Study Design and Subjects

This study comprised two parts: (1) validation of VFM in the quantification of PR in patients with repaired ToF by CMR and (2) clinical application of VFM to determine PR in patients after biventricular repair of PAIVS and PS.

For the validation part, 14 patients with repaired ToF who were scheduled to undergo CMR as part of clinical follow-up for serial assessment of PR and RV function were studied. For the clinical application part, 14 patients with repaired PAIVS and 14 with repaired PS were recruited consecutively from the cardiac clinic, while 14 healthy subjects were recruited as control subjects. The period of study for the two parts extended from July 2014 to December 2016. The RV outflow could be imaged satisfactorily in all of the patients and control subjects. Exclusion criteria included significant residual PS as defined by a Doppler-derived systolic pressure gradient > 25 mm Hg and cardiac arrhythmias. Patients with significant residual PS were excluded because the presence of significant flow turbulence and aliasing of color Doppler velocity data would render VFM analysis inaccurate. The following clinical data were retrieved from the case notes: diagnosis, types of surgical and transcatheter procedures received, age at interventions, and duration of follow-up since biventricular repair. Body weight and height were measured, and the body mass index was calculated accordingly. Approval from the institutional review board and informed consent from all of the subjects were obtained.

Color Doppler and VFM

Color Doppler echocardiographic recording was performed using the ProSound Alpha 7 ultrasound machine (Hitachi Aloka, Tokyo, Japan). The color Doppler acquisitions were performed from the parasternal short-axis outflow tract view for assessment of pulmonary regurgitant flow. Images were saved digitally and transferred to an offline workstation for analysis with DAS-RS1 software (Hitachi Aloka). The average values of measurements from three cardiac cycles were obtained for statistical analysis.

VFM determines velocity vectors of forward and regurgitant blood flow on the basis of the continuity equation, taking into account velocities obtained by color Doppler and speckle-tracking echocardiography ( Figure 1 ), the principles of which have been reported previously. The color flow sector that focused on the RV outflow and proximal pulmonary trunk, obtained from the parasternal short-axis view, was reduced to maximize the frame rate to 30 to 60 frames/sec, the Nyquist limit was optimized to minimize aliasing, and care was taken to clearly image the wall of the main pulmonary trunk ( Figure 2 ). Intravascular flow vectors ( Figure 3 ) were calculated using the continuity equation, taking into account velocity components parallel to the ultrasound beam as determined from color Doppler mapping and those perpendicular to the ultrasound beam determined by speckle-tracking of wall motion as illustrated in Figure 1 . The PR time-flow curve ( Figure 4 ) was generated by placing a measuring line 5 mm distal to the pulmonary valve orifice. The velocities of blood flow and directions of flow were determined, and flow rate was derived by integrating the velocities along the measuring line. Forward and backward flow rates were calculated respectively during systole and diastole. The area under the time-flow curve was further calculated to obtain measures of forward and backward flow volumes. The pulmonary regurgitant ratio (PR _VFM ) was calculated as (backward flow volume/forward flow volume) × 100%. The derivation of VFM parameters in patients with ToF was performed with the investigator (V.W.L.) blinded to CMR findings.

The principle of VFM is illustrated. Flow within the pulmonary trunk is divided into grids of small squares. The vertical velocities V ₁ and V ₂ parallel to the ultrasound beam are derived by Doppler interrogation, while the horizontal velocity H ₁ is determined by two-dimensional speckle-tracking of vessel wall motion. The remaining horizontal velocity H ₂ is derived from the equation of continuity, according to which influx of blood into the square is equal to the outflux. Velocity vectors are then calculated on the basis of the vertical and horizontal velocities, and integration of the velocity vectors along the measuring line placed in the proximal pulmonary arterial trunk provides an assessment of the area flow rate of the bloodstream.

Color flow mapping of the pulmonary outflow during ventricular systole ( top ) and diastole ( bottom ) in a patient with repaired ToF and severe PR. The white dots encircle the region of interrogation.

VFM of the pulmonary outflow during systole ( top ) and diastole ( bottom ) of the same patient described in Figure 2 . The white dots encircle the region of interrogation, while the yellow arrows represent the velocity and direction of the vector flow.

The transpulmonary time-flow curves in a control subject ( top ) and a patient with severe PR ( bottom ). FV _b , Transpulmonary backward flow volume; FV _f , transpulmonary forward flow volume.

