ORIGINAL ARTICLE
Right
ventricular dysfunction and the role of
pulmonary valve replacement after correction of tetralogy of Fallot F.T.H. de Ruijter, I. Weenink, J.F. Hitchcock, G.B.W.E. Bennink, E.J. Meijboom
Background. Correction of tetralogy ofFallot (ToF) often leads to pulmonary regurgitation, sometimes warranting pulmonary valve replacement (PVR), for which the indications and timing to achieve optimal results are not yet dear. This retrospective study describes follow-up and reinterventions in our ToF population. Methods. Review ofall consecutive patients operated for ToF between 1977 and 2000. Included are date and type of repair, Doppler echocardiography (2D-echo), ECGs, re-operations and physical condition. Results. Total repair was performed in 270 patients, mean age 1.9±2.5 years, 82 were exduded because of follow-up abroad. Right ventriculotomy was used in 92%, transatrial VSD dosure in 8%, while 69% received a transannular outflow patch. Pulmonary atresia required a pulmonary graft in 13 (8%) patients. Overall 20-year survival was 88%. Last follow-up: ECG showed RBBB in 67% (QRS complex 129±29.3 msec). RVOT aneurysms were detected in 16%. 2D-echo demonstrated mild pulmonary insufficiency (PI) in 40%, severe in 31%, dilated RV in 76%, both increasing with post-repair age. In 39%, RV dimensions were equal or even exceeded LV dimensions, 45% showed tricuspid insufficiency and the RA was enlarged in 14%. Reintervention was necessary in 39/185 patients, this induded angioplasty for residual stenosis and PVR (22/19 homografts, six patients in PA group) at a mean age of 11.2 years after correction. In seven patients, the RV returned to normal F.T.H. de RuliJter. 1. Weenink. J.F. Hitchcock. G.B.W.E. Bennink. E.J. Melijboom. Children's Heart Centre, Wilhelmina Children's Hospital, University Medical Centre, Department of Paediatric Cardiology, P0 Box 85090, 3508 AB Utrecht. Address for correspondence: E.J. Meijboom. E-mail: [email protected]
Netherlands Heart Journal, Volume 9, Number 7, October 2001
dimensions and symptoms disappeared, but in three severe dysfunction developed. Eleven others still have RV dilatation and/or PI. In total, 75% were free of reintervention in the first ten years. The right atrial approach diminishes severe RV dilataton and prolonged QRS duration (p=0.001 and 0.007). Early correction reduces the risk of re-operation (p=0.011). Conclusions. Severe RV dilatation (39%) and PI (31%) secondary to outflow tract repair in ToF are frequently occurring sequels developing slowly over time. Timing of PVR remains controversial, still best guided by the clinical condition. (Neth HeartJ2001;9:269-74.) Key words: Pulmonary valve replacement, RV dysfunction, tetralogy of Fallot
The current trend in clinical management of tetralogy ofFallot (obstruction ofright ventricular outflow, ventricular septum defect, right ventricular hypertrophy and an overriding aorta) involves complete surgical repair in early childhood. This early intracardiac correction decreases the necessity of prior palliative shunt procedures and accounts for a low operative mortality and excellent long-term results.'-' However, amongst other residual lesions in the followup, pulmonary valve insufficiency is frequently encountered even in asymptomatic patients.57 Severe long-standing pulmonary regurgitation (PR) can lead to potentially deleterious complications." 2"8"15 In a small number of patients with both deterioration of symptomatic status and objective evidence of progressive right heart failure, pulmonary valve replacement (PVR) is considered to relieve symptoms.",4"16 20 The small group that needs reintervention is expected to grow, as the first patients who received total repair are reaching mid-life ages,'6,2' especially those in which a transannular patch was used to enlarge the right ventricular outflow tract.22 But specific indications and timing of PVR remain unclear. This study makes an inventory of our tetralogy population from initial repair to present status, focussing on the development of RV 269
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
into four groups: I: common tetralogy of Fallot (ToF) patients, II: with pulmonary atresia (PA), III: with pulmonary valve replacement and IV: both PVR and PA.
Table 1. Surgical approaches used in complete repair.
Surgical technique relief of outflow obstruction Infundibulectomy Transannular patch Commissurotomy Valvectomy Pulmonary graft/conduit VSD closure Right ventriculotomy Transatrial
n
%
122 127 40 53 13
66 69 22 29 8
170 15
92 8
indicators and occurrence of reinterventions in followup with special attention to PVR. Methods
Population The reports of all consecutive surviving patients, operated in the Children's Heart Centre Utrecht between 1977 and 2000 and residing in the Netherlands, were examined retrospectively. The population (n=188) consisted of 116 (62%) male and 72 female patients with a mean follow-up time of9.75±7.2 years (range 0.01-32.9) and mean age of 12.0±8.0 years (0.01-36.2); over 15% was older than 20 years at the latest follow-up. Doppler echocardiographic data (especially RV dimensions, pulmonary stenosis and regurgitation, RA dilatation and tricuspid insufficiency), cardiac catheterisations, ECGs and 24-hour Holter recordings (right axis deviation, QRS-complex duration, dysrhythmias) were reviewed. Furthermore, physical condition (NYHA functional class I to IV), cause and time of death, age, indications and type of reintervention were recorded. Patients were divided
*i1.0Q
n=188
U)0.8
147
0.6
-
0.4
-
0.2
-
O -i 0
5
99 (88%)
10
63
34(88%)
2
15
20
25
Age (years)
Figure 1. Survival.
270
RV dilatation and pulmonary regurgitation Echocardiographic data (M-mode and two-dimensional views) describing the RV were categorised as follows: a normal RV, i.e. LV:RV ratio = 3:1, was attributed the number 0 or none, a severely dilated RV (RV size equal to LV or even exceeding LV dimensions) with 2 and anything in between as a (mildly) dilated RV, associated with the number 1. Pulmonary valve incompetence was classified by the cardiologist on a scale from 1 to 4: 1 indicating trivial, 2 mild, 3 and 4 are regarded as severe in this study.21'23
Statistical analysis All data are presented as the mean value ± 1 SD (range). Probability ofsurvival, freedom of reintervention and PVR after repair were calculated by Kaplan-Meier analysis with the use of the SPSS programme. Differences between groups were calculated with Fisher's exact test and Student's t-test. For the time analysis of RV dilatation and PR, data were clustered and adjusted for dependence ofthe outcome within a patient. The Mixor programme (version 2) then provided a graph of the mean probability in every category and year after corrective surgery. Results
Diagnosis and preoperative status Uncomplicated tetralogy ofFallot was encountered in 99 patients (5 3%), 40% (n=76) had additional cardiac complications (abnormal coronary artery, systemic to pulmonary collaterals, pulmonary artery hypoplasia, branch stenosis or valvular hypoplasia) and 13 (7%) were diagnosed with pulmonary atresia. Double outlet right ventricle (>50% override) occurred in 28 (15%) and pentalogy (with atrial septum defect) in 26 (14%), in total 14 had a persistent ductus arteriosus and 22 a biscuspid pulmonary valve. Two patients presented with a complete atrioventricular septal defect, two with dextrocardia. Comorbidity included Down's syndrome, velocardiofacial-syndrome, VATER association (vertebral-anal-tracheal-oesophageal-renal) and tracheobronchomalacia (54 patients, 29%). In 44 (23%) patients a palliative shunt was required to overcome symptoms: (age 0.9±1.4 years), BlalockTaussig in and 14, central aortopulmonary in 30). Three patients died after shunt placement, two with severe other problems (microcephalia/atrioventricular septum syndrome and Edward's syndrome).
