Curr Cardiol Rep (2015) 17:15 DOI 10.1007/s11886-015-0568-x

ECHOCARDIOGRAPHY (JM GARDIN, SECTION EDITOR)

Strain, Strain Rate, Torsion, and Twist: Echocardiographic Evaluation Anders Opdahl & Thomas Helle-Valle & Helge Skulstad & Otto A. Smiseth

# Springer Science+Business Media New York 2015

Abstract Deformation imaging by tissue Doppler imaging (TDI) and speckle-tracking echocardiography (STE) are emerging clinical methods. TDI- and STE-derived parameters, such as myocardial strain and strain rate, as well as torsion and twist, provide detailed information about myocardial function and are associated with cardiovascular morbidity and mortality. However, only echocardiographic laboratories with experience in deformation imaging have included these methods in daily clinical practice. In this review, we describe myocardial deformation parameters and relevant echocardiographic methods and address recent developments in the clinical application of deformation imaging. Keywords Echocardiography . Strain . Strain rate . Torsion . Speckle tracking . Tissue Doppler

currently widely used in echocardiography laboratories, whereas the more recently introduced echocardiographic deformation imaging is undergoing testing in clinical trials and used clinically by early adopters of this approach. The visual assessment of LV function suffers from being a subjective and semi-quantitative method and subtle changes in LV function may, therefore, not be recognized. Echocardiographic deformation imaging by the calculation of strain obtained by tissue Doppler imaging (TDI) [1, 2] and more recently speckletracking echocardiography (STE) [3] have been introduced as more objective and quantitative methods to quantify regional and global LV systolic and diastolic function. This paper reviews the LV deformation as assessed by strain, strain rate, and LV torsion, as well as the technical features of TDI and STE. The physiological meaning of the parameters will be addressed as well as recent developments in the clinical application of the methodologies.

Introduction Assessment of global and regional cardiac function by twodimensional (2D) echocardiography is pivotal in the evaluation of patients with established or suspected cardiovascular disease. Visual assessment of left ventricular (LV) function is This article is part of the Topical Collection on Echocardiography A. Opdahl (*) : T. Helle-Valle : H. Skulstad : O. A. Smiseth Department of Cardiology, Oslo University Hospital, Rikshospitalet, Postbox 4950, Nydalen, 0424 Oslo, Norway e-mail: [email protected] T. Helle-Valle e-mail: [email protected] H. Skulstad e-mail: [email protected] O. A. Smiseth e-mail: [email protected]

Normal LV Deformation It is essential to understand the physiology of LV function in order to interpret deformation imaging. Normal LV systolic function is the result of coordinated contraction of myocardial fibers of different orientations. During systole, the longitudinal component of myocardial contraction causes the LV base to descend approximately 12 to 15 mm toward the apex, while the circumferential component causes a reduction in the LV short-axis diameter, both mechanisms contributing to approximately 50 % wall thickening [4]. In addition, due to the contraction of obliquely oriented fibers, the LV undergoes a twisting or wringing deformation along its long axis involving oppositely directed rotations of the apex relative to the base (Fig. 1) [6]. Systolic LV deformation is reversed or reformatted during diastole, primarily during the early phase.

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Representative strain and strain rate traces of normal and ischemic myocardium during a cardiac cycle are shown in Fig. 2. In normal ventricles, systolic deformation of elastic myocardium contributes to the early diastolic lengthening or reversal of systolic deformation which is a consequence of the rate of active myocardial relaxation [8, 9], the release of restoring forces generated during systolic deformation [10], as well as the load applied to the LV during early diastole [11, 12]. Passive-elastic properties and the pericardium modulate myocardial deformation. Magnitude and rate of systolic and diastolic deformation along the three main LV axes (longitudinal, circumferential, and radial) can be quantified by measurements of strain and strain rate, respectively. The more complex wringing LV deformation can be assessed by twist and torsion.

