Study Population

We included 106 consecutive adult patients referred for clinically indicated CMR and echocardiography at Tsukuba University Hospital between May 2012 and April 2016 in a retrospective study setting. Transthoracic 3D echocardiography, focused on the right ventricle, was performed within 1 month of CMR. Serum brain natriuretic peptide (BNP) level within 1 month of CMR was measured. The study was approved by a local institutional review committee, and all subjects provided informed consent.

Conventional Echocardiography and 2D Strain

Echocardiographic examinations were performed with an ARTIDA ultrasound system (Toshiba Medical Systems, Tochigi, Japan). A 5-MHz transducer was used for conventional 2D echocardiography. Our echocardiography laboratory is maintained according to guidelines established by the Japanese Society of Echocardiography. Left ventricular volume and ejection fraction were measured using the modified Simpson rule. RV diameter and function were also measured using a standard method that assesses basal RV linear dimension, midcavity RV linear dimension, fractional area change, tricuspid annular plane systolic excursion (TAPSE), and peak systolic velocity of the tricuspid annulus (S′) using a tissue Doppler method. Furthermore, 2D speckle-tracking for RV free wall longitudinal contraction was performed using an RV-focused four-chamber view (2D Wall Motion Tracking; Toshiba Medical Systems).

Three-Dimensional RV Echocardiographic Acquisition

Full-volume electrocardiographically gated 3D RV images with six subvolumes were acquired using an appropriate duration of breath holding with a matrix-array 3D transducer. Echocardiographers were trained to obtain 3D images of the entire right ventricle, including the RV inlet, apex, and outflow, using a dedicated bed with an adjustable cut-out section located at the left chest area for optimal probe access when obtaining high lateral apical views. The size of the ultrasonic scanning angle was set as small as possible to obtain a high temporal resolution of >20 volumes/sec. Data were stored and transferred to a computer (Inspiron 1300; Dell, Round Rock, TX) for offline analysis. RV 3D speckle-tracking echocardiographic images were analyzed using prototype software for dedicated RV assessment (Toshiba Medical Systems).

Three-Dimensional Wall Motion Tracking Algorithm for the Right Ventricle

Details of the 3D wall motion tracking algorithm for the right ventricle were reported previously. Five cross-sectional images were obtained: a four-chamber RV inlet-to-apex view, coronal apex-to-outflow view, and three axial views for the tricuspid annular plane, mid-RV level, and apical level, respectively ( Figure 1 , top ). The end-diastolic frame was chosen at the beginning of the QRS complex of the electrocardiographic monitoring signal. Endocardial borders were traced manually in the coronal plane and the three axial planes of the end-diastolic frame. RV trabeculations and papillary muscles were included in the intraventricular blood volume. For anatomically faithful segmentation, the attachment sites of the moderator band in the ventricular septum and anterior papillary muscle in the free wall, which are the landmarks that divide the inlet, outflow, and apex segments, can be adjusted manually. The software automatically tracks the voxel pattern of the speckles frame by frame in 3D space ( Figure 1 , bottom ). Ultimately, the software produces a complete data set comprising RVEDV, RVESV, RVEF, longitudinal strain, circumferential strain, and area strain ( Figure 2 ). Longitudinal strain was defined as the percentage change in regional length in the direction of the longitudinal axis of the endocardium, circumferential strain was defined as the percentage change in regional circumference of the endocardium, and area strain was defined as the percentage change of the regional area of the endocardium, which can be regarded as the product of both longitudinal strain and circumferential strain. Manual correction of the endocardial border was prohibited after tracking was completed. Each segmental data set could be deleted from the results of strain analysis if tracking quality was determined to be inappropriate by eyeball judgment. Temporal changes in strain data were obtained as time-strain curves ( Figure 2 ). We defined each strain measurement as the peak systolic strain value globally and in seven segments: inlet lateral, inlet inferior, inlet septum, outflow septum, outflow free wall, apical free wall, and apical septum. The SD of the time to peak area strain of the seven segments was measured as the RV dyssynchrony parameter.

Multiplanar view ( top ) of the 3D RV speckle-tracking echocardiographic model with segmentation into seven parts ( bottom ). The top panel shows multiplanar views of the four-chamber view (A) , coronal view (B) , and short-axis views (SAX) of the apex (C1) , apical-mid (C2) , mid (C3) , and base (C4) levels. Green lines indicate the manually traced endocardial border. The bottom panels show the reconstructed 3D RV endocardial wire model in which the mesh surface with dotted lines corresponds to the RV endocardium. Red solid lines indicate the borders of the seven segments, which consisted of the inlet lateral, inlet inferior, inlet septum, outflow septum, outflow free wall, apical free wall, and apical septum. (D) The RV free wall as viewed from the inferior side. (E) The septal wall side of the right ventricle (RV). The attachment of the anterior papillary muscle (PM) in the free wall ( D , red circle with arrows ) and the modulator band on septum ( E , blue circle with arrows ), which are defined as the boundary points among the inlet, outflow, and apex, can be modified manually. LA , Left atrium; LV , left ventricle; RA , right atrium; TV , tricuspid valve; VIF , ventriculo-infundibular fold.