Complete repair At a mean age of 1.9±2.5 years (0.12-21.7 years), 185 patients had a total correction; table 1 shows the surgical specifications. In the 13 pulmonary atresia Netherlands Heart Joumal, Volume 9, Number 7, October 2001
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
patients, eight homografts, two Hancock grafts and three Ionesu-Shiley conduits were used. Mean followup time postoperatively was 7.9±6.6 years (0-27.9). A total of 20 patients died after complete repair (15 postoperatively and five late deaths), while two patients died of tracheobronchomalacia, one of cystic fibrosis combined with septic shock and two oftrisomy 13 and VATER association, respectively. Late deaths included two unrelated deaths and two patients with sudden cardiac death. Overall survival was 88.1% at both ten and twenty years (figure 1). Total mortality attributed only to the heart disease itselfamounted to 8% and if calculated over the last five years to 2%. Follow-up Most patients were in NYHA class I, of which a considerable number presented with some insufficiency ofthe pulmonary valve, RV dilatation, tricuspid valve regurgitation and RA dilatation (table 2). Right axis deviation was noted in 31 patients (30%, n=104 observations), in 16% (28) RVOT aneurysms were detected (one requiring reoperation) and in 27% (48) echocardiography showed a residual VSD, 11 were dosed and 37 were very small or closed spontaneously.
Post-repair cardiac catheterisation was performed in 38 cases, mostly associated with pulmonary valve replacement (21) or to quantify pulmonary stenosis (9) prior to angioplasty. MRIs were performed in 12 patients. Arrhythmias Cardiac arrhythmias were encountered in 33 patients (19%), first manifestation 9.9±6.0 years (1.1-24.3 years). First degree AV-block was found in 16 patients, in six ofthem this preceded the onset of more complex rhythm disturbances. Furthermore, one patient with Wolff-Parkinson-White syndrome and one with sick sinus syndrome were encountered. Severe arrhythmias were found in 18 patients, three receiving medication and one a pacemaker implantation. Of these patients six had a pulmonary valve replacement. Development of PR and RV dilatation Figure 2 demonstrates that RV dimensions slowly increase over time. A similar plot could be drawn for pulmonary valve insufficiency. Statistical analysis showed that the increase was significant in both cases (p180 msec Arrhythmias (important)
113/168(67%) 92/144 129±29.3 3 33(18)
128±31.6 0 21 (10)
PA group
7 3.7±2.6 2.1±2.4
PVR group before after
16 0 9.2±6.7
0 16
6/7 3/4 116±46.1 132±31.5 0 1 0 8 (6)
2 (1)
PA+PVR group before after
6 0
11.9±5.9 4.4±6.6
4.8±2.7
0 9.2±3.7 8.7±4.1
14 2
6 0
5 1
12/14 6 6 148±46.0 147±19.0 157±20.9 0 3 0 2 3 (1) (0) 9 (7)
Echocardiographic data Mild PR Severe PR Normal RV Mild RV dilation Severe RV dilation Tricuspid insufficiency RA dilation Pulmonary stenosis >30 mmHg
66/166(40%) 51(31%) 41(25%) 60(37%) 65(39%) 75(45%) 23(14%) 30(18%)
Netherlands Heart Joumal, Volume 9, Number 7, October 2001
56 54 33 50 58 64 20 21
3 0 0 2 1 2 0 1
6 5 0 3 13 12 5 6
2 1 6 6 4 5 3 6
1 4
0 0 6 4 1 4
0 1 2 2 2 4 0 2
271
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
x 2.0-
1.0 - n=185
severe
0
0 .2
X
1.5-
co
~ ~
~
~
,g
/
o o
0
la!
0.8
6
-
(5%) 52
S . _
'o0.6 0 1i.o- mild C 00.4 -W
0.5-
00.2 0.0 - normal LL
5
10
20 15 Post-repair age (years)
Figure 2. Development of RVdilatation. Reinterventions A total of 39 (2 1%) patients underwent reoperation at a mean age of 8.4±5.6 years (1.3-22.3; at 5.7±5.8 years post-correction) of which ten more than once. Follow-up time after the first reintervention was 6.0±5.8 years. Reintervention (10-year freedom 75%, figure 3) included PVR(n=22), angioplasty for residual pulmonary stenosis (n-14) and residual VSD closure (n=7).
Pulmonary valve replacement In 22 patients (12%) both physical and heart condition deteriorated to such an extent that PVRwas considered (mean age post-repair 8.0±6.2 years). Besides the clinical symptoms present in every case, indications for a repeated operative solution were: severe RV dilatation (n=21, 95%), severe PR (20, 91%), arrhythmias (6, 27%), tricuspid regurgitation (14, 64%), pulmonary stenosis (6, 27%) and calcification of a previously implanted valve (8, 36%, of which 6 with PA). Most valves used were homografts (19); others consisted of two Hancock heterografts and one hemax conduit. Of the 16 patients who came from the common ToF group, five had a very good result with a RV that returned to normal dimensions and symptoms that disappeared. Five other patients still show some residual problems: two with mild RV dilatation slowly developing after PVR, two with severe residual pulmonary stenosis and one with mild but stable homograft valve insufficiency present since implantation. Severe RV dilatation after PVRwas found in six patients: one with a calcified homograft, in one persisting after PVR, one died shortly after the operation and in three it occurred in combination with QRS >180 msec. Of these three patients, one developed severe heart failure requiring heart transplantation 19 years post-PVR and one patient had a pacemaker and second homograft (6.7 years after the first) but died of late sudden cardiac death 12 years later, at an age of 22 years). All the important 272
-
0
5
0
10
15
20 Age (years)
Figure 3. Freedom ofreintervention/pulmonary valve replacement.
arrhythmias present before reoperation persisted after the procedure. When replacement was performed within four years after correction (n=6), most patients (4) had had a reintervention for residual pulmonary stenosis first (of which two died later). Tricuspid insufficiency as indication for PVRwas documented in patients with both good and less favourable outcome. Pulmonary atresia This small group (n=13) presented with the most problems. Four patients died, of which three immediately postoperatively, however two ofnon-cardiac causes (including one late death). Of the four remaining patients who did not receive a new homograft, all showed mild pulmonary insufficiency and RV dilatation. Both Hancock grafts (0.6 and 5.5 years post-op), 2/3 Ionescu-Shiley conduits (2.8 and 7.3 years) and 2/8 homografts (1.5 and 3.0) were replaced without mortality (mean age at PVR was 4.8±2.7 years). Severe RV dilatation and PR persisted in two cases. Two patients clearly improved both objectively and subjectively. Serious dysrhythmias were not found in this group before or after the reoperation. Time and type of repair and outcome The incidence of RV dilatation was considerably higher in patients who underwent correction with the use of a transannular outflow patch (p=0.020). The group in which the VSD was closed by transatrial approach (n=15) showed the opposite (p=O.001) and moreover presented with lower QRS duration (p=0.007). Results of patients with complete correction before three years of age (n=158, 75%) demonstrated more reoperations (p=0.011), but most of them came from the cohort operated before 1985 and a difference in RV dysfunction could not be established.
