Tricuspid annular plane systolic excursion and right ...

Tricuspid annular plane systolic excursion and right ventricular ejection fraction in pediatric and adolescent patients with tetralogy of Fallot, patients with atrial septal defect, and age-matched normal subjects

Clinical Research in Cardiology ISSN 1861-0684 Volume 100 Number 1 Clin Res Cardiol (2010) 100:67-75 DOI 10.1007/s00392-010-0213z

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Author's personal copy Clin Res Cardiol (2011) 100:67–75 DOI 10.1007/s00392-010-0213-z

ORIGINAL PAPER

Tricuspid annular plane systolic excursion and right ventricular ejection fraction in pediatric and adolescent patients with tetralogy of Fallot, patients with atrial septal defect, and age-matched normal subjects Martin Koestenberger • Bert Nagel • William Ravekes • Allen D. Everett Hans Peter Stueger • Bernd Heinzl • Erich Sorantin • Gerhard Cvirn • Andreas Gamillscheg

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Received: 2 May 2010 / Accepted: 19 August 2010 / Published online: 12 September 2010 Ó Springer-Verlag 2010

Abstract Aims To determine whether TAPSE is an accurate marker of right ventricular (RV) systolic function in patients with tetralogy of Fallot (TOF) and patients with small atrial septal defect (ASD). The tricuspid annular plane systolic excursion (TAPSE) values were measured and compared with RV ejection fraction (EF). Methods and results A prospective study was conducted in pediatric and adolescent patients with TOF (n = 110), with isolated small secundum ASD (n = 200), and agematched patients with normally structured heart. The TAPSE values showed a positive correlation with age in both patients with ASD and normal subjects. No significant

difference of TAPSE values was seen in control subjects and age-matched ASD patients. The TAPSE was not decreased compared to normal subjects in eight infant TOF patients before corrective surgery. A reduction of TAPSE values with increasing time interval following corrective surgery was seen. After a mean of 7 years TAPSE values become significantly reduced compared to age-matched controls, being below the lower bound of the -2 SD. Conclusion In ASD patients the systolic RV function was preserved over the pediatric age group when compared to normal subjects. In contrast, although initially preserved, we found an impaired TAPSE with increasing postoperative period in our TOF patients. Keywords Tricuspid annular plane systolic excursion Right ventricular systolic function Pediatric patients Tetralogy of Fallot

M. Koestenberger (&) B. Nagel B. Heinzl A. Gamillscheg Division of Pediatric Cardiology, Department of Pediatrics, Medical University Graz, Auenbruggerplatz 30, 8036 Graz, Austria e-mail: [email protected]; [email protected] W. Ravekes A. D. Everett Division of Pediatric Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD, USA H. P. Stueger Data, Statistics and Risk Assessment, Austrian Agency for Health and Food Safety, Graz, Austria E. Sorantin Division of Pediatric Radiology, Department of Radiology, Medical University Graz, Graz, Austria G. Cvirn Institute of Physiological Chemistry, Centre of Physiological Medicine, Medical University Graz, Graz, Austria

Abbreviations ASD Atrial septal defect BSA Body surface area EF Ejection fraction LV Left ventricle EDV End-diastolic volume TOF Tetralogy of Fallot SD Standard deviation PR Pulmonary regurgitation PA Pulmonary artery RV Right ventricle MRI Magnetic resonance imaging NYHA New York Heart Association TAP Transannular patch TAPSE Tricuspid annular plane systolic excursion TR Tricuspid regurgitation

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Introduction The application of the tricuspid annular plane systolic excursion (TAPSE) as an additional echocardiographic tool to analyze right ventricular (RV) systolic function has been recently established in adults with and without acquired heart disease [1–5]. Measurement of the TAPSE has provided an opportunity to assess RV function in a simple, repeatable, and reproducible way [5, 6]. Studies on TAPSE in adults have demonstrated a strong correlation of TAPSE with RV ejection fraction (EF) measured by echocardiography [6, 7]. American and European guidelines for chamber quantification have also recommended that the assessment of RV systolic function should be part of the echo exam [4]. Adult reference values of TAPSE measurements are available in the literature [3, 6]. Recently we have published reference intervals of TAPSE values in the pediatric age group [8]. Little is known about TAPSE values in selected pediatric patient groups with congenital heart disease such as TOF. Nowadays patients with postoperative TOF are one important group among the increasing number of survivors of corrective cardiac surgery in early childhood [9]. Recently, a follow-up study has revealed a persistent postoperative RV systolic and diastolic dysfunction in this group of patients [10]. Therefore, the noninvasive evaluation of the RV volume and function is of great importance. Advancements in the field of cardiac MRI have established this technique as the ‘‘gold standard’’ for quantitative assessment of RV volume, and function in adults and pediatric patients [11–13]. However, these methods are time consuming and cannot be routinely performed without sedation in smaller children. A simple and reproducible test would be most advantageous. The first objective of this study was to determine TAPSE values in pediatric patients with TOF and to compare these values to pediatric patients with mild RV volume overload arising from pretricuspid left-to-right shunts (e.g., unrepaired isolated secundum ASD), and with age-matched normal subjects. Another objective was to compare the TAPSE values in our TOF patients to the RVEF measured with MRI.

