Background
There is a paucity of data on left ventricular (LV) rotational physiology, twist, and torsional mechanics in preterm infants. The principal aims of the present study were to assess the feasibility and reproducibility of measuring LV rotation, twist, and torsion in preterm infants (<29 weeks’ gestation) using two-dimensional speckle-tracking echocardiography and to examine the changes in those parameters over the first week after birth.
Methods
This was a prospective observational study involving preterm infants <29 weeks’ gestation. Echocardiographic evaluations were performed on days 1, 2, and 5 to 7 after delivery. LV basal and apical rotation, LV twist, LV twist rate (LVTR), and LV untwist rate (LVUTR) were measured from the basal and apical short-axis parasternal views and calculated using two-dimensional speckle-tracking echocardiography. Torsion was also calculated by normalizing LV twist to LV end-diastolic length. One-way repeated-measures analysis of variance was used to compare values across the three time points. Intra- and interobserver reproducibility were assessed using Bland-Altman analysis and the intraclass correlation coefficient.
Results
Fifty-one infants with a mean ± SD gestational age of 26.8 ± 1.5 weeks and a mean birth weight of 945 ± 233 g were included. There was high intra- and interobserver reproducibility for basal and apical rotation, LV twist, and LV torsion, with intraclass correlation coefficients ranging from 0.78 to 0.96 ( P < .001 for all). Intra- and interobserver intraclass correlation coefficients for LVTR and LVUTR ranged from 0.70 to 0.88 ( P < .001 for all). Apical rotation remained constant over the first week of age in a positive counterclockwise fashion (11.8 ± 5.0° vs 12.1 ± 6.1° vs 11.7 ± 8.3°, P = .92). Basal rotation changed from counterclockwise on day 1 to clockwise on day 7 (median, 5.5° [interquartile range, −0.3° to 8.3°] vs 4.0 [interquartile range, −4.7° to 7.2°] vs −4.5° [interquartile range, −5.8° to −2.3°], P < .001), with resultant net increases in twist and torsion ( P < .05). There was no change in LVTR ( P = .60), but LVUTR increased across the same time period ( P = .01).
Conclusions
Assessment of twist, LVTR, and LVUTR is feasible in preterm infants, with acceptable reproducibility. There are increases in LV twist and torsion in addition to LVUTR, suggesting changes in LV mechanics during the first week of age.
Left ventricular (LV) twist is the wringing motion of the left ventricle during systole and is the net result of the rotation of the apex and the base in opposite directions along the long axis of the left ventricle. LV torsion is twist normalized to LV length at end-diastole. This wringing motion improves the ejection of blood from the LV cavity during systole. LV untwist is the recoil during early diastole, thereby generating a suction force for LV filling. LV twist is facilitated by the helical arrangement of the subepicardial (left-handed) and subendocardial (right-handed) fibers and is influenced by contractile function and loading conditions. LV untwist contributes directly to early diastolic filling and is influenced by muscle fiber compliance and elastic recoil properties. These rotational parameters can add important information on myocardial performance.
LV rotational mechanics can be assessed by two-dimensional (2D) speckle-tracking echocardiography (STE) at the bedside in an intensive care unit. This technique has been validated against both magnetic resonance imaging tissue tagging and Doppler tissue imaging. Two-dimensional STE is also angle independent and is the selected modality for measuring LV rotation in older populations. Recent studies have established rotational mechanics values and patterns in healthy pediatric populations and the change in rotational mechanics after exercise in children and in children with a variety of cardiopulmonary disease states. Despite the growing application of 2D STE in children and neonates, there is a lack of data on LV rotation and twist mechanics in preterm infants. The rotational mechanics of the left ventricle could potentially be different in the preterm population because of differences in myocardial contractile properties, different loading conditions, and the interaction between the left and right ventricles, especially during the transitional period.
The primary aim of this study was to assess the clinical feasibility and reproducibility of apical and basal rotation, LV twist and torsion, and LV twist rate (LVTR) and LV untwist rate (LVUTR) measurements in hemodynamically stable preterm infants <29 weeks’ gestation. The secondary aim was to assess the physiologic adaptations of rotational and twist parameters across three time points during the first week of age. We hypothesized that the measurement of rotational mechanics in the preterm population is feasible and reproducible. In addition, we hypothesized that those parameters undergo important changes in the first week after delivery.
Methods
This was a prospective observational study carried out in the neonatal intensive care unit of the Rotunda Hospital (Dublin, Ireland). All infants <29 weeks’ gestation were considered eligible for the study. Infants were excluded if they were small for gestational age (weight less than the 10th centile for any given gestation), received inotropes or inhaled nitric oxide in the first 48 hours of age, died within the first 7 days of age, had suspected or definite chromosomal abnormalities, or had congenital heart disease other than patent ductus arteriosus (PDA). Our unit currently adopts a conservative approach to PDA treatment. Prophylactic indomethacin is not used, and medical treatment of the PDA with nonsteroidal anti-inflammatory drugs is not provided during the first 7 days after birth. Written parental informed consent was sought from all participants, and ethical approval was obtained from the hospital ethics committee before recruitment.