Example of a 3D RV endocardial wire model and time-strain curves from a healthy subject and a patient with repaired TOF. The images in the top panels were acquired from the normal right ventricle of a healthy subject (A) and an impaired right ventricle (RV) from a patient with repaired TOF (B) . The bottom panels show the longitudinal, circumferential, and area time-strain curves in each vector. The normal right ventricle (A) shows sequential contraction from the inlet and ending in the outflow tract, with the outflow tract showing relatively circumferential dominant contraction. In contrast, the abnormal right ventricle of the patient with TOF (B) shows dyssynchronous contraction, in which systolic lengthening is indicated by the positive peaks on the strain curves, with mildly enlarged volumes.

In the validation study of 3D STE-derived RV volume and systolic function, RVEDV, RVESV, and RVEF were compared with those derived from CMR. To evaluate the significance of echocardiographic measurements, correlations between the CMR-derived RVEF and conventional echocardiographic parameters or 3D STE-derived strain measurements were assessed.

CMR for RV Volume and Function

CMR examinations were performed with a 1.5-T superconducting unit (Philips, Best, the Netherlands) with a phased-array cardiac coil. Electrocardiographically gated cine mode images using a steady state were obtained in a short-axis view with 10-mm slice thickness without an intersection gap. The acquisition time was 10 to 16 sec while patients held their breath. CMR images were analyzed using offline software (ViewForum; Philips). From short-axis images, we selected the slice that contained the tricuspid valve and the slice that contained the apex of the right ventricle. Subsequently, we manually traced the endocardial contour of the right ventricle for each slice from the tricuspid level to the apex level, respectively, in the end-diastolic phase. An automatic trace function was used to determine the RV endocardial line of all phases. All lines were checked by an observer and manually corrected where necessary. The software automatically calculated RV volume data in each phase. Minimum volume was defined as the RVESV. RVEF was calculated using RVEDV and RVESV as follows: RVEF = (RVEDV − RVESV) × 100/RVEDV.

Reproducibility of 3D Echocardiography

RVEDV, RVESV, RVEF, and global longitudinal, circumferential, and area strain from 3D STE were used to assess intra- and interobserver reproducibility. To test intraobserver variability, a single observer analyzed 10 selected RV data sets on two occasions separated by an interval of >1 month. To test interobserver variability, a second observer analyzed the data without knowledge of measurements made by the first observer. We expressed intraobserver and interobserver variability using the coefficient of variation, which was defined as the SD of the difference between intra- and interobserver measurements and the mean value of that measurement.

Statistical Analysis

Data are shown as mean ± SD, number (percentage), median (interquartile range), or mean with 95% CI. Comparisons between 3D speckle-tracking echocardiographic and CMR data were performed using paired t tests. Data were statistically analyzed using linear regression and Bland-Altman analysis to determine the bias and limits of agreement between the two modalities. Comparisons between the two groups were performed using Student’s t test for continuous variables and the χ ² test for categorical variables. Logarithmic transformation was performed for BNP analysis. The area under the receiver operating characteristic curve was calculated to determine the capability of echocardiographic parameters to detect CMR-derived RVEF impairment. A CMR-derived RVEF value of 30% has been shown to correlate with poor prognosis in previous studies and was therefore chosen as the cutoff value. Multivariate models were developed using stepwise regression with the Akaike information criterion to determine CMR-derived RVEF with regional RV strain. A P value < .05 was considered to indicate statistical significance. All statistical analyses were performed using JMP version 11 (SAS Institute, Cary, NC).

Baseline Characteristics

Analysis of RV volumes and function was feasible in 75 patients (70%). The remaining 31 patients (30%) were excluded because of suboptimal 3D echocardiographic image quality. Reasons for exclusion included an absence of RV outflow tract (RVOT) echo contours in 26 patients, mildly unclear images from the apex to anterior wall in three patients, and an incomplete scanning angle with which to obtain the entire right ventricle in two patients. Among the 31 patients who were excluded from the 3D echocardiographic analysis, 25 (80%) had satisfactory 2D apical acoustic windows for measurement of TAPSE, S′, fractional area change, and 2D RV strain. RV contour assessment took 3 to 5 min for a trained analyzer but only 9 sec for 3D speckle-tracking by computer. The background characteristics of excluded and included patients were similar in terms of age, sex, height, and weight. The volume rate on 3D full-volume echocardiographic imaging was 31.6 ± 3.2 volumes/sec (range, 22.1–37.2 volumes/sec). Of these 75 patients, 42% were men, the mean age was 40 ± 18 years (range, 18–70 years), and the mean body surface area was 1.59 ± 0.19 m ² ( Table 1 ). Thirty-nine patients (52%) had cardiomyopathy or pulmonary arterial hypertension, and the remaining 36 (48%) had congenital heart diseases, consisting of repaired tetralogy of Fallot (TOF) in 14, unrepaired TOF in two, and transposition of the great arteries with atrial switch in four and with arterial switch in two patients. A summary of RV size and function parameters measured by CMR, conventional 2D echocardiography, and the new 3D speckle-tracking echocardiographic analysis is presented in Table 2 .