Discussion In conjunction with recent large studies, the prognosis of a newborn with tetralogy of Fallot is excellent.'4'2'
Netherlands Heart Joumal, Volume 9, Number 7, October 2001
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
Most patients were in NYHA functional class I and we found a 20-year actuarial survival of 88%. The authoritative article of Murphy et al. clearly pointed out that this is lower than the general population, but it is still a very reasonable outcome compared with other serious congenital heart defects.' The group of patients with pulmonary atresia needs to be distinguished; present with more problems in follow-up, confirming the results of Knott-Craig and associates.3 As most severe forms of tetralogy are in immediate need of a shunt or pulmonary graft, it is not surprising that these patients come forward with a higher probability of reoperation and mortality. We doubt whether an earlier timing of the initial operation will greatly affect the late outcome. Our data indeed show that patients operated after the age of two have a higher probability of needing reintervention or PVR, but no difference in RV dimensions could be established. The fact that their follow-up time was significantly longer and most operations were performed in the early days of our centre certainly militate for a time or surgically dependent effect. Evaluating transannular patching, this time factor was ruled out and our results met those of previous observations,22 concluding that both severe PR and RV dilatation were more prevalent in those patients who received this outflow patch. The positive impact of the transatrial approach was confirmed, although this technique was not extensively used in our population. The shorter duration of the QRS complex, an electrophysiological advantage, did not result in less dysrhythmias in their follow-up, in accordance with Oechslin et al., indicating that the site of ventricular arrhythmia is predominantly around the margins of the VSD patch and not the ventriculotomy per se, therefore putting every patient at equal risk.'9 In regard to the severity of late RVOT complications, our results did confirm those of Dietl et al.,24 speaking in favour of the right atrial technique. Recommending preservation ofthe pulmonary valve or if a transabdominal punction (TAP) is necessary restricting its width (miniimising regurgitant flow) and having a preference for the transatrial approach now seems to be not only logical but also well founded.
Right ventricular dysfunction and pulmonary valve insufficiency slowly develop after repair of tetralogy of Fallot and seem to appear in almost all patients to some degree. Very similar to Meijboom,2' Zakha,9 Jonsson7 and Homeffer with colleagues,2 who used echocardiography in follow-up as well, we found evidence of more than trivial pulmonary regurgitation in a considerable number of patients. Meijboom, however, did not confirm the increase we found over time of both PR and RV dilatation. Exercise capacity is found to be decreased in patients with dilated RV,'3'2' but the most patients by far remain asymptomatic. Although some Netherlands Heart Journal, Volume 9, Number 7, October 2001
argue that long-standing PR has no adverse effect on
survival, 1,2,21,22,25,26 PVR will become a more frequent consideration as the population ages. Shimazaki et al. have already made relevant that patients without surgery and with anatomically normal hearts, except for a congenitally incompetent pulmonary valve, will develop symptoms of right heart failure 30 to 40 years later in life.27 A considerable variation exists between patients regarding the ability to tolerate PR as a result the development of RV dilation. Especially additional lesions make the detrimental effects more difficult to endure: five of our patients had already had a reoperation before undergoing PVR_813,2 26 Furthermore Gatzoulis, Norgard and colleagues demonstrated the protective effect (limited PR, less ventricular dilatation and superior exercise performance) of a poorly compliant RV.28,29
Quite a high percentage in our population (almost 11%) underwent PVR. In a few patients symptoms clearly diminished and the severity of regurgitation and dilatation improved, but unlike other reports,'6"18-20 objective outcome was not as good as expected. Some outcomes can be explained by 'normal' deterioration of the implanted valve (in this case mostly homografts), as also seen in the group with pulmonary atresia. But in the dawn of longer lasting valves, discovering a highrisk individual in an earlier stage and offering pulmonary valve replacement before the onset of myocardial degeneration is now becoming the ultimate quest. Answers to this search are then to be found in more specific indications for the replacement. Some authors have emphasised the importance of coexisting tricuspid valve insufficiency,17'26 resulting from progressive RV dilatation and advocate earlier replacement, because the onset of tricuspid regurgitation may represent a very late and possibly irreversible stage of RV failure.20 The scar tissue is an important factor in the development of malignant ventricular arrhythmias and particularly when combined with poor haemodynamics, a high-risk situation can evolve.30 In contrast to Niezen et al.,"1 recently Meijboom et al. could not show a correlation between RV dilatation and arrhythmias (and sudden death).2' Neither could this be confirmed in our study, but we agree with the findings of Redington's group that QRS prolongation (>180 ms) is their most sensitive predictor.3' The presence of a significant arrhythmia in itself can therefore not be an indication for pulmonary valve replacement. Perhaps a great factor in this problem is not the indication itself, but the evidence of its presence. Different patients have different ways of responding to haemodynamics after complete repair and this should be accounted for in diagnostic methods. Doubts about a deteriorated RV function by echocardiographic data should best be confirmed by MRI 273
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
mapping studies to allow optimal timing in the decision-making process tailored to the individual patient."132 Limitations In the 33 years of cardiac surgery for ToF in our centre, techniques and timing ofthe operation have changed and the experience of the surgeons has increased, suggesting a more favourable outcome in the youngest patients. During follow-up, ECG and echocardiography devices have been modernised, presenting clearer pictures, detecting problems earlier and moreover observations were performed by different cardiologists. Comparison of results may also be hazardous because no standardised method is used in literature to quantify either pulmonary regurgitation or RV dilatation.
