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Ann Thorac Surg 2003;76:1587-1592
© 2003 The Society of Thoracic Surgeons

Original article: cardiovascular

"Demand" stimulation of latissimus dorsi heart wrap: experience in humans and comparison with adynamic girdling

Gianluca Rigatelli, MD*a, Giorgio Rigatelli, MDb, Mario Barbiero, MDb, Angelo Cotogni, MDb, Attilio Bandello, MDb, Roberto Riccardi, MDc, Ugo Carraro, MD, PhDd

a EndoCardioVascular Therapy Research, Verona, Italy
b Cardiomyoplasty Project Unit, Legnago General Hospital, Verona, Italy
c Division of Cardiology, Montescano Medical Center, Pavia, Italy
d C.N.R. Institute of Neuroscience, Unit for Neuromuscularbiology and Physiopathology, Laboratory of Applied Myology of the Department of Biomedical Science, University of Padua, Padua Medical School, Padua, Italy

Accepted for publication April 29, 2003.

* Address reprint requests to Dr Rigatelli, EndoCardioVascular Therapy Research, Via T. Speri, 18, 37040 Legnago, VR, Italy
e-mail: jackyheart{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Questionable systolic assistance and latissimus dorsi (LD) muscular degeneration as a result of continuous electrical stimulation constitute important drawbacks to dynamic cardiomyoplasty. To avoid full transformation of the LD and thereby cause better systolic assistance, a new stimulation protocol was developed. Fewer impulses per day are delivered so that the LD wrap has daily periods of rest (demand), based on a heart rate cutoff. We describe our experience of demand dynamic wrapping by discriminating between patients with active systolic assistance and those with a passive girdle effect (adynamic-girdling).

METHODS: Fourteen patients with primary dilated cardiomyopathy (13 men, 1 woman; mean age, 58.2 ± 5.8 years; 12 sinus rhythm, 2 atrial fibrillation) underwent dynamic cardiomyoplasty between 1993 and 1996 as well as the demand protocol at different intervals. Clinical, echocardiographic, mechanographic, and cardiac invasive assessment records, as well as cardiovascular events (death and arrhythmias), were retrospectively reviewed. The patients were divided into two groups on the basis of the mechanographic measurement of speed of contraction of the heart wrap, as measured by tetanic fusion frequency analysis before starting demand stimulation: demand dynamic wrapping patients with fast LD (high tetanic fusion frequency, 7 patients), and adynamic-girdling patients with slow LD contraction times (low tetanic fusion frequency, 7 patients). It was assumed that in adynamic-girdling patients dynamic assistance was virtually absent, so the wrapping acted only as a passive constraint wall.

RESULTS: The two groups were comparable for sex, age, dilated cardiomyopathy cause, New York Heart Association class, and left ventricular ejection fraction at the start of the demand protocol period. After a mean duration of follow-up of 41.4 ± 21.1 months (range, 23 to 69 months), the demand dynamic wrapping group showed improved New York Heart Association class (1.14 ± 0.34 versus 2.07 + 0.18; p = 0.0004), higher values of left ventricular ejection fraction (34.6 ± 8.0 versus 26.5 ± 3.1; p = 0.005) and LD wrap tetanic fusion frequency (38.3 ± 5.88 versus 24.3 ± 2.93; p = 0.002), and a better survival (85.7% versus 28.6%; p = 0.037) than the adynamic-girdling group.

CONCLUSIONS: Demand dynamic wrapping offers good results in terms of fewer cardiovascular events and greater survival. When compared with the passive constraint effect of LD muscle, demand dynamic wrapping proved to be more effective.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
In the recent American College of Cardiology/American Heart Association guidelines for evaluation and management of chronic heart failure [1], dynamic cardiomyoplasty (DyCMP) is excluded as a treatment option. Questionable systolic assistance and latissimus dorsi (LD) degeneration have been considered the main drawbacks of this technique. Many authors only recognize the passive girdle effect of DyCMP (adynamic cardiomyoplasty) to be its mechanism of action [2–5].

