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Does right ventricular outflow tract damage play a role in the genesis of late right ventricular dilatation after tetralogy of Fallot repair?
Yves d’Udekem d’Acoz, MD, Agnes Pasquet, MD, Laurent Lebreux, MD, Caroline Ovaert, MD, Franc¸oise Mascart, MD, Annie Robert, ScD, PhD, and Jean E. Rubay, PhD, MD Departments of Cardiovascular and Thoracic Surgery, Cardiology, and Pediatric Cardiology, Cliniques Universitaires Saint-Luc, Brussels, Belgium, and the Public Health School, Universite´ Catholique de Louvain, Brussels, Belgium
Background. The aim of this study was to determine the relative role of pulmonary insufficiency and right ventricular outflow tract damage in the genesis of late symptoms related to right ventricular dilatation. Methods. In a retrospective study we compared the late outcomes of patients who had undergone operations known to generate pulmonary insufficiency, namely, transventricular repair of tetralogy of Fallot and pulmonary commissurotomy for isolated pulmonary stenosis. Results. In our institution, between 1964 and 1984, a total of 44 patients were found to have had an isolated pulmonary commissurotomy and 189 survived a transventricular repair of tetralogy of Fallot. Of these patients, 134 had patching of the right ventricle and 55 direct closure of a right ventriculotomy. Follow-up was 94% complete after a mean of 22 ⴞ 7 years. On echocardiography, patients with isolated commissurotomy had similar degrees of moderate and severe pulmonary insufficiency as tetralogy of Fallot patients who had a right
ventricular patch (p > 0.2). However, freedom from adverse events related to right ventricular dilatation was far better (log rank p < 0.001) in patients with isolated commisurotomy. Conclusions. Pulmonary insufficiency is not the only determinant of late symptomatic right ventricular dilatation after repair of tetralogy of Fallot. Pulmonary insufficiency seems much more deleterious in patients who have had right ventricular outflow tract patching. Longterm pulmonary insufficiency alone is responsible for a slight degree of right ventricular dilatation, but symptoms may develop much later if the contractility of the pulmonary infundibulum is preserved. The pulmonary infundibulum may be essential for right ventricular ejection, and for maintaining pulmonary valve competence.
A
ciency as did patients who had undergone operation with a transannular patch. A recent magnetic resonance imaging study performed on 85 adult patients who had undergone operation for tetralogy of Fallot confirmed that right ventricular volumes and pulmonary regurgitant volumes were equal regardless of whether the pulmonary annulus had initially been spared [5]. In that study, the predictive factors of right ventricular dilatation were not only the presence of pulmonary insufficiency, but also the identification of an akinetic or dyskinetic area in the right ventricular outflow tract. Therefore, we suspected that right ventricular outflow tract damage may play an important role in the late genesis of ventricular dilatation. We wanted to investigate this hypothesis in a clinical model. A randomized prospective study would be impractical because the results would be apparent only about 20 years after the repair. Therefore we decided to
lthough surgical correction of tetralogy of Fallot offers a favorable long-term outcome, an increasing proportion of patients with this condition experience the deleterious consequences of progressive right ventricular dilatation: sudden death, congestive heart failure, or decreased exercise capacity [1–3]. For many years, longterm pulmonary insufficiency related to transannular patching has been incriminated as the main determinant leading to late right ventricular dilatation. In a recent follow-up study, we demonstrated that attempts to preserve pulmonary valve competence at operation by limiting the patching to the ventricular area below the pulmonary valve did not protect patients from the late deleterious consequences of right ventricular dilatation [4]. Twenty-five years after this repair, these patients had extremely similar outcomes, including the same degree of right ventricular dilatation and pulmonary insuffi-
(Ann Thorac Surg 2003;76:555– 61) © 2003 by The Society of Thoracic Surgeons
Accepted for publication Feb 21, 2003. Address reprint requests to Dr d’Udekem d’Acoz, Service de Chirurgie Cardiovasculaire et Thoracique, Cliniques Universitaires Saint-Luc— Avenue Hippocrate 10, B-1200 Brussels, Belgium; e-mail: dudekem@ chir.ucl.ac.be.
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Inc
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Does Right Ventricular Outflow Tract Damage Play a Role in the Genesis of Late Right Ventricular Dilatation After Tetralogy of Fallot Repair?
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Table 1. Patient Characteristics Characteristic CARDIOVASCULAR
Patients, n Age at operation (y) Previous palliation, n (%) Pulm commissurotomy, n (%) Fallot ⫽ tetralogy of Fallot;
Isolated Pulmonary Commissurotomy
Fallot: Direct Closure RV
Fallot: Limited RV Patch
Fallot: Transannular Patch
44 6.7 (0.3– 4) 0 44 (100)
55 7 (0.5–25) 18 (33) 31 (56)
35 4 (0.3– 45) 8 (23) 24 (69)
99 3.3 (0.6 –27) 32 (32) 99 (100)
Pulm ⫽ pulmonary;
RV ⫽ right ventricular.
perform a retrospective study in patients with pulmonary regurgitation for a similar period to compare their outcomes with those of patients who had undergone operation for tetralogy of Fallot. We identified patients who had had operations for an isolated pulmonary commissurotomy as the ideal candidates, inasmuch as this operation is known to create valvar insufficiency [6 – 8].
Patients and Methods The study design was approved by the hospital ethics committee before any investigation.
Study Groups Between 1964 and 1984, a total of 152 patients underwent a pulmonary commissurotomy for isolated pulmonary stenosis at our institution. After 1984, this procedure was almost exclusively performed by interventional catheterization and the surgical procedure was virtually abandoned. Of the patients who underwent operation, 44 who had no concomitant resection or incision of muscular bundles of their right ventricular outflow tract and no associated cardiac defects constitute the study group. Their operative data were reviewed and they all were contacted and offered a follow-up consultation with 12lead ECG and transthoracic echocardiography. If they were unwilling to return to our hospital, they were asked questions about their functional status. Follow-up was completed between June and November 2000. During the same period, we updated the follow-up of all the 189 consecutive hospital survivors of a transventricular repair of tetralogy of Fallot operated between 1964 and 1984 in our institution. We excluded patients who had atrio-ventricular septal defect or pulmonary atresia as well as those who needed a right ventricular outflow tract conduit at the time of the repair.
Surgical Procedures In all, 58 of the tetralogy of Fallot patients and none of the pulmonary commissurotomy patients had a systemicopulmonary shunt as a palliative procedure before the operation. All ventricular septal defects in patients with tetralogy of Fallot were closed through a right ventriculotomy. Relief of the right ventricular outflow tract obstruction was obtained by widely resecting all septoparietal and parieto-parietal muscle bundles of the pulmonary infundibulum. If the pulmonary annulus itself seemed narrowed, the incision extended through the pulmonary annulus up to the main pulmonary artery and
the whole area was patched. If the right ventricular outflow tract seemed wide enough, the ventriculotomy was closed directly. If the surgeon believed that direct closure of the ventriculotomy would compromise the size of the pulmonary infundibulum, this incision was closed with a patch. Characteristics of the patients are displayed in Table 1. Their age at operation was not significantly different among the various patients groups except in patients undergoing a transannular patch repair, who were younger than the others (p ⬍ 0.03). Of the isolated pulmonary commissurotomy patients, 20 underwent operation under caval occlusion and 24 under cardiopulmonary bypass. The main pulmonary artery was opened with a longitudinal incision and under direct vision, the commissures were separated with a blade, and redundant dysplastic tissue was excised. After completion of the pulmonary commissurotomy, the arteriotomy was closed directly without patch interposition.
