Myocardial Strain Evaluation with Cardiovascular MRI: Physics, Principles, and Clinical Applications
Abstract
Myocardial strain is a measure of myocardial deformation, which is a more sensitive imaging biomarker of myocardial disease than the commonly used ventricular ejection fraction. Although myocardial strain is commonly evaluated by using speckle-tracking echocardiography, cardiovascular MRI (CMR) is increasingly performed for this purpose. The most common CMR technique is feature tracking (FT), which involves postprocessing of routinely acquired cine MR images. Other CMR strain techniques require dedicated sequences, including myocardial tagging, strain-encoded imaging, displacement encoding with stimulated echoes, and tissue phase mapping. The complex systolic motion of the heart can be resolved into longitudinal strain, circumferential strain, radial strain, and torsion. Myocardial strain metrics include strain, strain rate, displacement, velocity, torsion, and torsion rate. Wide variability exists in the reference ranges for strain dependent on the imaging technique, analysis software, operator, patient demographics, and hemodynamic factors. In anticancer therapy cardiotoxicity, CMR myocardial strain can help identify left ventricular dysfunction before the decline of ejection fraction. CMR myocardial strain is also valuable for identifying patients with left ventricle dyssynchrony who will benefit from cardiac resynchronization therapy. CMR myocardial strain is also useful in ischemic heart disease, cardiomyopathies, pulmonary hypertension, and congenital heart disease. The authors review the physics, principles, and clinical applications of CMR strain techniques.
Online supplemental material is available for this article.
©RSNA, 2022
SA-CME LEARNING OBJECTIVES
After completing this journal-based SA-CME activity, participants will be able to:
■ Review the principles and components of myocardial strain.
■ Discuss the different MRI techniques for imaging myocardial strain.
■ Describe the clinical applications of myocardial strain evaluation with MRI.
Introduction
Early detection of cardiovascular disease facilitates prompt initiation of appropriate therapy and prevents the development of irreversible complications. Although ejection fraction is the most common imaging biomarker for myocardial systolic function, it is not a sensitive metric. Ejection fraction is normal in 40% of patients with heart failure (ie, heart failure with preserved ejection fraction [HFpEF]). Ejection fraction may also be normal in regional entities, such as ischemic heart disease and myocarditis. Conversely, an abnormal ejection fraction usually implies a late potentially irreversible stage of the underlying cardiovascular disease.
Myocardial strain is an indicator of myocardial deformation as it shortens, lengthens, thickens, and rotates during the cardiac cycle. Strain refers to deformation of a structure following application of stress (1).
Myocardial strain is a change in the measurement of the tissue between relaxed and contracted states
Figure 1. Schematic illustration depicts myocardial strain. Myocardial strain is the change in measurement (eg, length, thickness) of the myofiber between relaxed and contracted states. If LO is the initial fiber length and L1 is the final fiber length, Lagrangian strain is computed as (L1−L0)/L0. Strain values are positive if the final fiber length or thickness is larger than the original fiber length or thickness. Conversely, strain values are negative if the final fiber length or thickness is smaller than the original fiber length or thickness.
Movie 1. Animation demonstrating myocardial strain. Myocardial strain is the change in the length of myofiber between relaxed and contracted states, calculated as L0–L1/L0, where L0 is the initial fiber length and L1 is the final fiber length.
Myocardial systolic motion is complex owing to varied orientation of myofibers in different myocardial layers. The subepicardial fibers are oriented in a left-handed helix (−60° helical angle) and the subendocardial fibers are oriented in a right-handed helix (+60° helical angle) (3,4). The midwall myofibers are oriented circumferentially (Fig 2). Longitudinal strain (€l) occurs along the longitudinal axis of the heart owing to myocardial shortening from the base to apex (Movie 2). Circumferential strain (€c) occurs along the short-axis circumference owing to concentric intramural myocardial shortening along a curved line parallel to the epicardial surface (Movie 3). Radial strain (€r) involves thickening of the myocardium in the radial direction toward the center of the ventricular cavity (Movie 4).
In ventricular systole, longitudinal and circumferential strains have negative values, whereas radial strain has positive values
Figure 2. Schematic illustration shows the orientation of myofibers. The orientation of myofibers is different in each layer of the myocardium. The subepicardial (green circle) and subendocardial (yellow circle) myofibers are oriented helically, with a left-handed helical orientation (−60° angle) of the subepicardial layer and a right-handed helical orientation of the subendocardial layer (+60° helical angle). The midwall myofibers (red circle) are oriented circumferentially.
Movie 2. Animation demonstrating longitudinal strain. Longitudinal strain is the contraction along the longitudinal axis of the heart owing to myocardial shortening from the base to apex.
Movie 3. Animation demonstrating circumferential strain. Circumferential strain is the contraction along the circumference in the short axis owing to concentric intramural myocardial shortening along a curved line parallel to the epicardial surface.
Movie 4. Animation demonstrating radial strain. Radial strain is the thickening of the myocardium in the radial direction toward the center of the ventricular cavity.
Figure 3. Schematic illustration shows the types of myocardial strain. Longitudinal strain is along the longitudinal axis of the heart owing to myocardial shortening from the base to the apex. Circumferential strain is along the short-axis circumference owing to concentric intramural myocardial shortening. Radial strain involves thickening of the myocardium in the radial direction toward the center of the ventricular cavity. Torsion is motion that is relative to a stationary midventricular reference, with clockwise rotation of the basal segments and counterclockwise rotation of the apical segments.