Conclusions Severe RV dilatation and pulmonary regurgitation secondary to outflow tract repair in ToF are frequently occurring sequels in 39% and 31%, respectively, of our population, developing slowly along a time-dependent course. Timing of PVR remains controversial, until now best guided by clinical condition. U References 1
Murphy JG, Gersh BJ, Mair DD, Fuster V, McGoon MD, Ilstrup DM, et al. Long-term outcome in patients undergoing repair of tetralogy ofFallot. NEnglJMed 1993;329:595-9. 2 Homeffer PJ, Zakha KG, Rowe SA, Manolio TA, Gott VL, Reitz BA, et al. Long-term results of total repair of tetralogy of Fallot in childhood. Ann Thorac Surg 1990;50:179-85. 3 Knott-Craig CJ, Elkins RC, Lane MM, Holz J, McCue C, Ward KE. A 26-year experience with surgical management of tetralogy of Fallot: risk analysis for mortality or late reintervention. Ann Thorac Surg 1998;66:506-11. 4 Zhao HX, Miller DC, Reitz BA, Shumway NE. Surgical repair of tetralogy of Fallot. Long-term follow-up with particular emphasis on late death and reoperation. J Thorac Cardiovasc Surg 1985; 89:204-20. 5 Fuster V, McGoon DC, Kennedy MA, Ritter DG, Kirklin JW. Long-term evaluation (12 to 22 years) of open heart surgery for tetralogy ofFallot. Am J Cardiol 1980;46:635-42. 6 Joransen JA, Lucas RVJr, Moller JH. Postoperative haemodynamics in tetralogy of Fallot. A study of 132 children. Br Heart J 1987;41:33-9. 7 Jonsson H, Ivert T, Brodin LA. Echocardiographic findings in 83 patients 13-26 years after intracardiac repair of tetralogy of Fallot. Eur HeartJ 1995;16:1255-63. 8 Ilbawi MN, Idriss FS, DeLeon SY, Muster AJ, Gidding SS, Berry TE, et al. Factors that exaggerate the deleterious effects of pulmonary insufficiency on the right ventricle after tetralogy repair. JThorac Cardiovasc Surg 1987;93:36-44. 9 Zakha KG, Homeffer PJ, Rowe SA, Neil CA, Manolio TA, Kidd L, et al. Long-term valvular function after total repair of tetralogy of Fallot. Circulation 1988;78(Suppl III):14-9. 10 Bove EL, Byrum CJ, Thomas FD, Kavey RE, Sondheimer HM, Blackman MS, et al. The influence of pulmonary insufficiency on ventricular function following repair of tetralogy of Fallot: evaluation using radionuclide ventriculography. J Thorac Cardiovasc
Surg 1983;85:691-6. 11 Niezen RA, Helbing WA, Wall EE van der, Geest RJ van der, Rebergen SA, Roos A de, et al. Biventricular systolic function and mass studied with MR Imaging in children with pulmonary regurgitation after repair of tetralogy of Fallot. Radiology 1996; 201:135-40.
274
12 Carvalho JS, Shineboume EA, Busst C, Rigby ML, Redington AN. Exercise capacity after complete repair of tetralogy ofFallot: deleterious effects of pulmonary regurgitation. Br Heart J 1992; 67:470-3. 13 Jonsson H, Ivert T, Jonasson R, Holmgren A, Bjork VO. Work capacity and central hemodynamics 13 to 26 years after repair of tetralogy of Fallot. J Thorac Cardiovasc Surg 1995;110:416-26. 14 Lange PE, Onnasch DGW, BemardA, Heintzen PH. Left and right ventricular adaptation to right ventricular overload before and after surgical repair oftetralogy ofFallot. AmJCardiol 1982;50:786-94. 15 Kavey REW, Thomas FD, Byrum CJ, Blackman MS, Sondheimer HM, Bove EL. Ventricular arrhythmias and biventricular dysfunction after repair of tetralogy of Fallot. J Am Coll Cardiol 1984;4:126-31. 16 Yemets IM, Whlliams WG, Webb DG, Harrison DA, McLaughlin PR, Trusler GA, et al. Pulmonary valve replacement after late repair of tetralogy of Fallot. Ann Thorac Surg 1997;64:526-30. 17 Misbach GA, Turley K, Ebert PA. Pulmonary valve replacement for regurgitation after repair oftetralogy of Fallot. Ann Thorac Surg 1983;36:684-91. 18 Bove EL, Kavey REW, Byrum CJ, Sondheimer HM, Blackman MS, Thomas FD. Improved right ventricular function following late pulmonary valve replacement for residual pulmonary insufficiency or stenosis. JThorac Cardiovasc Surg 1985;90:50-5. 19 Oechslin EN, Harrison DA, Harris L, Downar E, Webb GD, Siu SS, et al. Reoperation in adults with repair of tetralogy of Fallot: indications and outcomes. J Thorac Cardiovasc Surg 1999; 118:245-51. 20 Warner KG, Anderson JE, Fulton DR, Payne DD, Geggel RL, Marx GR Restoration of the pulmonary valve after right ventricle volume overload after previous repair of tetralogy of Fallot. Circulation 1993;88:189-97. 21 Meijboom F, SzatmariA, Deckers JW, Utens EM, Roelandt JRTC, Bos E, et al. Cardiac status and health related quality oflife in the long term after surgical repair of tetralogy of Fallot in infancy and childhood. JThorac Cardiovasc Surg 1995;110:883-91. 22 Kirklin JK, Kirklin JW, Blackstone EH, Milano A, Pacifico AD. Effect of transannular patching on outcome after repair of tetralogy ofFallot. Ann Thorac Surg 1989;48:783-91. 23 Meijboom EJ, Valdes-Cruz L, Horowitz S, Sahn DJ, Larson DF, et al. A two-dimensional Doppler echocardiographic method for calculation of pulmonary and systemic blood flow in a canine model with a variable-sized left-to-right extracardiac shunt. Circulation
1983;68:437-45. 24 Died CA, Cazzaniga ME, Dubner SJ, Perez-Balino NA, Torres AR, Favaloro RG. Life threatening arrhythmias and RV dysfunction after surgical repair of tetralogy of Fallot. Circulation 1994; 90:7-12. 25 Wessel HU, Cunningham WJ, Paul MH, Bastanier CK, Muster AJ, Idriss FS. Exercise performance in tetralogy ofFallot after intracardiac repair. JThorac Cardiovasc Surg 1980;80:582-93. 26 Finck SJ, Puga FJ, Danielson GK Pulmonary valve insertion during reoperation for tetralogy of Fallot. Ann Thorac Surg 1988;45: 610-3. 27 Shimazaki Y, Blackstone EH, Kirklin JW. The natural history of isolated congenital pulmonary valve incompetence: surgical implications. Thorac Cardiovasc Surg 1984;32:257-9. 28 Norgard G, Gatzoulis MA, Moraes F, Lincoln C, Shore DF, Shinebourne, et al. Relationship between type of outflow tract repair and postoperative right ventricular diastolic physiology in tetralogy of Fallot. Implications for long-term outcome. Circulation
1996;94:3276-80. 29 Gatzoulis MA, Clark AL, Cullen S, Claus GH, et al. Right ventricular diastolic function 15 to 35 years after repair of tetralogy of Fallot. Circulation 1995;91:1775-81. 30 Friedli B. Electrophysiological follow-up of tetralogy of Fallot. Pediatr Cardiol 1999;20:326-30. 31 Gatzoulis MA, Till JA, Somerville J, Redington AN. Mechanoelectrical interaction in tetralogy of Fallot [QRS Prolongation relates to right ventricular size and predicts malignant ventricular arrhythmias and sudden death] Circulation 1995;92:231-7. 32 Rebergen SA, Chin JGJ, Ottenkamp J, Wall EE van der, Roos A de. Pulmonary regurgitation in the late postoperative follow-up of tetralogy of Fallot [Volumetric quantitation by NMR velocity mapping] Circulation 1993;88:2257-66.
