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Published online before print February 9, 2007, 10.1148/radiol.2431060213
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(Radiology 2007;243:212-219.)
© RSNA, 2007

Pediatric Imaging

Diastolic Function in Repaired Tetralogy of Fallot at Rest and during Stress: Assessment with MR Imaging1

Jochem van den Berg, MD, Piotr A. Wielopolski, PhD, Folkert J. Meijboom, MD, PhD, Maarten Witsenburg, MD, PhD, Ad J. J. C. Bogers, MD, PhD, Peter M. T. Pattynama, MD, PhD and Willem A. Helbing, MD, PhD

1 From the Department of Pediatric Cardiology, Sophia Children's Hospital (J.v.d.B., M.W., W.A.H.), and Departments of Radiology (J.v.d.B., P.A.W., P.M.T.P., W.A.H.), Cardiology (F.J.M.), and Cardiothoracic Surgery (A.J.J.C.B.), Erasmus Medical Center, Dr Molewaterplein 60, 3015 GJ Rotterdam, the Netherlands. Received February 3, 2006; revision requested March 31; revision received May 12; accepted June 7; final version accepted September 1. Address correspondence to W.A.H. (e-mail: w.a.helbing{at}erasmusmc.nl).


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively assess, with magnetic resonance (MR) imaging, right ventricular (RV) diastolic function after repair of tetralogy of Fallot (TOF) at rest and during pharmacologic stress and to study relationship between main pulmonary artery end-diastolic forward flow (EDFF) (indicative of restrictive RV physiology) and clinical status.

Materials and Methods: Institutional medical ethics committee approval and patient or parent informed consent were obtained. Patients with TOF corrected through the transatrial-transpulmonary approach underwent MR imaging at rest and during dobutamine stress and maximal exercise testing. Two-dimensional (2D) cine volumetric data were acquired. Flow measurements were performed with a standard 2D flow-sensitized sequence. MR imaging flow curves for tricuspid and pulmonary valves were combined into RV time-volume change curves, from which indexes of RV filling were derived. Patient results were compared with published data in control subjects. Student t tests, Mann-Whitney U tests, analysis of covariance, and paired and one-sample t tests were used.

Results: Thirty-six patients (mean age at repair, 0.9 year ± 0.5 [standard deviation]; median age at study inclusion, 17 years [range, 7–23 years]; 26 male and 10 female patients) were included. Abnormalities in RV filling included impaired relaxation (prolonged deceleration time, P = .002; smaller early filling fraction, P = .02) in the entire group compared with published data in healthy control subjects and signs of restriction to RV filling (smaller atrial filling fraction and higher early filling/atrial filling peak ratio, P < .05 for both) in patients with EDFF (n = 24) compared with patients without EDFF (n = 12). Stress response was abnormal in patients with EDFF, who developed impaired RV relaxation not appreciated at rest. Patients with EDFF had more severe pulmonary regurgitation (P < .05) and poorer exercise performance (P < .001).

Conclusion: In patients with TOF corrected with currently widely accepted surgical strategies, pulmonary artery EDFF relates to worse clinical state at mid- to long-term follow-up. Dobutamine stress imaging may unmask abnormalities in RV diastolic filling not appreciated with rest imaging alone.

© RSNA, 2007

Outcome after surgical correction of tetralogy of Fallot (TOF) is good, despite the presence of pulmonary regurgitation (PR) in the majority of patients (1,2). PR is initially well tolerated, but long-term negative effects of PR on right ventricular (RV) dimensions, RV systolic function, and exercise performance have been well documented (3,4). Diastolic dysfunction may precede systolic dysfunction and therefore may play a role in early detection of ventricular dysfunction. Different types of RV diastolic dysfunction have been reported in repaired TOF (5–8). Restriction to diastolic RV filling, indicated by end-diastolic forward flow (EDFF) in the main pulmonary artery, has been documented throughout follow-up (5–8). Reports have been equivocal on how restriction to RV filling affects functional outcome in TOF (5–8).