Movie 5. Animation demonstrating torsion. Torsion is rotational motion caused by clockwise rotation of the basal segments and counterclockwise rotation of the apical segments.
Strain Imaging Techniques
Echocardiography is the most performed imaging technique for myocardial strain, either by using speckle-tracking echocardiography (STE) or tissue Doppler imaging (TDI). The high temporal resolution of echocardiography is well suited to evaluate rapid events such as myocardial activation and patients with high heart rates (7). Two-dimensional or three-dimensional (3D) STE uses dedicated postprocessing software to track the myocardial speckles produced by reflection of myofibers throughout the cardiac cycle (Fig 4) (2,8). Depending on the algorithm, STE helps evaluate speckle motion mainly at the endocardial border (2). TDI helps evaluate velocity between two points in the myocardium. TDI is limited to one direction along the ultrasound beam to evaluate global longitudinal strain (GLS) in the apical window, which is sensitive to noise. Variable image quality, operator dependency, limited acoustic windows, and lower signal-to-noise ratio are limitations of echocardiography (2).
Figure 4. STE in a patient with cardiac amyloidosis shows decreased global longitudinal strain (GLS) in the myocardial segments with characteristic sparing of the apical segments. At echocardiography, normal longitudinal strain values are more negative than −18. The yellow numbers on the echocardiogram correspond to peak systolic strain value (%) for the each myocardial segment. The graph depicts longitudinal strain over time for the left ventricular myocardial segments highlighted in the left images. The color-coded polar map shows peak left ventricular systolic longitudinal strain by myocardial segment according to the American Heart Association 17-segment model. ANT = anterior, AVC = aortic valve closure, INF = inferior, LAT = lateral, POST = posterior, SEPT = septal.
CT is another imaging technique that can help in the evaluation of myocardial strain by using a retrospective electrocardiographically-gatedtechnique and feature-tracking (FT) algorithm. CT strain values correlate well with echocardiography and have been evaluated in several pathologic conditions including aortic stenosis and coronary artery disease (9). Although the evidence for CT strain is limited, it has a potential role in providing ancillary information in patients undergoing cardiac CT for other purposes or those with contraindications to cardiovascular MRI (CMR) and poor echocardiographic windows.
CMR Strain Techniques
CMR, the current reference standard for myocardial function and volumes, can also be used for the evaluation of myocardial strain. Several CMR strain techniques are available, with most requiring dedicated CMR sequences and some requiring dedicated postprocessing software (10,11) (Table 1).
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Myocardial Tagging
Myocardial tagging is the oldest CMR strain technique, in which dark tags or lines are applied on the myocardium and their deformation followed through the cardiac cycle. In the commonly used spatial modulation of magnetization (SPAMM) sequence, two nonselective radiofrequency pulses (usually 90°) are applied, separated by a tagging gradient. The tagging gradient disperses the spins on the basis of phase shifts, which is stored in the longitudinal direction by the second radiofrequency pulse, and a crusher gradient is used to eliminate the remaining transverse magnetization. The myocardium in between the tags is not dark (Fig 5, Movie 6). The tags are usually applied at end diastole and followed through the rest of the cardiac cycle. Owing to longitudinal relaxation, the tags typically fade in early diastole, limiting the assessment of diastolic function (11). Longer persistence throughout the cardiac cycle can be achieved by using 3-T magnets. Complementary SPAMM is a variation of SPAMM that acquires two SPAMM sequences with different polarities, generating positive and negative sinusoidal tagging patterns. Subtracting these two images eliminates nontagged offset signal, and using ramped flip angles enhances the tagging contrast throughout the cardiac cycle. As a result, complementary SPAMM has brighter, better-defined, and sharper lines than those of SPAMM, and these lines persist in diastole. However, complementary SPAMM has a longer acquisition time, with potential for motion artifacts.
Figure 5. SPAMM myocardial tagging. (A) Short-axis SPAMM myocardial tagged image shows multiple dark grids on the myocardium, which can be tracked during the cardiac cycle. The myocardium in between the tags is not dark. (B) Another example shows a two-chamber SPAMM myocardial tagged image by using lines.
Movie 6. Myocardial tagging. Short-axis SPAMM grid-tagged clips show the deformation of the grids during the cardiac cycle. Note that the tags fade in diastole.
Quantitative postprocessing of tagging is usually time consuming and complex. Harmonic phase analysis (HARP) is the most used technique, which analyzes the k-space rather than the image itself. By using a spatial band-pass filter, only the first harmonic peak is extracted from the original SPAMM acquisition. Using Fourier transform, magnitude and phase HARP images are obtained, which are then multiplied to generate a modulation pattern like the original tag to generate a HARP image with strain encoding (11).
Strain-encoded Imaging
Strain-encoded imaging (SENC) also uses myocardial tags, but the tagging gradients are applied perpendicular to the imaging plane to record through-plane strain. During the imaging phase, tuning gradients are applied in the z-direction between section selection and readout gradients. Low-tuning and high-tuning gradients modulate the magnetization with low and high frequencies, respectively. The resulting low-tuning and high-tuning images represent static tissue (which maintains low modulation frequency owing to noncontraction) and contracting tissue (which undergoes high modulation frequency owing to tissue contraction), respectively. Therefore, by pixelwise comparison of the relative signals in the low-tuning and high-tuning images, myocardial strain can be accurately measured. The pixelwise high-spatial-resolution color-coded strain map can be visually evaluated (12) (Fig 6, Movie 7). Longitudinal strain can be evaluated on short-axis images and circumferential strain on long-axis images, but radial strain cannot be calculated.
