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Endoscopic ligation of intercostal arterial perforators to the latissimus dorsi muscle with a time delay improves collateral blood supply
Endoscopic Ligation Of Intercostal Arterial Perforators To The Latissimus Dorsi Muscle With A Time Delay Improves Collateral Blood Supply John M. Alvarez,
FRACS,
Megan Carter,
RVN,
Gregory McKie,
BSC(HONS),
MBA
Department of Cardiothoracic Surgery, Sir Charles Gairdner Hospital, Nedlands, Perth, Western Australia Background: The latissimus dorsi muscle (LDM) derives its blood supply from the thoracodorsal (TDR) pedicle and from perforating branches (ICP) arising from the intercostal arteries. Current methods of surgical harvesting can cause significant ischaemic damage to this muscle. Objective: To show that by endoscopically dividing the perforating vessels of the in situ muscle and by allowing a delay of 2 weeks, angiographically detectable new collateral vascular channels develop between the terminal branches of the TDR pedicle and the vascular territories of the ICP. Methods: Six sheep underwent endoscopic ligation of the ICP of the LDM on one side. After 2 weeks, both LDMs were surgically dissected. By injecting dye into the thoracodorsal artery, angiograms were obtained. The opposite LDM served as the control. Histological sections were taken at 6 transverse levels along the length of these LDMs. Creatine kinase (CK) assays were taken before surgery and at days 1 and 2 after surgery. In 4 separate sheep which solely underwent formal surgical dissection, CK assays were also taken before surgery and days 1 and 2 after surgery. Results: In the endoscopically prepared LDMs, new vascular collaterals were convincingly demonstrated to have developed between the vascular networks of the TDR pedicle and the ICP vascular networks. Histological examination revealed minimal or no evidence of myocyte necrosis in the distal half of the LDMs of the endoscopically prepared group compared to extensive myocyte necrosis in the control LDMs of the same animal. The mean peak CK elevation of the endoscopically dissected LDM was 307&22 U/L versus a mean peak CK elevation of 910&l U/L in the 4 sheep having surgical dissection only. In this surgically dissected group, gross muscle necrosis occurred in all animals. Conclusions: Endoscopic ligation of the ICP vessels followed by a 2-week delay allows the development of collateral channels such that the TDR can solely and adequately supply the entire LDM. Subsequent surgical dissection is then tolerated with minimal or no ischaemic myocyte necrosis. (Asia Pacific Heart Journal 1998;7(2):108-113) Introduction The latissimus dorsi muscle (LDM) is the muscle of choice for muscle-assist procedures.QJ Following formal surgical dissection of this muscle, its initial viability is dependent solely on the integrity of the thoracodorsal vascular pedicle (TDP). This pedicle, however, is responsible for nourishing only 30% to 40% of the in situ muscle. The perforating branches of the intercostal arteries supply the remainder of the in situ muscle.
By endoscopically ligating the intercostal perforators of the in situ muscle followed by a delay of 2 weeks, it is possible to demonstrate the growth of angiographically detectable blood vessels from the terminal branches of the TDP to the angiographically visible vascular network derived from the intercostal perforators and, amongst these, intercostal vascular networks themselves. Methods Following the approval of our research protocol from the University of Western Australia’s Animal Experimentation Ethics Committee (AEEC), 10 sheep were used in these experiments. All animals were treated in accordance with the guidelines of the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes.
Hence, following surgical dissection of this muscle, the potential exists for a large proportion of the muscle to be damaged by ischaemia. In particular, it is the crucially important distal two-thirds which are the part of the muscle which actually wrap the heart and therefore are presumably critical in generating systolic compression and or diastolic bracing of the failing heart. To those who have dissected this muscle, the frequent striking feature after dissection is the appearance of a well-perfused proximal muscle and a cyanotic distal muscle.
Six adult cross Merino sheep weighing from 22 to 28 kilograms were anaesthetised using 35 mg/kg pentabarbitone and intubated; anaesthesia was
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Fig. 1. Insufflating CO2 between the lattissimus dorsii (LD)
and the chest wall (CW) lifts the LDM above and off the CW, allowing clear visualisation and division of the ICP by the endoscopic dissectionscissors. Fig. 2. Creatine kinase levels (U/L) for the control group of
maintained using 2% Halothane with oxygen and nitrous oxide at a ratio of 1:2. The sheep’s flank from shoulder to rump was then shaved. The side to be used was determined in a prospective and randomised manner by the toss of a coin.
surgically dissected LDM vs the prepared (endoscopically ligated ICP) LDM. blood to assay creatine kinase (CK) levels were taken prior to commencement of the surgical procedure and on the morning of postoperative days 1 and 2.
Two small skin incisions (2 cm) were made a hand’s breadth from the posterior forelimb crease and a hand’s breadth proximal to the anterior hind limb crease at the level of the lower palpable border of the LDM. Using arterial forceps, dissection to the level of the chest and abdominal wall was performed. Two Endopath Tristar 512B blunt-tip 12mm surgical trocars fitted with Endopath MS 5 12 Multiseal caps (Ethicon Endo-Surgery, Johnson & Johnson) were inserted. Carbon dioxide was insufflated into the plane between the LDM and the body wall with an Olympus Surgical CO2 Insufflator. By this manoeuvre the LDM is lifted off the body wall by the accumulating C02.
Two weeks following this surgery, the sheep were anaesthetised, intubated and prepared in the same manner. A formal surgical dissection of the LDM was performed both on the previously prepared LDM in which thoracoscopic ligation of the intercostal perforators had been performed and on the unprepared contralateral LDM which served as the control. The surgical dissection was performed by means of a longitudinal incision from the shoulder to the rump at the level of the palpable lower border of the muscle. The number of intercostal perforators (ICP) encountered on both sides were noted. The TDP was then isolated and the artery, vein and nerve identified. The artery was cannulated with a 22 G Insyte cannula (Becton Dickinson Pty Ltd, Australia), and 10 rnL of sodium heparin were injected. The LDM was removed from the sheep and placed under an image intensifier; 8-10 mL of Omnipaque dye (350 mg 12/mL, Sanofi-Winthrop), diluted in a 1:l ratio with 0.9% normal saline, were injected into the thoracodorsal artery until the arterial tree within the LDM was clearly defined. The TDR vascular pedicle was then ligated and an X-ray film (small focus, 42kV and 3.2 mAs) using a retail UVG film (Kodak) was obtained.