In most patients, RV diastolic filling can be evaluated by using the Doppler echocardiographic flow pattern across the tricuspid valve. However, in patients with PR, RV filling occurs through both the tricuspid and the pulmonary valves. In this setting, Doppler echocardiography cannot enable adequate quantification of total RV diastolic filling. Flow-sensitive magnetic resonance (MR) imaging techniques with the patient at rest have been successfully validated for the assessment of RV diastolic function in patients with PR (6). Stress imaging may provide additional information but, to our knowledge, has not been used to assess RV diastolic function in corrected TOF. Thus, the purpose of our study was to prospectively assess, by using MR imaging, RV diastolic function after repair of TOF at rest and during pharmacologic stress and to evaluate the relationship between EDFF in the main pulmonary artery (indicative of restrictive RV physiology) and clinical status.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Approval of the institutional medical ethics committee at Erasmus Medical Center was obtained. Informed consent was obtained from patients or parents (if patients were not of the legal age to provide consent). Forty patients were included between October 2002 and February 2004. Patients were selected on the basis of the following criteria: total TOF repair before the age of 2 years, repair with the transatrial-transpulmonary approach, no residual intracardiac shunt, and a residual RV outflow tract Doppler gradient of 40 mm Hg or less. One author (J.v.d.B.), using patient medical records, reviewed these criteria, as well as the presence of a transannular patch in the RV outflow tract and the use of medication. Patients with pulmonary atresia, absent pulmonary valve syndrome, or other associated heart defects were excluded. The preoperative parameters (arterial oxygen saturation, RV-aortic systolic pressure ratio, and hemoglobin substance concentration) shown in Table 1 were obtained from reports of diagnostic heart catheterization procedures. Patient height and weight were measured, and body surface area was calculated. The total population was subdivided into the following groups: Group 1 contained all patients with EDFF, and group 2 contained all patients without EDFF. EDFF was defined as being present when detected at rest in more than one time frame at end expiration. Independent of its volumetric amount, EDFF was considered pathologic and indicative of restriction to RV filling. Patient data obtained at rest were compared with published data in healthy control subjects (6) by one author (J.v.d.B.). Clinical state was assessed with cardiac MR imaging, which was used to evaluate the amount of PR, RV volume, and RV ejection fraction, and with maximal exercise testing.


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  		Table 1. Patient Characteristics

 
MR Imaging Protocol
Imaging was performed with a 1.5-T MR unit (Signa CVi; GE Medical Systems, Milwaukee, Wis) with version 8 and version 9.1 softwares and a four-channel phased-array cardiac coil. Standardized localizer imaging planes were acquired for flow measurements in the tricuspid valve, pulmonary valve, and inferior vena cava and a volumetric ventricular data set in the short-axis direction. Flow measurements were performed perpendicular to flow at end expiration during breath holding by using a standard two-dimensional flow-sensitized retrospectively gated sequence starting at the R-wave. Special attention was given to adequate electrocardiographic registration and triggering. Thirty cardiac phases were reconstructed retrospectively. Imaging parameters were as follows: two-dimensional fast spoiled gradient-echo sequence; repetition time msec/echo time msec, 6–7/3; flip angle, 20°; readout bandwidth, 90 KHz; section thickness, 6 mm; six views per segment; a rectangular field of view; and a scanning matrix of 256 x 128.

The volumetric data set was acquired with two-dimensional fast imaging by using a steady-state free precession sequence. Imaging parameters were as follows: flip angle, 45°; 3.4–3.6/1.4–1.7; section thickness, 8–9 mm; intersection gap, 0–1 mm; 12 views per segment; readout bandwidth, 111 KHz; a square field of view (30–34 cm); and an imaging matrix of 160 x 128. Twenty-four cardiac phases were reconstructed retrospectively.

Examinations were performed with the patient at rest and were repeated during dobutamine (Centra Farm Services, Etten-Leur, the Netherlands) stress with a maximal dosage of 7.5 µg per kilogram of body weight per minute. Heart rate (in beats per minute), heart rhythm, and blood pressure (in millimeters of mercury) were continuously monitored. Administration of dobutamine was decreased when heart rate increased more than 50%, when systolic and/or diastolic blood pressure increased or decreased more than 20%, when serious rhythm disturbances were seen, and when the patient complained of discomfort. No severe adverse effects of dobutamine necessitating discontinuation of the MR imaging examination were encountered.