Figure 6. Strain-encoded imaging. (A) Short-axis SENC image shows tagging gradients applied perpendicular to the imaging plane, which records through-plane strain. (B) Short-axis SENC color-coded map shows high-resolution pixel-by-pixel calculation of myocardial strain. (Fig 6B courtesy of Benjamin Freed, MD, Northwestern University, Chicago, Il.)
Movie 7. SENC. High-spatial-resolution color-coded strain map using the SENC technique based on pixel-by-pixel calculation with strain values shown on the graph at the bottom. (Courtesy of Benjamin Freed, MD, Northwestern University, Chicago, Il.)
Composite SENC (cSENC) is a variation of SENC in which nontuning images are obtained in addition to low-tuning and high-tuning images following contrast material administration. Owing to accumulation of gadolinium-based contrast material, scar tissue has high signal intensity on T1-weighted images, whereas normal tissue has low signal intensity. Thus, cSENC allows simultaneous evaluation of myocardial strain and viability (11) (Fig 7). Since the acquired nontuning image is a T1-weighted image based on saturation recovery, image contrast between scar and normal myocardium is lesser than that at conventional inversion recovery late gadolinium enhancement (LGE) imaging (11).
Figure 7. Composite SENC technique. Composite SENC images include low-tuning (LT) images from noncontracting tissues, high-tuning (HT) imagesfrom contracting tissues, and images without additional tuning (NT). Infarcted myocardial tissue results in larger signal than that in the normal myocardium 15 minutes after gadolinium-based contrast material injection owing to preferential accumulation in the infarct. The NT image shows a noticeable difference between normal and abnormal myocardium. (Reprinted, under a CC BY 4.0 license, from reference 11.)
Displacement Encoding with Stimulated Echoes
Displacement encoding with stimulated echoes (DENSE) technique encodes tissue displacement into the phase of an image. DENSE is performed by using a stimulated echo acquisition mode (STEAM) sequence in which three radiofrequency pulses are used to generate a stimulated echo. Equal displacement encoding (modulation) and decoding (demodulation) gradients are added after the first and third radiofrequency pulses, respectively, in the direction where displacement is needed. Large crusher gradients are used in between to diphase transverse magnetization, and hence the remaining magnetization is stored in the longitudinal direction (13). Position encoding of magnetization is performed at the end-diastolic phase, with imaging of subsequent tissue displacement with the cardiac cycle (Movie 8). Gradients encode this tissue displacement into the phase of the image. Representative vectors are drawn at each pixel, with vector magnitude and direction representing the displacement value and orientation, respectively. DENSE uses pixel-by-pixel displacement and has higher spatial resolution without the need for user interaction (Fig 8). A fast cine DENSE sequence uses echo combination reconstruction and intrinsic phase correction by using a balanced steady-state free precession (SSFP) sequence (5). DENSE can also be performed with a true 3D volumetric acquisition (14). DENSE has a low signal-to-noise ratio and diastolic fading owing to T1 relaxation properties.
Movie 8. DENSE. Magnitude and phase clips used for DENSE strain imaging. These images are the result of encoding displacement into the phase of the image.
Figure 8. DENSE technique. Tissue displacement maps were obtained at near end diastole and end systole in short-axis sections generated from DENSE acquisition.
Tissue Phase Mapping
Tissue phase mapping uses velocity-encoded bipolar gradients to encode the tissue velocity in the phase of the CMR signal. This calculates the velocities/trajectories of different points within the myocardium (15). Integrating the myocardial velocities in three directions over time yields myocardial displacements. Spatial derivatives of these displacements yield strain, whereas spatial derivatives of myocardial velocities yield strain rate. Segmental and regional strains can be evaluated in the longitudinal, circumferential, and radial directions (Movie 9). As this method has been traditionally subject to long imaging times that can lead to motion artifacts, large movements cannot be assessed (16). The potential for these phase errors to be magnified over the course of the cardiac cycle may make strain derivation less accurate with this method. Thus, tridirectional velocity data are typically reported with this method, rather than the strain (Figs 9, 10). Parallel imaging techniques allow tissue phase mapping sequences to be performed within a single breath-hold (17). Three-dimensional information can be obtained from two continuous two-dimensional sections acquired with a single-shot hybrid gradient-echo–echo-planar sequence (17).
Movie 9. Cine phase clips used for tissue phase mapping. By integrating the myocardial velocities in the three directions, the spatial derivatives of velocities are calculated at each pixel, and strain is derived from the motion.
Figure 9. Tissue phase mapping. (A) Short-axis phase image of a tissue mapping sequence in which velocity-encoding gradient is used to encode tissue velocity in the phase image. (B) From the velocity-encoded phase images, segmental myocardial velocities are displayed in the short-axis plane. Blue arrows = velocities of individual pixelwise velocities (small dots and lines) in eight evenly-spaced LV areas.
Figure 10. Tissue phase mapping. Images show the contributions of radial, circumferential, and longitudinal motion during different phases of the cardiac cycle. The left column shows late diastole images, the middle column shows early systole images, and the right column shows late systole images. The top row shows short-axis magnitude images, the middle row shows color-coded velocity maps, and the bottom row shows pixelwise arrow plots of the in-plane velocity component.
