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Eur J Cardiothorac Surg 1999;14:304-310
© 1999 Elsevier Science NL

Preconditioning of the latissimus dorsi muscle in cardiomyoplasty: vascular delay or chronic electrical stimulation¹

Jewish Hospital Cardiothoracic Surgical Research Institute, Department of Surgery, University of Louisville School of Medicine, Louisville, KY, USA

Received 29 September 1997; received in revised form 5 April 1998; accepted 12 May 1998.

Corresponding author. 511 S. Floyd Street, MDR Building #315, University of Louisville, Louisville, KY 40292, USA. Tel.: +1 502 8524345; fax: +1 502 8521795.

	Abstract

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Objectives: In standard single stage cardiomyoplasty (CMP), the latissimus dorsi muscle (LDM) is not preconditioned prior to surgery. We hypothesized that latissimus dorsi preconditioning by vascular delay or by chronic electrical stimulation would result in an improved LV hemodynamic function early (14 days) after CMP. Methods: Mongrel dogs had preconditioning of the latissimus dorsi by a vascular delay procedure followed by CMP 14–18 days later (group I VD). Dogs in group II underwent 4 weeks of chronic stimulation (CS) of the latissimus dorsi (2 V/30 Hz, six bursts/min) followed by CMP. The latissimus dorsi muscle was fully stimulated from 48 h after cardiomyoplasty in both groups (2 V/30 Hz, three bursts/min). Two weeks after myoplasty, injecting 2.0–3.0x10⁵ 90 µm latex microspheres in the left main coronary artery induced global cardiac dysfunction. Hemodynamic function was then evaluated for latissimus dorsi muscle assisted (S) beats and non-stimulated beats (NS) in each group by measuring peak systolic aortic pressure (AOP), left ventricular pressure (LVP) and end diastolic pressure (LVEDP), and by calculating maximum and minimum dP/dt. Results: Dogs with vascular delay of the latissimus dorsi showed a marked increase for all hemodynamic indices (AOP: 23.9±2.5%, LVP: 23.5±2.2%, max dP/dt: 49.4±3.3%) for LDM assisted (S) beats compared to non-stimulated beats (P<0.001). Animals with chronic electrical training did not demonstrate a significant increase in any hemodynamic parameter with LDM stimulation. Conclusion: Preconditioning the LDM may play an important role in providing early cardiac assistance in CMP. Preconditioning the LDM with vascular delay resulted in improving performance of the LDM with consistent increases in LV hemodynamics. This was not observed after preconditioning with chronic electrical stimulation. Vascular delay of the latissimus dorsi can significantly improve muscle performance in CMP and could provide hemodynamic assistance early after surgery.

Key Words: Cardiomyoplasty • Vascular delay • Preconditioning • Chronic stimulation

	Introduction

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Dynamic cardiomyoplasty (CMP) is a surgical treatment for congestive heart failure, in which the latissimus dorsi muscle (LDM) of the patient is wrapped around the heart to work as a cardiac assist. The outcome of the procedure depends on the performance of the latissimus dorsi. While the NYHA class status improves almost uniformly after CMP [1] [2] [3] [4], most experimental and clinical studies have not consistently demonstrated active cardiac assistance by the LDM contraction [1] [2] [3] [4] [7] [8] [9] [10]. The improvement in clinical status has been hypothesized to be through mechanical support or `girdling' of the heart by the LDM [1] [5]. Ischemia of the distal LDM has been blamed for lack of objective hemodynamic benefit [9] [10] [11].

The training of the LDM starts 2 weeks after CMP surgery and lasts for 12 weeks. During this 12-week period, the LDM is transformed into a fatigue resistant muscle. The rationale for the delayed stimulation has been to allow the thoracodorsal artery to gradually adapt itself as the main blood supply to the LDM and to allow adhesions to form between the LDM and the epicardium [1] [4] [6]. Thus, substantial systolic assistance by the LDM is not available initially after surgery, when it is critically required.

We hypothesized that preconditioning the LDM prior to CMP would improve its performance in providing significant cardiac assistance after myoplasty. To test this hypothesis, LDM preconditioning with either vascular delay or chronic electrical stimulation was performed prior to cardiomyoplasty followed by hemodynamic evaluation 2 weeks later.

	Methods

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Animals received humane care according to the guidelines set by the `Guide for Care and Use of Laboratory Animals' (NIH publication 85–23, revised 1985). All the animals were previously healthy. The University Animal Care and Use Committee approved this study.