MR Image Analysis
MR imaging data analyses were performed by one author (J.v.d.B.) with 1–3 years of MR imaging experience who was supervised by a second author (W.A.H.) with 10 years of MR imaging experience. Flow images were quantitatively analyzed by using software (Flow Analysis, version 2.0; Medis Medical Imaging Systems, Leiden, the Netherlands). Flow velocity curves were calculated by multiplying the manually drawn vessel and/or valve area on each time frame with the spatial average flow velocities. EDFF and PR (both in milliliters) were normalized for net forward flow volume and systolic forward stroke volume measured in the pulmonary artery, respectively. Presence of retrograde flow coincident with atrial systole was assessed in the inferior vena cava. The volume of tricuspid insufficiency was normalized for total forward flow across the tricuspid orifice. Volumetric data were analyzed by using another software (Mass Analysis, version 3.1; Medis Medical Imaging Systems). End-diastolic and end-systolic time frames were used, according to analysis techniques widely reported in the literature (9,10), to assess RV end-diastolic volume, end-systolic volume, stroke volume, ejection fraction, and wall mass.

Calculations
RV time-volume change curves were reconstructed by summing flow data from the main pulmonary artery and the tricuspid valve as previously described (6). Time-volume curves were obtained by integrating the time-volume change curves (Figure). If heart rates (trigger delays) during both measurements were not identical, the averaged heart rate (trigger delay) was calculated and used for the summed curves. From the RV curves, the following indexes of diastolic function were derived: (a) PEFR (in milliliters per second); (b) time to PEFR (in milliseconds) measured from end-systole; (c) early filling fraction, defined as volume increase (in milliliters) during the first one-third of diastole, normalized for ventricular stroke volume; (d) deceleration time (in milliseconds), which measures the time from PEFR to the extrapolation point of deceleration of flow to the baseline; (e) PAFR (in milliliters per second); (f) time to PAFR (in milliseconds), defined as time from end-systole to maximal increase in ventricular volume after atrial contraction; (g) atrial filling fraction, defined as the increase in ventricular volume after atrial contraction, normalized for ventricular stroke volume; and (h) the ratio of PEFR to PAFR (Figure). RV stroke volume (in milliliters) was defined as the maximal ventricular volume measured on the ventricular time-volume change curve.


Figure 1A
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  		Figure a: (a) RV time-volume change curve. (b) RV time-volume curve. AFF = atrial filling fraction, Dt = deceleration time, FF = early filling fraction (first one-third of diastole), PaFR = peak atrial filling rate, PeFR = peak early filling rate, TtPa = time to PAFR, TtPe = time to PEFR.

 

Figure 1B
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  		Figure b: (a) RV time-volume change curve. (b) RV time-volume curve. AFF = atrial filling fraction, Dt = deceleration time, FF = early filling fraction (first one-third of diastole), PaFR = peak atrial filling rate, PeFR = peak early filling rate, TtPa = time to PAFR, TtPe = time to PEFR.

 
Exercise Testing
So that we could assess peak workload (in watts) and peak oxygen consumption (as maximum oxygen consumption), all patients performed a maximal exercise test by using a stepwise incremental protocol on a bicycle ergometer (Jaëger Oxycom Champion System; Viasys Healthcare, Hoechberg, Germany) that allowed breath-by-breath ergometry. Patients were encouraged to perform until exhaustion. The respiratory quotient was used to objectify maximal performance (respiratory quotient more than 1.1 at peak exercise). Peak workload was compared with that in a reference population (11) by one author (J.v.d.B.).

Statistical Analysis
Results are expressed as means ± 1 standard deviation for normally distributed data; otherwise, medians and ranges are shown. Patient characteristics were compared between groups by using the Student t test or the Mann-Whitney U test. Diastolic MR imaging parameters were compared by using analysis of covariance with correction for heart rate and body surface area to deal with possible confounding introduced by age differences in this partly pediatric population. To meet the data considerations of analysis of covariance, all diastolic parameters except time to PEFR and early filling fraction had to be log10 transformed. Paired measurements were analyzed by using the paired t test. Analysis was performed for diastolic time-related parameters that were normalized for R-R interval duration and on PEFR and PAFR values that were normalized for RV stroke volume. Mean percentage of predicted workload (in watts) in the study population was compared with that in the reference population by using the one-sample t test. In our patients, the agreement between RV stroke volume as determined with tomographic cine MR imaging and RV stroke volume as determined with velocity-encoded MR imaging was evaluated by using intraclass correlation coefficients. Analysis was performed by using statistical software (SPSS, version 11.5; SPSS, Chicago, Ill). A P value of less than .05 was considered to indicate a statistically significant difference. No adjustments were made regarding the multiple tests performed.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patient Characteristics
Four patients with incomplete MR imaging data were excluded from the final analysis (see below). A review of the characteristics of the remaining 36 patients (26 [72%] male patients and 10 [28%] female patients) and of the patient subgroups (Table 1) indicated that patients did not take medication related to their cardiac condition. Insufficiency of the tricuspid valve indexed for forward flow across the valve (median, 4% [range, 1%–14%]) was found in 13 (36%) patients: eight patients in group 1 (median, 4% [range, 1%–14%]) and five patients in group 2 (median, 3% [range, 1%–7%]). Patients in group 1 showed a tendency toward larger RV volumes (P = .07 for RV end-diastolic volume and P = .09 for RV end-systolic volume).