Strain and Strain Rate Fig. 1 Left ventricular fiber orientation and three-dimensional deformation. The left panel shows a schematic representation of the myocardial fiber orientation in the left ventricle that changes continuously from a right-handed helix in the subendocardial region to a left-handed helix in the subepicardial region, as seen over the anterior wall of the left ventricle. The panels to the right show block of myocardial tissue in which the xaxis is oriented at a tangent to the circumferential (C) direction, the y-axis is oriented longitudinally (L), and the z-axis corresponds to the radial (R) direction of the left ventricle and the components of shear strain (CR, CL) (with permission from Modesto and Sengupta [5])

Fig. 2 Strain and strain rate from normal and ischemic myocardium. Strain rate and strain traces from typical normal (gray) and mildly ischemic (black) myocardium. Ischemic myocardium is characterized by an early peak positive strain (PPS), and peak systolic strain (PSS) is typically lower than endsystolic strain (ESS). A post systolic shortening is often seen, and peak strain (PS) therefore occurs after end systole (with permission from Gjesdal and Edvardsen [7])

In echocardiography, the term Bstrain^ is applied to describe lengthening, shortening, and thickening. As myocardial strain reflects magnitude of deformation, strain has predominantly been used as a measure of regional LV function. By using an average value for multiple regions, a more global measure of LV function can be obtained, and global longitudinal strain (GLS), assessed as the average longitudinal strains from the three standard apical projections, has recently been introduced as a relevant clinical marker of LV function. Strain is a measure of how much an object has been deformed, and several formulas can be used to calculate

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different types of strain. In cardiac mechanics, we use a simplified approach and calculate strain as percent change in dimension. Linear strain or the amount of deformation along a line can be defined as the change in length divided by the original length according to the formula: ε=ΔL/L0, where ε = strain, ΔL = change in length, and L0 = original length. Thus, the formula can be applied for strain calculation for each of the three cardiac axes: longitudinal, circumferential, and radial. This implies that systolic strain is a measure of percentage shortening when measurements are done in the long axis or circumferentially, and percent thickening for radial measurements (Fig. 1). In reality, the myocardial wall undergoes a complex three-dimensional (3D) deformation that can be described by linear strain along each of the three axes (x-, y-, and z-axes) as well as shear strain (angular in-plane deformation) within the three planes. In a clinical setting, one-dimensional strains are mostly used. When evaluating LV systolic function, strain can be measured as peak systolic strain (positive or negative), as peak strain at end systole (at time of aortic valve closure), or as peak strain regardless of timing (in systole or early diastole). There is no consensus regarding which time point should be used to measure peak strain in the assessment of systolic function [13]. Timing of strain during the cardiac cycle provides information about the time course of myocardial deformation. The standard deviation of time to peak negative strain in multiple myocardial segments can be used as a measure of inhomogeneous contraction or mechanical dispersion. The rate of strain change vs. time is called strain rate (SR). It reflects the rate of deformation change and is expressed as 1/s. Strain rate may be calculated as the time derivative of strain by STE or estimated from a velocity gradient between two spatial points by TDI. SR corresponds to the velocity profile in a myocardial segment through the cardiac cycle. However, SR reflects the shortening/lengthening rate of the studied myocardial segment relatively independently of possible tethering or whole body effects, which may be included in the measured velocity measurements (Fig. 3).

Twist and Torsion LV twist is the relative rotation of the apex around the LV long axis with respect to the base during the cardiac cycle. The apex rotates counterclockwise during systole, and the base rotates in the opposite direction when viewed from apex to base. Both rotation and LV twist (apex-to-base difference in rotation) are expressed in degrees. The term torsion is twist normalized value to the distance between LV apex and base and refers to the base-to-apex gradient in rotation angle, expressed in degrees per centimeter (°/cm). It is feasible

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to measure LV rotation and twist by modern echocardiographic techniques by quantifying apical and basal rotation followed by the calculation of LV twist [15–18]. However, because 2D echocardiography does not provide an accurate measure of the distance between the two image planes, it is difficult to measure torsion. Therefore, the 2D echocardiographic measures are limited to rotation and twist. Twisting and untwisting rate are calculated as the time derivative of twist. The early diastolic peak untwisting rate has been investigated as a marker of LV diastolic function.

Tissue Doppler Imaging The Doppler principle has traditionally been used to measure blood flow velocities, but may also be used to measure myocardial and other tissue velocities. Separation between the high amplitude, low-velocity signals in the relatively slowly moving myocardium from the more rapid-velocity, low amplitude flowing blood signals is possible by using filters that reject echoes originating from the blood pool. The fundamental data produced by TDI are velocity data, which can be recorded using color Doppler or pulsed Doppler mode. The theoretical basis for measuring strain by TDI is that myocardial velocity gradient is an estimate of strain rate (SR), and strain can be calculated as the temporal integral of strain rate. Thus, strain rate can be estimated by TDI as the difference in velocity between two spatial points divided by the distance between the two points by the equation: SR=(v1 − v2)/L, where SR=strain rate, v1 =velocity at point 1, v2 =velocity at point 2, and L=length or distance between the two points (usually set at 10 mm for TDI). By mathematical conversion from natural strain to Lagrangian strain, an estimate of strain rate is feasible by TDI. Strain and strain rate by TDI require the ultrasound scan lines to be along the direction of the myocardial wall motion. Thus, apical windows have been often used because of the favorable myocardial motion along the ultrasound beam. The majority of published literature on echocardiographic strain by TDI has assessed longitudinal strain from the apical windows with LV shortening and lengthening aligned with the Doppler scan lines. In principle, strain rate is not influenced by overall motion of the heart or by motion caused by contraction in adjacent segments. Therefore, strains and strain rates are essentially similar between apex and base [14, 19] and are in principle superior to velocity as markers of regional contraction. However, there are technical issues that make strain rate imaging more challenging than velocity imaging [20, 21].