To hopefully improve systolic assistance, and to reduce muscular damage, fewer impulses per day were delivered than with the standard clinical stimulation protocol [6]. This was achieved by providing the LD wrap with daily periods of rest (demand stimulation) based on a heart rate cutoff [7, 8]. Our previous studies proved that effective measurable systolic assistance is possible in patients who undergo a demand stimulation protocol early. Its value was high when the demand protocol was started early after surgery and much lower to virtually absent when the demand protocol was started several months after continuous burst stimulation. In particular we proved that systolic assistance is strictly related to the contractile properties of the LD, ie, to the speed of contraction expressed in tetanic fusion frequency (TFF) value [9, 10].

We report our experience with demand dynamic wrapping (DemDynWrap) in humans by discriminating between patients with active systolic assistance and those with virtually passive girdle effect. We discuss the impact of this new stimulation protocol on classic adynamic cardiomyoplasty results to reopen the debate about the role of this type of cardiac assistance as an alternative to passive constraint and mechanical devices.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
We retrospectively reviewed clinical, echocardiographic, mechanographic, and cardiac invasive assessment records as well as cardiovascular events (death and arrhythmias) in 14 patients (13 men, 1 woman; mean age, 58.3 ± 5.7 years; sinus rhythm 12, atrial fibrillation 2, mean New York Heart Association [NYHA] class, 3.2 ± 0.4) suffering from idiopathic dilated cardiomyopathy and congestive heart failure who underwent DyCMP according to the original Broussais Hospital procedure [11] from 1993 to 1996.

The stimulator was programed for demand stimulation at the Department of Cardiology, Cardiomyoplasty Project Unit—Center for Advanced Heart Failure, Legnago Teaching Hospital, Verona, Italy, whereas follow-up was performed at this center as well as at the Division of Cardiology and Rehabilitation, Montescano Medical Center, Maugeri Foundation, Montescano, Pavia, Italy.

The demand protocol was electively introduced in a pool of patients forming the Italian Trial of Demand Dynamic Cardiomyoplasty and in patients who had previously undergone DyCMP according to one of these criteria: worsening of clinical conditions during DyCMP continuous stimulation, or no amelioration of clinical condition during DyCMP continuous stimulation with no short-term to mid-term prospect of heart transplantation.

Informed consent to the intervention and then to the demand stimulation protocol was obtained from all patients. Therapy was personalized with diuretics, low-dose ß-blockers, digitalis, and amiodarone as needed in each patient.

Demand stimulation protocol
The demand stimulation protocol was introduced [6, 7] in hopes of avoiding complete LD wrap transformation caused by the continuous stimulation protocol of the US Food and Drug Administration phase 2 trial used by the American Cardiomyoplasty Group [12].

It is well known that a muscle that has been fully transformed by continuous stimulation displays significant loss of power, generally attributed to fiber type change or loss of type 2 myofibers (fast-contracting myofibers). The inclusion of daily rest periods during chronic burst electrical conditioning maintains myofiber cross-sectional area and produces fatigue-resistant myofibers of faster contraction speed, and creates a more powerful fatigue-resistant muscle. The improved performance of such LD is because of the maintenance of an intermediate level of LD transformation, thanks to the activity-rest regimen on demand [6, 12–14]. The LD was stimulated with a single impulse at a 1:3 synchronization ratio after a healing period of 10 to 14 days. An extra impulse was then added every week at a 23-ms interval (43 Hz) for a final burst of four impulses, with a cardiac amplitude more than 5 V and pulse width of 1.5 ms. After 6 to 12 months of this light daily stimulation, the patients took part in the demand regimen, which gave the LD wrap a daily period of rest [8].

