European Heart Journal Advance Access published online on November 19, 2008
European Heart Journal, doi:10.1093/eurheartj/ehn511
Assessment of subendocardial vs. subepicardial left ventricular rotation and twist using two-dimensional speckle tracking echocardiography: comparison with tagged cardiac magnetic resonance
1 Division of Cardiology, Cliniques Universitaires Saint-Luc, Université Catholique de Louvain, Avenue Hippocrate 10, Boite 2881, B-1200 Brussels, Belgium
2 Ecole de santé publique, Epidemiology and Biostatistics, Université Catholique de Louvain, Brussels, Belgium
3 Philips Medical System, Paris, France
Received 6 March 2008; revised 9 October 2008; accepted 23 October 2008.
* Corresponding author. Tel: +32 2 764 2803, Fax: +32 2 764 2811, Email: vanoverschelde{at}card.ucl.ac.be
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Abstract |
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Aims: The aim of this article is to evaluate the accuracy and reproducibility of two-dimesional speckle tracking echocardiography (2D-STE) for the estimation of left ventricular (LV) twist, using tagged cardiac magnetic resonance (cMR) as the reference standard, and to assess how much 2D-STE rotational parameters are affected by the level at which measurements are made within the LV.
Methods and results: Forty-three patients with various heart diseases and 10 healthy volunteers underwent cMR and 2D-STE on the same day. With both methods, basal and apical time–rotation curves were generated at endocardial, midwall, and epicardial levels. By using the most apical cMR short-axis cross-section as a comparator, apical rotation was significantly underestimated by 2D-STE. When 2D-STE and cMR short-axis cross-sections were matched for their internal dimensions, measurements of endocardial, midwall, and epicardial twists no longer differ between cMR and 2D-STE (12.6 ± 5.9 vs. 12.5 ± 5.7°, 10.5 ± 4.6 vs. 9.7 ± 4.1°, and 8.9 ± 4.0 vs. 8.4 ± 3.7°, respectively, all P = ns).
Conclusion: Compared with tagged cMR, 2D-STE underestimates apical rotation and LV twist. This is related to the inability of 2D-STE to image the real LV apex in most of the patients. However, when 2D-STE and cMR data are compared at similar acquisition levels, both techniques provide similar values.
Key Words: LV twist • Speckle tracking • MRI • Comparative studies
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Introduction |
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The orientation of left ventricular (LV) muscle fibres varies across the LV wall, from a right hand helix in the subendocardium to a left hand helix in the subepicardium, the midwall fibres exhibiting an intermediary, circumferential orientation. The shortening of these obliquely oriented LV fibres during systole generates a wringing motion that is responsible for LV torsion.1 When viewed from the apex during systole, the apex rotates counterclockwise relatively to the base. It has been shown experimentally as well as clinically that the torsional behaviour of the LV closely parallels changes in its global ejection performance.2–10 LV torsion, or twist, is also a key element in the storage of potential energy at the end of systole, the release of which as elastic recoil during early diastole assists ventricular suction.11–13
Among the methods used to assess LV twist, tagged cardiac magnetic resonance (cMR) is currently considered as the reference standard.14 Recently, two-dimensional speckle tracking echocardiography (2D-STE) was introduced as a novel non-invasive approach to measure LV deformation mechanics.15–18 2D-STE indeed offers the opportunity to track myocardial motion independent of both cardiac translation and angle dependency. So far, very few studies have examined the ability of 2D-STE to measure LV torsional mechanics.15,16 Although their results suggested that measurements of LV twist by 2D-STE are feasible and correlate reasonably well with those obtained by sonomicrometry or cMR, these studies were either experimental or only recruited a limited number of patients and none investigated the impact of missing the real LV apex on the accuracy of the method. Accordingly, we designed the present study to investigate whether 2D-STE accurately measures LV basal and apical rotation, in comparison with tagged cMR, and to evaluate how much 2D-STE rotational and torsional parameters are affected by the level at which measurements are made within the LV.
