European Heart Journal Advance Access published online on October 19, 2007
European Heart Journal, doi:10.1093/eurheartj/ehm440
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Reduced and delayed untwisting of the left ventricle in patients with hypertension and left ventricular hypertrophy: a study using two-dimensional speckle tracking imaging
1 Department of Cardiology and Internal Medicine, Tane General Hospital, 1-2-31 Sakaigawa, Nishi-ku, Osaka 550-0024, Japan
2 Noninvasive Cardiac Imaging Laboratory, Section of Cardiology, Department of Medicine, University of Chicago Medical Center, Chicago, IL, USA
Received 11 May 2006; revised 6 July 2007; accepted 13 September 2007.
* Corresponding author. Tel: +81 6 6581 1071; fax: +81 6 6581 2520. E-mail address: masaaki_takeuchi{at}hotmail.com
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Abstract |
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Aims: Newly developed two-dimensional ultrasound speckle tracking imaging allows measurements of left ventricular (LV) rotation and twist. Because LV untwisting predominantly occurs during the isovolumic relaxation period, its assessment reflects the process of LV relaxation. The aim of this study was to examine whether LV hypertrophy (LVH) adversely affects LV untwisting and abnormalities in LV untwisting could become a novel marker in assessing LV relaxation abnormalities.
Methods and results: We acquired basal and apical LV short-axis images in 49 hypertensive patients. Using two-dimensional strain software, a time-domain speckle tracking was performed, and the mean value of LV rotation was obtained at each plane. LV twist was defined as apical rotation relative to the base. In order to adjust for inter-subject differences in heart rate, the time sequence was normalized to the percentage of systolic and diastolic duration. The degree of LV untwisting was calculated as the percentage of systolic twist : untwisting = (TwistES–Twistt/TwistES) x 100, where Twistt is twist at time t and TwistES is twist at end-systole. Although peak systolic twist was not different, early diastolic LV untwisting and untwisting rate during isovolumic relaxation period was significantly delayed and reduced in parallel to the severity of LVH, as assessed by LV mass index.
Conclusion: The observed delayed and reduced diastolic untwisting during the isovolumic relaxation period noted in hypertensive patients with LVH may contribute towards the LV relaxation abnormality. Two-dimensional speckle tracking imaging is a novel tool which can be used for the non-invasive assessment of LV relaxation.
Key Words: Two-dimensional speckle tracking • Untwisting • Relaxation • Left ventricular hypertrophy
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Introduction |
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Left ventricular hypertrophy (LVH) is usually associated with alterations in left ventricular (LV) diastolic function with preserved global LV systolic function until the latter stages of the disease.1,2 In clinical practice, echocardiographic assessment of LV filling using pulsed-Doppler flow velocity of the LV inflow in conjunction with pulmonary veins flow and mitral annulus velocity measurements using tissue Doppler imaging have been used to identify and stratify patients with LV diastolic dysfunction.3,4 However, all these indices are load-dependent, measuring events that occur after mitral valve opening (MVO), thus evaluating the later stages of LV relaxation.5 Accordingly, novel non-invasive methods for assessing the earlier stages of LV relaxation need to be developed.
LV torsion is the wringing motion, or twist of the heart imparted by contraction of its oblique spiral fibres.6,7 Counterclockwise torsion develops during systolic ejection, whereas the clockwise recoil of torsion, or untwisting, constitutes the deformation that largely occurs during the period of isovolumic relaxation.5,8,9 This recoil is associated with the release of restoring forces that accumulate during systole and is thought to contribute towards diastolic suction, which is a major determinant of early LV filling.8,9 The recent development of two-dimensional ultrasound speckle tracking imaging has allowed LV strain, strain rate, and twist to be evaluated non-invasively.10–18 This novel method has been shown to be highly feasible, and when accompanied by user-friendly analysis software has the potential of generating clinically useful measurements which may be applicable to clinical practice. Thus, the aim of this study was to examine whether (i) LVH adversely affects LV untwisting and (ii) abnormalities in LV untwisting could become a novel marker in assessing LV relaxation abnormalities.