To provide the LD wrap with daily periods of rest, a 24-hour Holter study was performed first to determine the average heart rate during sleep. The pacing variables of the cardiomyostimulator (Transform, model 4710; Medtronic, Inc, Minneapolis, MN) were programed at a rate of 70 to 80 beats/min, with minimum pulse amplitude (<1 V) and pulse width (<0.05 ms). Muscle output was programed to "Sense," occurring only with sensed cardiac events, not with paced events. In this way, the lower rate was set just above the average nighttime heart rate and the cardiomyostimulator worked during resting hours at an energy level well below requirements for activating the heart. During these pacing episodes, muscle output was inhibited. The result was that muscle stimulation was inhibited during the resting hours and occurred at the programed synchronization ratio during activity, providing an activity-rest stimulation regimen. The differences between conventional continuous burst stimulation and the new demand protocol are shown in Table 1 [7].


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  		Table 1. Old Continuous-Burst Stimulation Versus the New Demand Stimulation Protocols

 
Monitoring latissimus DORSI wrap function: the mechanogram
Dynamic contractile characteristics of the LD wrap, ie, speed of contraction and relaxation, can be monitored using a standard polygraph (MegaCart or Mingophon, Siemens Elema, Solna, Sweden). Electrocardiogram and pressure changes caused by LD contraction can be simultaneously recorded as previously described [7, 8, 15]. The dynamic characteristics of the LD wrap are determined by the LD response to stimuli delivered at increasing frequency up to TFF. At low stimulation frequency, the mechanogram shows that some relaxation occurs in between in-burst impulses (unfused tetanus). At higher stimulation frequency, a smooth curve is recorded (fused tetanus), which lasts as long as the tetanic contraction is maintained (<200 ms with four impulses delivered at 43 Hz). The higher the TFF, the faster the contractile characteristics of the LD wrap. The normal value of TFF for human LD muscle is 43 Hz; the fused tetanus is obtained with in-burst impulses delivered at 23-ms intervals [7].

The mechanogram is also useful to precisely synchronize the LD wrap contraction to cardiac systoles [7, 12].

The value of 43-Hz TFF, which characterizes a fast-contracting muscle, provides systolic assistance, whereas a TFF less than 26 Hz, characterizing a slow-contracting muscle, provides a very low or immeasurable systolic assist [9, 10]. Therefore, the patients were divided into two groups on the basis of TFF cutoff value of 26 Hz at starting time of demand stimulation of the LD wrap, one group with an expected systolic assistance, the other acting as the adynamic-girdling group. The results of the two groups were compared.

Statistical analysis
Paired Student's t test was used to compare data before and after demand DyCMP, whereas frequencies were compared using the {chi}2 test. A p value less than 0.05 was considered significant. Clinical and laboratory data were expressed as mean ± standard deviation or as percentage. The Pearson correlation coefficient was used to evaluate linear correlation. Survival rate was expressed as mean ± standard error of the mean. To evaluate effectiveness of the DemDyWrap, patients who switched to the heart transplantation program as a result of worsening clinical conditions, occurrence of malignant ventricular arrhythmias, or need for implantable cardioverter defibrillator were counted as dropouts, whereas a death because of noncardiovascular-related causes was counted as censored data. StatView (SAS Institute Inc, Cary, NC) and GraphPad Prism 3 (GraphPad Software Inc, San Diego, CA) systems were used for data analysis and graphic output.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
The mean duration of follow-up after starting the demand stimulation of the LD wrap was 41.4 ± 17.5 months (range, 23 to 69 months). Clinical, echocardiographic, mechanographic, and invasive catheterization data are given for the start and end of follow-up.

Cumulative results of 14 patients
There were no perioperative deaths. The mean NYHA class was significantly lower when compared with preoperative values: 1.7 ± 0.8 versus 3.2 ± 0.4 (p < 0.0001). The mean ejection fraction at follow-up was significantly higher than preoperative value: 0.32 ± 0.07 versus 0.226 ± 0.044 (p < 0.001); furthermore, the mean end-diastolic volume did not significantly change during the follow-up (114 ± 41.1 versus 104 ± 9.9 mL/m2; p < 0.67). Right-heart catheterization data also demonstrated an insignificant decrease in capillary wedge pressure (12.2 ± 6.1 to 11.7 ± 7.2 mm Hg; p = 0.83).