Large chest mongrel dogs (27–30 kg) underwent dynamic CMP in two groups. In group I (VD, n=5) animals underwent vascular delay of the LDM followed by cardiomyoplasty 14–18 days later. Group II (CS, n=5) had 4–5 weeks of chronic LDM stimulation followed by CMP. In both groups muscle stimulation was initiated 48 h after the CMP surgery.

Sterile surgical procedures were carried out in designated operating suites. Cefazolin sodium 500 mg (Marsam Pharmaceutical, Cherry Hill, NJ) and gentamicin 75 mg (Gentocin^TM, Ayerst Laboratories, Rouses Point, NY) were administered before the incision. Oxygen saturation and ECG (Hewlett Packard Model No. 78346A) were monitored continuously. Animals received Lactated Ringer's solution intravenously (250 ml–350 ml/h) during surgery.

Vascular delay
After fasting overnight, the animals in group I (vascular delay) were anesthetized with intravenous 2.5% sodium thiopental (Pentothal sodium, 15–25 mg/kg i.v.) and atropine (0.01 mg/kg). The animals were intubated and placed on a ventilator (Quantiflex, VMC Anesthesia Machine, Orchard Park, NY). Anesthesia was maintained by isoflurane at 2% (Isoflurane Vaporizer, Oharda, Isotec 3, Aushell, GA), 0.5–1.0% nitrous oxide and oxygen. Antibiotics were administered before, and 6 h after, the procedure. Using sterile techniques, a 15–20 cm left oblique thoracic incision was made parallel to the anterior margin of the LDM. The margin of the LDM was elevated, and all the perforating blood vessels supplying the undersurface of the LDM were ligated. The superior, or the subcutaneous, surface of the muscle was left undisturbed. The incision was closed in layers using absorbable sutures. The animal was then returned to its cage and allowed to recover. Buprenorphine hydrochloride 0.3–0.6 mg IV (Bupernex HCl, Reckitt and Coleman Pharmaceuticals, Richmond VA) was used for analgesia every 3–4 h, as needed, for 1–2 days after the procedure. CMP was performed 14–18 days later.

Muscle stimulator (ITREL) implantation
After fasting overnight, the animals in group II (chronic stimulation) were anesthetized with atropine (0.01 mg/kg) and sodium thiopental (2.5% Pentothal 15–25 mg/kg i.v.) followed by isoflurane at 2% with 0.5–1.0% nitrous oxide and oxygen. Using sterile techniques, a 7–10 cm left oblique thoracic incision was made. The margin of the LDM was elevated and the thoracodorsal neurovascular bundle identified. Two epimysial leads (model YY38403403 Medtronic, Minneapolis, MN) were implanted across the neurovascular pedicle and connected to the stimulator (ITREL model 7420 Medtronic, Minneapolis, MN). An A-V Pacing System Analyzer 5311 (Medtronic, Minneapolis, MN) was used to determine the stimulation threshold. The stimulator was switched on at 30 Hz, 1–2 V, and a pulse train duration of 185 ms. Stimulation was started on the second postoperative day at three pulse trains/min. This stimulation was then increased to deliver pulse trains six times/min after 2 weeks and maintained at this level for the next 2–3 weeks. No vascular delay was performed in this group. The CMP procedure was performed after 4–5 weeks of in situ chronic electrical stimulation of the LDM.

In both groups, CMP surgery was performed with the model used in our laboratory in the past and as described below [21] [22]. Anesthesia was induced as described previously, and the animals were placed in the right lateral decubitus position. An oblique 15–20 cm incision was made along the anterior border of the LDM. The left LDM was elevated and carefully taken down from all of its attachments except proximally on the humerus. The neurovascular pedicle with the thoracodorsal nerve and artery were identified and preserved. The tendon of the LDM was then carefully isolated and divided. In the group I with vascular delay, epimysial leads were implanted on the pedicle with nylon sutures. The ITREL muscle stimulators were implanted and connected to the epimysial leads in all animals. The stimulation threshold was determined by an A-V Pacing System Analyzer 5311. Group II (CS) had the ITREL stimulators implanted prior to CMP and did not require lead attachment and threshold determination. The stimulator in this group, however, was switched off just before surgery and then activated again from second post-operative day. A 4–5 cm section of the left second rib was removed and LDM rotational flap moved inside the chest. The incision was closed in layers.