Feature Tracking
FT is the most recent CMR strain technique based on postprocessing of routinely acquired SSFP cine imagesFT postprocessing begins with defining endocardial and epicardial borders on short- and long-axis cine images (Fig 11). The axes of the annular planes are then defined, and the ventricular long axis is delineated on long-axis images. The contours are then propagated to all the cardiac phases. Longitudinal strain is obtained from long-axis images, circumferential strain is obtained from short-axis images, and radial strain can be obtained from either long- or short-axis images (Movie 10). Three-dimensional technique allows simultaneous estimation of radial, circumferential, and longitudinal strain parameters (18,20). The postprocessing can be rapid with the use of artificial intelligence techniques. Color-coded strain data can be overlaid on cine SSFP images (Movie 11).
Figure 11. Left and right ventricular contours for MRI FT strain analysis. Four-chamber (A) and mid short-axis cine (B) SSFP images show left and right subendocardial (red and yellow contours, respectively) and left and right subepicardial (green and light blue contours, respectively) contours. Left and right ventricular long axes (dark blue and orange lines in A, respectively) are defined according to lines extending the ventricular apices to their respective atrioventricular valve planes. The purple and olive lines in A are drawn through the mitral and tricuspid annular planes.
Movie 10. FT myocardial points. Short-axis cine SSFP clip with FT overlay of the myocardial points are shown in yellow.
Movie 11. CMR FT strain depiction with cine color overlay. Four-chamber cine SSFP clip with LV longitudinal strain color overlay is depicted on the left. Midventricular short-axis SSFP section with LV circumferential strain color overlay is in the center. Three-dimensional cine clip demonstrating LV and RV radial strains with color overlay is on the right.
Like other CMR-based strain techniques, temporal resolution of FT is lower than that of echocardiography, which limits its ability to resolve short-lived phases of the cardiac cycle. Although CMR FT can reliably distinguish epicardial and endocardial borders, precise delineation of the features within the myocardium remains relatively limited by pixel size (20). Blood motion can affect tracking close to the endocardium (5). Through-plane loss of features is seen with the two-dimensional technique.
Deformable Registration Analysis
Deformable registration analysis (DRA) is another recent CMR strain technique that can be performed on routine cine SSFP images. DRA is an inverse of the motion correction algorithms that are used for calculating pixelwise deformation maps for nonrigid image registration in CMR techniques such as perfusion. Each myocardial pixel is divided into three layers, and the deformation is calculated over the entire cardiac cycle. This technique has been validated against tagging and is more reproducible than FT (21).
Strain Measurements
Several strain metrics are available. Strain, expressed without a unit or as a percentage, is measured in longitudinal, circumferential, and radial directions (Figs 12, 13). Strain rate is the rate of change of strain (1/sec), which is a better marker of actual contractility owing to lesser dependence on load and chamber size than strain (22). Strain rates can be registered as peak systolic, early diastolic, and late diastolic strain rates, useful for the evaluation of cardiomyopathies and HFpEF. Time to peak strain (in seconds) is the time from the beginning of the cardiac cycle to the maximal positive or negative strain, normalized to the RR interval duration, useful in left ventricular (LV) dyssynchrony. Displacement (in millimeters) and velocity (millimeters per second) can also be obtained. Torsion can be expressed either as twist angle (degrees), circumferential longitudinal shear angle (degrees), torsion (degree/centimeter), or torsion rate (degree/(centimeter × second). Torsion is a sensitive marker for both systolic and diastolic dysfunction and is useful in cardiomyopathies. All of the previously mentioned strain values can be displayed for the entire (global) heart, section position (basal, mid, apical), American Heart Association 17 segments, endocardium and epicardium, or specific region of interest. Polar maps can display strain metrics in all of the 17 segments (Fig E1). There is no consensus on the optimal strain parameter that can be used in all clinical applications.
Figure 12. FT strain measurements. (A) FT with longitudinal strain overlay on a four-chamber cine SSFP image and corresponding map show the longitudinal strain values in all 17 American Heart Association segments. Longitudinal values are usually in the negative range. Color scale ranges from −20% to +20%. On the graph, the vertical axis shows longitudinal strain (%), and the horizontal axis shows time in milliseconds. (B) FT with circumferential strain overlay on a short-axis cine SSFP image and corresponding map show the circumferential strain values in all 17 American Heart Association segments. Circumferential strain values are also usually in the negative range. On the graph, the vertical axis shows circumferential strain (%), and the horizontal axis shows time in milliseconds (C) FT with radial strain overlay on a four-chamber cine SSFP image and corresponding map show the radial strain values in all 17 American Heart Association segments. Radial strain values are usually positive. Color scale ranges from −10% to +10%. On the graph, the vertical axis shows radial strain (%), and the horizontal axis shows time in milliseconds.
Figure 13. FT metrics. FT strain measurements can be obtained at different levels, including the entire heart (top left), entire section (top middle), sections (typically basal, mid, apical; top right), 17 American Heart Association segments (bottom left), endocardium-epicardium (bottom middle), or a specific region of interest (ROI, bottom right). On these example graphs, longitudinal strain has been measured at different levels. Each vertical axis shows longitudinal strain (%), and each horizontal axis shows time in milliseconds.
There is wide variability in normal reference ranges for LV strain (Table 2) owing to multiple factors, including those related to the modality (eg, spatial and temporal resolutions), software (eg, search region size, boundary definition, and computation algorithms), operator (eg, contour tracing), patient demographics (age, sex, race), and hemodynamic factors (heart rate, blood pressure, loading conditions) (2,5,23). For example, increasing age is associated with decreased peak circumferential or longitudinal strains, and women have higher strain values than men (24). Strain assessment at the global level is more robust than at the section or segmental level (5). Within global values, greater heterogeneity of global radial strain is seen compared with GLS and global circumferential strain (GCS) (2). GLS is the most robust and commonly used strain metric. GLS is measured either in a single four-chamber view or three long-axis views (23). Global radial strain and GCS are usually measured in short-axis sections, either at the mid ventricular level or three sections at the basal, mid, and apical ventricular levels. The clinical application of a given strain technique requires comparison with the appropriate reference range, preferably one that closely matches the imaging technique, postprocessing method, and clinical cohort being evaluated. Ideally a local normal reference range for strain values from healthy volunteers should be followed.