Electrocardiographic and Echocardiographic Studies In all ECG collected from the patients with isolated pulmonary commissurotomies, QRS duration was measured manually and defined as the maximal QRS duration over all leads. On echocardiographic examination, pulmonary insufficiency was described as mild if the regurgitant jet started at the valve, moderate if it started in the main pulmonary artery, and severe if it started in the pulmonary artery branches. End-diastolic dimensions of both ventricles were measured by M-mode echocardiography performed on parasternal short-axis views obtained just below the level of the tips of the mitral valve leaflets [9]. Restrictive physiology was defined as the presence of a forward flow in the main pulmonary artery during atrial systole independently of the breathing cycle [10].
Statistical Analysis Data are reported as means ⫾ standard deviations or as percentages. Groups were compared using 2 tests for dichotomous variables and Student’s t tests for continuous variables. Survival curves were estimated using the product-limit method described by Kaplan and Meier, and standard errors were computed using the Rothman method [11]. Different adverse long-term outcomes related to progressive right ventricular dilatation were investigated: (1) cardiac death, defined as sudden unexpected death or death related to heart failure; (2) reoperation for symptomatic right ventricular dilatation; and (3) New York
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Results Follow-Up There were no operative deaths among the patients who had an isolated pulmonary commissurotomy. Follow-up was 95% complete for the tetralogy of Fallot patients and 91% for those with an isolated pulmonary commissurotomy. Mean follow-up was 22.4 ⫾ 6.9 years. Because they believed that there was no need for follow-up, only 13 of the 44 patients who had undergone a pulmonary commissurotomy had been reviewed by a cardiologist in the 5 years preceding our contact and follow-up investigation.
Late Outcome In all, 16 of the tetralogy of Fallot patients who had undergone repair had died during the follow-up period. Of these cases, 10 were considered as cardiac deaths (7 cases of sudden unexpected deaths and 3 of congestive heart failure). The other patients died of unrelated causes (2 of trauma from motor vehicle accidents, 1 of chronic glomerulonephritis, 1 of chronic viral hepatitis, 1 after a reoperation for tracheal stenosis, and 1 in septic shock related to a GI tract infection). There were no cardiac deaths among the patients who were operated for isolated pulmonary stenosis; 1 patient died of trauma from a motor vehicle accident and 1 of a chest chondrosarcoma. In all, 28 tetralogy of Fallot patients had a cardiac reoperation after a mean of 15.9 ⫾ 8.7 years. One patient underwent a heart transplantation, 6 patients had a reoperation for residual or associated cardiac lesions (2 residual ventricular septal defects, 1 partial anomalous pulmonary venous return, 1 closure of a giant aortopulmonary collateral, and 2 aortic valve replacements), 1 patient had open heart cryoablation, and 20 patients had pulmonary valve replacement in their right ventricular outflow tract with a homograft (1 for a mixed regurgitation and stenosis, and the remaining for severe pulmonary regurgitation and symptomatic right ventricular dilatation. All patients who underwent a valvulation of their outflow tract underwent a preoperative catheterization to rule out pulmonary artery stenosis on hypoplasia. There were no reoperations among patients who underwent an isolated pulmonary commissurotomy. At the last follow-up, the distribution of the patients in NYHA
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Heart Association (NYHA) class II or III functional status. The following Kaplan-Meier curves of freedom from adverse event that might be related to right ventricular dilatation were calculated: (1) freedom from cardiac death, (2) freedom from reoperation for symptomatic right ventricular dilatation, (3) freedom from reoperation for symptomatic right ventricular dilatation and cardiac death, and (4) freedom from NYHA class II or III status, from reoperation for right ventricular dilatation, and from cardiac death. Independent contributions to prognosis of operative techniques were then assessed using Cox regressions. All tests were two-tailed and a p value of less than 0.05 was considered to be significant. Fig 1. Freedom from reoperation for right ventricular dilatation. Dashed lines indicate isolated pulmonary commissurotomy; dotted lines indicate tetralogy of Fallot repair with direct closure; solid lines indicate tetralogy of Fallot repair with right ventricular patch.
functional classes I, II, and III were respectively 73%, 24%, and 3% for the tetralogy of Fallot patients and 82%, 15%, and 3% for those who had undergone an isolated pulmonary commissurotomy.
Survival Analysis The 30-year actuarial survival was 86% ⫾ 5% for the tetralogy of Fallot patients and 93% ⫾ 5% for the pulmonary commissurotomy patients. Although there were no significant differences in freedom from cardiac death, none of the pulmonary commissurotomy patients experienced cardiac death, whereas the 30-year freedom from cardiac death was 92% ⫾ 4% for the tetralogy of Fallot patients (p ⫽ 0.11). Freedom from cardiac death was not significantly different among the various surgical techniques for correction of tetralogy of Fallot. The heart transplantation and the 20 valvular operations on the right ventricular outflow tract were considered as reoperations for symptomatic right ventricular dilatation. In Fallot patients, the 30-year freedom from reoperation was 68% ⫾ 8% and the 30-year freedom from cardiac death and reoperation was 64% ⫾ 8%. The freedom from adverse events related to right ventricular dilatation for the various surgical techniques is illustrated in Figures 1 to 3, and 15- and 25-year values are reported in Table 2. There were no differences in the late occurrence of these events among tetralogy of Fallot patients with limited right ventricular or a transannular patching (log-rank p ⬎ 0.21). Patients undergoing direct closure of a right ventriculotomy had fewer events than did patients with a patch (log-rank p ⬍ 0.02).
Echocardiographic Data Echocardiographic studies were obtained for 26 isolated commissurotomy patients and 119 tetralogy of Fallot patients. In 14 of the 20 patients who underwent reoperation for symptomatic right ventricular dilatation, the last examination before reoperation was taken into consideration. Echocardiographic data are summarized in
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Comment
CARDIOVASCULAR Fig 2. Freedom from cardiac death and reoperation for right ventricular dilatation. Dashed lines indicate isolated pulmonary commissurotomy; dotted lines indicate tetralogy of Fallot repair with direct closure; solid lines indicate tetralogy of Fallot repair with right ventricular patch.
Table 3. Patients with an isolated pulmonary commissurotomy as well as tetralogy of Fallot patients who had right ventricular patching (transannular or otherwise) had similar amounts of of moderate and severe pulmonary regurgitation (p ⬎ 0.2). Tetralogy of Fallot patients with a direct closure of their right ventricle had a smaller proportion of moderate and severe pulmonary regurgitation than did patients with commissurotomy (p ⫽ 0.09), limited right ventricular patching (p ⫽ 0.09), and transannular patching (p ⬍ 0.001). Right ventricular sizes appeared to be larger in patients with a transannular patch than in those with direct closure of a right ventriculotomy or an isolated commissurotomy (p ⱕ 0.01), but the differences in right ventricular size among those who had a patch closure of a right ventriculotomy did not reach statistical significance (p ⫽ 0.07). There were no differences between the right ventricular dimensions of the patients with an isolated pulmonary commissurotomy and the tetralogy of Fallot patients with either a direct closure of a right ventricular patch or a patch closure of an incision limited to the right ventricle (p ⬎ 0.2). None of the patients with an isolated pulmonary commissurotomy had a significant residual gradient. One patient had a transpulmonary gradient of 35 mm Hg and the remaining patients had gradients of less than 15 mm Hg. Only 3 commmissurotomy patients showed a restrictive physiology.