MR Imaging
MR imaging data were incomplete because of bigeminy during stress in one patient and one or more missing or failed flow measurement in three patients. In our patients, the mean difference between RV stroke volume determined by using velocity-encoded MR imaging and RV stroke volume determined by using tomographic cine MR imaging at rest was –1 mL ± 8 (standard deviation). The resulting intraclass correlation coefficient was 0.98, indicating excellent agreement between both methods. Similarly, for RV stroke volume measured during stress, the mean difference was 4 mL ± 12. The associated intraclass correlation coefficient was 0.96, again indicating excellent agreement between both methods. RV free wall mass (in grams per meter squared) was larger in our patients compared with published values for control subjects (24 g/m2 ± 6 vs 17 g/m2 ± 2, P < .05) (9).

RV Diastolic Function
Patients had a longer mean deceleration time and a smaller early filling fraction compared with published data for control subjects (Table 2). This indicates impairment of RV relaxation. With stress (Table 3), increases in PAFR, atrial filling fraction, and deceleration time and decreases in time to PEFR, PEFR, and PEFR/PAFR ratio were seen. The change in filling pattern with stress is compatible with further impairment of RV relaxation.


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  		Table 2. RV Indexes of Diastolic Function at Rest

 

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  		Table 3. RV Indexes of Diastolic Function during Dobutamine Stress

 
Patients with and Those without EDFF
At rest, 24 (67%) patients showed EDFF (group 1). In 20 (83%) group 1 patients, flow was measured in the inferior vena cava, which showed retrograde flow coinciding with atrial contraction in 16 (80%) of these patients. Twelve (33%) patients did not have EDFF (group 2). In seven (58%) of these patients, inferior vena cava flow measurements were performed, and retrograde flow was found to be absent in all seven. Median contribution of EDFF to net forward flow in group 1 was 6% (range, 1%–24%) and did not change significantly during stress (median, 4% [range, 0%–18%]). In three patients in whom EDFF was present at rest, EDFF was absent during stress, while three patients without EDFF at rest showed EDFF during stress.

At rest, patients in group 2 had a larger mean atrial filling fraction, a smaller early filling fraction, a smaller PEFR/PAFR ratio, a higher PAFR, and a shorter time to PAFR compared with patients in group 1 (Table 2). Compared with published data in healthy control subjects, group 2 patients had a larger mean atrial filling fraction, a higher PAFR, a longer deceleration time, a smaller early filling fraction, and a smaller PEFR/PAFR ratio (Table 2). Patients in group 1 showed only a significantly longer deceleration time compared with published data in healthy control subjects.

With stress (Table 3), patients in group 1 showed increases in atrial filling fraction, PAFR, and deceleration time, while decreases were noted for early filling fraction, PEFR, PEFR/PAFR ratio (corrected for stroke volume), and time to PAFR. Patients in group 2 had a shorter time to PEFR during stress, with no marked changes in any of the other RV diastolic parameters.

Exercise Capacity
All patients successfully performed a maximal exercise test. Percentage of predicted workload for the total population was 92% ± 13, which is significantly (P < .01) smaller than the predicted 100%. In group 1, this percentage was 89% ± 11 (P < .001 compared with 100%), and in group 2, it was 97% ± 17 (P = .67 compared with 100%). Percentage of predicted workload was not significantly different (P = .08) between the subgroups. Mean maximum oxygen consumption was 39 mL/kg/min ± 9 in group 1 and 45 mL/kg/min ± 8 in group 2 (P = .09).


