Study Subjects

The TGA-MS population consisted of all the adult subjects who were identified for strain-protocol echocardiography with the three apical RV views during routine adult congenital heart clinic visits from June 2010 to September 2012 at Duke University Medical Center. The patients with TGA-MS for this study were ambispectively identified, with subjects imaged before January 2012 retrospectively identified and those after that date prospectively enrolled. However, all subjects with TGA-MS in this study were imaged with the same echocardiographic protocol, including comprehensive RV apical acquisitions on the GE Vivid E9 (GE Vingmed Ultrasound AS, Horten, Norway) optimized for strain analysis, because the protocol was implemented in early 2010 for all patients with systemic right ventricles. This is believed to represent a consecutive capture of all subjects with TGA-MS imaged during this period. No subjects were excluded because of inadequate image quality. Health information and electrocardiograms were obtained from the medical record. A small subset of this population was previously described as pilot data.

The control population was prospectively enrolled from a population of healthy young adults recruited for a study to assess echocardiographic predictors of pulmonary edema when diving underwater. In the normal population, feasibility of the 18S RV strain analysis, normal ranges, and reproducibility were previously presented. A normal cohort ( n = 30) was age- and sex-matched to the TGA-MS population. All subjects underwent comprehensive screening echocardiography with the comprehensive apical RV views with strain analysis. Inclusion criteria for control subjects were age ≤18 years, no history of cardiac abnormalities, and normal echocardiographic findings, including anatomy, LV ejection fraction, fractional area change (FAC), and tricuspid annular plane systolic excursion (TAPSE). Exclusion criteria for control subjects were any abnormal echocardiographic findings, prolonged QRS duration, and serious systemic disease. This study was approved by the institutional review board at Duke, and all prospectively enrolled subjects provided informed consent.

Echocardiography with Comprehensive Apical RV Views

Echocardiography was performed with grayscale images optimized for longitudinal speckle-tracking strain analysis (50–90 frames/sec). Three apical RV views were obtained with the subject in the standard left lateral recumbent position. The three apical RV views have equivalent imaging planes to the four-, two-, and three-chamber LV apical views with the transducer angled rightward ( Figure 1 ), as previously published. To name the apical RV views, the view with the outflow tract (transducer notch at 1 o’clock) was named the RV outflow view. The view isolating the RV inflow and apical regions (transducer notch at 11 o’clock) was named the RV inflow view. The RV four-chamber view name was maintained (transducer notch at 3 o’clock). Optimizing these views often required repositioning of the transducer a few centimeters toward the axillary line from the typical LV-focused apical view and angling the imaging plane anteriorly and rightward. All echocardiographic studies were acquired with a Vivid E9 using a 3.5-MHz ultrasound probe. RV systolic function was also assessed by FAC and TAPSE.

Comprehensive RV 18S image acquisition. Center : a gross anatomic image of a short axis of the normal heart through the ventricles and the RV outflow tract (RVOT) looking toward the cardiac base. The three RV apical echocardiographic imaging planes are represented by the white lines ( arrowhead = transducer notch) and obtained by 60° counterclockwise transducer rotations starting from the four-chamber view. The three echocardiographic RV apical images are obtained from a patient with TGA-MS with moderate systemic RV dilation and systolic dysfunction. The wall numbering system is maintained through the figure (1 = septum, 2 = anterior septum, 3 = anterior free wall, 4 = lateral free wall, 5 = posterior free wall, 6 = posterior septum). TV , Tricuspid valve.

In the planning stage of this study, efforts were made to obtain high-quality short-axis views of the right ventricle for circumferential strain assessment. However, imaging of the anterior right ventricle was rarely adequate, and the decision was made to focus only on longitudinal strain in this study. Furthermore, the criteria for the classic pattern of ADI-MD were created using longitudinal strain and have never been studied with circumferential or short-axis strain analysis, even in the left ventricle.