Clinical information regarding pregnancy, delivery, and the postnatal period were collected. Three echocardiographic assessments were performed, during which the following cardiorespiratory parameters were collected: systolic and diastolic blood pressure, heart rate, mode of ventilation, mean airway pressure, oxygen requirement, arterial saturation, total fluid intake, and pH.
Echocardiography
Echocardiography was performed using the GE Vivid I ultrasound system with a 10-MHz probe (GE Healthcare, Milwaukee, WI). Echocardiographic scans were performed at a median of 10 hours (interquartile range [IQR], 6–13 hours) (day 1), 45 hours (IQR, 41–48 hours) (day 2), and 143 hours (IQR, 122–163 hours) (days 5–7). All studies were conducted using a standardized functional protocol adapted from recently published guidelines. The images were stored as raw Digital Imaging and Communications in Medicine data (EchoPAC version 112, revision 1.3; GE Healthcare) for later offline analysis.
Standard echocardiographic examinations were performed on all infants. Congenital heart disease was ruled out during the first examination. The presence and hemodynamic significance of a PDA was determined using methods previously described. PDA diameter in two dimensions was measured at the pulmonary end, and peak systolic velocity was measured using continuous-wave Doppler. Left atrial–to–aortic root ratio and LV end-diastolic diameter were measured using M-mode imaging from the long parasternal view. LV length was measured from the apical four-chamber view in diastole by measuring the distance between the midpoint of the mitral valve annulus and the apex ( Appendix ). The timing of end-systole was identified at the time of aortic valve closure using pulsed-wave Doppler of the LV outflow tract from the apical five-chamber view.
LV wall stress (grams per square centimeter) was calculated as (1.35 × mean arterial pressure × LV end-systolic diameter)/[4 × LV posterior wall thickness × (1 + LV posterior wall thickness/LV end-systolic diameter)], where 1.35 is the conversion factor from millimeters of mercury to grams per square centimeter. Mean arterial pressure was used because it has been shown to provide a reasonable estimate of LV end-systolic pressure in children.
Terminology
LV basal and apical rotation, LV twist, LV torsion, LVTR, and LVUTR were measured using STE of the parasternal short-axis views of the LV base and apex. Rotation was defined as the circumferential clockwise or counterclockwise movement of the apex and base along the long axis of the left ventricle occurring during systole (in degrees). Viewed from the apex, counterclockwise rotation is displayed as positive and clockwise rotation as negative. Figure 1 demonstrates basal and apical rotation plotted against time during one cardiac cycle.
Twist was defined as the net difference between apical and basal rotation using the following formula: LV twist (°) = apical rotation (°) − basal rotation (°).
LV torsion was defined as twist normalized to LV end-diastolic length and was calculated as follows: torsion (°/cm) = twist (°)/LV end-diastolic length (cm).
LVTR is the velocity at which twist occurs per unit time and is depicted as a positive value (degrees per second). Untwisting is the motion opposite to the direction of twist occurring in diastole. LVUTR is the velocity of untwist during diastole per unit time and is depicted as a negative value (degrees per second).
Measurements of Twist, LVTR, and LVUTR
The LV base and apex in short axis were obtained from the LV short-axis parasternal view. The basal plane was defined as the image at the level of the mitral valve leaflets while ensuring that no left atrial tissue was visible. The apical plane was defined as the image distal to the papillary muscles. Image acquisition at the two planes of interest was carried out to ensure that the LV cross-section was as circular as possible ( Appendix ). Three consecutive cardiac cycles were acquired and digitally stored as raw Digital Imaging and Communications in Medicine data for offline analysis.
We aimed for frame rates between 120 and 130 frames/sec for all image loops to achieve a frame rate–to–heart rate ratio of 0.7 to 0.9. Recently, Sanchez et al . demonstrated that the intra- and interobserver reproducibility of measuring LV and right ventricular longitudinal strain in preterm infants <29 weeks’ gestation using 2D STE was highest when the cine loops were acquired with frames rates ranging from 110 to 130 frames/sec and achieving a frame rate–to–heart rate ratio of 0.7 to 0.9.
Data were analyzed using the 2D speckle-tracking echocardiographic software described earlier. A region of interest (ROI) was obtained manually by tracing around the endocardial border of the LV wall during end-systole. The software package divides the LV wall in short axis into six segments and measures the rotation on the basis of the change in speckle movement within each segment. This produces six rotational curves and a global average ( Figures 1 and 2 ). The quality of the tracings was assessed by the software and a visual assessment of tracking adequacy. We accepted only tracings for which all six segments were adequately traced. The peak rotation of the apex and base, LV twist, LVTR, and LVUTR were determined. Peak rotation was defined as the maximal amount of rotation, positive or negative, during systole. Similarly, the peak LVTR was defined as the maximal amount of twist per unit time between these time points, with the LVUTR in the opposite direction during early diastole ( Figure 3 ).