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
Our study results demonstrate that RV diastolic filling abnormalities are present in TOF at mid- to long-term follow-up, even in patients who underwent repair performed according to currently widely accepted surgical strategies. Diastolic filling results from (in part) active relaxation in early diastole and passive filling in the later parts of diastole. Compared with published data in control subjects, RV diastolic filling at rest in our total population demonstrated signs of impaired relaxation (prolonged deceleration time, smaller early filling fraction). EDFF, a generally recognized marker of restriction to RV filling (5,7,12), was found in two-thirds of our patients (group 1). Compared with patients in group 2 (no EDFF), patients in group 1 showed signs of restriction to RV filling, had more severe PR, and tended to have a more dilated RV. Furthermore, patients with EDFF had the poorest exercise performance compared with a reference population, and this finding was not explained by a difference in global systolic RV function. Moreover, in direct comparison with published data in control subjects, RV diastolic filling at rest was most abnormal in group 2. Somewhat to our surprise, considering the abnormal finding of EDFF, RV filling in group 1 was fairly normal compared with published data in control subjects. However, dobutamine stress imaging revealed important RV diastolic filling abnormalities in this subgroup that fit an increase in relaxation-related abnormalities. In the group without EDFF, RV diastolic filling did not change, although EDFF occurred during stress in three patients who did not have EDFF at rest.

EDFF and Outcome in Repaired TOF
The presence of EDFF, a marker of restriction to RV filling, immediately after TOF repair has been associated with longer intensive care unit and hospital stays (5). EDFF tends to disappear in the first weeks after repair (5) but has been shown to predict presence of EDFF at midterm follow-up (13). Reports have been equivocal on how restriction to RV filling, as evidenced by EDFF, affects long-term clinical state in repaired TOF. Gatzoulis et al (7) found that patients with EDFF had shorter PR duration, less cardiomegaly, and better exercise capacity; these findings suggest a protective effect of restriction to RV filling. Results of other studies (8,13,14) only partly confirmed these results. At long-term follow-up, our patients with EDFF had more severe PR than patients without EDFF and had worse exercise capacity than a reference population. In a small and somewhat younger population with TOF compared with ours, but with similar MR imaging techniques, another group (6) also found that exercise capacity was worse in patients with EDFF. This observation could not be explained by differences in the severity of PR, RV dilation, or RV global systolic function (6). In agreement with our study results, and somewhat unexpectedly, RV diastolic filling abnormalities at rest were most clear in patients without EDFF. Considering the abnormal finding of EDFF, we would expect most abnormal findings in patients with EDFF. In our study, the use of stress imaging unmasked highly abnormal RV filling in the EDFF-positive patients, a finding that may serve to explain the observed exercise limitation.

The differences in results between studies of RV diastolic filling in repaired TOF may be due to differences in the studied populations (age at repair, surgical techniques used, duration of follow-up since repair) and differences in the diagnostic tools used. We measured EDFF during breath holds at end expiration because EDFF at inspiration is also seen in healthy subjects. In 16 (80%) of 20 patients with EDFF in whom inferior vena cava flow was assessed, EDFF coincided with reverse inferior vena cava flow, a combination previously associated with restriction to RV filling (5,7). Detection of EDFF with MR imaging velocity mapping and that with Doppler echocardiography have been shown to be in good agreement (6). In contrast to echocardiography, flow-sensitized MR imaging offers volumetric flow quantification, which enables the inclusion of both tricuspid and pulmonary flow in the analysis of RV filling. Furthermore, we selectively studied patients who had undergone TOF repair according to current surgical strategies. Therefore, ventricular dysfunction cannot be ascribed to myocardial damage after extensive ventriculotomies, to long-standing prerepair hypoxemia, or to high RV pressures. Our results apply to patients with TOF with residual PR and mild to moderate pulmonary stenosis only. We thus avoid difficulties in interpretation of results due to mixed pressure and volume overload effects.