Methods Patient population Group 1 The TOF group consisted of 110 pediatric patients (61 male; 49 female) before (n = 12) or after (n = 98) corrective surgery for TOF in early childhood and who were undergoing routine clinical follow-up. RV outflow tract was repaired by means of a transannular patch (TAP)

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Clin Res Cardiol (2011) 100:67–75

made of autologous untreated pericardium in all patients at a mean age of 8 month (range 3–15 month). The patients were evaluated in a cross-sectional study design from the newborn age to the age of 28 years. Patients were in NYHA class I (n = 81) or NYHA class II (n = 29) at the time of the study. The patients had only mild residual RV outflow tract mean systolic gradient of 15 ± 8 mmHg measured by echocardiography. TOF patients with a higher degree of RV outflow tract obstruction, valvular or pulmonary artery (PA) branch stenosis were excluded from the study. Patients with restrictive physiology of the RV (determined by presence of late antegrade diastolic flow in the MPA) were excluded from this study. Patients with moderate to severe tricuspid regurgitation (TR) were excluded from this study because significant TR may lead to falsely better determined RV function by higher enddiastolic filling of the RV. A history of supraventricular arrhythmias was present in six of our patients in group 1. Twenty-four of our patients (mainly adolescents and young adults) had received an aorto-pulmonary shunt procedure before corrective surgery. In 74 patients TAPSE could be compared with the RVEF measured by MRI. The time interval between the MRI and TAPSE measurement was 78 ± 46 days. The recordings and measurements of the TAPSE were performed without access to MRI data and vice versa. Group 2 The ASD group consisted of 200 patients (107 male, 93 female; age, 0–21 years) with unrepaired isolated secundum type ASDs with mild left-to-right shunting at atrial level and mild signs of RV volume overload. All ASD patients had normal RV systolic pressure as assessed by tricuspid regurgitation velocity (calculated from the modified Bernoulli equation) [14]. However, in ASD patients MRI measurements were not performed due to ethical reasons. Group 3 Control group consisted of 643 patients with a normal echocardiogram and a TAPSE inside the previously published age-related normal z-score values [8]. 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; BSA, 0.12–2.25 m2), including 41 neonates and 87 infants. 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 (PFO) with a diameter of less than or equal 2 mm and trivial left-to-right

Author's personal copy Clin Res Cardiol (2011) 100:67–75

shunt were accepted for analysis. All patients with congenital heart disease (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. Data from the control group was taken to calculate age-specific reference values respecting confidence bounds of TAPSE for a healthy population. Echocardiographic techniques Echocardiograms were performed with echocardiographic systems (Sonos 7500 and iE33, Philips, Andover, Mass, USA) using transducers of 5–1, 8–3, and 12–4 MHz depending on patients 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 2dimensional echocardiograph-guided M-mode recordings from the apical 4-chamber view with the cursor placed at the free wall of the tricuspid annulus as previously described [2]. Care was taken to align the sample volume as vertical as possible with respect to the cardiac apex. Angle correction and respiratory gating were not used. 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, and/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 fourchamber view. To consider interobserver variability, data were measured by three observers (M.K, B.H., and B.N.) who were blinded to each others results. Intraobserver variability was considered in 18 participants by repeating the measurements on two occasions. The variability was calculated as the mean percentage error, derived as the difference between the two sets of measurements, divided by the overall mean of the observed values by the two measurements. Observer variability was low with measured intraobserver variability of 3.5 ± 1.8% and interobserver variability of 3.9 ± 2.1%. Magnetic resonance imaging RV volumes were quantified by means of breath-hold segmented gradient-recalled echo sequences in 74