A 30” Olympus thoracoscope was inserted into one of the trochars. This was connected to an Olympus CLV/S light source attached to an Olympus OTV/S4 camera control unit displaying the underlying anatomical dissection on a Sony Trinitron monitor. A DC512 disposable curved scissor with unipolar cautery (Endopath, Johnson & Johnson) was inserted via the remaining trocar. With both the thoracoscope and the dissecting scissors in the plane between the body wall and the LDM, careful dissection allows clear visualisation of the intercostal perforating vascular pedicles (Fig. 1) as well as the thoracodorsal vascular pedicle. The intercostal perforators were counted and divided using cautery or surgical clips.
The LDMs were weighed and stored in a 10% formalin solution. The time interval from surgical removal of the LDMs to immersion in the formalin solution was in all cases less than 20 min. The sheep were then euthanased with a dose of 10 mL of Lethabarb (pentabarbitone, 325 mg/rnL, Virbac Pty Ltd Australia) administered intravenously. The protocols granted by the AEEC did not allow these sheep to be maintained alive following the second operation.
The extent of the dissection proceeded from the point of insertion of the TDR pedicle to the point of contiguity of the LDM with anterior abdominal wall and from the level of its free margin to the vertebral spines. We called this LDM the prepared side. Haemostasis being secured, the 2 skin incisions were closed with non-absorbable sutures. Samples of venous
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Fig. 3. Angiogram of an endoscopically prepared LDM. Extensive new vascular channels (arrows) are evident throughout the LDM communicating the TDR pedicle to the ICP vascular networks. In 4 adult cross Merino sheep weighing from 20 to 29 kg, a formal surgical dissection of the muscle was performed following the same protocol for anaesthesia, intubation and preparation. The LDM was left attached along its vertebral border and where it became contiguous with the distal abdominal wall. The ICP vessels were divided. The TDR pedicle was left intact and, hence, was the sole vascular supply to the LDM. The LDM was, therefore, dissected off the body wall and from the overlying subcutaneous tissues. Its sole attachment being the fibrous continuity along its vertebral border to the distal abdominal wall aponeurosis. Venous blood samples were taken immediately prior to the commencement of surgery and on the morning of postoperative days 1 and 2. As a consequence of their clinical condition on the morning of postoperative day 2, these 4 sheep were euthanased immediately (following the collection of this last sample of blood) with 10 mL. of intravenous Lethabarb. CK levels were also assayed in these 4 sheep. The mean levels of CK, and the standard deviations, for these 2 groups of sheep from baseline to 48 hours after surgery are provided in Fig. 2.
Fig. 4. Angiograms
of the endoscopically unprepared LDM on the left versus the endoscopically prepared LDM on the right. New vascular connections are predominant throughout the LDM (arrows) from the thoracodorsal pedicle (TDR) to the intercostal perforator vascular networks (ICP)
specimens from all 6 sheep. Histological staining (haematoxylin and eosin staining) was performed on these sections. The clinical appearance of the LDM of the 4 sheep that had the formal complete surgical dissection of the LDM, which was then left in situ, were those of gross macroscopic extensive distal half necrosis. Such necrosis
Histological analysis Full thickness transverse sections at 3-cm intervals from the point of insertion of the TDR pedicle were taken of the LDM from both the prepared and control
precluded
histological
of the LDM.
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Histological staining of the prepared LDM revealed minimal to no evidence of cell necrosis in the distal half of the prepared LDMs as opposed to extensive cell necrosis and degeneration in the unprepared controls. The proximal part of the LDM revealed no differences in terms of cellular integrity between the prepared and control group of muscles.
ReSUltS In all 6 sheep with endoscopically ligated ICP, angiograms revealed striking patterns of new vessel development from the TDR pedicle to the ICP vascular networks (Figs. 3 and 4). The striking macroscopic appearance at the time of surgical dissection of these prepared LDMs after a 2-week delay was the absence of cyanosis of the distal muscle and visible and palpable pulsations of the ICP vascular networks. Clinically, there was no exudative collection nor tenderness to palpation in the prepared sides. The animals tolerated the procedure apparently with minimal discomfort.
Discussion Following the innovative work of the French surgeon Dr A. Carpentier,’ the operation of dynamic cardiomyoplasty (DC) has captured the imagination of cardiac surgeons worldwide. Despite a decade since the first human report, however, the role which this procedure may have in patients with heart failure remains imprecise.zJ There are undoubtedly many causes for the discrepancies in results reported following this operation. In the most recent series reported by Carpentier, of those patients having DC who died postoperatively and prior to hospital discharge, half died from cardiac failure; at postmortem, half of the patients were found to have extensive necrosis of the LDM.3
The number of ICP present per LDM was 6-9 branches, with 2-3 branches usually having a substantial diameter of 2-3 mm. At the time of the formal surgical dissection, no ICP were found to have been missed at the initial endoscopic dissection. There were no differences either in the number or calibre of these ICP vessels from the prepared to the control LDM. In contrast, the 4 sheep with the surgically dissected LDMs left in situ developed gross clinical evidence of extensive distal muscle necrosis and marked tenderness to palpation. These animals became increasingly distressed from the procedure such that following the collection of the third sample of blood for serial CK assays, the animals were promptly euthanased with 10 mL of intravenous thiopentone (Abbott). At autopsy, these LDMs revealed extensive distal muscle necrosis involving some 60-70% of the entire LDM. The protocols approved by the AEEC did not allow the 6 sheep with endoscopically prepared LDM to survive beyond the second operation. Their survival would have allowed serial CK measurements to be performed, but the AEEC stipulated that to maintain these animals alive, after this type of surgery and with the associated postoperative pain to be expected following this specific procedure, was unacceptable.