Two-Dimensional Speckle-Tracking Strain Analysis

Offline strain analysis was performed using EchoPAC PC version BT11 (GE Vingmed Ultrasound AS). The reference point was placed at QRS onset to ensure that early systolic events were not missed. The systemic semilunar valve closure timing relative to the QRS complex was defined on spectral Doppler from the parasternal short-axis or apical view. The endocardial border was manually traced in end-systole for speckle-tracking. The region of interest was adjusted to exclude the pericardium. The integrity of speckle-tracking was automatically detected and visually confirmed. In case of poor tracking, tracing was readjusted or the shape of the region of interest changed. Segments with persistent inadequate tracking were excluded from analysis. Feasibility was determined as the percentage of all segments with adequate tracking. Segmental peak longitudinal systolic strain (PLS) was measured in six segments in each of the three RV views as peak strain between QRS onset and semilunar valve closure. These six segments included the basal, mid, and apical segments on the septal and RV walls, with a total of 18 segments from the three apical views.

The software calculated a segmental PLS score for each segment, and these were averaged from all 18 segments to produce global PLS. Segmental PLS was also averaged by walls (apical, septal, and free wall) to produce regional PLS. This software has been validated for the determination of global PLS in LV strain from the four-, two-, and three-chamber apical LV views, and those imaging places were maintained with our comprehensive RV views.

Because longitudinal peak strain is by convention a negative value (shortening in systole), the nomenclature of this report will refer to greater strain as a larger negative number (e.g., peak strain of −15% is greater than −5%, or peak strain −15% > −5%).

TTP Dyssynchrony Analysis

TTP intervals were measured as the duration from the onset of the QRS complex to the first distinct peak in a strain curve. One TTP measure of RV mechanical synchrony was the SD of this duration in all 18 segments (TTP _SD ). Another TTP measure was the maximum opposing wall interval (TTP _op ), measured as the maximal interval between the opposing walls in the mid or basal segments. TTP _SD ≥ 60 msec and TTP _op ≥ 130 msec were used as traditional predictors of CRT response in adults with LBBB cardiomyopathy.

Regional Strain Pattern Analysis

The methodology for LV regional strain pattern analysis has been published in a population with LBBB heart failure to identify a classic dyssynchronous contraction pattern reflective of a significant ventricular activation delay. The three criteria to define the classic pattern are (1) early peak contraction with early termination of shortening in at least one septal or apical segment and early stretching in at least one opposing wall segment, (2) early peak contraction occurring in the first 70% of the systolic ejection phase, and (3) late contraction after semilunar valve closure in the segment with early stretch. If these criteria are met in a single view, the classic pattern is diagnosed. Examples of this RV classic pattern in patients with TGA-MS are provided in Figure 2 .

Comprehensive RV strain pattern analysis of two subjects. (A) The three RV views in a patient with TGA-MS with classic-pattern dyssynchrony in the RV4 view. Early terminated peak septal contraction ( yellow arrow ) is opposed by early lateral free wall stretch ( blue arrow ), followed by late peak contraction ( red arrow ) after systemic semilunar valve closure (called AVC by the software). The yellow arrow identifies the early termination seen most prominently in the mid and apical septal segments ( dark blue and purple curves ). Less pronounced dyssynchrony was present in the RV inflow view ( far right ), without meeting criteria for the classic pattern. The early terminated posterior septal contraction ( yellow , light blue , and green curves ) does not peak before 70% of the systolic ejection phase. (B) The three RV views of a patient with TGA-MS with the classic-pattern criteria met only in the outflow view (criteria identified by arrows ). In the outflow view, the dyssynchrony is seen between the early terminated anterior septum ( red and dark blue curves ) and late activated posterior free wall ( green and light blue curves ). This classic pattern would have been missed if only the single RV4 view was analyzed. Segmental strain color definition: the RV4 and outflow views: basal septum ( red ), mid septum ( dark blue ), apical septum ( purple ), apical free wall ( green ), mid free wall ( light blue ), and basal free wall ( yellow ). In the inflow view, the colors are reversed because the transducer notch is at 11 o’clock (similar to the LV three-chamber view in the three LV views).

