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Eur J Cardiothorac Surg 1998;13:213-215
© 1998 Elsevier Science NL


Case report

Preserved skeletal muscle structure with modified electrical stimulation protocol in a cardiomyoplasty patient: a clinico-pathological report

Roberto Lorussoa, Ottavio Alfieria, Ugo Carrarob, Jan J. Schreuderc, Hein J.J. Wellensc

a Cardiac Surgery Division, IIa Divisione Cardiochirurgica, Ospedale Civile, Brescia, 25125, Italy
b Pathology Department, Padua, Italy
c Department of Cardiology, Academic Hospital, Maastricht, The Netherlands

Received 7 August 1997; received in revised form 8 December 1997; accepted 16 December 1997.

Corresponding author. Tel.: +39 30 3995638; fax: +39 30 3995004; e-mail: roberto_lorusso@iol.it


    Abstract
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 Abstract
 Introduction
 Case report
 Comment
 References
 
Experimental and clinical studies have recently shown variable degrees of structural abnormalities in the transposed and chronically stimulated muscle graft after cardiomyoplasty procedure. The postoperative stimulation protocol of wrapped skeletal muscle has been claimed to be a major determinant of late structural derangement. Therefore, a modified stimulation protocol had been used after a cardiomyoplasty procedure in a 63-year-old patient. Improved postoperative hemodynamic data could be detected by pressure/volume analysis. After unexpected sudden death occurred at 15 months, autoptic examination showed preserved muscle structure, suggesting that a prudent stimulation protocol may maintain muscle viability and contribute to effective cardiac support.

Key Words: Cardiomyoplasty • Stimulation protocol • Muscle viability


    Introduction
 Top
 Abstract
 Introduction
 Case report
 Comment
 References
 
Skeletal muscle integrity is a fundamental factor for optimal power to be expressed during muscle contraction. Concerns regarding long-term muscular structure have been raised in cardiomyoplasty procedure [1]. The pattern of muscle electrical stimulation has been shown to be responsible for muscle ischemia [2] which may ultimately lead to myocellular death, to lypomathosys, and to fibrotic tissue replacement. Based on these concepts, a modified stimulation protocol has been applied in a patient submitted to cardiomyoplasty procedure. Despite subjective and documented hemodynamic improvements, the patient died because of sudden death 15 months after surgery. Autoptic findings of conditioned and unconditioned muscles are herein described.


    Case report
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 Abstract
 Introduction
 Case report
 Comment
 References
 
A 63-year-old gentleman affected by progressive deterioration of chronic heart failure secondary to coronary artery disease, and unresponsive to maximal pharmacological therapy was referred for surgical treatment. The patient was not suitable for myocardial revascularization because of severely depressed left ventricular function and absence of viable myocardium in the akinetic segments. Heart transplantation was contraindicated for complicated diabetes (peripheral vascular disease) and chronic renal insufficiency (previous excision of one kidney because of malignant tumor). Pressure–volume analysis of cardiac performance was carried out preoperatively by using a conductance catheter, as previously reported [3]. Cardiomyoplasty was deemed an appropriate therapeutic option for this patient and carried out by using the left latissimus dorsi muscle (LDM) in a clockwise cardiocostal wrapping. No extra-corporeal circulation was required during the wrapping procedure. Following 2 weeks of no muscle pacing to allow muscle graft recovery and enhance muscular revascularization, the stimulation protocol was started, adopting a modified pattern. The heart/muscle contraction ratio was programmed at 4 to 1, and the pacing frequency was gradually increased every other week up to 30 Hz. This protocol allowed maintenance of a reduced muscle workload compared with that commonly used in the clinical setting (1:1 or 2:1). Muscle pulse amplitude was programmed at 4 V. At 6 months from cardiomyoplasty the patient was submitted to hemodynamic evaluation by pressure-volume study. Pre- and postoperative data are shown in Table 1. Significant hemodynamic changes were documented, and remarkable reduction of cardiac dilatation was observed ( Fig. 1 ). Despite maintained clinical improvement, the patient died because of sudden death 15 months after surgery. Postmortem evaluation was carried out. The left LDM appeared well wrapped and grossly viable. Six muscle biopsies were collected from the proximal portion till the peripheral part of the pedicled graft, taking care to include even some portion of the heart/muscle interface. Five specimens from the contralateral unconditioned LDM were also collected for control morphological analysis and measurements. All biopsies were analyzed for morphology, enzyme-histochemistry, and electron microscopy. Muscle fiber diameter and composition, and intramuscular capillaries were studied. Contralateral unstimulated LDM was composed by fascicles of polygonal muscle fibers (mean diameter 40±3.0 µm) with focally interposed lobules of fat tissue (18% of the total cross sectional area). A moderate variation in muscle fiber size was observed, but no structural alterations were detected. Reactions for myosin-ATPase and densitometric determination of myosin heavy chain showed the expected fast pattern dominated by type 2B fibers (Table 2). Distribution of intramuscular capillaries was normal and they appeared with restricted lumen. Morphological analysis of wrapped LDM showed homogeneous results in the specimens obtained at different regions except for the muscle portion close to the electrode insertion. In this area only, variation in fiber size (mean fiber diameter 28±4 µm), scattered degenerative alterations of muscle fiber, moderate reduction in the number of capillaries per fiber, and increase in endomysial connective tissue, were observed. In the remaining specimens fascicles composed by polygonal fibers with moderate variation in size were documented (mean fiber diameter 36±2 µm). Rare atrophic fibers with round profile were observed. Myosin-ATPase and the electrophoretic analysis of myosin heavy chains revealed a partial fiber type transformation (up to 60% of type 1 fiber), whereas the fast fibers were mainly of type 2A (Table 2). The percentage of interfascicular fat tissue was 24% of the total cross sectional area. Dilated capillaries were observed in all studied specimens while the number of capillaries per fiber was similar to that of contralateral muscle.