At a mean follow-up of 39 months in 5 selected patients, Moreira demonstrated by MRI scanning extensive fatty-fibrous degeneration of the LDM associated with a reduction of 61% in the LDM’s thickness.4 In animal studies, it has been documented that severe degenerative changes occur in the LDM at periods of 3 to 8 months after DC.s.6 It is reasonable to hypothesise that a currently indeterminate proportion of this destructive pathology is due to the initial ischaemic insult from current techniques of LDM harvesting. Furthermore, although as yet unsubstantiated, the potential would exist for subsequent and continued loss of myocytes consequent to the initial ischaemic insult. Such myocyte loss may be due to immediate necrosis and/or subsequent degeneration of the neural tissue in the thoracodorsal nerve. We believe that, at least in sheep, the LDM is damaged by current surgical methods of dissection and immediate cardiac wrapping. This vascular insult, however, may be quite variable and unpredictable as limited human necropsy cases do reveal that some LDM are in good shape, at least macroscopically, at 7 months after DC.7 Not only is it known that extensive necrosis can occur following dissection of the LDM, but the extent of damage may be significantly decreased by a timed vascular delay.829 Our study has demonstrated that endoscopic dissection of the LDM and division of the ICP branches is possible. The damage done to the muscle as assayed by serial CK levels is significantly less. Due to the conditions imposed by the AEEC, we were unable to keep the 6 sheep alive after the second operation, so we were unable to assay CK levels in the same animal after surgical dissection. We believe that the CK levels
Hence, we proposed to study additional sheep in which we would perform the traditional surgical dissection but leave the LDM in situ, measure the CK levels before and at days 1 and 2 after surgery. Our aim was to re-expose the LDM two weeks later, and perform TDR angiograms and sectional histological assays. However, it became clinically evident that extensive necrosis of the LDM was causing profound distress to the animal such that, by postoperative day 2, humane care dictated that the animal be euthanased. Consequently, this part of the experiment was concluded with procedures to only 4 animals.’ In 4 of the 6 sheep in which the LDM was prepared by endoscopic ligation, CK assays were complete. CK elevation was 307k22 U/L. In the 4 sheep in which the LDM was surgically dissected, the peak mean CK elevation was 910&38 U/L (p=O.OOl). CK levels were twice the baseline levels in the surgically dissected unprepared group at day 3 (Fig. 2).
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obtained in the 4 sheep which underwent formal surgical dissection in the unprepared LDM provide supportive evidence, particularly in view of their adverse clinical outcome.
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Whether by this means the results of DC surgery will be improved can only be speculated upon. The premise that clinical failure is due to inadequate muscle perfusion may not be the sole reason for the reported results.12 However, we can state with reasonable confidence that, if the DC procedure is going to have the best opportunity to demonstrate clinical efficacy, endoscopic ligation with a time delay of 2 weeks may enable the TDR pedicle to supply adequate blood flow to the entire muscle after transposition into the chest. This procedure is preferable to relying on those LDMs in which the TDR pedicle supplies a substantial majority of the muscle (in our experience, some lo-15% of sheep have such anatomy).
Histological examination reveals significantly less or no cell necrosis due to this method. This is consistent with the macroscopic appearance of a pink healthy muscle with palpable blood flow in its distal vascular networks. This finding has been documented by others.*Vs Angiography revealed the formation of significant vascular collaterals between the terminal branches of the TDR pedicle and the vascular networks of the ICP vessels. We believe the ischaemic stimulus consequent to the removal of the ICP vascular supply is therefore capable of inducing the development of vascular channels which enables the TDR pedicle to supply the blood flow requirements of the entire LDM.
If DC is to be successful, and this at this stage is only a supposition, it will need to be approached in a staged manner. The LDM will need to be prepared endoscopically prior to any other manoeuvre. The impact of electrical conditioning on this prepared LDM and its subsequent role in the operation of DC remain to be determined.
It has been presumed that tension and/or kinking on the TDR pedicle upon transposition into the chest may be the cause of preoperative LDM ischaemic damage. We believe that although this may occur and explain some instances of LDM necrosis, it is unlikely to be a significant factor in experienced hands. In our 4 sheep having surgical dissection in the unprepared LDM, the extent of damage to this muscle was gross, and the TDR pedicle was at no stage interfered with. We aimed to expose this muscle to the procedure that occurs in the human clinical setting but without any possibility of trauma to the TDR pedicle.
Limitations of this study As much as possible, we designed the experiments to mimic the effect of a staged approach on DC. We wished to have a cohort of sheep that had the LDM dissected but left in situ in order to provide proper controls for both the TDR angiograms and the CK elevations obtained with the histological assays. In 4 of these experimental animals, all LDMs suffered from gross extensive necrosis. Both the TDR angiograms and the subsequent histological analyses were performed in 2 temporally distinct LDMs. However, the histological slices confirmed the presence of extensive cell necrosis in the unprepared side as opposed to cell preservation in the prepared LDM. The TDR angiograms of the prepared and the unprepared LDMs were starkly different.
Lucas et al 10reported that 14 out of 16 goats (87%) with surgically dissected LDM had “severe degenerative changes”, but in the in situ LDM these changes “were not seen”. This occurred despite both groups of LDM being electrically conditioned to produce fatigue-resistant transformation of the myocytes. Mayne et al 11 in a meticulously analysed series of experiments described no instance of LDM destruction in the “in situ” electrically conditioned LDM.
Similarly, the CK levels reflected the 2 different groups of sheep. We believe that results from these 2 groups accurately reflect the clinical setting. It was unavoidable that we could not measure the CK elevation, if any, which occurred in the prepared LDMs when the sheep had the second surgical dissection. We had to work within the constraints imposed by the AEEC which we believe were in keeping with humane care to the animals.
