to 6 months.
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An example of changes in pressure amplitude during DCMP and the heart contractions is shown in Figs. 2 and 3. The curves in Fig. 3 depict the relative pressure development. The amplitude of the relative DCMP signal showed an increase to a maximum of 421%, followed by a decline to a steady state of 67.6%. The relative pressure amplitude from the heart signal decreased to a steady state of 44.2%. Maximal relative pressure amplitudes of DCMP signals in all animals showed an increase up to a maximum of 336.2% ± 69.4% on day 24 ± 6.1 (n = 7) and decreased to a steady state with an end-stage value of 59.8% ± 9.7%. The relative heart signal declined from 100% initially (definition) to 44.9% ± 5.1% (Table II).
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At autopsy 
(Table I), the muscle wraps showed impressive morphologic differences. The LD muscle wrapped around the heart in goats 1, 2, and 3 was thin and fibrotic (Fig. 5, B), compared with that in goats 4 and 5 (Fig. 6, B). The muscle wrap in the two pigs was well preserved (Fig. 7, B), like that in goats 4 and 5.
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9,10 at a pH of 4.53. Type I fibers were dark, type IIa white, and type IIb gray. (Type I are slow twitch and fatigue resistant and type II are fast twitch but fatiguable muscle fibers.) Nonstimulated muscle tissue consisted of a mixture of type I and type II fibers as shown in Figs. 5, A, 6, A, and 7, A. After a stimulation period of about 6 months, the LD muscles in goats 1, 2, and 3, stimulated at 1:2 and 1:4, contained only a few fibers (type I), surrounded by connective and fatty tissue (Fig. 5, B). Most muscular tissue (type I fiber) was maintained in goats 4 and 5 and the two pigs, all with a final synchronization mode of 1:8 (Figs. 6, B, and 7, B). In these four animals the DCMP signals were detected up to the end of study. In this study the loss of the DCMP signals was found to correlate with severe morphologic deterioration of the muscle tissue. Discussion
Investigations with a fluid-filled measuring balloon interposed between the myocardium and LD muscle were reported previously to evaluate the transmural myocardial pressure after a DCMP procedure. 11 The pressure difference between the left ventricular cavity and the balloon was defined as transmural myocardial pressure. In that short-term study, a significant decrease in transmural myocardial pressure as an effect of DCMP was demonstrated. The purpose of our study, however, was to monitor the functional state of a DCMP over 6 months.
All seven monitoring catheters reported here showed an excellent transfer of pressure signals caused by heart activity from the beginning to the end of the study and from the DCMP when it was contracting well. The use of the hyperosmotic saline solution in the inner lumen of the catheter was intended to avoid a major volume loss. Nevertheless small quantities of volume had to be replaced before each pressure measurement to achieve comparable filling conditions.
Signals from the DCMP catheter provided information about the synergically contracting muscle in the entire area of the posterior wrap. The balloon was placed in the region where the DCMP covered the largest circumference of the heart. In the classic DCMP using the left LD muscle, the posterior wall of the left ventricle is always covered with the best textured part of the LD muscle. Therefore a balloon of 30 mm in length in that position gave representative information on the functional state of this consequential part of the muscle wrap. Perhaps a longer balloon might integrate a larger area of contracting tissue for a more representative evaluation of DCMP function.
The increase in amplitude within the first 3 weeks after operation might have been caused mostly by the increasing number of pulses per burst by our stimulation pattern and partly by the postoperative recovery of the muscle. The decrease in amplitude of the DCMP signals might have been caused by the loss in power, which was about one eighth of the original state, as is well-known and documented. 12 This was a result of fiber transformation from powerful type II fibers to less powerful but fatigue-resistant type I fibers (Figs. 5, B, 6, B, and 7, B).
Connective tissue reaction to the foreign material of the measuring balloon is supposed to have an influence on the measured signals. This was indicated by the relative heart amplitude, which decreased over time to 59.5% ± 13.9% of its original value. Of course, this decrease may be a dampening caused by encapsulation, but this effect could be overcome by the relative pressure calculation in which both pressure values (DCMP and heart) were influenced by the same connective tissue.
Muscle damage described after a stimulation mode of 1:2 and 1:4 was combined with an increase in connective and fatty tissue between the remaining type I fibers. These morphologic findings might be a result of extreme overstimulation with muscle damage and neural degeneration. Nevertheless, an ischemic origin of this muscular destruction cannot be excluded. A 1:8 mode was associated with maintained function and preserved muscle tissue. These findings are related to good clinical outcome in 14 patients with DCMP after 5
years with a 1:6 stimulation ratio. 13 We speculate that muscle damage will be key to long-term successful therapy. Further studies need to be undertaken to verify this finding under conditions that control for other possible causes of muscle damage.
Mechanical activity of the base of the posterior wall of the left ventricle (Fig. 4, MON) consisted of an ascending curve, a peak, and a descending part. The descending part was characterized by a small peak, which separated an ejection part from a relaxation section as shown in the measurements of the conductance catheter. These signals of the DCMP catheter allow synchronization of the DCMP with the heart cycle. If the ejection fraction of the heart should be improved, stimulation can be adjusted to induce contraction during the ejection phase. If a girdling or a remodeling is needed, 8 stimulation during the relaxation part might be conceivable but would need to be applied in a way that does not impair diastolic filling. It could be worthwhile to consider a "walk behind" contraction, which would mimic dynamic training during electrical conditioning, shown in skeletal muscle ventricles, to maintain or increase muscle power. 14,15
Clinical complications of applying an extravascular catheter should be low. Covering the catheter near the measuring chamber with a piece of Dacron felt for better integration with the tissue could prevent spreading of infection from skin to the heart.
Whereas the conductance catheter enables direct analysis of myocardial improvement, 16,17 this monitoring catheter can be applied to verify the contractile function of the LD muscle and the relative intensity of its contraction. Even contraction velocity can be documented by the slope of the DCMP contraction curve (not evaluated in this study). The coupling of the DCMP to the heart cycle can be observed, as well as the effect of varying stimulation parameters. Therefore this catheter could be useful in optimizing stimulation patterns; muscle damage can be prevented by adjusting the stimulation energy and by adjusting the loading conditions of DCMP through careful timing of the contraction during the heart cycle. Any benefit of drugs administered to strengthen the LD muscle could also be monitored. In our opinion, this monitoring catheter could be helpful in improving the outcome of the surgical treatment of heart failure with DCMP (Table III).
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Acknowledgments
We thank Mrs. Kerstin Lünsmann for her excellent care of the goats.
Footnotes
From the Clinic of Cardiac Surgery,a Medical University of Lübeck, Germany, and from the Department of Cardio-Thoracic and Vascular Surgery, Skejby Sygehus, Aarhus University Hospital,b Aarhus, Denmark. Institute of Anaesthesiology,c Department of Experimental Animal Care,d 
References
years: Russian clinical experience. J Thorac Cardiovasc Surg 1995;109:189-90.
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