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postoperative TOF patients (67.3% of all 110 TOF patients) using a 1.5-T machine (Symphony, Siemens, Forchheim, Germany). 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. Multiplication of the delineated cavity area with the slice thickness yielded the slice volume, and summarization of all slice volumes yielded ventricular volume at end diastole and end systole. The indexed value of RV enddiastolic volume [150 ml/m2 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/m2 [11, 15]. Ejection fraction was calculated as stroke volume divided by end-diastolic volume and multiplied by 100. Based on the published normal for RVEF of 61 ± 7% [16], for the purpose of this study, we arbitrarily defined an RVEF of 40–50% as mildly decreased RV function, RVEF 30–40% as moderately decreased, and RVEF \30% severely decreased RV function. All volume and flow measurements were indexed for BSA and expressed in ml/(beat m2). Measurements were made by an individual (E.S.) blinded to the echocardiographic data. 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 [2]. For data analysis SAS 9.2 was used. The correlation structure between age 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 as well as ratios for the relative deviations were calculated. The cut-off value for the age, 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% confidence interval 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 two samples at several ages. Ethics This study complies with all institutional guidelines related to patient confidentiality and research ethics including institutional review board approval (No. 20-294 ex 08/09). There are no financial or other potentially conflicting relationships to report.

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Table 1 Classification table for the TAPSE values of our control patients

Table 2 TAPSE mean values of control subjects, patients with ASD, and TOF

Age

Age

n

TAPSE (cm) Mean

±2s (95%)

Control

ASD

TOF

Mean

-2s

n

Mean

n

Mean

0–30 days

41

0.91

0.68 (1.15)

0–30 days

0.911

0.677

18

0.936

3

1.355

1–3 months

45

1.14

0.85 (1.42)

1–3 months

1.135

0.849

22

1.223

5

1.313

4–6 months 7-12 months

20 22

1.31 1.44

1.01 (1.65) 1.13 (1.77)

4–6 months 7–6 months

1.311 1.444

1.007 1.130

11 10

1.360 1.480

3 4

1.265 1.343

1 years

25

1.55

1.25 (1.88)

1 year

1.549

1.251

3

1.270

3

1.337

2 years

39

1.65

1.36 (1.94)

2 years

1.655

1.365

9

1.710

5

1.562

3 years

27

1.74

1.48 (2.02)

3 years

1.744

1.478

12

1.782

6

1.593

4 years

47

1.82

1.56 (2.07)

4 years

1.817

1.561

7

1.899

4

1.618

5 years

29

1.87

1.60 (2.13)

5 years

1.866

1.605

9

1.857

4

1.458

6 years

41

1.90

1.62 (2.18)

6 years

1.905

1.622

17

1.824

5

1.496

7 years

32

1.94

1.64 (2.25)

7 years

1.937

1.637

11

1.882

3

1.545

8 years

23

1.97

1.67 (2.28)

8 years

1.973

1.670

10

1.840

5

1.800

9 years

20

2.01

1.73 (2.30)

9 years

2.011

1.727

7

1.917

2

1.355

10 years

27

2.05

1.79 (2.31)

10 years

2.054

1.786

2

2.060

3

1.500

11 years

25

2.10

1.83 (2.36)

11 years

2.096

1.827

3

2.147

5

1.488

12 years

18

2.14

1.84 (2.43)

12 years

2.140

1.836

7

2.049

6

1.545

13 years

20

2.20

1.85 (2.54)

13 years

2.195

1.850

6

2.192

4

1.593

14 years 15 years

35 25

2.26 2.33

1.87 (2.65) 1.93 (2.75)

14 years 15 years

2.259 2.328

1.873 1.934

7 5

2.229 2.428

4 2

1.560 1.645

16 years

34

2.39

1.98 (2.78)

16 years

2.391

1.982

8

2.219

10

1.630

17 years

27

2.45

2.04 (2.88)

17 years

2.446

2.036

9

2.292

3

1.564

18 years

21

2.47

2.05 (2.91)

18 years

2.472

2.036

3

2.603

5

1.476

[18 years

2.472

2.036

4

2.250

16

1.451

For the purpose of the study only echocardiograms with an official reading of completely normal study were accepted for analysis. The values in the classification table are: for each age group the standard deviation (s) of TAPSE was taken to construct ranges of the mean ± 2s. These ranges represent the expectable normal intervals of deviation for a certainty level of 95% TAPSE tricuspid annular plane systolic excursion, s standard deviation