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Study population
Between March and December 2006, 114 consecutive patients undergoing clinically indicated cMR studies were considered for inclusion into this study. Among these, 63 patients had either haemodynamic instability, constant arrhythmia (atrial fibrillation or more than five premature beats per minute), or other contraindications to cMR (ferrometallic cerebral aneurysm clips, pacemaker or implantable defibrillator, or severe claustrophobia) and were therefore not considered for inclusion. The 51 remaining patients were all proposed and accepted to participate in the study. Of these, an additional eight ‘technically difficult patients’ for transthoracic echocardiographic examinations were finally excluded from the analysis. The final study population thus consisted of 43 patients (33 men, mean age: 56 ± 14 years, range 22–84 years). These patients had a variety of cardiac pathologies, allowing us to encompass a broad clinical range of LV torsion or twist: aortic valve disease (n = 12), mitral valve disease (n = 3), dilated or restrictive cardiomyopathy (n = 14), previous myocardial infarction (n = 8), arrhythmogenic right ventricular dysplasia (n = 3), and myocarditis (n = 3). We also recruited 10 normal volunteers via local advertisement (seven men, mean age 34 ± 7 years, range 28–48 years). Table 1 summarizes the clinical characteristics of the 53 subjects included in the study. No former sample size calculation was performed beforehand.
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The study protocol was approved by the Ethics Committee of our Institution, and all subjects gave their informed consent prior to inclusion in the study.
Two-dimensional speckle tracking echocardiography
The research echocardiographic study was performed on the same day as cMR. Following a standard two-dimensional and Doppler echocardiographic examination, high frame rate (84 ± 13 Hz) second harmonic LV short-axis cross-sections were obtained from the parasternal or para-apical windows,19 using an IE33 echocardiographic system (Philips Medical System, Andover, MA, USA) equipped with a broad-band phased-array S3 transducer. Images were obtained at both basal and apical levels. Care was taken to ensure that the basal short-axis planes contained the mitral valve, that the apical plane was acquired distally to the papillary muscles, and that in each short-axis acquisition, the LV cross-section was made as circular as possible. To acquire the apical plane, care was taken to be at the most apical level of the LV. At each plane, five consecutive cardiac cycles were acquired during one breath-hold and stored for offline analysis.
Cardiac magnetic resonance
cMR was performed with a 1.5 T scanner (Intera CV, Philips Medical System, Best, The Netherlands), using a five-element cardiac synergy coil for signal reception. Following acquisition of scout images to identify cardiac axes, 8–12 short-axis images loops were acquired using an ECG-triggered, segmented K space, grid-tagged imaging protocol with echoplanar readout, during short breath-holds. The following parameters were used: spatial modulation of magnetization in a grid pattern with a 7 mm distance between tags; image matrix: 256 x 154; flip angle: 13°; repetition time: 19 ms; echo train length 7–9; slice thickness: 10 mm; field of view: 320–380 mm. Following tagging sequences, balanced fast-field echo sequences were acquired to measure LV volumes and ejection fraction.
Data analysis
Images were anonymized and transferred onto dedicated workstations for further analysis. To avoid recalling the patients' images, 2D-STE and cMR images were analysed on separate days. Inter-observer variability was estimated by comparing data collected by two blinded observers on 20 randomly selected patients. To assess intra-observer variability, in a randomly selected subgroup of 20 patients, measurements were repeated 1 month after the first reading.
Two-dimensional speckle tracking echocardiography
2D-STE data were analysed using a prototype version of the 2DQ-QLab software, version 6 (Philips Medical systems, Einthoven, The Netherlands), which allows for speckle tracking in the subendocardial, mid-myocardial, and subepicardial layers. This tracking algorithm does not require a minimal wall thickness to track different layers. Briefly, the user first manually places several small kernel regions (10–50 pixels in size, depending on image resolution) along the endocardial and epicardial borders onto the end-diastolic image. The program then automatically places additional kernels at mid-distance between the endocardial and epicardial borders and tracks the three borders (endo-, mid-, and epi-) on a frame-by-frame basis by use of a least-squares global affine transformation. The rotational component of this affine transformation is then used to generate rotational profiles for the endocardium, mid-myocardium, and epicardium (Figure 1). Counterclockwise rotation was expressed as a positive value and clockwise rotation as a negative one.
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Cardiac magnetic resonance tagging
cMR data were analysed offline using HARP (version 1.7, Diagnosoft Inc., Palo Alto, CA, USA), as described previously.20 Briefly, the user first defined manually the endocardial and epicardial contours on each serial contiguous 10 mm thick LV short-axis section. Contour points were then automatically tracked by the software to determine the rotational profiles of endocardial, midwall, and epicardial layers at each level. As with 2D-STE, counterclockwise rotation was expressed as a positive value and clockwise rotation as a negative one.