Validation of CMR-Derived RV Volumetric Data and RVEF with 3D STE

RVEDV, RVESV, and RVEF showed strong relationships between CMR and 3D STE ( Figure 3 , left ; r = 0.94, r = 0.94, and r = 0.84, respectively, P < .001 for all). The Bland-Altman plot showed significant proportional underestimation bias for RVEDV (−9.1 mL, P = .002) and RVEF (−2.3%, P = .002) but not for RVESV (−1.7 mL, P = .099). The 95% limits of agreement between the two methods were −56.9 and 38.7 mL for RVEDV, −39.6 and 33.3 mL for RVESV, and −14.7% and 9.9% for RVEF ( Figure 3 , right ).

Correlation between RV volume and RVEF determined by 3D STE and CMR. The left panel shows correlation diagrams, and the right panel shows Bland-Altman plots for RV volume and RVEF. The top panel shows RVEDV data, the middle panel shows RVESV data, and the bottom panel shows RVEF data. The black solid lines in the left panels are regression lines of all measurements, and the black dotted lines indicate Y = X. The red solid lines in the right panels indicate the mean difference, the red dashed lines indicate the 95% range of mean difference, and the black dotted lines indicate the 95% limits of agreement (LOA). Red circles indicate patients with adult congenital heart disease (ACHD), and blue circles indicate patients with noncongenital structural heart disease. Echo , 3D STE; EDV , end-diastolic volume; ESV , end-systolic volume; MRI , magnetic resonance imaging; nACHD , non–adult congenital heart disease.

RV Function Measures Using CMR and Echocardiographic Methods

Moderate to modest correlations were found with respect to CMR-derived RVEF for global area strain ( r = −0.60, P = .004), global longitudinal strain ( r = −0.43, P < .001), global circumferential strain ( r = −0.32, P = .004), and fractional area change ( r = 0.34, P = .003). On the other hand, significant correlations were not observed for RV tissue Doppler imaging S′ ( r = 0.06, P = .75), TAPSE ( r = 0.02, P = .85), or RV free wall 2D strain ( r = −0.19, P = .07).

In patients with severely impaired right ventricles (CMR-derived RVEF ≤ 30%), RV strain was universally reduced for all vectors. The SD of time to peak area strain was significantly prolonged in the group with RV impairment compared with the group without RV impairment ( Table 2 ). Among the conventional echocardiographic parameters, only fractional area change decreased in the patients with severely impaired RV. On receiver operating characteristic analysis to determine the factors associated with severely impaired CMR-derived RVEF ( Table 3 ), only fractional area change and 3D strain for all vectors showed significant results. Among these parameters, 3D STE-derived RVEF showed the largest area under the curve (0.93, P < .001).

Association Between Regional RV Strain and CMR-Derived RVEF

Most regional RV strain values, except for apical longitudinal strain and septal circumferential strain, were associated with severe RV dysfunction as defined by RVEF ≤ 30% on CMR ( Table 4 ). By using stepwise variable selection in both longitudinal and circumferential strain, the inlet longitudinal strain and inlet circumferential strain, and the RVOT circumferential strain were selected as the independent variables ( Table 4 , middle row ). Among all strain values, inlet area strain and outflow circumferential strain were selected ( Table 4 , right row ).

Table 4

RV segmental strain and global systolic function

Strain	Univariate		Model 1 ( R 2 = 0.38)		Model 2 ( R 2 = 0.49)
	R 2	P	F	P	F	P
LS
Inlet	0.08	.012	4.32	.040		.601
Apex		.112
Outflow	0.07	.036		.606		.689
Septum	0.10	.007		.361		.421
CS
Inlet	0.17	<.001	8.73	.004		.326
Apex	0.08	.021		.464		.521
Outflow	0.25	<.001	14.00	<.001	17.70	<.001
Septum		.239
AS
Inlet	0.31	<.001			26.23	<.001
Apex	0.08	.002			3.16	.080
Outflow	0.27	<.001				.852
Septum	0.11	.004				.801

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