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Fig. 3 Myocardial strain and velocity. Representative traces at baseline, during left anterior descending (LAD) stenosis, and occlusion in an anesthetized dog showing myocardial Doppler velocities, strain, and pressure traces. Note that the ejection velocities are relatively similar during LAD stenosis and LAD occlusion, whereas the isovolumic contraction (IVC) and isovolumic relaxation (IVR) velocities are

markedly different. During LAD occlusion, the large negative velocity spike during IVC corresponds to systolic lengthening, as demonstrated in the strain trace. Furthermore, the marked postsystolic velocity during IVR corresponds to late systolic and postsystolic shortening in the strain trace (modified with permission from Skulstad et al. [14])

Speckle-Tracking Echocardiography

Two-dimensional (2D) speckle-tracking echocardiography (STE) is a relatively new approach for assessment of myocardial deformation. STE utilizes the phenomenon in which natural acoustic markers in gray scale ultrasound images form interference patterns (speckles) within myocardial tissue. Dedicated software filters out random noise, yielding small segments of myocardium with temporarily stable and unique speckle patterns (Bkernels^) [22]. The speckle patterns are

identified and myocardial deformation is automatically being tracked on a frame-by-frame basis (Fig. 4). The principal measurement is 2D displacement vs. time for the region of interest. Subsequently, regional deformation measures, such as strain and strain rate are calculated from each LV segment in circumferential, longitudinal, or transversal directions (Fig. 5). Furthermore, in short-axis projections, average angular motion can be quantified as average rotation [15], and circumferential and radial deformation can be measured. The ability of STE to measure LV strain and twist has been documented in studies that have used both sonomicrometry and magnetic resonance imaging as reference methods [3, 15, 25].

Fig. 4 Speckle Tracking by block matching. A speckle pattern within a region of interest is identified in one frame and tracked within a search region of the successive frame. After comparing this block with all possible matching regions within this search region (dotted blocks), the

position of the best matching block compared with the original block determines tissue motion. By repeating this process for multiple regionof-interest blocks, motion between two successive frames for the whole myocardium may be estimated (from Jasaityte et al. [23•])

Two-Dimensional Speckle Tracking

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Fig. 5 Presentation of 2D strain. a Tracking quality approval screen; segments with adequate tracking are assigned a green V mark. b Strain profiles from each apical view. Average segmental values in each segment are used to generate a parametric (bull’s eye) display of the entire left

ventricle. 2CH 2-chamber, 4CH 4-chamber, ANT anterior, APLAX apical long axis, AVC atrioventricular canal, INF inferior, LAT lateral, POST posterior, SEPT septal (with permission from Marwick et al. [24])

In contrast to TDI-based strain, which measures velocities from a fixed point in space with reference to an external probe, STE measures instantaneous distance between two kernels. This implies that unlike TDI, STE is relatively angle independent and can measure strain in different directions in the same image—including circumferential and radial strain in multiple segments from LV short-axis images and longitudinal strain from myocardial areas close to the LV apex. However, STE is not totally angle independent, because ultrasound images have better resolution along the ultrasound beam than perpendicular to the beam direction. Therefore, in principle, STE works better for measurements of motion and deformation in the direction along the ultrasound beams than for other directions.