Netherlands Heart Journal, Volume 9, Number 7, October 2001
Right
ventricular dysfunction and the role of
pulmonary valve replacement after correction of tetralogy of Fallot F.T.H. de Ruijter, I. Weenink, J.F. Hitchcock, G.B.W.E. Bennink, E.J. Meijboom
Background. Correction of tetralogy ofFallot (ToF) often leads to pulmonary regurgitation, sometimes warranting pulmonary valve replacement (PVR), for which the indications and timing to achieve optimal results are not yet dear. This retrospective study describes follow-up and reinterventions in our ToF population. Methods. Review ofall consecutive patients operated for ToF between 1977 and 2000. Included are date and type of repair, Doppler echocardiography (2D-echo), ECGs, re-operations and physical condition. Results. Total repair was performed in 270 patients, mean age 1.9±2.5 years, 82 were exduded because of follow-up abroad. Right ventriculotomy was used in 92%, transatrial VSD dosure in 8%, while 69% received a transannular outflow patch. Pulmonary atresia required a pulmonary graft in 13 (8%) patients. Overall 20-year survival was 88%. Last follow-up: ECG showed RBBB in 67% (QRS complex 129±29.3 msec). RVOT aneurysms were detected in 16%. 2D-echo demonstrated mild pulmonary insufficiency (PI) in 40%, severe in 31%, dilated RV in 76%, both increasing with post-repair age. In 39%, RV dimensions were equal or even exceeded LV dimensions, 45% showed tricuspid insufficiency and the RA was enlarged in 14%. Reintervention was necessary in 39/185 patients, this induded angioplasty for residual stenosis and PVR (22/19 homografts, six patients in PA group) at a mean age of 11.2 years after correction. In seven patients, the RV returned to normal F.T.H. de RuliJter. 1. Weenink. J.F. Hitchcock. G.B.W.E. Bennink. E.J. Melijboom. Children's Heart Centre, Wilhelmina Children's Hospital, University Medical Centre, Department of Paediatric Cardiology, P0 Box 85090, 3508 AB Utrecht. Address for correspondence: E.J. Meijboom. E-mail: [email protected]
Netherlands Heart Journal, Volume 9, Number 7, October 2001
dimensions and symptoms disappeared, but in three severe dysfunction developed. Eleven others still have RV dilatation and/or PI. In total, 75% were free of reintervention in the first ten years. The right atrial approach diminishes severe RV dilataton and prolonged QRS duration (p=0.001 and 0.007). Early correction reduces the risk of re-operation (p=0.011). Conclusions. Severe RV dilatation (39%) and PI (31%) secondary to outflow tract repair in ToF are frequently occurring sequels developing slowly over time. Timing of PVR remains controversial, still best guided by the clinical condition. (Neth HeartJ2001;9:269-74.) Key words: Pulmonary valve replacement, RV dysfunction, tetralogy of Fallot
The current trend in clinical management of tetralogy ofFallot (obstruction ofright ventricular outflow, ventricular septum defect, right ventricular hypertrophy and an overriding aorta) involves complete surgical repair in early childhood. This early intracardiac correction decreases the necessity of prior palliative shunt procedures and accounts for a low operative mortality and excellent long-term results.'-' However, amongst other residual lesions in the followup, pulmonary valve insufficiency is frequently encountered even in asymptomatic patients.57 Severe long-standing pulmonary regurgitation (PR) can lead to potentially deleterious complications." 2"8"15 In a small number of patients with both deterioration of symptomatic status and objective evidence of progressive right heart failure, pulmonary valve replacement (PVR) is considered to relieve symptoms.",4"16 20 The small group that needs reintervention is expected to grow, as the first patients who received total repair are reaching mid-life ages,'6,2' especially those in which a transannular patch was used to enlarge the right ventricular outflow tract.22 But specific indications and timing of PVR remain unclear. This study makes an inventory of our tetralogy population from initial repair to present status, focussing on the development of RV 269
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
into four groups: I: common tetralogy of Fallot (ToF) patients, II: with pulmonary atresia (PA), III: with pulmonary valve replacement and IV: both PVR and PA.
Table 1. Surgical approaches used in complete repair.
Surgical technique relief of outflow obstruction Infundibulectomy Transannular patch Commissurotomy Valvectomy Pulmonary graft/conduit VSD closure Right ventriculotomy Transatrial
n
%
122 127 40 53 13
66 69 22 29 8
170 15
92 8
indicators and occurrence of reinterventions in followup with special attention to PVR. Methods
Population The reports of all consecutive surviving patients, operated in the Children's Heart Centre Utrecht between 1977 and 2000 and residing in the Netherlands, were examined retrospectively. The population (n=188) consisted of 116 (62%) male and 72 female patients with a mean follow-up time of9.75±7.2 years (range 0.01-32.9) and mean age of 12.0±8.0 years (0.01-36.2); over 15% was older than 20 years at the latest follow-up. Doppler echocardiographic data (especially RV dimensions, pulmonary stenosis and regurgitation, RA dilatation and tricuspid insufficiency), cardiac catheterisations, ECGs and 24-hour Holter recordings (right axis deviation, QRS-complex duration, dysrhythmias) were reviewed. Furthermore, physical condition (NYHA functional class I to IV), cause and time of death, age, indications and type of reintervention were recorded. Patients were divided
*i1.0Q
n=188
U)0.8
147
0.6
-
0.4
-
0.2
-
O -i 0
5
99 (88%)
10
63
34(88%)
2
15
20
25
Age (years)
Figure 1. Survival.
270
RV dilatation and pulmonary regurgitation Echocardiographic data (M-mode and two-dimensional views) describing the RV were categorised as follows: a normal RV, i.e. LV:RV ratio = 3:1, was attributed the number 0 or none, a severely dilated RV (RV size equal to LV or even exceeding LV dimensions) with 2 and anything in between as a (mildly) dilated RV, associated with the number 1. Pulmonary valve incompetence was classified by the cardiologist on a scale from 1 to 4: 1 indicating trivial, 2 mild, 3 and 4 are regarded as severe in this study.21'23
Statistical analysis All data are presented as the mean value ± 1 SD (range). Probability ofsurvival, freedom of reintervention and PVR after repair were calculated by Kaplan-Meier analysis with the use of the SPSS programme. Differences between groups were calculated with Fisher's exact test and Student's t-test. For the time analysis of RV dilatation and PR, data were clustered and adjusted for dependence ofthe outcome within a patient. The Mixor programme (version 2) then provided a graph of the mean probability in every category and year after corrective surgery. Results
Diagnosis and preoperative status Uncomplicated tetralogy ofFallot was encountered in 99 patients (5 3%), 40% (n=76) had additional cardiac complications (abnormal coronary artery, systemic to pulmonary collaterals, pulmonary artery hypoplasia, branch stenosis or valvular hypoplasia) and 13 (7%) were diagnosed with pulmonary atresia. Double outlet right ventricle (>50% override) occurred in 28 (15%) and pentalogy (with atrial septum defect) in 26 (14%), in total 14 had a persistent ductus arteriosus and 22 a biscuspid pulmonary valve. Two patients presented with a complete atrioventricular septal defect, two with dextrocardia. Comorbidity included Down's syndrome, velocardiofacial-syndrome, VATER association (vertebral-anal-tracheal-oesophageal-renal) and tracheobronchomalacia (54 patients, 29%). In 44 (23%) patients a palliative shunt was required to overcome symptoms: (age 0.9±1.4 years), BlalockTaussig in and 14, central aortopulmonary in 30). Three patients died after shunt placement, two with severe other problems (microcephalia/atrioventricular septum syndrome and Edward's syndrome).
