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Cardiovascular Research 1998 40(1):131-137; doi:10.1016/S0008-6363(98)00094-7
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Copyright © 1998, European Society of Cardiology

Observation and basis of improved blood flow to the distal latissimus dorsi muscle: a case for electrical stimulation prior to grafting

Augustine T.M Tanga,b, Jonathan C Jarvisa, Timothy L Hooperb and Stanley Salmonsa,*

aDepartment of Human Anatomy and Cell Biology, University of Liverpool, Liverpool L69 3GE, UK
bDepartment of Cardiothoracic Surgery, Wythenshawe Hospital, Southmoor Road, Manchester, M23 9LT, UK

* Corresponding author: Tel.: 0-44-151-7945455; Fax: 0-44-151-7945517.

Received 3 September 1997; accepted 12 March 1998


   Abstract
Top
 Abstract
1 Introduction
 2 Methods
 3 Results
 4 Discussion
 References
 
Objective: Dynamic cardiomyoplasty, using a functional graft of the latissimus dorsi muscle, has shown promise as a treatment for selected patients with advanced heart failure. The success of this approach depends on maintaining the viability of the muscle, whose distal portion is susceptible to ischaemic damage. We investigated the effects of surgical mobilization on regional muscle blood flow and the influence of electrical stimulation of the muscle. Methods: Ten sheep were randomly assigned to two equal groups. In one group, the latissimus dorsi muscle was stimulated continuously in situ at 2 Hz for two weeks; in the other group, the muscle was not stimulated. Regional blood flows in the muscles were determined by a fluorescent microsphere technique. Serial measurements were made (a) under baseline conditions before intervention, (b) with the thoracodorsal artery occluded and (c) after interruption of the perforating collateral arteries. Results: Surgical mobilization of the unstimulated latissimus dorsi muscles had little effect on blood flow in the proximal region, which remained at 93.1±16.9% of baseline (mean±SEM). The distal region was rendered significantly more ischaemic (55.8±13.5% of baseline, p<0.002 compared to the proximal region). Electrical prestimulation abolished any significant proximodistal gradient in blood flow and improved distal muscle perfusion following mobilization (proximal vs. distal: 75.0±8.8 vs. 63.0±10.9%; p>0.4). Conclusions: Distal muscle ischaemia occurred when the entire latissimus dorsi muscle was acutely elevated on the thoracodorsal pedicle alone. Electrical prestimulation of the muscle in situ improved the thoracodorsal perfusion of the distal muscle by abolishing the proximal-to-distal gradient in flow, with a substantial benefit to distal flow after mobilization. Although electrical stimulation is known to induce vascular proliferation, we argue that this effect of stimulation is brought about mainly by enhancement of the flow through anastomotic connections between proximal and distal arterial territories.

KEYWORDS Sheep; Latissimus dorsi muscle; Regional blood flow; Electrical prestimulation; Fluorescent microspheres; Thoracodorsal artery; Perforatoring collateral blood supply


   1 Introduction
Top
 Abstract
 1 Introduction
2 Methods
 3 Results
 4 Discussion
 References
 
Dynamic cardiomyoplasty (DCM) has been used as a treatment for selected patients with end-stage heart failure since 1985 [1]. We and others have previously demonstrated that latissimus dorsi (LD) muscle grafts may suffer damage following cardiomyoplasty, especially in the distal portion [2–6]. During surgical mobilization, it is necessary to divide perforating arteries that enter the distal portion of the muscle, and it is therefore reasonable to assume that the major cause of muscle damage following DCM is ischaemia of the distal LD graft [7].

There is a further reason why muscle grafts used for cardiac assistance would be particularly susceptible to ischaemia. The basis for cardiac assistance from skeletal muscle is the induction of fatigue-resistant characteristics by chronic electrical stimulation, referred to as ‘conditioning’, a procedure that adapts the muscle to the performance of cardiac levels of work [8, 9]. Although such stimulation does not cause significant damage when applied to an undisturbed muscle, it represents a serious, and potentially damaging, metabolic challenge to a muscle whose blood supply is in any way impaired [6]. Thus, even if ischaemia were not a direct cause of muscle damage, it would be expected to increase the vulnerability of the distal LD graft to stimulation-induced damage.