In most patients, 2D strain can be successfully assessed by STE in multiple LV segments. Strain values are calculated for each segment (segmental strain), for each of the theoretical vascular distribution areas (territorial strain), and as the average value of all segmental strains (global strain, Fig. 6) [27]. Feasibility is best for longitudinal and circumferential strain and is more challenging for radial strain [26]. One explanation for the lower feasibility for radial assessment of strain is that fewer speckles are present in this direction. Normal global longitudinal strain values are reported between 18 and 25 % in healthy individuals [25, 27]. Yingchoncharoen et al. have provided a detailed report on normal ranges of various LV strain measures [28]. A

Fig. 6 Global strain assessment. Global strain curves from patient with large MI are shown on the left and medium-sized MI on the right. Longitudinal strain (red) was assessed in apical 2-chamber, 4-chamber, and long-axis views; circumferential strain (black) and radial strain (blue)

were assessed in basal, midventricular, and apical short-axis views. An ECG trace is displayed below the strain curves. ES end systole (with permission from Gjesdal et al. [26])

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number of studies have demonstrated that measurements of longitudinal and circumferential LV deformation are superior to LV ejection fraction (EF) as measures of LV function in patients with myocardial infarction [26, 29]. It is also feasible to measure right ventricular (RV) and atrial strain by STE. However, because of the thin walls of these structures, signal quality may be suboptimal.

Three-Dimensional Speckle Tracking Three-dimensional (3D) STE has recently been introduced as a method to measure cardiac deformation and volumes, and preliminary results are promising. LV strain by 3D-STE has been validated against sonomicrometry [30] and cardiac magnetic resonance imaging (CMR) [31]; however, challenges remain regarding accuracy of the tracking algorithms [32]. A thorough review of echocardiographic deformation imaging was provided by Jasaityte et al. [23•]. In contrast to 2D-STE, which cannot track motion occurring out of plane, 3D-STE can track motion of speckles within the scan volume, irrespective of its direction. Thus, in addition to strain measures of longitudinal, radial, and circumferential deformation, as well as combinations of these, rotation and twist parameters may also be quantified. 3D cine loops of LV with regional strain may be displayed as color codes superimposed on the LV, and strain vs. time curves can be displayed for all measured myocardial regions (Fig. 7). The effect of out of plane and twisting motion on LV strain by 2D-STE was assessed in a recent study by Wu et al. by directly comparing 2D- and 3D-STE [33]. They concluded that through-plane motion caused discrepancies in circumferential and longitudinal strain between the two methods, especially in the basal LV base. As for most 2D and 3D techniques, a limitation of the 3D-STE technique is its dependency on high image quality and, in particular, its ability to define the myocardial borders. Furthermore, 3D-STE is limited by relatively low temporal and spatial resolution. Several studies have shown feasibility of LV 3D strain in a clinical setting

Fig. 7 Presentation of strain by 3D-STE. After 3D speckle tracking has been performed, deformation is estimated and presented in different ways, for example, a with strain curves for different segments, b using

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[34–38]; however, few studies have assessed whether 3D strain provides added value to 2D strain. Thorstensen et al. demonstrated significant correlations between LV 2D strain and 3D strain by STE and delayed-enhancement MRI measurements of myocardial infarct size. However, even if 3D strain was feasible, it provided no added value to 2D strain [39]. In contrast, Urbano-Moral et al. found that LV global longitudinal and circumferential strain by 3D-STE, but not strain by 2D-STE, were predictive of NYHA functional class in heart transplant recipients [40]. Recently, 3D-STE has been applied to other cardiac chambers, including the left atrium (LA) [41] and right ventricle (RV) [42]. In a recent study by Smith et al., patients with pulmonary hypertension were assessed by 3D strain of the right ventricle (RV), compared to healthy controls, and followed up for 14 to 44 months [43]. Their study showed that patients with pulmonary hypertension had reduced RV strain compared to controls and that RV strain was related to clinical outcomes. The findings suggest that deformational imaging by 3D-STE can be useful in predicting outcomes and detecting subclinical disease in cardiac patients.

Limitations of Deformation Imaging by 2D and 3D Speckle-Tracking Echocardiography Like other 2D imaging techniques, 2D-STE relies on the assumption that morphologic details can be tracked from one frame to the next—that is, that they can be identified in consecutive frames. Because of the complex motion of the LV, this assumption may not always be valid. Suboptimal tracking of the endocardial border may be a problem, in particular when image quality is poor. Because of the spatial smoothing, an erroneous segmental tracking might influence neighboring segmental strain values. When strain traces appear unphysiological or are inconsistent with known pathophysiology, one should consider signal quality and suboptimal tracking as potential causes. Averaging of multiple regional strain values in order to obtain a Bglobal^ strain might be misjudged

bull’s eye plots, or c by showing the deformed surface. ES End systole, RS radial strain, CS circumferential strain, LS longitudinal strain (with permission from Jasaityte et al. [23•])