With both 2D-STE and cMR, LV rotation, at each corresponding myocardial layer, was computed at both basal and apical levels. From these data, LV twist was calculated as the instantaneous difference between apical and basal rotation. To adjust for intersubject differences in heart rate, the time sequence was normalized to the percentage of systolic duration (i.e. at end systole, t was 100%). End-systole was defined at aortic valve closure. In addition to these parameters, peak torsional velocity was calculated as the time derivative of LV twist and expressed in °/s. The time from the R wave of the QRS complex to the peak twisting velocity was also computed. Finally, because imaging of the real LV apex is not always possible with 2D-STE, 2D-STE and cMR data were matched by measuring the end-diastolic internal transverse dimensions of the available 2D-STE short-axis cross-section and on each cMR short-axis cross-section. Data from the cMR short-axis cross-section, whose internal dimensions best matched those measured on the 2D-STE short-axis cross-section, were then compared with those from the available 2D-STE cross-section.
Statistical analysis
Statistical analyses were performed using SPSS 12.0 statistical software (Chicago, IL, USA). Values are reported as mean±1 standard deviation. The rotation and twist measurements obtained by cMR and 2D-STE were compared using Bland and Altman method.21,22 Differences in measurements between the two modalities were compared using Student's paired t-test. Correlation with the LV ejection fraction was assessed using linear regression. Intra- and inter-observer reliability in measurements of LV twist was assessed using intraclass correlation coefficient and Bland–Altman method. All tests were two-sided, and the statistical significance level was set to 0.05.
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Left ventricular rotation by cardiac magnetic resonance
As shown in Figure 2, in subjects with a normal ejection fraction, LV rotation measured by cMR progressively decreased from apex to base. On average, LV rotation decreased by 23 ± 6% of its maximal value for each centimetre away from the apex and by 16 ± 6% of its maximal value for each 10% of the long-axis length away from the apex.
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Left ventricular rotation by two-dimesional speckle tracking echocardiography and cardiac magnetic resonance
The mean values of basal rotation, apical rotation, and LV twist in the three myocardial layers measured by 2D-STE and cMR are summarized in Table 2. As shown in Figures 3 and 4, apical rotation by 2D-STE significantly underestimated that by cMR.
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Because LV rotation progressively decreases from apex to base, we investigated whether failure to image the real apex by 2D-STE contributed to its underestimation of apical rotation. To achieve this, we measured the LV end-diastolic internal dimensions on the sole 2D-STE short-axis cross-section available per subject and compared them with those measured on each of the serial contiguous cMR LV short-axis cross-sections. This analysis demonstrated that the 2D-STE cross-section corresponded to the most apical cMR cross-section in only 10% of the subjects. In other subjects, the cMR cross-section, whose internal dimensions best matched those measured on 2D-STE, was located 1, 2, and 3 cm away from the apex in, respectively, 27, 50, and 13% of the subjects. When the best matched cMR short-axis cross-section was chosen for comparison between 2D-STE and cMR, 2D-STE and cMR measures of apical rotation and LV twist were no longer different from each other (Table 2 and Figures 3 and 5), with only small intertechnique differences and acceptable limits of agreements. For subendocardial twist, the mean difference between the two techniques was 0.09°, with 95% limits of agreement (–3.1°; 3.3°) [95% confidence interval (CI) on limits of agreement were (–3.9°; –2.3°) and (2.5°; 4.0°), respectively]. For mid-myocardial twist, the mean difference between the two techniques was 0.78°, with 95% limits of agreement (–3.2°; 4.8°) [95% CI on limits of agreement were (–4.2°; –2.2°) and (3.8°; 5.8°), respectively]. Finally, for subepicardial twist, the mean difference between 2D-STE and cMR was 0.42°, with 95% limits of agreement (–4.7°; 5.5°) [95% CI on limits of agreement were (–5.8°; –3.4°) and (4.3°; 6.6°), respectively].
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As shown in Figure 6, peak twisting velocities [63 ± 23°/s; range (20°/s; 114°/s) vs. 54 ± 18°/s; range (16°/s; 95°/s), P = 0.001] and the time to peak twisting velocity [55 ± 9; range (33% of systole; 72% of systole) vs. 53 ± 10% of systole; range (37% of systole; 90% of systole), P = 0.06] were also similar between 2D-STE and cMR with acceptable inter-techniques differences. For the peak twisting velocities, the mean difference between 2D-STE and cMR was –7.9°/s, with 95% limits of agreement (–36.0°/s; 20.0°/s) [95% CI on limits of agreement were (–42.7°/s; –29.2°/s) and (13.4°/s; 27.0°/s), respectively]. For the time to peak twisting velocities, the mean difference between the two techniques was –2.1% of systole, with 95% limits of agreement of (–16.4%; 12.2%) [95% CI on limits of agreement were (–19.8%; –12.9%) and (8.8%;15.6%), respectively].
