Objective
The tricuspid annular plane systolic excursion (TAPSE) as an echocardiographic index to assess right ventricular (RV) systolic function has not been investigated thoroughly in pediatric patients and adolescents with tetralogy of Fallot (TOF) after surgical repair.
Methods
TAPSE was determined in 131 patients with TOF and 252 age-matched normal subjects. TAPSE values were compared with RV ejection fraction (EF) and indexed RV end-diastolic volume (EDVi) determined by magnetic resonance imaging in a cross-sectional study design. TAPSE values were also correlated to QRS duration (QRSd) determined by electrocardiogram.
Results
The TAPSE values showed a positive correlation with age in normal subjects. The TAPSE was not decreased in infants and young children with TOF compared with normal subjects. A significant reduction of TAPSE values with increasing time after surgical repair was observed. After a mean of 7 years after surgical repair, the TAPSE values become significantly reduced compared with age-matched controls, being below the lower bound of –2 standard deviations. A positive correlation between TAPSE with RVEF and a negative correlation between TAPSE with RVEDVi were observed. A significant positive correlation was found between QRSd and RVEDVi, and a significant negative correlation was found between QRSd and RVEF.
Conclusion
Although TAPSE was initially preserved, impaired TAPSE was observed with increasing time after surgical repair in pediatric patients with TOF.
Tetralogy of Fallot (TOF) is the most common cause of cyanotic heart disease and accounts for 3.5% of infants born with congenital heart disease (CHD). Surgical relief of the right outflow tract obstruction using a transannular patch (TAP) can lead to pulmonary regurgitation (PR), which may lead to progressive right ventricular (RV) dilatation and dysfunction with age. It is therefore crucial to assess RV volume and systolic function in these patients. Quantification of RV size and systolic function by echocardiography was recently compared with contrast angiography and magnet resonance imaging (MRI). RV volume determined by MRI compared favorably with echocardiographic measurements in adults and pediatric patients. New indices for assessment of RV function have been published, including tricuspid annular plane systolic excursion (TAPSE), tricuspid annular peak systolic velocity (TAPSV), and the TEI index. TAPSE, obtained in M-mode, reflects the base to apex shortening of the RV in systole. American and European guidelines for chamber quantification have recommended that the assessment of RV systolic function should be part of the echocardiographic examination. A decreased TAPSE has been demonstrated to be associated with a poor prognosis in adults with heart failure. Reference values for adults and children of TAPSE measurements are available in the literature. The TAPSV, measured by tissue Doppler imaging, has also been suggested as a good quantitative parameter of RV systolic function. TAPSE is especially useful for the RV because these measurements have the potential to assess ventricular contractile function independently of the shape of the ventricle. Still, little is known about these methods in a selected pediatric patient group such as those with TOF. A correlation between RV dysfunction and prolonged QRS duration (QRSd) has been reported in patients with TOF and should be measured in all patients with TOF. The first objective of this study was to determine TAPSE values in patients with TOF after a TAP repair in early childhood. The data were compared with corresponding data sets measured in normal subjects. The second objective of this study was to compare TAPSE values with RV ejection fraction (EF) and RV indexed end-diastolic volume (EDVi) measured by MRI in our patients with TOF. The third objective was to determine QRSd and possible correlations of QRSd with RVEDVi, and RVEF values.