We are only starting to appreciate the extent of the problem posed by right ventricular dilatation occurring after surgical correction of tetralogy of Fallot. After 30 years, this dilatation was responsible for either death or reoperation in as many as 35% of patients in this study. Until a few years ago, our team believed that we could limit the magnitude of the problem if our surgeons did not extend their incisions and patching through the pulmonary annulus. This policy has revealed itself to be ineffective. In our hands, patients who had transannular patching or patching limited to the right ventricle had the same outcome. Given that, in our patients, the policy of not patching the pulmonary annulus appeared to have no positive consequences on the risk of long-term right ventricular dilatation, we raised the hypothesis that pulmonary infundibular contractility might play a key role in protection of the right ventricle against deleterious consequences of the chronic volume overload related to pulmonary insufficiency [4]. To ascertain the validity of this hypothesis, we needed a clinical study. Randomized prospective trials would be impractical, because results can only be obtained after more than two decades. We wanted to compare our tetralogy of Fallot patients to patients with isolated pulmonary insufficiency, and believed that patients who had undergone operation for isolated pulmonary stenosis were the ideal group. Follow-up studies of balloon dilatation of pulmonary valve stenosis have shown that after a median of 8 years, more than 85% of patients experience some degree of pulmonary regurgitation, and that the amount of pulmonary regurgitation seems to be worse in patients undergoing a surgical pulmonary commissurotomy [6 – 8]. Although we could not get echocardiographic examinations in every patient, the examinations performed reassure us that these patients experienced significant pulmonary regurgitation. The severity of pulmonary regurgitation seemed similar to that in the patients who had tetralogy Fallot
Electrocardiographic Studies None of the patients who had an isolated pulmonary commissurotomy developed bundle branch block. Their mean QRS duration was 87 ⫾ 11 milliseconds. The longest QRS measured was 100 milliseconds, even in the 5 patients who had a ratio between the end-diastolic dimensions of the right and the left ventricle of more than 0.7.
Fig 3. Freedom from all adverse events related to right ventricular dilatation. Dashed lines indicate isolated pulmonary commissurotomy; dotted lines indicate tetralogy of Fallot repair with direct closure; solid lines indicate tetralogy of Fallot repair with right ventricular patch.
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Freedom From Cardiac Death or Reoperation
Freedom from Reoperation Characteristic (1) Isolated pulmonary commissurotomy (2) Tetralogy of Fallot: direct RV closure (3) Tetralogy of Fallot: limited RV patching (4) Tetralogy of Fallot: transannular patching Log-rank p value (1) vs (2) (1) vs (3) (1) vs (4) NYHA ⫽ New York Heart Association;
Freedom From Cardiac Death, Reoperation or NYHA Class II or Greater
15 y (%)
25 y (%)
15 y (%)
25 y (%)
15 y (%)
100 100 97 ⫾ 3 95 ⫾ 2
100 98 ⫾ 2 87 ⫾ 7 81 ⫾ 6
100 94 ⫾ 3 97 ⫾ 3 90 ⫾ 3
100 92 ⫾ 4 87 ⫾ 7 75 ⫾ 6
100 92 ⫾ 4 97 ⫾ 3 85 ⫾ 4
0.19 ⬍0.001 ⬍0.001
0.047 ⬍0.001 ⬍0.001
25 y (%) 87 79 65 40
⫾ ⫾ ⫾ ⫾
6 6 10 7
0.02 ⬍0.001 ⬍0.001
RV ⫽ right ventricle.
repair with a patch limited to the right ventricle, and were slightly less significant than in the tetralogy of Fallot patients with a transannular repair. Patients who have undergone a pulmonary balloon valvuloplasty have signs of right ventricular overload with enlarged right ventricles; however, it is not yet known whether this will continue long term, as in patients with repair of tetralogy of Fallot [12]. An excellent rate of survival has been demonstrated in patients undergoing surgical pulmonary valvotomy, but the late consequences of the created pulmonary insufficiency have not yet been determined [13]. Our results showed that after two decades, if the ventricles of these patients appear to be slightly enlarged, this seems to bear no clinical consequences. The outcome of tetralogy of Fallot patients is by far worse. Interestingly, the outcome of patients with a transannular patch, who had more pulmonary regurgitation and larger right ventricles than did other patients, was similar to the outcome of patients treated with a limited right ventricular patch. It is noteworthy that patients who had an isolated pulmonary commissurotomy did not have increased QRS length, which would confirm that in tetralogy of Fallot, the right bundle branch block is caused by damage created to the muscular bundles of the pulmonary infundibulum [14].
Limitations of the Study Obviously, tetralogy of Fallot is a much more severe disease than isolated pulmonary stenosis. The anatomy of the outflow tract of these patients is different and, if they experience right ventricular outflow tract obstruction before operation, the hearts of patients with tetralogy of Fallot are subjected to long-term cyanosis. In tetralogy of Fallot patients there seem to be additional factors promoting right ventricular dilatation. Hypoplastic or stenotic pulmonary arteries, even if present in a limited number of cases, contribute to right ventricular dilatation by increasing afterload. Nonetheless, by far the most important recognized factor is pulmonary insufficiency. By comparing these two patients groups, we believed that we could identify whether ventricular damage contributed to ventricular dilatation in tetralogy of Fallot patients, even if a few patients may have had unnoticed hypoplastic or stenotic pulmonary arteries. If there is no doubt that surgical valvotomy of a congenital pulmonary stenosis will often create some degree of pulmonary insufficiency, its importance is difficult to appreciate solely on the basis of echocardiographic examination. Magnetic resonance imaging studies, which are more suitable for quantifying pulmonary regurgitation, are not available at our institution. Despite these limitations, there is such a striking dif-
Table 3. Echocardiographic Characteristics
Pulmonary Regurgitation Trivial Moderate Severe RV/LV end-diastolic diameter LV ⫽ left ventricle;
RV ⫽ right ventricle.