It would seem that removal of the LDM, as is done currently, causes substantial muscle damage. Leaving the muscle in situ with ligation of the ICP allows the TDR time to nourish adequately the entire muscle. The importance of the contribution from the vascular collaterals via the Platysma-subcutaneous tissues should not be under estimated as these may be critical during the time that angiogenesis from the TDR pedicle to the ICP vascular territories is developing. This endoscopic procedure can be performed expeditiously within 20 min. We believe that in humans it will be technically simpler as there is not the confluence of teres major, scapula and LDM which is seen in most quadrupeds. Furthermore, in humans it should be possible to perform this procedure without general anaesthesia, and as such with minimal or no haemodynamic insult in patients with heart failure.
Conclusion Current techniques of harvesting the LDM can, and in many instances are likely to, cause substantial muscle damage. By means of endoscopic ligation of the ICP followed by a delay of 14 days, new vascular channels will develop to an angiographically detectable calibre capable of allowing the TDR pedicle to supply adequately the entire LDM. This technique is associated with significantly less muscle damage than current surgical dissection. If DC is
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References
2.
Carpentier A, Chacques ulated skeletal muscle: 1985;1:1267. Silverman NA. Clinical
JC. Myocardial first successful and left ventricular
substitution clinical function
with a stimcase. Lancet outcomes
improves
Alvarez, Carter, McKie collateral blood supply
to five years after dynamic cardiomyoplasty. J Thorac Cardiovasc Surg 1995;109:397-8. 3. Carpentier A, Chacques JC, Acar C, Relland J, Mihaileanu S, Bensasson D, et al. Dynamic cardiomyoplasty at seven years. J Thorac Cardiovasc Surg 1993;106;42-54. 4. Kalil-Filho R, Bocchi E, Wiss RG, et al. Magnetic resonance imaging evaluation of chronic changes in latissimus dorsii cardiomyoplasty. Circulation 1994;9O;B102-6. 5. Lucas C, van der Veen F, Kloosterman E, Habets J, Wellers H. Long-term dynamic cardiomyoplasty in the goat is accompanied by major degenerative changes in the wrapped latissimus dorsii muscle. J Am Co11 Cardiol 1993;21:469A. 6. Anderson WA, Andersen JS, Acker MA, et al. Skeletal muscle grafts applied to the heart. A word of caution. Circulation 1988;78:111:180-90. 7. Robinson JS, Truong DT, Odim J, et al. A 62-year-old man is scheduled for a new cardiac surgical procedure: dynamic cardiomyoplasty. J Cardiothorac Vast Anaes 1992;6:476-87. 8. Keelen PC, Barker JH, Frank JM, Anderson GC, Tobin GR. Optimal latissimus dorsii viability for heart wrap. World symposium cardiomyoplasty, biomechanical assist and artificial heart (proceedings) 1993:66. 9. Tobin G, Gu JM, Tobin AE, et al. Latissimus dorsii flap loss in cardiomyoplasty: anatomical basis and prevention by delay. World symposium cardiomyoplasty, biomechanical assist and artificial heart (proceedings) 1993:76. 10. Lucas CMHB, Van der Veen FH, Cheriex EC, et al. Long-term follow up (12-35 weeks) after dynamic cardiomyoplaaty. J Am Co11 Cardiol 1993;22:758-67. 11. Mayne CN, Anderson WA, Hammond RL, Eisenberg BR, Stephenson LW, Salmons S. Correlates of fatigue resistance in canine skeletal muscle stimulated electrically for up to one year. Am J Physiol 1991;261:C259-70. 12. Silverman NA. On dynamic cardiomyoplasty. J Thorac Cardiovasc Surg 1995;110:1775.
to have the optimum opportunity to achieve clinical efficacy, optimal preservation of the LDM blood supply is imperative and hence requires a staged approach; that is, the endoscopic procedure to enhance collateral blood supply to the LDM followed in 2 weeks by the DC procedure itself. This technique lends itself to other surgical procedures which require the use of this muscle dependent on the TDR pedicle as the sole source of blood supply * Acknowledgments Although this research was commenced and continued briefly in March and April 1993, it was only possible to continue and complete these experiments successfully from May 1995 by the generous funding, provision of thoracoscopic and audiovisual equipment, and excellent technical expertise from Ethicon EndoSurgery, a division of Johnson & Johnson Medical. We wish to thank Dr S. Straface of Johnson & Johnson without whose support this could not have been possible. We also thank Mr Mark A.J. Newman, FRACS, Head, Department of Cardiac Surgery, Sir Charles Gairdner Hospital for his guidance.
1.
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up
Book Review Atlas Of Ischemic Heart Disease Edited by Hisao Manabe and Chikao Yutani, 185 pages, illustrated. New York: Churchill Livingstone. ISBN 044 3079 242. $270. This new colour atlas seeks to present a comprehensive review of the pathology of coronary artery disease and myocardial infarction. The volume is divided into two sections containing a general overview of the anatomy of the coronary arteries and the pathology of atherosclerosis and myocardial infarction, followed by a section detailing numerous case presentations covering the spectrum of myocardial ischaemia and infarction.
the case presentations. Many of the anatomical specimens display meticulous dissection of the coronary arteries with careful sequential sectioning to document the extent of atherosclerosis. This is a well-produced atlas and is nicely presented. It should be a part of the teaching library in any major cardiology department as it provides a wealth of information for both undergraduate and postgraduate teaching, including the teaching of Fellows in cardiology.
This book provides a very good pathological and clinical comparison of the wide range of manifestations of ischaemic heart disease. It is richly illustrated with large, good-quality colour reproductions of the gross and microscopic pathology of coronary artery disease and myocardial infarction.
This atlas is a highly recommended cardiology library.