Materials and Methods
Patient Population
The TOF group consisted of 131 pediatric patients (69 male; 62 female) from infants to late after surgical repair for TOF in early childhood who were undergoing routine clinical follow-up. RV outflow tract was repaired by means of a TAP made of autologous untreated pericardium in all patients at a mean age of 8.2 months (range 3.2–18.4 months). The patients who had received a TAP repair were included in this study regardless of the degree of PR. The 131 patients with TOF were selected from among 272 patients with TOF regularly followed in our outpatient department. The patients were evaluated from the newborn age to the age of 28 years, at a time interval from 0 to 27.2 years after surgery. The patient group had a mild residual RV outflow tract gradient of 15 ± 8 mm Hg as determined by routine echocardiography. Patients with TOF with a higher degree of RV outflow tract obstruction and valvular or pulmonary artery (PA) branch stenosis were excluded from the study. Seven patients with restrictive physiology of the RV, defined as the presence of laminar antegrade diastolic main PA flow throughout the respiratory cycle by Doppler echocardiography were excluded from the study. Twenty-nine patients (22% of all patients with TOF) received an aorto-pulmonary shunt procedure before surgical repair. Patients with moderate to severe tricuspid regurgitation (TR) were excluded from this study because significant TR may lead to falsely normalized RV function by higher end-diastolic filling of the RV. In 88 patients (67% of all patients with TOF), the TAPSE could be compared with RVEF and RVEDV measured by MRI. The time interval between the MRI and TAPSE measurements was 76 ± 44 days. In a subset of 31 patients (35% of the MRI investigated patients with TOF), clinical follow-up and MRI investigation were performed on the same day. Recordings and measurements of the TAPSE, RVEDVi, and RVEF were performed without access to MRI data and vice versa.
The second group consisted of 252 (135 male; 117 female) healthy age-matched patients with a normal echocardiogram and a TAPSE inside published age-related normal z-score values. The patients were selected from healthy individuals referred to our cardiology service for evaluation of a heart murmur or family history of heart disease. The study group encompassed neonates to adolescents (age 1 day to 18 years; body surface area [BSA] 0.13–2.1 m 2 ) and was age-matched with our patients with TOF. In the group of patients aged more than 18 years, we could only collect 35 patients for age-matching of patients. For the purpose of the study, only echocardiograms with an official reading of completely normal study or completely normal study except for patent foramen ovale with a diameter of ≤ 2 mm were accepted for analysis. All patients with CHD or acquired heart disease or chromosomal syndromes were excluded from analysis. Patients were examined in a resting state without prior sedation. Infants were allowed to be bottle fed during the examination.
Echocardiographic Techniques
Echocardiograms were performed using echocardiographic systems (Sonos 7500 and iE33, Philips, Andover, MA) using transducers of 5-1, 8-3, and 12-4 MHz depending on patient size. Images were recorded digitally and later analyzed by one of the investigators (M.K.) using off-line software (Xcelera Echo; Philips Medical Systems, Eindhoven, The Netherlands). TAPSE was measured by two-dimensional echocardiography-guided M-mode recordings from the apical four-chamber view with the cursor placed at the free wall of the tricuspid annulus as previously recommended. Care was taken to align the sample volume as vertical as possible with respect to the cardiac apex. Maximal TAPSE was determined by the total excursion of the tricuspid annulus from its highest position after atrial ascent to the lowest point of descent during ventricular systole. The investigation of TAPSE was performed in a quiet state without sedation. Patients were classified as having RV pressure overload based on elevated tricuspid regurgitation velocities, RV outflow tract gradients, or systolic septal flattening. Patients were classified as having RV volume overload based on qualitative echocardiographic impression of RV dilation and the presence of diastolic septal flattening. The RV dimensions were evaluated by measuring the RV diameter on the two-dimensional images in the four-chamber view. The degree of PR was evaluated semiquantitatively using color Doppler and pulsed-wave Doppler mapping. PR was classified as severe (retrograde diastolic flow into the branch pulmonary arteries), moderate (retrograde diastolic flow in the main PA), and mild (regurgitant jet detectable in the RV outflow tract but no retrograde diastolic flow in the pulmonary trunk).
Magnetic Resonance Imaging
RV volumes were quantified by means of breath-hold segmented gradient-recalled echo sequences in 88 patients with TOF using a 1.5 T machine (Symphony, Siemens, Forchheim, Germany). This means that 67.2% of all 131 study patients with TOF have been investigated with MRI. The RV was encompassed by means of continuous short-axis views from base to apex. RV volumes were calculated after delineation of the endocardial surfaces of the end-diastolic and end-systolic images. The indexed value of RV end-diastolic volume (RVEDVi) > 150 mL/m 2 was defined on the basis of MRI data reported for adults and adapted for the pediatric age group and corresponded to 150% of the normal upper limit for RV end-diastolic volume in children, which is 100 mL/m 2 . EF was calculated as described previously. All volume and flow measurements were indexed for BSA and expressed in milliliters/beat/meters squared. Measurements were made by an individual (E.S.) blinded to the echocardiographic data.