Reproducibility
Intra- and interobserver reproducibility of apical rotation, basal rotation, LV twist and torsion, and LVTR and LVUTR were assessed by two observers. Twenty-five studies from the cohort were randomly selected for analysis. One investigator (A.J.) assessed intraobserver variability by performing two offline analyses 4 weeks apart to avoid recall bias. A second investigator (A.K.) carried out an assessment blinded to the results of the first observer for interobserver variability. Agreement was assessed using the intraclass correlation coefficient version 2.1. Additionally, agreement between investigators was further demonstrated using the Bland-Altman method by calculating the bias between the two repeated measurements (mean difference) and the 95% limits of agreement (1.96 SDs around the mean difference).
Statistical Analysis
Continuous variables were tested for normality using the Shapiro-Wilk test and are presented as mean ± SD or as median (IQR), as appropriate, unless otherwise stated. Differences in the echocardiographic values across the three time points were compared using a one-way analysis of variance with repeated measures. The Greenhouse-Geisser adjusted P value was used if the assumption of sphericity was violated. Skewed data were compared using the Kruskal-Wallis test. Categorical data are presented as proportions. Correlation between wall stress and functional parameters were assessed using Pearson correlation coefficients for normally distributed data or Spearman correlation coefficients for skewed data. To assess the systolic-diastolic relationship of the rotational mechanics, correlation between systolic torsion and LVUTR at each time point was assessed using Spearman correlation coefficients. We accepted a P value of <.05 as indicating statistical significance. The statistical analysis was performed using SPSS version 21 (SPSS, Inc, Chicago, IL).
Results
Seventy-three infants <29 weeks’ gestation were considered for inclusion during the study period between January and December 2013. Seven were excluded because of investigator unavailability, one lacked parental consent, three had weights less than the 10th centile, four received inotropes during the study period, four died in the first week of age, and in three infants, short-axis views were not acquired during at least two time points. Fifty-one infants with a mean gestational age of 26.8 ± 1.5 weeks and a mean birth weight of 945 ± 233 g were included. Thirty-nine infants (77%) were delivered by cesarean section, with a mean 5-min Apgar score of 8 ± 2 and a mean cord pH of 7.34 ± 0.05. Twenty-eight infants (55%) were male. There were 24 singleton births (47%), nine sets of twins (35%), and three sets of triplets (18%). All infants received surfactant before the first echocardiographic examination. None of the infants received inotropes during the first 7 days of age. During the first scan, 32 (63%) were invasively ventilated. This reduced to 19 (37%) on day 2 and 15 (29%) by days 5 to 7. All infants survived to hospital discharge. The remainder of the clinical characteristics are displayed in Table 1 . On day 1, 48 infants (94%) had PDAs, compared with 43 (84%) on day 2 and 35 (69%) on days 5 to 7 ( P = .003). None of the infants received medical treatment for PDA during the first week of age. There was an increase in PDA maximum systolic velocity and a decrease in the number of bidirectional PDA shunts across the three time points. There were significant but not clinically relevant changes in heart rate, LV end-diastolic diameter, and LV length over the study period ( Table 1 ).