Richmond W Jeremy Department of Cardiology Royal Prince Alfred Hospital Sydney, N.S.W., Australia
Complementing this are electrocardiographic, radionuclide and echocardiographic illustrations providing a detailed clinico-pathological comparison in
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to a
FRACS,
Megan Carter,
RVN,
Gregory McKie,
BSC(HONS),
MBA
Department of Cardiothoracic Surgery, Sir Charles Gairdner Hospital, Nedlands, Perth, Western Australia Background: The latissimus dorsi muscle (LDM) derives its blood supply from the thoracodorsal (TDR) pedicle and from perforating branches (ICP) arising from the intercostal arteries. Current methods of surgical harvesting can cause significant ischaemic damage to this muscle. Objective: To show that by endoscopically dividing the perforating vessels of the in situ muscle and by allowing a delay of 2 weeks, angiographically detectable new collateral vascular channels develop between the terminal branches of the TDR pedicle and the vascular territories of the ICP. Methods: Six sheep underwent endoscopic ligation of the ICP of the LDM on one side. After 2 weeks, both LDMs were surgically dissected. By injecting dye into the thoracodorsal artery, angiograms were obtained. The opposite LDM served as the control. Histological sections were taken at 6 transverse levels along the length of these LDMs. Creatine kinase (CK) assays were taken before surgery and at days 1 and 2 after surgery. In 4 separate sheep which solely underwent formal surgical dissection, CK assays were also taken before surgery and days 1 and 2 after surgery. Results: In the endoscopically prepared LDMs, new vascular collaterals were convincingly demonstrated to have developed between the vascular networks of the TDR pedicle and the ICP vascular networks. Histological examination revealed minimal or no evidence of myocyte necrosis in the distal half of the LDMs of the endoscopically prepared group compared to extensive myocyte necrosis in the control LDMs of the same animal. The mean peak CK elevation of the endoscopically dissected LDM was 307&22 U/L versus a mean peak CK elevation of 910&l U/L in the 4 sheep having surgical dissection only. In this surgically dissected group, gross muscle necrosis occurred in all animals. Conclusions: Endoscopic ligation of the ICP vessels followed by a 2-week delay allows the development of collateral channels such that the TDR can solely and adequately supply the entire LDM. Subsequent surgical dissection is then tolerated with minimal or no ischaemic myocyte necrosis. (Asia Pacific Heart Journal 1998;7(2):108-113) Introduction The latissimus dorsi muscle (LDM) is the muscle of choice for muscle-assist procedures.QJ Following formal surgical dissection of this muscle, its initial viability is dependent solely on the integrity of the thoracodorsal vascular pedicle (TDP). This pedicle, however, is responsible for nourishing only 30% to 40% of the in situ muscle. The perforating branches of the intercostal arteries supply the remainder of the in situ muscle.
By endoscopically ligating the intercostal perforators of the in situ muscle followed by a delay of 2 weeks, it is possible to demonstrate the growth of angiographically detectable blood vessels from the terminal branches of the TDP to the angiographically visible vascular network derived from the intercostal perforators and, amongst these, intercostal vascular networks themselves. Methods Following the approval of our research protocol from the University of Western Australia’s Animal Experimentation Ethics Committee (AEEC), 10 sheep were used in these experiments. All animals were treated in accordance with the guidelines of the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes.
Hence, following surgical dissection of this muscle, the potential exists for a large proportion of the muscle to be damaged by ischaemia. In particular, it is the crucially important distal two-thirds which are the part of the muscle which actually wrap the heart and therefore are presumably critical in generating systolic compression and or diastolic bracing of the failing heart. To those who have dissected this muscle, the frequent striking feature after dissection is the appearance of a well-perfused proximal muscle and a cyanotic distal muscle.
Six adult cross Merino sheep weighing from 22 to 28 kilograms were anaesthetised using 35 mg/kg pentabarbitone and intubated; anaesthesia was
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AsiaPacificHeartJ 1998;7(2) Endoscopic
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improves
collateral
blood supply
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Fig. 1. Insufflating CO2 between the lattissimus dorsii (LD)
and the chest wall (CW) lifts the LDM above and off the CW, allowing clear visualisation and division of the ICP by the endoscopic dissectionscissors. Fig. 2. Creatine kinase levels (U/L) for the control group of
maintained using 2% Halothane with oxygen and nitrous oxide at a ratio of 1:2. The sheep’s flank from shoulder to rump was then shaved. The side to be used was determined in a prospective and randomised manner by the toss of a coin.
surgically dissected LDM vs the prepared (endoscopically ligated ICP) LDM. blood to assay creatine kinase (CK) levels were taken prior to commencement of the surgical procedure and on the morning of postoperative days 1 and 2.
Two small skin incisions (2 cm) were made a hand’s breadth from the posterior forelimb crease and a hand’s breadth proximal to the anterior hind limb crease at the level of the lower palpable border of the LDM. Using arterial forceps, dissection to the level of the chest and abdominal wall was performed. Two Endopath Tristar 512B blunt-tip 12mm surgical trocars fitted with Endopath MS 5 12 Multiseal caps (Ethicon Endo-Surgery, Johnson & Johnson) were inserted. Carbon dioxide was insufflated into the plane between the LDM and the body wall with an Olympus Surgical CO2 Insufflator. By this manoeuvre the LDM is lifted off the body wall by the accumulating C02.
Two weeks following this surgery, the sheep were anaesthetised, intubated and prepared in the same manner. A formal surgical dissection of the LDM was performed both on the previously prepared LDM in which thoracoscopic ligation of the intercostal perforators had been performed and on the unprepared contralateral LDM which served as the control. The surgical dissection was performed by means of a longitudinal incision from the shoulder to the rump at the level of the palpable lower border of the muscle. The number of intercostal perforators (ICP) encountered on both sides were noted. The TDP was then isolated and the artery, vein and nerve identified. The artery was cannulated with a 22 G Insyte cannula (Becton Dickinson Pty Ltd, Australia), and 10 rnL of sodium heparin were injected. The LDM was removed from the sheep and placed under an image intensifier; 8-10 mL of Omnipaque dye (350 mg 12/mL, Sanofi-Winthrop), diluted in a 1:l ratio with 0.9% normal saline, were injected into the thoracodorsal artery until the arterial tree within the LDM was clearly defined. The TDR vascular pedicle was then ligated and an X-ray film (small focus, 42kV and 3.2 mAs) using a retail UVG film (Kodak) was obtained.
