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Ann Thorac Surg 2005;79:198-203
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Cardiac "Fitness" Training: An Experimental Comparative Study of Three Methods of Pulmonary Artery Banding for Ventricular Training

Emmanuel Le Bret, MD, PhDa,*, Jean Marc Lupoglazoff, MD, PhDa, Nicolas Borenstein, DVMa, Gaelle Fromont, MDb, François Laborde, MDa, Jean Bachet, MDa, Pascal Vouhé, MDc

a Department of Cardiac Diseases Institut Mutualiste Montsouris, Paris, France
b Department of Pathology, Institut Mutualiste Montsouris, France
c Pediatric Cardiac Surgery, Hôpital Necker Enfants Malades, Paris, France

Accepted for publication June 25, 2004.

* Address reprint requests to Dr Le Bret, Department of Cardiac Diseases, Institut Mutualiste Montsouris, 42 Bd Jourdan, 75014Paris, France (E-mail: emmanuel.lebret{at}imm.fr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: When the left ventricle is unable to sustain a systemic pressure in transposition of the great arteries (TGA), left ventricular retraining is mandatory before the morphologic left ventricle under the aorta is switched. This is currently achieved by creating a ventricular overload through pulmonary artery banding, usually associated with an aortopulmonary shunt in case of a TGA with an intact ventricular septum. Our experimental study compared three different modes of increased ventricular afterload to obtain ventricular hypertrophy.

METHODS: Fifteen lambs (mean weight 48 kg) underwent pulmonary artery banding. Five animals (group I) received a classic band; 5 (group II) received a classic band which was adjusted at week 1 and 3; and 4 (group III) received a band which was tightened for 1 hour, twice a day (early morning and late afternoon). After 5 weeks, the lambs were evaluated hemodynamically before they were sacrificed and their hearts harvested for histologic examination.

RESULTS: No difference was noted in the hemodynamic data between groups 1 and II. Group III showed a greater ability to increase ventricular pressure in this model. No significant difference was noted between the three groups in terms of macroscopic alterations, but all animals demonstrated an increase in right ventricular wall thickness compared with control animals. Several fibrosis areas were evident in group I and II but none in group III.

CONCLUSIONS: Intermittent pulmonary artery banding is able to induce hemodynamically sufficient ventricular hypertrophy without fibrosis.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The arterial switch operation (ASO) is the currently preferred mode of treatment for transposition of the great arteries (TGA) with an intact ventricular septum (IVS) [1, 2]. After birth, progressive regression of the left ventricular mass in TGA-IVS [3, 4] restricts the adequate period for primary ASO to within the first [5] or second months [6] of life. First described by Yacoub and colleagues in 1977 [7], left ventricular preparation has been reported for a two-stage arterial switch in infants with simple TGA [8–10], but also when atrial baffles are converted into ASO [11–12] or when a double switch intervention for corrected transposition of the great arteries is to be performed [12, 13].

Preoperative left ventricular retraining consists of pulmonary artery banding (PAB), usually associated with an aortopulmonary shunt in case of TGA with IVS. One of the main limitations of this method is proper adjustment of the PAB to obtain an adequate level of ventricular constraint. For many authors, a minimum of two procedures is necessary to adjust the pulmonary constriction for good ventricular preparation [12].

To avoid those reinterventions, many authors have developed various techniques of adjustable PAB [14–19]. We have developed our own adjustable device, which was used in the present experimental study [20]. However, the best technique to create an adequate ventricular hypertrophy with an adjustable band that results in good hemodynamic efficacy is not yet well defined yet. Therefore, this study compared three protocols of PAB: permanent, progressive, or intermittent ("fitness" banding) to evaluate the differences in hemodynamic efficacy and histologic alterations between the three methods.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Animal Model and Anesthesia Protocol
Fifteen lambs (Ile de France), weighing from 35 to 61 kg and 4 to 10 months old, were operated for PAB. Anesthesia was induced with sodium thiopental (10 mg/kg intravenously) and maintained with a mixture of isoflurane (Forene; Abbot, Rungis, France) (1% to 2%) and oxygen. Animals were ventilated through a single lumen tube at 10 mI/kg with a volume-cycled ventilator at 20 breaths per minute and FIO2 60%. Monitoring included continuous electrocardiographic tracing, invasive blood pressure through the auricular artery, and central venous pressure through the jugular vein. Anesthetized animals were reclining on the right side for left lateral thoracotomy.