Isolated Pulmonary Commissurotomy
Tetralogy of Fallot: Direct Closure RV
Tetralogy of Fallot: Limited RV Patch
Tetralogy of Fallot: Transannular Patch
27% 45% 27% 0.56 ⫾ 0.14
52% 39% 9% 0.61 ⫾ 0.17
27% 41% 31% 0.64 ⫾ 0.27
16% 42% 42% 0.75 ⫾ 0.25
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Table 2. Freedom From Adverse Events Related to Right Ventricular Dilatation
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ference between the clinical outcome of tetralogy of Fallot patients and those who have undergone operation for an isolated pulmonary stenosis that we are reassured that pulmonary infundibulum plays an active role in protecting the right ventricle against the deleterious consequences of chronic pulmonary regurgitation. Shimazaki and colleagues [15] have proposed, on the basis of a meta-analysis of patients with the extremely rare condition of a congenitally absent pulmonary valve, that symptoms related to pulmonary regurgitation alone may take up to three to four decades to appear. It is difficult to predict whether patients who had undergone a pulmonary commissurotomy will someday become symptomatic; however, our study shows that in the time frame in which up to one third of patients who have undergone repair of tetralogy of Fallot experience serious complications, none of them seem to develop right ventricular dilatation. We therefore suspect that the damage created to the right ventricular outflow tract during tetralogy of Fallot repair plays a major role in the development of right ventricular dilatation in these patients. This difference might be explained by the very peculiar role played by the pulmonary infundibular area in right ventricular function. Previous investigators thought that the outlet portion of the right ventricle had only a passive role in right ventricular contraction, carrying the blood from the trabecular portion of the right ventricle to the pulmonary artery and, as such, had to be as large as possible. Right ventricular contraction is a peristaltic movement, and this peristaltic mode of function may be crucial to achieving a complete emptying of the right ventricular cavity. Studies in animals have shown that the right ventricular contraction begins at the base of the heart and progress as a wave toward the pulmonary annulus. As the pulmonary infundibulum receives blood thrusted during this initial part of the contraction, it is not only relaxed but is also subjected to an outward bulge [16 –20]. Only 50 ms after the beginning of the contraction will the infundibulum start contracting, thereby evacuating the accumulated blood [20]. It will then remained squeezed as a sphincter until late in the diastolic phase. This peristaltic motion of the right ventricle is demonstrated by the progression of a pressure wave from the trabecular to the outlet portion of the right ventricle in experiments recording simultaneously the pressures in different positions of the right ventricle [18]. It had been known for years that the pulmonary valve remains open very late with forward flow still occurring while the trabecular portion of the right ventricle is already relaxing [21, 22]. The paradox of having a continuous flow at the valvar level during the beginning of the relaxation of the right ventricle has been explained by both the extremely high compliance of the pulmonary arterial system and the high kinetic energy transmitted to the bolus of blood ejected, the authors describing the initial right ventricular contraction as very powerful [21, 22]. We do believe that the delayed opening of the pulmonary valve might be more suitably explained by the peristaltic mode of function of the right ventricle than by its intrinsic power, the pulmonary infundibulum ejecting the blood
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that it had accumulated at a time when the rest of the right ventricle was already relaxing. The role of the pulmonary infundibulum might not be limited to its systolic function. The fact that it remains contracted until late in diastole is probably essential to maintaining pulmonary valve competence. The pulmonary valve has the peculiarity of being inserted inside the inner shell of an exclusively muscular cylinder. The contraction of this cylinder inevitably approximates the pulmonary cusps to each other and increases their coaptation length. Brock [23] previously demonstrated that the pulmonary pressure that the pulmonary valve could withstand without leaking was greater when the pulmonary infundibulum was stimulated by adrenergic stimulation. It is obvious that tetralogy of Fallot patients with a greater extent of disease will require greater enlargement of the annular area and will be more susceptible to developing late right ventricular dilatation. However, if the pulmonary infundibulum is not the passive conduit that it was once thought to be and instead takes an active part in the right ventricular contraction and in pulmonary valve function, then operations should be designed to aim at its preservation. In transatrial as in transventricular repair, the annular area often need a patch enlargement; however, in transatrial repair, the incision starts from the pulmonary artery rather than from the midventricle, such as in the transventricular approach [24, 25]. Even though transatrial approach necessitates wide resection of the inner muscular features of the pulmonary infundibulum, one can hope that this approach may better preserve the contractile function of the subpulmonary area. In conclusion, the striking difference observed in the follow-up of patients with transventricular repair of tetralogy of Fallot and those with an isolated pulmonary commissurotomy lead us to think that pulmonary insufficiency may not be the leading factor causing right ventricular dilatation after a tetralogy of Fallot repair. Long-term pulmonary regurgitation is responsible for a slight degree of right ventricular enlargement, but provided that patients have normal pulmonary arteries and pulmonary infundibulum, symptoms may never develop. The pulmonary infundibulum may be essential to complete right ventricular ejection and to maintaining pulmonary valve competence. Operations should be designed to preserve its contractility.
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INVITED COMMENTARY This paper provides us with a true long-term follow-up of a troublesome cohort of patients. The point the authors want to make is that the infundibulum plays a more active role for right ventricular function than commonly thought. In the current era, where there is a considerable trend to avoid right ventricular incisions, these are important data. It is obvious that the authors are strongly in favor of a “transatrial-transpulmonary” surgical approach for the repair of tetralogy of Fallot and would like to support their attitude with the data collected for this manuscript. The major point of criticism is probably the comparison of two different pathological entities, one of which by definition has a malformed infundibulum, the area under investigation. Obviously, the authors have some experience as fruiterers, for they make their apples almost look like oranges. Suffice it to say that there seems to be more to the infundibulum than currently meets the eye, and that the authors have succeeded in expanding our awareness of that finding. One must, however, bear in mind that the pathology of tetralogy of Fallot varies considerably and that there will always be patients in whom transannular enlargement will be essential. The surgical community is, yet again, facing the problem of inconsistent (or inappropriate) use of terminology. If, for instance, in a symptomatic four-
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Inc
week old infant, an incision starting in the main pulmonary artery is carried across a severely hypoplastic pulmonary valve ring and into the RVOT (right ventricular outflow tract) for a limited distance, when, at the same time, VSD (ventricular septal defect) closure and transection of RV (right ventricle) muscle bands have been performed through the tricuspid valve, this, semantically and anatomically, should be called a “transannular” repair. This does definitely not make it a classical “transventricular” repair. Many surgeons, however, would probably call it a “transatrial-transpulmonary” repair, either unintentionally or because this is what one has to do today. The extremely interesting and valuable results the authors were able to show should serve as one more incentive to continue to investigate the enigma of the right ventricle in health and in disease. It must, however, not be abused to promote techniques which are still evolving. Markus K. Heinemann, MD, PhD Department of Pediatric Cardiac Surgery Mainz University Hospital Langenbeckstr 1, # 505 55131 Mainz, Germany e-mail: [email protected]
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Background. The aim of this study was to determine the relative role of pulmonary insufficiency and right ventricular outflow tract damage in the genesis of late symptoms related to right ventricular dilatation. Methods. In a retrospective study we compared the late outcomes of patients who had undergone operations known to generate pulmonary insufficiency, namely, transventricular repair of tetralogy of Fallot and pulmonary commissurotomy for isolated pulmonary stenosis. Results. In our institution, between 1964 and 1984, a total of 44 patients were found to have had an isolated pulmonary commissurotomy and 189 survived a transventricular repair of tetralogy of Fallot. Of these patients, 134 had patching of the right ventricle and 55 direct closure of a right ventriculotomy. Follow-up was 94% complete after a mean of 22 ⴞ 7 years. On echocardiography, patients with isolated commissurotomy had similar degrees of moderate and severe pulmonary insufficiency as tetralogy of Fallot patients who had a right
ventricular patch (p > 0.2). However, freedom from adverse events related to right ventricular dilatation was far better (log rank p < 0.001) in patients with isolated commisurotomy. Conclusions. Pulmonary insufficiency is not the only determinant of late symptomatic right ventricular dilatation after repair of tetralogy of Fallot. Pulmonary insufficiency seems much more deleterious in patients who have had right ventricular outflow tract patching. Longterm pulmonary insufficiency alone is responsible for a slight degree of right ventricular dilatation, but symptoms may develop much later if the contractility of the pulmonary infundibulum is preserved. The pulmonary infundibulum may be essential for right ventricular ejection, and for maintaining pulmonary valve competence.