The animal was then placed in the supine position and the chest was opened by median sternotomy. The posterior wrap of the LDM was performed in a clockwise direction around the heart approximating the costal surface of the LDM to the epicardium. We were able to perform a complete 360° posterior wrap in all animals. Bilateral chest tubes were inserted and the chest was closed with steel wire sutures. Animals were extubated and returned to their cages. Intravenous buprenorphine hydrochloride (0.3–0.6 mg) was given as needed for analgesia. Acepromazine (0.25–0.5 mg; PromAce^TM Fort Dodge Lab., Fort Dodge, IA) was given every 10–12 h for sedation for the first 24 h. To avoid prolonged pressure on the left side, animals were positioned to lie on their right side overnight. Chest tubes were removed on the first post-operative day. Antibiotics (cefazolin 500 mg and gentamicin 75 mg every 12 h) were used for 48 h post-operatively.

In both groups, LDM stimulation was started 48 h after surgery. Asynchronous muscle stimulation was initiated using the following settings: 1–2 V or twice the threshold voltage, a 30 Hz inter-pulse frequency, and a pulse train duration of 185 ms. The muscle was stimulated at three pulse trains/min in the first week and six pulse trains/min during the second week.

Hemodynamic evaluation
Experimental preparation
Animals were evaluated 15±2 days after the CMP procedure. Anesthesia was induced as described previously and maintained with intravenous phenobarbital 50–100 mg/h (Nembutal® Sodium Abbott Laboratories, Chicago, IL). No atropine was used. Arterial cut downs were made to place introducer catheters in the carotid and femoral arteries. Micro-manometer tipped catheters (Millar® Instruments, Houston, TX) were used to measure pressure. Using fluoroscopic guidance, the pressure transducer catheters were placed, via the femoral and carotid arteries, into the left ventricle and the descending aorta, respectively. Analog signals from the pressure transducers were amplified (PM-1000 CWE, Admore, PA). The epimysial leads were disconnected from the ITREL pulse generator and connected to an external pulse generator (GRASS®Model 8800, Grass Systems, Quincy, MA). A Cardiotachometer (Model 1000 CWE, Admore, PA) detected the R wave from the analog ECG signal (Hewlett Packard Model No. 78346A). The cardiotachometer in turn triggered the GRASS stimulator, synchronizing LDM stimulation with the R wave of every fourth to sixth heart beat.

Cardiac dysfunction was induced by an intracoronary injection of microspheres. A 5F or 6F left Ampltz coronary artery catheter was placed in the left anterior descending artery using fluoroscopic guidance. Latex microspheres 1.0–2.0x10⁵ 90µm (Polyscience, Warrington, PA) were then injected into the left anterior descending artery to depress cardiac function by decreasing the +dP/dt by 20% [20]. Data acquisition was performed after myocardial damage was verified.

Data acquisition
Data were recorded simultaneously on a chart recorder (Model TA-11, Gould Instrument Systems, Cleveland, OH) and on a computer (WINBOOK XP5 120 MHz Pentium, Winbook Computer Corp., Columbus, OH). The analog signals (ECG, pressures) were digitized using an A/D circuit board (model DAS-1601 Keithley Metrabyte, Taunton, MA). The data were acquired using LABTEC NOTEBOOK® software (Laboratory Technologies Corp., Wilmington, MA). The muscle stimulator was switched on for every fourth to sixth heartbeat using supra-maximal threshold voltage. Pulse train duration was adjusted between 150 and 190 ms, pulse duration 0.5 ms, pulse interval of 20–40 ms, and delay after the R wave was adjusted between 20 and 80 µs. Each data run was 30 s long with an interval of at least 3–5 min between files. The ventilator was switched off during data acquisition to avoid respiratory variations.

After the experiment, the anesthetized animal was euthanized by intravenous injection of pentobarbital (10 mg/kg), followed by 20–30 ml of intravenous saturated potassium chloride solution.

Data analysis
Using software developed in Visual Basic (Microsoft Excel for Windows 95, Microsoft, Cambridge, MA), hemodynamic variables were extracted from digitally stored data files. Ectopic beats and post ectopy beats were excluded from the analysis. For each beat, the peak left ventricular systolic pressure (LVP), peak aortic pressure (AOP), LV end diastolic pressure (LVEDP), and the positive and negative first derivative of the left ventricle pressure (±dP/dt) were recorded. Data were reported as mean±SEM.

Statistical analysis
A software package (StatView 4.5; Abacus^TM Concepts; Berkley, CA) was used for statistical analysis. The hemodynamic data of stimulated beats were compared with those of the immediately preceding non-stimulated beats within each group. Statistical significance was determined using a one-way analysis of variance (ANOVA) if P<0.05.

