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Ann Thorac Surg 1997;63:1034-1040
© 1997 The Society of Thoracic Surgeons
Division of Plastic and Reconstructive Surgery, Department of Surgery, and Department of Physiology and Biophysics, School of Medicine, University of Louisville, Louisville, Kentucky
Accepted for publication October 26, 1996.
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Methods. Canine (n = 9) LDMs were subjected to a 10-day period of vascular delay followed by a simulated CMP. Two weeks after simulated CMP (corresponding to the healing delay between CMP and the onset of LDM stimulation used in the clinical setting), LDM perfusion was measured in the distal, middle, and proximal segments of the muscle, and circumferential (distal and middle squeezing muscle function) and longitudinal (proximal pulling muscle function) force generation and fatigue rates were measured. The results were compared with the contralateral nondelayed simulated CMP.
Results. Muscle perfusion was significantly (p < 0.05) greater in the distal and middle segments of vascular-delayed LDMs. Circumferential muscle force generation and fatigue rates were significantly (p < 0.05) improved in the vascular-delayed LDMs.
Conclusions. Vascular delay can significantly improve LDM perfusion and function in a model that closely reflects clinical CMP, and the use of vascular delay may improve clinical outcomes in CMP.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Our group has demonstrated that canine LDMs first subjected to a 10-day period of vascular delay showed no evidence of ischemia when subsequently elevated in total [6]. Isoda and colleagues [5] also demonstrated that a 1-month vascular delay period significantly enhanced muscle flap perfusion at rest and during exercise. We have previously reported that a 10-day delay improves both muscle perfusion and function in the distal and middle segments of the canine LDM [11]. In the present study, we investigated the effects of a 10-day delay period on muscle perfusion and function 2 weeks after simulated CMP. This study differs from our previous work in that it closely approximates the clinical protocol of waiting 2 weeks from the time the heart is wrapped to the onset of stimulation. Because the beneficial effects of vascular delay occur primarily in the distal and middle segments [5, 11], we designed an experiment in which we could measure distal and middle muscle function independent of proximal muscle function. We believe that the present study provides valuable information with regard to the perfusion and function of the muscle at this critical time of onset of LDM training and that this strongly supports incorporating vascular delay into the clinical CMP procedure.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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SURGICAL PREPARATION.
Dogs were fasted on the night before the operation and were anesthetized in a similar fashion for all procedures. Preoperatively, all animals were given atropine subcutaneously (1 mL/9 kg). Anesthesia was induced by intravenous administration of pentothal (6 to 12 mg/kg). The animals were then intubated with an endotracheal tube and mechanically ventilated with a 2% isoflurane/94% oxygen/4% nitrous oxide gas mixture (1 L/min per 4.5 kg). The operating room temperature was regulated at 23°C, and each dog was kept normothermic with a heating blanket (Aquamatic K 20 Heating Blanket; American Hamilton, Cincinnati, OH). An intravenous infusion of lactated Ringer's solution (5 mL•h-1•kg-1) was maintained for the duration of all procedures. Each dog received a twice-daily intravenous injection of antibiotic (cefazolin sodium, 600 mg) for 3 days beginning at the induction of anesthesia. Antibiotics were given only for survival operations. Intravenous analgesia (buprenorphine hydrochloride, 0.3 mg every 4 to 6 hours) was given as needed for 24 hours postoperatively.
Operative Procedures
VASCULAR DELAY.
The experimental and control muscles were randomized for each experiment. The operative field on each side was prepared with iodine scrub (Operand, Prichard, WV). An 8-cm longitudinal incision was made over the anterior border of the LDM. The anterior muscle border was identified and the dissection was extended into the submuscular plane. Vascular delay was accomplished by dividing all the perforating branches entering the costal surface of the muscle from the underlying intercostal vessels. The thoracodorsal neurovascular pedicle was left intact. The LDM normally receives its blood supply from numerous vessels entering the muscle from both superficial and deep surfaces, ie, multipedicled. This procedure converted the LDM into a predominantly bipedicled muscle flap, with the primary pedicle being the thoracodorsal vessels and the secondary pedicle being those vessels running in the muscular connections to the lower two ribs and the small vessels in the areolar tissue on the surface of the broad tendon of origin. All myocutaneous vessels were left intact, thus contributing to the secondary pedicle. Sham delay procedures were performed on the contralateral control side by lifting the muscles off the costal surface without dividing the intercostal perforators. The incisions were then closed in layers and the animals were allowed to recover. Upon recovery, the animals were placed in a postoperative recovery room for observation overnight. The following morning, all animals were examined by the surgical team and were returned to the animal holding rooms. All dogs were examined by the surgical team on a daily basis for the duration of the delay period (10 days).