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We also evaluated the possibility to retrospectively correct 2D-STE apical rotation data for the distance between the 2D-STE imaging plane and the real apex. For this purpose, the LV end-diastolic internal dimensions were measured on the available 2D-STE apical short-axis cross-section and every centimetre from the apex on a standard apical two-chamber view. The distance between the apex and the best-matched apical two-chamber level was then measured and used to normalize 2D-STE apical rotation and twist according to the relationship between rotation and distance from the apex that was delineated by use of cMR in the subjects with a normal ejection fraction. As shown in Table 3 and Figure 7, normalization of 2D-STE rotational and twisting data mollified the differences between 2D-STE and cMR and improved the agreement between the two measurements.
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Relation between left ventricular twist and ejection fraction
Significant correlations were found between LV ejection and LV twist, measured by either cMR (r2 = 0.61, P < 0.001 for the most apical cross-section and r2 = 0.38, P < 0.001 for the 2D-STE best-matched apical cross-section) or 2D-STE (r2 = 0.42, P < 0.001). LV ejection fraction also correlated with apical rotation (r2 = 0.53, P < 0.001 for the most apical cMR cross-section, r2 = 0.30, P < 0.001 for the 2D-STE best-matched cMR cross-section, and r2 = 0.32, P < 0.001 for 2D-STE). Weaker correlations were observed between LV ejection fraction and basal rotation (r2 = –0.13, P = 0.01 for cMR and r2 = –0.12, P = 0.011 for 2D-STE).
Reliability
Inter- and intra-observer variabilities were estimated by comparing data collected by two blinded observers from 20 randomly selected patients. Results are summarized in Table 4. In five volunteers free of any cardiac disease, 2D-STE and cMR were repeated twice, on 2 different days, to assess test–retest reproducibility. As shown in Table 5, the test–retest reproducibility was excellent for both modalities.
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Discussion |
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STE is a new, non-invasive method for the assessment of LV global and regional function. 2D-STE offers the opportunity to track myocardial deformation independent of both cardiac translation and insonation angle. Unlike tissue Doppler imaging, it not only allows to measure longitudinal deformation and strain, but also to assess myocardial rotational and torsional mechanics. Before the advent of 2D-STE, the only technique for angle-independent assessment of LV rotation was tagged cMR. Although cMR remains the reference method for the assessment of LV torsional and rotational deformation, its use is limited by inherent low frame rate acquisition, high cost, time-consuming and complex data analysis, and limited availability. So far, very few studies have examined the ability of 2D-STE to measure LV torsional mechanics.15,16 Although their results suggested that measurements of LV twist by 2D-STE are feasible and correlate reasonably well with those obtained by sonomicrometry or cMR, these studies were either experimental or only recruited a limited number of patients. In addition, none of them investigated the impact of missing the real LV apex on the accuracy of the method. Accordingly, in the present study, we evaluated the accuracy of 2D-STE-derived LV rotation and torsion using cMR as the reference standard and tested the influence of the level at which measurements are made within the LV on the accuracy of the method. Our results can be summarized as follows.
- LV rotation measured by cMR progressively decreases from apex to base.
- 2D-STE estimates of apical rotation are significantly lower than those obtained by cMR.
- 2D-STE underestimation of apical rotation is due to the inability of 2D-STE to visualize the true LV apex in a significant number of normal and diseased subjects.
- When LV rotational data are obtained with 2D-STE and cMR at a similar level, estimates of apical rotation and LV twist by the two methods are no longer different, are similarly reproducible, and are highly correlated.
- Normalization of 2D-STE data for the relative distance between the 2D-STE apical cross-section and the real LV apex allows attenuating the underestimation of apical rotation and LV torsion by 2D-STE and improves their correlation to cMR.