Electrocardiogram
All patients had a 12-lead surface electrocardiogram at a speed of 25 mm/s and 1 mV/cm standardization. The maximum QRS duration in any lead was measured from the first to the last sharp vector crossing the isoelectric line. Nine patients were excluded from this study because of pacemakers for complete heart block, and 25 patients who received antiarrhythmic drugs were not included. Electrocardiograms were evaluated by a single investigator (P.F.) blinded to the results of echocardiographic measurements at the same time as TAPSE measurements were performed.
Statistical Analysis
All data were measured from three well-trained observers (M.K, B.H, and B.N.) from 3 to 5 consecutive beats and averaged as previously recommended. For data analysis, SAS 9.2 (SAS Institute Inc, Cary, NC) was used. The correlation structure between time after surgical repair and MRI determined RVEF in the TOF group was analyzed with Spearman’s nonparametric rank correlation coefficient. To analyze the difference between TAPSE values and the reference values of the control group, absolute deviations and ratios for the relative deviations were calculated. The cutoff value for the time period, where the TAPSE value is significantly (a = 0.05) lower than the reference value, was taken from a linear regression analysis. This was done by using the upper bound of a one-sided 95% CI of the mean value, which has to be lower than 0 for the absolute deviations and lower than 1 for the ratios. Significant difference of central levels of TAPSE values was tested by using the nonparametric Wilcoxon test for 2 samples at several ages. To consider interobserver variability, data were measured by 2 observers (M.K, B.N.) who were blinded to each others results. Intraobserver variability was considered in 16 participants by repeating the measurements on two occasions. Interobserver and intraobserver variability were examined with an intraclass correlation coefficient.
Ethics
This study complies with all institutional guidelines related to patient confidentiality and research ethics, including institutional review board approval. There are no financial or other potentially conflicting relationships to report.
Results
Demographic data of our 131 patients with TOF are summarized in Table 1 .
| Demographic data | |||
|---|---|---|---|
| Patients with TOF | Fulfill inclusion criteria | ( n ) | 131 |
| Female | ( n ) | 62 | |
| Age range | (y) | 0–28 | |
| BSA range | (m 2 ) | 0.19–2.21 | |
| NYHA | Class I | 102 | |
| Class II | 29 | ||
| Time of surgical repair | (mo) | 8.2 | |
| (Range; mo) | 3.2–18.4 | ||
| Aortopulmonary shunts | ( n ) | 29 | |
| (% of measured) | 22% | ||
| Echocardiography | |||
| TAPSE data | ( n ) | 131 | |
| Residual PS | (Mean ± SD; mm Hg) | 15 ± 8 | |
| PR | Mild ( n ) | 53 | |
| Moderate ( n ) | 47 | ||
| Severe ( n ) | 31 | ||
| MRI data | |||
| All patients with TOF | ( n ) | 88 | |
| RVEDVi | (Mean ± SD; mL/m 2 ) | 142.9 ± 40.9 | |
| (Range; mL/m 2 ) | 68–220 | ||
| RVEDVi > 150 mL/m 2 | ( n ) | 21 | |
| Subset of patients | ( n ) | 31 | |
| (% of all measured) | 35 | ||
| RVEDVi (mL/m 2 ) | (Mean ± SD; mL/m 2 ) | 136.7 ± 51.2 | |
| (Range; mL/m 2 ) | 79–203 | ||
| RVEDV > 150 mL/m 2 | ( n ) | 8 | |
| ECG | |||
| All patients with TOF | ( n ) | 131 | |
| QRS duration | (Mean ± SD; ms) | 136 (29) | |
| (Range; ms) | 70–210 | ||
| QRS duration < 100 ms | ( n ) | 32 | |
| QRS duration > 100 ms | ( n ) | 99 |
Data in Healthy Subjects
TAPSE values for the 252 age-matched control subjects are given for all age groups ( Table 2 ). TAPSE and age are strongly correlated in our control group: Spearman’s rank correlation coefficient was 0.94 for (age – TAPSE). No significant correlation was found between TAPSE and BSA ( r = 0.15; P = .09) or between TAPSE and time after surgical repair ( r = 0.02; P = .83) in our patients with TOF ( Table 3 ). There was no statistically significant difference of normal TAPSE values between female and male patients (data not shown). TAPSE normal values increase with age ( Figure 1 ).