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if too many segmental strain values are discarded because of suboptimal tracking. This is particularly true in localized myocardial diseases where strain values are unevenly distributed. Raw tracking data are often quite noisy, so temporal and spatial averaging is needed to extract useful information. By turning off spatial and/or temporal smoothing, if possible, one gets a reasonable impression of the underlying signal quality that may be used for clinical decision-making. The relatively low temporal resolution of 2D-, and especially 3D-STE, is a limitation in particular in regard to assessment of strain rates, because accurate measurement of these variables may require higher frame rates. Reverberation with resulting underestimation of the true deformation represents an important and common source of error. Furthermore, any artifacts that resemble speckles will influence the speckle-tracking quality, and care should be taken to avoid these artifacts. Reproducibility of STE Measurements Since quantification of myocardial deformation by STE recently became available, the method has predominantly been utilized as a research tool but is now used increasingly in clinical practice. One important reason for the delay in implementation of the methodology is the relatively poor agreement for 2D-STE measurements among different ultrasound vendors [44, 45•, 46]. Discordant inter-vendor results for measurements by 3D-STE have also been reported [47]. In principle, there are three main sources of this variation in STE measurements: the hemodynamic status of the patient, acquisition parameters, and post-processing. Information on the hemodynamic status of the patient, and loading conditions in particular, is important in strain assessment since strain is sensitive to loading conditions [28, 48]. Thus, variation in systolic blood pressure may explain variation in strain in follow-up exams. The acquisition part of STE has traditionally been focused on avoiding under-sampling by obtaining a sufficient frame rate (40 to 60 frames/s is recommended). One should also note that by increasing frame rate, reduced image quality may be experienced because of reduction in line density and reduced tracking quality. Post-processing is probably the most important determinant in inter-vendor variation in STE measures [49]. These algorithms contain inherent assumptions of geometrical shape and direction of deformation of the area being tracked. Moreover, the raw data tends to be quite noisy, so different fitting and smoothing algorithms are being used before the data are presented to the user. Some vendors primarily include the epicardium in the STE analysis, others include the endocardium, and some the entire wall thickness. Strain can be calculated by different approaches, and different strain calculations are being used (Lagrangian vs. natural strain). In a community-based study, Cheng et al. investigated reproducibility of 2D-STE. Participants underwent regular 2D echocardiography exams three times during a period of

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12 months, and global strain measures including GLS and GCS were analyzed using vendor-independent software. Excellent reproducibility of GLS and GCS measurements were observed; the authors concluded that the findings demonstrate the reproducibility of performing 2D-STE measurements in a large, epidemiologic community-based setting [50]. Recently, Badano et al. investigated inter-vendor agreement of 3D-STE by comparing ultrasound scanners and vendorspecific STE software. Global longitudinal (GLS), circumferential, radial, and area strain from 3D-STE recordings were measured in patients with a wide range of LV end-diastolic volumes. All strain measurements were significantly different between the vendors, and apart from GLS, the inter-vendor agreement was poor. The authors suggest that reference values specific for each system should be determined, and follow-up exams should be done on the same 3D equipment [51]. In an effort to reduce inter-vendor variability of echocardiographic deformation imaging, the American Society of Echocardiography (ASE) and the European Association of Cardiovascular Imaging (EACVI) invited technical representatives from interested vendors to participate by joining the EACVI-ASE industry initiative to standardize deformation imaging [52]. In several recent studies, normal ranges of STE measurements by various vendors have been reported. Fine et al. reported reference values for RV and LV 2D-STE measurements by vendor-independent software from recordings obtained from different ultrasound scanners [53]. Cheng et al. reported age- and sex-specific reference limits for LV 2D-STE measures by vendor-independent STE software in a large communitybased study [54]. Maharaj et al. provided reference values for LV twist and strain values by vendor-independent 2D-STE software in a healthy African adult population [55].