A 30” Olympus thoracoscope was inserted into one of the trochars. This was connected to an Olympus CLV/S light source attached to an Olympus OTV/S4 camera control unit displaying the underlying anatomical dissection on a Sony Trinitron monitor. A DC512 disposable curved scissor with unipolar cautery (Endopath, Johnson & Johnson) was inserted via the remaining trocar. With both the thoracoscope and the dissecting scissors in the plane between the body wall and the LDM, careful dissection allows clear visualisation of the intercostal perforating vascular pedicles (Fig. 1) as well as the thoracodorsal vascular pedicle. The intercostal perforators were counted and divided using cautery or surgical clips.
The LDMs were weighed and stored in a 10% formalin solution. The time interval from surgical removal of the LDMs to immersion in the formalin solution was in all cases less than 20 min. The sheep were then euthanased with a dose of 10 mL of Lethabarb (pentabarbitone, 325 mg/rnL, Virbac Pty Ltd Australia) administered intravenously. The protocols granted by the AEEC did not allow these sheep to be maintained alive following the second operation.
The extent of the dissection proceeded from the point of insertion of the TDR pedicle to the point of contiguity of the LDM with anterior abdominal wall and from the level of its free margin to the vertebral spines. We called this LDM the prepared side. Haemostasis being secured, the 2 skin incisions were closed with non-absorbable sutures. Samples of venous
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Pacific Heart J 1998;7(2) Endoscopic
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Fig. 3. Angiogram of an endoscopically prepared LDM. Extensive new vascular channels (arrows) are evident throughout the LDM communicating the TDR pedicle to the ICP vascular networks. In 4 adult cross Merino sheep weighing from 20 to 29 kg, a formal surgical dissection of the muscle was performed following the same protocol for anaesthesia, intubation and preparation. The LDM was left attached along its vertebral border and where it became contiguous with the distal abdominal wall. The ICP vessels were divided. The TDR pedicle was left intact and, hence, was the sole vascular supply to the LDM. The LDM was, therefore, dissected off the body wall and from the overlying subcutaneous tissues. Its sole attachment being the fibrous continuity along its vertebral border to the distal abdominal wall aponeurosis. Venous blood samples were taken immediately prior to the commencement of surgery and on the morning of postoperative days 1 and 2. As a consequence of their clinical condition on the morning of postoperative day 2, these 4 sheep were euthanased immediately (following the collection of this last sample of blood) with 10 mL. of intravenous Lethabarb. CK levels were also assayed in these 4 sheep. The mean levels of CK, and the standard deviations, for these 2 groups of sheep from baseline to 48 hours after surgery are provided in Fig. 2.
Fig. 4. Angiograms
of the endoscopically unprepared LDM on the left versus the endoscopically prepared LDM on the right. New vascular connections are predominant throughout the LDM (arrows) from the thoracodorsal pedicle (TDR) to the intercostal perforator vascular networks (ICP)
specimens from all 6 sheep. Histological staining (haematoxylin and eosin staining) was performed on these sections. The clinical appearance of the LDM of the 4 sheep that had the formal complete surgical dissection of the LDM, which was then left in situ, were those of gross macroscopic extensive distal half necrosis. Such necrosis
Histological analysis Full thickness transverse sections at 3-cm intervals from the point of insertion of the TDR pedicle were taken of the LDM from both the prepared and control
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Histological staining of the prepared LDM revealed minimal to no evidence of cell necrosis in the distal half of the prepared LDMs as opposed to extensive cell necrosis and degeneration in the unprepared controls. The proximal part of the LDM revealed no differences in terms of cellular integrity between the prepared and control group of muscles.
ReSUltS In all 6 sheep with endoscopically ligated ICP, angiograms revealed striking patterns of new vessel development from the TDR pedicle to the ICP vascular networks (Figs. 3 and 4). The striking macroscopic appearance at the time of surgical dissection of these prepared LDMs after a 2-week delay was the absence of cyanosis of the distal muscle and visible and palpable pulsations of the ICP vascular networks. Clinically, there was no exudative collection nor tenderness to palpation in the prepared sides. The animals tolerated the procedure apparently with minimal discomfort.
Discussion Following the innovative work of the French surgeon Dr A. Carpentier,’ the operation of dynamic cardiomyoplasty (DC) has captured the imagination of cardiac surgeons worldwide. Despite a decade since the first human report, however, the role which this procedure may have in patients with heart failure remains imprecise.zJ There are undoubtedly many causes for the discrepancies in results reported following this operation. In the most recent series reported by Carpentier, of those patients having DC who died postoperatively and prior to hospital discharge, half died from cardiac failure; at postmortem, half of the patients were found to have extensive necrosis of the LDM.3
The number of ICP present per LDM was 6-9 branches, with 2-3 branches usually having a substantial diameter of 2-3 mm. At the time of the formal surgical dissection, no ICP were found to have been missed at the initial endoscopic dissection. There were no differences either in the number or calibre of these ICP vessels from the prepared to the control LDM. In contrast, the 4 sheep with the surgically dissected LDMs left in situ developed gross clinical evidence of extensive distal muscle necrosis and marked tenderness to palpation. These animals became increasingly distressed from the procedure such that following the collection of the third sample of blood for serial CK assays, the animals were promptly euthanased with 10 mL of intravenous thiopentone (Abbott). At autopsy, these LDMs revealed extensive distal muscle necrosis involving some 60-70% of the entire LDM. The protocols approved by the AEEC did not allow the 6 sheep with endoscopically prepared LDM to survive beyond the second operation. Their survival would have allowed serial CK measurements to be performed, but the AEEC stipulated that to maintain these animals alive, after this type of surgery and with the associated postoperative pain to be expected following this specific procedure, was unacceptable.