SIMULATED CARDIOMYOPLASTY.
After a 10-day delay period, each animal was returned to the operating room and reanesthetized using the same anesthetic protocol as described previously. The cutaneous surfaces of the muscles were then exposed through the previous incisions and meticulously cleared of the overlying fatty layer. Perfusion measurements were done with a laser Doppler perfusion imager (Lisca Development AB, Sweden). Each muscle was then raised in its entirety as a thoracodorsally based unipedicled flap. A 2-cm cuff of lumbosacral fascia was taken with the muscle and used later to stitch the distal end of the flap. The muscle's tendon of insertion into the humerus was left intact. The distal and middle portions of the muscles were then wrapped around flexible silicone polyurethane foam-filled stents (model 430-3016; Mentor Corp, Santa Barbara, CA) in much the same way as these regions of the LDM are wrapped around the heart in a clinical CMP procedure (Fig 1
). The muscle was held in this position by 3.0 interrupted silk sutures passed through the fascial cuff and the superficial portion of the middle muscle segment. This method ensured minimal interruption in blood supply to the muscle wrap. A stainless-steel pin, inserted through the center of each stent and attached to the sixth rib by surgical steel sutures (Ethicon, Somerville, NJ), held the muscle wrap and stent in place. Silicone sheeting (Applied Silicone Corp, Ventura, CA) was used to isolate the muscle from the costal surface below and the cutaneous surface above and thus prevent any potential vascular ingrowth from adjacent tissues. The incisions were then closed in layers and the animals were allowed to recover. Animals were treated postoperatively in the same manner as described previously. All dogs were examined by the surgical team on a daily basis over the next 2 weeks.
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Animals were then placed in the prone position, and a custom-made metal frame was placed around them. The frame was fixed to the operating table using C clamps. The stents and surrounding muscle wrap were attached to a sliding coupling device incorporated into the frame. This allowed the stent and muscle wrap to slide backward and forward on the frame. Longitudinal isometric force was measured by a force transducer (model FT 10 C; Grass Medical Instruments, Quincy, MA) connected to the sliding aluminum bar with Kevlar wire. Circumferential isotonic force was measured by a pressure transducer (model P23 ID; Gould, Cleveland, OH) attached directly to the silicone stent. This arrangement (see Fig 1
) permitted independent measurements of longitudinal contraction from the proximal muscle and circumferential contraction from the distal and middle muscle. The resulting transducer signals were recorded on a multiple-channel line recorder (model WR 3310 Graphtek Linerecorder; Western Graphtec, Irvine, CA). The animal's forelimbs and shoulders were then fastened securely with straps to the operating table to prevent any extraneous skeletal movement during muscle function measurement.
MUSCLE PERFUSION MEASUREMENTS.
Perfusion of the LDM was measured at the time of stent implantation, immediately before flap elevation, and 15 minutes after flap elevation. Perfusion was recorded again 2 weeks later at the time of the protocol procedure. Measurements were taken of 10-cm2 muscle segments in each of the distal, middle, and proximal portions of the muscle. The laser Doppler perfusion imager was used to monitor perfusion in delayed muscle and nondelayed muscle. This device uses conventional laser Doppler principles but, unlike conventional laser Doppler perfusion monitors, which measure temporal variations in perfusion at a single point on the surface of a given tissue, the Doppler perfusion imager can measure perfusion over a large area [12–14]. The ability to measure and analyze surface perfusion in large areas of muscle makes the Doppler perfusion imager an ideal instrument with which to measure alterations in LDM perfusion induced by vascular delay.
STIMULATION PROTOCOLS.