Loss of the perforating arteries cannot be avoided, but the configuration of the vascular supply to the LD muscle appears to offer a potential solution to the problem. Radiographic and resin injection studies have pointed to the existence of arterial anastomoses connecting intramuscular branches of the thoracodorsal artery and perforating arteries in the LD muscle [10–14]. In principle, such anastomotic channels should enable blood delivered by the thoracodorsal artery to perfuse the distal region of the mobilized muscle via an existing vascular network.

Chronic stimulation is associated with a sustained increase in blood flow that may be responsible for the marked changes produced in the vascular component of the muscle [15]. On this basis, we reasoned that anastomotic connections between the two vascular territories of the LD muscle might well be enhanced if the muscle were stimulated before raising it as a graft. This should achieve more effective perfusion of the distal part of the LD graft from the thoracodorsal artery after interruption of the perforating collateral blood supply. In the present study, we set out to investigate the effects of surgical mobilization on the regional blood flow in the LD muscle and the added influence of prior stimulation of the muscle.


   2 Methods
Top
 Abstract
 1 Introduction
 2 Methods
3 Results
 4 Discussion
 References
 
Adult Suffolk sheep (60–90 kg) were operated on and cared for in accordance with the Animals [Scientific Procedures] Act, 1986, which regulates animal experimentation in the United Kingdom. Animals were randomly assigned to two groups: the left LD muscle of animals in Group 2 (n=5) were stimulated continuously in situ for two weeks prior to the measurement of blood flow; those in Group 1 (n=5) did not receive electrical stimulation.

2.1 Blood flow measurements
Blood flow was measured by a fluorescent dye-extraction microsphere technique, using polystyrene microspheres with a diameter of 15.0±0.5 µm (mean±SD; FluoSpheresTM, Triton Technology, San Diego, CA, USA). Flow was determined by the reference blood sampling method [16]. The principles are well established [16–19]and the technique that we validated and optimized in our laboratory has yielded reliable measurements of skeletal muscle blood flow in both rabbits [20]and sheep [21].

2.2 Anaesthetic techniques
Animals were given intramuscular xylazine (0.5 mg/kg) as premedication 1 h prior to induction of general anaesthesia with intravenous thiopentone (4 mg/kg). Following endotracheal intubation, anaesthesia was maintained with an equal mixture of nitrous oxide and oxygen supplemented with halothane (1 to 2%). Analgesia was provided by intramuscular buprenorphine (4µg/kg), which was administered at induction of anaesthesia and followed by further 12-hourly doses, as required. Respiratory assistance was provided by a volume-controlled ventilator (OAV 7710, Ohmeda, Essex, UK) which was adjusted to maintain oxygen saturation above 90%, as measured at the tongue by continuous pulse oximetry (Minimon 7137B, Kontron, Watford, UK). A rumen tube was inserted for continuous gastric drainage. Fluid maintenance was provided by warmed crystalloid (Ringer's lactate solution) at a rate of 10 ml/kg/h, and blood loss was made good with a mixture of crystalloid (0.9% saline) and colloid (Gelofusine; Braun Medical, Aylesbury, UK). The electrocardiogram and left ventricular pressure were monitored continuously during the blood flow experiments. In recovery operations, a single, 1 g dose of cefotaxime (Roussel, Uxbridge, UK) was given intravenously at induction of anaesthesia for antimicrobial prophylaxis.

2.3 Operative procedures
In a preliminary procedure conducted under aseptic conditions, the anterior border of the left LD was approached via a limited flank incision. The thoracodorsal nerve was identified within the neurovascular hilum and, with minimal trauma, an open bipolar electrode cuff (SP5528; Medtronic, Minneapolis, USA) was secured across the main trunk of the nerve. This technique was used in preference to the intramuscular electrode placement of clinical cardiomyoplasty because it was essential to avoid any possibility of damage to intramuscular branches of the thoracodorsal artery. Physiologically, there is no distinction between the two techniques, although the voltage required for supramaximal activation is lower and more consistent when the electrodes are adjacent to the nerve trunk. The cuff was connected to a bipolar stimulator (Itrel SP4721, Medtronic), which was implanted separately in a subcutaneous pocket over the upper abdomen. The assembly was tested for satisfactory and uniform activation of the LD muscle. Following haemostasis, the wounds were closed in layers and the animal was allowed to recover for one week. At this stage, the stimulators in Group 2 were activated to deliver to the thoracodorsal nerve supplying the left LD muscle a continuous train of pulses with a supramaximal intensity of 5 V and a duration of 210 µs, at a frequency of 2 Hz; the stimulators in Group 1 remained switched off.