Results The mean TAPSE values and the ±SD for the 643 control subjects are given for all age groups (Table 1). TAPSE and age are strongly correlated in our control group: Spearman’s rank correlation coefficient was 0.93 for (age– TAPSE). There was no statistically significant difference of normal TAPSE values between female and male patients (data not shown). No significant difference between female and male was found also for our TOF and ASD patients. In patients with small secundum type ASD TAPSE values were not statistically different from those of normal children (Table 2). Representative M-Mode images of a normal TAPSE (patient with normal RV and LV function), and of a decreased TAPSE (17-year-old TOF patient) are shown in Fig. 1a and Fig. 1b, respectively.

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The values in the classification table are: in control subjects for each age group the mean of TAPSE and the -2s was taken, for the ASD and TOF patients the number of patients (n) and the mean TAPSE values are shown for all investigated age groups TAPSE tricuspid annular plane systolic excursion, ASD atrial septal defect, TOF tetralogy of Fallot

In ASD patients TAPSE values increase with age similar to TAPSE normal values (Fig. 2). For patients above 18 years of age reference data from healthy adults were chosen for the normal group [3]. In infant TOF patients TAPSE values were slightly but not significantly increased compared to normal subjects. TAPSE values of postoperative TOF patients show a different course. A reduction of TAPSE values with increasing time interval following corrective surgery was seen. TAPSE values become significantly reduced after a mean of 7 years postoperative compared to the lower bound of the -2 SD of age-matched control patients (Fig. 2). The absolute deviation of measured TAPSE values of TOF patients was calculated compared to TAPSE reference values (Fig. 3). In TOF patients a negative correlation (r = -0.76; p = \ 0.05) can be seen between the duration of the postoperative period and the TAPSE values.


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Fig. 1 Apical 4-chamber view. a The white broken line indicates M-Mode cursor placement at the tricuspid lateral annulus. Representative M-Mode image of the tricuspid annular plane systolic excursion (TAPSE) in a patient with normal right and left ventricular function. The absolute longitudinal displacement measure is shown as the red line. The yellow arrow marks the upper and lower measure point of 1 cm. b Representative M-Mode image of the tricuspid annular plane systolic excursion (TAPSE) in a 17-year-old patient with TOF and a decreased TAPSE. The absolute longitudinal displacement measure is shown as the red line. The green arrow shows the decreased TAPSE value and flat course of the excursion

Of the MRI investigated postoperative TOF patients the RVEF was normal in 11 patients, mildly diminished in 38 patients, moderately diminished in 16 patients, and severely diminished in 9 patients (Fig. 4). Correlation between echocardiography measurements of TAPSE and MRI measurements of RVEF was weak (n = 74, r = 0.50). In our postoperative TOF patients measured by MRI a relevant RV volume overload was proofed by a

mean indexed RV end-diastolic volume (EDV) of 143.9 ± 40.7 ml/m2 (range 68–259 ml/m2).

Discussion Study of systolic function of the right side of the heart, especially in children, has been limited for many years,

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Fig. 2 Relationship between age and TAPSE values for control group resp. ASD and TOF patients. The interpolated mean values of control group are given as the black solid line. The -2 standard deviation line (-2s) of the control group measurements is given as a blue smooth-dashed line. The interpolated TAPSE values of the ASD patient group are given as a light green dashed line. Above the age of 21 years data of ASD patients is missing. The interpolated TAPSE values of the TOF patient group are given as the red solid line. TAPSE tricuspid annular plane systolic excursion, TOF tetralogy of Fallot, ASD atrial septal defect

Fig. 3 Deviation of TAPSE values in TOF patients from reference values versus increasing postoperative time period. The TAPSE value data points are given as black dots. a Shows the absolute deviation of the measured TAPSE values of TOF patients compared to TAPSE reference values. The difference of TAPSE values is expressed in centimeter (cm). The black solid line is an interpolation for a linear trend for the TOF patients. TAPSE tricuspid annular plane systolic excursion, TOF tetralogy of Fallot

mainly because assessment of the RV form and function is conceptually and technically more difficult than of the left ventricle (LV) [17]. Recently, publications have shown that TAPSE measurement is more reproducible than other echocardiographic indices of RV systolic function [4], and has a high specificity for detecting abnormal RV systolic function in adults [2, 18] and in patients with heart failure [19]. This parameter can therefore be considered a physiologic index of RV systolic function. In healthy adults it