Motor threshold (MT) of each LDM (ie, the stimulus intensity that elicited minimal visible contraction) was determined with a constant-current stimulator (Grass S88 with PSIU6; Quincy, MA). The stimulator was then set at eight times MT (8 x MT), and all further muscle stimulations were performed at this level. Optimal length was defined as that length that elicited the greatest longitudinal force generation when the muscle was stimulated by a single pulse at 8 x MT. Optimal length was determined for each muscle, and all further measurements in the loaded position (ie, with passive resting tension at this muscle length) were performed at this muscle length.
Muscles were stimulated in both rhythmic and tetanic fashions. When stimulated, the muscles produced two different forces of contraction. The proximal segment of the muscle produced longitudinal contractions, which were recorded by a force transducer and expressed in kiloponds (kp, the force acting on a 1-kg mass at normal acceleration of gravity). The distal and middle segments produced circumferential contractions (ie, "squeezing" of the silicone stent), which were recorded by a pressure transducer and expressed in mm Hg. Longitudinal force generations were measured isometrically in the loaded position only (ie, optimal muscle length for the proximal LDM). Circumferential force generations were measured in both the loaded and unloaded (ie, suboptimal muscle length for the proximal muscle) positions. Therefore, longitudinal contractions contributed to circumferential contractions in the loaded position but not in the unloaded position, thus allowing (by subtraction) independent measurement of circumferential iostonic and longitudinal isometric contractions.
CONTRACTILE RESPONSES.
The muscles were intermittently stimulated at 8 x MT with a duty cycle of 500 milliseconds on, 750 milliseconds off, a frequency of 25 Hz, and a 320-microsecond duration. The stimulus was maintained until the muscle had fatigued (one half maximal force generation) or for 30 minutes if the muscle had not yet fatigued. Recordings of maximal force generation and fatigue rates were taken with the muscle in both the loaded and unloaded positions.
The muscles were also tetanically stimulated at 8 x MT at a frequency of 50 Hz and a 320-microsecond duration. The stimulus was maintained until the muscle had fatigued (one half maximal force generation). Recordings of maximal force generation and fatigue rates were taken with the muscle in both the loaded (ie, with resting passive tension at optimal length) and unloaded positions.
STATISTICAL METHODS.
All data from the delayed muscles were compared with data from the paired contralateral control muscles. Paired Student's t tests were used for all statistical evaluations. All data are presented as mean ± standard error of the mean; p values less than 0.05 were considered significant.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Muscle Perfusion
When comparing vascular delay versus control, muscle perfusion is expressed as a percentage of pre-elevation perfusion (as in Figs 2 and 3). When observing trends in perfusion over time, perfusion is expressed in arbitrary units (as in Fig 4). Total muscle perfusion was significantly (p < 0.05) greater in delayed muscle both 15 minutes (see Fig 2) and 2 weeks (see Fig 3) after flap elevation as compared with nondelayed muscle flaps. This improved perfusion was most marked in the distal segments of delayed muscle flaps (see Fig 4). There was no statistical difference in proximal muscle flap perfusion between the groups. There was no difference in overall muscle perfusion between the delayed and nondelayed muscles before flap elevation.
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). Longitudinal maximal force generation was greater in the delayed muscle for both rhythmic and tetanic contractions, although only the latter reached significance (Fig 6).
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). Tetanic fatigue rates were significantly (p < 0.05) greater in delayed muscle for unloaded circumferential tetanic contractions, but not for loaded circumferential or longitudinal contractions.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Although the efficiency of vascular delay in improving muscle flap survival is not in doubt, the exact mechanism is still not fully understood. It is thought to be due to the development of improved perfusion [16, 17] combined with greater tissue resistance to ischemia [18]. There are many ways of performing a vascular delay procedure. In his experiments in skin flaps, Milton [19] determined that the bipedicled technique (as used in this experiment) resulted in the greatest flap survival.
Distal muscle ischemia occurs when the entire LDM is acutely elevated on a single neurovascular pedicle (ie, thoracodorsal artery, vein, and nerve) in the experimental setting [3, 5, 6, 7, 8, 11]. In CMP, this distal muscle ischemia is further exacerbated by the work the LDM is compelled to perform during the electrical preconditioning protocol after muscle wrapping around the myocardium. An essential part of this work is done by the distal and middle regions of the LDM, which provide circumferential "squeezing" contractions to assist systolic ventricular emptying and thus cardiac function. In the clinical setting, distal LDM flap ischemia probably decreases the circumferential contractile force and thus minimizes the full assist potential of the muscle wrap [4]. In fact, in the experimental setting, minimal or no circumferential contractions have been recorded [10]. It is the proximal portion of the muscle, by lateral displacement, that provides any cardiac compression [9].