Three weeks after the initial procedure, blood flow measurements were performed in an acute experiment, for which the animals were anaesthetized as described previously. The left carotid artery was exposed and cannulated (Desivalve 6F, Vygon, Cirencester, UK) to facilitate the passage of a cardiac catheter (SupertorqueTM Castillo II 5.2F, Cordis, Miami, FL, USA) into the left ventricle. The catheter was connected to a pressure transducer (Gaeltec, Dunvegan, UK), which was coupled via a digital-to-analogue converter to a 486 IBM-compatible PC running real-time data acquisition software (CODAS, Dataq Instruments, OH, USA). The tip of the catheter was manoeuvred into the left ventricle just below the aortic valve, the position being established by reference to the recorded pressure waveform. A cannula (LeaderCath 18G, Vygon) was inserted into the right femoral artery and connected to a syringe pump (55-2226 Harvard Apparatus, Kent, UK). This provided access for the withdrawal of reference blood samples at a rate of 12 ml/min during the subsequent blood flow measurements. The left LD muscle was exposed through an incision extending from the posterior axilla to the mid-point of the eleventh rib. The Itrel stimulator was reprogrammed (30 Hz, on for 0.19 s and off for 1.5 s; pulse duration, 210 µs, at a supramaximal amplitude of 5 V) to produce intermittent tetanic contractions of the LD muscle for 2 min. This induced a functional hyperaemia in the muscle and was repeated for each of the blood flow measurements, which therefore measured the maximum capacity for blood flow under each condition. Microspheres were injected via the left ventricular catheter immediately after cessation of tetanic stimulation, with simultaneous withdrawal of blood from the right femoral artery. The first injection of 20x106 blue FluoSpheresTM was given to measure baseline blood flow prior to any disturbance of the blood supply of the LD muscle. The thoracodorsal artery was then cross-clamped and the second injection of 20x106 blue–green FluoSpheresTM was given, to measure hyperaemic blood flow via the perforating collateral vessels. The clamp was then released to restore thoracodorsal blood flow. Next, the perforating arteries were divided and the LD muscle was mobilized from the truncal attachments; it was then restored to the in-situ position in order to preserve its resting length. The third injection of 20x106 yellow–green FluoSpheresTM was given at this stage, to measure hyperaemic blood flow via the thoracodorsal artery. In three animals in each group, the thoracodorsal artery was again cross-clamped and an injection of 20x106 orange FluoSpheresTM was given, to measure residual blood flow from any other source, again under hyperaemic conditions. The animal was killed with an overdose of anaesthetic and the entire LD muscle was excised.

2.4 Recovery of microspheres and dye extraction
The LD muscle was divided into proximal, middle and distal thirds (Fig. 1). To facilitate subsequent digestion, these regions were further subdivided into segments, each of at least 6 g wet weight. The muscle segments and blood samples were digested in a mixture of 4 M potassium hydroxide and 2% Tween-80 (BDH, Poole, UK) at 60°C. Microspheres were recovered by vacuum-filtration of the digested samples through a 10-µm pore filter. A fixed volume of diethylene glycol monoether ethyl acetate (Fluka, Dorset, UK) was then added to each filtrate, to dissolve the polystyrene, releasing the fluorescent dye contained in the microspheres. The samples were vortex-mixed briefly and centrifuged, to minimize scatter during fluorescence measurement. The absorbances of the supernatants were read in a spectrofluorophotometer (Shimadzu RF-540, Kyoto, Japan) that was set at the optimal excitation–emission wavelengths. If the emission of a sample exceeded the linear range of measurement, it was diluted by adding more dissolution agent and the reading was repeated. Samples with an emission corresponding to less than 400 microspheres were excluded [22]. To minimize any loss of fluorescent dye intensity, the samples were shielded from direct light and analyzed as a single batch without delay.