Severity of PR was also evaluated semiquantitatively on the basis of the size of color regurgitant jet and graded as mild, moderate, or severe. Mild PR was defined by the presence of a thin color jet, which measured usually <10 mm in length, with a narrow origin, while severe PR was characterized by a large color jet with a wide origin together with flow reversal flow in the branch pulmonary arteries. Moderate PR has a color jet width intermediate between the two together with absence of pulmonary arterial flow reversal. The ratio of PR color jet to RV outflow tract width was also calculated.

Cardiac Magnetic Resonance

The patients with ToF underwent CMR imaging using a 3-T Philips Achieva (Philips Healthcare, Best, The Netherlands) with an eight-channel torso coil within 2 months of echocardiographic assessments. Analyses of RV volumes and ejection fraction were obtained by balanced steady-state free precession cine images gated retrospectively and acquired at end-expiration on axial and short-axis planes. A dedicated CMR analyst contoured the right ventricle on the short-axis cine stack. Contours were cross-referenced with the axial cine stack. Flow analysis of the pulmonary artery was obtained using two-dimensional phase-contrast imaging (repetition time 4.7 msec, echo time 2.7 msec, slice thickness 8 mm, field of view 320 × 320 mm, matrix size 256 × 256, flip angle 10°, velocity encoding 200 cm/sec) and taking a plane perpendicular to the flow direction of the RV outflow tract just above the pulmonary valve but before bifurcation. RV function and flow analyses were performed using commercially available software (CMR42; Circle Cardiovascular Imaging, Calgary, AB, Canada). Pulmonary regurgitant fraction was calculated as (retrograde flow/antegrade flow volume) × 100% on the basis of the flow data obtained from the pulmonary arterial phase contrast sequence.

Statistical Analysis

All data are expressed as mean ± SD. For the validation study, relationships between VFM- and CRM-derived parameters were explored using Pearson correlation analysis. For the clinical application part, comparisons of continuous variables among groups were performed using simple analysis of variance, with post hoc comparison by the Bonferroni method. Categorical variables in three groups were analyzed using the Freeman-Halton extension of the Fisher exact test. Intra- and interobserver variability in measurements of pulmonary time-flow curves was assessed in 10 subjects, five patients and five control subjects, and reported as coefficients of variation. A P value < .05 was considered to indicate statistical significance. All statistical analyses were performed using SPSS version 22 (SPSS, Chicago, IL).

Validation Study in Patients with ToF

Fourteen patients with ToF (six men) aged 31.3 ± 7.3 years were studied. They had undergone surgical repair at 4.5 ± 3.3 years of age. Six patients had systemic-to-pulmonary arterial shunt palliation before total surgical repair, and seven required transannular patch repair of RV outflow. Pulmonary valve replacement was performed subsequently in five patients. Table 1 summarizes their demographics and CMR findings.

On the basis of semiquantitative assessment by color flow mapping, PR was absent in two, mild in two, moderate in five, and severe in five patients. A significant progressive increase in PR _VFM was found with increasing severity of PR (analysis of variance for trend, P < .001; Figure 5 ).

PR _VFM in repaired patients with ToF with different degrees of PR.

There were significant correlations between PR _VFM and CMR-derived pulmonary regurgitant fraction ( r = 0.95, P < .001) and RV end-systolic volume ( r = 0.84, P < .001; Figure 6 ).

Scatterplots showing associations between PR _VFM and (a) CMR-derived pulmonary regurgitant fraction and (b) RV end-diastolic volume.

Clinical Application in Patients with PAIVS and PS

Table 2 summarizes the demographic and clinical parameters of the patients and healthy control subjects. Of the 14 patients with PAIVS, eight had closed pulmonary valvotomy, three had RV outflow reconstruction, two had laser-assisted pulmonary valvotomy, and one had open pulmonary valvotomy as the initial intervention. Seven patients required additional balloon valvuloplasty, and two required surgical reconstruction of the RV outflow to relieve residual PS. Of the 14 patients with PS, 12 had undergone balloon valvuloplasty, and two had surgical valvotomy as the initial intervention. Two of the 14 patients required additional balloon valvuloplasty, and one required transannular patch repair of RV outflow. Color flow mapping showed mild tricuspid regurgitation in eight (36%) patients with PAIVS and two (14%) with PS. None of the patients had severe tricuspid regurgitation.

Table 2

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