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Fig. 4 Relationship between age and RVEF mean values (in %) of TOF patients are given as a typical scatter plot. The TAPSE value data points are given as black dots. The black solid line is an interpolation for a linear trend for the TOF patients. TOF tetralogy of Fallot, RV right ventricle, EF ejection fraction

has been shown that the tricuspid annulus has the greatest motion along its lateral aspect [20]. In adults the largest TAPSE values were found when RV and LV systolic function were normal [21]. To date these adult studies describe the usefulness of TAPSE to diagnose RV systolic dysfunction; it has been shown that a TAPSE of less than 2 cm indicates a RVEF of less than 40% [21, 22]. Heart rate has been shown not to have an influence on the longitudinal motion of the atrioventricular annuli in children [23]. Therefore, its usefulness can be extended to the pediatric age group. Only few studies of TAPSE measurements in infants and children exist [8, 23, 24]. Comprehensive data on TAPSE in pediatric patients with TOF and ASD are lacking. In this study TOF was chosen as the type of CHD of interest because of frequent RV dysfunction, abnormal wall motion, and distorted ventricular geometry. ASD patients were chosen because of the usually preserved RV function despite mild RV volume overload. Because of the lack of a simple measurement of RV performance, this was a clinical study correlating conventional indexes of RV function with the TAPSE. Systolic velocity of the tricuspid annulus of the RV free wall, as a concurrent measurement of RV function, has been shown to be a reliable indicator of the global RV systolic function [25, 26]. Harada et al. [27] showed that for patients with TOF after repair the mean velocity during systolic ejection was lower compared with age-matched control subjects. In a group of 22 patients who underwent repair of TOF, Toyono et al. [28] also demonstrated decreased RV myocardial velocities compared with 27 agematched control subjects. By employing pwTDI to the tricuspid annulus, it is possible to analyze the TAPSV. Meluzin et al. [26] demonstrated that TAPSV \11.5 cm/s


is able to predict RV impairment. In a recent study, multivariable analyses demonstrated that both TAPSE and TAPSV were good predictors of worse mid-term outcomes in patients with dilated cardiomyopathy [29]. Normal values of myocardial velocities have been published for healthy children [25], and TAPSV have been reported to be abnormal in patients with CHD [30]. A nonsignificant correlation was described by Kjaergaard et al. [31] between the RVEDV and the RVEF while the TAPSE significantly correlated with the RVEF determined by MRI. TAPSE and TAPSV have been shown to inversely correlate with the RV end-diastolic diameter [32]. Strain echocardiography, as a new noninvasive imaging of the RV, has also been shown to allow accurate noninvasive assessment of RV function in patients with pulmonary artery hypertension [33] and TOF [34, 35]. Since the tricuspid valve moves toward the RV apex during ventricular systole as lengthwise shortening of the RV free wall, it is intuitively evident that TAPSE must be somewhat related to systolic RV function. We evaluated systolic RV function using the TAPSE and the RVEF measured by MRI in our TOF patients. In infant TOF patients before corrective surgery the TAPSE was slightly but not significantly increased compared to age-matched controls. This might be related to RV hypertrophy of the TOF patients before corrective surgery. The systolic RV function seems to be preserved in those patients. With increasing time interval following corrective surgery for TOF the TAPSE values decrease compared to age-matched control patients. After a mean of 7 years TAPSE values become significantly reduced compared to age-matched controls, being below the lower bound of the -2 SD. The RVEF in our TOF patients was investigated using the MRI. Cardiac MRI has emerged as a powerful tool in the noninvasive imaging of cardiac structure and function, and has shown to have advantages over other noninvasive imaging modalities such as echocardiography or computed tomography [36–38]. The low TAPSE values in our TOF patients after a mean of 7 years patients could be confirmed by corresponding low RVEF. This is in good agreement with recent studies showing RV systolic and diastolic dysfunction in adult TOF patients [10, 39, 40]. TAPSE deviated increasingly from normal subjects with increasing age of TOF patients, but did not significantly decrease over time in absolute terms. Interestingly the mean TAPSE value of normal 1-year-old children is 1.55 cm, with very similar mean TAPSE value of 1.56 cm in a 17-year-old TOF patient. In our subjects with a decreased TAPSE a positive but weak correlation was seen between TAPSE and the RVEF measured by MRI. An explanation of the only weak correlation could be a global RV dyssynchrony which only partially affects RV longitudinal function. This is in agreement with recent data by Morcos et al. [41], showing

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a weak correlation of TAPSE and RVEF determined by MRI. In our ASD patients with only mild RV volume overload we could not find significant differences of TAPSE values compared to our age-matched control subjects. TAPSE may provide good indirect parameter of systolic RV function. Especially in smaller children, in whom the ‘‘gold standard’’ MRI requires deep sedation, the TAPSE may become useful to easily assess systolic RV function in follow-up of pediatric patients with TOF.