Pulmonary Artery Banding
After opening the chest through the fourth left intercostal space, the pericardium was opened anterior and parallel to the left phrenic nerve, and the pulmonary trunk was dissected at its mid portion. The right ventricular pressure was monitored by direct catheterization. Baseline right ventricular pressure, pulmonary pressure, and maximal right ventricular pressure were recorded.

In group I, (5 lambs) the PAB was achieved by using a 4 mm wide Dacron (DuPont, Wilmington, DE) band. The degree of constriction was adjusted according to the method described by Mee [21]. After tightening the band acutely for 4 to 5 seconds and recording the maximal right ventricular pressure, the band was loosened until hemodynamic stability returned. The band was then gradually tightened to achieve a right ventricular pressure of about 70% to 80% of the previously observed maximal pressure. The band was then fixed to the pulmonary artery wall and hemodynamic stability was assessed for 20 to 30 minutes before the chest was closed. The lambs were left with the pulmonary artery banding for 5 weeks.

In group II, (5 lambs) the first PAB was achieved exactly in the same way as in group I, but all animals were reoperated at week 1 and 3 to readjust the PAB. The maximal right ventricular pressure was reassessed, and whenever necessary, the band was retightened to achieve a right ventricular pressure of about 70% to 80% of the maximal right ventricular pressure. The total duration of PAB was also 5 weeks.

In group III, (5 lambs), our adjustable pulmonary artery band was used to perform the PAB [20]. The balloon was snared around the pulmonary artery trunk, the maximal right ventricular pressure was measured, and sterile water was injected to inflate the balloon. The volume of sterile water required to obtain a ventricular pressure of about 70% to 80% of the maximal ventricular pressure was noted for each animal. The balloon was connected to the subcutaneous chamber placed on the lateral face of the chest. In this group of lambs, ventricular training was achieved by inflating the balloon for 1 hour twice a day (early morning and late afternoon) at the level noted during implantation. Duration of training was also 5 weeks. No statistical difference was noted concerning weight and age of the animals in the three groups.

Animal Care
After surgery and the following day, if needed, the animals were left to recover with the required analgesic regimen (morphine, 0.5 mg/kg; flunixin, 1 mg/kg).

The study was approved by the institutional ethics committee for animal research, and all animals received humane care in compliance with the Guide for the Care and Use of Laboratory Animals prepared by the Institute of Laboratory Animal Resources, National Research Council, and published by the National Academy Press, revised 1996.

Hemodynamic Exploration
After 5 weeks of training, the lambs were reanesthetized and reoperated to remove the band and to record the hemodynamic data. Under control of central venous and systemic arterial pressures, the right ventricular pressure was measured and the maximal right ventricular pressure was estimated by acute clamping of the pulmonary trunk for a few seconds. Two ratios were calculated: the maximal right ventricular pressure/systemic arterial pressure ratio and the maximal right ventricular pressure/initial right ventricular pressure ratio. These ratios were compared with the equivalent ratios obtained during the implantation of the band.

Histologic Studies
After recording the hemodynamic data, the animals were sacrificed and the hearts were harvested for histologic examination. They were compared to a control group of nonoperated animals. Macroscopic data included the weight, the size, and the right and left ventricular wall thickness in fresh and fixed heart. Microscopic examination was particularly focused on evidencing fibrotic reactions on the right ventricular free wall or on the interventricular septum. Histologic examination was carried out in a blind fashion regarding the mode of training.