Complete repair At a mean age of 1.9±2.5 years (0.12-21.7 years), 185 patients had a total correction; table 1 shows the surgical specifications. In the 13 pulmonary atresia Netherlands Heart Joumal, Volume 9, Number 7, October 2001
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
patients, eight homografts, two Hancock grafts and three Ionesu-Shiley conduits were used. Mean followup time postoperatively was 7.9±6.6 years (0-27.9). A total of 20 patients died after complete repair (15 postoperatively and five late deaths), while two patients died of tracheobronchomalacia, one of cystic fibrosis combined with septic shock and two oftrisomy 13 and VATER association, respectively. Late deaths included two unrelated deaths and two patients with sudden cardiac death. Overall survival was 88.1% at both ten and twenty years (figure 1). Total mortality attributed only to the heart disease itselfamounted to 8% and if calculated over the last five years to 2%. Follow-up Most patients were in NYHA class I, of which a considerable number presented with some insufficiency ofthe pulmonary valve, RV dilatation, tricuspid valve regurgitation and RA dilatation (table 2). Right axis deviation was noted in 31 patients (30%, n=104 observations), in 16% (28) RVOT aneurysms were detected (one requiring reoperation) and in 27% (48) echocardiography showed a residual VSD, 11 were dosed and 37 were very small or closed spontaneously.
Post-repair cardiac catheterisation was performed in 38 cases, mostly associated with pulmonary valve replacement (21) or to quantify pulmonary stenosis (9) prior to angioplasty. MRIs were performed in 12 patients. Arrhythmias Cardiac arrhythmias were encountered in 33 patients (19%), first manifestation 9.9±6.0 years (1.1-24.3 years). First degree AV-block was found in 16 patients, in six ofthem this preceded the onset of more complex rhythm disturbances. Furthermore, one patient with Wolff-Parkinson-White syndrome and one with sick sinus syndrome were encountered. Severe arrhythmias were found in 18 patients, three receiving medication and one a pacemaker implantation. Of these patients six had a pulmonary valve replacement. Development of PR and RV dilatation Figure 2 demonstrates that RV dimensions slowly increase over time. A similar plot could be drawn for pulmonary valve insufficiency. Statistical analysis showed that the increase was significant in both cases (p180 msec Arrhythmias (important)
113/168(67%) 92/144 129±29.3 3 33(18)
128±31.6 0 21 (10)
PA group
7 3.7±2.6 2.1±2.4
PVR group before after
16 0 9.2±6.7
0 16
6/7 3/4 116±46.1 132±31.5 0 1 0 8 (6)
2 (1)
PA+PVR group before after
6 0
11.9±5.9 4.4±6.6
4.8±2.7
0 9.2±3.7 8.7±4.1
14 2
6 0
5 1
12/14 6 6 148±46.0 147±19.0 157±20.9 0 3 0 2 3 (1) (0) 9 (7)
Echocardiographic data Mild PR Severe PR Normal RV Mild RV dilation Severe RV dilation Tricuspid insufficiency RA dilation Pulmonary stenosis >30 mmHg
66/166(40%) 51(31%) 41(25%) 60(37%) 65(39%) 75(45%) 23(14%) 30(18%)
Netherlands Heart Joumal, Volume 9, Number 7, October 2001
56 54 33 50 58 64 20 21
3 0 0 2 1 2 0 1
6 5 0 3 13 12 5 6
2 1 6 6 4 5 3 6
1 4
0 0 6 4 1 4
0 1 2 2 2 4 0 2
271
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
x 2.0-
1.0 - n=185
severe
0
0 .2
X
1.5-
co
~ ~
~
~
,g
/
o o
0
la!
0.8
6
-
(5%) 52
S . _
'o0.6 0 1i.o- mild C 00.4 -W
0.5-
00.2 0.0 - normal LL
5
10
20 15 Post-repair age (years)
Figure 2. Development of RVdilatation. Reinterventions A total of 39 (2 1%) patients underwent reoperation at a mean age of 8.4±5.6 years (1.3-22.3; at 5.7±5.8 years post-correction) of which ten more than once. Follow-up time after the first reintervention was 6.0±5.8 years. Reintervention (10-year freedom 75%, figure 3) included PVR(n=22), angioplasty for residual pulmonary stenosis (n-14) and residual VSD closure (n=7).
Pulmonary valve replacement In 22 patients (12%) both physical and heart condition deteriorated to such an extent that PVRwas considered (mean age post-repair 8.0±6.2 years). Besides the clinical symptoms present in every case, indications for a repeated operative solution were: severe RV dilatation (n=21, 95%), severe PR (20, 91%), arrhythmias (6, 27%), tricuspid regurgitation (14, 64%), pulmonary stenosis (6, 27%) and calcification of a previously implanted valve (8, 36%, of which 6 with PA). Most valves used were homografts (19); others consisted of two Hancock heterografts and one hemax conduit. Of the 16 patients who came from the common ToF group, five had a very good result with a RV that returned to normal dimensions and symptoms that disappeared. Five other patients still show some residual problems: two with mild RV dilatation slowly developing after PVR, two with severe residual pulmonary stenosis and one with mild but stable homograft valve insufficiency present since implantation. Severe RV dilatation after PVRwas found in six patients: one with a calcified homograft, in one persisting after PVR, one died shortly after the operation and in three it occurred in combination with QRS >180 msec. Of these three patients, one developed severe heart failure requiring heart transplantation 19 years post-PVR and one patient had a pacemaker and second homograft (6.7 years after the first) but died of late sudden cardiac death 12 years later, at an age of 22 years). All the important 272
-
0
5
0
10
15
20 Age (years)
Figure 3. Freedom ofreintervention/pulmonary valve replacement.
arrhythmias present before reoperation persisted after the procedure. When replacement was performed within four years after correction (n=6), most patients (4) had had a reintervention for residual pulmonary stenosis first (of which two died later). Tricuspid insufficiency as indication for PVRwas documented in patients with both good and less favourable outcome. Pulmonary atresia This small group (n=13) presented with the most problems. Four patients died, of which three immediately postoperatively, however two ofnon-cardiac causes (including one late death). Of the four remaining patients who did not receive a new homograft, all showed mild pulmonary insufficiency and RV dilatation. Both Hancock grafts (0.6 and 5.5 years post-op), 2/3 Ionescu-Shiley conduits (2.8 and 7.3 years) and 2/8 homografts (1.5 and 3.0) were replaced without mortality (mean age at PVR was 4.8±2.7 years). Severe RV dilatation and PR persisted in two cases. Two patients clearly improved both objectively and subjectively. Serious dysrhythmias were not found in this group before or after the reoperation. Time and type of repair and outcome The incidence of RV dilatation was considerably higher in patients who underwent correction with the use of a transannular outflow patch (p=0.020). The group in which the VSD was closed by transatrial approach (n=15) showed the opposite (p=O.001) and moreover presented with lower QRS duration (p=0.007). Results of patients with complete correction before three years of age (n=158, 75%) demonstrated more reoperations (p=0.011), but most of them came from the cohort operated before 1985 and a difference in RV dysfunction could not be established.