Lastly, mechanographic interrogation shows TFF values were significantly higher (33 ± 8.0 versus 15.8 ± 11 Hz; p < 0.0001) than at the start of the demand protocol.

During the follow-up, 1 patient died of hepatic cancer at 36 months and another died of massive pulmonary embolism at 18 months from the operation. Both were in NYHA class 1 one month before death. One patient implanted with a biventricular defibrillator for the development of left bundle block and ventricular arrhythmias died after 60 months as a result of cardiogenic shock. Similar to previous observations with stimulated LD wrap [16], the autopsy examination revealed some atrophy and fat degeneration of the muscle wrap, but with a fast–slow checkerboard appearance of the myofibers and a small heart. Three patients, continuously stimulated for many months (107, 64, and 57 months) were switched to the heart transplant program for worsening clinical conditions. The actuarial 5-year survival rate was 46.36%.

Comparison between groups
Seven patients had TFF more than 26 Hz (DemDynWrap) and the other 7 had TFF less than 26 Hz (adynamic-girdling). At the start of the demand protocol, the two groups were comparable for sex, age, dilated cardiomyopathy cause, NYHA class, and left ventricular ejection fraction (LVEF; Table 2).


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  		Table 2. Data of Dem and Dynamic Wrapping Versus Adynamic-Girdling Groups at Starting Time of Demand Stimulation of the Latissimus Dorsi Wrap

 
At follow-up, the DemDynWrap group showed a better NYHA class, higher LVEF, and TFF (Table 3), and a better survival (85.7% versus 28.6%; p = 0.037; Fig 1) than the adynamic-girdling group. Event-free survival rate was not significantly higher (50% versus 45%; p = 0.217; Fig 2) in the DemDynWrap patients.


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  		Table 3. Summary of Results of Dem and Dynamic Wrapping Versus Adynamic-Girdling

 


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  		Fig 1. Actuarial survival in the two groups of patients. Data are expressed as mean ± standard error of the mean. (DEM = demand dynamic cardiomyoplasty; ADYN = adynamic cardiomyoplasty.)

 


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  		Fig 2. Event-free survival in the two groups of patients. Data are expressed as mean ± standard error of the mean. (DEM = demand dynamic cardiomyoplasty; ADYN = adynamic cardiomyoplasty.)

 
Duration of continuous burst stimulation correlates directly with TFF (r = 0.64; p = 0.014) and indirectly with LVEF (r = 0.61; p = 0.009) values, suggesting that the longer the duration of continuous stimulation, the greater the LD atrophy and thus, the smaller the systolic assistance.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Dynamic cardiomyoplasty has recently been excluded as a treatment option from the American College of Cardiology/American Heart Association guidelines for the evaluation and management of chronic heart failure in the adult [1], owing to the poor long-term results. Indeed, many authors have failed to prove any systolic assistance.

In DyCMP, there are two possible mechanisms to explain improved clinical results: limited heart dilation (heart remodeling) and the enhancement of systolic contraction. Systolic assistance has been suggested but not proven by studies revealing low-to-moderate increase in LVEF and stroke volume [16, 17].

Nevertheless, a real and notable improvement in NYHA class, usually from class III or higher to class II or lower, has been reported worldwide, although improvements in LVEF seem to be limited to early follow-up periods [12, 17–21]. Therefore, there is a general consensus that only a passive girdle effect occurs with time with classic DyCMP.