	Results

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Fig. 1 shows a typical data trace for one experiment with chronic electrical stimulation. LV pressure, maximum and minimum dP/dt and the ECG tracings are shown. The LDM was stimulated on every fifth to sixth heartbeat. Muscle stimulation resulted in a small increase in left ventricular and aortic pressure and no increase in +dP/dt.

View larger version (46K): [in this window] [in a new window]   Fig. 1. Typical data trace for group (CS) showing LVP: LV pressure, ±dP/dt and ECG. Note slight increases for stimulated beats compared to non-stimulated beats.

View larger version (30K): [in this window] [in a new window]   Fig. 2. Typical data trace for animal in VDES showing LVP: LV pressure, ±dP/dt and ECG. Note marked increases for stimulated beats compared to non-stimulated beats.

View larger version (43K): [in this window] [in a new window]   Fig. 3. Increase for LVP (mmHg) in both groups. Marked increases for LV pressure increase for vascular delay.

View larger version (44K): [in this window] [in a new window]   Fig. 4. Absolute increases for first derivative of LV contraction +dP/dt with LDM stimulation. Note marked increase for group with vascular delay.

View larger version (27K): [in this window] [in a new window]   Fig. 5. Absolute changes in minimum dP/dt with LDM stimulation. The minusdP/dt is more negative with LDM stimulation in vascular delay group, whereas it is more positive with LDM stimulation in the chronic stimulation group, indicating a restrictive filling.

	Discussion

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Since the first clinical cardiomyoplasty in 1985, this procedure has been performed in over 600 patients. The most common form of the procedure involves wrapping the left latissimus dorsi muscle around the heart as a posterior wrap [1] [2] [3] [4] [10]. Although functional class improvement is present in most patients after cardiomyoplasty, active systolic support with LDM stimulation has not been demonstrated consistently [1] [2] [3] [4] [8] [9] [10].

To improve the LDM performance and institute early cardiac assistance, several approaches to precondition the LDM before CMP have been suggested. Two reported methods of preconditioning have been chronic electrical stimulation and vascular delay of the muscle before CMP [12] [13] [14] [15] [16] [17] [18] [19] [20].

Chronic electrical training of the LDM prior to CMP has been studied in various experimental models [12] [13] [14] [16]. Mannion et al. [12] examined chronic electrical stimulation and/or vascular delay as done for CMP. They demonstrated that, after mobilizing the LDM, chronic electrical preconditioning of the LDM prior to CMP significantly increased, but did not totally restore, exercise-induced blood flow to the distal part of the muscle when compared to contralateral in situ LDM. They concluded that, after chronic electrical training of the muscle, the LDM can withstand mobilization better than muscle that did not have chronic electrical training. Mobilizing the LDM after vascular delay of the LDM showed improved blood perfusion of the distal part of the muscle. Chagas et al. [13] performed vascular delay of the flap followed by 6–8 weeks of chronic electrical stimulation of the muscle before CMP surgery. One week after CMP they found no difference in hemodynamic function between conditioned and non-conditioned groups. Soberman et al. [14] used electrical preconditioning of the LDM prior to cardiomyoplasty. He also did not find any difference in hemodynamic indices between conditioned and non-conditioned groups.

Tobin et al. [18] [19] determined that humans had an average of 15 perforating intercostal arteries, which contributed 67% of the vascular supply to the LDM. In dogs, the perforating intercostal arteries contributed 69% of the vascular supply to the canine LDM. Muscle mobilization resulted in decreasing its blood supply by more than 90%. In a similar study, Durham et al. [23] evaluated blood flow before and after LDM manipulation for CMP. After severing all collateral vessels, they found decreases in blood flow to the proximal and distal LDM of 40% and 70%, respectively. After CMP (LDM mobilization and re-attachment), they found decreases in blood flow to the proximal and distal LDM of 70% and 82%, respectively.

Role of vascular delay
In dogs, Isoda et al. [17] demonstrated that a 1 month vascular delay period significantly enhanced muscle flap perfusion at rest and during exercise. Carroll et al. [15] wrapped the LDM around a silicone tube after 10 days of vascular delay of the flap. They concluded that a 10-day vascular delay not only significantly increased perfusion in the middle and distal LDM during exercise but also improved the degree of fatigue resistance in the muscle.

You et al. [24] ligated the collateral blood vessels to the LDM 2 weeks before CMP. Histological examination confirmed that the two-stage procedure preserved normal LDM architecture. Immediately after CMP surgery, acute heart failure was produced, and LV hemodynamic function was assessed. LDM stimulation increased stroke volume and left ventricular elastance. However, the effects of LDM stimulation were only observed immediately after surgery.