We have demonstrated previously that a 10-day vascular delay period significantly improved distal LDM flap perfusion and survival [6, 11] as well as force of contraction and fatigue resistance [11]. Others have also reported positive results for the role of vascular delay in LDM fatigue rates [3] and perfusion [5, 20]. It is of note therefore that in this model, 2 weeks after simulated CMP, almost half (4 of 9) of all nondelayed muscle wraps developed muscle ischemia and necrosis sufficient to result in muscle wrap disruption. On the other hand, in vascular-delayed muscle wraps, there was no evidence of ischemia, necrosis, or disruption. Other investigators [5, 20] have also questioned to what extent the LDM survives in CMP and to what extent it depends on its surroundings (eg, the heart) to maintain perfusion. It has been shown that ischemic skin flaps can survive when they are transferred into a well-vascularized bed [21, 22], probably because they quickly revascularize by receiving blood from the healthy bed. In the present study, to exclude the possibility of collateral vascular ingrowth into the LDM, we wrapped the muscle in an isolating silicone sheet during the simulated CMP period.
We have demonstrated that a 10-day period of vascular delay significantly improves the muscle's overall perfusion at the time that electrical preconditioning of the LDM would begin clinically (ie, 2 weeks from the wrapping operation). This was significant in the distal and middle regions of the muscle, whereas perfusion was not improved in the proximal muscle (see Fig 2). This improvement in perfusion was maintained at 2 weeks (see Fig 3) and was amplified in the distal segment (see Fig 4). We believe that the beneficial effects of vascular delay on LDM survival, perfusion, and thus function are regional rather than global.
We showed that circumferential muscle function and fatigue rates-indices of distal and middle muscle flap function-benefited from vascular delay (see Figs 5, 7). The proximal LDM region, well perfused by the thoracodorsal vessels, is relatively unaffected by both acute elevation and the intercostal perforator ligation during vascular delay. This is demonstrated by our findings in vascular-delayed LDMs of only moderate increases in proximal muscle perfusion (see Figs 2, 3) and in function (see Fig 6) compared with nondelayed LDMs.
The importance of converting the LDM into a more fatigue-resistant muscle through chronic electrical stimulation has been demonstrated experimentally and clinically as fundamental to the success of CMP [9, 23]. The results of the present work indicate that before initiating chronic electrical stimulation, the LDM should have its vascular supply delayed. By significantly enhancing blood perfusion to the distal regions of the LDM, vascular delay provides a better-perfused, more contractile muscle for the subsequent electrical stimulation protocol. A noted complication of CMP is the variability of clinical outcome. Because an inherent variability in flap survival patterns is known to exist, this variability among individuals could be due to differences in the vasculature nourishing the LDM. Vascular delay can minimize this cause of variability by optimizing LDM perfusion and thus survival and function.
It has been suggested that like vascular delay, chronic electrical stimulation can be used to accelerate revascularization of the distal LDM [23]. Mannion and co-workers [20] investigated the interrelation between electrical training and vascular delay and recognized the beneficial effect of a combined approach. Mannion and associates [24, 25] and Bailey and colleagues [26] suggested that CMP may be used to revascularize an ischemic myocardium and demonstrated that acute and chronic stimulation increased latissimus-derived collateral blood flow to the myocardium. If CMP is to be used in this manner, a vascular delay period would provide a better-perfused LDM and conditions more favorable for the development of extramyocardial collaterals. Further work is required to determine the temporal relation between vascular delay and initiation of the electrical preconditioning regimen. It is perhaps possible that combining vascular delay with in situ preconditioning could yield a well-perfused and partially or completely trained LDM. In this case, the LDM could be used almost immediately after wrapping to augment cardiac function and thus accelerate a patient's postoperative recovery.
From this and previous studies [6, 11], we conclude that vascular delay improves distal LDM perfusion and function. These improvements persist for at least 2 weeks when, in the currently used clinical stimulation protocol, electrical stimulation training of the muscle begins. Combining vascular delay with stimulation preconditioning may perhaps provide optimal function of the LDM for CMP.
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Acknowledgments |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Footnotes |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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