A
ciency as did patients who had undergone operation with a transannular patch. A recent magnetic resonance imaging study performed on 85 adult patients who had undergone operation for tetralogy of Fallot confirmed that right ventricular volumes and pulmonary regurgitant volumes were equal regardless of whether the pulmonary annulus had initially been spared [5]. In that study, the predictive factors of right ventricular dilatation were not only the presence of pulmonary insufficiency, but also the identification of an akinetic or dyskinetic area in the right ventricular outflow tract. Therefore, we suspected that right ventricular outflow tract damage may play an important role in the late genesis of ventricular dilatation. We wanted to investigate this hypothesis in a clinical model. A randomized prospective study would be impractical because the results would be apparent only about 20 years after the repair. Therefore we decided to
lthough surgical correction of tetralogy of Fallot offers a favorable long-term outcome, an increasing proportion of patients with this condition experience the deleterious consequences of progressive right ventricular dilatation: sudden death, congestive heart failure, or decreased exercise capacity [1–3]. For many years, longterm pulmonary insufficiency related to transannular patching has been incriminated as the main determinant leading to late right ventricular dilatation. In a recent follow-up study, we demonstrated that attempts to preserve pulmonary valve competence at operation by limiting the patching to the ventricular area below the pulmonary valve did not protect patients from the late deleterious consequences of right ventricular dilatation [4]. Twenty-five years after this repair, these patients had extremely similar outcomes, including the same degree of right ventricular dilatation and pulmonary insuffi-
(Ann Thorac Surg 2003;76:555– 61) © 2003 by The Society of Thoracic Surgeons
Accepted for publication Feb 21, 2003. Address reprint requests to Dr d’Udekem d’Acoz, Service de Chirurgie Cardiovasculaire et Thoracique, Cliniques Universitaires Saint-Luc— Avenue Hippocrate 10, B-1200 Brussels, Belgium; e-mail: dudekem@ chir.ucl.ac.be.
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Inc
This article has been selected for the open discussion forum on the CTSNet Web site: http://www.ctsnet.org/discuss
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Does Right Ventricular Outflow Tract Damage Play a Role in the Genesis of Late Right Ventricular Dilatation After Tetralogy of Fallot Repair?
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Table 1. Patient Characteristics Characteristic CARDIOVASCULAR
Patients, n Age at operation (y) Previous palliation, n (%) Pulm commissurotomy, n (%) Fallot ⫽ tetralogy of Fallot;
Isolated Pulmonary Commissurotomy
Fallot: Direct Closure RV
Fallot: Limited RV Patch
Fallot: Transannular Patch
44 6.7 (0.3– 4) 0 44 (100)
55 7 (0.5–25) 18 (33) 31 (56)
35 4 (0.3– 45) 8 (23) 24 (69)
99 3.3 (0.6 –27) 32 (32) 99 (100)
Pulm ⫽ pulmonary;
RV ⫽ right ventricular.
perform a retrospective study in patients with pulmonary regurgitation for a similar period to compare their outcomes with those of patients who had undergone operation for tetralogy of Fallot. We identified patients who had had operations for an isolated pulmonary commissurotomy as the ideal candidates, inasmuch as this operation is known to create valvar insufficiency [6 – 8].
Patients and Methods The study design was approved by the hospital ethics committee before any investigation.
Study Groups Between 1964 and 1984, a total of 152 patients underwent a pulmonary commissurotomy for isolated pulmonary stenosis at our institution. After 1984, this procedure was almost exclusively performed by interventional catheterization and the surgical procedure was virtually abandoned. Of the patients who underwent operation, 44 who had no concomitant resection or incision of muscular bundles of their right ventricular outflow tract and no associated cardiac defects constitute the study group. Their operative data were reviewed and they all were contacted and offered a follow-up consultation with 12lead ECG and transthoracic echocardiography. If they were unwilling to return to our hospital, they were asked questions about their functional status. Follow-up was completed between June and November 2000. During the same period, we updated the follow-up of all the 189 consecutive hospital survivors of a transventricular repair of tetralogy of Fallot operated between 1964 and 1984 in our institution. We excluded patients who had atrio-ventricular septal defect or pulmonary atresia as well as those who needed a right ventricular outflow tract conduit at the time of the repair.
Surgical Procedures In all, 58 of the tetralogy of Fallot patients and none of the pulmonary commissurotomy patients had a systemicopulmonary shunt as a palliative procedure before the operation. All ventricular septal defects in patients with tetralogy of Fallot were closed through a right ventriculotomy. Relief of the right ventricular outflow tract obstruction was obtained by widely resecting all septoparietal and parieto-parietal muscle bundles of the pulmonary infundibulum. If the pulmonary annulus itself seemed narrowed, the incision extended through the pulmonary annulus up to the main pulmonary artery and
the whole area was patched. If the right ventricular outflow tract seemed wide enough, the ventriculotomy was closed directly. If the surgeon believed that direct closure of the ventriculotomy would compromise the size of the pulmonary infundibulum, this incision was closed with a patch. Characteristics of the patients are displayed in Table 1. Their age at operation was not significantly different among the various patients groups except in patients undergoing a transannular patch repair, who were younger than the others (p ⬍ 0.03). Of the isolated pulmonary commissurotomy patients, 20 underwent operation under caval occlusion and 24 under cardiopulmonary bypass. The main pulmonary artery was opened with a longitudinal incision and under direct vision, the commissures were separated with a blade, and redundant dysplastic tissue was excised. After completion of the pulmonary commissurotomy, the arteriotomy was closed directly without patch interposition.
Electrocardiographic and Echocardiographic Studies In all ECG collected from the patients with isolated pulmonary commissurotomies, QRS duration was measured manually and defined as the maximal QRS duration over all leads. On echocardiographic examination, pulmonary insufficiency was described as mild if the regurgitant jet started at the valve, moderate if it started in the main pulmonary artery, and severe if it started in the pulmonary artery branches. End-diastolic dimensions of both ventricles were measured by M-mode echocardiography performed on parasternal short-axis views obtained just below the level of the tips of the mitral valve leaflets [9]. Restrictive physiology was defined as the presence of a forward flow in the main pulmonary artery during atrial systole independently of the breathing cycle [10].