For negative strain variables (ie, circumferential and longitudinal strains), a value that is mathematically higher (ie, on the positive side) than the threshold is considered abnormal, whereas for positive strain variables (ie, radial strain), a value that is lower than the threshold is considered abnormal |
The correlation between strain values in CMR and echocardiography is variable. One study showed good agreements between myocardial tagging and two-dimensional STE for GLS and GCS, with STE systematically overestimating strain. However, this agreement was poorer at the regional level (25). Another study showed modest correlation between CMR FT and STE global strain values, with GLS being systematically lower in FT, whereas global radial strain and GCS were higher in FT than in STE (26). Given these variable agreements, strain parameters derived across modalities should not be used interchangeably.
Quality Assurance
Since strain, particularly FT, is derived from CMR images, the quality of the original images (ie, those affected by arrhythmia, limited breath holding, or poor contrast-to-noise ratio) will impact quantitative analysis. Accurate myocardial contours, annular planes, and long-axis boundaries are also essential for accurate quantification. A measure of the internal consistency of the FT and SENC analysis is whether the strain curve returns to zero at the end of the cardiac cycle; this indicates that the entire cardiac cycle was sampled and that the algorithm determined that the cardiac tissue returned to its original location at the start of the cycle. Care should be taken in assessing diastolic strain indices in tagging and DENSE techniques owing to diastolic signal fading, especially at low heart rates. SENC has good contrast-to-noise ratio even in late diastole, but the planes must be carefully proscribed for assessing myocardial changes over time (12). Tissue phase mapping is impacted by velocity noise, velocity aliasing, and eddy currents and hence preprocessing is required with this technique.
Right Ventricular Strain
Right ventricular (RV) strain imaging is challenging because of the complex shape, thin wall, trabeculations, and retrosternal location of the RV. Hence, echocardiography is limited to four-chamber longitudinal strain, whereas CMR can provide multidirectional strain information (Fig 14, Movie 12). SENC is superior to FT in the assessment of RV strain owing to its higher spatial and temporal resolutions with a single four-chamber acquisition in one heartbeat with fast SENC (27). FT requires several heartbeats and breath holding, is vulnerable to through-plane motion, and involves labor-intensive contouring of the thin RV wall. The orientation of RV myofibers is distinct from the LV, with predominant inner longitudinal and outer oblique orientations (5,28). Hence, diminished longitudinal strain may be related to endocardial damage, whereas a diminished circumferential strain could be because of epicardial damage. RV strain and strain rates are higher in the apex than in the base (28). Validation of reference ranges for RV strain is relatively lacking (Table 2) (29).
Figure 14. RV strain map. (A) Four-chamber cine SSFP image shows RV strain measurement by using FT. (B) Screen shot shows strain values measured by using FT. The radial strain rate has been measured and is depicted on the graph (yellow curve). The blue curve on the bottom right graph represents RV area over time (left vertical axis). The pink curve on the bottom right graph denotes change in area of change in time (dA/dt; right vertical axis).
Movie 12. Right ventricular strain. Short-axis cine SSFP image shows FT overlay of the right ventricular myocardial features.
The RV has higher global circumferential and radial strain and strain rates than the LV owing to thinner walls and larger circumference. RV GLS is more robust than GCS and global radial strain. Owing to the predominant longitudinal orientation of fibers, longitudinal shortening is a more important contributor to RV systolic function in healthy individuals. However, circumferential strain becomes more important in patients with pulmonary hypertension (5,30). RV strain is abnormal (ie, reduced) in arrhythmogenic right ventricular dysplasia (ARVD), pulmonary hypertension, and congenital heart diseases, including repaired tetralogy of Fallot (28).
Left Atrial Strain
The left atrium is the main modulator of LV filling with three distinct functions, namely collection of pulmonary venous return (reservoir), early LV filling (conduit), and late LV filling (booster pump). Strain can evaluate these physiologic features of the left atrium by using passive strain (ƐE, corresponding to conduit function), active strain (ƐA, related with booster pump function), and total strain (ƐS, representing reservoir function) (Fig 15) (31). Left atrium strain is measured by tracing contours in two- and four-chamber views at the atrial contraction phase and then following the contours. Normal left atrium values are 29% ± 5 for the reservoir, 21% ± 6 for the conduit, and 8% ± 3 for the booster pump (32). Higher booster pump strain values are seen with normal aging (32). Left atrium strain analysis has shown clinical utility and prognostic assessment in hypertrophic cardiomyopathy, HFpEF, and ischemic heart disease (18,33,34).
Figure 15. Left atrial (LA) strain. The vertical axis in both graphs shows GLS (%), and the horizontal axis shows time in milliseconds. (A) Left atrial strain analyzed by using FT in a two-chamber cine SSFP image in a 38-year-old healthy man shows that the GLS reservoir function is 50%, the conduit is 19.6%, and the boost is 17.4%. (B) Left atrial strain analysis in an 83-year-old woman with heart failure with preserved ejection fraction (LVEF, 55%) and left bundle branch block shows a decrease in all of the components of left atrial longitudinal strain compared to those in the healthy patient in A. A GLS reservoir function of 16.5%, a conduit of 9.9%, and a booster of 10.2% were noted.