LV Deformation Imaging in Ischemic Heart Disease Myocardial ischemia leads to reduction in regional myocardial function, which ranges from reduced systolic shortening (hypokinesis) to systolic lengthening (dyskinesis). Furthermore, myocardial ischemia leads to postsystolic shortening, that is, segmental shortening after end of LVejection. Reduced systolic shortening (or in transmural ischemia, systolic lengthening) and postsystolic shortening, which are the two hallmarks of ischemic dysfunction, can be quantified by deformation imaging [1, 2, 19, 56–58]. Typical strain tracing during acute myocardial ischemia are shown in Figs. 2 and 3. The main advantage of strain relative to velocity imaging is that measurements are less influenced by translational motion and tethering, and this makes strain more specific with regard to segmental localization of ischemia [2]. Therefore, in patients with acute infarction, strain better defines the transitional zone between intact and dysfunctional myocardium and is superior

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to velocity imaging for defining anatomical extension of dysfunctional myocardium [14]. LV strain imaging is also useful in the assessment of myocardial viability by stress echocardiography. Importantly, global longitudinal strain (GLS) has been demonstrated to be a sensitive marker of LV function [59] and to predict outcomes [60]. Postsystolic shortening can be used as a marker of acute as well as stress-induced myocardial ischemia [58, 61–63]. The mechanism of postsystolic shortening can be delayed active contraction, passive recoil of dyskinetic myocardium, or a combination of active contraction and passive recoil [64]. One should remember, however, that postsystolic shortening can be present in normal myocardium, although the magnitude is less than in an ischemic ventricle [65]. A postsystolic strain of more than 2.5 % in absolute value, or more than 20 % relative to maximal systolic deformation, has been suggested as cut-off values for pathological vs. normal postsystolic shortening [58]. In a recent study on patients with MI and LVEF >40 %, Ersboll et al. assessed GLS by a semi-automated 2D-STE algorithm. A significant and independent association was found for GLS and all-cause mortality and hospitalization for heart failure during the median follow-up of 30 months. GLS provided important prognostic information in patients with LVEF >40 % above and beyond traditional indexes of high-risk MI [66•]. In another study by Ersboll et al., GLS and mechanical dispersion by 2D-STE were assessed in patients with acute myocardial infarction as measures of infarct size and LV deformation heterogeneity, respectively. Both GLS and mechanical dispersion were significantly and independently related to sudden cardiac death or admission with ventricular arrhythmia during the median follow-up of 30 months. Moreover, GLS improved risk stratification above and beyond existing risk factors [67]. In a similar study, Haugaa et al. assessed GLS and mechanical dispersion by 2D-STE in patients with a recent MI. Mechanical dispersion predicted sudden cardiac death or sustained ventricular tachycardia during a median follow-up of 30 months, irrespective of LVEF. Patients with ischemic cardiomyopathy were examined for layer-specific LV circumferential strain by 2D-STE and strainencoded CMR (SENC) in a study by Altiok et al. Strain by both methods was compared for the assessment of infarct transmurality by late gadolinium enhancement CMR. Layerspecific LV deformation analysis by STE and SENC allowed discrimination between different transmurality categories of myocardial infarction with similar accuracy. However, accuracy of both methods is non-optimal, indicating that further improvement is needed. Patients with suspected stable angina pectoris were assessed by 2D-STE-derived GLS in a study by Biering-Sorensen et al. Peak systolic GLS assessed at rest was an independent predictor of angiography-determined significant coronary artery disease and significantly improved the diagnostic performance of exercise testing [68]. In a study by Sarvari et al., patients referred to coronary angiography

due to suspected non-ST-segment elevation acute coronary syndromes were assessed by 2D-STE. Layer-specific circumferential and longitudinal strain measured prior to angiography identified patients with significant coronary stenosis. Endocardial function was more affected than epicardial function and LVEF in patients with significant coronary stenosis [69].

LV Deformation Imaging-Mechanical Dyssynchrony Dyssynchronous LV contraction is associated with ineffective LV pump function. Mechanical dyssynchrony (MD) is conventionally defined as an increased time delay between contractions of the various LV regions. Several indices exist: MD may be quantified as the standard deviation of time to peak regional LV strain or regional differences in timing of peak strain and end-systolic strain. Some studies have suggested that indices of mechanical dyssynchrony may predict response to cardiac resynchronization therapy (CRT) [70]. A large number of dyssynchrony indices have been introduced; however, due to somewhat disappointing results, there is currently a lack of consensus on which index should be used to predict CRT response [71]. Recently, Park et al. assessed GLS by 2D-STE in addition to standard echocardiographic measurements prior to CRT at baseline and after 1-year follow-up. The combined echocardiographic score allowed prediction of LV reverse remodeling, and the score was independently associated with all-cause death [72]. Kydd et al. assessed radial strain by 2D-STE in patients before CRT implantation. The index combining magnitude and timing of regional LV radial strain predicted response to CRT treatment and survival during 6 months follow-up [73]. Importantly, a number of imaging-based dyssynchrony markers have been tested, but none of these has proven to increase CRT responder rate when studied in prospective clinical trials. Therefore, current guidelines do not recommend assessment of dyssynchrony by any imaging modality in the diagnostic work up when patients are evaluated for CRT [74].