Discussion In conjunction with recent large studies, the prognosis of a newborn with tetralogy of Fallot is excellent.'4'2'
Netherlands Heart Joumal, Volume 9, Number 7, October 2001
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
Most patients were in NYHA functional class I and we found a 20-year actuarial survival of 88%. The authoritative article of Murphy et al. clearly pointed out that this is lower than the general population, but it is still a very reasonable outcome compared with other serious congenital heart defects.' The group of patients with pulmonary atresia needs to be distinguished; present with more problems in follow-up, confirming the results of Knott-Craig and associates.3 As most severe forms of tetralogy are in immediate need of a shunt or pulmonary graft, it is not surprising that these patients come forward with a higher probability of reoperation and mortality. We doubt whether an earlier timing of the initial operation will greatly affect the late outcome. Our data indeed show that patients operated after the age of two have a higher probability of needing reintervention or PVR, but no difference in RV dimensions could be established. The fact that their follow-up time was significantly longer and most operations were performed in the early days of our centre certainly militate for a time or surgically dependent effect. Evaluating transannular patching, this time factor was ruled out and our results met those of previous observations,22 concluding that both severe PR and RV dilatation were more prevalent in those patients who received this outflow patch. The positive impact of the transatrial approach was confirmed, although this technique was not extensively used in our population. The shorter duration of the QRS complex, an electrophysiological advantage, did not result in less dysrhythmias in their follow-up, in accordance with Oechslin et al., indicating that the site of ventricular arrhythmia is predominantly around the margins of the VSD patch and not the ventriculotomy per se, therefore putting every patient at equal risk.'9 In regard to the severity of late RVOT complications, our results did confirm those of Dietl et al.,24 speaking in favour of the right atrial technique. Recommending preservation ofthe pulmonary valve or if a transabdominal punction (TAP) is necessary restricting its width (miniimising regurgitant flow) and having a preference for the transatrial approach now seems to be not only logical but also well founded.
Right ventricular dysfunction and pulmonary valve insufficiency slowly develop after repair of tetralogy of Fallot and seem to appear in almost all patients to some degree. Very similar to Meijboom,2' Zakha,9 Jonsson7 and Homeffer with colleagues,2 who used echocardiography in follow-up as well, we found evidence of more than trivial pulmonary regurgitation in a considerable number of patients. Meijboom, however, did not confirm the increase we found over time of both PR and RV dilatation. Exercise capacity is found to be decreased in patients with dilated RV,'3'2' but the most patients by far remain asymptomatic. Although some Netherlands Heart Journal, Volume 9, Number 7, October 2001
argue that long-standing PR has no adverse effect on
survival, 1,2,21,22,25,26 PVR will become a more frequent consideration as the population ages. Shimazaki et al. have already made relevant that patients without surgery and with anatomically normal hearts, except for a congenitally incompetent pulmonary valve, will develop symptoms of right heart failure 30 to 40 years later in life.27 A considerable variation exists between patients regarding the ability to tolerate PR as a result the development of RV dilation. Especially additional lesions make the detrimental effects more difficult to endure: five of our patients had already had a reoperation before undergoing PVR_813,2 26 Furthermore Gatzoulis, Norgard and colleagues demonstrated the protective effect (limited PR, less ventricular dilatation and superior exercise performance) of a poorly compliant RV.28,29
Quite a high percentage in our population (almost 11%) underwent PVR. In a few patients symptoms clearly diminished and the severity of regurgitation and dilatation improved, but unlike other reports,'6"18-20 objective outcome was not as good as expected. Some outcomes can be explained by 'normal' deterioration of the implanted valve (in this case mostly homografts), as also seen in the group with pulmonary atresia. But in the dawn of longer lasting valves, discovering a highrisk individual in an earlier stage and offering pulmonary valve replacement before the onset of myocardial degeneration is now becoming the ultimate quest. Answers to this search are then to be found in more specific indications for the replacement. Some authors have emphasised the importance of coexisting tricuspid valve insufficiency,17'26 resulting from progressive RV dilatation and advocate earlier replacement, because the onset of tricuspid regurgitation may represent a very late and possibly irreversible stage of RV failure.20 The scar tissue is an important factor in the development of malignant ventricular arrhythmias and particularly when combined with poor haemodynamics, a high-risk situation can evolve.30 In contrast to Niezen et al.,"1 recently Meijboom et al. could not show a correlation between RV dilatation and arrhythmias (and sudden death).2' Neither could this be confirmed in our study, but we agree with the findings of Redington's group that QRS prolongation (>180 ms) is their most sensitive predictor.3' The presence of a significant arrhythmia in itself can therefore not be an indication for pulmonary valve replacement. Perhaps a great factor in this problem is not the indication itself, but the evidence of its presence. Different patients have different ways of responding to haemodynamics after complete repair and this should be accounted for in diagnostic methods. Doubts about a deteriorated RV function by echocardiographic data should best be confirmed by MRI 273
Right ventricular dysfunction and the role of pulmonary valve replacement after correction of tetralogy of Fallot
mapping studies to allow optimal timing in the decision-making process tailored to the individual patient."132 Limitations In the 33 years of cardiac surgery for ToF in our centre, techniques and timing ofthe operation have changed and the experience of the surgeons has increased, suggesting a more favourable outcome in the youngest patients. During follow-up, ECG and echocardiography devices have been modernised, presenting clearer pictures, detecting problems earlier and moreover observations were performed by different cardiologists. Comparison of results may also be hazardous because no standardised method is used in literature to quantify either pulmonary regurgitation or RV dilatation.