Clinical Applications
Given the higher sensitivity of myocardial strain in detecting ventricular dysfunction compared with routine ejection fraction estimations, CMR strain is mainly used in the early diagnosis of several cardiovascular diseases, including screening of family members in inherited cardiomyopathies. Strain also provides risk stratification and prognostic markers, which can guide therapeutic planning. However, CMR strain imaging and analysis are not standardized, and there are only limited data on outcomes. With these limitations in mind, we discuss the clinical scenarios where strain can provide valuable complementary information (Table 3).
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Cardiotoxicity of Anticancer Therapeutics
Cardiotoxicity is an important complication of some anticancer therapeutics including chemotherapeutic agents (eg, anthracyclines), immunotherapeutic agents (eg, immune checkpoint inhibitors), and signaling pathway inhibiting agents (eg, trastuzumab). The mechanisms of cardiotoxicity include ventricular dysfunction, coronary artery disease, vascular toxicity, thromboembolic disease, valvular disease, and pericardial disease. Cardiotoxicity may require withholding certain drugs and therefore result in suboptimal treatment of the underlying cancer. Hence, careful monitoring and treatment to prevent the development of adverse cardiovascular events is of paramount importance.
Current guidelines for evaluation of adult patients undergoing chemotherapy recommend echocardiographically based LV ejection fraction and GLS for surveillance and early detection of LV dysfunction. Overt cancer treatment–related LV systolic dysfunction is diagnosed when the LV ejection fraction drops 10 percentage points to a value less than 50% or when the LV ejection fraction drops 20 percentage points from the baseline value. Early cancer treatment–related myocardial toxicity is diagnosed when the troponin level rises greater than or equal to the 99th percentile of the upper reference limit and/or absolute GLS drop of 5% or more or a relative GLS drop of 12% or more (Fig 16, Movie 13). The American Society of Echocardiography, the European Society of Cardiology, and the American Society of Clinical Oncology recommend a relative GLS drop cut-off of greater than 15% compared with baseline as clinically significant, while a change less than 8% is not significant (35). It is possible that ejection fraction and strain changes occur in parallel, and echocardiography is not able to confidently identify small ejection fraction changes (ie, <10 percentage points from baseline).
Figure 16. Chemotherapy cardiotoxicity. (A) FT with longitudinal strain overlay on a four-chamber cine SSFP image in a 47-year-old woman with lung cancer who underwent treatment with carboplatin shows decreased longitudinal strain. (B) Polar map in the same patient shows decreased circumferential strain in several segments, particularly the mid inferolateral segment. (C) Graph shows decreased longitudinal strain in the mid and apical segments (top and middle curves).
Movie 13. Chemotherapy cardiotoxicity. Four-chamber cine SSFP clip with FT longitudinal strain overlay in a 47-year woman with lung cancer who underwent treatment with carboplatin shows decreased longitudinal strain values.
CMR is also increasingly used in the evaluation of cardiotoxicity owing to its higher accuracy and reproducibility for LV ejection fraction assessment and the ability to assess strain as well as tissue characterization by T1 mapping, T2 mapping, and LGE (36). CMR has demonstrated decreases in the LV ejection fraction and GCS in patients receiving low-dose anthracyclines from baseline to 6 months (37). Clinical trials assessing the prognostic value of CMR parameters as well as the value of initiating cardioprotective medication triggered by a reduction in GLS are underway (38). These studies will help provide much-needed information on the value of various modalities as well as the impact of strain on clinical outcomes.
Ischemic Heart Disease
Strain is a sensitive marker of myocardial ischemia that can be used for early diagnosis of coronary artery disease. Impaired circumferential strain in ischemic segments has been shown by using CMR FT (39). Myocardial tagging increases the detection of regional wall motion abnormalities in dobutamine stress CMR, which is an indicator of ischemia (40). Recently a single-beat fast-SENC technique using GLS and GCS has been shown to be a rapid and accurate technique in diagnosing myocardial ischemia in patients with acute chest pain and suspected coronary artery disease without the need for stress agents, electrocardiography, or even troponin (41). Strain is also impaired in myocardial infarction, correlating directly with infarct size and inversely with the area at risk (42) (Fig 17). Strain can distinguish subendocardial and transmural infarction more accurately than wall thickness (43). Strain also helps in the identification of segments that will recover function after myocardial infarction, with poor response in segments with reduced circumferential strain (44). Strain outperforms well-known risk markers like LV ejection fraction, infarct size, or microvascular obstruction in prediction of major adverse cardiac events in ischemic heart disease (18).
Figure 17. Acute myocardial infarction in the left anterior descending artery (LAD) territory reperfused with stent placement in a 53-year-old man. (A) Short-axis T2-weighted short inversion time inversion-recovery (STIR) image shows an area of high-signal-intensity edema in the basal anterior and anteroseptal segments (arrow), indicating the area at risk. (B) Short-axis LGE delayed postcontrast CMR image in the same patient shows a subendocardial LGE (arrow) in the same segment, consistent with an established infarct. (C) FT overlays of circumferential strain on a short-axis SSFP CMR image (left image) and on a corresponding four-chamber 3D volume map (center image) show decreased strain in the mid anterior and anteroseptal segments. (D) FT overlays of radial strain on a short-axis SSFP CMR image (left image) and on a four-chamber 3D volume map (center image) show decreased strain in the mid anterior and anteroseptal segments. (E) Short-axis parametric mapping shows elevated native T2 (84.3 ± 10.8 msec), elevated native T1 (1479 ± 155 msec), decreased postcontrast T1 (451 ± 56.3 msec), and elevated extracellular volume (56.4%.).