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Table 1. Hemodynamic data as measured by conductance catheter preoperatively and 6 months after cardiomyoplasty procedure

 


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Fig. 1. Pressure–volume loops of the left ventricle are presented. The right loops (A) correspond to preoperative cardiac pressures and volumes, whereas left loops (B) relate to postoperative situation (6-month follow-up). A reduction of ventricular volumes is evident (shift to the left). These loops were obtained with cardiomyostimulator switched off. Plv, left ventricular pressure; Vlv, left ventricular volume.

 

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Table 2. Distribution of myosin heavy chain in different regions of LDMs

 

    Comment
 Top
 Abstract
 Introduction
 Case report
 Comment
 References
 
In cardiomyoplasty procedure a skeletal muscle is to be harvested, transposed, wrapped around the ventricles, and synchronously stimulated to provide permanent cardiac support. Patterns of electrical stimulation have been shown to exert profound influence in muscle structural response. Evidence of altered muscle structure (myofibre abnormalities and replacement with fatty and fibrotic tissues) have been described experimentally [1] [4] and clinically [5]. Mechanical properties of the chronically-stimulated muscle are intimately related to the preserved structure [4]. The importance of the LDM stimulation mode was recently addressed by van Doorn and colleagues [2] who demonstrated that a 1:1 mode was associated with impairment in blood flow of stimulated LDM, whereas a 2:1 mode was able to maintain LDM blood supply/demand balance. Indirect evidences of long-term muscle degeneration in patients submitted to cardiomyoplasty procedure was described by Kalil-Filho and collaborators using MRI evaluation [5]. Nonetheless, those findings had been mainly obtained adopting a 1:1 stimulation mode. In our patient, the use of increased ratio between heart and muscle contractions (4:1) was meant to reduce wrapped muscle workload and prevent muscle ischemia, while maintaining an acceptable rate of supported beats. Hemodynamic study in our patient after cardiomyoplasty procedure documented effective LDM cardiac assist and important changes in left ventricular volumes. Nonetheless, despite overall cardiac improvement, high LV end-diastolic pressure persisted and might have provoked a fatal arrhythmia. Clinically, just a few reports described detailed inspection of muscle histology after cardiomyoplasty with controversial findings [6] [7] [8], but, to our knowledge, no study showed histological muscle changes at more than 1 year from cardiomyoplasty related with significant hemodynamic changes. In our patient, the modified stimulation pattern was able to induce a partial transformation (high percentage of type 2A fibers) of the transposed muscle which may account for preserved original muscle power. In conclusion, this study showed that a modified stimulation protocol of the wrapped LDM was able to preserve muscle integrity up to more than 1 year from cardiomyoplasty. Maintained LDM structure was moreover linked to substantial changes in hemodynamics.


    References
 Top
 Abstract
 Introduction
 Case report
 Comment
 References
 

  1. Lucas CMHB, van der Veen FH, Cheriex EC, Lorusso R, Havenith M, Penn OCKM, et al. Long-term follow-up (12 to 35 weeks) after dynamic cardiomyoplasty. J Am Coll Cardiol 1993;22:758-767.[Abstract]
  2. van Doorn CAM, Bhabra MS, Hopkinson DN, Barman D, Cranley JJ, Hooper TL Latissimus dorsi muscle blood flow during synchronized contraction: implications for cardiomyoplasty. Ann Thorac Surg 1996;61:603-609.[Abstract/Free Full Text]
  3. Schreuder JJ, van der Veen FH, van der Velde ET, Delahaye F, Alfieri O, Jegaden O, et al. Beat-to-beat analysis of left ventricular pressure–volume relation and stroke volume by conductance catheter and aortic model flow in cardiomyoplasty patients. Circulation 1995;91:2010-2017.[Abstract/Free Full Text]
  4. Kratz JM, Johnson WS, Mukherjee R, Hu J, Crawford FA, Spinale FG The relation between latissimus dorsi skeletal muscle structure and contractile function after cardiomyoplasty. J Thorac Cardiovasc Surg 1994;107:868-878.[Abstract/Free Full Text]
  5. Kalil-Filho R, Bocchi E, Weiss RG, Rosemberg L, Bacal F, Moreira LFP, et al. Magnetic resonance imaging evaluation of chronic changes in latissimus dorsi cardiomyoplasty. Circulation 1994;90(part 2):102-106.
  6. Odim JNK, Burgess JH, Williams BH, Blundell PE, Rabinovtich MA, et al. Pathophysiology of dynamic cardiomyoplasty: a clinico-pathological case study. J Cardiovasc Surg 1990;5:336-346.
  7. Rossi MA, Braile DM, Souza DRS, Santos JLV, Thevenard RS, Pinto GH, et al. Dynamic cardiomyoplasty in chronic Chagas’ heart disease: clinico-pathological data. Ann Thorac Surg 1991;51:649-651.[Abstract]
  8. Carraro U, Chachques JC, Desnos M, Hagège A, Fontarilan F, Carpentier A. Eight-year human dynamic cardiomyoplasty: preserved structure of myofibres and vessels of the latissimus dorsi. Basic Appl Myol 1996;6:333-336.



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