LV Deformation Imaging in Cardiomyopathies and Drug-Induced Cardiotoxicity Cardiomyopathies Urbano-Moral et al. studied patients with hypertrophic cardiomyopathy (HCM) by 3D-STE and CMR with late gadolinium enhancement (LGE). They conclude by stating that both hypertrophy and fibrosis contribute to regional impairment of myocardial shortening. The extent of hypertrophy is the primary factor altering global myocardial mechanics, whereas circumferential LV shortening seems to be directly

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involved in preservation of LV systolic performance in HCM [36]. In another study on HCM patients, Kobayashi et al. examined regional septal function by 2D-STE and degree of fibrosis by histopathology prior to myectomy. They found an inverse association between various histopathologic findings and septal strain rate [75]. In a similar study on HCM patients, Almaas et al. examined the degree of LV fibrosis by LGE CMR and histopathology, and quantified septal function by 2D-STE prior to myectomy. Longitudinal septal strain correlated better with interstitial and total fibrosis by histopathology and was a more powerful predictor of arrhythmias than LGE [76]. In a recent study by Quarta et al., patients with cardiac amyloidosis (CA) were assessed by 2D-STE. Despite a preserved LVEF, longitudinal strain was severely impaired in CA. Worsening LV function correlated with increasing wall thickness regardless of pathogenesis. Reduced longitudinal strain and advanced New York Heart Association class were negative predictors of survival [77]. Patients with arrhythmogenic right ventricular dysplasia (ARVC) without symptoms of RF heart failure were studied by Vitarelli et al. Patients and healthy controls were examined by 2D- and 3D-STE at rest and after stress. A low increment in RV free wall strain during stress had an additive value to conventional measures in predicting ARVD [78].

GLS was an independent predictor of reduction in LVEF and was incremental to established predictors for drug-induced cardiotoxicity [87]. Many studies that have shown prognostic information on drug-induced cardiotoxicity derived from echocardiographic deformation indices have been relatively small. However, Thavendiranathan et al. recently published an important systematic review with more than 1500 patients. They found that echocardiographic deformation parameters indeed had value for the early detection of myocardial changes and prediction of cardiotoxicity in patients receiving cancer therapy. A 10 to 15 % early reduction in global longitudinal strain (GLS) by STE appeared to be the most useful parameter for the prediction of cardiotoxicity [88•]. Several papers have reported that echocardiographic deformation indices carry important prognostic information for drug-induced cardiotoxicity in cancer patients, beyond LVEF. Even if more outcome studies are needed, echocardiographic deformation imaging has the potential to become an important clinical tool in the cardiac assessment of cancer patients.

Drug-Induced Cardiotoxicity

Right Ventricular Deformation

In contrast to the decreased mortality rate in cancer patients over the past decades, cardiac toxicity (cardiotoxicity) from cancer therapy has become a leading cause of morbidity and mortality in survivors [79]. In patients who develop heart failure from cancer therapy, the 2-year mortality rate is above 50 % [80]. Traditionally, diagnosis has relied upon serial echocardiographic imaging to identify reduction in LVEF [81]. However, reduction in LVEF is often a late phenomenon, and myocardial deformation imaging has been shown to be a sensitive tool for the detection of early cardiotoxicity [82, 83]. Lipshultz et al. recently published a comprehensive description of cardiovascular toxicity in children and young adults who receive cancer therapy in a scientific statement from the American Heart Association [84]. Sawaya et al. studied breast cancer patients treated with chemotherapy and found that longitudinal systolic strain in combination with ultrasensitive troponin I predicted subsequent cardiotoxicity over 15 months [85]. In a recent paper by Stoodley et al., breast cancer patients underwent strain and strain rate measurements by 2D-STE at baseline and immediately after anthracycline chemotherapy. They observed altered LV diastolic function immediately after anthracycline therapy and that changes in diastolic function were associated with reduced systolic function [86]. Negishi et al. measured GLS by 2D-STE in breast cancer patients treated by trastuzumab.