Statistical Analysis Data are reported as means ⫾ standard deviations or as percentages. Groups were compared using 2 tests for dichotomous variables and Student’s t tests for continuous variables. Survival curves were estimated using the product-limit method described by Kaplan and Meier, and standard errors were computed using the Rothman method [11]. Different adverse long-term outcomes related to progressive right ventricular dilatation were investigated: (1) cardiac death, defined as sudden unexpected death or death related to heart failure; (2) reoperation for symptomatic right ventricular dilatation; and (3) New York
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Results Follow-Up There were no operative deaths among the patients who had an isolated pulmonary commissurotomy. Follow-up was 95% complete for the tetralogy of Fallot patients and 91% for those with an isolated pulmonary commissurotomy. Mean follow-up was 22.4 ⫾ 6.9 years. Because they believed that there was no need for follow-up, only 13 of the 44 patients who had undergone a pulmonary commissurotomy had been reviewed by a cardiologist in the 5 years preceding our contact and follow-up investigation.
Late Outcome In all, 16 of the tetralogy of Fallot patients who had undergone repair had died during the follow-up period. Of these cases, 10 were considered as cardiac deaths (7 cases of sudden unexpected deaths and 3 of congestive heart failure). The other patients died of unrelated causes (2 of trauma from motor vehicle accidents, 1 of chronic glomerulonephritis, 1 of chronic viral hepatitis, 1 after a reoperation for tracheal stenosis, and 1 in septic shock related to a GI tract infection). There were no cardiac deaths among the patients who were operated for isolated pulmonary stenosis; 1 patient died of trauma from a motor vehicle accident and 1 of a chest chondrosarcoma. In all, 28 tetralogy of Fallot patients had a cardiac reoperation after a mean of 15.9 ⫾ 8.7 years. One patient underwent a heart transplantation, 6 patients had a reoperation for residual or associated cardiac lesions (2 residual ventricular septal defects, 1 partial anomalous pulmonary venous return, 1 closure of a giant aortopulmonary collateral, and 2 aortic valve replacements), 1 patient had open heart cryoablation, and 20 patients had pulmonary valve replacement in their right ventricular outflow tract with a homograft (1 for a mixed regurgitation and stenosis, and the remaining for severe pulmonary regurgitation and symptomatic right ventricular dilatation. All patients who underwent a valvulation of their outflow tract underwent a preoperative catheterization to rule out pulmonary artery stenosis on hypoplasia. There were no reoperations among patients who underwent an isolated pulmonary commissurotomy. At the last follow-up, the distribution of the patients in NYHA
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Heart Association (NYHA) class II or III functional status. The following Kaplan-Meier curves of freedom from adverse event that might be related to right ventricular dilatation were calculated: (1) freedom from cardiac death, (2) freedom from reoperation for symptomatic right ventricular dilatation, (3) freedom from reoperation for symptomatic right ventricular dilatation and cardiac death, and (4) freedom from NYHA class II or III status, from reoperation for right ventricular dilatation, and from cardiac death. Independent contributions to prognosis of operative techniques were then assessed using Cox regressions. All tests were two-tailed and a p value of less than 0.05 was considered to be significant. Fig 1. Freedom from reoperation for right ventricular dilatation. Dashed lines indicate isolated pulmonary commissurotomy; dotted lines indicate tetralogy of Fallot repair with direct closure; solid lines indicate tetralogy of Fallot repair with right ventricular patch.
functional classes I, II, and III were respectively 73%, 24%, and 3% for the tetralogy of Fallot patients and 82%, 15%, and 3% for those who had undergone an isolated pulmonary commissurotomy.
Survival Analysis The 30-year actuarial survival was 86% ⫾ 5% for the tetralogy of Fallot patients and 93% ⫾ 5% for the pulmonary commissurotomy patients. Although there were no significant differences in freedom from cardiac death, none of the pulmonary commissurotomy patients experienced cardiac death, whereas the 30-year freedom from cardiac death was 92% ⫾ 4% for the tetralogy of Fallot patients (p ⫽ 0.11). Freedom from cardiac death was not significantly different among the various surgical techniques for correction of tetralogy of Fallot. The heart transplantation and the 20 valvular operations on the right ventricular outflow tract were considered as reoperations for symptomatic right ventricular dilatation. In Fallot patients, the 30-year freedom from reoperation was 68% ⫾ 8% and the 30-year freedom from cardiac death and reoperation was 64% ⫾ 8%. The freedom from adverse events related to right ventricular dilatation for the various surgical techniques is illustrated in Figures 1 to 3, and 15- and 25-year values are reported in Table 2. There were no differences in the late occurrence of these events among tetralogy of Fallot patients with limited right ventricular or a transannular patching (log-rank p ⬎ 0.21). Patients undergoing direct closure of a right ventriculotomy had fewer events than did patients with a patch (log-rank p ⬍ 0.02).
Echocardiographic Data Echocardiographic studies were obtained for 26 isolated commissurotomy patients and 119 tetralogy of Fallot patients. In 14 of the 20 patients who underwent reoperation for symptomatic right ventricular dilatation, the last examination before reoperation was taken into consideration. Echocardiographic data are summarized in
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Comment
CARDIOVASCULAR Fig 2. Freedom from cardiac death and reoperation for right ventricular dilatation. Dashed lines indicate isolated pulmonary commissurotomy; dotted lines indicate tetralogy of Fallot repair with direct closure; solid lines indicate tetralogy of Fallot repair with right ventricular patch.
Table 3. Patients with an isolated pulmonary commissurotomy as well as tetralogy of Fallot patients who had right ventricular patching (transannular or otherwise) had similar amounts of of moderate and severe pulmonary regurgitation (p ⬎ 0.2). Tetralogy of Fallot patients with a direct closure of their right ventricle had a smaller proportion of moderate and severe pulmonary regurgitation than did patients with commissurotomy (p ⫽ 0.09), limited right ventricular patching (p ⫽ 0.09), and transannular patching (p ⬍ 0.001). Right ventricular sizes appeared to be larger in patients with a transannular patch than in those with direct closure of a right ventriculotomy or an isolated commissurotomy (p ⱕ 0.01), but the differences in right ventricular size among those who had a patch closure of a right ventriculotomy did not reach statistical significance (p ⫽ 0.07). There were no differences between the right ventricular dimensions of the patients with an isolated pulmonary commissurotomy and the tetralogy of Fallot patients with either a direct closure of a right ventricular patch or a patch closure of an incision limited to the right ventricle (p ⬎ 0.2). None of the patients with an isolated pulmonary commissurotomy had a significant residual gradient. One patient had a transpulmonary gradient of 35 mm Hg and the remaining patients had gradients of less than 15 mm Hg. Only 3 commmissurotomy patients showed a restrictive physiology.