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Methods |
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Study subjects
We included patients with medically controlled essential hypertension defined as ambulatory blood pressure that was measured in the outpatient clinic showing <140/80 mmHg in at least three consecutive visits and normal LV systolic function in transthoracic echocardiography (LV ejection fraction (LVEF)>50%). Subjects were recruited from both inpatient services and outpatient clinics at Tane General Hospital, Osaka, Japan. Patients were excluded if they had evidence of ischemic heart disease, echocardiographic evidence of either regional and/or global wall motion abnormalities, valvular heart disease, and hypertrophic cardiomyopathy. The patients' flow through the selection and recruitment process is given in Figure 1. As shown in Figure 1, a total of 49 patients were finally analysed (mean age: 63 ± 11 years, 31 men). The study complied with the Declaration of Helsinki and was approved by the local Ethics Committee. Informed consent was obtained from all patients.
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Echocardiography
Echocardiography data was acquired using a commercially available ultrasound transducer and equipment (M3S probe, Vivid 7, GE medical systems, Milwaukee, WI, USA). All two-dimensional grey scale echocardiographic images were obtained using the second harmonic mode. LV volumes and LVEF were measured using the modified biplane Simpson method as recommended by the American Society of Echocardiography. LV mass and LV mass index (LVMI) were calculated using the formula proposed by Devereux and Reichek.19 LV hypertrophy was defined as an LVMI of more than 115 g/m2 in men and more than 95 g/m2 in women.20 According to the severity of LVH, patients were divided into three groups [absence of LVH, mild LVH (LVMI: 116–131 g/m2 in men and LVMI: 96–108 g/m2 in women), and moderate–severe LVH (LVMI
132 g/m2 in men and LVMI 109 g/m2 in women)].20 To assess LV twist, two LV short-axis planes were acquired at the basal and apical levels at high frame rates (mean: 78 ± 6 frame/s, range: 67–99 frame/s). Care was taken to ensure that the basal plane contained the mitral valve, and that the apical plane was acquired distally to the papillary muscles. At each plane, three consecutive cardiac cycles were acquired during a breath hold, and stored digitally in a hard-disk for off-line analysis. In order to time cardiac events, LV inflow and outflow velocities were recorded using pulsed-Doppler echocardiography.
Left ventricular rotation and rotational velocity
The time interval between the peak of the R-wave on the electrocardiogram and the aortic valve opening and closure, as well as the time interval between the R-wave to the MVO and closure were measured using pulsed-Doppler acquired from the LV outflow and inflow, respectively. Our method for measuring LV rotation and rotational velocities has been described in detail elsewhere.17,18 Briefly, from the basal and apical short-axis datasets, one cardiac cycle was selected for subsequent analysis. Using commercially available two-dimensional strain software (Echopac PC, version 4.0.3, GE Healthcare, Milwaukee, WI, USA), the endocardial border of the end-systolic frame was manually traced. A region of interest was then drawn to include the entire myocardium. The software algorithm first automatically segmented the LV short-axis into six equidistant segments and then performed speckled tracking on a frame by frame basis using the sum of absolute difference algorithm. This resulted in the calculation of the time domain LV rotation and LV rotational velocity profiles for each of the segments in both short-axis planes. The average LV rotation and rotational velocity profiles from the entire LV were used for the calculation of LV twist and twist velocity. As in previous studies, LV twist and twist velocity were defined as apical LV rotation and rotational velocity relative to the basal plane.5,14,17,18
Counterclockwise rotation as viewed from the LV apex was expressed as a positive value, whereas a clockwise rotation as a negative value. Data points describing the basal and apical LV rotation and rotational velocities were exported to a spread sheet program (Microsoft Excel, Microsoft Corp., Seattle, WA, USA) to calculate LV twist and twist velocity. In order to adjust for intersubject differences in heart rate, the time sequences were normalized to the percentage of systolic duration (i.e. at end-systole, t was 100%) as well as diastolic duration (i.e. at end-diastole, t was 100%). End-systole was defined as the time of aortic valve closure. In addition to the twist vs. time profiles, peak twist, peak positive twist velocity, peak negative twist velocity (PNTV) and time from the R-wave to peak positive and negative twist velocities were measured. The degree of untwisting, defined as the directional reversal of systolic counterclockwise twist during diastole, was expressed as the percentage of end-systolic twist: untwisting = (TwistES–Twistt/TwistES) x 100, where Twistt is twist at time t and TwistES is twist at end-systole. Because the isovolumic relaxation time interval varied from subject to subject, the untwisting rate was defined as [(TwistES–TwistMVO/TwistES) x 100]/IVRT, where TwistMVO is twist at mitral valve opening and IVRT is the time of isovolumic relaxation.18
Using pulsed-Doppler velocity data of the LV inflow and outflow tract, peak E-wave velocity, peak A-wave velocity, deceleration time (Dct) of the E-wave, E/A ratio, isovolumic contraction time and isovolumic relaxation time were calculated.