Contractile characteristics and fat and fibrotic degeneration of the LD wrap, caused by the continuous burst stimulation, play an important role in this general opinion. From pathologic and morphologic studies [6, 13], it appears that muscle degeneration is caused by surgical dissection of the muscle and is exacerbated by chronic stimulation. Moreover, the 2-week delay in stimulation after cardiomyoplasty may also contribute to muscle atrophy and loss of function [22]. These studies led to the concept that intermittent burst stimulation may result in less muscle damage and a fatigue-resistant, fast-contracting LD wrap, contributing to more-effective cardiac support. To improve the results of classic DyCMP activity-rest patterns were introduced [6, 13, 14]. We use this technique in patients with a demand stimulation of the LD wrap [7–10].

Our previous studies suggested that muscular properties correlated well to the amount of systolic assistance and are maintained with time [9, 10]. Altogether, these results explain the higher TFF values and the improvements in NYHA class and in LVEF value, as well as the good survival rate in the DemDynWrap group of patients. Moreover, surprisingly in the patients in whom demand protocol was started after several years of the continuous burst stimulation protocol, the TFF not only maintained its initial value, but in many cases increased. This is sound evidence of muscle plasticity in humans, and further supports the opinion that muscle degeneration is not a necessary outcome of long-term continuous burst stimulation of LD wrap in DyCMP.

On the other hand, analyses here also suggest that the demand protocol may reverse full fast-to-slow transformation and atrophy or degeneration of the LD wrap. Thus it provides an active systolic assistance, improving LVEF and quality of life also in those patients, in whom LD degeneration was suspected owing to long-term continuous stimulation. Indeed, in these cases demand protocol was expected to only provide a prolonged passive girdle effect.

In the era of heart transplantation and great technological advances in the field of circulatory assistance devices and of the artificial heart, we think demand dynamic girdling by muscle tissue may still play a role.

Unfortunately, donor organs are still scarce in comparison to clinical needs; transplantation itself as well as immunosuppressive therapy and its follow-up remain extremely expensive, and chronic rejection limits survival to 38% at 12 years. Ventricular assist devices, which also are expensive, carry a high incidence of complications and some contraindications. The Acorn (recently developed as a containment heart dilation support device [23]) has the advantage of its low cost and simple implantation procedure, but it acts only as a barrier to heart dilation without systolic contribution, which is very important in achieving not only palliative but also curative results.

Demand dynamic wrapping, on the other hand, is moderately complex and expensive. It does not require extracorporeal circulation, immunosuppression, anticoagulation therapy, or follow-up with endocardial biopsy, and may achieve real cardiac assistance. Our previous studies on demand stimulation protocol demonstrated not only that this protocol can make DyCMP more effective, but also that an adequate follow-up of the LD wrap is obtained by a standard economic polygraph combined with echocardiographic analyses [7, 8, 15].

Limitations
Our study comes with some limitations, ie, small number of patients and absence of randomization. The difficulty of enrollment of patients was because the procedure is among the clinical research options, and also because of the negative attitude of cardiologists who are well aware of the outcomes of the old DyCMP.

Conclusion
We believe that the demand approach and related activity-rest protocols are the most effective adjuncts to DyCMP. The more physiologic utilization of the LD wrap, by preventing excessive muscle degeneration, provides an amelioration of the response to DyCMP in terms of systolic assistance and survival. These "new" improved techniques may refresh the role of DyCMP as an option for patients who are considered for heart transplantation or mechanical devices. In light of the results described above, reconsideration of the role of demand dynamic girdling is not only rational and reasonable, but also appropriate. Combined with muscle engineering by myoblast or myogenic stem cell delivery [24, 25], demand dynamic girdling could answer the increasing clinical demands of aging societies.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
Supported in part by funds from the Italian National Research Council Institute of Neuroscience, Unit for Neuromuscular Biology and Physiopathology at The University of Padua. Supported by the Italian Ministry of University and Scientific and Technologic Research (M.U.R.S.T. no. 9806192428): Italian Trial of Demand Dynamic Cardiomyoplasty (ITDDC); and 60% of the funds to U.C. The authors thank Anne Holdstock for her assistance in the preparation of this manuscript and Larry Stephenson, MD, for his invaluable competence in language editing.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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