Figure 1
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  		Fig. 1 Division of latissimus dorsi muscle into three regions at right angles to the long axis of the muscle.

 
2.5 Calculation of blood flow
After adjusting for background fluorescence of the dissolution agent, and applying dilution factors where appropriate, the actual blood flow (ml/min) of each muscle sample was calculated from:


Formula

The specific flow (ml/min/g) for the whole region was calculated as the sum of the blood flows in the constituent segments divided by their combined mass. Both thoracodorsal and perforating arterial blood flows were subsequently expressed as percentages of the baseline values obtained before disturbing the blood supply.

2.6 Statistical analysis
All values have been expressed as mean±standard error of the mean. One-way analysis of variance was employed to detect differences in baseline blood flow between the three LD regions in each group and also between the corresponding LD regions in the two groups. A two-tailed paired t-test, applied to the proximal and distal regions, was used to assess differences in the regional blood flow derived from the thoracodorsal and perforating arteries within each group. Differences were considered to be significant if p<0.05. Computations were performed with statistical software (InstatTM, Graphpad Software V2.00, San Diego, CA, USA).


   3 Results
Top
 Abstract
 1 Introduction
 2 Methods
 3 Results
4 Discussion
 References
 
The animals remained haemodynamically stable during the successive blood flow measurements, with no significant changes in left ventricular pressure, heart rate or electrocardiogram.

3.1 Group 1 animals — unstimulated LD muscle
Under baseline conditions, before the blood supply was disturbed, no significant differences in hyperaemic blood flow were measured between the three regions of the LD muscle (Fig. 2). Cross-clamping the thoracodorsal artery resulted in a characteristic pattern of changes in the regional blood flow: the collateral arteries alone were able to maintain most of the baseline blood flow in the distal region, but flow was reduced in the middle region, and was least in the proximal region (Fig. 3). The difference in blood flow between the distal region and the proximal region was significant (p=0.01). Interruption of the collateral blood supply and surgical mobilization revealed the reverse of this pattern of changes: there was a reduction in blood flow in each region relative to the baseline measurement, with the middle region being more, and the distal region being most, affected (Fig. 3). There was a highly significant difference between the blood flow to the proximal region and that to the distal region (p=0.002).


Figure 2
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  		Fig. 2 Regional blood flow in the unstimulated latissimus dorsi muscle under baseline conditions. No significant difference in blood flow was found between the regions.

 

Figure 3
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  		Fig. 3 Regional blood flow in the unstimulated latissimus dorsi muscle after cross-clamping the thoracodorsal artery (dark columns), representing flow derived from the collateral arteries and that after interruption of the collateral arteries and surgical mobilisation (light columns), representing flow derived from the thoracodorsal artery. *There was a significant difference in blood flow between the proximal region and the distal region (p=0.01). **There was a highly significant difference in blood flow between the proximal region and the distal region (p=0.002).

 
Orange microspheres were injected into three animals to measure residual flow after both thoracodorsal and collateral routes had been interrupted. In most of the samples, the corresponding fluorescent signals were below the threshold required for reliable measurement. In the few samples that registered above this level, residual flow accounted for no more than 1–2% of the baseline value.

3.2 Group 2 animals — stimulated LD muscle
Two weeks of electrical stimulation in situ did not alter the uniform distribution of hyperaemic blood flow across the regions of the LD muscle at baseline (Fig. 4). Blood flows were not significantly different in corresponding regions of the stimulated (Group 2) muscles and unstimulated (Group 1) muscles (p~1). Cross-clamping the thoracodorsal artery resulted in a pattern of change in regional blood flow that was distinct from that seen in Group 1 (Fig. 5): reduction in blood flow was similar across the three regions relative to baseline measurement, so that blood flow was not significantly different in the proximal and the distal regions (p>0.4). In the same way, surgical mobilization of the LD muscle, with interruption of the collateral arteries, produced similar reductions in blood flow across the three regions of the LD muscle (Fig. 5) (p>0.5).