Nonischemic Cardiomyopathies
Strain is decreased in various cardiomyopathies, which can be used for early detection as well as risk stratification
Figure 18. Cardiac amyloidosis. (A) Two-chamber cine SSFP image in a patient with cardiac amyloidosis with an overlay of longitudinal strain shows decreased longitudinal strain. (B) Polar map in the same patient shows decreased longitudinal strain in most of the segments. (C) Graph shows decreased GCS in the same patient, with a value of −8%.
Movie 14. Cardiac amyloidosis. Two-chamber cine SSFP clip with FT longitudinal strain overlay in a patient with cardiac amyloidosis shows significantly decreased longitudinal strain values.
Figure 19. Graph shows decreased circumferential strain at the anterior and anteroseptal segments (arrows) in a 14-year-old boy with hypertrophic cardiomyopathy.
Movie 15. Hypertrophic cardiomyopathy. FT circumferential strain overlay on short-axis cine SSFP image in a 14-year-old boy with hypertrophic cardiomyopathy shows decreased circumferential strain in the anterior and anteroseptal walls.
Impaired GCS and GLS are independent predictors of adverse outcomes in patients with cardiomyopathies and nonischemic cardiomyopathies, respectively (49,50). An FT study on dilated cardiomyopathy showed LV global transverse strain (a surrogate for radial strain) and RV longitudinal strain to be the strongest predictors of adverse outcomes (51). LV GLS is a stronger predictor of outcomes in patients with dilated cardiomyopathy, more than clinical and laboratory markers, ejection fraction, or LGE (50). In patients who underwent heart transplant, LV GLS can strongly predict major adverse cardiac events and mortality (52). In hypertrophic cardiomyopathy, lower LV strain with FT predicts ventricular tachycardia, appropriate implantable cardioverter defibrillator discharge, or death. Left atrium longitudinal strain by using FT also predicts adverse cardiac events in hypertrophic cardiomyopathy, even in patients with normal left atrium volumes and LV filling pressures (33). In HFpEF, impaired left atrium conduit strain correlates with exercise intolerance (32).
Valvular Heart Disease
Strain has a potential role in optimal selection of surgical candidates in patients with valvular heart disease. For example, longitudinal and circumferential strains are reduced in patients with severe aortic stenosis with preserved LV ejection fraction, even in those with no or only mild symptoms. This decrease is comparable to that in those with symptoms, which is a current class 1 indication for surgery. Hence, there is a potential future role for a more nuanced patient selection for surgery, especially those with equivocal symptoms (53).
Cardiac Resynchronization Therapy
Dyssynchronous electrical activation of different LV segments (LV dyssynchrony) owing to conduction delay results in dyssynchronous myocardial contraction, reducing the efficiency of cardiac pump. Cardiac resynchronization therapy (CRT) is useful in management of heart failure and LV dyssynchrony. However, 20%–30% of patients do not show favorable improvement in clinical symptoms or ejection fraction following CRT. Indices of mechanical dyssynchrony are used to augment the prediction of outcomes following CRT. Mechanical LV dyssynchrony is characterized by a difference in mechanical activation (Tonset) to peak contraction (Tpeak) times between the septum and lateral LV walls. Mechanical LV dyssynchrony has a substantial delay (≥130 msec) in peak strain between the anteroseptal and lateral LV segments by STE (54). The standard deviation of contraction durations (ie, time for peak shortening and strain) for the myocardial segments is low in a normal individual but high in a patient with LV dyssynchrony. Another CMR-derived parameter is the uniformity estimate ratio (URE), which grades the spatial homogeneity of strain over time, measured in circumferential (CURE), radial (RURE), or longitudinal (LURE) directions (55). The values of CURE range from 0 (dyssynchronous) to 1 (synchronous) and are reproducibly measured by using cine SSFP images (56). LV reverse remodeling is more likely to occur when leads are placed in areas without scar that had delayed time to peak circumferential strain than in patients with scar and normal time to peak circumferential strain (57) (Fig 20, Movie 16). Lead placement at the latest site of mechanical activation and/or thickening and without scar has a superior outcome.
Figure 20. LV dyssynchrony. (A) Short-axis FT circumferential strain overlay on a cine SSFP image shows abnormal circumferential strain with variable values in different segments. (B) Graph shows the strain curves with variable circumferential strains in various segments. (C) Polar map of time to peak circumferential strain shows various times to peak strain in the septal and lateral segments, consistent with LV dyssynchrony.
Movie 16. LV dyssynchrony. Short-axis cine SSFP clip with FT overlay shows different times to peak strain in the septal and lateral segments, consistent with LV dyssynchrony.
Pulmonary Hypertension
Pulmonary hypertension is a progressive and heterogeneous disease, with high mortality rates. Adaptive changes of the RV have a great impact on disease severity and prognosis (22). RV strain and strain rates are impaired in pulmonary hypertension and correlate with disease severity (Fig 21, Movie 17). GCS is significantly reduced in patients with pulmonary hypertension, even in those with preserved RV ejection fraction, indicating its potential role in the early discrimination of RV decompensation (58–61). LV GLS, GLS rate, and GCS rate are independently associated with death, lung transplant, and New York Heart Association (NYHA) functional class (59).