At a mean follow-up of 39 months in 5 selected patients, Moreira demonstrated by MRI scanning extensive fatty-fibrous degeneration of the LDM associated with a reduction of 61% in the LDM’s thickness.4 In animal studies, it has been documented that severe degenerative changes occur in the LDM at periods of 3 to 8 months after DC.s.6 It is reasonable to hypothesise that a currently indeterminate proportion of this destructive pathology is due to the initial ischaemic insult from current techniques of LDM harvesting. Furthermore, although as yet unsubstantiated, the potential would exist for subsequent and continued loss of myocytes consequent to the initial ischaemic insult. Such myocyte loss may be due to immediate necrosis and/or subsequent degeneration of the neural tissue in the thoracodorsal nerve. We believe that, at least in sheep, the LDM is damaged by current surgical methods of dissection and immediate cardiac wrapping. This vascular insult, however, may be quite variable and unpredictable as limited human necropsy cases do reveal that some LDM are in good shape, at least macroscopically, at 7 months after DC.7 Not only is it known that extensive necrosis can occur following dissection of the LDM, but the extent of damage may be significantly decreased by a timed vascular delay.829 Our study has demonstrated that endoscopic dissection of the LDM and division of the ICP branches is possible. The damage done to the muscle as assayed by serial CK levels is significantly less. Due to the conditions imposed by the AEEC, we were unable to keep the 6 sheep alive after the second operation, so we were unable to assay CK levels in the same animal after surgical dissection. We believe that the CK levels
Hence, we proposed to study additional sheep in which we would perform the traditional surgical dissection but leave the LDM in situ, measure the CK levels before and at days 1 and 2 after surgery. Our aim was to re-expose the LDM two weeks later, and perform TDR angiograms and sectional histological assays. However, it became clinically evident that extensive necrosis of the LDM was causing profound distress to the animal such that, by postoperative day 2, humane care dictated that the animal be euthanased. Consequently, this part of the experiment was concluded with procedures to only 4 animals.’ In 4 of the 6 sheep in which the LDM was prepared by endoscopic ligation, CK assays were complete. CK elevation was 307k22 U/L. In the 4 sheep in which the LDM was surgically dissected, the peak mean CK elevation was 910&38 U/L (p=O.OOl). CK levels were twice the baseline levels in the surgically dissected unprepared group at day 3 (Fig. 2).
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obtained in the 4 sheep which underwent formal surgical dissection in the unprepared LDM provide supportive evidence, particularly in view of their adverse clinical outcome.
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Whether by this means the results of DC surgery will be improved can only be speculated upon. The premise that clinical failure is due to inadequate muscle perfusion may not be the sole reason for the reported results.12 However, we can state with reasonable confidence that, if the DC procedure is going to have the best opportunity to demonstrate clinical efficacy, endoscopic ligation with a time delay of 2 weeks may enable the TDR pedicle to supply adequate blood flow to the entire muscle after transposition into the chest. This procedure is preferable to relying on those LDMs in which the TDR pedicle supplies a substantial majority of the muscle (in our experience, some lo-15% of sheep have such anatomy).
Histological examination reveals significantly less or no cell necrosis due to this method. This is consistent with the macroscopic appearance of a pink healthy muscle with palpable blood flow in its distal vascular networks. This finding has been documented by others.*Vs Angiography revealed the formation of significant vascular collaterals between the terminal branches of the TDR pedicle and the vascular networks of the ICP vessels. We believe the ischaemic stimulus consequent to the removal of the ICP vascular supply is therefore capable of inducing the development of vascular channels which enables the TDR pedicle to supply the blood flow requirements of the entire LDM.
If DC is to be successful, and this at this stage is only a supposition, it will need to be approached in a staged manner. The LDM will need to be prepared endoscopically prior to any other manoeuvre. The impact of electrical conditioning on this prepared LDM and its subsequent role in the operation of DC remain to be determined.
It has been presumed that tension and/or kinking on the TDR pedicle upon transposition into the chest may be the cause of preoperative LDM ischaemic damage. We believe that although this may occur and explain some instances of LDM necrosis, it is unlikely to be a significant factor in experienced hands. In our 4 sheep having surgical dissection in the unprepared LDM, the extent of damage to this muscle was gross, and the TDR pedicle was at no stage interfered with. We aimed to expose this muscle to the procedure that occurs in the human clinical setting but without any possibility of trauma to the TDR pedicle.
Limitations of this study As much as possible, we designed the experiments to mimic the effect of a staged approach on DC. We wished to have a cohort of sheep that had the LDM dissected but left in situ in order to provide proper controls for both the TDR angiograms and the CK elevations obtained with the histological assays. In 4 of these experimental animals, all LDMs suffered from gross extensive necrosis. Both the TDR angiograms and the subsequent histological analyses were performed in 2 temporally distinct LDMs. However, the histological slices confirmed the presence of extensive cell necrosis in the unprepared side as opposed to cell preservation in the prepared LDM. The TDR angiograms of the prepared and the unprepared LDMs were starkly different.
Lucas et al 10reported that 14 out of 16 goats (87%) with surgically dissected LDM had “severe degenerative changes”, but in the in situ LDM these changes “were not seen”. This occurred despite both groups of LDM being electrically conditioned to produce fatigue-resistant transformation of the myocytes. Mayne et al 11 in a meticulously analysed series of experiments described no instance of LDM destruction in the “in situ” electrically conditioned LDM.
Similarly, the CK levels reflected the 2 different groups of sheep. We believe that results from these 2 groups accurately reflect the clinical setting. It was unavoidable that we could not measure the CK elevation, if any, which occurred in the prepared LDMs when the sheep had the second surgical dissection. We had to work within the constraints imposed by the AEEC which we believe were in keeping with humane care to the animals.