Limitation The population described in the present study is relatively heterogeneous and small since patients have been enrolled by only two centers. However, the study included a respectable contemporary cohort of TOF patients. We cannot exclude the possibility that the patient population enrolled in this study is biased toward more significant residual lesions after TAP repair for TOF. Nevertheless, our study reflects an overview of TOF patients from initial diagnosis to TOF patient’s years after TAP repair in early childhood in a cross-sectional study design.

Conclusion In TOF patients awaiting corrective surgery, the TAPSE was similar than in the age-matched control group. With increasing age of the TOF patients and with an increasing time period from the corrective surgery TAPSE values significantly decreased compared to control subjects. Low TAPSE values as indicators for an impaired systolic RV function could be confirmed by lower RVEF measurements. In our ASD patients with mild left-to-right shunting no significant differences of TAPSE values compared to our age-matched control subjects were seen. In our opinion, TAPSE deserves further clinical investigation. Acknowledgments There are no financial relationships relevant to this article to disclose. Conflict of interest of interest.

The authors declare that they have no conflict

References 1. Gupta S, Khan F, Shapiro M, Weeks SG, Litwin SE, Michaels AD (2008) The associations between tricuspid annular plane systolic excursion (TAPSE), ventricular dyssynchrony, and ventricular interaction in heart failure patients. Eur J Echocardiogr 9:766–771

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Author's personal copy 74 2. Ghio S, Recusani F, Klersy C, Sebastiani R, Laudisa ML, Campana C, Gavazzi A, Tavazzi L (2000) Prognostic usefulness of the tricuspid annular plane systolic excursion in patients with congestive heart failure secondary to idiopathic or ischemic dilated cardiomyopathy. Am J Cardiol 85:837–842 3. Lamia B, Teboul JL, Monnet X, Richard C, Chemla D (2007) Relationship between the tricuspid annular plane systolic excursion and right and left ventricular function in critically ill patients. Intensive Care Med 33:2143–2149 4. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pelikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ, Chamber Quantification Writing Group, American Society of Echocardiography’s Guidelines, Standards Committee, European Association of Echocardiography (2005) Recommendations for chamber quantifications: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18:1440–1463 5. Miller D, Farah MG, Liner A, Fox K, Schluchter M, Hoit BD (2004) The relation between quantitative right ventricular ejection fraction and indices of tricuspid annular motion and myocardial performance. J Am Soc Echocardiogr 17:443–447 6. Kaul S, Tei C, Hopkins JM, Shah PM (1984) Assessment of right ventricular function using two-dimensional echocardiography. Am Heart J 107:526–531 7. Popescu BA, Antonini-Canterin F, Temporelli P, Giannuzzi P, Bosimini E, Gentile F, Maggioni AP, Tavazzi L, Piazza R, Ascione L, Stoian I, Cervesato E, Popescu AC, Nicolosi GL, GISSI-3 Echo Substudy Investigators (2005) Right ventricular functional recovery after acute myocardial infarction: relation with left ventricular function and interventricular septum motion. GISSI-3 echo substudy. Heart 91:484–488 8. Koestenberger M, Ravekes W, Everett A, Stueger HP, Heinzl B, Gamillscheg A, Cvirn G, Boysen A, Fandl A, Nagel B (2009) Right ventricular function in infants, children and adolescents: reference values of the tricuspid annular plane systolic excursion (TAPSE) in 640 healthy patients and calculation of z-score values. J Am Soc Echocardiogr 22:715–719 9. Berdat PA, Immer F, Pfammatter JP, Carrel T (2004) Reoperations in adults with congenital heart disease: analysis of early outcome. Int J Cardiol 93:239–245 10. Abd El Rahman MY, Abdul-Khaliq H, Vogel M, AlexiMeskischvili V, Gutberlet M, Hetzer R, Lange PE (2002) Value of the new Doppler-derived myocardial performance index for the evaluation of right and left ventricular function following repair of tetralogy of Fallot. Pediatr Cardiol 23:502–507 11. Lorenz CH (2000) The range of normal values of cardiovascular structures in infants, children, and adolescents measured by magnetic resonance imaging. Pediatr Cardiol 21:37–46 12. Grison A, Maschietto N, Reffo E, Stellin G, Padalino M, Vida V, Milanesi O (2007) Three-dimensional echocardiographic evaluation of right ventricular volume and function in pediatric patients: validation of the technique. J Am Soc Echocardiogr 20:921–929 13. Helbing WA, Bosch HG, Maliepaard C, Rebergen SA, van der Geest RJ, Hansen B, Ottenkamp J, Reiber JH, de Roos A (1995) Comparison of echocardiographic methods with magnetic resonance imaging for assessment of right ventricular function in children. Am J Cardiol 76:589–594 14. Yock PG, Popp RL (1984) Noninvasive estimation of right ventricular systolic pressure by Doppler ultrasound in patients with tricuspid regurgitation. Circulation 70:657–662