| TAPSE (cm) | ||||||
|---|---|---|---|---|---|---|
| Control | TOF | |||||
| Age | n | Mean | −2 s | +2 s | n | Mean |
| 0–30 d | 8 | 0.9 | 0.7 | 1.1 | 4 | 1.4 |
| 1–3 mo | 16 | 1.1 | 0.8 | 1.4 | 8 | 1.3 |
| 4–6 mo | 8 | 1.3 | 1.0 | 1.6 | 4 | 1.3 |
| 7–12 mo | 18 | 1.4 | 1.1 | 1.8 | 9 | 1.3 |
| 1 y | 6 | 1.5 | 1.3 | 1.9 | 3 | 1.3 |
| 2 y | 9 | 1.7 | 1.4 | 1.9 | 5 | 1.6 |
| 3 y | 12 | 1.7 | 1.5 | 2.0 | 6 | 1.6 |
| 4 y | 14 | 1.8 | 1.6 | 2.1 | 7 | 1.6 |
| 5 y | 8 | 1.9 | 1.6 | 2.1 | 4 | 1.5 |
| 6 y | 10 | 1.9 | 1.6 | 2.2 | 5 | 1.5 |
| 7 y | 6 | 1.9 | 1.6 | 2.3 | 3 | 1.5 |
| 8 y | 10 | 2.0 | 1.7 | 2.3 | 5 | 1.7 |
| 9 y | 6 | 2.0 | 1.7 | 2.3 | 3 | 1.4 |
| 10 y | 6 | 2.1 | 1.8 | 2.3 | 3 | 1.5 |
| 11 y | 10 | 2.1 | 1.8 | 2.4 | 5 | 1.5 |
| 12 y | 12 | 2.1 | 1.8 | 2.4 | 6 | 1.5 |
| 13 y | 8 | 2.2 | 1.9 | 2.5 | 4 | 1.6 |
| 14 y | 8 | 2.3 | 1.9 | 2.6 | 4 | 1.6 |
| 15 y | 12 | 2.3 | 1.9 | 2.7 | 6 | 1.6 |
| 16 y | 20 | 2.4 | 2.0 | 2.8 | 10 | 1.6 |
| 17 y | 10 | 2.4 | 2.0 | 2.9 | 5 | 1.6 |
| ≥18 y | 35 | 2.5 | 2.0 | 2.9 | 22 | 1.5 |
| RVEDVi (mL/m 2 ) | RVEF (%) | BSA (m 2 ) | Age (y) | |
|---|---|---|---|---|
| TAPSE (cm) | ||||
| r | −0.35 | 0.47 | 0.15 | 0.02 |
| P | <.001 | <.0001 | .089 | .833 |
| n | 88 | 88 | 131 | 131 |
| QRS width (s) | ||||
| r | 0.66 | −0.83 | 0.76 | 0.81 |
| P | <.0001 | <.0001 | <.0001 | <0001 |
| n | 88 | 88 | 131 | 131 |
| RVEF (%) | ||||
| r | −0.68 | 1.00 | −0.63 | −0.64 |
| P | <.0001 | <.0001 | <.0001 | |
| n | 88 | 88 | 88 | 88 |
| Data of a subset of 31 patients with TOF in whom echocardiography and MRI measurements were performed on the same day | ||||
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