Figure 4
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  		Fig. 4 Regional blood flow in the prestimulated latissimus dorsi muscle under baseline conditions. No significant difference in blood flow was found between the regions.

 

Figure 5
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  		Fig. 5 Regional blood flow in the prestimulated latissimus dorsi muscle after cross-clamping the thoracodorsal artery (dark columns), representing flow derived from the collateral arteries and that after interruption of the collateral arteries and surgical mobilisation (light columns), representing flow derived from the thoracodorsal artery. There was no significant difference in blood flow between the proximal region and the distal region (p>0.4 and p>0.5, respectively).

 
As in the corresponding Group 1 animals, residual flow was at an extremely low or undetectable level in all samples.


   4 Discussion
Top
 Abstract
 1 Introduction
 2 Methods
 3 Results
 4 Discussion
References
 
Since DCM was introduced in 1985, about 700 procedures have been performed world-wide. In a recent review of 127 patients who underwent DCM over a ten-year period, the two-year survival rate was found to be less than 60%; heart failure accounted for a significant proportion of both early and late postoperative mortality [23]. Other surveys showed that approximately 20% of survivors report no functional benefit from the procedure [24]. Such a poor outcome has been attributed to LD graft dysfunction associated with muscle damage detected in the early postoperative period [25]. Damage is also seen when such grafted muscles are examined after longer periods in both man [25, 26]and animals [2–6]. Typically, this manifests as degeneration of muscle fibres and their replacement by fat and fibrous tissue, particularly in the distal region of the LD graft. A combination of factors may be responsible for this damage, including changes in vascular conformation, loss of resting tension and chronic electrical stimulation [6], but ischaemia of the muscle graft is increasingly suspected to be the most important element [27]. Interruption of the perforating collateral blood supply, even in the absence of other factors, has been shown to produce damage, primarily in the distal region of the LD muscle, in pigs [28], sheep [6], dogs [29]and goats [30]. It seems likely that this damage is exacerbated by the increased metabolic demand associated with stimulation for continuous cardiac assist [31]. The use of a modified orthotopic pedicled graft in our experimental model isolated this influence from other factors and reaffirmed the key role of surgical mobilisation in mediating muscle ischaemia.

We chose the ovine model for this study because significant damage to the sheep LD muscle following surgical mobilization has been demonstrated previously in this laboratory [6]. On the assumption that much of this damage was ischaemic in origin, any effects on blood flow in the LD muscle resulting from surgical mobilization should be readily demonstrable in the same model. The sheep LD muscle is also regarded as a clinically relevant model for studying cardiomyoplasty, based on a comparison of the biochemical parameters (aerobic capacity, glycolytic capacity and contractile potential) with those of the human muscle [32]. Furthermore, there was no evidence of haemodynamic disturbance resulting from the administration of microspheres: left ventricular pressure, heart rate and electrocardiogram remained stable throughout the experiment. In this respect the sheep provides a more suitable experimental model than smaller laboratory animals, such as the rabbit [20].

Our findings confirmed the deleterious effects of surgical mobilization and interruption of the collateral arterial supply of the LD muscle. Although the thoracodorsal artery alone was able to maintain most of the blood flow to the proximal LD muscle that had been observed under baseline conditions, it was unable to maintain much more than half of the baseline level in the distal region. This finding is consistent with the results of previous studies in dogs [33–36]and goats [27]. Furthermore, the characteristic distribution of thoracodorsal blood flow observed in the unstimulated sheep muscle in this study agrees with earlier observations in both canine [36]and goat LD grafts [27]. Our results show that the territory supplied by the thoracodorsal artery extends over the whole LD muscle, but diminishes from proximal to distal, whereas the territory supplied by the perforating arteries also extends over the whole muscle, but diminishes from distal to proximal. The contribution of the perforating arteries to the blood supply of the LD muscle, shown here quantitatively for the first time, is substantial and perhaps greater than has been customarily supposed [12].