We are only starting to appreciate the extent of the problem posed by right ventricular dilatation occurring after surgical correction of tetralogy of Fallot. After 30 years, this dilatation was responsible for either death or reoperation in as many as 35% of patients in this study. Until a few years ago, our team believed that we could limit the magnitude of the problem if our surgeons did not extend their incisions and patching through the pulmonary annulus. This policy has revealed itself to be ineffective. In our hands, patients who had transannular patching or patching limited to the right ventricle had the same outcome. Given that, in our patients, the policy of not patching the pulmonary annulus appeared to have no positive consequences on the risk of long-term right ventricular dilatation, we raised the hypothesis that pulmonary infundibular contractility might play a key role in protection of the right ventricle against deleterious consequences of the chronic volume overload related to pulmonary insufficiency [4]. To ascertain the validity of this hypothesis, we needed a clinical study. Randomized prospective trials would be impractical, because results can only be obtained after more than two decades. We wanted to compare our tetralogy of Fallot patients to patients with isolated pulmonary insufficiency, and believed that patients who had undergone operation for isolated pulmonary stenosis were the ideal group. Follow-up studies of balloon dilatation of pulmonary valve stenosis have shown that after a median of 8 years, more than 85% of patients experience some degree of pulmonary regurgitation, and that the amount of pulmonary regurgitation seems to be worse in patients undergoing a surgical pulmonary commissurotomy [6 – 8]. Although we could not get echocardiographic examinations in every patient, the examinations performed reassure us that these patients experienced significant pulmonary regurgitation. The severity of pulmonary regurgitation seemed similar to that in the patients who had tetralogy Fallot
Electrocardiographic Studies None of the patients who had an isolated pulmonary commissurotomy developed bundle branch block. Their mean QRS duration was 87 ⫾ 11 milliseconds. The longest QRS measured was 100 milliseconds, even in the 5 patients who had a ratio between the end-diastolic dimensions of the right and the left ventricle of more than 0.7.
Fig 3. Freedom from all adverse events related to right ventricular dilatation. Dashed lines indicate isolated pulmonary commissurotomy; dotted lines indicate tetralogy of Fallot repair with direct closure; solid lines indicate tetralogy of Fallot repair with right ventricular patch.
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Freedom From Cardiac Death or Reoperation
Freedom from Reoperation Characteristic (1) Isolated pulmonary commissurotomy (2) Tetralogy of Fallot: direct RV closure (3) Tetralogy of Fallot: limited RV patching (4) Tetralogy of Fallot: transannular patching Log-rank p value (1) vs (2) (1) vs (3) (1) vs (4) NYHA ⫽ New York Heart Association;
Freedom From Cardiac Death, Reoperation or NYHA Class II or Greater
15 y (%)
25 y (%)
15 y (%)
25 y (%)
15 y (%)
100 100 97 ⫾ 3 95 ⫾ 2
100 98 ⫾ 2 87 ⫾ 7 81 ⫾ 6
100 94 ⫾ 3 97 ⫾ 3 90 ⫾ 3
100 92 ⫾ 4 87 ⫾ 7 75 ⫾ 6
100 92 ⫾ 4 97 ⫾ 3 85 ⫾ 4
0.19 ⬍0.001 ⬍0.001
0.047 ⬍0.001 ⬍0.001
25 y (%) 87 79 65 40
⫾ ⫾ ⫾ ⫾
6 6 10 7
0.02 ⬍0.001 ⬍0.001
RV ⫽ right ventricle.
repair with a patch limited to the right ventricle, and were slightly less significant than in the tetralogy of Fallot patients with a transannular repair. Patients who have undergone a pulmonary balloon valvuloplasty have signs of right ventricular overload with enlarged right ventricles; however, it is not yet known whether this will continue long term, as in patients with repair of tetralogy of Fallot [12]. An excellent rate of survival has been demonstrated in patients undergoing surgical pulmonary valvotomy, but the late consequences of the created pulmonary insufficiency have not yet been determined [13]. Our results showed that after two decades, if the ventricles of these patients appear to be slightly enlarged, this seems to bear no clinical consequences. The outcome of tetralogy of Fallot patients is by far worse. Interestingly, the outcome of patients with a transannular patch, who had more pulmonary regurgitation and larger right ventricles than did other patients, was similar to the outcome of patients treated with a limited right ventricular patch. It is noteworthy that patients who had an isolated pulmonary commissurotomy did not have increased QRS length, which would confirm that in tetralogy of Fallot, the right bundle branch block is caused by damage created to the muscular bundles of the pulmonary infundibulum [14].
Limitations of the Study Obviously, tetralogy of Fallot is a much more severe disease than isolated pulmonary stenosis. The anatomy of the outflow tract of these patients is different and, if they experience right ventricular outflow tract obstruction before operation, the hearts of patients with tetralogy of Fallot are subjected to long-term cyanosis. In tetralogy of Fallot patients there seem to be additional factors promoting right ventricular dilatation. Hypoplastic or stenotic pulmonary arteries, even if present in a limited number of cases, contribute to right ventricular dilatation by increasing afterload. Nonetheless, by far the most important recognized factor is pulmonary insufficiency. By comparing these two patients groups, we believed that we could identify whether ventricular damage contributed to ventricular dilatation in tetralogy of Fallot patients, even if a few patients may have had unnoticed hypoplastic or stenotic pulmonary arteries. If there is no doubt that surgical valvotomy of a congenital pulmonary stenosis will often create some degree of pulmonary insufficiency, its importance is difficult to appreciate solely on the basis of echocardiographic examination. Magnetic resonance imaging studies, which are more suitable for quantifying pulmonary regurgitation, are not available at our institution. Despite these limitations, there is such a striking dif-
Table 3. Echocardiographic Characteristics
Pulmonary Regurgitation Trivial Moderate Severe RV/LV end-diastolic diameter LV ⫽ left ventricle;
RV ⫽ right ventricle.