Patients with pulmonary hypertension (PHT) were recently studied by Smith et al. and examined by 3D-STE of the right ventricle (RV). Compared to controls, PHT patients had reduced RV strain patterns and more dyssynchronous ventricles. RV area strain correlated best to RVEF and provided prognostic information during 14 to 44 months follow-up, independent of other variables [43]. In another study on PHT patients, Motoji et al. obtained RV 2D-STE strain measurements. They concluded that RV free wall strain might serve as a non-invasive predictor of cardiovascular events, especially when assessed in combination with tricuspid annular plane systolic excursion [89]. Hardegree et al. studied PHT patients by assessment of RV and LV function by 2D-STE. The increased RV afterload in PHT patients was associated with geometrical alterations and functional decline of the RV, with marked reduction in RV systolic strain. However, despite preserved LVEF, LV systolic strain was also reduced and associated with early mortality [90]. Ternacle et al. studied patients referred to cardiac surgery by assessing RV function by 2D-STE prior to surgery. Of the systolic RV indices studied, RV-GLS was an independent predictor of 1-month mortality by multivariate analysis adjusted to EuroSCORE-II and duration of cardiopulmonary bypass [91]. Dandel et al. assessed RV function by longitudinal strain rate by 2D-STE in addition to regular

Myocardial Deformation Imaging of the Right Ventricle and Left Atrium

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echocardiography, laboratory, and invasively measured hemodynamic data in patients prior to implantation of LV assist devices (LVADs). A jointly preoperatively assessment of RV geometry and shortening rate, as well as RV load and tricuspid regurgitation, predicted postoperative RV function and may improve decision-making before LVAD implantation [92]. Left Atrial Deformation Although no direct validation has been performed, 2D- and 3D-STE analyses have been applied to the atria. Leong et al. related LA strain by transthoracal 2D-STE and TDI and to transesophageal echocardiographic measures of LA appendage emptying velocity and spontaneous echo contrast. The authors found that assessment of LA mechanical function by STE-derived strain was a clinically feasible and valid approach compared with transesophageal echocardiography [93]. LA mechanical function is associated with LA fibrosis and development of atrial fibrillation (AFib). Obokata et al. studied patients with persistent or paroxysmal AFib with or without embolus and assessed LA strain by 2D-STE. Peak LA global longitudinal strain (LA-GLS) during AFib rhythm was lower in patients with, than without, embolism. LA-GLS had incremental value over CHA2DS2-VASc score for predicting embolism. Moreover, LA-GLS independently predicted mortality after embolism [94]. Mochizuki et al. assessed LA function by 2Dand 3D-STE in patients with AFib and in healthy controls. They concluded by stating that 3D-STE enables the measurement of both LA strain and synchrony with excellent reproducibility and that 3D LA strain appears to be beneficial compared with 2D LA strain for identifying patients with paroxysmal AFib [38]. Chadaide et al. assessed LA deformation by 3D-STE in patients with AFib. Compared to controls, 3D-derived strain measures were reduced in patients with AFib. LA strain provides incremental value for embolism risk over traditional risk scores and carries prognostic impact in patients with atrial fibrillation [95]. LV global diastolic strain rate provides prediction of cardiac outcomes in patients with atrial fibrillation when assessed in combination with early mitral inflow velocity [96]. In a recent study by Ring et al., patients with mitral valve prolapse were assessed by 2D-STE-derived LA strain. Measures of LA strain, in addition to total LA emptying fraction, were independent predictors of severe mitral regurgitation requiring surgery [97].

Conclusions Deformation imaging by echocardiography allows for objective quantification of mechanical myocardial function.

LV strain and strain rate by TDI, and more recently, strain and twist assessment by STE, have provided increased pathophysiologic understanding of heart diseases—including ischemic heart disease, cardiomyopathies, electrical LV dyssynchrony, as well as RV and LA function. Three-dimensional strain assessments have provided even further pathophysiologic understanding of the complex three-dimensional LV deformation. Thus, echocardiographic quantification of myocardial deformation has been established as a powerful tool for cardiac research. Furthermore, deformation imaging is emerging as a promising clinical tool in experienced echocardiographic laboratories. Some studies suggesting added value in predicting outcome have been published; however, more studies are needed. When a standardization of deformation measurements allowing for less measurement difference between various vendors is achieved, deformation imaging by echocardiography has the potential to become an important clinical tool in the evaluation of patients with heart disease. Compliance with Ethics Guidelines Conflict of Interest Anders Opdahl, Thomas Helle-Valle, Helge Skulstad, and Otto A. Smiseth declare that they have no conflict of interest. Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.

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Strain, strain rate, torsion, and twist: echocardiographic evaluation.

Deformation imaging by tissue Doppler imaging (TDI) and speckle-tracking echocardiography (STE) are emerging clinical methods. TDI- and STE-derived pa...
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