Two-dimensional speckle tracking echocardiography for the assessment of left ventricular twist
Because of scattering, reflection, and interference of the ultrasound beam in myocardial tissue, speckles appear in grey scale two-dimensional echographic images. These speckles represent tissue markers that can be tracked from frame to frame throughout the cardiac cycle. These fingerprints are randomly distributed throughout the myocardium. Each speckle can be identified and tracked by calculating frame-to-frame changes—similar to analysis with tagged cMR—using a sum of absolute difference algorithm. Motion is analysed by integrating frame-to-frame changes. Out-of-plane motion occurs due to rotation and motion of the heart into the chest cavity and may cause the disappearance of the speckles over a few frames, but rarely within two consecutive frames.23 By tracking speckles over time, strain, strain rate, tissue velocity, and LV rotation can be easily calculated. Recently, experimental and clinical studies have indicated that 2D-STE was able to accurately measure both apical and basal rotations and hence to accurately estimate LV twist.15,16 The results of the present study are thus somewhat at variance with those of these previous investigations. Unlike in these earlier reports, we found that 2D-STE significantly underestimates the degree of apical rotation, and hence of global LV twist, when compared with cMR. Interestingly, our data indicate that underestimation of apical rotation by 2D-STE is probably not related to intrinsic inaccuracies in the estimation of myocardial rotation by this technique, but rather to its inability to image the real LV apex. Because LV rotation progressively decreases from apex to base, from a predominantly counterclockwise rotation at the level of the apex to a clockwise rotation at the level of the base, failure to image the real apex results in the underestimation of true apical rotation, as recently shown by van Dalen et al.19 This was also observed in our study. By comparing end-diastolic internal dimensions among the available 2D-STE apical cross-sections with the serial consecutive 10 mm cMR LV cross-sections, we found that 2D-STE images were acquired at the real LV apex in only 10% of the subjects. In the remaining patients, the 2D-STE cross-section was acquired at a variable distance from the apex, resulting in the ‘distance from the apex’-dependent underestimation of apical rotation. However, if only the best-matched cross-sections between 2D-STE and cMR were used for analysis, similar to previous studies, excellent correlations were found between the two techniques. We do not have a definite explanation as to why a similar degree of underestimation was not observed in previous investigations. In contrast, in the study by Helle-Valle et al., 2D-STE even tended to overestimate cMR estimates of apical rotation by 
21%.
In an attempt to compensate for the underestimation of apical rotation by 2D-STE, we tested the effect of normalizing 2D-STE apical rotation for the relative distance between the 2D-STE apical cross-section and the real LV apex. For this purpose, end-diastolic LV internal dimensions were measured on the available 2D-STE apical cross-section and every centimetre from the apex on a standard apical two-chamber view. The distance between the apex and the best-matched apical two-chamber view level was then measured and used to normalize 2D-STE apical rotation and derived LV twist according to the relationship between rotation and distance from the apex that had been delineated by cMR in normal subjects. As indicated earlier, although normalization of 2D-STE rotational and torsional data attenuated the difference between 2D-STE and cMR, it only modestly improved the correlation between the two measurements.
Limitations
The tracking algorithm does not require a minimal wall thickness. If the wall thickness is too small (inferior to kernel size), it is possible to obtain suboptimal tracking. Because none of our patients had extremely thin walls, tracking of very thin walls was not tested with the software in our study.
Clinical implications
Although 2D-STE allows for a robust, accurate, and reproducible assessment of myocardial rotation, it seldom permits sampling of the real LV apex. Careful selection of apical most LV section is necessary. If LV most apical section is not at the level of the real apex, this results in a systematic and mostly unpredictable underestimation of apical rotation and LV twist that is only partially compensated for when correcting the data for the estimated distance between the 2D-STE apical cross-section and the real apex. This has major implications for the use of this technique in daily clinical practice. It indeed makes it difficult, if possible, to compare apical rotation and LV twist between groups of patients, unless a large number of subjects are included in each comparison group. Directional changes in rotational or twisting parameters in the same patient appear to be less problematic in view of the excellent test–retest reproducibility seen in our study. It is, nonetheless, probable that clinical use of these parameters will await the development of 3D-STE.
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Conclusion |
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Compared with tagged cMR, 2D-STE underestimates apical rotation and LV twist. This is related to the inability of 2D-STE to image the real LV apex in most of the patients. However, when 2D-STE and cMR data are compared at similar acquisition levels, both techniques provide similar values for segmental rotation, LV twist, and peak twisting velocities.
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This work is supported by the Fonds National de la Recherche Scientifique of the Belgian Government (FNRS). C.G. is an aspirant of the Fonds National de la Recherche Scientifique of the Belgian Government.
Conflict of interest: O.G. is from Philips Medical System.
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