Figure 21. Pulmonary hypertension. (A) Short-axis SENC image in a patient with pulmonary hypertension shows markedly decreased strain values. (Fig 21A courtesy of Benjamin Freed, MD, Northwestern University, Chicago, Il.) (B) Two-dimensional myocardial FT on a short-axis cine SSFP image shows an impaired circumferential strain of −9.2% (arrow). (C) 3D myocardial FT of the RV shows decreased circumferential strain (arrow). There was also a reduced systolic circumferential strain rate (−0.3).
Movie 17. Pulmonary hypertension. Short-axis SENC clip in a patient with pulmonary hypertension shows markedly decreased strain values. (Courtesy of Benjamin Freed, MD, Northwestern University, Chicago, Il.)
LV dysfunction is known to occur in late stages of pulmonary hypertension and is related to disease severity and poor prognosis (22). FT can also detect LV dysfunction in patients with known pulmonary hypertension before a decline in ejection fraction. Strain abnormalities are more pronounced in the septum and correlate with RV end-diastolic volume, a well-known prognostic factor in pulmonary hypertension (62). LV GCS in the septum is more affected than RV GLS in the free wall in pulmonary hypertension.
Congenital Heart Diseases
Myocardial strain is useful in several congenital heart diseases, such as repaired tetralogy of Fallot, transposition of the great arteries (TGA), Fontan palliation, Ebstein anomaly, and coarctation, for early diagnosis of dysfunction after surgery and identification of early markers predictive of adverse outcomes. In repaired tetralogy of Fallot, exercise capacity is strongly related to RV strain (Fig 22, Movie 18) (63,64). Ventricular tachycardia and death in patients with repaired tetralogy of Fallot have been shown to be related to the peak LV circumferential strain and reduced LV and RV GLS and GCS (63–65). In Fontan palliation, FT-based systemic ventricle strain parameters are better predictors of NYHA class and exercise capacity than ejection fraction (66). Similarly, in patients with TGA who underwent an atrial switch procedure, reduced longitudinal and circumferential strains were seen in the systemic RV (67). Peak exercise capacity was found to be strongly related to LV GLS (68,69). In Ebstein anomaly, FT-based strain parameters are associated with heart failure and longer QRS duration (70) and detect LV dysfunction earlier than ejection fraction (67). RV free wall GLS relates to functional health status, even in patients with normal RV ejection fraction. LV dyssynchrony predicts death or sustained ventricular tachycardia (71) (Fig 23). In repaired aortic coarctation with preserved LV ejection fraction, impairment of LV GLS has been associated with LV hypertrophy (72).
Figure 22. Tetralogy of Fallot. (A) Four-chamber SSFP image and FT analysis in a patient with repaired tetralogy of Fallot show decreased RV longitudinal strain. (B) Short-axis FT image in a 61-year-old woman with repaired tetralogy of Fallot with a preserved RV ejection fraction and RV outflow tract dilatation (36 mm) shows impaired RV circumferential strain of −13.3% (arrow) at the RV outflow tract. (C) Impairment of radial strain is also seen at the same level (arrow), although radial strain in the rest of the myocardium is normal.
Movie 18. Tetralogy of Fallot. Short-axis cine SSFP clip with FT longitudinal strain overlay in a patient with repaired tetralogy of Fallot shows diminished RV longitudinal strain.
Figure 23. Tetralogy of Fallot. Strain curves in a patient with tetralogy of Fallot show LV dyssynchrony with delayed peak strain of septal segments (straight arrow) and normal time to peak strain for the inferolateral wall (curved arrow).
Screening for Cardiac Pathologic Conditions
CMR myocardial strain may be an efficient cost-effective screening test for asymptomatic patients with early heart failure. Fast SENC is highly accurate in the early diagnosis of heart failure and also more cost-effective than echocardiography ($24 647 vs $39 097 U.S. dollars, respectively), with an estimated lifetime cost savings of 37% (73). Fast SENC can efficiently help confirm normal systolic function with a gradient on-time of 105 seconds (74). Fast SENC demonstrates good agreement with imaging for quantitation of LV ejection fraction and LV end-diastolic volume. Similarly, midventricular peak longitudinal strain derived from fast SENC correlates well with RVEF in pulmonary hypertension, suggesting a role for efficient monitoring of patients with this condition (75). These studies suggest that fast-SENC could serve as an efficient screening test to distinguish subjects with normal function or could provide an efficient noncontrast monitoring strategy for patients with known cardiac disease. CMR can be started with a strain technique. If strain is normal, no further imaging such as cine imaging and LGE may be required. Additional sequences can be performed only if there is abnormal strain, which will improve the operational efficiency of CMR.
Conclusion
CMR myocardial strain imaging is now increasingly available and performed, primarily owing to the development of the FT technique. Myocardial strain is clinically useful in the early diagnosis of myocardial dysfunction, particularly in anticancer therapeutics cardiotoxicity. CMR strain is also used for risk stratification and prognostication of several entities, including ischemic heart disease, cardiomyopathies, congenital heart disease, and pulmonary hypertension. CMR strain may be useful in identifying patients with LV dyssynchrony who will benefit from cardiac resynchronization therapy.
Recipient of a Cum Laude award for an education exhibit at the 2020 RSNA Annual Meeting.
For this journal-based SA-CME activity, the authors P.S.R., J.D.C., and P.P.A. have provided disclosures (see end of article); all other authors, the editor, and the reviewers have disclosed no relevant relationships.
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Article History
Received: June 15 2021Revision requested: Nov 2 2021
Revision received: Nov 4 2021
Accepted: Nov 5 2021
Published online: May 27 2022
Published in print: July 2022