Statistical Analysis
Hemodynamic variables are expressed as mean ± standard deviation. They were compared in each group by means of the Student's t test. As the Levene test for equal variances was not significant when the results of the different ratios were studied, we have compared the three groups by an analysis of variance with the Bonferroni test. Macroscopic data were compared by means of the Student's t test, and the existence of myocardial fibrosis in each group was compared by means of the {chi}2 test with the Yates adjustment for little subgroup (Fisher test). Results were considered as significant if p was less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Hemodynamic Results
The hemodynamic data are summarized in Tables 1 and 2. No differences were noted among the 3 groups in terms of preoperative hemodynamic data. After 5 weeks of training, the maximal right ventricular pressure/systemic pressure ratio had significantly increased in the three groups compared with the calculated baseline ratio. The mean increment was 28%, 15%, and 18% in group I, II, and III, respectively, without any significative difference between the groups. The maximal right ventricular pressure/basic right ventricular pressure ratio increased after 5 weeks of training. Student's t test revealed that this increase was not significant for groups I (p = 0.14) and II (p = 0.32) but was significant for group III (p = 0.007). Analysis of variance (Bonferroni) showed that the increment in group III was significant when compared with group II (p = 0.013) and group I (p = 0.037). There was no significant difference between group I and II (Table 3).


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  		Table 1. Evolution of the Maximal Right Ventricular Pressure/Aortic Pressure Ratio During the Five Weeks of Training in Each Group
 

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  		Table 3. Analysis of Variance (Bonferonni Test)
 
No hemodynamically adverse effect was noted concerning the right ventricular function.

Histologic Results
MACROSCOPIC EXAMINATION
The results of the macroscopic examination are reported in Table 4. To avoid variations caused by the differences in the weight of the animals, all data were indexed to the weight. Weights were comparable in the three PAB groups and in the control group. All three PAB groups demonstrated an increase in the ventricular wall thickness compared with the control group (p < 0.05), but no significant differences were noted among the three groups. The left ventricular wall thickness was similar in the three PAB groups.


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  		Table 4. Histologic Results (Indexed Data)
 
MICROSCOPIC EXAMINATION
Fibrosis was noted in 2 patients out of 5 in group I and in 3 patients out of 5 in group II. Fibrosis was present on the septal portion of the right ventricle in 1 patient and on the right ventricular wall in 4 patients (Fig 1). In each sample, no more than one limited area of fibrosis (less than 2 mm in diameter) was observed. No quantitative measurement was performed. No area of fibrosis was noted in group III or in the control group. No other morphologic differences were noted among the groups.



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  		Fig 1. Trichrome-Masson staining shows the myocardial fibrosis in blue. (A) Focal myocardial fibrosis is present in group I and II (x20). (B) No fibrotic reaction in group III (x20).

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
When the concept of a two-stage arterial switch was introduced in 1977, Yacoub and colleagues suggested that this should allow anatomic correction of TGA to be performed after the neonatal period (at a mean of 12 to 24 months). Others have reported successful left ventricular "slow" retraining in patients until teenage or early adulthood [22]. However, a two-stage arterial switch has been associated with a certain drawbacks:
• The incidence of aortic regurgitation (anatomic pulmonary valve) is consistently higher in case of PAB for left ventricular retraining than with a primary repair [23].
• Sievers and colleagues have demonstrated that a certain degree of dilatation of the pulmonary root may occur in response to pulmonary banding [24].
• Several authors have reported the need for a tube to reconstruct the pulmonary outflow tract after the two-stage correction.
• The Lecompte maneuver can be performed for a direct anastomosis after a short interval period of preparation, but it seems to be very difficult in the presence of adhesions after PAB.
• Most authors report the necessity of several interventions to adjust the pulmonary artery band.

All these shortcomings of left ventricular retraining had led most authors to favor an early, rapid, two-stage arterial switch whenever possible. It has also been reported that, despite the reduced duration of pulmonary artery banding, left ventricular retraining in an early two-stage procedure may adversely affect myocardial function in some patients.

Myocardial hypertrophy because of chronic pressure overload is known to be associated with depressed ventricular function in animals and adult humans, [25] although the mechanism is unclear. The myocardial response to hemodynamic constraint by myocyte hypertrophy results in an increase in oxygen uptake and requires a proportional growth of the mitochondria responsible for supplying energy. Although myocardial angiogenesis and coronary perfusion were reported to be preserved in young lambs with pressure overload hypertrophy, limitations in coronary vascular reserve have been observed in adult animal and human models of pressure-overload hypertrophy.

In addition, the increment of the ventricular wall stress contributes to the reduction in myocardial perfusion especially in the subendocardial area. Ventricular hypertrophy secondary to acute pressure overload may be associated with focal areas of necrosis and collagen fibrosis [26, 27]. In the present study, this type of fibrosis was observed in group I and II but not in group III. It seems that the ventricular hypertrophy observed in this "fitness" group remained adaptive, with no pathologic consequences, mimicking the results observed in trained athletes.