Statistical analysis
The study was designed with 80% power to detect a significant difference in untwisting rates between patients with no LVH and those with mild LVH at a significance level of 5%. The effect difference with mild LVH was used because the difference between no LVH and moderate to severe LVH was presumed to be easier to detect. A difference in untwisting rates between no LVH and mild LVH of 0.1%/ms was defined as clinically important, with an estimated standard deviation (SD) of 0.1%/ms. We calculated that 16 patients would be required in each group. Therefore, 52 patients were enrolled in order to account for potential unequal distribution of degrees of LVH.
For the initial analyses of patient demographic and general echocardiographic characteristics, the patients were grouped according to LVMI into no LVH, mild LVH, and moderate–severe LVH in order to demonstrate the differences between groups using validated clinically meaningful categories. In these analyses, the categorical data were expressed as percentages and continuous data as mean ± SD. Categorical data were analysed using the 
2 test, whereas continuous data were analysed using analysis of variance. Each time point was analysed separately and a Bonferroni's correction was applied to account for multiplicity.
To analyse the effect of untwisting on LVMI, including the linear regression and the multivariable regression analyses, the response variable of LVMI was kept as a continuous variable to maintain consistency across the analyses. To assess for trends amongst differing degrees of LVH, LVMI was compared to untwisting variables using non-parametric trend tests (Cuzick–Wilcoxon type test for trend) analysed on Stata 9.2 (StataCorp, College Station, TX, USA). A simple linear regression analysis was performed to determine the correlation between two variables, with the linearity assumption verified by a scatter plot of the data. A P-value of <0.05 was considered significant. Multivariable linear regression analysis was used to test for independent associations between LVMI and known echocardiographic parameters associated with diastolic function including E-wave velocity, A-wave velocity, E/A ratio, E-wave Dct, and isovolumic relaxation time. Untwisting at various time points in diastole as well as untwisting rate were then tested in the model and assessed for significance as independent predictors with a P-value of <0.05. We tested the multivariable regression analysis with a plot of the residuals vs. the fitted values, demonstrating no correlation. As for inter- and intra-observer variabilities for LV twist and twist velocity, we have already reported good results using the same equipment and analysis software in the previous study.18
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Results |
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Among the 52 patients who had met eligibility criteria, three patients were excluded from the study due to poor acoustic windows (Figure 1). These patients had low tracking scores, representing the reliability of tracking based on the degree of decorrelation of the block-matching algorithm in the basal short-axis view. The number of patients with absent, mild, and moderate–severe LVH was 17, 12, and 20, respectively. No significant inter-group differences in mean age, sex distribution, body mass index, and other risk factors were noted (Table 1). The frequency of anti-hypertensive medication usage between groups was significantly different (75% in no LVH, 100% with mild LVH and 90% with moderate to severe LVH, P = 0.037). Table 2 depicts the M-mode, two-dimensional and Doppler echocardiographic parameters of all groups. As expected, the isovolumic relaxation time was significantly prolonged and A-wave velocity significantly increased in patients with moderate–severe LVH.