The actual weight-adjusted blood flow values measured during hyperaemia in our study differed somewhat from those obtained in other animal models. In addition, the size of the reduction in blood flow following surgical mobilization varied in these studies, from 70 [34]to 40% [36]in the distal LD muscle. The disparity in these values has been ascribed to variations in muscle fibre composition in different species, the effect of different electrical stimulation regimes, limitation of blood flow through the thoracodorsal artery, the effects of anaesthesia, incomplete loading during muscle exercise, and differences in methodology [35].

Stimulating the muscle electrically in situ for two weeks with a continuous low-level pattern significantly improved the ability of the thoracodorsal artery to perfuse the distal part of the LD muscle following surgical mobilization. Chronic electrical stimulation is known to improve vascularity in skeletal muscle, as evidenced by increased capillary density [37], increased capillary-to-fibre ratio [27]and increased latissimus-derived collateral blood flow to ischaemic myocardium [38]. These changes occur early in the course of stimulation [39]. However, stimulation-induced angiogenesis alone would not be expected to abolish the proximal-to-distal gradients in blood flow. Moreover, we did not observe any significant increases in baseline flow following stimulation. The results therefore point not so much to elaboration of arterial territories as to a reduction in vascular resistance in the central part of the muscle.

Radiographic and resin injection studies have provided evidence for anastomotic channels or ‘choke arteries’ linking the two vascular territories in the LD muscle [10–14]. We demonstrated cross-filling of the proximal and distal arterial trees in the rat and the rabbit when resin was injected via either the thoracodorsal or the collateral arterial route [40], and we have recently confirmed that this is due to anastomotic connections, and not merely to an overlap in arterial territories [41]. The fact that the gradients in blood flow observed in the control muscle were abolished in the electrically stimulated muscle is consistent with enlargement of anastomotic connections between the two vascular territories and, consequently, to a reduced resistance to blood flow.

There are some conflicts in the literature regarding the effects of chronic electrical stimulation on hyperaemic blood flow in skeletal muscle: Hudlicka et al. [42]observed a marked increase in hyperaemic flow in rabbit fast muscles after four weeks of chronic stimulation at 10 Hz for 8 h per day; Acker et al. [43], working with canine LD muscles that had been stimulated continuously with a burst pattern for eight weeks, found maximum hyperaemic flows that were similar to those of control muscles. Considerably lower blood flows were detected in other studies that employed similar stimulation regimes in dogs [33]and goats [27]. We have not observed any significant changes in baseline hyperaemic blood flow following two weeks of continuous electrical prestimulation at 2 Hz. Such inconsistencies may be a consequence of the factors already mentioned. In any case, it should not be assumed that an increased blood flow is a prerequisite of adequate function in chronically stimulated muscles, in which adaptation may be accompanied by an increased efficiency of oxygen extraction [43]and a decreased energy cost of contraction [44].

A skeletal muscle that is used to provide continuous circulatory assistance is entirely dependent on aerobic metabolism for its energy supply. Although the necessary metabolic adaptations are produced by chronic stimulation of a muscle in situ [45, 46], compromise of the blood flow to a muscle that has been mobilized as a graft could be a limiting factor. The clinical practice that is currently recommended in DCM is to include a stimulation-free period, or vascular delay [36], envisaged as an opportunity for the thoracodorsal artery to extend its territory through a process of neovascularization. The disadvantage of this approach is that it contributes to an extended postoperative period, during which the patients are recovering from a highly invasive procedure without the benefit of cardiac assistance. The present study provides the basis for an alternative approach. It shows that a moderate regime of electrical stimulation delivered prior to surgical mobilization can significantly enhance blood flow to the distal part of the LD graft from the thoracodorsal artery via an existing arterial network. Since the stimulation would also accomplish at least part of the conditioning required for the muscle to perform cardiac levels of work, it would allow for the earlier introduction of postoperative circulatory support, to the evident advantage of patients who have a limited cardiac reserve.

Time for primary review 28 days.


   Acknowledgements
 
We are grateful to the British Heart Foundation for their financial support. We would like to thank Dr. J Yates and Mr. R Galvin for their technical assistance during this project.


   References
Top
 Abstract
 1 Introduction
 2 Methods
 3 Results
 4 Discussion
 References
 

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