Conclusions Severe RV dilatation and pulmonary regurgitation secondary to outflow tract repair in ToF are frequently occurring sequels in 39% and 31%, respectively, of our population, developing slowly along a time-dependent course. Timing of PVR remains controversial, until now best guided by clinical condition. U References 1
Murphy JG, Gersh BJ, Mair DD, Fuster V, McGoon MD, Ilstrup DM, et al. Long-term outcome in patients undergoing repair of tetralogy ofFallot. NEnglJMed 1993;329:595-9. 2 Homeffer PJ, Zakha KG, Rowe SA, Manolio TA, Gott VL, Reitz BA, et al. Long-term results of total repair of tetralogy of Fallot in childhood. Ann Thorac Surg 1990;50:179-85. 3 Knott-Craig CJ, Elkins RC, Lane MM, Holz J, McCue C, Ward KE. A 26-year experience with surgical management of tetralogy of Fallot: risk analysis for mortality or late reintervention. Ann Thorac Surg 1998;66:506-11. 4 Zhao HX, Miller DC, Reitz BA, Shumway NE. Surgical repair of tetralogy of Fallot. Long-term follow-up with particular emphasis on late death and reoperation. J Thorac Cardiovasc Surg 1985; 89:204-20. 5 Fuster V, McGoon DC, Kennedy MA, Ritter DG, Kirklin JW. Long-term evaluation (12 to 22 years) of open heart surgery for tetralogy ofFallot. Am J Cardiol 1980;46:635-42. 6 Joransen JA, Lucas RVJr, Moller JH. Postoperative haemodynamics in tetralogy of Fallot. A study of 132 children. Br Heart J 1987;41:33-9. 7 Jonsson H, Ivert T, Brodin LA. Echocardiographic findings in 83 patients 13-26 years after intracardiac repair of tetralogy of Fallot. Eur HeartJ 1995;16:1255-63. 8 Ilbawi MN, Idriss FS, DeLeon SY, Muster AJ, Gidding SS, Berry TE, et al. Factors that exaggerate the deleterious effects of pulmonary insufficiency on the right ventricle after tetralogy repair. JThorac Cardiovasc Surg 1987;93:36-44. 9 Zakha KG, Homeffer PJ, Rowe SA, Neil CA, Manolio TA, Kidd L, et al. Long-term valvular function after total repair of tetralogy of Fallot. Circulation 1988;78(Suppl III):14-9. 10 Bove EL, Byrum CJ, Thomas FD, Kavey RE, Sondheimer HM, Blackman MS, et al. The influence of pulmonary insufficiency on ventricular function following repair of tetralogy of Fallot: evaluation using radionuclide ventriculography. J Thorac Cardiovasc
Surg 1983;85:691-6. 11 Niezen RA, Helbing WA, Wall EE van der, Geest RJ van der, Rebergen SA, Roos A de, et al. Biventricular systolic function and mass studied with MR Imaging in children with pulmonary regurgitation after repair of tetralogy of Fallot. Radiology 1996; 201:135-40.
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12 Carvalho JS, Shineboume EA, Busst C, Rigby ML, Redington AN. Exercise capacity after complete repair of tetralogy ofFallot: deleterious effects of pulmonary regurgitation. Br Heart J 1992; 67:470-3. 13 Jonsson H, Ivert T, Jonasson R, Holmgren A, Bjork VO. Work capacity and central hemodynamics 13 to 26 years after repair of tetralogy of Fallot. J Thorac Cardiovasc Surg 1995;110:416-26. 14 Lange PE, Onnasch DGW, BemardA, Heintzen PH. Left and right ventricular adaptation to right ventricular overload before and after surgical repair oftetralogy ofFallot. AmJCardiol 1982;50:786-94. 15 Kavey REW, Thomas FD, Byrum CJ, Blackman MS, Sondheimer HM, Bove EL. Ventricular arrhythmias and biventricular dysfunction after repair of tetralogy of Fallot. J Am Coll Cardiol 1984;4:126-31. 16 Yemets IM, Whlliams WG, Webb DG, Harrison DA, McLaughlin PR, Trusler GA, et al. Pulmonary valve replacement after late repair of tetralogy of Fallot. Ann Thorac Surg 1997;64:526-30. 17 Misbach GA, Turley K, Ebert PA. Pulmonary valve replacement for regurgitation after repair oftetralogy of Fallot. Ann Thorac Surg 1983;36:684-91. 18 Bove EL, Kavey REW, Byrum CJ, Sondheimer HM, Blackman MS, Thomas FD. Improved right ventricular function following late pulmonary valve replacement for residual pulmonary insufficiency or stenosis. JThorac Cardiovasc Surg 1985;90:50-5. 19 Oechslin EN, Harrison DA, Harris L, Downar E, Webb GD, Siu SS, et al. Reoperation in adults with repair of tetralogy of Fallot: indications and outcomes. J Thorac Cardiovasc Surg 1999; 118:245-51. 20 Warner KG, Anderson JE, Fulton DR, Payne DD, Geggel RL, Marx GR Restoration of the pulmonary valve after right ventricle volume overload after previous repair of tetralogy of Fallot. Circulation 1993;88:189-97. 21 Meijboom F, SzatmariA, Deckers JW, Utens EM, Roelandt JRTC, Bos E, et al. Cardiac status and health related quality oflife in the long term after surgical repair of tetralogy of Fallot in infancy and childhood. JThorac Cardiovasc Surg 1995;110:883-91. 22 Kirklin JK, Kirklin JW, Blackstone EH, Milano A, Pacifico AD. Effect of transannular patching on outcome after repair of tetralogy ofFallot. Ann Thorac Surg 1989;48:783-91. 23 Meijboom EJ, Valdes-Cruz L, Horowitz S, Sahn DJ, Larson DF, et al. A two-dimensional Doppler echocardiographic method for calculation of pulmonary and systemic blood flow in a canine model with a variable-sized left-to-right extracardiac shunt. Circulation
1983;68:437-45. 24 Died CA, Cazzaniga ME, Dubner SJ, Perez-Balino NA, Torres AR, Favaloro RG. Life threatening arrhythmias and RV dysfunction after surgical repair of tetralogy of Fallot. Circulation 1994; 90:7-12. 25 Wessel HU, Cunningham WJ, Paul MH, Bastanier CK, Muster AJ, Idriss FS. Exercise performance in tetralogy ofFallot after intracardiac repair. JThorac Cardiovasc Surg 1980;80:582-93. 26 Finck SJ, Puga FJ, Danielson GK Pulmonary valve insertion during reoperation for tetralogy of Fallot. Ann Thorac Surg 1988;45: 610-3. 27 Shimazaki Y, Blackstone EH, Kirklin JW. The natural history of isolated congenital pulmonary valve incompetence: surgical implications. Thorac Cardiovasc Surg 1984;32:257-9. 28 Norgard G, Gatzoulis MA, Moraes F, Lincoln C, Shore DF, Shinebourne, et al. Relationship between type of outflow tract repair and postoperative right ventricular diastolic physiology in tetralogy of Fallot. Implications for long-term outcome. Circulation
1996;94:3276-80. 29 Gatzoulis MA, Clark AL, Cullen S, Claus GH, et al. Right ventricular diastolic function 15 to 35 years after repair of tetralogy of Fallot. Circulation 1995;91:1775-81. 30 Friedli B. Electrophysiological follow-up of tetralogy of Fallot. Pediatr Cardiol 1999;20:326-30. 31 Gatzoulis MA, Till JA, Somerville J, Redington AN. Mechanoelectrical interaction in tetralogy of Fallot [QRS Prolongation relates to right ventricular size and predicts malignant ventricular arrhythmias and sudden death] Circulation 1995;92:231-7. 32 Rebergen SA, Chin JGJ, Ottenkamp J, Wall EE van der, Roos A de. Pulmonary regurgitation in the late postoperative follow-up of tetralogy of Fallot [Volumetric quantitation by NMR velocity mapping] Circulation 1993;88:2257-66.
Netherlands Heart Journal, Volume 9, Number 7, October 2001