| Variable | Day 1 | Day 2 | Days 5–7 | ANOVA P |
|---|---|---|---|---|
| Clinical parameters | ||||
| Heart rate (beats/min) | 156 ± 13 | 165 ± 13 | 164 ± 12 | <.001 |
| Systolic BP (mm Hg) | 45 ± 8 | 52 ± 9 | 52 ± 8 | <.001 |
| Mean BP (mm Hg) | 35 ± 8 | 39 ± 8 | 37 ± 6 | .004 |
| Diastolic BP (mm Hg) | 29 ± 8 | 31 ± 8 | 30 ± 7 | .07 |
| Total fluid intake (mL/kg/day) | 83 ± 8 | 117 ± 25 | 170 ± 18 | <.001 |
| FiO 2 (%) | 21 (21–60) | 21 (21–35) | 21 (21–35) | .20 |
| Oxygen saturation (%) | 95 ± 2 | 96 ± 3 | 96 ± 3 | .05 |
| Mean airway pressure (cm H 2 O) | 8 ± 2 | 8 ± 2 | 7 ± 2 | .009 |
| pH | 7.33 ± 0.06 | 7.29 ± 0.06 | 7.30 ± 0.06 | .002 |
| Echocardiographic parameters | ||||
| Wall stress (g/cm 2 ) | 22 (16–32) | 28 (19–35) | 20 (15–27) | .01 |
| LVESD (mm) | 7.0 ± 1.7 | 7.3 ± 1.6 | 7.0 ± 1.5 | .30 |
| LVPWT (mm) | 3.1 ± 0.6 | 3.3 ± 0.7 | 3.8 ± 0.8 | <.001 |
| LVEDD (mm) | 11.0 ± 2.1 | 11.7 ± 2.1 | 11.9 ± 2.2 | .002 |
| LV length (mm) | 17.8 ± 1.5 | 18.4 ± 1.9 | 19.4 ± 2.0 | <.001 |
| LA/Ao | 1.4 ± 0.3 | 1.5 ± 0.4 | 1.6 ± 0.4 | .06 |
| Proportion with PDAs | 48 (94%) | 43 (84%) | 35 (69%) | .003 |
| PDA diameter (mm) | 2.4 (2.1–2.9) | 2.9 (2.2–3.2) | 2.8 (2.3–3.4) | .021 |
| Bidirectional PDA | 19 (40%) | 7 (16%) | 5 (16%) | .009 |
| PDA maximum velocity (cm/sec) | 1.1 (0.8–1.6) | 1.4 (1.1–2.0) | 1.6 (1.2–2.5) | .001 |
Feasibility and Reproducibility of Twist Measurements
Measurements of rotation, twist, torsion, LVTR, and LVUTR were possible in 130 of 153 scans (85%). In the remainder, the software was unable to track the walls because of poor image quality. The mean frame rates during the examinations were 127 ± 11 on day 1, 125 ± 8 on day 2, and 125 ± 9 on days 5 to 7 ( P = .40). The mean frame rate–to–heart rate ratio was 0.83 ± 0.1 on day 1, 0.76 ± 0.1 on day 2, and 0.77 ± 0.1 on days 5 to 7 ( P = .001). The results of the Bland-Altman analysis and intraclass correlation coefficient demonstrated better intra- and interobserver reproducibility of apical rotation, basal rotation, twist, and torsion compared with LVTR and LVUTR ( Table 2 , Figure 4 ).
| Variable | Intraobserver variability | Interobserver variability | ||
|---|---|---|---|---|
| ICC (95% CI) | Bias (LOA) | ICC (95% CI) | Bias (LOA) | |
| Apical rotation | 0.96 (0.92 to 0.98) | 0.04 (−1.51 to 1.59) | 0.78 (0.50 to 0.90) | 1.21 (−1.46 to 3.88) |
| Basal rotation | 0.93 (0.85 to 0.97) | 0.11 (−3.77 to 3.99) | 0.89 (0.78 to 0.94) | −0.21 (−2.8 to 2.34) |
| LV twist | 0.86 (0.74 to 0.93) | −0.13 (−2.89 to 2.63) | 0.78 (0.18 to 0.92) | 1.4 (−1.05 to 3.85) |
| LV torsion | 0.93 (0.86 to 0.97) | 0.06 (−1.74 to 1.86) | 0.93 (0.67 to 0.98) | 0.61 (−0.85 to 2.07) |
| LV twist rate | 0.83 (0.47 to 0.94) | −6 (−65 to 53) | 0.70 (0.18 to 0.88) | 21 (−28 to 70) |
| LV untwist rate | 0.88 (0.74 to 0.94) | 0 (−53 to 52) | 0.73 (0.48 to 0.87) | −7 (−89 to 75) |
Longitudinal Rotation, Twist, Torsion, LVTR, and LVUTR
Apical rotation remained constant over the first week in a positive counterclockwise fashion. However, basal rotation changed from a positive counterclockwise rotation to a negative clockwise rotation, resulting in an overall net increase in twist and torsion across the three time points ( Table 3 , Figure 5 ). There was no change in LVTR over the first week of age ( P = .60). The LVUTR increased over the time period ( Table 3 , Figure 6 ).
| Variable | Day 1 | Day 2 | Days 5–7 | ANOVA P |
|---|---|---|---|---|
| Apical rotation (°) | 11.8 ± 5.0 | 12.1 ± 6.1 | 11.7 ± 8.3 | .92 |
| Basal rotation (°) | 5.5 (−0.3 to 8.3) | 4.0 (−4.7 to 7.2) | −4.5 (−5.8 to −2.3) | <.001 |
| Twist (°) | 8.5 ± 5.7 | 9.3 ± 7.9 | 12.9 ± 9.4 | .01 |
| Torsion (°/cm) | 4.4 ± 3.3 | 5.8 ± 3.3 | 7.0 ± 4.3 | .005 |
| LV twist rate (°/sec) | 120 (94 to 164) | 127 (92 to 182) | 142 (107 to 213) | .16 |
| LV untwist rate (°/sec) | −127 (−98 to −155) | −142 (−106 to −195) | −166 (−107 to −259) | .013 |
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