Our study evaluated hemodynamic function after using two common modes of preconditioning of the LDM. In the chronic stimulation group (CS), the muscle was left in situ and chronically stimulated for 4–5 weeks. In the group with vascular delay (VD) the muscle was delayed in situ and not stimulated until after being mobilized, (48 h after the CMP surgery). After CMP surgery, in both groups, the muscle stimulation was initiated from the second post-operative day at three pulse trains/min. This rate was increased to six pulse trains/min in the week before final evaluation. The data from the current study suggests that preconditioning of the LDM with vascular delay, prior to CMP, can result in significant hemodynamic augmentation with LDM assistance when measured at 2 weeks after the CMP.

The limitations of this study should be kept in mind. In both groups, the LDM was similarly stimulated after CMP surgery. However, in the vascular delay group, the LDM was not stimulated prior to CMP surgery. Thus, the percent conversion to slow type I fibers was probably different between the groups. Unfortunately, we did not perform histological analysis for fiber typing.

For clinical cardiomyoplasty, the muscle has to be trained and changed from a fast twitch muscle to a fatigue resistant muscle. The present study demonstrates that the hemodynamic benefit for LDM assisted beats with increases in LV systolic and diastolic function is present after cardiomyoplasty if the LDM is prepared with a vascular delay procedure. The LDM preconditioning may play an important role for providing early benefit after cardiomyoplasty and shortening the overall training period.

	Acknowledgments

 
We would like to express our gratitude to Medtronic Inc., Minneapolis, MA, for providing technical support and ITREL muscle stimulators. Our thanks to Dr. Sam Haydar for providing technical assistance in setting up Labtec Notebook software and data acquisition hardware. We would also like to thank Dr. James Sharp, Nancy Hughes, Edwin Ford, Dorothy Wilson and the RRC staff at the University of Louisville, KY, for providing dedicated animal care in the pre- and post-operative period. This study was supported in part by a grant from The Jewish Hospital Heart and Lung Foundation.

	Footnotes

 
Presented at the 11th Annual Meeting of the European Association for Cardio-thoracic Surgery, Copenhagen, Denmark, September 28 – October 1, 1997.

	Appendix A. Conference discussion

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Dr W. Klepetko (Vienna, Austria): Could you comment a little bit more on the technique of the vascular delay, how you achieved that? I didn't really pick that up completely.

Dr Ali: Vascular delay has been referred to in the literature as the delay before the stimulation is started after myoplasty. In our institution, vascular delay is ligating the intercostal vessels supplying the latissimus dorsi, especially the distal part of the latissimus dorsi, 15 days before mobilizing it. We do that, leave the muscle in situ, and then mobilize it. In studies by Dr. Mannion and Dr. Tobin, vascular delay has been shown to improve blood supply to the distal part, which does get ischemic in myoplasty because most of the latissimus dorsi is supplied by the intercostal vessels in the distal third.

Dr J. Pepper (London, UK): I have two questions. Do you have any histological data on damage to the latissimus dorsi muscle? Secondly, your model of failure doesn't look very profound. The ventricle was able to generate pressure of 150 mmHg. Do you have any comments about that? Are you satisfied with the quality of your heart failure model?

Dr Ali: I'll answer the second part first. The typical model that I showed was the best dog in that group. Our mean LV pressure was 128 and that was after we gave at least 1 million microspheres. We had a decrease of dP/dt by 20%. Then we proceeded with the hemodynamic evaluation. However, there is a paper that is coming in next month's ASAIO Journal that has compared hemodynamic changes in the heart failure model vs. normal heart model, and if cardiomyoplasty works, it will work in both models. And what was your first question?

Dr Pepper: Do you have any documentation of damage caused to the muscle?

Dr Ali: In our institution Dr. Tobin and our plastic surgery department have conducted a study where they looked at histological damage to the muscle. In the present study we did not look at histology. We only did hemodynamic evaluation after doing the actual cardiomyoplasty. It had been well documented that the muscle blood supply is improved with vascular delay.

Dr Pepper: And this was an acute study that you did?

Dr Ali: It was at 2 weeks after cardiomyoplasty. However, I would like to show you a slide. Your point is well taken that we should see it long term. This slide shows an animal in which we had cardiac dysfunction before cardiomyoplasty. The aortic flow is at the top, increasing the dP/dt, as you can see with the stimulated beats. Every third beat is stimulated. This is 3 months out, and this is the next step in our study. Before doing a 3-month study we felt we should find out the right direction. If something is not working at 2 weeks, it's not going to work at 3 months. But your point is well taken, that we have to see a long-term study in this model.

	References

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