This experimental study has demonstrated that intermittent PAB can produce almost the same results as permanent or progressive pulmonary artery banding. The hemodynamic results show that acute maximal right ventricular pressure after 5 weeks of the "fitness" program is higher than in the groups with regular PAB. The results of the cardiac fitness group can be explained by several observations made on athletes in training.

De Maria and colleagues in 1977 [28] reported a study of 26 healthy subjects, 20 to 34 years old, who participated in an 11-week program of endurance physical conditioning. The training sessions consisted of a walk-jog-run program, designed to maintain the heart rate at 70% of exercise-determined maximum, for a 1-hour period, 4 days a week. Echocardiography was performed before, during, and after the training program. The results of the echocardiographic study indicated that physical conditioning induced significant alterations in cardiac anatomy. The left ventricular end diastolic dimension was increased, the left ventricular end systolic dimension was decreased, and stroke volume and shortening fraction were increased. The mean fiber shortening velocity and left ventricular mass were also increased. Cardiac output and peripheral vascular resistance were identical. This study suggested that the mature human myocardium also responds within days to an acute increase in workload. Similarly, Ehsani and colleagues [29] demonstrated in 8 swimmers (17 to 19 years old), who were followed up with weekly echocardiograms during a 9-week training program, that the left ventricular mass increased from 84.1 to 103 g/m2 within only 1 week and then plateaued for the remainder of the training period.

Interestingly, the reverse was observed with deconditionning. The fact that the maximal result in terms of left ventricular mass increment appears after only 1 week of training has been also reported in left ventricular training for two-staged arterial switch. For Boutin and colleagues [9], the compensatory hypertrophy after pulmonary artery banding was almost complete after 7 to 10 days.

That intermittent cardiac fitness can train a ventricle can be explained by molecular biology studies [30–35]. As soon as 1968, Nair and colleagues [30] demonstrated that banding of the adult rat aorta resulted in a rapid increase in heart weight within 2 to 3 days. Within 48 hours, cardiac weight increased by a mean of 30% and RNA content increased by 65%. The heart weight and RNA content reached a plateau by the second or third day. More precisely, gene expression of c-myc, c-fos proto-oncogene, which regulates the growth of cardiomyocytes, occurs in rat cardiac cells within 1 hour of an acute pressure load. Similarly, hsp70, the gene of a major heat shock protein that protects the cell under various conditions, is also induced within 1 hour. Transcription of c-myc, c-fos and hsp70 messenger ribonucleic acids ceases within 24 to 48 hours, but the presence of the related proteins in the nucleus may play a permissive role in facilitating the hypertrophic response. Thus an acute right ventricular pressure overload elicits a rapid change in the gene expression and can initiate the processus of cardiac hypertrophy.

After the 2-hour training done in group III, the stress condition of the myocardium was released, and this rest condition may have facilitated tissue oxygenation and protein synthesis when compared with groups I and II.

Study Limitations
This study suffers from certain limitations: no molecular biology study was done to measure the molecular response, but such a study will be implemented in the near future. In addition, no cellular count was done to evaluate hyperplasia and angiogenesis. We think that such a count would have been meaningless because the animals in this study were to old to show evidence myocardial hyperplasia in response to ventricular training.

In conclusion, adequate training of a ventricle can be obtained by an intermittent increase of afterload, similar to fitness training. The probable mechanism is that the hypertropic process initiates a molecular cascade that can develop in good conditions during periods of rest and optimal oxygen transfer and, therefore, without the development of fibrosis related to ischemia. This mode of training could represent a safe and effective method for retraining the left ventricle in view of late arterial switch for TGA.


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  		Table 2. Evolution of the Maximal Right Ventricular Pressure/Initial Right Ventricular Pressure Ratio During the Five Weeks of Training in Each Group
 

   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was supported by a grant from the Fondation de l'Avenir pour la Recherche Médicale Appliquée. The authors wish to thank the members of the Centre d'Experimentation et de Recherche Appliquée for technical assistance and collaboration, and Fabrice Larrazet for statistical support.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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