CRT

CRT was performed in three subjects with TGA-MS with FAC ≤ 25% who were dyssynchronous by TTP and had prolonged QRS durations on electrocardiography. Echocardiograms including 18S RV regional strain analysis were obtained before CRT and after CRT pacer optimization. Patients 1 and 2 had transvenous, dual-chamber pacemakers with LV septal leads before the addition of epicardial, unipolar leads placed in the basal region of the lateral RV free wall. Patient 3 had the same pre-CRT pacing system and was upgraded with the same epicardial RV lead, but it was placed in the basal region of the anterolateral free wall.

Statistical Analysis

Continuous variables are reported as mean ± SD and were compared using paired or unpaired t tests after visualizing the data to confirm normality. Categorical variables (reported as percentages) were tested for differences using χ ² tests. Univariate logistic regression was used to model predictors of the classic pattern. The r ² statistic was calculated to determine correlations between two linear variables using the Spearman rank correlation test. P values <.05 were considered to indicate statistical significance.

Interobserver variability of regional pattern analysis using the same cardiac cycle was performed on all 30 control subjects and the first 19 patients with TGA-MS by a second experienced reader blinded to the primary analysis. The strain curves were redrawn by the second reader de novo. In case of disagreements, subgroup analysis was based on the primary read. Statistical analyses were performed using Stata version 12 (StataCorp LP, College Station, Texas).

Population Characteristics

Subject characteristics for 30 control subjects and 25 patients with TGA-MS are reported in Table 1 . Control subjects were in the normal range for all electrocardiographic and echocardiographic measures. Patients with TGA-MS had at least moderate dilation or hypertrophy of the systemic right ventricle and prolonged QRS duration due to paced RBBB, intrinsic RBBB, or incomplete RBBB (RBBB morphology with QRS duration of 100–120 msec). Dysrhythmias were also frequently seen in the TGA-MS population, including ventricular tachycardia (16%), atrial fibrillation or flutter (64%), and other supraventricular tachycardias (24%). These dysrhythmias led to ablation procedures in 12 subjects (48%). Most subjects with TGA-MS were in New York Heart Association (NYHA) class II or III.

Functional Strain Analysis

Strain measurements are reported in Table 2 (global and regional) and Figure 3 (segmental). RV global PLS was significantly lower in the TGA-MS population, with 22 of 25 subjects (88%) demonstrating abnormal global PLS (<−17%). The regional differences in PLS between the free wall, apex, and septum seen in the control subjects ( P < .001) were not present in the TGA-MS population ( P > .50). Analyzing all 55 subjects, global PLS correlated well with TAPSE ( r ² = −0.80, P < .001) and FAC ( r ² = −0.75, P < .001) across the entire range of systolic RV function. Evaluating only the TGA-MS population ( n = 25), the correlation between global PLS and TAPSE ( r ² = −0.68, P < .001) or FAC ( r ² = −0.69, P < .001) is slightly lower but remains good.

Table 2

Echocardiographic measures of systemic RV function and contraction timing

	Control subjects ( n = 30)	Patients with TGA-MS ( n = 25)	P
Functional analysis
RV FAC (%)	42.2 ± 5.1 (35 to 57)	27.4 ± 7.4 (10 to 45)	<.001
RV TAPSE (mm)	21.7 ± 3.5 (16 to 30)	10.2 ± 3.1 (3 to 16)	<.001
RV global PLS	−23.3 ± 2.3% (−18 to −27)	−12.0 ± 4.0% (−3 to −20)	<.001
Septal PLS	−19.5 ± 2.0% (−15 to −24) ∗	−12 ± 4.1% (−1 to −24) †	<.001
Apical PLS	−21.9 ± 3.6% (−15 to −30) ∗	−11.6 ± 4.7% (−3 to −23) †	<.001
Free wall PLS	−27.7 ± 3.8% (−20 to −36) ∗	−12.0 ± 4.7% (0 to −22) †	<.001
Timing analysis
TTP SD (msec)	25.2 ± 7.9 (10 to 42)	80.5 ± 34.1 (28 to 140)	<.001
TTP SD > 60 msec	0	15 (60%)	<.001
TTP op ≥ 130 msec	0	19 (76%)	<.001
Classic pattern	0	11 (44%)	<.001

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