Patients

The University of Nebraska Medical Center institutional review board approved the study. One hundred two pregnant women were enrolled through an advertisement in our institutional news bulletin inviting participation in a longitudinal study of normal fetuses. Written informed consent was obtained from all recruited pregnant women. Inclusion criteria were maternal age ≥ 18 years; maternal body mass index 18.5 to 29.9 kg/m ² ; intact membranes; no history of medical, surgical, or obstetric complications; absence of labor; and normal fetal growth on the basis of US percentiles (estimated fetal weight [EFW] by 2D ultrasound between the 10th and 90th centiles). Fetuses with congenital or known genetic and chromosomal anomalies, heart failure, abnormal cardiac rhythm, or intrauterine growth retardation, as well as multiple-gestation pregnancies, were excluded from the study. Other exclusion criteria were maternal self-reported use of illegal drugs, maternal smoking, antepartum hemorrhage, proven chorioamnionitis, chronic maternal illness, and recent acute illness. Gestational age (GA) was determined by last menstrual period and had been confirmed by a first-trimester sonographic measurement of crown-rump length.

Fetal Ultrasound Acquisition

At enrollment, all pregnant women underwent detailed fetal echocardiographic evaluation in accordance with published guidelines. All images were obtained using a Vivid E9 ultrasound system (GE Medical Systems, Milwaukee, WI) with a C2-9 MHz broadband transducer. Two research sonographers, each with >7 years’ fetal echocardiography experience, performed all examinations (L.L., M.C.).

Images were optimized for gain, compression, depth, and sector width and acquired at frame rates of 70 to 110 frames/sec. Apical or subcostal four-chamber, LV basal and apical short-axis images were acquired. Anatomic landmarks were used to define the basal and apical short-axis levels. The basal level was defined by the mitral valve, and the apical level was defined as the segment of the left ventricle distal to the insertion of the moderator band on the ventricular septum, proximal to the apical cap. Data collected included maternal age, GA, maternal height and weight, fetal biparietal diameter, head circumference, abdominal circumference, femur length, and EFW.

Fetal Heart Orientation

Because of variable fetal position, fetal LV short-axis images are different from the standard postnatal transthoracic parasternal short-axis images. Therefore, fetal heart orientation was established using two parameters: the location of liver and the LV position in relation to the right ventricle. Accordingly, there are four types of orientation for fetal heart short-axis images: (I) the liver is toward the “left of the image” and the left ventricle is at the “bottom of the image,” similar to the traditional transthoracic short-axis image; (II) the liver is toward the “right of the image” and the left ventricle is at the “top of the image”; (III) the liver is toward the “right of the image” and the left ventricle is at the “bottom of the image”; and (IV) the liver is toward the “left of the image” and the left ventricle is at the “top of the image” ( Figure 1 ).

Four types of orientation for fetal heart short-axis images: (I) the liver is toward the “left of the image” and the left ventricle is at the “bottom of the image,” similar to the traditional transthoracic short-axis image; (II) the liver is toward the “right of the image” and the left ventricle is at the “top of the image”; (III) the liver is toward the “right of the image” and the left ventricle is on the “bottom of the image”; and (IV) the liver is toward the “left of the image” and the left ventricle is at the “top of the image.” RV , Right ventricle.

In orientation II, as viewed from the apex toward the base, the LV apex undergoes counterclockwise rotation, whereas the LV base rotates in the opposite direction, clockwise in systole ( Figure 2 A). In orientations III and IV, the fetal heart is viewed from the base toward the apex, so the LV apex rotates in the clockwise direction and the LV base rotates counterclockwise, which are opposite directions compared with orientations I and II ( Figure 2 B). Therefore, in orientations III and IV, the rotation and twist directions on software output were inverted.

The positional relationship between transducer, fetal position, and fetal heart location in the four types of orientation. (A) Left ventricle viewed from apex to base. (B) Left ventricle viewed from base to apex.

Fetal Twist and Torsion Analysis

The raw echocardiographic data sets were transferred from the ultrasound system to a computer workstation for semiautomated analysis (2D Cardiac Performance Analysis version 1.2.3.6 and Image Arena version 4.6; TomTec, Unterschleissheim, Germany). One experienced observer (L.L.) performed all analyses. The fetal cardiac cycle was decided on the basis of anatomic M-mode imaging by detecting atrioventricular valve and LV wall movement. One fetal cardiac cycle was selected from end-diastole to end-diastole. The LV endocardial surfaces were manually traced in basal and apical images using a point-and-click approach when the chamber was at its maximum size after diastole. The software, creating a region of interest, automatically generated an epicardial surface tracing. The region of interest was adjusted to fit the ventricular wall thickness before the automated tracking algorithm was applied. Tracking performance was reviewed to ensure accurate tracking of the ventricular myocardium, and when necessary, manual adjustments were made to the region of interest width and shape before the algorithm was reapplied. The software provided segmental and average values for rotational displacement in degrees on basal and apical views for one complete heart cycle.