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Clin Res Cardiol (2011) 100:67–75 15. Vliegen HW, van Straten A, Roest AA, Schoof PH, Zwinderman AH, Ottenkamp J, van der Wall EE, Hazekamp MG (2002) Magnetic resonance imaging to assess the hemodynamic effects of pulmonary valve replacement in adults late after repair of tetralogy of Fallot. Circulation 106:1703–1707 16. Lorenz CH, Walker ES, Morgan VL, Klein SS, Graham TP (1999) Normal human right and left ventricular mass, systolic function, and gender differences by cine magnetic resonance imaging. J Cardiovasc Magn Reson 1:7–21 17. Redington AN (2002) Right ventricular function. Cardiol Clin 20:341–349 18. Meluzin J, Spinarova L, Dusek L, Toman J, Hude P, Krejci J (2003) Prognostic importance of the right ventricular function assessed by Doppler tissue imaging. Eur J Echocardiogr 4:262–271 19. Karapolat H, Demir E, Bozkaya YT, Eyigor S, Nalbantgil S, Durmaz B, Zoghi M (2009) Comparison of hospital-based versus home-based exercise training in patients with heart failure: effects on functional capacity, quality of life, psychological symptoms, and hemodynamic parameters. Clin Res Cardiol 98:635–642 20. Kukulski T, Hubbert L, Arnold M, Wranne B, Hatle L, Sutherland G (2000) Normal regional right ventricular function and its change with age: a Doppler myocardial imaging study. J Am Soc Echocardiogr 13:194–204 21. Lopez-Candales A, Rajagopalan N, Saxena N, Gulyasy B, Edelman K, Bazaz R (2006) Right ventricular systolic function is not the sole determinant of tricuspid annular motion. Am J Cardiol 98:973–977 22. Lee CY, Chang SM, Hsiao SH, Tseng JC, Lin SK, Liu CP (2007) Right heart function and scleroderma: insights from tricuspid annular pane systolic excursion. Echocardiography 24:118–125 23. Arce O, Knudson O, Ellison M, Baselga P, Ivy D, DeGroff C, Valdes-Cruz L (2002) Longitudinal motion of the atrioventricular annuli in children: reference values, growth related changes, and effects of right ventricular volume and pressure overload. J Am Soc Echocardiogr 15:906–916 24. Promphan W, Attanawanit S, Wanitkun S, Khowsathit P (2002) The right and left ventricular function after surgical correction with pericardial monocusp in tetralogy of Fallot: mid-term result. J Med Assoc Thai 85(Suppl 4):1266–1274 25. Frommelt PC, Ballweg JA, Whitstone BN, Frommelt MA (2002) Usefulness of Doppler tissue imaging analysis of tricuspid annular motion for determination of right ventricular function in normal infants and children. Am J Cardiol 89:610–613 26. Meluzin J, Spinarova L, Bakala J, Toman J, Krejcı´ J, Hude P, Ka´ra T, Soucek M (2001) Pulsed Doppler tissue imaging of the velocity of tricuspid annular systolic motion; a new, rapid, and non-invasive method of evaluating right ventricular systolic function. Eur Heart J 22:340–348 27. Harada K, Toyono M, Yamamoto F (2004) Assessment of right ventricular function during exercise with quantitative Doppler tissue imaging in children late after repair of tetralogy of Fallot. J Am Soc Echocardiogr 17:863–869 28. Toyono M, Harada K, Tamura M, Yamamoto F, Takada G (2004) Myocardial acceleration during isovolumic contraction as a new index of right ventricular contractile function and its relation to pulmonary regurgitation in patients after repair of tetralogy of Fallot. J Am Soc Echocardiogr 17:332–337 29. Di Mauro M, Calafiore AM, Penco M, Romano S, Di Giammarco G, Gallina S (2007) Mitral valve repair for dilated cardiomyopathy: predictive role of right ventricular dysfunction. Eur Heart J 28:2510–2516 30. Watanabe M, Ono S, Tomomasa T, Okada Y, Kobayashi T, Suzuki T, Morikawa A (2003) Measurement of tricuspid annular diastolic velocities by Doppler tissue imaging to assess right