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Left ventricular rotation, twist, and twist velocity
LV rotation at the basal and apical plane, and twist among the three groups is shown in Figure 2. As seen from the apex, the LV performs a systolic wringing motion with a clockwise rotation at the base and counterclockwise rotation at the apex in all groups. Systolic rotation reached its peak value at end-systole in both basal and apical planes. Although the degree of basal rotation appeared to be larger in patients with moderate–severe LVH compared to patients without LVH or those with mild LVH, the basal (F = 2.816, P = 0.070) and apical (F = 0.53, P = 0.59) rotational profiles over time were not different among three groups. The time domain LV twist profile was also not statistically different among groups (F = 2.806, P = 0.070). Peak twist was also not different between groups (no LVH: 11.5 ± 3.6°, mild LVH: 10.9 ± 3.6°, moderate–severe LVH: 13.8 ± 5.0°, P = 0.12). Twist velocity, defined as apical rotational velocities relative to the base, had two peaks with a systolic positive velocity and a diastolic negative velocity.
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Effect of left ventricular hypertrophy on untwisting
We performed a trend test to determine significant differences of untwisting variables among the three groups. Significant differences in untwisting at t = 5, 10, 15, 20, and 30% in diastole, untwisting rate, and time to PNTV corrected by diastolic time interval were noted among groups (Table 3).
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Multivariable linear regression analysis using known echocardiographic parameters associated with diastolic function was performed separately testing untwisting at t = 105, 110, 115, 120, and 130%, as well as testing untwisting rate. Upon testing each of these untwisting parameters, a significant association with LVMI was found with untwisting at t = 105% (P = 0.0459), t = 110% (P = 0.0302), t = 115% (P = 0.0300), and with untwisting rate (P = 0.0455) independent of the traditional echocardiographic measures of diastolic function (Table 4). The effect of LV untwisting rate on LVMI is shown in Figure 3. The statistically significant inverse correlation between untwisting rate with LVMI reflects the summation of the untwisting during diastole, however, this model has not been independently validated.
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Simple linear regression analysis was performed between traditional Doppler-derived diastolic parameters and novel diastolic parameters derived from two-dimensional speckle tracking imaging (Table 5). A weak but significant correlation was observed between the degree of untwisting or untwisting rates and E/A ratio or isovolumic relaxation times. Good correlations were noted between the degree of untwisting (r = 0.40–0.64) or untwisting rate (r = 0.51) and time to PNTV corrected by diastolic time interval.
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Discussion |
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The major findings in this study were as follows: (i) When viewed from the apex, the LV in hypertensive patients performs a systolic wringing motion with a clockwise rotation at the base and a counterclockwise rotation at the apex, which is similar to that previously described in normal volunteers.17,18 (ii) No inter-group differences were noted in peak systolic twist among patients with different degrees of LVH. (iii) The time to PNTV was significantly prolonged, whereas untwisting early in diastole and untwisting rate were significantly reduced in parallel to increasing LVMI. (iv) A weak but significant correlation was noted between traditional diastolic parameters and untwisting or untwisting rates during early diastole. These data are in agreement with tagged magnetic resonance imaging data.21–23 We therefore conclude that the untwisting motion of the LV predicts the presence and severity of LVH as measured by LVMI. Accordingly, abnormalities in LV untwisting could be used as novel indices to assess abnormalities in LV relaxation.
Current study
LVH is not only one of the leading causes of congestive heart failure (CHF), but is also associated with an increased risk of cardiovascular events.1,2 The mechanism leading to CHF is believed to predominantly be an impairment in diastolic function, including abnormalities in both myocardial relaxation and passive filling.1 Currently, echocardiographic pulsed-Doppler indices of LV filling and pulmonary venous flow together with tissue Doppler mitral annular velocities have been used to assess LV diastolic dysfunction.3,4 However, these indices are load-dependent and only describe events that occur after MVO. Accordingly these indices provide little information on the relaxation process that predominantly occurs prior to MVO, (i.e. during the isovolumic relaxation period).5,9 Myocardial relaxation is often quantified using the first derivative of LV pressure decay (–dp/dt) and by modelling the time course of LV pressure decay during isovolumic relaxation to an exponential function to obtain the time constant (
) of LV pressure decline. Although myocardial relaxation using the index has been used in studies to calculate it, LV pressure needs to be acquired using high fidelity catheters at the time of cardiac catheterization. The process of myocardial relaxation may at times be prolonged and dyssynchronous, and extend beyond MVO in diseased hearts.1
Torsional deformation of the LV or twist during systole results in potential energy storage during ejection. The recoil of the systolic torsional deformation that occurs largely during isovolumic relaxation, is associated with the release of restoring forces, which are thought to contribute to LV suction and enhanced early diastolic filling.5,8,9 Thus, the assessment of torsional recoil, or untwisting, should provide an accurate estimate of LV relaxation. This deformation can be readily quantified using two-dimensional speckle tracking imaging. In this study, we found that early diastolic untwisting and untwisting rates were significantly reduced in parallel to the degree of LVH in hypertensive patients. We also measured that the time to PNTV, which may constitute another index of LV relaxation, was significantly prolonged in patients with LVH. The reduction of untwisting together with the prolongation of untwisting results in an overlap of untwisting and filling, which in turn may impair early diastolic filling.22 These results support the assessment of untwisting using two-dimensional speckle tracking as a novel parameter for evaluating LV relaxation.