LV counterclockwise rotation as viewed from the apex is expressed as a positive value, whereas clockwise rotation is expressed as a negative one. The data depicting basal and apical LV rotation from the software were imported into a custom spreadsheet (Microsoft Excel 2010, Microsoft, Redmond WA) and plotted as graphs (rotational displacement over time). The stepwise calculation of rotational mechanics is shown in Figure 3 with a representative example of apical and basal rotation and LV twist data obtained. Details of the custom Excel spreadsheet are shown in Supplemental Figure 1 (see the Appendix; available at www.onlinejase.com ). Twist is the net difference between apical and basal rotation (value of instantaneous apical rotation − basal rotation). Torsion is the twist value normalized to end-diastolic length, which was obtained from the four-chamber view, measuring from the center of a horizontal line connecting the hinge points of the mitral valve to the apex.

The stepwise calculation of rotational mechanics and a representative example of apical and basal rotation and LV twist data obtained.

To determine the reproducibility of fetal heart rotation, twist, and torsion parameters, a blinded second observer (M.C.) repeated fetal torsion assessment in 20 randomly selected studies, and the first observer (L.L.) repeated the analysis after a 3-month interval.

Statistical Analysis

All values are expressed as mean ± SD. Values of fetal LV strain, strain rate, rotation, twist, and torsion were evaluated against GA and EFW using linear and nonlinear regression. Although many fetuses were examined more than once, the primary analytic design was cross-sectional, in which only one examination per fetus was included. The examinations for any fetus seen more than once were randomized to allow nonbiased selection of a single examination to represent that fetus. The secondary design of the study was longitudinal, in which only those fetuses examined more than once were included. For each echocardiographic parameter, two-way analysis of variance on a general linear model was applied to determine if a “case effect” was present, in which the identity of the fetus carried a significant correlation with the parameter value independent of GA and EFW. Bland-Altman limit-of-agreement analysis was used to assess inter- and intraobserver reliability. Intraclass correlation coefficients were calculated to test measurement variability. P values < .05 were considered to indicate statistical significance. Statistical analyses were performed using SPSS version 17.0 (IBM, Armonk, NY) and Minitab version 16.0 (Minitab, State College, PA).

Feasibility (All 240 Examinations)

Sixty-five studies (37 with inadequate apical images and 28 with inadequate basal images) were excluded from the analysis. Technical issues in these 65 studies that precluded basal and apical image acquisitions were multifactorial and included ultrasound window limitations in 13 (20%), transducer-heart distance in nine (14%), high maternal body mass index in 18 (28%), placental interposition in five (8%), and unfavorable fetal position in 20 (31%). Measurement of rotational indices was feasible in the remaining 175 studies (73%). Demographic data are shown in Table 1 .

Fetal LV Strain and Strain Rate (Cross-Sectional Sample, 102 Examinations)

Global longitudinal strain (GLS), global circumferential strain, longitudinal strain rate, and circumferential strain rate were −22.3 ± 4.3%, −25.0 ± 6.1%, −1.4 ± 0.5 sec ⁻¹ , and −1.6 ± 0.5 sec ⁻¹ , respectively ( Table 2 ). There was no significant correlation of GLS or longitudinal strain rate with GA or EFW. Absolute value of global circumferential strain and circumferential strain rate declined moderately with GA and EFW ( P < .05; Figure 4 ).

Table 2

Fetal LV rotation, twist, torsion, strain, and strain rate

GA	n	Twist (deg)	Base rotation (deg)	Apex rotation (deg)	Torsion (°/cm)	GLS (%)	GCS (%)	LSR (sec− 1 )	CSR (sec− 1 )
Total		13.1 ± 2.3	−4.4 ± 1.1	9.5 ± 2.0	7.9 ± 3.4	−22.3 ± 4.3	−25.0 ± 6.1	−1.4 ± 0.5	−1.6 ± 0.5
15–19 wk + 6 d	25	13.9 ± 2.1	−4.4 ± 1.1	10.5 ± 2.0	12.0 ± 3.0	−22.3 ± 3.6	−27.0 ± 7.0	−1.5 ± 0.6	−1.8 ± 0.6
20–23 wk + 6 d	34	13.6 ± 2.2	−4.8 ± 1.3	9.7 ± 1.7	8.4 ± 1.9	−22.2 ± 4.7	−25.9 ± 5.8	−1.4 ± 0.5	−1.6 ± 0.4
24–27 wk + 6 d	18	13.0 ± 2.1	−4.2 ± 1.1	9.6 ± 2.0	6.0 ± 1.1	−21.2 ± 3.2	−23.0 ± 4.8	−1.5 ± 0.4	−1.4 ± 0.4
28–31 wk + 6 d	11	11.3 ± 1.9	−4.1 ± 0.9	7.9 ± 1.4	4.9 ± 1.1	−24.1 ± 3.9	−21.2 ± 4.0	−1.2 ± 0.3	−1.4 ± 0.3
32–35 wk + 6 d	8	11.7 ± 2.6	−4.5 ± 1.2	7.8 ± 2.3	4.5 ± 1.0	−22.6 ± 5.1	−26.7 ± 5.9	−1.4 ± 0.4	−1.7 ± 0.4
36–40 wk	6	12.1 ± 1.4	−3.9 ± 0.7	8.9 ± 1.6	3.8 ± 0.6	−23.3 ± 6.7	−22.9 ± 6.7	−1.3 ± 0.3	−1.5 ± 0.4

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