31.

32.

33.

34.

35.

36.

ventricular function in patients with congenital heart disease. Pediatr Cardiol 24:463–467 Kjaergaard J, Petersen CL, Kjaer A, Schaadt BK, Oh JK, Hassager C (2006) Evaluation of right ventricular volume and function by 2D and 3D echocardiography compared to MRI. Eur J Echocardiogr 7:430–438 Chrustowicz A, Gackowski A, El-Massri N, Sadowski J, Piwowarska W (2010) Preoperative right ventricular function in patients with organic mitral regurgitation. Echocardiography 27:282–285 Filusch A, Mereles D, Gruenig E, Buss S, Katus HA, Meyer FJ (2010) Strain and strain rate echocardiography for evaluation of right ventricular dysfunction in patients with idiopathic pulmonary arterial hypertension. Clin Res Cardiol 99(8):491–498 Knirsch W, Dodge-Khatami A, Kadner A, Kretschmar O, Steiner J, Bo¨ttler P, Kececioglu D, Harpes P, Valsangiacomo Buechel ER (2008) Assessment of myocardial function in pediatric patients with operated tetralogy of Fallot: preliminary results with 2D strain echocardiography. Pediatr Cardiol 29:718–725 Scherptong RW, Mollema SA, Blom NA, Kroft LJ, de Roos A, Vliegen HW, van der Wall EE, Bax JJ, Holman ER (2009) Right ventricular peak systolic longitudinal strain is a sensitive marker for right ventricular deterioration in adult patients with tetralogy of Fallot. Int J Cardiovasc Imaging 25:669–676 Grothues F, Smith GC, Moon JC, Bellenger NG, Collins P, Klein HU, Pennell DJ (2002) Comparison of interstudy reproducibility of cardiovascular magnetic resonance with two-dimensional echocardiography in normal subjects and in patients with heart failure or left ventricular hypertrophy. Am J Cardiol 90:29–34

75 37. Grothoff M, Spors B, Abdul-Khaliq H, Adb El Rahman M, AlexiMeskishvilli V, Lange P, Felix R, Gutberlet M (2006) Pulmonary regurgitation is a powerful factor influencing QRS duration in patients after surgical repair of tetralogy of Fallot. A magnetic resonance imaging (MRI) study. Clin Res Cardiol 95:643–649 38. Schroeder J, Peterschroeder A, Vaske B, Butz T, Barth P, Oldenburg O, Bitter T, Burchert W, Horstkotte D, Langer C (2009) Cardiac volumetry in patients with heart failure and reduced ejection fraction: a comparative study correlating multi-slice computed tomography and magnetic resonance tomography. Reasons for intermodal disagreement. Clin Res Cardiol 98:739–747 39. Vogel M, Sponring J, Cullen S, Deanfield JE, Redington AN (2001) Regional wall motion and abnormalities of electrical depolarization and repolarization in patients after surgical repair of tetralogy of Fallot. Circulation 103:1669–1673 40. Oosterhof T, Tulevski II, Vliegen HW, Spijkerboer AM, Mulder BJ (2006) Effects of volume and/or pressure overload secondary to congenital heart disease (tetralogy of Fallot or pulmonary stenosis) on right ventricular function using cardiovascular magnetic resonance and B-type natriuretic peptide levels. Am J Cardiol 97:1051–1055 41. Morcos P, Vick GW 3rd, Sahn DJ, Jerosch-Herold M, Shurman A, Sheehan FH (2009) Correlation of right ventricular ejection fraction and tricuspid annular plane systolic excursion in tetralogy of Fallot by magnetic resonance imaging. Int J Cardiovasc Imaging 25:263–270

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