It would seem that removal of the LDM, as is done currently, causes substantial muscle damage. Leaving the muscle in situ with ligation of the ICP allows the TDR time to nourish adequately the entire muscle. The importance of the contribution from the vascular collaterals via the Platysma-subcutaneous tissues should not be under estimated as these may be critical during the time that angiogenesis from the TDR pedicle to the ICP vascular territories is developing. This endoscopic procedure can be performed expeditiously within 20 min. We believe that in humans it will be technically simpler as there is not the confluence of teres major, scapula and LDM which is seen in most quadrupeds. Furthermore, in humans it should be possible to perform this procedure without general anaesthesia, and as such with minimal or no haemodynamic insult in patients with heart failure.
Conclusion Current techniques of harvesting the LDM can, and in many instances are likely to, cause substantial muscle damage. By means of endoscopic ligation of the ICP followed by a delay of 14 days, new vascular channels will develop to an angiographically detectable calibre capable of allowing the TDR pedicle to supply adequately the entire LDM. This technique is associated with significantly less muscle damage than current surgical dissection. If DC is
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References
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Carpentier A, Chacques ulated skeletal muscle: 1985;1:1267. Silverman NA. Clinical
JC. Myocardial first successful and left ventricular
substitution clinical function
with a stimcase. Lancet outcomes
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to five years after dynamic cardiomyoplasty. J Thorac Cardiovasc Surg 1995;109:397-8. 3. Carpentier A, Chacques JC, Acar C, Relland J, Mihaileanu S, Bensasson D, et al. Dynamic cardiomyoplasty at seven years. J Thorac Cardiovasc Surg 1993;106;42-54. 4. Kalil-Filho R, Bocchi E, Wiss RG, et al. Magnetic resonance imaging evaluation of chronic changes in latissimus dorsii cardiomyoplasty. Circulation 1994;9O;B102-6. 5. Lucas C, van der Veen F, Kloosterman E, Habets J, Wellers H. Long-term dynamic cardiomyoplasty in the goat is accompanied by major degenerative changes in the wrapped latissimus dorsii muscle. J Am Co11 Cardiol 1993;21:469A. 6. Anderson WA, Andersen JS, Acker MA, et al. Skeletal muscle grafts applied to the heart. A word of caution. Circulation 1988;78:111:180-90. 7. Robinson JS, Truong DT, Odim J, et al. A 62-year-old man is scheduled for a new cardiac surgical procedure: dynamic cardiomyoplasty. J Cardiothorac Vast Anaes 1992;6:476-87. 8. Keelen PC, Barker JH, Frank JM, Anderson GC, Tobin GR. Optimal latissimus dorsii viability for heart wrap. World symposium cardiomyoplasty, biomechanical assist and artificial heart (proceedings) 1993:66. 9. Tobin G, Gu JM, Tobin AE, et al. Latissimus dorsii flap loss in cardiomyoplasty: anatomical basis and prevention by delay. World symposium cardiomyoplasty, biomechanical assist and artificial heart (proceedings) 1993:76. 10. Lucas CMHB, Van der Veen FH, Cheriex EC, et al. Long-term follow up (12-35 weeks) after dynamic cardiomyoplaaty. J Am Co11 Cardiol 1993;22:758-67. 11. Mayne CN, Anderson WA, Hammond RL, Eisenberg BR, Stephenson LW, Salmons S. Correlates of fatigue resistance in canine skeletal muscle stimulated electrically for up to one year. Am J Physiol 1991;261:C259-70. 12. Silverman NA. On dynamic cardiomyoplasty. J Thorac Cardiovasc Surg 1995;110:1775.
to have the optimum opportunity to achieve clinical efficacy, optimal preservation of the LDM blood supply is imperative and hence requires a staged approach; that is, the endoscopic procedure to enhance collateral blood supply to the LDM followed in 2 weeks by the DC procedure itself. This technique lends itself to other surgical procedures which require the use of this muscle dependent on the TDR pedicle as the sole source of blood supply * Acknowledgments Although this research was commenced and continued briefly in March and April 1993, it was only possible to continue and complete these experiments successfully from May 1995 by the generous funding, provision of thoracoscopic and audiovisual equipment, and excellent technical expertise from Ethicon EndoSurgery, a division of Johnson & Johnson Medical. We wish to thank Dr S. Straface of Johnson & Johnson without whose support this could not have been possible. We also thank Mr Mark A.J. Newman, FRACS, Head, Department of Cardiac Surgery, Sir Charles Gairdner Hospital for his guidance.
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Book Review Atlas Of Ischemic Heart Disease Edited by Hisao Manabe and Chikao Yutani, 185 pages, illustrated. New York: Churchill Livingstone. ISBN 044 3079 242. $270. This new colour atlas seeks to present a comprehensive review of the pathology of coronary artery disease and myocardial infarction. The volume is divided into two sections containing a general overview of the anatomy of the coronary arteries and the pathology of atherosclerosis and myocardial infarction, followed by a section detailing numerous case presentations covering the spectrum of myocardial ischaemia and infarction.
the case presentations. Many of the anatomical specimens display meticulous dissection of the coronary arteries with careful sequential sectioning to document the extent of atherosclerosis. This is a well-produced atlas and is nicely presented. It should be a part of the teaching library in any major cardiology department as it provides a wealth of information for both undergraduate and postgraduate teaching, including the teaching of Fellows in cardiology.
This book provides a very good pathological and clinical comparison of the wide range of manifestations of ischaemic heart disease. It is richly illustrated with large, good-quality colour reproductions of the gross and microscopic pathology of coronary artery disease and myocardial infarction.
This atlas is a highly recommended cardiology library.
Richmond W Jeremy Department of Cardiology Royal Prince Alfred Hospital Sydney, N.S.W., Australia
Complementing this are electrocardiographic, radionuclide and echocardiographic illustrations providing a detailed clinico-pathological comparison in
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to a