Although statistically not significant, it is interesting to note that basal rotation appears to be more pronounced in patients with moderate–severe LVH. It is well known that torsional deformation is determined by the combined net effects of positive torsional deformation from forces originating in the subepicardial fibre wrapped in a left-handed helix and negative torsional deformation from forces developed in the subendocardial fibre wrapped in a right-handed helix.24 A counter-rotating torque in the subepicardium dominates the subendocardial fibre torque, because the subepicardial fibres are at a larger radius. We did not describe the exact mechanism of this finding, but moderate–severe LVH is associated with an increase in relative wall thickness. This finding would, in turn, result in producing larger radius differences between endocardium and epicardium, resulting in an augmentation of basal rotation compared to patients without LVH.
Previous studies
LV torsional deformation has been extensively evaluated using magnetic resonance tagged imaging.5,6,8,9,21–23,25,26 Rademakers et al.9 studied diastolic recoil in an animal model in which contractility was altered reporting that LV untwisting principally occurs during isovolumic relaxation and is markedly augmented during inotropic stimulation. Dong et al.5 performed experimental studies altering load and contractility. This investigation showed that untwisting rate (recoil rate) correlated with the invasively measured relaxation time constant (). Several studies demonstrated that torsion significantly increased and diastolic apical untwisting prolonged in aortic stenosis.21,22 A similar prolongation of diastolic untwisting has been reported in patients with hypertrophic cardiomyopathy.23 These results consistently support the concept that the assessment of untwisting provides a novel parameter for LV relaxation. Although tagged magnetic resonance imaging currently is the gold standard for the assessment of LV torsion, it is not widely available and its analysis is tedious and time-consuming, thus precluding its use in routine clinical practice. The higher spatial and temporal resolution and relatively easy analysis of two-dimensional speckle tracking imaging has the potential for non-invasive assessment of LV untwisting in routine clinical studies.
Limitations
The time constant of isovolumic relaxation was not acquired invasively in this study. Accordingly, we were unable to determine the correlation between untwisting indices derived from two-dimensional speckle tracking imaging and . However, previous studies have recently validated the accuracy of speckle tracking imaging vs. tagged magnetic resonance imaging.12,14–16 The exact location of the basal and apical plane may vary from patient to patient and may introduce measuring errors. Two-dimensional speckle tracking analysis cannot eliminate the errors introduced by through-plane motion, particularly in the basal plane. As with all tomographic methods, the same point may not be seen during systolic contraction and diastolic relaxation. Lastly, the statistical model of adding untwisting to the traditional diastolic parameters in a stepwise multivariable regression analysis to predict LVMI is merely suggestive of an association and would require further study for empiric validation.
Conclusions
Two-dimensional speckle tracking imaging provides a novel index for the non-invasive assessment of LV relaxation. A delayed and reduced early diastolic untwisting in patients with LVH was observed in this study which may have contributed to the abnormal LV relaxation. This novel method allows the detailed study of LV diastolic function in various cardiovascular diseases.
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Supplementary material |
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Supplementary material is available at European Heart Journal online.
Conflict of interest: none declared.
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References |
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