Isolated Pulmonary Commissurotomy
Tetralogy of Fallot: Direct Closure RV
Tetralogy of Fallot: Limited RV Patch
Tetralogy of Fallot: Transannular Patch
27% 45% 27% 0.56 ⫾ 0.14
52% 39% 9% 0.61 ⫾ 0.17
27% 41% 31% 0.64 ⫾ 0.27
16% 42% 42% 0.75 ⫾ 0.25
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Table 2. Freedom From Adverse Events Related to Right Ventricular Dilatation
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ference between the clinical outcome of tetralogy of Fallot patients and those who have undergone operation for an isolated pulmonary stenosis that we are reassured that pulmonary infundibulum plays an active role in protecting the right ventricle against the deleterious consequences of chronic pulmonary regurgitation. Shimazaki and colleagues [15] have proposed, on the basis of a meta-analysis of patients with the extremely rare condition of a congenitally absent pulmonary valve, that symptoms related to pulmonary regurgitation alone may take up to three to four decades to appear. It is difficult to predict whether patients who had undergone a pulmonary commissurotomy will someday become symptomatic; however, our study shows that in the time frame in which up to one third of patients who have undergone repair of tetralogy of Fallot experience serious complications, none of them seem to develop right ventricular dilatation. We therefore suspect that the damage created to the right ventricular outflow tract during tetralogy of Fallot repair plays a major role in the development of right ventricular dilatation in these patients. This difference might be explained by the very peculiar role played by the pulmonary infundibular area in right ventricular function. Previous investigators thought that the outlet portion of the right ventricle had only a passive role in right ventricular contraction, carrying the blood from the trabecular portion of the right ventricle to the pulmonary artery and, as such, had to be as large as possible. Right ventricular contraction is a peristaltic movement, and this peristaltic mode of function may be crucial to achieving a complete emptying of the right ventricular cavity. Studies in animals have shown that the right ventricular contraction begins at the base of the heart and progress as a wave toward the pulmonary annulus. As the pulmonary infundibulum receives blood thrusted during this initial part of the contraction, it is not only relaxed but is also subjected to an outward bulge [16 –20]. Only 50 ms after the beginning of the contraction will the infundibulum start contracting, thereby evacuating the accumulated blood [20]. It will then remained squeezed as a sphincter until late in the diastolic phase. This peristaltic motion of the right ventricle is demonstrated by the progression of a pressure wave from the trabecular to the outlet portion of the right ventricle in experiments recording simultaneously the pressures in different positions of the right ventricle [18]. It had been known for years that the pulmonary valve remains open very late with forward flow still occurring while the trabecular portion of the right ventricle is already relaxing [21, 22]. The paradox of having a continuous flow at the valvar level during the beginning of the relaxation of the right ventricle has been explained by both the extremely high compliance of the pulmonary arterial system and the high kinetic energy transmitted to the bolus of blood ejected, the authors describing the initial right ventricular contraction as very powerful [21, 22]. We do believe that the delayed opening of the pulmonary valve might be more suitably explained by the peristaltic mode of function of the right ventricle than by its intrinsic power, the pulmonary infundibulum ejecting the blood
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that it had accumulated at a time when the rest of the right ventricle was already relaxing. The role of the pulmonary infundibulum might not be limited to its systolic function. The fact that it remains contracted until late in diastole is probably essential to maintaining pulmonary valve competence. The pulmonary valve has the peculiarity of being inserted inside the inner shell of an exclusively muscular cylinder. The contraction of this cylinder inevitably approximates the pulmonary cusps to each other and increases their coaptation length. Brock [23] previously demonstrated that the pulmonary pressure that the pulmonary valve could withstand without leaking was greater when the pulmonary infundibulum was stimulated by adrenergic stimulation. It is obvious that tetralogy of Fallot patients with a greater extent of disease will require greater enlargement of the annular area and will be more susceptible to developing late right ventricular dilatation. However, if the pulmonary infundibulum is not the passive conduit that it was once thought to be and instead takes an active part in the right ventricular contraction and in pulmonary valve function, then operations should be designed to aim at its preservation. In transatrial as in transventricular repair, the annular area often need a patch enlargement; however, in transatrial repair, the incision starts from the pulmonary artery rather than from the midventricle, such as in the transventricular approach [24, 25]. Even though transatrial approach necessitates wide resection of the inner muscular features of the pulmonary infundibulum, one can hope that this approach may better preserve the contractile function of the subpulmonary area. In conclusion, the striking difference observed in the follow-up of patients with transventricular repair of tetralogy of Fallot and those with an isolated pulmonary commissurotomy lead us to think that pulmonary insufficiency may not be the leading factor causing right ventricular dilatation after a tetralogy of Fallot repair. Long-term pulmonary regurgitation is responsible for a slight degree of right ventricular enlargement, but provided that patients have normal pulmonary arteries and pulmonary infundibulum, symptoms may never develop. The pulmonary infundibulum may be essential to complete right ventricular ejection and to maintaining pulmonary valve competence. Operations should be designed to preserve its contractility.
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4. d’Udekem Y, Ovaert C, Grandjean F, et al. Tetralogy of Fallot. Transannular and right ventricular patching equally affect late functional status. Circulation 2000;102(Suppl III): III-116 –22. 5. Davlouros PA, Kilner PJ, Hornung TS, et al. Right ventricular function in adults with repaired tetralogy of Fallot assessed with cardiovascular resonance imaging: detrimental role of right ventricular outflow aneurysms or akinesia and adverse right-to-left interaction. J Am Coll Cardiol 2002;40:2044 –52. 6. Rao PS, Galal O, Patnana M, Buck SH, Wilson AD. Results of three to 10-year follow-up of balloon dilatation of the pulmonary valve. Heart 1998;80:591–5. 7. O’Connor BK, Beekman RH, Lindauer A, Rocchini A. Intermediate-term outcome after pulmonary balloon valvuloplasty: comparison with a matched surgical control group. J Am Coll Cardiol 1992;20:169 –73. 8. Nugent EW, Freedom RM, Nora JJ, Ellison RC, Rowe RD, Nadas AS. Clinical course in pulmonary stenosis. Circulation 1977;56(Suppl I):I-38 –47. 9. Atallah-Yunes NH, Kavey REW, Bove EL, et al. Postoperative assessment of a modified surgical approach to repair of tetralogy of Fallot: long-term follow-up. Circulation 1996; 94(Suppl II):II-22–6. 10. Gatzoulis MA, Clark AL, Cullen S, Newman CGH, Redington AN. Right ventricular diastolic function 15 to 35 years after repair of tetralogy of Fallot. Circulation 1995;91:1775–81. 11. Borgan O, Liestol K. A note of confidence intervals and bands for the survival curve based on transformations. Scand J Stat 1990;17:35–41. 12. Masura J, Burch M, Deanfield JE, Sullivan ID. Five-year follow-up after balloon pulmonary valvuloplasty. J Am Coll Cardiol 1993;21:132–6. 13. Kopecky SL, Gersh BJ, McGoon MD, et al. Long-term outcome of patients undergoing surgical repair of isolated pulmonary valve stenosis. Circulation 1988;78:1150 –6. 14. Horowitz LN, Simson MB, Spear JF, et al. The mechanism of
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INVITED COMMENTARY This paper provides us with a true long-term follow-up of a troublesome cohort of patients. The point the authors want to make is that the infundibulum plays a more active role for right ventricular function than commonly thought. In the current era, where there is a considerable trend to avoid right ventricular incisions, these are important data. It is obvious that the authors are strongly in favor of a “transatrial-transpulmonary” surgical approach for the repair of tetralogy of Fallot and would like to support their attitude with the data collected for this manuscript. The major point of criticism is probably the comparison of two different pathological entities, one of which by definition has a malformed infundibulum, the area under investigation. Obviously, the authors have some experience as fruiterers, for they make their apples almost look like oranges. Suffice it to say that there seems to be more to the infundibulum than currently meets the eye, and that the authors have succeeded in expanding our awareness of that finding. One must, however, bear in mind that the pathology of tetralogy of Fallot varies considerably and that there will always be patients in whom transannular enlargement will be essential. The surgical community is, yet again, facing the problem of inconsistent (or inappropriate) use of terminology. If, for instance, in a symptomatic four-
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Inc
week old infant, an incision starting in the main pulmonary artery is carried across a severely hypoplastic pulmonary valve ring and into the RVOT (right ventricular outflow tract) for a limited distance, when, at the same time, VSD (ventricular septal defect) closure and transection of RV (right ventricle) muscle bands have been performed through the tricuspid valve, this, semantically and anatomically, should be called a “transannular” repair. This does definitely not make it a classical “transventricular” repair. Many surgeons, however, would probably call it a “transatrial-transpulmonary” repair, either unintentionally or because this is what one has to do today. The extremely interesting and valuable results the authors were able to show should serve as one more incentive to continue to investigate the enigma of the right ventricle in health and in disease. It must, however, not be abused to promote techniques which are still evolving. Markus K. Heinemann, MD, PhD Department of Pediatric Cardiac Surgery Mainz University Hospital Langenbeckstr 1, # 505 55131 Mainz, Germany e-mail: [email protected]
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