Mechanisms of RV Diastolic Dysfunction
The reasons for restriction to RV filling in patients with TOF remain unknown. Potential relationships have been reported with age at repair, staging and timing of repair, degree of preoperative pulmonary stenosis, and amount of postoperative PR (5,8,13,14). In our study, severity of PR was the only significantly different factor between patients with and those without EDFF. Mechanisms underlying abnormalities of diastolic filling are complex. Combined hypoxemia and pressure overload, which are present preoperatively in TOF, result in increased fibrosis of the RV (15). However, it is unknown how these preoperative factors contribute to postoperative diastolic abnormalities. Data on the effects of chronic volume overload on RV diastolic function are limited. Experimentally induced subacute PR has resulted in increased RV myocardial compliance (16), while RV diastolic function was well preserved after 3 months of RV volume overload in growing swine (17). Chronic left ventricular volume overload in rats resulted in diastolic filling abnormalities, with dynamic shifting of inflow patterns (18). These models, however, only partly mimic the chronic and progressive RV volume overload seen in patients with TOF. Left ventricular hypertrophy is a common cause of diastolic filling abnormalities and heart failure (19). The RV hypertrophy present in our patients with TOF could not be associated with a particular type of diastolic filling abnormalities.

Changes in Diastolic Function with Stress and Aging
Changes observed with dobutamine stress in our patients are compatible with impaired relaxation. This is a highly abnormal finding, because dobutamine is considered to improve diastolic relaxation (20,21). In response to dobutamine stress, healthy subjects show an increase in PEFR and/or PAFR, while the PEFR/PAFR ratio remains unchanged or increased (21,22).

In adults, relaxation-related impairment is observed with aging (23). In children, changes in diastolic function mainly appear during the first 3 years of life (24,25). Therefore, age is not a likely explanation for the differences found in diastolic filling between our subgroups.

Study Limitations
The evaluation of diastolic function should include indexes of isovolumic relaxation. However, in the absence of normal pulmonary valve closure, as is the case in most patients with surgically repaired TOF, isovolumic relaxation cannot be assessed.

Physical stress in the MR imaging environment has been reported to be feasible (26). We used pharmacologic stress because of the limited bore diameter of the available MR imaging unit. Ethical limitations involved in administering dobutamine to healthy children prevented their inclusion. Therefore, we compared our patient data at rest with published control data from a previous study performed in another center with another type of MR imaging system but with similar techniques (6).

A limitation of all noninvasive studies is the lack of pressure measurements. Increased RV filling pressures augment the effect of restriction to filling and may mask signs of impaired RV relaxation. However, RV end-diastolic pressure usually is normal in repaired TOF, as is pulmonary vascular resistance in the absence of pulmonary valve stenosis.

To quantify blood flow, we used phase velocity-encoded MR imaging, which is regarded as a valuable tool in congenital heart disease (27,28). Velocity-encoded MR imaging has many possible sources of errors, including the following: technical issues (mismatched encoded velocity, inadequate temporal resolution, inadequate spatial resolution, phase-offset errors, low signal-to-noise ratio), local flow and/or anatomy-related issues (accelerated flow, vessel motion), and issues of proper imaging plane delineation (valve motion, deviation of the imaging plane) (27,29,30). Proper sequence setup combined with careful planning can keep the overall error in the great vessels below 10% (27,30). We have shown that our RV stroke volume results determined with velocity-encoded MR imaging are in excellent agreement with those determined by using the current reference standard, multisection tomographic cine MR imaging.

Conclusion
In patients with TOF corrected according to currently widely accepted surgical strategies, EDFF in the pulmonary artery relates to a worse clinical state at mid- to long-term follow-up, as indicated by worse exercise capacity and more severe PR. Dobutamine stress imaging may unmask abnormalities in RV diastolic filling that are not appreciated at rest imaging alone.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   ACKNOWLEDGMENTS
 
We thank Rob J. van der Geest, MSc, Division of Image Processing, Department of Radiology, Leiden University Medical Centre, the Netherlands.


   FOOTNOTES
 

Abbreviations: EDFF = end-diastolic forward flow • PAFR = peak atrial filling rate • PEFR = peak early filling rate • PR = pulmonary regurgitation • RV = right ventricle • TOF = tetralogy of Fallot

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, J.v.d.B., W.A.H.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, J.v.d.B., F.J.M., A.J.J.C.B., W.A.H.; clinical studies, J.v.d.B., P.A.W., F.J.M., M.W., W.A.H.; statistical analysis, J.v.d.B., W.A.H.; and manuscript editing, J.v.d.B., P.A.W., M.W., A.J.J.C.B., P.M.T.P., W.A.H.


   References
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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